Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact [1 ed.] 9781614709046, 9781614708339

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Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved. Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise, Nova

Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved. Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

ANIMAL SCIENCE, ISSUES AND PROFESSIONS

RODENTS HABITAT, PATHOLOGY AND ENVIRONMENTAL IMPACT

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Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

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Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

ANIMAL SCIENCE, ISSUES AND PROFESSIONS

RODENTS HABITAT, PATHOLOGY AND ENVIRONMENTAL IMPACT

ALFEO TRIUNVERI AND

Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved.

DESI SCALISE EDITORS

Nova Science Publishers, Inc. New York

Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

Copyright © 2012 by Nova Science Publishers, Inc. All rights reserved. No part of this book may be reproduced, stored in a retrieval system or transmitted in any form or by any means: electronic, electrostatic, magnetic, tape, mechanical photocopying, recording or otherwise without the written permission of the Publisher. For permission to use material from this book please contact us: Telephone 631-231-7269; Fax 631-231-8175 Web Site: http://www.novapublishers.com NOTICE TO THE READER The Publisher has taken reasonable care in the preparation of this book, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained in this book. The Publisher shall not be liable for any special, consequential, or exemplary damages resulting, in whole or in part, from the readers’ use of, or reliance upon, this material. Any parts of this book based on government reports are so indicated and copyright is claimed for those parts to the extent applicable to compilations of such works.

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Independent verification should be sought for any data, advice or recommendations contained in this book. In addition, no responsibility is assumed by the publisher for any injury and/or damage to persons or property arising from any methods, products, instructions, ideas or otherwise contained in this publication. This publication is designed to provide accurate and authoritative information with regard to the subject matter covered herein. It is sold with the clear understanding that the Publisher is not engaged in rendering legal or any other professional services. If legal or any other expert assistance is required, the services of a competent person should be sought. FROM A DECLARATION OF PARTICIPANTS JOINTLY ADOPTED BY A COMMITTEE OF THE AMERICAN BAR ASSOCIATION AND A COMMITTEE OF PUBLISHERS. Additional color graphics may be available in the e-book version of this book. LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA Rodents : habitat, pathology, and environmental impact / editors, Alfeo Triunveri and Desi Scalise. p. cm. Includes index. ISBN  ((%RRN) 1. Rodents. 2. Rodents--Ecology. I. Triunveri, Alfeo. II. Scalise, Desi. QL737.R6R628 2011 599.35--dc23 2011028141

Published by Nova Science Publishers, Inc. † New York

Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

CONTENTS Preface Chapter 1

Chapter 2

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Chapter 3

vii Rodents in Urban Ecosystems of Russia and the USA Lyudmila Khlyap, Gregory Glass and Michael Kosoy

1

Extrinsic and Intrinsic Factors of Regulation of Reproductive Potential in the Water Vole (Arvicola amphibius) Population from Western Siberia Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka, Olga F. Potapova and Vadim I. Evsikov

23

Rodents and Space: What Behavior Do We Study under Semi-Natural and Laboratory Conditions? Vladimir S. Gromov

43

Chapter 4

Proechimys: A Rodent Still Poorly Understood Carla Alessandra Scorza, Bruno Henrique Silva Araujo, Laila Brito Torres and Esper Abrão Cavalheiro

Chapter 5

Niche Overlap and Resource Partitioning among Three Urban Rodent Species Eduardo de Masi and Francisco Alberto Pino

77

Helminth Parasites of Hydromyine Rodents from the Island of New Guinea Lesley R. Smales

99

Chapter 6

Chapter 7

Rodent Management in Animal Farms by Anticoagulant Rodenticides Shmuel Moran

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119

vi Chapter 8

Contents Sustained Agriculture: The Need to Manage Rodent Damage Gary Witmer and Grant Singleton

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Index

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145 183

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PREFACE This book gathers topical research from across the globe in the study of the habitat, pathology and environmental impact of the rodent population. Topics discussed include rodents in urban ecosystems of Russia and the USA; the European water vole of Western Siberia; a study of rodents in field investigations; the potential use of Proechimys (spiny rat) in the field of neuroscience; niche overlap and resource partitioning among three urban rodent species; helminth parasites of hydromyine rodents from the island of New Guinea and rodent management in animal farms by anticoagulant rodenticides. Chapter 1 - The chapter discusses the distribution and biology of major groups of rodents that are most likely to be encountered in urban areas in Russia and the USA. Emphasis is made on the factors affecting the abundance of these animals and the likelihood they will invade human dwellings. Commonalities between analyzed geographic areas include a dominance of Norway rats (Rattus norvegicus) and house mice (Mus musculus), which have historically colonized urban ecosystems, globally. These species were introduced into the USA much later than to the European and Asian parts of Russia and some differences in their ecology were noticed between two countries. The wild rodents that occupy urban territories can represent many other species. Species compositions are influenced by rodent communities in natural habitats surrounding cities. The striped field mouse (Apodemus agrarius) and the East European vole (Microtus levis) are common in cities of the European part of Central Russia, the striped field mouse and the reed vole (Microtus fortis) can occasionally occupy some urban territories in the south of Russian Far East. The rodents that periodically invade urban territories in the USA include the New World rats and mice (Neotoma, Peromyscus, and Sigmodon), Microtus voles, and tree and ground squirrels. Differences in the terminology related to describing invasive species used in Russia and the English-speaking countries are discussed. Urban rodents present a great risk to human health, especially to people whose health is already compromised. Though the epidemiology of many rodent-borne diseases in urban environment remains ill-defined, numerous studies have shown that rodents can be infected with a large variety of infectious and parasitic agents. During the last decades the authors have seen a rise in human diseases that are associated with rodent reservoirs and their presence can have serious implications for public and veterinary health. In additions to being reservoirs for zoonotic diseases, urban rodents historically present threat to food supplies and are important competitors with humans for food where they live together. Rodents within human settlements are also seen as pest because of their destructive behaviors that can cause economic losses and lead to structural damages. To

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viii

Alfeo Triunveri and Desi Scalise

develop an effective control strategy, the true rate, locations of infestations, ecological characteristics of urban rodents, and some other risk factors need be assessed. As David Davis (1951) stated 60 years ago, because of the economic and epidemiologic importance of reducing urban rat populations, these efforts rarely provided data of value for science and also rarely reduced the pests except temporarily. The subject of this review is the characteristics of an ecologically diverse group of rodents, for which their urban environment is common, between Russia and the United States. Rodents became human neighbors at the very early stage of human civilization; however, during last century city developments dramatically extended habitats within urban territories suitable for rodents and this process reached the global scale. The process of invading urban habitats by rodents continues and creates dramatic changes in rodent diversity within urbanized territories. Chapter 2 - The European water vole (Arvicola amphibius) dominates in rodent assemblies in Northern Baraba Lowland (Western Siberia) where its populations exhibit pronounced 4–9 year-long cyclic fluctuations in numbers. One of the principle peculiarities of water voles ecology in West Siberia is usage of different habitat sites during reproductive season and wintering. In summer they are aquatic and live and reproduce in wetlands, while in winter they are fossorial and live underground in meadows. The water vole has proved an excellent model species to investigate the role of both extrinsic and intrinsic mechanisms in driving population cycles. Using data from multi-annual study, the authors investigated the dependence of female’s breeding success on extrinsic conditions influencing the availability of wet biotopes, food resources and intrinsic factors (density dependent). The authors also investigated the relation of winter survival to mass of food storage. Abiotic factors have a direct influence on the availability of habitat-related resources. In summer, the main extrinsic factor influencing reproductive potential of the water vole is hydrological regime, i.e. variable water supply determining the area of suitable biotopes. The authors analysis has revealed correlation between flow intensity of the Om River in the study area and population dynamics, average number of live embryos in overwintered females, and percentage of mature young-of-the-year females in different years of study. Female reproductive characteristics appeared to be sensitive to effects of both extrinsic (availability of suitable biotopes) and intrinsic (density) factors. It was found that interaction of these factors determines the level of competition among reproductively active females as detected by number of injuries on skins and consequently embryonic losses and decline of population numbers. In severe continental Siberian climate winter survival of voles depends on amount of food stores which, in turn, depends on population density influencing competition level. Participating of the young-of the-year females in reproduction has effect on their winter survival. They stay in wet biotopes for late summer and have not enough time to gather necessary for safe wintering amount of food stores. Because of higher female winter mortality, sexual structure of the population in spring is unbalanced. This leads to high level of inter-male competition for receptive females and strong selection among overwintered males. Thus, the obtained data indicate that in the water vole from Western Siberia the extrinsic and intrinsic factors closely interact both in summer and in winter regulating reproductive potential and density of the population. Chapter 3 - Over the last several decades, a tendency has appeared of focusing upon laboratory studies of various activities of rodents instead of field investigations. Of cause, laboratory studies usually do not take so much labour, time and money as do investigations in the field, and in many cases researchers can make proper inferences based on data obtained

Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

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Preface

ix

due to observations of rodents in captivity. But my own experience shows that the authors can lose very valuable information and, moreover, draw incorrect conclusions when carrying out behavioral studies on rodents under laboratory conditions only. It is well known that rodents are sedentary animals, and every one possesses a home range used for various purposes: foraging, construction of shelters and burrows, interactions with conspecific individuals, reproduction, etc. Rodent home ranges are usually of a large size, and comprise several hundreds and even a few thousand square meters. Restriction of space under semi-natural conditions (for instance, in large enclosures) and, moreover, in small laboratory cages can lead to essential alteration of rodent behavior. This especially concerns behavior related to territoriality, scent marking, social interactions, and parental care. Chapter 4 - Rodentia is the largest order of living mammalia encompassing 2277 species, or approximately 42% of worldwide mammalian biodiversity. The predominantly South American representative families are Echimyidae and Cricetidae. The Neotropical spiny rats of the family Echimyidae are the most taxonomically, ecologically, and morphologically diverse group of all extant hystricognath rodents. They are small-bodied animals distributed throughout the Neotropical region from Central America to Argentina. It has been suggested that most of the cladogenesis leading to the extant echimyid genera probably occurred during the Late Miocene, about eight million years ago. In addition to be the most species-rich caviomorph family, the Echimyidae have the greatest diversity of ecomorphological adaptations within hystricognath rodents. Proechimys (suborder hystricomorpha, infraorder histricognathi, family echimyidae, subfamily eumysopinae) are the most abundant and widespread terrestrial lowland small mammals in Neotropical rainforests, occurring from Honduras in Central America to Paraguay in South America. Virtually, any forested lowland habitat is likely to harbor at least 1 species of Proechimys (spiny rat), and some areas may have up to 4 sympatric species. Spiny rodents are generalists with respect to use of forested habitats. In particular, these rodents were associated with forest gaps and areas with shorter canopies and higher densities of smaller trees, logs, and lianas. Younger forests and tree-fall gaps within older forests represent areas of rapid plant recruitment and growth due to increased light availability. Effects of spiny rodents on seed survival via predation and dispersal and on arbuscular mycorrhizal fungal infection via spore dispersal may be particularly pronounced in such areas. In this sense, Proechimys plays an important role in forest dynamics through their activities as seed predators and dispersers of seeds. Moreover, Proechimys has received some attention as a natural host to infectious parasites and recently, the brain of the Proechimys (P. guyannensis) started to be studied. Previous findings have shown that Proechimys are extremely sensitive to epileptogenic treatments, but they seem unable to establish an epileptic focus and subsequent spontaneous seizures. In this line of evidence, Proechimys was designated as an animal model of resistance to epilepsy. These findings provide new directions for the potential use of Proechimys in the field of neuroscience. Furthermore, they have direct implications for the study of the normal brain as well as for elucidating intrinsic mechanisms of central nervous system disorders. Chapter 5 - There are very few studies showing sympatric coexistence among roof rat (Rattus rattus), Norway rat (Rattus norvegicus) and house mouse (Mus musculus) in urban environment. This chapter deals with overlapping in space use and interspecific competition among those three rodent species in the urban area of Sao Paulo city, Brazil. It is based on a rodent survey carried out in 2006: 16,467 premises were inspected and infestation rates were annotated by rodent species and infested place (dwelling internal or external area). The niche

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Alfeo Triunveri and Desi Scalise

complementarity hypothesis was tested by polytomous logistic regression modelling. The results indicate extensive spatial segregation among the three species, with coexistence limited by the occupation of different places inside the dwelling. R. rattus infests internal and external area equally, R. norvegicus infests mainly external area, and M. musculus infests mainly internal area. The niche complementarity hypothesis was confirmed, since some niche axes overlap and others were characteristically associated to a single species. In conclusion, there is strong competition among the three urban rodent species, and thus the control of one species may be favorable to high infestation of another one. The importance of the results for public health polices and for urban rodent ecology understanding is pointed out. As a matter of fact, public health and pest control policies must emphasize integrated rodent control techniques in order to decrease the ecological support capacity of urban environment for rodents. Chapter 6 - New Guinea has an abundant and diverse murid fauna, ranging from tiny insectivores to carnivores to giant folivores and including tree mice and moss mice as well as more typical rat species. This ecological and species diversity appears to be paralleled by a complex and diverse helminth parasite fauna that has only recently begun to be investigated. Each study that has been carried out has revealed helminth species and genera new to science. This helminth fauna includes cosmopolitan species, regionally endemic species and locally endemic species indicating a complex evolutionary history. It has apparently arisen as a consequence of both co-evolution and host switching leading to speciation events, as migrating ancestral rodent hosts colonized the Sunda and Sahul regions, travelling from Southeast Asia down the Indonesian Island chain through New Guinea to continental Australia. Until all the endemic murid species have been studied in sufficient numbers the complete pattern of helminth diversity and relationships will not be fully understood. Chapter 7 - Three rodent species are commensal around the globe: the Norway rat (Rattus norvegicus Berk.), the roof rat (R. rattus L.), and the house mouse (Mus musculus L.). These species thrive in livestock farms, where they find unlimited food, water and shelter. They inflict damage mainly through consumption and contamination of animal feed; they are carriers of disease and parasites to livestock and humans; they also damage structures and electric wiring, which sometimes causes fires; among poultry they may prey on eggs and chicks; and their excreta may contaminate milking equipment in dairy farms. Preferably the commensal rodent populations are managed by reducing available food, water and shelter, or excluding them from the livestock structures, but these procedures are impossible to attain in most livestock farms. Therefore, in most cases, control by toxic baits has to be used. Today, second-generation anticoagulants are the most common group of rodenticides. The efficacy of the rodent pesticides is estimated in field tests by comparing indices of population size before and after the poison treatment. The census indices used are live trapping, counts of tracks, droppings and re-opened burrows, and consumption rates of pre- and post-treatment untreated baits. The efficacy of commercial formulations of the second-generation rodenticides brodifacoum, bromadiolone and flocoumafen in controlling house mice and roof rats was tested in eight henhouses, a piggery, and a dairy farm. The formulations used were pellets, wax blocks and paste, offered in tamper proof bait stations and cardboard boxes. The control efficacies were assessed by the re-opened mouseholes census, and by consumption of untreated census bait before and after the treatment. The progress of the control procedure was assessed by measuring bait consumption, amounts of bait added to the boxes, or number of rodent visits in the bait boxes (takes). The experiments resulted in high control rates,

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Preface

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achieved in 2-3 weeks. When rat-size bait boxes were used for mouse control, the rodents gathered soil inside the boxes, which highlights the need the use the appropriate bait box size. Recovered mouse carcasses were found inside the henhouses, as expected by their limited home ranges. In contrast, most of the dead roof rats were not found, as they dispersed outside the treated farm buildings throughout their home ranges. These findings indicate that the environmental risk presented by the rodenticides used is negligible in henhouse mouse control, and considerable in farm building rat control. It was found that any of the parameters – bait consumption, mouse carcass recoveries, and bait takes – can be used to monitor the progress of control operations. Chapter 8 - The need for sustained agricultural production increases as the world’s human population increases, many natural resources grow scarce, and the amount of land devoted to agriculture declines. For example, Vietnam loses 30,000 ha annually of prime rice land to urban development, yet it is the second highest exporter of rice in a world market that reached crisis levels during 2008 (Meerburg et al., 2009b). Between 1960 and 2000, the world’s population doubled; in Asia alone the annual population growth until 2020 is estimated at 75 million, which is a lot of new mouths to feed (FAO, 2008). Hence, feeding the world’s growing population continues to be a challenge for governments, especially in light of accelerated population growth, loss of agricultural land to urbanization and industrialization, shortage of agricultural labor due to migration of youth to cities, sustained economic growth leading to increase demands for meat protein (energy to produce 1 kg of meat protein requires 5 times that of proteins from cereals (Kawashima et al., 1997)), and pressures brought by climate change, loss of biodiversity, growing water scarcity, liberalized trade regimes, and inappropriate technology applications (e.g. growing of some food crops for bio-fuels). The future requires a sustainable agriculture base in which farms can produce food without causing severe or irreversible damage to ecosystem health.

Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

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In: Rodents Editors: Alfeo Triunveri and Desi Scalise

ISBN: 978-1-61470-833-9 ©2012 Nova Science Publishers, Inc.

Chapter 1

RODENTS IN URBAN ECOSYSTEMS OF RUSSIA AND THE USA Lyudmila Khlyap1, Gregory Glass2 and Michael Kosoy3 1

A. N. Severtsov Institute of Ecology and Evolution, Moscow, Russia 2 Bloomberg School of Public Health, John Hopkins University, Baltimore, Maryland, US 3 Centers for Disease Control and Prevention, Fort Collins, Colorado, US

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ABSTRACT The chapter discusses the distribution and biology of major groups of rodents that are most likely to be encountered in urban areas in Russia and the USA. Emphasis is made on the factors affecting the abundance of these animals and the likelihood they will invade human dwellings. Commonalities between analyzed geographic areas include a dominance of Norway rats (Rattus norvegicus) and house mice (Mus musculus), which have historically colonized urban ecosystems, globally. These species were introduced into the USA much later than to the European and Asian parts of Russia and some differences in their ecology were noticed between two countries. The wild rodents that occupy urban territories can represent many other species. Species compositions are influenced by rodent communities in natural habitats surrounding cities. The striped field mouse (Apodemus agrarius) and the East European vole (Microtus levis) are common in cities of the European part of Central Russia, the striped field mouse and the reed vole (Microtus fortis) can occasionally occupy some urban territories in the south of Russian Far East. The rodents that periodically invade urban territories in the USA include the New World rats and mice (Neotoma, Peromyscus, and Sigmodon), Microtus voles, and tree and ground squirrels. Differences in the terminology related to describing invasive species used in Russia and the English-speaking countries are discussed. Urban rodents present a great risk to human health, especially to people whose health is already compromised (Battersby et al., 2008). Though the epidemiology of many rodent-borne diseases in urban environment remains ill-defined, numerous studies have shown that rodents can be infected with a large variety of infectious and parasitic agents. During the last decades we have seen a rise in human diseases that are associated with rodent reservoirs and their presence can have serious implications for public and veterinary health (Meerburg et al. 2009). In additions to being reservoirs for zoonotic

Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

2

Lyudmila Khlyap, Gregory Glass and Michael Kosoy diseases, urban rodents historically present threat to food supplies and are important competitors with humans for food where they live together. Rodents within human settlements are also seen as pest because of their destructive behaviors that can cause economic losses and lead to structural damages. To develop an effective control strategy, the true rate, locations of infestations, ecological characteristics of urban rodents, and some other risk factors need be assessed. As David Davis (1951) stated 60 years ago, because of the economic and epidemiologic importance of reducing urban rat populations, these efforts rarely provided data of value for science and also rarely reduced the pests except temporarily. The subject of this review is the characteristics of an ecologically diverse group of rodents, for which their urban environment is common, between Russia and the United States. Rodents became human neighbors at the very early stage of human civilization; however, during last century city developments dramatically extended habitats within urban territories suitable for rodents and this process reached the global scale. The process of invading urban habitats by rodents continues and creates dramatic changes in rodent diversity within urbanized territories.

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TERMINOLOGY AND DIFFERENCES IN TERMS BETWEEN WESTERN AND RUSSIAN LITERATURES Though it was not our initial intention to go deeply into semantic issues of specific categories that unify all rodent inhabitants in urban areas, there is a serious reason to start this paper by discussing some terminology before we concentrate on specific groups. This is especially important because of some traditional differences in describing urban rodents between Russian and US scientists. Among rodents occupying urbanized territories, it is easy to distinguish two major groups. One group represented by two species of Rattus rats (Rattus norvegicus and R. rattus) and house mice (Mus musculus), which are highly adapted to survive within urban landscapes and can be found throughout the world. The other group is represented by rodent species that may be found within city limits, but do not show a long history of living in close proximity to humans, most of them are more common outside of human dwelling and are adapted to a natural environment. In the western literature, the most common term for the first group is ‘commensal rodents’ while the second is ‘non-commensal rodents’. For example, in the book recently published by the World Health Organization and entitled ‘Public health Significance of Urban Pests’ (2008), there are two chapters ‘Commensal rodents’ and ‘Non-commensal rodents and lagomorphs’. In the first of these chapters, the authors (Battersby et al., 2008) stated that “rats and mice are thought of as commensal rodents because of their close association with human activity. In ecological sense, the term commensalism refers to a symbiotic condition in which one participant benefits while the other is neither benefited nor harmed. Etymologically, commensalism refers to a sharing of one’s table. These rodents benefit from their association with people in that they share dwelling with human occupants and, metaphorically speaking (though sometimes literally), eat from the same table. People, however, not only do not benefit from an association with these rodents, but they also may in fact suffer harm” (italic here is ours). The mentioned contradiction was noticed by other biologists as well and is one of the reasons why the term ‘commensal’ was not widely adapted among Russian and Eastern-European zoologists. Instead, in these countries more common definition for such

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Rodents in Urban Ecosystems of Russia and the USA

3

rodents is ‘synanthropic rodents’ (Kucheruk, 1965, 1988; Kucheruk and Karaseva, 1992). The term ‘synanthropic’ indicates that these animals are inhabitants of human settlements or ‘ecologically associated with humans’. An application of the term ‘synanthropic rodents’ in Russian literature on rodent ecology has two meanings: in strict sense, when it was restricted to the rodent species, which were unintentionally introduced to new territories from the areas of their origin (Tikhonova et al. 2001, 2006; Rechkin et al., 2001); and in a wider sense, when it was applied to all rodents that can occupy urban habitats while maintaining their connection to natural biotopes (Kucheruk, 1965, 1988; Kucheruk and Karaseva, 1992). Calling all these rodents as ‘synanthropes’, the prominent Russian zoologist Valent Kucheruk proposed to distinguish so-called ‘true’ synanthropes versus ‘semi-synanthropes’. In this sense, the term ‘true’ synanthropes are close to the term ‘commensal’ used in the western literature. There is another pair of terms that sometimes is applied for urban rodents such as ‘alien’ or invasive’ species versus ‘native species’. This terminology reflects that R. norvegicus, R. rattus, and M. musculus are not native to the most part of Earth except some Asian regions and invaded all continents except Antarctica through human activities. These rodents are distributed all over the world principally through occasional introductions and becoming established in human settlements. The integrity of their distribution is determined mainly by transport connections and freight traffic. In the past, the distribution depended mainly on cart traffic and ship navigation. The latter was a leading factor for crossing ocean barriers. In the modern world, the role of automobile and air transport is growing. These notions were suggested in the global strategy on invasive alien species (A Global Strategy…, 2001; 100 of the Word’s Worst Invasive Alien Species…2001). However, accepting the term ‘alien species’ as a wide notion and using this term in this paper and elsewhere, we also think that the state of being alien always manifests itself at the population level (each species has an area where it is local). The state of being alien is always regional. One of the clear signs of being alien is expansion of the area both due to displacement of borders and by introduction of animals to areas where formerly representatives of this species were absent (Dgebuadze, 2000). Colonizing some regions a long time ago, the invasive species become so common there that an application of the term “alien” to them seems odd (Khlyap and Warshavsky, 2010). ‘Peridomestic animals’is a term that is widely used in epidemiology and zoology. It is used to describe animals, which though not domesticated, live in close proximity to humans. Rats are sometimes used as an example of peridomesticity, however, it is not a so obvious description of indoor rats compared with rats living adjacent to buildings. This distinction becomes important in the epidemiology of zoonotic diseases because the extent of contact between humans and peridomestic animals (some rodent species along with other wildlife and domestic animals) that serve as potential carriers of pathogens such as Yersinia pestis or hantaviruses influence the likelihood of transmission.

SPECIFIC CHARACTERISTICS OF URBAN TERRITORIES AS AN ENVIRONMENT FOR RODENTS Rodents living in urban environments often show specific adaptations. An urban area is characterized by closely located buildings and other human features, and by higher human

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Lyudmila Khlyap, Gregory Glass and Michael Kosoy

population density compared to areas surrounding it. Urban regions may be cities and towns, but usually are not rural settlements such as villages and small clusters of houses. Sometimes it is not easy to define from ecological perspectives urban areas, especially in suburban parts. It is also important to remember that ecological conditions in urban territories vary among countries such as Russian and the USA as well as within each country. Within urban territories land surface temperature is commonly higher and humidity lower compared to surrounding natural habitats (= urban heat island). Another important aspect is the extent of sites that are not suitable for rodents, such as roads and squares covered by asphalt or concrete within urban areas. The habitats that can be potentially occupied by rodents are commonly separated from one another and this tends to fragment rodent populations within urban sites. As a result, rodent species that adapt to urban habitats need to survive periods of restricted movement but likely need some portion of their lives when long distance dispersal (allowing recolonization of available habitats) occurs. There are exceptions such as rodents occupying large green areas such as parks, and cemeteries. Habitats suitable to rodents within urban areas can roughly classified as 1) buildings, 2) human created features outside buildings, and 3) resembling natural habitats. The latter can be created by humans or to be remnant habitat patches survived during an urban development. Specifics of these habitats vary greatly depending on history and geography. The lowest rate of rodent diversity is usually observed inside buildings and the highest rate is common within patches resembling natural habitats. Rodents experience the most stable conditions inside buildings. Among factors affecting invasive ecology of rodents are architectural peculiarities such as construction materials, presence of empty spaces between walls, damage (holes) in walls; and accessibility to food. Access to food waste, such as garbage dumps, is an especially important factor. For their movement, urban rats tend to use existing features, but also can create burrow systems, which cause additional damages to house. Movement between suitable habitat patches may either be directly across the surface, through underground features created by people, such as drains, or by the animals themselves or by unintentional transportation by people, with cargo. In industrialized countries rats are often found in considerable numbers within the sewer system of cities (Lund, 1994). This is sometimes their main refuge in modern situations where slums are no longer present and where efficient refuse removal operations make it difficult to find food sources above ground. Among habitats outside buildings, we emphasize a role for lawns and roadsides for distribution of urban rodents. Such areas can be exposed to intensive burrowing by rodents. Some authors stressed an importance of railroads for invasion of rodents inside urban territories (Tikhonova et al., 1997). Having settled in urban areas, rats and mice may secondarily expand to recreational zones (Zjigarev, 2004) and via favorable biotopes disperse to other human settlements (Kucheruk, 1965, 1988). When considering urban rodents we also need to evaluate the roles that predators play in influencing the distribution of rodents. Inside and near buildings rodents may become prey for stray and outdoor cats and dogs (Glass et al 2009), and in areas resembling natural habitats, there is a wider range of potential predators including foxes, weasels, ferrets, martens (Karaseva et al. 1999), as well as raptors. A special study in forested areas within Moscow during the period of 1975-1996 revealed a presence of weasels, stoats, foxes, and to a lesser degree polecats and martens. In many US cities, the expansion of foxes, coyotes, skunks, raccoons and other wild mammals has become more evident during last decades. Birds of

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prey represent over 70% of all predator attacks on rodents (Nour et al. 1993), but their importance (especially nocturnal raptors) likely decreases in areas close to human houses. Finally, pest control can significantly reduce and in some cases completely eliminate rodents in cities and towns (Lambropoulos et al., 1999; Rylnikov, 2010). Regardless of these limiting factors, expansion of urban areas provides some rodent species with all they need to survive and thrive.

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BIOLOGICAL TRAITS OF URBAN RODENTS The synanthropic rodents possess a unique set of ecological and ethological adaptations enabling them to exist in proximity to people. Biological traits of synanthropic rodents enabling them to be neighbors of man were firstly formulated for the house mouse by Tupikova (1947). Later, these efforts were expanded by other Russian zoologists to other species (Sokolov and Karaseva, 1985; Meshkova and Fedorovich, 1996; Karaseva et al., 1999; Kotenkova, 2000; Kotenkova, Munteanu, 2007; Khlyap and Warshavsky, 2010; Bobrov et al., 2008). Among specific traits for obligate synanthropic rodents, the authors identified that they : 1) can easily penetrate into new territories; 2) are capable of quickly colonizing new territories; 3) are able to live in close proximity to each other; 4) are capable of rapid population growth; 5) can live in strongly fragmented space, e.g. in houses separated by streets or in suitable fragments of undeveloped territories; 6) are omnivorous but can switch to a very restricted kind of food; 7) prefer high calories food but can starve for long periods of time; 8) can freely travel with transport vehicles and therefore became widely distributed and overcome oceanic barriers. The potential for rapid population growth by rodents in anthropogenic biotopes is a key aspect for these species. It is not accidental that prominent representatives of synanthropic animals—the black rat and the house mouse—are included on the list of the 100 most dangerous invasive alien species (100 of the World’s…, 2000). Many other dangerous alien species are similar to synanthropic rodents in their biology. For example, Ehrlich’s review (1989) identified a similar list of properties for successful invaders to that described by Tupikova (1947): large native range; abundant in original territory; ‘r’ tendency of a species to disperse in a given environment; broad diet; short generation cycle; capacity for shifting between r- and k-strategies; high genetic variability; ability to aggregate; females able to colonize alone; larger size comparing to related species; associated with people; able to function in a wide range of environmental conditions.

NORWAY RATS Among more than 60 species of Rattus genus, only two species: Norway or brown rats (Rattus norvegicus) and black or roof rats (R. rattus), have colonized urban ecosystems globally for a historically long period of time. Other species, such as Rattus exulans may be associated with humans, but are less common in urban areas. Black and Norway rats are characterized as historically introduced species, cosmopolitan in their distribution, and alien by their introduction to places where they did not inhabit previously, and mostly living inside

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houses or using other man-made features. These two species are distributed throughout the world principally through occasional introductions. The extent of their range is determined mainly by transport connections and freight traffic. In the past, the distribution depended mainly on cart traffic and ship navigation. The latter was a leading factor for crossing ocean barriers. In the modern world, the role of ground and air transport is increasingly growing. However, this happens more rarely than occasional introductions. In many regions, the network of the area of true synanthropic species depends on the density of settlements. The Norway rat is one of the most common and dominant rodents in the most cities and small towns in both Russia (especially in its European part) and the USA (especially in eastern North America). Though this species is believed to have originated from the plains of Northern China, it has spread to all continents, except Antarctica and with rare exceptions these rats live wherever humans live, particularly in urban areas (fig. 1). The question of when Norway rats became commensal with humans remains disputed, but as a species they have spread and established themselves along routes of human migration and now live almost everywhere humans do. The Norway rats colonized the southern Far-East Russian (Primorsky Krai, Amur region and Transbaikal) in the Late Pleistocene - Holocene (Milutin,1990), may have been present in Europe as early as 1553 and occupied the European part of Russia in the 17th century. Invasion of Norway rats to some parts of Russia continued during the last decades of 20th century, most notably their penetration to the north along the Yenisey River and Lena River reaching Chukotka (Kucheruk, 1990). In Russia, the distribution of Norway rats depends on density of human populations. These rats are practically absent in regions where less one person per square kilometer. In the European part, this species is absent in the middle of Kolskiy peninsula, between Mezen River and Pechora River, and in Bolshezemelnaya tundra. Significant parts of Eastern Siberia

Figure 1. Range of Rattus norvegicus (after Kucheruk, 1990). Shaded parts (1) are areas of continuous distribution of the rats and dots (2) indicate separate findings.

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and Western Siberia are still free from rats. In the Russian Far East, brown rats are reported mainly in urban centers located along transport lines, including seaports (Kucheruk, 1990). Norway rats reached North America much later - between 1750 and 1775 (Nowak, 1999; Silver, 1927). This can explain one of the differences in ecology of R. norvegicus between Russian and the USA such as a more common occupancy of natural habitats by the rats in some parts of Eurasia compared to America. Within the territory of Russia, the degree that rats are restricted to urban environments can vary greatly depending on environmental conditions. In the north-eastern parts of Russia, these rats are strictly synanthropic; in the northern part of European part of Russia Norway rats can migrate to natural habitats during the summer; while in central and southern part of Russia they can live in the natural habitats throughout the year. There Norway rats prefer damp environments, such as river banks, reeds, bamboo, and fields of rice (Kucheruk, 1990; Rylnikov, 2010). Norway rats colonized urban areas practically through all US states. The outdoor Norway rat population in residential neighborhoods in Baltimore, Maryland, was estimated around 48,000 rats (Easterbrook et al., 2005). A survey of 1,363 residents of Baltimore City found that 64% of respondents observed rats in streets but only 6% saw rats inside residences (Childs et al., 1991). This difference reflects the rat’s tendency to burrow under structures in this region. The northern Rocky Mountain States were last remaining sections of this country where much territory was wholly free of rats. According to Silver (1927), rats were reported in Denver in 1886 and by 1907 they were reported in most of the large towns of Colorado. The studies in five states (Colorado, Idaho, Montana, Utah, and Wyoming) conducted from 1947 through 1955 showed that rats were present in each of the above listed States (Harmston and Wright, 1960). In the central Great Plains Norway rats were often associated with agricultural activities and the urban areas that supported them (Bee et al. 1981) and in recent years have become less abundant. The first appearance of rats in Alaska is unrecorded, but as Rausch (1969) stated, the rat became established soon after the arrival of Europeans. It was a report of Norway rats traveling on Russian ships in 1828, and infestation increased steadily. In the early 1940s hundreds of U.S. military ships routinely visited the Aleutians and the rat infestation grew during this time. Since 1950s, presence of Norway rats in Alaska were reported by Clark (1958), Manville and Young (1965), and Haas (1986). In the USA, the Norway rats are mostly restricted to man-made environments, within urban areas, especially at more northern latitudes. Cities like New York are particularly attractive places for rats because of its aging infrastructure, high moisture and poverty rates. Rats are very comfortable living in alleyways and residential buildings, as there is usually a large and continuous food source in those areas (Sullivan, 2003). They commonly occupy areas around warehouses, stores, slaughterhouses, and docks, although most commercial sites are required to maintain rodent control efforts. Thus, populations are often largest in high human density residential areas. The rats build their nests in burrows along the outside the walls of homes or in various clumps of vegetation. Norway rats may also construct their homes under buildings, beneath the edges of sidewalks, concrete patios, along stream banks, around ponds, and in garbage dumps. In more southern regions of the USA, Norway rats also can live away from human populations in more rural areas such as marshes and grasslands (Davis, 1953; Glass et al. 1989; Glass et al. 1998). Though Norway rats can disperse long distances, investigations of marked animals demonstrated that they tend to live within small individual territories that sometimes does not exceed one building (Sudeykin, 1976). A study in Baltimore, Maryland demonstrated that

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most rats remained within 25 m of the burrows during an evening’s foray (Glass et al 1989) and genetic analyses using microsatellite probes showed that rats were assigned to the city block of their capture, indicating strong site fidelity and that rats from one block could be genetically distinguished from rats in the block across the street. (Gardner-Santana et al, 2009). There was evidence of some infrequent, long-distance movement within the city as several rats were assigned to areas 2-11.5 km away (Gardner-Santana et al, 2009). Norway rats are usually active at night and are good swimmers, both on the surface and underwater. Unlike R. rattus they are not especially good climbers though they can climb rough surfaces and tend to inhabit the lower floors of multistory buildings. Norway rats dig well, and often excavate extensive burrow systems (Davis 1953). This rat is a true omnivore and will consume almost anything (Schein and Orgain 1953). Rats require a substantial amount of grain in their diet. In general, the number of rats is directly proportional to the amount of food, e.g. 10g of food supports one rat (Davis, 1951). Foraging behavior is often population-specific, and varies by environment and food source (Fragaszy and Perry, 2003; Glass et al 1989), e.g. rats living near a hatchery in West Virginia caught fingerling fish (Cottam et al. 1948). In urban environments the life span of rats can be up to four years though more than 90% barely manage one (Davis, 1953; Glass et al 1989; Rylnikov, 2010). A yearly mortality rate was estimated around 95% with predators and interspecies conflict contributing to such high rate (Davis, 1948). Norway rats live in large hierarchical groups, either in burrows or subsurface places such as sewers and cellars.

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BLACK RATS The black rat (Rattus rattus) originated in India or Southeast Asia, and spread to the Near East and Egypt, and then throughout the Roman Empire, reaching England as early as the 1st century (Engels, 1999). This species appeared not later than the Neolithic Age on the northeastern coast of the Black Sea. During the 5th century they were introduced north to the Baltic Sea through trade routes along Dnepr River and Don River (Kucheruk, 1991). At that time and later, this species has been introduced through human travel overseas to all continents. Black rats are most often found in large numbers in coastal areas because of the way the species is spread by people via sea ships (Kucheruk and Lapschov, 1994). During the Middle Ages populations of black rats were common in Moscow and other large cities in the Central part of Russia and outbreaks of plague occurred in these regions (Nikolaev, 1968). In 1346– 1350, one third of the human population in Europe perished from the plague and black rats were claimed to be the main source for this pandemic (McNeill, 1976). Black rats are generally found in any area that can support its mainly vegetarian diet. Because R. rattus is an excellent climber and often lives in high places, it can be found in the top floors of buildings or in attics. Even though it can be found near water, this species rarely swims and unlike its close relatives, rarely finds a home in sewers or in aquatic areas. Today the black rat is again largely confined to warmer areas, having been largely driven out by Norway rats in cooler regions and urban areas. The presence of Norway rats is one of the leading factors affecting the distribution and behavior of black rats (Kalinin, 1995). Ecke (1954) recorded a Norway rat invasion through the southwestern part of Georgia, US that almost eliminated the population of black rats in this region. The invasion overran about

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1,000 square miles in six years. Similar processes were observed in Russia starting the 2nd half of the 18th century (Kuznetsov, 1930) and during last decades in Tula region (Panina, 1986). In addition to being larger and more aggressive, the change from wooden structures and thatched roofs to bricked and tiled buildings favored the burrowing Norway rats over the arboreal black rats. In addition, Norway rats eat a wider variety of foods, and are more resistant to weather extremes. Currently, there are two isolated populations of the black rats in the western part of Russia (Pskov region and along Don River from Smolensk region through north of Voronezh region) with occasional reports from cities located on Oka River, Volga River, on the lower reaches of Don River, and on the Black Sea coast of the Caucasus region (Kucheruk, 1991). In the Asian part of Russia, the black rats were mostly reported from sea ports in Primorsky Krai, Sakhalin, and Kamchatka, and sometimes reach mainland cities (Irkutsk region) (Kucheruk, 1994). In the USA, black rats range along the lower half of the East Coast (e.g. Glass et at 1998) and throughout the Gulf States upward into Arkansas. They also exist all along the Pacific Coast and are found on the Hawaiian Islands. Being a better climber then Norway rats, they tend to flee upwards in case of the danger. The home range of R. rattus is usually not more than 100 square meters or even smaller. Black rats generally feed on fruit, grain, cereals, and other vegetation. They are omnivorous, however, and will feed on insects or other invertebrates if necessary. Not only does it gnaw through many materials but it ruins more by excreting on the remains of its foraging efforts (Nowak, 1999). In a suitable environment it will breed throughout the year, with a female producing three to six litters of up to ten young. Females may regulate their production of offspring during times when food is scarce, producing as few as only one litter a year. R. rattus lives for about 2–3 years. Social groups of up to sixty can be formed.

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HOUSE MICE House mouse (Mus musculus s.l.) has spread to all continents (fig. 2). Investigations of house mice by using different genetic markers demonstrated that Mus musculus represents a complex of closely related forms of different taxonomic ranks (Wilson & Reeder, 2005). Several taxonomic groups of house mice can be identified within the territory of Russia (Yakimenko et al., 2003; Spiridonova et al., 2008). Those include M. m. musculus in the west of the Black Sea coast, M. m. wagneri in the northern Caspian zone, and M. m. castaneus in the south of Russian Far-East. Yonekawa et. al. [2003] could not find any domestic-type mtDNA in East of Russia before 1996, but now it was found near Vladivostok and Irkutsk. It was suggested that M. m. domesticus was introduced in Russia after 1996, probably via the Vladivostok port and spread around Vladivostok city. The most taxonomic groups of M. musculus can hybridize between themselves. Hybrid zones between these groups can be narrow or quite wide [Boursot et al, 1993; Sage et al., 1993; Yakimenko et al., 2000; 2003; Kotenkova, 2002; Spiridonova et al., 2011 and other]. The oldest record of mice of the genus Mus on the territory of Russia (Lower Volga region) is dated to the second half of the Middle Pleistocene (Tesakov and Kirillova, 2007), but synanthropic mice Mus musculus colonized Europe in the Late Pleistocene (Klein et al., 1987; Lavrenchenko, 1994; Bonhomme et al., 1994). It is possible that, during this period,

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Figure 2. Area of distribution of Mus musculus s.l. (after Kucheruk, 1994). Shaded parts (1) are areas of continuous distribution of the house mouse and dots (2) indicate separate findings.

they might have penetrated to northern latitudes where encampments of ancient hunters and scavengers were discovered (Verpoorte, 2008). However, the scale of these invasions could not have been large. In Russia house mice exist where the density of human populations is above one person per one square kilometer and also where arable land is present. The house mouse (M. musculus) is not so demanding in its need for abundant food and water compared to Rattus rats. These rodents can be well established in separate buildings and even within an individual apartment. There are three ‘belt’ zones within the territory of the former USSR based on the association between house mice and the natural environment (Tupikova, 1974, fig. 3). In the northern zone, house mice can live only inside buildings. In the second zone, located immediately south, house mice can occupy natural habitats within 1-2 km from urban centers during summer, but they always return to human houses during a cold season. In both above mentioned zones, house mice can survive only in close association with human dwellings and, when people abandon these places, the mice disappear as well (Chabovsky, Dargolts, 1964; Istomin, 1994; Kucheruk, 1994; Shilova, Kalinin, 1994). In the third (southern) zone, including Primorsky Krai, house mice can leave both within urban centers, and in the field and some natural habitats where they can survive a whole year around. Because arable land significantly expanded during 1990s, house mice have practically occupied all territory within the third zone. As a result, the total number of house mice has increased up to a hundred fold during this period (Tupikova et al., 2000; Neronov et al., 2001). In the USA Mus shows many similar habitats to those seen in Russia. In urban areas this species is often associated with high density human residential areas, living in the spaces between common walls and foraging at night within the human habitation. There is substantial clustering of family groups within households of a neighborhood (Childs et al 1992). In the more mild climate of the southern US, house mice will live away from human residences throughout the year, in grasslands and marshes (Korch et al 1989).

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Figure 3. Distribution of house mice in Russia (Tupikova 1947; Khlyap, Warshavsky, 2010): 1) synanthropic populations only; (2) synanthropic populations all year round, agrophilic and exoanthropic in summer only; (3) synanthropic, agrophilic, and exoanthropic populations all year round; (4) as 3, but agrophilic populations prevail. Time of penetration: (all shading and triangles) the area as of the first half of the 20th century; (solid circles) house mice noted in the second half of the 20th century.

WILD RODENTS WITHIN URBAN TERRITORIES Although the most common mammals in urban environments are Rattus rats and Mus mice, some wild rodents also invade urban territories and can be especially common in areas undergoing development and conversion from rural landscapes to ones that are more urbanized. These species can dominate in areas that are only moderately urbanized and still contain significant patches of natural rodent habitat (Gage and Kosoy, 2008). Voles are among the most common wild rodents in cities and small towns of Russia and can be found in some US cities as well. Bank voles (Myodes glareolus) are common in the deciduous woodland regions of the European part of Russia. Bank voles require ground cover and are found most frequently in hedgerows, banks, roadsides, city parks and other wellvegetated areas, although in the northern reaches of Europe they can be found on relatively open ground, and they have been reported to enter homes. They are often considered pests, because of their habit of stripping bark from small trees, especially larch, elder and young conifers. Among other species of Myodes, the northern red-backed vole (M. rutilus) can found in urban and rural areas in Siberia and the Far East of Russia, and southern red-backed vole (M. gapperi) can be found in coniferous, deciduous and mixed forests in the western United States.

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More than 40 species of Microtus voles are known to exist. Important species include the East European vole (Microtus levis) and common vole (Microtus arvalis) in European part of Russia (Kucheruk, 1988; Tikhonova et al. 2001, 2006), reed vole (Microtus fortis) in Transbaikalia and the southern Far East, root vole (Microtus oeconomus) in Yakutia and narrow-headed Vole (Microtus gregalis) in Yakutia and South Siberia. These species also occur in gardens and open woodlands, as they seek out their primary food sources, which consist of grasses, as well as the stems, roots and bark of other plants. At least 17 species of Microtus voles occur in North America. Among the most important of these are the meadow vole (M. pennsylvanicus), California vole (Microtus californicus), prairie vole (Microtus ochrogaster), montane vole (Microtus montanus) and long-tailed vole (Microtus longicaudus). The meadow vole occurs in moist grassy fields and meadows over much of the northern two thirds of North America. The California vole occurs throughout much of California and southern Oregon in low-elevation grasslands, wet meadows, coastal wetlands and open oak savannahs with adequate ground cover (Kays & Wilson, 2002). Muskrats (Ondatra zibethicus) are basically large aquatic voles that are native to North America, but have been transplanted to many regions in Eurasia. They occur frequently in ponds and waterways in suburban and largely urban areas both America and Russia. Mountains species of voles are rarely can be found in towns: Alticola strelzowi and A.barakshin occur in the in the mountains of Siberia, voles of genus Chionomys - in Caucasus Mountains. Near 13 species of subfamily Cricetinae are known in Russia, 8 of them are found in human settlements. They are: Cricetulus barabensis (it is common in settlements of the steppe regions of Buryatia and Chita, and also leads among rodents trapped in the buildings of Tuva and Ubsunursk basins and high mountains of Tuva), Allocricetulus eversmanni, Phodopus sungorus, Phodopus campbelli, Cricetulus longicaudatus, Tscherskia triton, Cricetulus migratorius, Cricetus cricetus. For example, in Moscow, there is an island population of Cricetus cricetus (Karaseva et al., 1999) that is separated from the main part of the area for tens of kilometers to the north.Mice of the genus Apodemus can occupy urban centers of Russia in both European and Asian parts. They eat primarily grasses, seeds, nuts, fruits and other plant materials, as well as some insects and snails. Striped field mice (Apodemus agrarius) and pygmy field mice (A. uralensis) are widely spread and persistent species in some cities of Russia. The striped field mice enter houses, barns and stables and have been reported to colonize highly urbanized areas (Kucheruk, 1988; Tikhonova et al. 2001, 2006); this process is well described in Warsaw, Poland (Andrzejewski et al., 1978). Being highly adaptable, they often occupy gardens and city parks and will enter houses in winter, particularly when house mice are absent. Another species of Apodemus, the yellownecked mouse (A. flavicollis) is also common in woodlands, hedgerows, field margins, orchards and wooded gardens. Yellow-necked mice also frequently enter homes as winter approaches, but typically depart by spring. They are known to store caches of nuts in small spaces and under floorboards. In the Russian Far East, these mice replaced with Apodemus peninsulae (Kucheruk, 1988). All 3 species of gerbils in Russian can occur in the human settlements. The most important is Meriones unguiculatus that is common in the southern of semi-desert part of Tuva (Kucheruk, 1988). In the USA, native rodent species commonly belonged to the subfamily Sigmodontinae that contains a wide variety of species, including some that occur near human habitations. The most important genera are Peromyscus (deer mice and their allies), Neotoma (wood rats) and Sigmodon (cotton rats). Carlton (1989) recognized 53 species of Peromyscus, and all of these

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are likely to invade human dwellings under certain circumstances (Cahalane, 1961). However, the two species of Peromyscus most likely to be encountered by people are the widespread deer mouse (P. maniculatus) and white-footed mouse (P. leucopus) (Glass et al 1997; King, 1968; Kays & Wilson, 2002). Both species are abundant over large areas of the USA, with the deer mouse occupying all but the south-eastern portion of temperate North America and the white-footed mouse occurring over the eastern half of the continent and in portions of the south-western US. In many respects, including behavior, appearance and general ecology, these mice resemble European species of Apodemus mice and can be considered ecological equivalents. Peromyscus mice consume a variety of seeds, other vegetable matter and insects. Deer mice are particularly common in grasslands or mixed grass and brush habitats; white-footed mice are more likely to occur in woodland or mixed woodland and brush habitats. Both species will enter homes and other buildings, particularly as winter approaches. Their gnawing near nest entry points on homes or other structures can cause limited damage to wood siding and their excreta can create an unsanitary situation. Although wood rats (Neotoma spp.) occur in both the eastern and western portions of temperate North America, the diversity of species is greatest in the western half of the continent. Their other name (pack rats) comes from the distinctive nests they build, which consist of large piles of sticks that are often placed at the base of a tree or sometimes next to a man-made wall. Several species of Neotoma woodrats are known to build their nests in the walls or crawl spaces of homes, garages or other buildings. The gnawing activities of these rats, as well as the extensive piles of excreta associated with their nests, can result in damage to homes or other property and cause an unsightly mess. Cotton rats (genus Sigmodon) are common in grassy and weedy fields in many areas of southern US. The most important species in the temperate regions of the continent is the hispid cotton rat (S. hispidus), which is often extremely abundant in thick grassy habitats in the south-eastern and south-central United States (Cameron & Spencer, 1981; Glass and Slade 1980). In many ways, the behavior and ecology of cotton rats resemble those of voles, which are more common in the northern parts of the continent. These similarities include not only types of habitats selected, but also include the construction of grass nests and runways, extremely high reproduction rates and populations that often fluctuate dramatically from year to year. Cotton rats can be destructive to food supplies. Chipmunks are members of the genus Tamias. The Siberian chipmunk (Tamias sibiricus), which can be found frequently in parks and towns, is widely distributed in parts of the Russian Federation (the north-eastern part of Europe, Siberia and the far-eastern part). The 22 species of North American chipmunks occur primarily in the mountain forests and nearby sagebrush habitats of the western third of the continent. A single species, the eastern chipmunk (T. striatus), occurs abundantly in the deciduous forest regions of the eastern United States and south-eastern Canada, routinely entering yards and gardens in many suburban areas (Mahan & O’Connell, 2005). Some western species occasionally invade homes, where they build nests in attics or wall spaces, sometimes damaging these structures in the process. Invaded spaces are often partially filled with large stockpiles of nuts, pine cones and other edible items. Although chipmunk nesting and hoarding activities can cause some damage, they are of little economic importance. Their primary foods are fruits, nuts, berries, seeds and occasional invertebrates.

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Tree squirrels provide a classic example of the successful use of urbanized environments by rodents. In the European part of Russia the red squirrel (Sciurus vulgaris), is the most common species of tree squirrel and in the USA common tree squirrels include the gray squirrel and fox squirrel (Sciurus niger) in the eastern United States. Both species are common in urban environments, and the latter has been introduced into various cities in the western United States. Glaucomys spp (flying squirrels) occasionally invade attics and wall spaces in mountainous areas. Although tree squirrels forage on the ground, they rarely stray far from a tree, where they can flee to safety. These squirrels also can occur at high densities in parks and gardens, raising the likelihood of contact with people. Another big group of rodents belonging to the family Sciuridae that can occupy urban habitats in the USA and some Asian parts of Russia are ground squirrels (genus Spermophilus). Because ground squirrels are large and active during daylight hours, people frequently notice them, and some enjoy having them near their homes, while others consider them destructive and try to eliminate them. North American species of ground squirrels are found primarily in the western grasslands, mountains and deserts, although a couple of species have ranges that extend into the eastern half of the continent. In many instances, these ground squirrels live in wilderness or highly rural areas, but a few species occur regularly near human dwellings and city parks, where they can damage structures, gardens, orchards, crops and other items. Foremost among the ground squirrels encountered in peridomestic environments are two closely related species, the rock squirrel (Spermophilus variegatus) and the California ground squirrel (S. beecheyi). Rock squirrels occur throughout much of the south-western United States and California ground squirrels are found in many areas of California, western Nevada and southern Oregon. Both species behave similarly and often dig burrows under concrete slabs, woodpiles or other sites near people’s homes (Oaks et al., 1987; Jameson & Peeters, 2004). Some have suggested that rock squirrel numbers in the south-western United States have increased as a result of home building and other human activities that provide these animals with novel sources of food (such as pet foods, seeds from bird feeders and water from dripping faucets) and shelter (such as rock piles and walls) (Barnes, 1982). A third species of ground squirrel, the golden-mantled ground squirrel (S. lateralis), can occur near human dwellings in mountainous areas of western North America. It is frequently encountered in recreational sites, including heavily used campgrounds in California and adjoining areas, as well as many regions of the Rocky Mountains. Other species of North American ground squirrels also occur occasionally near human habitations, but they generally have limited distribution in urban environments. Within the Russian territory Spermophilus undulatus occurs in towns in the Altai and Spermophilus parryi in the Yakutia [Kucheruk, 1988]. Prairie dogs are the most common sciurid rodents in some urban areas of the western US, especially in small cities of Colorado, Wyoming, Montana, South Dakota, Kansas, Arizona and New Mexico. Among the five prairie dog species, the blacktailed prairie dog (C. ludovicianus) is most likely to occur in close proximity to people, being fairly common in many suburban and even some urban areas, particularly those along the Front Range of the Colorado Rocky Mountains, a region that includes the Denver Metropolitan Area and numerous smaller cities. In some instances, small colonies of this species occur in isolated patches of habitat that are almost completely surrounded by urban development. When living in urbanized environments, prairie dogs can be destructive to shrubs or other plants that are eaten for food or instinctively cropped, White-tailed prairie dogs (C. leucurus) are quite abundant and widespread, but also typically live in environments

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far removed from major urbanized areas (Clark et al., 1971). The closely related Gunnison’s prairie dog (C. gunnisoni) is found on the Colorado Plateau and surrounding regions of the south-western United States. Unlike the above three species, Gunnison’s prairie dogs often establish colonies near human dwellings, such as near Albuquerque, New Mexico. Within urban areas in Russia there were also reported of members of families Castoridae (Castor fiber in Moscow), Dipodidae (Allactaga sibirica – Altai, Sicista betulina – Moscow), Gliridae (Muscardinus avellanarius – Moscow, Dryomys nitedula – near Makhachkala, and Glis glis – Caucasus). Urban development clearly creates dramatic changes in rodent communities. The higher level of urbanization, the higher intensity of changes in fauna of rodents within city limits can be observed. Commonalities between analyzed geographic areas include a dominance of Norway rats and house mice, which have historically colonized urban ecosystems, globally. Some differences in their ecology between two countries can be partially explained by the fact that these species were introduced into the USA much later than to the European and Asian parts of Russia. The wild rodents that occupy urban territories in both countries can represent many other species and species compositions are influenced by rodent communities in natural habitats surrounding cities. Various aspects of the biology of urban rodents, such as enormous reproductive potential, feeding behavior and adaptations to city environment contribute to the failure of many rodent control programs, but also grant a necessity to investigate many aspects of biology and ecology of these animals. There is a need for characterization of demographic and population density changes of rodents caused by urbanization and its effect on their diversity, ecology, and behavior patterns, including their dispersal rates. Development of mathematical models based on such information can be useful in predicting expansions of rodent species in areas that were not infested by rodent of these species. The possible effects of climate changes on distribution of urban rodents should be also further investigated.

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Kotenkova, E. V. 2000. Synanthropic and Wiled Mice of the superspecies Complex M. musculus s. l.: Systematics, Distribution, Mode of Life, Isolation Mechanisms, and Evolution, Extended abstract of Doct. Sci. (Biol.) Dissertation, Moscow, 56 p. [in Russian]. Kotenkova, EV. 2002. Hybridization of synanthropic species of house mice and its role in evolution. Uspehi sovremennoi biologii, v. 122 (6): 580-593 [in Russian] Kotenkova EV, Muntyanu AI. 2007. Phenomenon of synathropy: adaptation and development of synanthropic style of life in the process of evolution of house mice Mus musculus L. Uspehi sovremennoi biologii, v. 127 (5): 525-539 [in Russian] Kucheruk V. V. 1965. Synanthropic Rodents and their Significance in the Transmission of Infections, In: Theoretical Questions of Natural Foci of Diseases, Proceedings of a Symposium held in Prague, Ed. B. Rosicky and K. Heyberger, Prague, 1965, pp 353-366. Kucheruk, V. V. 1988. Rodents as inhabitants of buildings and human settlements in various regions of the USSR, In: General and Regional Theriogeography, Ed. A. G. Voronov, Moscow: Nauka, pp. 165-237. [in Russian]. Kucheruk V. V. 1990. Area. In: Seraya krysa: sistematika, ekologiya, regulaytrsiya chislennosti (The Norway rat: Systematic, Ecology, Abundance, and Control), Eds. V. E. Sokolov and E. V. Karaseva, Moscow: Nauka, pp. 34–84. [in Russian]. Kucheruk V. V., 1991. The area of the black rat in the USSR. The European Part and the Caucasus, Byull. Mosc. Obschestva isp. Prir., Biol., vol. 96, 6, pp. 19–30. [in Russian]. Kucheruk, V. V., 1994. The area of house mice of the superspecies complex Mus musculus s. lato, In: House Mouse: Origin, Distribution, Systematics, Behavior, Eds. E. V. Kotenkova and N. Sh. Bulatova, Moscow: Nauka, pp. 56–81. [in Russian]. Kucheruk, V. V., 1994a. Distribution of black rat in Russia: Siberia and Far East, Byull. Mosc. Ob_va isp. Prir., Biol., vol. 99, 5, pp. 33–36. [in Russian]. Kucheruk, V.V., Karaseva, E.V., Synathropy of Rodents, in: Synanthropy of Rodents and Control of Their Abundance, Eds. V. E. Sokolov and E. V. Karaseva, Moscow: RAN, 1992, pp. 4-36. [in Russian]. Kucheruk VV, Lapschov VA, 1994. Transoceanic area of the black rat (Rattus rattus L.). Zoologicheskyi Zhurnal, v. 73(8): pp 179-193. [in Russian]. Kulik, I. L. 1979. Mus musculus Linnaeus, 1758—the House Mouse, in: Medical Theriology, Ed. V. V. Kucheruk, Moscow: Nauka, , pp. 204–218. [in Russian]. Kuznetsov BA 1930. Black rat (Epimys rattus L.) in Maloyaroslavetsky district of Kaluga province. Proc.Forest experienced the case. Vol. 7. M.: TSLOS. pp. 143-150. Lavrenchneko, L. A., 1994. Formation of Recent Area of House Mice. 2.1. Possible Pathways of Evolution and Distribution, In: The House Mouse: Origin, Distribution, Systematics, Bahvior, Eds. E. V. Kotenkova and N. Sh. Bulatova, Moscow: Nauka, pp. 51-55. [in Russian]. Lambropoulos, A.S., Fine J.B., Perbeck, A., Torres, D., Glass, G., Mchugh, P., Elias A. Dorsey, E.A. 1999. Rodent control in urban areas: an interdisciplinary approach. Journal of Environmental Health, Vol. 61, Lund, M. 1994. Commensal rodents. In: Rodent pests and their control. Buckle, A.P., and Smith, R.H. (eds). CAB International. Mahan CG, O’Connell TJ. 2005. Small mammal use of suburban and urban parks in central Pennsylvania. Northeastern Naturalist, 12:307–314.

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Manville RH, Young SP. 1965. Distribution of Alaskan mammals. U.S. Department of the Interior, Bureau of Sport Fisheries and Wildlife Circular 211. 74 pp. McNeill, W.H., 1976. Plagues and Peoples, Garden City, New York: Anchor Press, Doubleday, Meerburg, B.G., Singleton, G.R., Kijlstra, A. 2009. Rodent-borne diseases and their risk for public health. Critical Rewiews in Microbiology, 35 (3): 221-270. Milutin, A. I., 1990. Systematic, In: Seraya krysa: sistematika, ekologiya, regulaytrsiya chislennosti (The Norway rat: Systematics, Ecology, Abundance Control), Eds. V. E. Sokolov and E. V. Karaseva, Moscow: Nauka, pp. 7–33. [in Russian]. Neronov, V. M., Khlyap, L. A., Tupikova, N. V., Warshavsky. 2001. Investigation of Formation of Communities of Rodents on Arable Lands of Northern Eurasia. Ekologiya, No. 5, pp. 355–362 [in Russian, English translation as: Neronov, V.M., Khlyap, L.A., Tupikova, N.V., and Warshavsky A.A., Formation of Rodent Communities in Arable Lands of Northen Eurasia, Russian Journal of Ecology, vol. 32 (5), pp. 326–333]. Nikolaev, N. I., Chuma (klinika, diagnostika, lechenie i profilactica) (Plague (Clinics, Diagnostics, Treatment, and Prevention)), Moscow: Meditsina, 1968 [in Russian]. Nowak, R. 1999. Walker's Mammals of the World (6th Edition). Baltimore, Maryland: Johns Hopkins University Press. Nour N, Matthysen E, Dhondt A. 1993, Artificial nest predation and habitat fragmentation: different trends in bird and mammal predators. Ecography, 16 (2): 111-116. Oaks EC et al. 1987. Spermophilus variegatus. Mammalian Species, 272:1–8. Panina TB, 1986. Expansion of area of the Norway rat in Tula region and interrelations between the Norway rat and the black rat. In: Seraya Krysa (Ekologiya I Rasprostranenie), part 1, Moscow, pp. 178-216. [in Russian]. Pelican J., Zeida J., Homolka M., 1983. Mammals of the urban aglomeration of Brno Acta scientarium naturalium academiae scientiarum bohemoslovacae Brno. 49 p. Psychological Mechanisms of Adaptation of Higher Veretabrates to the Urbanized Environment), Moscow: Argus, 1996. Rausch R.L. 1969. Origin of the terrestrial mammalian fauna of the Kodiak Archipelago. Pp. 216-234. In: The Kodiak Island refugium: its geology, flora, fauna and history. Eds: T.N.V. Karlstrom and G.E.Ball. Rechkin AI, Ladygina GN, Dmitriev AI, Zimoreva Zh. 2001. City’s small mammals as reservoirs of anthropogenic pathogens. Features in distribution of small mammals within the Territory of Nizhnyi Novgorod. Annals of the Nizhnyi Novgorod University named after N. Lobachevsky, Issue 1, p. 49-51. [in Russian]. Rylnikov V.A. Brown rat /Rattus norvegicus Berk./ Ecological bases and approaches to management of number /Ed. Schilova S.A. M: Institute of Pest Management; 2010. [In Russian] Sage R.D., Atchley W.R., Capanna E. House mice as a model in systematic biology Systematic Biology. 1993. V. 42. P. 523-561. Schein, M.W., Orgain, H. 1953. A preliminary analysis of garbage as food for the Norway rat. Am J Trop Med Hyg. 2:1117-1130. Silver, J. 1927. The introduction and spread of house rats in the United States. Journal of Mammalogy 8 (1): 58-60. Shilova SA, Kalinin AA. 1994. Abandoned villages: the problem of the fauna dynamics. In: Synatropia gryzunov, Moscow, pp. 101-108 [in Russian]

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Sokolov V. E., Karaseva, E. V., 1985. The Norway Rat - a life form of synanthropic rodent, In: Distribution of Ecology of Norway Rat and Methods of Its Abundance Control, Eds. V. E. Sokolov and E. V. Karaseva, Moscow: Nauka,1985, pp. 6-17. [in Russian]. Spiridonova, L.N., Korobitsina, K. V., Yakimenko, L. V., Bogdanov A.S. Генетическая дифференциация подвидов домовой мыши Mus musculus и их таксономические взаимоотношения: данные RAPD-PCR анализа Genetics. 2008. V. 44, 6, p. 841–849. Spiridonova, L.N., Kiselev K.V., Korobitsyna, R.V. Несогласованность распространения маркеров разных систем наследования (я-, мтДНК и хромосомы) в надвидовом комплексе Mus musculus как следствие обширной гибридизации в Приморье Genetics. 2011. V. 47, 1, p. 115-125. Sullivan, R. 2003. Rats: observations on the history and habitat of the city's most unwanted inhabitants. New York: Bloomsbury Tesakov, A. S., Kirillova, I. V., 2007. Mice of the Genus Mus in the Middle Pleistocene of the Lower Volga: Synanthropic or Natural Element? In: Theriofauna of Russia and of Adjacent Territories, International Conferecne, January 31—February 2, , Moscow, Ed. V. V. Rozhnov, Moscow: KMK, 2007, p. 491. [in Russian]. Tikhonova GN, Tikhonov IA, Bogomolov PL, Bodyak ND, Surov AV. 1997. Small mammals occupying areas near railroad tracks. The Advances of Modern Biology (Uspehi Sovremennoi Biologii), 117 (3): 310-323. [in Russian]. Tikhonova GN, Tikhonov IA, Bogomolov PL, Polyakova LV. 2001. Distribution and abundance of small mammals in nonbuilding territories of small cities. Zoologicheskyi Zhurnal, v. 80 (8): pp 207-216. [in Russian]. Tikhonova GN, Davi’dova LV, Tikhonov IA, Bogomolov PL. 2006. Small mammals in Yaroslavl. Zoologicheskyi Zhurnal, v. 85 (10): pp 277-283. [in Russian]. Tupikova, N. V. 1947. Ecology of House Mouse in the Temperate Zone of the USSR. In: The Fauna and Ecology of Rodents, Ed. A. N. Formozov, Moscow: Mosk. Obschestvo Ispytateley Prirody, 2, pp. 5-67. [in Russian]. Tupikova, NV, Khlyap L A, Warshavsky AA, Rodents of Fields of North-Eastern Palearctic, Zool. Zh., 2000, vol. 79, no. 4, pp. 480–494. [In Russian] Wilson, D. E., and D. M. Reeder (eds). 2005. Mammal Species of the World: A taxonomic and geographic reference (3rd ed). JohnHopkins University Press, 2, 142 pp. Verpoorte, A., Geagraphic Area of Man of the Recent Type: Dynamics of the Northern Boundary of Man at the Verge from the Pleistocene to the Holocene, in: Evolution of Ecosystems of Europe at the Verge from the Pleistocene to the Holocene (24000_8000 years BP), Eds. A, K, Markov and T. Van Kofshoten, Moscow: KMK, 2008, pp. 489_518. [in Russian]. Yakimenko, L. V., Korobitsina, K. V., Frisman, L. V., Morivaki, K., Yonekawa H. Genetics studies on house from the hybrid zone of Primorskii Krai Russian J. Genetics. 2000. Vol. 36, pp. 66-75. Yakimenko, L. V., Korobitsina, K. V., Frisman, L. V., Morivaki, K., Yonekawa H., Cytogenetics and Systematics of House mice of Russia and of Adjacent Countries, In: Problems of Evolution, Eds.A. P. Kryukov and L. V. Yuakimenko, Vladivostok: Dalnauka, 2003, vol. 5, pp. 62-89. [in Russian]. Yonekawa, H., Tsuda, K., Tsuchiya, K. Yakimenko, L.V., Korobitsyna, R.V., Chelomina, G.N., Spiridonova, L.N., Frisman, L.V., Krykov, A.P., and Morivaki K., Genetic diversity, geographic distribution and evolutionary relationships of Mus musculus

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subspecies based on polymorphisms of mitochondrial DNA, In: Problems of Evolution, A. P. Kryukov and L. V. Yuakimenko, Eds. Vladivostok: Dalnauka, 2003, vol. 5, pp. 90– 108. Zjigarev, I. A., Melkie mlekopitayushchie rekreatsionnykh i estestvennykh lesov Podmoskovya (Small mammals of recreational and natural forests of Moscow area), Moscow: Prometei, 2004. [in Russian].

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ISBN: 978-1-61470-833-9 ©2012 Nova Science Publishers, Inc.

Chapter 2

EXTRINSIC AND INTRINSIC FACTORS OF REGULATION OF REPRODUCTIVE POTENTIAL IN THE WATER VOLE (ARVICOLA AMPHIBIUS) POPULATION FROM WESTERN SIBERIA Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka, Olga F. Potapova and Vadim I. Evsikov Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia

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ABSTRACT The European water vole (Arvicola amphibius) dominates in rodent assemblies in Northern Baraba Lowland (Western Siberia) where its populations exhibit pronounced 4– 9 year-long cyclic fluctuations in numbers. One of the principle peculiarities of water voles ecology in West Siberia is usage of different habitat sites during reproductive season and wintering. In summer they are aquatic and live and reproduce in wetlands, while in winter they are fossorial and live underground in meadows. The water vole has proved an excellent model species to investigate the role of both extrinsic and intrinsic mechanisms in driving population cycles. Using data from multi-annual study, we investigated the dependence of female’s breeding success on extrinsic conditions influencing the availability of wet biotopes, food resources and intrinsic factors (density dependent). We also investigated the relation of winter survival to mass of food storage. Abiotic factors have a direct influence on the availability of habitat-related resources. In summer, the main extrinsic factor influencing reproductive potential of the water vole is hydrological regime, i.e. variable water supply determining the area of suitable biotopes. Our analysis has revealed correlation between flow intensity of the Om River in the study area and population dynamics, average number of live embryos in overwintered females, and percentage of mature young-of-the-year females in different years of study. Female reproductive characteristics appeared to be sensitive to effects of both extrinsic (availability of suitable biotopes) and intrinsic (density) factors. It was found that

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Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka et al. interaction of these factors determines the level of competition among reproductively active females as detected by number of injuries on skins and consequently embryonic losses and decline of population numbers. In severe continental Siberian climate winter survival of voles depends on amount of food stores which, in turn, depends on population density influencing competition level. Participating of the young-of the-year females in reproduction has effect on their winter survival. They stay in wet biotopes for late summer and have not enough time to gather necessary for safe wintering amount of food stores. Because of higher female winter mortality, sexual structure of the population in spring is unbalanced. This leads to high level of inter-male competition for receptive females and strong selection among overwintered males. Thus, the obtained data indicate that in the water vole from Western Siberia the extrinsic and intrinsic factors closely interact both in summer and in winter regulating reproductive potential and density of the population.

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INTRODUCTION Regular cycles of animal numbers are well known in northern populations of lemmings and voles [Krebs & Myers 1974]. A central issue in population studies lies in determining the mechanisms of density regulation. Discussing causes, factors, and mechanisms of cyclic population dynamics, ecologists have not yet agreed upon the role of external factors in fulfillment of biological potential of populations [Duhamel et al. 2000, Krebs 2002, Zhigal’skii 2002, Rogovin & Moshkin 2007]. Because none of the more than 20 proposed hypotheses is sufficient to explain the cycles’ phenomenon [Saucy & Gabriel 1998], it is obvious that in general a combination of factors acts to regulate population numbers [Lidicker 1999]. In practice, populations respond to both extrinsic factors such as climatic oscillations and habitat heterogeneity, and intrinsic factors such as density, sexual structure and behavioral tendencies. The effect of external factors is mediated through individual physiological and behavioral responses of individuals and manifests at the level of local reproductive groups in different ecological conditions. Individual and “family” heterogeneity facilitates maintaining homeostasis in a population. Nevertheless, in particular situations one or a few regulating factors may be considered determinative [Lidicker 1999]. Multi-annual oscillations of population number may be related to climatic cycles which are known in the Northern Hemisphere [Saucy & Gabriel 1998]. In Western Siberia, they develop first of all into cycles of humidity [Maksimov 1982]. The humid phase is characterised by low summer temperature, high precipitation, extended surface of water-filled wetlands and maximal river flow. The expansion of the water-bearing wetlands suitable for reproduction of water voles provides condition for the outbreaks of their “mass breeding” and increase in the numbers [Maksimov 1982]. Widespread in Eurasia, the European water vole (Arvicola amphibius (Linnaeus, 1758)) dominates in rodent assemblies in Northern Baraba Lowland (the forest-steppe zone of Western Siberia) where populations of this species exhibit pronounced regular cyclic fluctuations in numbers [Evsikov et al. 1997]. In the course of four- to nine-year cycles, their numbers changes drastically up to four orders of magnitude, comparing the maximal and minimal values [Rogov 1999]. In Western Siberia, water voles change their habitat sites twice during life cycle. In summer they are aquatic and live and reproduce in wetlands and along

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Extrinsic and Intrinsic Factors of Regulation of Reproductive Potential …

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banks of natural streams and artificial ditches, while in winter they are fossorial and live underground in meadows. Vast range, pronounced population dynamics, specific life style, and a huge body of accumulated data make the water a convenient model for solving theoretical problems of population ecology [Panteleyev 1971, 2001a, Maksimov 2001]. The first part of our work is aimed to determine how existing habitat hydrology affects intra-specific competition, reproduction, and population dynamics in the water vole, and differentiation of reproductive groups in density and demographic structure, i.e. structural and functional stability of the population of interest. The aim of the second part of the present study was to test the hypothesis of winter food deficit as a possible cause for population decline and so as one of the main factors for cyclicity in Siberian water voles. Since any biological system consists of interacting parts but functions as a unit in higher level context [Lidicker 1988], better understanding of population processes requires “looking in and looking out” of the system [Lidicker 1999]. We adopt this concept and try to “look in” – on different intrinsic demographic factors (density, the role of age/sex cohorts) and “look out” – on the interrelation of the population and its environment. We investigated the dependence of breeding success and survival on environmental conditions (water supply in summer and food availability in winter) and intrinsic effects in the water vole, using data from long-term study commenced in 1980 in Northern Baraba Lowland (vicinity of Lisii Norki village, Ubinskoye rayon, Novosibirsk oblast, 55°50 N, 80°00 E.).

POPULATION REGULATION IN REPRODUCTIVE SEASON

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Materal and Methods Long-term hydro-meteorological data were obtained from State Institution “Novosibirsk Center for Hydrometeorology and Environmental Monitoring”. Since flow intensity of minor Baraba rivers can be an indicator of the humidity, or amount of water in the study area [Maksimov et al. 1979], we used data on summer total runoff and monthly, May through July, flow intensity of the Om River measured at the gauging station in Kreshchenskoye village, the nearest point to the study area. An index of area of watered biotopes was calculated from summer runoff raised to the power of 2/3. Population numbers (voles/km2) were estimated in May and August every year [Rogov 1999, Rogov et al. 1999]. From these data we calculated the rate of population growth over the breeding season. Percentage of males in May indicated intensity of inter-male competition for reproductive resource. Percentage of females, taking into account the total population numbers allowed us to estimate female density per 1 km2 of the studied area. Female density divided by the area index of watered biotopes indicated strength of inter-female competition for essential resources. When studying the effect of local hydrology on the structure of reproductive settlements, we used data obtained in 1994, 1997, 1999, 2008, and 2009. Wetlands, characteristic habitats of the water vole, have seasonal and year-to-year hydrological fluctuations. In years of low water they may remain uninhabited by water voles. The banks of perennial water bodies, e.g.

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Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka et al.

lakes, streams, rivers, anabranches, and man-made channels, were inhabited by reproductive groups during breeding seasons in all study years [Panteleyev 1971]. To obtain comparable data for the entire study period, we trapped voles with “Kulunda” live traps [Barbash et al. 1971] set at 10 m intervals in local settlements along the banks of irrigation channels that had been built decades ago. The trapping was conducted at the peak of breeding season, mid May through early June. Evsikov and co-workers [1999b] showed that with pronounced population waves in total numbers, the average density of breeding individuals in reproductive groups remains relatively stable, while the average density of populations varies annually. Nevertheless, the intra-annual variability of local densities allows their classification. Local density of the animals in the settlements was calculated as the number of reproductively active voles per 100 m of bank line [Plyusnin 1985, Plyusnin & Evsikov 1985, Evsikov et al. 1999b]. Each settlement was identified as “dense” if its numbers were higher than local mean annual density or “sparse” if its numbers were lower. Data on 318 individuals of 26 local populations were analyzed. Water depths measured at 0.5 m from the water edge perpendicular to the live traps were supplied with data on the amount of water at every settlement. At autopsy, the captured animals and their internal organs were weighed, and animals’ reproductive status was determined. The voles were identified as either overwintered or young-of-the-year according to the external traits and reproductive organs. Female reproductive characteristics were estimated from the state of the uterus and ovaries. Embryo loss was calculated as the difference between the number of corpora lutea in the ovaries and live embryos in the uterus, divided by the number of corpora lutea. The number of injuries (wounds and scars) on the inner side of the skins in females and males served as measure of intensity of intra-specific aggressive interactions [Rose 1979, Plyusnin 1985].

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Results and Discussion Some authors supposed that the role of a “pace maker” of the population dynamics is played by changing amount of water in the habitat [Maksimov 1959, Evsikov & Moshkin 1994]. However the effect of varying hydrology on population structure has not been studied well. Our analysis of the effect of total amount of water in the habitats on the population numbers revealed that May–August population growth correlates positively with the Om flow intensity in the study area in May (r16 = +0.60, p < 0.01), June (r16 = +0.67, p < 0.01), and July (r16 = +0.47, p = 0.05). This is evidence that reproduction rate is dependent on climate (habitat hydrological regime). Nevertheless, the multi-year data show that the numbers may continuously grow at different levels of humidity and may decline even at high humidity [Evsikov et al. 1999a]. Thus, Maksimov’s [1982] hypothesis alone cannot explain the cause of regular population crashes in this species. Explaining the causes of decline is important for understanding the phenomenon of cyclicity in species with high reproductive capacity Water vole populations are known to be structured and consist of numerous local vole settlements in breeding season, which inhabit areas with heterogeneous biotic and abiotic conditions [Nikolaev et al. 1976, Evsikov et al. 1999b, 2001, Zav’yalov et al. 2007].

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Extrinsic and Intrinsic Factors of Regulation of Reproductive Potential …

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Reproduction in a population and maximum adaptation of water voles to considerable changes in land capacity are maintained through feedback in ethological and geneticphysiological mechanisms of animals’ adaptive potential. Density of reproducing individuals in local habitats correlates in all study years with the amount of water at the settlements estimated from average depths of the water bodies (r24 = +0.83, p < 0.05). The results are consistent with those obtained by Zav’yalov and coworkers [2007]. This work, however, gives data on one settlement studied in different years, whereas our data show variation among settlements with different amount of water. Similarly to larger rodents, the muskrat or the beaver, that occur in watered habitats too, and use water as a temporal refuge to hide from possible enemies and predators, the water vole also needs that water body be sufficiently deep near its nest during breeding season. Hence bottom shape and water level adjacent to a specific area determine how suitable and attractive this area is to the water vole. According to the hypothesis proposed by Ostfeld [1985], the structure of spatial distribution of reproductive groups in voles is formed by breeding females. Female small rodents often are territorial; this is widely accepted to result from competition by females for resources [Ostfeld 1985, 1990, Ims 1987, 1988, Wolff 1993, Keesing & Ostfeld 1999]. Particularly, territoriality of females comprises defense of habitat-related resources: forage [Ostfeld 1985, 1990, Ims 1987], and/or nest sites to deter intra-specific infanticide [Wolff 1993, Wolff & Peterson 1998]. Breeding-season ranges of female water voles are small and non-overlapping, whereas ranges of males are larger, may overlap with each other and with the ranges of several females [Pelikán & Holisova 1969, Stoddart 1970]. To have enough resources, female water voles have to establish sufficient-sized territories within an available area [Stoddart 1970, Evsikov et al. 1997, Moorhouse & Macdonald 2005], which results in inter-female competition for more preferable, deeper parts of a water body along the bank line. The effect of habitat hydrological regime on a population’s reproductive potential is produced therefore through inter-female competition for territory. Our results have shown that the water supply determines the intensity of competition among females for the most preferable watered biotopes. The more females there are per a unit of watered area suitable for reproduction of the species, the more injuries are received in the aggressive competition (r17 = +0.59, p = 0.007; Fig. 1). Along with that, tougher competition for territories results in decreased reproductive output: the number of injuries in females correlates with embryo loss (r17 = +0.73, p < 0.001). Population growth depends on fertility of overwintered females and rate of sexual maturity of young-of-the-year ones [Evsikov et al. 1999a]. Puberty is reached in the birth year by females that had been born before June, similar to other seasonally breeding rodents [Schwarz et al. 1964, Boonstra 1989; Nazarova & Evsikov 2007]. Data obtained showed that intensity of reproduction depends on the amount of water in a biotope: the more the territory is watered in May, the more young-of-the-year females are reproductively active (Fig. 2). Our data are in accordance with those of Moorhouse and co-workers [2008] showing that reduced maturation rates in female water voles are accounted by reduction of mean range size and limited availability of forage.

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Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka et al.

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Figure 1. The dependence of the number of injuries on males’ skins on the number of males per 1 female among overwintered animals. The dependence of the number of injuries on females’ skins on the number of females per area unit of watered biotopes [Muzyka et al. 2010].

Figure 2. The effect of Om flow intensity in May on the percentage of mature young-of-the-year females [Muzyka et al. 2010].

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Extrinsic and Intrinsic Factors of Regulation of Reproductive Potential …

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When the local density of breeding voles increases, inter-male competition for females toughens, resulting in a greater number of aggressive contacts. According to Ostfeld [1985], males compete for “reproductive resource”: the number of injuries depends on intensity of the competition, i.e. on the number males per 1 female of reproductively active animals (r19 = +0.53, p = 0.013; Fig. 1). Competition results in a rigid hierarchy that maintains stable density in local reproductive settlements [Potapov & Muzyka 1994, Evsikov et al. 1999b]. Larger dominant males occupy areas closer to females and have breeding advantages [Evsikov et al. 1997]. When we studied local settlements, we obtained similar data. We found that the frequency of aggressive contacts, i.e. the number of injuries on overwintered males’ skins, is affected by local density of breeding voles (r27 = +0.63, p < 0.05). The density determines the intensity of inter-male competition for reproductive females. Here, it was shown that the denser is the breeding segment within a settlement, the better is reproductive state of overwintered males. Mass of seminal vesicles correlates positively with settlement density (r27 = +0.41, p < 0.05). Taking into account that dominant males live closer to reproductive females and high-ranking males have better reproductive qualities [Evsikov et al. 1994, 1999b], one may reasonably assume that vesicle mass predicts male competitiveness and adaptive value. The comparison of age-class structure of settlements with various densities of breeding individuals showed that the ratio of the young-of the-year males per 1 overwintered female is higher in settlements with relatively low density than in those with high density (4.05 and 0.87, respectively). This may be evidence of either of the following processes: (1) pregnant females move out of dense habitats to sparser ones before parturition to provide their expected young with essential resources [Stoddart 1970, Jeppsson 1986]; (2) the young-of-the-year are driven out of dense settlements by breeding individuals, as was assumed by Solomonov [1980], and settle in vacant areas or move to meadows and prepare for winter; (3) the young-of-the-year more frequently die in dense settlements. Existing local settlements with low-density of breeding voles can support excessive numbers of non-breeding animals. If conditions are good for breeding, young-of-the-year females may breed in new areas, replacing overwintered ones who left these areas.

WINTER FACTORS OF POPULATION REGULATION Material and Methods To estimate the significance of food supply during winter for the population demography, we studied: (1) the burrow systems and the dynamics of foraging activity at different phases of the population cycles; (2) the inter-sexual differences of tunnel length and mass of food stores; (3) age differences in daily consumption of natural food in captivity; (4) the change of body mass during winter; (5) winter survival. In different years, a total of 46 burrows were studied in September and 93 burrows in October (Table 1). We dug up the burrows and recorded the natural wet mass of food stores.

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Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka et al. Table 1. Number of excavated burrows (Burr), the burrows with determined tunnel length (Tunn) and mass of food stores (Store) and number of captured water voles (Anim) in different years and months of the study [Potapov et al. 2004]

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Year 1986 1987 1988 1990 1991 1992 1993 1994 1995 1998 1999 2001 Sum

Cycle phase Peak

Burr 10

Decline Increase

7 2 1 9 9 8

September Tunn Store 10 10 – 2 1 9 7 4

7 2 1 – 8 4

Anim 10 6 2 – – 4 8

Peak Increase

46

33

32

30

Burr

October Tunn Store

Anim

10 4

7 –

10 4

5 2

8 10

7 10

8 10

6 9

26 4 21 10 93

26 4 21 10 85

26 4 21 10 93

20 3 20 9 74

The majority of burrows were mapped and the tunnel length was measured. Usually, animals were caught by hand and their sex and age were recorded. Water voles are attached to their burrows and when they were not caught immediately, they often returned and were captured with traps.The voles can only get rhizomes from the upper soil layer before it freezes. To determine the length of time voles were feeding on their stored food, we used average multiyear dates of soil freezing down to a depth of 10 cm (15 November) and that of the appearance of thawed patches (17 April) when the voles are able to feed on the soil surface [Anonymous 1978]. Food consumption was studied in October 1999 and 2001. On the day of capture, 16 young-of-the-year and three overwintered voles in 1999 and nine young-of-the-year voles in 2001 were weighed and placed in a field vivarium in separate stainless steel meshed cages supplied with water and measuring 22 × 45 × 22 cm. In the vivarium room air temperature was maintained at +10 ± 3 °C. Each cage was provided with two blind plastic tubes 24 cm long with a square cross-section 8 × 8 cm. One of these tubes served as a shelter and it was supplied with nest material, while the other served as a pantry and it was supplied with weighed quantity of food storage (100–150 g). Both the nest and food were taken from the burrow of a given animal. To control for natural drying of food, one similarly prepared cage was left unoccupied. Every day all animals, nests and food remains in the tubes plus minor quantities on the cage bottoms were weighed. Then the tubes were reloaded with fresh nest material and food. The animals were kept under such conditions for two to seven days. The daily consumption of each animal was determined by calculating the mean difference in the mass of the food provided and the remaining food, considering its water loss. Obviously, the voles almost did not consume their nest material because its mass did not change appreciably in consecutive days. The nest mass was ignored later on. To determine the mean body mass change during winter, the October and the next May samples of captured animals were used. Embryo mass was subtracted from the body mass of pregnant females.

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To determine winter survival, ratios (%) between population densities defined by standard capture procedures with the use of “Kulunda” live-traps and pitfall grooves [Rogov 1999] in May and in the previous October were calculated. The density data were borrowed from Evsikov and co-workers [1999a] and augmented with additional data. We carried out statistical analyses using ANOVA, Student’s test for independent samples, Mann-Whiney U-test, Pearson linear and Spearman rank correlations. Because distributions of the tunnel length (L, m) and food stores’ mass (S, kg) are asymmetrical [Airoldi 1976, Rogov et al. 2000], nearly normally distributed logarithms were used when computing parametric statistics: ln (100×L) for tunnel length and ln (S+1) for food stores (“one” was added to take stock of “zero” stores). To estimate the amount of stored food on 15 November (average date of soil freezing), we extrapolated it from a linear regression based on the September and October data. Means are given ± 1 SD. Statistical significance was considered at p < 0.05 level.

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Results and Discussion During autumn, young-of-the-year water voles move from wetlands to meadows and prepare for wintering by constructing a system of underground galleries and storing food (mainly rich roots and grass rhizomes) [Sasov 1965, Panteleyev 1971]. The size of food storage depends on the productivity of the habitats they occupy since both the structure of burrow systems and the quantity of food available depend on habitat richness, particularly, on abundance of plant biomass in the soil [Airoldi 1991, Rogov et al. 2000]. Usually water voles build individual burrows. During the study we found only two burrows shared by two voles, an overwintered female and a young male in both cases [Rogov et al. 2000]. The adult and subadult voles were caught in different parts of the burrows, which were connected by single paths. Because the individuals differed markedly by size in both cases, the burrows were divided to parts belonging likely to each of them according to the diameter of connecting tunnels. The majority of tunnels are at a depth of 5–15 cm (from the ceiling to the ground surface). One-third of the October burrows had one or two deep (30–115 cm) tunnels, 1–5 m long, and terminated by an enlarged chamber with a dry and well-developed nest inside (in 75 % of the deep tunnels). The absence of deep tunnels or the lack of nests in the other burrows corresponds probably to incomplete constructions by mid October. Cavities with food stores were dispersed throughout the burrow and consisted of unenlarged blind passages densely packed with roots and rhizomes of meadow plants. The average length of burrow systems was 18.2 ± 11.9 m (n = 33) in mid September and 41.0 ± 28.5 m (n = 85) in mid October. The tunnel length was significantly different between the peak and increase phases of population density both in September (11.9 ± 11.0 m, n = 10 and 21.0 ± 11.4 m, n = 23, respectively; Student’s test for log data: t31 = 2.82, p = 0.008) and October (23.6 ± 13.3 m, n = 33 and 52.0 ± 30.2 m, n = 52; Student’s test for log data: t83 = 5.56, p < 0.001). Seasonal changes in food stores show that water voles begin gathering food in early September (Fig. 3). By mid September the food stores weighed on average 0.27 ± 0.56 kg (n = 32), and there were no marked differences between the phases (peak, decline and increase) of population density (respectively: 0.01 ± 0.03 kg, n = 10, 0.25 ± 0.15 kg, n = 7

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Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka et al.

and 0.45 ± 0.77 kg, n = 15; ANOVA for log data: F2,29 = 3.29, p = 0.052). In about 40 % of burrows no stores were found in September. By mid October the mean mass of the food stores per burrow reached 3.0 ± 2.6 kg (n = 93). Overall, there was a significant difference among the density phases (peak: 1.9 ± 2.4 kg, n = 36; decline: 2.0 ± 1.5 kg, n = 4; increase: 3.8 ± 2.4 kg, n = 53; ANOVA for log data: F2,90 = 11.67, p < 0.001). However, only the difference between the increase phase and the peak phase was statistically significant (LSD test: p < 0.001). The peak and the decline phases did not differ (LSD test: p = 0.49) and they were combined for further consideration. Thus food stores in October were 1.9 ± 2.3 kg (n = 40) during years of population peak and decline combined, and they were twice as high during years of increase (Student’s test for log data: t91 = 4.80, p < 0.001). The linear extrapolation shows that by the date of soil freezing food stores may reach on average 3.4 kg at the peak and decline phases and 7.0 kg at the increase phase (Fig. 3). In October, we only caught seven voles that had overwintered previously. They had rather small stores (1.9 ± 1.8 kg, n = 7) compared to those of young voles (3.3 ± 2.7 kg, n = 67; two-way ANOVA for log data: “AGE” – F1,70 = 4.85, p = 0.031; “PHASE” – F1,70 = 12.96, p < 0.001; “AGE×PHASE” – F1,70 = 1.13, p = 0.29).

Increase phase

11

9

Peak and decline phases combined

8

Increase, regression

7 Peak and decline, regression

6 5

Critical amounts for safe wintering

4

Date of soil freezing

Food stores, kg

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10

3 2 1 0 0

September

30

October

61 November

Number of days from 31 August Months Figure 3. The mass of food stores per individual burrow at different phases of the population cycle and the linear regression of food stores (FS) on the number of days from 31 August (D = 0). The equations of linear regressions look as follows. Increase phase: FS = −1.0 + 0.11×D; n = 68, r = 0.48, p = 0.0005. Peak and decline phases combined: FS = −0.4 + 0.05×D; n = 57, r = 0.41, p = 0.001. Critical amounts for safe wintering (see text): FS = −1.2 + 0.13×D [Potapov et al. 2004].

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Extrinsic and Intrinsic Factors of Regulation of Reproductive Potential …

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When feeding animals with natural food in captivity, the daily consumption was 57.3 % of the body mass or 54.7 ± 8.0 g (n = 25) in the young-of-the-year voles and 42.0 % or 68.3 ± 9.3 g (n = 3) in the overwintered ones. Although the overwintered voles consumed less per g of body mass (ANOVA: F1,26 = 4.70, p = 0.04), their absolute consumption exceeded that of the young (ANOVA: F1,26 = 7.45, p = 0.01). It was found that the absolute daily consumption positively depended on body mass (Pearson linear correlation: r27 = +0.48, p < 0.01), while the relative one depended on body mass negatively (Pearson linear correlation: r27 = −0.72, p < 0.001). The estimations of the experimentally defined levels of consumption (54.7 g per day in young voles) show that the critical value of food stores necessary during the under-snow period (153 days) is at least 8.4 kg in mid November. Assuming a linear rate of storage accumulation (starting on 10 September), voles should have about 4.5 kg of food in their burrows by mid October (Fig. 3). Only a small fraction of individuals had sufficient food supply. Both tunnel length and mass of food stores in mid October were greater in young males than in females: 49.8 ± 29.1 m, n = 39 vs. 33.2 ± 26.8 m, n = 26 (two-way ANOVA for log data: “SEX” – F1,61 = 10.90, p = 0.002; “PHASE” – F1,61 = 21.77, p < 0.001; “SEX×PHASE” – F1,61 = 2.43, p = 0.12) and 3.9 ± 2.9 kg, n = 41 vs. 2.3 ± 1.9 kg, n = 26 (two-way ANOVA for log data: “SEX” – F1,63 = 6.99, p = 0.01; “PHASE” – F1,63 = 19.78, p < 0.001; “SEX×PHASE” – F1,63 = 1.66, p = 0.20). The body mass in May of overwintered voles did not correlate with the previous October body mass (Spearman rank correlations: rS = +0.02, n = 8, p = 0.96 in males and rS = −0.05, n = 8, p = 0.91 in females). At the same time, the winter body mass change correlated with the average October food store both in males and females (Spearman rank correlations: rS = +0.74, n = 8, p = 0.035 and rS = +0.82, n = 7, p = 0.023, respectively; Fig. 4). Survival FS, females

8

FS, males

7

MC, females

6

80

60

MC, males

5

40

4 20

3 2

Mass change, g Survival, %

Food stores, kg

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9

0

1 0

-20 1987

1988

1992

1993

1995

1998

1999

2001

Years

Figure 4. Food stores in October (FS), changes in body mass (MC) and survival during the subsequent winters. Bars represent SE [Potapov et al. 2004]. Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

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Mikhail A. Potapov, Galina G. Nazarova, Vladimir Yu. Muzyka et al.

Winter survival of water voles varied widely among the years of our study (Fig. 4). The density phases differed by the survival: peak and decline combined - 10.5 ± 9.9 %, n = 3; increase - 53.1 ± 28.1 %, n = 5 (ANOVA: F1,6 = 6.10, p < 0.05). The winter survival correlated with the mean size of food stores (Spearman rank correlation: rS = +0.86, n = 8, p = 0.007). Also, the survival correlated with the winter body mass change both in males and females (Spearman rank correlations: rS = +0.95, n = 8, p = 0.0003 and rS = +0.90, n = 8, p = 0.002, respectively). Thus, one of the possible causes for the decline in numbers of water vole populations may be increased winter mortality which results from winter food deficit [Evsikov et al. 1995, 2001, Evsikov & Ovchinnikova 1999, Rogov et al. 2000, 2003, Potapov et al. 2004]. During the phase of high vole density, the biomass of the underground parts of vegetation in meadow habitats decreases three times or more, and its recovery then takes at least three years [Evsikov & Ovchinnikova 1999, Evsikov et al. 2001]. The intensive exploitation of food resources, leading to their depletion at high population density is also considered a cause for population crashes in the fossorial water voles, A. scherman, from Switzerland [Airoldi 1991]. Furthermore, long-term data indicate that in Western Siberia the mortality among females from birth to the beginning of the next-year reproductive season is three times greater than in males. The maximal losses occur during winter [Rogov et al. 1999], which is a critical period in the life history of female water voles. The data on burrow systems of water voles are still fragmentary [Panteleyev 1971, 2001a, Mesch 1984], except for those of the fossorial form, A. scherman, studied by Airoldi [1976, 1991, 1992]. The average length of burrow systems we obtained is lower than that for the fossorial voles from Switzerland [Airoldi 1976]. Nevertheless, the values per individual vole are comparable taking into account that the majority of the burrows in the fossorial voles are inhabited not by solitary voles but by adult pairs or by females with young [Airoldi 1976, 1991, Saucy 2001]. Moreover, a burrow system in a terrarium has been shown to be longer when inhabited by a couple [Airoldi 1992]. In the fossorial voles, winter breeding was recorded and could be responsible for population outbreaks [Meylan & Airoldi 1975]; this never has been documented in the aquatic voles from Siberia [Sasov 1965, Panteleyev 1971]. The foraging activity of water voles at the beginning of winter in Siberia is still poorly known. It was reported that in Western Siberia food stores in burrows amounted to 0.5 kg, the biggest one reaching 3.8 kg [Sasov 1965]. These data are close to those (0.2 to 4.0 kg) of Mesch [1984]. In the centre of European Russia the stores amount to only 0.2 kg on average [Panteleyev 1971]. On the other hand, they are of great importance for winter survival of water voles in Yakutia and average 2.8 kg. In some fertile sites such as lakeshores or potato fields they can even reach 18–30 kg per burrow [Solomonov 1980]. Our results indicate that water voles in Western Siberia accumulate rather large food reserves in their burrows by mid October, comparable to those in Yakutia. Nevertheless, the estimation of food consumption in the vivarium shows that animals could face a food deficit during winter. Our data on food consumption are the first obtained from feeding water voles on their natural winter stores. According to Alekseyeva and co-workers [1959], the daily consumption of edible roots and juicy grasses by water voles in different seasons is 76–91 g or 50–75 % of the vole’s body mass. When feeding separately on grasses or vegetables, voles consumed about 59 g or 80 % of body mass [Drozd et al. 1971]. Voles weighing 100 g consumed about 85 g of succulent feed per day [Mesch 1984]. The revealed dependence of daily consumption on animals’ age and/or body mass is very close to that reported by Panteleyev [2001b]. According to the calculated critical amounts of winter feed, almost all overwintered animals

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had insufficient food stores for a safe second overwintering. Moreover, their relatively high daily consumption would not allow surviving a second winter. Among the young, only 15% have sufficient stores during peak and decline phases and less than 50% during the years of increasing numbers [Rogov et al. 2000]. Indeed, these figures are very close to those on winter survival during different phases of population dynamics. In Siberia, contrary to the European part of the range [Mesch 1984], water voles cannot get rhizomes from frozen soil. During the five months from the date of soil freezing to the first thaw, they have to feed on their stores. Of course, these dates may vary from year to year and a decrease in metabolic rate and food consumption may occur in winter. However, Panteleyev [2001b], who kept captive voles on juicy roots throughout winter, showed that their food consumption was rather stable and only depended negatively on air temperature, which, in its turn, was stable in shelters. In any case, the correlations between the food stores, the change in body mass and survival during winter demonstrates the dependency of animals’ welfare on their forage activity in autumn. The voles may additionally feed on withered plants and green sprouts under the snow cover [Sasov 1965]. However, the poor nutritional quality of last year’s vegetation and the small quantity of sprouts limit such possibility. The quantity of stored food may be dependent both on its availability in the soil [Rogov et al. 2000] and on the density of wintering voles. Indeed, the situation is aggravated during peaks in population numbers, when habitats lack sufficient amounts of root biomass to feed all the voles adequately [Evsikov & Ovchinnikova 1999, Evsikov et al. 2001]. Furthermore, the high density of voles and consequently that of their burrows in the occupied habitats increases the risk that hungry neighbours will compete with each other for forage [Panteleyev 2001a]. The depletion of the food supply at the peak probably determines the prolonged effect of winter under-nourishment for subsequent years, thus being one of the reasons for the deepening of the population decline [Airoldi 1991, Evsikov & Ovchinnikova 1999, Evsikov et al. 2001]. The females are those which strongly suffer from the winter food deficiency because they do not manage to prepare adequately for wintering. It is the most important demographic factor, determining high female mortality in winter, greatly exceeding that in males. In May the number of overwintered males is almost always twice or more as high as those of females [Rogov et al. 1999]. The loss of 2/3 of the females during winter leads to a decrease in the reproductive potential of water vole populations. As a result, the increase phase, despite the pronounced r-strategy of the species, stretches for three to six years. Analysis of the multiyear data shows that the duration of the whole population cycle of water voles in Siberia varies from four to nine years [Rogov 1999], and it is longer on average than that in most other vole species [Krebs & Myers 1974]. Thus, the conditions of winter food availability are rather severe, especially during the peak and decline of numbers in populations of the water vole from Siberia. Over-exploitation of under-ground phytomass reserves at the peak keeps the situation critical during one or two subsequent years. It is slightly better in meadows with restored fertility, but during years of density increase, about half of animals still suffer from food deficit. The data presented suggest that the winter food deficit is a real factor affecting dynamics of numbers, sexual and age structures, and reproductive potential in the water vole population in Western Siberia.

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CONCLUSION The water vole has proved a convenient species to investigate the role of both extrinsic and intrinsic mechanisms in driving population cycles. Both in reproductive season and in winter well-being of water voles strongly depends on climatic conditions having a direct influence on the availability of resources and the carrying capacity of the environment. In summer, the main extrinsic factor influencing realization of reproductive potential of the water vole is hydrological regime, i.e. variable water supply determining the area of suitable biotopes. The level of the water vole population reproductive output, estimated by ratio of autumn to spring population numbers, correlates with hydrological fluctuations in summer reflecting the availability of suitable habitats. Taking in account the extremely high amplitude of interannual numbers fluctuations in the water vole, the extrinsic conditions interact with intrinsic factors such as density predetermining a level of competition for the limiting resources. At different population numbers and flooding levels, habitats vary in attractiveness and suitability for the animals. As a result, the intensity of intra-specific competition naturally varies with habitat heterogeneity. It is possible to state that the amount of water at breeding sites in Northern Baraba Lowland affects local density of the breeding animals and rate of population growth. It was found that the most variable characteristics determining reproductive output of the population are a portion of participating in breeding young-of-the-year females and a rate of embryonic losses during pregnancy. These characteristics appeared to be essentially sensitive to effects of both extrinsic (availability of suitable biotopes) and intrinsic (density) factors. The interaction of these factors determines the level of competition among reproductively active females as detected by number of injuries on skins and consequently embryonic losses and reproductive output of the population. The data obtained indicate that climate (habitat hydrological regime) affects individual qualities (reproductive characteristics, aggression) of animals and results in differentiation of reproductive groups in density and demographic structure. Land capacity directly depends upon the amount of water in the biotope. In turn, local settlements with different densities provide a “reserve” of reproductive individuals to maintain population homeostasis. Participating of the young-of the-year females in reproduction has its effect on their winter survival. They stay in summer biotopes and have not enough time to gather necessary for safe wintering amount of food stores. Indeed, Siberian climate is severe continental, with long and cold winter. This fact is responsible for the dependence of winter survival of voles on amount of gathered beforehand food stores which, in its turn, depends on density influencing competition level. Because of higher female winter mortality, sexual structure of the population in spring is unbalanced. This leads to high level of inter-male competition for receptive females and strong selection among overwintered males. During the multi-year study of wintering burrows of water voles in Western Siberia it was found out that the size of food stores are smaller at the peak and the decline phases of the population cycle compared to that at the increase. Females have smaller stores compared to males. Comparison of the mass of stores in burrows and the daily consumption of natural foods indicates that only a small fraction of individuals have sufficient food supply for safe

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wintering. In support, it is shown that the size of food stores in October affects both winter change in body mass and winter survival. Our results support the hypothesis of winter food deficit as a cause of population decline. Thus, the obtained data indicate that in the water vole from Western Siberia the extrinsic and intrinsic factors closely interact regulating reproductive potential and density of the population and affecting competition level, efficiency of natural selection and formation of demographic structure.

ACNOWLEDGMENTS We are grateful to those participated in the study in different years. Here are just some of them: N. A. Romashov, V. G. Rogov, L. E. Ovchinnikova, O. A. Rogova, A. V. Bragin. We would like to thank W. Z. Lidicker, Jr., and J.-P. Airoldi for help and advice, and J. Zima for permission to republish a part of our data. The study was supported by Russian Foundation for Basic Research (grants Nos. 09-04-01712, 11-04-00277, and 11-04-01690) and Presidium of the Russian Academy of Sciences (“Biological Diversity” program, project No. 26.6).

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REFERENCES Airoldi, J.-P. (1976). Le terrier de la forme fouisseuse du campagnol terrestre, Arvicola terrestris scherman Shaw (Mammalia, Rodentia). Z. Säugetierkd., 41, 23-42. Airoldi, J.-P. (1991). Le terrier de la forme fouisseuse du campagnol terrestre (Arvicola terrestris L.): Structure et fonction. In M. Le Berre, & L. Le Guelte (Eds.), Le Rongeur et l’Espace. Actes du Colloque International, Lyon, Mars 1989 (pp. 285-297). Paris: Editions R. Chabaud. Airoldi, J.-P. (1992). Dynamique du développement du terrier de la forme fouisseuse du campagnol terrestre (Arvicola terrestris L.) en terrarium vertical et dans le terrain. Rev. Suisse Zool., 99(1), 87-108. Alekseyeva, M. A., Maksimov, A. A., & Folitarek, S. S. (1959). On the baits for the water rat control. In A. P. Kuzyakin (Ed.), The Water Rat and its Control in Western Siberia (pp. 339-350). Novosibirsk: Novosibirskoe knizhnoe izd-vo. [In Russian.] Anonymous (1978). Reference Book on the Climate of the USSR. Soil Temperature, Part 8, Vol. 2. Novosibirsk. [In Russian.] Barbash, L. A., Folitarek, S. S., & Leonov, Yu. A. (1971). Live traps of new design for the water vole. In Ecology and Control of the Water Vole in Western Siberia (pp. 359-366). Novosibirsk: Nauka, Siberian Branch. [In Russian.] Boonstra, R. (1989). Life history variation in maturation in fluctuating meadow vole populations (Microtus pennsylvanicus). Oikos, 54, 265-274. Duhamel, R., Quere1, J.-P., Delattre, P., & Giraudoux, P. (2000). Landscape effects on the population dynamics of the fossorial form of the water vole (Arvicola terrestris sherman). Landscape Ecology, 15, 89-98. Drozd, A., Gorecki, A., Grodzinski, W., & Pelikán, J. (1971). Bioenergetics of water voles from Southern Moravia. Ann. Zool. Fennici, 8, 97-103.

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Evsikov, V. I., & Moshkin, M. P. (1994) Dynamics and homeostasis of natural populations. Sibirskii Ekologicheskii Zh., 1(4), 331-346. Evsikov, V. I., & Ovchinnikova, L. E. (1999). Population ecology of the water vole (Arvicola terrestris L.) in West Siberia. IV. Intra-population variability in food digestibility. Sibirskii Ekologicheskii Zh., 6(1), 89-98. Evsikov, V. I., Gerlinskaya, L. A., Moshkin, M. P., Muzyka, V. Yu., Nazarova, G. G., Ovchinnikova, L. E., Potapov, M. A., & Rogov, V. G. (2001). Genetic-physiological basis for the population homeostasis. In P. A. Panteleyev (Ed.), The Water Vole: Mode of the Species (pp. 386-412). Moscow: Nauka. [In Russian.] Evsikov, V. I., Moshkin, M. P., Potapov, M. A., Gerlinskaya, L. A., Nazarova, G. G., Novikov, E. A., Ovchinnikova, L. E., Rogov, V. G., & Muzyka, V. Yu. (1995). Evolutionary-genetic and ecological aspects of the problem of the population homeostasis in mammals. In I. A. Shilov (Ed.), Ecology of Populations: Structure and Dynamics, Vol. 1 (pp. 63-96). Moscow: Rossel’khozakademiya. [In Russian.] Evsikov, V. I., Nazarova, G. G., & Potapov, M. A. (1994). Female odor choice, male social rank, and sex ratio in the water vole. In R. Apfelbach, D. Müller-Schwarze, K. Reutter, & E. Weiler (Eds.), Advances in the Biosciences, Vol. 93: Chemical Signals in Vertebrates VII (pp. 303-307). Oxford: Pergamon. Evsikov, V. I., Nazarova, G. G., & Potapov, M. A. (1997). Genetic-ecological monitoring of a cyclic population of water voles Arvicola terrestris L. in the south of Western Siberia. Russian Journal of Genetics, 33, 963-972. [Original Russian text is published in: Genetika, 1997, 33, 1133-1143.] Evsikov, V. I., Nazarova, G. G., & Rogov, V. G. (1999a). Population ecology of the water vole (Arvicola terrestris L.) in West Siberia. I. Population numbers, coat color polymorphism, and reproductive effort of females. Sibirskii Ekologicheskii Zh., 6(1), 5968. Evsikov, V. I., Potapov, M. A., & Muzyka, V. Yu. (1999b). Population ecology of the water vole (Arvicola terrestris L.) in West Siberia. II. Spatial-ethological structure of population. Sibirskii Ekologicheskii Zh., 6(1), 69-77. Ims, R. A. (1987). Responses in spatial organization and behavior manipulations of the food resources in the vole Clethrionomus rufocanus. J. Anim. Ecol., 56, 585-596. Ims, R. A. (1988). Spatial clumping of sexually receptive female indices space sharing among male voles. Nature, 335, 541-543. Jeppsson, B. (1986). Mating by pregnant water voles (Arvicola terrestris): A strategy to counter infanticide by males? Behav. Ecol. Sociobiol., 19(4), 293-296. Keesing, F., & Ostfeld, R. S. (1999). Linking dispersal and population dynamics of small mammals to community dynamics in a patchy landscape: A prospectus for research. Sibirskii Ekologicheskii Zh., 6(1), 15-22. Krebs, C. J. (2002). Two complementary paradigms for analyzing population dynamics. Phil. Trans. R. Soc. Lond. B., 357, 1211-1219. Krebs, C. J., & Myers J. H. (1974). Population cycles in small mammals. Adv. Ecol. Res., 8, 267-399. Lidicker, W. Z., Jr. (1988). The synergistic effects of reductionist and holistic approaches in animal ecology. Oikos, 53, 278-281. Lidicker, W. Z., Jr. (1999). Population regulation in mammals: An evolving view. Sibirskii Ekologicheskii Zh., 6(1), 5-15.

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Maksimov, A. A. (1959). Reproduction and population dynamics of the water vole in various landscapes of West Siberia. In A. P. Kuzyakin (Ed.), The Water Rat and its Control in Western Siberia (pp. 71-121). Novosibirsk: Novosibirskoe knizhnoe izd-vo. [In Russian.] Maksimov, A. A. (1982). Cycles of change in the natural environment and multiyear fluctuations of the numbers of animals. Doklady Akad. Nauk SSSR, 264, 1273-1275. Maksimov, A. A. (2001). Population dynamics. In P. A. Panteleyev (Ed.), The Water Vole: Mode of the Species (pp. 346-385). Moscow: Nauka. [In Russian.] Maksimov, A. A., Pon’ko, V. A., & Sytin, A. G. (1979). Changing of Wetness Phases of the Baraba Lowland (Characteristics and Prognosis). Novosibirsk: Nauka, Siberian Branch. [In Russian.] Mesch, H. (1984). Wühlmaus und Maulwurf im Garten. Berlin: VEB Deutscher Landwirtschaftsverlag. Meylan, A., & Airoldi, J.-P. (1975). Reproduction hivernale chez Arvicola terrestris scherman Shaw (Mammalia, Rodentia). Rev. Suisse Zool., 82, 689-694. Moorhouse, T. P., & Macdonald, D. W. (2005). Temporal patterns of range use in water voles: do females' territories drift? J. Mammal., 86(4), 655-661. Moorhouse, T. P., Gelling, M. I., & Macdonald, D. W. (2008). Effects of forage availability on growth and maturation rates in water voles. J. Anim. Ecol., 77, 1288-1295. Muzyka, V. Yu., Nazarova, G. G., Potapov, M. A., Potapova, O. F., & Evsikov, V. I. (2010). The effect of habitat hydrology on intraspecific competition, population structure, and reproduction in the water vole (Arvicola terrestris). Contemporary Problems of Ecology, 3(5), 606-610. [Original Russian text is published in: Sibirskii Ekologicheskii Zh., 2010, 17(5), 827-833.] Nazarova, G. G., & Evsikov, V. I. (2007). Sexual maturation of daughters depends on the mother’s body condition during pregnancy: An example of the water vole Arvicola terrestris L. Doklady Biol. Sci. 412(1), 53-55. [Original Russian text is published in: Doklady Akad. Nauk, 2007, 412(4), 568-570.] Nikolaev, A. S., Glotov, I. N., Erdakov, L. N., & Sergeev, V. E. (1976). Water vole populations in 1966–1974. Prospectus. In A. A. Maksimov (Ed.), Outbreak of the Water Rat (pp. 64-74). Novosibirsk: Nauka, Siberian Branch. [In Russian.] Ostfeld, R. S. (1985). Limiting resources and territoriality in microtine rodents. Am. Nat., 126, 1-15. Ostfeld, R. S. (1990). The ecology of territoriality in small mammals. Trends Ecol. Evol., 5, 411-415. Panteleyev, P. A. (1971). Population Ecology of the Water Vole. Boston Spa, Yorkshire: National Lending Library for Science and Technology. [Original Russian book: Panteleyev, P. A. (1968). Populyatsionnaya Ekologiya Vodyanoi Polevki i Mery Bor’by. Moscow: Nauka.] Panteleyev, P. A. (2001a). Mode of life. In P. A. Panteleyev (Ed.), The Water Vole: Mode of the Species (pp. 193-235). Moscow: Nauka. [In Russian.] Panteleyev, P. A. (2001b). Feeding: Ecological data. In P. A. Panteleyev (Ed.), The Water Vole: Mode of the Species (pp. 268-274). Moscow: Nauka. [In Russian.] Pelikán, J., & Holisova, V. (1969). Movements and home ranges of Arvicola terrestris on a brook. Zoologicke Listy, 18, 207-224.

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Plyusnin, Yu. M. (1985). Ethological Structure of the Water Vole Population in Various Phases of the Population Cycle. Candidate’s Dissertation. Novosibirsk: Biological Institute SB AS USSR. [In Russian.] Plyusnin, Yu. M., & Evsikov, V. I. (1985). Seasonal differences in social organization of demes in the water vole. Russian J. Ecol., 3, 47-55. Potapov, M. A., & Muzyka, V. Yu. (1994). Ethological structure in the population cycle of the water vole, Arvicola terrestris L. Pol. Ecol. Stud., 20(3-4), 427-430. Potapov, M. A., Rogov, V. G., Ovchinnikova, L. E., Muzyka, V. Yu., Potapova, O. F., Bragin, A. V., & Evsikov, V. I. (2004). The effect of winter food stores on body mass and winter survival of water voles, Arvicola terrestris, in Western Siberia: The implications for population dynamics. Folia Zool., 53(1), 37-46. Rogov, V. G. (1999). Population Demography of the Water Vole (Arvicola terrestris) in Western Siberia. Candidate’s Dissertation. Novosibirsk: Institute of Systematics and Ecology of Animals SB RAS. [In Russian.] Rogov, V. G., Potapov, M. A., & Evsikov, V. I. (1999). Sexual structure of the water vole population Arvicola terrestris (Rodentia, Cricetidae) in Western Siberia. Zool. Zh., 78(8), 979-986. Rogov, V. G., Potapov, M. A., & Evsikov, V. I. (2003). The dependence of winter survival of water voles on the size of food stores. In V. N. Orlov (Ed.), Mammalian Fauna of Russia and Contiguous Territories (pp. 293-294). Moscow: Severtsov Institute of Ecology and Evolution RAS. [In Russian.] Rogov, V. G., Potapov, M. A., Muzyka, V. Yu., Ovchinnikova, L. E., Potapova, O. F., Bragin, A. V., & Evsikov, V. I. (2000). Wintering burrows and forage stores of water voles in West Siberia. In N. A. Kolchanov (Ed.), Biodiversity and Dynamics of Ecosystems in North Eurasia, Vol. 3, Part 1 (pp. 205-207). Novosibirsk: IC&G. Rogovin, K. A., & Moshkin, M. P. (2007). Autoregulation in mammalian populations and stress: An old theme revisited. Zh. Obshch. Biol., 68(4), 244-267. Rose, R. K. (1979). Levels of wounding in meadow vole Microtus pennsylvanicus. J. Mammal., 60(1), 37-45. Sasov, N. P. (1965). Materials on the ecology of the water rat in the autumn, winter, and early-spring periods. In A. A. Maksimov (Ed.), Fauna of Baraba (pp. 45-69). Novosibirsk: Nauka. [In Russian.] Saucy, F. (2001). Systematics: Features of fossorial water vole. In P. A. Panteleyev (Ed.), The Water Vole: Mode of the Species (pp. 172-174). Moscow: Nauka. [In Russian.] Saucy, F., & Gabriel, J.-P. (1998). Population Cycles and Climate, Vol. 1. Fribourg, Switzerland: Université de Fribourg. Schwarz, S. S., Pokrovski, A. V., Istchenko, V. C., Olenjev, V. G., Ovtshinnikova, N. A., & Pjastolova, O. A. (1964). Biological peculiarities of seasonal generations of rodents, with special reference to the problem of senescence in mammals. Acta Theriologica, 8(1), 1143. Solomonov, N. G. (1980). Ecology of the Water Vole in Yakutia. Novosibirsk: Nauka, Siberian Branch [In Russian.] Stoddart, D. M. (1970). Individual range, dispersion, and dispersal in population of the water vole (Arvicola terrestris L). J. Anim. Ecol., 39(2), 403-425. Wolff, J. O. (1993). Why are female small mammals territorial? Oikos, 68, 364-370.

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Wolff, J. O., & Peterson, J. A. (1998). An offspring-defence hypothesis for territoriality in female mammals. Ethol. Ecol. Evol., 10, 227-239. Zav’yalov, E. L., Gerlinskaya, L. A., Ovchinnikova, L. E., & Evsikov, V. I. (2007). Stress and territorial organization of a local population of the water vole (Arvicola terretstris). Zool. Zh. 86(2), 242-251. Zhigal’skii, O. A. (2002). Analysis of population dynamics of small mammals. Zool. Zh., 81(9), 1078-1106.

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Chapter 3

RODENTS AND SPACE: WHAT BEHAVIOR DO WE STUDY UNDER SEMI-NATURAL AND LABORATORY CONDITIONS? Vladimir S. Gromov1 A.N. Severtsov Institute of Ecology and Evolution RAS, Moscow, Russia

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INTRODUCTION Over the last several decades, a tendency has appeared of focusing upon laboratory studies of various activities of rodents instead of field investigations. Of cause, laboratory studies usually do not take so much labour, time and money as do investigations in the field, and in many cases researchers can make proper inferences based on data obtained due to observations of rodents in captivity. But my own experience shows that we can lose very valuable information and, moreover, draw incorrect conclusions when carrying out behavioral studies on rodents under laboratory conditions only. It is well known that rodents are sedentary animals, and every one possesses a home range used for various purposes: foraging, construction of shelters and burrows, interactions with conspecific individuals, reproduction, etc. Rodent home ranges are usually of a large size, and comprise several hundreds and even a few thousand square meters. Restriction of space under semi-natural conditions (for instance, in large enclosures) and, moreover, in small laboratory cages can lead to essential alteration of rodent behavior. This especially concerns behavior related to territoriality, scent marking, social interactions, and parental care. As an example, I’d like to present some results of my studies of the Mongolian gerbil (Meriones unguiculatus) carried out in the wild as well as under semi-natural conditions (in open enclosures located outdoors at a field station in Chernogolovka about 50 km north-east of Moscow, Russia) and in a laboratory. The Mongolian gerbil is a medium-sized rodent (adult wt 60-80 gm) inhabiting the steppe regions (Fig. 1) in Eastern Siberia, Mongolia and 1

E-mail: [email protected].

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Vladimir S. Gromov

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Figure 1. A typical habitat of the Mongolian gerbil in the Ubsu-Nuur Lake Valley, Eastern Siberia. Coarse grass – Achanatherum splendens, lower vegetation cover – Chenopodium album.

Northern China, and preferring agricultural areas, especially old cultivated fields (lay-lands) as well as sites of sheep corrals, the “kosharas” (Gromov & Popov 1979; Gromov 1981, 2000a, 2008; Ågren et al. 1989). I used a capture-mark-release technique, and observed marked gerbils through binoculars on 0.3-0.5 ha plots. Within each plot, a grid of squares 10 × 10 m or 5 × 5 m was laid out, and the corners of the squares were marked by small flags with numerical symbols allowing location of the gerbils during the observations. Visual observations revealed that Mongolian gerbils live in extended family groups. As a rule, such groups include one adult male, one or two, less frequently three adult females, and their offspring. The number of young individuals in a group depends on the number of reproducing females which in spring and summer bring in as many as three litters, each litter having four to seven individuals. The total number of members in a large family group can amount to 30 individuals. Each family group occupies its own home range (the territory), marks it by scent marks and actively protects from any conspecific intruders (Fig. 3). All adult and sub-adult members of a family group take part in protection of their territory. Family-group territories average about 750 m2, and the minimum protected area occupied by a pair of adult individuals without offspring comprised 100 m2. Aggressive interactions between members of the neighboring family groups allow correct location of the boundaries between protected territories. Usually, there is a narrow overlap zone not exceeding 2-3 m in width where an observer can see the most frequent boundary encounters including attacks, two-way chases, fights, and so-called

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Figure 2. Approximate locations of the boundaries of protected and marked territories occupied by two family groups and a single male of the Mongolian gerbil at the area of small sheep yard (“koshara”). The contours are smoothed minimum convex polygons encircling the areas with scent marks of males (thick lines) and females (dotted lines). 1 – sheds, 2 – areas covered by vegetation (mainly Chenopodium album).

Figure 3. Specialized motor patterns of territorial marking in Mongolian gerbils. 1 – marking with secretion of the ventral gland (ventral rubbing), 2 – building up a "signal heap".

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Vladimir S. Gromov

ritualized agonistic demonstrations (Gromov & Popov 1979; Ågren et al. 1989; Gromov 2000a). Such boundary encounters occur in populations of the Mongolian gerbil during the whole breeding season – in spring, summer and early autumn. Along with protection of the family-group home ranges, Mongolian gerbils actively mark them. Due to numerous laboratory studies, it is well known that Mongolian gerbils have the ventral sebaceuos gland and use its secretion for scent marks (Thiessen 1968; Lindzey et al. 1968; Thiessen et al. 1969; Whitsett & Thiessen 1972; Owen & Thiessen 1973). In adult males, this gland looks like a fusiform pad approximately 2–3 cm in length, 0.5 cm in width and 0.2 cm in depth. Adult females also possess the sebaceous gland complex, but it is generally about one-half the size of the male’s glands. Thus, adult individuals of both sexes are able to mark their home ranges with secretion of the ventral gland. Scent marking by the ventral gland occurs as follows: the animal crawls over some objects, its abdomen closely pressed to the substrate, and leaves the secretion of the ventral gland on that place (so-called ventral rubbing, Fig. 3, 1). In the natural habitat, the objects of this kind of marking include burrow entrances, soil hammocks, small stones, lumps of ground and other ones both inside the protected territory and along its border. Unfortunately, laboratory studies and even observations in enclosures (Payman & Swanson 1981) did not reveal the second, also very common and undoubtedly important kind of territorial marking in the Mongolian gerbil. Observations in nature showed that along with ventral rubbing, gerbils leave a drop of their urine in some places (often near the ventral marks) where the substrate is loose enough. Simultaneously, they can also leave 1 to 3 fecal pellets at the same place. Throwing the sand beneath its belly by its anterior legs the animal builds up a conic hillock of the substrate covering the drop of urine and fecal pellets (Fig. 3, 2). Such a "signal heap" serves both a visual and scent mark. My observations showed the second way of territorial marking to be used by the gerbils much more often than the first one: out of the 6,547 registered scent marks only 1,192 marks (I8.2%) were ventral rubbing. In the overwhelming majority of cases (89.3%) the ventral rubbing was characteristic only of adults – family group founders (Gromov 1997). Besides these two main scent marking behaviors, Mongolian gerbils mark their territories by genital rubbing and by chinning of some objects, but a summarized portion of these scent marks does not exceed 1-3%. So, the most common kinds of the territory marking in the gerbils are ventral rubbing and building up "signal heaps". A summarized portion of these two kinds of scent marks is about 97–99%. The intensity of the scent marking in the gerbils is rather high – on the average, 2.0 marks per one hour of observations as calculated per one adult individual (Sokolov & Gromov 1998). Usually, scent marks are unevenly distributed within the protected home ranges. The bulk of scent marks are found to be concentrated near burrow entrances and along the commonly used routes as well as along the territory borders, especially within the overlap zones. So, spatial distribution of scent marks can be also used for proper sizing of the home ranges and correct location of the boundaries between neighboring territories. To study the social and scent marking behavior in detail, I observed M. unguiculatus under semi-natural conditions – in enclosures of 20 × 20 m and 15 × 15 m (Fig. 4). The enclosures are of solid constructions of a wooden framework studded with galvanized tin 1.5 m in height and fenced by a small-meshed stainless steel net dug deep down to 1 m along the perimeter, so clearly no movements of the animals into or out of them were possible. Sufficiently loose loam soil inside the enclosures allowed proper burrowing. Within the

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Figure 4. Open enclosures at the Chernogolovka field-station used for visual observations of captive gerbils.

enclosures, squares of 2.5 × 2.5 m were laid out. The corners of the squares were marked by numerical symbols. The positions of the observed gerbils were identified with reference to these flags. At the beginning of the observations (in May), a group of adult gerbils (4 males and 4 females) was introduced into every enclosure. The animals were chosen from different family groups caught in the wild and bred under laboratory conditions. Direct observations in the larger enclosures (20 × 20 m) showed that after a period of aggressive encounters, only two pairs of gerbils remained in each enclosure. These pairs divided the area of the enclosure into two nearly equal parts with a narrow overlap zone, and successfully protected and marked their territories for a long period of observations (until October). The gerbils successfully reproduced, and every adult female gave birth to two litters, so that the number of the animals achieved 7-10 individuals per family. Space use patterns in one of the large enclosure populations are shown in Fig. 5. Such patterns were obtained due to a computer graphic program processing the data of continuous registration of the animals in the squares of the enclosure in 5-min intervals (Gromov 2008). Contour lines encircle the areas used by adult and sub-adult individuals as well as the centers of their activity. Similar patterns were characteristic of other sub-adult and young members of the family groups, and the graphs clearly show that the areas used by the members of different family groups in the enclosure nearly do not overlap as in the natural habitat.

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Figure 5. Contour mapping of the frequency of visual registration of Mongolian gerbils in enclosure of 20 × 20 m. Contour lines connect points of equal frequency of registration per unit area (square 2.5 × 2.5 m). Higher density of the lines corresponds to the activity centers of the animals related to their nest burrows. Family group 1: adult male # 30, adult female # 31, sub-adult male # 43; family group 2: adult male # 40, adult female # 42, sub-adult male # 34.

The rate of marking activity in adults was the highest as compared with other members of the family groups as in the field (Fig. 6 A). However, the marking rate of the gerbils in the enclosure populations was found to be much higher than in natural habitats. This fact could be mainly explained by better conditions for direct observations of the animals in captivity because there were no objects related for instance to dense vegetation or relief preventing observation of the gerbils when they were active on the ground surface. With the exception of the marking rate, no other significant differences were found in the territorial and marking behavior as well as in the social interactions of gerbils housed in the larger enclosures as compared with the natural habitat (Gromov 2000b). Quite a different situation took place when I started the observations of a group of gerbils (4 males, 4 females) introduced into a smaller enclosure (15 × 15 m). After some period of aggressive encounters, only two pairs of the gerbils remained, and one of the pairs became a dominant one, using and marking all the available area. The second pair was a subordinate one for as many as three weeks, did not possess its own territory, used temporary shelters, exhibited very low rate of the marking activity (Fig. 6 B), and finally died because of

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Figure 6. Averaged making rates (M ± SE) of adult Mongolian gerbils in dependence on the housing conditions: A – in enclosures of 20 × 20 m, B – in enclosure of 15 × 15 m; I – ventral rubbing, II – building up “signal heaps”. Vertical axis – number of scent marks per 1 h of observations.

permanent agonistic encounters with dominants. A month later, I introduced another group of eight individuals into the enclosure, and the result of the second experiment was the same (Gromov 2000b). Thus, restriction of space has led to significant alteration of the behavior of some individuals and to the suppression of their activity related to territoriality and scent marking. I can conclude that an area of about 200 m2 is too small for two family groups of the Mongolian gerbil to occupy and use separate home ranges. Similar results were obtained in studies of another rodent – the California vole (Microtus californicus). The family-group mode of life is rather typical of this vole species which family groups usually consist of an adult pair and their offspring (Pearson 1960; Lidicker 1980). Field investigations showed that during the breeding season adult individuals occupy protected territories averaging 100 m2 in females and about 170 m2 in males. As a rule, in a family pair a larger territory of the male overlap a smaller home range of the female. Sometimes, two or three females can occupy significantly overlapping home ranges in association with a protected territory of the male (Lidicker 1973; Ostfeld 1985, 1986; Ostfeld et al. 1985). Lidicker (1979, 1980) carried out observations of seven enclosure populations of the California vole that were initiated with two or three pairs of adults, which were trapped in natural habitats or were laboratory-born offspring of the animals captured in the wild. Two predator- and escape-proof enclosures 9.1 × 9.1 m (83 m2) were utilized in his study. In five cases, a single pair of voles remained after a short period of observations (one-two weeks). In another case, a male with two females remained in the enclosure, and both females occupied separate ranges. And in the last case, two pairs of the voles remained in the enclosure, both occupying separate and protected territories. All other voles died in agonistic encounters. Reproduction in the experimental populations was initiated as soon as the colonizers were

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reduced to a single social unit. I’d like to emphasize that average home ranges of female California voles in the natural habitat are about 100 m2, so that the area of the enclosure was in 6 of 7 cases too small for more than one family pair or a complex social unit consisting of a male with two females. Therefore, one can conclude that family groups both in the Mongolian gerbil and the California vole occupy not so large and protected territories whose size seems can’t be too small to co-exist successfully with adjacent families. This rule appears to hold for all rodent species with a family-group manner of life. But there are species whose behavior does not markedly alter under semi-natural conditions like, for example, in the Tamarisk gerbil (Meriones tamariscinus) that is also a medium-sized rodent (adult wt 80-120 gm) inhabiting semi-arid regions of Kalmykia to north-west of the Caspian Sea and preferring habitats with Tamarix romasissima shrubs that grow on sand hills (Fig. 7). To study the use of space by the Tamarisk gerbil we applied a capture-recapture method on a 7.4 ha plot and adjacent area of about 30 ha (Gromov et al. 1996, Gromov 2001). Our study revealed that adults of both sexes occupy individual home ranges of a large size comprising several thousand square meters (Fig. 8). During the mating season, male Tamarisk gerbils did not exhibit strong territorial behavior. Aggregations of males in the vicinity of ranges of receptive females were regularly found, so that male home ranges overlapped in a great extent (Fig. 8 A). Male and female Tamarisk gerbils appear to occupy

Figure 7. A typical habitat of the Tamarisk gerbil in the north-western Caspian Sea region. Shrubs – Tamarix romasissima. Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

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overlapping individual home ranges rather than live in pairs during much of the breeding season. Territoriality, i.e. protection of the home range, was characteristic of females and some young individuals, but they defended the core area in the vicinity of their burrows only (Gromov & Gromova 1996). Female home ranges averaged 2267  332 m2 (n = 12) and were mutually exclusive (Fig. 8 B). Another typical feature of space use in the Tamarisk gerbil is high mobility of males during the breeding season (in spring and early summer) so that it was not possible to size their home ranges correctly. Sometimes we record males moving up to 700-900 m away from the original place of capture. As an appropriate measure of male home ranges, we used Range Length (RL) defined as the straight-line distance between the two most distant points where the male was recorded. In spring and early summer, i.e. at the mating season, mean male RL = 336  59 m (n = 10). With termination of reproduction in late summer and autumn, males became more sedentary, their home range sizes were found to be reduced (RL = 165  45 m, n = 8), and the spatial distribution of the male ranges was revealed to be similar to that of the females. Thus, distinct seasonal changes in use of space related to reproduction cycle are very typical of M. tamariscinus males.

Figure 8. Map of the distribution of smoothed minimum convex polygon home ranges (thick line contours) of adult males (A) and females (B) of the Tamarisk gerbil within rectangular plot (7.4 ha) used for regular trapping of the animals during the breeding season (May-June 1993), and on 30 ha adjacent area. TS – Tamarix shrubs. Arrows indicate movements of the males between their home ranges overlapping the ranges of the females.

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The Tamarisk gerbil is active at night-time only, so it was impossible to observe the animals in the wild. To continue the study of social behavior and other activities of M. tamariscinus, we carried out visual observations of the animals, caught in their natural habitats, under semi-natural conditions in the outdoor enclosures (20 × 20 m) using artificial illumination and the same method of registration of their activities as in the study of the Mongolian gerbil (Gromov & Gromova 1996). At the beginning of the observations (in May), a group of adult individuals (2 males and 2 females) was introduced into each of two enclosures. After some period of agonistic encounters females established separate territories (Fig. 9 A) whose location remained reasonably stable during the whole observation period (till October) with the exception of shifting of the female activity centers related to the change of their nest burrows in September (Fig. 9 B). As for males, they used all the available area till September (Fig. 9 A), and one of the males became dominant in each enclosure population and regularly chased the subordinate one. Dominant males were more active in social contacts and visited female burrows more frequently than subordinate males. The gerbils successfully reproduced in the enclosures, and to the end of the observations, every female gave birth to two litters. Young individuals of the second litters became active above ground at the beginning of September, and by this time adult males established separate ranges in the enclosures (Fig. 9 B) while their relationships also altered: dominance hierarchy changed into territoriality or at least minimization of direct contacts between the males with prevalence of mutual avoidance. Thus, spacing dynamics in the enclosure populations of M. tamariscinus was found to be very similar to that in the natural habitat. It is surprising, but young individuals were also able to occupy small protected territories (not exceeding several square meters) along with adults within the enclosures. Frequency of agonistic interactions in the enclosure populations was rather high, but the aggressiveness did not lead to the death of the gerbils even when an extraordinary density was achieved – as many as 23 individuals including 8 adults per enclosure. Bearing in mind the very large M. tamariscinus home ranges in the natural habitat, such a situation in the enclosure populations was rather unexpected.

Figure 9. Contour mapping of the frequency of visual registration of Tamarisk gerbils in enclosure of 20 × 20 m. Contour lines connect points of equal frequency of registration per unit area (square 2.5 × 2.5 m). Higher density of the lines corresponds to the activity centers of the animals related to their nest burrows. A – in early summer (the mating season), B – in autumn (after termination of reproduction).

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To resume the results of studies of enclosure populations of different rodent species with various spacing strategies and social organization I can conclude that a minimum space that is needed for vital functions and which does not alter rodent behavior is species-specific, and it is necessary to take this fact into account when planning any behavioral studies on rodents. Besides, I’d like to emphasize that based on data obtained due to field investigations of space use (for example, on multiple-catch data), a researcher can predict the behavior of rodents in relation to their territoriality, social structure and mating system. For instance, overlapping home ranges of males associated with female ranges during the breeding season indicate a lack of territoriality, weak pair-bonding and promiscuous or polygynous mating. On the contrary, the concordance in home ranges is typical of heterosexual pairs in species with a family-group mode of life exhibiting distinct territoriality and behavioral monogamy. It means particularly that there is no sense in housing and observing multi-male-multi-female groups of these species in captivity: it can only leads to death of the animals because of aggressive encounters. Other examples concern the effect of different laboratory conditions on parental behavior of two rodent species – the meadow vole (Microtus pennsylvanicus) and the wood-mouse (Peromyscus leucopus). Population ecology and behavior of the meadow vole has been studied quite thoroughly (Getz 1961, 1962, 1972; Ambrose 1969; Turner & Iverson 1973; Madison 1980a, b; Webster & Brooks 1981; Madison et al. 1984; Ostfeld et al. 1988). In brief, field investigations showed that males of this vole species occupy significantly larger home ranges and show significantly greater intrasexual overlap than do females. For males, there was no relationship between breeding success and either home range’s size or intrasexual overlap. No indication was found of lasting pair formation or of siblings remaining together once they had dispersed from their site of birth. There was also no indication of formalized social structure within the meadow vole population: movement and association of individuals within the population appeared to be random. As a result of promiscuity, multiple paternity is very characteristic of the meadow vole (Berteaux et al. 1999). Interactions between adult individuals of the same sex were found to be mainly aggressive. A lack of tolerance is rather typical of male-female interactions. But in late autumn, male meadow voles were found to share nests with the female and the last litter of the season, and these voles also overwinter in groups. Based on this data, one can conclude that pair-bonding is not characteristic of the meadow vole, especially during the breeding season. However, a laboratory study (Hartung & Dewsbury 1979) showed that breeding pairs exhibited nest-cohabitation, and moreover, males like the females were engaged in some care-giving activities like pup grooming when housed and observed in small laboratory cages 48 × 27 × 13 cm. Each of the cages was lined with San-i-cel bedding material and had a cotton pad as nesting material. Sex differences were found to be insignificant under such housing conditions (Fig. 10 A). In another study (McGuire & Novak 1984), each breeding pair was placed into a unit of two 1.3 × 1.3-m tablelike pens which were joined by two Plexiglas tunnels. Each pen contained a 3-cm peat substrate and a 10-20-cm layer of hay cover. Under such semi-natural conditions, females spent significantly less time in the nest (Fig. 10 B). As for males, they showed a tendency to enter the nest when the female left the young unattended, but paternal care was never observed. Observations in nature also showed that males avoid entering the natal nests (Madison et al. 1984; Ostfeld et al. 1988). It was supposed that the limited space and lack of

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Figure 10. Mean values (M ± SE) of some care-giving activities in breeding pairs of the meadow vole in dependence on housing conditions. A – in a small laboratory cage of 48 × 27 × 13 cm, B – in a unit of two 1.3 × 1.3-m table-like pens. I – nest-attendance, II – pup grooming. Vertical axis – time in seconds per 15-min period of observations (adapted after Hartung & Dewsbury 1979 and McGuire & Novak 1984).

cover in small cages may alter male-female tolerance, so that the male can enter the maternal nest and socialize with the young (Hartung & Dewsbury 1979; Wilson 1982). Similar results were obtained in studies of the wood-mouse. Field investigations showed that like most small rodents these mice occupy distinct home ranges which tend to be exclusive of the ranges of others of the same sex, and females exhibit this trend more strongly than males (Sheppe 1966; Metzgar 1971). Mutually exclusive home ranges (i.e. with very little overlap) usually reflect intolerance or social interactions between individuals of the same sex and even between males and females referred to as agonistic and overt aggressive except for interactions in bisexual pairs during the mating season. The female wood-mice appeared to form a closed community in which the residents occupy home ranges of a stable size (05-0.9 ha). Adult male home ranges are usually larger than those of females, so that males protect or advertise a much larger area (up to 1.3 ha) than females (Beer 1961; Metzgar 1973; Mineau & Madison 1977). Male and female home ranges do not correspond closely, as would be expected if the wood-mouse formed typical pair bonds, and electrophoresis indicates promiscuity in this species (Xia & Millar 1988). During the breeding season, males tend to form temporary associations (for 1-2 weeks) with receptive females but avoid entering the natal nests (Nicholson 1941). However, when housed in small laboratory cages 48 × 27 × 13 cm (Hartung & Dewsbury 1979), males of the wood-mouse exhibited nest-cohabitation with the female mate and parental care related particularly to pup retrievals and pup grooming (Fig. 11). Sex differences in parental behavior were found to be insignificant under such housing conditions.

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Figure 11. Mean values (M ± SE) of some care-giving activities in breeding pairs of the wood-mouse in small laboratory cages 48 × 27 × 13 cm. I – nest-attendance, II – pup grooming. Vertical axis – time in seconds per 30-min period of observations (adapted after Hartung & Dewsbury 1979).

Xia and Miller (1988) examined relationships among males and their mates in an in-room enclosure (2.4 m long, 1.8 m wide, and 0.8 m high, open at the top), constructed of wood partitions and contained four nest boxes (21.5 × 14.5 × 13.5 cm, inside dimensions). The wood-mice could leave the enclosure by climbing up one corner of the enclosure, which gave them access to a 3.2 × 4.5 m room. Neither food nor water was provided outside the enclosure, and mice could easily reenter the enclosure by climbing one of several support struts. Fourteen pairs of wood-mice were initially maintained in laboratory cages until females were in the late stages of pregnancy or had given birth. At that time, pairs were transferred to the enclosure. Whole-night (7-h) observations of the mice during the course of a week showed that 5 of 14 females were very aggressive towards their mates and, except during postpartum estrus, actively search for and chased them throughout most of the observation period. Another three females were aggressive only when the males attempted to enter their nests. No male was aggressive towards females. Males shared nests with nonaggressive females when they were pregnant, but not when they were lactating. Males in pairs with aggressive females built their own nests. Eight males left the enclosure, built nest outside, and stopped visiting nest boxes in the enclosure. Males rarely entered the female’s nest with young. Moreover, even if a male did enter his female’s nest box, the duration of his stay never exceeded 2 min. These results show that direct paternal care did not occur, even with full paternity and no chance of extra mating. It means that paternal behavior (at least the direct one) is very unlikely in the wood-mouse in nature. The fact that 5 of 14 females were aggressive towards their mates and another 3 actively prevented their mates from entering their nests suggests that females do not tolerate paternal involvement in raising the pups.

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Thus, there is a paradox – males of some species exhibit paternal care when housed together with the female mates in small laboratory cages, but do not exhibit care of young under semi-natural condition as well as in the natural habitat. One explanation for this paradox is that the paternal behavior patterns documented under observations in small cages are laboratory artifacts. Another conclusion is that formerly altered behavior can be subsequently normalized in a semi-natural environment. But in any case a researcher needs to be advised of the “normal” behavior of the subject under study based on data obtained in natural habitats due to either his own field investigations or those carried out by others. Reading a publication that describes results of pair encounters of, for example, some voles, hamsters or gerbils on a neutral arena with reference to their territorial behavior, or occurrence of a dominance hierarchy established between adult males in confined laboratory groups of a species that lives in families in the wild, I know that the author of such a publication errs himself and misleads his readers because there is no sense in studying territorial behavior of the overwhelming majority of rodent species under laboratory conditions (with very few exceptions, such as house mice, Mus musculus or Mus domesticus), and dominance hierarchy between males is characteristic of species that form multi-male-multi-female aggregations or breeding colonies like house mice, some voles (e.g. Clethrionomys spp., Viitala 1977; Bujalska & Grϋm 1989), gerbils (e.g. Meriones meridianus, Gromov 2000a, 2008) or squirrels (e.g. Sciurus niger, Benson 1980), but not those living in family groups (e.g. M. unguiculatus or the mandarin vole, Lasiopodomys mandarinus, Smorkatcheva 1999). Indeed, if several males of, for example, the mandarin vole, were housed together in a small cage, aggressive encounters could often occur between them, and one of the males would become a dominant and some others would become subordinate for a relatively short period. But such a situation is a laboratory artifact because male mandarin voles, like males of other rodent species living in family groups, do not compete for receptive females during the mating season, like in species living in multi-male-multi-female breeding colonies, and hence do not establish dominance hierarchy in their natural habitats. Resuming this paper, I’d like to draw the following main conclusions: (i) space (or home range) is a very important factor affecting rodent behavior, and laboratory studies underestimate or even neglect the role of space in the performance of various rodent activities; (ii) in any rodent species, there is a minimum limit of space that is needed for vital functions, and essential restriction of the space can dramatically alter various behavioral activities, especially those related to territoriality, scent marking, social interactions or parental care; (iii) to avoid laboratory artifacts, behavioral studies of rodents in captivity have to be carried out after, but not before, appropriate field investigations.

REFERENCES Ågren, G., Zhou Q. & Zhong W. (1989). Ecology and social behaviour of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China. Anim. Behav., 37, 11-27. Ambrose III, H.W. (1969). A comparison of Microtus pennsylvanicus home ranges as determined by isotope and live trap methods. Amer. Midland Nat., 81, 535-555.

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Beer, J.R. (1961). Winter home ranges of the red-backed mouse and white-footed mouse. J. Mammal., 42, 174-180. Benson, B.N. (1980). Dominance relationships, mating behaviour and scent marking in fox squirrels (Sciurus niger). Mammalia, 44, 143-160. Berteaux, D., Bety, J., Rengifo, E. & Bergeron, J.-M. (1999). Multiple paternity in meadow vole (Microtus pennsylvanicus): investigating the role of the female. Behav. Ecol. Sociobiol., 45, 283-291. Bujalska, G. & Grϋm, L. (1989). Social organization of the bank vole (Clethrionomys glareolus, Schreber, 1780) and its demographic consequences: A model. Oecologia, 80, 70-81. Getz, L.L. (1961). Home ranges, territory and movement of the meadow vole. J. Mammal., 42, 24-36. Getz, L.L. (1962). Aggressive behavior of the meadow and prairie voles. J. Mammal., 43, 351-358. Getz, L.L. (1972). Social structure and aggressive behavior in a population of Microtus pennsylvanicus. J. Mammal., 53, 310-317. Gromov, V.S. (1981). Social organization of the family groups of clawed jird Meriones unguiculatus in natural colonies. Zool. Zhurnal, 60, 1683-1694 [in Russian with English summary]. Gromov, V.S. (1997). Territory scent marking in gerbils: A comparative analysis in four species of genus Meriones. Zhurnal Obshch. Biol., 58, 46-80 [in Russian with English summary]. Gromov, V.S. Ethological Mechanisms of Population Homeostasis in Gerbils (Mammalia, Rodentia). Moscow: IPEE Press; 2000a [in Russian]. Gromov, V.S. (2000b). A comparative analysis of behavior of Mongolian gerbil (Meriones unguiculatus) in nature and captivity. Zool. Zhurnal, 79, 1344-1354 [in Russian with English summary]. Gromov, V.S. (2001). Environmental heterogeneity and spatial structure of gerbil colonies (Rodentia, Gerbillinae. Entomol. Review, 81, Suppl., 161-166. Gromov, V.S. Spatial-and-ethological Structure of Rodent Populations. Moscow: KMK Press; 2008 [in Russian with English summary]. Gromov, V.S. & Gromova, L.A. (1996). Use of space, social relationships, and scent marking in the Tamarisk gerbil (Meriones tamariscinus) under semi-natural conditions. Zool. Zhurnal, 75, 280-296 [in Russian with English summary]. Gromov, V.S. & Popov, S.V. (1979). Some peculiarities of spatial-ethological structure of the clawed jird (Meriones unguiculatus) colonies and attempts of influencing it with pharmaca. Zool. Zhurnal, 58, 1528-1535 [in Russian with English summary]. Gromov, V.S., Tchabovsky, A.V., Paramonov D.V. & Pavlov A.N., (1996). Seasonal dynamics of demographic and spatial structure of a population of the Tamarisk gerbil (Meriones tamariscinus) in the Kalmykia semi-desert. Zool. Zhurnal, 75, 413-428 [in Russian with English summary]. Hartung, T.G. & Dewsbury, D.A. (1979). Paternal behavior of six species of muroid rodents. Behav. Neural Biol., 26, 446-478. Lidicker, W.Z., Jr. (1973). Regulation of numbers in an island population of the California vole, a problem in community dynamics. Ecol. Monogr., 43, 271-302.

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Lidicker, W.Z., Jr. (1979). Analysis of two freely-growing enclosed populations of the California vole. J. Mammal., 60, 447-466. Lidicker, W.Z., Jr. (1980). The social biology of the California vole. The Biologist, 62, 46-55. Lindzey, G., Thiessen, D.D., Tucker, A. (1968). Developmental and hormonal control of territorial marking in the male Mongolian gerbil (Meriones unguiculatus). Develop. Psychobiol., 1, 97-99. Madison, D.M. (1980a). Space use and social structure in meadow vole, Microtus pennsylvanicus. Behav. Ecol. Sociobiol., 7, 65-71. Madison, D.M. (1980b). An integrated view of the social biology of Microtus pennsylvanicus. The Biologist, 62, 20-33. Madison, D.M., Fitzgerald, R.W. & McShea, W.J. (1984). Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences of population cycling. Behav. Ecol. Sociobiol. 15, 9-17. McGuire, B. & Novak, M. (1984). A comparison of maternal behaviour in the meadow vole (Mictotus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim. Behav., 32, 1132-1141. Metzgar, L.H. (1971). Behavioral population regulation in the wood-mouse, Peromyscus leucopus. Amer. Midland Nat., 86, 434-448. Metzgar, L.H. (1973). A comparison of trap- and track-revealed home ranges in Peromyscus. J. Mammal., 54, 513-515. Mineau, P.M. & Madison, D. (1977). Radio-tracking of Peromyscus leucopus. Can. J. Zool., 55, 465-468. Nicholson, A.J. (1941). The homes and social habits of the wood-mouse (Peromyscus leucopus noveboracensis) in Southern Michigan. Amer. Midland Nat., 25, 196-223. Ostfeld, R.S. (1985). Limiting resources and territoriality in microtine rodents. Amer. Nat., 126. 1-15. Ostfeld, R.S. (1986). Territoriality and mating system of California voles. J. Anim. Ecol., 55, 691-706. Ostfeld, R.S., Lidicker, W.Z., Jr. & Heske. E.J. (1985). The relationship between habitat heterogeneity, space use, and demography in a population of California voles. Oikos, 45, 433-442. Ostfeld, R.S., Pugh, S.R., Seamon, J.O. & Tamarin, R.H. (1988). Space use and reproductive success in a population of meadow voles. J. Anim. Ecol., 57, 385-394. Owen, K. & Thiessen, D.D. (1973). Regulation of scent marking in the female Mongolian gerbil Meriones unguiculatus. Physiol. Behav., 11, 441-445. Payman, B.C. & Swanson, H.H. (1981). Scent marking and dominance in enclosure colonies of gerbils. Behav. Brain Res., 2, 271-272. Pearson, O.P. (1960). Habits of Microtus californicus revealed by automatic photographic recorders. Ecol. Monog., 30, 231-249. Sheppe, W. (1966). Determinants of home range in the deer mouse, Peromyscus leucopus. Proc. Calif. Acad. Sci. 34, 377-418. Smorkatcheva, A.V. (1999). The social organization of the mandarin vole, Lasiopodomys mandarinus, during the reproductive period. Z. Säugetierk, 64, 344-355. Sokolov, V.E. & Gromov, V.S. Territorial Scent Marking in Gerbils (Mammalia, Rodentia). Moscow: IPEE Press; 1998 [in Russian with English summary].

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Thiessen, D.D. (1968). The roots of territorial marking in the Mongolian gerbil: A problem of species-common topography. Behav. Res. Meth. and Instr., 1, 70-76. Thiessen, D.D., Blum, S.L. & Lindzey G. (1969). A scent marking response associated with the ventral sebaceous gland of the Mongolian gerbil, Meriones unguiculatus. Anim. Behav., 18, 26-30. Turner, B.N. & Iverson S.L. (1973). The annual cycle of aggression in male Microtus pennsylvanicus, and its relation to population parameters. Ecology, 54, 967-981. Viitala, J. (1977). Social organization in cyclic subarctic populations of the voles Clethrionomys rufocanus (Sund.) and Microtus agrestis (L.). Ann. Zool. Fennici, 14, 5393. Webster, A.B. & Brooks, R.G. (1981). Social behavior of Microtus pennsylvanicus in relation to seasonal changes in demography. J. Mammal., 62, 738-751. Whitsett, J.M. & Thiessen, D.D. (1972). Sex differences in the control of scent marking behaviour in the Mongolian gerbil (Meriones unguiculatus). J. Comp. Physiol. Psychol., 78, 381-385. Wilson, S.C. (1982). Parent-young contact in prairie and meadow voles. J. Mammal., 63, 300-305. Xia, X. & Millar, J.S. (1988). Paternal behavior by Peromyscus leucopus in enclosures. Can. J. Zool., 66, 1184-1187.

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In: Rodents Editors: Alfeo Triunveri and Desi Scalise

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Chapter 4

PROECHIMYS: A RODENT STILL POORLY UNDERSTOOD Carla Alessandra Scorza1, Bruno Henrique Silva Araujo1, Laila Brito Torres1,2 and Esper Abrão Cavalheiro1 1

Disciplina de Neurologia Experimental, Universidade Federal de São Paulo/Escola Paulista de Medicina (UNIFESP/EPM), São Paulo, Brasil 2 Instituto Evandro Chagas, IEC/Centro Nacional de Primatas, Ananindeua, Pará, Brasil

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ABSTRACT Rodentia is the largest order of living mammalia encompassing 2277 species, or approximately 42% of worldwide mammalian biodiversity. The predominantly South American representative families are Echimyidae and Cricetidae. The Neotropical spiny rats of the family Echimyidae are the most taxonomically, ecologically, and morphologically diverse group of all extant hystricognath rodents. They are small-bodied animals distributed throughout the Neotropical region from Central America to Argentina. It has been suggested that most of the cladogenesis leading to the extant echimyid genera probably occurred during the Late Miocene, about eight million years ago. In addition to be the most species-rich caviomorph family, the Echimyidae have the greatest diversity of ecomorphological adaptations within hystricognath rodents. Proechimys (suborder hystricomorpha, infraorder histricognathi, family echimyidae, subfamily eumysopinae) are the most abundant and widespread terrestrial lowland small mammals in Neotropical rainforests, occurring from Honduras in Central America to Paraguay in South America. Virtually, any forested lowland habitat is likely to harbor at least 1 species of Proechimys (spiny rat), and some areas may have up to 4 sympatric species. Spiny rodents are generalists with respect to use of forested habitats. In particular, these rodents were associated with forest gaps and areas with shorter canopies and higher densities of smaller trees, logs, and lianas. Younger forests and tree-fall gaps within older forests represent areas of rapid plant recruitment and growth due to increased light availability. Effects of spiny rodents on seed survival via predation and dispersal and on arbuscular mycorrhizal fungal infection via spore dispersal may be particularly pronounced in such areas. In this sense, Proechimys plays an important role

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Carla Alessandra Scorza, Bruno Henrique Silva Araujo, Laila Brito Torres et al. in forest dynamics through their activities as seed predators and dispersers of seeds. Moreover, Proechimys has received some attention as a natural host to infectious parasites and recently, the brain of the Proechimys (P. guyannensis) started to be studied. Previous findings have shown that Proechimys are extremely sensitive to epileptogenic treatments, but they seem unable to establish an epileptic focus and subsequent spontaneous seizures. In this line of evidence, Proechimys was designated as an animal model of resistance to epilepsy. These findings provide new directions for the potential use of Proechimys in the field of neuroscience. Furthermore, they have direct implications for the study of the normal brain as well as for elucidating intrinsic mechanisms of central nervous system disorders.

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INTRODUCTION Forty percent of mammal species are rodents, and they are found in vast numbers on all continents other than Antarctica (Myers, 2000). The most structurally diverse and speciose group of living hystricognath rodents in South America are the tree rats and spiny rats of the family Echimyidae (Lara & Patton, 2000). The terrestrial spiny rats, genera Proechimys, occur from Honduras in Central America to the northern temperate region of Argentina in South America, in all lowland tropical forest and savanna habitats. However, aspects of their distribution, species limits, and taxonomy are still poorly understood (Lara & Patton, 2000). Furthermore, despite the ecological and evolutionary diversity within the family, systematic studies of echimyids at all levels are still in their infancy (Leite & Patton, 2002). The Amazon and the Atlantic forests morphoclimatic domains of South America encompass the most diverse tropical forests in the world (Ab’Saber, 1977). Between these two forests lies a belt of more open vegetation, including the Argentinean and Paraguayan Chaco, the Caatinga in northeastern Brazil, and the central Brazilian Cerrado, the latter being the second largest domain in Brazil extending over 2 million km2 (Costa, 2003). If, at first glance, these two forests appear widely isolated, it has been showed that the ubiquitous gallery forests and series of deciduous and semi-deciduous forest patches constitute a network of interconnected forests through otherwise open landscape (Oliveira-Filho & Ratter, 1995; Vivo, 1997; Costa, 2003). Under this scenario, echimyid rodents of the genus Proechimys often are the most abundant and widespread lowland forest rodents throughout much of their range in the Neotropics (Fig. 1) (Eisenberg 1989). Virtually any forested lowland habitat is likely to harbor at least 1 species of Proechimys, and some areas may have up to 4 sympatric species (Patton & Gardner 1972; Lambert & Adler, 2000). Proechimys is a generalist species with respect to use of forested habitats (Adler 1996; Tomblin & Adler 1998). However, presence of spiny rats was best predicted by variables that characterized younger or more disturbed forest (Gonzalez & Alberico 1993; Tomblin & Adler 1998; Lambert & Adler, 2000). Specific structural features of secondary forest that may promote an abundance of spiny rats remain unknown. Such information is essential to unveil the role of these animals in Neotropical forests, especially with respect to forest regeneration (Lambert & Adler, 2000). In this line of evidence, studies suggested that Proechimys rodents play an important role in forest dynamics. Proechimys rodents are mostly herbivores, feeding primarily on fallen fruits, seeds, but sometimes on fungi. Because of their diet and abundance, these animals affect seed placement and survival, thus influencing plant species distributions and community structure. Nevertheless, it has been noted the potential importance of such small rodents as frugivores

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Figure 1. Proechimys occurrence.

and seed dispersers in the Neotropics (Vieira et al., 2003). Certainly, the potentially role of spiny rats in affecting forest regeneration warrants further investigations. The spiny rat Proechimys (Fig. 2) is about the size of a common house rat, except with a larger head, smaller prominent ears and spiny pelage. The stiff pointed hairs or spines allow for protection. The eyes are large and protuberant with vertical slit pupil (Weir, 1973). Their fur is orange-brown on the upper body and white underneath. The forefeet have four functional digits, and the hindfeet five. Adults weight from about 240 to 500 grams (Gliwicz,

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Carla Alessandra Scorza, Bruno Henrique Silva Araujo, Laila Brito Torres et al.

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Figure 2. Proechimys rodent.

1984; Weisbecker & Schmid, 2007). In captivity, Proechimys at 100 days of age, males (302+/-7g) were significantly heavier than females (237+/-6g) (Weir, 1973). Head and body length is about 6.4 to 12 inches (16.0 to 30.0 centimeters) and a tail length of 4.4 to 12.8 inches (11.2 to 32.5 centimeters). These animals can break off their tails when attacked. The almost naked scaly tail readily autotomizes at the base, between the 5th and 6th caudal vertebrate (Hamilton, 1939) and does not regenerate (Weir, 1973). This action confuses predators long enough for the animal to escape. However, obviously, this technique can be used only once in each individual's lifetime. The spiny rat Proechimys is nocturnal, meaning it is mostly active at night. It sleeps, nests, and stores food in burrows dug by other animals, rock crevices, or hollows in trees or logs. The rodents spent the day in natural dens and did not appear to dig burrows (Emmons, 1982; Emmons & Feer, 1997). According to Emmons (1982), home areas are small and nightly movements are short. Usually, only a single adult inhabits a burrow system (Guillotin, 1982). The male defends its burrow against other males. The incisor teeth are light orange (Weir, 1973). Proechimys rodents are generally docile in captivity and if handled carefully they do not attempt to bite. However, adults are intolerant and may be aggressive towards one another. When threatening a rival, the rodent can produce vocalizations (Eisenberg, 1974). Some groups would fight continually, whilst others remain placid for long periods and then suddenly become angry (Weir, 1973). But, a male and a female can be housed together. During courtship, a variety of vocalizations are employed (Maliniak & Eisenberg, 1971). In laboratory captivity, the first vaginal opening occurred at 65.6+/-2.4 days of age in females that were caged with competent males, and at 95.2+/-7.5 days in females isolated from males (Weir, 1973). Oestrus occurs throughout the year (Weir, 1973). Females present a vaginal closure membrane which is perforated only at oestrus and parturition. The mean cycle length is 22.5+/- 3.4 days (Weir, 1973). Females have three pairs of mammae, one inguinal and two lateral thoracic pairs (Weir, 1974). The species breeds throughout the year and the length of gestation period ranges from fifty-five to about sixty-three days. Jones and Pugsley (1980) described high incidence of dystokia in Proechimys. According to their observation, of over 50 species of rodents examined post mortem, this high incidence of dystokia has only been seen in Proechimys. Litter sizes averaged 2.5 (Fleming, 1970) and 2.8 (Maliniak & Eisenberg, 1971). Everard and Tikasingh (1973) reported that the young animals are weaned at 31 to 35 days. The mean weight at birth was about 20.9 grams (Weir, 1973). The animals are born

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fully haired and with their eyes open. Furthermore, newly-born Proechimys are active within a few hours and they are able to walk supporting their full weight. In these rodents, adult proportions are reached at ninety days of age. They reach sexual maturity at six to seven months. Life spans of most tropical mammals are poorly known, particularly for wild populations, mainly because most studies of tropical mammals are of insufficient duration in order to estimate life spans (Oaks et al., 2008). Oaks and colleagues, in an over 9-year period study, estimated Proechimys´s median life spans ranging from 6.5 to 10 months, and maximum life spans from 36 to 53 months. Moreover, they also found that life spans did not differ between sexes and, surprisingly, survival curves of males and females displayed remarkable congruence (Oaks et al., 2008). In captivity, maximum reported lifespan was 5.8 years (Weigl, 2005).

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PROECHIMYS TAXONOMY The determination and distinction of species and their relationships were held based on their morphological differences and similarities (Guerra, 1988). The taxonomy of the rodents is often hampered by slight variations in cranial and external morphology of these individuals. However, the wide range of morphological variation observed in the genus Proechimys has made species determination difficult. This has caused problems in the taxonomy of the genus (Thomas, 1927, 1928a, 1928b; Hershkovitz, 1948; and Moojen, 1948). Thomas (1928a) remarked that "The bewildering instability of the characters of these spiny rats makes it, at present, impossible to sort them according to locality into separate species, subspecies, or local races." Although the extremely high character variability within and among the genus Proechimys, some progress has been made in defining species units and this has only been possible due to the development of molecular and biochemical techniques. In this sense, cytogenetics is a critical tool for separation of cryptic species or species complexes especially when they occur in sympatry (Aniskin & Volobouev, 1999; Weksler et al. 2001; Granjon and Dobigny, 2003), as observed in studies in the genus Proechimys (Gardner & Emmons, 1984, Patton et al. 2000, Weksler et al., 2001). Cytogenetic most commonly used to characterize species are the number, morphology and chromosomal banding pattern (Guerra, 1988). These studies can detect chromosome polymorphisms, which may cause the formation of individuals with different karyotypes in the population may or may not lead to a differentiation of species by reproductive isolation and the consequent speciation (Volobouev & Catzeflis, 2000). Some species of rodents present a karyotype very similar to each other, however, exhibit intraspecific variation in morphology and number of chromosomes (Aniskin & Volobouev, 1999), indicating the presence of chromosomal rearrangements, which makes the chromosomal characterization in this group to be increasingly useful. Since the early 1970's, karyological studies have been conducted in species of the genus Proechimys (Patton and Gardner, 1972). In 1976, 13 karyotypic forms were known for probably the same number of species (Reig & Useche, 1976). Almost a decade later, in 1984, those numbers have doubled, with 28 karyotypic forms for 25 species (Gardner & Emmons, 1984). In a recent review of cytogenetics to the genus, 52 forms of karyotypes were identified, with diploid chromosome numbers ranging from 14 to 62 chromosomes (Weksler et al., 2001). Later, at least five other new karyotypic forms were described (Bonvicino et al.,

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2005, Machado et al., 2005), totaling 57 forms to the genus Proechimys. Due to the existing taxonomic chaos to the genus Proechimys, a simple comparison of the chromosomal data obtained with those available in literature becomes a difficult task. Thus, an additional molecular or biochemical technique, like mitochondrial DNA (mtDNA) might be desirable for discriminating each species of Proechimys. The mitochondrion is the major cellular organelles due of its energy function. It is found in all eukaryotic organisms and has genome itself. For years, the mtDNA are being used as an accessory tool in studies of closely related species and in phylogenetic reconstruction of recent history (Avise et al. 1987; Avise, 1994; Simon et al., 1994). Among the key features that favor the mitochondrial genome as a good source of data for molecular taxonomy, we can mention the difference in sequences between closely related species is 5 to 10 times higher in mitochondrial genes than in nuclear genes, the absence of introns, the larger number of copies within a single cell; fewer sequence differences within a single species due to recombinant mitochondrial genome and in most cases of maternal origin (Brown et al., 1979; Wilson et al. 1985; Moritz et al. 1987; Avise et al. 1987; Avise, 1994). Phylogenetic analysis using mitochondrial genes have been proven effective in elucidating relationships among small mammals. One of the key genes used, the cytochrome b gene (cyt b), encodes one of the most important and well-conserved mitochondrial proteins related to cellular respiration and is one of the most well-known of the 13 protein coding genes in the mitochondrial genome (Hatefi, 1985, Smith & Patton, 1991; Mustrangi & Patton, 1997, Harris et al. 2000; Costa, 2003; Leite, 2003, Gonçalves & Oliveira, 2004, Reeder et al. 2006). Lara et al. (1996), based on sequences of cyt b, propose the simultaneous diversification of the family Echimyidae amounted Trinomys, formerly belonging to Proechimys, to the category of gender. In another study, da Silva (1998) used the sequences of mitochondrial cyt b, and morphological and karyological data to describe four new species of Proechimys (echinothrix, gardneri, kulinae and patton). In this work, the author also presented a molecular phylogeny of 12 species of Proechimys (amphicoricus, brevicauda, cayennensis, cuvieri, echinothrix, gardneri, kulinae, patton, spp., quadruplicatus, simons and steerei) showing that despite the phylogeny appearing to have little support for relationships among the species, its topology is consistent with the species identification. In the same year, da Silva and Patton (1998) presented a molecular phylogeny of Proechimys spp. belonging to the group goeldii, and concluded that out the four clades found, three of them could be treated as distinct species, which were Proechimys amphichoricus, goeldii and steerei. In addition, Matocq and coworkers (2000) compared the patterns of genetic diversity and population structure of steerei and simons from the Juruá river, based on the use of gene cyt b. They found that both species had approximately the same number of mitochondrial haplotypes but steerei showed a lower mean genetic diversity (7.09%) than simons (11.76%). Moreover, Steiner et al. (2000) and Van Vuuren (2004) analyzed two species from French Guiana, Proechimys cuvieri and cayennensis, through variations of the mtDNA. The authors observed the monophyly of clades in each species, confirming the syntopy of their populations and noting a divergence around 12% between these two species. Currently, 25 species are assigned to the Proechimys genus (Table. 1) (Woods & Kilpatrick, 2005), but this number may change as new areas are sampled and further studies on the systematics of Proechimys are made by combining ecological data, morphological, cytogenetic and molecular studies. This diversity, coupled with the difficulty in distinguishing

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Proechimys Table 1. All species of the genus Proechimys currently described and its territorial distribution (Woods & Kilpatrick., 2005) Species Proechimys brevicauda Proechimys canicollis

Common Name

Distribution

Reference

Huallago spiny rat

Bolivia; Brazil; Colombia; Ecuador; Peru; Venezuela

Günther, 1877

Colombian spiny rat

Colombia; Venezuela

Allen, JA., 1899

Proechimys chrysaeolus

-

Boyaca spiny rat

Thomas, 1898

Proechimys cuvieri

-

Cuvier’s spiny rat

Proechimys decumanus

-

Pacific spiny rat

Colombia Brazil; French Guiana; Guyana; Peru; Suriname; Venezuela Ecuador, Peru

Proechimys echinothrix

-

Stiff-spine spiny-rat

Brazil

da Silva, 1998

Proechimys gardneri

-

Gardner´s spiny rat

Bolivia; Brazil

da Silva, 1998

Proechimys goeldii

-

Goeldi’s spiny rat

Brazil; Colombia

Thomas, 1905

Guaira spiny rat

Venezuela

Thomas, 1901

Cayenne Spiny Rat

Brazil; French Guiana; Guyana; Suriname; Venezuela

Geoffroy É., 1803

Proechimys guairae Proechimys guyannensis Proechimys hoplomyoides

Proechimys cayennensis (Desmarest, 1817);Proechimys warreni (Thomas, 1905) -

Petter, 1978 Thomas, 1899

Guyanan spiny rat

Brazil; Guyana; Venezuela

Tate, 1939

Proechimys kulinae

-

Kulina Spiny-rat -

Brazil; Peru

da Silva, 1998

Proechimys longicaudatus

-

Long-tailed spiny rat

Bolivia; Brazil; Paraguay

Proechimys magdalenae

-

Magdalena spiny rat

Colombia

Proechimys mincae

-

Minca spiny rat

Colombia

Rengger, 1830 Hershkovitz, 1948 Allen, JA., 1899

Proechimys oconnelli

-

O’Connell’s spiny rat

Colombia

Allen, JÁ., 1913

Proechimys pattoni

-

Patton´s spiny rat

Brazil; Peru

da Silva, 1998

Gray-footed spiny rat

Colombia; Venezuela Brazil; Colombia; Ecuador; Peru; Venezuela

Osgood, 1914 Hershkovitz, 1948

Brazil

Thomas, 1901

Proechimys poliopus Proechimys quadruplicatus Proechimys roberti Proechimys semispinosus Proechimys simonsi Proechimys steerei Proechimys trinitatus Proechimys urichi

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Synonym/s Proechimys bolivianus (Thomas, 1901); Proechimys gularis (Thomas, 1911) -

Proechimys amphichoricus (Moojen, 1948) Proechimys oris (Thomas, 1904) Proechimys gorgonae (Bangs, 1905) Proechimys hendeei (Thomas, 1926) Proechimys trinitatis (J.A. Allen & Chapman, 1893) -

Napo spiny rat Roberto's Spiny Rat

Steere’s spiny rat

Colombia; Costa Rica; Ecuador; Honduras; Nicaragua; Panama Bolivia; Brazil; Colombia; Ecuador; Peru Bolivia; Brazil; Peru

Trinidad spiny rat

Trinidad and Tobago

Sucre spiny rat

Venezuela

Tome´s spiny rat Hendee’s spiny rat

Tomes, 1860 Thomas, 1900 Goldman, 1911 Allen, JA and Chapman, 1893 Allen, JA.,1899

these species in the genus, suggests that this is a group of vertebrates in active evolution, suitable for studying the evolutionary process and its onset (Reig & Useche, 1976).

PROECHIMYS: POTENTIAL RESERVOIR OF DISEASES In the last few decades, the global process of urbanization has greatly accelerated. By 2025, it is estimated that more than half of the world’s population will live in urban areas and most of the urban growth will occur in Latin America. This massive increase in urban population will be probably accompained by a significant increase of arthropod pests and rodents population. The impact in health in the urban conglomerations is visible, since these animals carry the spread of many communicable diseases. The rodent Proechimys can be considered as potential reservoir of diseases. Many features make this rodent as a potential reservoir, such as: transient infectivity to vectors; ability to reproduce year-round if environmental conditions are favorable (Fleming 1971, Adler & Beatty 1997), thereby providing a constant source of naive individuals (primarily juveniles) that are susceptible to infection; flexible demography, which apparently enables them to respond to favorable environmental conditions and thereby quickly increase in abundance (Adler 1996). Since they are habitat generalists, they are able to thrive in highly

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disturbed forest (Lambert & Adler 2000, Adler 2000), often in close proximity to humans. Thus, Proechimys could exhibit considerable reservoir potential when summed over an entire population or region. There is evidence that the genus Proechimys is related to the natural history of arbovirus, excelling as an indicator of activity of the Venezuelan Equine Encephalitis Virus (VEEV), a zoonosis that circulates in the forests of South America (Barrera et al. 2002). The role of spiny rats as VEEV reservoirs was reinforced by a study conducted in Venezuela and Colombia in which a correlation was established between the abundance of these rodents and levels of enzootic virus circulation. Futhermore, there are records of animal populations of this genus parasitized by Trypanosoma cruzi in Venezuela (Travi et al., 1994). In Brazil, populations of Proechimys guyannensis are identified as important reservoirs of tegumentary leishmania, a fact also observed in Panama (P. semispinosus) and Venezuela (P. guyannensis) (Travi et al., 2002). Currently, South America is a major endemic area for most tropical diseases to exist. Countries such as Costa Rica, Panama, Venezuela, Peru, Brazil, Argentina, Uruguay, Paraguay, Bolivia and Chile have added new reports of illnesses associated with endemic distribution hosts, most by wild rodents. In this way, Proechimys may be a useful tool for studying the pathogenesis and mechanisms of natural resistence to the diseases here reported. Additional studies of the immunologic responses in these rodents may provide valuable information that could be used to improve the development of therapeutic targets for humans and domestic animals.

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PROECHIMYS RODENTS AND NEUROSCIENCE Several approaches indicate that the variability in genome size in eukaryotes is consistently achieved through a quantitative variability in copy numbers of repetitive DNA sequences, usually organized in heterochromatic domains. Studies in mammals show that differences in heterochromatin contents between closely related species, or even individuals of the same species, may account for several phenotypic effects, clearly bringing heterochromatin into the field of functional genomics (Viegas et al., 2002). Proechimys raised interest for its remarkable genome size, which is one of the highest recorded so far in mammals and harbors several repetitive DNA families (Garagna et al.,1997). Up to now, the Proechimys´s brain has been minimally studied and even neglected. However, recent investigations shed light to the potential use of Proechimys in the field of neuroscience. The hippocampus of this neotropical rodent was investigated for the first time only in 2001 (Fabene et al., 2001). The hippocampal formation is thought to play a role in memory, spatial navigation and control of attention. In this scenario, the most notable among human patients has been H.M., who suffered from intractable epilepsy and underwent experimental surgery involving bilateral removal of the medial temporal lobe, including large parts of both hippocampi. The procedure left H.M. with an inability to form new episodic memories (anterograde amnesia), coupled to a substantial loss of old memories (retrograde amnesia) (Scoville & Milner, 1957; Neves et al., 2008). In the framework of comparative studies on animal models of experimental epilepsy, the susceptibility of Proechimys to epileptogenic treatments was tested, and, surprisingly, the findings indicated a striking resistance of these

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animals to several different paradigms of experimental epilepsy (Fabene et al., 2001; Carvalho et al., 2003; Arida et al., 2005). In this line of evidence, Proechimys was designated as an animal model of resistance to epilepsy. Thus, Proechimys rodents may have natural endogenous anti-epileptogenic mechanisms and future studies to expand our knowledge about the subject are required. Recent body of evidence suggests that changes in the distribution and activity of some endocannabinoid compounds are described in different pathological conditions, suggesting the possible involvement of the endocannabinoid system in neurodegenerative diseases (Ludányi et al., 2008). In epilepsy, for example, the endocannabinoid system is considered by some authors as an endogenous mechanism implicated in seizure termination and in the epileptogenic process as well (Wallace et al., 2003; Falenski et al., 2007). In this context, the activation of CB1 receptors seems to protect hippocampal cells, preventing cytoskeletal damage and loss of synapses from the excitotoxicity mediated by the increase of glutamatergic activity (Gilbert et al., 2007; Karanian et al., 2007). Experiments of our laboratory encountered higher hippocampal expression and different distribution of CB1 receptors in Proechimys rodents when compared to Wistar rats (Araujo et al., 2010). This data could, to some extent, contribute to the resistance of Proechimys to epileptogenic treatments. It is also worth noting that Proechimys presents large limbic structures (Fig. 3) and, in addition, the hippocampal commissural system was found to be highly developed in these rodents (Fabene et al., 2001; Scorza et al., 2010). In this sense, the relative sizes of the hippocampal commissures and corpus callosum suggest that a crosstalk between limbic structures could play a crucial role in the inter-hemispheric communication of the Proechimys´s brain (Fabene et al., 2001). Furthermore, we described a remarkably different Proechimy’s cytoarchitecture organization of the hippocampal cornu Ammonis 2 (CA2) subfield (Scorza et al., 2010). A very distinctive Proechimy´s CA2 sector exhibiting disorganized cell presentation of the pyramidal layer and atypical dispersion of the pyramidallike cells to the stratum oriens has been identified, strongly contrasting to the densely packed CA2 cells in the Wistar rats (Fig. 4). Hence, the distinctive features of CA2 neurons may play a unique role in hippocampal circuitry and opens up a new set of possibilities to explore the contribution of CA2 neurons in normal and pathological brain circuits. In addition, the high level of calcium buffer proteins found in these rodents could be a distinct calcium signaling toolkit in order to exactly adjust their spatiotemporal aspects of calcium signaling to their physiological function. Another striking finding in Proechimys rodents was the presence of large pyramidal-like neurons throughout the stratum oriens layer from hippocampal CA2 to CA1 area (Scorza et al., 2011). This newly identified population of pyramidal-shaped neurons exhibited distinct electrophysiological and morphological properties. At this point, we asked whether such dissimilarities could reflect evolutionary or adaptive advantages of an animal that lives in the Amazon rainforest (Scorza et al., 2010). We can brainstorm and dream about the functional roles and why these cells are arranged in such peculiar cytoarchitecture. Has the hippocampus of these rodents evolved and changed in response to their wild and complex habitat? Or even, structures and functions of the Proechimys´s brain are adaptations to this rodent´s physical and social environment? Anyhow, these findings provide new direction for the potential use of Proechimys in the field of neuroscience. A great deal of the knowledge that has improved our understanding of the brain mechanisms has derived from appropriate animal models and, certainly, Proechimys represents an important tool of investigation. In this context, the

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challenge that basic science research needs to meet is to make use of a comparative approach to benefit the most from what each animal model can tell us. Progress in understanding and treating brain pathologies will require translational research efforts. Translation research means the transformation of knowledge through successive fields of research from basic science discovery to public health impact. The authors would like to thank FAPESP, CNPq, CAPES and The National Institute for Translational Neuroscience – INCT, for supporting this work.

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Figure 3. Nissl-stained coronal sections illustrating larger hippocampal formation of Proechimys (left) versus commonly used laboratory rat - Wistar (right).

Figure 4. Photomicrographs of NeuN-stained coronal sections showing CA2 section. A1-A3 Proechimys, B1-B3 Wistar (white laboratory rat). A1, B1 Hippocampal formation (20x). Proechimys shows a very distinctive neuronal distribution in the CA2 subfield of the hippocampal formation (A2A3), strongly contrasting to the densely packed CA2 cells and unclear boundaries seen in the Wistar rats (B2-B3). A2, B2: 100x; A3, B3: 200x.

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Weisbecker, V., Schmid, S. (2007). Autopodial skeletal diversity in hystricognath rodents:Functional and phylogenetic aspects. Mamm. Biol. ;72:27–44. Weksler, M., Bonvicino, C.R., Otazu, I.B., Junior, J.S.S. (2001). Status of Proechimys roberti and P. oris (Rodentia:Echimyidae) from Eastern Amazonia and Central Brasil. Journal of Mammalogy ;82(1):109-122. Wilson, A.C., Cann, R.L., Carr, S.M., George, M., Gyllensten, U.B., Helm-Bychowski, K.M., Higuchi, R.G., Palumbi, S.R., Prager, E.M., Sage, R.D., Stoneking, M. (1985). Mitochondrial DNA and Two perspectives on evolutionary genetics. Biological Journal of the Linnean Society ;26:375-400. Woods, C.A. & Kilpatrick, C.W. (2005). Infraorder Hystricognathi. In: Wilson, D.E. & Reeder, D.M.D. (eds), Mammal Species of the World. The Johns Hopkins University Press, Baltimore, MD, USA. 1538-1599.

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In: Rodents Editors: Alfeo Triunveri and Desi Scalise

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Chapter 5

NICHE OVERLAP AND RESOURCE PARTITIONING AMONG THREE URBAN RODENT SPECIES Eduardo de Masi1 and Francisco Alberto Pino2 1

Municipal Health Department, Municipal Government of Sao Paulo, Sao Paulo, Brazil 2 Institute of Agricultural Economics, Sao Paulo, Brazil

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ABSTRACT There are very few studies showing sympatric coexistence among roof rat (Rattus rattus), Norway rat (Rattus norvegicus) and house mouse (Mus musculus) in urban environment. This chapter deals with overlapping in space use and interspecific competition among those three rodent species in the urban area of Sao Paulo city, Brazil. It is based on a rodent survey carried out in 2006: 16,467 premises were inspected and infestation rates were annotated by rodent species and infested place (dwelling internal or external area). The niche complementarity hypothesis was tested by polytomous logistic regression modelling. The results indicate extensive spatial segregation among the three species, with coexistence limited by the occupation of different places inside the dwelling. R. rattus infests internal and external area equally, R. norvegicus infests mainly external area, and M. musculus infests mainly internal area. The niche complementarity hypothesis was confirmed, since some niche axes overlap and others were characteristically associated to a single species. In conclusion, there is strong competition among the three urban rodent species, and thus the control of one species may be favorable to high infestation of another one. The importance of the results for public health polices and for urban rodent ecology understanding is pointed out. As a matter of fact, public health and pest control policies must emphasize integrated rodent control techniques in order to decrease the ecological support capacity of urban environment for rodents. Keywords: Urban rodent, niche overlapping, resource partitioning, rodent ecology, urban ecology.

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INTRODUCTION Commensal rodents are relevant to both public and animal health, as the reservoirs for several diseases. From the economic point of view, they cause damage to agricultural stored products, especially grains [Meehan 1984]. It also causes extinction of wild animals and plants in off-shore islands by competition, predation or diseases transmission [Gillies & Pierce 1999; Donlan et al. 2003; Robertson & Gemmell 2004, Abdelkrim et al. 2005]. Other environmental impacts associated with rodent infestation are due to chemical control: soil and water contamination by rodenticides active ingredients [Papini et al. 2008], and rodenticide resistance [Endepols 2002; Pelz et al. 2005]. Rodent infestation has been monitored in some countries, e.g., in England by the English House Condition Survey [DEFRA 2005], in Baltimore, USA, [Easterbrook et al. 2007], in Salzburg, Austria [Traweger et al. 2006], in Luang Prabang, Laos [Promkerd et al. 2008], in Buenos Aires, Argentina, [Cavia et al. 2009] and in Sao Paulo, Brazil. In the latter city, where leptospirosis is endemic and affects nearly 200 people per year (incidence coefficient of 1.8 cases/100,000 inhabitants), nearly 80% in urban area, the Rodent Infestation Survey is performed by the municipality government since 2005 [Santos et al. 2006]. The results found in these surveys are used for planning educative policy and preventive strategy. Almost all the studies cited above registered the sympatric coexistence between Norway rat (Rattus norvegicus) and house mouse (Mus musculus), but there are few studies showing sympatric coexistence among roof rat (Rattus rattus) and the other two species. The 2006 edition of Sao Paulo Rodent Infestation Survey found 23.1% of the premises infested by urban rodents, and the main species were the roof rat in 12.7% of the premises, the Norway rat in 9.4% and the house mouse in only 1.7%, showing to have sympatric coexistence of these three species in the city. It is also shown that socio-economical conditions, such as income and educational level, are determinant of rodent infestation in a given urban area and that once the area is infested, the premises infestation depends on environmental factors, as access, harborage and food sources; it is also shown that different species have different intensity responses for each factor studied [Masi et al. 2010]. In the latter paper the ecological relationship among the three rodent species was not studied, but they will be considered in the current chapter. According to the ecological theory, similar species tend to have similar resource needs, consequently overlapping their niches [Ricklefs 2003; Odum 2004]. If species have a low niche overlap, competition is expected not to play an important role, and they could coexist in the same environment, depending on the respective resource needs. On the other hand, if the species have high niche overlaps, the superior competitor tend to exclude the inferior competitor [Schoner 1974; Amarasekare 2003]. In urban rodent community it is assumed that Norway rat is a superior competitor related to roof rat and house mouse, and that the latter is an inferior competitor related to the second one. In this context, Norway rat should displace the other species and roof rat should displace house mouse from occupied patches, landscape or premise, due to the larger size and aggressiveness [Brooks 1973; Mehan 1984]. In other environments the relationship among species may be different: in New Zealand offshore island the roof rat is a superior competitor related to Norway rat and the distribution of the latter is heavily mediated by the distribution of the former [Russel & Clout 2004]. Moreover, in wild rodent communities, the coexistence seems to occur along complementary niche

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dimensions, allowing the partitioning of resources and spatial segregation among species [Castro-Arellano & Lacher Jr. 2009]. The niche complementarity means a high overlap in one niche dimension that should be compensated by a low overlap in at least one of the other dimensions [Schoener 1974]. From this point of view, the niche is an interval in each ecological dimension which is dynamic in character and depends on the current environment [Yimin et al. 2006]. According to this logic, the three primary mechanisms that facilitate coexistence involve interspecific subdivision of food, space and time, as well as resource partitioning involves differential utilization of these components by different species [Schoener 1974]. In this manner, the hypothesis of niche complementarity and resource partitioning was investigated in this chapter, because preliminary evidences suggest that these are the mechanisms controlling the relationship in urban rodent community [Masi 2009; Masi et al. 2010; Cavia et al. 2009]. Deeper urban ecological studies of rodents are necessary, in order to understanding their interspecific interaction, as well as their interaction with human beings, especially with the architectural urban concepts. Such knowledge may lead to more effective pest control strategies. The aim of this paper was threefold: firstly, to define the elective premises microhabitat use for each rodent species; secondly, to understand the resource partition and interspecific interaction among urban rodent; and finally, to assess niche overlapping in space use, food, and interspecific competition dimensions. This information will be used by municipal public administration for understanding the likelihood of competition and to make recommendations for future environmental management, for rodent control and for leptospirosis prevention.

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METHODS Study Area Fieldwork was carried out in the whole city of Sao Paulo. This city is inhabited by 10.4 million people living in 1,509 km2, and comprises more than 3 million dwellings dispersed in 31 boroughs. Almost 100% of the dwellings are reached by treated water, 70% by sewage collection and disposal system, and 99% by regular collection of solid residues [Brazilian Institute of Geography and Statistics 2000]. The climate is high-altitude tropical, with two well defined weather seasons, a hot and rainy from October to March (spring and summer) and a cold and relatively dry from April to September (autumn and winter). The city is located on the Atlantic Plateau of Sao Paulo State, 720-850 meters high. The average annual temperature is 19.3°C (15.5°C in winter and 27°C in summer), and the average annual precipitation is 1455 mm, with relative humidity 74%-80% [Tarifa & Armani 2000].

Data Collection Data on rodent infestation and environmental variables were obtained during the Urban Rodent Infestation Survey of premises carried out in July 2006 by the Sao Paulo city hall,

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Eduardo de Masi and Francisco Alberto Pino

according to a model proposed for such problems [Davis et al. 1977]. A probabilistic two stage cluster sample design was used [Kish 1965]: primary sampling units were census tracts, stratified by city boroughs, and randomly selected; secondary sampling units were blocks, randomly selected within each selected census tract. All the premises, including domestic dwellings, commercial premises and unused plots of land, were visited and as many as possible were also inspected. Nevertheless, some premises were disregarded from the analysis in this paper: refusals and non authorized inspections after three attempts, unused plots of land, and some cases in which the rodent species or the local of infestation was not annotated. Qualified and trained personnel searched for traces or vestiges of rodents, like faeces, rub marks, burrow, rat runs and trails, in order to characterize the premise infestation and to identify the infesting species. Data were also collected on architectural urban aspects, microhabitat use, food and harbourage resources. All the variables were categorized as binary (or dichotomous), assuming the values 1 for its presence and 0 for its absence in the premise.

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Data Analysis The niche was qualified in four dimensions: microhabitat use (rodent preference for internal or external premise area), the access sources (by building structure imperfections and by the sewage system), the harbourage source (waste material/rubbish, building material, discarded objects, ceiling cracks, wall cracks, dense bush) and food sources (animal food, available human food, exposed garbage, fruit trees). The microhabitat use was characterized by the area where rodent signs were found. Internal area included living-rooms, kitchens, bathrooms, ceilings, basements and others (the bedrooms were inspected only by request of the dweller) and external area included any garden, back yard, laundry and other external buildings [Masi 2009]. The study design was a cross-section, and no temporal, seasonal or diel cycle variable was considered. The individual niches and resource partitioning were indirectly measured by logistic regression models. For each rodent species a polytomous nominal response variable was considered, and four possible responses were defined as: non infestation, strictly external infestation, strictly internal infestation, both internal and external infestation. A generalized logit model, also known as discrete choice model or multinomial model, was used to investigate the niche width. The niche was estimated by association of each niche axis with the rodent infestation rate [SAS 2007]. The results are better visualized if graphically presented in natural logarithms to avoid too large or too small values. Two socioeconomic variables were introduced in the models as confounding variables in this context: first, the Human Development Index (HDI), which includes information on life expectancy, literacy, educational attainment and gross domestic product per capita, ranges between 0.00 and 1.00, with higher values being associated with better life conditions; second, income up to 2 minimum wages, defined as 1=more than 50% of the private dwellings in the census tract have the head of the family earning up to 2 minimum wages monthly, and 0=otherwise. The presence of infestation by other rodent species was also taken into account in the models. Parameters were estimated by LOGISTIC procedure of Statistical Analysis Software (SAS®), version 9.1 for Windows.

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RESULTS The analysis was based on data from 16,467 premises, of which 3,263 (19.8%) were infested by rodent (Table 1). The main species was R. rattus occurring in 62.3% of the infested premises, followed by R. norvegicus, in 53.2%, and M. musculus, in 8.1% (Table 2). In some cases, the premises were infested by more than one species at the same time. In 2,054 (62.9%) premises strictly external infestation was found, in 577 (17.7%) strictly internal infestation, and in 632 (19.4%) both, internal and external infestation (Tables 1 and 3). Table 1. Internal and external premise commensal rodent infestation by species, Sao Paulo city, Brazil, 2006 External infestation R. rattus

Internal infestation

Number of premises 891

Percentage infested 27.31

801

24.55

R. rattus

355

10.88

R. rattus

201

6.16

R. norvegicus R. rattus R. norvegicus

267

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R. rattus R. norvegicus

R. norvegicus

R. rattus

R. rattus

232

8.18 0.00 7.11 0.00

R. norvegicus

120

3.68

R. norvegicus

R. norvegicus

98

3.00

R. norvegicus

R. norvegicus

R. rattus

R. rattus

M. musculus

R. rattus M. musculus R. rattus R. rattus

R. rattus

M. musculus

M. musculus

M. musculus

33 47

35 25

R. rattus M. musculus R. norvegicus

R. norvegicus

M. musculus

M. musculus

0.00 0.00

40

M. musculus

R. rattus

37

M. musculus R. norvegicus

R. norvegicus

1.13

15 22 13

1.01 0.00 1.44 1.23 0.00 1.07 0.00 0.77 0.46 0.00 0.67 0.00 0.40 0.00

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Eduardo de Masi and Francisco Alberto Pino Table 1. (Continued) M. musculus

0.00

R. norvegicus

17

M. musculus R. norvegicus M. musculus R. norvegicus R. rattus M. musculus M. musculus

M. musculus Sum

0.52 0.00 0.12 0.00 0.09

4

3 7 3,263

0.00 0.00 0.21 100.00

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Table 2. Premise commensal rodent infestation by species, Sao Paulo city, Brazil, 2006 Specific infestation

Number of infested premises

Percentage infested

Only R. rattus

1357

41.6

Only R. norvegicus

1109

34.0

Only M. musculus

79

2.4

R. rattus and R. norvegicus

532

16.3

R. rattus and M. musculus

90

2.8

R. norvegicus and M. musculus

43

1.3

R. rattus and R. norvegicus and M. musmusculus

53

1.6

Sum

3.263

100.0

R. rattus

2032

62.3

R. norvegicus

1737

53.2

M. musmuculus

265

8.1

General infestation

In the general infestation, 78.0% of the premises were infested by only one rodent species (Table 3). The presence of only one species occurred in 83.6% of the premises with strictly external area infested, in 90.5% when strictly internal area was infested, and in 48.2% when both, internal and external areas were infested. The main species occurring alone in the infested premises was R. rattus (44.3%), followed by R. norvegicus (31.2%) and M. musculus (2.4%). In simultaneous infestation, 16.3% of the premises were infested by R. rattus and R. norvegicus at the same time (Table 3): both species infested external area (8.2%), internal and external area (7.1%), and internal area (1.0%); additionally, in 1.6% of the infested premises, this two species occurred together with M. musculus (Table 1). According to the location, strictly external infestation by R.

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Table 3. Dwelling commensal rodent infestation by infested area and species number, Sao Paulo city, Brazil, 2006 Infested area

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Strictly external infestation By only one species By two species By three species Strictly internal infestation By only one species By two species By three species Internal and External infestation By only one species By two species By three species General infestation Only one species With two species Three species

Number of premises 2,054 1,717 324 13 577 522 52 3 632 306 289 37 3,263 2,545 665 53

Percentage infested 62.9 52.6 9.9 0.4 17.7 16.0 1.6 0.1 19.4 9.4 8.9 1.1 100 78.0 20.4 1.6

Percentage by response 100.0 83.6 15.8 0.6 100.0 90.5 9.0 0.5 100.0 48.4 45.7 5.8 100.o 78.0 20.4 1.6

rattus (27.3%) was followed by strictly external infestation by R. norvegicus (24.5%) and strictly internal infestation by R. rattus (10.9%) (Table 1). The results from logistic models are tabularly detailed (Tables 4 to 6), but they are better understood when graphically presented (Figures 1 to 3). Each axis correspond to a particular niche dimension and its value represent the natural log of the respective premises infestation odds ratio, given the niche dimension, i.e., the presence or the absence of a certain resource or another species. In harbourage dimension, harbourage in ceiling cracks seem to be particularity important (high odds ratio) for R. rattus infestation, especially for internal infestation, while harbourage in dense bush showed to be important for external infestation by R. norvegicus, and harbourage in waste and in building material were important for external and internal infestation by M musculus, respectively. Respecting to access dimension, in any location, the existence of access by building structure was important as a niche axis for R. rattus infestation, and access by the sewage system for R. norvegicus. Concerning to food dimension, the fruit trees were important for external infestation by R. norvegicus and R .rattus. Human food was the more important axis for internal infestation by M. musculus. In summa, R. rattus infestation was strongly associated to building structure imperfections in any location, R. norvegicus infestation to urban conservation, especially sewage system, and to external area characteristics, and M. musculus infestation to premises hygiene maintenance, mainly food packaging, and internal area characteristics.

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Eduardo de Masi and Francisco Alberto Pino

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Figure 1. Niches axes for premises commensal rodent infestation in internal area, Sao Paulo city, Brazil, 2006.

Figure 2. Niches axes for premises commensal rodent infestation in external area, Sao Paulo city, Brazil, 2006. Rodents: Habitat, Pathology and Environmental Impact : Habitat, Pathology and Environmental Impact, edited by Alfeo Triunveri, and Desi Scalise,

Niche Overlap and Resource Partitioning among Three Urban Rodent Species

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Figure 3. Niches axes for premises commensal rodent infestation in internal and external area, Sao Paulo city, Brazil, 2006.

Figure 4. Niches axes for premises commensal rodent infestation, Sao Paulo city, Brazil, 2006.

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Table 4. Internal and external Rattus rattus infestation by risk factor, Sao Paulo, Brazil, 2006 Interna

Externa

Int_ext

Effect in log

Norway rat

Norway rat

Norway rat

Access by the sewage system

1.3468

1.8420

2.1384

Internal infestation by R.rattus External infestation by R.norvegicus

1.7878 0.0000

0.0000 0.0000

3.7994 0.0000

Accessible garbage

-0.2446

0.4028

0.3315

Available animal food

-0.1532

0.2593

0.4240

Intern a Roof rat 1.5233 0.0000 0.0000 0.4780 0.3307

Available human food

0.0000

0.0000

0.0000

0.3702

Available fruit trees

-0.2705

0.7448

0.6238

Harbourage in building material

0.3082

0.1756

0.2554

Harbourage in waste material

0.2476

0.0705

0.4929

Harbourage in dense bush Harbourage in wall cracks Harbourage in ceiling cracks Access by the building structure

-0.1199 0.4048 0.0000 0.7966

0.8286 0.5318 0.0000 -0.2169

0.3832 0.7178 0.0000 -0.3682

0.5852 0.2345 0.1233 0.0000 0.3485 1.7520 1.3345

Extern a Roof rat 0.6694 0.0000 0.9944

Int_ex t Roof rat 0.9163 0.0000 2.1729

0.0159

Interna

Externa

Int_ext

House mouse

House mouse

House mouse

0.0000

0.0000

0.0000

2.1778 0.0000

0.0000 0.8368

3.9366 1.6096

0.1579

-0.5092

0.1017

-0.1054

0.5510 0.4354

0.4259

0.0935

0.2469

0.8548

0.1026

1.6106

0.2964

0.4581

0.5289

0.4095

0.0000

0.0000

0.0000

0.0344

0.1914

0.8742

0.7328

0.7580

0.5140

0.4154

-0.0233

1.3712

0.2608

0.0000 0.3981 1.1066 1.2247

0.0000 0.5032 1.6639 1.0619

0.0000 0.1196 -1.6296 0.4101

0.0000 0.0760 0.4637 -0.4732

0.0000 0.1458 -0.5852 -0.2510

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Niche Overlap and Resource Partitioning among Three Urban Rodent Species Effect

Response variable level

Odds ratio (OR)

HDI

Internal

2 minimum wages  wages

Available fruit trees No Yes

Harbourage in wall cracks No Yes

Premises features Strictly residential

Internal External Internal and external

Internal External Internal and external