Ladybirds (Vol. 10) (Naturalists' Handbooks, Vol. 10) [2 ed.] 1907807071, 9781907807077

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Naturalists’ Handbooks 10

Ladybirds H E LE N E . ROY P E T E R M .J . BROW N R IC H A R D F. COMON T R E M Y L . P OL A N D JOH N J . SL O G GE T T Revised from Majerus and Kearns 1989

With illustrations by Sophie Allington and Chris Shields

Pelagic Publishing www.pelagicpublishing.com

Published by Pelagic Publishing www.pelagicpublishing.com PO Box 725, Exeter, EX1 9QU

Ladybirds (2nd Edition) Naturalists’ Handbooks 10 Series editors S. A. Corbet and R. H. L. Disney ISBN 978-1-907807-07-7 (paperback) ISBN 978-1-907807-37-4 (eBook) Text © Pelagic Publishing 2013 Key illustrations © Sophie Allington 1989 Other illustrations © Sophie Allington 1989 and © Chris Shields 2012 All rights reserved. Apart from short excerpts for use in research or for reviews, no part of this document may be printed or reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, now known or hereafter invented or otherwise without prior permission from the publisher.

British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library.

Contents

Editors’ preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . iv Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .v 1

 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1

2

 Life history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .5

3

 Ladybirds in their environment . . . . . . . . . . . . . . . . . . . . .15

4

 Ladybirds and their natural enemies . . . . . . . . . . . . . . . . .30

5

 Variation in ladybirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .42

6

 Population and evolutionary biology. . . . . . . . . . . . . . . . .56

7

 Ladybird distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .74

8

 Identification of British ladybirds . . . . . . . . . . . . . . . . . . .85 I: Field key to adult British ladybirds . . . . . . . . . . . . . . . . . . . 85 II: Key to all the adult British Coccinellidae . . . . . . . . . . . . . . 94 III: Field key to the larvae of British ladybirds . . . . . . . . . . . . 106

9

 Study techniques and materials . . . . . . . . . . . . . . . . . . . .115 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .132 Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .138

Editors’ preface The fi rst edition of this book appeared in 1989, and since then there have been great changes in the world of ladybirds. Our friend and colleague Mike Majerus, who died suddenly in 2009, was the senior author of the first edition, and did much to stimulate interest in the group through his books, through the Cambridge Ladybird Survey and in his teaching. The enthusiasm that he inspired lives on, and we are delighted that such a strong team of his co-workers has agreed to produce this second edition. New discoveries and changes in the British ladybird fauna have made this a major undertaking. When the first edition was prepared male killers had not been recognised, the bryony and harlequin ladybirds were not yet established in Britain, and some important topics had hardly been explored. This book incorporates the newly-arrived species into the keys, and includes much other new material, notably on the evolutionary relationships of ladybirds, the role of chemical cues in searching behaviour, the distributional response to environmental change, and the impact of the recentlyintroduced harlequin ladybird. We are also fortunate to have splendid new illustrations by Chris Shields to supplement the excellent artwork that Sophie Allington prepared for the first edition. Thanks to the work of numerous research workers and amateur recorders throughout the country, the subject of ladybird natural history has made important advances since the book first appeared. This substantially revised edition will make the new developments accessible to a wider audience, and perhaps encourage readers to undertake further research on these engaging insects. SAC RHLD

Acknowledgements First and foremost we would like to express our deepest thanks to Mike Majerus and Peter Kearns. The fi rst edition of this book has been an inspiration to so many people and it has been a privilege and a pleasure to build on their tremendous work. Many others have played a part in the production of this book and we are grateful to them all. We would like to thank Dr Sally Corbet for her diligent editing and encouragement throughout. We have also been extremely pleased to have supportive comments from Dr Henry Disney. Both Sally and Henry have inspired us throughout our careers and we have enjoyed the opportunity of working with them on this book. There are many entomologists who have contributed to our understanding of ladybirds in Britain and we are grateful to them all. We would particularly like to thank the people involved in promoting biological recording of ladybirds in Britain over the years, both the volunteers who have led the Coccinellidae Recording Scheme in its various guises and staff from the Biological Records Centre (within the NERC Centre for Ecology & Hydrology). We are extremely grateful to Andrew Duff, Mark Telfer, Darren Mann and Amoret Spooner for kindly providing comments on the revised keys. Charlotte Coombes scanned the original text and her help was greatly appreciated. We thank our families (David, Katy and Ella Roy, Clare Walker, Cameron and Jodie Brown, John, Sue, David and Jenny Comont, Guy Poland, Ilja Zeilstra) for their patience and interest in our passion for these amazing beetles. Finally, we must thank all the people who have enthusiastically sent us their observations and records of ladybirds. One recorder Robert (Bob) Frost is worthy of special mention. His contribution to ladybird recording is represented by both the outstanding number of ladybird observations that he provided to the UK Ladybird Survey and also the happy memories that we have of working with him. He will be greatly missed. Helen Roy, Peter Brown, Richard Comont, Remy Poland and John Sloggett

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About Pelagic Publishing We publish scientific books to the highest editorial standards in all life science disciplines, with a particular focus on ecology, conservation and environment. Pelagic Publishing produces books that set new benchmarks, share advances in research methods and encourage and inform wildlife investigation for all. If you are interested in publishing with Pelagic please contact [email protected] with a synopsis of your book, a brief history of your previous written work and a statement describing the impact you would like your book to have on readers.

1 Introduction Biological science must stand on its foundations in basic observations of organisms in the field: what they do, when they do it, why they do it, and how they have come to do it. Majerus, 1994

1.1 Introduction Ladybirds are among the most attractive and popular of British insects. Many species are common. They may be found in almost any habitat from sea coast to mountain top, and from city wastelands to windswept heathlands. Almost every garden will have at least one species and many will have five or more species. There are a number of reasons for the popularity of ladybirds. Firstly, ladybirds are charismatic insects. Many ladybirds have bright contrasting colour patterns, although not all are red with black spots. Some are black with red spots, others are yellow and black, or brown with cream spots. Some have stripes instead of spots and some no spots at all. Secondly, most species of ladybird are carnivorous. Both adults and larvae feed on aphids or other pest insects, which suck sap and damage many crops and garden plants. So, ladybirds are important predators of these pests and are considered ‘beneficial insects’. Finally, ladybirds are connected with good fortune in many myths and legends. The name ‘ladybird’ is itself derived from the commonest species in Britain, the 7-spot ladybird, Coccinella septempunctata. The lady in question is Our Lady, the Virgin Mary. The red colour is said to represent her cloak, which in early paintings and sculptures was usually depicted as being red, and the seven black spots represent the seven joys and seven sorrows of Mary. Yet, despite their popularity and important function as predators of pest insects, much is still unknown about the behaviour and ecology of British ladybirds. This book aims to outline what is known about the species found in Britain, and to highlight areas worthy of scientific exploration. We hope that the book will encourage you to discover more for yourselves, particularly through your own natural history studies and scientific research. Ladybirds offer great scope for original observations and experiments, and their potential as biological control agents of plant pests makes new contributions

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Ladybirds

* References cited under the authors’ names in the text appear in full in the reference list.

Ladybirds

a

b True bugs

c d

Fig. 1. The differences between ladybirds and true bugs (Hemiptera). Ladybirds (a) The wing cases (elytra) meet on the centre line and do not overlap, and are hard. (b) Head with biting mouthparts and with palps. True bugs (c) The forewings overlap, and are partly or completely membranous. (d) Head with mouthparts modified into a pointed structure for piercing and sucking. The rostrum usually points backwards. Lacks palps.

Fig. 2. The membranous hind wing of a 7-spot ladybird.

to our knowledge of ladybirds even more worthwhile. Additionally although a few species of ladybird are increasing in number, there are some historically widespread and common species that are currently declining dramatically (Roy and others, 2011; Roy and others, 2012)* and so increased understanding of their ecology and response to our rapidly changing environment is critical.

1.2 What are ladybirds? Ladybirds are beetles and so belong to the largest order of organisms, the Coleoptera. There are two important characteristics that, taken together, distinguish ladybirds and most beetles from insects of other orders. (i) The forewings are modified to form hard or leathery elytra (wing cases) that meet in the centre line, covering the abdomen. (ii) The mouthparts are adapted for biting rather than sucking. Beetles generally and ladybirds in particular are unlikely to be confused with any other order except the Hemiptera (true bugs). The characters that distinguish ladybirds from bugs are shown in fig. 1. Ladybirds are one family of beetles called the Coccinellidae. Coccinellids are small or medium-sized beetles, 1–10mm long; they are usually round or oval. The most obvious features of the upperside of a resting ladybird are the elytra, which in many species are brightly coloured and usually patterned with spots, bands or stripes. The elytra cover and protect the membranous flight wings (fig. 2) which are usually folded under the elytra when the ladybird is not flying. Between the elytra and the head is the pronotum. This is a plate which covers the upper surface of the thorax. It is broader than it is long and it extends forwards at the margins (fig. 3). The pronotum is often patterned, though not as brightly as the elytra. The head is retractable under the pronotum and the antennae are short and slightly clubbed. The legs are short and retract into grooves under the body. The feet (tarsi) have four segments, but because the third segment is small and hidden inside the deeply lobed second segment, only three segments are readily visible (fig. 4). More than 4,500 species of coccinellid have been described worldwide. Forty-seven species are resident (established and reproducing) in Britain, and 27 of these also reside in Ireland. Various other species have been recorded on a few occasions in Britain, but they are not

Introduction Fig. 3. The position of the pronotum between the head and elytra (eyed ladybird, Anatis ocellata). head pronotum elytron

Fig. 4. The lower part of a leg of a ladybird showing the tibia, the four tarsal segments (note the small third segment almost hidden within the second segment) and the tarsal claw.

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generally considered resident here (see chapter 7). Some of the British coccinellids (sub-family Coccidulinae) are small and unspotted, and would not normally be recognised as ladybirds. Whilst all 47 coccinellid species are listed in Table 1 and included in the key, this book primarily covers the 26 species that have received most research attention and were designated as conspicuous species in the first edition of this book. tibia

Table 1. Classification of coccinellids occurring in Britain and Ireland (According to Duff, 2008; Roy and others, 2011, but also refer to Plate 1 for proposed revised phylogeny)

Family: Coccinellidae English name

Plate number

Sub-family

Latin name

Coccidulinae Mulsant, 1846

*Coccidula rufa (Herbst, 1783)

11.2

Coccidula scutellata (Herbst, 1783)

11.3

Rhyzobius chrysomeloides (Herbst, 1792) *Rhyzobius litura (Fabricius, 1787)

11.1

Rhyzobius lophanthae (Blaisdell, 1892) Clitostethus arcuatus (Rossi, 1794) Stethorus punctillum (Weise, 1891) *Scymnus suturalis Thunberg, 1795 *Scymnus auritus Thunberg, 1795

11.6

Scymnus frontalis (Fabricius, 1787)

11.5

Scymnus haemorrhoidalis Herbst, 1797 Scymnus femoralis (Gyllenhal, 1827) *Scymnus schmidti Fürsch, 1958 *Scymnus nigrinus Kugelann, 1794 *Scymnus limbatus Stephens, 1832 Scymnus interruptus (Goeze, 1777) *Nephus redtenbacheri (Mulsant, 1846) Nephus quadrimaculatus (Herbst, 1783) #Nephus bisignatus (Boheman, 1850) Chilocorinae Mulsant, 1846

*Hyperaspis pseudopustulata Mulsant, 1853

11.4

Platynaspis luteorubra (Goeze, 1777)

11.7

*Chilocorus bipustulatus (Linnaeus, 1758)

Heather ladybird

Chilocorus renipustulatus (Scriba, 1791)

Kidney-spot ladybird

6.11 6.10

Exochomus quadripustulatus (Linnaeus, 1758)

Pine ladybird

6.12

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Ladybirds

Table 1. Continued.

English name

Plate number

Sub-family

Latin name

Coccinellinae Latreille, 1807

*Anisosticta novemdecimpunctata (Linnaeus, 1758) Water ladybird

6.4

Tytthaspis sedecimpunctata (Linnaeus, 1761)

16-spot ladybird

6.5

*Myzia oblongoguttata (Linnaeus, 1758)

Striped ladybird

4.7

*Myrrha octodecimguttata (Linnaeus, 1758)

18-spot ladybird

*Propylea quattuordecimpunctata (Linnaeus, 1758) 14-spot ladybird

Epilachninae Mulsant, 1846

5.2 6.1–6.2

*Calvia quattuordecimguttata (Linnaeus, 1758)

Cream-spot ladybird

5.1

*Halyzia sedecimguttata (Linnaeus, 1758)

Orange ladybird

6.6

*Psyllobora vigintiduopunctata (Linnaeus, 1758)

22-spot ladybird

*Anatis ocellata (Linnaeus, 1758)

Eyed ladybird

6.3

*Aphidecta obliterata (Linnaeus, 1758)

Larch ladybird

6.9

*Hippodamia tredecimpunctata (Linnaeus, 1758)

13-spot ladybird

5.3

4.4–4.5

Hippodamia variegata (Goeze, 1777)

Adonis’ ladybird

*Coccinella hieroglyphica Linnaeus, 1758

Hieroglyphic ladybird

5.9

Coccinella magnifica Redtenbacher, 1843

Scarce 7-spot ladybird

4.2

Coccinella quinquepunctata Linnaeus, 1758

5-spot ladybird

4.3

*Coccinella septempunctata Linnaeus, 1758

7-spot ladybird

4.1

*Coccinella undecimpunctata Linnaeus, 1758

11-spot ladybird

5.6

*Adalia bipunctata (Linnaeus, 1758)

2-spot ladybird

5.7–5.8

*Adalia decempunctata (Linnaeus, 1758)

10-spot ladybird

5.10–5.12

*Harmonia axyridis (Pallas, 1773)

Harlequin ladybird

3.1–3.4

Harmonia quadripunctata (Pontoppidan, 1763)

Cream-streaked ladybird

4.8–4.9

6.7–6.8

Henosepilachna argus (Geoffroy in Fourcroy, 1762) Bryony ladybird

4.6

*Subcoccinella vigintiquattuorpunctata (Linnaeus, 24-spot ladybird 1758)

5.4–5.5

* indicates the species is found in Ireland, as well as in Britain # thought to be extinct in Britain

Henosepilachna (= Epilachna); Hippodamia variegata (= Adonia variegata); Tytthaspis (= Micraspis); Myzia (= Neomysia); Psyllobora (= Thea); Coccinella magnifica (= C. distincta). A comprehensive checklist of Coleoptera (including synonyms) was published by Duff in 2008. The checklist can be accessed through the Coleoptera website (www.coleoptera.org.uk) hosted by the Biological Records Centre.

Scientific names: In the entomological literature the numbers in the scientific names may be given in full (for example Subcoccinella vigintiquattuorpunctata), or may be simplified (for example Subcoccinella 24-punctata). Throughout this book we will refer to the ladybirds using the English name (where appropriate) but table 1 can be used as a cross-reference to the Latin name.

2 Life history 2.1 General life cycle Like all beetles, ladybirds pass through three stages egg, larva and pupa - before reaching the adult state. So, like butterflies and moths (Lepidoptera), bees, wasps Janua ry Fe br

r be m

ry ua

No ve

ber cem De

st

April

eber ptm Se

Octob er

ch Mar

M

ay

Au gu e Jun

July

Fig. 5. General life cycle scheme of a ladybird (based on the 7-spot ladybird).

and ants (Hymenoptera) and true flies (Diptera), they are said to be holometabolous insects (undergoing complete metamorphosis). For many ladybird species in Britain the full life cycle takes a year. Eggs are laid in spring or early summer. The larvae feed up over the next month or so, and the new generation of adults emerge from the pupae in mid to late summer. These adults feed but do not usually breed until the following spring, and so most species have just one generation a year (fig. 5). However, there are exceptions to this pattern. The rate at which larvae develop is affected by both temperature and food availability, and the development of eggs and pupae is also affected by the temperature. In some years, a number of species such as the 2-spot and 14-spot ladybirds have a second generation. Harlequin ladybirds in Britain generally have

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Ladybirds

Fig. 6. 7-spot ladybird laying a batch of eggs.

two generations, and sometimes a partial third generation, each year. For species completing more than one generation a year, individuals from both the early and late generations overwinter together. There are records of the 2-spot, 14-spot, cream-spot and eyed ladybirds surviving through a second winter. However, more information is needed if we are to be sure how common these exceptions to the normal pattern are, particularly in response to climate change.

2.2 Eggs The eggs of most ladybird species are elongate and oval, and vary from a light yellow to a deep orange colour. They are laid on the leaves, stems and sometimes the bark of plants, often in the vicinity of prey. Most species fix their eggs at one end so they are found in an upright position (fig. 6), though the eggs of the pine ladybird are frequently laid on their sides. There is considerable variation in the number of eggs laid at one time, though most species lay batches of eggs, which are tightly packed together forming a cluster on the substrate. Females of the 2-spot ladybird typically lay between 20 and 50 eggs at a time. There is also substantial variation within a species in the number of eggs laid per female (fecundity). One of the more important influences is the type of food eaten by the adults. Hariri (1966) found that the 2-spot ladybird laid a lifetime total of 738 eggs per female, averaging 9.3 per day when fed on the black bean aphid (Aphis fabae), but when the pea aphid (Acyrthosiphon pisum) was used, the total was 1535 eggs, laid at an average of 20.4 per day. Fecundity is also affected by the quantity of food eaten, so, for example, there is a positive correlation between food consumption and egg production in the 11-spot ladybird (Ibrahim, 1955a, b). Influences on larval development also affect subsequent female fecundity. Sundby (1966) fed 7-spot ladybird larvae one third the normal amount of food and found the emerging adults were small and laid fewer eggs. It is also known that mating behaviour affects the number of eggs laid in the 2-spot ladybird; Sem’yanov (1970) showed that females increased their rate of egg laying after each mating. Ladybird eggs generally take about four days to hatch, though there can be considerable variation depending on ambient temperature. Table 2 shows that increasing

Life history

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7

ambient temperature reduces the length of time spent in the egg stage by the 7-spot ladybird, so that at 15°C it is 10.3 days, while at 35°C it is 1.8 days. However, there is an upper threshold temperature, above which the eggs will fail to hatch. Fig. 7. Newly-hatched larvae of the 7-spot ladybird on their eggshells.

Table 2. Development time (days) of the early stages of the 7-spot ladybird at different temperatures (data from Hodek, 1973).

Temperature (°C)

Egg

Larva

Pupa

15

10.3

35.5

15.0

20

5.0

18.6

8.4

25.6

2.6

8.7

4.0

30

1.9

6.7

2.9

35

1.8

5.4

2.5

2.3 Larvae Fig. 8. Young, first-instar larva of the 2-spot ladybird, ‘piggybacking’ on a pea aphid.

instar: the stage between two moults. A newlyhatched ladybird larva which has not yet moulted is in the first instar

Like all beetles, ladybirds have larvae lacking wingbuds (pl. 7 and 12). When the eggs hatch, the young larvae usually remain on or near their egg shells for about a day (fig. 7). They eat their egg shells and very often eat any later-hatching eggs, or any infertile eggs that have failed to hatch. After leaving their shells, the first-instar larvae must find food, which they do by actively hunting for prey. Mortality of newly-hatched larvae is high because capturing the first aphid is difficult for a first-instar larva, which is often smaller than many of the aphids it is trying to eat. The consumption of other eggs in the clutch (sibling egg cannibalism) provides vital nutrition to the cannibalistic larva and increases the chances of it surviving the first instar (Roy and others, 2007). Evidence suggests that larvae discover prey by physical contact rather than scent or sight although this undoubtedly needs further investigation (see 3.2). The way the food is taken depends largely on the relative sizes of prey and predator. A tiny first-instar larva can be found perched on the backs of relatively large aphids as if riding ‘piggy-back’ (fig. 8). Its jaws are embedded into the aphid and it feeds by sucking the body fluid of the aphid. Indeed all larval stages of the small and inconspicuous ladybird Platynaspis luteorubra suck the body fluid of aphids using the leg of the aphid as a straw to facilitate feeding. However, as the larvae of most species grow and become larger relative to their prey, they begin to eat solid parts such as the legs and antennae of the

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Ladybirds

Fig. 9. Larva of the 10-spot ladybird shedding its skin to become a final-instar larva.

Fig. 10. Pre-pupa of the eyed ladybird.

Pupa in normal resting position

Pupa in raised position

Fig. 11. Pupal alarm behaviour of the creamstreaked ladybird.

prey as well as the body fluid. Most larvae regurgitate fluid from the gut into the chewed aphid, allowing some pre-digestion before the aphid body fluid is sucked in. A larva sheds its skin, or moults, three times before pupating, so there are four larval instars. The old skin splits on the upperside at the front and the larva frees itself over a period of about an hour. The new skin is initially pale and soft (fig. 9) but quickly darkens and hardens. The length of time spent as a larva depends to a large extent on environmental conditions. Prey density is important; the more prey is available, the faster the larvae can feed and grow. Very low prey density can lead to starvation. Banks (1957) calculated that the larvae of the 14-spot ladybird die unless they find food within 1–1.5 days after hatching. If prey levels are low, but above starvation levels, then development is slower than normal. Above a certain prey density, development rate is not increased but the resulting adults are larger. Prey type also influences development and reproduction of ladybirds and this is discussed in detail in chapter 3. Temperature also affects development rate. In general, development is faster at higher temperatures but this relationship is not straightforward, as is obvious from table 2. As the temperature approaches the upper tolerance level, further increases produce only small increases in development rate. So, an increase from 15°C to 20°C reduces the larval phase of the 7-spot ladybird by 16.9 days; but a similar increase from 30°C to 35°C reduces it by only 1.3 days (table 2). Still higher temperatures will retard development, or even cause death.

2.4 Pupae The fourth-instar larva stops feeding at least 24 hours before pupation. It becomes immobile as the tip of the abdomen is attached to the substrate, usually a leaf, stem or bark. It also adopts a characteristic hunched position (fig. 10). This stage is called the pre-pupa. There are two main types of ladybird pupae. In the first, the final larval skin of the pre-pupa is shed right back to the point of attachment to the substrate, so that the pupa is naked. Most ladybird species have this type of pupa (pl. 12.1 and 12.2). The second type is found in ladybirds of the genera Exochomus (pine ladybird) and Chilocorus (kidney-spot and heather ladybirds), in which the skin splits lengthwise but is not shed (pl. 12.3). The duration of the pupal phase varies with the ambient

Life history

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9

temperature. Table 2 shows that in the 7-spot ladybird this stage lasts 15 days at 15°C but only 2.5 days at 35°C. Although pupae are generally thought of as inactive, they are not completely immobile. If they are irritated there is an alarm response in which the fore region of the pupa is rapidly raised and lowered several times (fig. 11). This is probably a mechanism for dislodging parasites and startling predators. There appears to be considerable variation among pupae in the strength of this alarm response, and it is almost absent in some pupae. There is also variation in the strength of the response throughout the life of a single pupa, though a pupa can show the response almost immediately after pupation, and until a few hours before the adult emerges. Pupal colouration is variable in some species. At least some of this variation is due to environmental conditions. Pupae of the 7-spot ladybird are light orange at high temperatures and much darker at low temperatures.

2.5 Adults

Fig. 12. Adult 2-spot ladybird emerging from the pupa and sitting on the empty pupal case.

The adult ladybird emerges by splitting the front end of the pupal case. It takes several minutes to pull itself out, and then generally rests on the empty case to expand and dry the elytra and wings (fig. 12). At this stage the elytra and wings are very soft and contain very little pigment. The colour of the elytra is usually light yellow or orange in most species, although ladybirds with predominantly black elytra (such as the pine, kidney-spot and heather ladybirds) have red elytra on eclosion from the pupa. The basic adult pattern and colouration may take several hours or even days to develop, and more subtle changes take place over a longer period (pl. 8). This is most obvious in species such as the 2-spot and 7-spot ladybirds that have a red background colour, which gradually deepens over the weeks and months. One consequence is that newly-emerged adults are readily distinguishable from those that have overwintered, which are a much deeper shade of red. There are two main groups of pigments in ladybirds. The dark colours are the result of melanins, and the lighter orange, red and yellow pigments are derived from carotenes. Most adults emerge in mid to late summer. They feed, perhaps for several weeks, before dispersing to their overwintering sites. In many species mating takes place in the spring. Ladybirds are most active in sunshine and mating pairs are a common sight in suitable habitats on

10 | Ladybirds

Fig. 13. A pair of eyed ladybirds mating.

Fig. 14. Female 2-spot ladybird rejecting a male’s advances by lifting her abdomen. abdomen: the hindmost of the three main body divisions of an insect

warm, sunny spring days. In contrast to some insect species there is often no obvious courtship ritual. In many cases a male simply approaches a female and places his front legs on her elytra. If she accepts him he positions his genitalia and mating takes place (fig. 13). More elaborate behaviour occurs when a female rejects a male. The female may simply run or fly away. But if a male has a strong grip on the female she may raise her abdomen (fig. 14), or kick him with her hindlegs. If this does not deter the male, then the female rolls over to dislodge him (fig. 15), or in extreme cases she climbs up a plant stem and drops to the ground or attempts flight. A female may reject a male’s advances if she is too young to mate, has recently mated, is about to lay eggs, or has a specific mating preference for a different type of male (see 6.4). It is generally considered to be difficult to distinguish between male and female ladybirds. In most species the females are slightly larger than the males, and there may be small differences in shape, but these criteria are not totally reliable. Careful examination of the underside of the abdomen of 23 British species of ladybirds has

♂

♀

2-spot ladybird

eyed ladybird

14-spot ladybird

pine ladybird

Fig. 15. Female 2-spot ladybird attempting to prevent a male from mating with her by rolling onto her side.

Fig. 16. Underside of abdominal segments showing the differences between the sexes of ladybirds. Males are shown on the left of each pair.

Life history

cuticle: non-cellular outer layer secreted by the epidermis. In insects it is firm enough to act as a skeleton and is composed of chitin and protein

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11

revealed sexual differences in every case. These are best seen with a low-power dissecting microscope. Surprisingly, there is no single set of criteria that is applicable to all species, as each has its own distinctive features. These involve the size, shape and number of cuticular plates at the end of the underside of the abdomen. In some species the abdomen is pointed in the female, in others in the male, and in still others in both, or neither. The cuticular plates may be notched in the male, or undulating in the female. The only feature found in all males, and absent in all females we have examined, is three curved bands of thin flexible cuticle at the back margins of the abdominal segments. These are, for example, yellow in the eyed ladybird and glossy black in the 2-spot ladybird. They enable the abdomen of the male to be flexed at right angles during mating and hence provide a very useful diagnostic sexual feature. Figure 16 shows a representative selection of the sex differences in a variety of species.

2.6 Environmental change and life history of ladybirds The importance of the relationship between ladybirds and temperature is widely recognized. Coccinellids usually survive seasonally unfavourable conditions, lack of food or adverse climatic factors in the adult stage. If climatic conditions are favourable when food becomes scarce, ladybirds generally disperse to seek food elsewhere. Conversely, under unfavourable climatic conditions, ladybirds become inactive, some species entering diapause, while other species simply become dormant or quiescent. The difference between these states is important in the context of potential climatic change. It is predicted that there will be an increase in global mean surface temperature of between 2 and 6.4°C above pre-industrial levels by 2100 (Millennium Ecosystem Assessment, 2005). Additionally it is anticipated that there will be an increase in the incidence of floods and droughts and a rise in sea level (Millennium Ecosystem Assessment, 2005). There is growing concern that such changes to the climate will increase the loss of biodiversity and the risk of extinction for many species (Parmesan and Yohe, 2003). There are a number of factors that will exacerbate the situation for some species, such as low population sizes, limited range of accepted food, high degree of habitat or host plant specificity and limited tolerance of wide climatic ranges. Changes in climate over

12 | Ladybirds quiescence: a response to sudden, unpredictable periods of unfavourable weather; the ladybirds simply become inactive but resume activity as soon as conditions become favourable again dormancy: a response to unfavourable conditions that are seasonally predictable. Ladybirds become inactive, generally for a fixed period, surviving on fat reserves, but they are capable of becoming active to feed for short periods within the unfavourable period if conditions permit diapause: a response to predictably unfavourable seasons following a preparatory period in which ladybirds build up their fat reserves and either do not mature their gonads, or reabsorb their eggs. Ladybirds in diapause do not become active in brief favourable periods, and cannot reproduce until diapause is terminated

the last few decades, particularly warmer temperatures, have already begun to impact on species distributions, population sizes, the timing of reproduction and migration events in Britain. In some species, a diapause before reproduction is obligatory (Dobzhansky, 1922), but for many species, diapause is a highly variable response initiated by one or more environmental factors. The factors that induce dormancy or diapause vary among species of ladybird; the nature and availability of food, day length, temperature, humidity and the physiological state of host plants are all involved in some species (reviewed in Hodek and others, 2012). The likelihood that an individual ladybird survives through a dormant period is dependent on a number of factors, but the level of reserves that it has accumulated prior to dormancy is particularly important (Barron and Wilson, 1998). Fat, glycogen and water reserves all diminish during dormancy, rates of reduction being affected by changes in ambient temperature, and in the case of water loss, by humidity. Fluctuating temperatures, or abnormally high temperatures, during overwintering cause reserves to be used up faster than they are at constant low temperatures (Majerus, 1994). Consequently, increases in winter temperature or in fluctuations in winter temperatures due to climate change could increase rates of winter mortality in diapausing species. The relationships between ladybirds and climatic factors are complex and vary with life stage. Although it may be expected that ladybirds will be negatively affected by climate change, evidence is sparse (Roy and Majerus, 2010). However, there are some early indications that climate change is influencing the life histories of ladybirds in Britain. Distribution data collated from 1980 to 2005 suggest that the times of movement of 7-spot ladybirds from overwintering sites, first records of mating and first hatching in spring have all shifted 11 to 18 days earlier over the 25 year period (Majerus, unpublished data). There is no indication as to whether these changes have had an effect on the population trends of this species but such rapid changes do have the potential to temporally decouple predators from peak numbers of their preferred prey. There are several potential consequences of such a decoupling, for example, aphid populations may suffer reduced predation by ladybirds, ladybirds may consume alternative prey (including other beneficial insects) and

Life history

specialists: species that thrive on only a narrow range of foods or in a narrow range of habitats or require specific environmental conditions* generalists: species that can develop and reproduce on a wide range of foods or in many habitats or across a wide range of environmental conditions* *The terms specialist and generalist are necessarily vague because they refer to a continuum rather than a dichotomy

|

13

cannibalism may increase. All of these have the potential to reduce ladybird numbers but all require further study to provide a clear picture of these very complex interactions. It is possible to make some testable predictions on which to base further research. For example, some generalist species of ladybird could be buffered against some of the detrimental effects of climatic change. If decoupled (isolated in time) from their primary food source, generalist feeders are more likely to find alternative foods than are specialist feeders. Polymorphic species (those with a variety of colour forms) may also be less affected. For example, the 2-spot ladybird is a highly variable species (chapter 5) and its colour forms can be broadly classified into melanic (black with red spots) and non-melanic (red with black spots). The frequency with which these colour morphs occur varies geographically (Brakefield, 1984b). De Jong and Brakefield (1998) reported a decrease in melanic forms from 1978 to 1998 and this change coincided with an increase in local ambient spring temperatures. Melanic forms may have an advantage at low temperatures because they warm up earlier in the day than non-melanic forms; this advantage is reduced with an increase in spring temperature. Some species are habitat and prey generalists when near the centre of their geographic distributions, but close to the edge of their range they behave as specialists; here they may only be able to survive through adaptation to some specific type of habitat. 5-spot ladybirds are widespread generalists in continental Europe, but in Britain are confined to unstable river shingles in Wales and the Spey Valley in Scotland. Climate warming could result in 5-spot ladybirds becoming more widespread in Britain. Similarly, 13-spot ladybirds are relatively common in continental Europe, but are only sporadically reported in Britain, on the south and east coasts, arriving from continental Europe and establishing small colonies that soon become extinct (Majerus, 1994). An increase in temperature and humidity might be favourable for the long-term establishment of 13-spot ladybirds in England in the near future. In the summer of 2011 a 13-spot ladybird larva was found in Devon; an encouraging indication that this species might have recolonised the country. Further surveys are required to elucidate the current status of the 13-spot ladybird in Britain. Orange ladybirds have increased in abundance in Britain over

14 | Ladybirds

recent years. This mildew-feeding species was once considered to feed primarily on mildews on sycamore, but has recently been found more widely on deciduous trees (Roy and others, 2011). Warmer, wetter springs in Britain may have increased the prevalence of mildew and consequently the distribution of orange ladybirds. There will undoubtedly be winners and losers as a consequence of climate change, but the exact nature of the outcomes is hard to predict because of the complexity of interactions and the lack of available data. Climatic factors are likely to influence the interactions between ladybirds and their prey, predators and parasites (see chapter 4). For example, the prevalence of a sexually-transmitted fungus (Hesperomyces virescens) infecting 2-spot ladybirds is associated with urbanisation and has been linked with increased temperatures within the urban environment (Welch and others, 2001). A second sexually-transmitted parasite of 2-spot ladybirds may also be affected by climate change. The ectoparasitic mite Coccipolipus hippodamiae infects 2-spot ladybirds over much of continental Europe, but is absent from Britain (Webberley and others, 2006). Transmission of this mite requires the ladybirds to have overlapping generations, which is the case in most of continental Europe but has not been so in Britain (Hurst and others, 1995). From surveys over the last 28 years, it appears that 2-spot ladybirds are now commonly achieving two generations per year in southern England (Majerus, unpublished data) and so rising temperatures are likely to increase the long-term survival of this mite in British populations of 2-spot ladybirds. Natural enemies of ladybirds are discussed in detail in chapter 4. Studies of the effects of current climate changes on ladybirds at a global scale are lacking, but historic evidence suggests that ladybirds move rather than adapt. Large-scale geographic range alterations are illustrated by the ladybird Ceratomegilla ulkei which was recorded from an organic silt from the River Thames around 40,000 years ago (Briggs and others, 1985), is now absent from Europe, but still occurs at high latitudes or high altitudes in north-western Canada and north-eastern Asia. It appears that ladybirds maintain environmental constancy rather than geographic constancy. There is no doubt that our understanding of the effects of climate change on ladybirds is limited by lack of data, and research on this theme would be extremely worthwhile.

3 Ladybirds in their environment 3.1 Habitat and dietary preferences Ladybirds can be found all over Britain in almost any terrestrial habitat. Some species are found in a wide range of habitats, as long as suitable food is available. Others are much more specific. For generalists, such as the 2-spot, 7-spot and harlequin ladybirds, a wide variety of different aphids seem to be suitable food for growth, development and reproduction. So these ladybirds and their immature stages may be found on a wide range of plants. The specialist species tend to be found on one or a small group of host plants. At least some of these species may require food of a specific type for successful reproduction (essential food). For example, the early stages of the striped ladybird are found exclusively on conifers. When adults of this species are given species of aphids not found on conifers, such as pea aphids, black bean aphids, or nettle aphids (Microlophium carnosum), they readily feed on them, but will not lay eggs. The essential food of the hieroglyphic ladybird is the larva of the heather leaf beetle (Chrysomelidae). Other specialist species, such as the eyed, water and 18-spot ladybirds, are predominantly found on a small range of host plants in the wild, but in captivity they breed successfully when fed aphids not found on these host plants. There is some evidence that these ladybirds may be restricted by microclimatic factors, thus limiting the prey species encountered in the wild. For example, one of the most habitat specific species is the water ladybird, which is almost exclusively confined to wetland areas where reedmace (Typha latifolia) and reed (Phragmites australis) are its host plants. Some species, although not confined to specific host plants, seem to have habitat preferences. The 11-spot ladybird is most often found in coastal areas, although it may be found inland. Adonis’ ladybird seems to prefer dryish, warm habitats, and is commonly found on sandy soils and disturbed habitats such as brownfield sites. Both the 10-spot and cream-spot ladybirds are, in broad terms, generalists, but they will most often be seen in deciduous woodland or along hedgerows. The scarce

16 | Ladybirds Table 3. Habitat preferences of the British ladybirds

Species

Preferred habitats

Coccidula rufa

Wetland, on reeds, rushes and reedmace. Occasionally in grassland.

Coccidula scutellata

Wetland, on reeds, rushes and reedmace.

Rhyzobius chrysomeloides

Pines, particularly in heathland.

Rhyzobius litura

Grassland and low growing vegetation. Often on nettles.

Rhyzobius lophanthae

Trees and shrubs, mainly in gardens.

Clitostethus arcuatus

Deciduous and coniferous woodland, especially ivy on ash.

Stethorus punctillum

Deciduous and coniferous woodland, orchards and hedgerows.

Scymnus suturalis

Coniferous woodland, particularly on Scots pine.

Scymnus auritus

Oaks, particularly in woodland.

Scymnus frontalis

Low growing vegetation, usually in dry habitats such as heathland and dunes.

Scymnus haemorrhoidalis

Low growing vegetation and shrubs, usually in damp areas.

Scymnus femoralis

Low growing vegetation, on chalk or sandy soils.

Scymnus schmidti

Low growing vegetation, usually in dry areas.

Scymnus nigrinus

Coniferous woodland, particularly on Scots pine.

Scymnus limbatus

Deciduous trees, particularly on willows, sallows and poplars in marshy habitats.

Scymnus interruptus

Deciduous trees and low growing vegetation.

Nephus redtenbacheri

Grassland, heathland and dunes.

Nephus quadrimaculatus

Deciduous and coniferous woodland and gardens, usually on ivy.

Nephus bisignatus

Woodland.

Hyperaspis pseudopustulata

Diverse, but often coastal or wet habitats. Often found in moss on or below trees.

Platynaspis luteorubra

Low growing vegetation, grassland. Lives in association with ants such as Lasius niger.

Heather ladybird

Heathland and conifer scrub.

Kidney-spot ladybird

Deciduous woodland, mainly on ash, sallow, poplar and birch.

Pine ladybird

Diverse, including deciduous and coniferous woodland.

Water ladybird

Wetland, on reeds and reedmace. Occasionally in grassland.

16-spot ladybird

Grassland.

Striped ladybird

Coniferous woodland, particularly on mature Scots pine.

18-spot ladybird

Coniferous woodland, particularly on mature Scots pine.

14-spot ladybird

Diverse, but usually on low herbage.

Cream-spot ladybird

Deciduous trees, particularly in woodland.

Orange ladybird

Deciduous or coniferous woodland, particularly on sycamore but also on oak, ash, lime and hawthorn.

22-spot ladybird

Grassland.

Eyed ladybird

Coniferous woodland, particularly on Scots pine.

Larch ladybird

Coniferous woodland.

Ladybirds in their environment | 17 Table 3. Continued

Species

Preferred habitats

13-spot ladybird

Lowland marshland.

Adonis’ ladybird

Diverse, but favours dry, sandy soils.

Hieroglyphic ladybird

Heathland.

Scarce 7-spot ladybird

Heathland and woodland near to the nests of wood ants.

5-spot ladybird

Unstable river shingle.

7-spot ladybird

Diverse, but usually on low herbage.

11-spot ladybird

Diverse, but mainly in coastal areas.

2-spot ladybird

Diverse, including deciduous woodland, scrub and grassland.

10-spot ladybird

Deciduous and coniferous woodland, hedgerows.

Harlequin ladybird

Diverse, including gardens, deciduous and coniferous woodland, scrub and low herbage.

Cream-streaked ladybird

Coniferous woodland, particularly on Scots pine.

Bryony ladybird

Hedgerow and scrub where white bryony is present.

24-spot ladybird

Grassland.

7-spot ladybird is found in a range of habitats, but almost invariably close to nests of the wood ant, Formica rufa (see 4.1). Table 3 gives a list of the preferred habitats of all British ladybirds. In some cases the data on which the table is based are limited, and further research and observations are needed. Some of the habitat preferences are very strong; the water, hieroglyphic and kidney-spot ladybirds will rarely be found far from their host plants. However, it must be remembered that as ladybirds can fly, all species will, at least occasionally, be found away from their expected habitats or normal host plants. This is particularly true of the conifer specialists if aphids become scarce. All of the conifer species, except the larch and 18-spot ladybirds, will readily leave their normal host trees to hunt for food on deciduous trees or lower vegetation. Some, such as the eyed ladybird, will even occasionally breed on other trees such as oak, maple, lime and sycamore. The larch ladybird, which is commonly found on larch, Douglas fir, Norway spruce (Christmas tree) and Scots pine, and the 18-spot ladybird, which breeds almost exclusively on mature Scots pine, do not seem to follow this habit. Rather they either search for other conifers where aphids are more plentiful, or stay put until aphid numbers have increased.

18 | Ladybirds

Although the generalists may be found on a range of plants, even these have some preferences. The 2-spot ladybird is only rarely found on conifers, while the 14-spot and 7-spot ladybird are often found on conifers. Indeed, in conifer habitats the 7-spot ladybird is often the most abundant ladybird. This is particularly true later in the year, when ladybirds disperse away from their breeding habitats and can be found in more unusual areas. Some of the generalists show a rather regular cycle in their movements from one host plant to another through the year. These cycles vary from one area to another and may be disrupted in some years if the aphids on one of the host plants are unusually scarce. Table 4 shows the most common host plants for the 2-spot ladybird in Cambridge for the years 1981–1986. The basic order of the cycle is fairly constant, but occasionally a regularly used plant does not support a sufficient aphid population for it to be used. This was true for fat hen (Chenopodium species) in 1981. On other occasions the order may be changed, so willows (Salix species) were used after nettles (Urtica dioica) in 1986. One or two non-regular host plants are also sometimes important, such as birch in 1984.

3.2 Ladybirds as predators Ladybirds are considered to be beneficial insects because most species are predatory, feeding on aphids or other pest insects. Both adults and larvae feed on the same Table 4. Cycle of host plants on which 2-spot ladybirds were commonly found in the Fen Causeway area of Cambridge, 1981–1986

1981

1982

1983

1984

1985

1986

April

-

-

HSL

-

-

-

May

LW

LWN

SL

LWB

LW

-

June

LWN

LWN

PN

LBN

LN

SLNG

July

NG

N

N

N

N

NG

August

NT

TF

NTF

NF

TN

NGC

September

T

TF

TF

FO

TF

CWTF

L - lime (Tilia) W - willow (Salix) N - nettles (Urtica dioica) G - long grasses T - thistle (Cirsium) F - fat hen (Chenopodium) H - hawthorn (Crataegus) S - sycamore (Acer pseudoplatanus P - fruit trees (Prunus) B - birch (Betula) O - oak (Quercus) C - chamomile (Matricaria and Tripleurospermum)

Ladybirds in their environment | 19

food. Female ladybirds assist their progeny in finding food by laying eggs in the vicinity of aphid colonies, or on or under coccid (scale insects) prey (Dixon, 2000). Indeed, female 2-spot ladybirds assess aphid colonies and only lay eggs if the aphids are at a sufficiently high density to support the larvae, but not so high that a population crash is imminent. Furthermore, females avoid laying eggs in patches where they detect tracks left by individuals of the same species (conspecifics) (Ruzicka, 1997), which contain an oviposition-deterring pheromone (Fréchette and others, 2004). It was previously thought that ladybirds appear to detect their prey only at a short range using mainly visual cues (Nakamuta, 1984) but there is increasing evidence to suggest that long range chemical cues are important (Sloggett and others, 2011). Indeed, ladybird searching behaviour is far from random. Hungry ladybirds tend to walk upwards because they are both attracted to light and negatively geotactic (that is, they walk against the pull of gravity). Aphids are often located on the growing tips of plants, which are the most nutritious parts, and so by heading upwards ladybirds are more likely to encounter aphids. Similarly, both adults and larvae tend to walk along prominent leaf veins, and it is alongside leaf veins that many aphids feed. It is thought that harlequin and 7-spot ladybirds are att racted to chemical cues produced by plants that have been damaged by aphid feeding, but not to chemicals produced by the aphids themselves (Obata, 1986; Ninkovic and others, 2001). The chemical ecology of ladybirds is an area that is advancing rapidly and there will undoubtedly be some exciting finds in coming years. The searching behaviour of ladybirds also changes once a prey item has been found and consumed, for they then begin ’area restricted searching’ or ‘intensive searching’. This involves an increase in the turning rates, and a slower rate of movement, so that a small area is intensively searched. Both adults and larvae often move their head from side to side (‘head flagging’) and this increases the area scanned for prey. This type of behaviour is obviously advantageous when searching for colonial prey, where many prey individuals may be found close together. If the ladybird does not fi nd another prey item within a few minutes, the turning rate decreases, speed of movement gradually increases, the rate of head flagging decreases and the ladybird re-starts ‘extensive searching’.

20 | Ladybirds

siphunculi: tubular appendages on the final abdominal segment

When a ladybird adult or larva encounters an aphid it may or may not manage to capture and eat it. Although aphids may appear to be completely helpless, they do possess a range of defence and escape mechanisms. If a ladybird approaches an aphid from the front, the aphid may simply move so that the ladybird misses it. If the ladybird seizes the aphid, the aphid may kick or attempt to pull itself free. Aphids may also back away from the attacker, or drop off the plant. The likelihood of kicking, pulling, backing off or dropping seems to vary from one species of aphid to another, but relatively little is known about the way different species of aphid defend themselves when confronted by ladybird adults or larvae, and further studies in this area are needed (Evans, 1976a,b; Rotheray, 1989; Roy and others, 1999). In at least one case the size of aphid seems to affect the probability of a successful attack. Older larvae of the 2-spot ladybird were successful in capturing 90–100% and 60–70% of first-instar and adult peach-potato aphids (Myzus persicae) respectively, but only 0–50% of the much larger pea aphid (Klingauf, 1967). Aphids have other defence mechanisms. If a ladybird seizes an aphid, the aphid may exude, from the tip of the siphunculi, a droplet of an oily liquid which it will dab onto the ladybird. This behaviour, which is called waxing, may induce the ladybird to release the aphid in order to clean. In some species of aphid, the liquid exuded from the siphunculi contains an ‘alarm’ pheromone. This induces other aphids in the colony to withdraw their mouthparts and walk away or drop off the plant. Some aphids, such as the beech aphid (Phyllaphis fagi), are covered in wax. This may inconvenience predators by making individual prey selection difficult. However, the full effect of this material on predators has not been studied. Another aphid defence is to be poisonous to ladybirds and other enemies. Larvae of the 10-spot ladybird will attack and eat both the black bean aphid and the vetch aphid (Megoura viciae), but after a minute or two they will reject the prey and regurgitate their gut contents (Dixon, 1958). Despite this rejection and regurgitation, some larvae die as a result of this ’tasting’, even when fed afterwards with suitable non-toxic food. The vetch aphid has also been shown to be poisonous to both larval and adult 2-spot ladybirds. When offered a mixture of toxic vetch aphids and non-toxic pea aphids, neither larvae

Ladybirds in their environment | 21

nor adults could differentiate between the two, and any that consumed vetch aphids died soon afterwards (Blackman, 1965, 1967). Some species of ladybird appear to have evolved tolerance to the poisons contained in some aphids. For example, the 7-spot ladybird can feed and breed on a diet of vetch aphids. The oleander aphid (Aphis nerii) is poisonous to 2-spot, 7-spot and 14-spot ladybirds, but is readily accepted by Adonis’ ladybirds, which develop normally on this prey (Iperti, 1966). A more complex problem for aphid predators is that aphid occurrence can be very unpredictable. Overall aphid occurrence throughout the year is quite predictable, with peak numbers occurring in spring and early summer, but aphid occurrence can be patchy over time and across localities. Most species of aphid change their host plants periodically. Their migration off a particular host is often induced by deterioration in the quality of the foodplant, and aphid migrations can leave ladybird larvae stranded without food midway through their development. There is variation in the rate of development of ladybirds on different species of acceptable aphid. The 2-spot ladybird, for example, has been shown to develop faster, experience lower mortality, and reach a higher adult weight when fed on the pea aphid than it did on the black bean aphid (Blackman, 1967). However, the 7-spot ladybird does equally well on both prey species. Not all predatory ladybirds feed on aphids, although most will do so if their more favoured diet is not available. The larch ladybird prefers to feed on adelgids, a group of sap-sucking insects closely related to aphids, although it will feed on aphids, such as the pea aphid and the black bean aphid, and will breed at a low rate on these prey. In the wild, the kidney-spot and heather ladybirds both feed mainly on scale insects (coccids), although adelgids and small aphids are also eaten. In captivity, both species of ladybird will breed on a diet of nettle or pea aphids, although fecundity is low.

3.3 Ladybirds as herbivores and mildew feeders Five species of ladybird resident in Britain are rarely, if ever, carnivorous. The 24-spot ladybird feeds on leaves of a range of herbaceous plants (campions, vetches, trefoils,

22 | Ladybirds incisor

molar projection

Fig. 17. Mandible of the 2-spot ladybird, a carnivorous (predatory) species which feeds on aphids.

Fig. 18. Mandible of the 24-spot ladybird, a herbivorous (plant-feeding) species.

small blunt teeth

Fig. 19. Mandible of the 16-spot ladybird, a mycophagous (mildewfeeding) species.

incisor subdivided into a row of smaller teeth

chickweed, grasses and plantains); the bryony ladybird feeds on white bryony; and the 16-spot, 22-spot and orange ladybirds all feed on powdery mildews (moulds of the family Erysiphaceae). The mouthparts of these species differ from those of predatory species (fig. 17). The mandibles of the 24-spot ladybird are specialized for scraping away layers of plant tissue (fig. 18). The incisor region comprises four or five blunt teeth, which carry a number of accessory teeth of various sizes. The distinct molar projection of carnivorous species is replaced by a row of coarse teeth. The mandibles of the mildew-feeding species are of two types, reflecting the supposed taxonomic affinities of the three species involved. The 16-spot ladybird, which is related to the aphid-eating Coccinellini, has similar mandibles to these species, but with the inner part of the mandible covered with small blunt teeth (fig. 19) for feeding on mildew and also pollen (Ricci, 1986). In both the 22-spot and the orange ladybirds, the tip of the mandible has two teeth, the lower one subdividing into a row of smaller teeth (fig. 20). As with the aphid-feeding species, the mildew feeders display some host-plant specialisation. The 16-spot ladybird feeds on a wide range of species of powdery mildews, while the 22-spot ladybird seems to favour mildews growing on the leaves of umbellifers such as hogweed (Heracleum sphondylium) or wild angelica (Angelica sylvestris). The orange ladybird is a woodland species and feeds principally on mildews growing on the leaves of deciduous trees, particularly sycamore, although it will feed on honeydew and occasionally on small aphids, particularly in the spring and early summer before mildews have developed substantially on the young leaves of deciduous trees. Over the last decade the orange ladybird has been found increasingly on hawthorn and a few other deciduous trees in addition to sycamore. Feeding tests using a variety of mildew species still need to be done with all of these species, to assess their diet breadths.

3.4 Ladybirds as intraguild predators Fig. 20. Mandible of the orange ladybird, a mycophagous (mildewfeeding) species.

Although ladybirds often have a preference for a particular typical food (aphids, coccids, mildew or leaves), they also eat other types of food. For example in addition to mildew, the orange ladybird will occasionally eat aphids, and many aphid-eating ladybirds will sometimes eat the

Ladybirds in their environment | 23

Fig. 21. 7-spot ladybird larvae.

conspecific: belonging to the same species guild: a group of organisms with similar requirements, such as food intraguild predation: predation between predators that generally share a common prey, for example aphids

eggs or larvae of other beetles or butterflies and moths. In some cases this food serves to keep the ladybird alive during times of scarcity of their typical food. However, in many cases it appears that such food is a part of the ladybird diet even when their characteristic food is abundant. This habit has been extensively studied in the aphid-eating species. For example, Triltsch (1999) dissected out the guts of 7-spot ladybirds collected in Germany and examined the food remains inside them. He found that in addition to aphids, 7-spot ladybirds consumed the larvae of flies and beetles (including ladybirds), smaller insects such as thrips, fungal spores and pollen. Aphid populations rarely persist for very long and so aphid-eating ladybirds face periods of starvation. This can affect their larvae if aphid populations decline while they are still developing. One solution to this problem is cannibalism (eating individuals of your own species). This is particularly common amongst immature stages. Indeed larvae will invariably feed on conspecific egg clutches, which are highly nutritious and cannot defend themselves or escape, even when aphids are abundant. Another solution is to eat other aphid predators. This is referred to as intraguild predation. Ladybirds eat other ladybird species; they can also eat lacewing or hoverfly larvae, or other aphid predators. The reverse can also occur. For example, lacewing larvae are known to occasionally eat ladybird larvae. Intraguild predation by ladybirds certainly occurs when ladybirds are starving, but the extent to which it occurs in many species is unclear. For example, because ladybirds are chemically defended, including against each other, they risk being poisoned when they eat other ladybird species, so it is thought they only do this as a last resort (see 6.3). An interesting exception is the harlequin ladybird. This species appears to be well adapted to eating other aphid predators, including ladybirds, and they apparently form a regular part of its diet (Pell and others, 2008; Thomas and others, 2012). The arrival of this invasive species in America and Europe, including Britain, has been associated with declines in native ladybirds (Roy and others, 2012), possibly as a consequence of harlequin intraguild predation (Brown and others, 2011). We still need to find out a lot more about intraguild predation in ladybirds. Further observations in nature would be of great value, especially if they are related to observations of aphid or predator abundance. Similarly,

24 | Ladybirds

it would be of interest to know whether there are any circumstances in which intraguild predation occurs in non-aphid eating ladybirds.

3.5 Alternative foods Food that supports both maturation of the ovaries and complete larval development is described as ‘essential food’. Even if they are fairly specific with respect to their essential food, many predatory species of ladybird readily accept a diverse array of alternative foods which are ‘accepted but inadequate’ – foods on which egg laying and larval development are prevented or reduced. Predatory ladybirds will often eat a wide range of other insects if their normal food is scarce. Ladybirds will also eat pollen and nectar from flowers when insect food is scarce. This allows the ladybirds to survive, at least for short periods, and can be important in spring, when ladybirds emerge from overwintering. Once their normal insect prey becomes available again, ladybirds will resume normal egg laying. It may be important for ladybirds to maintain relatively high water content, and when food is scarce, ladybirds have often been observed drinking from dew or rain drops. Very occasionally ladybirds have been reported biting humans. This was particularly true during the great 7-spot ladybird population explosion of 1976, when millions of these ladybirds, having decimated the aphid populations of southern England, were reported biting humans and, indeed, virtually everything else. A similar population boom was observed in 2009 and again there were occasional reports of biting. In summary, 28 ladybird species preferentially consume aphids (greenfly/blackfly); eight species consume coccids (scale insects); one species consumes Acari (mites); four species consume adelgids (conifer woolly aphids); three species consume mildew; one species consumes pseudococcids (mealybugs); one species consumes aleyrodids (whiteflies); one species consumes phylloxera; one species consumes chrysomelid larvae (heather leaf beetle); two consume diaspidids (armoured scale insects); one consumes psyllids (jumping plant lice) and two species consume plants (table 5).

3.6 Overwintering In Britain the winter is an unfavourable period for ladybirds. Lack of food and relatively low temperatures mean

Ladybirds in their environment | 25 Table 5. Principal foods of the Coccinellidae resident in Britain and notes on other foods (adapted from Majerus, 1994; Klausnitzer and Klausnitzer, 1997; Hodek and Honěk, 2009; Roy and others, 2011).

Species

Principal food

Notes on other foods

Coccidula rufa

Aphids

Coccidula scutellata

Aphids

Rhyzobius chrysomeloides

Coccids

Rhyzobius litura

Aphids

Rhyzobius lophanthae

Coccids / diaspidids

Clitostethus arcuatus

Aleyrodids

Stethorus punctillum

Mites

Aphids, honeydew, pollen

Scymnus suturalis

Adelgids especially Pineus pini

Aphids, coccids, pollen

Scymnus auritus

Phylloxera

Pollen

Scymnus frontalis

Aphids

Pollen, nectar, mildew

Scymnus haemorrhoidalis

Aphids

Coccids

Scymnus femoralis

Aphids

Pollen, nectar

Aphids

Scymnus schmidti

Aphids

Pollen

Scymnus nigrinus

Aphids / adelgids

Coccids, pollen

Scymnus limbatus

Aphids / coccids

Scymnus interruptus

Pseudococcids / diaspidids

Nephus redtenbacheri

Coccids

Nephus quadrimaculatus

Coccids

Hyperaspis pseudopustulata

Aphids

Platynaspis luteorubra

Aphids

Aphids

Coccids, honeydew, pollen, nectar

Heather ladybird

Coccids

Aphids, adelgids

Kidney-spot ladybird

Coccids

Diaspidids, aphids, adelgids, mites

Pine ladybird

Coccids/ adelgids

Aphids, mites, honeydew, pollen, nectar

Water ladybird

Aphids

Honeydew, pollen, nectar

16-spot ladybird

Mildew

Thrips, mites, pollen, nectar

Striped ladybird

Aphids

Coccids, adelgids, honeydew

18-spot ladybird

Aphids

Adelgids, pollen

Aphids

Coccids, adelgids, mites, honeydew, pollen, nectar, mildew

Cream-spot ladybird

Aphids/ psyllids

Mites, honeydew

Orange ladybird

Mildew

Aphids, honeydew

22-spot ladybird

Mildew

14-spot ladybird

Eyed ladybird

Aphids

Coccids, adelgids, honeydew, pollen

Larch ladybird

Adelgids

Aphids, coccids

13-spot ladybird

Aphids

Pollen, nectar

Adonis’ ladybird

Aphids

Coccids, honeydew, pollen, nectar

Hieroglyphic ladybird

Aphids/ larvae of heather leaf beetles

Scarce 7-spot ladybird

Aphids

Coccids, adelgids, honeydew, nectar

Aphids

Coccids, adelgids, honeydew, pollen, nectar, mildew

5-spot ladybird

26 | Ladybirds Table 5. Continued.

Species

Principal food

Notes on other foods

7-spot ladybird

Aphids

Coccids, adelgids, mites, honeydew, pollen, nectar, mildew

11-spot ladybird

Aphids

Coccids, adelgids, mites, honeydew, pollen, nectar, mildew

2-spot ladybird

Aphids

Coccids, adelgids, mites, honeydew, pollen, nectar, mildew

10-spot ladybird

Aphids

Coccids, adelgids, mites, honeydew, pollen, nectar

Harlequin ladybird

Aphids

Coccids, adelgids, aleyrodids, psyllids, mites, various insect larvae, honeydew, pollen, nectar

Cream-streaked ladybird

Aphids

Coccids, adelgids, honeydew, pollen, nectar

Bryony ladybird

White bryony

24-spot ladybird

Red campion, false oat grass

Nectar

that this period is unsuitable for high levels of activity, so the period is passed in a more or less inactive or dormant state. All the ladybirds resident in Britain pass the winter as adults; in the autumn, ladybirds that emerged from pupae in the summer will feed up and then find a suitable place to pass the winter. Most species select their winter quarters in September or early October. Different species choose different types of sites in which to pass the winter. Some, such as the 7-spot and 14-spot ladybirds, will overwinter in almost any slightly sheltered position, in curled up leaves, or hollow plant stems close to the ground. The 2-spot ladybird usually chooses an elevated position, either exposed on tree trunks, or in cracks in or under bark. Many 2-spot ladybirds are found in cracks around window frames, or actually inside buildings, which is where the harlequin is usually found. Pine ladybirds usually pass the winter on Scots pine, some fi nding sheltered positions under bark, or in pine cones, others simply tucking themselves up in a twig joint or shoot axil. The pine ladybird seems to favour south-facing overwintering sites. Conversely, the heather ladybird, when it overwinters on trees, almost invariably does so in a north-facing situation. The 24-spot, 22-spot and 16-spot ladybirds all usually stay close to the ground in their grassland habitats, but usually select a slightly raised piece of earth like a grass clump. Presumably this particular microhabitat will stay drier in wet weather

Ladybirds in their environment | 27 Table 6. Overwintering sites of the conspicuous British ladybirds

Species

Preferred habitats

Heather ladybird*

Leaf litter, bark crevices, commonly on conifers

Kidney-spot ladybird*

Deciduous trees, at the base of the trunks

Pine ladybird

Leaf litter, bark crevices, especially on pine trees

Water ladybird

Striped ladybird*

Between leaves and stems of reed and reedmace, and in grass tussocks Plant litter and low herbage, on logs, fence posts and stone walls, often in extremely large aggregations. Remains partially active Soil or moss below Scots pine trees

18-spot ladybird

Crowns or bark crevices of mature Scots pine

14-spot ladybird

Low herbage

16-spot ladybird

Cream-spot ladybird

Plant litter, bark crevices, beech nuts

Orange ladybird*

Leaf litter or sheltered positions on deciduous and coniferous trees

22-spot ladybird

Adonis’ ladybird*

Low herbage. Remains partially active Soil, leaf litter and sheltered low herbage in coniferous or mixed woodlands Bark crevices on larch, Norway spruce and Douglas fir Unknown in Britain. In mainland Europe, leaf litter or upper soil layers in damp habitats Leaf litter and low herbage in dry habitats

Hieroglyphic ladybird*

Leaf litter under heather, pine trees and gorse

Scarce 7-spot ladybird*

Low herbage near the nests of wood ants

5-spot ladybird*

11-spot ladybird*

Leaf litter, gorse and under stones Low herbage, gorse, conifer foliage and in leaf litter, often in curled dead leaves Leaf litter, gorse and buildings

2-spot ladybird

Buildings, on tree trunks, under bark, usually in elevated positions

Eyed ladybird* Larch ladybird 13-spot ladybird*

7-spot ladybird

10-spot ladybird

Leaf litter, plant debris, beech nuts

Harlequin ladybird

Bryony ladybird

In and on buildings, sometimes on trees (usually in elevated positions) Under conifer bark and in bark crevices; usually needled conifers but occasionally scale-leaved conifers such as Leyland cypress Low herbage

24-spot ladybird

Low herbage, grass tussocks, gorse. Remains partially active

Cream-streaked ladybird*

*indicates information based on limited field observations

compared to flat ground. Table 6 gives a list of preferred overwintering sites of ladybirds resident in Britain. In some cases, the proposed sites are based on relatively few records, and work is needed to verify these speculations, and to add to the list of overwintering sites. Species that come into this category are marked with asterisks. Some ladybird species form aggregations during the winter. For most species these aggregations are usually small. So, although both 7-spot and pine ladybirds are

28 | Ladybirds

pheromone: chemical substance which when released or secreted by an animal influences the behaviour or development of other individuals of the same species

found singly, they also occur in groups of up to a dozen or so. However, occasionally much larger aggregations occur. Groups of the harlequin may be as large as a thousand or more individuals. Large aggregations of several hundred 22-spot ladybirds are sometimes found in grass tussocks. However, the largest winter aggregations found in Britain are of the 16-spot ladybird (over 10,000 have been found together). Often, aggregations will involve more than one species. 7-spot ladybirds have been recorded with a range of other species including the 2-spot, 11-spot, 14-spot, 16-spot, 22-spot, larch, cream-spot and pine ladybirds. 2-spot, 14-spot and 11-spot ladybirds sometimes form mixed aggregations. The larch ladybird has been found with aggregations of 18-spot and cream-streaked ladybirds. The orange ladybird has been found with cream-spot, 10-spot and 2-spot ladybirds. The 16-spot ladybird is often found with the 22-spot ladybird as well as the 7-spot ladybird, and many other combinations have been reported. It is not entirely clear how ladybirds find and join overwintering aggregations. Research indicates that an aggregation pheromone (chemical scent) seems to be an important cue (Al Abassi and others, 1998). The chemical appears to be a pyrazine, a chemical group also important in chemical defence (see 6.3), and it is likely that it is released by ladybirds at their overwintering sites. Furthermore, it appears likely, from the occurrence of mixed aggregations, that the aggregation pheromone is not species specific and, as many sites are used by ladybirds year after year, the scent possibly persists from one winter to the next. However, these theories require further testing. The winter is a critical period for ladybirds, as it occupies the major part of the adult lives of most species. Most species of ladybird remain dormant or inactive for most of the winter, and mortality during this dormant period is often very high. The winter mortality rate depends on a number of factors: the dietary condition of ladybirds entering the dormant phase; the severity of the winter, particularly with respect to temperature and humidity; the timing of the onset of spring; and the availability of food as day length and temperature increase in the spring. In extremely severe winters over 90% of 2-spot ladybirds may die at their overwintering sites. In milder years the mortality rate may be as low as 7%. Fungal disease is a major cause of overwintering mortality in 7-spot ladybirds (Ormond and others, 2010).

Ladybirds in their environment | 29

glycogen: a polymer built of numerous glucose molecules. Animals store carbohydrates as glycogen lipids: substances with fat-like properties, including true fats, sterols and steroids

The ability of ladybirds to survive low temperatures also varies during the inactive period. Generally, the level of cold resistance increases during the first few weeks of winter, so that resistance to sub-zero temperatures is rather high in the middle of winter, but declines again with the onset of spring. Hard early or late frosts can therefore lead to very high mortality. The degree of cold resistance also seems to vary in different species. Generally, species that overwinter in leaf litter or close to the ground are more sensitive than those that overwinter in more exposed positions or in bark crevices. Most predatory species do not feed during the winter months, and so they have to survive on their food reserves. Ladybirds about to enter their overwintering sites typically show a high fat content, and the probability of survival through the winter depends, in the main, on the amount of fat that an individual has been able to accumulate before the winter (Hodek, 1973). Both stored lipids and glycogen are used as energy sources during the winter. Hariri (1966) found that about half the fat content was used up by 7-spot ladybirds between 17th September and 5th May in Britain. Smaller species used up more of their fat: in 14-spot ladybirds over 70% of fat reserves were used, while in 2-spot ladybirds the usage was over 75% for both lipids and glycogen. In some species of ladybird, the ovaries will only mature after a period of dormancy. These include the eyed, striped, kidney-spot and pine ladybirds. Other species have no such requirement, so 2-spot, 10-spot and 14-spot ladybirds will mate and lay eggs shortly after emergence from the pupa unless environmental factors such as shortening day length, falling temperatures or lack of food initiate dormancy. In still other species, such as 5-spot, 7-spot and 11-spot ladybirds, the need or lack of need for a dormant period before the ovaries mature is variable within the species. Ladybirds may leave their overwintering sites in response to an increase in either day length or temperature. In some species either factor may induce the end of the inactive period. Little is known about the requirement for an inactive or dormant winter phase in other species. Investigations of the effects of a range of environmental factors on the winter behaviour of ladybirds in Britain would certainly be worthwhile and provide useful scientific information.

4 Ladybirds and their natural enemies There is still much to explore about the predators, parasites and diseases of ladybirds in Britain. Most of the information has been accumulated from careful and meticulous observations of ladybirds in their natural habitats. However, there are a number of reasons why an even deeper understanding of the strategies and effectiveness of the enemies of ladybirds would be advantageous. First, the mortality imposed by such enemies on ladybird populations might affect the potential use of ladybirds in controlling plant pests. Secondly, the arrival of the harlequin, cream-streaked and bryony ladybirds in Britain represents a unique opportunity to study the adaptation of native natural enemies to novel non-native species. Thirdly, and more broadly, understanding interactions between ladybirds and their enemies enables us to address fundamental questions in ecology.

4.1 Predators of ladybirds When disturbed, ladybirds generally withdraw their legs into depressions on the abdomen, and exude a yellowish fluid called reflex blood. This substance, which has a bitter taste and a strong smell, gives the ladybirds some protection against many potential predators, especially when allied to their strongly contrasting ‘warning colouration’ (see 6.3). Yet there is no doubt that ladybirds do suffer predation, including from spiders, birds and ants. There have been numerous observations of ladybirds being attacked and eaten both by other arthropods and by vertebrates. Some species of spider fi nd ladybirds quite acceptable, and are not deterred by the reflex bleeding of a ladybird that has blundered into a web. Records of birds preying on ladybirds have been obtained by observation and by analysis of gut contents. Most species of ladybird are at least partially repellent or toxic to birds, but nonetheless bird predation of ladybirds does occur. For example, birds that catch flying insects on the wing do eat ladybirds. Other bird species have been recorded preying on ladybirds when other foods are scarce. This suggests that at least some species of ladybird are not actually poisonous, and that their distastefulness can be overcome if birds are hungry enough.

Ladybirds and their natural enemies | 31

parasite: organism that lives in or on another organism (the host) and benefits by deriving nutrients at the expense of the host parasitoid: insect whose larvae live as parasites that eventually kill their hosts

Perhaps the predators that are most often found together with ladybirds are ants, although this varies with the species of both ants and ladybirds. Many species of ant attend honeydew-producing aphids. These ants feed on the honeydew and protect the aphids from predators and parasitoids, in a mutually beneficial arrangement or symbiosis (Stadler and Dixon 2008). Ants seem to be more aggressive towards intruders when they are near their nest or a food source, such as a colony of aphids. El-Ziady and Kennedy (1956) showed that the common black ant Lasius niger attending the black bean aphid accelerated the rate of growth of the aphid colony, and the ants were aggressive towards ladybird larvae, driving them away or picking them up and dropping them over the edge of a leaf. Ladybirds that are attacked by ants either fly away or clamp down onto the substrate (if this is a flat surface). On uneven surfaces, the ladybird cannot clamp down, but instead endeavours to keep the side of the elytra being attacked in contact with the substrate. This prevents the ant gaining access to its more vulnerable undersurface. A confrontation between a ladybird and an ant rarely results in the ladybird’s death, but some ladybirds do fall prey to ants when they are attacked by several at one time. In these cases the ants may take the ladybird’s corpse back to the nest. An unusual case is that of the scarce 7-spot ladybird, which is said to be ‘myrmecophilous’ or ‘ant-loving’. Unlike other species, this ladybird is not attacked by ants, although they do react to its movement by tapping it with their antennae (Pontin, 1960). The scarce 7-spot is usually found close to nests of Formica species of ant, although it does not seem to rely on the ants for any basic life function and can be bred quite easily in the laboratory in the complete absence of ants. However, its immunity to ant attacks, thought to be due to physical, behavioural and chemical adaptations (Sloggett and others, 1998; Sloggett and Majerus, 2003), seems to enable it to live in a niche free from other ladybirds, which are driven off by the ants.

4.2 Parasitoids and parasites of ladybirds Hymenoptera: the insect order that includes bees, wasps, ants and sawflies

Organisms known to parasitise ladybirds in Britain include flies (Diptera), parasitic wasps (Hymenoptera), mites (Acari), and roundworms (Nematoda). There are also records of infection with ‘male-killing’ bacteria and

32 | Ladybirds

a number of fungal diseases (pathogens). Generally, only larvae, pupae and adults are attacked. Egg parasites have never been recorded in Britain. In some cases, this may be due to the habit of young ladybird larvae of eating any unhatched eggs (see 6.2). As egg parasites usually emerge from parasitised eggs after the larvae have hatched from non-parasitised eggs, the parasites themselves would be devoured before completing their development.

endoparasite: a parasite that lives inside the body of its host

ovipositor: the egg-laying apparatus of a female insect

Parasitoid flies Among the true flies, or Diptera, the commonest species of endoparasite (parasites that develop inside the host) belong to the genus Phalacrotophora (the phorid fl ies, family Phoridae). In the south of England and East Anglia P. fasciata is usually the commoner species, but elsewhere in Britain, P. berolinensis is more frequent. Both species are small, around 2mm long, with squat bodies and a characteristic hunch-backed stance. They are pale yellow-brown in colour, with darker legs. All phorid species have a characteristic pattern of wing venation, with three thick, dark veins running along the leading edge of the wing to the halfway point, and a few pale, thin veins branching from these and extending to the wing’s trailing edge. Identification of these fl ies to a species level is tricky and for conclusive identification it is necessary to examine the female (ovipositor) or male genitalia (see Disney, 1983). However, it is also helpful to take a close look at the hind feet (P. fasciata has a broader and darker first segment (metatarsus) of the hind foot in comparison to the narrow, brownish to yellowish metatarsus of P. berolinensis). Until 1920 P. fasciata and P. berolinensis were not distinguished and all records were given as P. fasciata. Interestingly, a single host can be parasitised by both P. fasciata and P. berolinensis – a case of multiparasitism. Further European species are described in Disney and Beuk (1997), including P. beuki, which was recognized as a parasitoid of eyed ladybirds (Durska and others, 2003). These phorid parasitoids provide an interesting study system, despite the difficulties with their identification. It is possible to carefully collect ladybird pupae and monitor them for emergence of either a ladybird adult or phorid flies. Further details are provided in chapter 9. There are many questions that could be addressed including assessing the phenology (timing of key events in the life-cycle) of the phorids in association with different

Ladybirds and their natural enemies | 33

Fig. 22. Puparia of Phalacrotophora fasciata which had parasitised a kidney-spot ladybird pupa.

Fig. 23. Puparium and adult of Medina separata which had parasitised an eyed ladybird adult.

hosts and in various habitats. One research area that is particularly appealing is the colonisation of non-native species, such as the harlequin ladybird, by these phorid parasitoids, and it will be fascinating to observe how quickly phorids adapt to this new host. In Britain, P. fasciata has been recorded from the 2-spot, eyed, cream-spot, heather, kidney-spot, 7-spot, harlequin, Adonis’, striped, and 22-spot ladybirds; and P. berolinensis from the 2-spot, eyed, larch, cream-streaked, harlequin, and striped ladybirds. Other host records await discovery or require confirmation. The eggs of these parasites are laid between the legs of pre-pupal ladybird larvae, or on the underside of newly formed pupae. The parasite larva hatches out in a few hours and immediately bores into its host, where it develops, before exiting to pupate through a ragged hole beneath the host’s head. The first sign of the effects of these parasites on ladybird pupae taken into the laboratory is usually the appearance of the dark red-brown, strongly segmented puparia (fig. 22). Several parasites may develop in a single ladybird pupa with the maximum viable number within a pupa dependent on the pupal size. The 7-spot and eyed ladybirds may contain over six parasites, while the 2-spot will rarely have more than three or four. The level of parasitisation is generally low, but may reach 50% of 2-spot or larch ladybird pupae in some populations. The rate of parasitisation of harlequin ladybird pupae by Phalacrotophora species has been closely monitored since the harlequin’s arrival in 2004. Evidence shows that while it is not currently attacked at the same level as native ladybirds, parasitisation rates are increasing, suggesting that the parasitoids are beginning to adapt to this novel and abundant host (Ware and others, 2010). The other dipteran parasite which has been recorded from ladybirds in Britain is Medina separata (Tachinidae) (fig. 23). Most records on the parasitism of ladybirds by Medina species erroneously refer to Degeeria (=Medina) luctuosa (Meigen), which is specific to adult chrysomelids of the genus Haltica (Ceryngier and others, 2012), and all records from ladybirds are thought to be M. separata. This species similar in appearance to a house-fly or bluebottle, but is 5–6 mm long and almost entirely black, with a slender, hairy abdomen. Medina separata has been recorded from 2-spot, 10-spot, eyed, and cream-spot ladybirds in Britain, and

34 | Ladybirds

from a range of other species including the 2-spot, larch, 7-spot, pine, harlequin, Adonis’, 18-spot, 14-spot, and 22-spot ladybirds in continental Europe. The eggs of the parasite are laid singly, and only one larva will develop in a host. The adult host is killed when the parasite consumes its vital organs. The parasite larva emerges through the upper abdominal wall, and pupates in the soil, emerging about a week later. Fig. 24. Adult Dinocampus coccinellae.

parthenogenesis: a form of reproduction in which eggs develop without having been fertilised

gonad: an organ in which sex cells are produced; a testis or an ovary

Parasitoid wasps Of the Hymenoptera, the most important ladybird parasite is Dinocampus coccinellae (Braconidae, Euphorinae) (fig. 24). This wasp is exclusively a solitary, internal parasitoid of adult ladybirds, and it is by far the best studied of the parasitoids. The wasp is around 4 mm long, black to dark red, and has iridescent green-black eyes. It has long antennae, and a dark spot halfway along the leading edge of the wing. The abdomen is narrow where it joins the thorax (the ‘wasp waist’), and at the rear it tapers to a pointed ovipositor. The species is parthenogenetic; viable eggs are laid without fertilisation. These give rise only to females. Adult females pursue ladybirds with the abdomen flexed forward between the legs, and under the head. The female will feel the ladybird with her antennae before attempting to lay her egg with a powerful thrust of her ovipositor, through any weak point in the cuticle. The egg hatches in about five days and the larva passes through three instars. Only one parasitoid ever completes its development in a particular ladybird, although a number of female wasps may lay eggs in the same host. The first-instar parasitoid larvae are equipped with grasping mandibles, with which one of the larvae eventually destroys the others, so only one larva will reach the second instar. The feeding larva does not kill its host directly. It feeds on nutrients in the haemolymph (insect blood) that would normally go to the gonads of the ladybirds, which remain immature. The vital organs are left intact. The fully grown larva emerges from the ladybird through the membrane between the fi fth and sixth, or sixth and seventh plates on the underside of the abdomen. The ladybird becomes virtually immobile about half an hour before the appearance of the larva. The parasitoid does not usually kill its host, but leaves it partially paralysed and unable to walk. The larva then spins a cocoon between the legs of the ladybird (fig. 25),

Ladybirds and their natural enemies | 35

Fig. 25. Cocoon of the parasitoid Dinocampus coccinellae spun between the legs of a paralysed 7-spot ladybird.

where it gains some protection from predation from its host’s warning colouration. Although the paralysed ladybird can live for over a week, ensnared by the cocoon it usually eventually dies of starvation or fungal infection, although ladybirds can recover the use of their legs and occasionally escape. When the adult parasitic wasp emerges about a week later, it already contains ripe eggs, so is able to attack other ladybirds almost immediately. Dinocampus coccinellae has been recorded from the 2-spot, 10-spot, eyed, cream-spot, hieroglyphic, 5-spot, 7-spot, 11-spot, pine, orange, harlequin, cream-streaked, Adonis’, 18-spot, striped, 14-spot, 22-spot, and 16-spot ladybirds in Britain. Smaller species of ladybird do not seem to be particularly suitable hosts for this parasitoid. As with the phorids described above, evidence suggests that the harlequin ladybird is a less suitable host for D. coccinellae than native British species, but that the rate of successful parasitism, including the parasitism of juvenile stages, is increasing (Ware and others, 2010). Dinocampus coccinellae may have several generations in a year, the exact number being dependent on the weather conditions. In cool summers there may be only a single generation, in warm ones up to three or even four. The parasitoid passes the winter as a larva inside an overwintering ladybird. Ladybirds are also parasitised by small chalcidoid wasps of the genera Oomyzus and Aprostocetus (Hymenoptera: Eulophidae) and Homalotylus (Hymenoptera: Encyrtidae). Oomyzus and Aprostocetus were previously placed within the genus Tetrastichus. Three species of Homalotylus parasitise coccinellids. Homalotylus eytelweini is a gregarious parasitoid of a number of ladybird species. Eggs are laid in the larvae, usually when the larvae are att ached to a substrate when moulting. The parasitoids take only a few days to develop and pupate inside the ladybird larva, which again attaches itself to the substrate as though preparing to moult, but instead it swells and the cuticle becomes hard and darkens. The adult parasitoid bores a small hole in the cuticle through which it leaves its host. The number of parasitoids that develop in a particular larva again depends on the size of the host, so a larva of the small heather ladybird may harbour only one to three parasitoids, while that of the large 7-spot ladybird may contain up to six. The adults, which are sexually mature when they

36 | Ladybirds

emerge, feed on honeydew, and live for one to two weeks. They have up to four generations per year in Britain. They have been recorded from the 7-spot, 14-spot and heather ladybirds, and may use other species as hosts. Two further Homalotylus species, H. flaminius and H. platynaspidis, generally parasitise only small coccinellid species. Homalotylus flaminius is a solitary internal parasitoid of coccinellids of the genera Scymnus and Nephus. Probably the only known host of H. platynaspidis in Britain is Platynaspis luteorubra. However, in eastern Europe it is also reported from Scymnus (Ceryngier and others, 2012). The adults of all these species are minute black wasps, with dark bands across the middle of the forewing. The principal ladybird parasitoid belonging to the genus Oomyzus is O. scaposus (formerly named Tetrastichus coccinellae). This is a gregarious internal parasitoid of the larvae and pupae of a number of aphid-feeding ladybirds. Up to 25 parasitoids have been recorded in a single 7-spot, while in the 2-spot the average number of parasitoids is ten and in the heather ladybird six. Oomyzus scaposus was recorded from harlequin ladybird pupae for the first time in 2009 (Ware and others, 2010). The adults are minute all-black wasps, similar in appearance to D. coccinellae but much smaller, around 1 mm long. The wings are clear, without the bands typical of the Homalotylus species. Eggs are occasionally laid in pupae, but third- or fourth-instar larvae are usually parasitised, pupating before the emergence of the parasitoids. All the parasitoids that emerge from a host do so through a single neat exit hole, usually in the top of the thorax. The complete development of the parasitoid takes three to five weeks, and there are several generations per year. A gregarious parasitoid that is closely related to and resembles O. scaposus is Aprostocetus neglectus. Separation of these species requires microscopic examination and familiarity with the small hairs on the main wing vein (the presence of 6–7 setae on the upper surface of the submarginal vein is indicative of A. neglectus, as opposed to the single bristle present for O. scaposus). There is very little known about the ecology of this parasitoid other than it parasitizes pupae and, occasionally, late larval stages of ladybirds. There are records in Britain from two host species: pine ladybird (Sheffield in 2002) and Adalia species (Oxfordshire in 2010) (Richard Comont, personal observation). It is widespread across continental Europe, where it has also been recorded from the heather ladybird.

Ladybirds and their natural enemies | 37

Parasitic mites Ladybirds are also attacked by parasitic mites (Acari) of the genus Coccipolipus. The parasites develop on the inside of the elytra, with several females usually present. They feed on the blood of the host and lay several hundred eggs. The nymphs fill the space between the elytra and the abdomen. The 2-spot ladybird is the most common host, but other species may also be attacked. Although the parasitoids do not usually kill the ladybird, they do weaken it and render females sterile. Coccipolipus hippodamiae (the most studied of the 14 known species of Coccipolipus mites) has recently been found infecting the harlequin ladybird in parts of North America and Europe; infection causes females to become sterile within three weeks (Rhule and others, 2009). These mites are not established within Britain. Nematodes Several species of nematode worm, from two families (Allantonematidae and Mermithidae), are internal parasites of ladybirds. Parasitylenchus coccinellinae (Allantonematidae) lives in several species of ladybird, particularly the 14-spot but also the 2-spot and Adonis’ ladybirds, and Oenopia conglobata and Semiadalia undecimnotata in continental Europe (Iperti, 1964). As many as 140 adult females have been found in a single ladybird, with up to 10,000 larvae and young adults. Although the nematodes do not usually cause death, they inhibit the maturation of the ovaries of the ladybirds, and also consume the food reserves of the hosts. A new species of allantonematid nematode from the genus Howardula was found in adults and larvae of the 2-spot in 1965 (Hariri, 1965). Interestingly, this nematode did not seem to alter the host gonads, as is the case with other allantonematids, but resulted in a reduction in size of host fat bodies. A species of Mermis has also been recorded in the 7-spot, 14-spot and Adonis’ ladybirds.

4.3 Microorganisms

gametocyst: a cyst within which sex cells are produced

Very little work has been carried out on diseases of ladybirds. Protozoa of the family Gregarinidae (Sporozoa) are known to destroy intestinal cells of coccinellid larvae and adults, and may be fatal by blocking the gut with gametocysts.

38 | Ladybirds

endosymbiont: organism that lives within the cells of another organism

Bacteria Understanding of bacterial diseases of ladybirds is limited, with one intriguing exception, the male-killing bacteria (Majerus and Hurst, 1997). These cause their hosts to produce female-biased sex-ratios amongst their offspring. The bacteria live within the ladybird’s cells, and are transferred from parents to offspring only in the egg cytoplasm. Therefore both sexes are born infected, but only the females can pass the bacteria on to their offspring so, to the bacteria, male ladybirds are a dead end. Consequently only around half the eggs laid will hatch, as the male offspring are killed as eggs. These unhatched eggs are eaten by their female siblings on hatching, increasing their fitness, and that of the bacteria within them (Hurst, 1991; Majerus, 2003). This large-scale non-hatching of eggs is the most obvious sign of an infection, which can be confirmed by treatment with antibiotics. Bacteria from five different groups have been identified as male-killers of ladybirds (Rickettsia, Wolbachia, Spiroplasma, Flavobacteria and Alpha-proteobacteria). Male-killers have been recorded from fourteen species of ladybird worldwide, but in Britain only five species are known to host them: the 2-spot, 10-spot, cream-spot, water, and Adonis’ ladybirds. 2-spot ladybirds are host to four different male-killers (a Rickettsia, two species of Wolbachia and Spiroplasma) and so they are a particularly interesting species in which to study male-killing. However, only Rickettsia has been noted within Britain. Roy (2010) demonstrated that 2-spot ladybirds infected with male-killing Spiroplasma and Rickettsia were more susceptible to the fungal pathogen Beauveria bassiana (see below) than either uninfected or Wolbachia-infected 2-spot ladybirds. The evolutionary relationship between Wolbachia and ladybirds is longer than that of either Spiroplasma or Rickettsia with ladybirds, and this is possibly why Wolbachia infection is less costly than infection by the other endosymbionts. Fungi Another microbial group that has received increased attention over the last decade is the pathogenic fungi (Roy and Cottrell, 2008). A number of fungi can infect insects and cause diseases, just as is the case for humans. However, unlike fungal pathogens of humans which usually cause minor symptoms (such as athlete’s foot), fungal diseases of insects often result in death. The most

Ladybirds and their natural enemies | 39

ectoparasite: parasites that occur on the outside of the host

important group of fungi infecting ladybirds is called the hypocrealean fungi, including Beauveria bassiana, Metarhizium anisopliae, Isaria farinosa (= Paecilomyces farinosus), I. fumosorosea (= P. fumosoroseus) and Lecanicillium (= Verticillium) lecanii. None of these fungal pathogens have English names and their scientific names are under some debate because taxonomists are investigating the status of these fungi as species complexes (for example, the name B. bassiana is known to encompass more than one species but the exact resolution is currently unclear). The taxonomy of these fungal pathogens is fascinating but can also be confusing. The best-studied genus of hypocrealean fungi infecting ladybirds is Beauveria (Roy and Cottrell, 2008). This fungus produces spores which germinate and invade the body of the insect, eventually filling the entire body cavity, at which stage the fungus emerges back through the surface of the infected individual and produces spores, and so the infection cycle begins again. Overwintering ladybirds are particularly susceptible because they become stressed by the adverse environmental conditions. Indeed B. bassiana is a major mortality factor for overwintering 7-spot ladybirds; 10–15% of 7-spot ladybirds succumb to infection (Ormond, 2007). Similar levels of B. bassiana infection appear to occur for other overwintering ladybirds, particularly those that are gregarious. This fungus was thought to be a soil-borne pathogen and so ladybirds such as the 7-spot, which overwinter in the soil or leaf litter, were considered most at risk. However, research has demonstrated that B. bassiana is found above and below ground and so could also infect species of ladybird that overwinter on trees (Roy and others, 2008; Ormond and others, 2010). Roy and others (2008) showed that harlequin ladybirds are more resistant to infection by B. bassiana than 2-spot or 7-spot ladybirds, but that infected harlequins laid fewer eggs, suggesting there is a sub-lethal cost to infection by this fungal pathogen. Clearly, there is still much to be revealed about this fascinating fungus and its interactions with ladybirds. Another group of fungi, the Laboulbeniales, are obligate ectoparasites that can be found infecting many arthropod hosts, particularly beetles (Weir and Hammond, 1997). Ladybirds are infected by several species of the genus Hesperomyces, the most common of which is H. virescens, and infections have been found

40 | Ladybirds prevalence: the proportion of hosts infected

on the 2-spot, heather, kidney-spot, 7-spot, harlequin, 14-spot, and 22-spot ladybirds. Infection can be observed as small yellow cylindrical-shaped fruiting bodies (thalli, around 1 mm long) projecting from the adult ladybird, usually on the elytra of females and the ventral surface of males (contact during sexual reproduction is thought to be the major transmission mechanism of H. virescens). Laboulbenialean fungi do not kill their hosts, but heavy infections can impede flight, mating, foraging and feeding (Nalepa and Weir, 2007). Microsporidia are highly specialised fungi that live inside the cells of their host, and have very complex life cycles (Roy and Cottrell, 2008). Microsporidian species are often highly specific and confined not only to single host species but to specific tissues within the hosts, such as the fat body, the midgut wall or the reproductive tissues. Nosema species are common microsporidians found infecting ladybirds.

4.4 Future work There is still much to be learned about the enemies of ladybirds. The lack of knowledge of ladybird predators, parasites and pathogens means that most new studies will be valuable. Our understanding could be much improved by straightforward surveys of ladybird parasites in field populations, indeed there is a very real possibility that new species of ladybird parasites still await discovery. It is currently hard to assess the relative importance of predators, parasites and pathogens as causes of mortality in ladybird populations, and equally their importance in regulating ladybird populations. Much further work is needed to evaluate the regulatory effects of these natural enemies. Studies needed include the percentage of individuals of different ladybird species that are attacked by the various species of parasite; and the effect of ladybird population density or season on parasitisation rate. In 2010 the UK Ladybird Survey launched a natural enemy survey primarily concerned with recording the incidence of ladybird parasites across Britain. It is hoped that the information collected by members of the public participating in this survey will greatly improve our understanding of ladybird-natural enemy interactions and perhaps provide more general information about how insects interact with their predators, parasites and pathogens.

Ladybirds and their natural enemies | 41 Table 7 The enemies (parasites and pathogens) of ladybirds and their hosts, with an estimation of prevalence in Britain (low = less than 1%, medium = 1–5 %, high >5%).

Enemy

Ladybird hosts

Prevalence

Phalacrotophora fasciata

2-spot, 10-spot*, eyed, cream-spot, heather, kidneyspot, scarce 7-spot*, 5-spot*, 7-spot, 11-spot*, pine*, orange*, harlequin, cream-streaked*, 13-spot*, Adonis’, 18-spot*, striped, 14-spot*, and 22-spot ladybirds

High (about 10% in 7-spot populations)

Phalacrotophora berolinensis

2-spot, 10-spot*, eyed, larch, cream-spot*, kidneyspot*, scarce 7-spot*, 7-spot*, pine*, cream-streaked, harlequin, and striped ladybirds

Medium

Medina separata

2-spot, 10-spot, eyed, larch*, cream-spot, 7-spot*, pine*, harlequin*, Adonis’*, 18-spot*, 14-spot*, and 22-spot* ladybirds

Low

Dinocampus coccinellae

2-spot, 10-spot, eyed, cream-spot, hieroglyphic, scarce 7-spot*, 5-spot, 7-spot, 11-spot, pine, orange, harlequin, cream-streaked, 13-spot*, Adonis’, 18-spot, striped, 14-spot, 22-spot, and 16-spot ladybirds

High (about 75% in some populations)

Homalotylus eytelweini

Heather, 7-spot, and 14-spot ladybirds

Low

Homalotylus flaminius

Scymnus and Nephus species (inconspicuous ladybirds)

Low

Homalotylus platynaspidis

Platynaspis luteorubra (an inconspicuous ladybird)

Low

Oomyzus scaposus

2-spot, eyed*, heather, 5-spot*, 7-spot, and harlequin ladybirds

Medium

Aprostocetus neglectus

2-spot, heather*, and pine ladybirds

Low

Mites

2-spot, 10-spot, cream-spot, scarce 7-spot, 7-spot, 11-spot, harlequin and cream-streaked ladybirds

Low

Nematode worms

2-spot, 10-spot, larch, 7-spot, Adonis’, and 14-spot ladybirds

Low†

Protozoa

2-spot, 10-spot, 5-spot, 7-spot, pine, creamstreaked, 13-spot, Adonis’, 18-spot, 14-spot, 16-spot ladybirds

Low†

Male-killing bacteria

2-spot, 10-spot, water, cream-spot, 7-spot, 11-spot, harlequin, cream-streaked, and Adonis’ ladybirds

Medium

Pathogenic fungi

2-spot, eyed, larch, cream-spot, scarce 7-spot, 5-spot, 7-spot, pine, cream-streaked, 14-spot, and 16-spot ladybirds

Low to medium (sometimes high over winter)

Hesperomyces sp

2-spot, heather, kidney-spot, 7-spot, harlequin, 14spot, and 22-spot ladybirds

Low†

Microsporidia

7- spot and harlequin ladybirds

Low†

Parasitoid fl ies

Parasitoid wasps

Parasites

Microorganisms

* = Not recorded from this host species in Britain (data only available for well-studied species: Dinocampus coccinellae, Aprostocetus neglectus, Oomyzus scaposus, and the parasitoid flies) † = very limited number of studies

5 Variation in ladybirds 5.1 Colours and patterns in ladybirds

epidermis: outermost layer of cells. In insects it is one cell thick and secretes the cuticle

melanic: dark or black

Individuals of the same species of ladybird often differ from one another in colour and pattern; many colour forms have been given names. For example, the commonest form of the 2-spot ladybird is called form (f.) typica. There is a common belief that the number of spots on a ladybird indicates its age, but this is a myth. In general, the number of spots on a ladybird does not change once the normal pigments have been laid down in the epidermis. However, rates at which pigments are laid down do vary and so contribute to the variation seen in some species. When an adult ladybird emerges from its pupal case, its elytra are soft and a translucent creamy, yellow, orange or red colour. The distinctive colour patterns soon begin to appear. Plates 8.1–3 show the colours of the typical form of the 2-spot ladybird 30 minutes, 12 hours and 48 hours after emergence. Similarly, a newly emerged eyed ladybird is cream-yellow, both on the elytra and on the underside of the abdomen. The reddish-brown colour begins to appear within the first 24 hours, together with the black spots, and the underside of the abdomen darkens considerably. The cream rings begin to appear on the second day. A week after emerging from the pupa, the ladybird is a rich reddish brown with sharply defi ned black spots surrounded by bright, cream rings. However, pigments continue to be laid down so that the insect gradually becomes darker during the rest of its adult life. This can be seen if the colours of ladybirds in autumn and spring are compared. The colours of dead specimens fade and so can be misleading for identification purposes. The rate of pigment development is variable in some species. The melanic form (f. bimaculata) of the 10-spot ladybird is black with bright red shoulder flashes in its final form. After emergence, the ladybirds pass through a period when the elytra are a darkening maroon or brown, and the shoulder flashes are yellow or orange, before the final colours are achieved. This transition may take anything from a day to several months. Similar variation in the rate of pigment development contributes to the range of ground and marking colours in f. decempustulata of the 10-spot (see 5.3). The rate of pigment

Variation in ladybirds

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deposition in 10-spot ladybirds is genetically controlled. There appear to be two genes involved (one for the black melanin and one for the red carotenoids) but both are so closely linked they essentially act as one gene. Each gene has a ‘fast’ allele and a ‘slow’ allele; the ‘fast’ allele is dominant over the ‘slow’ allele. 10-spot ladybirds expressing the dominant ‘fast’ allele will develop the melanic regions of the elytral colour pattern within a few days, whereas colour pattern development for those expressing the recessive ‘slow’ allele can take many months (Majerus, 1994). Recent research suggests that 10-spot ladybirds exposed to low temperatures during development will behave as if they are expressing the ‘fast’ allele regardless of their actual genetics (Jones, 2004; Michie, 2010). In ladybirds that are black with a pattern of red spots, the elytra are red on emergence, and the darker pigments are gradually laid down over specific areas. This transition is very rapid in the kidney-spot, heather, pine and melanic harlequin ladybirds, which achieve their full colour within 24–48 hours of emergence. In melanic forms of the 2-spot the process is slower, and the order in which melanic pigments are laid down over particular areas can be studied. Plates 8.4–9 show the development of black pigment over the first 48 hours after emergence of f. sexpustulata of the 2-spot.* The changes in pattern due to variations in the rate of pigment development can make it hard to quantify the frequencies of different forms of a species in a population. For example, black pigment may be laid down over the hindmost pair of red spots of the f. sexpustulata pattern of the 2-spot (pl. 9.2) as much as three months *The nomenclature of ladybird colour forms is very complex. This is largely due to a German entomologist named Mader, who described and catalogued all the varieties of European ladybirds he could discover (see Mader, 1926–37). In many cases, individuals that differ in pattern by only very minute details are afforded different names. For example, Mader lists 119 different pattern forms of the 10-spot, but most British populations consist of only three main forms, with minor variations of each (see 5.3). Many species vary much less in Britain than in the rest of their range. For example, Mader described forms of the 5-spot ladybird with anything from one to 11 spots, but all known British specimens have either five or seven. Similarly, in the water ladybird, he described spot numbers from 0 to 21, but all British individuals we have examined have had at least 15 spots. In addition we have discovered a number of forms in Britain that were not known to Mader. In this chapter and chapter 6, we follow Mader’s nomenclature only when strictly applicable. We group colour forms that have some basic feature in common together under one name.

44 | Ladybirds

genetic: concerned with or controlled by genes which enable characteristics to be passed from one generation to the next

after emergence. This effectively converts the form from sexpustulata to quadrimaculata (pl. 5.8). Consequently, if a significant proportion of the melanics in a population are of this type, an increase in the proportion of quadrimaculata and a decrease in the proportion of sexpustulata may be expected as a new generation ages, and changes in the frequency of these forms between autumn and spring may be due to pigment deposition rather than other factors such as different chances of survival through the winter. The rates of pigment development and variations in the rates and the order in which different components of the patterns become apparent have only been studied in a few species. Others await attention, including all the yellow and black species and some of the species having the most complex patterns, such as the creamstreaked ladybird. One of the surprising features of ladybirds is that some species are very variable in colour and pattern, while others are relatively uniform. In Britain, the 7-spot, cream-spot and kidney-spot ladybirds vary little. On the other hand, the 2-spot, 10-spot and harlequin ladybirds all have a considerable range of forms. In some species, a number of distinct forms occur. For example, in the hieroglyphic ladybird, three main forms are common (pl. 6.7–8 and pl. 10.12). In others, such as the 14-spot, the variation seems to be more or less continuous, so that no distinct classes can be defined. The factors that produce this variation are unknown in many species, although it is suspected that much of the variation is under genetic control.

5.2 Colour pattern variation in the 2-spot One of the most variable of the British ladybirds is the 2-spot. In this species, over a hundred different colour patterns have been described, ranging from all red to all black. The variation is most obvious on the elytra, but the black markings on the basically-white pronotum also vary considerably. In Britain, over a dozen genetically distinct forms have been identified. The commonest (typical) form is red with a single black spot on each elytron (f. typica). However, in many populations melanic forms in which the elytra are black with either four (f. quadrimaculata, pl. 5.8) or six (f. sexpustulata pl. 9.2) red spots are common, and a third melanic form with just two red spots (f. sublunata, pl. 9.1) occurs more rarely.

Variation in ladybirds gene: an hereditary factor or heritable unit that controls a characteristic and can be transmitted from one generation to the next. Genes are composed of DNA and usually situated in the thread-like chromosomes within the nucleus alleles: different forms of a gene. Genes are considered alleles of each other when they occur in the same positions on the members of a chromosome pair, have different effects in respect of a particular characteristic, and can mutate one to another. Not more than two alleles at any gene locus can be present in a normal ladybird cell, as one allele is inherited from each parent recessive: a recessive allele is only expressed in the homozygote in which two identical copies are present modifier genes: a series of genes, each with small effects, which modify the exact expression of a major gene dominant: a dominant allele suppresses or overshadows the expression of another allele at the same locus. It is fully expressed in one of the homozygotes, and in the heterozygote heterozygote: an individual that has inherited two different alleles of the gene in question, one from each parent homozygote: an individual that has inherited two identical alleles, one from each parent

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The range of black patterns on a red background is even greater. The two black spots present in the typical form may be extended slightly or greatly. In some individuals there are simply small extensions, either towards the centre line or towards the outer margin, while in others these extensions may spread both forward and backwards so that there are roughly equal areas of red and black. Although the range of patterns is extreme, a number of discrete patterns occur. These include f. extreme annulata (pl. 9.6) which is similar to sexpustulata but has larger red spots and a thin streak of red running backwards from the shoulder patch. Form duodecempustulata (pl. 9.7) has a chequered pattern of black on red; ‘spott y’ (pl. 9.9) has a set of eight or nine small and generally discrete black spots on each red elytron, and ‘strong spott y’ (pl. 9.10) is similar but has the spots enlarged and fused. The genetic relationships between many of these forms have been studied by breeding experiments, looking at the offspring produced by particular pairs of parents (Majerus and others, unpublished). A single pair of alleles controls the three melanic forms (sublunata, quadrimaculata and sexpustulata), and the typica form. The dominant allele of this main colour pattern gene produces the melanic form and the recessive allele produces typica. The differences between the three melanic forms are produced by modifier genes, which slightly alter the basic melanic pattern. Extreme annulata, duodecempustulata, spotty and strong spott y are each controlled by a different allele of the main colour pattern gene. All these alleles are recessive to the melanic allele. The dominance relationships between these four alleles and the typica allele are complicated. The typica, spott y, and strong spott y alleles are usually dominant to the duodecempustulata allele, although occasionally heterozygotes are slightly affected by the presence of the duodecempustulata allele. The typica allele is also more or less dominant to spott y. However, the heterozygote combination of typica and strong spotty alleles produces a form called ‘semi-spotty’. The extreme annulata allele shows no dominance with any of these forms. With typica, extreme annulata gives a range of intermediates from ‘weak annulata’ (pl. 9.3) through ‘bar annulata’ (pl. 9.4) to ‘intermediate annulata’ (pl. 9.5). Extreme annulata and either spott y or strong spotty produce a heterozygote called ‘zigzag spotty’. The

46 | Ladybirds

Fig. 26. Black form of the 2-spot ladybird

heterozygote between duodecempustulata and extreme annulata is a form called ‘new duodecempustulata’ (pl. 9.8). Thus, much of the colour pattern variation is controlled by different alleles of a single gene. Other genes may also affect the colour or pattern. The recessive allele of another gene, when present with the spotty homozygote, modifies the spotty form to produce a form called ‘sexpustulata spotty’ (pl. 9.11), which appears intermediate between sexpustulata and extreme annulata. This allele, which seems to increase the amount of black patterning, also modifies the extreme annulata form, to a form called ‘melanic annulata’ (pl. 9.12) which has almost as much black as f. quadrimaculata. The recessive allele of a third gene can modify melanic annulata or strong spotty to produce a form that is almost completely black (fig. 26). The rate of deposition of red pigment varies amongst the forms of the 2-spot. Red pigment appears sooner in the melanics and f. typica than it does in the other forms. In f. duodecempustulata and spott y, the ground colour may still be a relatively pale orange a month after emergence from the pupa. In addition, the orange and red pigments seem to be laid down at different rates in different regions of the elytra, giving the ladybirds a rather streaky appearance. Very occasionally the ground colour may be very different indeed. In the form purpurea, the final colour of the adult is dark purple. This pigment is laid down over a number of weeks. The insect appears typical when it first emerges from the pupa. The first evidence of variation occurs two or three days later when the normal red ground colour begins to look somewhat dirty, as darker pigment begins to appear. This form is again controlled by a single recessive gene (Majerus and others, 1987). Although a certain amount of work has been carried out on the inheritance of colour pattern variation in the 2-spot ladybird, there is still plenty of scope for further work. New undescribed forms are still being discovered. The genetic relationships between many of the forms still have to be determined. The effect of environmental factors such as temperature and food availability on pigment deposition and pattern still needs further investigation. In addition the question of why some species of ladybird show so much natural variation needs to be addressed (see chapter 6).

Variation in ladybirds

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5.3 Colour pattern variation in the 10-spot

polygenic: a character controlled polygenically is affected by a large number of genes, each of which has a small effect

The 2-spot ladybird is not the only species to show substantial genetic variation. Its closest British relative, the 10-spot ladybird, also boasts considerable variation in pattern and colour. The 10-spot ladybird comes in three main forms. The commonest is generally f. decempunctata (pl. 5.10). It is usually a shade of orange, red or brown, with small black, dark brown, or reddish spots on the elytra. The number of spots varies from 0 to 12, although very rarely higher spot numbers have been recorded. Form decempustulata (pl. 5.11) has a chequered pattern, not unlike f. duodecempustulata of the 2-spot. However, the pattern may comprise a black or brown grid on a yellow, orange or red background. There is also some variation in the width and strength of the grid, giving some individuals a much coarser pattern than others. There are reports of decempustulata-like 10-spots that have a pale grid on a dark background (Moon, 1986), but we have never come across any of this type. The third main colour type is f. bimaculata (pl. 5.12), a melanic form with just two pale shoulder flashes, one on each elytron at the side of the base, near the pronotum. The ground colour varies from mid-maroon to black, and the flash from yellow to red. In this form particularly, the variation in colour seems to depend on age, as mentioned above. There have been reports that the three main forms are genetically controlled by three different alleles of the same gene, and that f. decempunctata is dominant to f. decempustulata, which in turn is dominant to f. bimaculata. However, recent work has shown that the inheritance is not so simple (Majerus and others, unpublished). For example, two different alleles control f. decempunctata. One, the top dominant, produces f. decempunctata in which the number of dots varies under polygenic control. This means that if two ladybirds each with eight spots mate, the majority of progeny will have eight spots, but some will have six or 10 and a few will even have four or 12. However, another allele, recessive to the decempunctata allele, produces a form which is basically f. decempunctata but it always has precisely 12 spots (pl. 10.10). This form is called duodecempunctata, and the allele controlling it T12. If two f. duodecempunctata mate, there is no spread in the number of spots in the progeny - all will have 12. Unfortunately, f. decempunctata with 12 spots and f. duodecempunctata are not visibly distinguishable,

48 | Ladybirds

their genetic differences being revealed only by carefully controlled breeding experiments. The f. decempustulata and f. bimaculata do appear to be controlled by two further alleles of the same gene as f. decempunctata and f. duodecempunctata, but in these there is a considerable variation with respect to colour and the rate of pigment development. This variation appears to be genetic, but it is not clear whether it is controlled by a range of alleles of a single gene or by one or more other genes. The full picture in respect of the inheritance of colour pattern variation in the 10-spot still has to be resolved. This can only be done by a series of carefully designed and controlled breeding experiments. Forms intermediate between the three main classes do occur, but only rarely, perhaps as a result of matings between individuals which have originated in different populations. The inheritance of colour pattern is by no means straightforward. There is evidence in both the 2-spot and 10-spot ladybirds that the dominance relationships between the alleles controlling the common colour forms are altered by additional modifier genes, which vary between populations. When individuals from different populations with different sets of modifier genes are crossed, the dominance relationships between colour forms may break down, producing a wide range of intermediate individuals rather than the expected clear distinction between colour forms.

5.4 Colour pattern variation in the harlequin ladybird polymorphic: variable in phenotypic form of the same species

The harlequin ladybird is highly polymorphic in elytral and pronotum colour pattern. Indeed, by 1945 more than two hundred different colour forms were documented at varying frequencies across its native range from southern Siberia (Altai Mountains) to Manchuria, Korea, Japan and China (Tan, 1946). Only three colour forms have been recorded in Britain: succinea, conspicua and spectabilis (pl. 3.1–3.4). Early studies confirmed that the major colour forms are controlled by 15 alleles at one multiallelic locus (Tan, 1946; Komai, 1956). Eleven of these alleles are rare, with a combined frequency of less than one per cent in populations. Conspicua, spectabilis, axyridis and succinea are the four major alleles and all apart from succinea are melanic forms (Michie and others, 2011). Form succinea is orangered with 0–21 black spots; form spectabilis is black with

Variation in ladybirds

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four red spots; form conspicua is black with two red spots; and form axyridis has a black and red chequered pattern. Dominance is known to increase with darkness, so the order of dominance (high – low) is: conspicua, spectabilis, axyridis, succinea (Tan and Li, 1934). Some conspicua and spectabilis individuals possess black spots within the large red spots on their elytra. This is due to the phenomenon of mosaic dominance (Tan, 1946), in which a heterozygote will form black pigment in any part of the elytron that is pigmented in the respective homozygotes. So a succinea-conspicua heterozygote will express the black spots of the succinea allele in any areas that would not be black in conspicua. Research nearly a century ago demonstrated that the frequency of the four main alleles varies tremendously across the native range of the harlequin ladybird (Dobzhansky, 1924, 1933). The geographic variation in colour forms appeared to be linked to climate – f. succinea was found in hot and arid regions whereas the melanic forms were most commonly associated with cooler, humid regions. However, the prevalence of colour forms varies in frequency across Japan but with no obvious link to climate (Komai and others, 1950). Furthermore, there is temporal (seasonal) variation in colour forms within the native range. Wang and others (2009) attributed the high frequency of melanics found in spring compared to autumn to thermal melanism and mate choice, concluding that the melanic forms have a large fitness advantage in the winter and a disadvantage in the summer. Interestingly, this geographic variation has been reflected across the invaded range. The possible explanations for these trends will be explored in more detail in the next chapter.

5.5 Colour pattern variation in other species Variation in the colour and patterns on the pronotum and elytra is not confined to these three species. Indeed, all the ladybirds resident in Britain show some variation. There are five main components of the colour patterns: ground colour, colour of markings, number of spots, strength (contrast) of spots, and fusions between the spots. All these components show variation in some species. In a few species, the variation is even more complex. In the eyed ladybird, the compound nature of the markings - black spots surrounded by cream rings means that there is variation in both the presence of the rings and the spots.

50 | Ladybirds Table 8. Components of colour and pattern variation in British ladybirds (for Adalia species see 5.2 and 5.3). These notes have been compiled from British specimens only; many species show additional variation in other parts of their range

Spot number Species

Ground colour

Spot colour Range

Commonest

24-spot

Russet or very rarely buff

Black or very rarely yellow

0–26

20

Bryony

Orange

Black

11

11

13-spot

Red

Black

7–15

13

Adonis’

Red

Black

3–15

7

15–21

19

0–6

0

Water Larch

Buff with reddish or Black yellowish tinge Pink, pale tan, orange, Black brown or mid-tan

16-spot

Creamy-buff

Black

16–18

16 (3 lateral spots fused)

7-spot

Red

Black

0–9

7

Scarce 7-spot

Red

Black

5–11

7

5-spot

Red

Black

5–7

5

11-spot

Red

Black, rarely with yellow rings

7–11

11

Hieroglyphic

Brown

Black (stripes and spots)

0–7

5

Cream-streaked

Pink, salmon or orange Black

4–16

4 or 16

0–21

16

14

14

4–14

14

0–15

13

0–22

18

Harlequin Cream-spot 14-spot Striped Eyed

Yellow-orange or Black orange-red Maroon-brown or very Cream rarely black Yellow or black

Black or yellow

Chestnut or rarely dark Cream stripes, rarely brown with black inside Russet red or burgundy Black often with cream red rings

22-spot

Yellow

Black

20–22

22

Orange

Orange

White or creamy-yellow

12 or 16

16

18-spot

Maroon

Cream or pale buff

14 or 18

18

Kidney-spot

Black

Orange or red

2

2

Heather

Black

Red

2–6

6

Pine

Black

Red

2–4

4

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Table 8. Continued.

Species

Variation in strength of spots

Fusion between spots

Fully melanic form

24-spot

Considerable

Common, may be considerable

f. nigra (rare)

Bryony

Slight

Rare

None

13-spot

Slight

Rare, but may be considerable

f. borealis (very rare)

Adonis’

Slight

May be considerable

None

Water

Considerable

Not uncommon, may be considerNone able

Larch

Considerable

Rare, but may be considerable

f. fumata (dark brown, rare)

16-spot

Slight

Common, may be considerable

f. poweri (uncommon)

7-spot

Considerable

Very rare

f. anthrax (rare)

Scarce 7-spot

Slight

Thin fusion lines may occur but very rarely

None

5-spot

Some

Variable

None

11-spot

Considerable

Uncommon, but some

None

Hieroglyphic

Considerable

Common, but considerable

f. areata (common)

Cream-streaked

Some

Uncommon, considerable

f. haneli (rare)

Harlequin

Very variable

Common, considerable

f. conspicua (2 red spots, common), f. spectabilis (4 red spots, common)

Cream-spot

Little

Rare, slight

f. nigripennis (rare)

14-spot

Very variable

Very common, considerable

f. merkeri (rare)

Striped

Some

Common, may be considerable

f. lignicolor (rare)

Eyed

Considerable

Rare, may be considerable

f. hebraea (very rare)

22-spot

Little

Rare, little

None

Orange

Little

None

None

18-spot

Some

Common, some

None

Kidney-spot

Some

None

None

Heather

Little

Common, some

None

Pine

Some

None

None

52 | Ladybirds

Mendelian gene: a gene that behaves in accordance with the laws of inheritance discovered by Gregor Mendel

Table 8 outlines the variation found in Britain with respect to ground colour, marking colour, spot number, strength of spot, and fusions between spots. Many species have forms that are almost or completely black, and the existence and approximate commonness of these melanic forms is also indicated. A detailed discussion of all the minute variation in all the British species is outside the scope of this book, and the reader is referred to Majerus (1994) for more information. However, it is worth mentioning a few particular cases to illustrate certain facets of variability, and to indicate examples suitable for genetic analysis of the variation. In the eyed ladybird, forms with cream spots but lacking the black centres to the spots (pl. 10.2) are found occasionally in the wild. There is evidence that the basis of this ‘blind’ form is genetic, but the precise mode of inheritance has not been worked out. The hieroglyphic ladybird has three main forms. The most common of these has a tan colour, usually with five black spots (pl. 6.7). There is also a black form (f. areata) (pl. 6.8), and a form intermediate between the tan and black forms (pl. 10.12). There is as yet no evidence to indicate whether the variation is genetic or environmental. In Britain, the cream-streaked ladybird usually has either 16 spots (pl. 4.9), or only the two outermost spots on the edge of each elytron (pl. 4.8). As with the ‘blind’ form of the eyed ladybird, there are indications that the difference between these forms is genetic, but again the exact mechanism is not known. This species also has a dark form in which the black spots are enlarged and diffuse at the edges (pl. 10.5). It is known that this form is controlled by a single Mendelian gene, but whether it is dominant or recessive to the normal forms has not been analysed. In species where some aspect of the variation is apparently continuous, like the strength of the black markings of the 14-spot, there is considerable scope for research. The most probable explanation for this type of variation is the interplay between environmental factors (such as temperature and food) and many genes at several loci. The role of polygenic inheritance may be explored by selecting the darkest individuals from a large sample for breeding; this should lead to an average increase in amounts of black in the next generation. If

Variation in ladybirds

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Table 9. Variation in spot number in Adonis’ ladybird in a series of samples from a Staffordshire population recorded during 1985, 1986 and 1987

Spot number

Number of ladybirds % of total

3

3

1.9

5

10

6.4

7

61

39.1

8*

1

0.6

9

49

31.4

10*

1

0.6

11

18

11.5

13

12

7.7

15

1

0.6

Total

156

*Occasionally there is a difference in the number of spots between the two elytra of a particular ladybird. The 8 and 10 spotted individuals are a product of such asymmetry. In each case one elytron has one spot fewer than the other.

Fig. 27. Unusual form of the 2-spot ladybird with the hindpart of both elytra purple.

Fig. 28. Bilateral mosaic 7-spot ladybird, with the left elytron red, and the right elytron brown.

this is done repeatedly for three or four generations, it should be possible to produce ladybirds that are very much blacker than any in the original sample. As long as the rearing of ladybirds is always carried out under similar conditions, such a result would be good evidence that the black patterning in this species is controlled polygenically. It is possible that the strength of markings in the 18-spot and 24-spot ladybirds is also under polygenic control, but similar selective breeding experiments are needed to confirm this suggestion. Adonis’ ladybird exhibits considerable variation in spot number, as shown by counts for a series of samples from a Staffordshire population between 1985 and 1987 (table 9). Spot number ranged from three to 15. Most individuals had seven or nine spots. This distribution of spot numbers, with the low and high values rare and the medium values common, is suggestive of polygenic inheritance, but again, breeding experiments are needed to confirm this. Occasionally, ladybirds are found with very unusual markings. Figure 27 shows a typical 2-spot with a dark patch covering the hind part of the elytra. Figure 28 shows a 7-spot in which the normal red pigment is replaced by brown pigment on the right elytron, the left elytron being normal. In some 7-spots, the larger part of both elytra has normal red pigments with just

54 | Ladybirds

Fig. 29. Asymmetrical 14-spot ladybird, the markings on the left being less pronounced than those on the right. mitosis: the normal process of cell division in growth, involving the duplication of chromosomes, and the division of the nucleus into two, each with an identical complement of chromosomes to the original cell mutation: a sudden change in the genetic material controlling a particular character or characters of an organism. Such a change may be due to a change in the number of chromosomes, to an alteration in the structure of a chromosome, or to a chemical or physical change in an individual gene

Fig. 30. A 2-spot ladybird with stunted elytra and wings.

a small patch being brown. Figure 29 is an asymmetric 14-spot ladybird with much bolder black markings on the right elytron than on the left. The causes of such oddities are not known. In each of the three examples shown, the ladybirds were mated to normal individuals and resulting progeny were allowed to breed, yet in none of them did the unusual patterns recur in the progeny of either the first or second generation, suggesting that these pattern variations are not inherited. They may be due to disruption in pigment production resulting from injury to larvae or pupae, or to mitotic mutation in early development. Such suggestions can only be speculative until more is known of the biochemistry of pigment production and deposition. In some cases, it may even be the result of environmental conditions affecting a perfectly normal adult – for example, overwintering with one elytron permanently in shadow, and another exposed to the elements may cause weathering only on one side. Perhaps the most unusual facet of colour pattern variation within a species is demonstrated by the water ladybird: this species has the remarkable ability to change colour during the year. Water ladybirds spend the winter tucked down between the sheaths of dead reedmace leaves, and at this time are buff-coloured with 19 black spots. This colour pattern offers superb camouflage against their winter habitat. However, during the spring they disperse to new reeds in search of food and rapidly develop bright warning colours, the background colour of their elytra changing from buff to red. This change in colour is intriguing and unique among British ladybirds, but its mechanism is not yet known.

5.6 Other morphological variation The colour and pattern of the elytra are not the only characteristics that vary. For example, some species show great variation in size. This is usually a reflection of variation in environmental factors such as food availability or temperature. It should also be noted that male ladybirds are often considerably smaller than female ladybirds. Perhaps one of the most surprising features that is subject to variation involves the structure of the elytra or wings. For example, in the 2-spot, the elytra and wings may be reduced to miniature stumps (fig. 30). This is very rare, but does occur naturally and appears to be controlled by a recessive allele. It should be noted, however, that this effect can also be produced envi-

Variation in ladybirds

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55

ronmentally, and is often seen in individuals that have struggled to emerge successfully from their pupa. The ladybird has a brief window of opportunity to expand its elytra immediately after emergence, while they are still soft, and if something disrupts the expansion, for example getting stuck half-out of the pupa, the elytra will set in a shrunken, crumpled form. The wings are also involved in a most unusual type of variation in the 24-spot ladybird. In the majority of individuals of this species found in Britain, the flight wings are fused together and reduced in size, making them quite useless as flight organs. The frequency of this fl ightless form decreases further east in Europe and Asia. Variation in flight wing length has been observed in several of the inconspicuous ladybird species: for example, Rhyzobius litura and R. chrysomeloides. Hammond (1985) also revealed that R. litura has two different forms of wing-folding mechanism, and we echo his call to look beneath the elytra, particularly of these smaller species. Other insects that exhibit variations in wing length, such as bush-crickets, have provided good case studies for investigating the northward spread of species in response to climate change (Hickling and others, 2006). Ladybirds have not yet been studied in such analyses, but could be a useful study group in this regard, especially as many ladybird species are predicted to spread northwards with climate change.

6 Population and evolutionary biology 6.1 Population size Female ladybirds have the capacity to lay over a thousand eggs each, so, theoretically at least, ladybird populations could increase more than 500-fold each generation. In fact, this potential is never realised, although the population size of some species can vary markedly from year to year and from place to place. Many factors can affect population size. Ladybird mating and egg-laying are affected by temperature, sunshine and rainfall. The number of eggs laid by a female is determined by her condition, particularly with respect to her past diet, the climate and especially the availability of food. Not all the eggs that are laid hatch. Some will be infertile. Even some fertile eggs fail to hatch. They may be eaten, for although egg parasitism has not been recorded amongst ladybirds in Britain, ladybird eggs are preyed upon by a variety of invertebrate predators, including other ladybirds, lacewing larvae, ants and predatory Hemiptera (see chapters 3 and 4). The eggs of some species are also infected by male-killing bacteria (see 4.3), in which case most or all of the male eggs fail to hatch. Of the larvae that do hatch from eggs, only a small proportion will survive to reach the adult stage. Mortality during the larval and pupal stages may be due to starvation, parasitism, disease, predation, cannibalism or other events such as severe weather (see chapters 3 and 4). When the ladybirds finally emerge from their pupae, most species need to build up food reserves before the winter. Their chances of survival over this period particularly depend on the state of these food reserves, coupled with the winter climate and the suitability of the overwintering habitat found by the ladybird (see 2.6). All these factors influence the size of ladybird populations. Occasionally, favourable conditions lead to enormous population explosions. Large numbers of aphids, together with favourable climatic conditions during both summer and winter, may permit the high potential fecundity of females to be realised. In Britain, such conditions were widespread in 1975 and 1976. The long warm summer of 1975, followed by a mild winter,

Population and evolutionary biology | 57

led to huge populations of aphids in the spring of 1976. The ladybird populations, particularly of 7-spots, 2-spots and 14-spots, began to increase during 1975 and mortality over the winter of 1975–76 was lower than usual. Ladybirds emerging from their overwintering sites were faced with an abundance of aphids and optimum weather conditions for mating and egg-laying. Their larvae found abundant food, and in the hot weather of 1976 completed their development rapidly. Larval and pupal mortality were low, so enormous numbers of ladybirds attained the adult state in mid-summer 1976. At the same time, aphid populations decreased dramatically, partly because of predation by ladybirds and their larvae, and partly because the hot dry conditions adversely affected the plants upon which the aphids were feeding. When short of food, ladybirds become very mobile. On hot days, huge numbers can take to the air, where warm currents may carry them for considerable distances. In 1976 enormous numbers of ladybirds were recorded across southern and eastern Britain. Most of them were 7-spots, but there were also good numbers of 2-spots and 14-spots and smaller numbers of 10-spots and 11-spots. The numbers were greatest along the south and east coasts. Tide-lines consisted of millions of dead ladybirds for kilometre after kilometre, and live ladybirds became a serious nuisance to holiday-makers in seaside resorts. There were many reports of ladybirds biting or stinging people. In fact, ladybirds cannot sting, and in normal circumstances will not bite people. The explanation of the reports in 1976 is that the starving ladybirds were biting into anything they landed on to test if it was edible, and injecting a tiny amount of digestive enzyme at each bite. When such foreign enzymes react with the body’s chemical defences a stinging sensation is produced. The enormous numbers of ladybirds recorded along the south and east coasts in 1976 led to a general belief that there had been a massive migration of ladybirds into Britain from the Continent. This was not so. Some ladybirds do arrive on British shores from neighbouring European countries but the vast majority of the ladybirds observed on this occasion had simply migrated in search of food, from populations spread across Britain, until their dispersal was arrested by the coast. There have been other reports of similar explosions in 7-spot numbers. In 1952 millions of 7-spots appeared on the east coast of Britain. Again the tide-line was

58 | Ladybirds

documented to be coloured red by the dead ladybirds. Cannibalism was said to be rife; resting ladybirds were observed attacking other individuals as they landed and before they had the time to gain protection by folding their wings. More recently, in the summer of 2009, the UK Ladybird Survey received reports of 7-spot ladybirds reaching ‘plague proportions’ along the south-east coast and particularly along the North Norfolk coastline. Similarly in the summer of 2011 high numbers of 7-spot ladybirds were encountered alongside unprecedented numbers of 14-spot ladybirds. Population explosions like these are usually followed by a population crash due to starvation and high levels of cannibalism, and often due to an increase in parasite populations. Ladybirds can then become rather scarce and it may take several seasons for the balance between aphids, ladybirds and ladybird parasites to stabilise again. Generally, these occasional population explosions involve only the aphid- or adelgid-feeding species. This suggests that they depend on the occasional, exceptional abundance of prey. Population explosions are almost unknown in herbivorous, mildew-feeding or scale-insect feeding species, whose food supply tends to fluctuate less. Even in ordinary years, ladybirds can become more obvious when searching for overwintering sites in autumn, leading to press reports about ladybird plagues in late summer or early autumn. The harlequin ladybird has received particular attention due to its favouring buildings as an overwintering habitat. Since its arrival in Britain in 2004 it has reached large population sizes across much of the country, particularly in the southeast of England. Every autumn the UK Ladybird Survey receives reports of large groups of harlequin ladybirds from buildings. In some cases the numbers reported exceed 1,000, but generally aggregations of 100 or more are reported from buildings, particularly houses, and most commonly around bedroom windows. Reports from churches are also common and this is possibly linked to the proximity of suitable summer habitats; harlequin ladybirds are commonly found on deciduous trees in graveyards. In some cases people find the number of harlequin ladybirds occupying their house a nuisance. There are frequent reports of the defensive secretions (reflex blood) produced by harlequin ladybirds when disturbed staining wallpaper, curtains and other

Population and evolutionary biology | 59

furnishings. Some people fi nd the smell of harlequin ladybirds, also from reflex blood, unpleasant. There have been a few reports of harlequin ladybirds biting people. In early spring harlequin ladybirds disperse from buildings, but people report them returning to the same locations every year. The numbers entering houses provide the UK Ladybird Survey with a useful measure of the population size of harlequin ladybirds. For this reason, people are encouraged to send their sightings to the UK Ladybird Survey on a regular basis. Many people ask if there is anything they can do to get rid of the harlequin ladybirds. However, often this species overwinters in mixed groups with other, native species of ladybird; any direct action could also affect the other species, which is undesirable. It is also unlikely that removing aggregations would make much difference to the overall population size. It is possible that in years to come there will be a sustainable and effective method of controlling harlequin ladybirds, but currently this is not the case (Kenis and others, 2008). Many factors are known to affect overall ladybird abundance. However, the relative importance of the different factors is still poorly understood, and almost any carefully conducted population study is likely to produce useful information. For example, studies might investigate the incidence of the different types of parasite, or how the availability of food or climatic conditions affect population density. Mortality over the winter period could be investigated by carrying out mark-release-recapture experiments (see 9.3) in the autumn and spring. Counting the number of harlequin ladybirds within window frames throughout the winter months, and of remaining harlequin corpses after winter is over, would provide useful information and would be very easy. Ladybird migrations also need to be studied. We know ladybirds move in search of food, and they also migrate to and from overwintering sites, but we know little about how far ladybirds may move from one generation to the next. Ladybird movement can also be investigated by marking ladybirds (as in Brakefield, 1984a).

6.2 The evolutionary biology of sibling egg cannibalism Aphid-eating ladybirds lay their eggs in clutches. When the larvae hatch they eat any unhatched eggs around them before dispersing to look for aphids. These eggs

60 | Ladybirds

trophic egg: a non-hatching egg that provides nutrition for hatching larvae within an egg clutch

kin selection: a process whereby an individual increases the representation of its own genes in later generations by helping related individuals that possess the same genes by common descent

can be infertile or only have partially developed before dying (in which case they are coloured yellow), or latehatching viable eggs (in which case they are grey). There are numerous benefits of this process of ‘sibling egg cannibalism’ (so-called because larvae eat their sibling eggs) for the cannibal (see 2.3). The larvae will be larger when they disperse and this will make catching the first aphid, which can be bigger than the larva, easier. Similarly the larvae will survive longer before they need to catch this first aphid. This is important because many first-instar larvae starve to death before catching an aphid. Larvae that have eaten an egg generally develop faster than those that have not (Roy and others, 2007). Experiments suggest that female harlequin ladybirds may produce more non-hatching eggs when there are fewer aphids available to eat (Perry and Roitberg, 2005). These trophic eggs could be produced specifically to provide additional nutrition for hatching larvae, because they have fewer opportunities for finding aphids. They are identical to ordinary ladybird eggs (Osawa and Yoshinaga, 2009), suggesting that perhaps even when food is not scarce, some eggs are produced deliberately to provide nutrition for hatching larvae. Trophic eggs have not been recorded from other ladybirds and further studies are needed to examine whether other ladybirds produce a higher proportion of non-hatching eggs when less food is available for the larvae. Similarly, field studies are needed, in both the harlequin and other ladybirds, to examine whether fewer ladybird eggs hatch in clutches on plants with low aphid populations compared to those with high aphid populations. Another consequence of sibling egg cannibalism is the occurrence of male-killing bacteria in aphideating ladybirds (see 4.3). The bacteria are only transmitted from generation to generation through the eggs of females; they are not transmitted with male sperm. Therefore, these bacteria have no interest in being in males, but by killing the male eggs they enhance the survival of females, which eat the dead male eggs. In this way, bacteria in male eggs enhance the survival of their relatives, which carry the same genes in females, an example of kin selection (Elnagdy and others, 2011). A number of different bacteria have evolved to do this in aphid-eating ladybirds. This example of convergent evolution has arisen because of the pre-existing occurrence of sibling egg cannibalism in the aphid-eating

Population and evolutionary biology | 61 convergent evolution: a process where unrelated organisms evolve characteristics similar to each other

species. Ladybirds with male-killing bacteria lay clutches of which only about half the eggs hatch, and the adults arising from these clutches are predominantly or exclusively female. The eggs of aphid-eating ladybirds appear to develop exceedingly quickly. This could be because late hatching viable eggs get eaten by the first larvae to hatch, providing a selective pressure for eggs to develop very fast. Generally, aphid-eating ladybirds develop quickly as their aphid prey do not persist for very long. Smaller eggs develop more quickly, so it is expected that the eggs of aphid-eaters should be as small as possible for fast development. The larvae can then avoid sibling egg cannibalism, as well as cannibalism and predation coming from outside of the clutch. However, it has also been suggested that the eggs of aphid-eaters are constrained in how small they can be by the need of the larvae to catch aphids and by the length of time required to grow to adulthood. If the larvae were any smaller, prey capture would be impossible and the time to grow to adult size would be exceedingly long (Stewart and others, 1991). Thus egg size appears to be a compromise between the time needed for egg development, which is short if the egg is small, the time required for a larva to develop to an adult, which is short if the egg is large, and the capacity to catch aphids, which is high if the egg is large. Many coccid-, mildew- and plant-eating ladybird species also lay their eggs in clutches, although these clutches are generally smaller than those of aphid eaters, numbering up to 10 eggs. In many cases it is not clear whether these species cannibalise the eggs of their siblings or not. As the occurrence of sibling egg cannibalism affects so many other aspects of a ladybird species’ biology, it would be of great interest to know whether it does occur in these species. This would be relatively easy to find out by getting such species to lay eggs in captivity (see 9.2) and making observations of what happens when the larvae hatch.

6.3 Warning colouration and chemical defence Most ladybirds are patterned with two or more bright contrasting colours, such as red and black or yellow and black. This is warning (aposematic) colouration; that is it tells potential predators that ladybirds are distasteful or poisonous. Warning colours are used as a defensive

62 | Ladybirds

Fig. 31. An eyed ladybird reflex bleeding.

strategy by a wide variety of organisms. Naïve predators will learn to associate bright colours with an unpleasant experience, such as a sting or a nasty taste, so that similarly coloured prey are avoided in the future. Aposematic species usually behave in a way that helps both to make them obvious to predators and to advertise their distastefulness or toxicity. Ladybirds often rest in exposed positions where they can easily be seen. They make little attempt to escape when disturbed, rather, they tend to ‘play dead’ by pulling their legs and antennae close into the body, and keeping still, a behaviour known as thanatosis. The adults of most ladybird species also exude a yellowish fluid from their leg joints (fig. 31); some species’ larvae (which may also have bright patches of colour: see pl. 7) can also produce this fluid directly through the body wall. This behaviour is called reflex bleeding. The secretion produced contains nasty tasting or toxic alkaloid chemicals that protect the ladybird; the exact type of alkaloid varies from species to species (Daloze and others, 1995). Ladybird secretions also contain foulsmelling pyrazine chemicals (Moore and others, 1990) which, like a bright colour pattern, also warn predators that ladybirds are inedible. Although eggs cannot reflex bleed and reflex bleeding is rare, though not unknown, in ladybird pupae, both stages are also protected by alkaloids and pyrazines. Other chemicals such as histamines and quinolenes may also play a role in ladybird chemical defence (Brakefield, 1985). The unpalatability or toxicity of ladybirds has been demonstrated against a variety of enemies of ladybirds. These include both vertebrates, such as birds and mammals, and invertebrates, such as ants. An interesting function of ladybird alkaloids is to protect ladybirds from predation by other species of ladybird that do not share the same type of alkaloid. In such cases, the alkaloids of the victim can be toxic to the predator. Thus when 7-spot larvae eat eggs of the 2-spot, which uses alkaloids different from those used by the 7-spot, and vice versa, the larvae often die (Hemptinne and others, 2000). Due to this, ladybirds probably rarely eat other species of ladybird. An exception is the harlequin ladybird, which often eats other species of ladybird and does not seem to suffer any ill effects from the alkaloids of many of the species it consumes (Sloggett and others, 2011). Chemical protection is also ineffective against some

Population and evolutionary biology | 63

other predators. The degree of protection afforded to ladybirds by their unpleasant-tasting chemicals is likely to vary with the species of ladybird, the ability of the predator to deal with the toxic ladybird chemicals, the predator’s state of hunger, its taste and scent perception, and its method of hunting. For example, among the birds, house martins are known to eat 2-spots, 7-spots, 10-spots, 11-spots and 14-spots. House martins feed on the wing and catch flying insects, so ladybirds have little chance of advertising their distastefulness before being devoured. Some species of ladybird, including the larch ladybird and some of the smaller coccinellids, are not warningly coloured, even though they generally do reflex bleed. Experiments have suggested that these species are palatable to predators and thus that they may not contain toxic chemicals or warning pyrazines (Pasteels and others, 1973). They probably obtain protection by being camouflaged and tend to rest in sheltered or hidden positions. Several other species of ladybird may employ both camouflage and warning colouration as defensive mechanisms, including the conifer-specialised eyed, striped, 18-spot, and cream-streaked ladybirds, which all do possess defensive alkaloids. The cream-streaked ladybird is very obvious from some distance away when it is moving about, or basking on the pine needles and twigs. At these times the colour pattern seems to act as a warning advertisement. However, when resting, this species sits on pine shoots, which it matches in colour and pattern to a very high degree. It is then extremely difficult to see. This ladybird is therefore aposematic when active or in an exposed position, and camouflaged when in its normal resting position. Similar observations have subsequently been made in respect of the eyed, striped and 18-spot ladybirds. Further investigations are necessary, using a variety of natural enemies to test the relative palatabilities of aposematic species, nonaposematic species and species that use both strategies. It has been suggested that many of the aposematic species of ladybirds mimic each other. When a number of species, each protected by some device such as a sting, a bite, or an unpleasant taste, resemble one another, they are said to exhibit Müllerian mimicry. This will evolve if predators learn which potential items of prey are inedible. If a number of inedible species look alike, then predators need learn only one pattern, and fewer of each prey species are killed than would be the case if

64 | Ladybirds

each had a unique pattern which had to be learnt individually. Brakefield (1985) hypothesised that most British ladybirds fall into five Müllerian mimicry complexes or rings, as indicated in table 10. However, Majerus (1994) points out that other factors could also lead to close resemblance between ladybirds. For example members of the tribe Chilocorini, such as the pine, heather and kidney-spot ladybirds, are all black with red spots. This most likely arose because the ancestor of all these species was also black with red spots; the resemblance between its descendant species could arise due to their close relatedness, rather than as a result of mimicry. An interesting case of mimicry involves the polymorphism of the 2-spot ladybird. In this case (and also in the case of the 10-spot), different forms fall into different mimicry rings. Melanic forms resemble members of the subfamily Chilocorinae. Indeed the resemblance between f. quadrimaculata of the 2-spot and the pine ladybird is very striking (see pl. 5.8 and 6.12). By contrast non-melanics fall into the ‘red with black marks’ group, along with species such as the 7-spot. There is a strong possibility that 2-spot mimicry is not full Müllerian mimicry, but another form of mimicry called Batesian mimicry. Batesian mimicry occurs where a more palatable species resembles a more strongly unpalatable one. In this case the mimic obtains protection from its resemblance to the nastier ‘model’ species. However, for the more palatable mimic to gain protection from predators it must be rarer than the unpalatable model. If there are more mimics than models, predators will learn to associate the colour pattern with a tasty prey. One way for a common species to remain rarer Table 10. Brakefield’s proposed Müllerian mimetic rings in ladybirds. (Based on Brakefield, 1985)

Red or orange-red Black with red with black marks marks

Yellow with Brown with Red-orange, pink or black spots yellow marks yellow with black lattice pattern

7-spot

Pine

16-spot

Cream-spot

5-spot

Kidney-spot

22-spot

Orange

Hieroglyphic

11-spot

Heather

Water

Cream-streaked

10-spot (f. decempustulata)

13-spot

2-spot (melanics)

Eyed

10-spot (f. bimaculata)

Adonis’ 2-spot (non-melanic) 10-spot (f. decempunctata)

18-spot

14-spot

Population and evolutionary biology | 65

than its models is for different individuals of the species to mimic very different models; that is for the species to evolve polymorphism. Although 2-spot ladybirds possess alkaloids and are unpalatable, experiments with birds and ants have shown that this species is more palatable, or less toxic, to birds than the 7-spot ladybird (Pasteels and others, 1973; Marples and others, 1989). Similarly it also appears to be more palatable to birds than the pine or kidneyspot ladybirds (Marples, 1993). It therefore seems likely that rather than being simply a Müllerian mimic of these species, the 2-spot is at least a partial Batesian mimic and that Batesian mimicry plays at least a part in maintaining polymorphism in this species (Brakefield, 1985). However this is clearly not a full explanation for its polymorphism. The abundance of the different forms of the 2-spot sometimes matches the abundances of the proposed model species, but sometimes does not (Muggleton, 1978; Majerus, 1994). Without doubt many other factors also play roles in maintaining polymorphism in the 2-spot. Some of these are probably more important than mimicry (Brakefield, 1985).

6.4 Polymorphism in the 2-spot ladybird In the laboratory, the highly variable colour patterns of 2-spot ladybirds and their underlying genetics have been very well studied (see 5.2). However we are still some way from a full understanding of the selective forces acting on the different colour pattern forms in nature and in particular why the different forms have population frequencies that vary over space (geographic variation) and time (temporal variation). Like the studies on mimicry discussed above, most of the research on this question has been concerned with the differences between melanic and typical forms. Early research established the geographic distribution of the different forms, particularly the melanics, throughout the range of the 2-spot. These studies, over many years, have shown a high frequency of melanics only from the climatic extremes of the species range, including north-west and southern Europe as well as central Asia. In Britain, high frequencies of melanic forms are found mainly in urban populations in the north and west, although there are exceptions to this pattern. For example, melanic forms have been recorded at an appreciable frequency from some populations in south-west London.

66 | Ladybirds

thermal melanism: black individuals absorb the sun’s radiation more readily than paler ones and so ectothermic species could benefit from increased melanism at low ambient temperatures, in which they can become active more rapidly than non-melanic individuals.

The co-existence of two different genetic colour forms suggests that there is a balance of benefits and costs to the different forms. Certain factors favouring melanics over non-melanics must be balanced by other factors favouring non-melanics over melanics. Timofeeff-Ressovsky (1940) found changes in the frequency of forms between spring and autumn in Berlin, Germany. Melanic ladybirds were more common in the autumn than they were in the spring. He suggested that in the spring and summer, melanic ladybirds warm up more quickly than non-melanics, absorbing radiation faster than the red typical forms. Indeed, by measuring body temperature with very fine thermocouples, Brakefield and Willmer (1985) showed that in simulated sunlight, melanic 2-spot ladybirds warmed up faster, and reached higher temperatures, than non-melanic morphs of the same species. Consequently, they reproduce more quickly, leading to the increase in melanic frequencies observed during the summer. Among overwintering ladybirds, mortality was greater in melanics than in non-melanics. TimofeeffRessovsky (1940) attributed this to the greater fluctuations in temperature to which the melanics would be subjected; black surfaces absorb and emit radiation faster than red ones. The high winter mortality of the melanics would account for the drop in their frequency between autumn and spring. Seasonal changes in the frequency of different colour forms have occasionally been reported but the vast majority of studies have not revealed any consistent pattern. Nevertheless, other associations with climatic conditions are known. Scali and Creed (1975) found fewer melanics at higher altitudes in northern Italy, and att ributed this to lower temperatures. In Britain, Muggleton and others (1975) found that the important environmental factor was not temperature itself, but the amount of sunshine. They suggested that because melanics absorb more radiation, they are more liable to overheat and desiccate in summer. This would explain the association between melanic forms and the urban areas of north-west Britain, because smoke pollution reduces levels of solar radiation. Observations have shown a decline in the frequency of melanic forms as aerial pollution has declined after anti-pollution legislation (maps 1 and 2, p. 68). This strongly suggests a link between melanism in Britain and atmospheric pollution. It should be noted that the effect of

Population and evolutionary biology | 67

being melanic during the spring and summer appears to be quite different in Berlin and Britain. In Berlin, because melanics absorb more radiation, their activity and reproductive output are greater than those of non-melanics. However, in many parts of Britain melanics are rare because, it is suggested, they absorb too much radiation. This is despite the fact that Britain has a cooler summer climate than Berlin. Such differences in interpretation highlight the difficulties encountered when attempting to interpret or explain 2-spot form frequency data using climate. There does not appear to be a uniform association between single climatic factors and form frequency throughout the range of the 2-spot ladybird. Indeed some studies have documented opposing trends in different places (for example Bengtson and Hagen, 1977; Brakefield, 1984b). A likely factor affecting the maintenance of melanism involves the mating behaviour of the ladybirds. In the Netherlands, Brakefield (1984c) found that because they warm up faster, melanic ladybirds of both sexes enjoy a mating advantage because they begin mating earlier in the year. In Britain, studies by Majerus and others (1982a) found that some female ladybirds from a number of populations preferred to mate with melanic males rather than non-melanics. The mating preference appeared to be under the control of a single gene; females lacking that allele mated at random (Majerus and others, 1982b, 1986). The advantage that individual melanics receive from such ‘female choice’ would be greatest when melanics are rare, because when melanic males are common the choosy females have plenty of potential melanic mates, while when they are rare each melanic male will mate with many of the choosy females. This is an example of negative frequency dependent selection: as the frequency of a given trait increases, the advantage of having that trait decreases. Later studies have been contradictory over the occurrence of mating preferences for melanics (Kearns and others, 1990, 1992; O’Donald and Majerus, 1992; Tomlinson, 1996) and further investigations would be immensely valuable. Such studies could include the recording of forms of mating and non-mating individuals in natural populations, regular recording of the mating partners of marked and released individuals, or experiments providing captive females with a choice of mates of different colour forms. Despite all the work that has been done on variation

68 | Ladybirds

Map 1. The frequencies of melanic (black segments) and non-melanic (white segments) 2-spot ladybirds in Britain during the 1960s (after Creed, 1971). (Minimum sample size ten ladybirds.)

Map 2. The frequencies of melanic (black segments) and non-melanic (white segments) 2-spot ladybirds in Britain, 1985–1987. Data from the Cambridge Ladybird Survey.

in the 2-spot, we are still far from understanding how it evolved, or why it is maintained. Much research is still needed and many questions remain unanswered. For example, why is the frequency of the melanic form of the 10-spot relatively constant throughout Britain when the frequency of melanic 2-spots varies so greatly from place to place (see maps 2 and 3)? These species are closely related and similar in many aspects of behaviour, ecology and variation. Yet the melanic form of the 10-spot appears in almost all British populations of the species, with frequencies usually ranging from 5 to 20%, while melanic forms of 2-spot are absent from many populations, but have been found to be over 70% of others. Only by collecting form frequency data over a long period of time, and by a close and detailed comparison of the life-history strategies of these two species, will the different factors influencing their respective melanic polymorphisms be unravelled. Records of ladybird sightings and their colour patterns sent to the UK Ladybird Survey provide valuable data for addressing some of these questions.

6.5 Polymorphism in the harlequin ladybird Although there have been extensive studies of the maintenance of colour pattern variation in this species’ native range in Asia, there have only been more limited investigations in Britain and Europe. There was a significant decline in frequency of melanic alleles during the first two years of spread of the harlequin in Britain, indicating adaptation of this invasive alien ladybird to its newly invaded range. A similar pattern is seen across the wider invaded range of the harlequin ladybird, whereby f. succinea now dominates in Europe and North America (Majerus and others, 2006). There is some evidence that factors important in maintaining colour pattern variation in the 2-spot are also important in this species. For example, like 2-spots, melanic forms absorb radiation more effectively and warm up more quickly, and so probably have an advantage at lower temperatures, for example early in the season (Soares and others, 2003). There are two processes that influence the extent of the black colour on the elytra of the harlequin ladybird (Michie and others, 2010). The first is genetic polymorphism controlled by a major-effect gene with multiple alleles that switch development from f. succinea to the various melanic forms. In f. succinea the number and

Population and evolutionary biology | 69

Map 3. The frequencies of melanic, chequered (black segments), and typical (white segments) forms of the 10-spot ladybird in Britain, 1985–1987. Data from the Cambridge Ladybird Survey. (Minimum sample size 40 ladybirds.)

phenotypic plasticity: change in an individual’s behaviour, morphology or physiology induced by the environment

size of the black spots on the elytra are further modified in response to the temperature at which the ladybirds develop. Ladybirds that develop at lower temperatures have more and larger black spots as adults than ladybirds developing at higher temperatures. In Britain, comparisons of adult harlequin ladybirds that develop early and later in the year demonstrate this difference. The delicate small spots of the adults that emerge from pupae in late spring are a sharp contrast to the large black splodges of the adults that emerge in autumn. This high level of phenotypic plasticity in the colour pattern of f. succinea probably represents an adaptation to temperature. The greater amount of black in ladybirds that emerge in autumn allows them to warm up more rapidly in spring and thus to mate and reproduce more quickly at the beginning of the year (Michie and others, 2011). The advantage of more and bigger spots could be investigated through monitoring of natural populations, as f. succinea individuals clearly vary in their pattern to some extent, even at one time of year. Similarly any possible costs in winter, through greater radiation of heat by individuals with a higher proportion of black on their elytra, could be investigated through the close monitoring of mortality in overwintering aggregations. This could easily be achieved by monitoring harlequin ladybirds overwintering in the window frames of houses. Recent research has also suggested that f. succinea harlequin ladybirds with proportionally more red on the elytra (that is, smaller or fewer black spots) had higher alkaloid concentrations within the body and were thus better defended than those with more black on the elytra (Bezzerides and others, 2007). Further work is needed to test whether melanics, which have even less red on their elytra, are even less well defended than the nonmelanic form, but the possibility exists that there is a trade-off between repellency or toxicity and thermal melanism. This requires further investigation. It would, for example, be interesting to know whether predators of ladybirds, such as ants, find melanic ladybirds less repellent than non-melanic ones, or even whether repellency in f. succinea varies in ladybirds emerging at different times of year, as might be expected given this form’s temperature-related phenotypic plasticity.

6.6 Evolutionary relationships It is generally accepted that members of the ladybird

70 | Ladybirds

phylogeny: an evolutionary tree, showing the pattern of relationships between organisms phylogenetic: based on the closeness of evolutionary descent taxonomy: the classification of living things into species and groups (taxa)

family (Coccinellidae) are monophyletic, that is that they are a complete group of descendants of a single common ancestor. However, within this group, how are all the different species of ladybird related to each other? A related question is how members of the Coccinellidae should be grouped or classified within the family, in subfamilies, tribes and genera, for example. It is generally considered desirable that these groupings should reflect the relatedness of the different species to each other (‘phylogenetic classification’ or ‘phylogenetic taxonomy’), although this is not always carried out in practice. A phylogenetic classification of the family Coccinellidae would involve placing closely related species together in genera, closely related genera in tribes and closely related tribes in the subfamilies that make up the whole family Coccinellidae. To study evolutionary relationships, the presence/ absence or type of particular characters need to be compared. They could involve almost any aspect of biology, be it behavioural, biochemical, anatomical or morphological, but the characters used for studying relationships have to be chosen carefully. They must vary enough so that there are differences between species or groups. It is also useful if the characters are easily studied. Mouthpart morphology has often been used in the study of insect evolutionary patterns, but this character is of limited use in the ladybirds because the divergence that exists seems to reflect diet rather than evolutionary history. Carnivorous species have mouthparts that are quite different from those of the mildew feeders and the herbivorous 24-spot and bryony ladybirds. The similarities in the mouthparts of the carnivorous species are probably examples of convergent evolution, rather than a reflection of close evolutionary relationships. They resemble one another not because they have recently diverged but because they have the same function. At the other extreme, highly variable characters, such as colour patterns in ladybirds, are of little value in phylogenetic studies. New patterns emerge through simple genetic changes, so that a diverse range of colour patterns may occur in a single species. In addition, apparently similar colour patterns occur in distantly related species, possibly through mimicry (see above). When using morphological characters, those most often used in phylogenetic studies of ladybirds are the genitalia. They are useful because they are highly variable through the group, each species having a unique

Population and evolutionary biology | 71

paramere

basal lobe basal piece

sipho

Fig. 32. Male genitalia.

DNA (deoxyribonucleic acid): a long chain molecule that forms the basic hereditary material of cells. It is made of four base types (adenine, thymine, cytosine and guanine) also called nucleotides; their order on the chain determines the genetic sequence chromosomes: small elongated bodies, consisting largely of DNA, in the nuclei of most cells, existing generally in a definite number of pairs for each species, and generally accepted to be the carriers of hereditary qualities sister-group: a taxonomic group more closely related to the group in question than any other group

apparatus, and because distinct trends are evident. One example of this is seen in the sipho, the part of the male genitalia inserted into the female during copulation. In primitive members of the tribe Coccinellini, a part of the subfamily Coccinellinae, the siphonal tube is short, thick and simple, and ends in a point. There are no examples of this type among the British fauna, but in the larch ladybird the sipho is short and pointed, the only elaboration being an enlargement towards the middle and grooving along its length. In more advanced members of the group, the sipho is longer and more complex, often ending in a bulb, and the tube is often elaborately grooved and may bear flagella or other protuberances. Nowadays, the characters most often used to reconstruct phylogenies are molecular in nature; it is now possible to sequence the order of bases (nucleotides) in strands of DNA. This is the material of which genes are made and which passes from one generation to the next. Differences in the sequence of nucleic acid bases along the DNA molecule can be used to determine the closeness of the relationship between a number of species. Such differences arise at a relatively constant rate through mutation and so the DNA of very closely related species will differ little and that of more distantly related species will differ more. New molecular techniques allow very rapid sequencing of DNA, and, although this requires expensive and sophisticated equipment, the potential of using such tools is great. Since the advent of such technology, traditional views about the phylogeny of ladybirds, based on morphology, are being readdressed. Recent studies using DNA sequences have made it clear that current taxonomy (for example, seen in table 1, chapter 1) is not fully phylogenetic and poorly reflects the evolutionary relationships within the ladybirds (Giorgi and others, 2009; Magro and others, 2010). Many of the traditionally recognised ladybird subfamilies are in fact polyphyletic. This means that not all the members of the subfamily are a complete group of descendants from a single common ancestor. They are split between two or more lineages on the phylogenetic tree, as can be seen for the Coccidulinae, Epilachninae, Scymninae and Chilocorinae in pl. 1. It therefore seems that the system for ladybird classification needs revision if it is to fully reflect the phylogenetic groupings of the species. Phylogenies can also be used to study the evolutionary histories of particular traits. A good example

72 | Ladybirds

Fig. 33. Hybrid progeny from a cross between a chequered 10-spot and a weak annulata 2-spot, with markings similar to those of a 2-spot ladybird.

of this is the study of feeding preferences in the family Coccinellidae. We can ask what the original (ancestral) feeding preference of the Coccinellidae was and how many times particular feeding habits have evolved. Both Giorgi and others (2009) and Magro and others (2010) have used their DNA-sequence-based phylogenies to investigate the evolutionary history of coccinellid feeding habits. Both studies found feeding on coccids to be the original state and that other feeding strategies evolved from this (pl. 1). Giorgi and others (2009) found that a preference for eating aphids had evolved from other feeding preferences three times within the Coccinellidae and a preference for eating leaves had evolved from other feeding habits twice, while mycophagy (fungus-feeding) evolved from aphidophagy. The different hierarchical groupings used to classify species, such as subfamilies and genera, are essentially based on arbitrary decisions regarding the rank to be assigned to each group. Named ranks are used for convenience to produce some order out of the chaos of the millions of different species that inhabit the earth today and the millions more that have existed in the past but are now extinct. The one exception is the species. There have been many definitions of a species. One of the most sensible and commonly used is that a species consists of actually or potentially interbreeding groups of organisms, which are reproductively isolated from other such groups (Mayr, 1963). This means not only that individuals of a species must have the capacity to mate with one another, producing offspring that also have this capacity, but also that matings between individuals of different species should not produce viable and fertile offspring. The definition of species holds good for most sexually reproducing organisms. However, evolution is a dynamic process, and problems may arise with this definition in the case of groups that are undergoing, or have recently undergone, speciation. In such cases, the courtship and mating cues in different species may be similar enough to allow occasional hybrid matings. The occurrence of such hybrid matings in the wild usually suggests that the species involved have only recently diverged. Studies of the occurrence and results of hybrid matings can be informative. We ourselves have observed only a few types of hybrid mating in the wild, between 2-spot and 10-spot, 2-spot and harlequin, 7-spot and 11-spot, 5-spot and 7-spot, pine and 7-spot, and pine and

Population and evolutionary biology | 73

Fig. 34. Hybrid progeny from a cross between a chequered 10-spot and a weak annulata 2-spot, with markings similar to a 10-spot ladybird.

Fig. 35. Hybrid progeny from a cross between a chequered 10-spot and a weak annulata 2-spot, with unique markings.

Fig. 36. Hybrid progeny from a cross between a melanic 10-spot and a quadrimaculata 2-spot, with unique markings.

heather (Majerus, 1997). The most unusual wild hybrid mating we have recorded involved a beetle that was not even a ladybird: a small male chrysomelid (leaf-eating) beetle was observed mating with a female 2-spot (M.O. Ransford and others, personal observation). It is interesting that in most cases, matings involve presumed close relatives, that is 2-spot and 10-spot; 5-spot, 7-spot, and 11-spot (all members of the genus Coccinella); pine and heather (both close relatives in the tribe Chilocorini, part of the subfamily Chilocorinae). Virtually all such matings do not produce any viable offspring (Majerus, 1997). However the situation is slightly different in the commonest type of mating which is observed, between 2- and 10-spot ladybirds (Ireland and others, 1986). The number of eggs laid by females after such matings is relatively normal, but most of the eggs fail to hatch, as occurs with other hybrid matings. However a few do. The larvae develop fairly normally and produce offspring, some of which are similar in appearance to 2-spots (fig. 33), others to 10-spots (fig. 34), and some of which have a unique pattern (figs. 35 and 36). All of these progeny of hybrid matings have been sterile. Examination of the hybrids has shown various reasons for their sterility. For example, of four sterile males examined, in one the testes were malformed, in a second there appeared to be no sperm formation, and in the other two the chromosomes behaved aberrantly during sperm formation so that chromosome breakages, and univalent (unpaired) chromosomes, were common. It thus seems that even though the two species can produce a few hybrid offspring, the hybrids are not viable. The fact that the 2-spot and 10-spot ladybirds will hybridise and produce viable offspring supports the view that they are closely related, and suggests that their divergence is comparatively recent. However, the fact that the hybrid progeny are sterile confirms the view that they are distinct species.

Plate 1 The revised phylogeny of the Coccinellidae based on comparisons of DNA sequences (adapted from Magro and others, 2010)

Plate 2 Spread of the harlequin ladybird in Britain and Ireland. The coloured dots indicate 10km squares in which the harlequin ladybird has been recorded in different time periods from arrival in 2003 to present. 2003-2004 2005-2006 2007-2008 2009-2010

Plate 3 1.

Harmonia axyridis (f. conspicua) Harlequin ladybird

2.

Harmonia axyridis (f. spectabilis) Harlequin ladybird

3.

Harmonia axyridis (f. succinea) Harlequin ladybird

4.

Harmonia axyridis (f. axyridis) Harlequin ladybird

1

2

3

4

Plate 4 1.

Coccinella 7-punctata 7-spot ladybird

2.

Coccinella magnifica Scarce 7-spot ladybird

3.

Coccinella 5-punctata 5-spot ladybird

4.

Anatis ocellata Eyed ladybird

5.

Anatis ocellata Eyed ladybird

6.

Henosepilachna argus Bryony ladybird

7.

Myzia oblongoguttata Striped ladybird

8.

Harmonia 4-punctata Cream-streaked ladybird

9.

Harmonia 4-punctata Cream-streaked ladybird

2

1

3

4

6

5

7

8

9

Plate 5 1.

Calvia 14-guttata Cream-spot ladybird

2.

Myrrha 18-guttata 18-spot ladybird

3.

Hippodamia 13-punctata 13-spot ladybird

4.

Subcoccinella 24-punctata 24-spot ladybird

5.

Subcoccinella 24-punctata 24-spot ladybird

6.

Coccinella 11-punctata 11-spot ladybird

7.

Adalia 2-punctata (f. typica) 2-spot ladybird (typical)

8.

Adalia 2-punctata (f. quadrimaculata) 2-spot ladybird (melanic)

9.

2

1

3

4

5

6

Hippodamia variegata Adonis’ ladybird

10. Adalia 10-punctata (f. decempunctata) 10-spot ladybird (typical)

7

11. Adalia 10-punctata (f. decempustulata) 10-spot ladybird (chequered) 12. Adalia 10-punctata (f. bimaculata) 10-spot ladybird (melanic)

8

9

10

11

12

Plate 6 1.

Propylea 14-punctata 14-spot ladybird

2.

Propylea 14-punctata 14-spot ladybird

3.

Psyllobora 22-punctata 22-spot ladybird

4.

Anisosticta 19-punctata Water ladybird

5.

Tytthaspis 16-punctata 16-spot ladybird

6.

Halyzia 16-guttata Orange ladybird

7.

Coccinella hieroglyphica (f. typica) Hieroglyphic ladybird (typical)

8.

Coccinella hieroglyphica (f. areata) Hieroglyphic ladybird (melanic)

9.

Aphidecta obliterata Larch ladybird

10. Chilocorus renipustulatus Kidney-spot ladybird

1

2

3

4

5

6

7

8

11. Chilocorus 2-pustulatus Heather ladybird 9

12. Exochomus 4-pustulatus Pine ladybird

11 10

12

Plate 7 1.

Coccinella septempunctata 7-spot ladybird fourth-instar larva

2.

Coccinella septempunctata 7-spot ladybird pupa

3.

Harmonia axyridis Harlequin ladybird fourthinstar larva

4.

Halyzia 16-guttata Orange ladybird fourth-instar larva

5.

Exochomus 4-pustulata Pine ladybird fourth-instar larva

6.

Subcoccinella 24-punctata 24-spot ladybird fourth-instar larva

1

2

3

5

4

6

Plate 8 Pigment development in the 2-spot ladybird (Adalia 2-punctata) 1–3: f. typica 4–9: f. sexpustulata Shown at various times after emergence from the pupa 1.

30 minutes

2.

12 hours

3.

48 hours

4.

30 minutes

5.

1 hour

6.

3 hours

7.

12 hours

8.

24 hours

9.

48 hours

1

2

3

4

5

6

7

8

9

Plate 9 Forms of the 2-spot ladybird 1.

sublunata

2.

sexpustulata

3.

weak annulata

4.

bar annulata

5.

intermediate annulata

6.

extreme annulata

7.

duodecempustulata

8.

new duodecempustulata

9.

spotty

10. strong spotty 11. sexpustulata spotty 12. melanic annulata

Plate 10 Varieties of some British ladybirds 1.

Eyed ladybird lacking cream rings

2.

Eyed ladybird spots lacking black centres

3.

7-spot ladybird miniature spotted

4.

Striped ladybird dark pronotal mark and additional stripes

5.

Cream-streaked ladybird melanic

6.

Larch ladybird boldly marked

7.

Adonis’ ladybird 13 spotted

8.

Adonis’ ladybird 5 spotted

9.

10-spot ladybird typical form with no elytra spots

10. 10-spot ladybird form duodecempunctata 11. 10-spot ladybird abnormally heavily marked chequered form 12. Hieroglyphic ladybird intermediate melanic

Plate 11 1.

Rhyzobius litura

2.

Coccidula rufa

3.

Coccidula scutellata

4.

Hyperaspis pseudopustulata

5.

Scymnus frontalis

6.

Scymnus auritus

7.

Platynaspis luteorubra

8.

Vibidia 12-guttata

9.

Exochomus nigromaculatus

10. Calvia 10-guttata 11. Procula douei 12. Cryptolaemus montrouzieri

Plate 12 Immature stages of ladybirds: eggs, larvae and pupae

1.

7-spot ladybird

2.

Eyed ladybird

3.

Pine ladybird

7 Ladybird distribution 7.1 Present residents in Britain Running for over forty years, the Coccinellidae Recording Scheme (now called the UK Ladybird Survey - www.ladybird-survey.org) collates distribution data for ladybird species in Britain. Further details of the UK Ladybird Survey are given in chapter 9. This and over eighty other recording schemes are supported by the NERC Centre for Ecology & Hydrology (Biological Records Centre funded by JNCC and NERC). Increased interest in ladybirds has led to an upsurge in species records in recent years, culminating in 2011 with the publication of an atlas of the ladybirds of Britain and Ireland (Roy and others, 2011). Distribution maps were produced from records of ladybird species presence in 10km squares throughout Britain and Ireland. Distribution maps may show biases caused by an uneven spread of recorders throughout Britain and Ireland. Generally, more records are sent from areas where more people live! Nonetheless, it is fair to say that the south-east of England is the most species-rich part of Britain for ladybirds. Both the species diversity and the population density of ladybirds appear to drop away to the west and north. However, many species have a wide distribution, so even in the Highlands of Scotland about half of the British ladybird species are found. Despite increased recording levels, targeted surveys can reveal exciting results, particularly in under-recorded areas. Apparent gaps in species distributions may simply be due to the fact that ladybirds have not been looked for in particular areas, or that they have been considered too common to be worthy of note. Thus it can be relatively easy to add new 10km square records. Distribution trends in the data for UK ladybirds were derived (Roy and others, 2011), revealing that ten species declined over the period 1990 to 2010, whilst five species showed an increase (table 11). The remaining 31 species were stable. Many of the declining ladybirds were common generalist species; conversely most of the rarer species appeared to be stable. This is in contrast to UK butterfly data, where the rarer specialised species tended to have a declining long-term trend, whilst commoner species fared better (Botham and others, 2009).

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Table 11. General distribution status of British ladybirds based on UK Ladybird Survey data (listed in order of decreasing number of UK Ladybird Survey 10km square records). Adapted from Roy and others (2011)

Species

UK distribution Distribution notes trend (1990– 2010)

7-spot ladybird

Stable

Widespread

10-spot ladybird

Decreasing

Widespread

14-spot ladybird

Decreasing

2-spot ladybird

Stable*

Harlequin ladybird

Increasing

Cream-spot ladybird

Decreasing

Widespread. Less common in the north and uncommon in Scotland Widespread. Less common in the north and uncommon in Scotland Widespread in England and Wales. Rare in Scotland, but spreading Widespread

11-spot ladybird

Decreasing

Coccidula rufa

Decreasing

22-spot ladybird

Decreasing

Orange ladybird

Increasing

Widespread. Less common in the north and uncommon in Scotland Widespread

Rhyzobius litura

Decreasing

Widespread

Pine ladybird

Increasing

Kidney-spot ladybird

Stable

24-spot ladybird

Increasing

16-spot ladybird

Stable

Larch ladybird

Stable

Widespread. Less common in the north and uncommon in Scotland Widespread in England and Wales. Single recent record from Scotland Widespread in southern and central England and in Wales. Largely coastal in western Britain. Rare in Scotland Widespread in southern and central England. Largely absent from northern England and from Scotland Widespread

Eyed ladybird

Stable

Widespread

Water ladybird

Decreasing

Adonis’ ladybird

Stable

Cream-streaked ladybird

Stable

Widespread and locally common in England and Wales. Single recent record from Scotland Widespread in eastern and central England. Rare elsewhere but apparently spreading northwards Widespread in southern and central England and Wales

Scymnus suturalis

Stable

Widespread

18-spot ladybird

Stable

Widespread and locally common

Scymnus auritus

Stable

Hieroglyphic ladybird

Decreasing

Widespread throughout England and east Wales. Very rare in Scotland Widespread and locally common

Commonest near coasts, but in England also widely distributed inland Widespread and locally common throughout Britain

* but decreasing since arrival of harlequin ladybird

76 | Ladybirds Table 11. Continued.

Species

UK distribution Distribution notes trend (1990– 2010)

Nephus redtenbacheri

Decreasing

Widespread and locally common

Heather ladybird

Stable

Locally common in southern Britain. First records from Scotland recently

Striped ladybird

Stable

Widespread and locally common

Scymnus haemorrhoidalis

Stable

Widespread in southern and central England, rarer to the north and west. Not recorded from Scotland

Scymnus frontalis

Stable

Southern and central England, and on coasts from Merseyside south around to Humberside. Absent from Scotland

Coccidula scutellata

Stable

Widespread in England. Few records from Wales and none from Scotland

Hyperaspis pseudopustulata Stable

Widespread and locally common

Scymnus femoralis

Widespread in south-eastern & central England. Few records from elsewhere

Stable

Stethorus punctillum

Stable

Widespread in southern and central England

Scymnus schmidti

Stable

Widespread but local in southern England. Also recorded from some western coasts

Scymnus nigrinus

Stable

Widespread

Scarce 7-spot ladybird

Stable

Largely restricted to southern England

Platynaspis luteorubra

Stable

Largely restricted to south-eastern England

Scymnus limbatus

Stable

Largely confi ned to southern and central England

Nephus quadrimaculatus

Stable

Largely confined to south-eastern England and East Anglia

Rhyzobius chrysomeloides

Increasing

Largely restricted to south-eastern England, spreading after establishment in 1997. Absent from Wales and Scotland

5-spot ladybird

Stable

Restricted to Wales and northern Scotland

13-spot ladybird

Stable

Extremely rare. A few recent records from southern coast of England, including a single larval record

Bryony ladybird

Stable

Locally common around London and recently established in Oxfordshire. Absent elsewhere but possibly spreading

Clitostethus arcuatus

Stable

Rare in southern and central England

Scymnus interruptus

Stable

Sparse records from south-eastern England, one from the north-west coast. Absent elsewhere. May not be native

Rhyzobius lophanthae

Stable

Occasional outdoor populations in London. Unlikely to regularly overwinter successfully outside

–

Only three known British specimens, all from the southeastern coast. May not be resident

Nephus bisignatus

UK distribution trend (1990–2010): statistically significant trends - see Roy and others (2011) for details of how these were calculated. Distribution notes: General pattern of UK distribution, based on Roy and others (2011). ‘Widespread’ does not necessarily imply common and abundant (some less abundant species have a wide distribution).

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Whilst the distribution trends as in table 11 were carefully calculated, the extent of the decline in the ladybird fauna of Britain is difficult to assess from a historical perspective. This is partly because of natural fluctuations in ladybird populations and partly because of the paucity of specific data on ladybird abundance and distribution until recent times. There is little information available on the main causes of declines in ladybirds in recent decades but habitat loss and changes in land use (such as intensification of agriculture) are possible contributors. The increasing prevalence of non-native plants, including the use of fast-growing imported species of conifer in place of Scots pine as timber plantation trees, could also be a contributing factor. There is considerable scope for looking into these drivers of change in more detail through empirical studies. A recent study used the long-term large-scale distribution data collated through the UK Ladybird Survey and the Belgian equivalent (Coccinula Recording Scheme) to assess the effect of the harlequin ladybird on the distribution of other species of ladybird resident in Britain and Belgium (Roy and others, 2012). Seven (Britain) and five (Belgium) of eight species studied showed substantial declines attributable to the arrival of the harlequin ladybird. Indeed, the 2-spot ladybird declined by 44% (Britain) and 30% (Belgium) over five years after the arrival of the harlequin ladybird. Much can be learnt about the biology of a particular species by the study of its geographic distribution. Some ladybirds, such as the 7-spot and cream-spot, seem to be able to cope with almost any climatic conditions found in the British Isles. On the other hand, the 11-spot, which is most often found on the coast, was at one time thought to require salt. However, Benham and Muggleton (1970) showed that in south-east England it is also found inland on non-saline soils, and that its limitation to coastal areas further north seems to be due to climatic factors. Benham and Muggleton (1970) conclude that the most likely explanation of 11-spot distribution is that the species is intolerant of wet conditions, but extremely tolerant of desiccation. A similar situation may apply to Adonis’ ladybird. This species can be highly abundant in continental Europe, particularly in the south. It appears to thrive in dry conditions in areas with sandy soils. In Britain it is most easily found in late summer on weedy dry land with patches of bare ground. Adonis’ ladybird may be a species that will increase in Britain due to

78 | Ladybirds

global warming. The precise distributions of many species are determined by their habitat or host plant preferences, many of which have been described in chapter 3.1. For example, although the larch ladybird is described as a widespread species, it is found almost exclusively on conifers, so the precise distribution is determined by the distribution of conifers. The same is true for many other species. The heather ladybird is a heather specialist, and is widespread on heathland in southern England. However, presumably for climatic reasons it is rarely found in Scotland and so overall is classed as local. The orange ladybird is a mildew-feeding species and one of the five species that show an increasing trend (fig. 39). Formerly thought to be restricted to sycamore and ash, in recent years it has been found feeding on an increasing range of deciduous trees, including birch, field maple and dogwood. Table 11 should be used in conjunction with table 3 on habitat preferences. Some species that are common and fairly generalist in central Europe are rare and much more specialised in Britain and north-west Europe. One example is the 5-spot ladybird, which in central Europe occupies a variety of habitats, but in Britain seems restricted to shingles on the banks of fast-flowing rivers (fig. 37). This species was thought to have become extinct in Britain and until 1987 had only been recorded in two 10 km squares in England, and two in Scotland. However, the 5-spot was discovered in west Wales in 1987, thriving on the unstable river shingle on the banks of the Afon Tywi, the Afon Ystwyth and the Afon Rheidol. Also in 1987, the 5-spot was recorded from the Spey Valley in Scotland, close to a site where it had been recorded earlier, in 1953. Again it was found on shingle and the species had probably been present at suitable sites along the Spey Valley throughout the intervening period. The species is still found in these areas and can be locally abundant in its specialised habitat. The 13-spot ladybird is a common species in mainland Europe but until recently was thought to be extinct in Britain, with no records received over a period of about fifty years (fig. 38). A handful of records in the last few years, mainly on the south coast of England, suggest that the species may be re-colonising from Europe. Indeed in July 2011 a 13-spot larva was found in Devon (Comont and Willerton, 2012), representing the first confirmed

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breeding record of the species in Britain (although the species seems also to be established in central Ireland). The distributions of ladybirds are not static, but change from year to year due to changes in the environment, habitat destruction, and changes in aphid populations. In addition, occasionally new species are recorded in Britain and if the climate is suitable and appropriate habitat is available, these may become established. An interesting comparison can be made between two closely related recent arrivals – the cream-streaked ladybird and the harlequin ladybird. We regard the cream-streaked ladybird as a native species, which has expanded its native range northwards within Europe, and which is assumed to have reached Britain by natural means (Majerus, 1994). The cream-streaked was first recorded in Britain in West Suffolk (East Anglia) in 1937 (Morley, 1941; Hawkins, 2000), and the evidence based on the earliest records for each vice county indicates that it took fifty years to spread west as far as Devon (fig. 40). It is not considered invasive. In contrast, the harlequin ladybird took just three years to spread to Devon from a similar starting point (Brown and others, 2008; fig. 41, pl. 2). The cream-streaked ladybird is a conifer specialist and is therefore more habitat-specific than the harlequin ladybird, and the mechanisms of spread of the two species are unlikely to be the same – the harlequin ladybird has inadvertently been aided by people, arriving with goods and produce as well as of its own accord by flight across the English Channel. Nevertheless, the seventeen-fold difference in spread rate between the two species is striking. Another recent arrival is the bryony ladybird. This herbivorous species seems restricted to its preferred food plant, white bryony. It was not recorded in Britain until 1997, when it was found in Surrey (Menzies and Spooner, 2000). It has spread very slowly, with most records of the species being from around the London area; however in 2010 it was reported in Oxfordshire for the first time (fig. 42). A warmth-loving species, the northward spread of the bryony ladybird in Europe has been linked to recent changes in climate.

80 | Ladybirds Fig. 37 Distribution of the 5-spot ladybird. (Source: UK Ladybird Survey, Biological Records Centre within the NERC Centre for Ecology & Hydrology)

Fig. 38 Distribution of the 13-spot ladybird. (Source: UK Ladybird Survey, Biological Records Centre within the NERC Centre for Ecology & Hydrology)

1800-1986 1987-Present

1800-1950 1951-2000 2001-Present

Ladybird distribution Pre 1990 Pre and Post 1990 Post 1990

1930-1959 1960-1989 1990-Present

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81

Fig. 39 Distribution of the orange ladybird. (Source: UK Ladybird Survey, Biological Records Centre within the NERC Centre for Ecology & Hydrology)

Fig. 40 Distribution of the cream-streaked ladybird. (Source: UK Ladybird Survey, Biological Records Centre within the NERC Centre for Ecology & Hydrology)

82 | Ladybirds Fig. 41 Distribution of the harlequin ladybird. (Source: UK Ladybird Survey, Biological Records Centre within the NERC Centre for Ecology & Hydrology)

Fig. 42. Distribution of the bryony ladybird. (Source: UK Ladybird Survey, Biological Records Centre within the NERC Centre for Ecology & Hydrology)

2003-2005 2006-2008 2009-Present

1997-1999 2000-2002 2003-Present

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7.2 Occasional species The majority of new species of ladybird found in Britain are vagrants, probably imported accidentally by people. Many have been tropical species found near ports, and it is suspected that most arrived on cargo ships. The largest group of such vagrants is a series of species housed in the Stevens Collection, in the Natural History Museum (London). They were collected between 1815 and 1845, mostly in the Bristol area. There were similar records of vagrants in the 20th century. For example, in the 1920s a specimen of a Jamaican species, Procula douei (pl. 11.11), was found in the New Forest, about 20km from Southampton. In recent years the African species Cheilomenes lunata has been recorded from time to time, usually originating from imported grapes (Mabbott, 2005). Not all records can so easily be put down to accidental human-assisted importations. In 1927, a specimen of Calvia 10-guttata (pl. 11.10) was recorded at Killarney in Ireland. This large orange ladybird with pale spots had been recorded once before, in the west of England some time before 1861. From time to time climatic conditions are such that insects are carried, more or less passively, for vast distances. Large quantities of sand and soil, sucked up from North Africa by the wind, have sometimes been deposited on northern Europe, including Britain. On some of these occasions, beetles and other insects have been carried along by the wind with the sand and soil. Similarly, Britain is occasionally visited by species of insect from America, carried across the Atlantic by the prevailing south-westerly winds. The best known example of this is the Monarch butterfly (Danaus plexippus). It is therefore not impossible that natural forces may occasionally bring foreign species of ladybird to Britain. The records of Calvia 10-guttata, a continental European species, may fall into this category. So may records of two other species. One is Vibidia 12-guttata (pl. 11.8) which has from time to time been included in the British list on the strength of just a handful of records. This small orange ladybird has white spots, and is a mildew feeder usually found on deciduous trees. It is common in Europe and the occasional British records are probably natural migrants. The other is Exochomus nigromaculatus (pl. 11.9), a single specimen of which was found in September 1967, near Rossington Bridge on the outskirts of Doncaster (Skidmore, 1985). This heathland

84 | Ladybirds

species resembles the other British Chilocorini in shape, but is immediately distinguished by the wholly black elytra and broad yellow side margins of the pronotum. Stephens (1831–2) recorded two British specimens, one captured near Windsor in June 1816, the other taken near Bristol. The absence of any further records until 1967 led to the omission of the species from all lists of British Coccinellidae apart from that of Donisthorpe (1939). Not all records of ladybirds that are considered nonnative can be classed as accidental vagrants. The potential use of ladybirds in controlling aphids and other plant pests has resulted in the intentional import of non-native ladybirds into Britain. Although stringent measures are taken to ensure that such imports do not escape, some escapes undoubtedly do occur, and at least three Australian species have been recorded in the wild in Britain as a result. The first, Cryptolaemus montrouzieri (pl. 11.12), has origins that are certainly accounted for in this way. This species has been used successfully in many parts of the world to control mealy bugs or mealy aphids. It is bred in this country for greenhouse use, and is available commercially. The second is the steelblue ladybird Halmus chalybeus, which was recorded in London in June 2009. The third, Rhyzobius lophanthae, a tiny black ladybird, has become established and has been added to the latest British checklist (Duff, 2008); it has been recorded breeding outdoors in several parts of London (Barclay, 2007). Climate warming may lead to establishment of further species such as these in parts of Britain with milder winters. Many species of ladybird that occur in continental Europe are absent from Britain. One is Oenopia conglobata, a pink ladybird common on trees as close to Britain as coastal Belgium and France. It is quite possible that this and others will one day be transported across the English Channel or North Sea and become established in Britain, much as the cream-streaked ladybird has done over the last 75 years.

8 Identification of British ladybirds 8.1 Introduction to keys This chapter consists of three keys, two for the identification of adult ladybirds, and one for their larvae. Most ladybirds should be identifiable in the field, using the colour plates in this book and the field key (key I), so that they can be released again where they are found. Key I does not cover some of the unusual colour forms, or the smaller coccinellids which can be identified using key II. Some of the characters used in key II will only be visible under a dissecting microscope; however, we have avoided using characters that make it necessary to kill the beetles, and hope that whenever possible the insects are returned to the site of collection after a definite identification has been made, and clarified by an expert where appropriate. Key III is for the identification of final-instar ladybird larvae*. All these keys have been constructed using live material rather than dead specimens. Some keys to adults and larvae already exist, and our choice of distinguishing characteristics owes a lot to these previous keys, which we wish to acknowledge. They are Joy (1932), van Emden (1949), Pope (1953), Pope (1973), Hodek (1973), and Moon (1986).

I: Field key to adult British ladybirds This key covers only the 26 species of coccinellid that we refer to as ladybirds (see table 1). It uses only characters easily seen in the field, and therefore it cannot include all forms of every ladybird species in Britain. However, it covers all but a few rare variants, and should permit identification of more than 99% of ladybirds observed in the field. We suggest that this key is used for field identification in conjunction with the colour plates (plates 3–6), which show the most usual forms of all the British ladybirds, and the black-and-white plates (plates 9 and 11), which * Identification charts equivalent to keys I & III of this book, and including details of habitat preferences, overwintering sites, and hints to help with identification, are available from the Field Studies Council, www.field-studies-council.org.

86 | Ladybirds

illustrate some pattern varieties of the 2-spot ladybird and some of the commoner forms of other species. Specimens should first be compared with the plates. Then the field key should be used to check identifications made using the plates, or to name species in cases where comparisons with plates do not give a definite identification. If a specimen cannot be identified using this key, first check that it is a coccinellid using the basic diagnostic features of the group, particularly the leg segments (see key II). If it is indeed a coccinellid, use key II. If an identification still cannot be made, we suggest that the specimen be referred to the UK Ladybird Survey (www. ladybird-survey.org, see chapter 9), or to the Natural History Museum (London). As outlined in Chapter 5 there are five main components of the colour patterns: ground colour, colour of markings, number of spots, strength (contrast) of spots, and fusions between the spots. All these components show variation in some species. Ground colour refers to the background colouration on which the markings are evident. This field key may not be much help with recently-emerged adults which are still pale because the pigments have not been fully laid down. However, size and the pronotum marks may allow an identification to be made before the elytral pigments darken. A hand lens (10) and a ruler are useful for some parts of this key. The parts of a ladybird are named in II.1 and II.2 (p. 95). 1

Upper surfaces covered in fine hairs (sometimes visible with the naked eye, but often only with a hand lens). (Elytra and pronotum a uniform dirty or brownish red, with black spots) 2

-

Upper surfaces not hairy

2

(1) Large (5–7mm), with a scutellary spot and 5 black spots on each elytron (pl. 4.6)

3

bryony ladybird (Henosepilachna argus) -

Small (3–4mm), with no scutellary spot and 0–12 black spots on each elytron (usually 10 although spot fusions are common) (pl. 5.4 and 5.5) 24-spot ladybird (Subcoccinella 24-punctata)

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3

(1) Ground colour of elytra not black

4

-

Ground colour of elytra black

7

4

(3) With elytral marks

5

–

No elytral marks

5

(4) Main elytral marks darker than the ground colour

–

Main elytral marks paler than the ground colour

34

6

(5) Ground colour of elytra bright orange or red

16

–

Ground colour of elytra some other colour (e.g. yellow, pink, brown)

25

7

(3) With pale (yellow, orange or red) marks touching the edges of the elytra

8

–

Marks not touching the edges of the elytra, or no paler elytral marks

10

14

6

8

(7) White flashes on the front of the elytra (either side of the scutellum). White on pronotum front corners triangular in shape (pl. 6.8)

–

No white marks on the front edge of the elytra. White marks on the pronotum not triangular

hieroglyphic ladybird (Coccinella hieroglyphica)

I.1

9

9

(8) Legs and underside of abdomen black. (Marks variable but usually with 1, 2, or 3 red or reddish orange spots on each elytron. If one spot, always at front angle touching the side margin (pl. 9.1); second spot (if present) round and central (pl. 5.8); third spot (if present) at hind tip) (pl. 9.2) 2-spot ladybird (Adalia 2-punctata)

–

Legs brown, underside of abdomen orange or yellow; end of abdomen usually brown or orange. (Forward angle mark curved, extending to margin, and widening towards margin (I.1). Marks red, orange or yellow) (pl. 5.12) 10-spot ladybird (Adalia 10-punctata)

88 | Ladybirds

10 (7) Marks form a thin red band or row of 3 (occasionally 2 or 4) small spots across middle of elytron (I.2). (Body highly domed with lip around sides) (pl. 6.11) heather ladybird (Chilocorus 2-pustulatus) –

Marks not lined up in a row across the elytra. Either a single spot on each elytron or 2 lined up one behind the other 11

I.2 11 (10) One large red/orange mark on each elytron

12

Two large red/orange marks on each elytron

13

–

12 (11) White marks on the pronotum, usually at the sides. Elytral mark slightly forward of centre, may be round, curved or a ring. Legs brown (pl. 3.1) harlequin ladybird (Harmonia axyridis) – I.3

Pronotum entirely black. Single large bright red or orange spot centrally on each elytron (I.3). Legs black. (Body almost circular with definite lip at edge) (pl. 6.10) kidney-spot ladybird (Chilocorus renipustulatus)

13 (11) White marks on the pronotum, usually at the sides. Forward mark slightly forward of centre, may be round, curved or a ring. Rear mark just behind centre, usually round. Legs brown (pl. 3.2) harlequin ladybird (Harmonia axyridis) – I.4

I.5

14 (4) Length 5–8.5 mm. Pronotum marks M-shaped, black, usually one continuous mark but sometimes split into two, occasionally into four (I.5). (Elytra sometimes show faint or weak spots) on each elytron and an additional scutellary spot, but spot fusions are common. Elytra usually with a distinct transverse fold (keel) at rear, just before the tip (I.6)) (pl. 3.3) harlequin ladybird (Harmonia axyridis) –

I.6

Pronotum entirely black. Forward mark curved (thicker at rear than at front) and just in from the marginal lip (I. 4). Second mark round, just behind centre (pl 6.12) Almost circular, with a definite lip around the edge of elytra pine ladybird (Exochomus 4-pustulatus)

Length