Ladybirds

HELEN E. ROY, PETER M.J. BROWN, RICHARD F. COMONT, REMY L. POLAND AND JOHN J. SLOGGETT
revised from MAJERUS & KEARNS (1989)

With illustrations by Sophie Allington & Chris Shields

UBLISHING

ELAGIC

PELAGIC
PUBLISHING

Naturalists Handbooks 10 Ecology and identification

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 2 3 4 5 6 7 8 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Life history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Ladybirds in their environment . . . . . . . . . . . . . . . . . . . . . 15 Ladybirds and their natural enemies . . . . . . . . . . . . . . . . . 30 Variation in ladybirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42 Population and evolutionary biology. . . . . . . . . . . . . . . . . 56 Ladybird distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74 Identication 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

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 aect 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 uid called reex 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 suer 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 nd ladybirds quite acceptable, and are not deterred by the reex 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 ying 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 benets 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 benecial 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 y away or clamp down onto the substrate (if this is a at 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 ladybirds 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 ladybirds 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 o by the ants.

4.2 Parasitoids and parasites of ladybirds

Hymenoptera: the insect order that includes bees, wasps, ants and sawies

Organisms known to parasitise ladybirds in Britain include ies (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. Parasitoid flies Among the true ies, or Diptera, the commonest species of endoparasite (parasites that develop inside the host) belong to the genus Phalacrotophora (the phorid 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 wings trailing edge. Identi cation of these ies to a species level is tricky and for conclusive identication 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 rst 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 diculties with their identication. It is possible to carefully collect ladybird pupae and monitor them for emergence of either a ladybird adult or phorid ies. 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 dierent

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

ovipositor: the egg-laying apparatus of a female insect

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 conrmation. 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 hosts head. The rst sign of the eects of these parasites on ladybird pupae taken into the laboratory is usually the appearance of the dark red-brown, strongly segmented puparia (g. 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 harlequins 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) (g. 23). Most records on the parasitism of ladybirds by Medina species erroneously refer to Degeeria (=Medina) luctuosa (Meigen), which is specic 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-y or bluebottle, but is 56 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) (g. 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 exed 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 ve 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 rst-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 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 (g. 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 hosts 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. aminius and H. platynaspidis, generally parasitise only small coccinellid species. Homalotylus aminius 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 rst 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 ve 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 67 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 (Sheeld 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 ll 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
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.

gametocyst: a cyst within which sex cells are produced

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 ospring. The bacteria live within the ladybirds cells, and are transferred from parents to ospring only in the egg cytoplasm. Therefore both sexes are born infected, but only the females can pass the bacteria on to their ospring so, to the bacteria, male ladybirds are a dead end. Consequently only around half the eggs laid will hatch, as the male ospring are killed as eggs. These unhatched eggs are eaten by their female siblings on hatching, increasing their tness, 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 conrmed by treatment with antibiotics. Bacteria from ve dierent groups have been identied 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 ve species are known to host them: the 2-spot, 10-spot, cream-spot, water, and Adonis ladybirds. 2-spot ladybirds are host to four dierent 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 athletes 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 scientic 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 lling 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; 1015% 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 ight, 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 specic and conned not only to single host species but to specic 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 eld 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 eects of these natural enemies. Studies needed include the percentage of individuals of dierent ladybird species that are attacked by the various species of parasite; and the eect 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 = 15 %, high >5%).

Enemy
Parasitoid ies

Ladybird hosts
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 2-spot, 10-spot*, eyed, larch, cream-spot*, kidneyspot*, scarce 7-spot*, 7-spot*, pine*, cream-streaked, harlequin, and striped ladybirds 2-spot, 10-spot, eyed, larch*, cream-spot, 7-spot*, pine*, harlequin*, Adonis*, 18-spot*, 14-spot*, and 22-spot* ladybirds

Prevalence

Phalacrotophora fasciata

High (about 10% in 7-spot populations)

Phalacrotophora berolinensis

Medium

Medina separata

Low

Parasitoid wasps 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 Heather, 7-spot, and 14-spot ladybirds Scymnus and Nephus species (inconspicuous ladybirds) Platynaspis luteorubra (an inconspicuous ladybird) 2-spot, eyed*, heather, 5-spot*, 7-spot, and harlequin ladybirds 2-spot, heather*, and pine ladybirds High (about 75% in some populations) Low Low Low Medium Low

Dinocampus coccinellae

Homalotylus eytelweini Homalotylus aminius Homalotylus platynaspidis Oomyzus scaposus Aprostocetus neglectus Parasites Mites Nematode worms Microorganisms Protozoa

2-spot, 10-spot, cream-spot, scarce 7-spot, 7-spot, 11-spot, harlequin and cream-streaked ladybirds 2-spot, 10-spot, larch, 7-spot, Adonis, and 14-spot ladybirds

Low Low

2-spot, 10-spot, 5-spot, 7-spot, pine, creamstreaked, 13-spot, Adonis, 18-spot, 14-spot, 16-spot ladybirds 2-spot, 10-spot, water, cream-spot, 7-spot, 11-spot, harlequin, cream-streaked, and Adonis ladybirds 2-spot, eyed, larch, cream-spot, scarce 7-spot, 5-spot, 7-spot, pine, cream-streaked, 14-spot, and 16-spot ladybirds 2-spot, heather, kidney-spot, 7-spot, harlequin, 14spot, and 22-spot ladybirds 7- spot and harlequin ladybirds

Low

Male-killing bacteria

Medium Low to medium (sometimes high over winter) Low Low

Pathogenic fungi

Hesperomyces sp Microsporidia

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

138 | Ladybirds

Index
Ladybirds are indexed by common names where they exist. Ladybird names beginning with numbers (e.g. 2-spot ladybird) are listed at the start of the index. Bold locators preceded by P refer to Plate numbers. Page numbers in italics refer to tables or gures.

2-spot ladybird (Adalia bipunctata) 4, 86, P5, P8, P9; breeding/rearing 120, 122, 123, 124; defence 62, 63, 64, 65; distribution 75, 77; environmental impacts 14; foods/ feeding 19, 20, 21, 22, 26; habitat 17, 18, 18; hybrid matings 72, 72, 73, 73; identication 87, 91, 103, 111; life history 5, 6, 10; mimicry 6465, 64; morphological variation 13, 53, 53, 54, 54; overwintering 6, 26, 27, 28, 29; parasites/diseases 33, 34, 35, 36, 37, 38, 39, 40; pattern/colouration 9, 9, 42, 43, 4344, 4446, 46; polymorphism 6568, 68; population size 57; predators 63; sexing 10, 11 5-spot ladybird (Coccinella quinquepunctata) 4, P4; breeding/rearing 124; distribution 76, 78, 80; foods/feeding 25; habitat 17; hybrid matings 72, 73; identication 89, 105, 111; life history 13; mimicry 64; overwintering 27, 29; parasites/diseases 35, 41; pattern/colouration 50, 51 7-spot ladybird (Coccinella septempunctata) 1, 4, 17, P4, P7, P10, P12; breeding/rearing 122123, 123, 124; defence 62, 65; development stages 6, 7, 7, 8, 9, 23; diseases 28, 39, 3940, 41; distribution 75; environmental impacts 12; foods/feeding 19, 21, 23, 26; habitat 17, 18; humans, biting 24; hybrid matings 72, 73; identication 90, 90, 105, 111; mimicry 64, 64; overwintering 26, 2728, 27, 28, 29; parasites 33, 34, 35, 35, 36, 37, 41; pattern/colouration 9, 50, 51, 5354, 53; population size 57, 5758; predators 63; wings 2 10-spot ladybird (Adalia decempunctata) 4, P5, P10; breeding/rearing 124; development stages 8; distribution 75; foods/ feeding 22, 26; habitat 15, 17; hybrid matings 72, 72, 73, 73; identication 87, 89, 91, 92, 93, 94, 103, 111; melanic form 68, 69; mimicry 64, 64; overwintering 27, 28, 29; parasites/diseases 33, 35, 38, 41; pattern/colouration 42, 4243, 44, 4748; population size 57; predators 63 11-spot ladybird (Coccinella undecimpunctata) 4, P5; breeding/rearing 124; distri-

bution 75, 77; egg laying 6; foods/feeding 26; habitat 15, 17; hybrid matings 72, 73; identication 89, 104, 111; mimicry 64; overwintering 27, 28, 29; parasites/ diseases 35, 41; pattern/colouration 50, 51; population size 57; predators 63 13-spot ladybird (Hippodamia tredecimpunctata) 4, P5; breeding/rearing 124; distribution 76, 7879, 80; environmental impacts 13; foods/feeding 25; habitat 17; identication 89, 102, 110; mimicry 64; overwintering 27; parasites/diseases 41; pattern/colouration 50, 51 14-spot ladybird (Propylea quatt uordecimpunctata) 4, P6; breeding/rearing 124; development stages 8; distribution 75; foods/feeding 25; habitat 16, 18; identication 92, 106, 109; life history 5, 6; mimicry 64; overwintering 26, 27, 28, 29; parasites/diseases 34, 35, 36, 37, 40, 41; pattern/colouration 44, 50, 51, 52, 54, 54; population size 57, 58; predators 63; sexing 10 16-spot ladybird (Tytthaspis sedecimpunctata) 4, P6; breeding/rearing 125; collecting 116; distribution 75; foods/feeding 22, 22, 25; habitat 16; identication 91, 102, 108; mimicry 64; overwintering 26, 27, 28; parasites/diseases 35, 41; pattern/colouration 50, 51 18-spot ladybird (Myrrha octodecimguttata) 4, P5; breeding/rearing 124; defence 63; distribution 75; foods/feeding 25; habitat 15, 16, 17; identication 93, 106, 110; mimicry 64; overwintering 27, 28; parasites/diseases 34, 35, 41; pattern/colouration 50, 51, 53 22-spot ladybird (Psyllobora vigintiduopunctata) 4, P6; breeding/rearing 124125; collecting 116; distribution 75; foods/ feeding 22, 25; habitat 16; identication 92, 106, 109; mimicry 64; overwintering 26, 27, 28; parasites/diseases 33, 34, 35, 40, 41; pattern/colouration 50, 51 24-spot ladybird (Subcoccinella vigintiquattuorpunctata) 4, P5, P7; breeding/rearing 124125; collecting 116; distribution 75; foods/feeding 2122, 22, 22, 26; habitat 17; identi cation 86, 96, 107, 109, 113; overwintering 26, 27; pattern/colouration 50, 51, 53, 55 Adalia spp. 36 Adonis ladybird (Hippodamia variegata) 4, P5, P10; breeding/rearing 124; distribution 75, 7778; foods/feeding 21, 25;

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habitat 15, 17; identication 89, 102, 110, 111; mimicry 64; overwintering 27; parasites/diseases 33, 34, 35, 37, 38, 41; pattern/ colouration 50, 51, 53, 53 Adults 910, 9, 8594, 138 Aggregations 2728, 58 Anaesthetising 127 Anatomy 138, 139 Antennae 2, 95, 107, 125, 138 Ants 17, 30, 31 Aphids 1; as adult food 1821, 24; ant defenders 31; defence 2021; as food for captive ladybirds 119120, 123; and host plants 15, 17; as larval food 7, 7, 8, 1819, 6061 Articial diets 120122 Bacteria 38, 41, 56, 6061 Beating 115, 115, 116 Birds 3031, 63, 65 Breeding/Rearing 118125, 124 Bryony ladybird (Henosepilachna argus) 4, P4; breeding/rearing 124125; distribution 76, 79, 82; foods/feeding 22, 26; habitat 17; identication 86, 96, 107, 109; overwintering 27; pattern/colouration 50, 51 Calvia 10-guttata 83, 113, P11 Cannibalism 7, 1213, 23, 58, 5961, 119 Cheilomenes lunata 83 Chilocorinae 3, 71, 73 Chilocorini 73 Chromosomes 45, 54, 71, 73, 128129 Classication 34, 7073 Climate change 1114, 79, 84 Clitostethus arcuatus 3, 16, 25, 76, 97 Coccids 21, 24, 72 Coccidula rufa 3, 16, 25, 75, 101, P11 Coccidula scutellata 3, 16, 25, 76, 101, P11 Coccidulinae 3 Coccinellidae 23, 34, 6973, 94106, P1 Coccinellinae 4 Coccinellini 71 Collecting 115118, 115, 116 Colour: development 9, 4244, P8; environmental impacts 13; as identication tool 8694; mimicry 6465, 64; polymorphism 6569, 68, 69; variation 4249, 46, 5051, 5254, 53, 54; warnings 30, 6162, 63 Conspecic 23 Cream-spot ladybird (Calvia quattuordecimguttata) 4, P5; breeding/rearing 124; distribution 75, 77; foods/feeding 25; habitat 15, 16; identication 94, 106, 109;

life history 6; mimicry 64; overwintering 27, 28; parasites/diseases 33, 35, 38, 41; pattern/colouration 44, 50, 51 Cream-streaked ladybird (Harmonia quadripunctata) 4, P4, P10; breeding/rearing 124; chromosomes 128; defence 63; distribution 75, 79, 81; foods/feeding 26; habitat 17; identi cation 93, 103, 110; mimicry 64; overwintering 17, 28; parasites/diseases 33, 35, 41; pattern/colouration 50, 51, 52 Cryptolaemus montrouzieri 84, 114, P11 Cynegetis impunctata 113 Defence 6165, 62 Development rate 56, 7, 8, 21 Diapause 12 Diseases 28, 3740, 41 Distribution 74, 7576, 7779, 80, 81, 82; climate change impacts 1112, 14, 79, 84 Dormancy 12 Ectoparasites 39 Egg cannibalism 5961, 119 Egg laying 5, 6, 6, 19, 24, 56, 123124 Eggs 67, 32, 38, 56, 60, 122, P12 Elytra 2, 2, 9see also Colour Endoparasites 32 Endosymbionts 38 Epilachninae 4, 71 Evolutionary relationships 38, 6973 Exochomus nigromaculatus 8384, 114, P11 Eyed ladybird (Anatis ocellata) 4, P4, P10, P12; breeding/rearing 124; chromosomes 128; defence 62, 63; distribution 75; foods/feeding 25; habitat 15, 16, 17; identication 90, 93, 94, 105, 110; life history 6; mating 10; mimicry 64; overwintering 27, 29; parasites/diseases 32, 33, 33, 35, 41; pattern/colouration 42, 49, 50, 51, 52; prepupa 8; pronotum 3; sexing 10 Fecundity 6, 56 Field keys 85; adult Coccinellidae 94106; adult ladybirds 8594; larval ladybirds 106111 Flies 3234, 33, 41 Foods/feeding 15, 2526; alternative foods 24; captive ladybirds 117, 119122, 125; essential food 15, 24; fecundity, impact on 6; herbivory and mildew feeding 2122; intraguild predation 2224; in larval stage 78, 8; and migration 57; and population explosions 58; predation 1821 Foods/feeding, mandibles 22, 22 Fungal pathogens 14, 28, 3840, 41

140 | Ladybirds

Gametocysts 37 Genes/Genetics 44, 45, 47, 54, 60, 71; in pattern/colour variation 43, 4546, 48, 52, 6869 Genitalia 7071, 71, 127, 128 Gregarinidae 37 Guilds 23 Habitat 15, 1617, 1718 Harlequin ladybird (Harmonia axyridis) 4, 56, P3, P7; breeding/rearing 120, 123, 124; distribution 75, 77, 79, 82, P2; eggs 60; foods/feeding 19, 23, 26, 62; habitat 15, 16; humans, biting 59; hybrid matings 72; identication 88, 91, 93, 104, 110; overwintering 26, 27, 28; parasites/diseases 33, 34, 35, 36, 37, 39, 40, 41; pattern/colouration 43, 44, 4849, 50, 51; polymorphism 6869; population size 5859 Heather ladybird (Chilocorus bipustulatus) 3, 8, P6; breeding/rearing 124; chromosomes 128; collecting 116; distribution 76, 78; foods/feeding 21, 25; habitat 16; hybrid matings 7273; identication 88, 97, 108; mimicry 64, 64; overwintering 26, 27; parasites/diseases 33, 35, 36, 40, 41; pattern/colouration 43, 50, 51 Hibernation see Overwintering Hieroglyphic ladybird (Coccinella hieroglyphica) 4, P6, P10; breeding/rearing 123, 124; collecting 116; distribution 75; foods/feeding 25; habitat 15, 17, 17; identication 87, 91, 104, 111; mimicry 64; overwintering 27; parasites/diseases 35, 41; pattern/colouration 44, 50, 51, 52 Host plants 15, 1718, 18, 22 Hybrids 7273, 72, 73 Hyperaspis pseudopustulata 3, 16, 25, 76, 97, P11 Instars 7 Kidney-spot ladybird (Chilocorus renipustulatus) 3, P6; breeding/rearing 124; distribution 75; foods/feeding 21, 25; habitat 16, 17; identication 88, 97, 108; mimicry 64; overwintering 27, 29; parasites/diseases 33, 33, 40, 41; pattern/colouration 43, 44, 50, 51 Kin selection 60 Labelling 125, 126, 126 Lacewing larvae 23 Larch ladybird (Aphidecta obliterata) 4, P6, P10; breeding/rearing 124; chromosomes

128129; defence 63; distribution 75, 78; foods/feeding 21, 25; genitalia 71; habitat 16, 17; identication 89, 92, 105, 110; overwintering 27, 28; parasites/diseases 33, 34, 41; pattern/colouration 50, 51 Larvae 5, 78, 7, 8, 23, 139, P7, P12; identication 106111; rearing 122123 Life cycle 511, 5 Mandibles 22, 22 Mark-release-recapture 129130, 129 Mating 911, 10, 56, 57, 67; hybrid matings 7273, 72, 73 Melanic forms 13, 4244, 51, 52, P5, P6, P9, P10; 2-spot ladybird 4446, 46, 6568, 68; 10-spot ladybird 4748, 69; harlequin ladybird 4849, 6869; mimicry 64 Microsporidia 40, 41 Migrations 57, 59 Mimicry 6365, 64 Mites 37, 41, 126 Mortality 56; cold 2829, 66; disease 3740, 41; of larvae 7; parasitoids/parasites 3137, 33, 34, 35, 41; predators 3031 Moulting 8, 8 Mutations 54 Nematodes 37, 41 Nephus bisignatus 3, 16, 76, 100 Nephus quadrimaculatus 3, 16, 25, 76, 100 Nephus redtenbacheri 3, 16, 25, 76, 100 Nephus spp. 95 Oenopia conglobata 84, 113 Orange ladybird (Halyzia sedecimgutt ata) 4, 1314, 125, P6, P7; distribution 75, 78, 81; foods/feeding 22, 22, 25; habitat 16; identication 94, 105, 109; mimicry 64; overwintering 27, 28; parasites/diseases 35, 41; pattern/colouration 50, 51 Overwintering 24, 2629, 27, 39 Ovipositor 32, 34 Parasitoids/Parasites 3137, 33, 34, 35, 3940, 40, 41 Pattern variation 4249, 46, 5051, 5254, 53, 54 Pest control 1, 12, 84 Phenotypic plasticity 69 Pheromones 19, 20, 28 Phylogenies 70, 71, P1 Pigments 9, 4243 Pine ladybird (Exochomus quadripustulatus) 3, P6, P7, P12; chromosomes 128; distribution 75; eggs 6; foods/feeding 25; habitat 16; hybrid matings 7273;

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identication 88, 96, 108; mimicry 64, 64; overwintering 26, 2728, 27, 29; parasites/ diseases 34, 35, 36, 41; pattern/colouration 43, 50, 51; pupae 8; sexing 10 Pinning 125126, 125, 126 Platynaspis luteorubra 3, 7, 16, 25, 36, 41, 76, 96, P11 Polymorphism 48, 6469 Poplar leaf-beetle (Chrysomela populi) 112 Population explosions 24, 5658 Population size 40, 5659, 129130 Predators 3031, 40 Pre-pupa 8, 8 Procula douei 83, P11 Pronotum 2, 3 Protozoa 37, 41 Pupae 7, 89, 8, 9, 123, P12 Pupal alarm 8, 9 Quiescence 12 Recording schemes 74, 117118 Reex bleeding 30, 62, 62 Rhyzobius chrysomeloides 3, 16, 25, 76, 101, 112 Rhyzobius litura 3, 16, 25, 55, 75, 101, P11 Rhyzobius lophanthae 3, 16, 25, 76, 84, 101, 112 Scale insects 19, 21, 24 Scarce 7 spot ladybird (Coccinella magnica) 4, P4; breeding/rearing 124; distribution 76; foods/feeding 25; habitat 17; identication 90, 104, 111; overwintering 27; parasites/diseases 31, 41; pattern/colouration 50, 51 Scymninae 71 Scymnus auritus 3, 16, 25, 75, 99, P11 Scymnus femoralis 3, 16, 25, 76, 99, P11 Scymnus frontalis 3, 16, 25, 76, 98, P11 Scymnus haemorrhoidalis 3, 16, 25, 76, 99 Scymnus interruptus 3, 16, 25, 76, 98 Scymnus limbatus 3, 16, 25, 76, 99 Scymnus nigrinus 3, 16, 25, 76, 98 Scymnus schmidti 3, 16, 25, 76, 99 Scymnus subvillosus 114 Scymnus suturalis 3, 16, 25, 75, 99 Setting 125126, 125, 126 Sex di erentiation 1011, 10, 7071, 71, 128129 Size variation 2, 54 Spiders 30 Steelblue ladybird (Halmus chalybeus) 84 Stethorus punctillum 3, 16, 25, 76, 100 Striped ladybird (Myzia oblongoguttata) 4, P4, P10; breeding/rearing 123124, 124; defence 63; distribution 76; foods/

feeding 25; habitat 15, 16; identication 94, 102, 111; overwintering 27, 29; parasites/diseases 33, 35, 41; pattern/colouration 50, 51 Study techniques 125131, 125, 126, 127, 129 Sweeping 115116, 116 Tarsi 95, 95 Taxonomy 70 Temperature 8, 89, 1114 Tibiae 3, 95 UK Ladybird Survey 117118 Vagrants 8384 Vedalia ladybird (Rodolia cardinalis) 114 Vibidia 12-guttata 83, 113, P11 Warning colouration 30, 6162, 63 Wasps 3436, 34, 35, 41 Water ladybird (Anisosticta novemdecimpunctata) 4, P6; breeding/rearing 124; diseases 38, 41; distribution 74; foods/ feeding 25; habitat 15, 16, 17; identication 92, 102, 109; mimicry 64; overwintering 27; pattern/colouration 50, 51, 54 Wings 2, 2, 9, 5455, 54

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antenna head eye

pronotum
scutellum scutellary spot epimeron epipleuron epimeron elytron centre line

prosternum prosternal keel mesosternum metasternum coxa postcoxal line

femur tibia tarsus tarsal claw

1st abdominal segment 6th abdominal segment

head prothorax mesothorax metathorax 1st abdominal segment outer bump middle bump inner bump 8th abdominal segment 9th abdominal segment