Laboratory study of cannibalism and interspecific predation in ladybirds

Abstract.

• 1 In the absence of aphids, adult females of Adalia bipunctata (L.) showed a greater reluctance to eat eggs than males.
• 2 Eggs and young larvae were more vulnerable to cannibalism than older larvae and starved larvae were more vulnerable than well-fed larvae.
• 3 Both egg and larval cannibalism is inversely related to the abundance of aphids.
• 4 Eggs are a better food, in terms of larval growth and survival, than aphids.
• 5 In the absence of aphids interspecific predation occurred, but not equally, between the coccinellids A.bipunctata, A.decempunctata (L.), Coccinella septempunctata L. and C.undecempunctata L.
• 6 Larvae and adults of A. bipunctata and C.septempunctata were reluctant to eat conspecific eggs painted with a water extract of the other species' eggs and larvae of C. septempunctata were more likely to die after eating a few eggs of A.bipunctata than vice versa.
• 7 These results indicate that cannibalism occurs mainly when aphid prey is scarce and is adaptive in that it improves the chances of survival, and coccinellids, to varying degrees, are defended against interspecific predation.

     

Why do ladybirds (Coleoptera: Coccinellidae) cannibalize?

Cannibalism of eggs by larvae ofAdalia bipunctata, an aphidophagous species of ladybirds, is important for survival when aphids are scarce. Ladybirds survive longer by eating eggs of their own species rather than aphids. Since it costs less, in terms of larval growth, to eat eggs rather than aphids, cannibalism has a strong advantage under conditions of prey scarcity.     

Assessment of patch quality by ladybirds: role of larval tracks

Gravid females of the two-spot ladybird, Adalia bipunctata (L.), were deterred from ovipositing when kept in petri dishes that had previously contained conspecific larvae but not conspecific adults, or the larvae of another two species of ladybird, Adalia decempunctata (L.) and Coccinella septempunctata L. The deterrent effect was density dependent and mediated via a chloroform-soluble contact pheromone present in the larval tracks. Similarly, gravid females of C. septempunctata were deterred from ovipositing by conspecific larval tracks and chloroform extracts of these tracks, but not by the tracks or extracts of tracks of A. bipunctata larvae. That is, in ladybirds the larvae produce a species-specific oviposition-deterring pheromone. In the field, the incidence of egg cannibalism in ladybirds increases very rapidly with the density of conspecific eggs or larvae per unit area. Thus, in responding to the species specific oviposition deterring pheromone female ladybirds reduce the risk of their eggs being eaten and spread their offspring more equally between patches. Received: 14 March 1997 / Accepted: 26 August 1997     

Egg cannibalism by Coleomegilla maculata lengi neonates: preference even in the presence of essential prey

Abstract 1. Egg cannibalism among coccinellids has been reported widely, however reasons why this type of behaviour is observed so frequently have been neglected. This experiment was undertaken to clarify whether cannibalistic behaviour is advantageous to Coleomegilla maculata lengi Thimberlake neonates and to understand the reasons for high levels of egg cannibalism.
2. Benefits gained by neonate cannibals were ascertained by comparing survival, developmental time, and second-instar weight of C. maculata larvae that were allowed to cannibalise conspecific eggs or not. Preference and behaviour tests were also conducted to assess the reasons for high levels of egg cannibalism.
3. Cannibal neonates grew faster and were heavier than non-cannibals. The developmental time of neonates was influenced more by prey vulnerability than by prey quality.
4. In choice tests, where three different proportions of conspecific eggs and aphids were offered (33–67, 50–50, and 67–33%), C. maculata neonates always consumed significantly more eggs. Manly's preference indexes indicated that neonates showed a consistent preference for conspecific eggs.
5. Seventy-five per cent of neonates observed went directly towards eggs and 90% of the first prey consumed by neonates were an egg. When aphids were painted with extract of crushed eggs and eggs with crushed aphids to determine whether neonates found eggs by chemical cues, neonates preferred aphids painted with egg extract to eggs painted with aphid extract.
6. It was concluded that C. maculata neonates benefited from cannibalistic behaviour. Moreover, egg cannibalism is not related only to frequency of encounter; chemical cues are also involved in egg searching.     

Divergent preferences of Rhagoletis pomonella host races for olfactory and visual fruit cues

The quality of different species of aphids as food for aphidiphagous ladybird beetles varies greatly. The optimal oviposition theory predicts that a female should lay eggs preferentially in patches of suitable prey and should be reluctant to oviposit in patches of less suitable prey. A no‐choice experiment was used to test whether aphids (Homoptera: Aphididae) of different suitability influence the oviposition behaviour of the two‐spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae). The results indicate that A. bipunctata females are not more reluctant to lay eggs in the presence of moderately suitable compared to highly suitable aphids. However, females laid fewer eggs in the presence of toxic aphids.     

Effect of cannibalism on predation,oviposition and longevity of the predacious mite,Agistemus exsertus Gonzalez (Acari: Stigmaeidae)

Cannibalism (intraspecific predation) on conspecific eggs was investigated in the predatory stigmaeid mite, Agistemus exsertus Gonzalez in the absence of eggs of Tetranychus urticae Koch (no-choice tests) and presence of three densities of prey eggs simultaneously (choice tests) in the laboratory. Data show that cannibalism occurs in immatures and adult females of the predator, which successfully developed and reproduced on conspecific eggs as an alternative prey in the absence of prey eggs. In no-choice tests, cannibalism rate on conspecific eggs by A. exsertus stages was significantly lower than the predation rate on T. urticae eggs. The predatory mite exhibited a marked decline in oviposition rate when preyed on conspecific eggs compared with feeding on prey eggs. The developmental duration and longevity of A. exsertus females were significantly longer 1.9 and 1.7 times, respectively, when fed on conspecific eggs than feeding on T. urticae eggs. The propensity of the predator towards cannibalism depends on the prey density, when T. urticae eggs and conspecific eggs are present simultaneously. Provision of increased densities of prey eggs significantly decreased cannibalism and predation by A. exsertus stages, which fed generally less on conspecific eggs than on T. urticae eggs in choice tests. The oviposition rate of the predator increased significantly, as the egg density of the prey increased. The developmental period and longevity of A. exsertus females showed significantly gradual shortness with increasing egg density of the prey.     

Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species

Abstract 1 Survival and development of hatchling larvae of three aphidophagous ladybirds (Coleoptera: Coccinellidae), Harmonia axyridis Pallas, Coccinella septempunctata brucki Mulsant and Adalia bipunctata Linnaeus, when fed their own and the other species eggs were recorded. 2 In all three species, the larvae survived when fed conspecific eggs. 3 The percentage of larvae of H. axyridis that survived decreased to 35% and 85% when fed eggs of A. bipunctata and C. s. brucki, respectively. All the larvae of A. bipunctata and C. s. brucki died after eating eggs of H. axyridis. None of the larvae of C. s. brucki died after eating eggs of A. bipunctata, whereas 46% of those of A. bipunctata died after eating eggs of C. s. brucki. 4 In general, larvae were reluctant to eat the eggs of other species. However, larvae of C. s. brucki showed less reluctance than H. axyridis to eat the eggs of A. bipunctata. 5 The consequence of this for invasive species of ladybird is discussed.     

Evolution of cannibalism and female's response to oviposition-deterring pheromone in aphidophagous predators

1.  Egg cannibalism by larvae is common in Coccinellidae and is known to be advantageous for the cannibals. Furthermore, larvae of aphidophagous ladybirds usually produce an oviposition-deterring pheromone (ODP), which inhibits oviposition by adult females. It has been proposed that the response to ODP has evolved because of the high costs of cannibalism. However, this has never been formally proved.
2.  In this paper, we study the theoretical evolution of this system. We first look at the conditions under which cannibalism and the response to ODP can evolve. Subsequently, we examine the occurrence of polymorphism both in the production of larval tracks and in the sensitivity of females to specific pheromones.
3.  The models predict that the amount of cannibalism should not depend on prey density and that evolution should lead to a continuous increase in cannibalism, and consequently larvae should always cannibalize eggs when possible. In response to the cost of cannibalism, ODP recognition can evolve, so that females avoid laying eggs in patches of prey already occupied by conspecific larvae. The result is an arms race between larvae and adult females, which favours a diversification of ODP pheromones. Our models show that: (i) females should be able to recognize mixtures of hydrocarbons rather than a single molecule; and (ii) females should be more sensitive to the tracks of their own offspring than those of non-related larvae.     

Oviposition Behavior of the Predatory Midge Aphidoletes aphidimyza in Response to Aphid Patch Quality

Female Aphidoletes aphidimyza confronts serious challenges from both aphid prey and conspecifics. These challenges constitute strong selective pressures on the predatory midge to have an adaptive oviposition strategy. We did laboratory experiments to investigate clutch size of A. aphidimyza in response to the aphid Rhopalosiphum padi (density and age) and the presence of conspecific eggs (density) and larvae (age) in aphid colonies. The results of our study show that A. aphidimyza female adjusts its foraging effort by assessing the quality of prey patches. The number of eggs laid increased in response to aphid density. However, patches consisting of older aphids received fewer eggs. The number of eggs laid decreased in response to the presence of conspecific eggs, and in response to the presence of 2-day old conspecific larvae. Our study reveals deterrent effects on A. aphidimyza oviposition decisions on clutch size in response to older aphids and the presence of more conspecific eggs and older larvae.     

Development and reproduction of Adalia bipunctata on factitious and artificial foods

The native coccinellid Adalia bipunctata (L.) (Coleoptera: Coccinellidae) may be an alternative to exotic species like Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) for the biological control of aphid pests in Europe. The availability of adequate factitious or artificial foods may help optimize its mass production. This study examines the nutritional value of Ephestia kuehniella Zeller (Lepidoptera: Phycitidae) eggs plus bee pollen, pea aphids Acyrthosiphum pisum (Harris) (Hemiptera: Aphididae) and mixtures of bee pollen and cysts of Artemia franciscana Kellogg (Branchiopoda: Artemiidae) and/or a lyophilized artificial diet based on bovine meat and liver. Reproducing adults of A. bipunctata were obtained on all diets tested, but immature survival, adult weights, development times and reproductive rates differed among diets. Over 84% of first instars fed on E. kuehniella eggs plus pollen or aphids survived to adulthood. Feeding predator larvae on pollen combined only with A. franciscana cysts or artificial diet yielded 40–55% immature survival, but survival increased to 74% when all of these components were mixed. Adult weights of A. bipunctata on the mixtures of pollen, A. franciscana cysts and/or artificial diet were 55–75% of those on aphids or on E. kuehniella eggs plus pollen. Lifetime fecundity was superior on E. kuehniella eggs plus pollen (1,864 eggs) to that on the other diets (264–889 eggs). The use of mixtures of plant and animal foods for A. bipunctata and other predators may contribute to increasing the cost-effectiveness of commercial mass production by reducing inputs of natural prey like aphids, or of nutritious but expensive factitious foods like lepidopteran eggs.     

Habitat or prey specialization in predatory ladybird beetles: a case study of two closely related species

This study examines the niche and diet breadth of two closely related sympatric aphidophagous ladybirds: Adalia decempunctata and A. bipunctata. The degree of habitat specialization of these species is investigated, and its effect on life history traits of females is explored. The importance of prey quality in determining the diet breadth is also examined. The niches occupied by these species in three countries, the UK, Belgium and southern France, are similar: A. decempunctata is an arboreal habitat specialist with a narrower set of prey than A. bipunctata, which is commonly found on several types of vegetation. The niches of the two species overlap on trees. Experiments indicate that habitat specialization has resulted in A. decempunctata investing more in each of its offspring than A. bipunctata. A. decempunctata females lay, relative to their body size, heavier eggs than those of the more generalist A. bipunctata, which results in A. decempunctata having bigger larvae. In addition, A. decempunctata larvae are better at surviving starvation than A. bipunctata larvae. In contrast to the expected pattern in food specialization, our study failed to demonstrate a better efficiency of the specialist when fed its usual prey and a detrimental effect when fed on prey that it is unlikely to encounter in the field. The reproductive performance of the specialist ladybird was better when fed an aphid that it was unlikely to regularly feed on in the field. Therefore, the narrow diet of the specialist ladybird is most likely a consequence of it occupying a narrow habitat rather than the quality of the prey. Although further studies on specialization in predatory insects are needed, the results indicate that unlike the role of plant quality in host specialization in herbivorous insects, prey quality has not been the main determinant of ecological specialization in these predatory insects.     

Differentiated egg size of the cannibalistic salamander <Emphasis Type="Italic">Hynobius retardatus</Emphasis>

Larvae of the salamander, Hynobius retardatus, are carnivorous, and even though there are two morphs, a typical morph and a broad-headed or “cannibal” morph, both are cannibalistic. They also sometimes eat other large prey, for example larvae of the frog, Rana pirica. In natural habitats, use of both conspecific and R. pirica larvae as food may contribute more strongly to high survival and substantially to fitness when larval densities are higher, because early-stage H. retardatus larvae sometimes experience scarcity of their typical prey. In cannibalistic oviparous amphibians, larger individuals that developed from larger eggs can more efficiently catch and consume larger prey and thus their survival may be better than that of smaller individuals developed from smaller eggs. Populations might therefore diverge in respect of egg size in response to variation in the density of conspecific and R. pirica larvae in natural ponds, with eggs being larger when larval density is higher. I examined how variance in hatchling size correlated with the incidence of cannibalism, and whether increasing larval density in natural ponds correlated with increasing egg size. Variance in initial larval body size facilitated cannibalism, and egg size increased as larval density in the ponds increased. In ponds with high larval density, where cannibalism and large prey consumption is a critical factor in offspring fitness, the production of fewer clutches with larger eggs, and thus of fewer and larger offspring, results in greater maternal fitness. Variation among the mean egg size in populations is likely to represent a shift in optimum egg size across larval density gradients.     

Learned Recognition of Intraspecific Predators in Larval Long-Toed Salamanders Ambystoma macrodactylum

The ability of prey to detect predators and respond accordingly is critical to their survival. The use of chemical cues by animals in predator detection has been widely documented. In many cases, predator recognition is facilitated by the release of alarm cues from conspecific victims. Alarm cues elicit anti‐predator behavior in many species, which can reduce their risk of being attacked. It has been previously demonstrated that adult long‐toed salamanders, Ambystoma macrodactylum, exhibit an alarm response to chemical cues from injured conspecifics. However, whether this response exists in the larval stage of this species and whether it is an innate or a learned condition is unknown. In the current study, we examined the alarm response of naïve (i.e. lab‐reared) larval long‐toed salamanders. We conducted a series of behavioral trials during which we quantified the level of activity and spatial avoidance of hungry and satiated focal larvae to water conditioned by an injured conspecific, a cannibal that had recently been fed a conspecific or a non‐cannibal that was recently fed a diet of Tubifex worms. Focal larvae neither reduced their activity nor spatially avoided the area of the stimulus in either treatment when satiated, and exhibited increased activity towards the cannibal stimulus when hungry. We regard this latter behavior as a feeding response. Together these results suggest that an anti‐predator response to injured conspecifics and to cannibalistic conspecifics is absent in naïve larvae. Previous studies have shown that experienced wild captured salamanders do show a response to cannibalistic conspecifics. Therefore, we conducted an additional experiment examining whether larvae can learn to exhibit anti‐predator behavior in response to cues from cannibalized conspecifics. We exposed larvae to visual, chemical and tactile cues of stimulus animals that were actively foraging on conspecifics (experienced) or a diet of Tubifex (naïve treatment). In subsequent behavioral treatments, experienced larvae significantly reduced their activity compared to naive larvae in response to chemical cues of cannibals that had recently consumed conspecifics. We suggest that this behavior is a response to alarm cues released by consumed conspecifics that may have labeled the cannibal. Furthermore, over time, interactions with cannibals may cause potential prey larvae to learn to avoid cannibals regardless of their recent diet.     

Evolution of slow and fast development in predatory ladybirds

The frequency distribution of the durations of development of 516 larvae of Adalia bipunctata is unimodal, and the fast‐ and slow‐developing larvae can be identified at the beginning of the fourth (=last) instar. To determine the advantages of fast and slow development, the survival, duration of development, growth and number of aphids consumed by fast‐ and slow‐developing fourth instar larvae fed different numbers aphids were recorded. The percentages of fast‐ and slow‐developing fourth instar larvae that survived when fed 0.5, 1 or an excess of aphids per day, surprisingly, did not differ. The slow‐developing larvae of both sexes took longer to complete their development than the fast‐developing larvae when fed 1 or an excess of aphids per day, and although the weights of the fast‐ and slow‐developing fourth instar larvae differed at the beginning of the instar, they did not differ at the end of this instar when fed 1 aphid per day. However, when reared on an excess of aphids per day, the adult weights of the fast‐developing individuals was greater than that of slow‐developing individuals. The average durations for which the larvae in the two groups survived when fed 0.5 aphids/day differed with the larvae of the fast‐developing individuals surviving for 9.8 ± 0.5 days and slow‐developing individuals 17 ± 1.3 days. Assuming that it is the rate of predator biomass increase, which is maximized by evolution, a model of the relationship between the rate of development/growth of a predator and that of its prey indicates that the optimum growth rate of a predator is positively associated with that of its prey. The evolutionary implications of these results are discussed.     

Essential versus alternative foods of insect predators: benefits of a mixed diet

Although many predatory insects appear to be opportunistic generalists in their selection of prey, only a subset of prey species may in fact serve as “essential foods” capable of supporting immature growth and adult reproduction. It has been suggested that other, “alternative foods” serve only to maintain the predator when essential foods are not available, but little research has evaluated the significance of a mixed diet of essential and alternative foods for predator growth or reproduction. Here we test the general hypothesis that although alternative prey may be inadequate to support reproduction when consumed alone by adult predators, consumption of such prey may enhance the predator's reproductive output when the predator also has access to essential prey. We compared egg production by two aphidophagous lady beetles, Coccinella septempunctata and C. transversoguttata, provided with diets of aphids (essential prey) and weevils (alternative prey). As predicted, female predators produced greater numbers of eggs when a diet of pea aphids in limited number was supplemented by alfalfa weevil larvae. The predators laid no eggs when provided only with weevils or only with sugar. But once aphids were added to the diet, females of C. transversoguttata (but not C. septempunctata) laid eggs in greater numbers when they had fed previously on weevils than on sugar. Females of both species also produced eggs in modest numbers when provided with both weevils in excess and sugar, but this diet supported a lower rate of egg production than did a diet of weevils in excess plus a limited number of aphids. Although C. septempunctata has a longer history of association with the alfalfa weevil than does C. transversoguttata, the former species was not more effective in exploiting this alternative prey in support of reproduction. The tendency of generalist predators such as adult lady beetles to consume alternative as well as essential prey probably enhances considerably their ability to capitalize on short-lived and scattered opportunities as they seek out suitable sites in which to reproduce. Received: 11 May 1998 / Accepted: 1 May 1999     

Is assessment of oviposition sites using conspecific larval cues a general mechanism in aphidophagous ladybirds (Coccinellidae)?

Aphidophagous ladybirds of the Coccinellinae subfamily are deterred from oviposition in the presence of chemical cues deposited by conspecific larvae, therefore avoiding the detrimental effects of competition and cannibalism to their offspring. However, it is still unknown whether aphidophagous species from other Coccinellidae subfamilies similarly behave. Here, we investigate this question for species of the Scymninae subfamily. A GC‐MS analysis of Scymnus interruptus (Goeze) larval tracks shows that larvae deposit a cocktail of hydrocarbons containing at least five branched‐chain alkanes. Furthermore, our experiments on the oviposition behaviour of S. interruptus and S. nubilus (Mulsant) in the presence of conspecific larval tracks and of conspecific larval wax covering Scymninae larvae show that females do not refrain from ovipositing in the presence of these larval cues. We recommend that more attention is paid to the role of Scymnus spp. in the regulation of aphids because their oviposition strategy might strengthen aphid suppression in agrosystems.     

Cannibalism inEpisyrphus balteatus (Ditp: Syrphidae)

Cannibalism occurred frequently in a laboratory population ofEpisyrphus balteatus. The third instar larva was the most voracious cannibal and are mainly eggs. Pupae were never eaten. Egg cannibalism was inversely dependent on aphid density, but even occurred when prey was present in excess. Syrphid larvae can complete their development on conspecific eggs.     

Consumption of flea faeces and eggs by larvae of the cat flea,Ctenocephalides felis

The effects of the consumption of flea faeces and non-viable eggs on larval development in the cat flea Ctenocephalides felis (Bouché) (Siphonaptera: Pulicidae) were investigated. Only 13.3% of larvae developed into adults when fed a diet of male or female flea faeces alone; however, 90% of larvae developed into adults when fed on flea faeces supplemented with non-viable flea eggs. When fed with non-viable eggs alone, larvae did not develop into adults. Nevertheless, non-viable eggs may provide critical supplemental nutrients, lacking in flea faeces and required for larval development. None of the larvae fed on flea faeces or non-viable eggs alone formed a cocoon. A diet of flea faeces alone significantly extended the second as well as third larval stadia compared to larvae fed on diets containing non-viable eggs. It is suggested that the cannibalism of fertile eggs may limit population growth in the cat flea.     

Propensity towards cannibalism among Hypoaspis aculeifer and H. miles, two soil-dwelling predatory mite species

In biological control programmes, the two predatory soil mites Hypoaspis aculeifer and H. miles are often applied against soil-borne pests like mushroom flies, springtails and mites. Although the mites show high consumption rates on varying prey types in Petri dish experiments and in greenhouses, their overall efficiency is sometimes limited. We hypothesized that intraspecific interactions, like cannibalism, could contribute to this decreased competence. Therefore, experiments were conducted to show the propensity of H. aculeifer and H. miles to cannibalise. Adult mites and nymphs were introduced as predators with conspecific eggs, larvae, nymphs, adult females or males as prey and the number of killed individuals was recorded. Additionally, the oviposition rate on conspecific prey was quantified and the correlation with the number of prey consumed was calculated to assess the influence of cannibalism on egg production. The results illustrate that cannibalism occurs infrequently in both Hypoaspis spp., the only exception being H. aculeifer nymphs, which cannibalised one conspecific egg per day. Moreover, cannibalism never occurred in the presence of alternative prey. Oviposition rate decreased during the experiment in both species but it was positively correlated with the cannibalism rate only for H. aculeifer. The benefit of cannibalism for populations of H. aculeifer and H. miles is discussed.     

Cues for cannibalism: cane toad tadpoles use chemical signals to locate and consume conspecific eggs

Although animals of many species kill and consume conspecifics, most such cases probably involve serendipitous encounters between the individuals concerned. In some taxa, however, cannibalism is an active process, with predatory individuals searching out and consuming specific types of conspecific prey items. Although anuran tadpoles often have been reported to consume conspecific eggs, this behaviour has been interpreted as a by‐product of usual foraging behaviours rather than a result of targeted searching. Our field and laboratory studies in tropical Australia show that the tadpoles of invasive cane toads Bufo marinus are strongly attracted to chemical cues from conspecific eggs; the effective cues are released late in embryonic development, as the jelly coat breaks down. Tadpoles of native Australian frog species were attracted to the eggs of toads only rarely. If deployed as bait in traps, chemical cues from toad eggs could provide a way to selectively remove toad larvae from waterbodies.