Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars

1. Aposematism is a widely used antipredator strategy in which an organism possesses both warning coloration and unprofitable characters. Theoretical evidence suggests that aposematic colour should develop when high opportunity costs imposed by crypsis force an organism to engage in conspicuous behaviours. Hence, it is expected that ontogenetic colour change (OCC) in larval insects should include aposematism when foraging needs compel behavioural modifications that preclude a continued state of crypsis. 2. To test this idea, I first investigated whether OCC in caterpillars of the panic moth Saucrobotys futilalis was indicative of a switch from cryptic to aposematic coloration. I then examined the context of panic moth OCC as it related to foraging patterns and behavioural conspicuousness. 3. Early Saucrobotys instars are a cryptic green, but later instars become progressively more orange and develop black spots. Early instar larvae forage cryptically on the inner parenchyma of silked-together host plant leaves to avoid predation, but are rapidly forced to engage in conspicuous foraging behaviours as they outgrow the resources afforded by their shelters. Both coloration and behaviour reach maximal conspicuousness in final instar larvae. 4. As predicted, OCC encompassed a change from crypsis to aposematism in Saucrobotys. Aposematic function was demonstrated by changes in both antipredator behaviour patterns and effectiveness of predator deterrence in early and late instars. Moreover, increased opportunity costs of crypsis and behavioural conspicuousness coincided with the onset of aposematic coloration. 5. This pattern of OCC suggests that aposematic coloration in Saucrobotys develops as a response to constraints imposed by crypsis. Moreover, my study illustrates the importance of the study of ontogenetic patterns in determining how behaviour, morphology, and predator responses interact to influence the initial evolution of phenomena such as aposematism.     

Camouflage and selective predation in caterpillars of the poplar and eyed hawkmoths (Laothoe populi and Smerinthus ocellata)

Final instar caterpillars of the poplar hawkmoth ( Laothoe populi ) are usually yellow-green when they have been feeding on Salix fragilis but white when on Populus alba. Similarly final instar caterpillars of the eyed hawkmoth (Smerinthus ocellata) vary in colour from yellow-green when fed on Salix cinerea or S. fragilis to grey-green when fed on Salix ripens or S. alba. Most caterpillars of these two moths are thus very cryptic to the human eye. It has already been shown that colour matching is brought about by young caterpillars changing colour depending on the colour of the substrate perceived by their eyes. Evidence is presented here for selective predation, probably by birds. Yellow-green poplar hawk caterpillars disappeared from P. alba more rapidly than did white caterpillars, but there was no significant difference in the survival of the two colour forms on S. fragilis. Yellow-green caterpillars survived better on S. fragilis than on P. alba , but there was no significant difference in the survival of white caterpillars on the two plants. Reasons why selective predation did not occur in all of the experiments are discussed.     

Determinants of predation on phytophagous insects: the importance of diet breadth

To evaluate the role of predation in the evolution of diet specialization and to determine the effectiveness of various larval defenses, we offered lepidopteran larvae to colonies of the tropical ant Paraponera clavata. We recorded behavioral and physical characteristics of prey items and used log-linear models to analyze their importance as deterrents to predation by P. clavata. The most important determinant of probability of prey rejection by P. clavata was a prey's diet breadth; specialists were rejected by the ants significantly more than generalists. Other less important, but significant, predictors of prey rejection included ontogeny, morphology and chemistry. Late instar caterpillars were rejected more frequently than early instars, hairy caterpillars were rejected more frequently than caterpillars with other morphologies, and one caterpillar species with an unpalatable extract was rejected more frequently than two species with palatable extracts.     

Cardenolide content of Danaus chrysippus butterflies from three areas of East Africa

The African butterfly Danaus chrysippus , like other members of the family Danaidae, feeds as a larva on species of milkweeds (Asclepiadaceae). It has been demonstrated in a sample from a West African population that only a minority of adult D. chrysippus accumulated detectable amounts of poisonous and presumably emetic cardenolides from their larval foodplants. It has also been shown in D. chrysippus and the related monarch butterfly ( D. plexippus ) that the cardenolide content of adults varies with that of their respective milkweed foodplants.
Three population samples of D. chrysippus from sites in East Africa are analysed for cardenolides using the spectrophotometric technique refined by Brower, Edmunds & Moffitt (1975), which allows the assay of individual butterflies. The East African samples all have a palatability spectrum with a considerably higher percentage of cardenolide-containing individuals than the West African one.
This is discussed in terms of its effect on potential bird predators and the 'automimicry' of emetic by palatable individuals. In East Africa D. chrysippus is polymorphic and appears to act as a model in a complex mimicry ring, whereas in West Africa it is monomorphic and may have 'shed' most of its mimics. This latter hypothesis is discussed in the light of our results.     

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.     

两种蚜小蜂对烟粉虱寄主的产卵选择性(英文)

双斑恩蚜小蜂和桨角蚜小蜂是华南地区烟粉虱的两种优势种寄生蜂。本文研究了两种寄生蜂对不同龄期烟粉虱寄主的产卵选择特性。结果表明:两种寄生蜂均可寄生烟粉虱的1~4龄若虫。当只有1个龄期的烟粉虱若虫存在时,双斑恩蚜小蜂更多地寄生3龄和4龄若虫,较少寄生1龄和2龄若虫;而桨角蚜小蜂则更多地寄生3龄和2龄若虫,较少寄生1龄和4龄若虫。在4个龄期若虫同时存在时,双斑恩蚜小蜂会明显增加对3龄和4龄若虫的产卵寄生,降低对1龄和2龄若虫的寄生;而桨角蚜小蜂则增加对2龄和3龄若虫的寄生,减少对1龄和4龄若虫的寄生。寄主植物的差异不影响这二种蚜小蜂对各龄期烟粉虱若虫的产卵选择倾向。结果提示,烟粉虱若虫3龄和4龄是双斑恩蚜小蜂最适宜的寄主,而桨角蚜小蜂最适宜的寄主是烟粉虱2龄和3龄若虫。     

两种蚜小蜂对烟粉虱寄主的产卵选择性（英文）

双斑恩蚜小蜂和桨角蚜小蜂是华南地区烟粉虱的两种优势种寄生蜂。本文研究了两种寄生蜂对不同龄期烟粉虱寄主的产卵选择特性。结果表明: 两种寄生蜂均可寄生烟粉虱的1～4龄若虫。当只有1个龄期的烟粉虱若虫存在时,双斑恩蚜小蜂更多地寄生3龄和4龄若虫,较少寄生1龄和2龄若虫;而桨角蚜小蜂则更多地寄生3龄和2龄若虫,较少寄生1龄和4龄若虫。在4个龄期若虫同时存在时,双斑恩蚜小蜂会明显增加对3龄和4龄若虫的产卵寄生,降低对1龄和2龄若虫的寄生;而桨角蚜小蜂则增加对2龄和3龄若虫的寄生,减少对1龄和4龄若虫的寄生。寄主植物的差异不影响这二种蚜小蜂对各龄期烟粉虱若虫的产卵选择倾向。结果提示,烟粉虱若虫3龄和4龄是双斑恩蚜小蜂最适宜的寄主,而桨角蚜小蜂最适宜的寄主是烟粉虱2龄和3龄若虫。     

Predation capacity and prey preference of <Emphasis Type="Italic">Chrysoperla carnea</Emphasis> on <Emphasis Type="Italic">Pieris brassicae</Emphasis>

The predation capacity and prey preference of larvae of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) on eggs or larvae of Pieris brassicae (Linnaeus) (Lepidoptera: Pieridae) in the absence and presence of cabbage aphids as an alternative prey were evaluated in laboratory experiments at 25°C. Both instars preyed upon butterfly eggs and larvae as well as on cabbage aphids with the third instar being the most voracious. The lacewings had a strong preference for caterpillars to butterfly eggs. In the presence of the aphids the predation on P. brassicae eggs or larvae was either completely abandoned or reduced by about 70%, respectively, by second instar lacewings and either reduced by about 80% or maintained, respectively, by third instar lacewings. Both instars thus had a clear preference for aphids compared to eggs of P. brassicae. However, second instar lacewings preferred aphids to caterpillars whereas the opposite was the case for third instar lacewings. The results indicate that 3rd instar C. carnea has a potential as biocontrol agent against P. brassicae.     

Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate

Abstract.  1. Many moth and butterfly larvae are gregarious early in development, but become solitary in late instars. This ontogenetic variation in behaviour is probably the result of temporal changes in the costs and benefits associated with gregariousness. This study provides observational and experimental evidence that, in one particular moth species, a series of different ecological factors influence larval behaviour at different times during development.
2. Field observations show that young caterpillars of the limocodid Doratifera casta form large aggregations while foraging, but that mature larvae are largely solitary.
3. A field experiment revealed that individual first to third instar larvae in larger groups develop more rapidly, but that group size had no detectable influence on survival. The developmental advantage associated with gregariousness is affected by host plant species, but not by predator exclusion, suggesting that group living in these cryptic early instar larvae promotes feeding facilitation, but does not provide individuals with protection from natural enemies.
4. Laboratory experiments revealed that aposematic fourth instar caterpillars in large groups were less likely to be attacked by a generalist insect predator than those in small groups.
5. Field observations provided no evidence that group living affects body temperature, suggesting that microclimatic factors do not favour gregariousness in this species.
6. It is concluded that gregariousness in D. casta confers at least two different advantages on larvae at different stages early in development, but that these advantages disappear, or are outweighed by costs associated with intraspecific competition, in final instars.     

The parasitoidCotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instars of its hostPieris brassicae,on the basis of contact cues from frass,silk, and herbivore-damaged leaf tissue

Adult females of the larval parasitoidCotesia glomerata (L.) respond to chemical cues associated with feeding damage inflicted on cabbage plants by its host,Pieris brassicae (L.). The use of these infochemicals by the parasitoid during selection of the most suitable host instar was investigated. The parasitoid can successfully parasitize first-instar host larvae, while contacts with fifth-instar larvae are very risky since these caterpillars react to parasitization attempts by biting, spitting, and hitting, resulting in a high probability of the parasitoid being seriously injured or killed. Observations of the locomotor behavior of individual wasps on leaves with feeding damage inflicted by the first and the fifth larval instars and on host silk and frass showed that several cues affect the duration of searching by the parasitoids after reaching a leaf: cues on the margin of the feeding damage and cues in the host frass and silk. Whole frass, silk, and hexane extracts of frass obtained from first-instar elicited parasitoid's searching behavior significantly longer than frass, silk, and hexane extract of frass from the fifth instar. The results demonstrate thatC. glomerata can discriminate between first instars, which are more suitable hosts, and fifth instars ofP. brassicae without contacting the caterpillars, by exploiting instar-related cues.     

Bemisia tabaci (Homoptera: Aleyrodidae) instar effects on rate of parasitism by Eretmocerus mundus and Encarsia pergandiella (Hymenoptera: Aphelinidae)

Studies were conducted to compare preference among Bemisia tabaci Gennadius, biotype B instars for parasitization by Eretmocerus mundus Mercet and Encarsia pergandiella Howard when provided one instar only, two different instars, and four different instars simultaneously. In the single‐instar no choice treatment, Er. mundus was more successful in parasitizing the younger host instars, while En. pergandiella parasitized a greater proportion of the older instars. Similar results were observed when parasitoids were provided a choice of two instars in six different pair combinations. When all four instars were provided simultaneously, the numbers of first, second, and third instars parasitized by Er. mundus were not significantly different from each other (range 10.3–16.4%), but all were significantly higher than parasitism of fourth instar nymphs (2.1%). The highest percentage parasitization by En. pergandiella was in third instar (17.2%), and the lowest in first instar (2.8%).     

Prey selection by wild birds can allow novel and conspicuous colour morphs to spread in prey populations

Conspicuous warning coloration helps to protect prey because it signals to potential predators that the prey is unprofitable. However, such signals only work once predators have come to associate the conspicuous colour with the unprofitability of the prey. The evolution of warning coloration is generally considered to be paradoxical, because it has traditionally been assumed that the first brightly coloured individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naïve to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous colour morph could ever avoid rapid extinction, and instead survive and spread in the population until predators have become educated about the signal. In the present study, we experimentally simulated the appearance of a single novel coloured mutant in small populations (20 individuals) of palatable artificial pastry "prey". The colour morph frequencies in each "generation" of prey (presented on successive days of a trial) were determined by the relative survival of the previous generation under predation by free-living birds. We found that the novel colour morphs regularly persisted and increased from a starting frequency of 1/20 to reach fixation (100%), despite being fully palatable, even when the novel morph was much more conspicuous against the background than the familiar morph. This was true for both green (not normally considered a warning colour) and red (a classic warning colour) novel morphs. Novel colours reached fixation significantly faster than could be accounted for by random drift, indicating differential predation in relation to prey colour by the birds. Our experiments show that the immediate demise of a fully palatable new prey morph is not an inevitable outcome of predator behaviour, because even very conspicuous prey can gain protection from conservative foragers, simply by being novel.     

Size dependent predation risk in cryptic and conspicuous insects

It is not clear which selective pressures balance the strong fecundity advantage associated with large female body size in insects. A positively size-dependent mortality risk could provide a solution. In aviary experiments with artificial larvae, we studied if larger larvae of folivorous insects are more readily found (= detectability) and/or attacked (= acceptability) by birds. As size and colouration are likely to interact in determining birds’ responses, both cryptic and conspicuous prey items were used. As detectability is likely to be context-dependent, both simple (smooth) and complex (plants) backgrounds were used in respective experiments. In the conspicuous larvae, acceptability correlated negatively with prey size. However, their detectability was context dependent, being positively correlated with size on the simple background, whereas no significant effect was found on the complex background. Surprisingly, cryptic larvae showed no correlation between detectability and size, and there was only a weak tendency for birds to attack large larvae more readily. On the basis of a quantitative model, we conclude that the effect of positively size dependent bird predation, as a single factor, is not likely to counterbalance the fecundity advantage in cryptic species, and may thus not be crucial in determining the optimum for body sizes in these insects. In conspicuous species, there is a potential for different outcomes, because detectability and acceptability affect survival in different directions. The net outcome is, therefore, likely to be highly context-dependent. Furthermore, our results provide an explanation for the recently reported absence of systematic body-size differences between cryptic and conspicuous Lepidopteran larvae: although conspicuous larvae benefit from increasing their warning signal when growing larger, they also suffer a much sharper rise in detectability. Estonian Science Foundation grant # 5746; Centre for International Mobility (Finland).     

Within‐generation dynamics of leatherjackets (Tipula paludosa Meig.)

Larvae of Tipula paludosa (leatherjackets) are pests of grassland and cereals, and important prey items for a range of farmland birds. Their population dynamics from year to year have been the subject of study, but within‐generation dynamics have received much less attention. The duration and occurrence of instars and size of the population is important to both pest management and bird conservation. Leatherjackets were collected monthly from four grass fields over five generations (October to September). Count data were analysed for sources of variability and used to estimate the timing and duration of instars and population changes over a single generation. Instar durations were correlated with temperature. From the first to third instars, sample counts were strongly influenced by the location of the site and the generation. Fourth instar larvae showed a similar decline in numbers across all sites and generations. The duration and timing of first to third instars was more variable than that of the fourth instar, but there was limited evidence that this was influenced by temperature. Only the durations of the third and fourth instars were correlated. The population decline from April to September coincided with the onset of the fourth instar. Our results show that the factors influencing leatherjacket numbers change over the life cycle, but by the fourth instar, these are biotically driven. The predictability of its numerical decline indicates defined windows for crop damage and availability as prey. The stability of its timing suggests that day length may synchronize the annual cycle. Fixed timing of the fourth instar will have important consequences for the timing of crop damage and the conservation of farmland birds as climate changes.     

Acoustic stimuli from predators trigger behavioural responses in aggregate caterpillars

Prey detect their predators through predator signals and cues and, consequently, respond with anti‐predatory behaviours to inhibit the action of their aggressors. Lepidopterans can intercept signals emitted by predators and may defend themselves through chemical, morphological or behavioural responses. In this study, we investigated the effect of acoustic stimuli of different predators on defensive behaviour of gregarious caterpillars. Our results demonstrated that Hylesia nigricans (Lepidoptera, Saturniidae) caterpillars alter their behaviour (i.e. abruptly raising the head) in response to the acoustic stimulus of the predators (i.e. predation risk signals from birds and wasps). The magnitude of this response depended on predator identity and caterpillar body size. Larger caterpillars responded more strongly to predatory stimuli than smaller caterpillars. However, regardless of the size of the caterpillars, they responded more strongly to the stimuli of wasps. In addition, we identified that H. nigricans caterpillars emit ultrasonic noise after detecting the stimuli of the predators – this noise seems to function as an alert about the risk of predation during the early stages of development (second and fifth instars). The duration of ultrasonic emission (i.e. milliseconds) increases with the number of repetitions of the stimuli (i.e. wing‐beat sounds of the wasps and insectivorous birds). These results provide novel information about predation risk in interactions among caterpillars and their predators, and indicate possible communication among invertebrates mediated by the risk of predation.     

Suitability of Bemisia tabaci (Hemiptera: Aleyrodidae) instars for the parasitization by Encarsia bimaculata and Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae) on glabrous and hirsute host plants

The host instar preferences of Encarsia bimaculata and Eretmocerus sp. nr. furuhashii parasitizing Bemisia tabaci and their development on four host plants, collard, eggplant, cucumber and tomato, were studied in the laboratory. Both of the parasitoids accepted all nymphal stages of B. tabaci, but E. bimaculata preferred third and fourth instars while Er. sp. nr. furuhashii preferred second and third instars under both choice and no choice conditions. Regardless of host stage parasitized, adults of parasitoids emerged only from fourth instars. When given the simultaneous choice of all instars, E. bimaculata reduced parasitization of first and second instars (3.73 and 4.76%, respectively) while increasing parasitization of third and fourth instars (5.44 and 6.93%, respectively), in contrast Er. sp. nr. furuhashii increased its parasitization of second and third instar nymphs (1.27 and 3.17%, respectively) and decreased that of first and fourth instars (7.0 and 3.06%, respectively). Host plants did not significantly influence instar preference for either parasitoid. Developmental periods of both the parasitoids from egg to adult emergence were longest when first instars were parasitized and shortest when fourth instars were selected. Parasitoid developmental time was generally shorter on glabrous plants than on hirsute plants.     

Phenotypic plasticity in Daphnia magna Straus: variable maturation instar as an adaptive response to predation pressure

Life history responses of four Daphnia magna clones at two food levels were studied to assess the importance of maturation instar on the plasticity of fitness responses under simulated mortality regimes. Females of the clones studied could vary offspring size with consequent effects on their maturation time. Significant genetic variability in life history and fitness responses, measured as the intrinsic rate of population increase, within and across food levels was observed, but most of this variation could be attributed to maturation instar differences among clones within and across environments. In the laboratory, without extrinsic mortality, females maturing earlier always had higher fitness than those maturing later, indicating a clear fitness cost of delaying maturity. Nevertheless using a model, we showed that the observed maturation instar effects on life history responses can lead to differences in fitness under different size-selective predation regimes, such that females with delayed maturity have higher fitness under invertebrate predation while females maturing earlier have higher fitness under fish predation regimes. These results suggest that intraclonal variation in offspring size and hence in the number of maturation instars can be an adaptation to living in habitats subject to temporal fluctuations in fish and invertebrate predation pressure.     

Clutch predation in great tinamous Tinamus major and implications for the evolution of egg color

Egg camouflage has been found to reduce predation in several ground‐nesting species. Therefore, the evolution of eggs that lack camouflage in ground nesting birds is puzzling. Even though clutch predation in the tropics is high, tinamous are the only tropical ground‐nesting birds that do not build a nest and do not lay cryptic eggs. I studied predation of great tinamou clutches in a lowland tropical forest and found that risk of predation was higher during incubation when the eggs are covered by the parent, than during laying when they are exposed, suggesting that predators primarily use cues from the incubating males to locate the clutch and not cues from the eggs. Clutch size had no effect on predation rate, even though larger clutches are more conspicuous to a human observer. Predation by visual cues is likely reduced during incubation by the camouflaged plumage and high nest attendance of males. If most predators use cues from the incubating male and not the eggs to locate clutches, then conspicuous egg color may have evolved in great tinamous as an intra‐specific signal. I evaluate hypotheses that may explain the maintenance of conspicuous egg color in tinamous.     

Evidence for search image in blackbirds (Turdus merula L.): short-term learning

A ‘search image’ is acquired as a result of a change in the ability of a predator to detect cryptic familiar prey. Blackbirds were presented with artificial prey dyed either to match the colour of the background (cryptic prey) or to contrast with the background (conspicuous prey). The results of experiment 1 provide some evidence that 10 wild blackbirds had more difficulty detecting cryptic prey than conspicuous prey. Detailed analysis of experiments 2 (11 wild blackbirds) and 3 (six captive blackbirds) revealed subtle changes in the reactions of the birds to cryptic prey. At first these birds were unable to detect cryptic prey, but subsequently improved their ability to detect such food. This short-term change is interpreted as evidence for search images.     

Cotesia plutellae parasitizing Plutella xylostella: Host-age dependent parasitism and its effect on host development and food consumption

The braconid Cotesia plutellae(Kurdjumov) (Hymenoptera: Braconidae) is amajor solitary, larval endoparasitoid of thediamondback moth, Plutella xylostella(L.) (Lepidoptera: Plutellidae). Parasitism oflarvae of different host instars and fourdevelopmental ages of the 4th instar ofthe pest was examined. The effects of hostinstar at initial parasitization on thedevelopment, survival, size and fecundity ofthe parasitoid were determined in thelaboratory at 25 °C. The effects ofparasitism on host development and foodconsumption were investigated at 28 °C.Cotesia plutellae could parasitize larvaeof all four instars of P. xylostella, butpreferred 2nd and 3rd instars. In achoice test, the relative parasitism indicesfor 2nd, 3rd and 4th instarswere 0.37, 0.39 and 0.24, respectively.Parasitism decreased sharply with increasinghost age in the 4th instar and approachedzero in host larvae that had gone beyond 37%of 4th stadium. The development time andthe final adult size of the parasitoid variedwith the host instar at initial parasitization.Parasitoids with initial parasitism in the4th instar hosts had the shortestdevelopment time, followed by those in the3rd instar, and then by those in the2nd instar. Parasitoids startingparasitism in 2nd instar hosts weresmaller in body size than those starting in the3rd or 4th instar. However, resultantfemales starting parasitism in 3rd instarhosts had the highest fecundity. Parasitizedlarvae exhibited longer development time andincreased food consumption compared withunparasitized ones. This study presents thefirst record that a solitary parasitoidregulates host behavior leading to an increasein food consumption by the host.