Assessment of patch quality by ladybirds: relative response to conspecific and heterospecific larval tracks a consequence of habitat similarity?

Summary. Aphid colonies can reach high levels of abundance but last for short periods of time. The larvae of aphidophagous ladybirds (Coleoptera: Coccinellidae) that feed on these colonies might therefore suffer from starvation, which favours the occurrence of cannibalism and intraguild predation. Thus, the assessment of patch quality becomes crucial and it has been shown that female ladybirds refrain from laying eggs in the presence of an oviposition deterring semiochemical deposited by their larvae. Adalia bipunctata (L.), Adalia decempunctata (L.) and Coccinella septempunctata L. are 3 sympatric species of ladybirds, which can co-occur in aphid colonies. As a consequence, their eggs and larvae are under threat, not only from cannibalism but also intraguild predation. Females should, therefore, also use the tracks deposited by heterospecific larvae to assess the quality of aphid colonies as oviposition sites. The expectation is that: 1- the strength of the reaction to each other’s larval tracks should be correlated with percentage habitat overlap and that 2- the reaction to conspecific larval tracks should be stronger than to heterospecific tracks. In order to test these hypotheses, females’ oviposition behaviour was analysed and a chemical analysis of the tracks of their larvae undertaken. The results show that oviposition behaviour is not related to habitat overlap. Both species of Adalia react to tracks of their own larvae and those of C. septempunctata, but A. decempunctata reacted more strongly than A. bipunctata. C. septempunctata reacted very slightly to its own tracks but not to those of either species of Adalia. The larval tracks are mainly composed of alkanes. Those of the two species of Adalia are qualitatively 100% similar and 60% so when the quantitative results are compared. They are, however, only 24–29% similar to those of Coccinella septempunctata.     

Social feeding in ladybird beetles: adaptive significance and mechanism

Summary. Young larvae of Adalia bipunctata search an area more intensively when exposed to the odour from other larvae feeding on aphids than when exposed only to the odour of aphids. In an olfactometer young larvae were significantly attracted either to the odour of crushed aphids or larvae feeding on aphids, but not to that of aphids, larvae, larvae plus aphids or larvae feeding on an artificial diet. That is, the change in searching behaviour appears in response to a volatile released by aphids when attacked. The odour released by crushed aphids is made up entirely of aphid alarm pheromone, β-farnesene. It is likely that the adaptive significance of this response is that it increases the ability of larvae to locate larvae that have already caught prey. By sharing the aphid kill of another larva it is likely that a first instar ladybird larva greatly increases its probability of surviving to the next instar. It is suggested that this social feeding is facilitated by egg clustering, which also may additionally account for why aphidophagous ladybirds lay their eggs in clusters. Received 28 February 2000; accepted 24 March 2000     

Intraguild predation by <Emphasis Type="Italic">Harmonia axyridis</Emphasis> on coccinellids revealed by exogenous alkaloid sequestration

Summary.  Under laboratory conditions, the multicolored Asian lady beetle, Harmonia axyridis is well known as an intraguild predator of other ladybirds. However the real impact of this exotic species on native species was poorly investigated in the field. Because many ladybird species produce alkaloids as defensive compounds, we propose here a new method of intraguild predation monitoring in coccinellids based on alkaloid quantification by GC-MS. In laboratory experiments, adaline was unambiguously detected in fourth instar larvae of H. axyridis having ingested one egg or one first instar larva of Adalia bipunctata. Although prey alkaloids in the predator decreased with time, traces were still detected in pupae, exuviae and imagines of H. axyridis having ingested one prey when they were fourth instar larvae. Analysis of H. axyridis larvae collected in two potato fields shows for the first time in Europe the presence of exogenous alkaloids in 9 out of 28 individuals tested. This new method of intraguild predation detection could be used more widely to follow the interactions between predators and potential chemically defended insect preys.     

The effects of three sympatric ladybird species on oviposition by Menochilus sexmaculatus (Coleoptera: Coccinellidae)

Oviposition site selection has a strong impact on the spatial distribution and sustenance of a species. This site selection by ladybirds (Coleoptera: Coccinellidae) is known to be well mediated amongst other factors by the oviposition deterring pheromones present in conspecific larval tracks. It would be also useful to the organism to be sensitive to heterospecific larval tracks, to protect from intraguild predation; however, this has not yet garnered much attention and there are only a few scattered studies with ambiguous results. The present study thus investigates the oviposition deterring effects of heterospecific presence and semiochemicals of heterospecific life stages (eggs, fourth instar larvae, pupae, adult males and females) of ladybird species, viz. Coccinella septempunctata, C. transversalis, Propylea dissecta on females of Menochilus sexmaculatus. Results reveal that the presence of all heterospecific life stages inhibits oviposition of M. sexmaculatus and the inhibition is density dependent. Semiochemicals of eggs, larval and adult tracks also show density-dependent inhibitory effects. The semiochemical-induced oviposition inhibition was stage specific with respect to the degree of inhibition. Of all heterospecific species tested, maximum and minimum oviposition deterrence of M. sexmaculatus was against C. septempunctata and P. dissecta, respectively. Comparison of our previously published results on oviposition inhibition in M. sexmaculatus due to conspecific presence with the current ones revealed increased inhibition in conspecific presence than heterospecific indicating ability to differentiate.     

Does cannibalism in Spodoptera frugiperda (Lepidoptera: Noctuidae) reduce the risk of predation?

The incidence of cannibalism of larval Spodoptera frugiperda (Lepidoptera: Noctuidae) on maize under field conditions was investigated using field cages. Cannibalism was found to account for approximately 40% mortality when maize plants were infested with two or four fourth-instar larvae over a 3-day period. Field trials examined the effect of larval density on the prevalence of natural enemies of S. frugiperda. The abundance of predators (earwigs, staphylinids, other predatory beetles, and Chrysoperla spp.) was significantly greater on maize plants with higher levels of larval feeding damage, while the relationship between predator abundance and number of S. frugiperda larvae per plant was less clear. As larval damage is probably a more reliable indicator of previous larval density than numbers collected at an evaluation, this indicates that predation risk will be greater for larvae living in large groups. Parasitism accounted for 7.1% mortality of larvae in sorghum, and involved six species of Hymenoptera and Tachinidae. There was no effect of larval density or within-plant distribution on the probability of larval attack by parasitoids. The selective benefits of cannibalism, in relation to the risk of predation and parasitism, are discussed. Received: 23 March 2000 / Accepted: 24 June 2000     

Ladybird mothers mitigate offspring starvation risk by laying trophic eggs

A large proportion of ladybird beetle (Coleoptera: Coccinellidae) eggs are apparently infertile—they do not develop an embryo and are consumed by larvae hatching within the egg batch. The predicted benefits of egg consumption for larvae are empirically well supported. An important question, however, remains: are these eggs a maternal strategy to feed offspring (i.e., trophic eggs) or did egg eating evolve to exploit unavoidably infertile eggs? We investigated the adaptive value of infertile eggs in laboratory experiments with multicoloured Asian ladybirds (Harmonia axyridis). Female H. axyridis were assigned to low and high resource environments for brief intervals; we predicted that tactics to facilitate egg cannibalism, such as infertile egg production and hatching asynchrony, would be adopted in low food environments in which starvation risk for offspring is greater. We conducted two experiments in this manner that provided females with information about resource levels through prey feeding or scent. We also observed female oviposition patterns and tested for infertile egg distributions that departed from random. Females produced 56% more infertile eggs in the low vs. the high food treatment; however, hatching synchrony did not change. We consider a potential confound between information and nutrition state unlikely because ladybirds are well able to tolerate low food for 24 h, the duration of trials, and because females were in good condition when trials began. Results suggest that ladybirds use information from prey encounter to manipulate the proportion of trophic eggs in a manner consistent with the adaptive hypothesis, the first evidence of trophic egg plasticity in a non-eusocial insect.     

The occurrence of aristolochic acids in neotropical troidine swallowtails (Lepidoptera: Papilionidae)

Summary. Analysis of individuals of 17 troidine species demonstrated the presence of aristolochic acids in these butterflies in varying concentrations. Although aristolochic acids do not occur in Aristolochia galeata leaves, they were present in Battus polydamas larvae reared on these leaves, and thus may be synthesized by the larvae from chemical precursors in the plant. Received 17 August 1999; accepted 20 January 2000     

Seaweed secondary metabolites as antifoulants: effects of Dictyota spp. diterpenes on survivorship, settlement, and development of marine invertebrate larvae

Summary. A recent investigation showed that the brown seaweed Dictyota menstrualis was unfouled relative to co-occurring seaweeds, and that larvae of fouling invertebrates avoided settling on D. menstrualis due to chemicals on its surface. The secondary metabolites dictyol E and pachydictyol A are among the compounds found on this alga's surface. In the present study, we tested the effects of specific diterpenes from Dictyota on the survivorship, growth, and development of invertebrate larvae and developing juveniles that could foul seaweeds. Exposure to dictyol E, dictyol B acetate, pachydictyol A, and dictyodial from Dictyota menstrualis and D. ciliolata caused significant larval mortality, abnormal development, and reduce growth rates for three species of co-occurring invertebrates when their larvae were forced into contact with these metabolites. Larvae were damaged at metabolite concentrations as low as 5% of maximum possible surface concentrations of these compounds for the populations of Dictyota we studied. The negative effects of these secondary metabolites on potential foulers, in conjunction with data demonstrating larval avoidance of dictyol-covered surfaces, suggest that these compounds could function as chemical defenses against fouling, and could select for larvae that avoid hosts producing these metabolites. Received 25 May 1998; accepted 22 June 1998.     

Toxicity assays of ladybirds using natural predators

Nestling blue titsParus caeruleus L. were given diets containing homogenized ladybirds, to assess the effects of their chemical defences. The 2spot, 10spot and water ladybirds produced no apparent toxic effects when small numbers were given at regular intervals.The pine and kidney-spot ladybirds slightly inhibit growth and may be toxic to very young nestlings. The Water ladybird is extremely distasteful to this predator, despite its lack of toxicity. The results are discussed with reference to the proposed Müllerian and Batesian mimetic relationships between the ladybird species.     

Lingual and biting responses to prey chemicals by ingestively naive scincid lizards: discrimination from control chemicals,time course,and effect of method of stimulus presentation

Summary. We tested responses to prey chemicals by lizard hatchlings of an oviparous species and neonates of a viviparous species, neither of which had never eaten. Both species responded more strongly to prey chemicals than to odorous and odorless control stimuli presented on cotton swabs. Although only a few species have been examined, all that have been tested have an innate capacity for prey chemical discrimination, suggesting that this innate response to prey chemicals is widespread among lizards that use the lingual-vomeronasal system to locate and identify prey. Innate prey chemical discrimination has the great advantage of permitting lizards lacking prior experience with food to respond appropriately to chemical cues associated with food. Both species discriminated prey chemicals from control substances at age three days, earlier than previously known. Our data hint that Mabuya macularia may be capable of discrimination on its day of birth, but further study is needed to determine the exact onset. A stronger tendency to attack swabs bearing prey chemicals by Scincella lateralis than by M. macularia may be explained by differences in defensiveness near an experimenter or by differences in the importance of visual prey cues for confirmation of chemical cues in the natural habitats of these species. In M. macularia responses to the control stimuli declined over days of testing, suggesting habituation, but responses to prey chemicals did not habituate by the third day of testing, which is interpreted as a possible adaptive response to permit location of food. In the standard method of stimulus presentation, a cotton swab bearing a chemical stimulus is placed anterior to a lizard's snout. We tested a new method in which the swab was placed in continuous contact with the lizard's anterior labial scales. The new method elicited significantly stronger responses from M. macularia. We discuss reasons for this finding and applications for the new method. Received 2 September 1999; accepted 15 December 1999     

Is the alkaloid in 2spot ladybirds (Adalia bipunctata) a defence against ant predation?

Garden black ants,Lasius niger L., in a laboratory colony, attacked three species of live ladybirds found near their nest, killing the smaller two species. A second colony was offered artificial diets containing crushed ladybirds of two species, and the ants' choice of feeding site noted. Both the diets were aversive compared to control, but that containing 7spot,Coccinella septempunctata L., was more aversive than the diet containing 2spot,Adalia bipunctata L. The implications of this lesser protection for 2spots in terms of the chemical defence of the species are discussed.     

The role of intraguild predation in the population dynamics of small pelagic fish

In this paper, we argue that understanding marine ecosystem functioning requires a thorough appreciation of the role of intraguild predation to system dynamics. The theoretical predictions of intraguild predation models might explain some of the community features observed in marine ecosystems such as low diversity in upwelling and productive systems and species alternation in response to moderate external forcing. Finally, we argue that an ecosystem approach to fisheries requires that the size–structure of fish populations should be taken into account and that it is extremely important to account for the predators of early stages (eggs and larvae) to gain a thorough understanding of the key interactions between species.     

Sequestration of aristolochic acids by the pipevine swallowtail, Battus philenor (L.): evidence and ecological implications

Summary. It has long been assumed that the North American pipevine swallowtail, Battus philenor (L.) (Papilionidae, Troidini), is protected from natural enemies by aristolochic acids sequestered from its Aristolochia food plants. This study confirmed that populations of B. philenor from Virginia and east Texas sequester these compounds. A comparison of the aristolochic acid profiles of the Virginia butterflies and their A. macrophylla food plants revealed several differences. The aristolochic acid fraction of the foliage was dominated by aristolochic acids I and II, whereas the insects had a much lower proportion of aristolochic acid II and contained, in addition, substantial amounts of aristolochic acids Ia and IVa, which were not detected in the plants. The eggs, larval integument, osmeterial glands, pupal cuticle, and adults (wings and bodies) all contained aristolochic acids. These findings help explain the abundant ecological data indicating that both immature and adult B. philenor are unpalatable and protected from natural enemies. Received 7 April 2000; accepted 31 May 2000     

Induction of host specificity in larvae of Manduca sexta: chemical dependence controlling host recognition and developmental rate

Summary. The tobacco hornworm, Manduca sexta L. (Lepidoptera: Sphingidae) is a specialist on Solanaceae. This host specificity is induced as the larva feeds on solanaceous foliage, so that solanaceous-reared larvae will refuse to feed on other plants. Experiments were designed to determine the role of dietary constituents on the induction of host specificity and the effects of these on development of M. sexta. Choice assays using leaf discs of cowpea, Vigna sinensis (Fabaceae), were used to monitor the isolation of relevant chemical cues from foliage of potato. An aqueous extract of potato foliage strongly stimulated feeding. This extract was partitioned with n-butanol under alkaline conditions to obtain a highly active butanol extract. Reversed phase flash chromatography with a water-methanol gradient gave an active fraction that was used as a supplement for wheat germ-based artificial diet. Larvae reared on this s-diet became dependent on potato allelochemicals for initiation and continuation of feeding activity. These larvae also developed faster than larvae reared on the control p-diet, but no effect on adult mass was detected. Further flash chromatography of the active fraction under alkaline conditions provided a highly active sub-fraction, and semi-preparative HPLC using gradients of water and acetonitrile resulted in the isolation of a single compound. Bioassays indicated that this compound alone can account for host recognition by solanaceous-reared larvae. The results suggest that the mechanism of induced host specificity in M. sexta involves development of dependence on this compound. Received 21 December 1999; accepted 14 March 2000     

Larval chemical defence and evolution of host shifts in Chrysomela leaf beetles

Summary. Larvae of Chrysomela leaf beetles release for defence volatile compounds belonging to various chemical families. This study focuses on the defensive strategy based on the esterification of isobutyric acid and 2-methylbutyric acid with a wide variety of alcohols taken up from the host plant. To date, only two species are known to produce these repellents C. interrupta, which is associated with Betulaceae and C. lapponica which occurs either on Betulaceae or Salicaceae.? In order to know if other species have developed this chemical defence and how the food plant influences the secretion of these toxins, we targeted by mass spectrometry the presence of iso- and 2-methylbutyric acids and esters of them in the defensive secretions of Chrysomela larvae exclusively associated with Betulaceae or Salicaceae. ?Screening analyses reveal that the synthesis of these compounds is a common character restricted to all the members belonging to the C. interrupta group sensu Brown (1956) regardless of the host-plant family. These results suggest that the biochemical mechanism leading to the synthesis of these compounds could be considered as a synapomorphy meaning that the group is probably monophyletic. ?Defensive secretions of the members of the interrupta group are quantitatively assayed for iso- and 2-methylbutyric acids and their (Z)-3-hexenyl esters. Results reveal a chemical plasticity developed by Chrysomela species associated with Salicaceae. The amounts of iso- and 2-methylbutyric acids derivatives and of salicylaldehyde in their larval secretions depend on the food plant and on its content in phenolglucosides. Received 5 October 1998; accepted 25 November 1998.     

Chemical mimicry in the root aphid parasitoid Paralipsis eikoae Yasumatsu (Hymenoptera: Aphidiidae) of the aphid-attending ant Lasius sakagamii Yamauchi & Hayashida (Hymenoptera: Formicidae)

Summary. An aphidiid wasp, Paralipsis eikoae, was associated with both Lasius niger and L. sakagamii attending the wormwood root aphid Sappaphis piri. An L. sakagamii worker was observed carrying a winged female P. eikoae to its nest with its mandible, but it did not kill the wasp. Once accepted by the ants, the wasp often mounted and rubbed against the worker ants and sometimes teased them to regurgitate food to itself. No workers in the colony attacked the wasp. Conspecific foreign workers, however, viciously attacked the wasp when encountered. Gas chromatography-mass spectrometry analyses showed that the accepted wasp had complex cuticular hydrocarbons that were very similar to those of its host ants, whereas the winged wasps collected outside the ant nest showed only a series of n-alkanes. Additionally, the accepted wasp had a hydrocarbon profile closer to that of its host ants than to the conspecific foreign ants. We believe the wasp mimics ant cuticular hydrocarbons to integrate into the ant nest, acquiring the hydrocarbons by mounting and rubbing against the ants. In contrast, the cuticular hydrocarbons of the emerged wasp contained larval and pupal hydrocarbons of L. sakagamii that were also similar to those of L. niger. Both ant species rejected adult workers of the other species but accepted their larvae and pupae. We suggest that the emerged P. eikoae mimics the cuticular hydrocarbons of these Lasius larvae and pupae, which allows P. eikoae to be accepted by both L. sakagamii and L. niger. Received 11 March 1998; accepted 22 July 1998.     

Different antipredator behaviour in two anuran tadpoles: effects of predator diet

Recent investigations have indicated that animals are able to use chemical cues of predators to assess the magnitude of predation risk. One possible source of such cues is predator diet. Chemical cues may also be important in the development of antipredator behaviour, especially in animals that possess chemical alarm substances. Tadpoles of the common toad (Bufo bufo) are unpalatable to most vertebrate predators and have an alarm substance. Tadpoles of the common frog (Rana temporaria) lack both these characters. We experimentally studied how predator diet, previous experience of predators and body size affect antipredator behaviour in these two tadpole species. Late-instar larvae of the dragonfly Aeshna juncea were used as predators. The dragonfly larvae were fed a diet exclusively of insects, R. temporaria tadpoles or B. bufo tadpoles. R. temporaria tadpoles modified their behaviour according to the perceived predation risk. Depending on predator diet, the tadpoles responded with weak antipredatory behaviour (triggered by insect-fed predators) or strong behaviour (triggered by tadpole-fed predators) with distinct spatial avoidance and lowered activity level. The behaviour of B. bufo in predator diet treatments was indistinguishable from that in the control treatment. This lack of antipredator behaviour is probably related to the effective post-encounter defenses and more intense competitive regime experienced by B. bufo. The behaviour of both tadpole species was dependent on body size, but this was not related to predator treatments. Our results also indicate that antipredator behaviour is largely innate in tadpoles of both species and is not modified by a brief exposure to predators. Received: 22 August 1996 / Accepted after revision: 31 January 1997     

The roles of nicotine and natural enemies in determining larval feeding site distributions of Manduca sexta L. and Manduca quinquemaculata (Haworth) on tobacco

Summary. Field observations indicated that hornworms select feeding sites non-randomly on tobacco. We tested the hypotheses that differences in feeding site locations of larvae of Manduca sexta L. and Manduca quinquemaculata (Haworth) (Lepidoptera: Sphingidae) on tobacco could be explained by differential nicotine concentrations within plants and leaves, species-specific responses to nicotine, or pressure exerted by natural enemies. Results showed that third-instar larvae of M. sexta fed more proximally and centrally on the leaf, whereas M. quinquemaculata fed more distally. Within-plant selection of leaves did not differ; both species selected leaves in the middle region of the plant. Nicotine concentrations in a high nicotine genotype, NC95, varied within each leaf, increasing 2—3 fold from the basal to apical portion of the leaf, and within each plant, increasing 7—10 fold from the first fully expanded leaf to the twelfth (lowest) leaf. In laboratory bioassays, both Manduca species responded to nicotine as a feeding deterrent. Electrophysiological studies demonstrated that gustatory organs of both species responded to nicotine at concentrations found in tobacco leaves and that M. quinquemaculata generally showed a less vigorous response to nicotine than M. sexta. Field mortality of M. sexta due to parasitism by Cotesia congregata (Say) and to parasitism and predation combined differed among feeding sites; predation alone did not. Results suggest that although nicotine concentration and species specific responses to nicotine play a role in determining feeding site locations, pressure exerted by natural enemies, especially parasitism by C. congregata, is more important. Received 22 February 2000; accepted 20 July 2001.     

Filial cannibalism in burying beetles

Summary Infanticide is a common phenomenon in many animal groups, but filial cannibalism, the deliberate killing and consumption by parents of their own young, is extremely unusual. The burying beetle Nicrophorus vespilloides Herbst has a limited food supply, in the form of a buried corpse, on which to raise its young. On corpses weighing 10–15 g, clutch size in the lab is such that complete hatching can support without severe reduction in the individual weights of final instars. The parents reduce the brood by killing and eating almost half of the first stage larvae. It is suggested that, in the field, predation of eggs and newly hatched larvae may be heavy, and that the excess eggs are laid as an insurance. If survival is then unusually high, superfluous young are killed by the parents before competition for food can occur.     

Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis

Carotenoid- and melanin-based colors are valuable indicators of quality in many vertebrates, but their signaling role in invertebrates remains relatively unexplored. The Asian ladybird beetle Harmonia axyridis is an ideal organism for studies of this nature because males and females exhibit highly variable red and black colors on their elytra and are chemically defended with an alkaloid (harmonine). We used digital photography to quantify elytra coloration and absorbance spectrophotometry and gas chromatography mass spectrometry analyses to quantify pigment and alkaloid concentrations, respectively, in wild-caught male and female H. axyridis. We predicted that extensive or intense coloration would be an aposematic signal of high-alkaloid stores. We found that carotenoid pigments largely controlled variation in red elytra coloration. There was no relationship between alkaloid content and either elytra redness or carotenoid pigment concentration in either sex. However, we found a positive correlation between the extent of elytra coloration and alkaloid content. Animals with proportionally more red (or less black) on the elytra were more alkaloid-rich; this relationship was particularly strong in females. We also found that females with lighter black spots had greater amounts of harmonine than those with darker spots. These results suggest that elytra color patterns have the potential to reveal information about chemical defensiveness to mates or predators. Prior studies in this species show that nonmelanic forms are typically less active and yet more sexually attractive than melanic forms, and both results may be explained by the fact that nonmelanics are better chemically defended.