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.     

Costs of reproduction and geographic variation in the reproductive tactics of the mosquito Aedes triseriatus

Intraspecific host discrimination is widespread in solitary parasitoids whose adult females forage for and evaluate host suitability, whereas interspecific discrimination is less common. In some parasitoid species, mostly Diptera and Coleoptera, the larva performs the last step of host searching. It has been suggested that host discrimination will rarely occur in such host-seeking larvae because their low mobility results in a low host encounter rate. We determined the extent to which the larvae of Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae), a solitary parasitoid of aggregated Diptera pupae: (1) discriminated between unparasitized hosts and hosts parasitized by conspecifics; (2) used semiochemical cues to discriminate; (3) were influenced by life expectancy, presence of conspecifics and host availability in their host acceptance decision; and the extent to which (4) A. bilineata and A. bipustulata L., a species exploiting the same hosts and occurring sympatrically, showed interspecific host discrimination. A. bilineata larvae were able to discriminate between unparasitized hosts and hosts parasitized by conspecifics in a choice experiment. Such behavior has never previously been described for a coleopteran parasitoid or for a parasitoid species whose larvae perform host searching. Host discrimination in this species was not based on the presence of visual or tactile cues (e.g., entrance holes) but rather on chemical cues. The life expectancy of A. bilineata larvae was significantly shorter in the presence than in absence of hosts, and older larvae had lower parasitism success than young larvae in a 24-h experiment. However, the host acceptance decision of A. bilineata larvae was not influenced by larval age or the presence of conspecifics when the ratio of hosts per larva was greater than or equal to 1. When hosts were scarce, the degree of superparasitism increased significantly with the number of foraging conspecifics and the age of the larvae. Both species of Aleochara showed intra- and interspecific host discrimination in a choice experiment. In contrast to A. bipustulata, A. bilineata larvae more frequently parasitized hosts parasitized by A. bipustulata than those parasitized by conspecifics. We suggest that host discrimination will be frequent in solitary parasitoids with host-seeking larvae when hosts are aggregated. Received: 4 June 1998 / Accepted: 1 September 1998     

Aggressive Interactions and Risk of Fish Predation for Larval Damselflies

Larval damselflies frequently engage in aggressive interactions that may increase their risk of fish predation. To test this we analyzed the behavior of larval Ischnura verticalis exposed to both conspecifics and fish predators. Larvae in the presence of conspecifics oriented, struck, and swam more but crawled less compared to solitary larvae; the presence of fish reduced, or tended to reduce, all behaviors. Fish struck more at interacting larvae compared to noninteracting larvae. Increased attack rate by fish likely reflects the increase in the very active swimming behavior by larvae and suggests a conflict between antipredator behaviors. Swimming is an appropriate response to avoid predation by odonate larvae which normally ambush prey but is clearly dangerous when fast-swimming fish that cue in on movement are nearby.     

Behavioral responses to fish kairomones and autotomy in a damselfly

The threat-sensitivity hypothesis predicts that prey species assess and adjust their behavior in accordance with the magnitude of the threat posed by a predator. A largely overlooked characteristic of a prey that will affect its sensitivity to predators is its history of autotomy. We studied threat-sensitive behavior to fish kairomones in larvae of Ischnura elegans damselflies, which had undergone autotomy, from a fishpond and from a fishless pond. In agreement with their higher perceived risk, larvae from the fishpond showed fewer rigid abdomen bends, foraged less and walked more slowly than larvae from the fishless pond. In line with their higher vulnerability to predators, larvae without lamellae spent less time foraging than larvae with lamellae. There was a decrease in swimming activity in the presence of fish kairomones except for larvae with lamellae from the fishless pond. This may reflect differences in vulnerability of larvae without lamellae between pond types. Such context-dependent responses in activity to kairomones should be kept in mind when evaluating the ability of a prey to recognize kairomones.     

A tadpole-induced polyphenism in the salamander Hynobius retardatus

Abstract.— Larvae of the salamander Hynobius retardatus have two distinct morphs: normal and broad-headed, cannibal morphs. We performed three experiments to differentiate among the following hypotheses: The broad-headed morph is induced to allow: (1) feeding on nutritious conspecifics; (2) exclusion of strong competitors for food or space; or (3) feeding on large, tough prey when smaller prey items are unavailable. When newly hatched larvae were reared with a heterospecific, Rana pirica (an anuran amphibian) tadpoles, the broad-headed morph was induced more frequently compared with those reared with conspecifics. The phenotype expressed depended on the size of the tadpoles: The broad-headed morph occurred more frequently with small and the normal morph with large tadpoles. Metamorphosis occurred sooner in larvae fed conspecifics compared with those fed heterospecific tadpoles, and the mean growth rate of larvae fed conspecifics was significantly faster than that of those fed tadpoles, suggesting that the heterospecific tadpoles were less nutritive than the conspecifics. These results do not support the hypotheses that the broad-headed morph evolved for consuming conspecifics because of their better balance of nutrients or for excluding strong competitors for food or space. We tentatively conclude that the morph evolved to eat large, tough prey, including both conspecifics and heterospecific tadpoles. Because H. retardatus usually spawns very early in the spring in small ponds partially covered with ice and snow, newly hatched larvae may starve from the lack of proper food owing to extremely low water temperatures. Thus, the broad-headed morph of H. retardatus may represent a cold-habitat adaptation to overcome the severe circumstance when the only food items available are relatively large conspecifics or heterospecific tadpoles.     

Mating tactics and courtship behavior inCleogonus rubetra (Fabricius) (Coleoptera: Curculionidae)

Females of the tropical weevilCleogonus rubetra oviposit into fruits of the leguminous treeAndira inermis, and larvae develop in the pulp and seed of these fruits. We hypothesized three alternative tactics by which males might secure matings. By using focal observations of males and by evaluating predictions specific to each hypothesis, we demonstrate that males search within aggregations of conspecifics for receptive females, and upon finding a suitable partner, males mount and perform courtship behavior consisting of stroking the eyes and sides of the female's abdomen. Males also stridulate and emit a sequence of short buzzing sounds. While mounted, males actively prevent rival males from mating with their partner. Males defend their mates for a mean duration of 3.7 h (including copulation). As predicted, paired males were larger than solitary individuals, although the difference was marginally nonsignificant. The overabundance of fruits relative to males, the prolonged period during which females are active, and the probability of last male sperm precedence are factors that may have contributed to the evolution of this female-defense tactic by males. Paired females were significantly larger than solitary females. We observed no competition among females for mates, and the correlation between elytron length of paired males and females was not significant.     

Facilitated predation through interaction between life stages in the stinkbug predatorperillus bioculatus (Hemiptera: Pentatomidae)

Competitive interactions in arthropod predators are well-known, but positive interactions have received less attention. The two-spotted stinkbugPerillus bioculatus often feeds gregariously on leaf beetle larvae and caterpillar prey. Consequences of prey sharing amongP. bioculatus conspecifics of dissimilar size (instar) was studied using Colorado potato beetle (CPB) prey. Rearing second-instar (N2) nymphs ofP. bioculatus with an N5 conspecific facilitated early feeding on L4 CPB larvae (a difficult prey to handle by N2 nymphs but not by N5’s), thus increasing survival and accelerating development. One in every 20 cases ofP. bioculatus foraging in the field was accounted for by pairs or small groups of mostly feeding individuals. CPB egg masses and L4’s represented a disproportionate number of cases of aggregated feeding byP. bioculatus, compared to feeding singly. Small CPB larvae decreased in the diet of aggregated stinkbugs compared to L4 larvae and egg masses, suggesting that sharing these prey may be favorable or unavoidable. In a field test measuring residence/survival of N2’s limited to L4 prey, the N2’s rate of residence/survival increased significantly when large nymphs acting as food providers were also present. The function of communal feeding inP. bioculatus is discussed, as well as the potential for greater impact on prey density that may be expected from tolerance to opportunistic feeding by conspecifics in slightly gregarious predators.     

Do damselfly larvae recognize and differentially respond to distinct categories of macroinvertebrates?

Zygopteran larvae normally encounter other aquatic macroinvertebrates that are predators, competitors, and prey and should therefore demonstrate varied responses when faced with different categories of opponent. In a laboratory experiment individual final-instarIschnura posita (Hagen) larvae were observed in interactions with six categories of invertebrate opponents. The opponent categories were a nonconspecific damselfly and a small crayfish, which represented threatening opponents because they were larger than theI. posita subject larva, and a mayfly and a stonefly, which constituted nonthreatening opponents because they were smaller than the subject larva. The levels of threat posed by conspecific larvae of final and penultimate instar were inferred by comparison to the other opponent categories. Multivariate analysis showedI. posita's response differed between the two larger opponents, but responses were statistically indistinguishable between the two smaller opponents. Larvae retreated, moved around the stalk, and struck their opponents with their lamellae more often in the presence of a crayfish than the nonconspecific zygopteran. In contrast, they assumed an S-bend posture frequently with the zygopteran. Responses toward final-instar conspecifics differed from responses toward the larger opponents. Effectively, larvae wagged their abdomens only in the presence of final-instar conspecifics and retreated and moved around the stalk less frequently in these trials. Responses toward the smaller conspecifics differed from the responses to the small opponents. Larvae struck penultimate-instar conspecifics with their lamellae more frequently than the other small opponents. Our results suggest that larval zygopteran behaviors (such as S-bend and SCS) that have previously been described as intraspecific displays are of a more general nature and used toward a variety of opponents, whereas wag is unique to intraspecific interactions inI. posita.     

Trail Marking and Processionary Behavior of the Larvae of the Weevil Phelypera distigma (Coleoptera: Curculionidae)

We present here the results of an investigation of the behavioral bases of the first documented instance of trail marking and processionary behavior in a beetle. The larvae of Phelypera distigma (Coleoptera: Curculionidae) forage communally, moving over the host plant in head-to-tail processions. Our study shows that the larvae secrete a pheromone from the ventral surface of the posterior abdomen that both elicits and guides the collective locomotion of the cohort. The pheromone is soluble in acetone and other nonpolar solvents and is relatively short-lived, eliciting trail following for less than 4 h after its deposition. When in processionary formations, larvae stimulate locomotion in others by rapidly bobbing their heads against sets of setae that occur on the lateral flanks of the posterior tips of the abdomens of precedent individuals. Larvae are also strongly attracted to tactile or chemotactile stimuli found at the tip of the abdomen of other larvae and their response to lures made of eviscerated abdomens show that such stimuli take precedence over the trail pheromone in eliciting and orienting locomotion. The cycloalexic formations adopted by resting larvae maximize the amount of body contact possible in a two-dimensional aggregate and allow tactile signals to rapidly radiate through the groups, alerting all members of a cohort to the onset of bouts of activity.     

Ontogenetic changes in habitat selection during settlement in a coral reef fish: ecological determinants and sensory mechanisms

The behavior of marine larvae during and after settlement can help shape the distribution and abundance of benthic juveniles and therefore the intensity of ecological interactions on reefs. Several laboratory choice-chamber experiments were conducted to explore sensory capabilities and behavioral responses to ecological stimuli to better understand habitat selection by “pre-metamorphic” (larval) and “post-metamorphic” (juvenile) stages of a coral reef fish (Thalassoma hardwicke). T. hardwicke larvae were attracted to benthic macroalgae (Turbinaria ornata and Sargassum mangarevasae), while slightly older post-metamorphosed juveniles chose to occupy live coral colonies (Pocillopora damicornis). Habitat choices of larvae were primarily based upon visual cues and were not influenced by the presence of older conspecifics. In contrast, juveniles selected live coral colonies and preferred those occupied by older conspecifics; choices made by juveniles were based upon both visual and olfactory cues from conspecifics. Overall, the laboratory experiments suggest that early life-history stages of T. hardwicke use a range of sensory modalities that vary through ontogeny, to effectively detect and possibly discriminate among different microhabitats for settlement and later occupation. Habitat selection, based upon cues provided by environmental features and/or by conspecifics, might have important consequences for subsequent competitive interactions.     

Social Behavior of Larvae of the Neotropical Processionary Weevil Phelypera distigma (Boheman) (Coleoptera: Curculionidae: Hyperinae)

Socially gregarious behavior among free‐living leaf‐eating insect larvae occurs mostly among Lepidoptera, Symphyta, and a few Chyrsomelidae (Coleoptera). However, the Neotropical hyperine curculionid Phelypera distigma has also evolved this lifestyle, exhibiting a suite of social behaviors unique among beetles. The larvae are nomadic processionary foragers that punctuate foraging bouts with rosette‐shaped resting formations (cycloalexy). Larvae also vibrate or bob their heads rapidly when moving, especially when in contact with conspecifics, and this suggests acoustic or vibrational communication. In this study we used observational and experimental approaches to investigate the basis of processionary, cycloalexic,and head‐vibration behavior of this species. Larvae used both trail pheromones and thigmotactic signals to organize themselves into head‐to‐tail processionary columns. The trail pheromone, produced from the center of the abdomen, remains active for up to 4 h. Processions are not consistently led by particular individuals, but dynamically change over time and often temporarily break into two or more subprocessions. Subprocessions reunite through use of the trail pheromone. We found no evidence that head‐bobbing generates attraction through substrate‐borne or acoustic signals, but this behavior functions in direct contact to excite group activity. Time‐lapse videography used to analyze cycloalexic group formation showed that larvae transition from feeding in a line along the leaf margin to cycloalexic formations on the upper leaf surface via a coordinated back‐up movement that brings the posterior tip of their abdomens into contact. We identify three phases of cycloalexic formation: line‐up, back‐up, and an adjustment phase. Complete assembly can be achieved in as little as 5 s, but often the two phases establishing the basic rosette lasts 5–10 min, while the adjustment phase slowly tightens the group over a period of up to an hour. Collectively these studies present the first documented case of chemical trail marking in a beetle, and provide insight into a remarkable social‐behavioral repertoire convergent in key respects with the better‐studied social caterpillars and sawflies.     

Abdominal grooming in the cockroach: Development of an adult behavior

Chemical or tactile irritants delivered to the dorsomedial region of the abdomen of the cockroach Periplaneta americana. evoke a complex grooming response. In larvae the response consitsts of extension of all six legs and arching of the abdomen which is rubbed against any solid surface presented. In adults, leg extension and arching are accompanied by side to side wagging of the abdomen and rapid scissoring of the wings.In some decapitated late instar larvae, abdominal wagging behavior can be evoked by chemical or tactile stimulation of the dorso-medial region of the abdomen. The form of the wag is somewhat different in these animals than in the adults, and it occurs at a lower frequency.Neuronal circuitry underlying the rhythmic wagging response of the adult may therefore be laid down or made functional in the mid- to late-larval stages. The wagging behavior is not normally expressed until the final ecdysis.A population of sensory setae is found on the abdomen at all stages of development, and some of these are presumed to trigger the grooming behavior when stimulated. The morphology and distribution of some of the adult receptors differs from some of the larval receptors.All larvae, including those late-instar individuals which show an adult-like response (wagging) have identical receptors on the abdomen in terms of morphology, distribution, and general responsiveness. Thus, no obvious changes in abdominal sensory receptors are correlated with the emergence of the wagging behavior. Anatomical and/or functional changes within the central nervous system are most likely responsible for the emergence of adult wagging behavior.     

The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum

Previous studies have examined abiotic and biotic factors that facilitate agonistic behavior. For larval amphibians, food availability and conspecific density have been suggested as important factors influencing intraspecific aggression and cannibalism. In this study, we examined the separate and combined effects of food availability and density on the agonistic behavior and life history of larval long-toed salamanders, Ambystoma macrodactylum. We designed a 2Ƕ factorial experiment in which larvae were raised with either a high or low density of conspecifics and fed either a high or low level of food. For each treatment, we quantified the amount of group size variation, biting, and cannibalism occurring. Additionally, we examined survival to, time to and size at metamorphosis for all larvae. Results indicated that differences in both density and food level influenced all three life history traits measured. Moreover, differences in food level at which larvae were reared resulted in higher within-group size variation and heightened intraspecific biting while both density and food level contributed to increased cannibalism. We suggest that increased hunger levels and an uneven size structure promoted biting among larvae in the low food treatments. Moreover, these factors combined with a higher encounter rate with conspecifics in the high density treatments may have prompted larger individuals to seek an alternative food source in the form of smaller conspecifics.     

Comparison of gregariousness in larvae and adults of four species of zetoborine cockroaches

Insects observed in groups in nature may be gathered either by attractants from the environment or by conspecifics. Field distribution data alone are thus insufficient to assess congregation by conspecifics and complementary laboratory tests of spacing patterns are required. Such tests were performed in four species of Zetoborinae (Insecta, Blattaria), for which field studies showed differences in spatial distribution (Schultesia lampyridiformis Roth, Phortioeca nimbata Burmeister, Lanxoblatta emarginata Burmeister and Thanatophyllum akinetum Grandcolas). Gregariousness, mobility, and sticking to shelters were compared between these four species. Tests were performed on pairs of adults of the same sex and opposite sexes, and also on first instar larvae, either in isolation or in groups of two and four individuals. In S. lampyridiformis, adults were strongly gregarious, whereas larvae dispersed early after birth and were very mobile during the first instar. In P. nimbata, larvae and adults were gregarious, while in L. emarginata larvae were weakly gregarious, and gregariousness decreased when density increased. Adults of L. emarginata seemed to be indifferent to each other. Larvae and adults of T. akinetum were solitary and they actively dispersed. The varying levels of gregariousness among species are discussed according to the known ecological habits in Zetoborinae.     

Information transfer and the facilitation and inhibition of feeding in a schooling fish

Synopsis Recent studies show that fish forage actively when perceived risk is low, but decrease foraging and increase vigilance when perceived risk is high. Isolated juvenile chum salmon,Oncorhynchus keta, were visually exposed to groups of conspecifics engaged in different activities to examine their ability to gain information about foraging opportunity and risk by interpreting conspecific behavior. Isolates ate most when exposed to feeding groups, less when exposed to nonfeedig groups, and least when exposed to alarmed groups. Isolates exposed to alarmed conspecifics also spent more time motionless than did fish exposed to either feeding or nonfeeding conspecifics. These findings indicate that schooling fish gain information by interpreting conspecific behavior, and are consistent with research showing that animals balance the conflicting demands of foraging and vigilance.     

Visual and chemical cues in habitat selection of sepioid larvae

The present study explored, by experiments in aquaria, the modality of senses used by sepioid larvae (Euprymna scolopes) when searching for their species’ settlement habitat (Rangiroa, French Polynesia). Our results showed that E. scolopes larvae made active choices among the four habitats tested (living coral, dead coral, macroalgae and sand), and that their selective choice was influenced by presence or absence of conspecifics on the habitat. Sensory experiments showed that E. scolopes larvae differentiated between conspecifics and heterospecifics (and not between their preferred habitat versus the least preferred habitat) using both visual and olfactory cues. Overall, our results suggest species-specific cues may play a vital role in establishment spatial patterns at settlement.     

Larval behavioral syndrome does not affect emergence behavior in a damselfly (<Emphasis Type="Italic">Lestes congener</Emphasis>)

Activity is a key behavioral trait that often mediates a trade-off between finding food for growth and evading predation. We investigated how activity of the damselfly Lestes congener is affected by larval state and predator presence and if larval behavioral type (BT) can be used to predict larval emergence behavior. Activity level of individual larvae was studied without predators at two different physiological states (hungry, fed) and in two predator treatments (familiar or unfamiliar predator cues). Larvae did not adjust their activity depending on state or when subjected to unfamiliar predator cues but a general reduction in activity was seen in the familiar predator treatment. Hence, active individuals remained active compared to their conspecifics, independent of state or predator treatment illustrating the presence of a behavioral syndrome. However, we found no correlation between larval BT and emergence behavior. Active individuals did not differ from less active individuals in any emergence characteristics. The results illustrate that the larval BT occurs in many situations keeping active larvae active even in maladaptive situations. Furthermore, we show that damselfly emergence behavior can be completely decoupled from larval BT, indicating a loss of stability in individual BT during critical stages in ontogeny.     

Responses of Mamestra brassicae (Lepidoptera: Noctuidae) to crowding: interactions with disease resistance,colour phase and growth

This study examines phenotypic plasticity in relation to rearing density in larvae of the moth, Mamestra brassicae. Larval phase, growth rate, weight at moulting and susceptibility to disease were quantified when reared at five densities. Larvae develop more quickly, but attain a smaller size and are more susceptible to disease, when reared at high than at intermediate densities. They also exhibit a higher degree of melanisation than larvae reared at intermediate densities, or singly. A review of the literature suggests that a switch to a rapidly developing dark phase at high densities is a widespread phenomenon within the Lepidoptera. Rapid development at the expense of attaining a large size, and increased melanisation, are interpreted as adaptive responses to reach pupation before food supplies are depleted, as is likely when larval density is high. High susceptibility to viral infection at high density may be a result of physiological stress associated with rapid development, or due to a shift in allocation of resources from resistance to development: larvae that developed quickly were more susceptible to infection. Larvae reared singly appeared to be less fit than larvae reared at intermediate densities: they exhibited many of the characteristics of larvae reared at high density, particularly low weight, a right-hand skew in their weight frequency distribution, and high susceptibility to disease. I hypothesise that expression of resistance may be phenotypically plastic with regard to environment. Contact with other larvae may, up to a point, stimulate both growth and resistance to infection, for the risk of infection will increase with the density of conspecifics.