Defense mechanisms and antipredator behavior in two sympatric species of spiny lobsters, Panulirus argus and P. guttatus

The congeneric spiny lobsters Panulirus argus and P. guttatus co-occur throughout the Caribbean Sea, where they may share the coral reef habitat. Despite their phylogenetic closeness, both species have many different life-history traits that may partially explain their coexistence. However, even though both species may face the same predators, their defense mechanisms and antipredator strategies had not been compared. We compared the performance between species in 18 morphological and behavioral defense mechanisms commonly expressed by most spiny lobsters, including predator-avoidance mechanisms (activity schedule, sheltering behavior, delay to disturbance, and effect of conspecific damage-released scents on shelter choice) as well as antipredator mechanisms (body size, several parameters of the escape response and limb autospasy, clinging strength, antennal strength, and cooperative defense). As hypothesized, both species expressed all these defense mechanisms (except cooperative defense, shown only by P. argus), reflecting their phylogenetic closeness, but performed significantly differently in most, in accordance with their particular ontogenetic traits. Their comparative performance in individual defense mechanisms as well as the antipredator strategies displayed by groups of lobsters of each species in the presence of a common predator (the triggerfish Balistes vetula) showed that, in general, the defensive behavioral type of P. argus is more bold and that of P. guttatus more shy. Therefore, their distinct defensive behaviors contribute to their niche differentiation.     

Antipredator activity and endogenous biosynthesis of defensive secretion in larval and pupal Delphastus catalinae (Horn) (Coleoptera: Coccinellidae)

Delphastus catalinae (Horn) is a predatory ladybird beetle (Coccinellidae) commonly used as a biocontrol agent against greenhouse infestation by whiteflies. It belongs to the basal subfamily Microweisinae, a group for which chemical defenses have not been previously investigated. The larval and pupal stages of D. catalinae possess minute secretory hairs that produce droplets containing compounds of both isoprenoid and polyketide origin. Bioassays with the predatory ant Crematogaster lineolata showed both the larval and pupal secretions to be deterrent. Moreover, isolated secretion components, from both classes of compounds, displayed antipredator activity against the ant. Experiments with D. catalinae larvae fed isotopically labeled glucose showed ¹³C-incorporation into both categories of compounds within the pupal secretion, demonstrating that these antipredator compounds, which differ from the typical nitrogenous defensive molecules of coccinellids, are biosynthesized endogenously. This suggests that the wide use of alkaloids by more derived coccinellids may have arisen after their divergence from the more basal Microweisinae.     

Socially facilitated antipredator behavior by ringed salamanders (<Emphasis Type="Italic">Ambystoma annulatum</Emphasis>)

Many aspects of animal behavior can be socially facilitated, including foraging behavior, exploration behavior, and antipredator behavior. Although larvae of the ringed salamander (Ambystoma annulatum) are not gregarious, they can live in high densities and face intense predation pressure during a short period following hatching. In a predator-recognition experiment, we found that these salamanders responded to chemical cues from dragonfly nymphs (Family: Libellulidae) with appropriate antipredator behavior (decreased activity), and this response was absent when salamanders were exposed to chemical cues from nonpredatory mayfly nymphs (Family: Heptageniidae). In a second experiment, we tested whether antipredator behavior in response to chemical cues of dragonflies could be socially facilitated by larval ringed salamanders. We placed an “observer” salamander into a central arena with four “demonstrator” salamanders behind clear barriers around an arena. The barriers ensured that chemical cues would not be detected by the observer. When demonstrators were exposed to chemical cues from dragonflies, the data were consistent with the hypothesis that both demonstrators and observers decreased activity relative to a blank control. Our results provide evidence that social facilitation can occur in larval ringed salamanders, a nonsocial species.     

Age and sex influence marmot antipredator behavior during periods of heightened risk

Animals adjust their antipredator behavior according to environmental variation in risk, and to account for their ability to respond to threats. Intrinsic factors that influence an animal’s ability to respond to predators (e.g., age, body condition) should explain variation in antipredator behavior. For example, a juvenile might allocate more time to vigilance than an adult because mortality as a result of predation is often high for this age class; however, the relationship between age/vulnerability and antipredator behavior is not always clear or as predicted. We explored the influence of intrinsic factors on yellow-bellied marmot (Marmota flaviventris) antipredator behavior using data pooled from 4 years of experiments. We hypothesized that inherently vulnerable animals (e.g., young, males, and individuals in poor condition) would exhibit more antipredator behavior prior to and immediately following conspecific alarm calls. As expected, males and yearlings suppressed foraging more than females and adults following alarm call playbacks. In contrast to predictions, animals in better condition respond more than animals in below average condition. Interestingly, these intrinsic properties did not influence baseline time budgets; animals of all ages, sexes, and condition levels devoted comparable amounts of time to foraging prior to alarm calls. Our results support the hypothesis that inherent differences in vulnerability influence antipredator behavior; furthermore, it appears that a crucial, but poorly acknowledged, interaction exists between risk and state-dependence. Elevated risk may be required to reveal the workings of state-dependent behavior, and studies of antipredator behavior in a single context may draw incomplete conclusions about age- or sex-specific strategies.     

Training Captive-Bred or Translocated Animals to Avoid Predators

Abstract: Animal reintroductions and translocations are potentially important interventions to save species from extinction, but most are unsuccessful. Mortality due to predation is a principal cause of failure. Animals that have been isolated from predators, either throughout their lifetime or over evolutionary time, may no longer express appropriate antipredator behavior. For this reason, conservation biologists are beginning to include antipredator training in pre-release preparation procedures. We describe the evolutionary and ontogenetic circumstances under which antipredator behavior may degenerate or be lost, and we use principles from learning theory to predict which elements can be enhanced or recovered by training. The empirical literature demonstrates that training can improve antipredator skills, but the effectiveness of such interventions is influenced by a number of constraints. We predict that it will be easier to teach animals to cope with predators if they have experienced ontogenetic isolation than if they have undergone evolutionary isolation. Similarly, animals should learn more easily if they have been evolutionarily isolated from some rather than all predators. Training to a novel predator may be more successful if a species has effective responses to similar predators. In contrast, it may be difficult to teach proper avoidance behavior, or to introduce specialized predator-specific responses, if appropriate motor patterns are not already present. We conclude that pre-release training has the potential to enhance the expression of preexisting antipredator behavior. Potential training techniques involve classical conditioning procedures in which animals learn that model predators are predictors of aversive events. However, wildlife managers should be aware that problems, such as the emergence of inappropriate responses, may arise during such training.     

Innate antipredator responses of Arctic charr (<Emphasis Type="Italic">Salvelinus alpinus</Emphasis>) depend on predator species and their diet

The ability to discriminate between more dangerous and less dangerous predators can have serious fitness advantages for fish juveniles. This is especially true for hatchery-reared fish young used for stocking, because their post-release mortality is often much higher than that of wild-born conspecifics. We tested whether two coexisting fish predators and their different diets induce innate behavioral responses in predator-naive Arctic charr (Salvelinus alpinus) young originating from an endangered hatchery-bred population used for re-introductions. We predicted the antipredator responses of charr to be stronger towards chemical cues of brown trout (Salmo trutta) and pikeperch (Stizostedion lucioperca) than towards odorless control water. More pronounced antipredator behavior was predicted in treatments with predators fed on charr than when their diet consisted of another sympatric salmonid, European grayling (Thymallus thymallus), or when they were food-deprived. The Arctic charr young showed strong antipredator responses in all brown trout treatments, whereas odors of the less likely predator pikeperch were avoided with conspecific diet only. Freezing was the most sensitive antipredator behavior, as it was completely absent in control treatments. We found considerable individual variation in the amount and strength of antipredator responses. Although almost half of the charr failed to show antipredator behavior towards the piscivores, those with the innate ability showed highly sensitive recognition of predator odors. Our results indicate that the innate antipredator behavior of the juvenile fish is already finely tuned to respond specifically to chemical cues from different fish predators and even their diets.Communicated by J. Krause     

Patterns of co-occurrence and interactions between age classes of the common triplefin,Forsterygion lapillum

Many marine organisms have pelagic larval stages that settle into benthic habitats occupied by older individuals; however, a mechanistic understanding of intercohort interactions remains elusive for most species. Patterns of spatial covariation in the densities of juvenile and adult age classes of a small temperate reef fish, the common triplefin (Forsterygion lapillum), were evaluated during the recruitment season (Feb–Mar, 2011) in Wellington, New Zealand (41°17′S, 174°46′E). The relationship between juvenile and adult density among sites was best approximated by a dome-shaped curve, with a negative correlation between densities of juveniles and adults at higher adult densities. The curve shape was temporally variable, but was unaffected by settlement habitat type (algal species). A laboratory experiment using a “multiple-predator effects” design tested the hypothesis that increased settler mortality in the presence of adults (via enhanced predation risk or cannibalism) contributed to the observed negative relationship between juveniles and adults. Settler mortality did not differ between controls and treatments that contained either one (p = 0.08) or two (p = 0.09) adults. However, post hoc analyses revealed a significant positive correlation between the mean length of juveniles used in experimental trials and survival of juveniles in these treatments, suggesting that smaller juveniles may be vulnerable to cannibalism. There was no evidence for risk enhancement or predator interference when adults were present alongside a heterospecific predator (F. varium). These results highlight the complex nature of intercohort relationships in shaping recruitment patterns and add to the growing body of literature recognizing the importance of age class interactions.     

Oxygen consumption of pelagic juveniles and demersal adults of the deep-sea fish Sebastolobus altivelis,measured at depth

Oxygen consumption rates of the deep-sea fish Sebastolobus altivelis were measured in situ on pelagic juveniles at mesopelagic depths (608 m) and on demersal adults at bathyal depths (1 300 m) in the Santa Catalina Basin in March 1982. Two pelagic juveniles were individually collected, and respiration was measured continuously for approximately 2 d with a slurp gun respirometer manipulated from the submersible “Alvin”. Oxygen consumption rates of these juveniles were highly variable and were 1.5 to 1.8 times higher during the night than during the day. Gut contents of the juveniles were mainly euphausiids (Euphausia pacifica and Nematoscelis difficilis). Four demersal adults were collected by “Alvin” and individually placed in fish-trap respirometers on the bottom where respiration was measured continuously for approximately 1 d. Weight-specific O₂ consumption rates for adults decreased with increasing body weight and were consistent in magnitude throughout the incubation period. Population O₂ consumption for demersal S. altivelis (calculated from abundance, size-frequency distribution, and O₂ consumption regression equation) was 11.01 μl O₂ m^-2 h^-1, which is two orders of magnitude less than the O₂ consumption rate for the population of the most abundant epibenthic megafaunal species in the Santa Catalina Basin, the ophiuroid Ophiophthalmus normani. O. normani is a principal prey for adults of S. altivelis based on gutcontent analysis. Given the population O₂ consumption rate as an estimate of food energy demand, the demersal population of S. altivelis would assimilate only 0.007% of the standing crop of O. normani per day.     

Determinants of vigilance behavior in the ring-tailed coati (Nasua nasua): the importance of within-group spatial position

Individuals living in social groups are predicted to live under unequal predation risk due to their spatial location within the group. Previous work has indicated that individuals located at the edge of groups have higher “domains of danger”, thus are more likely to engage in vigilance or antipredator behavior. We studied the determinants of vigilance behavior in two groups of ring-tailed coatis in Iguazu National Park, Argentina. In addition to the expected pattern that coatis were more vigilant at the edge of the group, we found that individuals were particularly vigilant at the front edge of the group. This pattern conforms to predictions of differing predation risk caused by sit-and-wait predators with respect to mobile animal groups. In addition, coatis exhibited less vigilance when the number of neighbors within 5 m and group size increased. Of the three spatial variables tested, within-group spatial position was the most important predictor variable determining vigilance levels. These results confirm that spatial position has major effects on vigilance behavior, and that group directionality is an important factor which should be taken into account when measuring vigilance behavior. Coatis were more vigilant when juveniles less than 6 months old were in the groups. The presence of these young juveniles also affected the relationship between alarm response and vigilance levels. Coatis were more vigilant after strong alarm reactions, but only when young juveniles were not present in the groups. This may indicate that coatis give differential responses to alarm calls depending on the age of the caller. A comparison of antipredator vigilance between coatis and sympatric capuchin monkeys is consistent with the hypothesis that terrestriality leads to higher perceive predation risk for coatis.     

Colorful tails fade when lizards adopt less risky behaviors

Colorful tails that become cryptic during ontogeny are found in diverse taxa. Nevertheless, the evolutionary bases for this change remain debated. Recent work suggests that colorful tails, deflective displays, and striped patterns may represent antipredator mechanisms used by immature lizards to compensate for being more active and hence more vulnerable to predation (increased movement hypothesis, IMH). I challenged the generality of IMH by comparing foraging behavior and frequency of tail displays across five Acanthodactylus lizards that vary in fundamental life history traits, before and after the tail changed color. As these species underwent changes in tail coloration, they congruently adopted less risky behaviors and reduced the frequencies of tail displays. Contrary to expectation, in two species, the hatchling risky behavior resulted not from increased movements but from longer stay in exposed microhabitats. I suggest that colorful tails and deflective tail displays are synergistic antipredator mechanisms neonates use to minimize the fitness consequences of using various risky behaviors rather than increased movement alone.     

Stereochemistry affects sesquiterpene lactone bioactivity against an herbivorous grasshopper

Sesquiterpene lactones are defensive compounds which protect plants against a variety of herbivores and other natural enemies. Sesquiterpene lactones from higher plants can be divided into two groups based on the stereochemistry of their lactone ring junction, either cis-fused or trans-fused. It is unclear whether and how this variation affects potentially important ecological interactions. To investigate whether stereochemical variation in sesquiterpene lactone ring junctions can influence resistance to herbivorous insects, we performed controlled feeding trials with two pairs of diastereomeric sesquiterpene lactones and examined the deterrent effect of each compound on feeding by the polyphagous grasshopper Schistocerca americana (Drury). Sesquiterpene lactone stereochemistry and concentration significantly influenced feeding behavior with grasshoppers consuming less of the trans-fused compounds than the cis-fused compounds. To our knowledge, this is the first demonstration that sesquiterpene lactone ring junction stereochemistry influences the feeding behavior of herbivores. Because this stereochemical trait polymorphism is widely distributed in nature, it could have substantial consequences for the ecology and evolution of large groups of plants, particularly the Asteraceae.     

Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition

How individuals assess, respond and subsequently learn from alarm cues is crucial to their survival and future fitness. Yet this information is not constant through time; many individuals are exposed to different predators throughout their life as they outgrow some predators or move to habitats containing different predators. To maximise overall fitness, individuals should discriminate between different cues and respond and learn from only those that are relevant to their current ontogenetic stage. We tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues from conspecific donors of different ontogenetic stages and whether the cue ontogenetic stage of the cue donor affected the efficacy of learning about predators. Juveniles displayed a significant antipredator response when conditioned with juvenile chemical alarm cues paired with predator odour but failed to respond when conditioned with predator odour paired with either adult alarm cues or with saltwater. Subsequently, individuals only recognised the predator odour alone as a threat when conditioned with juvenile alarm cues. This demonstrates that prey may be highly specific in how they use information from conspecific alarm cues, selectively responding to and learning from only those cues that are relevant to their developmental stage.     

Male endogenous pheromonal component of Bactrocera carambolae (Diptera: Tephritidae) deterred gecko predation

Summary. Geckos consumed immature Bactrocera carambolae males readily, but their consumption was reduced significantly when offered sexually mature males. They showed a similar aversion for sexually mature males previously fed with methyl eugenol. When male flies at different ages were offered to starved geckos, geckos’ consumption showed an age-related anti-feeding effect, which was concomitant with the production trend of 6-oxo-1-nonanol, a major endogenous component synthesized in the male rectal gland. The production of 6-oxo-1-nonanol was also age-related and corresponded with sexual maturity as reported previously. Topical application of the authentic chemical of 6-oxo-1-nonanol onto the thorax of female fruit flies, at the amount normally detected in the rectal gland of a sexually mature male, had the same deterrent effect against geckos.     

Anti-predation behaviour of red colobus monkeys in the presence of chimpanzees

Predator-prey interactions are usually regarded as evolutionary “arms races”, but evidence is still scarce. We examined whether the anti-predation strategies of red colobus monkeys (Procolobus badius) are adapted to the hunting strategies of chimpanzees (Pan troglodytes) in the Taï National Park, Ivory Coast. Taï chimpanzees search for red colobus groups, approach them silently and hunt co-operatively. Our playback experiments and observations of natural encounters revealed that red colobus hid higher up the trees in positions where exposure to the forest floor is minimal and became silent, when chimpanzees were close. They moved away silently through the canopy, when chimpanzees were still at some distance. However, if a group of diana monkeys was nearby in the latter situation, red colobus sought their presence even if they had to move towards the chimpanzees. Chimpanzees refrained from hunting associated red colobus groups, probably because diana monkeys are excellent sentinels for predators approaching over the forest floor. Thus several elements of both the predator's and the prey's strategies correspond to each other. Finally, we compared the interactions between the two species in Taï and in Gombe, Tanzania. We suggest that the difference in size ratio between the two species at the two sites and adaptation of hunting techniques and of escape modes to different forest structures can explain why Gombe red colobus attack chimpanzees while Taï red colobus try to escape. We conclude that predator-prey interactions can indeed lead to evolutionary arms races, with the specific form of co-adaptations depending on environmental factors.     

Antipredator responses of koomal (Trichosurus vulpecula hypoleucus) against introduced and native predators

Antipredator behavior studies generally assess prey responses to single predator species although most real systems contain multiple species. In multi-predator environments prey ideally use antipredator responses that are effective against all predator species, although responses may only be effective against one predator and counterproductive for another. Multi-predator systems may also include introduced predators that the prey did not co-evolve with, so the prey may either fail to recognize their threat (level 1 naiveté), use ineffective responses (level 2 naiveté) or succumb to their superior hunting ability (level 3 naiveté). We analyzed microhabitat selection of an Australian marsupial (koomal, Trichosurus vulpecula hypoleucus) when faced with spatiotemporal differences in the activity/density levels of one native (chuditch, Dasyurus geoffroii) and two introduced predators (red fox, Vulpes vulpes; feral cat, Felis catus). From this, we inferred whether koomal recognized introduced predators as a threat, and whether they minimized predation risk by either staying close to trees and/or using open or dense microhabitats. Koomal remained close to escape trees regardless of the predator species present, or activity/density levels, suggesting koomal employ this behavior as a first line of defense. Koomal shifted to dense cover only under high risk scenarios (i.e., with multiple predator species present at high densities). When predation risk was low, koomal used open microhabitats, which likely provided benefits not associated with predator avoidance. Koomal did not exhibit level 1 naiveté, although further studies are required to determine if they exhibit higher levels of naiveté (2–3) against foxes and cats.     

Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica

Antarctic krill (Euphausia superba) occupy a key position in the Southern Ocean linking primary production to secondary consumers. While krill is a dominant grazer of phytoplankton, it also consumes heterotrophic prey and the relative importance of these two resources may differ with ontogeny. We used stable isotope analyses to evaluate body size-dependent trophic and habitat shifts in krill during the austral summer around the South Shetland Islands, Antarctica. We found evidence for an asymmetric, ontogenetic niche expansion with adults of both sexes having higher and more variable δ¹⁵N values but consistent δ¹³C values in comparison with juveniles. This result suggests that while phytoplankton likely remains an important life-long resource, krill in our study area expand their dietary niche to include higher trophic food sources as body size increases. The broader dietary niches observed in adults may help buffer them from recent climate-driven shifts in phytoplankton communities that negatively affect larval or juvenile krill that rely predominately on autotrophic resources.     

Minimizing predation risk in a landscape of multiple predators: effects on the spatial distribution of African ungulates

Studies that focus on single predator-prey interactions can be inadequate for understanding antipredator responses in multi-predator systems. Yet there is still a general lack of information about the strategies of prey to minimize predation risk from multiple predators at the landscape level. Here we examined the distribution of seven African ungulate species in the fenced Karongwe Game Reserve (KGR), South Africa, as a function of predation risk from all large carnivore species (lion, leopard, cheetah, African wild dog, and spotted hyena). Using observed kill data, we generated ungulate-specific predictions of relative predation risk and of riskiness of habitats. To determine how ungulates minimize predation risk at the landscape level, we explicitly tested five hypotheses consisting of strategies that reduce the probability of encountering predators, and the probability of being killed. All ungulate species avoided risky habitats, and most selected safer habitats, thus reducing their probability of being killed. To reduce the probability of encountering predators, most of the smaller prey species (impala, warthog, waterbuck, kudu) avoided the space use of all predators, while the larger species (wildebeest, zebra, giraffe) only avoided areas where lion and leopard space use were high. The strength of avoidance for the space use of predators generally did not correspond to the relative predation threat from those predators. Instead, ungulates used a simpler behavioral rule of avoiding the activity areas of sit-and-pursue predators (lion and leopard), but not those of cursorial predators (cheetah and African wild dog). In general, selection and avoidance of habitats was stronger than avoidance of the predator activity areas. We expect similar decision rules to drive the distribution pattern of ungulates in other African savannas and in other multi-predator systems, especially where predators differ in their hunting modes.     

Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (<Emphasis Type="Italic">Lepomis cyanellus</Emphasis>)

Within aquatic communities, individuals may gain survival benefits by responding to the chemical alarm signals of heterospecific prey guild members. Piscivorous individuals, however, should be selected to use such chemical signals as foraging cues. A variety of centrarchid species, such as largemouth bass (Micropterus salmoides), undergo an ontogenetic change in their response to the chemical alarm cues of heterospecific guild members, switching from antipredator to foraging responses. This ontogenetic shift should occur when potential foraging benefits outweigh any survival advantage gained from an antipredator response. To test this model, we exposed juvenile green sunfish (Lepomis cyanellus) to the skin extracts of conspecifics, a heterospecific prey guild member (finescale dace, Phoxinus neogeaus) or an allopatric heterospecific (green swordtails, Xiphophorus helleri). Juvenile sunfish exhibited a significant positive relationship between standard length and time spent moving and a significant negative relationship between length and time in a spine-erect posture, when exposed to dace skin extract, but not to either swordtail or conspecific skin extracts. Smaller individuals of less than 90 mm standard length (SL) decreased time moving and increased time with spines erect (indicating an antipredator response) while larger individuals (>90 mm SL) increased time moving and decreased time with spines erect (indicating a foraging response), when exposed to dace skin extract. Conversely, juvenile sunfish, regardless of size tested, always exhibited an antipredator response to conspecific skin extract. Sunfish exhibited no change in behaviour in response to swordtail skin extracts. These data further support our model of a threat sensitive trade-off in the response to chemical alarm signals by juvenile centrarchids.     

Modeling outcomes of approaches to sustained human and snow leopard coexistence

The snow leopard (Uncia uncia) is in danger of extinction. Killing to protect livestock is among the primary causes of its decline. Efforts to mitigate this threat have focused on balancing the need to conserve the snow leopard with the needs of local people in snow leopard habitat, many of whom rely on raising livestock for their livelihoods. Conservation of the snow leopard has the characteristics of a public good, and outside funding is required to support conservation efforts. There are 5 commonly discussed approaches to resolving this issue: (1) direct payments for conservation, (2) investments in protection from predation, (3) damage compensation payments, (4) investments in better livestock husbandry, and (5) leases of pastureland for wild prey. After a review of these 5 conservation strategies, an economic–ecologic model, which includes the interactions between the snow leopard, its wild prey, and livestock, is used to evaluate the 2 most promising conservation strategies. The model reveals that investments in protection from predation and leases of pastureland for wild prey are effective but only in delaying the eventual extinction of the snow leopard. To preserve the snow leopard, these approaches must be applied more aggressively and new ones explored.