Footdrumming and other anti-predator responses in the bannertail kangaroo rat (Dipodomys spectabilis)

Summary Anti-predator behaviors of the bannertail kangaroo rat (Dipodomys spectabilis) toward snake predators were investigated. We induced responses by presenting a live (tethered) snake and an inflatable snake decoy to rats of known ages and sex in their territories. Comparisons of behaviors during spontaneous activity (baseline), naturally occurring snake-rat interactions, and experimental procedures further clarified anti-predator behaviors. The tethered snake immediately induced high rates of footdrumming (the repeated striking of the hind feet on the ground) in all rats (n=24) (Table 2), and individuals of both sexes and all ages footdrummed significantly more at the tethered snake than at the decoy. Other antipredator behaviors included alert postures, jumpback, kicking sand and avoidance. Juvenile rats exhibited more avoidance behavior and alert postures than adults and footdrummed at the decoy only if they experienced the snake first. We conclude that footdrumming functions as an individual alarm signal against predation by snakes in D. spectabilis. The drumming probably informs a snake that it has been detected and may cause it to leave. Because rats did not footdrum in response to aerial predators (owls), we suggest that kangaroo rats use different anti-predator strategies that depend on the kind of threat and the type of predator.     

Prey odor discrimination by ingestively naive coachwhip snakes(Masticophis flagellum)

Summary Ingestively naive hatchling coachwhip snakes(Masticophis flagellum) detected integumentary chemicals from several potential prey species and discriminated them from chemical stimuli from other animals and from distilled water, strongly suggesting a genetic basis for these abilities. The strongest responses were to lizard and snake stimuli, which form a major part of the diet. Variable responses to chemical cues from other taxa are discussed. Responses by coachwhip snakes to prey chemicals appear to be highly specific, as suggested by the stronger reaction to vomodors of sympatric than of allopatric lizard species. The highly developed use of chemical cues by the diurnal, visually oriented coachwhip snake emphasizes the general importance of chemical senses to predation by nonvenomous snakes, regardless of the involvement of vision.     

Territorial defense in the bannertail kangaroo rat (Dipodomys spectabilis): footdrumming and visual threats

Summary Footdrumming and visual displays associated with territorial defense in the bannertail kangaroo rat (Dipodomys spectabilis) were studied in the field in Arizona. We predicted that foot-drumming functioned like bird song in territorial advertisement. Rats were tested in their territories for their responses to the presentation of four different stimuli: a playback of airborne footdrumming patterns (audio); a stuffed and mounted kangaroo rat in an aggressive posture (visual); a combination of both (audio-visual); and a playback of cricket stridulation as a control. Kangaroo rats investigated all experimental stimuli equally by becoming alert, approaching, and retreating (Fig. 2). Rats, therefore, seemed to assess the amount of threat and footdrummed at higher rates and sooner in response to the more threatening visual stumulus of a stuffed rat than to the apparently less threatening ones of a airborne footdrumming playback or cricket stridulation (Fig. 1). We conclude that rats footdrum at long ranges to repel a potential intruder and also at close ranges when territories are threatened by a persistent intruder. Chase and attack, as in territorial birds, are the final lines of defense.     

Correlational evidence of a sexually-selected handicap

Handicap models of sexual selection predict that ornaments must be costly to produce and/or to wear and maintain; only then can they evolve as reliable signals of genetic quality. We investigated in the laboratory one potential cost of possessing ornaments, using the viviparous fish Girardinichthys multiradiatus and its natural predator, the snake Thamnophis melanogaster. We found that female G. multiradiatus show preferences for males with larger fins, as measured from body correlates. Males with a morphology attractive to females, however, were more likely to be captured by snakes than were other males (Fig. 5). Greater vulnerability to snakes cannot be explained as a result of snake visual preferences, because snakes responded similarly to males and females (Fig. 6). Finally, males, particularly dominant ones, were more likely to inspect foraging snakes than were females (Fig. 7). We conclude that male Girardinichthys multiradiatus experience a sexually-selected handicap due to reduced mobility resulting from having enlarged fins.     

Does responsiveness to predator scents affect lizard survivorship?

Many prey organisms respond to predator scent by shifting behaviour. These alterations to behaviour are often assumed to increase an animal's chances of evading predators. Responsiveness to predator scents is therefore believed to ultimately increase a prey's chances of surviving encounters with predators. This notion is widely accepted among behavioural ecologists but has rarely been empirically tested. I staged encounters between adult snakes (Demansia psammophis) and pairs of unrestrained adult lizards (Lampropholis guichenoti) that responded strongly to snake predator scent ("responsive") or weakly to snake predator scent ("non-responsive"). Responsive lizards decreased activity and mobility during the staged encounters with snake predators. In turn this shift in behaviour decreased the chances that snakes detected responsive lizards. Since snakes almost always captured lizards that were detected, responding strongly to predator scent decreased a lizard's chances of being captured by predators. This finding is the first experimental demonstration in any terrestrial animal that responsiveness to predator scents can function to increase survival probability.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

Use of different signaling modalities to communicate status by dominant and subordinate Heermann’s kangaroo rats (<Emphasis Type="Italic">Dipodomys heermanni</Emphasis>)

Dominance relationships in solitary species may be an important factor in the maintenance of long-term, stable relationships among territorial neighbors. We examined the mediation of intraspecific interactions in a solitary, territorial kangaroo rat, Dipodomys heermanni, and tested whether unfamiliar kangaroo rats establish a dominance hierarchy and then decrease aggression and increase communication (via footdrumming and sandbathing) after initial interactions and the establishment of a social structure. Results revealed that both dominance hierarchies and familiarization with particular individuals are likely to mediate social interactions. After only one pairing per dyad, an almost linear dominance hierarchy emerged, which became perfectly linear after a 90-min familiarization period. During the course of subsequent interactions between dyad partners, fighting decreased and non-agonistic communication increased. Dominant kangaroo rats sandbathed at higher rates than subordinates, possibly to deposit scent to advertise competitive ability, whereas subordinate kangaroo rats footdrummed from inside the burrow, which seemed to indicate an unwillingness to interact. We suggest the kangaroo rats use a conditional strategy when deciding to fight (be dominant) or withdraw (be subordinate) by employing different modes to communicate status and minimize the potential risk of injury during unnecessarily prolonged fights.     

Influences of divergent behavioral strategies upon risk allocation in juvenile flatfishes

Animals balance feeding and anti-predator behaviors at various temporal scales. When risk is infrequent or brief, prey can postpone feeding in the short term and temporally allocate feeding behavior to less risky periods. If risk is frequent or lengthy, however, prey must eventually resume feeding to avoid fitness consequences. Species may exhibit different behavioral strategies, depending on the fitness tradeoffs that exist in their environment or across their life histories. North Pacific flatfishes that share juvenile rearing habitat exhibit a variety of responses to predation risk, but their response to risk frequency has not been examined. We observed the feeding and anti-predator behaviors of young-of-the-year English sole (Parophrys vetulus), northern rock sole (Lepidopsetta polyxystra), and Pacific halibut (Hippoglossus stenolepis)—three species that exhibit divergent anti-predator strategies—following exposure to three levels of predation risk: no risk, infrequent (two exposures/day), and frequent (five exposures/day). The English sole responded to the frequent risk treatment with higher feeding rates than during infrequent risk, following a pattern of behavioral response that is predicted by the risk allocation hypothesis; rock sole and halibut did not follow the predicted pattern, but this may be due to the limited range of treatments. Our observations of unique anti-predator strategies, along with differences in foraging and species-specific ecologies, suggest divergent trajectories of risk allocation for the three species.     

Sea Snake Harvest in the Gulf of Thailand

Conservation of sea snakes is virtually nonexistent in Asia, and its role in human–snake interactions in terms of catch, trade, and snakebites as an occupational hazard is mostly unexplored. We collected data on sea snake landings from the Gulf of Thailand, a hotspot for sea snake harvest by squid fishers operating out of the ports of Song Doc and Khanh Hoi, Ca Mau Province, Vietnam. The data were collected during documentation of the steps of the trading process and through interviewers with participants in the trade. Squid vessels return to ports once per lunar synodic cycle and fishers sell snakes to merchants who sort, package, and ship the snakes to various destinations in Vietnam and China for human consumption and as a source of traditional remedies. Annually, 82 t, roughly equal to 225,500 individuals, of live sea snakes are brought to ports. To our knowledge, this rate of harvest constitutes one of the largest venomous snake and marine reptile harvest activities in the world today. Lapemis curtus and Hydrophis cyanocinctus constituted about 85% of the snake biomass, and Acalyptophis peronii, Aipysurus eydouxii, Hydrophis atriceps, H. belcheri, H. lamberti, and H. ornatus made up the remainder. Our results establish a quantitative baseline for characteristics of catch, trade, and uses of sea snakes. Other key observations include the timing of the trade to the lunar cycle, a decline of sea snakes harvested over the study period (approximately 30% decline in mass over 4 years), and the treatment of sea snake bites with rhinoceros horn. Emerging markets in Southeast Asia drive the harvest of venomous sea snakes in the Gulf of Thailand and sea snake bites present a potentially lethal occupational hazard. We call for implementation of monitoring programs to further address the conservation implications of this large‐scale marine reptile exploitation. Cosecha de Serpientes Marinas en el Golfo de Tailandia     

Do predators control prey species abundance? An experimental test with brown treesnakes on Guam

The effect of predators on the abundance of prey species is a topic of ongoing debate in ecology; the effect of snake predators on their prey has been less debated, as there exists a general consensus that snakes do not negatively influence the abundance of their prey. However, this viewpoint has not been adequately tested. We quantified the effect of brown treesnake (Boiga irregularis) predation on the abundance and size of lizards on Guam by contrasting lizards in two 1-ha treatment plots of secondary forest from which snakes had been removed and excluded vs. two 1-ha control plots in which snakes were monitored but not removed or excluded. We removed resident snakes from the treatment plots with snake traps and hand capture, and snake immigration into these plots was precluded by electrified snake barriers. Lizards were sampled in all plots quarterly for a year following snake elimination in the treatment plots. Following the completion of this experiment, we used total removal sampling to census lizards on a 100-m2 subsample of each plot. Results of systematic lizard population monitoring before and after snake removal suggest that the abundance of the skink, Carlia ailanpalai, increased substantially and the abundance of two species of gekkonids, Lepidodactylus lugubris and Hemidactylus frenatus, also increased on snake-free plots. No treatment effect was observed for the skink Emoia caeruleocauda. Mean snout-vent length of all lizard species only increased following snake removal in the treatment plots. The general increase in prey density and mean size was unexpected in light of the literature consensus that snakes do not control the abundance of their prey species. Our findings show that, at least where alternate predators are lacking, snakes may indeed affect prey populations.     

Resembling a Viper: Implications of Mimicry for Conservation of the Endangered Smooth Snake

The phenomenon of Batesian mimicry, where a palatable animal gains protection against predation by resembling an unpalatable model, has been a core interest of evolutionary biologists for 150 years. An extensive range of studies has focused on revealing mechanistic aspects of mimicry (shared education and generalization of predators) and the evolutionary dynamics of mimicry systems (co‐operation vs. conflict) and revealed that protective mimicry is widespread and is important for individual fitness. However, according to our knowledge, there are no case studies where mimicry theories have been applied to conservation of mimetic species. Theoretically, mimicry affects, for example, frequency dependency of predator avoidance learning and human induced mortality. We examined the case of the protected, endangered, nonvenomous smooth snake (Coronella austriaca) that mimics the nonprotected venomous adder (Vipera berus), both of which occur in the Åland archipelago, Finland. To quantify the added predation risk on smooth snakes caused by the rarity of vipers, we calculated risk estimates from experimental data. Resemblance of vipers enhances survival of smooth snakes against bird predation because many predators avoid touching venomous vipers. Mimetic resemblance is however disadvantageous against human predators, who kill venomous vipers and accidentally kill endangered, protected smooth snakes. We found that the effective population size of the adders in Åland is very low relative to its smooth snake mimic (28.93 and 41.35, respectively).Because Batesian mimicry is advantageous for the mimic only if model species exist in sufficiently high numbers, it is likely that the conservation program for smooth snakes will fail if adders continue to be destroyed. Understanding the population consequences of mimetic species may be crucial to the success of endangered species conservation. We suggest that when a Batesian mimic requires protection, conservation planners should not ignore the model species (or co‐mimic in Mullerian mimicry rings) even if it is not itself endangered. Implications of mimicry for Conservation of the endangered smooth snake     

Natal philopatry in bannertailed kangaroo rats

Summary I describe prolonged retention of offspring in natal home ranges, or natal philopatry, in the bannertailed kangaroo rat Dipodomys spectabilis. Though weaning occurs at about one month of age, offspring shared natal burrows with their mothers for three to seven months, and 39% of surviving offspring remained within natal home ranges through reproductive maturity. Males as well as females were philopatric. Data on the availability of burrows and on patterns of resettlement suggest that natal philopatry in this species may be a means of providing juveniles with access to essential resources, in this case food caches and large complex burrow systems, that are not readily available outside natal home ranges.     

Performance level and efficiency of two differing predator-avoidance strategies depend on nutritional state of the prey fish

Animal prey has developed a variety of behavioural strategies to avoid predation. Many fish species form shoals in the open water or seek refuge in structurally complex habitats. Since anti-predator strategies bear costs and are energy-demanding, we hypothesised that the nutritional state of prey should modify the performance level and efficiency of such strategies. In aquaria either containing or lacking a structured refuge habitat, well-fed or food-deprived juvenile roach (Rutilus rutilus) were exposed to an open-water predator (pikeperch, Sander lucioperca). Controls were run without predators. In the presence of the predator, roach enhanced the performance of the anti-predator strategy and increased the use of the refuge habitat whereby food-deprived roach were encountered more often in the structure than well-fed roach. Nonetheless more starved than well-fed roach were fed upon by the predator. In the treatments offering only open-water areas, roach always formed dense shoals in the presence of the predator. The shoal density, however, was lower in starved roach. Starving fish in shoals experienced the highest predation mortality across all experimental treatments. The experiment confirmed the plasticity of the anti-predator behaviour in roach and demonstrated that food deprivation diminished the efficiency of shoaling more strongly than the efficiency of hiding. The findings may be relevant to spatial distribution of prey and predator–prey interactions under natural conditions because when prey are confronted with phases of reduced resource availability, flexible anti-predator strategies may lead to dynamic habitat use patterns.     

Territorial defense and advertisement by footdrumming in bannertail kangaroo rats (Dipodomys spectabilis) at high and low population densities

Summary Behaviors associated with territorial defense of large dirt mounds by bannertail kangaroo rats (Dipodomys spectabilis) at high and low population densities are reported. Rats were observed for 640 h during three summers and one spring from 1980–1982 in SE Arizona.Bannertail kangaroo rats defended their territories by footdrumming, as a long-distance warning signal, and chasing as a closer-distance threat. They footdrummed on or near their mounds spontaneosly during the night, in response to neighbors' footdrums, and durint mound challenges. There were no sexual differences in footdrumming, and juveniles frequently performed the behavior. The low frequency sounds were within the auditory sensitivities of the rats and footdrumming patterns differed somewhat between individuals. A playback experiment provided preliminary evidence that rats can differentiate between the footdrums of neighbors and strangers. When a bannertail visited the mound of another bannertail the mound owner actively defended its mound and immediately chased the visitor away. Fighting and mound challenges occurred infrequently, and the uniformly dispersed distribution of mounds suggested an effort by rats to avoid mutual interference.When population densities were high, dispersing juveniles built new mounds, consequently, distances between mounds decreased. Rats responded by tolerating closer neighbors, spending more time active on their mounds, and visiting neighboring mounds less. Adults increased footdrumming rates at high population densities, but juveniles footdrummed at high rates regardless of the population size.     

How unpredictable is the individual scanning process in socially foraging mammals?

In group-forming prey species, theory assumes that individuals within groups should scan independently of one another, with vigilance sequences being relatively unpredictable, making interscan durations highly variable. We attempted to detect any divergence from randomness in the scanning process in three mammalian prey species phylogenetically and geographically separated and exposed to different levels of predation: waterbuck, Kobus ellipsiprymnus defassa, under a high observed predation risk, eastern grey kangaroo, Macropus giganteus, still experiencing occasional predation and European roe deer, Capreolus capreolus, under a very low natural predation risk. Our results revealed that the focal interscan duration increased when the duration of the preceding interscan increased, whatever the studied species and the predation risk that its individuals experienced, and decreased with the preceding scan duration in two species under, respectively, occasional and low predation risks. The exponential distribution was the tested model that fitted the observed distributions of interscan durations least well. We discuss what can trigger non-randomness in scanning, through a non-homogenous Poisson process, at both intra-individual and inter-individual levels, particularly with regard to previous studies that have demonstrated synchronisation of vigilance in such mammals. Our results suggest the need to reconsider any assumption of randomness in scanning in the basic model predicting form and frequency of scanning behaviour by prey species.     

Population differences in predation on Batesian mimics in allopatry with their model: selection against mimics is strongest when they are common

Batesian mimicry evolves when a palatable species, the “mimic,” resembles a dangerous species, the “model,” because both receive protection from predation. Yet, this protection should break down where the model is absent, because predators in such areas would not be under selection to avoid the model. Here, we test this prediction in a coral snake mimicry complex. We exposed plasticine replicas of milk snakes that closely mimic coral snakes to natural predators to determine if good mimetic milk snakes are preferentially attacked in allopatry with their model. Moreover, we evaluated whether attack rates on these replicas varied among three different allopatric regions that differed in the type of mimic found locally (i.e., good mimic, poor mimic, or no mimic). When all three regions were considered together, mimics were not preferentially attacked. When regions were analyzed separately, however, attacks on mimics were significantly greater than randomness only where good mimics were found. These variable levels of predation on good mimics might reflect frequency-dependent (i.e., apostatic) predation. In allopatric regions where good mimics are present, predators might have learned or evolved preferences for conspicuous, palatable prey that they encounter frequently. By contrast, in allopatric regions where good mimics are absent, predators might not have learned or evolved preferences for novel phenotypes. Thus, when predation is frequency-dependent, as long as good mimics are rare, they might not experience elevated levels of predation in allopatry with their model as predicted by the Batesian mimicry hypothesis.     

Cercopagis pengoi and Mysis spp. alter their feeding rate and prey selection under predation risk of herring (Clupea harengus membras)

The anti-predator behaviour of Baltic crustacean planktivores was studied in feeding experiments under predation pressure of herring. The experiments were conducted with pelagic mysids: Mysis mixta and Mysis relicta, and with Cercopagis pengoi, a non-indigenous cladoceran, which invaded the Baltic Sea in 1992. Zooplankton was offered as prey. Two kinds of experiments were performed in the absence and presence of chemical predator cues: (1) two-prey experiments with prey, which have poor or good escape responses and all three planktivores and (2) natural prey experiments with mysids in natural zooplankton assemblages. The results showed that all three species reacted to the chemical cue of herring by decreasing their feeding rate and altering prey selection. C. pengoi selected easily captured prey (rotifers) in two-prey experiments under predation risk while selection for any prey was evident in mysids in natural prey experiments only in the absence of predator cues. This indicates that planktivores have different anti-predator strategies, which are modified by their own prey capture abilities. C. pengoi was a very efficient predator on small prey with size-specific prey consumption rate 5 to 18 times the rate of mysids. Results show that the studied planktivores are capable of adjusting their feeding behaviour to decrease their conspicuousness in order to increase survival under predation risk. Further, results support the view that C. pengoi has adapted well to the Baltic ecosystem, sharing food niche with pelagic mysids and most probably having a strong influence on the whole pelagic food web.     

An overlooked side effect of nest-scattering behavior to decrease predation risk (Acari: Tetranychidae,Stigmaeidae)

The number of nests containing egg masses a female makes over her lifetime and the pattern of scattering nests vary among species in a genus of nest-weaving spider mites (Stigmaeopsis). We hypothesized that the scattered nests of small nest builders have a previously overlooked indirect effect in that the void nests created after predation take on a new role as hindering devices that effectively decrease predator searching efficiency. First, we demonstrated that the experimental design used in this study is a good reflection of the nest distribution pattern of Stigmaeopsis takahashii (an intermediate-sized nest builder) in the field. Using this species as a model, we tested how different nest-scattering patterns affect the predator to examine how scattering may indirectly provide an anti-predation strategy by increasing a predators searching time. Next, we observed how artificially arranged void nests disturb predatory behavior in both starved and fully fed predator females and showed that void nests have a strong hindering effect on predators. Thus, we concluded that the nesting behavior of this mite species not only has anti-predator effects but must also have a stabilizing effect on predator–prey interaction systems at the population level.     

Indirect effects of large herbivores on snakes in an African savanna

Many large mammal species are declining in African savannas, yet we understand relatively little about how these declines influence other species. Previous studies have shown that the removal of large herbivorous mammals from large-scale, replicated experimental plots results in a dramatic increase in the density of small mammals, an increase that has been attributed to the relaxation of competition between rodents and large herbivores for food resources. To assess whether the removal of large herbivores also influenced a predator of small mammals, we measured the abundance of the locally common olive hissing snake, Psammophis mossambicus, over a 19-mo period in plots with and without large herbivores. Psammophis mossambicus was significantly more abundant in plots where large herbivores were removed and rodent numbers were high. Based on results from raptor surveys and measurements of vegetative cover, differences in snake density do not appear to be driven by differences in rates of predation on snakes. Instead, snakes appear to be responding numerically to greater abundances of small-mammal prey in areas from which large herbivores have been excluded. This is the first empirical demonstration of the indirect effects of large herbivores on snake abundance and presents an interesting example of how the influence of dominant and keystone species can move through a food web.     

Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts

Snakes are common predators of organisms, such as amphibians, with toxic defenses that can be lethal to other predators. Because snakes do not have the option of dissecting prey into edible versus inedible components, they face a full dose of any chemical defenses encountered during attempted predation. This limitation has likely resulted in intense selection favoring the evolution of alternative mechanisms for dealing with prey toxins. These mechanisms can be physiological (e.g., resistance to prey toxins) or behavioral (e.g., toxin sampling and rejection). When physiological resistance arises, the possibility of bioaccumulation of a toxin results. We examined the coevolutionary interaction between the common garter snake (Thamnophis sirtalis) and the rough-skinned newt (Taricha granulosa), which contains a powerful neurotoxin called tetrodotoxin (TTX). In some populations syntopic with newts, individuals of T. sirtalis have evolved resistance to TTX. We examined the persistence of TTX in T. sirtalis after administration of an oral dose of TTX to investigate the possibility that snakes are sequestering TTX. The half-life of TTX in snake liver was estimated at 8.1?days. Accordingly, clearance of 99% of a single dose of TTX averages 61?days. Negative fitness consequences of intoxication during and after newt consumption may be balanced by co-opting the newts?? chemical defense for protection from the snakes?? own predators. Accounting of the coevolutionary dynamic between snakes and newts must incorporate post-consumption affects of lingering TTX.