Threat-sensitive generalization of predator recognition by larval amphibians

Despite the importance of acquired predator recognition in mediating predator–prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments with mammals and fish indicate that some prey lacking innate predator recognition have the ability to display anti-predator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. This phenomenon is referred to as generalization of predator recognition. In this experiment, we documented for the first time that larval amphibians (woodfrog, Rana sylvatica) have the ability to generalize the recognition of known predators to closely related novel predators. Moreover, we demonstrated that this ability is dependent on the level of risk associated with the known predator. When red-bellied newt, Cynops pyrrhogaster (known predator), was paired with simulated low risk, tadpoles displayed fright responses to newts and novel tiger salamanders, Ambystoma tigrinum, but not to novel African clawed frogs, Xenopus laevis. However, when the newt was paired with simulated high risk, tadpoles generalized their responses to both tiger salamanders and African clawed frogs. Larval anurans seem to have a wider generalization frame than other animals.     

Colonial breeding and nest defence in Montagu's harrier (Circus pygargus)

We assessed whether colonial breeding allows individuals to decrease their investment in predator defence, by presenting decoys of owls, foxes and crows to Montagu's harrier, Circus pygargus. Decoy detection increased with colony size, as did the number of individuals mobbing the decoy. The number of mobbers was greater for predators potentially risky for the adults (owl or fox) than for non-dangerous predators (crow). Recruits (breeding neighbours, fledglings and non-breeders) were present a lower percentage of the time, and attacked and alarm called less frequently than tested individuals. Nevertheless, the overall attack rate on the predator increased with the number of mobbers. When the size of the mobbing group increased, individuals were more likely to attack predators that represented a risk for adults, but did so less intensively and with a lower frequency of close dives. Thus, coloniality decreased the individual costs of defence in terms of risk taken, whilst enhancing defence efficacy. Birds alarm called more intensively when presented with dangerous predators than with the crow. The number of recruits significantly increased with increasing alarm rate of the tested individuals, even when taking colony size into account. Furthermore, the alarm rate of the tested birds also had a significant effect on the proportion of recruits that engaged in attacks against dangerous predators but not against the crow. The higher recruitment and attack rates for dangerous predators were thus apparently modulated through alarm calling. We discuss whether tested birds may manipulate recruits' behaviour to lessen their own risk.     

Choice and utilization of oviposition sites by female Calopteryx maculata (Odonata: Calopterygidae)

Summary Females of the damselfly Calopteryx maculata (de Beauvois) initially choose the larger of a pair of adjacent oviposition sites, about 70% of the time (Table 1), or whichever of two equal sized sites had other ovipositing females on it (about 88% of the time-Table 2). These criteria for initial choice between a pair of sites also interact. Incoming females generally (57 to 74% of the time-Table 3) joined others on the small site rather than ovipositing alone at the adjacent, bigger site. When pairs of large and small sites were replicated across eight locations, there were nonsignificant trends towards greater utilization (eggs laid) of the larger of a pair of oviposition sites within locations (Table 4). The lack of agreement between initial choice and utilization shows that other factors besides size are important in the choice and use of oviposition sites. These include disturbance by males, the presence of other females and choice criteria that can only be assessed during oviposition. When all sites at the eight locations were equal in size, there was considerable day to day and location to location variation in eggs laid (Fig. 1). Viewed over periods of several days, some sites are obviously less attractive than others in terms of cumulative numbers of eggs laid at them. When the amount of vegetation was varied among locations, those with the bigger oviposition sites were used more often, somtimes significantly so, but there were also significant reversals (small sites used more often) (Table 5, Fig. 1). Thus, there is no simple effect of size on the utilization of oviposition sites by Calopteryx maculata females, despite a clear tendency for females to make initial choices based on this criterion. The considerable among and within location variation in number of eggs laid may reflect additional choice criteria or the interaction of size, the presence of other females, disturbance, and location.     

Loss of mating opportunities influences refuge use in the Iberian rock lizard,<Emphasis Type="Italic"> Lacerta monticola</Emphasis>

Because time spent in refuge may be costly if prey lose opportunities to forage, fight, or mate, prey allow predators to approach closer before beginning to flee when opportunity costs are high. Because the same opportunity costs may apply to refuge use as to escape, prey should make similar trade-offs between risk of emerging and cost of remaining in refuge. In the Iberian rock lizard, Lacerta monticola, we studied the effects of sex, reproductive season, speed of predator approach, and potential loss of mating opportunities on time spent in refuge following simulated predatory attacks. Lizards of both sexes adjusted refuge use to the level of risk by spending more time in refuge when approached rapidly than slowly. Females remained in refuge for equal times in the mating and postreproductive seasons, but males emerged sooner during the mating season, suggesting adjustment to a cost of lost opportunity to search for mates during the mating season. When a tethered female was nearby, males emerged from refuge earlier than if no female was present, indicating a trade-off between risk and mating opportunity. Approach speed affected emergence time when females were absent, but not when a female was present. Approach speed did not affect the probability that, after emerging, a male would return to court the female. For males that courted females intensely (bit them) before entering refuge, approach speed did not affect latency to emerge, but males that courted less intensely emerged sooner if approached slowly than rapidly. These findings show that males adjust the length of time spent in refuge to both risk of predation and reproductive cost of refuge use.Communicated by A. Mathis     

Why are larger convict cichlid (Cichlasoma nigrofasciatum) fry sometimes adopted into broods of smaller fry?

Females of Elasmucha grisea defend their eggs and small nymphs against invertebrate predators. Females sometimes guard their clutches side by side on the same birch leaf. We studied benefits of this joint guarding both in the field and in the laboratory. We found that adjacent females had significantly larger clutches than solitary females. In the laboratory, we studied the effectiveness of joint versus single defence against ant (Formica uralensis) predators. We established female pairs from initially singly guarding females by cutting off pieces of leaves with egg clutches and pasting them beside another female guarding her clutch. In the control group the females with their clutches were similarly cut off but these clutches were placed on another leaf without any female. The birch twigs where females guarded their clutches were placed in cages in close proximity to laboratory ant nests. In the experimental treatment, two females guarded their clutches together and at the same nest there was another birch twig without a female. In the control treatment two twigs with one female on each were placed close to another ant nest. Two females defended their clutches significantly more successfully, losing fewer eggs than did the single females. This primitive form of female sociality in parent bugs resembles colonial nesting in birds, where communal defence is also important. However, to our knowledge this is the first experiment where the benefit of joint guarding has been tested directly by manipulating the size of the breeding group rather than by measuring the risk of predation in groups of different size.     

The special role of male Cebus monkeys in predation avoidance and its effect on group composition

Summary Vigilance behavior, predator detection abilities, and responses to real and model predators were studied in two species of capuchin monkeys (Cebus albifrons and C. apella) in a Peruvian lowland rain forest. Adult males were more vigilant than adult females in both species, mainly because the males spent less time feeding and foraging and partly because they were at the periphery more often than the females. The increased vigilance of adult males is reflected in their superior performance in the detection of (model) predators. Adult and subadult males were also far more likely to approach and mob real and model predators. Adults that were outside the center of the group increased foraging activities but cut back an feeding, much of which was done in exposed tree crowns. Current theory suggests that primate groups are multi-male when a single male is unable to defend sexual access to the group of females. In these small capuchin groups, which are multimale, the enhanced safety of females and young provided by extra adult males furnishes a more plausible explanation. A comparison of the two capuchins with the ecologically similar Southeast Asian Macaca fascicularis suggests that the high predation risk outside the group may also have caused the unusual male career profile in capuchins, which have a long tenure of dominants and a very long potential lifespan. Further predictions of this hypothesis are developed.     

Conspicuous displays in cryptic males of a polytypic poison-dart frog

The evolution of aposematism is linked to increased opportunities for conspicuous sexual displays since detection by potential predators is no longer disadvantageous. Therefore, phenotypic divergence in aposematic species leading to relatively cryptic forms is expected to constrain such opportunities, by restoring the trade-off between natural and sexual selection on the boldness of sexual displays. We asked if and how a derived phenotype of the poison-dart frog Oophaga granulifera that appears relatively cryptic to potential predators exhibits conspicuous sexual displays for potential mates. We used visual modeling of frog contrasts against their natural backgrounds to test if for conspecifics green frogs appear less conspicuous than red frogs as they do for birds. We conducted behavioral observations of focal red and green males to determine if green frogs adjust their display behavior to the availability of potential mates. Dorsal brightness is known to influence female preferences in at least one poison frog species. We found that, despite being less visible under some measures, green frogs may appear as bright as red frogs for conspecifics but not birds, when viewed on dark backgrounds. Additionally, green males called more intermittently than red males when advertising to distant females, but they exhibited a dramatic increase in calling activity in proximity of a female and were as active as red males in this context. Together, our results suggest that green frogs retain context-dependent conspicuousness to conspecifics despite the evolution of relative crypsis to potential predators.     

Pair territoriality of wintering stonechats : behaviour,function and hormones

Migratory stonechats (Saxicola torquata) spend the winter in the northern Negev desert in Israel. After arrival in October most birds defend territories throughout the winter either as heterosexual pairs or as single birds. In this population we examined: (1) aggressive behaviour of pairs; (2) the functional significance of pair territoriality; and (3) hormonal correlates of territorial behaviour. Pairs were aggressive towards both conspecific intruders and stonechat dummies, particularly in autumn when territories were established. Males were more aggressive than females and aggression was primarily intrasexual. More frequent than intraspecific interactions were interspecific encounters, with 94% involving the local mourning wheatear (Oenanthe lugens). With one exception these encounters consisted of attacks of mourning wheatears against stonechats, mainly males. Two functions of winter territoriality of migrant pairs are proposed: (a) a reduction of individual defense costs associated with the maintenance of a territory; (b) an increase of the net vigilance to reduce the risk of attacks by competitors or predators. The levels of testosterone (males and females) and estradiol (females only) were close to or below the lower detection limit of the assay throughout the winter. Therefore, high levels of gonadal steroids are not required for pair formation and aggression in the non-reproductive context. The results indicate that both the function and the proximate control mechanisms of territoriality during the non-breeding season in winter are different from those during the breeding season in spring.     

Aphid alarm pheromone (E)-β-farnesene: A host finding kairomone for the aphid primary parasitoidAphidius uzbekistanicus (Hymenoptera: Aphidiinae)

Summary The present study aimed to test the possible function of the aphid alarm pheromone (E)--farnesene (EBF) as a host finding kairomone for aphid primary parasitoids. Extracts of volatile emissions of undisturbed aphids and of aphids under parasitoid attack were obtained by air entrainment. Extracts of cornicle secretions were gained by disturbing aphids and taking their secretions into solution. Extracts were compared by gas chromatography. Only air entrainments of aphids under attack and solvent extracts of cornicle secretions contained the alarm pheromone. In Y-tube olfactometer bioassays, femaleA. uzbekistanicus were attracted to aphid groups under attack of parasitoids, presumably by released EBF. High concentrations of synthetic EBF (1.4 µg to 5.7 µg) also attractedA. uzbekistanicus females. Females with oviposition experience reacted more readily to lower concentrations of EBF than females without experience. In experiments designed as Petri-dish bioassays, the test animals could contact filter paper discs that were treated with solutions containing EBF. Behavioural effects like antennation or stinging attack were not observed. With computer video analysis of parasitoid movements, some effects onA. uzbekistanicus behaviour were detected, again indicating attraction to EBF.As the volatile aphid alarm pheromone attractedA. uzbekistanicus females, it can be concluded that this chemical stimulus acts as a host finding kairomone for this parasitoid species. However, its effect over long distances seems to be limited due to the relatively high concentrations required for reactions. Of two other parasitoid species examined (P. volucre andL. testaceipes) onlyP. volucre was also significantly attracted to the volatile EBF in the Y-tube olfactometer.     

Vigilance in wild Thomas's langurs (Presbytis thomasi ): the importance of infanticide risk

This study examines vigilance as a behavioural indicator of the importance of infanticide risk by comparing the infanticide avoidance hypothesis with the predation avoidance and mate defence hypotheses for wild Thomas's langurs (Presbytis thomasi) in Sumatra. We found that all individuals were more vigilant in situations of high predation risk, i.e. lower in the trees and in the absence of neighbours. Females were also more vigilant on the periphery of the group. However, there were variations in vigilance levels that could not be accounted for by the predation avoidance hypothesis. Males without infants showed higher levels of vigilance in areas of home range overlap than in non-overlap areas during the early phase of their tenure, strongly suggesting mate defence. In these areas of home range overlap where Thomas's langur groups can interact, males may attack females and infants, and so the infanticide risk for males and females with infants is likely to be high in these areas. Only females with infants, but not males with infants or females without infants, showed higher vigilance levels in overlap areas than in non-overlap areas; in addition, in overlap areas, females with an infant were more vigilant than females without an infant, while this was not the case in non-overlap areas. Both females and males with infants were more vigilant high in the trees than at medium heights in overlap areas but not elsewhere. These findings can only be explained by the infanticide avoidance hypothesis. In contrast to predator attacks, infanticidal male attacks come from high in the canopy, and only occur in overlap areas. There was a significant sex difference in vigilance, but males were only more vigilant than females without an infant, and not more vigilant than females with an infant. We conclude that vigilance varied mainly in relation to the risk of predation and infanticide. Mate competition only played a role for males during the early phase of their tenure. Predation risk seems to offer the best explanation for vigilance for all individuals in the absence of infants. Both predation risk and infanticide risk played a role for females and males with infants. Received: 4 April 1998 / Accepted after revision: 6 September 1998     

Lekking behavior in the neotropical frog Ololygon rubra

Summary This is the first study to document in detail the satisfaction of Bradbury's four criteria for categorizing any anuran as a classical lekking species. The paternal care of male neotropical frogs, Ololygon rubra, consisted of minimal contributions of their genes. Males competed acoustically at traditional, defended, clustered sites (Fig. 1, Table 3) to attract gravid females, who paired with the males at these locations but took the amplectant males to oviposition sites away from the pairing sites. Individual males apparently did not control resources necessary for attracting females, because there were no correlations between male numbers and measured habitat variables, or between male numbers and oviposition sites. On chorusing nights, males always arrived at their display arenas before any females were observed. Females moved freely among clusters and males, before making their choices of mates. However, males employed other mate acquisition strategies that tended to undermine the initial female choices. The predictions that lekking species should have a relatively extended breeding season, a highly biased operational sex ratio (OSR), and an absence of male control of resources essential for female acquisition were also evaluated and corroborated. These frogs have two long breeding seasons encompassing a total of about 6 months (Fig. 2). There were strongly male biased nightly OSRs (Table 1), that contributed to high variance in male reproductive success (RS), but reduced indices of sexual selection, and a relatively low coefficient of variation (CV) of male RS (Table 5) compared to other amphibians. Thus, all of this evidence supports the conclusion that O. rubra in coastal Guyana uses a lek mating system.     

Client preferences by Caribbean cleaning gobies: food,safety or something else?

Predation risk is amongst the most pervasive selective pressures influencing behaviour and animals have been repeatedly shown to trade-off foraging success for safety. We examined the nature of this trade-off in cleaning symbioses amongst Caribbean coral reef fishes. We predicted that cleaning gobies (Elacatinus evelynae and Elacatinus prochilos) should prefer fish clients that pose a low risk of predation (e.g. herbivores) over clients that may have more ectoparasites but pose a higher risk (e.g. piscivores). Our field observations revealed that cleaners did clean preferentially client species with more parasites but predatory and non-predatory clients had similar ectoparasite loads. Despite the lack of a foraging advantage for inspecting predators, cleaners did not avoid risky clients. On the contrary, a larger proportion of visiting predators than non-predators was inspected, gobies initiated more interactions with predatory clients, and predators were attended to immediately upon arrival at cleaning stations. This preferential treatment of dangerous clients may allow the rapid identification of cleaners as non-prey item or may be due to the effect of predators on the rest of the cleaners’ clientele, which avoided cleaning stations whilst predators were present. Dealing with potentially risky clients may allow gobies to regain access to their main food source: non-predatory clients.     

Hunted hunters? Effect of group size on predation risk and growth in the Australian subsocial crab spider Diaea ergandros

A reduced predation risk is considered to be a major adaptive advantage of sociality. While most studies are concerned with non-predatory prey species, group-living predators are likely to face similar threats from higher-order predators. We studied the relationship between group size and predation risk in the subsocial crab spider Diaea ergandros by testing predictions from theoretical models including attack abatement as well as the formation of protective retreats. In a field survey, we found predatory clubionid spiders in 35 % of the D. ergandros nests and as predicted, nest size did not correlate with predator presence. In a subsequent laboratory experiment, we observed survival probability, nest construction activity and feeding behaviour including weight development between groups of different sizes as well as in the absence or presence of a predator. Large groups had an advantage in terms of survival and growth compared to smaller groups or single individuals. They also built significantly larger nests than smaller groups, supporting the idea of protective retreat formation being an adaptive benefit to group living. Even though clubionids did attack D. ergandros, they did not significantly affect overall mortality of D. ergandros. The feeding experiment showed that spiders fed on a larger proportion of flies in the presence of a predator. However, these groups gained significantly less weight compared to the control groups, indicating that the potential predators not only act as predators but also as food competitors, constituting a twofold cost for D. ergandros.     

Competition with flies promotes communal breeding in the burying beetle,Nicrophorus tomentosus

Communal breeding through nest-sharing may benefit cooperating individuals indirectly, in increased inclusive fitness, or directly, when environmental constraints reduce the fitness of solitary breeders. Burying beetles provide extensive parental care and can breed either in pairs or in larger groups of unrelated males and females. Parentage of communally-reared broods is usually shared but is skewed in favor of the individuals of each sex that provide longer care. Females provide care longer than males, and two females are more likely to remain together in the brood chamber than two males are. Flies and other burying beetles are the major competitors for carcasses and this study suggests that it is competition with flies that promotes communal breeding inNicrophorus tomentosus On medium-size carcasses (35–40 g) the presence or absence of oviposition by flies had a significant effect on the size of the brood reared, and on large carcasses (55–60 g) the number of beetles present, two or four, had a significant effect on brood size. On both medium and large carcasses, pairs rearing broods on flyblown carcasses had fewer young than pairs on clean carcasses or foursomes on flyblown carcasses. There was a strong trend for an interaction effect between number of beetles and competition with flies (Table 1). Duration of parental care was not affected by competition with flies except for that of the first male to depart, which provided care longer on flyblown carcasses (Table 2). Pairs and foursomes were equally able to defend the carcass and brood from conspecific intruders and from larger intrudingNicrophorus orbicollis (Table 3).     

Fieldfare (Turdus pilaris) breeding success in relation to colony size,nest position and association with Merlins (Falco columbarius)

Summary Clutch size, nestling production and breeding success were studied in colonial Fieldfares (Turdus pilaris) in a subalpine birch forest during ten breeding seasons. Reproductive success was highest for central pairs in large colonies; such pairs benefited most from communal defence against nest predators. Fieldfares and Merlins (Falco columbarius) usually bred in association. Fieldfares breeding away from Merlins had lower breeding success than pairs associated with Merlins, which also benefited by reduced nest predation. Fieldfares apparently chose to nest near Merlins, which had already laid eggs when the thrushes started nest-building.     

Male mating speed promote hybridization in the Rana lessonae–Rana esculenta waterfrog system

Hybridization is a widespread phenomenon in many vertebrate groups. Prezygotic isolating mechanisms, probably caused by selection against hybrids with reduced fitness, reduce the likelihood of such events. Although hybrid-reduced fitness relatively to parental species is common, hybridization can also be beneficial, and hybrids sometimes outperform the pure species type. In this study, we examined two potential processes, Hubbs’s principle and male–male competition, which could enhance hybridization in the waterfrog complex and thus explain the proportion of heterospecific pairs collected in a natural pond. Firstly, by collecting 791 frogs in the field to study pair and chorus composition, we showed that in a mixed Rana lessonae–Rana esculenta population, the scarcity of hybrid R. esculenta males did not account for the proportion of heterospecific pairs: indeed, when examining pairing composition in six different choruses, we found that hybrid males were always under-represented and that R. esculenta females were found paired with R. lessonae males. Secondly, we investigated experimentally whether or nor male–male competition mechanism could explain pair formation in waterfrogs. Our mating speed experiment highlights mechanisms that could explain heterospecific pairs in a context of promiscuous mating where scramble competition was intense. To measure the rapidity with which a male grasps a female, we placed males in a grid cage with a female, and the dynamics of pair formation was monitored. R. esculenta males showed a lower pairing success than R. lessonae males as a smaller proportion of them amplexed females, and more time was needed for them to get amplexed. Thus, a less adaptative mechanism than female mate choice may also explain the mating pattern observed in waterfrog species.     

Replacement males in the western bluebird: opportunity for paternity, chick-feeding rules, and fitness consequences of male parental care

In western bluebirds (Sialia mexicana), most pairs remain together for life and share equally in post-hatching parental care. We removed resident males of socially monogamous pairs during laying and after clutch completion to examine chick-feeding rules used by replacement males and current and future fitness consequences of paternal care. Replacement males were not infanticidal and 7 (47%) fed nestlings. Feeding replacement males and the females they joined fed at rates similar to controls. Females without a feeding replacement male compensated by feeding more themselves so that overall feeding rates were not compromised, but they reduced their brooding time. Unlike assisted females, unassisted females exhibited reduced nesting success and their 14-day-old chicks weighed less than controls. Field metabolic rates of unassisted females were 17% higher than those of control females, but the difference was not statistically significant. Older females were better able to raise young without the male's help than were yearling females. Female condition was not affected by male provisioning and unassisted females were as likely to survive to the next breeding season as assisted females. We found no future benefits of provisioning by replacement males; those that fed were no more likely to breed with the female on her subsequent attempt than were males that did not feed, and subsequent clutch sizes were not reduced for females rearing young without the male's help. These experiments suggest that male parental care increases nesting success in western bluebirds and that replacement males use an all-or-none rule to determine whether or not to feed chicks: if they are present during the fertile period they feed at typical rates; if they are not, they usually do not feed at all. Because chick-feeding by males is tied to opportunity for paternity, influences success in the current nest, and does not affect the male's future breeding success, it appears to be parental rather than mating effort. Received: 8 May 1998 / Accepted after revision: 23 July 1998     

Habituation in the green frog, Rana clamitans

Habituation and its role in the dear enemy effect was investigated in a population of green frogs, Rana clamitans. Green frogs have a prolonged breeding season, and males defend territories centered around suitable oviposition sites. We tested the prediction that male green frogs will habituate to broadcasts of synthetic conspecific stimuli. Our results indicate that male green frogs can discriminate familiar from unfamiliar stimuli. We suggest that habituation helps to mediate the territorial interactions between male green frogs. Strangers present a greater threat than familiar neighbors. By habituating to the advertisement vocalizations of their near neighbors, males avoid costly interactions with individuals that are not a major threat to their territories. Received: 20 July 1998 / Accepted after revision: 6 September 1998     

Differential predator escape performance contributes to a latitudinal sex ratio cline in a migratory shorebird

Sexual segregation outside the mating season is common in vertebrates, and has been attributed to sexual differences in predator escape performance in ungulates and fish, but not in birds. Here, we tested the hypothesis that sex- and latitude-specific predator escape performance underlies the differential nonbreeding distribution of western sandpipers (Calidris mauri), a migratory shorebird. Females overwinter further south along the American Pacific coast, creating a latitudinal cline in sex ratio. Escape performance is reduced with increasing body mass, and birds generally carry less fat further south. Western sandpipers with poor escape performance were therefore predicted to prefer southern sites to reduce the risk of mortality posed by predators. Data from four nonbreeding latitudes showed that wing loading, used as an index of escape performance, was overall higher for females, and that it decreased with latitude in both sexes. Within latitudes, wing loading was lower at smaller, and presumably more dangerous, sites. Flight response to a predatory attack was longer in the south. Mortality risk offers a novel and candidate explanation for differential distribution patterns in western sandpipers and possibly other avian migrants.