Acoustic recognition of predators by mantled howler monkeys (Alouatta palliata): A playback experiment with naïve and experienced subjects.

OBJECTIVES: When the production of antipredator behaviors is costly, prey is expected to stop displaying such behaviors and lose the ability to recognize extirpated predators. However, the loss or maintenance of predator recognition abilities is conditional on the eco-evolutionary context of prey. Here, we examined the behavioral responses of naïve and experienced mantled howler monkeys (Alouatta palliata) to simulated acoustic cues from natural predators. METHODS: We studied experienced individuals in the Uxpanapa Valley and naïve individuals in Los Tuxtlas (Veracruz, México). Jaguars (Panthera onca) and harpy eagles (Harpia harpyja), the main predators of howler monkeys, are extant in the Uxpanapa Valley but have been extirpated in Los Tuxtlas for approximately 70 and 45 years, respectively. We exposed six naïve and six experienced groups to playbacks of acoustic stimuli from the two predators and a non-predator control species (plain chachalacas, Ortalis vetula), and recorded the latency, frequency, and duration of antipredation behaviors (n = 127 trials). RESULTS: In contrast with experienced mantled howler monkeys, naïve subjects did not respond to trials from harpy eagles. However, response patterns were generally similar between naïve and experienced individuals when exposed to jaguar stimuli. DISCUSSION: Our findings suggest that naïve mantled howler monkeys do not recognize harpy eagle calls, but they respond to jaguar calls in a manner consistent with experienced individuals. These results illustrate how different mechanisms for the recognition of extirpated predators operate within a single species according to evolutionary and ecological experience.

Behavioral trade-offs and multitasking by elk in relation to predation risk from Mexican gray wolves.

Predator non-consumptive effects (NCE) can alter prey foraging time and habitat use, potentially reducing fitness. Prey can mitigate NCEs by increasing vigilance, chewing-vigilance synchronization, and spatiotemporal avoidance of predators. We quantified the relationship between Mexican wolf (Canis lupus baileyi) predation risk and elk (Cervus canadensis) behavior. We conducted behavioral observations on adult female elk and developed predation risk indices using GPS collar data from Mexican wolves, locations of elk killed by wolves, and landscape covariates. We compared a priori models to determine the best predictors of adult female behavior and multitasking. Metrics that quantified both spatial and temporal predation risk were the most predictive. Vigilance was positively associated with increased predation risk. The effect of predation risk on foraging and resting differed across diurnal periods. During midday when wolf activity was lower, the probability of foraging increased while resting decreased in high-risk areas. During crepuscular periods when elk and wolves were most active, increased predation risk was associated with increased vigilance and slight decreases in foraging. Our results suggest elk are temporally avoiding predation risk from Mexican wolves by trading resting for foraging, a trade-off often not evaluated in behavioral studies. Probability of multitasking depended on canopy openness and an interaction between maternal period and predation risk; multitasking decreased prior to parturition and increased post parturition in high-risk areas. Openness was inversely related to multitasking. These results suggest adult female elk are altering the type of vigilance used depending on resource availability/quality, current energetic needs, and predation risk. Our results highlight potentially important, but often-excluded behaviors and trade-offs prey species may use to reduce the indirect effects of predation and contribute additional context to our understanding of predator-prey dynamics.

Risk effects cascade up to an obligate scavenger.

The effects of predation risk on prey populations have been studied extensively; yet, how risk is manifested in a trophically linked guild-scavengers-has been overlooked. Risk could be particularly consequential for obligate scavengers that are vulnerable while foraging and rely on carrion provisioned by, and shared with, apex predators. We investigated whether Andean condors (Vultur gryphus) respond to predation risk in a landscape where the main source of carrion are camelids killed by pumas (Puma concolor). We hypothesized that condors would exhibit different behavioral responses to predation risk while they search, encounter, and exploit carrion. We explored condor habitat selection while flying by tracking nine birds with satellite transmitters and monitored via camera traps 41 natural carcasses and 25 experimental carrion stations. We found that condors searched for carrion in areas with a high probability of occurrence of puma kills. However, condors avoided exploiting carrion in areas featuring tall vegetation and steep slopes-selected by pumas to stalk prey-suggesting that condors manage risk primarily through the identification of safe foraging sites prior to landing. Our finding that condors avoided foraging near stalking cover for pumas highlights the importance of risk effects beyond predator-prey interactions, particularly for obligate scavengers.

Co-occurrence between the presence of epidermal giant cells and alarm chemical cues in tadpole skin homogenates: An ontogenetic and cross-species comparison analysis.

In amphibians, intra- or interspecific chemical cues are an important source of information about possible predation risk. In anuran tadpoles, this information causes changes at different levels including behavior, morphology, and growth and development. It has been shown that chemical alarm cues trigger antipredator behaviors, such as decreased exploratory activity, in a wide variety of anuran species; however, the cellular origin of the chemical cues has not yet been confirmed by new evidence. Previous works have suggested that the alarm cues originate from a particular cell type in the skin in tadpoles of the family Bufonidae: the epidermal giant cells (GCs). Here, we confirm the presence of GCs in the epidermis of Rhinella arenarum larvae from developmental stages as early as G22, when free-swimming larvae show gregarious behavior. In addition, larval skin homogenates trigger antipredator behaviors in conspecifics from stage G22 onwards, but not at early stages (G19 and G21). This fact exposes experimental evidence for the coexistence between the appearance of GCs and the production of chemical alarm cues during the development of R. arenarum. Furthermore, the antipredator behavioral response of R. arenarum larvae triggered by skin preparations of other species that belong to the same family who also exhibit GCs allows us to speculate that chemical cues appear to be conserved among phylogenetically related species, allowing them to cross-respond to heterospecific cues. Our experimental approaches support the role of GCs as the source of alarm cues in anuran larvae of the family Bufonidae.

Development of snake-directed antipredator behavior by wild white-faced capuchin monkeys: III. the signaling properties of alarm-call tonality.

In many primates, the acoustic properties of alarm calls can provide information on the level of perceived predatory threat as well as influence the antipredator behavior of nearby conspecifics. The present study examined the harmonics-to-noise ratio (tonality of spectral structure) of alarm calls emitted by white-faced capuchin monkeys (Cebus capucinus) in trees directed at photographic models of a boa constrictor, neotropical rattlesnake, scorpion eater snake, and white snake-shaped control presented on the ground. The average and peak harmonics-to-noise ratios of initial alarm calls by infants, juveniles, and adults and those of nearby second callers were analyzed using PRAAT software. Averaged for age class, the peak harmonics-to-noise ratio of alarm calls directed at the boa constrictor model, characterizing a primary capuchin predator, was reliably higher than the peak harmonics-to-noise ratio of alarm calls directed at the harmless scorpion eater model. This effect was influenced by the higher harmonics-to-noise ratio of infant alarm calls and it disconfirmed our prediction, based on primate vocalization research, that snake perception would increase arousal and alarm-call noisiness. Levels of call tonality did not distinguish the boa and rattlesnake or rattlesnake and scorpion eater models for any age class. Higher alarm-call tonality appeared contagious to nearby perceivers, with focal alarm calling influencing the level of tonality of the first calls of second callers. Together, these findings suggest that the higher peak harmonics-to-noise ratio of capuchin alarm calling directed at snakes is contagious and possibly conveys information about the level of perceived predatory threat.

Ventilation responses to predator odors and conspecific chemical alarm cues in the frillfin goby.

The chemical detection of predation risk is direct when based on predator odors, or indirect when an injured conspecific or heterospecific signal it. Physiological adjustments may be necessary in parallel to defensive reactions to cope with an imminent risk. Here, we tested the effects of predator odors and conspecific chemical alarm cues in ventilation response (VR) of frillfin goby, Bathygobius soporator, because this response increases oxygen uptake for supporting behavioral tasks. No VR change was detected in response to odors of predators (catfish) that fed on conspecific, heterospecific fish (tilapia), or were deprived of food and to non-predator (tilapia) that fed chow (non-specific odor control) and odor eluent. The goby's VR, however, increased in response to conspecific alarm cues, but not to heterospecific cues or eluent. Clearly, the VR response in fish depends on the nature of the chemical cue. It is in line with 'threat-sensitive hypothesis' as a chemical cue from an injured prey might mean a foraging predator, whilst the mere presence of a predator odor might not. In addition, because VR can increase, decrease or remains unchanged in response to predation risk in other fish species (including other gobies), we reinforces the species-specific chracteristic of VR responses in fish, regarding the results obtained here for frillfin gobies.

Fatal attack on a Rylands' bald-faced saki monkey (Pithecia rylandsi) by a black-and-white hawk-eagle (Spizaetus melanoleucus).

Predation risk has played an important role in primate behavioral evolution, yet natural primate-predator interactions are rarely observed. We describe the consumption and probable predation of an adult bald-faced saki monkey (Pithecia rylandsi) by a black-and-white hawk-eagle (Spizaetus melanoleucus) at the Los Amigos Biological Station in lowland Amazonian Peru. To our knowledge, this is the first published case of a black-and-white hawk-eagle consuming any primate species. We contend that while most reported observations of successful and attempted predation by raptors involves the largest and most notorious species (i.e. the harpy eagle), smaller and lesser known species like S. melanoleucus should be considered more seriously as a predator of neotropical primates. We discuss the predation event in the context of understanding what other neotropical primates might be vulnerable to S. melanoleucus predation given its body size and hunting tactic.

Predatory threat of harpy eagles for yellow-breasted capuchin monkeys in the Atlantic Forest.

We describe seven encounters between different harpy eagle individuals (Harpia harpyja) and a group of yellow-breasted capuchin monkeys (Sapajus xanthosternos) in Una Biological Reserve. These interactions lasted 58 min on average. In each of those encounters, the capuchin monkeys used particular behavioral strategies against the harpy eagle that were not employed in reaction to other aerial predators. We did not observe any successful predation events, but after one of those encounters an infant disappeared from the capuchin group. As a whole, these observations indicate that the presence of harpy eagles in the group's home range increases predation risk for capuchin monkeys. The present report also suggests a reoccupation by H. harpyja of this area, as no previous recent records identify harpy eagle occurrence in Una Biological Reserve.

Inter-individual variation and temperature-dependent antipredator behavior in the snake Tomodon dorsatus (Dipsadidae).

Although many studies assessed the influence of temperature on the behavior of ectotermic vertebrates, little attention has been given to interindividual variation in the defensive responses of reptiles. In the present study we investigated the defensive behavior of the snake Tomodon dorsatus, in order to test the hypotheses that (1) individuals differ in their antipredator behavior consistently with the concept of behavioral syndromes, (2) temperature influences the defensive behavior, and (3) these two factors interact with each other. There was significant interindividual variation in defensive behavior, as well as consistently aggressive, passive or evasive behaviors. Temperature influenced aggressiveness, which was slightly higher when body temperature was lower, but this trend was only evident in animals with aggressive disposition. Our results corroborate the hypothesis of interaction between individuality of behavior and temperature-dependent defensive behavior in T. dorsatus. These results, together with results from previous studies, suggest that the evolution of temperature-dependent defensive behavior differs among lineages of ectothermic tetrapods. This article is part of a Special Issue entitled: insert SI title.

Variación intraespecifica en el uso de Percha Nocturna de Basiliscus galeritus (Sauria: Corytophanidae) en Isla Palma, Pacífico Colombiano

Las variaciones en el uso de percha nocturna son en parte un reflejo de la partición de recursos que permite la coexistencia al disminuir la competencia intraespecifica entre individuos de diferentes sexos y tamaños. En este trabajo se evaluó el uso de percha nocturna en los machos, las hembras y los juveniles de Basiliscus galeritus en Isla Palma - Pacífico Colombiano en abril de 2011. Los individuos fueron capturados manualmente y se tomó la información de la altura de la percha, posición en la que estaban perchados, longitud rostro cloacal y cobertura vegetal. Se registraron 39 individuos, encontrando que el tipo de percha utilizado con mayor frecuencia fueron las ramas (46,15%) seguido por las hojas (38,46%) y ocasionalmente fueron observados sobre lianas, suelo y tallos. Se evaluo el grado de asociación entre los sexos y cada una de las variables estudiadas con la altura de percha utilizando tablas de contingencia. No se detectó asociación alguna aunque el uso de percha estuvo relacionado con el tamaño corporal del individuo, independiente de su sexo. (rs = 0,08, p = 0,7).

Variations in night perch use reflects the partitioning of resources, which allows coexistence by reducing intraspecific competition between individuals of different sexes and sizes. In this study we evaluated nocturnal perch use for males, females and juveniles of Basiliscus galeritus in Isla Palma - Pacífico Colombiano. In April of 2011, individuals were captured manually and we recorded the perch height, position in which they were perched, snout-vent length and vegetation cover. Thirty-nine individuals were recorded. We found that the most frequently used perch types were branches (46.15%), followed by leaves (38.46%), and occasionally individuals were observed on vines, soil and stems. The existence of an association between gender and each of the variables studied was evaluated using contingency tables. This was not a statistically significant association. However, we determined that the use of the night perch is more related to body size of an individual than sex or gender, as a positive correlation was found between the size and height of the perch (rs = 0.08, p = 0.7).

Variación intraespecifica en el uso de Percha Nocturna de Basiliscus galeritus (Sauria: Corytophanidae) en Isla Palma, Pacífico Colombiano

Las variaciones en el uso de percha nocturna son en parte un reflejo de la partición de recursos que permite la coexistencia al disminuir la competencia intraespecifica entre individuos de diferentes sexos y tamaños. En este trabajo se evaluó el uso de percha nocturna en los machos, las hembras y los juveniles de Basiliscus galeritus en Isla Palma - Pacífico Colombiano en abril de 2011. Los individuos fueron capturados manualmente y se tomó la información de la altura de la percha, posición en la que estaban perchados, longitud rostro cloacal y cobertura vegetal. Se registraron 39 individuos, encontrando que el tipo de percha utilizado con mayor frecuencia fueron las ramas (46,15%) seguido por las hojas (38,46%) y ocasionalmente fueron observados sobre lianas, suelo y tallos. Se evaluo el grado de asociación entre los sexos y cada una de las variables estudiadas con la altura de percha utilizando tablas de contingencia. No se detectó asociación alguna aunque el uso de percha estuvo relacionado con el tamaño corporal del individuo, independiente de su sexo. (rs = 0,08, p = 0,7).

Variations in night perch use reflects the partitioning of resources, which allows coexistence by reducing intraspecific competition between individuals of different sexes and sizes. In this study we evaluated nocturnal perch use for males, females and juveniles of Basiliscus galeritus in Isla Palma - Pacífico Colombiano. In April of 2011, individuals were captured manually and we recorded the perch height, position in which they were perched, snout-vent length and vegetation cover. Thirty-nine individuals were recorded. We found that the most frequently used perch types were branches (46.15%), followed by leaves (38.46%), and occasionally individuals were observed on vines, soil and stems. The existence of an association between gender and each of the variables studied was evaluated using contingency tables. This was not a statistically significant association. However, we determined that the use of the night perch is more related to body size of an individual than sex or gender, as a positive correlation was found between the size and height of the perch (rs = 0.08, p = 0.7).

Interactions mediated by predators in arthropod food webs / Interações mediadas por predadores em teias alimentares de artrópodes

Studies on interactions among plants, herbivores and natural enemies are important for understanding population dynamics of species in food webs, but they are also important for the practice of pest control with natural enemies. Biological control programs heavily rely on the occurrence of trophic cascades, where the addition of one natural enemy causes a decrease of pest densities and an increase of plant biomass. However, when more that one natural enemy is used to control various pests in the same system, artificial food webs are created and simple tritrophic interactions change to more complicated ones. The occurrence of complex interactions and omnivory in these food webs may modify the sign and the strength of direct effects of natural enemies on pests. In this paper, we show and discuss the experimental results on interactions mediated by predators in an artificial food web that occurs on cucumber plants in greenhouses where biological control is applied. The two pests in this food web are the two-spotted spider mite Tetranychus urticae Koch, and the western flower thrips Frankliniella occidentalis (Pergande). The predatory mites Phytoseiulus persimilis Athias-Henriot and Neoseiulus californicus (McGregor) are used to control spider mites, and the generalist predatory bug Orius laevigatus (Fieber) and a specialist predatory mite Neoseiulus cucumeris (Oudemans) are predators of thrips. Results from behavioural studies showed that some of these species are attracted to the same patch and do not avoid each other's presence. We show some complex interactions arising from the meeting of these species: (a) the intraguild predation by O. laevigatus on P. persimilis, (b) the use of spider-mite web as a refuge by thrips larvae against their predators. The consequences of such interactions for population dynamics of predators and prey and their implications for success of biological control are discussed.

Estudos sobre interações entre plantas, herbívoros e inimigos naturais são importantes para o entendimento da dinâmica populacional das espécies em teias alimentares, bem como para o sucesso do controle de pragas por inimigos naturais. Os programas de controle biológico fundamentam-se na ocorrência de sucessões tróficas, onde a adição de um inimigo natural causa o decréscimo na densidade da presa/hospedeiro e o aumento da biomassa da planta. Entretanto, quando mais de uma espécie de inimigo natural é usada para controlar várias pragas no mesmo sistema, teias alimentares artificiais são criadas e as interações tritróficas simples transformam-se em outras mais complicadas. A ocorrência de interações complexas e de onivoria nestas teias alimentares pode modificar a direção e a intensidade dos efeitos diretos dos inimigos naturais sobre as pragas. Neste artigo, são apresentados e discutidos os resultados experimentais sobre interações mediadas por predadores em uma teia alimentar artificial. Esta teia é formada em plantas de pepino em casa de vegetação onde o controle biológico é aplicado. A teia constitui-se de duas pragas, o ácaro rajado Tetranychus urticae Koch e o tripes Frankliniella occidentalis (Pergande). Para o controle dos ácaros rajados são liberados os ácaros predadores Phytoseiulus persimilis Athias-Henriot e Neoseiulus californicus (McGregor). O controle dos tripes é feito através de liberações do percevejo generalista Orius laevigatus (Fieber) e do ácaro predador especialista Neoseiulus cucumeris (Oudemans). Resultados de estudos comportamentais mostraram que algumas destas espécies são atraídas para o mesma planta e não evitam plantas ocupados por outras espécies. Quando estas espécies são encontradas na mesma planta, interações complexas ocorrem: (a) predação intraguilda de O. laevigatus sobre P. persimilis, (b) uso da teia produzida pelo ácaro rajado pelas larvas de tripes como refúgio contra seus predadores. As conseqüências ...