Low Predation Risk Research Articles

Predation pressure and food abundance during early life alter risk-taking behaviour and growth of guppies (Poecilia reticulata)

AbstractThe trade-off between predation risk and the need to feed is one of the major constraints animals have to cope with. Virtually all animals have a higher risk of being preyed upon when being active (e.g., searching for food or mating partners), compared with being inactive (e.g., staying at their burrows, nests, etc.). Yet, staying safe leads to a higher risk of starvation and may reduce reproductive success and body growth. Hence selection on behaviour optimizing the search, handling and digestion of food while avoiding the risk of predation is strong and should lead to strategies maximising survival chances and inclusive fitness. These facts call for integrative studies manipulating both, abundance of food and predation risk in a factorial set up, analysing the effects of both factors on behaviour and physiological parameters. We present results of a 2 × 2 factorial experiment, manipulating risk of predation and food abundance in guppies. We found that the two factors have an additive effect on body growth, but that predation risk by a pike cichlid is the main factor affecting the expression of behavioural strategies in guppies. Low food availability and high predation risk led to lower body growth. High predation risk affected swimming depth and risk sensitivity of guppies and might represent adaptive behavioural changes to the environmental context experienced in early life. Our study shows that integrative studies, analysing multiple interdependent and interconnected factors in the wild and in the lab are needed to further understand animal behaviour and development.

Cost-free vigilance during feeding in folivorous primates? Examining the effect of predation risk, scramble competition, and infanticide threat on vigilance in ursine colobus monkeys (Colobus vellerosus)

Vigilance often decreases with increasing group size, due to lower predation risk or greater scramble competition for food. A group size effect on vigilance is seldom seen in primates, perhaps because scanning and feeding often occur simultaneously or because the distinction between routine and induced vigilance has not been investigated. We analyzed feeding and resting observations separately while distinguishing between routine and induced scans in four groups of wild ursine colobus monkeys (Colobus vellerosus) experiencing scramble competition for food and infanticide risk. We used linear mixed-effect models to test the effect of group size, age–sex class, number of neighbors, number of adult male neighbors, and height in the canopy on scanning rates (vigilance) with and without evident conspecific threat. Food type was also examined in the feeding models. Perceived predation risk affected vigilance more than scramble competition for food and infanticide risk. Routine and induced vigilance were greatest at lower canopy heights during feeding and resting and increased when individuals had fewer neighbors while resting. A group size effect was found on induced vigilance while resting, but scanning increased with group size, which probably indicates visual monitoring of conspecifics. Scanning rates decreased while feeding on foods that required extensive manipulation. This supports the idea that vigilance is relatively cost free for upright feeders when eating food that requires little manipulation, a common feature of folivore diets. In the presence of threatening conspecific males, close proximity to resident males decreased individual vigilance, demonstrating the defensive role of these males in the group.

Contrasting behavioural responses of grazing mayflies and detritivorous caddisflies to predatory fish

Invertebrates living in streams where predatory fish are present are often able to detect them through water-borne chemical cues and respond with behavioural changes that lower predation risk. We hypothesised that behavioural responses to a predatory fish (brown trout, Salmo trutta) would be stronger in grazing mayflies (Baetis sp. and Epeorus sp.) than in detritivorous caddisflies (Potamophylax latipennis and Chaetopteryx sp.) in a montane stream in central Spain, because of differences in their foraging ecology and the presence of a protective case in the latter. Grazing mayflies reduced their rates of movement and entrance into the drift when trout were present, but this response disappeared shortly after trout removal by electrofishing. Mayflies also showed marked drift diel periodicity when trout were present. In contrast, detritivorous caddisflies responded to the potential predation threat by withdrawing into their case. However, their response was the same regardless of the presence of trout, which also had no influence on their movement patterns or drift activity. Our results suggest that effects of predatory fish on stream invertebrates vary with invertebrate traits such as foraging ecology and predator-avoidance strategies.

Intraspecific variation in diet, growth, and morphology of landlocked Galaxias maculatus during its larval period: the role of food availability and predation risk

Food availability and predation risk have been shown to affect phenotypes during early life history of fishes. Galaxias maculatus, a small fish widely distributed around the southern hemisphere, clearly exhibits a complex trade-off between feeding and predation avoidance during growth over the larval period. We studied the effect of different environmental variables on diet, growth, mortality, and morphology through field surveys and data revision in the literature for limnetic G. maculatus larvae in five oligotrophic lakes of Patagonia. Both number of food categories and prey ingested by larvae were directly related to zooplankton density. Larval growth rate was related with zooplankton density and temperature. Lakes with high zooplankton densities and low predation risk had larvae with deeper bodies and shorter caudal peduncles, while in lakes with less food and high predation risk larvae were slender with shallower bodies and longer peduncles. Food availability and predation risk seem to operate on the swimming performance of G. maculatus larvae through the slenderness of the body and the length of the caudal peduncle. The observed phenotypic variation in growth and morphology could be a key feature that has allowed this species to successfully colonize a wide variety of environments in the southern hemisphere.

Critical threshold size for overwintering sandeels (Ammodytes marinus)

Several ecologically and commercially important fish species spend the winter in a state of minimum feeding activity and at lower risk of predation. To enable this overwintering behaviour, energetic reserves are generated prior to winter to support winter metabolism. Maintenance metabolism in fish scales with body size and increases with temperature, and the two factors together determine a critical threshold size for passive overwintering below which the organism is unlikely to survive without feeding. This is because the energetic cost of metabolism exceeds maximum energy reserves. In the present study, we estimated the energetic cost of overwintering from a bioenergetic model. The model was parameterised using respirometry-based measurements of standard metabolic rate in buried A. tobianus (a close relative to A. marinus) at temperatures from 5.3 to 18.3°C and validated with two independent long-term overwintering experiments. Maximum attainable energy reserves were estimated from published data on A. marinus in the North Sea. The critical threshold size in terms of length (L th) for A. marinus in the North Sea was estimated to be 9.5 cm. We then investigated two general predictions: (1) Fish smaller than L th display winter feeding activity, and (2) size at maturation of iteroparous species is larger than L th to ensure sufficient energy reserves to accommodate both the metabolic cost of passive overwintering and reproductive investments. Both predictions were found to be consistent with data on size at maturation and total body energy in December and February.

Heterothermy, and the Energetic Consequences of Huddling in Small Migrating Passerine Birds

The success of migration of small passerine birds depends largely on effective refueling at stopover sites. In our previous studies, we found that hypothermia facilitates accumulation of fuel at the beginning of a stopover. Later we found that blackcaps, Sylvia atricapilla, might further reduce their energy expenditure by huddling while at rest. Here, we report experimental results supporting our hypothesis that huddling is beneficial to small migrating passerines both from energetic and thermoregulatory points of view. To test this hypothesis we measured metabolic rates and body temperatures of seven blackcaps placed in respirometry chambers overnight, either solitarily or in groups of three or four at ambient temperatures of 5, 10, and 15°C. Concurring with our predictions, huddling blackcaps maintained higher body temperatures than did solitary birds, but had mass-specific metabolic rates lower by ∼30% than those of solitary individuals. Based on our previous studies, we estimated energy savings through huddling to be comparable to energy savings through hypothermia in solitary blackcaps and suggest that huddling may be an important way of saving energy for small passerine birds resting at migratory stopovers. At the same time it might offer the additional benefit of lower risk of predation. In this light, we predict that huddling occurs frequently in nature, leading to significant savings of energy, faster accumulation of fuel, presumably lower risk of becoming a prey, more successful migration, and eventually increased fitness.

Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology ofSapajus libidinosusandSapajus nigritus

Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in São Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi-arid habitat in Piauí state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low-quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus.

High predation is of key importance for dominance of small-bodied zooplankton in warm shallow lakes: evidence from lakes, fish exclosures and surface sediments

The mean body size of limnetic cladocerans decreases from cold temperate to tropical regions, in both the northern and the southern hemisphere. This size shift has been attributed to both direct (e.g. physiological) or indirect (especially increased predation) impacts. To provide further information on the role of predation, we compiled results from several studies of subtropical Uruguayan lakes using three different approaches: (i) field observations from two lakes with contrasting fish abundance, Lakes Rivera and Rodo, (ii) fish exclusion experiments conducted in in-lake mesocosms in three lakes, and (iii) analyses of the Daphnia egg bank in the surface sediment of eighteen lakes. When fish predation pressure was low due to fish kills in Lake Rivera, large-bodied Daphnia appeared. In contrast, small-sized cladocerans were abundant in Lake Rodo, which exhibited a typical high abundance of fish. Likewise, relatively large cladocerans (e.g. Daphnia and Simocephalus) appeared in fishless mesocosms after only 2 weeks, most likely hatched from resting egg banks stored in the surface sediment, but their abundance declined again after fish stocking. Moreover, field studies showed that 9 out of 18 Uruguayan shallow lakes had resting eggs of Daphnia in their surface sediment despite that this genus was only recorded in three of the lakes in summer water samples, indicating that Daphnia might be able to build up populations at low risk of predation. Our results show that medium and large-sized zooplankton can occur in subtropical lakes when fish predation is removed. The evidence provided here collectively confirms the hypothesis that predation, rather than high-temperature induced physiological constraints, is the key factor determining the dominance of small-sized zooplankton in warm lakes.

Can a scavenging gastropod with a mussel conspecific diet induce anti-predator defence in the mussel Perna viridis?

This study investigated whether a mussel predator (the swimming crab Thalamita danae) and a scavenger (the gastropod Babylonia lutosa) could induce anti-predator response in the green-lipped mussel Perna viridis by chemical means. The crabs and gastropods had been either starved or recently fed with the mussels. We examined the number, diameter, length and volume of byssus threads produced by the mussels in order to compare the intensity of anti-predator responses when they were exposed to different stimuli. Our results showed that the mussels produced a significantly larger volume of byssus threads when they were exposed to a crab that had recently consumed conspecifics than the mussels in the control group. The starved crab had a weak effect on increasing the number, length, diameter and volume of byssus threads. Furthermore, the scavenging gastropods failed to increase byssus thread production in the mussels, no matter they had been starved or consumed conspecifics. Indeed, byssus thread production is energetically costly. It would be maladaptive for the mussels to increase byssus thread production in response to a low predation risk presented by a scavenger.

BadgerMeles melesSpatial Structure and Diet in an Area of Low Earthworm Biomass and High Predation Risk

Investigating the endangered badger Meles meles population in Belarus we aimed to find out in accordance with which model, i.e. bottom-up or top-down, it is structured and functions. Two important factors (low earthworm biomass and high predation risk) were considered with a view to explaining the specificity in badger spatial structure and diet. The study was conducted in a semi-natural terrain in north-eastern Belarus. We analysed 1188 scats, radiotracked seven badgers and assessed variations in earthworm biomass. In the conditions of low biomass and uneven distribution of earthworms badgers were found to act as generalist predators tending to specialize on the more readily available foods during short seasonal periods. The earthworm portion in the species diet was relatively low and correlated with earthworm biomass and we did not find any evidence of badger feeding selectivity. Data on badger distribution and activity suggest that avoidance of high predation risk forces badgers towards the security of...

Pulsed-Resource Dynamics Constrain the Evolution of Predator-Prey Interactions

Although temporal variability in the physical environment plays a major role in population fluctuations, little is known about how it drives the ecological and evolutionary dynamics of species interactions. We studied experimentally how extrinsic resource pulses affect evolutionary and ecological dynamics between the prey bacterium Serratia marcescens and the predatory protozoan Tetrahymena thermophila. Predation increased the frequency of defensive, nonpigmented prey types, which bore competitive costs in terms of reduced maximum growth rate, most in a constant-resource environment. Furthermore, the predator densities of the pulsed-resource environment regularly fluctuated above and below the mean predator densities of the constant environment. These results suggest that selection favored fast-growing competitor prey types over defensive but slower-growing prey types more often in the pulsed-resource environment (abundance of resources and low predation risk). As a result, the selection for prey defense fluctuated more in the pulsed-resource environment, leading to a weaker mean response in prey defense. At the ecological level, the evolution of prey defense weakened the relative strength of top-down regulation on prey community. This was more evident in the constant-resource environment, whereas the slow emergence of defensive prey types gradually decreased the amplitude of predator peaks in the pulsed-resource environment. Our study suggests that rapid evolution plays a smaller role in the ecological dynamics of communities dominated by resource pulses.

Hormonal response of nestlings to predator calls

Chicks of altricial birds may perceive predation risk by acoustic cues produced by predators. This capacity involves changes to a less conspicuous behavior to avoid being detected and predated. However, little is known about the physiological mechanisms underlying this capacity. Potential mechanisms may involve corticosterone and testosterone, two hormones related to begging, an acoustic signal, which could be used by predators to locate and predate the nest. However, given the species-specificity of this relationship, it is difficult to make particular predictions. We manipulated perceived risk of nest predation in the common blackbird ( Turdus merula) and analyzed nestlings’ plasma levels of these hormones to look for nest predation risk effects. Our experimental manipulation showed hormonal changes in response to nest predation risk. Chicks under a high risk of nest predation reduced their corticosterone plasma levels but increased their testosterone levels in comparison with nestlings exposed to a low nest predation risk. We explain our results as mechanisms to reduce begging activity and discuss them within the framework of hormonal modifications in developing animals. These findings highlight the importance of studying nest predation from the unusually considered chick perspective and underlined the benefits from including physiological variables in the study of predator–prey interactions.

Resources driving landscape-scale distribution patterns of grazers in an African savanna

In order to effectively manage and conserve indigenous herbivores, a good understanding is needed of how resources drive their distribution patterns. This study employed a unique dataset to test a range of ecological theories and hypotheses on free-ranging grazers. Using aerial census data collected over 14 yr across the 2 million ha Kruger National Park (South Africa), this study employs spatial autologistic regression models to explore the spatial relationships that exist between the distribution of eight indigenous grazer species and a set of resource variables. It was found that ecological theories relating to feeding guild, water-dependence, allometric scaling, gut-morphology and vulnerability to predation could explain most of the grazer distribution patterns observed in relation to surface-water, forage quality, forage quantity and habitat openness. All the grazers studied were water-dependent and occurred close to a permanent source of water in the dry season. This was ascribed to the lack of moisture in the diet of grazers during the dry season. Most ruminants' distribution patterns were significantly associated with areas of high forage quality whereas hind-gut fermentors were neutral towards forage quality. Average forage quantity was not a significant predictor of long-term, landscape-scale distribution patterns for any of the grazer species studied. Most small- and medium-bodied grazers preferred open habitats above closed habitats, probably due to higher visibility and a lower predation risk. Large-bodied grazers did not bias their distribution patterns towards open habitats. The way in which grazers distribute themselves with respect to different resources can potentially inform management actions on appropriate scales.

Mate-feeding has evolved as a compensatory energetic strategy that affects breeding success in birds

In many animals, females are fed by males during courtship or incubation (mate-feeding). According to the mate appraisal hypothesis, females may evaluate the parental capacity of males, whereas the pair bond hypothesis suggests that feeding may strengthen the pair bonds with them. Following the nutrition hypothesis, by contrast, females obtain direct nutritional benefits from being fed by males during periods of high-energy expenditure, such as egg formation and incubation. However, there is little support for these hypotheses at an interspecific level. We tested predictions from these hypotheses in a dataset of 170 species of passerine birds. As predicted by the nutrition hypothesis, we found that mate-feeding has evolved more often in species in which the female incubates and builds the nest alone and have noncarnivorous diets. This suggests that mate-feeding is a behavioral strategy that compensates for nutritional limitations of females during breeding, as both incubation and nest building are energetically costly processes, and noncarnivorous diets are deficient in proteins. We also found that incubation feeding has evolved more often in species that place nests at elevated sites, suggesting that these species face low predation risk that allows males to feed females. In the particular case of incubation feeding, we found that species that have evolved this behavior produce larger clutch size and have higher hatching success. Our results support the nutrition hypothesis from an interspecific perspective, suggesting that matefeeding is a strategy to compensate for nutritional limitations of females during reproduction and that it has fitness consequences.

Intra-host competition between co-infecting digeneans within a bivalve second intermediate host: Dominance by priority-effect or taking advantage of others?

We experimentally investigated the interactions between two parasites known to manipulate their host’s phenotype, the trematodes Acanthoparyphium sp. and Curtuteria australis, which infect the cockle Austrovenus stutchburyi. The larval stages of both species encyst within the tissue of the bivalve’s muscular foot, with a preference for the tip of the foot. As more individuals accumulate at that site, they impair the burrowing behaviour of cockles and increase the probability of the parasites’ transmission to a bird definitive host. However, individuals at the foot tip are also vulnerable to non-host predators in the form of foot-cropping fish which selectively bite off the foot tip of exposed cockles. Parasites encysted at the foot base are safe from such predators although they do not contribute to altering host behaviour, but nevertheless benefit from host manipulation as all parasites within the cockle are transmitted if it is ingested by a bird. Experimental infection revealed that Acanthoparyphium sp. and C. australis have different encystment patterns within the host, with proportionally fewer Acanthoparyphium metacercariae encysting at the foot tip than C. australis. This indicates that Acanthoparyphium may benefit indirectly from C. australis and incur a lower risk of non-host predation. However, in co-infections, not only did C. australis have higher infectivity than Acanthoparyphium, it also severely affected the latter’s infection success. The asymmetrical strategies and interactions between the two species suggest that the advantages obtained from exploiting the host manipulation efforts of another parasite might be offset by traits such as reduced competitiveness in co-infections.

Out of the dark: Diurnal activity in the bat Hipposideros ruber on São Tomé island (West Africa)

Geographical areas historically characterized by a lower risk of diurnal avian predation should in theory allow bats to be active in daytime too, especially to forage. Oceanic islands are ideal for studying temporal niche shifts in bats since they often feature depauperate avian assemblages with fewer birds of prey. We report on the second case of diurnal activity known for an insular insectivorous bat, Hipposideros ruber on the island of São Tomé (Gulf of Guinea). We present observations of daylight flights made at several sites on the island in six months (from July to November and in January). We also carried out daytime (09h00–16h00) emergence counts at three roosts. In this time interval, bats were continuously active, although activity rates changed: bats tended to return to roosts in early afternoon and, at two sites, to decrease emergence rate under intense light probably to reduce the risk of hyperthermia. At one roost, we observed that heavy rain caused abrupt daytime returns of large numbers of bats. In daytime bats did forage and kept echolocating. Social interactions (chases) were also frequently observed. In daytime adult males were significantly more frequent than females, while the opposite was noticed at night, an intersexual segregation possibly leading to temporal niche partitioning.

Costly plastic morphological responses to predator specific odour cues in three-spined sticklebacks (Gasterosteus aculeatus)

Predation risk is one of the major forces affecting phenotypic variation among and within animal populations. While fixed anti-predator morphologies are favoured when predation level is consistently high, plastic morphological responses are advantageous when predation risk is changing temporarily, spatially, or qualitatively. Three-spined sticklebacks (Gasterosteus aculeatus) are well known for their substantial variability in morphology, including defensive traits. Part of this variation might be due to phenotypic plasticity. However, little is known about sticklebacks’ plastic ability to react morphologically to changing risks of predation and about the proximate cues involved. Using a split-clutch design we show that odour of a predatory fish induces morphological changes in sticklebacks. Under predation risk, i.e., when exposed to odour of a predator, fish grew faster and developed a different morphology, compared to fish reared under low predation risk, i.e., exposed to odour of a non-predatory fish, or in a fish-free environment. However, fast growing comes at cost of increased body asymmetries suggesting developmental constraints. The results indicate that sticklebacks are able to distinguish between predatory and non-predatory fishes by olfactory cues alone. As fishes were fed on invertebrates, this reaction was not induced by chemical cues of digested conspecifics, but rather by predator cues themselves. Further, the results show that variation in body morphology in sticklebacks has not only a strong genetical component, but is also based on plastic responses to different environments, in our case different predation pressures, thus opening new questions for this model species in ecology and evolution.

The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles

Deterministic filters such as competition and prey defences should have a strong influence on the community structure of animals like animalivorous bats which have life histories characterized by low fecundity, low predation risk, long life expectancy and stable populations. We investigated the relative influence of these two deterministic filters on the trophic structure of animalivorous bat assemblages in South Africa. We used null models to test if patterns of dietary overlap were significantly different from patterns expected by chance and multivariate analyses to test the correlations between diet and phenotype (body size, wing morphology and echolocation). We found little evidence that competition structured the trophic niche of coexisting bats. Contrary to predictions from competition, dietary overlap between bats of ensembles and functional groups (open-air, clutter-edge, and clutter foragers) were significantly higher than expected by chance. Instead, we found support for the predictions of the allotonic frequency hypothesis: there were significant relationships between peak echolocation frequency and the proportion of moths in the diets of bats at local and regional scales, and peak echolocation frequency was the best predictor of diet even after we controlled for the influence of body size and phylogeny. These results suggest that echolocation frequency and prey hearing exert more influence on the trophic structure of sympatric animalivorous bats than competition. Nonetheless, differential habitat use and sensory bias may also be major determinants of trophic structure because these are also correlated with frequencies of bat calls.

Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish

Ecosystems are intricately linked by the flow of organisms across their boundaries, and such connectivity can be essential to the structure and function of the linked ecosystems. For example, many coral reef fish populations are maintained by the movement of individuals from spatially segregated juvenile habitats (i.e., nurseries, such as mangroves and seagrass beds) to areas preferred by adults. It is presumed that nursery habitats provide for faster growth (higher food availability) and/or low predation risk for juveniles, but empirical data supporting this hypothesis is surprisingly lacking for coral reef fishes. Here, we investigate potential mechanisms (growth, predation risk, and reproductive investment) that give rise to the distribution patterns of a common Caribbean reef fish species, Haemulon flavolineatum (French grunt). Adults were primarily found on coral reefs, whereas juvenile fish only occurred in non-reef habitats. Contrary to our initial expectations, analysis of length-at-age revealed that growth rates were highest on coral reefs and not within nursery habitats. Survival rates in tethering trials were 0% for small juvenile fish transplanted to coral reefs and 24–47% in the nurseries. As fish grew, survival rates on coral reefs approached those in non-reef habitats (56 vs. 77–100%, respectively). As such, predation seems to be the primary factor driving across-ecosystem distributions of this fish, and thus the primary reason why mangrove and seagrass habitats function as nursery habitat. Identifying the mechanisms that lead to such distributions is critical to develop appropriate conservation initiatives, identify essential fish habitat, and predict impacts associated with environmental change.

Animal personality

Animal personality