Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation

The predation pressure and food availability to which individuals are exposed during their life histories shape inspection behaviour in animals. In this study, we aimed to test whether such behaviours varied with prior experience (predation, starvation or both treatments) or measurement condition (with or without the presence of a predator; here, the snakehead fish, Channa argus) in the fish species Spinibarbus sinensis, known as qingbo. Unexpectedly, prior predator experience showed no significant effect on inspection behaviour as demonstrated by either the frequency or the duration of each activity outside shelter or on cooperation as demonstrated by the inter-individual distance or synchronization of speed. This may have been due to the different adjustments in behaviour among individuals (more shelter use vs. more inspection), the predator treatment used in the present study (exposure to caged predator rather than direct predation) and/or a species-specific strategy in the qingbo. The starved fish displayed shorter inspection latency, increased inspection behaviour and greater cooperation when measured without the predator; however, when measured in the presence of the predator, the starved fish showed increased inspection frequency but shorter inspection duration, possibly due to the compromise between energy needs and predation risk. Similar to those of the predation group, the fish from the double-treated group showed no difference in inspection behaviour compared to the control group under the predator-absent condition, while the high-frequency, short-duration inspection behaviours remained the same as in the starved group. These findings suggested that the adjustment of inspection behaviour and related cooperation are rather complicated according to either predator experience or food deprivation, partially due to the inter-individual differences in behavioural adjustment and/or different environmental conditions.     

Chemical Predator Inspection in a Characin Fish (Hemigrammus erythrozonus, Characidae, Ostariophysi): The Effects of Mixed Predator Diets

Many prey organisms will approach (inspect) potential predators, primarily to assess local risk of predation. It has been demonstrated that Ostariphysan prey fishes can detect conspecific alarm pheromones in the diet of potential predators and use this chemical information to reduce their risk of predation while still gaining significant benefits associated with predator inspection. We conducted the current study to examine the possible effects of mixed diets on the use of these chemical predator diet cues during inspection visits. Shoals of four glowlight tetras ( Hemigrammus erythrozonus ) were exposed to Jack Dempsey cichlids ( Cichlasoma octofaciatum ) which had been fed diets consisting of: 100% tetras (with alarm pheromone); 75% tetra, 25% swordtail ( Xiphophorus helleri , which lack a recognizable alarm pheromone); 25% tetra, 75% swordtail; or 100% swordtails. Tetras significantly increased their anti-predator behaviour in response to predators fed 100% tetra or the two mixed predator diets, but not when exposed to predators fed a 100% swordtail diet. Likewise, we observed significant differences in inspection behaviour. Tetras took longer to initiate an inspection, inspected in smaller groups and directed a greater proportion of inspection visits towards the tail region of the predator when it had been fed 100% tetra or either of the two mixed prey diets. We found no significant differences in either anti-predator or inspection behaviour among the three diet treatments containing tetras. These data strongly suggest that glowlight tetras are capable of detecting relatively small amounts of conspecific alarm pheromone in the diet of potential predators and that they modify their behaviour based on the presence or absence of these cues.     

Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish

Individuals that dare approach predators (predator inspection behaviour) may benefit by acquiring information regarding the potential threat of predation. Although information acquisition based on visual cues has been demonstrated for fish, it is unknown whether fish will inspect predators on the basis of chemical cues or whether such inspection behaviour results in information acquisition. Here, we first ascertained whether predator inspection behaviour can be mediated by chemical cues from predators by exposing groups of predator-naive glowlight tetras (Hemigrammus erythrozonus) to the chemical cues of a potential fish predator (convict cichlid Cichlasoma nigrofasciatum) that had been fed either tetras (which possess an alarm pheromone) or swordtails (Xiphophorus helleri, which lack Ostariophysan alarm pheromones). Tetras showed a significant increase in antipredator behaviour when exposed to the tetra-diet cue, but not when exposed to the swordtail-diet cue. Chemically mediated predator inspection behaviour was also affected. Both the latency to inspect and the minimum approach distance to the predator significantly increased, and the mean number of inspectors per predator inspection visit significantly decreased when tetras were exposed to the tetra-diet versus the swordtail-diet chemical cues. We then examined a potential benefit associated with chemically mediated predator inspection behaviour. Only tetras that were initially exposed to the tetra-diet cue and that had inspected the predator acquired the visual recognition of a convict cichlid as a predation threat. Our results thus demonstrate that (1) predator inspection behaviour in the glowlight tetra can be initiated by chemical cues, (2) chemically mediated inspection behaviour is affected by the presence of alarm pheromone, and (3) inspectors benefit by acquiring the recognition of novel predators. Copyright 1999 The Association for the Study of Animal Behaviour.     

Predator Inspection Behaviour in a Characin Fish: an Interaction between Chemical and Visual Information?

Recent evidence suggests that predator inspection behaviour by Ostariophysan prey fishes is regulated by both the chemical and visual cues of potential predators. In laboratory trials, we assessed the relative importance of chemical and visual information during inspection visits by varying both ambient light (visual cues) and predator odour (chemical cues) in a 2 × 2 experimental design. Shoals of glowlight tetras (Hemigrammus erythrozonus) were exposed to a live convict cichlid (Archocentrus nigrofasciatus) predator under low (3 lux) or high (50 lux) light levels and in the presence of the odour of a cichild fed tetras (with an alarm cue) or swordtails (Xiphophorus helleri, with an alarm cue not recognized by tetras). Tetras exhibited threat‐sensitive inspection behaviour (increased latency to inspect, reduced frequency of inspection, smaller inspecting group sizes and increased minimum approach distance) towards a predator paired with a tetra‐fed diet cue, regardless of light levels. Similar threat‐sensitive inspection patterns were observed towards cichlids paired with a swordtail‐fed diet cue only under high light conditions. Our data suggest that chemical cues in the form of prey alarm cues in the diet of the predator, are the primary source of information regarding local predation risk during inspection behaviour, and that visual cues are used when chemical information is unavailable or ambiguous.     

Influence of Inter-Lake Variation in Natural Nest Predation Pressure on the Parental Care Behaviour of Smallmouth Bass (Micropterus dolomieu)

Predation risk has the ability to greatly influence the behaviour of reproducing individuals. In large long-lived species with low risk of predation for parents, reproductive behaviours often involve caring for offspring (i.e. defending broods from predators) and these behaviours are essential for offspring survival. Our objectives were to test for the presence of natural variation in nest predation pressure in an aquatic environment for a species that provides sole-paternal care, smallmouth bass ( Micropterus dolomieu ), and to determine if natural variation in predation pressure influences parental care behaviour. We used snorkeler observations and a series of metrics to assess predation pressure and parental care behaviour in six lakes within a narrow geographical range. Lakes differed in all predation pressure metrics: number of predators in proximity to nest when males were present, time to predator arrival and number of predators that consumed eggs when males were absent and total number of nests that was preyed upon. Similarly, parental behaviour varied between lakes. Parental smallmouth bass spent more time engaged in anti-predator defences in lakes with high predation pressure, while males from low predator pressure lakes remained close to their nest. Conversely, males from lakes with low and high predation pressure showed a similar willingness to defend their nests during simulated nest predation events. Our results show that natural variation in aquatic nest predation pressure across multiple lakes can be significant and has the ability to influence baseline parental care behaviour. Such variation provides opportunities to study the costs and consequences of parental care and to evaluate how this could influence demography and community interactions in aquatic systems.     

Predator‐inspection behaviour in female three‐spined sticklebacks Gasterosteus aculeatus is associated with status of gravidity

Differences in predator‐inspection behaviour between gravid and non‐gravid female as well as between male and female three‐spined sticklebacks Gasterosteus aculeatus were investigated. Gravid females confronted with a live rainbow trout Oncorhynchus mykiss showed bolder inspection behaviour than non‐gravid ones. The behaviour of gravid females was comparable with that of males, maybe because both face a high risk of predation. The results indicate that antipredator behaviour in female G. aculeatus is not fixed but adjusted to their reproductive state.     

Kinship reinforces cooperative predator inspection in a cichlid fish

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.     

Individual Behavioural Strategies Associated with Predator Inspection in Minnow Shoals

When confronted with a live pike, Esox lucius, European minnows, Phoxinus phoxinus, showed individual differences in rate of predator inspection. Predator inspection behaviour, in which single individuals or small groups approached the predator, was ordinated with several other behavioural parameters using principal components analysis. Individual minnows showed one of two strategies. Fish with high inspection rates were bolder, skittered more frequently and fed more persistently than fish with low inspection rates. Fish with low inspection rates showed the opposite strategy. Individuals did not show habituation of predator inspection during trials or over the experimental period.     

A model for the evolution of crèching behaviour in gulls

A crèche is an aggregation of chicks outside nesting territories, within chicks continue to be fed only by their own parents. Several adaptive functions of crèching have been proposed, the most frequent being a reduction in predator pressure. Using an evolutionary stable strategy approach based on the computation of individuals' fecundity, we examined which regime of aerial and terrestrial predation is likely to favour the evolution and stability of the crèching strategy (CS) in gulls. Our results confirm the hypothesis that habitat instability associated with high levels of terrestrial predation favours the evolution and maintenance of crèching behaviour. Moreover, our results suggest that a low aggressiveness against predators may be a pre-adaptation to a CS. In contrast, the high synchronisation often observed in crèching species does not favour the evolution of a crèching behaviour and is thus probably under selection pressures different from those modelled here.     

Tendency to inspect predators predicts mortality risk in the guppy (Poecilia reticulata)

Although predator inspection behavior in fishes has become amodel system for examining game theoretical strategies suchas Tit for Tat, the direct costs of inspection behavior havenot been quantified. To begin quantifying such costs, I conductedan experiment that examined mortality due to predation as afunction of predator inspection in the guppy (Poecilia reticulata).Before being subjected to a "survivorship" experiment, guppieswere assayed for their tendency to inspect a predator. Groupswere then composed of six guppies that differed in their tendencyto inspect. These groups were placed into a pool containinga predator, and survivorship of guppies with different inspectiontendencies was noted 36 and 60 h later. Results indicate thatindividuals that display high degrees of inspection behaviorsuffer greater mortality than their noninspecting shoalmates.     

Predation in a temporary pond with special attention to the trophic role of Triops cancriformis (Crustacea: Branchiopoda: Notostraca)

Temporary ponds are described as environments with a low predation pressure. Notostracans inhabit these types of ponds, and some populations acquire a high proportion of larger individuals, whose feeding behaviour is mainly predatory. The predation nature of Triops cancriformis is not widely accepted, because its diet is still partly controversial. We analysed the diet of one population of T. cancriformis in a Mediterranean temporary pond (Espolla pond, NE Iberian peninsula) to evaluate its predation behaviour. The gut content of the individuals bigger than 10 mm is mainly composed of detritus, plant fibres and microcrustaceans (cladocerans, ostracods and copepods). The prey number increases with the body size of individual T. cancriformis as previously described. Sex-biased predation was observed for one copepod prey, but not for the other. Predation pressure in that community was monitored along six hydroperiods as the percentage of predator biomass (not only T. cancriformis) in relation to the non-predator biomass. The proportion of predator biomass is high, and this contrasts with the low predation pressure expected for a temporary system with short hydroperiods.     

Behavioural Responses of European Roe Deer to Temporal Variation in Predation Risk

In natural environments, predation risk varies over time. The risk allocation hypothesis predicts that prey is expected to adjust key anti‐predator behaviours such as vigilance to temporal variation in risk. We tested the predictions of the risk allocation hypothesis in a natural environment where both a species‐rich natural predator community and human hunters are abundant and where the differences in seasonal and circadian activity between natural and anthropogenic predators provided a unique opportunity to quantify the contributions of different predator classes to anti‐predator behaviour. Whereas natural predators were expected to show similar levels of activity throughout the seasons, hunter activity was high during the daytime during a clearly defined hunting season. According to the risk allocation hypothesis, vigilance should then be higher during the hunting season and during daytime hours than during the non‐hunting season and night‐time hours. Roe deer (Capreolus capreolus) on the edge of Bia?owie?a Primeval Forest in Eastern Poland displayed vigilance behaviour consistent with these predictions. The behavioural response of roe deer to temporarily varying predation risks emphasises the behavioural plasticity of this species and suggests that future studies of anti‐predator behaviour need to incorporate circadian variation in predation pressure as well as risk gradients of both natural and anthropogenic predators.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Population Differences in the Schooling Behaviour of Newborn Guppies,Poecilia reticulata

Population differences in the schooling behaviour of adult guppies (Poecilia reticulata) from Trinidad have previously been well documented. This paper demonstrates that variation in schooling behaviour is also present in newborn fish. Guppies from the Aripo River of Trinidad display well-developed schooling behaviour from birth. In addition to forming cohesive and polarized groups, these newborn fish also exhibit predator inspection behaviour. Newborn guppies from the Paria River perform inspections but, unlike the Aripo fish, are poor schoolers. Population variation in behaviour at birth does not necessarily reflect the pattern observed in the adult fish. As adults, guppies from the Upper section of the Aripo River have a much lower schooling tendency and are less wary during inspection than the downstream Lower Aripo guppies. At birth, however, the schooling behaviour and inspection behaviour in the two populations is identical. These results suggest that different selective pressures operate on adult and newborn guppies in Trinidad.     

Heterogeneous landscapes and the role of refuge on the population dynamics of a specialist predator and its prey

How, and where, a prey species survives predation by a specialist predator during low phases of population fluctuations or a cycle, and how the increase phase of prey population is initiated, are much-debated questions in population and theoretical ecology. The persistence of the prey species could be due mainly to habitats that act as refuges from predation and/or due to anti-predatory behaviour of individuals. We present models for the former conjecture in two (and three) habitat systems with a specialist predator and its favoured prey. The model is based on dispersal of prey between habitats with high reproductive output but high risk of predation, and less productive habitats with relatively low risk of predation. We illustrate the predictions of our model using parameters from one of the most intriguing vertebrate predator–prey systems, the multi-annual population cycles of boreal voles and their predators. We suggest that cyclic population dynamics could result from a sequence of extinction and re–colonization events. Field voles (Microtus agrestis), a key vole species in the system, can be hunted to extinction in their preferred meadow habitat, but persist in sub-optimal wet habitats where their main predator, the least weasel (Mustela nivalis nivalis) has a low hunting efficiency. Re–colonization of favourable habitats would occur after the predator population crashes. At the local scale, the model suggests that the periodicity and amplitude of population cycles can be strongly influenced by the relative availability of risky and safe habitats for the prey. Furthermore, factors like intra-guild predation may lead to reduced predation pressure on field voles in sub-optimal habitats, which would act as a refuge for voles during the low phase of their population cycles. Elasticity analysis suggested that our model is quite robust to changes in most parameters but sensitive to changes in the population dynamics of field voles in the optimal grassland habitat, and to the maximum predation rate of weasels.     

Predator attack motivation influences the inspection behaviour of European minnows

Predator inspection behaviour at different levels of attack motivation (attack status of the predator) was investigated in European minnows Phoxinus phoxinus from a population sympatric with pike Esox lucius , during controlled laboratory experiments. Shoals of minnows performed more predator inspections and formed larger inspection group sizes shortly after an attack by a pike. After inspection, minnows returned to the safety of the main shoal, regardless of predator motivation. Minnows which inspected last-before and first-after a strike by a pike modified their behaviour after inspection; they reduced feeding, increased shoaling, flicked their dorsal and pectoral fins and skittered. This behaviour signified alarm and appeared to reflect the severity of the threat posed by the predator at the time of inspection. Fish that had inspected when the pike displayed low attack motivation did not modify their behaviour after inspection to reflect alarm. Information concerning the attack motivation of the predator is probably transferred passively throughout the shoal by changed inspector behaviour and by inspection rate. These data demonstrate that: (1) minnows modified their behaviour after inspection to reflect a predator's attack motivation; and (2) minnows which inspected immediately before a strike appeared to anticipate the future attack and modified their behaviour accordingly.     

Aerial hunting behaviour and predation success by peregrine falcons Falco peregrinus on starling flocks Sturnus vulgaris

Predators use diverse hunting strategies to maximize hunting success, while preys adopt anti‐predator strategies to maximize escape chances, among which flocking, communal roosting, and the related collective responses are a common pattern in gregarious species. Prey‐predator interactions involving a single predator and flocks, a common situation in birds, have received little attention. We studied predation behaviour and success of peregrine falcons Falco peregrinus on starlings Sturnus vulgaris, a highly gregarious species, in proximity of two winter roosts. A total of 328 hunting sequences, with an overall success of 23.1% were recorded. They usually consisted of several attacks, predation success being higher when hunting sequences lasted less than 1.5 min, included less than 3 attacks and no other falcons were hunting simultaneously. Predation success was higher when hunts were directed on singletons than on flocks. However, most hunting sequences were directed towards flocks. Nine hunting strategies on flocks were identified. The most frequent was the ‘surprise attack’, which was also the most successful. We suggest that this strategy minimizes the amount of anti‐predator display elicited by flocks and economizes energy spent in hunting. The constant predation pressure did not seem to affect the use of roosts by starlings, consistent with the ‘dilution’ hypothesis, while falcons captured at least one prey item every evening. Communal roosting may benefit predator and prey, as both sides could have reached a mutual local equilibrium.     

Picking personalities apart: estimating the influence of predation,sex and body size on boldness in the guppy Poecilia reticulata

Predation is a strong selective force in most natural systems, potentially fueling evolutionary changes in prey morphology, life history and behaviour. Recent work has suggested that contrasting predation pressures may lead to population differentiation in personality traits. However, there are indications that these personality traits also differ between sexes and not necessarily in a consistent way between populations. We used an integrative approach to quantify boldness (latency to emerge from a shelter) in wild‐caught guppies in relation to predation pressure, population origin, sex and size. In addition we quantified the repeatability of these personality traits. We show that predation regime had significant effects on emergence time. In general, fish from high predation localities emerged sooner from the shelter compared to those from low predation localities. We found strong sex differences; males were significantly bolder than females. The relationship between emergence time and body size was non‐significant in all populations. We discuss what responses to expect from predator‐naïve versus predator‐experienced individuals and how this can be linked to the shyness–boldness continuum.     

Functional Responses of Retaliatory Killing versus Recreational Sport Hunting of Leopards in South Africa

Predation strategies in response to altering prey abundances can dramatically influence the demographic effects of predation. Despite this, predation strategies of humans are rarely incorporated into quantitative assessments of the demographic impacts of humans killing carnivores. This scarcity largely seems to be caused by a lack of data. In this study, we contrasted predation strategies exhibited by people involved in retaliatory killing and recreational sport hunting of leopards (Panthera pardus) in the Waterberg District Municipality, South Africa. We predicted a specialist predation strategy exemplified by a type II functional response for retaliatory killing, and a generalist strategy exemplified by a type III functional response for recreational sport hunting. We could not distinguish between a type I, a type II, or a type III functional response for retaliatory killing, but the most parsimonious model for recreational sport hunting corresponded to a type I functional response. Kill rates were consistently higher for retaliatory killing than for recreational sport hunting. Our results indicate that retaliatory killing of leopards may have severe demographic consequences for leopard populations, whereas the demographic consequences of recreational sport hunting likely are less dramatic.     

Predation by Kelp Gulls Larus dominicanus at a mixed-species colony of Royal Terns Sterna maxima and Cayenne Terns Sterna eurygnatha in Patagonia

We studied the predator-prey interaction between Kelp Gulls Larus dominicanus and Royal Terns Sterna maxima and Cayenne Terns Sterna eurygnatha at Punta León, Argentina, from 1990 to 1992. Kelp Gulls were the main predator of tern eggs in all 3 years, accounting for 99% of observed predations (n = 454). A total of 99% of predations occurred on peripheral tern nests. Total predation rate on both tern species was highest in 1990 and varied significantly between years, with between 0.01 and 0.03 cases of predation per hour. Predation rates in all years were significantly higher on Cayenne than on Royal Terns probably because the latter were significantly more aggressive towards gulls than were Cayenne Terns. Royal and Cayenne Terns displayed aggressively towards gulls at least once in 64% and 10% of the observation periods, respectively. Defence behaviour, such as attacking and chasing the predator, was used more frequently by Royal than Cayenne Terns (13.2% v 3.6%). Predation on tern eggs was restricted to only a few Kelp Gulls which nested close to the tern colony periphery, and 50% of the eggs that were stolen were taken by only two pairs during 1991 and 47% by three pairs in 1992. This suggests that the current expansion of the Kelp Gull numbers at Punta León might not necessarily result in a proportional increase in predation rate on both tern species. Stealing eggs from the ground was more successful than from the air (77% v 17%). The nesting strategy shown by Royal and Cayenne Terns at Punta León appears to be an important factor which reduced the impact on their breeding success of high potential predation pressure by gulls.