High-predation Localities Research Articles

Shoaling in the Trinidadian guppy: costs, benefits, and plasticity in response to an ambush predator

AbstractShoaling, the formation of social groupings in fish, can provide benefits including reduced predation risk. However, it can also inflict costs including increased competition for resources, transmission of parasites, and salience to predators. Trinidadian guppies exhibit inter-population variation in shoaling behavior where individuals coexisting with large piscivorous predators (high predation localities) spend most of their time in shoals and those coexisting with an ambush predator, Rivulus hartii (recently, Anablepsoides hartii), that preys primarily on smaller guppies (low predation localities) do not. It has been suggested that this predator selects for reduced shoaling because doing so reduces salience to the predator. Here, as far as we know, we perform the first test of this idea. First, we investigated the effectiveness of shoaling in encounters with this predator. In survival trials, where one rivulus interacted with a group of guppies, we found that the predator was more likely to attack individuals in shoals than singletons. However, we also found that attacks directed at shoals were less likely to succeed. This suggests that the optimal strategy for guppies co-existing with this predator is to reduce shoaling to reduce the probability of being attacked, and to form shoals when an attack is initiated. We then asked if guppies modified their shoaling behavior in response to visual and olfactory cues from this predator during development. We found changes in guppy behavior in response to the treatment: guppies increased shoaling behavior when there was heightened risk of predation.

Environmental and genetic effects on exploratory behavior of high- and low-predation guppies (Poecilia reticulata)

Exploratory behavior—an individual’s response to novel environments, resources, or objects—should vary with the associated benefits, including new sources of food and reduced levels of competition, and the costs, such as predation pressure. Using guppies from multiple streams and rivers in Trinidad, we compared guppies from high- and low-predation populations. We found that wild-caught male and female guppies from low-predation populations were more exploratory than high-predation fish when tested in the field and in controlled laboratory conditions. We did not detect significant evidence for a genetic basis for differences in the behavior of high- and low-predation fish using a common-garden approach, but further study is required before conclusions can be made about the relative contribution of genes to population differences in exploratory behavior of guppies. Theory has assumed that predation risk is a cost that will select against high levels of exploratory behavior; this study is one of the few that has tested this assumption, and we show that exploratory behavior is indeed suppressed in guppies from high-predation localities. Exploratory behavior is a component of an individual’s responses to novel environments, resources, and objects (including potential predators) and thus can affect important decisions of animals in the wild (e.g., whether to sample new, potential sources of food, whether to disperse). We compared exploratory behavior of wild-caught guppies from sites with large, dangerous predators with those from sites with small predators that are only a threat to small individuals. Guppies co-occurring with large predators were less exploratory than those from sites with small predators. Factors contributing to this difference could include exposure to predators directly and to conspecifics’ responses to predators. Studies on general behavioral traits (e.g., temperament) combined with knowledge of animals’ environment and evolution are expanding our ability to test ideas about the origin and maintenance of intra-specific variation in fascinating and complex traits.

Categorization of shell fragments provides a proxy for environmental energy and predation intensity

Shell fragments are extremely abundant in many marine environments; the origins of these fragments can largely be attributed to either crushing by predators or post-mortem processes such as transport. We present and test a new approach to identifying the origin of shell fragments in marine environments by examining modern mollusc assemblages from three wave-exposed, low-predation and three wave-sheltered, high-predation intertidal localities in Bamfield, British Columbia. We hypothesized that fragments with all-rounded edges (AR) or a combination of rounded and sharp edges (R&S) are indicative of taphonomic processes such as transport and so should occur more often in wave-exposed, low-predation localities whereas fragments with all sharp edges (AS) or a combination of intact and sharp edges (I&S), indicative of predation, should be more common in wave-sheltered, high-predation settings. In keeping with the prediction, All-Rounded (AR) and Rounded and Sharp (R&S) fragments are more abundant at the wave-exposed localities than at wave-sheltered localities whereas Intact and Sharp (I&S) and All-Sharp (AS) fragments are more abundant at high-predation localities than at low-predation localities. The two types of localities were statistically distinguishable for either gastropod or bivalve fragments. This supports the hypothesis that I&S and AS result from predation, whereas AR and R&S have a taphonomic genesis.

Linking reproduction, locomotion, and habitat use in the Trinidadian guppy (Poecilia reticulata).

Pregnancy inhibits locomotion, increases predation risk and may translate into reduced survival. The extent to which animals modify behavior in the wild to compensate for the locomotor costs of pregnancy remains poorly understood. We have investigated how reproductive allocation (RA-the proportion of body mass devoted to reproduction) affects locomotor performance and habitat use in Trinidadian guppy (Poecilia reticulata) populations from low- and high-predation regimes. During steady swimming, females with high RA had increased tail beat amplitudes, indicating increased swimming costs. Females with high RA also exhibited slower escape velocities, which may result in an increased risk of predation. In low-predation localities, females with high RA used habitats with a lower water velocity, suggesting that females may be modifying behavior to offset the locomotor costs of pregnancy. Habitat use in high-predation localities was severely restricted to areas without predators, which had a relatively slower water velocity with little or no variation in current. These results provide a link between the performance-related costs of reproduction and behavior in a natural setting and show that animals may compensate for reproductive traits that constrain locomotor performance by modifying habitat use.

Predator exposure alters stress physiology in guppies across timescales

In vertebrates, glucocorticoids mediate a wide-range of responses to stressors. For this reason, they are implicated in adaptation to changes in predation pressure. Trinidadian guppies (Poecilia reticulata) from high-predation environments have repeatedly and independently colonized and adapted to low-predation environments, resulting in parallel changes in life history, morphology, and behavior. We validated methods for non-invasive waterborne hormone sample collection in this species, and used this technique to examine genetic and environmental effects of predation on basal glucocorticoid (cortisol) levels. To examine genetic differences, we compared waterborne cortisol levels in high- and low-predation fish from two distinct population pairs. We found that fish from high-predation localities had lower cortisol levels than their low-predation counterparts. To isolate environmental influences, we compared waterborne cortisol levels in genetically similar fish reared with and without exposure to predator chemical cues. We found that fish reared with predator chemical cues had lower waterborne cortisol levels than those reared without. Comparisons of waterborne and whole-body cortisol levels demonstrated that populations differed in overall cortisol levels in the body, whereas rearing conditions altered the release of cortisol from the body into the water. Thus, evolutionary history with predators and lifetime exposure to predator cues were both associated with lower cortisol release, but depended on distinct physiological mechanisms.

Interpopulation Differences in Shoaling Behaviour in Guppies (Poecilia reticulata): Roles of Social Environment and Population Origin

In Trinidad, guppies (Poecilia reticulata) in high-predation localities show more cohesive shoaling behaviour than those living with less dangerous predators in low-predation sites. We evaluated the relative contributions of population origin (i.e. genetic and/or maternal effects) and social environment on the expression of shoaling by assessing the behaviour of juveniles reared in a range of social conditions. Focal individuals, offspring of guppies from populations from high- or low-predation localities, were reared in a multifactorial experiment; we created four different social conditions by manipulating the source and demography of the conspecific residents with whom focal individuals interacted. We found that high-predation fish displayed a stronger propensity to shoal than low-predation ones. Our results also suggest a role for interactions between the source of the focal individuals, the demography of the group in which they were reared and the origin of the guppies with whom they were reared. Depending on their origin (high- vs. low- predation) and rearing density, our focal fish were more likely to shoal if they were reared with high-predation residents. Learning from high-predation residents, aggressive interactions with low-predation residents and/or phenotype matching could have played a role in driving this effect of social environment. This effect of the phenotype of conspecifics on shoaling development would enhance heritable differences in shoaling propensity such that both could contribute to the well-documented difference in shoaling behaviour of high- and low-predation guppies in natural populations.

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-nave versus predator-experienced individuals and how this can be linked to the shyness-boldness continuum. (Less)

Trade‐off between steady and unsteady swimming underlies predator‐driven divergence inGambusia affinis

Differences in predation intensity experienced by organisms can lead to divergent natural selection, driving evolutionary change. Western mosquitofish (Gambusia affinis) exhibit larger caudal regions and higher burst-swimming capabilities when coexisting with higher densities of predatory fish. It is hypothesized that a trade-off between steady (constant-speed cruising; important for acquiring resources) and unsteady (rapid bursts and turns; important for escaping predators) locomotion, combined with divergent selection on locomotor performance (favouring steady swimming in high-competition scenarios of low-predation environments, but unsteady swimming in high-predation localities) has caused such phenotypic divergence. Here, I found that morphological differences had a strong genetic basis, and low-predation fish required less hydromechanical power during steady swimming, leading to increased endurance. I further found individual-level support for cause-and-effect relationships between morphology, swimming kinematics and endurance. Results indicate that mosquitofish populations inhabiting low-predation environments have evolved increased steady-swimming abilities via stiffer bodies, larger anterior body/head regions, smaller caudal regions and greater three-dimensional streamlining.

Evolution of juvenile growth rates in female guppies ( Poecilia reticulata ): predator regime or resource level?

Recent theoretical and empirical work argues that growth rate can evolve and be optimized, rather than always being maximized. Chronically low resource availability is predicted to favour the evolution of slow growth, whereas attaining a size-refuge from mortality risk is predicted to favour the evolution of rapid growth. Guppies (Poecilia reticulata) evolve differences in behaviour, morphology and life-history traits in response to predation, thus demonstrating that predators are potent agents of selection. Predators in low-predation environments prey preferentially on small guppies, but those in high-predation environments appear to be non-selective. Because guppies can outgrow their main predator in low- but not high-predation localities, we predict that predation will select for higher growth rates in the low-predation environments.However, low-predation localities also tend to have lower productivity than high-predation localities, yield-ing the prediction that guppies from these sites should have slower growth rates. Here we compare the growth rates of the second laboratory-born generation of guppies from paired high- and low-predation localities from four different drainages. In two out of four comparisons, guppies from high-predation sites grew significantly faster than their low-predation counterparts. We also compare laboratory born descendants from a field introduction experiment and show that guppies introduced to a low-predation environment evolved slower growth rates after 13 years, although this was evident only at the high food level. The weight of the evidence suggests that resource availability plays a more important role than predation in shaping the evolution of growth rates.

Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata).

The empirical study of natural selection reveals that adaptations often involve trade-offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life-history evolution on locomotor performance in the live-bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast-start swimming performance to evade predators. Because embryo development increases a female's wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast-start performance. We find evidence for adaptive but constrained evolution of fast-start swimming performance in laboratory trials conducted on second-generation lab-reared fish. Female guppies from high-predation localities attain a faster acceleration and velocity and travel a greater distance during fast-start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high- and low-predation populations. This functional trade-off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole-organism level.

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

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

LIFE-HISTORY EVOLUTION IN GUPPIES (POECILIA RETICULATA) 6. DIFFERENTIAL MORTALITY AS A MECHANISM FOR NATURAL SELECTION.

We have previously reported a correlation between the life-history patterns of guppies and the types of predators with which they coexist. Guppies from localities with an abundance of large predators (high predation localities) mature at an earlier age and devote more resources to reproduction than those found in localities with only a single, small species of predator (low predation localities). We also found that when guppies were introduced from a high to low predation locality, the guppy life history evolved to resemble what was normally found in this low predation locality. The presumed mechanism of natural selection is differences among localities in age/size-specific mortality (the age/size-specific mortality hypothesis); in high predation localities we assumed that guppies experienced high adult mortality rates while in the low predation localities we assumed that guppies experienced high juvenile mortality rates. These assumptions were based on stomach content analyses of wild-caught predators and on laboratory experiments. Here, we evaluate these assumptions by directly estimating the mortality rates of guppies in natural populations. We found that guppies from high predation localities experience significantly higher mortality rates than their counterparts from low predation localities, but that these higher mortality rates are uniformly distributed across all size classes, rather than being concentrated in the larger size classes. This result appears to contradict the predictions of the age/size-specific predation hypothesis. However, we argue, using additional data on growth rates and the probabilities of survival to maturity in each type of locality, that the age-specific mortality hypothesis remains plausible. This is because the probability of survival to first reproduction is very similar in each type of locality, but the guppies from high predation localities have a much lower probability of survival per unit time after maturity. We also argue for the plausibility of two other mechanisms of natural selection. These results thus reveal mortality patterns that provide a potential cause of natural selection, but expand, rather than narrow, the number of possible mechanisms responsible for life-history evolution in guppies.

Life-History Evolution in Guppies (Poecilia reticulata: Poeciliidae). IV. Parallelism in Life-History Phenotypes

In earlier publications, we reported an association between the life-history patterns of guppies and the types of predators with which they co-occur. We contrasted guppies from high-predation sites (Crenicichla localities) with those from low-predation sites (Rivulus localities) found on the south slope of the Northern Range Mountains of Trinidad. Guppies from high-predation localities attain maturity at an earlier age and smaller size, produce more and smaller offspring per litter, and have higher reproductive allotments than their counterparts from low-predation sites. Here we present a parallel series of analyses for guppies from a new series of localities on the north slope of the Northern Range. These fish are also found in what appear to be high- and low-predation communities, but, with one exception, the species of predators are entirely different from those on the south slope. The larger predators are derived from marine families (gobies and mullets) that have invaded freshwater rivers; the south slope fauna is derived from families typical of mainland South America. If predator-induced mortality selects for life-history evolution, then guppies from high- and low-predation sites on the north slope should have life histories similar to their counterparts on the south slope. We compare the life-history phenotypes of guppies from the north slope communities and find that the high- and low-predation contrasts are remarkably similar to those reported earlier for the south slope communities. We reinforce this comparison with multivariate analyses that use discriminant functions derived for the south slope collections to classify north slope samples. Finally, we exploit recent molecular genetic data and the geographical distribution of high- and low-predation communities to argue for the independent origin of these life-history patterns in each drainage.

Life History Evolution in Guppies: a Model System for the Empirical Study of Adaptation

I have used a diversity of observations and experiments to evaluate whether or not guppy life histories represent an adaptation to predator-induced mortality rates. I have primarily worked on natural populations of guppies from Trinidad, but have also considered populations from Tobago and Venezuela. My first step was to compare the life histories of guppies from high and low predation environments. I found that guppies from high predation environments matured more quickly, reproduced more often, and devoted more of their consumed resources to reproduction. They also produced more and smaller offspring in each litter. All of these differences had a genetic basis and many conform to theoretical predictions for how the life history should evolve in response to differences in mortality patterns. I also found that these same patterns were obtained in a new series of localities that had a completely different suite of predators, but had the same contrast between high and low predation communities. I employed mark-recapture techniques to demonstrate that guppies from high predation localities also have significantly higher mortality rates than their counterparts from low predation localities. Such differences in mortality rate provide a potential mechanism for the evolution of these life history patterns. Finally, I have introduced guppies from high predation communities into low predation communities from which they had previously been excluded by waterfalls. These introduced populations evolved in the predicted fashion (delayed maturity, reduced resource allocation to reproduction). Some variables changed significantly in as little as four years, or approximately six generations. While each observation by itself represents an incomplete argument for adaptation, together they make a very strong case for predation and mortality playing a significant role in selecting for interpopulation differences in life histories.