Reduction of predation risk under the cover of darkness: Avoidance responses of mayfly larvae to a benthic fish

Summary Mayfly larvae of Paraleptophlebia heteronea (McDunnough) had two antipredator responses to a nocturnal fish predator (Rhinichthys cataractae (Valenciennes)): flight into the drift and retreat into interstitial crevices. Drift rates of Paraleptophlebia abruptly increased by 30 fold when fish were actively foraging in the laboratory streams but, even before fish were removed, drift began returning to control levels because larvae settled to the substrate and moved to areas of low risk beneath stones. This drifting response was used as an immediate escape behavior which likely decreases risk of capture from predators which forage actively at night. Surprisingly, drift most often occurred before contact between predator and prey, and we suggest that in darkness this mayfly may use hydrodynamic pressure waves for predator detection, rather than chemical cues, since fish forage in an upstream direction. Although drifting may represent a cost to mayfly larvae in terms of relocation to a new foraging area with unknown food resources, the immediate mortality risk probably out-weighs the importance of staying within a profitable food patch because larvae can survive starvation for at least 2 d. In addition to drifting, mayflies retreated from upper, exposed substrate surfaces to concealed interstitial crevices immediately after a predator encounter, or subsequent to resettlement on the substrate after predator-induced drift. A latency period was associated with this response and mayflies remained in these concealed locations for at least 3 h after dace foraging ceased. Because this mayfly feeds at night and food levels are significantly lower in field refugia under stones, relative to exposed stone surfaces, predator avoidance activity may limit foraging time and, ultimately, reduce the food intake of this stream mayfly.     

Changing risk of predation for a filter-feeding insect along a current velocity gradient

Flume experiments were carried out to examine whether larval blackflies (Simulium ornatum complex, Diptera: Simuliidae) use microhabitats with a highvelocity current to reduce the risk of predation by some of their main predators, viz. larvae of the stoneflies Isoperla grammatica and Diura nanseni (Plecoptera: Perlodidae), and the caddis-fly Rhyacophila nubila (Trichoptera: Rhyacophilidae). We exposed blackfly larvae to four different current velocities and measured their feeding rate using dye particles. The maximum feeding rate was recorded at intermediate velocities (18.8 and 36.2 cm/s), whereas at low (7.3 cm/s) and high (53.3 cm/s) velocities, the feeding rate was reduced. In separate experiments, we investigated the behaviour and attack success of the different predator species. The two perlodids showed a similar hunting behaviour, which was significantly less successful at higher velocities. Drift of the perlodids from the experimental arena resulted in reduced encounter and attack rates, especially in I. grammatica, which had completely lost efficiency at 36.2 cm/s. R. nubila had a slower mode of hunting and was unaffected by current speed within the velocity gradient studied. Drift in Rhyacophila was rare. Observations on the behaviour of blackfly larvae were performed in the same experiments. The larvae showed no apparent ability to sense the presence of the predators except when these disrupted the flow pattern or were in physical contact, which often resulted in aggressive defence, though without effect on the predators. Escape of blackfly larvae by drift did occur, but this was no more common than being captured. In a current velocity gradient, blackfly larvae showed a weak preference for increasing velocities. Thus, at velocities between 7 and 54 cm/s, blackfly larvae appear to select microhabitats with high current velocities, despite a reduction in feeding optimality, thereby easing the predation impact from perlodids, though not from Rhyacophila. The study demonstrates the importance of microhabitat selection by blackfly larvae both for efficient feeding and predator avoidance.     

Trade-offs in the response of mayflies to low oxygen and fish predation

Summary We examined how mayfly larvae (Ephemeroptera,Callibaetis montanus) balance the conflicting demands of avoiding both benthic hypoxia and fish predators. Using vertical oxygen and temperature gradients typical of ice-covered lakes, we observed the behavior of mayflies in the presence and absence of fish. In the absence of fish and with adequate oxygen, mayflies spent most of the time on the bottom substrate. As benthic oxygen concentration declined, mayflies increased their activity and moved up in the water column. In the presence of fish and with adequate oxygen, mayflies spent even more time associated with the bottom substrate and reduced their activity levels. As benthic oxygen concentrations declined, mayflies increased their activity and moved up in the water column, but to a lesser extent than when fish were absent. Because of this depression in activity and reluctance to leave the bottom substrate, mayflies endured lower oxygen concentrations in the face of predation threat relative to when fish were absent. Despite this trade-off, benthic hypoxia resulted in increased mortality due to fish predation. Because benthic invertebrates vary in their ability to tolerate hypoxia and in their vulnerability to fish predators, periods of benthic hypoxia could lead to selective predation on some taxa and be an important force structuring benthic invertebrate assemblages.     

Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk

In a series of experiments, we investigated the effects of food availability and risk frequency on the dynamics of predator-induced changes in growth and morphology of prey fish using goldfish (Carassius auratus) as our test species. In experiment 1, we fed goldfish high or low food rations and exposed them to either alarm cues from conspecifics, cues from swordtails or a water control. After 60 days, goldfish in the alarm cue treatment significantly increased their body depth and body weight but had smaller body length than goldfish exposed to swordtails cues or water, likely reducing their vulnerability to gape-limited predators. Importantly, food level had an impact on the amplitude of the morphological changes. In experiment 2, goldfish were exposed to two different frequencies of predation cues or a water control for 50 days. The cues were either continued or discontinued from day 51 to 100, and all cues were resumed from day 101 to 150. We found that goldfish exposed to predation cues increased their depth and weight at a faster rate than did the goldfish exposed to water, and of particular significance was the fact that frequency of risk had an effect on the amplitude of the change. When the cues were interrupted, the increase in growth rate parameters was reduced to the level of the goldfish exposed to water. However, when the cues were resumed, the rate increased to match the growth rate of the goldfish that were continuously exposed to the cues. Finally, we staged encounters between goldfish of differing morphologies and yellow perch (Perca flavescens) and found that deep-bodied goldfish had better survival than the shallow-bodied ones. These experiments illustrate the dynamic nature of inducible morphological defences.     

Life-history strategies of a freshwater snail in response to stream permanence and predation: balancing conflicting demands

Summary Life-history parameters for the freshwater snail Physella virgata virgata were estimated in temporary and permanent streams with and without crayfish (known snail predators). Snails from the permanent stream with crayfish exhibited higher age and size at first reproduction, as well as higher size and age at death, compared to snail populations from both temporary streams and the permanent stream without crayfish. Life-history patterns of snails from the permanent and temporary streams without crayfish were indistinguishable, with small sizes at first reproduction and at death, as well as lower age at first reproduction and at death. The snail population from the temporary stream with crayfish showed an intermediate life-history pattern. The results suggest that snail life-history patterns vary with both predation pressure and habitat stability, exhibiting phenotypically plastic responses to the variables.     

Phenotypically plastic responses of green frog embryos to conflicting predation risk

Predators have been shown to alter the timing of switch points between life history stages, but few studies have addressed switch point plasticity in prey exposed simultaneously to conflicting predation pressure. We tested hatching responses of green frog (Rana clamitans) embryos subject to perceived predation risk from chemical cues released by two stage-specific predators, predicting that these predators would elicit: (1) directional hatching responses when presented independently, and (2) intermediate phenotypic responses when presented simultaneously. R. clamitans embryos in outdoor exclosures were exposed to cues from an egg predator (freshwater leeches; Nephelopsis obscura), a larval predator (dragonfly nymphs, Aeschna canadensis), and both predators in a 2 × 2 factorial experiment, and changes in hatchling size, hatchling developmental stage, and hatching time were compared to those for control embryos. Leeches alone induced embryos to hatch at a smaller size and an earlier developmental stage than controls, while dragonfly nymphs elicited a delay in egg hatching time that was associated with larger size and later developmental stage at hatching. Embryos failed to respond to simultaneous exposure to both predators, implying that responses to each occurred concurrently and were therefore dampened. Our results indicate that prey under threat from conflicting predators may manifest intermediate defensive phenotypes. Such intermediate responses may result in elevated rates of prey mortality with possible consequences at the population level.     

Interspecific variation in the escape responses of aphids: effect on risk of predation from foliar-foraging and ground-foraging predators

A series of laboratory experiments was conducted to determine the effect of interspecific differences on prey defensive behavior on the susceptibility of two aphid species (Acyrthosiphon pisum and A. kondoi) to a ground-foraging predator, Harpalus pennsylvanicus, and a foliar-foraging predator, Coccinella septempunctata. These organisms are representative of a biologically and economically important predator/prey system in alfalfa. The primary defensive behavior of both aphid species toward C. septempunctata was to “drop” from the plant. Both aphid species were significantly more likely to drop from the plant in the presence of C. septempunctata. However, when C. septempunctata was present, a significantly lower proportion of A. kondoi individuals dropped (0.42 ± 0.07) compared to A. pisum (0.73 ± 0.08). As a result of their lower propensity to drop from the plant A. kondoi individuals are significantly more likely to be consumed by C. septempunctata. Conversely, the higher propensity of A. pisum individuals to drop increased their susceptibility to ground-foraging predators. When A. pisum was the prey species, ground-foraging predators made a significant contribution to overall aphid suppression and there was a significant synergistic interaction between ground and foliar-foraging predators. When A. kondoi was the prey there was no interaction between the predator species. As either a cause or consequence of its higher propensity to drop, A. pisum seems to be more adapted for survival and dispersal off the plant. In comparison to A. kondoi individuals, A. pisum individuals relocate plants more quickly (63 ± 41 s vs. 164 ± 39 s), disperse farther (18 ± 1.7 cm vs. 13 ± 0.66 cm), and survive longer (37 ± 2.0 h vs. 25 ± 2.0) off the plant. This study demonstrates the importance of prey defensive behavior in determining the susceptibility of a prey species to a multiple-predator complex. Received: 24 February 1997 / Accepted:17 December 1997     

Woody species colonisation in relation to habitat productivity

A study was conducted to analyse the effect of habitat productivity on woody species colonisation. Three soil types were distinguished: a relatively poor sandy soil type (1), a somewhat richer sandy type (2) and a relatively rich sandy loamy type (3). Chronosequences were established on these three soil types of 38 (type 1), 20 (type 2) and 54 years (type 3) after abandonment. In total 117 vegetation relevées were used to analyse life form change and species responses during old field succession via regression models. On the rich soil type the colonisation rate of woody species was slower than on the poor soil type. This can be explained by higher abundances of perennial species during the first 20 years after abandonment on the rich soil type in contrast to the poor soil type. Perennial species may delay the woody species colonisation. First they close the bare ground which inhibits germination and next they compete with woody seedlings for light, water and nutrients. The effect of habitat productivity on woody species colonisation can only be determined appropriately by taking life history traits into account. Early successional 'pioneer' woody species dispersed by wind have less difficulties colonising old fields than late successional 'forest' species; they colonise old fields prior to the development of a dense perennial sward. Forest species depend on animals to be dispersed which are attracted by vegetation structure. In ± 30 years on the poor soil type and in ± 45 years on the rich soil type woody species become dominant relative to other life forms. Forest species like Quercus robur L. invaded relatively early (<5 years) in contrast to other studies which probably coincides with the distance to seed sources (forest edges).     

Biogeographic variation in behavioral and morphological responses to predation risk

The expression of prey antipredator defenses is often related to ambient consumer pressure, and prey express greater defenses under intense consumer pressure. Predation is generally greater at lower latitudes, and antipredator defenses often display a biogeographic pattern. Predation pressure may also vary significantly between habitats within latitudes, making biogeographic patterns difficult to distinguish. Furthermore, invasive predators may also influence the expression of prey defenses in ecological time. The purpose of this study was to determine how these factors influence the strength of antipredator responses. To assess patterns in prey antipredator defenses based upon geographic range (north vs. south), habitat type (wave-protected vs. wave-exposed shores), and invasive predators, we examined how native rock (Cancer irroratus) and invasive green (Carcinus maenas) crab predators influence the behavioral and morphological defenses of dogwhelk (Nucella lapillus) prey from habitats that differ in wave exposure across an ~230 km range within the Gulf of Maine. The expression of behavioral and morphological antipredatory responses varied according to wave exposure, geographic location, and predator species. Dogwhelks from areas with an established history with green crabs exhibited the largest behavioral and morphological antipredator responses to green crabs. Dogwhelk behavioral responses to rock crabs did not vary between habitats or geographic regions, although morphological responses were greater further south where predation pressure was greatest. These findings suggest that dogwhelk responses to invasive and native predators vary according to geographic location and habitat, and are strongly affected by ambient predation pressure due to the invasion history of an exotic predator.     

Carrying food items to cover for consumption: the behavior of ten bird species feeding under the risk of predation

Summary In earlier work (Lima et al. 1985; Lima 1985), we found that gray squirrels (Sciurus carolinensis) and black-capped chickadees (Parus atricapillus) when exploiting a patch of food in the open often carried individual food items to protective cover for consumption. Their tendency to carry (i) decreased as distance of the patch from cover increased, and (ii) increased as size of the available food items increased. A simple model indicated that this behavior was consistent with a trade-off between efficient foraging and predation risk. Maximal feeding efficiency was achieved by always eating at the patch, whereas minimal time exposure to predators was achieved by carrying all items to cover for consumption. Because predation-riskrelated trade-offs are likely to be of importance in the determination of feeding behavior, we surveyed the behavior of 10 bird species feeding under similar conditions to assess both the generality of the above results and the adequacy of some simple assumptions concerning the assessment and perception of predation risk.We observed considerable interspecific variability in behavior. Of the 10 species studied, 4 behaved in a manner similar to the squirrels and chickadees. Five other species showed an increased tendency to carry with larger items but no clear tendency to decrease carrying from longer distances. The one remaining species exhibited neither behavioral trend.The model that predicted squirrel and chickadee behavior failed to account for all observed behavior. The behavior of all species, however, was influenced by predation risk, and the discrepancy between theory and observation most likely reflects shortcomings of the model. These discrepancies indicate that other factors, in addition to exposure time, may be of significance in the perception of predation risk by several (or all) of the species studied. Of particular importance may be a distance-dependent probability of escaping attack. Other results indicate that predation risk may influence handling times via aspects of the digestive process.     

Morphological and reproductive responses of dominant plant species to local conditions in herbaceous successional stages of a calcareous hillside

Secondary succession on calcareous hillsides, initiated following the abandonment of agro-pastoral practices, is characterized by the transformation of initial short sward into tall herbaceous vegetation and finally woody formations. These structural changes are accompanied by modifications in ecological conditions but some species are able to persist and flower along the successional gradient. In this study, we compare reproductive and morphological traits of seven perennial species present in three successional stages [short grassland (SG), tall grassland (TG), and encroached grassland (EG)] to test if plant species present modifications along the successional gradient. The results show that morphological traits as height, leaf area and leaf dry mass increase for all studied species. Along the successional gradient, Teucrium chamaedrys increases ramet biomass more than twice (+145%) while Brachypodium pinnatum increases it even more (+340%). Maximum specific leaf area was observed in Brachypodium pinnatum (SLA = 20.4 mm² mg⁻¹) in SG, whereas Helianthemum nummularium and Teucrium chamaedrys have both rising SLA and falling leaf dry matter content in TG and EG. Concurrently, Helianthemum nummularium, Hippocrepis comosa and Teucrium chamaedrys show a clear decrease in sexual reproduction, with between 18 and 40% fewer flowers during the progress of succession. By contrast, Festuca lemanii, Sesleria caerulea and Brachypodium pinnatum increase their flower numbers per inflorescence (×3.6, ×3.3, and ×3.5, respectively). Festuca lemanii and Sesleria caerulea increase seed production to a maximum in TG, and Brachypodium pinnatum and Carex flacca increase seed output in TG and EG (×4.5, ×5.5, respectively). Changes in plants traits underscore the idea that species allocate resources differently probably because of increasing competition and decreasing edaphic constraints. This study also implies the potential existence of specific responses allowing plants to maintain existence within a plant community and explaining their contrasting performance during the succession.     

Too risky to settle: avian community structure changes in response to perceived predation risk on adults and offspring

Predation risk is widely hypothesized as an important force structuring communities, but this potential force is rarely tested experimentally, particularly in terrestrial vertebrate communities. How animals respond to predation risk is generally considered predictable from species life-history and natural-history traits, but rigorous tests of these predictions remain scarce. We report on a large-scale playback experiment with a forest bird community that addresses two questions: (i) does perceived predation risk shape the richness and composition of a breeding bird community? And (ii) can species life-history and natural-history traits predict prey community responses to different types of predation risk? On 9 ha plots, we manipulated cues of three avian predators that preferentially prey on either adult birds or offspring, or both, throughout the breeding season. We found that increased perception of predation risk led to generally negative responses in the abundance, occurrence and/or detection probability of most prey species, which in turn reduced the species richness and shifted the composition of the breeding bird community. Species-level responses were largely predicted from the key natural-history trait of body size, but we did not find support for the life-history theory prediction of the relationship between species'' slow/fast life-history strategy and their response to predation risk.     

The evolution of life-history traits in parasitic and free-living platyhelminthes: a new perspective

Parasite life histories have been assumed to be shaped by their particular mode of existence. To test this hypothesis, we investigate the relationships between life-history traits of free-living and parasitic platyhelminthes. Using phylogenetically independent contrasts we examine patterns of interspecific covariation in adult size, progeny volume, daily fecundity, total reproductive capacity, age at first reproduction and longevity. The correlations obtained indicate a similar causal chain of life history variations for free-living and parasitic platyhelminthes. These results suggest that increased longevity favours delayed reproduction. Furthermore, growth pattern determines adult body size and age at maturity. For platyhelminthes, whether free-living or parasitic, the total reproductive capacity is found to be directly determined by the size of the worm. Within this group the parasitic way of life does not seem to influence the basic patterns of life history evolution. Received: 20 September 1997 / Accepted: 1 March 1998     

Massive leaping of Sardinella aurita valenciennes, 1847 under probable risk of predation in Northern Aegean sea (Greece)

On the morning of 15th December 2002, several hundred live round sardinella (Sardinella aurita) individuals leaped out of the water and became stranded on the breakwater of Nea Iraklitsa port (Kavala Gulf, northern Aegean Sea, Greece). The phenomenon was most likely caused by the attack of the cetacean predator Tursiops truncatus (bottlenose dolphin), which is abundant in the area and feeds upon pelagic fish. The ability of round sardinella to leap out of the water has never been reported for other pelagic fishes.     

Evolutionary responses of Drosophila melanogaster life history to differences in larval density

The study examined the effects of evolution at two different larval densities on pre-adult and adult fitness traits. Five replicate selection lines each were cultured at either 50 or 150 larvae per vial, avoiding selection on development time, age at breeding or for adaptation to adult density, one or more of which factors has been a confounding variable in previous studies. Low density selection lines evolved extended development times at both growth densities. The extended development times were associated with greater adult body size at the lower growth density only, and particularly in females. The lines did not differ significantly in larval competitive ability at either growth density. At neither growth density did the early adult fertility of females or the lifespan of either sex differ between the lines from the two selection regimes, but at the lower growth density the late fertility of low density line females was significantly enhanced. The results suggest that larval density does have important effects on the expression and resolution of life history trade-offs in Drosophila melanogaster, but that these may be somewhat different from those reported in previous studies.     

Life-history responses of a mayfly to seasonal constraints and predation risk

Abstract. 1. An experiment was conducted in the laboratory to examine the effects of photoperiod and predation risk on life-history variation in the mayfly Ephemerella subvaria .
2. Both photoperiod and predation risk affected age at maturity significantly but neither factor affected size at maturity. Mayflies perceiving themselves to be late in the growing season matured in fewer days than those perceiving themselves to be early in the growing season. The presence of predators delayed mayfly maturity significantly.
3. These results suggest that the large variation in life-history traits observed in aquatic insects may be attributed partially to seasonality but that other biotic and abiotic factors may also underlie variation in these traits.     

Effects of body size, age and maturity stage on diet in a large shark: ecological and applied implications

Ontogenetic diet shifts are a widespread phenomenon among vertebrates, although their relationships with life history traits are poorly known. We analyzed the relative importance of body size, age and maturity stage as determinants of the diet of a marine top predator, the copper shark, Carcharhinus brachyurus, by examining stomach contents using a multiple-hypothesis modeling approach. Copper sharks shifted their diet as size and age increased and as they became sexually mature, incorporated larger prey as they grew, and had a discrete shift in diet with body size, with only individuals larger than ≈200 cm total length able to prey on chondrichthyans. Body size was the most important trait explaining the consumption of chondrichthyans, while age determined the consumption of pelagic teleosts. Pelagic teleosts were consumed mostly by medium-aged sharks, a result, probably, of a risk-reducing feeding strategy at young ages coupled with either a senescence-related decline in performance or a change in sensory capabilities as sharks age. Copper sharks of all sizes were able to cut prey in pieces, implying that gape limitation (i.e., the impossibility of eating prey larger than a predator’s mouth) did not play a role in producing the diet shift. Our results suggest that, contrary to the current practice of setting minimum but not maximum size limits in catches, any plan to conserve or restore the ecological function of sharks, through their predatory control of large prey, should aim to maintain the largest individuals.     

A test of the risk allocation hypothesis: tadpole responses to temporal change in predation risk

The risk allocation hypothesis predicts that temporal variationin predation risk can influence how animals allocate feedingbehavior among situations that differ in danger. We testedthe risk allocation model with tadpoles of the frog Rana lessonae,which satisfy the main assumptions of this model because theymust feed to reach metamorphosis within a single season, theirbehavioral defense against predators is costly, and they canrespond to changes in risk integrated over time. Our experiment switched tadpoles between artificial ponds with different numbersof caged dragonfly larvae and held them at high and low riskfor different portions of their lives. Tadpoles responded stronglyto predators, but they did not obey the risk allocation hypothesis:as the high-risk environment became more dangerous, there wasno tendency for tadpoles to allocate more feeding to the low-riskenvironment, and as tadpoles spent more time at risk, they didnot increase feeding in both environments. Our results suggestthat the model might be more applicable when the time spentunder high predation risk is large relative to the time requiredto collect resources.     

Interpopulation and context-related differences in responses of a marine gastropod to predation risk

We conducted laboratory experiments to investigate interpopulation differences in the behavioural responses of the whelk Buccinum undatum to the predatory lobster Homarus americanus and the asteroid Leptasterias polaris, both in the absence and presence of feeding opportunities. Whelks from three populations in the eastern North Atlantic (1) responded to lobsters by displaying avoidance behaviours (burrowing in the sediments or retreating inside their shell), (2) responded to asteroids by displaying escape responses (rapid crawling, shell rocking behaviour or foot contortions), and (3) more often refrained from feeding in the presence of a lobster than in the presence of an asteroid. Although whelks from the three populations responded similarly to lobsters and asteroids, interpopulation differences were evident. Thus, whelks from populations sympatric with a given predator more frequently displayed 'appropriate' antipredator behaviours (i.e. avoidance in the presence of a lobster, and escape in the presence of an asteroid) than did whelks allopatric with that predator. Also, whelks from a population sympatric with both predators fed less readily in the presence of a given predator than did whelks allopatric with that predator. However, the presence of a lobster or an asteroid had the same impact on the feeding response of whelks from two populations with contrasting predator fields, one sympatric with lobsters, but allopatric with asteroids, and one sympatric with asteroids, but allopatric with lobsters. The results of our study indicate that coexistence (over evolutionary or ecological time) with lobsters and asteroids increases the propensity of the whelk to display avoidance and escape behaviours in the presence of lobsters and asteroids, respectively, but has a less predictable effect on how whelks trade off predation risk and food acquisition. Studies are needed to investigate the roles of inheritance and experience on the development of antipredator behaviours and decision making by prey animals when predation risk conflicts with other fitness-related activities such as the acquisition of food or reproductive opportunities. Copyright 1999 The Association for the Study of Animal Behaviour.