Environmental correlates of the intrinsic rate of natural increase in primates

Morphological and life history traits of two clones of the cladoceran Daphnia pulex were measured in the presence and absence of size-selective insect predators, the midge larva Chaoborus flavicans, which preys on small Daphnia, and the water bug Notonecta glauca, which preys on large Daphnia. The aim was to detect predator-induced phenotypic changes, particularly the effect of simultaneous exposure to both types of predators. Other work has shown that in the presence of Chaoborus americanus, Daphnia pulex produce a socalled neck spine which may carry several teeth. The morphological modifications are supposed to serve as an anti-predator device. Furthermore, females exposed to Chaoborus often delay their maturation; this has been interpreted as a cost that balances the benefits of the neck teeth. In this investigation, females of both clones produced fewer but larger offspring than control animals when reared in the presence of Chaoborus flavicans. The offspring showed the typical neck spine and delayed first reproduction. In the presence of Notonecta glauca, one of the clones produced more and smaller offspring, and maturation occurred at earlier instars. The other clone also produced more offspring than the control but there was no size difference. When both predators were present, in most cases the reactions of the daphnids were similar to those in the Notonecta experiment. The response to Chaoborus appeared to be suppressed. The observed modifications are interpreted as evolved strategies that reduce the impact of size-selective predation. They are consistent with predictions of life-history theory.     

Reversibility of predator‐induced plasticity and its effect at a life‐history switch point

In natural systems, organisms are frequently exposed to spatial and temporal variation in predation risk. Prey organisms are known to develop a wide array of plastic defences to avoid being eaten. If inducible plastic defences are costly, prey living under fluctuating predation risk should be strongly selected to develop reversible plastic traits and adjust their defences to the current predation risk. Here, we studied the induction and reversibility of antipredator defences in common frog Rana temporaria tadpoles when confronted with a temporal switch in predation risk by dragonfly larvae. We examined the behaviour and morphology of tadpoles in experimental treatments where predators were added or withdrawn at mid larval development, and compared these to treatments with constant absence or presence of predators. As previous studies have overlooked the effects that developing reversible anti‐predator responses could have later in life (e.g. at life history switch points), we also estimated the impact that changes in antipredator responses had on the timing of and size at metamorphosis. In the presence of predators, tadpoles reduced their activity and developed wider bodies, and shorter and wider tails. When predators were removed tadpoles switched their behaviour within one hour to match that found in the constant environments. The morphology matched that in the constant environments in one week after treatment reversal. All these responses were highly symmetrical. Short time lags and symmetrical responses for the induction/reversal of defences suggest that a strategy with fast switches between phenotypes could be favoured in order to maximise growth opportunities even at the potential cost of phenotypic mismatches. We found no costs of developing reversible responses to predators in terms of life‐history traits, but a general cost of the induction of the defences for all the individuals experiencing predation risk during some part of the larval development (delayed metamorphosis). More studies examining the reversibility of plastic defences, including other type of costs (e.g. physiological), are needed to better understand the adaptive value of these flexible strategies.     

Developmental responses to predation risk in morphologically defended mayflies

Densities and species composition of predators could affect morphological defences, larval development and the timing of emergence of their prey. To address this issue we studied the morphology and life history of an ephemerellid mayfly, Ephemerella invaria, from two streams in a deciduous forested drainage basin in central New York. Both streams contained predatory fish, but densities and species composition of fish differed. A field survey provided evidence that Ephemerella inhabiting a stream with 10 fish species and high relative densities of fish emerged several weeks earlier and at smaller sizes than Ephemerella inhabiting a nearby tributary with ~2 fish species and low relative densities of fish. However, the two populations of mayflies showed no differences in defensive morphology or growth rates. In laboratory rearing experiments, we exposed Ephemerella larvae from these two locations to fish chemical cues or control water (no fish) over 2 months to test whether differences in life histories could be attributed to fish. Fish cues induced faster larval development, but also smaller size of mature Ephemerella individuals from both high and low predator locations. Although shorter development times in more dangerous environments could increase larval survival, smaller size of females results in a fecundity cost associated with this life history shift. Consistent with the field studies, laboratory rearing experiments revealed no effects of fish cues on Ephemerella's morphological defences. These data suggest that variation in the density or species composition of predators may favour the evolution of developmental plasticity to reduce mortality in the larval environment.     

Costs of predator‐induced morphological defences in Daphnia

1. Inducible defences are advantageous because they protect the prey while limiting associated fitness costs. The presence of these costs is an essential component of this conditional strategy, since their absence would favour constitutive (fixed) defences. In some cases, however, these costs have been difficult to measure because of complex interactions between the defences themselves, resultant life history changes and the organism’s environment. 2. The pond‐dwelling water flea, Daphnia pulex, forms defensive neck spines in response to kairomones released by predatory larvae of the phantom midge, Chaoborus. This predator–prey interaction and the formation of these inducible defences have been well studied, but costs associated with the development of neck spines remain unclear. In this study, I address this problem by analysing the effect of Chaoborus kairomones on the life history responses (and fitness costs associated with these responses) of two clones of D. pulex that are from the same pond population, but differ greatly in their degree of neck spine development. 3. Both D. pulex clones exhibited the same predator‐induced shifts in life history: larger size at birth, reduced juvenile growth rate (producing a smaller size at maturity), delayed reproduction and a reduction in the number of neonates produced after the first clutch. Relative fitness decreased significantly and to the same degree (c. 10% reduction in r) in each clone. This observed fitness cost was not directly related to the neck spines per se since the cost was the same in both clones, despite their considerable differences in neck spine development. Rather, it appears to be indirectly related to this antipredator morphology via a combination of delayed reproduction and a set of life history trade‐offs (decreased growth rate, decreased reproduction after the first clutch) for increased neonate body size, which is necessary for neck spines to be effective defences. This suite of induced responses is probably a result of local adaptation of these two D. pulex clones to their common pond environment. 4. Costs of inducible defences do not always entail direct allocation costs associated with forming and maintaining a defence, but may also involve indirect life history responses that are specific to particular environmental situations. This local adaptation would explain the highly variable life history responses observed among D. pulex clones from different pond environments.     

Costs and benefits of defences induced by predators differing in dangerousness

While theoretical studies predict that inducible defences should be fine-tuned according to the qualities of the predator, very few studies have investigated how dangerousness of predators, i.e. the rate at which predators kill prey individuals, affects the strength of phenotypic responses and resulting benefits and costs of induced defences. We performed a comprehensive study on fitness consequences of predator-induced responses by involving four predators (leech, water scorpion, dragonfly larva and newt), evaluating costs and benefits of responses, testing differences in dangerousness between predators and measuring responses in several life history traits of prey. We raised Rana dalmatina tadpoles in the presence of free-ranging predators, in the presence of caged predators, and exposed naive and experienced tadpoles to free-ranging predators. Tadpoles adjusted the intensities of their behavioural and morphological defences to predator dangerousness. Survival was lower in the nonlethal presence of the most dangerous predator, while we could not detect costs of induced defences at or after metamorphosis. When exposed to free-ranging predators, small, but not large, tadpoles benefited from exhibiting an induced phenotype in terms of elevated survival when compared to naive tadpoles, but we did not observe higher survival either in tadpoles exhibiting more extreme phenotypes or in tadpoles exposed to the type of predator they were raised with. These results indicate that while predator-induced defences can mirror dangerousness of predators, costs and benefits do not necessarily scale to the magnitude of plastic responses.     

Precise time interactions between behavioural and morphological defences

Defences induced against predators fall into three basic categories – behavioural, morphological and life history. Many species induce changes in more than one category. A theoretical advantage of a behavioural change is its potential for rapid induction compared to morphology or life history. We tested this theory by comparing modifications in behaviour and morphology along a time line in the hypotrich ciliate Euplotes octocarinatus exposed to chemical cues from Stenostomum virginianum, a predatory flatworm. Behavioural defences were induced much more rapidly than morphological, although as morphological defences became expressed changes in behaviour were slightly relaxed. This suggests a temporal compensatory relationship between the two traits. Behavioural defences are quickly induced to rapidly reduce predation risk, however they are relaxed as morphology changes are realised to avoid paying the cost of expressing both types of defence.     

Effects of Ultraviolet Radiation on Diel Vertical Migration of Crustacean Zooplankton: An in situ Mesocosm Experiment

The objective of this study was to expand the spatial scale of previous experiments on the effects of ultraviolet radiation (UVR) on diel vertical migration (DVM) by freshwater zooplankton. We conducted an in situ mesocosm experiment in highly UVR transparent Lake Giles, Pennsylvania, in which we imposed two treatments: ambient UVR and UVR-shielded. Mesocosms (3440 L, 0.74 m diameter, 8 m deep) were large enough to include a spatial refuge from UVR and permit relatively large-scale DVM. Daphnia catawba adopted a significantly deeper distribution during the day in the ambient UVR treatment compared to the UVR-shielded treatment, but effects of UVR were absent at night. In contrast, DVM by Leptodiaptomus minutus was unaffected by the UVR treatment. In both treatments, Leptodiaptomus minutus were most abundant at the bottom of the mesocosms during the day and exhibited a more uniform distribution across depths at night. These results suggest that UVR, along with temperature, algal resources, and predators, may affect zooplankton DVM in aquatic ecosystems.     

Effects of a fluctuating temperature regime experienced by Daphnia during diel vertical migration on Daphnia life history parameters

Many freshwater zooplankton species perform a diel vertical migration (DVM) and spend the day within the lower, colder hypolimnion of stratified lakes. Trade-offs that arise from this migration have already attracted much attention and the cold temperature in the hypolimnion is thought to be the main cost of this behaviour. In this study we additionally looked at the extra costs daphnids have from being exposed to a fluctuating temperature regime (cold during the day and warm during the night) which is less well studied until today. In our experiment Daphnia hyalina Leydig and Daphnia magna Straus either spent 24 h in constant warm water (19 °C), 24 h in constant cold water (12 °C), or spent 12 h in warm and 12 h in cold water in an alternating way (fluctuating temperature regime). We expected the values of the life history parameters of Daphnia in the fluctuating temperature regime to be exactly halfway between the values of the life history parameters in the warm and cold treatments because the daphnids spent exactly half of the time in warm water, and half of the time in cold water. Concordant with earlier studies our results showed that age at first reproduction and egg development time were reduced at higher temperatures. In the fluctuating temperature regime the values of both parameters were exactly halfway between the values at permanently warm and cold temperature regimes. In contrast, somatic growth was higher at higher temperatures but was lower in the fluctuating temperature regime than expected from the mean somatic growth rate. This suggests that a fluctuating temperature regime experienced by migrating daphnids in stratified lakes involves additional costs for the daphnids.     

Multiple predator defence strategies in Daphnia pulex and their relation to native habitat

Daphnia may respond with an array of anti-predator defences(behavioural, morphological and life history) to a chemicalcue (kairomone) exuded by its predators: fish and Chaoborus.Given the wide array of potential responses, it is an interestingquestion whether anti-predator defences are coupled or independentof each other. Since anti-predator responses are costly andeven possessing the genetic information to respond to a certainpredator might involve a cost, clones may only react to predatorsthey co-occur with in nature. In this study, we provide evidencefor an uncoupling of responses by Daphnia pulex in several anti-predatordefences against Chaoborus. We were unable to detect a correlationbetween behavioural (migration), morphological (neck-spine induction)and life history [growth rate, neonate size and size at firstreproduction (SFR)] responses. Furthermore, anti-predator responsesdid not always comply with what is commonly believed. We foundthat Daphnia clones can migrate up or down when exposed to fishor Chaoborus kairomone and that population growth rate, neonatesize and SFR can increase or decrease in response to Chaoboruskairomone. We also show patterns in anti-predator defences thatseem to relate to the habitat from which clones were derived.Daphnia clones that were collected in habitats with Chaoborusas the dominant predator tended to react strongly to Chaoboruskairomone by migrating upward and producing neck-spines. Themigration behaviour against fish kairomone in these clones wasoften an unexpected upward migration. The Daphnia clone thatco-existed with fish predators showed a downward migration inthe presence of fish as well as Chaoborus kairomone. Clonesthat had occurred with either both or no predators had mixedresponses. We sometimes found an upward migration in combinationwith smaller body size as a response to Chaoborus kairomone.This may be interpreted as a behavioural defence against Chaoborusand a life-history defence against fish. Daphnia seem not toexhibit defence behaviour against predators they do not co-occurwith. It might be costly for Daphnia to maintain genetic informationto respond to these predators and protect that information fromgenetic drift.     

Diel vertical migration and feeding rhythm of Daphnia longispina and Bosmina corexoni in Lake Toya, Hokkaido, Japan

Diel vertical migration (DVM) and diel feeding rhythm of two cladocerans, Daphnia longispina and Bosmina coregoni were investigated at the pelagic area of Lake Toya (Hokkaido, Japan) in May, August and October 1992. Both species performed nocturnal DVM. The amplitude of DVM, however, became smaller from May to October. Such seasonal variations in DVM could not be explained by light penetration and/or water temperature. The two species had a clear feeding rhythm; they fed at night in May and October but also after sunrise in August. These feeding rhythms appeared to be related to the light-dark cycle, but were not necessarily associated with their DVM. We suggest that the diel feeding rhythm and DVM are regulated independently by light cues.     

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

While deploying immune defences early in ontogeny can trade‐off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade‐offs with important adult traits. Here, we tested for predator‐dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune‐challenged larvae had later emergence overall and lower survival in pools with predators. Immune‐challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.     

Divergent phenotypic responses to predators and cyanobacteria in Daphnia lumholtzi

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Diel vertical migration of zooplankton following optimal food intake under predation

A model is developed to investigate the trade-offs between benefitsand costs involved in zooplanktonic diel vertical migration(DVM) strategies. The ‘venturous revenue’ (VR) isused as the criterion for optimal trade-offs. It is a functionof environmental factors and the age of zooplankter. Duringvertical migration, animals are assumed to check instantaneouslythe variations of environmental parameters and thereby selectthe optimal behavioral strategy to maximize the value of VR,i.e. taking up as much food as possible with a certain riskof mortality. The model is run on a diel time scale (24 h) infour possible scenarios during the animal’s life history.The results show that zooplankton can perform normal DVM balancingoptimal food intake against predation risk, with the profileof DVM largely modified by the age of zooplankter.     

Comparison of fish and phantom midge influence on cladocerans diel vertical migration in a dual basin lake

Diurnal vertical migrations (DVM) behaviour of cladocerans was investigated in two mesotrophic Irish lakes connected by a canal, characterised by interesting differences in the presence of zooplanktivorous predators. In Doon Upper, fish (mostly juvenile perch and roach) and a little-studied phantom midge Mochlonyx fuliginosus (Chaoboridae) were found, but Doon Lower was solely inhabited by fish. As the presence of diverse predators may alter spatial avoidance behaviour of zooplankton prey in different ways, the aim of this study was to determine whether and how two predator types, fish and phantom midge larvae, have changed DVM pattern of cladocerans during day and night in Doon lakes. Two sampling series of phytoplankton, zooplankton, fish, and water physical analyses were conducted on 09–10 June and 19–20 September 2007 in both lakes. In the study conducted in June, under a similar distribution of M. fuliginosus and juvenile fish in Doon Upper, a reverse migration of Daphnia galeata was observed as a strategy allowing them to avoid both types of predators. However, in September, when M. fuliginosus lived in a 24 h refugium below the oxycline as a response to increasing predation risk posed by YOY fish penetrated the upper strata of water during day and night, reverse migrations of D. galeata were not clear. In Doon Lower, normal migration was observed as an advantageous behavioural response against visual predators (fish), in both large and small Cladocera species: D. galeata, Diaphanosoma branchyurum and Bosmina sp. Thus, our results indicate dissimilar migration patterns of D. galeata depending on the presence of one (Doon Lower) or two predators with different predation behaviour (Doon Upper).     

Multiple defence strategies of <Emphasis Type="Italic">Daphnia</Emphasis><Emphasis Type="Italic">galeata</Emphasis> against predation in a weakly stratified reservoir

In the presence of size-selective fish daphnids were shown to exhibit two alternative inducible defence strategies: They may either escape predation by active migration or adopt a life history strategy, e.g., reproduce earlier and at a smaller size. Depending on the type of habitat, migration may either be vertically (in deep stratified lakes) or horizontally (in shallow lakes with macrophytes) oriented. Concerning behavioural defence strategies, daphnids living in medium-deep, weakly stratified water bodies with a poorly developed littoral face a dilemma, since the littoral provides no shelter and the availability of a deep-water refuge is unpredictable. We studied the population dynamics, life history changes (size at maturity) and daytime vertical distribution of Daphnia galeata in a weakly stratified reservoir in relation to predation by juvenile fish during 6 years. While temperature gradients were usually small, oxygen concentrations suggest that a low-oxygen refuge for daphnids was available in every year to some extent. Our results indicate that, depending on predation intensity and stratification patterns, daphnids exhibit both, behavioural and life history defences. In years with a high biomass of young-of-the-year (YOY) perch Daphnia abundance declined rapidly at the end of the clear water stage while at the same time the vertical distribution at daytime shifted to deep strata providing a low-oxygen refuge and the size at maturity decreased. However, while the life history response in some years lasted throughout most of the summer period, a shift in daytime vertical distribution was exhibited for much shorter periods. Both traits were much less expressed in years with low YOY fish densities and no negative correlation between them could be verified. We suggest that under high predation pressure in this relatively shallow reservoir no strictly alternative (either behavioural or life history) strategies exist, but that daphnids make use of the full range of possible anti-predator defences available, at least during short periods when predation is most intense. Guest editor: Piet Spaak Cladocera: Proceedings of the 7th International Symposium on Cladocera     

Diel vertical migration of larval and early‐juvenile burbot optimises survival and growth in a deep,pre‐alpine lake

1. Burbot larvae (Lota lota) perform a substantial diel vertical migration (DVM) of increasing amplitude in the pelagic zone during a 3‐month period before migrating to the littoral zone as early‐juveniles. We hypothesised that feeding in the warm surface layers at night and then spending the day in cold water below the thermocline reduces metabolic costs and earns burbot larvae an energetic advantage. 2. To test our hypothesis, we mimicked the temperature conditions experienced by vertically migrating burbot in the pelagic zone. We also simulated three further scenarios, in which temperature remained constant. 3. Burbot showed the best performance (defined as specific growth rate multiplied by the probability of survival) in the treatments simulating DVM. The high temperature treatment, simulating permanent residence in the warm epilimnion, resulted in high growth combined with high mortality. At a permanently low temperature, simulating life in the hypolimnion, growth was poor and activity reduced. 4. In a deep, temperature‐stratified lake, where the apparently beneficial overall medium temperature is found in a restricted layer within the thermocline, DVM optimises performance in young burbot. Various ultimate factors might act synergistically in selecting for DVM in larval and early‐juvenile burbot.     

Food and temperature stressors have opposing effects in determining flexible migration decisions in brown trout (Salmo trutta)

With rapid global change, organisms in natural systems are exposed to a multitude of stressors that likely co‐occur, with uncertain impacts. We explored individual and cumulative effects of co‐occurring environmental stressors on the striking, yet poorly understood, phenomenon of facultative migration. We reared offspring of a brown trout population that naturally demonstrates facultative anadromy (sea migration), under different environmental stressor treatments and measured life history responses in terms of migratory tactics and freshwater maturation rates. Juvenile fish were exposed to reduced food availability, temperatures elevated to 1.8°C above natural conditions or both treatments in combination over 18 months of experimental tank rearing. When considered in isolation, reduced food had negative effects on the size, mass and condition of fish across the experiment. We detected variable effects of warm temperatures (negative effects on size and mass, but positive effect on lipids). When combined with food restriction, temperature effects on these traits were less pronounced, implying antagonistic stressor effects on morphological traits. Stressors combined additively, but had opposing effects on life history tactics: migration increased and maturation rates decreased under low food conditions, whereas the opposite occurred in the warm temperature treatment. Not all fish had expressed maturation or migration tactics by the end of the study, and the frequency of these ‘unassigned’ fish was higher in food deprivation treatments, but lower in warm treatments. Fish showing migration tactics were smaller and in poorer condition than fish showing maturation tactics, but were similar in size to unassigned fish. We further detected effects of food restriction on hypo‐osmoregulatory function of migrants that may influence the fitness benefits of the migratory tactic at sea. We also highlight that responses to multiple stressors may vary depending on the response considered. Collectively, our results indicate contrasting effects of environmental stressors on life history trajectories in a facultatively migratory species.     

Diel vertical migration of freshwater fishes – proximate triggers,ultimate causes and research perspectives

1. Diel vertical migrations (DVM) are typical for many cold‐water fish species such as Pacific salmons (Oncorhynchus spp.) and coregonids (Coregonus spp.) inhabiting deep lakes. A comprehensive recent overview of DVM in freshwater fish has not been available, however. 2. The main proximate trigger of DVM in freshwater fish is the diel change in light intensity, with declining illumination at dusk triggering the ascent and the increase at dawn triggering the descent. Additional proximate cues are hydrostatic pressure and water temperature, which may guide fish into particular water layers at night. 3. Ultimate causes of DVM encompass bioenergetics efficiency, feeding opportunities and predator avoidance. None of these factors alone can explain the DVM in all cases. Multi‐factorial hypotheses, such as the ‘antipredation window’ combined with the thermal niche hypothesis, are more likely to explain DVM. It is suggested that planktivorous fish move within a layer sufficiently well illuminated to capture zooplankton, but too dark for predators to feed upon the migrating fish. In complete darkness, fish seek layers with a temperature that optimises bioenergetics efficiency. The strength of each factor may differ from lake to lake, and hence system‐specific individual analyses are needed. 4. Mechanistic details that are still poorly explored are the costs of buoyancy regulation and migration, the critical light thresholds for feeding of planktivorous and piscivorous fish, and predator assessment by (and size‐dependent predation risk of) the prey fish. 5. A comprehensive understanding of the adaptive value of DVM can be attained only if the behaviour of individual fish within migrating populations is explicitly taken into account. Size, condition and reproductive value differ between individuals, suggesting that migrating populations should split into migrants and non‐migrants for whom the balance between mortality risk and growth rate can differ. There is increasing evidence for this type of partial DVM within populations. 6. Whereas patterns of DVM are well documented, the evolution of DVM is still only poorly understood. Because experimental approaches at realistic natural scales remain difficult, a combination of comprehensive data sets with modelling is likely to resolve the relative importance of different proximate and ultimate causes behind DVM in fish.