The change in phototactic behaviour of a Daphnia magna clone in the presence of fish kairomones: the effect of exposure time

Using a clone that responds to the presence of fishkairomones by a pronounced change in phototacticbehaviour, we determined how fast a change to morenegatively phototactic behaviour occurs in Daphnia magnaadults that are exposed to a highconcentration of fish kairomones. Kairomone exposedanimals showed an approximately linear decrease in thevalue of the phototactic index with time. Though theresponse was almost immediate, it took two hoursbefore the difference between fish-induced and controlanimals was significant. Extrapolation of the observedresponse indicates that a maximal change inphototactic behaviour, equivalent to animals that havebeen cultured in the presence of fish kairomones sincebirth, occurs after about 13 hours exposure. Weconclude that the predator-induced change in dielvertical migration of zooplankton is fast, and isfully developed in less than a day. The response timeto fish kairomones of Daphnia is shorter forphototactic behaviour than for life history traits,which may have important consequences with respect tothe evolution of trait-dependence in induced defenceresponses.     

Evolution of predator avoidance in a Daphnia population: evidence from the egg bank

Dormant propagule pools (egg banks) of zooplankton populations that accumulate in sediments provide biological archives of past conditions and enable the investigation of evolutionary changes in populations over relatively long periods of time (many decades). This study examined the egg bank of a Daphnia pulicaria population in a lake that has been stocked annually with rainbow trout (a zooplanktivore) since 1961. Resting eggs from sediments from the 1920s to 2001 (determined by ²¹⁰Pb dating) were hatched and established as isofemale clonal lines. The phototactic behavior (a proxy for vertical migration behavior) of clones was assessed in the presence and absence of fish kairomones to evaluate the hypothesis that the heavy and consistent level of predation imposed by the stocked trout would have selected for clones that are more negatively phototactic. In addition, exposure to kairomones was expected to induce stronger negative phototaxis for all clones relative to control conditions. The behavior of clones derived from resting eggs from the trout era (after 1961) was significantly more negatively phototactic than it was for pre-trout era clones. Kairomone exposure induced a more negative phototactic response in clones from both eras, but the response was much greater for the pre-trout era clones. These results suggest that the consistently high level of predation by trout over several decades has selected for a conservative (less plastic) vertical migration strategy in which Daphnia maintain a deep daytime distribution with or without the presence of chemical cues from fish predators.     

Differential life history responses of several pelagic Daphnia clones differing in migratory behaviour

Females of the hybrid Daphnia galeata × hyalina were isolated from a natural population in Lake Maarsseveen and from these individuals clones were cultured in the laboratory. Some clones were assumed to be migrating and some non-migrating. Life history experiments were performed with these clones in the presence and absence of fish kairomones. Results show that clones differed in life history strategy in concert with their presumed migration strategies which suggests a link between life history and behaviour. However, no sharp border exists between migrating and non-migrating clones since a gradual response pattern was found for the traits investigated. In the absence of fish kairomones, the relation between length at maturity and number of eggs was found to differ between the clones of the non-migrating and the migrating group. The latter had a lower number of eggs at similar length values. In the presence of fish kairomones, the length–clutch size relation was the same. However, non-migrating clones were smaller at the age at maturity and had fewer eggs. Although clones of both groups were thus found to differ significantly, overlap existed. Age at maturity was found to be the same.     

Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses

We studied the way 12 traits responded to fish kairomones in a set of 16 Daphnia magna clones derived from four different habitats-two where daphnids co-occur with fish and two without fish. These clones differed widely in their response to predator kairomones, with none of the clones showing a significant response in all traits and all clones showing a response for at least one trait. Most of the clones showed a significant response in one to four traits, with no evidence for an association between different traits. Clones from fish habitats were slightly more responsive to the presence of fish kairomones than clones from fishless locations. We conclude that most clones show an induced response to the presence of their predators (fish) but that there is a large genetic variability with respect to the traits for which clones show a response. Our results indicate that the major distinction is not between inducible and noninducible genotypes but rather that the genotypes differ in the combination of traits for which they show inducible responses.     

EVOLUTIONARY POTENTIAL AND LOCAL GENETIC DIFFERENTIATION IN A PHENOTYPICALLY PLASTIC TRAIT OF A CYCLICAL PARTHENOGEN,DAPHNIA MAGNA

The frequent use of neutral markers to quantify genetic variation in natural populations emphasizes the role of stochastic events in explaining genetic differentiation between populations. Complementary studies on ecologically relevant traits are needed to assess the role of natural selection acting on adaptive variation in the development of local genetic differentiation. To test the hypothesis of local adaptation in the cyclical parthenogenetic species Daphnia magna, the phototactic behavior in the absence and presence of fish kairomone was assayed for 30 clones derived from resting eggs isolated from three habitats characterized by a different predation pressure by fish. Clones derived from populations in which fish are present were, on average, more negatively phototactic in and more responsive to the presence of fish kairomone than clones derived from a fishless habitat. In addition, the results show a high genetic diversity for the traits studied in all three gene pools investigated, indicating a high potential for microevolutionary changes in behavior of these Daphnia populations in the face of changes in predation pressure. The results of the present study indicate that working with large samples at the expense of having less precise estimates of genotypic values for specific genotypes may result in a loss of information with regard to the evolutionary potential of local populations.     

Geographical and genetic distances among zooplankton populations in a set of interconnected ponds: a plea for using GIS modelling of the effective geographical distance

In systems of interconnected ponds or lakes, the dispersal of zooplankton may be mediated by the active population component, with rivulets and overflows functioning as dispersal pathways. Using a landscape-based approach, we modelled the effective geographical distance among a set of interconnected ponds (De Maten, Genk, Belgium) in a Geographic Information System (GIS) environment. The first model (the Landscape Model; LM) corrects for the presence of direct connections among ponds and was based on the existing landscape structure (i.e. network of connecting elements among ponds, travelling distance and direction of the current). A second model (the Flow Rate Model; FRM) also incorporated field data on flow rates in the connecting elements as the driving force for the passive dispersal of the active zooplankton population component. Finally, the third model (the Dispersal Rate Model; DRM) incorporated field data on zooplankton dispersal rates. An analysis of the pattern of genetic differentiation among Daphnia ambigua populations inhabiting 10 ponds in the pond complex reveals that the effective geographical distance as modelled by the flow rate and the dispersal rate model provide a better approximation of the true rates of genetic exchange among populations than mere Euclidean geographical distances or the landscape model that takes into account solely the presence of physical connections.     

Behavioural and genetic differences in populations of Daphnia subjected to different levels of predation

1. Predictions based on a genetic control mechanism for vertical migration were tested by monitoring the vertical migration behaviour of electro-phoretically distinct clones of Daphnia longispina and Daphnia magna collected from ponds with different levels of predation. 2. The number of predator species in a pond (a measure of predation) had a significant effect on the vertical migration behaviour of the clones found within that pond, and a phenogram constructed on the basis of the percentage dissimilarity between the genotypes of the clones indicated that clones from the same site were more closely related genetically than clones from different sites. 3. There were significantly different vertical migration behaviour patterns between clones from different sites and between-site variation in behaviour was significantly greater than that found within a site. 4. Clones differed in the average depth they maintained in the waterbody regardless of the pond from which they were collected, but clones from the same site did have similar behavioural profiles suggesting a tendency to show the same behavioural patterns. 5. These findings, which support predictions based on a genetic control mechanism, are discussed in relation to phenotypically plastic mechanisms of vertical migration control widely reported in the literature.     

Direct and indirect effects of predation on tadpole community structure in the Amazon rainforest

Abstract The relationship between the distribution of predators (fish, odonates and water beetles) and prey assemblages (amphibian larvae) was investigated in the tropical rainforest of central Amazonas, Brasil. The anuran community uses a variety of waterbodies for reproduction, ranging from streams and streamside ponds to isolated forest ponds. Predators in this system include fish in streams and streamside ponds, and invertebrates (primarily odonate naiads and beetles) in forest ponds. Tadpole species richness and assemblage structure were related to fish density and species richness. No relationships between tadpole assemblages and abiotic pond characteristics were detected. The presence offish explained much of the variation in both species composition and species richness within and among ponds. Some species of tadpole were consistently found to coexist with high densities of fish. Path analyses suggest that while fish have a strong direct effect on tadpole associations and species richness, they also have an indirect effect through invertebrate predators (odonate larvae and coleopteran beetles). Prey survival-strategies such as palatability and behaviour may explain how tadpole species composition is affected by predators at the community level. These findings suggest that the observed patterns of habitat use by larval anurans may be structured in response to the distribution of key predators (fish) in this system.     

Clonal diversity and spatial genetic structure of Potamogeton pectinatus in managed pond and river populations

Higher levels of genetic diversity of river macrophytes are expected in downstream parts because of potential accumulation of various genotypes from upstream sites. We assessed the clonal diversity and spatial genetic structure of fennel pondweed (Potamogeton pectinatus or Stuckenia pectinata) populations with emphasis on the estimation of dispersal via clonal propagules along a river in connection to upstream ponds. We analysed genetic diversity of 354 plant shoots sampled in 2005 and 2006 at three pond and five river sites in the Woluwe river catchment (Belgium). Nine microsatellite DNA markers revealed 88 genets of which 89% occurred in only one site. Clonal propagule dispersal was detected up to 10 km along the river. Few multilocus genotypes were repeatedly present along a major part of the river indicating vegetative spread. Populations of ponds contained a higher amount of clonal diversity, indicating the importance of local seed recruitment. A fine-scaled spatial genetic structure indicated that most seedling recruitment occurred at a distance <5 m in pond populations whereas clones in river sites were unrelated and showed no spatial autocorrelation. The clonal diversity decreased along the river from upstream to downstream due to establishment of few large clones.     

Genetic differentiation in life history between Daphnia galeata populations: an adaptation to local predation regimes?

Species of the water flea Daphnia exhibit constitutive as wellas phenotypically inducible anti-predator defence strategies,involving life history, morphological and behavioural traits.We explored the hypothesis of genetic differentiation in anti-predatordefence strategies using Daphnia clones originating from twodifferent water bodies: Tjeukemeer (the Netherlands) and FishPond (Belgium). Both water bodies are inhabited by zooplanktivorousfish. In contrast to Tjeukemeer, Fish Pond is also inhabitedby larvae of the phantom midge Chaoborus. The life history responsesof the two sets of clones to kairomones from fish (Perca), tokairomones from Chaoborus, and to a mixture of both were compared.Clones from Tjeukemeer and Fish Pond showed strong responsesto the presence of fish kairomone, with reductions in adultand neonate body length, in age at first reproduction and inthe total number of neonates produced during the first threeadult instars. Responses to Chaoborus kairomone were much lesspronounced, although there was a tendency towards an increasein the number of neonates in the first brood. Significant inter-populationgenetic differences were found for all the investigated traits.However, there was no indication for genetic adaptation of theFish Pond clones to negative size-selective predation by Chaoborus.Compared to Tjeukemeer clones, Fish Pond clones had a lowersize at first reproduction, produced smaller neonates and produceda higher number of neonates in their first brood. This suggestsadaptation to positive rather than to negative size selectivepredation. Genetic differences between populations were observedmainly for constitutive life history traits, rather than forphenotypic shifts in response to the presence of predator kairomones.     

Crustacean zooplankton community structure in temporary and permanent grassland ponds

Lentic community structure varies across a size gradient of ponds and lakes with physical factors, such as pond drying, and biotic factors, such as fish predation, determining the species assemblage. We studied the effects of pond drying and fish absence on crustacean zooplankton across a gradient of pond sizes in a Texas grassland. We determined the species compositions and size distributions of crustacean zooplankton in 20 temporary and 18 permanent ponds in April after March rains had refilled the ponds. The surface areas of temporary and permanent ponds ranged from <0.01 to 0.21 ha and 0.04 to 13.8 ha, respectively, and temporary ponds were significantly smaller, on average, than permanent ponds. Fish were absent from all temporary ponds and present in all permanent ponds. We detected a difference in the zooplankton species assemblages of the temporary and permanent ponds. Out of 14 total zooplankton taxa that occurred in eight or more ponds, seven taxa were significantly more prevalent in temporary ponds and four taxa were significantly more prevalent in permanent ponds. The sizes of zooplankton in the temporary fishless ponds were greater than those in the permanent ponds with fish present. We concluded that pond size mediated susceptibility to pond drying, and pond drying determined the presence and absence of fish and their secondary trophic-level effect on zooplankton community structure. Handling editor: Steven Declerck     

Reaction norms for metamorphic traits in natterjack toads to larval density and pond duration

The evolution of environmentally-induced changes in phenotype or reaction norm implies both the existence at some time of genetic variation within a population for that plasticity measured by the presence of genotype x environment interaction (G x E), and that phenotypic variation affects fitness. Otherwise, the genetic structure of polygenic traits may restrict the evolution of the reaction norm by the lack of independent evolution of a given trait in different environments or by genetic trade-offs with other traits that affect fitness. In this paper, we analyze the existence of G x E in metamorphic traits to two environmental factors, larval density and pond duration in a factorial experiment with Bufo calamita tadpoles in semi-natural conditions and in the laboratory. Results showed no plastic temporal response in metamorphosis to pond durability at low larval density. The rank of genotypes did not change across different hydroperiods, implying a high genetic correlation that may constrain the evolution of the reaction norm. At high larval density a significant G x E interaction was found, suggesting the potential for the evolution of the reaction norm. A sibship (#1) attained the presumed “optimal” reaction norm by accelerating developmental rate in short duration ponds and delaying it in longer ponds. This could be translated in fitness by an increment in metamorphic survival and size at metamorphosis in short and long ponds respectively with respect to non-plastic sibships. However, genetic variability for plasticity suggests that optimal reaction norm for developmental rates may be variable and hard to achieve in the heterogeneous pond environment. Mass at metamorphosis was not plastic across different pond durations but decreased at high larval density. Significant adaptive plasticity for growth rates appeared in environments that differed drastically in level of crowding conditions, both in the field and in the laboratory. The fact that survival of juveniles metamorphosed at high density ponds was a monotonic function of metamorphic size, implies that response to selection may occur in this population of natterjacks and that genetic variability in plasticity may be a reliable mechanism maintaining adaptive genetic variation in growth rates in the highly variable pond environment.     

Mosquito female response to the presence of larvivorous fish does not match threat to larvae

1. Several species with complex life‐history traits such as amphibians and insects with aquatic immature stages and terrestrial adults avoid ovipositing in pools containing larvivorous fish. This avoidance response was assumed to be a general one for most fish species. 2. The generality of ovipositing Culex to the presence of three, widespread larvivorous fish species was tested in a set of field experiments with artificial oviposition pools using caged fish. 3. Larval performance was further examined under actual predation by these three fish species. 4. Results show that ovipositing females responded strongly to the presence of caged mosquitofish, Gambusia affinis, while showing no significant response to the presence of caged green sunfish, Lepomis cyanellus, or the pirate perch, Aphredoderus sayanus. All three fish species consumed similar amounts of larvae. 5. This is the first example of species‐specific response differences to predators during mosquito oviposition habitat selection. These results point to the existence of predator‐released kairomones affecting mosquito behaviour. These kairomones may either be species‐specific or vary in concentration among fish, and probably have an important role in the understanding of mosquito spatial distribution.     

Preliminary experiments on resource competition between a migrating and a non-migrating clone of the hybrid D. galeata×hyalina

Competition experiments between two clones of thehybrid D. galeata × hyalina differing invertical migration behaviour were carried out in thelaboratory, in a set-up which separated the clonesspatially. The influence of fish kairomones,artificial predation and the imitation of dielvertical migration circumstances were investigated. Inthe presence of fish kairomones, the non-migratingclone outnumbered the migrating one. The introductionof artificial predation reduced this effect in such away that the migrating clone had a competitiveadvantage over the non-migrating clone. It wasconcluded that competition results do not contradictlife history studies performed with the same twoclones, since the presence of fish kairomones enhancesthe reproduction of the non-migrating clone more thanthat of the migrating one.     

A comparative study of phenotypic traits related to resource utilization in anuran communities

Larval anuran communities vary along a gradient of pond permanency. The families Hylidae, Ranidae, and Bufonidae have each diversified into multiple pond types. Species using ponds that dry seasonally (vernal ponds) must compete well to metamorphose before pond drying, while permanent ponds, which contain more predators, produce weaker selection for competitive ability. Quantifying phenotypic traits related to resource acquisition in 14 anuran species provides insight into the mechanistic underpinnings of adaptive radiation in anuran lineages. Under controlled laboratory conditions and at both early and late developmental stages, relative growth rate, relative consumption rate, assimilation efficiency and production efficiency varied significantly among species. As predicted, vernal pond species had high growth rates relative to species using more than one pond type. However, within a pond type, families frequently differed in phenotype. In species using permanent ponds with fish predators, hylids had high growth rates while ranids had low growth rates, and in species using vernal ponds, bufonids had higher assimilation efficiencies than hylids. Differences also occurred between stages; hylids and ranids in permanent, but fishless, ponds were similar at an early stage, but late stage hylids in the same pond type had lower growth and consumption rates, and higher assimilation efficiencies than ranids. Functional relationships between phenotypic traits also differed among species and developmental stage. Negative correlations between evolutionary change (independent contrast values) in both mass and growth rate (both stages), and mass and consumption rate (late stage), suggest the presence of trade-offs. These results indicate that different lineages have diversified in different ways into the same pond types.     

The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

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Molecular diversity of the methanotrophic bacteria communities associated with disused tin-mining ponds in Kampar,Perak, Malaysia

In a previous study, notable differences of several physicochemical properties, as well as the community structure of ammonia oxidizing bacteria as judged by 16S rRNA gene analysis, were observed among several disused tin-mining ponds located in the town of Kampar, Malaysia. These variations were associated with the presence of aquatic vegetation as well as past secondary activities that occurred at the ponds. Here, methane oxidizing bacteria (MOB), which are direct participants in the nutrient cycles of aquatic environments and biological indicators of environmental variations, have been characterised via analysis of pmoA functional genes in the same environments. The MOB communities associated with disused tin-mining ponds that were exposed to varying secondary activities were examined in comparison to those in ponds that were left to nature. Comparing the sequence and phylogenetic analysis of the pmoA clone libraries at the different ponds (idle, lotus-cultivated and post-aquaculture), we found pmoA genes indicating the presence of type I and type II MOB at all study sites, but type Ib sequences affiliated with the Methylococcus/Methylocaldum lineage were most ubiquitous (46.7 % of clones). Based on rarefaction analysis and diversity indices, the disused mining pond with lotus culture was observed to harbor the highest richness of MOB. However, varying secondary activity or sample type did not show a strong variation in community patterns as compared to the ammonia oxidizers in our previous study.     

Contrasting growth strategies of pond versus marine populations of nine-spined stickleback (Pungitius pungitius): a combined effect of predation and competition?

Gigantism in isolated ponds in the absence of sympatric fish species has previously been observed in nine-spined sticklebacks (Pungitius pungitius). Patterns in sexual size dimorphism suggested that fecundity selection acting on females might be responsible for the phenomenon. However, the growth strategy behind gigantism in pond sticklebacks has not been studied yet. Here, we compared von Bertalanffy growth parameters of four independent nine-spined stickleback populations reared in a common laboratory environment: two coastal marine (typical size) and two pond (giant size) populations. We found that both pond populations had larger estimated final size than marine populations, which in turn exhibited higher intrinsic growth rates than the pond populations. Female growth strategies were more divergent among marine and pond populations than those of males. Asymptotic body size and intrinsic growth rate were strongly negatively correlated. Hence, pond versus marine populations exhibited different growth strategies along a continuum. Our data suggest that quick maturation—even with the cost of being small (low fecundity)—is favoured in marine environments. On the contrary, growth to a giant final size (high fecundity)—even if it entails extended growth period—is favoured in ponds. We suggest that the absence (ponds) versus presence (marine environment) of sympatric predatory fish species, and the consequent change in the importance of intraspecific competition are responsible for the divergence in growth strategies. The sex-dependence of the patterns further emphasizes the role of females in the body size divergence in the species. Possible alternative hypotheses are also discussed.     

Does trimethylamine induce life-history reactions in Daphnia?

Laboratory experiments were carried out to investigate life-history reactions of Daphnia to trimethylamine (TMA), a substance, which has recently been found to induce a similar phototactic reaction in Daphnia as fish kairomones. The effects of different treatments (control, fish kairomone and TMA) on the life-history traits of five clones of D. magna and one clone of D. galeata and D. hyalina, respectively, were studied. Only D. magna exhibited significant reactions to TMA and to fish kairomone. D. galeata showed no significant responses to either TMA or to fish kairomone. D. hyalina reacted to the fish treatment with two traits (size and number of eggs at maturity). The comparison of the reaction norms to TMA and fish kairomone demonstrated that the directions of some responses to both factors were similar but were different for others such as for size at maturity. TMA resulted in a larger size at maturity in D. magna, whereas fish kairomone had no significant influence on this trait. We, therefore, conclude that trimethylamine is not the primary causative chemical agent in fish induced life-history adaptations in Daphnia.     

Population structure and genetic diversity of the threatened pygmy newt Triturus pygmaeus in a network of natural and artificial ponds

Pond physical characteristics (connectivity, hydroperiod) have shown to be highly relevant in explaining species presence, reproductive success, and survival in breeding-pond amphibians. However, few studies have addressed the influence that these factors may have on the genetic variability of pond populations. We examined genetic variation at 11 microsatellite loci in Iberian endemic, the pygmy newt (Triturus pygmaeus), from 58 breeding ponds in the Doñana National Park (Andalusia), including both temporary ponds and artificially deepened ponds that remain wet during the whole year. Temporary ponds are located in the North part of the region where the surrounding habitat-wet meadows-facilitates the connectivity among populations, whereas the deepest ponds (‘zacallones’) are located in the southern edge embedded in a matrix of unsuitable habitat (thickets and dry underbrush). We investigated genetic diversity and structure within and among ponds. Our results show that both regions (Doñana-North and Doñana-South) are well-differentiated and form two main clusters. We found higher genetic diversity within ponds from the North region, which also exhibited a higher degree of genetic admixture in comparison with populations from the southern edge. Although we found an isolation-by-distance pattern within each cluster, it arose due to the effect of a few isolated ponds located on the edge of each zone, suggesting the existence of substantial gene flow between ponds in the core area. According to our findings, landscape’s permeability to movement (pond connectivity) may constitute a more important factor than hydroperiod length in determining the genetic diversity and viability of pygmy newt populations in this area. Although Doñana populations show a good state, more peripheral and isolated populations present a more worrisome condition as a result of fragmentation and thus, require conservation efforts. Our study provides key insights that could help guide management practices of this threatened and poorly-studied salamander.