Initiation of Batrachochytrium dendrobatidis infection in the absence of physical contact with infected hosts – a field study in a high altitude lake

Understanding transmission is a critical prerequisite for predicting disease dynamics and impacts on host populations. It is well established that Batrachochytrium dendrobatidis (Bd), the amphibian fungal pathogen responsible for chytridiomycosis, can be transmitted directly, through physical contact with an infected host. However, indirect pathways of transmission remain poorly investigated. We conducted a five‐week long field infection experiment at a high altitude mountain lake in the French Pyrenees to investigate Bd transmission pathways in larval midwife toads Alytes obstetricans. Uninfected naïve tadpoles were co‐housed either with infected tadpoles (direct and indirect transmission) or with uninfected ones (indirect transmission only). We found that physical contact with an infected host is not necessary for initial infection with Bd and that all tadpoles became infected after only four weeks. However, physical contact with infected tadpoles led to a faster spread within a tadpole group and resulted in higher Bd loads and subsequently higher mortality. Our findings clearly demonstrate that in A. obstetricans, Bd can quickly spread in a population even without physical contact. Our experiment therefore stresses the importance of indirect transmission of Bd zoospores in infected lakes for disease dynamics, especially when a reservoir species such as A. obstetricans is present.     

Discovery of a Novel Alveolate Pathogen Affecting Southern Leopard Frogs in Georgia: Description of the Disease and Host Effects

In April of 2006, we observed southern leopard frog (Rana sphenocephala) tadpoles in a pond in northeast Georgia that were dying from an unknown pathogen. Examination of affected specimens, as well as PCR characterization, revealed that all were infected with a novel alveolate pathogen closely related to freshwater and marine eukaryotic organisms and, to a lesser degree, to members of the genus Perkinsus. This pathogen has been documented in numerous mortality events in anuran tadpoles in the United States, although it has not yet been named nor clearly described. We subsequently conducted a systematic survey of this and four other ponds in the same area to document the extent of the pathogen and to describe the nature of infections in leopard frog tadpoles. Of 87 live tadpoles examined, 25% were infected with the alveolate pathogen, based on visual inspection of tadpole liver tissue. Affected tadpoles frequently had enlarged abdomens, swam erratically, and could be captured by hand. All organs of infected tadpoles were infiltrated but typically to a lesser extent than the liver and kidneys, which often had hundreds of thousands of the spherical, 6-μm organisms. Infected tadpoles tended to weigh more than noninfected ones, likely due to the massive organ swelling that coincided with infections. Infected tadpoles did not differ in developmental stage from noninfected tadpoles. Infection prevalence varied widely among ponds, and in one pond, we witnessed a rapid die-off of R. spenocephala tadpoles during our surveys, although we did find infected metamorphic frogs. The rapid mortality we observed as well as the vast number of organisms seen in specimens suggests that this pathogen has tremendous transmission potential, and therefore deserves further monitoring and study.     

The effects of cannibalism on Amazonian poison frog egg and tadpole deposition and survivorship in Heliconia axil pools

This study investigated the influence of cannibalism on egg and larval mortality, and on the deposition strategies of adults, in a tropical anuran breeding in very small leaf axil pools. Patterns of egg and tadpole deposition and mortality in the Amazonian poison frog, Dendrobates ventrimaculatus, were monitored in rainforest near Pompeya in Sucumbios Province, Ecuador. Oviposition and tadpole deposition typically ocurred in leaf axils of Heliconia plants. Pools typically received more than one oviposition. Egg survivorship was low, and significantly lower when eggs were deposited in pools with large tadpoles, indicating that cannibalism is an important source of mortality. Tadpole survivorship was also associated with the presence of other tadpoles: most pools ended with only one surviving tadpole, regardless of the number of tadpoles deposited in the pool. Egg deposition was signifcantly less likely for pools that had a tadpole in them, suggesting that adults can detect the presence of tadpoles and avoid ovipositing in pools that contain them. This hypothesis was tested with a series of pool choice experiments, which revealed that D. ventrimaculatus avoid placing either eggs or tadpoles into a pool which contains a large tadpole. Several hypotheses which could explain multiple deposition in this species are discussed. Received: 14 September 1998 / Accepted: 25 January 1999     

Breeding habitat selection and larval performance of two anurans in freshwater rock-pools

I studied breeding habitat choice of common toad Bufo bufo and common frog Rana temporaria in 221 freshwater rock-pools on 15 small islands in the southwestern coast of Finland. I monitored tadpole growth rate in a number of rock-pools differing in size, competitors and predator regime. Furthermore, I carried out a short-term field experiment to investigate the effects of different predators on larval survival. Rana bred in pools of virtually all sizes, although the very smallest ones were usually avoided. A logistic regression analysis showed that the amount of aquatic macrophyte vegetation and pool surface area were the most important pool characters for Rana. Bufo preferred the largest pools, and pool surface area was by far the most important habitat variable. Rana avoided pools with the lowest pH. but was more common than expected at pools with pH around 6. In Bufo such an effect was not found, but this may be due to relatively low number of pools occupied by Bufo. In Rana there was a positive correlation between pool area and tadpole body length in early June, but two weeks later this relationship was not significant. In Bufo tadpole body size was not significantly affected by pool area. Presence of predators or presence of the other tadpole species did not affect growth or tadpole body size in either Rana or Bufo. A short-term experiment in wading pools indicated that both species suffered heavy mortality in the presence of a diving beetle larva. In the presence of predatory fish, mortality of Bufo did not differ from controls, whereas mortality was high among Rana tadpoles. It appears that although predators prey heavily on Rana tadpoles, they do not exclude Rana from larger rock-pools. However, it is not evident from this study why Bufo avoids smaller pools.     

Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism

We describe a novel mutualism between bullfrog tadpoles (Rana catesbeiana) and a tadpole-specific gastrointestinal nematode (Gyrinicola batrachiensis). Groups of tadpoles were inoculated with viable or nonviable nematode eggs, and development, morphology, and gut fermentation activity were compared between nematode-infected and uninfected tadpoles. Nematode infection accelerated tadpole development; the mean time to metamorphosis was 16 d shorter and the range of times to metamorphosis was narrower in nematode-infected tadpoles than in uninfected tadpoles. At metamorphosis, infected and uninfected bullfrogs did not differ in body size or condition. Colon width, wet mass of colon contents, and concentrations of most fermentation byproducts (short-chain fatty acids: SCFAs) in the hindgut were greater in infected tadpoles. Furthermore, in vitro fermentation yields for all SCFAs combined were over twice as high in infected tadpoles than in uninfected tadpoles. One explanation for accelerated development in infected tadpoles is the altered hindgut fermentation associated with the nematodes. Energetic contributions of fermentation were estimated to be 20% and 9% of the total daily energy requirement for infected and uninfected tadpoles, respectively. Infection by G. batrachiensis nematodes potentially confers major ecological and evolutionary advantages to R. catesbeiana tadpoles. The mutualism between these species broadens our understanding of the taxonomic diversity and physiological contributions of fermentative gut symbionts and suggests that nematodes inhabiting the gut regions of other ectothermic herbivores might have beneficial effects in those hosts.     

Impact of sediment and nutrient inputs on growth and survival of tadpoles of the Western Toad

1. Sediment and nutrient loading in freshwater systems are leading causes of aquatic habitat degradation globally. We investigated the impacts of fine-sediment and nutrient additions on the growth and survival of western toad ( Bufo boreas ) tadpoles and emergent metamorphs in mesocosm and exclosure experiments.
2. Mesocosm tanks received weekly pulses of fine sediments to create initial concentrations of 0, 130 and 260 mg L⁻¹ of suspended sediment and either bi-weekly additions of nutrients (N = 160 μg L⁻¹, P = 10 μg L⁻¹) or no additions in a factorial design. Within mesocosms, tadpole exclosures allowed for quantification of tadpole grazing pressure on periphyton biomass, chlorophyll- a and sediment deposition.
3. Tadpoles receiving sediment additions experienced slower growth rates and reduced survival to metamorphosis, although no effects of treatment were detected on size at metamorphosis or time to metamorphosis. Nutrient additions also lowered survival, but had no impact on other measured parameters of tadpole fitness. Dissections and gut content analysis revealed that tadpoles ingested sediment in large quantities altering the proportion of the organic content of ingested food.
4. Together these results suggest that although sediment was readily consumed by tadpoles, its presence in the larval environment had an overall negative effect on tadpole growth and survival, although not as severe as predicted.     

Effects of predator interactions, prey palatability and habitat structure on survival of natterjack toad Bufo calamita larvae in replicated semi-natural ponds

The significance of predation and aquatic habitat structures to the survivorship of natterjack toad Bufo calamita larvae was investigated by manipulating predator numbers and pond characteristics in a series of replicated semi-natural pools over three consecutive years Two species of fish (common carp Cyprinus carpio and perch Perca fluviatilis) increased the survival of small tadpoles severalfold by selectively consuming predatory invertebrates, but a third species of fish (rudd Scardinius erythrophthalmus) devoured tadpoles and invertebrates indiscriminately Survival of larger tadpoles later in larval development was less affected by the reduction of invertebrate predation pressure from carp and perch, probably because abiotic factors (pond desiccation and anoxia) were stronger agents of tadpole mortality In ponds of low pH (ca 4 5) there was greatly increased spawn mortality and reduced tadpole growth rates but no significant change in tadpole predation compared with circumneutral controls Neutralisation of acid ponds to pH 7 by addition of Ca(OH)₂ restored spawn viability and tadpole growth rates to control levels without affecting predation level Addition of organic nutrients stimulated tadpole growth rates significantly m ohgotrophic ponds but not sufficiently to improve survival of small larvae in the face of predation Extensive growths of macrophytes increased predator numbers up to more than twofold but effects on tadpole mortality rates differed between experiments Replacement of natural substrates by concrete basins substantially increased tadpole survival throughout development, probably because both predation by invertebrates and abiotic mortality factors were ameliorated Predation was a strong force early in natterjack tadpole development irrespective of chemical and biological conditions within ponds, but became much less important compared with abiotic factors as an agent of mortality at later tunes     

The combined influence of trematode parasites and predatory salamanders on wood frog (<Emphasis Type="Italic">Rana sylvatica</Emphasis>) tadpoles

Predators can have important impacts on host–parasite dynamics. For many directly transmitted parasites, predators can reduce transmission by removing the most heavily infected individuals from the population. Less is known about how predators might influence parasite dynamics in systems where the parasite relies on vectors or multiple host species to complete their life cycles. Digenetic trematodes are parasitic flatworms with complex life cycles typically involving three host species. They are common parasites in freshwater systems containing aquatic snails, which serve as obligate first intermediate hosts, and multiple trematode species use amphibians as second intermediate hosts. We experimentally examined the impact of predatory salamanders (Ambystoma jeffersonianum) and trematode parasites (Echinostoma trivolvis and Ribeiroia ondatrae) on short-term survival of wood frog tadpoles (Rana sylvatica) in 150-L outdoor pools. Two trematode species were used in experiments because field surveys indicated the presence of both species at our primary study site. Parasites and predators both significantly reduced tadpole survival in outdoor pools; after 6 days, tadpole survival was reduced from 100% in control pools to a mean of 46% in pools containing just parasites and a mean of 49% in pools containing just predators. In pools containing both infected snails and predators, tadpole survival was further reduced to a mean of 5%, a clear risk-enhancement or synergism. These dramatic results suggest that predators may alter transmission dynamics of trematodes in natural systems, and that a complete understanding of host–parasite interactions requires studying these interactions within the ecological framework of community interactions.     

The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Natural Stressors and Ranavirus Susceptibility in Larval Wood Frogs (Rana sylvatica)

Chronic exposure to stressors has been shown to suppress immune function in vertebrates, making them more susceptible to pathogens. It is less clear, however, whether many natural stressors are immunosuppressive. Moreover, whether stressors make disease more likely or more severe in populations is unclear because animals respond to stressors both behaviorally and physiologically. We tested whether chronic exposure to three natural stressors of wood frog tadpoles—high-densities, predator-cues, and low-food conditions—influence their susceptibility to a lethal ranavirus both individually in laboratory experiments, and collectively in outdoor mesocosms. Prior to virus exposure, we observed elevated corticosterone only in low-food treatments, although other treatments altered rates of growth and development as well as tadpole behavior. None of the treatments, however, increased susceptibility to ranavirus as measured by the proportion of tadpoles that became infected or died, or the time to death compared to controls. In fact, mortality in the mesocosms was actually lower in the high-density treatment even though most individuals became infected, largely because of increased rates of metamorphosis. Overall we find no support for the hypothesis that chronic exposure to common, ecologically relevant challenges necessarily elevates corticosterone levels in a population or leads to more severe ranaviral disease or epidemics. Conditions may, however, conspire to make ranavirus infection more common in metamorphosing amphibians.     

Factors influencing tadpole deposition site choice in a frog with male parental care: An experimental field study

Parents have evolved a variety of strategies to minimize risks to their offspring, including complex choices regarding suitable rearing sites, based on abiotic and biotic factors, which differentially affect offspring survival. Because availability and quality of these sites are variable, parents may have to choose between immediately available lower‐quality rearing sites or extended search time. In some frog species with larval transport, parents are known to select bodies of water that are free of predators, cannibalistic tadpoles, or intraspecific competitors for larval deposition and rearing sites. We tested whether abiotic factors and the presence of predators and conspecific tadpoles affect tadpole deposition behavior in a population of smooth guardian frog, Limnonectes palavanensis, on the island of Borneo. Females lay eggs on land and males guard them until they hatch; after hatching, tadpoles climb onto the male's back and are subsequently transported to small pools of water on the forest floor, which are scarce and patchily distributed. We estimated the abundance of natural tadpole rearing sites in our study area and conducted experiments using artificial pools to test whether abiotic characteristics of these pools affect the probability of larval deposition. We also performed choice experiments to test whether males of L. palavanensis avoid pools with conspecific tadpoles or predators. Lastly, we tested whether the tadpoles of this species exhibit cannibalism. The abundance of natural deposition sites was low, and males readily used artificial pools for tadpole deposition. Males were less likely to deposit tadpoles in artificial pools located in steep areas, and males did not avoid depositing tadpoles in pools with conspecifics or with experimentally introduced predators. Males exhibited clutch‐partitioning behavior, dividing tadpoles between adjacent artificial pools. Pool availability, rather than the presence of potential competitors or predators in a pool, affects tadpole deposition decisions in this species.     

Relationships among size, development, and Batrachochytrium dendrobatidis infection in African tadpoles

The fungal pathogen Batrachochytrium dendrobatidis contributes to the global decline of amphibians. Although mortality from B. dendrobatidis infections occurs primarily in postmetamorphic individuals, infected tadpoles may suffer reduced growth and developmental rates as a result of oral chytridiomycosis, possibly affecting adult fitness. We conducted a field study in which we examined South African tadpoles for oral chytridiomycosis and compared the body sizes of infected and uninfected individuals of 2 species, Heleophryne natalensis and Strongylopus hymenopus. Presence of B. dendrobatidis was determined by microscopic inspection of mouthparts. Infection prevalence was high in both species, 62.5 and 38.6%, respectively, and infected individuals were significantly larger in both species. The inclusion of developmental stage in the analysis of S. hymenopus body size eliminated the relationship between body size and infection status, suggesting that differences in body size were not due to differences in growth, but to differences in developmental stage of infected larvae. These results suggest that larvae at more advanced developmental stages are more likely to be infected with B. dendrobatidis and that infection in larval amphibians may be dependent on time or developmental status of larvae. Contrary to the results of past studies, there was no evidence that oral chytridiomycosis resulted in decreased growth of tadpoles, despite the occurrence of oral abnormalities in infected individuals of 1 species. Because tadpole performance can subsequently affect the health of anuran populations and because tadpoles can act as reservoirs of infection, the study of B. dendrobatidis in larval amphibians is important to understanding the effects of this emerging disease.     

Trophic roles of tadpoles in tropical Australian streams

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Frog virus 3 prevalence in tadpole populations inhabiting cattle-access and non-access wetlands in Tennessee, USA

Ranaviruses have been associated with most of the reported larval anuran die-offs in the United States. It is hypothesized that anthropogenically induced stress may increase pathogen prevalence in amphibian populations by compromising immunity. Cattle use of wetlands may stress resident tadpole populations by reducing water quality. We isolated a Ranavirus from green frog Rana clamitans (n = 80) and American bullfrog R. catesbeiana (n = 104) tadpoles collected at 5 cattle-access and 3 non-access wetlands on the Cumberland Plateau, Tennessee, USA. Sequencing confirmed Frog virus 3 (FV3); therefore, we compared its prevalence between tadpole populations inhabiting cattle-access and non-access wetlands, and among 3 seasons (winter, summer, and autumn) in 2005. We found FV3 in both tadpole species and cattle land-use types; however, prevalence of FV3 was greater in green frog tadpoles residing in cattle-access wetlands compared to those in non-access wetlands. No difference in FV3 prevalence was detected between cattle land uses for American bullfrog tadpoles. A seasonal trend in FV3 prevalence also existed, with prevalence greater in autumn and winter than in summer for both species. In addition, we found that FV3 prevalence decreased significantly as Gosner stage increased in American bullfrog tadpoles. No trend was detected between FV3 prevalence and developmental stage for green frog tadpoles. Our results suggest that cattle use of wetlands may increase prevalence of FV3 in Rana tadpoles, although this effect may depend on species, season, and tadpole developmental stage.     

Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages

Chytridiomycosis is an emerging infectious disease caused by the chytrid fungus Batrachochytrium dendrobatidis, which has been implicated in amphibian declines worldwide. The mountain yellow-legged frog Rana muscosa is a declining amphibian species that can be infected by B. dendrobatidis; however, transmission between conspecifics has not been documented. Here, we present experimental evidence that R. muscosa tadpoles can be infected by fungal zoospores and that they can transmit infection to each other and to postmetamorphic animals. We compared several techniques for detecting B. dendrobatidis transmission and found that histology with serial sectioning was able to detect infection before cytology or visual inspections. We also show that R. muscosa tadpoles appear healthy with B. dendrobatidis infection, while postmetamorphic animals experience mortality. In addition, we provide guidelines for visually detecting B. dendrobatidis in R. muscosa tadpoles, which may be useful in other affected species. Field surveys of infected and uninfected populations verify this identification technique.     

The thermal environment of arboreal pools and its effects on the metabolism of the arboreal, oophagous tadpoles of a Taiwanese tree frog, Chirixalus eiffingeri (Anura: Rhacophoridae).

We have studied seasonal and diurnal fluctuations of water temperature in bamboo stumps and the effect of temperature on the energy metabolism of arboreal, oophagous tadpoles of Chirixalus eiffingeri. We collected tadpoles (Gosner stage 28-29) in February and August from Chitou, Taiwan and acclimated them to 12 and 22 degrees C. Using a closed system, we measured tadpole oxygen consumption (V.O(2)) at 12, 17 and 22 degrees C. The water temperature was lowest in February (11-13 degrees C), increased rapidly during March and April and was highest from May to August (20-24 degrees C). Diel fluctuations in the temperature of the pools of water in bamboo stumps mirrored fluctuations in air temperature. Tadpoles collected in February and August exhibited metabolic compensation in that tadpoles acclimated at 12 degrees C had significantly higher V.O(2) than those acclimated at 22 degrees C. There are at least two possible explanations for the presence of metabolic compensation in C. eiffingeri tadpoles. Firstly, the larval period of C. eiffingeri ranges from 40 to 78 days, a tadpole could experience relatively large fluctuations in body temperature (up to 10 degrees C) during the development. As a result, C. eiffingeri tadpoles most likely evolved metabolic compensation to maintain activity levels under different thermal environments. Secondly, because arboreal pools are small, thermally unstratified, aquatic microhabitats, tadpoles are unable to behaviorally select preferred temperatures. As a result, metabolic compensation allows tadpoles to regulate their physiological functions.     

Predation and disease: understanding the effects of predators at several trophic levels on pathogen transmission

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The Reproductive Biology and Larvae of the First Tadpole-Bearing Frog,Limnonectes larvaepartus

Most of the reproductive modes of frogs include an exotrophic tadpole, but a number of taxa have some form of endotrophic development that lacks a feeding tadpole stage. The dicroglossid frog genus Limnonectes ranges from China south into Indonesia. The breeding biologies of the approximately 60 described species display an unusual diversity that range from exotrophic tadpoles to endotrophic development in terrestrial nests. There have been mentions of oviductal production of typical, exotrophic tadpoles in an undescribed species of Limnonectes from Sulawesi, Indonesia. Here we examine newly collected specimens of this species, now described as L. larvaepartus and present the first substantial report on this unique breeding mode. Typical exotrophic tadpoles that are retained to an advanced developmental stage in the oviducts of a female frog are birthed into slow-flowing streams or small, non-flowing pools adjacent to the streams.     

Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival

The effect of echinostome infections on the survival of Rana pipiens tadpoles was examined in relation to developmental stage of tadpoles. Individual tadpoles of Gosner stages 25, 27, 32-33, and 37-39 were exposed to 1 of 4 levels of cercariae (0, 20, 50, or 100). Only tadpoles at stage 25, the earliest stage infected, died within a 5-day experimental period. This stage-specific mortality rate could be explained, in part, by the stage-specific location of encystment of cercariae, which was documented in a separate experiment. In accordance with kidney development, cercariae predominately encysted in the pronephroi during early stages of tadpole development (stages 25 through 31-32) and only in the mesonephroi and associated ducts at later stages (stages 37 through 46). As the mesonephros develops, renal capacity presumably increases. Thus, tadpoles died only when metacercariae concentrated in the functional portion of the kidney with the most limited renal capacity. As tadpoles aged, they also became less susceptible to infections. On average, 69.5% of cercariae that were exposed to stage 25-26 tadpoles successfully encysted. compared with only 8.4% of cercariae exposed to stage 37-38 tadpoles. Exposures of metamorphic frogs (poststage 46) to cercariae revealed that these individuals can become infected with echinostomes. Collectively, our data highlight the host stage-dependent dynamics of tadpole-echinostome interactions.     

Tadpole mortality varies across experimental venues: do laboratory populations predict responses in nature?

Laboratory experiments are widely used to study how populations in nature might respond to various biological interactions, but the relevance of experiments in artificial venues is not known. We compiled mortality and growth data from 424 anuran populations carried out under laboratory, mesocosm, field enclosure, and field settings to determine if major differences exist amongst experimental venues and how this might influence experimental responses of tadpoles amongst venues. Our results show that there are fundamental differences in survival amongst venues, with the highest mortality occurring in field populations and the lowest in laboratory populations. Separation of mesocosm and field enclosure data based on the possibility of predatory interactions indicates that predation is an important factor leading to increased mortality in natural populations. Comparisons of size distributions across venues (although size data were limited for field populations) suggest that variation in tadpole size is low in natural populations compared to populations in artificial venues. We infer from this that mortality has a homogenizing effect on size in nature, resulting in natural populations that are not a random sample of hatched individuals. This finding suggests that populations reared under controlled laboratory conditions in the absence of predation (and other selective pressures) may not be representative of natural populations.