Tadpole Performance Research Articles

Fixation of deleterious mutations in clonal lineages: evidence from hybridogenetic frogs.

The hemiclonal waterfrog Rana esculenta (RL genotype), a bisexual hybrid between R. ridibunda (RR) and R. lessonae (LL), eliminates the L genome from its germline and clonally transmits the R genome (hybridogenesis). Matings between hybrids produce R. ridibunda offspring, but they generally die at an early larval stage. Mortality may be due to fixed recessive deleterious mutations in the clonally inherited R genomes that were either acquired through the advance of Muller's ratchet or else frozen in these genomes at hemiclone formation. From this hypothesis results a straightforward prediction: Matings between different hemiclones, that is, between R. esculenta possessing different R genomes of independent origin, should produce viable R. ridibunda offspring because it is unlikely that different clonal lineages have become fixed for the same mutations. I tested this prediction by comparing survival and larval performance of tadpoles from within- and between-population crossings using R. esculenta from Seseglio (Se) in southern, Alpnach (Al) in central, and Elliker Auen (El) in northern Switzerland, respectively. Se is isolated from the other populations by the Alps. Enzyme electrophoresis revealed that parents from Se belonged to a single hemiclone that was different from all hemiclones found north of the Alps. Parents from Al also belonged to one hemiclone, but parents from El belonged to three hemiclones, one of which was indistinguishable from the one in Al. Rana esculenta from Se produced inviable tadpoles when crossed with other hybrids of their own population, but when crossed with R. esculenta from Al and El, tadpoles successfully completed metamorphosis, supporting the hypothesis I tested. Within-population crosses from Al were also inviable, but some within-population crosses from El, where three hemiclones were present, produced viable offspring. Only part of the crosses between Al and El were viable, but there was no consistent relationship between hemiclone combination and tadpole survival. When backcrossed with the parental species R. ridibunda, hybrids from all source populations produced viable offspring. Performance of these tadpoles with a sexual and a clonal genome was comparable to that of normal, sexually produced R. ridibunda tadpoles. Thus, in the heterozygous state, the deleterious mutations on the clonal R genomes did not appear to reduce tadpole fitness.

FIXATION OF DELETERIOUS MUTATIONS IN CLONAL LINEAGES: EVIDENCE FROM HYBRIDOGENETIC FROGS

The hemiclonal waterfrog Rana esculenta (RL genotype), a bisexual hybrid between R. ridibunda (RR) and R. lessonae (LL), eliminates the L genome from its germline and clonally transmits the R genome (hybridogenesis). Matings between hybrids produce R. ridibunda offspring, but they generally die at an early larval stage. Mortality may be due to fixed recessive deleterious mutations in the clonally inherited R genomes that were either acquired through the advance of Muller's ratchet or else frozen in these genomes at hemiclone formation. From this hypothesis results a straightforward prediction: Matings between different hemiclones, that is, between R. esculenta possessing different R genomes of independent origin, should produce viable R. ridibunda offspring because it is unlikely that different clonal lineages have become fixed for the same mutations. I tested this prediction by comparing survival and larval performance of tadpoles from within- and between-population crossings using R. esculenta from Seseglio (Se) in southern, Alpnach (Al) in central, and Elliker Auen (El) in northern Switzerland, respectively. Se is isolated from the other populations by the Alps. Enzyme electrophoresis revealed that parents from Se belonged to a single hemiclone that was different from all hemiclones found north of the Alps. Parents from Al also belonged to one hemiclone, but parents from El belonged to three hemiclones, one of which was indistinguishable from the one in Al. Rana esculenta from Se produced inviable tadpoles when crossed with other hybrids of their own population, but when crossed with R. esculenta from Al and El, tadpoles successfully completed metamorphosis, supporting the hypothesis I tested. Within-population crosses from Al were also inviable, but some within-population crosses from El, where three hemiclones were present, produced viable offspring. Only part of the crosses between Al and El were viable, but there was no consistent relationship between hemiclone combination and tadpole survival. When backcrossed with the parental species R. ridibunda, hybrids from all source populations produced viable offspring. Performance of these tadpoles with a sexual and a clonal genome was comparable to that of normal, sexually produced R. ridibunda tadpoles. Thus, in the heterozygous state, the deleterious mutations on the clonal R genomes did not appear to reduce tadpole fitness.Corresponding Editor: J. Merilä

Effect of ontogenetic increases in body size on burst swimming performance in tadpoles of the striped marsh frog, Limnodynastes peronii.

The effect of ontogenetic increases in total length on burst swimming performance was investigated in tadpoles of the striped marsh frog (Limnodynastes peronii) over the total-length range of 1. 5-4 cm and Gosner developmental stages 25-38. The burst swimming performance of tadpoles at 10 degrees and 24 degrees C was determined by videotaping startle responses with a high-speed video camera at 200 Hz and analysing the sequences frame by frame. Maximum swimming velocity (Umax) and acceleration (Amax) increased with total length (L) at a rate that was proportionally greater than the increase in total length (i.e., positive allometry; exponents >1) and was described by the allometric equations Umax=0.061L1.34 and Amax=1.15L1.11 at 10 degrees C and Umax=0.114L1.34 and Amax=1.54L1. 11 at 24 degrees C. Stride length increased with a total-length exponent of approximately 1 but was unaffected by temperature. Tail-beat frequency was not affected by total length and increased from 7.8+/-0.2 Hz at 10 degrees C to 21.7+/-0.7 Hz at 24 degrees C. Developmental stage did not significantly influence the relationship between total length and Umax or Amax. Furthermore, temperature and the associated changes in water viscosity did not affect the relationship between total length and burst swimming performance. At their Umax, Reynolds numbers ranged from approximately 1,500 in the smaller tadpoles up to 50,000 for the larger animals at 24 degrees C. We suggest the positive allometry of Umax in larval L. peronii was due in part to the increases in tail width (TW) with total length (TW=-1.36L1.66), possibly reflecting the increasing importance of burst swimming performance to survival during larval development.

Effects of fish chemical cues on the interactions between tadpoles and crayfish

We studied the effects of predatory crayfish (Pacifastacus leniusculus), the non‐lethal effects of fish chemical cues (Oncorhynchus mykiss), and the combined effects of crayfish and fish chemical cues on the performance of tadpoles of two co‐existing anuran species, Rana temporaria and Bufo bufo, in experimental pools. We also examined grazing effects on periphyton, the main food source for the tadpoles. Crayfish significantly reduced tadpole survival, particularly by feeding on Bufo. Rana benefited from reduced numbers of competitors, resulting from crayfish predation, by increased growth rate, whereas the growth rate of Bufo was unaffected by crayfish. The proportion of Rana in refuges (in relation to the number of survivors at the end of the experiment) was unaffected by crayfish, whereas proportionally more Bufo stayed in refuges in the presence of crayfish, relative to controls. Fish cues had no effect on tadpole survival of either species. During the entire larval period, Rana responded to fish cues by increasing the use of refuges relative to controls, whereas Bufo did not show any significant behavioural response to fish cues. In accordance with these observations, the proportion of Rana in refuges at the end of the experiment was high in the presence of fish cues, whereas the use of refuges by Bufo was not affected by fish cues. Predatory crayfish and fish chemical cues had additive effects on tadpole survival, growth and refuge use. Tadpoles in all treatments reduced periphyton biomass. Both crayfish and fish cues had positive indirect effects on periphyton biomass. The positive indirect effect of fish cues on periphyton was likely an effect of reduced grazing from Rana. Thus lethal, as well as non‐lethal, predator effects on prey populations can influence lower trophic levels.

The effect of social interactions on tadpole activity and growth in the British anuran amphibians (Bufo bufo, B. calamita, and Rana temporaria)

AbstractTadpoles of different species of frogs and toads display different tendencies to aggregate. We investigated some of the costs and benefits of aggregating in three British species by examining their behavioural responses to the presence of conspecifics, and by monitoring the performance of tadpoles under different levels of social interaction with other individuals. The common toad (Bufo bufo), an aggregating species, displayed higher levels of activity than the natterjack toad (B. calamita) and common frog (Rana temporaria), two species that form aggregations less frequently. Moreover, out of the three species, only B. bufo increased activity in the presence of conspecifics. In all three species, increased interaction between individuals resulted in increased variation in size. However, average growth rate was affected only in B. bufo, which grew faster when raised in isolation and not interacting with other individuals. Under certain conditions intraspecific competition therefore seems to be more important than social facilitation, but may lead to average size at metamorphosis being larger within the population. The consequences of intraspecific competition within aggregations may therefore be different for individuals and populations.

Effects of cover and predator size on survival and development of Ranautricularia tadpoles.

Size-limited predation is an important process during the development of many aquatic species, and mortality rates of early larval stages and small individuals can be particularly high. Structurally complex habitats can mediate predator-prey interactions and provide a potentially important mechanism for decreasing predation pressure on larvae. To determine whether structurally complex habitats mediate predation on tadpoles of the southern leopard frog (Ranautricularia), we designed a factorial experiment, crossing two levels of cover with three predator treatments (none, small, or large Trameacarolina naiads). Predator size had a larger effect on tadpole performance (survival, mass and age at metamorphosis) than did cover level, largely because small predators were ineffective. Within the large-predator treatment, however, tadpole survival was higher (78%) under high than under low cover (46%), suggesting that increased cover decreased predator foraging efficiency allowing more larvae to reach a size refuge. This study demonstrates that habitat structural complexity can play an important role in mediating predator-prey interactions, even when tadpoles start out at a size disadvantage relative to predators. Consideration of habitat structural complexity in future research should provide a more complete understanding of the role of size relationships in predator-prey systems.

Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl

AbstractGeneral activity and swimming performance (i.e., sprint speed and distance) of plains leopard frog tadpoles (Rana blairi) were examined after acute exposure to three sublethal concentrations of carbaryl (3.5, 5.0, and 7.2 mg/L). Both swimming performance and spontaneous swimming activity are important for carrying out life history functions (e.g., growth and development) and for escaping from predators. Measured tadpole activity diminished by nearly 90% at 3.5 mg/L carbaryl and completely ceased at 7.2 mg/L. Sprint speed and sprint distance also decreased significantly following exposure. Carbaryl affected both swimming performance and activity after just 24 h, suggesting that 24 h may be an adequate length of exposure to determine behavioral effects on tadpoles. Slight recovery of activity levels was noted at 24 and 48 h post‐exposure; no recovery of swimming performance was observed. Reduction in activity and swimming performance may result in increased predation rates and, because activity is closely associated with feeding, may result in slowed growth leading to a failure to emerge before pond drying or an indirect reduction in adult fitness. Acute exposure to sublethal toxicants such as carbaryl may not only affect immediate survival of tadpoles but also impact critical life history functions and generate changes at the local population level.

Effects of pond size and consequent predator density on two species of tadpoles.

Experimental ponds were used as a model system of habitat patches to study the effect of habitat size on the relative growth performance of tadpoles of Bufo americanus and Pseudacris triseriata, and on colonization by predatory insects. Three pond depths and surface areas were habitat size treatments in a replicated, factorial experiment. Tadpoles of both species were astablished together at a single density and ponds were left open to natural colonization by aquatic insects. Pond area had a significant effect on the multivariate response of P. triseriata larval period, survival, and metamorphic mass. P. triseriata survived better relative to B. americanus in larger ponds. However, increasing pond area led to greater incidence of predacious beetle larvae (Dytiscus, Coleoptera: Dytiscidae). Dytiscus larvae had a significant negative effect on the survival of P. triseriata and led to reduced P. triseriata survival relative to B. americanus in colonized ponds. The results suggest that habitat size can influence community structure by altering the distribution of predation among habitat patches.

A Behavioral Trade‐Off and Its Consequences for the Distribution of Pseudacris Treefrog Larvae

Larval chorus frogs (Pseudacris triseriata) and spring peepers (P. crucifer) show marked differences in their distribution patterns, with chorus frogs tending to occur in less permanent ponds containing lower predator densities, and spring peepers tending to occur in more permanent ponds with higher predator densities. In order to understand this pattern I performed experiments at two levels. First, at the community level, I evaluated the importance of competition, predation, and pond permanence for patterns of larval performance. Second, at the behavioral level, I asked whether a hypothesized trade—off between gain and risk underlies ecological interactions, and ultimately, patterns of performance and distribution of these species. I employed a field manipulation to asses the contribution of competition and predation within different ponds that varied in permanence. In order to examine the effect of interspecific competition, enclosures contained each tadpole species either alone or in the presence of an equal density of the other species; these enclosures were placed in two temporary ponds, two intermediate ponds, and two permanent ponds. Tadpole stocking densities reflected local natural densities. This competition treatment was crossed with a predator treatment manipulating the absence or presence of predators (with "presence" representing the naturally occurring density within each pond). Patterns of relative performance were consistent with relative distribution patterns across the pond permanence gradient: chorus frogs performed best relative to spring peepers in temporary ponds while spring peepers performed best relative to chorus frogs in permanent ponds (performance was measured as survivorship and growth). The dominant sources of mortality were pond drying in temporary ponds and predation in more permanent ponds. In contrast to most previous experimental studies of larval anurans, competition had small effects on tadpole performance. Results from the field experiment suggest that pond drying and predation may be important determinants of performance, and that the two species are differentially susceptible to these mortality agents. In a set of laboratory experiments I evaluated the hypothesis that a trade—off between foraging gain and predation risk mediated through activity (proportion of time spent moving) might explain patterns of Pseudacris distribution. In both species, individuals facultatively reduced activity in the present of a caged predator with a corresponding drop in growth rate. In general, larval chorus frogs also tend to be more active and faster growing and developing than spring peepers. These results provide support for the existence of the trade—off and suggest that interspecific differences in activity may contribute to patterns of larval performance and distribution among ponds. The general nature of this trade—off suggests that it may also be important in other systems.

A comparison of the effects of three water-circulation regimes on the aquaculture of bullfrog ( Rana catesbeiana Shaw) tadpoles

A 15-week experiment was conducted with bullfrog ( Rana catesbeiana) tadpoles to determine the effects of three different water management strategies in rearing tanks: static, a daily exchange (100%/day) and a recirculating system (900% exchange rate/day). Survival, growth rate and feeding performance of tadpoles stocked at 3.5 individuals/l were compared among the three treatments. The static system gave the best results in terms of survival (57.9%), percent total weight gain (1803%), daily weight gain (6.919 mg/day) and SGR (2.34%/day), all of which were statistically greater than the corresponding values from the other treatments. The lowest performance was found in tadpoles reared in the recirculating system. These differences are attributed to a supplementary source of nourishment provided by microalgae covering the bottom and walls of rearing tanks of the static system. In recirculating systems, flushing of feed could have been an important component contributing to inadequate nourishment.

Evolutionary consequences of non-random mating: do large males increase offspring fitness in the anuran Bufo bufo?

The purpose of my study was to determine whether male body size, a trait known to be important to mating success, covaries with offspring performance. I tested the effects of male body size on the performance of Bufo bufo tadpoles reared at two food levels by mating large, small, and naturally-mated males to the same females. Survival of tadpoles in the high-food environment was affected by male size class, but in the opposite way to that expected. Tadpoles sired by large males had the lowest survival, and those sired by small males the highest. Neither body size at metamorphosis nor larval period were affected by male size class alone, but male size interacted with the female contribution: tadpoles sired by large males had short larval periods and large size at metamorphosis with some females,but long larval periods and small body sizes with others. Food level had a significant effect on both size at metamorphosis and larval period, and interacted with female contribution, but not male size class. This indicated that female contribution to tadpoles was dependent on food level, but that the effects of male size were not differentially expressed by tadpoles at the two food levels. My results indicate that traits with a direct effect on offspring fitness are not enhanced by large male body size, yet some males and females produced offspring with significantly better performance. I suggest that evolutionary change in this mating system is unlikely to occur through the non-random mating of males based on body size alone.

Performance of Tadpoles from the Hybridogenetic Rana esculenta Complex: Interactions with Pond Drying and Interspecific Competition

Performance of Tadpoles from the Hybridogenetic Rana esculenta Complex: Interactions with Pond Drying and Interspecific Competition

THE MATING SYSTEM GENETICALLY AFFECTS OFFSPRING PERFORMANCE IN WOODHOUSE'S TOAD (BUFO WOODHOUSEI).

To determine if the nonrandom, non-resource-based mating system of Bufo woodhousei affects tadpole performance, I performed a series of controlled matings and reared the tadpoles to metamorphosis in the laboratory and field. I asked whether differences in paternal identity, mating status, or body size were related to differences in tadpole mass, larval period duration, metamorphic mass, or survival of offspring. Although both laboratory and field rearings indicated that male and female parentage affected most offspring traits, no correspondence existed between either laboratory and field metamorphic mass or laboratory and field survival of offspring sired by the same male. The lack of correspondence between sire breeding values in the laboratory and field for two of three traits raises doubts as to the validity of drawing conclusions concerning how evolution might be expected to work from laboratory studies. Paternal effects were more pronounced in the field than in the laboratory, despite what is usually presumed to be a greater amount of environmental variation in the field. In the laboratory neither sire body size nor mating status affected any trait, but in the field larger males produced offspring that were 10% heavier at transformation than offspring sired by small males. This predictable relationship between sire phenotype (body size) and offspring performance means that nonrandom mating based on male body size could have a directional effect on offspring performance. Because larger males mate disproportionately often in this population (Woodward, 1982a; Mitchell, unpubl.), the mating system may exert a directional effect on metamorphic body size.

Effect of tectotomy and decerebration on spontaneous and elicited behavior of tadpoles and juvenile frogs.

The performance of tadpoles and juvenile frogs on a battery of behavioral tests was compared before and after tectotomy, removal of the telencephalon (decerebration), tectotomy in conjunction with decerebration, or before and after a sham operation. Posture, righting, and vestibular responses were not altered by any of the lesions at either stage of development, and gross motor abilities were not impaired. Cutaneous reflex thresholds of tadpoles were lower than those of juveniles prior to surgery, but removal of the tectum or the telencephalon, or of both, reduced the thresholds of juveniles to near-larval levels. All of the lesions abolished characteristic defensive responses of juveniles (freezing) and resulted in hyperreactivity to a wide variety of stimuli. Tectotomy and decerebration of larvae each resulted in a 50% reduction in spontaneous locomotion and, in combination, virtually eliminated spontaneous locomotion. None of the lesions had any effect on the level of spontaneous locomotion of juveniles, but activity elicited by the novelty of the testing environment was eliminated in decerebrate subjects. Visual and vestibular nystagmus consisted of eye movements in tadpoles and of head movements in juveniles. Neither nystagmus nor optokinetic locomotion was affected by any of the lesions at either stage.