Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival

Abstract

In organisms that have complex life cycles, factors in the larval environment may affect both larval and adult traits. For amphibians, the postmetamorphic transition from the aquatic environment to terrestrial habitat may be a period of high juvenile mortality. We hypothesized that lipid stores at metamorphosis may affect an animal's success during this critical transition period. We examined variation in total lipid levels among years and sites in recently metamorphosed individuals of two pond-breeding salamander species, the marbled salamander (Ambystoma opacum) and the mole salamander (A. talpoideum), with limited data for one anuran species (southern leopard frog, Rana sphenocephala). Lipid levels were allometrically related to body size and ranged from 1.9 to 23.8% of body dry mass. The two salamander species differed in lipid allocation patterns, with A. opacum apportioning a higher percentage of total lipid reserves into fat bodies than A. talpoideum. Species differences in lipid allocation patterns may primarily reflect that large metamorphs will mature as one-year olds, and, regardless of species, will alter lipid compartmentalization accordingly. We used mark-recapture data obtained at drift fences encircling breeding ponds for 13 A. opacum cohorts to estimate the proportion of postmetamorphic individuals that survived to breed (age 1-4) and the mean age at first reproduction. Regression models indicated that size-corrected lipid level at metamorphosis (i.e., lipid residuals), and to a lesser extent rainfall following metamorphosis, was positively related to adult survival. Snout-vent length at metamorphosis was negatively related to age at first reproduction. We suggest that lipid stores at metamorphosis are vital to juvenile survival in the months following the transition from aquatic to terrestrial habitat, and that a trade-off shaped by postmetamorphic selection in the terrestrial habitat exists between allocation to energy stores versus structural growth in the larval environment.

Energy allocation strategy modifies growth–survival trade-offs in juvenile fish across ecological and environmental gradients

“…Organisms distributed across geographical gradients experience variation in stored energy requirements and patterns of higher storage in areas with harsher winters have been observed along latitudinal (Schultz and Conover 1997;Berg et al 2009;Jönsson et al 2009;Finstad et al 2010) and altitudinal gradients (Tracy 1999;Takahashi and Pauley 2010). Other factors that affect energy allocation include body size (Deegan 1986;Henderson et al 1988;Heulett et al 1995;Lampo and Medialdea 1996;Post and Parkinson 2001;Scott et al 2007), life history Jonsson 1998, 2003;Rikardsen and Elliott 2000;Morgan et al 2002), and food availability and quality (Heulett et al 1995;Garvey and Marschall 2003;Sogard and Spencer 2004;Borcherding et al 2007).…”

“…A key component of energy allocation in pre-reproductive organisms is allocation to energy storage, thereby providing a means to survive periods of energy deficit such as metamorphosis (Scott et al 2007), night (Polo et al 2007) or winter (Biro et al 2004). Organisms in seasonal Communicated by Øyvind Fiksen.…”

Terrestrial distribution of pond‐breeding salamanders around an isolated wetland

“…The decreased body condition index of animals recaptured at outer distances, which we attempted to hydrate equally before weighing, suggests there may be an energetic cost to emigration in the first months post-metamorphosis (Windmiller 1996). Energy stores at metamorphosis are strongly related to juvenile survival (Scott et al 2007), and mortality is highest in the months immediately following metamorphosis (Rothermel and Semlitsch 2006), thus, there may be strong selection against long distance (energetically expensive) movements by juveniles. However, given our methodology, we cannot disentangle mass loss as a consequence of emigration from the use of energy stores for metabolic maintenance during the time since emergence (Scott 1994).…”

Deposição de nutrientes na carcaça de girinos de rã-touro

“…A deposição de gordura pode ser de origem genética (Leonhardt et al, 2006); no entanto, outros fatores contribuem para o acúmulo de gordura nos animais, como dieta e condições ambientais (Glencross et al, 2011;Amrkolaie et al, 2012). Verificou-se, também, que a quantidade de gordura depositada aumentou gradativamente (Tabela 3) em razão do desenvolvimento do corpo adiposo com o crescimento dos girinos, uma vez que, durante a metamorfose, ocorre grande gasto energético (Scott et al, 2007).…”