Ecological constraints on amphibian metamorphosis: interactions of temperature and larval density with responses to changing food level

Abstract

Phenotypic plasticity is adaptive for an organism inhabiting a variable environment if the optimal phenotype of a trait that affects fitness varies with environmental conditions, and if the organism can perceive environmental conditions and respond appropriately. Wilbur and Collins have proposed that amphibian larvae might respond adaptively to changes in their resource environment. If conditions for growth in the aquatic environment deteriorate, then a tadpole should metamorphose earlier and smaller than a tadpole under constant high growth conditions. Several experiments on a variety of species have tested this prediction, but only one demonstrated such a response. That experiment involved Couch's spadefoot toads (Scaphiopus couchii) and employed a gradual decrease in food level, whereas the others all used an abrupt switch from high to low food. The purpose of the present experiment was to examine the response of S. couchii to an abrupt change in food level, and to determine if the response depended on the level of two other factors, density and temperature, that also affect larval development. The average effects of the abrupt change in food level were similar to those seen in studies on other species: age at metamorphosis was primarily determined by the early food regime, and size at metamorphosis was determined by food level late in the larval period, suggesting that the effect of decreased food depends on how the food change is done. However, the response to even an abrupt food change depended on interactions with other environmental factors. At high temperature, high initial food, and low density, development was very rapid and tadpoles switched from high to low food metamorphosed at about the same time and size as those at constant high food. In contrast, under high temperature and high initial food conditions, but at high density, tadpoles switched to low food metamorphosed somewhat earlier and smaller, on average, than tadpoles kept at high food. At low temperature, the direction of response depended on density: tadpoles metamorphosed much smaller and slightly, but significantly, earlier at low density, but smaller and later at high density. The developmental response to increased food also varied with temperature. Larvae at high temperature metamorphosed earlier and larger than those at constant low food. At low temperature, larvae metamorphosed larger, but at nearly the same time as their counterparts at constant low food. The combination of high density and constant low food prevented any tadpoles from metamorphosing at high temperature, and allowed relatively few metamorphs at low temperature. Under conditions which impose either very rapid or retarded development, the opportunity to respond to altered food level may be limited. Interactions among environmental factors, therefore, may constrain responses to changing conditions, and may even prevent completion of development.

Assimilation efficiency in Bufo spinulosus tadpoles (Anura: Bufonidae): effects of temperature, diet quality and geographic origin

“…Temperature and the availability of nutrients have been considered the most important causes in the variation in size and age at metamorphosis (Beck 1997, Alvarez & Nicieza 2002a. Several studies have shown that, among individuals having recently metamorphosed, variation in food availability and diet quality during larval stage can affect the rate of differentiation, the size at metamorphosis and the capacity to escape predators (Travis & Trexler 1986, Beck 1997, Denver 1997, Kupferberg 1997, Newman 1998, Reading & Clarke 1999, Beck & Congdon 2000, Nicieza 2000, Alvarez & Nicieza 2002b, Loman 2002. Due to diets of highest nutritional quality generally produce an increase in the rates of growth and differentiation, it is assumed that the amount of energy and nutrients present in high quality foods would be better utilized by tadpoles.…”

The history of a developmental stage: Metamorphosis in chordates

“…TH levels reach a maximum during the climax, that is, when the major morphological changes (e.g., tail regression) occur. When environmental parameters (e.g., water volume or food availability) modulate the triggering of metamorphosis, it is always through alteration of the TH production that can thus be viewed as the key endogenous inducer of the metamorphosis process (Boelen et al, 2008;Boorse and Denver, 2003;Denver, 1998;Ito et al, 2004;Newman, 1998;Tata, 2006) (Fig. 2).…”

Life History of the Golden Puddle Frog, Phrynobatrachus auritus Boulenger 1900 (Anura: Phrynobatrachidae)

“…It has already been reported that densities of conspecific might actually give supplementary information, which individuals can use to 'fine-tune' the timing of their phenotypic transformations (Goldberg et al, 2012). Some authors have proposed changes in habitat, such as pond desiccation, limited food resources, and the presence of predators or competition as mean to affect the duration of the larval stage and the timing of metamorphosis (Newman, 1998). However, we do not throw away the potential of synergetic influence in the setting as a function of relatively stable habitat, where very low seasonal variation in environmental parameters, and no risk of the water body drying up.…”