Direct and indirect induction of a compensatory phenotype that alleviates the costs of an inducible defense

Abstract

Organisms often exhibit phenotypic plasticity in multiple traits in response to impending environmental change. Multiple traits phenotypic plasticity is complex syndrome brought on by causal relations in ecological and physiological context. Larvae of the salamander Hynobius retardatus exhibit inducible phenotypic plasticity of two traits, when at risk of predation by dragonfly larvae. One induced phenotype is an adaptive defense behaviour, i.e., stasis at the bottom of water column, directly triggered by the predation risk. Another one is a compensatory phenotype, i.e., enlarged external gills, for an unavoidable cost (hypoxia) associated with the induced defense. We identified two ways by which this compensatory phenotype could be induced. The compensatory phenotype is induced in response to not only the associated hypoxic conditions resulting from the induced defense but also the most primary but indirect cause, presence of the predator.

Figure 1. Conceptual schema of phenotypic plasticity in salamander larvae in the presence of dragonfly larvae.

In this schema, “Predation risk” is the starting point and “Enlargement of the external gills” is the end point. Dotted arrows originate at possible signals, solid arrows show adaptive causal connections, and the hollow arrow points to an unavoidable cost. Thus, hypoxia is an unavoidable cost of the adaptive behavioural response “Decreased surfacing”. Enlargement of the external gills can be reached by two pathways, a multi-step pathway via the antipredator behaviour (decreased surfacing) and the consequent hypoxia, and a direct pathway via predator-produced cues.

Figure 2. (a) Effects of predator presence and oxygen availability on the development of the external gills of salamander larvae.

(b) Low-oxygen tolerance of salamander larvae reared under predator presence or absence, and high- or low-oxygen treatment. Open and solid squares indicate that rearing condition of larval salamander is the high-oxygen treatment and the low-oxygen treatment, respectively. Error bars indicate ±1 s.e.m.

Figure 3. Representative salamander larvae reared under low-oxygen conditions in the gill induction experiment.

The individual on the left was subjected to the predator treatment and the one on the right to the no-predator treatment.

Figure 4. Morphmetric measurements of gill rachises.

Larval salamander gill measurements. sg, second gill; gh, gill height; gd, gill depth; gw, gill width; a+b, distance between the three gill rachises; , second gill length.