Ecology of ontogenetic body-mass scaling of gill surface area in a freshwater crustacean

Abstract

Several studies have documented ecological effects on intraspecific and interspecific body-size scaling of metabolic rate. However, little is known about how various ecological factors may affect the scaling of respiratory structures supporting oxygen uptake for metabolism. To our knowledge, our study is the first to provide evidence for ecological effects on the scaling of a respiratory structure among conspecific populations of any animal. We compared the body-mass scaling of gill surface area (SA) among eight spring-dwelling populations of the amphipod crustacean Gammarus minus. Although gill SA scaling was not related to water temperature, conductivity or G. minus population density, it was significantly related to predation regime (and secondarily to pH). Body-mass scaling slopes for gill SA were significantly lower in four populations inhabiting springs with fish predators than for four populations in springs without fish (based on comparing means of the population slopes, or slopes calculated from pooled raw data for each comparison group). As a result, gill SA was proportionately smaller in adult amphipods from springs with versus without fish. This scaling difference paralleled similar differences in the scaling exponents for the rates of growth and resting metabolic rate. We hypothesized that gill SA scaling is shallower in fish-containing versus fishless spring populations of G. minus because of effects of size-selective predation on size-specific growth and activity that in turn affect the scaling of oxygen demand and concomitantly the gill capacity (SA) for oxygen uptake. Although influential theory claims that metabolic scaling is constrained by internal body design, our study builds on previous work to show that the scaling of both metabolism and the respiratory structures supporting it may be ecologically sensitive and evolutionarily malleable.

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…A similar outcome occurred in brown garden snails (Cornu asperum, formerly Helix aspersa), whose growth rate had been increased by artificial selection for increased body size [220]. A natural experiment involving varying natural selection on growth rate in amphipod populations living in springs with versus without visually hunting fish predators also revealed a close match between the ontogenetic scaling of the rates of growth and metabolism [105,136].…”

“…Several studies in diverse species of plants [193], invertebrates [103,105,136,219,220,222] and vertebrates [218,221,223,224] have shown that increased growth rate is associated with steeper ontogenetic scaling of metabolic rate (slopes often approaching 1) (also see 19,20,98]. This support involves not only numerous correlative analyses, but also multiple experimental manipulations.…”

“…Body shape and associated surface area may have evolved to match metabolic demand [133]. This reverse causation likely explains parallel scaling of gill surface area and metabolic (oxygen consumption) rate in amphipod crustaceans [136] and perhaps fishes, as well [137,138] (also see Section 3.3).…”

“…Here I focus on explanations involving the metabolic demand of growth and development, which are especially relevant to body-size scaling [19,85,98,103,105,106,136,193,[218][219][220][221]. Most of these explanations (including DEB theory) consider how changes in growth rate during ontogeny affect the scaling of metabolic rate [19,85,98,103,105,136,193,[218][219][220][221]. As with SC models, growth-based RD explanations of metabolic scaling originated in the 1930s and 1940s ( [222][223][224]; reviewed in [20]), but most modern investigators appear to be unaware of this work.…”

“…Pulmonate snails that breathe relatively high-oxygen air also exhibit significantly higher metabolic rates than prosobranch snails of equivalent size that breathe relatively low-oxygen water [250]. In addition, close associations between the scaling of metabolic rate and the SA of respiratory structures or of the body in skin-breathing animals (e.g., [132,133,136,[251][252][253][254]) suggest that SA mechanisms are often importantly involved in metabolic scaling, if not as primary drivers, at least as necessary providers of required resources. Metabolic scaling may often involve a regulatory co-adjustment between resource supply and demand [20].…”