Ecological lifestyles and the scaling of shark gill surface area

Abstract

Fish gill surface area varies across species and with respect to ecological lifestyles. The majority of previous studies only qualitatively describe gill surface area in relation to ecology and focus primarily on teleosts. Here, we quantitatively examined the relationship of gill surface area with respect to specific ecological lifestyle traits in elasmobranchs, which offer an independent evaluation of observed patterns in teleosts. As gill surface area increases ontogenetically with body mass, examination of how gill surface area varies with ecological lifestyle traits must be assessed in the context of its allometry (scaling). Thus, we examined how the relationship of gill surface area and body mass across 11 shark species from the literature and one species for which we made measurements, the Gray Smoothhound Mustelus californicus, varied with three ecological lifestyle traits: activity level, habitat, and maximum body size. Relative gill surface area (gill surface area at a specified body mass; here we used 5,000g, termed the 'standardized intercept') ranged from 4,724.98 to 35,694.39 cm 2 (mean and standard error: 17,796.65 AE 2,948.61 cm 2 ) and varied across species and the ecological lifestyle traits examined. Specifically, larger-bodied, active, oceanic species had greater relative gill surface area than smaller-bodied, less active, coastal species. In contrast, the rate at which gill surface area scaled with body mass (slope) was generally consistent across species (0.85 AE 0.02) and did not differ statistically with activity level, habitat, or maximum body size. Our results suggest that ecology may influence relative gill surface area, rather than the rate at which gill surface area scales with body mass. Future comparisons of gill surface area and ecological lifestyle traits using the quantitative techniques applied in this study can provide further insight into patterns dictating the relationship between gill surface area, metabolism, and ecological lifestyle traits. K E Y W O R D Sallometry, ecomorphology, gill surface area, metabolism, scaling

Gill surface area provides a clue for the respiratory basis of brain size in the blacktip shark (Carcharhinus limbatus)

“…Additionally, as gill surface area is a metabolically important trait that supports the oxygen diffusion necessary for aerobic metabolism in fishes, it fits that gill surface area would also change with body mass throughout ontogeny to support the energetic requirements of a larger body and potentially the energetic requirements of a growing brain (Bigman et al ., 2018; Hughes, 1978). The allometric slope of gill surface area found in this study corresponds to previous work on gills that found allometric slopes between 2 / 3 and 1 (Bigman et al ., 2018; Wegner et al ., 2010; Wootton et al ., 2015), as well as an average of ontogenetic allometric slopes of metabolic rate in fishes (slope = 0.89; Jerde et al ., 2019). Although our results are correlational, the lower allometric slope of brain mass compared to gill surface area supports our prediction that gill surface area, and by extension oxygen supply capacity, may set an upper limit for the allometric slope of brain mass above which individuals would potentially reach a point where they had more neural tissue than they could supply oxygen to and energetically support (Karbowski, 2007).…”

“…As we found little effect of location for this small and biased sample size, we pooled the data for subsequent analyses (Supporting Information Figure S1 and Table S2). To be consistent with previous work, we used linear regression on log 10 ‐transformed data for both brain mass and gill surface area allometric relationships (Bigman et al ., 2018; Chapman & Hulen, 2001; Salas et al ., 2015). On a log 10 ‐transformed scale, the intercept is estimated at 1 g of body mass, which lies far outside the range of body masses for the specimens in this study.…”

The metabolic pace of life histories across fishes

“…Environmental and ecological factors such as activity levels, predation risk, food availability, and environmental temperature may obscure relationships between metabolic rate and life history traits, particularly in ectotherms, and this could also be considered in the future [22,42,48]. Fish species with a high metabolic rate for their body mass have a high growth performance, but they may also have high activity levels [22,32].…”

“…Metabolic rate is commonly used as a proxy for activity level, confounding studies of the relationship between metabolic rate and activity level [49]. Thus, future studies should investigate the interrelationships between activity level, metabolic rate, and life history by using morphological proxies of activity such as the caudal fin aspect ratio (= [height of the caudal fin] 2 /[surface area of the fin]) [22,48]. For example, the caudal fin morphology of the Japanese Amberjack is strongly lunate, suggesting that this species is more active compared to the Zander with its rounded tail ( Figure 1A).…”

Bridging disciplines to advance elasmobranch conservation: applications of physiological ecology

“…Both intraspecifically within and interspecifically across species, the relationship between gill surface area and mass is similar to that of maximum metabolic rate and mass, suggesting that gill surface area is matched to metabolic demand (Gillooly et al , 2016; Wegner, 2016). Further, gill surface area and metabolic rate have a basis in ecology since both are correlated with temperature, activity and habitat type (Bernal et al , 2012; Wootton et al , 2015; Bigman et al , 2018).…”