Intraspecific variation in aerobic and anaerobic locomotion: gilthead sea bream (Sparus aurata) and Trinidadian guppy (Poecilia reticulata) do not exhibit a trade-off between maximum sustained swimming speed and minimum cost of transport

Abstract

Intraspecific variation and trade-off in aerobic and anaerobic traits remain poorly understood in aquatic locomotion. Using gilthead sea bream (Sparus aurata) and Trinidadian guppy (Poecilia reticulata), both axial swimmers, this study tested four hypotheses: (1) gait transition from steady to unsteady (i.e., burst-assisted) swimming is associated with anaerobic metabolism evidenced as excess post exercise oxygen consumption (EPOC); (2) variation in swimming performance (critical swimming speed; U crit) correlates with metabolic scope (MS) or anaerobic capacity (i.e., maximum EPOC); (3) there is a trade-off between maximum sustained swimming speed (U sus) and minimum cost of transport (COTmin); and (4) variation in U sus correlates positively with optimum swimming speed (U opt; i.e., the speed that minimizes energy expenditure per unit of distance traveled). Data collection involved swimming respirometry and video analysis. Results showed that anaerobic swimming costs (i.e., EPOC) increase linearly with the number of bursts in S. aurata, with each burst corresponding to 0.53 mg O2 kg(-1). Data are consistent with a previous study on striped surfperch (Embiotoca lateralis), a labriform swimmer, suggesting that the metabolic cost of burst swimming is similar across various types of locomotion. There was no correlation between U crit and MS or anaerobic capacity in S. aurata indicating that other factors, including morphological or biomechanical traits, influenced U crit. We found no evidence of a trade-off between U sus and COTmin. In fact, data revealed significant negative correlations between U sus and COTmin, suggesting that individuals with high U sus also exhibit low COTmin. Finally, there were positive correlations between U sus and U opt. Our study demonstrates the energetic importance of anaerobic metabolism during unsteady swimming, and provides intraspecific evidence that superior maximum sustained swimming speed is associated with superior swimming economy and optimum speed.

Keywords: aerobic metabolic scope; anaerobic capacity; burst swimming; excess post exercise oxygen consumption; intraspecific variation and trade-off; locomotion; maximum sustained swimming speed; minimum cost of transport.

Figure 1

Measurements of (A) metabolic rate (mg O₂ kg⁻¹ h⁻¹) and (B) swimming speed (cm s⁻¹) in gilthead sea bream (Sparus aurata). Data include standard metabolic rate (MO_2stand), maximum sustained (or aerobic) metabolic rate (MO_2sus), active metabolic rate (MO_2active) and maximum metabolic rate (MO_2max). The measurements are defined in detail in the text. Corresponding swimming speeds (B) were derived from the metabolic measurements and include maximum sustained (U_sus), active (U_active) and maximum (U_max) swimming speeds. There are significant differences (P < 0.05) between the measurements of metabolism and swimming speed as indicated by the different letters.

Figure 2

(A) Metabolic rate (mg O₂ kg⁻¹ h⁻¹) and (B) recovery time (h) in relation to swimming speed (%U_crit) in individual gilthead sea bream (Sparus aurata). U_crit is the critical swimming speed and defined in detail in the text. For (A), metabolic rates were measured in the swimming fish (exercise MO₂; open symbols) and as excess post exercise oxygen consumption (EPOC; mg O₂ kg⁻¹). Exercise MO₂ and EPOC were combined to estimate the total metabolic cost of swimming (total MO₂; closed symbols). For (B), recovery time (h) reflects the duration of EPOC after single swimming exercises (up to 30 min).

Figure 3

The minimum speed with excess post exercise oxygen consumption (EPOC; mg O₂ kg⁻¹) correlates positively with the minimum speed with burst swimming (P < 0.0001; R² > 0.95) in gilthead sea bream (Sparus aurata). The relationship shows that the onset of burst swimming at increasing speeds indicates the onset of EPOC and therefore, anaerobic metabolism in individual fish.

Figure 4

The magnitude of excess post exercise oxygen consumption (EPOC; mg O₂ kg⁻¹) correlates positively with burst activity in gilthead sea bream (Sparus aurata) (blue symbols) and striped surfperch (Embiotoca lateralis) (red symbols). Data on S. aurata are from the present study, whereas data on E. lateralis are from Svendsen et al. (2010). The linear fit (P < 0.0001) reflects the pooled data set for both species (Equation 6), because species-specific regression slopes and intercepts with the y-axes are not statistically different (P > 0.34). The relationship suggests that a burst represents a metabolic cost of 0.53 mg O₂ kg⁻¹.

Figure 5

Minimum cost of transport (COT_min; mg O₂ kg⁻¹ m⁻¹) correlates negatively with maximum sustained swimming speed (U_sus; cm s⁻¹) in (A) gilthead sea bream (Sparus aurata; n = 13) and (B) Trinidadian guppy (Poecilia reticulata; n = 18). Data on S. aurata are from the present study, whereas data on P. reticulata are derived from Svendsen et al. (2013). Both relationships are statistically significant (P < 0.005; R² > 0.53). The relationships suggest that superior sustained swimming performance (i.e., high U_sus) is associated with superior swimming economy (i.e., low COT_min) in both species. Note that y-axes differ between the two panels.

Figure 6

Optimum swimming speed (U_opt; cm s⁻¹) correlates positively with maximum sustained swimming speed (U_sus; cm s⁻¹) in (A) gilthead sea bream (Sparus aurata; n = 13) and (B) Trinidadian guppy (Poecilia reticulata; n = 18). Data on S. aurata are from the present study, whereas data on P. reticulata are derived from Svendsen et al. (2013). Both relationships are statistically significant (P < 0.005; R² > 0.40). The relationships suggest that superior sustained swimming performance (i.e., high U_sus) is associated with superior optimum swimming speed (i.e., high U_opt) in both species. Note that y-axes differ between the two panels.