Summary
The concept of behavioural syndromes (i.e. correlations between behavioural traits) has provided an important framework for understanding individual variation in animal behaviour and its link to individual variation in physiology and life-history traits. The pace-of-life syndrome concept posits that behavioural, physiological and life-history traits coevolve in response to correlated selection pressures, and therefore predicts a positive correlation between boldness (i.e. exploration and risk taking) and metabolic capacity for locomotor performance in individuals. We tested for a pace-of-life syndrome linking boldness and metabolic capacity for locomotor activity in juvenile bluegill sunfish, Lepomis macrochirus. Individual fish were screened and classified as bold or shy using an established refuge emergence test. Subsequently, the aerobic and anaerobic metabolisms of bold and shy individuals were quantified using respirometry and by measuring the metabolic by-products of white muscle anaerobic glycolysis following exhaustive exercise, respectively. Bold fish demonstrated 25% greater metabolic scope for activity (i.e. aerobic capacity) than shy fish, which was attributable to a 15% greater maximum metabolic rate. However, there was no significant difference in resting metabolic rate or anaerobic energy expenditure (i.e. anaerobic capacity) between bold and shy fish. These results partially support a pace-of-life syndrome linking boldness and aerobic metabolism in juvenile bluegill sunfish, but did not reveal a link between boldness and anaerobic metabolism. Our findings suggest that aerobic and anaerobic capacities may be subject to different selection pressures, and that physiological processes governing maximum anaerobic performance in fishes are independent from behavioural and physiological traits related to boldness
Methodology
Juvenile bluegill sunfish (N = 82 in July 2009 and N = 56 in July 2010) were angled from near-shore, shallow habitats in Lake Opinicon, Ontario, Canada (44°33′32″N, 76°19′41″W), using small barbless hooks baited with a small piece (∼1 cm) of earthworm. To minimize angling stress and injury, we used a standardized angling protocol that required all fish be landed, have the hook removed and be placed into a cooler with fresh lake water within 10 s of the hook being set (i.e. from when the fish bit down on the hook). Any angled fish with visible signs of injury (i.e. hooked somewhere other than upper or lower jaw) or disease, or that took longer than 10 s to land and free from the hook, were excluded from the study.
Boldness Behavioural Assay
On the day after capture, we assessed individual fish for their boldness using the established refuge emergence test, modified for use in juvenile bluegill sunfish (Wilson et al., 2011, Wilson and Godin, 2009) and which has been shown in this species to be highly repeatable within individuals, even after 1–3 months post-release in the wild (Wilson & Godin, 2009). The premise of the emergence test is that an individual fish's boldness is related to its willingness to leave refuge to explore a novel environment, such that a shorter latency to emerge from a refuge into a novel environment is inferred to represent greater boldness or risk taking. Notwithstanding its potential limitations (Beckmann and Biro, 2013, Carter et al., 2013), this test has been widely used to quantify individual boldness in diverse taxa, including fishes (Carter et al., 2013, Näslund et al., 2015).
Test sunfish were carefully netted from holding tanks and transferred individually in water to one of two identical test aquaria (Wilson et al., 2011; 82-litre glass aquarium, 92 × 30 × 30 cm; Fig. 1). Each aquarium was divided into two compartments by an opaque white Plexiglas partition (located 25 cm from one side of the aquarium) equipped with a sliding door to allow movement of the fish between compartments. The smaller compartment had two artificial plants fixed to its substratum and served as a potential ‘refuge’ (occupying highly vegetated habitats reduces individual predation risk in sunfish; Spotte, 2007), whereas the larger compartment was left open and served as a ‘novel environment’. The bottom of the test aquarium was covered with aquarium gravel, and the ends and back of the aquarium were covered with cardboard to minimize external disturbances. Both aquaria were uniformly illuminated overhead with fluorescent lights. Between trials, water in the aquaria was drawn down using an aquarium pump and replaced with fresh aerated lake water.