Authors
  • Algera, Dirk A.
  • Brownscombe, Jacob W.
  • Gilmour, Kathleen M.
  • Lawrence, Michael J.
  • Zolderdo, Aaron J.
  • Cooke, Steven J.
Universities

Summary

Paternal care, where the male provides sole care for the developing brood, is a common form of reproductive investment among teleost fish and ubiquitous in the Centrarchidae family. Throughout the parental care period, nesting males expend energy in a variety of swimming behaviours, including routine and burst swimming, vigilantly monitoring the nest area and protecting the brood from predators. Parental care is an energetically demanding period, which is presumably made even more difficult if fish are exposed to additional challenges such as those arising from human disturbance, resulting in activation of the hypothalamic-pituitary-interrenal axis (i.e., elevation of cortisol). To study this situation, we examined the effects of experimental manipulation of the stress hormone cortisol on locomotor activity and behaviour of nest guarding male smallmouth bass (Micropterus dolomieu). We exogenously elevated circulating cortisol levels (via intracoelomic implants) and attached tri-axial accelerometers to wild smallmouth bass for three days. During the recovery period (i.e., ≤ 4 h post-release), cortisol-treated fish exhibited significantly reduced locomotor activity and performed significantly less burst and routine swimming relative to control fish, indicating cortisol uptake was rapid, as were the associated behavioural responses. Post-recovery (i.e., > 4 h post-release), fish with high cortisol exhibited lower locomotor activity and reduced routine swimming relative to controls. Fish were less active and reduced routine and burst swimming at night compared to daylight hours, an effect independent of cortisol treatment. Collectively, our results suggest that cortisol treatment (as a proxy for anthropogenic disturbance and stress) contributed to altered behaviour, and consequently cortisol-treated males decreased parental investment in their brood, which could have potential fitness implications.

Methodology

Experimental animals and protocol

The study was conducted between May 15th and 28th, 2015 in four lakes in the Rideau River system (Opinicon Lake, Sand Lake, Indian Lake, and Big Rideau Lake) located in southeastern Ontario. These lakes have a similar species composition and predator burden [50], and previous research indicated that the physiological cost of parental care is similar in these lakes [51]. Surface water temperature ranged from 12 to 16 °C during the study. Nesting male smallmouth bass (Micropterus dolomieu) guarding unhatched embryos (‘eggs’) 0 to 3 days old were located through snorkel surveys and angled from the nest, with fight time minimized (< 20 s) to reduce angling-associated stress [44], [46]. All nests selected for inclusion in the study were located in a rocky substrate in water depths ranging from 0.5 to 1.5 m. Following capture, fish were placed in a foam-lined trough containing fresh lake water and total length (TL) was measured. To limit handling time, mass was estimated from an established length-mass relationship [44] using the Eq. (1) where mass is reported in grams and TL in millimeters.

(1) log10 mass = -7.1004 + 3.884(log10 TL)

Following the general methods of Brownscombe et al. [52], accelerometers (see below for accelerometer details) were firmly attached through the dorsal musculature using 13.6 kg Dacron line and a backing pad; accelerometers were placed on the external surface of the right side of the fish under the soft area of the dorsal fin.

Fish were randomly assigned to one of three treatment groups; control fish that were untreated, fish that received an intraperitoneal injection of cocoa butter (5 mL kg− 1; NOW Foods, Bloomingdale, IL) mixed with a low (5 mg mL− 1) concentration of cortisol (hydrocortisone 21-hemisuccinate, Santa Cruz Biotechnology, Dallas, TX), and fish that received a high (10 mg mL− 1) cortisol concentration, again as an intraperitoneal implant in cocoa butter. The high cortisol concentration in this study (10 mg mL− 1) has been found to produce high elevated circulating cortisol levels in nesting black bass for 5–6 days [44], [45]. A sham treatment group (cocoa butter alone) was not included in the experimental design owing to inconsistent cortisol responses associated with sham treatment (see [53]). Prior to release, fish (with tag affixed) were rotated along known axes (forward pitching motion and rolled to the right) in a cooler containing fresh lake water, noting the corresponding times, to aid in calibrating accelerometers. Capture, tagging, cortisol administration (if applicable), and accelerometer calibration encompassed < 7 min.

Location