Authors
  • Elmer, Laura K.
  • O'Connor, Constance M.
  • Philipp, David P.
  • Van Der Kraak, Glen
  • Gilmour, Kathleen M.
  • Willmore, William G.
  • Barthel, Brandon L.
  • Cooke, Steven J.
Universities

Summary

Physiologically, oxidative stress is considered a homeostatic imbalance between reactive oxygen species production and absorption. From an ecological perspective, oxidative stress may serve as an important constraint to life-history traits, such as lifespan, reproduction and the immune system, and is gaining interest as a potential mechanism underlying life-history trade-offs. Of late, there has been much interest in understanding the role of oxidative stress in the ecology of wild animals, particularly during challenging periods such as reproduction. Here, we used a long-term study population of a fish with sole-male parental care, the smallmouth bass, Micropterus dolomieu, to examine the associations among oxidative stress indicators and life-history variables in nest-guarding males. In addition, we investigated the potential role of oxidative stress as a physiological mediator of the life-history trade-off decision of paternal smallmouth bass to stay with or abandon their brood. We found that oxidative stress was significantly related to the life history of paternal smallmouth bass, such that older, larger fish with greater reproductive experience and larger broods nesting in cooler water temperatures had lower levels of oxidative stress. However, we found no significant correlation between oxidative stress and nesting success, suggesting that oxidative stress may not be involved in the decision of male smallmouth bass to abandon their brood. Wild fish have been relatively understudied in the emerging field of oxidative ecology, and this study makes noteworthy contributions by revealing interesting connections between the life histories of paternal smallmouth bass and their oxidative status.

Methodology

Study site, study animals and sampling procedure

The fish used in the current study were parental care-providing males captured in Miller's Lake, part of the Mississippi River system in eastern Ontario, Canada (44°56′26.5″N, 76°41′55.0″W). This population has been the subject of a long-term (>20 years) study on the reproductive ecology of smallmouth bass, and the reproductive history of all adult males reproducing in the system is known for the study period (Barthel et al., 2008). For a full description of the study site, see Barthel et al. (2008). Briefly, the study site is composed of distinct upstream riverine (Mississippi River) and downstream lacustrine (Miller's Lake) habitats, separated by a 1 m waterfall that is not a complete barrier to smallmouth bass movement. The study site is bordered upstream by a 12 m waterfall and downstream by an extensive series of rapids and waterfalls, both of which serve as barriers to at least upstream movement. Radio telemetry studies have not detected fish movement out of the study site in either direction (Barthel et al., 2008). The study site is relatively isolated and receives negligible fishing pressure.

Fish used in the current study represent a subset of the fish used by O'Connor et al. (2012) to determine associations between life history and plasma physiology. As these fish are part of a long-term study population, it was necessary for all sampling to be non-lethal, and so only plasma samples were obtained. If we had used a lethal sampling approach to obtain tissues such as heart, brain or liver, we would have removed the majority of nesting bass for a given year, which would have serious ecological consequences. Previous studies have used plasma for the assessment of oxidative protection and damage (reviewed in Birnie-Gauvin et al., 2017), including research on nesting bass (see Wilson et al., 2012). In addition, other studies on teleost fish have compared different tissues and revealed that plasma concentrations are related to those in other tissues (Taylor et al., 2015).

For full details of the study and the sampling procedures, see O'Connor et al. (2012). Briefly, in May and June 2009, snorkellers identified parental males on nests. Only those fish guarding fresh eggs (<24 h old) were selected for sampling; this timing was required to account for decreases in androgen concentration over the course of parental care (O'Connor et al., 2011). The snorkeller assigned an egg score to each nest; the egg score is between 1 and 5, and indicates relative egg number, with 1 indicating few eggs and 5 indicating a large number of eggs (Stein and Philipp, 2015). Nest-guarding males were then caught using targeted rod and reel angling, and blood plasma samples were obtained using caudal puncture and lithium-heparinised 3 ml Vacutainer-style syringes (Becton, Dickinson, Franklin Lakes, NJ, USA). Separated plasma samples (initially frozen in liquid nitrogen in the field and then transferred to a −80°C freezer) were used to determine circulating concentrations of androgens and cortisol for a previous study (O'Connor et al., 2012), and antioxidant capacity and oxidative damage in the current study. Scales were collected to allow determination of age, and water temperature was recorded before the fish was released.

Smallmouth bass reproduce in both the river and lake habitats and tend to show high nest-site fidelity (Barthel et al., 2008). Parental males in the two habitats differ in physiology (O'Connor et al., 2012) and life history (Barthel et al., 2008; O'Connor et al., 2012). For simplicity, and to eliminate any discrepancies caused by nesting location, only the fish from Miller's Lake were used in the current study, resulting in a sample size of N=57 individuals. See Table 1 for measured characteristics from these fish.

Location