Authors
  • Algera, Dirk A.
  • Gutowsky, Lee F. G.
  • Zolderdo, Aaron J.
  • Cooke, Steven J.
Universities

Summary

Parental care is an advantageous reproductive behavior, as the fitness of the caregiver is increased through improving the chances of its offspring’s survival. Parental care occurs in a variety of teleost fishes. The body size of parental fish and the size of their brood can affect nest abandonment decisions, where compared with smaller fish with smaller broods, larger fish with larger broods typically invest more energy into reproductive events because they have less future reproductive potential. Although essential for basal metabolism and body maintenance functions, when glucocorticoid hormones (e.g., cortisol) are chronically elevated, as can occur during stress, fish may experience impairments in behavior and immune function, leading to compromised health and condition. Anthropogenic stressors during parental care can lead to elevated stress, therefore making it necessary to understand how stress influences an already-challenging period. Using smallmouth bass as a model, a gradient of body sizes, and experimentally manipulated brood size (i.e., reducing large broods and supplementing small broods) and cortisol levels (i.e., elevated via slow-release intraperitoneal cocoa butter implants containing cortisol versus controls), we tested the hypothesis that the reproductive success and parental care behaviors (i.e., aggression, nest tending) of nest-guarding male smallmouth bass are influenced by parental body size, brood size, and cortisol level. Overall, there was a relationship between cortisol treatment and nest success in which larger fish exhibited lower success when cortisol levels were elevated. Brood size had a significant effect on fish-tending behavior, independent of cortisol level and body size. Lending partial support to our hypothesis, the results of this study indicate that the reproductive success of guarding male smallmouth bass is influenced by cortisol level and that tending behavior is affected by brood size.

Methodology

Nest-guarding males were located through snorkel surveys using a trained team of snorkelers. If a nest-guarding male's length was estimated as falling within appropriate size ranges (i.e., large [>420 mm] or small [<330 mm]), their brood size (egg score) was also visually estimated. Egg score is a qualitative, highly repeatable assessment categorizing egg counts from 1 through 5, with 1 being few eggs and 5 being thousands of eggs (Kubacki [32]; Philipp et al. [38]; Suski et al. [53]; Zuckerman et al. [65]). The experimental design of this study purposefully avoided the inclusion of fish with an average body size and brood size, focusing on large and small body sizes and egg scores. Although we did not age fish, in this region the large fish would have been ∼8–14 yr old and the small fish would have been ∼4–7 yr old, on the basis of extensive aging work on a nearby system (i.e., O'Connor et al. [35]). A large brood size was a nest having an egg score of 4 and 5, whereas an egg score of 1 or 2 was considered a small brood (Kubacki 1992). Nests selected for the study were randomly distributed in similar habitats (rocky substrate) at 0.5–1.5-m water depth.

Behavioral assessments were designed to test a guarding male's nest-tending and aggression behaviors. Tending was assessed first, followed by aggression. To assess the tending and vigilance, a tending score was developed where each nest-guarding male was visually observed by a diver situated >3 m from the nest, limiting disturbance to the guarding male. After a 60-s acclimation period, the diver recorded how many times the male was within 1 m of his nest in 20-s increments for a total of 3 min (giving a total possible score of 9, as per Gravel and Cooke [[25]]). An aggression score was developed to test the nest-guarding male's defensive aggression toward a common brood predator. Aggression score was assessed using a bluegill sunfish (Lepomis machrochirus) between 130 and 140 mm in total length (TL) contained in a 4-L glass jar placed directly adjacent to the nest (Hanson et al. [28]). After an acclimation period of 30 s, a diver situated >3 m from the nest observed the engagement of the male with the brood predator, recording the duration of direct jar contact (s) and the number of strikes to the jar, mouth flares, and charges at the jar for a total of 60 s (Hanson et al. [28]). After the behavioral assessments, experimental fish were angled from the nest using rod and reel, placed into a foam-lined trough containing fresh lake water for TL measurement (all fish were angled and measured), and administered a cortisol treatment if applicable. The angling fight time was minimized (<20 s) in order to limit stress from capture and exhaustive exercise. No anesthesia was needed to sedate the fish while in the trough given that they were calm when in supine position.

Cortisol-treated fish received 10 mg kg−1 of cortisol (hydrocortisone 21-hemisuccinate; Sigma-Aldrich) suspended in a cocoa butter vehicle via intraperitoneal injection with a 16-gauge needle. Fish were injected with 0.005 mL per gram of fish body weight. Hydrocortisone 21-hemisuccinate is commonly used to experimentally elevate cortisol levels and is known to produce postreceptor effects comparable to those of endogenously produced cortisol in teleost fishes (Pickford et al. [39]; Chan and Woo [6]; Foster and Moon [17]; Kiilerich et al. [31]). Exogenous cortisol manipulation used in this study is a validated (for the same species, in the same watershed, at the same temperatures, using the same field methods and laboratory assays, by the same research group) method for elevating cortisol levels in smallmouth bass for 5–6 d (Gamperl et al. [18]; O'Connor et al. [36]; Dey et al. [15]). Mean posttreatment cortisol levels are expected to range from 750 to 2,250 ng mL−1 in black bass (O'Connor et al. [36]; Dey et al. [15]). For context, cortisol levels of control black bass engaged in parental care are typically <50 ng mL−1 (Dey et al. [15]). No sham treatment (injection containing only cocoa butter) was used in the experimental design due to inconsistent cortisol responses of sham-treated fish (see DiBattista et al. [16]). Although mass was not directly measured, a log10-transformed length-weight relationship equation from smallmouth bass in Opinicon Lake, a lake within the same system, was used to calculate fish weight from the TL measurements of experimental fish receiving cortisol treatment (Dey et al. [15]); the equation was log10 mass = −7.1004 × 3.884(log10 TL), with mass reported in grams and TL in millimeters. Time away from the nest was minimized; angling and cortisol administration took less than 120 s, and fish were released within 5 m of their nest after treatment. Throughout the treatment process a diver guarded the nest from brood predators in the guarding male's absence.

Location