- University of Western Ontario
- University of Oklahoma
- Grand Valley State University
Summary
Parental care can include two general types of behavior: (1) aggressive behavior, which is used to defend offspring from predators; and (2) nurturing behavior, which is used to provide offspring with environmental conditions or resources necessary for survival. Many studies have implicated androgens in promoting aggressive behavior and prolactin in promoting nurturing behavior. We experimentally manipulated these hormones to investigate their effects on parental care behavior in bluegill (Lepomis macrochirus). Parental males, which provide sole care to the developing eggs and larvae, received an implant with an androgen (11-ketotestosterone [11-KT]), an androgen antagonist (flutamide), prolactin, a prolactin-release inhibitor (bromocriptine), or castor oil (placebo). We found that 11-KT implants led to a significant increase in the frequency of aggressive behavior directed towards a simulated brood predator, and were associated with a nearly significant decrease in the frequency of nurturing behavior directed towards the developing eggs. In contrast, prolactin implants were associated with a significant increase in the frequency of nurturing behavior, but also reduced the frequency of aggressive behavior directed towards the simulated brood predator. These results suggest a hormone-mediated mechanistic trade-off between nurturing and aggressive behavior, whereby parental males are unable to be both highly nurturing and highly aggressive.
Methodology
Species and study site
We studied a population of bluegill in Lake Opinicon (44°34′N, 76°19′W), Ontario, Canada. This lake is approximately 900 ha and has been a study site for this species since the 1980s (e.g. Gross, 1982). In Lake Opinicon, during the June to July breeding season, parental males enter the littoral zone and build nests side-by-side in colonies. A colony is established over the course of a couple of days, after which females spawn with parental males at that colony during a single day. Multiple colonies are formed at different locations and different times during the breeding season. Parental males remain highly aggressive to each other during colony formation and spawning (Gross, 1982), and during this period, circulating 11-KT concentrations are high (Magee et al., 2006). After spawning, only the parental males remain in the colony to provide parental care to the offspring. The care period consists of about 3 days of caring for eggs, when parental males actively fan the eggs to move oxygenated water across the nest, remove dead or moldy eggs from the nest, and defend the eggs from brood predators in the water column, which include other bluegill, pumpkinseed (Lepomis gibbosus), smallmouth bass (Micropterus dolomieu), and bluegill × pumpkinseed hybrids (Côté and Gross, 1993; Gross and Macmillan, 1981). After the eggs hatch, the parental males will remain for another 4–7 days while the larvae continue to develop in order to defend the larvae from brood predators. Circulating concentrations of 11-KT tend to be low during the egg period of care, but can rise again during the larval period of care (Magee et al., 2006).
Hormone manipulation
The experimental protocol used in this study was approved by the University of Western Ontario Animal Care Committee. During the breeding seasons of 2015, 2016 and 2017, swimmers monitored bluegill activity in the lake and identified colony formation and the onset of spawning. On the day after spawning, nests were marked with numbered ceramic tiles, and parental males were captured one at a time using a dip net. A screen was placed over the nest to prevent egg predation during the male's absence. The number of eggs on each nest was estimated using a 5-point scale (see Claussen, 1991). Each parental male was taken to a nearby boat where 200 μl of whole blood was collected from the caudal vein using a 25G needle attached to a 1 ml, heparinized syringe. The time to collect blood never exceeded 2 min from capture. Blood samples were stored on ice until they were brought to the field-based laboratory and centrifuged to separate and extract plasma. The plasma was then stored at −20 °C. Each male was assigned to one of six treatments in a rotating order: (1) placebo (control), (2) 11-KT, (3) flutamide, an 11-KT antagonist, (4) low concentration of prolactin, (5) high concentration of prolactin, and (6) bromocriptine, a prolactin-release inhibitor. In 2015, all treatments were used except the prolactin treatments, in 2016 all treatments were used except the high prolactin treatment, and finally, in 2017, placebo, 11-KT and high prolactin were the only treatments used. The treatments vary among years partly due to logistical constraints. Within a colony, the locations of males assigned to different treatments were distributed haphazardly. As in Rodgers et al. (2012), implants were made with silastic tubing measuring 8 mm in length and 1.47 mm internal diameter. Placebo implants were filled with castor oil, flutamide implants were filled with flutamide powder (Sigma Aldrich, Oakville, ON), 11-KT implants were filled with 11-KT (Steraloids, Newport, RI) dissolved in castor oil (amount = 80 μg KT/implant), bromocriptine implants were filled with bromocriptine powder (Cayman Chemical, Ann Arbor, MI), and prolactin implants were filled with prolactin (Sigma Aldrich, Oakville, ON) dissolved in castor oil at one of two concentrations: low prolactin (amount = 1.25 IU/implant) and high prolactin (amount = 12.5 IU/implant). All implants were sealed at both ends with 1 mm of silicone.