Comparative endocrinology in studies of free-living animals

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Chapter 2: Hormonal mechanisms of reproductive suppression in helper males and effect of helper male presence on group members in the cooperatively breeding red-cockaded woodpecker (Picoides borealis)

ABSTRACT

In the cooperatively breeding red-cockaded woodpecker (Picoides borealis), male helpers are subordinate to male breeders, and do not mate with females. We investigated whether high levels of the stress hormone corticosterone suppress reproduction in helper males, whether the number of helper males present in a family group influences corticosterone levels of group members, and whether corticosterone levels changed seasonally. We compared baseline and maximal plasma levels of corticosterone between helper males and breeding males, and among helper males and breeders of both sexes living in groups of different sizes throughout the reproductive cycle. We also measured plasma levels of estrogen, progesterone and testosterone to examine other potential hormonal differences between helpers and breeders. Breeding status did not explain variation in any hormones, therefore our data do not support the hypothesis that helper males are reproductively suppressed via corticosterone or the other hormones investigated. However, the presence of two or more helper males in a group tended to reduce baseline corticosterone in breeding and helper males, but not breeding females, suggesting that helper males reduce the effort that males of both status classes put into parental care. Low corticosterone in helper males may also indicate that when several helpers are present they share aggression received from breeders and provide each other with social support. Seasonally, maximal corticosterone peaked during the nestling provisioning phase for breeding and helper males, but not breeder females, suggesting that males show an increased response to stressors posing a threat to survival of offspring.

INTRODUCTION

Cooperative breeding has been described in over one hundred mammal and nearly three hundred bird species (Brown 1987). In this unique reproductive strategy, some adults, termed helpers, remain reproductively inactive and help raise the young of breeding pairs to whom they are often, but not always, related. Ultimate causes for delayed reproduction in helpers have been investigated (Brown 1987, Walters et al. 1988, Arnold and Owens 1998, Conner et al. 2001), but studies describing proximate mechanisms controlling these differences in reproductive behavior between breeders and helpers are limited.
Several hypotheses have been advanced to explain the mechanisms of suppression of reproductive behavior in male helpers. Behavioral interference may prevent even reproductively capable helper males from mating. Helpers may be physically blocked from mating by breeding males, via direct aggression or mate-guarding. In pied kingfishers (Ceryle rudis), unrelated helpers are aggressively driven from the nest area by male breeders until the female is no longer receptive (Reyer et al. 1986). Dominant Mexican jay (Aphelocoma ultramarina) males actively guard their mates (Vleck and Brown 1999).
In many species, helper males exhibit lower plasma levels of testosterone than breeder males (Reyer et al. 1986, Mays et al. 1991, Schoech et al. 1991, Wingfield et al. 1991, Schoech et al. 1996). Reduced testosterone levels may be the result of lack of stimulation from breeding females (Wingfield and Ramenofsky 1985, Wingfield and Farner 1993, Schoech et al. 1996). Helpers may also exhibit high levels of progesterone (Schoech et al. 1991) or prolactin, two hormones associated with parental care (Hadley 2000) that may reduce testosterone levels or inhibit testosterone production (Nelson 2000). Low levels of testosterone may be accompanied by low body mass (Wingfield et al. 1991), small testes (Reyer et al. 1986, Wingfield et al. 1991, Schoech et al. 1996), or inability to produce sperm (Reyer et al. 1986), rendering helpers physiologically incapable of reproduction, independent of age.
Helper males may also be reproductively suppressed by the production of high levels of glucocorticoid stress hormones. Helpers are subordinate to breeders, and in socially living species, subordinates may have higher levels of the glucocorticoid hormone corticosterone (in birds) or cortisol (in most mammals) if they endure physical or psychological aggression from dominants or if they retain little control over resources such as food and mates (Goymann and Wingfield 2004). Since one of the main actions of glucocorticoids is to mobilize energy stores, subordinates may also produce high levels of these hormones if they must expend more energy than dominants to carry out daily activities such as foraging and territory defense (Goymann and Wingfield 2004). Stress hormones are well known for their suppressive effects on reproduction (Moore and Jessop 2003): they can inhibit the production of reproductive hormones or directly inhibit courtship and mating behaviors without affecting other hormones (Wingfield 1988, Moore and Jessop 2003).
The objective of this study was to investigate hormonal mechanisms that could explain reproductive suppression of subordinate helpers in the red-cockaded woodpecker (Picoides borealis). The cooperatively breeding red-cockaded woodpecker lives in family groups that consist of a breeding pair and zero to five non-breeding helpers, who are mostly male offspring of at least one member of the breeding pair. Helpers assist the breeding pair in territory defense, cavity construction, and care of offspring, including feeding and incubation, but appear to never copulate (Lennartz et al. 1987, Lape 1990, Walters 1990) or father offspring, even if the breeding bird of the opposite sex is unrelated to them (Haig et al. 1994). Male breeders and helpers maintain similar levels of testosterone throughout the breeding cycle. Furthermore, breeders and helpers are of comparable body condition and exhibit similar levels of prolactin over the duration of the breeding cycle (Khan et al. 2001). While males are capable of successful reproduction even in their first year (Lape 1990, Walters 1990), birds may remain helpers until up to eight years of age (Conner et al. 2001), therefore sexual inactivity is not due to age or sexual immaturity (Khan et al. 2001). Breeding males do not appear to engage in mate-guarding to physically block helpers from mating (Walters 1990). Therefore, it is likely that there is likely hormonal mechanism other than testosterone or prolactin inhibiting helper males from courtship and mating.
The primary goal of this study was to determine if high levels of corticosterone are a physiological mechanism mediating the reproductive inhibition of male helpers. Helpers may experience chronic stress for various reasons. Helpers partake in a significant amount of helping duties and they must cope with occasional mild aggression, other than mate guarding, from breeders (Lape 1990). Although red-cockaded woodpeckers live in stable social groups, access to potential mates may be unpredictable for helpers. Helpers maintain spatially separated foraging niches from breeders, suggestive of dominant birds maintaining greater control of food resources (Rudolph et al. 2007). As secondary objectives, we wished to determine whether the number of helper males present in a family group influences the stress levels of breeders, and whether the presence of additional helpers influences the stress levels of helpers. Since stress levels are often related to energetic demands (Goymann and Wingfield 2004), and since the breeders reduce their parental efforts in the presence of helpers (Khan and Walters 2002), stress levels of breeders may be lower in the presence of helpers. Alternatively, if the presence of helpers results in increased stress levels in male breeders, this could suggest that helpers present a challenge to the maintenance of breeding males’ social position. If the presence of additional helpers reduces the stress levels of helpers, this will lend support to the hypothesis that additional subordinate animals provide each other with “social support” (Goymann and Wingfield 2004). Finally, since energetic demands and social interactions may vary through the breeding cycle (Silverin 1998, Romero 2002), we measured corticosterone levels throughout the reproductive cycle.
We compared plasma levels of baseline and stress-induced corticosterone between helper males and breeding males, and among helpers and breeders living in family groups of different sizes, during six phases of the breeding cycle. In addition, we compared testosterone levels between male helpers and male breeders to confirm, in a second population, Khan et al’s (2001) previous finding that testosterone levels do not differ between male helpers and breeders. To investigate if there were other hormonal differences between male breeders and helpers, we also compared plasma levels of estrogen and progesterone between male helpers and breeders. Finally, we sampled breeding females opportunistically, to see if their seasonal hormonal profiles differed from those of males.

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METHODS

Study site

Our study was conducted on a population of red-cockaded woodpeckers on Marine Corps Base Camp Lejeune on the central coast of North Carolina, USA. Camp Lejeune is composed of two parts, the Main Base, an area of 110,000 acres, including 26,000 acres of open water, and the Greater Sandy Run Area, encompassing 41,000 acres (Convery 2002, Walters et al. 2005). It is only on the Main Base that red-cockaded woodpeckers reside. Woodpecker groups are divided into two subpopulations. Most groups live on the east side of the Main Base, in the Combat Town training area, the G-10 impact area, and the Northeast area. Much dispersal occurs among these areas. A smaller subpopulation resides on the west side of the Main Base, in the Verona Loop training area. There is relatively little dispersal between the two subpopulations (Walters et al. 2005). Camp Lejeune’s red-cockaded woodpecker population has been extensively monitored since 1986 (Walters et al. 2005). Birds are removed from the nest as nestlings and banded with a numbered USFWS leg band and a unique color band combination. Each individual’s group membership and social status is determined annually from behavioral observations, using criteria described in Walters et al. (1988).

Chapter 1: Introduction to stress physiology and natural history of the red-cockaded
woodpecker
Introduction
The vertebrate stress response
Comparative endocrinology in studies of free-living animals
Study species
Study area
Research goals and objectives
Literature cited
Chapter 2: Hormonal mechanisms of reproductive suppression in helper males and effect,of helper male presence on group members in the cooperatively breeding red-cockaded,woodpecker
Introduction
Methods
Results
Discussion
Literature cited
Chapter 3: Impacts of military training activities on stress hormone levels and body mass in the endangered red-cockaded woodpecker
Abstract
Introduction
Methods
Results
Discussion
Literature cited
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