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Logging Affects Fledgling Sex Ratios and Baseline Corticosterone in a Forest Songbird

Logging Affects Fledgling Sex Ratios and Baseline Corticosterone in a Forest Songbird

  • Rhiannon Leshyk, 
  • Erica Nol, 
  • Dawn M. Burke, 
  • Gary Burness
PLOS
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Abstract

Silviculture (logging) creates a disturbance to forested environments. The degree to which forests are modified depends on the logging prescription and forest stand characteristics. In this study we compared the effects of two methods of group-selection (“moderate” and “heavy”) silviculture (GSS) and undisturbed reference stands on stress and offspring sex ratios of a forest interior species, the Ovenbird (Seiurus aurocapilla), in Algonquin Provincial Park, Canada. Blood samples were taken from nestlings for corticosterone and molecular sexing. We found that logging creates a disturbance that is stressful for nestling Ovenbirds, as illustrated by elevated baseline corticosterone in cut sites. Ovenbirds nesting in undisturbed reference forest produce fewer male offspring per brood (proportion male = 30%) while logging with progressively greater forest disturbance, shifted the offspring sex ratio towards males (proportion male: moderate = 50%, heavy = 70%). If Ovenbirds in undisturbed forests usually produce female-biased broods, then the production of males as a result of logging may disrupt population viability. We recommend a broad examination of nestling sex ratios in response to anthropogenic disturbance to determine the generality of our findings.

Introduction

Natural selection should favour those parents who invest equally in both sexes [1]. However, when the quality of the investing parent is lowered, equal investment in both sexes may not result in the highest fitness [2]. Trivers and Willard (1973) predicted that parents should adjust the sex ratio of offspring to match the ability of a parent to invest. Specifically, mothers in better condition should produce more sons, while mothers in relatively poor condition should produce more daughters [3]. Production of sons should only be favoured if there is a reasonable probability that these sons will be able to out-compete conspecifics for mates [4], [5]. Since, in most monogamous and polygynous species males compete for females, females will nearly always reproduce while males may not be chosen for mating or may be unable to compete against other, better quality males [3]. Studies with a variety of vertebrates (feral horses [Equus caballus]: [6]; European starlings [Sturnus vulgaris]: [7]; Peafowl [Pavo cristatus]: [8]; White-crowned Sparrows [Zonotrichia leucophrys]: [9]) have shown that reducing maternal quality causes the sex-ratio to be shifted towards female offspring. Production of female offspring is linked to environmental quality [10], [11], a factor which strongly influences maternal condition.

Anthropogenic disturbances modify the landscape and consequently alter environmental quality. Such disturbances may cause stress in wildlife, resulting in elevated levels of the stress hormone corticosterone (e.g. tourism [12], pollution [13], habitat removal/disturbance [12], [13]). Since corticosterone can be quantified relatively easily from blood samples, and because of the link to quality and fitness [14], [15], it has become a tool used by conservation biologists in assessing population health in relation to environmental challenges [16]. Human landscape changes may thus have the ability to skew sex ratios if disturbance translates into a change in habitat quality.

Many neotropical migrant songbirds rely on forested habitats in temperate regions for successful breeding. Forest harvesting subjects breeding birds to conditions which can cause physiological stress [13], [17][19]. The degree to which forest environments are modified depends on the logging prescription and forest stand characteristics. For example, with group-selection silviculture (GSS), small clear-cuts (gaps, 0.03–0.07 ha) are made throughout a stand with the quantity and layout of the gaps differing across logging prescriptions. This method creates larger canopy gaps than those created through the single-tree selection system, a method applied frequently in hardwood forests [20]. GSS is favoured by some forest managers because it allows for more light to access seedlings for a longer period of time. With increased desire to shift from conventional forest harvesting (i.e., chainsaws and skidders) to more mechanized systems (i.e., feller-bunchers), and growing pressure to reduce operating costs [21], methods like GSS will likely be favoured for their efficiency.

The Ovenbird, a small (ca. 20 g) socially monogamous, sexually-monomorphic, forest interior, neotropical migrant passerine [22] is potentially, adversely impacted by GSS. Ovenbirds typically breed in large tracts of continuous forest with dense canopy cover and thick leaf litter that promotes their invertebrate prey [23], two characteristics that are disturbed or removed as a result of GSS [24]. Additionally, Ovenbirds have previously been shown as an informative species for physiology studies, making them an appropriate choice for the current study [25]. We compared the effects of no harvesting, to moderate and heavy GSS on offspring sex ratios and nestling plasma baseline corticosterone in Algonquin Provincial Park, Ontario, Canada. We do not know how Ovenbird sons and daughters differ in reproductive cost. Therefore, we predicted that broods from harvested sites would be female-biased, because poor-quality habitats may lack the resources necessary to produce the more risky males [10], [11]. In undisturbed reference sites we predicted that offspring sex ratios would not differ from parity [1]. Finally, we predicted nestling Ovenbirds from harvested sites would have elevated baseline corticosterone levels.

Materials and Methods

(a) Study area and treatments

The study was conducted in the southern portion of Algonquin Provincial Park, Ontario, Canada (45°32′N, 78°36′W) between May and August of 2008 and 2009. All sites were located in upland hardwood forest dominated by sugar maple (Acer saccharum; ∼72%). American beech (Fagus grandifolia), yellow birch (Betula alleghaniensis), eastern hemlock (Tsuga canadensis), and a very small proportion of black cherry (Prunus serotina; ∼1%) made up the remainder of the forest tree composition.

The study consisted of three harvesting treatments of differing intensity of disturbance: undisturbed, moderate disturbance and heavy disturbance. Undisturbed sites were chosen within the park's designated development and natural environment zones, or nature reserve zones. These areas do not currently permit harvesting and none has occurred within the last 60 years. Moderate disturbance sites had a mixture of small (0.03 ha) or large (0.07 ha) gaps placed strategically next to at least one mature shade sensitive tree for a total of 10–12 gaps per stand. At least 5 small gaps were placed next to yellow birch seed trees and 5 large gaps placed next to black cherry seed trees. The remainder of the stand was cut to a basal area of 18–20 m2 ha−1 following the single-tree guidelines of the Province of Ontario, Canada [26]. Heavy disturbance sites had medium-sized, 0.05 ha gaps placed uniformly in a grid 50 m from each gap centre. All harvesting was limited to the gaps and no harvesting, with the exception of skid trails for travel, was performed in the forested matrix. In the heavy disturbance sites, approximately 4 gaps of trees per hectare were removed, with an average harvested site (20 ha) containing 80 gaps (Figure 1). We used three replicate stands per each silvicultural treatment and per reference conditions, for a total of 9 sites. Sites ranged from 25–44 ha (heavy (25±10 ha [mean±SD]), moderate (35±6 ha), undisturbed (43±1 ha) and all harvesting occurred between August 2006 and February 2007. All sites were embedded in a mostly continuous forested landscape.

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Figure 1. Aerial image of two forest stands cut with group-selection silviculture (GSS) in Algonquin Provincial Park.

Heavy group-selection is outlined with a solid line in the upper left and Moderate group-selection is outlined with a dotted line in the bottom right. Undisturbed sites are similar to the unharvested forest in the upper right of the image (Source: Algonquin Forestry Authority).

https://doi.org/10.1371/journal.pone.0033124.g001

(b) Field procedures

Nest searching began when the first female Ovenbird was heard in any of the study sites; in both years, this occurred approximately in the third week of May. Nests were located by using visual or auditory cues such as female ovenbirds carrying nesting material, or defensive calls from either parent when in close proximity to the nest or by incidentally flushing incubating females. Nests were visited every 2–5 days during building and incubation to monitor status, and every day closer to the predicted hatch date (near 12 d of incubation). Nests were checked from a distance with binoculars, unless verifying the date of hatch in which case incubating females were usually flushed. Disturbance was therefore kept to a minimum and all nests were disturbed approximately equally.

Following hatching, nests were revisited once when the nestlings were 6–7 days of age, approx. 1–2 days before fledging. Individuals were weighed, measured and fitted with a unique combination of colour bands and an aluminum identification band. Two 20–50 µl blood samples were collected from each nestling within 3-min of disturbance of the nest site. Blood extraction within a 3-minute time-limit best represents a baseline sample because there is insufficient time for corticosterone to increase as a result of the acute stress response [27]. One sample (10 µl) was mixed in the field with 1 ml of lysis buffer (0.1M Tris, 0.1M EDTA, 0.1M NaCl, 0.3M n-laurylsarcosine, pH of 7.5) for later molecular sexing. The remaining sample was stored on ice for up to 4 hours before being centrifuged to remove the plasma. The blood and lysis buffer mixture, and plasma samples were initially stored at −20°C, and transferred to −80°C. All practices conformed to the rules and regulations of the Trent Animal Care Committee under Permit 08042 and samples were collected under a Canadian Wildlife Service collection permit CA 0202.

(c) Laboratory analysis

Total corticosterone concentration was determined using a corticosterone I125 double-antibody radio-immunoassay (RIA) kit (MP Biomedicals, Solon, OH, USA) following manufacturer's instructions with modifications as per [28]. Samples were run in duplicate and inter-assay variance was 9.5%.

We sexed nestlings using primers P8 and CW that amplify a gene from the CHD locus, located on both sex chromosomes [29]. Briefly, DNA was extracted using DNeasy kits (Qiagen, Mississauga, ON, Canada) following manufacturer's protocols. DNA was extracted into a final volume of 100 µl and frozen at −20°C until needed. Ovenbird nestlings were sexed using a polymerase chain reaction (PCR) amplification procedure previously outlined in [29]. PCR amplification was carried out in a Px2 Thermal Cycler (Thermo Electron Corporation, Waltham, MA, USA). PCR reaction conditions were as follows: 1.0× buffer, 2.0 mM MgCl2, 0.2 mM dNTPs, 1.6 µM CW/P2 primers, 1.25 U Taq polymerase (Invitrogen Canada Inc., Burlington, ON, Canada) and 150–250 ng extracted DNA; for a final volume of 25 µl. 10 µl PCR product was separated by gel electrophoresis at 100 V for 90 minutes on a 3% agarose gel, run in standard TAE buffer, then visualized by ethidium bromide staining. This percentage of agarose was used to aid in band separation. In addition to nestlings, blood samples collected from adults who had been sexed in the field by presence of either a cloacal protuberance (male) or brood patch (female) were molecularly sexed using the same procedure listed above to verify visual sexing techniques.

(d) Statistical Analyses

Statistical tests were performed using R 2.11.1 (The R Foundation for Statistical Computing, 2010). Data were tested for the assumptions associated with linear models where appropriate and p = 0.05 was set as the level of significance for all tests. Means are given with standard error of the mean (SE).

One nest was excluded from all analyses because it had an original clutch size of two eggs, one of which was later removed either by the parents or a predator. Daily survival rate (DSR) and nest success were calculated using the logistic exposure method [30]. We used PROC GENMOD (SAS Institute Inc. 2008) to calculate regression coefficients for logistic exposure models. Akaike's information criterion (AIC), adjusted for small sample sizes (AICc), was used to determine the best-supported models from a suite of candidate models. Models with ΔAIC values <2 were considered to have the most support. Importance weights (sum of the Akaike weights) were calculated for each parameter within the best model set to determine which should be included in the final model. To account for model uncertainty, model averaged parameter estimates were calculated for all parameters in the top model set.

Models were constructed a priori and included linear, quadratic (x+x2), and cubic (x+x2+x3) effects of nest age, and linear and quadratic (x+x2) effects of annual Julian date (hereafter, “Julian date”; Grant et al. 2005) [31]. The quadratic effect of date is plausible if we consider that survival can vary relative to temporal fluctuations in predator abundance and food availability. Furthermore, the quadratic and cubic effects of nest age take into consideration that survival can be dependent on nest stage with survival probability differing between incubation, hatching, and chick rearing. In addition to time effects, treatment (TREATMENT: heavy, moderate, or undisturbed) was included as a categorical variable in models predicting nest survival. In addition to candidate models, a constant survival model, and a global model comprised of all parameters, were constructed. Candidate models were constructed from combinations of the following parameters: linear (AGE), quadratic (AGE2), and cubic (AGE3) nest age, and linear (JULDATE), and quadratic (JULDATE2) Julian date, YEAR, TREATMENT and the interaction between linear nest age and Julian date (AGE×JULDATE). Daily survival rate and nest success (NS) were calculated using top model parameter estimates (β0 and β1x) after Shaffer (2004) [30].

Offspring sex ratio was analyzed using two common methods. A general linear mixed model (the function “lme” in the package nlme for R; the R Core team 2010) was run to determine if the proportion of males per brood (male sex ratio; calculated as a proportion of male nestlings per brood) differed across treatments. A generalized linear mixed model with binomial errors (the function “lmer” in the package lme4 for R; the R Core team 2010) was used to determine if the probability of obtaining a male nestling within a brood differed across treatments. The results were qualitatively the same, giving the same significance for both analyses. We present the results of the general linear mixed model because they are intuitively easier to interpret. We present results of two different models, one containing treatment, year and complete (complete or incomplete clutch) variables and a minimal model containing only Treatment. Site was added as a random effect to all models. To determine if male sex ratio differed from parity we used a G-test of contingency (the function “chisq.test”: the R Core team 2011).

We analyzed nestling baseline corticosterone levels and body condition using a general linear mixed model (the function “lme” in the package nlme for R; the R Core team 2010). Nestling corticosterone values was log10 transformed (Kolmogorov-Smirnov Test: d = 0.08, P>0.20) to improve spread of residuals. Nestling body condition was quantified as the residuals from a regression of individual mass on tarsus length [32] but we also present the results of analyses of mass and mass with tarsus as a covariate for comparison purposes. We chose to represent body condition as the residuals of a regression of mass on tarsus because it is a measure commonly used throughout literature and it has been shown previously that this measure satisfies critical assumptions [32]. For analysis of nestling corticosterone, treatment, body condition, sex, year and the interaction treatment×sex were included in the initial model but the interaction term was later removed as it was not significant. Initial inclusion of the treatment×sex interaction makes biological sense as either sex may respond differently to stressors (i.e. logging). Nest ID was added as a random effect to control for relatedness between siblings and was nested within Site. Site was included as a random effect to account for potential differences between sites within treatments. A Tukey's HSD test was used to identify significant differences between pairs of treatments. Nestling corticosterone results are presented as back-transformed values.

Results

During 1549 search hours over two years of study, we found 70 Ovenbird nests. More nests were found in the undisturbed treatment (n = 31) than either the moderate (n = 23) or heavy treatments (n = 15). The number of nests discovered/search hour for the undisturbed treatment was the same as for the moderate treatment (0.05), suggesting a similar abundance of nesting Ovenbird pairs in these treatment types. In contrast, the heavy treatment probably had fewer nesting Ovenbird pairs than the other treatments, as evidenced by both the lower number of nests discovered per hour of searching (0.03) and lower total number of nests found. The primary cause of nest failure was predation (55.7% of all nests) but a considerable number were abandoned (18.6%). Moreover, baseline corticosterone samples (within 3 minutes) could not be obtained for all nestlings. As a result, 106 nestlings from 23 nests were used in analyses of brood sex ratios, while 55 nestlings from 17 nests were used in corticosterone analysis. Sixty-two nests were used in calculations of nest success and daily survival rate (DSR).

The global model fit the observed data well (X2 = 258.48, df = 258, P = 0.52). The variable Treatment was not included in the top model set and was one of the least supported models overall (Table 1). Nest success was best explained by AGE and JULDATE2 (Table 1) with nest success declining both as a function of date and age. Nest success ranged from 50.2% (heavy) to 55.1% (moderate). Nest success in the undisturbed stands was intermediate (52.9%).

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Table 1. The top logistic exposure models of daily survival rate of Ovenbird nests in Algonquin Provincial Park in 2008 and 2009 as chosen using AIC model selection corrected for small sample size (AICc).

https://doi.org/10.1371/journal.pone.0033124.t001

Thirteen clutches had the same number of nestlings as eggs laid (primary sex ratio) and ten had a lower number of nestlings than eggs laid (fledgling sex ratio). Incomplete clutches resulted from unhatched eggs or nestling mortality and their subsequent removal from the nest. Because clutch reductions occurred in the time between nest checks, the mechanism responsible was usually undetermined. There was no significant difference in sex ratio between complete and incomplete nests (P = 0.19, Table 1), so both were pooled for analysis of fledging sex ratio.

Fledging sex ratio did not deviate from parity when all treatments were pooled (χ2 = 26.193, P = 0.34) but varied significantly among harvesting treatments (P = 0.031, Table 2). Broods were significantly more male-biased in the heavy treatment than the undisturbed but broods from the moderate treatment did not differ from either the heavy or undisturbed treatments (Figure 2 and Table 1). Male sex ratio did not differ across years (P = 0.91, Table 2). Nestling baseline corticosterone levels differed significantly across treatments (P<0.05, Table 3), but not across years (P = 0.25, Table 3) and nestlings from heavily harvested stands had more than twice the level of corticosterone than individuals from undisturbed stands (post hoc P = 0.003, Figure 3). Nestling corticosterone levels in moderately harvested stands were higher than those in the undisturbed stands but did not differ from those in the heavy treatment (Table 3). Nestling corticosterone values did not differ significantly between male and female nestlings (P = 0.33, Table 2; male = 8.46±4.4 ng/ml, female = 7.24±5.3 ng/ml) and there was no relationship between nestling body condition (calculated as the residuals of mass against tarsus length; r = 0.88, P<0.0001) and baseline corticosterone levels (P = 0.729, Table 3). As well, nestling body condition did not differ across treatments (F2,92 = 0.24, P = 0.80), sexes (F1,92 = 0.02, P = 0.90) or years (F1,92 = 0.01, P = 0.93; Table 4). Furthermore, neither nestling mass (F2,96 = 0.51, P = 0.60) nor nestling mass with tarsus as a covariate (F2,96 = 2.18, P = 0.12) differed across treatments (Table 4).

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Figure 2. The proportion of males within a brood within a given treatment.

Means are presented with standard error, and the number of nestlings and the number of broods within each treatment respectively are in parentheses. Different letters indicate significant differences.

https://doi.org/10.1371/journal.pone.0033124.g002

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Figure 3. Effect of harvesting treatment on the mean corticosterone levels in broods of Ovenbird nestlings.

Brood corticosterone levels were significantly higher in the Heavy logging treatment than the Undisturbed logging treatment (P = 0.003). The number of nestlings and the number of broods within each treatment respectively are in parentheses. Means and SE are presented. Different letters indicate significant differences using Tukey's unequal N HSD post hoc test.

https://doi.org/10.1371/journal.pone.0033124.g003

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Table 2. Results of a linear mixed model for nestling male sex ratio, represented as the proportion of male nestlings within a given brood.

https://doi.org/10.1371/journal.pone.0033124.t002

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Table 3. Results of a linear mixed model for nestling baseline corticosterone.

https://doi.org/10.1371/journal.pone.0033124.t003

Discussion

Logging, specifically heavy GSS, significantly increased baseline corticosterone in nestling Ovenbirds. We did not find a relationship between corticosterone and either body condition or mass, indicating that the observed increase in baseline corticosterone in logged sites was not likely the result of reduced food abundance, a mechanism previously known to elevate baseline corticosterone in nestling birds [33]. Elevation of baseline corticosterone is consistent with other studies that have shown elevated levels in response to forest harvesting [17][19] but contrasts with a specific study conducted on Ovenbirds in fragmented boreal habitats [25]. Mazerolle and Hobson (2002) found higher indices of stress in adult male Ovenbirds in contiguous forest patches but not in fragmented areas. While the results of this study are interesting, it is difficult to interpret their results in the context of our study as those authors measured both a different life stage and a different physiological index. While we investigated changes in stress hormones in developing young they measured haematological indices in adult males. Overall, chronic environmental stress in developing young as shown by elevated baseline corticosterone levels can have many sub-lethal detrimental effects including reduced immunocompetence [34], growth [34][37], cognitive ability [38] and dominance in adulthood [39].

We also detected significant nestling sex-ratio biases in logged forests. Under regular undisturbed conditions, broods contained more female nestlings, while logging shifted the offspring sex ratio towards males. It appears that logging, particularly heavy GSS, creates a more stressful environment that corresponds to an increased proportion of male offspring within a nest. However, while our patterns are strong and consistent between our two years of study, we acknowledge that our sample sizes were small and thus our results must be interpreted with caution.

Biases in avian sex ratios can occur at egg laying (primary sex ratio), hatching (secondary sex ratio) or fledging (tertiary sex ratio). Although some studies have shown that females can bias primary sex ratios in an adaptive way [40], the nature of our sampling regime did not allow us to distinguish between the various forms of sex ratio bias. In our study we are referring to fledging sex ratio as we only have gender data from nestlings at fledging age, although sex ratios in nests with complete clutches (hatching sex ratio) were not significantly different from those in which one or several eggs were lost.

Given sex allocation theory, we expected, that under undisturbed conditions, broods would contain offspring at parity (50∶50 sex ratio) [1], because breeding Ovenbirds show high reproductive success in these conditions [41]. The finding of a female-skew of Ovenbird nestling sex ratios in the undisturbed sites is thus unexpected, and intriguing. We hypothesize that the female-skew potentially stems from an opposite skew in the sex ratio of the adult breeding population. Much literature on passerine adult sex ratios shows a skew towards males [42], which is a result of lower survival rates of female birds [43][48]. This lower survival of females appears to be a result of differences in the behaviour and physiology of the sexes. In many passerines, females are the sole nest incubators, having increased metabolic demands and predation risk [49], [50]. For example in Northern Wheatears (Oenanthe oenanthe), females were depredated during 20–40% of all nest predation events, a loss that, for the most part, the male population would not experience. In migratory species, females often disperse farther even though they are usually the smaller sex [51][53]. Finally, dominant males often exclude females from resources on the wintering grounds [54], a move that further reduces survival rates of females. Given the resulting male-bias in adult sex ratios in many species, it is possible that selection favours the production of female offspring in undisturbed conditions, to counteract losses that may arise post-fledging.

Evidence exists that female sex ratio biases can arise in absence of explanatory variables [55], but what is equally difficult to understand is why a disturbance like logging would shift the sex ratio towards males. In disturbed conditions (i.e. logged sites) where parental quality might be reduced due to a general reduction in habitat quality [56], we expected that if a sex-ratio bias did occur, it would be towards the production of females [2]. However, Ovenbirds in both GSS treatments (moderate and heavy) skewed offspring sex ratio towards males, relative to the undisturbed site, suggesting an increased sensitivity of nestling females. Our observation of male-biased broods in logged sites suggests a different tactic for maximizing fitness. Experimental studies of zebra finches (Taeniopygia guttata) have shown that breeding females, when provided with low quality or restricted diets prior to laying, bias broods toward males [57], [58]. This is presumably because under poor food conditions, chick mortality is biased toward females, while under good conditions it is biased toward males [58]. Additionally, female Blue Tit (Parus caeruleus) offspring also are more sensitive to mortality than males [59]. Accordingly, a female can increase her fitness returns under conditions of food restriction if she biases her brood toward males [57], [58]. We do not have data on sex-specific mortality in Ovenbirds. However, if female nestlings are likely to suffer disproportionate mortality under heavy group-selection, perhaps in the presence of competition between the sexes for suitable post-fledgling habitat [60], then adult females may maximize fitness returns by biasing brood sex ratios toward males.

Male-biased offspring sex ratios can occur in nests with enlarged broods [59] and in those subjected to brood parasitism [61], an obvious stressor for host nestlings. The stressful post-harvest environment created by GSS harvesting may also be responsible for the male shift in our study through female nestling mortality. While female nestling mortality remains a potential mechanism, it is unlikely given the lack of significant difference in sex ratios of nestlings from complete and incomplete clutches and in the lack of difference in body condition across treatments. We speculate that female Ovenbirds manipulate the sex ratio internally prior to laying the clutch.

Although the mechanism behind the observed skew is unknown, the potential consequences can be problematic from a population standpoint. As adult female passerines already experience higher mortality throughout their annual cycle, a mechanism that further reduces their numbers could be highly detrimental to the larger breeding Ovenbird population by significantly reducing the effective population size of this monogamous species. Our study differs from other experimental studies, in that we manipulated the whole environment in contrast to a single parameter (e.g. parental provisioning [38], brood size [57]) within or directly affecting a brood. Much still remains to be understood and future studies could be focused on Ovenbird behaviour, such as whether Ovenbirds forage within the gaps or avoid them for risk of predators. Additionally, future monitoring of offspring sex ratios in both disturbed and undisturbed habitats will help to elucidate the generality of our findings for other sexually monomorphic species.

Acknowledgments

We thank all members of the field crew and others who helped to locate Ovenbird nests and to those who read and provided comments on earlier versions of this manuscript. We thank Joe Nocera for his advice on statistical analyses. Thanks to Gillian Humphries, Eleanor Proctor, Lisha Berzins, and Mitchell Beck for field assistance. We thank Paul Gelok, Rory Eckenswiller, and staff at the Algonquin Park Wildlife Research Station for providing lodging. We thank Christopher Johnstone and an anonymous referee for comments that improved the clarity of the manuscript.

Author Contributions

Conceived and designed the experiments: EN DMB GB. Performed the experiments: RFL. Analyzed the data: RFL EN GB. Contributed reagents/materials/analysis tools: EN DMB GB. Wrote the paper: RFL EN GB.

References

  1. 1. Fisher RA (1930) The genetical theory of natural selection. Oxford: Oxford University Press. RA Fisher1930The genetical theory of natural selectionOxfordOxford University Press
  2. 2. Trivers RL, Willard DE (1973) Natural Selection of Parental Ability to Vary the Sex Ratio of Offspring. Science 179: 90–92.RL TriversDE Willard1973Natural Selection of Parental Ability to Vary the Sex Ratio of Offspring.Science1799092
  3. 3. Cameron EZ, Linklater WL (2002) Sex bias in studies of sex bias: the value of daughters to mothers in poor condition. Animal Behaviour 63: F5–F8.EZ CameronWL Linklater2002Sex bias in studies of sex bias: the value of daughters to mothers in poor condition.Animal Behaviour63F5F8
  4. 4. Gorman HE, Nager RG (2004) Prenatal developmental conditions have long-term effects on offspring fecundity. Proceedings of the Royal Society of London Series B-Biological Sciences 271: 1923–1928.HE GormanRG Nager2004Prenatal developmental conditions have long-term effects on offspring fecundity.Proceedings of the Royal Society of London Series B-Biological Sciences27119231928
  5. 5. Whittingham LA, Dunn PO (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Molecular Ecology 9: 1123–1129.LA WhittinghamPO Dunn2000Offspring sex ratios in tree swallows: females in better condition produce more sons.Molecular Ecology911231129
  6. 6. Cameron EZ, Linklater WL, Stafford KJ, Veltman CJ (1999) Birth sex ratios relate to mare condition at conception in Kaimanawa horses. Behavioral Ecology 10: 472–475.EZ CameronWL LinklaterKJ StaffordCJ Veltman1999Birth sex ratios relate to mare condition at conception in Kaimanawa horses.Behavioral Ecology10472475
  7. 7. Love OP, Chin EH, Wynne-Edwards KE, Williams TD (2005) Stress hormones: A link between maternal condition and sex-biased reproductive investment. American Naturalist 166: 751–766.OP LoveEH ChinKE Wynne-EdwardsTD Williams2005Stress hormones: A link between maternal condition and sex-biased reproductive investment.American Naturalist166751766
  8. 8. Pike TW, Petrie M (2005) Maternal body condition and plasma hormones affect offspring sex ratio in peafowl. Animal Behaviour 70: 745–751.TW PikeM. Petrie2005Maternal body condition and plasma hormones affect offspring sex ratio in peafowl.Animal Behaviour70745751
  9. 9. Bonier F, Martin PR, Wingfield JC (2007) Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird. Behavioral Ecology 18: 1045–1050.F. BonierPR MartinJC Wingfield2007Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird.Behavioral Ecology1810451050
  10. 10. Addison B, Kitaysky AS, Hipfner JM (2008) Sex allocation in a monomorphic seabird with a single-egg clutch: test of the environment, mate quality, and female condition hypotheses. Behavioral Ecology and Sociobiology 63: 135–141.B. AddisonAS KitayskyJM Hipfner2008Sex allocation in a monomorphic seabird with a single-egg clutch: test of the environment, mate quality, and female condition hypotheses.Behavioral Ecology and Sociobiology63135141
  11. 11. Komdeur J, Daan S, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs. Nature 385: 522–525.J. KomdeurS. DaanJ. TinbergenC. Mateman1997Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs.Nature385522525
  12. 12. Martinez-Mota R, Valdespino C, Sanchez-Ramos MA, Serio-Silva JC (2007) Effects of forest fragmentation on the physiological stress response of black howler monkeys. Animal Conservation 10: 374–379.R. Martinez-MotaC. ValdespinoMA Sanchez-RamosJC Serio-Silva2007Effects of forest fragmentation on the physiological stress response of black howler monkeys.Animal Conservation10374379
  13. 13. Suorsa P, Helle H, Koivunen V, Huhta E, Nikula A, et al. (2004) Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment. Proceedings of the Royal Society of London Series B-Biological Sciences 271: 435–440.P. SuorsaH. HelleV. KoivunenE. HuhtaA. Nikula2004Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment.Proceedings of the Royal Society of London Series B-Biological Sciences271435440
  14. 14. Angelier F, Wingfield JC, Weimerskirch H, Chastel O (2010) Hormonal correlates of individual quality in a long-lived bird: a test of the ‘corticosterone-fitness hypothesis’. Biology Letters 6: 846–849.F. AngelierJC WingfieldH. WeimerskirchO. Chastel2010Hormonal correlates of individual quality in a long-lived bird: a test of the ‘corticosterone-fitness hypothesis’.Biology Letters6846849
  15. 15. Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Niño events. Proceedings of the National Academy of Sciences of the United States of America 98: 7366–7370.LM RomeroM. Wikelski2001Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Niño events.Proceedings of the National Academy of Sciences of the United States of America9873667370
  16. 16. Busch DS, Hayward LS (2009) Stress in a conservation context: A discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biological Conservation 142: 2844–2853.DS BuschLS Hayward2009Stress in a conservation context: A discussion of glucocorticoid actions and how levels change with conservation-relevant variables.Biological Conservation14228442853
  17. 17. Lucas JR, Freeberg TM, Egbert J, Schwabl H (2006) Fecal corticosterone, body mass, and caching rates of Carolina chickadees (Poecile carolinensis) from disturbed and undisturbed sites. Hormones and Behavior 49: 634–643.JR LucasTM FreebergJ. EgbertH. Schwabl2006Fecal corticosterone, body mass, and caching rates of Carolina chickadees (Poecile carolinensis) from disturbed and undisturbed sites.Hormones and Behavior49634643
  18. 18. Suorsa P, Huhta E, Nikula A, Nikinmaa M, Jantti A, et al. (2003) Forest management is associated with physiological stress in an old-growth forest passerine. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 963–969.P. SuorsaE. HuhtaA. NikulaM. NikinmaaA. Jantti2003Forest management is associated with physiological stress in an old-growth forest passerine.Proceedings of the Royal Society of London Series B-Biological Sciences270963969
  19. 19. Wasser SK, Bevis K, King G, Hanson E (1997) Noninvasive physiological measures of disturbance in the Northern Spotted Owl. Conservation Biology 11: 1019–1022.SK WasserK. BevisG. KingE. Hanson1997Noninvasive physiological measures of disturbance in the Northern Spotted Owl.Conservation Biology1110191022
  20. 20. Jobes AP, Nol E, Voigt DR (2004) Effects of selection cutting on bird communities in contiguous eastern hardwood forests. Journal of Wildlife Management 68: 51–60.AP JobesE. NolDR Voigt2004Effects of selection cutting on bird communities in contiguous eastern hardwood forests.Journal of Wildlife Management685160
  21. 21. McNamara R, Meek P, Alvarez É (1999) Strategies for reducing the cost of mechanized selection harvesting in hardwood forests. 8 p.R. McNamaraP. MeekÉ. Alvarez1999Strategies for reducing the cost of mechanized selection harvesting in hardwood forests.FERIC – Technical Note TN-298 Pointe Claire, QC. 8 FERIC – Technical Note TN-298 Pointe Claire, QC.
  22. 22. Van Horn MA, Donovan TM (1994) Ovenbird (Seiurus aurocapilla). MA Van HornTM Donovan1994Ovenbird (Seiurus aurocapilla).The Birds of North America Online: Cornell Lab of Ornithology. The Birds of North America Online: Cornell Lab of Ornithology.
  23. 23. Burke DM, Nol E (1998) Influence of food abundance, nest-site habitat, and forest fragmentation on breeding ovenbirds. Auk 115: 96–104.DM BurkeE. Nol1998Influence of food abundance, nest-site habitat, and forest fragmentation on breeding ovenbirds.Auk11596104
  24. 24. Brais S, Camire C (1998) Soil compaction induced by careful logging in the claybelt region of northwestern Quebec (Canada). Canadian Journal of Soil Science 78: 197–206.S. BraisC. Camire1998Soil compaction induced by careful logging in the claybelt region of northwestern Quebec (Canada).Canadian Journal of Soil Science78197206
  25. 25. Mazerolle DF, Hobson KA (2002) Physiological ramifications of habitat selection in territorial male ovenbirds: consequences of landscape fragmentation. Oecologia 130: 356–363.DF MazerolleKA Hobson2002Physiological ramifications of habitat selection in territorial male ovenbirds: consequences of landscape fragmentation.Oecologia130356363
  26. 26. Ontario Ministry of Natural Resources (OMNR) (2000) A silviculture guide to managing southern Ontario forests, Version 1.1 Queen's Printer for Ontario. 581 p.Ontario Ministry of Natural Resources (OMNR)2000A silviculture guide to managing southern Ontario forests, Version 1.1 Queen's Printer for Ontario.Toronto, ON. 581 Toronto, ON.
  27. 27. Romero LM, Romero RC (2002) Corticosterone responses in wild birds: The importance of rapid initial sampling. Condor 104: 129–135.LM RomeroRC Romero2002Corticosterone responses in wild birds: The importance of rapid initial sampling.Condor104129135
  28. 28. Washburn BE, Morris DL, Millspaugh JJ, Faaborg J, Schulz JH (2002) Using a commercially available radioimmunoassay to quantify corticosterone in avian plasma. Condor 104: 558–563.BE WashburnDL MorrisJJ MillspaughJ. FaaborgJH Schulz2002Using a commercially available radioimmunoassay to quantify corticosterone in avian plasma.Condor104558563
  29. 29. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Molecular Ecology 7: 1071–1075.R. GriffithsMC DoubleK. OrrRJG Dawson1998A DNA test to sex most birds.Molecular Ecology710711075
  30. 30. Shaffer TL (2004) A unified approach to analyzing nest success. Auk 121: 526–540.TL Shaffer2004A unified approach to analyzing nest success.Auk121526540
  31. 31. Grant TA, Shaffer TL, Madden EM, Pietz PJ (2005) Time-specific variation in passerine nest survival: New insights into old questions. Auk 122: 661–672.TA GrantTL ShafferEM MaddenPJ Pietz2005Time-specific variation in passerine nest survival: New insights into old questions.Auk122661672
  32. 32. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: Validating body condition indices. Ecology 86: 155–163.AI Schulte-HosteddeB. ZinnerJS MillarGJ Hickling2005Restitution of mass-size residuals: Validating body condition indices.Ecology86155163
  33. 33. Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 171: 701–709.AS KitayskyEV KitaiskaiaJC WingfieldJF Piatt2001Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks.Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology171701709
  34. 34. Saino N, Suffritti C, Martinelli R, Rubolini D, Møller AP (2003) Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behavioral Ecology 14: 318–325.N. SainoC. SuffrittiR. MartinelliD. RuboliniAP Møller2003Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica).Behavioral Ecology14318325
  35. 35. Loiseau C, Sorci G, Dano S, Chastel O (2008) Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in house sparrows. General and Comparative Endocrinology 155: 101–108.C. LoiseauG. SorciS. DanoO. Chastel2008Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in house sparrows.General and Comparative Endocrinology155101108
  36. 36. Love OP, Williams TD (2008) Plasticity in the adrenocortical response of a free-living vertebrate: The role of pre- and post-natal developmental stress. Hormones and Behavior 54: 496–505.OP LoveTD Williams2008Plasticity in the adrenocortical response of a free-living vertebrate: The role of pre- and post-natal developmental stress.Hormones and Behavior54496505
  37. 37. Müller C, Jenni-Eiermann S, Jenni L (2009) Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian kestrels Falco tinnunculus. Journal of Experimental Biology 212: 1405–1412.C. MüllerS. Jenni-EiermannL. Jenni2009Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian kestrels Falco tinnunculus.Journal of Experimental Biology21214051412
  38. 38. Kitaysky AS, Kitaiskaia E, Piatt J, Wingfield JC (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Hormones and Behavior 43: 140–149.AS KitayskyE. KitaiskaiaJ. PiattJC Wingfield2003Benefits and costs of increased levels of corticosterone in seabird chicks.Hormones and Behavior43140149
  39. 39. Spencer KA, Verhulst S (2007) Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata). Hormones and Behavior 51: 273–280.KA SpencerS. Verhulst2007Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata).Hormones and Behavior51273280
  40. 40. Arnold KE, Orr KJ, Griffiths R (2003) Primary sex ratios in birds: problems with molecular sex identification of undeveloped eggs. Molecular Ecology 12: 3451–3458.KE ArnoldKJ OrrR. Griffiths2003Primary sex ratios in birds: problems with molecular sex identification of undeveloped eggs.Molecular Ecology1234513458
  41. 41. Burke DM, Nol E (2000) Landscape and fragment size effects on reproductive success of forest-breeding birds in Ontario. Ecological Applications 10: 1749–1761.DM BurkeE. Nol2000Landscape and fragment size effects on reproductive success of forest-breeding birds in Ontario.Ecological Applications1017491761
  42. 42. Donald PF (2007) Adult sex ratios in wild bird populations. Ibis 149: 671–692.PF Donald2007Adult sex ratios in wild bird populations.Ibis149671692
  43. 43. Blums P, Mednis A (1996) Secondary sex ratio in Anatinae. Auk 113: 505–511.P. BlumsA. Mednis1996Secondary sex ratio in Anatinae.Auk113505511
  44. 44. Burger LW, Dailey TV, Kurzejeski EW, Ryan MR (1995) Survival and cause-specific mortality of northern bobwhite in Missouri. Journal of Wildlife Management 59: 401–410.LW BurgerTV DaileyEW KurzejeskiMR Ryan1995Survival and cause-specific mortality of northern bobwhite in Missouri.Journal of Wildlife Management59401410
  45. 45. Gardner JL, Magrath RD, Kokko H (2003) Stepping stones of life: natal dispersal in the group-living but noncooperative speckled warbler. Animal Behaviour 66: 521–530.JL GardnerRD MagrathH. Kokko2003Stepping stones of life: natal dispersal in the group-living but noncooperative speckled warbler.Animal Behaviour66521530
  46. 46. Gerlach J, Le Maitre S (2001) Sex ratio variation in small island populations of an endangered bird, the Seychelles Magpie Robin, Copsychus sechellarum. Ostrich 72: 114–117.J. GerlachS. Le Maitre2001Sex ratio variation in small island populations of an endangered bird, the Seychelles Magpie Robin, Copsychus sechellarum.Ostrich72114117
  47. 47. Githiru M, Lens L (2006) Annual survival and turnover rates of an Afrotropical robin in a fragmented forest. Biodiversity and Conservation 15: 3315–3327.M. GithiruL. Lens2006Annual survival and turnover rates of an Afrotropical robin in a fragmented forest.Biodiversity and Conservation1533153327
  48. 48. Woolfenden BE, Gibbs HL, Sealy SG (2001) Demography of Brown-headed Cowbirds at Delta Marsh, Manitoba. Auk 118: 156–166.BE WoolfendenHL GibbsSG Sealy2001Demography of Brown-headed Cowbirds at Delta Marsh, Manitoba.Auk118156166
  49. 49. Low M, Arlt D, Eggers S, Pärt T (2010) Habitat-specific differences in adult survival rates and its links to parental workload and on-nest predation. Journal of Animal Ecology 79: 214–224.M. LowD. ArltS. EggersT. Pärt2010Habitat-specific differences in adult survival rates and its links to parental workload and on-nest predation.Journal of Animal Ecology79214224
  50. 50. Reidy JL, Stake MM, Thompson FR (2009) Nocturnal Predation of Females on Nests: An Important Source of Mortality for Golden-checked Warblers? Wilson Journal of Ornithology 121: 416–421.JL ReidyMM StakeFR Thompson2009Nocturnal Predation of Females on Nests: An Important Source of Mortality for Golden-checked Warblers?Wilson Journal of Ornithology121416421
  51. 51. Catry P, Lecoq M, Araujo A, Conway G, Felgueiras M, et al. (2005) Differential migration of chiffchaffs Phylloscopus collybita and P ibericus in Europe and Africa. Journal of Avian Biology 36: 184–190.P. CatryM. LecoqA. AraujoG. ConwayM. Felgueiras2005Differential migration of chiffchaffs Phylloscopus collybita and P ibericus in Europe and Africa.Journal of Avian Biology36184190
  52. 52. Kjellen N (1994) Differences in age and sex-ratio among migrating and wintering raptors in southern Sweden. Auk 111: 274–284.N. Kjellen1994Differences in age and sex-ratio among migrating and wintering raptors in southern Sweden.Auk111274284
  53. 53. Stouffer PC, Dwyer GM (2003) Sex-biased winter distribution and timing of migration of Hermit Thrushes (Catharus guttatus) in Eastern North America. Auk 120: 836–847.PC StoufferGM Dwyer2003Sex-biased winter distribution and timing of migration of Hermit Thrushes (Catharus guttatus) in Eastern North America.Auk120836847
  54. 54. Marra PP, Holmes RT (2001) Consequences of dominance-mediated habitat segregation in American Redstarts during the nonbreeding season. Auk 118: 92–104.PP MarraRT Holmes2001Consequences of dominance-mediated habitat segregation in American Redstarts during the nonbreeding season.Auk11892104
  55. 55. Paxton EH, Sogge MK, McCarthey TD, Keim P (2002) Nestling sex ratio in the Southwestern Willow Flycatcher. Condor 104: 877–881.EH PaxtonMK SoggeTD McCartheyP. Keim2002Nestling sex ratio in the Southwestern Willow Flycatcher.Condor104877881
  56. 56. Tozer DC, Burke DM, Nol E, Elliott KA (2010) Short-term effects of group-selection harvesting on breeding birds in a northern hardwood forest. Forest Ecology and Management 259: 1522–1529.DC TozerDM BurkeE. NolKA Elliott2010Short-term effects of group-selection harvesting on breeding birds in a northern hardwood forest.Forest Ecology and Management25915221529
  57. 57. Bradbury RR, Blakey JK (1998) Diet, maternal condition, and offspring sex ratio in the zebra finch, Poephila guttata. Proceedings of the Royal Society of London Series B-Biological Sciences 265: 895–899.RR BradburyJK Blakey1998Diet, maternal condition, and offspring sex ratio in the zebra finch, Poephila guttata.Proceedings of the Royal Society of London Series B-Biological Sciences265895899
  58. 58. Kilner R (1998) Primary and secondary sex ratio manipulation by zebra finches. Animal Behaviour 56: 155–164.R. Kilner1998Primary and secondary sex ratio manipulation by zebra finches.Animal Behaviour56155164
  59. 59. Raberg L, Stjernman M, Nilsson JA (2005) Sex and environmental sensitivity in blue tit nestlings. Oecologia 145: 496–503.L. RabergM. StjernmanJA Nilsson2005Sex and environmental sensitivity in blue tit nestlings.Oecologia145496503
  60. 60. King DI, Degraaf RM, Smith ML, Buonaccorsi JP (2006) Habitat selection and habitat-specific survival of fledgling ovenbirds (Seiurus aurocapilla). Journal of Zoology 269: 414–421.DI KingRM DegraafML SmithJP Buonaccorsi2006Habitat selection and habitat-specific survival of fledgling ovenbirds (Seiurus aurocapilla).Journal of Zoology269414421
  61. 61. Zanette L, MacDougall-Shakleton E, Clinchy M, Smith JNM (2005) Brown-headed cowbirds skew host offspring sex ratios. Ecology 86: 815–820.L. ZanetteE. MacDougall-ShakletonM. ClinchyJNM Smith2005Brown-headed cowbirds skew host offspring sex ratios.Ecology86815820