Abstract

Age at first reproduction is a crucial component of individual fitness as it often determines the length of reproductive lifespan. The reproductive success of males generally varies more than that of females, but it is challenging to study because the genetic data or proper surrogate measure needed to investigate reproductive success are usually not available. In black grouse (Tetrao tetrix), a lekking species with strong male mating skew and female preference for older males, there is a strong relationship between observed matings and genetic paternity. Using this relationship, we studied the effects of morphological, and behavioral traits on probability of being territorial, mating success, and survival of yearling males. Heavier yearling males were more likely to be territorial, and higher population density increased the frequency of yearling male territoriality. Mating success was positively related to population density, lek attendance, and fighting rate, but not to morphological traits. Overwinter survival did not differ between territorial and nonterritorial yearling males. Our results show that yearling male black grouse in good condition can establish territories and have some limited mating success, especially during increasing population density. In black grouse, the direct fitness benefits gained as yearlings undoubtedly contribute substantially to individual fitness, as the high reproductive skew means few males successfully copulate during their lifetime. For other species, early reproduction may relate to individual lifetime mating success but depends both on the direction and magnitude of the relationship between age-specific mating success and survival, and, as our results also demonstrate, on extrinsic factors such as population density.

INTRODUCTION

Individual fitness is often more sensitive to changes in age at first reproduction than to changes in any other life history trait (Cole 1954; Lewontin 1965; reviewed in Roff 1992; Stearns 1992) and has consequently been the subject of much theoretical and empirical investigation. Reproduction is expected to begin when the fitness benefits of reproduction outweigh the costs of reproduction on reduced somatic growth, survival, or future reproduction opportunities (Pianka and Parker 1975; Stearns 1989, 1992). Early reproduction enables shorter generation interval and better survival to first reproduction event (Bell 1980; Stearns 1992), but delaying first reproduction can lead to longer lifespan with better reproductive success, which can compensate for the loss of early reproductive opportunities (Curio 1983; Stearns 1989; Forslund and Pärt 1995). Consequently, individuals are expected to optimize their reproductive effort according to their phenotypic quality (Pärt 1995). Understanding the factors affecting the variation in age at first reproduction is therefore seen as pivotal for estimating the consequences this variation has on individual lifetime reproductive success (Forslund and Pärt 1995).

Previous work has shown that individuals starting reproduction early in life can be both high-quality individuals capable of handling the costs of early reproduction (Zahavi 1975; Grafen 1990; Hunt et al. 2004; Descamps et al. 2006) or low-quality individuals with low likelihood of surviving to the next reproductive season (Pärt 1995). This suggests that individual determinants of early reproduction can vary especially in response to extrinsic factors, which can include population density (Ferrer et al. 2004; Krüger 2005; Cooper et al. 2009), environmental conditions during early life (Brommer et al. 1998; Prevot-Julliard et al. 2001; Descamps et al. 2008; Millon et al. 2010, 2011), timing of birth (Prevot-Julliard et al. 1999; Descamps et al. 2006), and social systems (Wiley 1974; Hawn et al. 2007; Charpentier et al. 2008). In particular, changes in population density can strongly influence the selection pressure on the age at first reproduction, and early reproduction is thought to be favored during increasing population densities because of low cost and high reward of reproduction due to less intense intraspecific competition and better offspring survival (Cole 1954; Lewontin 1965; Stevenson and Bancroft 1995). In contrast, selection should favor delayed first reproduction in stable or decreasing populations because of the low levels of reproductive success and offspring survival of young first-time breeders (Hamilton 1966; von Biela et al. 2009). Therefore, fluctuating population size might have substantial effects on individual lifetime reproductive success.

The factors influencing the age at first reproduction in females have been studied widely in birds (e.g. Brommer et al. 1998; Cooper et al. 2009; Millon et al. 2010, 2011) and mammals (e.g. Gaillard et al. 1998; Prevot-Julliard et al. 1999; Beauplet et al. 2006), but the factors underlying the age of first reproduction in males have received less attention (e.g. Komers et al 1996; Pyle 2001; Becker et al. 2008). This is because female reproductive success is easy to quantify, whereas the genetic data or reliable surrogate measures needed to accurately estimate male reproductive success are typically difficult to establish due to the mismatch of observed matings and genetic paternity (Griffith et al. 2002). However, if the field observation of male mating success is a reliable substitute for paternity data, such data can be used to estimate male reproductive success and enable the investigation of the factors underlying male life histories. Such studies are crucial, as males are generally more variable in their reproductive success than females; hence, studying solely variation in female reproductive success may lead to a biased view of the reproductive life histories of the sexes (Stearns 1992; Shuster and Wade 2003).

The black grouse (Tetrao tetrix) is a lekking species with strong sexual selection and extremely skewed mating success among males (Höglund et al. 1990; Alatalo et al. 1992). A few viable and active older males (≥2 years old; maximum observed lifespan in our study population is 7 years) obtain the vast majority of the matings at the lek, whereas yearling males are generally unsuccessful (Alatalo et al. 1992). Male mating success is related to multiple condition-dependent ornaments (e.g., eye comb size, Rintamäki et al. 2000; lyre length, Rintamäki et al. 2001; blue coloration of breast feathers, Siitari et al. 2007) and behavioral attributes (e.g., territory centrality, Hovi et al. 1994; fighting rate, and lek attendance, Höglund et al. 1997). Observed matings and genetic paternity are strongly correlated, because the act of mating and partners (if individually color ringed) are easily identifiable; most females (88%, N = 109, Lebigre et al. 2007) mate only once; and broods sired by multiple males are very rare (single-male paternity in 96.2% of the broods, N = 130, Lebigre et al. 2007). Therefore, observed mating success is an accurate measure of true male mating success and can be used as a reliable substitute for male reproductive success (assuming low variation in female reproductive success). These characteristics make black grouse an ideal species to study the variation in male reproductive success.

As female black grouse prefer older, vigorous males with multiple years of lek display for mates (Alatalo et al. 1992; Kokko et al. 1999) and experimentally increased lek display in yearling males led to substantial fitness costs (decreased survival to the next mating season, decreased future reproductive success, reduced sexual ornament size, Siitari et al. 2007), yearling males are generally assumed to delay their first breeding attempt to the following mating season. Nevertheless, some yearling male black grouse do join leks in their first year and some do successfully mate. However, it is not known what the key determinants of yearling male reproductive effort and mating success are and how these might relate to external factors such as population density, which naturally fluctuates in 6- to 7-year cycles due to the variation in annual breeding success and juvenile mortality (Ludwig et al. 2006; Helle and Wikman 2010).

In this study, we identified the factors underlying the variation in reproductive effort and mating success of yearling male black grouse using detailed behavioral observations and measures of key morphological traits. First, we identified which factors are related to yearling male territoriality, which is crucial to any mating success. Second, we investigated which morphological and behavioral traits are most significantly related to mating success of territorial yearling males. Third, we tested whether territorial and nonterritorial yearling males differ in their survival to the following mating season and identified the key determinants of survival.

MATERIALS AND METHODS

Study population

We monitored 5 study sites in Central Finland (lat 62°15′N, long 25°00′E) during the period 2001–2008. Each study site consisted of a mixed-sex winter flock and a local main lek with 5–40 territorial males. Because local hunting societies have agreed not to hunt on these leks and in the direct vicinity of our study sites, the age structure of males in our study population can be considered natural. During the study period, the local black grouse population density was first low but then increased rapidly and remained at a high level until the end of the study period (estimates are based on the wildlife triangle censuses in the preceding autumn; Helle and Wikman 2010), which resulted in a highly variable number of observed yearling males in different years and sites in the data (Figure 1).

Figure 1

Population density (line) of black grouse in Central Finland (the autumn preceding the captures and observations, based on the national wildlife triangle censuses; Helle and Wikman 2010) and the number of observed yearling males (bars) in our data during the study period 2001–2008. Number of study sites monitored in each year is shown in the bar labels.

Figure 1

Population density (line) of black grouse in Central Finland (the autumn preceding the captures and observations, based on the national wildlife triangle censuses; Helle and Wikman 2010) and the number of observed yearling males (bars) in our data during the study period 2001–2008. Number of study sites monitored in each year is shown in the bar labels.

Winter captures, and morphological and physiological measures

Each January–March, we captured black grouse from winter flocks with oat-baited walk-in traps. We sprung the traps simultaneously, and up to 20 birds were captured in 1 attempt. We covered all the traps immediately after capture to calm down the birds and to reduce any risk of hypothermia. Birds were removed from traps and placed in soft cloth bags only immediately prior to handling. Males were ringed individually with an aluminum tarsus ring and 3 colored plastic tarsus rings and aged as yearlings or older (≥2 years old) according to plumage differences (Helminen 1963). We measured the body mass (to the nearest 10g) and the maximum lyre (tail), tarsus, and wing length (to the nearest 1.0mm, 0.1mm, and 1.0mm, respectively) of all captured individuals. As physiological parameters are likely to influence males’ lekking performance, we sampled the blood (1–2ml taken from the brachial vein; Lebigre et al. 2012) from each bird to measure individual hematocrit level (the volume of red blood cells in the total blood volume) and microfilaria parasite counts (hereafter, microfilaria count).

Lek performance, mating success, and survival estimates

We monitored the lekking behavior and mating success of male black grouse from hides at the 5 study sites annually from late April to early May (i.e., during the mating season), daily from 0300 to 0900h. We drew activity maps at regular intervals and recorded the spatial location and current behavior (inactive, hissing, rookooing, or fighting; Höglund et al. 1997) of each male and the presence of females on the leks. All copulations were recorded and partners identified (if ringed). We estimated the relative proportion of behaviors carried out by each male during the entire lekking period, but due to the mutual dependence of the behaviors, we solely used male fighting rate in the analyses. Moreover, we estimated each male’s lek attendance (proportional to the highest attending male on the same lek) and territory distance from the lek center from the activity maps according to Rintamäki et al. (1995).

Males that were recorded in ≥30% of the activity maps and in ≥50% of the observation days were classified as territorial. Males that visited the leks less frequently than described above were classified as nonterritorial. This was because a male visiting a lek only occasionally might have had a territory in a nearby lek or no territory at all, and thus its lekking performance (or the lack of it) on the main lek might have been misleading. Thus, only yearling males classified as territorial were included in the male mating success analyses. We also monitored smaller leks surrounding the main leks, but yearling males classified as nonterritorial on the main lek were not observed elsewhere either. We excluded from the analyses the males (N = 8) that were captured in at least 3 consecutive years in the winter flock but had no territories at the main leks, as they may have joined the winter flocks only to forage but were not part of the lek.

We based the survival estimates on field observations. As male black grouse are strongly philopatric to the lek they first start displaying at (Höglund et al. 1999; Caizergues and Ellison 2002; Lebigre et al. 2008), we assumed that territorial males that were never seen again after the mating season had died (Alatalo et al. 1991; Siitari et al. 2007). False deaths (alive, but not seen) are more likely to occur among nonterritorial males, as they never had stable territories on the studied leks (Alatalo et al. 1992). However, as winter flocks formed of black grouse from a large area gather to feed at our study sites and the capturing rate of males is >95% of the number of individuals observed in the winter flock, the observation or capture of these males during winter is highly likely.

Statistical analyses

Our morphological, physiological, and behavioral variables were characterized by collinearity and some missing values, which are known to be problematic in model selection (Nakagawa and Freckleton 2008, 2011; Freckleton 2011). As we could not create relevant, satisfactorily loaded principal components, we selected a biologically relevant combination of individual variables without significant collinearity and missing values to form a suite of candidate models for each analysis (Supplementary Table S1). As the observed number of yearling males varied substantially between years and study sites, some year-sites had zero or very few observations. Thus, we disregarded systematic year and site effects, and combined the data from all sites and years for the analyses.

We tested which morphological traits and physiological parameters are crucial determinants of the territoriality (territorial/nonterritorial) of yearling male black grouse using binary logistic regression. To investigate the role of morphology and behavior on mating success of yearling males, we excluded the nonterritorial males from the analyses, because territoriality is a crucial step toward mating success in black grouse males, and copulations away from the lek are extremely rare (Alatalo et al. 1996a; Lebigre et al. 2007). We tested whether morphology or behavior had the strongest effects on the number of copulations of territorial yearling male black grouse with zero-inflated general linear model with Poisson error distribution. The coefficient estimates of the global submodels with standard errors are provided in the Supplementary material (Supplementary Table S2). To explore the role of morphological and physiological traits explaining the survival (survived/died) of territorial and nonterritorial yearling males to the following mating season, we used binary logistic regression. In the survival analyses of territorial males, we also included the behavioral variables in the models. The global models of each analysis are shown in Table 1.

Table 1

The global models used in the analyses

Response variable Explanatory variables 
Territoriality Mass + lyre + microfilaria + density 
No. of copulations Log(mass) + log(lyre) + microfilaria + fight+ attend + density 
Survivala Mass + lyre + microfilaria + fight + attend+ density 
Survivalb Mass + lyre + microfilaria + density 
Response variable Explanatory variables 
Territoriality Mass + lyre + microfilaria + density 
No. of copulations Log(mass) + log(lyre) + microfilaria + fight+ attend + density 
Survivala Mass + lyre + microfilaria + fight + attend+ density 
Survivalb Mass + lyre + microfilaria + density 

Mass = body mass, lyre = maximum lyre length, microfilaria = microfilaria count, density = population density in the preceding autumn, fight = fighting rate, attend = lek attendance. See MATERIALS AND METHODS for further details on the variables.

aterritorial males. bnonterritorial males.

All statistical analyses were performed in R version 2.12.2(R Development Core Team 2011). We used the Information theoretic approach based on Akaike’s information criterion (AIC-TH; Burnham and Anderson 2002) model selection procedure to select the variables that best explained our data. As the model selection indicated model uncertainty (Table 2), we used model averaging to combine the set of best models (Grueber et al. 2011). Currently, there is no consensus about the optimal cutoff point for model rejection (Burnham and Anderson 2002; Richards 2005, 2008; Bolker et al. 2009; Burnham et al. 2011; Richards et al. 2011). Therefore, we selected the models withΔi ≤ 3 (difference in the correct Akaike information criterion [AICc]) values between the best and the compared models) for model averaging, as this selection is expected to include the best model (Burnham and Anderson 2002) and was supported by large increases in AICc in the model selection after this point. Exceptionally, in the survival analysis of nonterritorial males, the null model had Δi of 2.12, but the likelihood ratio test indicated it fitted significantly worse to the data than the best candidate model (χ2 = 4.189, degrees of freedom [df] = 1, P = 0.041). Therefore, in this special case, we only averaged the candidate models with lower Δi value than the null model (Table 2).

Table 2

A suite of best candidate models (Δi ≤ 3) predicting territoriality, mating success, and survival of yearling male black grouse and their AICc values, model weights (wi), cumulative model weights (acc wi) and evidence ratios (ER). None of the analyses supported only one best model, but a suite of candidate models had considerable model weights and were averaged. Results of the model averaging are shown in Table 3. Variable names are explained in the footnote of Table 1 (and in more detail in MATERIALS AND METHODS)

Analysis/candidate model k AICc Δi wi acc wi ER 
Territoriality  
Mass + density 254.79 0.00 0.33 0.33 — 
Mass + microfilaria + density 254.86 0.07 0.32 0.65 1.04 
Mass + lyre + density 256.71 1.92 0.13 0.78 2.61 
Mass + lyre + microfilaria + density 256.80 2.01 0.12 0.90 2.73 
Mating success  
Lyre + fight + attend + density 86.28 0.00 0.34 0.34 — 
Lyre + microfilaria + fight + attend + density 87.13 0.85 0.22 0.56 1.53 
Mass + lyre + fight + attend + density 88.27 1.99 0.12 0.68 2.70 
Mass + lyre + microfilaria + fight + attend + density 88.83 2.55 0.09 0.77 3.58 
Mass + fight + attend + density 89.17 2.89 0.08 0.85 4.24 
Survivala  
Microfilaria + fight + density 100.14 0.00 0.20 0.20 — 
Microfilaria + fight + attend + density 101.29 1.15 0.11 0.31 1.78 
lyre + microfilaria + fight + density 101.85 1.71 0.08 0.39 2.35 
microfilaria + density 102.00 1.86 0.08 0.47 2.53 
mass + microfilaria + fight + density 102.40 2.26 0.06 0.53 3.10 
microfilaria + fight 103.09 2.95 0.04 0.57 4.37 
Survivalb  
mass 156.35 0.00 0.22 0.22 — 
mass + microfilaria 157.28 0.93 0.14 0.36 1.59 
mass + density 157.93 1.58 0.10 0.46 2.20 
mass + lyre 158.45 2.10 0.08 0.54 2.86 
Analysis/candidate model k AICc Δi wi acc wi ER 
Territoriality  
Mass + density 254.79 0.00 0.33 0.33 — 
Mass + microfilaria + density 254.86 0.07 0.32 0.65 1.04 
Mass + lyre + density 256.71 1.92 0.13 0.78 2.61 
Mass + lyre + microfilaria + density 256.80 2.01 0.12 0.90 2.73 
Mating success  
Lyre + fight + attend + density 86.28 0.00 0.34 0.34 — 
Lyre + microfilaria + fight + attend + density 87.13 0.85 0.22 0.56 1.53 
Mass + lyre + fight + attend + density 88.27 1.99 0.12 0.68 2.70 
Mass + lyre + microfilaria + fight + attend + density 88.83 2.55 0.09 0.77 3.58 
Mass + fight + attend + density 89.17 2.89 0.08 0.85 4.24 
Survivala  
Microfilaria + fight + density 100.14 0.00 0.20 0.20 — 
Microfilaria + fight + attend + density 101.29 1.15 0.11 0.31 1.78 
lyre + microfilaria + fight + density 101.85 1.71 0.08 0.39 2.35 
microfilaria + density 102.00 1.86 0.08 0.47 2.53 
mass + microfilaria + fight + density 102.40 2.26 0.06 0.53 3.10 
microfilaria + fight 103.09 2.95 0.04 0.57 4.37 
Survivalb  
mass 156.35 0.00 0.22 0.22 — 
mass + microfilaria 157.28 0.93 0.14 0.36 1.59 
mass + density 157.93 1.58 0.10 0.46 2.20 
mass + lyre 158.45 2.10 0.08 0.54 2.86 

aterritorial males. bnonterritorial males.

RESULTS

Territoriality

Our sample comprised 193 yearling males with complete data captured during the period 2001–2008. In total, 80 males were classified as territorial, but the number of territorial yearling males and the proportion of territorial yearling males of all yearling males varied substantially between the years. Model selection indicated that 4 candidate logistic regression models had Δi ≤ 3 and could therefore be regarded as equally describing the data (Table 2). Population density (Figure 2) and body mass were both significantly positively related to yearling male territoriality, whereas maximum lyre length and microfilaria count both contributed to model fits but were of low overall importance and had no significant individual effects on territoriality (Table 3; Supplementary Table S3). Furthermore, body mass was negatively related to population density (Figure 3) in both the territorial (rs = −0.23, N = 80, P = 0.039) and the nonterritorial yearling males (rs = −0.31, N = 113, P < 0.001).

Figure 2

The relationship between population density and the proportion of territorial yearling males (of all yearling males). Symbol size is related to the total number (log transformed) of observed yearling males in each study year. In 2001, only 1 study site was monitored and both yearling males observed were nonterritorial (i.e., 0% territorial).

Figure 2

The relationship between population density and the proportion of territorial yearling males (of all yearling males). Symbol size is related to the total number (log transformed) of observed yearling males in each study year. In 2001, only 1 study site was monitored and both yearling males observed were nonterritorial (i.e., 0% territorial).

Figure 3

The negative relationship between body mass (x– ± standard error, SE) of territorial (circles) and nonterritorial (squares) yearling male black grouse to population density. On average, territorial yearling males were heavier than nonterritorial ones. The reverse pattern in 2004 (population density: 7.0 individuals/km2) is due to the low sample size with bias toward very heavy nonterritorial males (indicated by a large SE). In 2001 (population density: 9.1 individuals/km2), only 2 yearling males were observed and both were nonterritorial.

Figure 3

The negative relationship between body mass (x– ± standard error, SE) of territorial (circles) and nonterritorial (squares) yearling male black grouse to population density. On average, territorial yearling males were heavier than nonterritorial ones. The reverse pattern in 2004 (population density: 7.0 individuals/km2) is due to the low sample size with bias toward very heavy nonterritorial males (indicated by a large SE). In 2001 (population density: 9.1 individuals/km2), only 2 yearling males were observed and both were nonterritorial.

Table 3

The coefficient estimates, unconditional standard errors, and relative importance of the explanatory variables after model averaging in territoriality, mating success, and survival analyses. Variable estimates, standard errors, and significance for each averaged model are shown in the Supplementary material (Tables S3, S4, S5 and S6)

Analysis/variable Coefficient Unconditionalstandard error Relative importance Variable significance 
Territoriality     
(intercept) −0.373 0.153   
body mass 0.870 0.328 1.00 a 
maximum lyre length 0.035 0.116 0.28 ns 
microfilaria count 0.216 0.299 0.49 ns 
population density 0.957 0.330 1.00 a 
Mating success     
(intercept) −56.584 32.015   
body mass −1.898 3.471 0.35 ns 
maximum lyre length 11.325 5.986 0.91 b 
microfilaria count −0.090 0.453 0.37 ns 
fighting rate 6.596 1.707 1.00 a 
lek attendance 1.814 1.581 1.00 ns 
population density 0.361 0.073 1.00 a 
Survivala     
(intercept) 0.437 0.270   
body mass 0.007 0.063 0.11 ns 
maximum lyre length 0.056 0.138 0.14 ns 
microfilaria count 1.750 0.757 1.00 a 
fighting rate 0.970 0.654 0.87 b 
lek attendance  −0.107 0.221 0.19 ns 
population density  −0.956 0.647 0.92 a 
Survivalb     
(intercept) −0.093 0.194   
body mass 0.790 0.414 1.00 b 
maximum lyre length −0.005 0.061 0.14 ns 
microfilaria count 0.111 0.215 0.26 ns 
population density −0.056 0.136 0.19 ns 
Analysis/variable Coefficient Unconditionalstandard error Relative importance Variable significance 
Territoriality     
(intercept) −0.373 0.153   
body mass 0.870 0.328 1.00 a 
maximum lyre length 0.035 0.116 0.28 ns 
microfilaria count 0.216 0.299 0.49 ns 
population density 0.957 0.330 1.00 a 
Mating success     
(intercept) −56.584 32.015   
body mass −1.898 3.471 0.35 ns 
maximum lyre length 11.325 5.986 0.91 b 
microfilaria count −0.090 0.453 0.37 ns 
fighting rate 6.596 1.707 1.00 a 
lek attendance 1.814 1.581 1.00 ns 
population density 0.361 0.073 1.00 a 
Survivala     
(intercept) 0.437 0.270   
body mass 0.007 0.063 0.11 ns 
maximum lyre length 0.056 0.138 0.14 ns 
microfilaria count 1.750 0.757 1.00 a 
fighting rate 0.970 0.654 0.87 b 
lek attendance  −0.107 0.221 0.19 ns 
population density  −0.956 0.647 0.92 a 
Survivalb     
(intercept) −0.093 0.194   
body mass 0.790 0.414 1.00 b 
maximum lyre length −0.005 0.061 0.14 ns 
microfilaria count 0.111 0.215 0.26 ns 
population density −0.056 0.136 0.19 ns 

Variable significance in averaged candidate models is expressed as a (significant effect in all averaged models), b (significant effect in at least one of the averaged models), and ns (no significant effects in any of the averaged models).

aterritorial males. bnonterritorial males.

Mating success

Of the 80 territorial yearling males, only 12 successfully copulated (median 1, range 1–10 copulations). Furthermore, only 1 nonterritorial male copulated (N = 1/113). All observed matings of yearling males took place during the mating seasons 2005–2007 when the population density was increasing, but not when it was high and stable (i.e., 2008). Moreover, 5 candidate models fitted the data equally well (Δi ≤ 3; Table 2). Lek attendance, fighting rate, and population density were positively associated with individual mating success (Figure 4), whereas morphology played a minor role (Table 3). The effects of fighting rate and population density were significant in all the averaged models (Supplementary Table S4). The successful yearling males tended to attend the lek more frequently and spent nearly twice the proportion of their attendance time fighting compared to the unsuccessful yearling males. We did not include male territory distance from the lek center in the analysis due to its collinearity with male fighting rate (rs = −0.45, N = 80, P < 0.001) and lek attendance (rs = −0.52, N = 80, P < 0.001). Instead, we tested the relation of the number of copulations to the male territory distance from the lek center separately: Yearling males who copulated had territories closer to the lek center than unsuccessful territorial yearling males (rs = −0.35, N = 80, P = 0.002).

Figure 4

The relationship between the number of observed copulations, lek attendance (%), and fighting rate (%) among territorial yearling male black grouse. Territorial yearling males that were frequently present at the lek and had high fighting rate were most likely togain mating success.

Figure 4

The relationship between the number of observed copulations, lek attendance (%), and fighting rate (%) among territorial yearling male black grouse. Territorial yearling males that were frequently present at the lek and had high fighting rate were most likely togain mating success.

Survival

There was no significant difference in survival to the following mating season between the territorial (58%: 46 of 80 survived) and nonterritorial (48%: 54 of 113 survived) yearling males (χ2 = 0.336, df = 1, P = 0.562). Thus, 6 candidate models for territorial yearling male survival and 4 candidate models for nonterritorial yearling male survival fitted the data equally well(Δi ≤ 3; Table 2). Fighting rate and microfilaria count were positively related and population density negatively related to the survival of territorial yearling males, whereas morphology and lek attendance were less important (Table 3; Supplementary Table S5). In contrast, body mass was positively related to survival in nonterritorial males, with other factors being of minor importance (Table 3; Supplementary Table S6).

DISCUSSION

Early reproduction is a crucial component of lifetime fitness, so it is fundamental to understand the drivers both of early reproductive effort and reproductive success. Territoriality, mating success, and survival of yearling male black grouse were related to both individual body condition and lekking behavior but in different proportions. Although yearling male territorial status (territorial/nonterritorial) was mainly determined by body mass, mating success was most strongly related to male lekking behavior, more specifically fighting rate and lek attendance. Survival to the following mating season did not differ between territorial and nonterritorial yearling males but was related to different factors. Moreover, our results indicate that population dynamics might have substantial effects on reproductive effort, mating success, and survival in yearling male black grouse. Hence, male black grouse in good body condition may be capable of establishing territories and can gain mating success as yearlings without direct survival costs, which can have a significant effect on male lifetime fitness. However, as there can be trade-offs between early reproductive effort and future reproductive success and/or survival (Williams 1966; Bell 1980; Stearns 1989), a longitudinal individual-level approach is needed to comprehensively understand the effects of age at first reproduction on lifetime fitness.

Territoriality

Territorial yearling male black grouse were significantly heavier than nonterritorial yearling males. Body mass is a key feature explaining territoriality in many lekking species, with heavy males being dominant in male–male interactions (e.g. Balmford et al. 1992; McElligott et al. 2001; Alonso et al. 2010). Moreover, lekking is energetically costly (Vehrencamp et al. 1989, Höglund et al. 1992), and heavy males are assumed to be better able at maintaining their muscle stores and dominance than light males (Bachman and Widemo 1999). In black grouse, dominance is largely determined by fighting success, and victorious males have the most central territories (Alatalo et al. 1991; Hämäläinen et al. unpublished data). However, body mass is not directly related to pairwise fighting success in yearling or older males, as other factors, including experience, may be more important in determining the outcome of fights (Kokko et al. 1998; Kokko et al. 1999; Hämäläinen et al. unpublished data). Instead, body mass is related to fighting rate (Hämäläinen et al. unpublished data) indicating that greater body mass in territorial yearling males is more likely linked to the ability to support the energetic costs of lekking, rather than the likelihood of succeeding in contests per se (see also Lebigre 2008).

Mating success

Territoriality is a crucial step toward mating success in many lekking species (e.g. Apollonio et al. 1989; Balmford et al. 1992; Höglund and Alatalo 1995). Even so, most yearling male black grouse (nearly 60% in this study) did not establish territories during their first mating season, and only 15% of the territorial yearling male black grouse managed to copulate. Moreover, as mating away from leks is rare (Lebigre et al. 2007), yearling male mating success in this species is certainly very low. Although body mass was an important determinant of yearling male territoriality, it did not directly relate to mating success, unlike in several other lekking species (e.g. Balmford et al. 1992; McElligott et al. 2001; Alonso et al. 2010). Although lyre length is related to mating success of older male black grouse (Rintamäki et al. 2001), it is unlikely to be an important determinant of yearling male mating success, despite its contribution to most of the best candidate models. As there is only minor overlap in the lyre length of yearling and older male black grouse (mean ± standard deviation [SD]: 190 ± 9 and 223±12mm for yearling (N = 92) and ≥2-year-old males (N = 103), respectively; Siitari et al. 2007), a relatively long lyre of a yearling male is nevertheless shorter compared to the lyres of older males on the same lek. This applies to other male sexual ornaments as well, and there is very little overlap in ornament size or quality (body mass, eye comb size and redness, and blue coloration; Siitari et al. 2007) between yearling and older males. Therefore, if mate choice is based purely on morphological traits, it is unlikely that yearling males would be selected and hence it is unsurprising that yearling male mating success in black grouse is unrelated to morphological traits.

Instead, yearling male reproductive success was directly related to lekking behavior and particularly to fighting rate. Fighting rate largely determines male dominance, with the most actively fighting, victorious males being the most dominant and reproductively successful (Alatalo et al. 1991; Komers et al. 1996; McElligott and Hayden 2000). Furthermore, high attendance at the lek is pivotal for mating success in many lekking species (e.g. Apollonio et al. 1989; Hill 1991; Fiske et al. 1998; Friedl and Klump 2005). In this study, lek attendance contributed to the best models explaining mating success of yearling male black grouse, but the effect of this variable was not significant in any of the best models. However, high lek attendance is important for male black grouse defending central territories, as unoccupied central territories are readily reoccupied by other males (Hovi et al. 1994, Rintamäki et al. 1999). Hence, in male black grouse, a combination of high fighting rate and high lek attendance are needed for high reproductive success.

In lekking species, the most successful males usually occupy central territories (e.g. Höglund and Lundberg 1987; Balmford et al. 1992; Hovi et al. 1994; Partecke et al. 2002; Shorey 2002, Bro-Jørgensen and Durant 2003). Male black grouse get closer to the lek center with increasing age and lekking experience, and territory centrality can be seen as an honest cue of male quality and viability (Kokko et al. 1998; Kokko et al. 1999). Leks are sometimes seen as queues where males move toward the lek center as they get older and more experienced (McDonald 1993; Bro-Jørgensen 2011). However, in black grouse, the queue discipline is not strict, and other male characteristics can strongly affect male mating success (Kokko et al. 1998). Our results indicate that yearling males that managed to copulate had territories closer to the lek center than their unsuccessful peers, supporting the idea that territory centrality is an honest cue of male quality irrespective of age.

All observed copulations of yearling males occurred in 2005–2007, when the local black grouse population started to increase after a few years of low population density (Helle and Wikman 2010). We showed that yearling male black grouse were more likely to be territorial when population density was increasing or high. Consequently, yearling males were more likely to mate in increasing population density, as they presumably had better access to females due to the presence of fewer older males in relation to yearling males compared with the situation under declining or low population density (Stevenson and Bancroft 1995; Mysterud et al. 2003). These results support the theory suggesting that early reproduction effort is favored in increasing populations (Cole 1954; Lewontin 1965) and are similar to a previous study on male Soay sheep (Ovis aries;Stevenson and Bancroft 1995). Some studies report a delayed age at first reproduction during increasing or high population density, through competition for limiting resources such as nest sites (Ferrer et al. 2004; Krüger 2005; Cooper et al. 2009). However, such resources are not as important for male black grouse, and therefore unlikely to be limiting their opportunities to mate.

Survival

Survival to the following mating season did not differ between territorial and nonterritorial yearling male black grouse. However, early reproductive investments can have negative effects on future reproductive success and/or survival (Williams 1966; Bell 1980; Stearns 1989). The fitness costs of reproductive investments usually depend on individual phenotypic quality and age (e.g. McElligott et al. 2003; Tavecchia et al. 2005; Hadley et al. 2007; Hamel et al. 2009) and can be related to external factors such as population density (Clutton-Brock et al. 1996; Festa-Bianchet et al. 1998). Therefore, the possible fitness costs of early reproductive effort in male black grouse could be deferred to their future reproductive success, and hence, were not seen in their survival to the following mating season.

For territorial yearling males, survival was positively related to fighting rate and microfilaria count. Display activity is positively related to testosterone level (Alatalo et al. 1996b, Siitari et al. 2007), but as testosterone is immunosuppressive, territorial male black grouse trade off increased display activity with lower immunity (Alatalo et al 1996b). Combined with the energetic costs of display (Vehrencamp et al. 1989, Höglund et al. 1992), this leads to increased microfilaria count (Lebigre 2008). As surviving territorial yearling males had higher microfilaria counts and fighting rates, both of which are costly, this indicates that the surviving territorial yearling males were in good condition and capable of handling the energetic costs of display, a pattern similar to that in fallow deer (Dama dama, McElligott et al. 2002). Moreover, survival of territorial yearling males was also negatively related to population density, which might reflect the favorable natal environmental conditions during population increase that enabled individuals with low body mass to survive to yearlings (see Figure 3).

Among the nonterritorial yearling males, survival was positively related only to body mass. Because territorial yearling males were heavier than nonterritorial yearling males, this indicates that body mass is a crucial parameter for all yearling males’ survival. Predation by goshawk (Accipiter gentilis) and red fox (Vulpes vulpes) is the main cause of mortality in male black grouse, with peaks during winter and especially in early summer, when males undergo a postnuptial molt (Angelstam 1984; Caizergues and Ellison 1997; Warren and Baines 2002). Molting is energetically costly (Murphy and King 1992), and the quality of the new feathers is related to body condition (Bortolotti et al. 2002). Poor-quality feathers can reduce survival by reducing flight capability and thermoregulation (Nilsson and Svensson 1996; Dawson et al. 2000). For black grouse, high predation pressure and thermoregulatory constraints during winter emphasize the importance of high body mass during molt and thus on survival.

CONCLUSIONS

We showed that territoriality, mating success, and survival of yearling male black grouse were related to both individual morphological and behavioral traits but that the determinants of each were different. Though yearling male mating success is generally low, most male black grouse do not achieve any copulation during their lifetime (Alatalo et al. 1992); hence any copulation as a yearling may be important.

Our results indicate that yearling males in good condition (heavier body mass) showed higher reproductive effort and that behavior primarily determined their mating success. Furthermore, population-level effects impacted yearling male reproductive effort, mating success, and survival. Our results support earlier conclusions that population-level effects are important determinants of age at first reproduction, and therefore also the length of reproductive lifespan. Understanding that these parameters are not only influenced by individual-level effects, but also by broader population processes such as changes in population density, is therefore fundamental to understanding the longitudinal differences in individual lifetime fitness.

Supplementary Material

Supplementary material can be found at http://www.beheco.oxfordjournals.org/

Funding

This study was funded by the Center of Excellence in Evolutionary Research in University of Jyväskylä (project no. 7211271 to R.V.A.), the Academy of Finland (project no. 7119165 to H.S.), and Emil Aaltonen’s Foundation (personal grant to M.K.). This research was carried out in compliance with the current laws of Finland. Birds were captured under the permission of the Central Finland Environmental Centre (permissions KSU-2003-L-25/254 and KSU-2002-L-4/254) and the Animal Care Committee of the University of Jyväskylä.

We thank Anna Dornhaus, 2 anonymous reviewers, and the members of the Journal Club in the division of Ecology and Evolutionary Biology in University of Jyväskylä for their helpful comments on earlier drafts of the manuscript. We would also like to thank the numerous people involved in the data collection during the project.

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