Behavioral Ecology Advance Access originally published online on December 15, 2005
Behavioral Ecology 2006 17(2):270-276; doi:10.1093/beheco/arj025
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The energetic cost of mate guarding is correlated with territorial intrusions in the New Zealand stitchbird
Ecology Group, Massey University, Private Bag 11 222, Palmerston North, New Zealand
Address correspondence to M. Low, who is now at the Australian Antarctic Division, Southern Ocean Ecosystem Program, 203 Channel Highway, Kingston 7050, Tasmania, Australia. E-mail: matt.low{at}aad.gov.au.
Received 15 June 2004; revised 12 November 2005; accepted 15 November 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Male stitchbirds (hihi) Notiomystis cincta attempt to minimize paternity losses by engaging in intense mate guarding centered on the fertile period of their social mate. While this strategy is directed at preventing intruding extrapair males from successfully achieving forced copulation with their female, it is likely to be energetically costly because of the large amount of time spent chasing intruders. In this study, I measured the energetic cost of mate guarding by recording the daily body weight of 28 breeding male stitchbirds during first clutch attempts and used a classification and regression tree (CART) analysis to assess the relationship between their weight fluctuations and (1) measures of mate-guarding intensity, (2) the total duration of extrapair male intrusions into their territory, (3) the age of the focal male, (4) the local population density, and (5) proximity to supplementary food. The CART model divided resident males into two groups based on the level of intrusions by extrapair males. For the low-intruder group, resident males maintained a stable weight during their female's fertile period, whereas, for the high-intruder group, males lost an average 4.3% of their body weight, with their weights reaching a minimum on days –1 and 0 relative to the date of first egg lay. This pattern of weight loss mirrored the pattern of extrapair territorial intrusions into the focal male's territory. While the costs of harassment associated with forced extrapair copulation have previously focused on females, this study shows that these costs can also be significant for the resident male.
Key words: body weight, energetic cost, forced copulation, mate guarding, reproductive cost, sexual conflict, sperm competition.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Whenever ejaculates of more than one male compete to fertilize the ova of a female, selection is predicted to drive the evolution of traits that maximize the fertilization success of the focal male and limit the success of rival males (Birkhead and Møller, 1992
; Prokop and Václav, 2005). Behavioral tactics used by males to overcome sperm competition involve (1) increasing the amount of their own spermatozoa delivered to the female—by increasing their ejaculate volume (Gage, 1991; Olsson, 2001) or copulation frequency (Prokop and Václav, 2005; Sillén-Tullberg, 1981) and/or (2) decreasing the amount of spermatozoa delivered to the female by rival males—by guarding the female and preventing other males from copulating (del Castillo, 2003; Herberstein et al., 2005; Westneat, 1994). These adjustments in male behavior result in reproductive expenditure being in excess of that ordinarily required to achieve fertilization (Parker, 1998) and may involve significant costs to the male (Alberts et al., 1996; Komdeur, 2001; Saeki et al., 2005).
Mate guarding, where a male closely follows a female during her fertile period to limit the copulation success of rival males, occupies a large proportion of a male's time during discrete periods of the breeding season. Because of this, mate guarding competes for expression against behaviors that would otherwise be performed. This is typically seen when mate guarding is traded-off against other factors necessary for reproduction and survival, such as (1) courtship feeding and copulation (Mougeot et al., 2002), (2) pursuit of extrapair copulations (Chuang-Dobbs et al., 2001), (3) attraction of secondary females (Pinxten and Eens, 1997), (4) predator avoidance (Cothran, 2004; Huck et al., 2004; Martín and López, 1999), (5) injury avoidance (Le Boeuf, 1974), (6) thermoregulation (Saeki et al., 2005), and (7) maintaining a positive or neutral energy balance—which may manifest as reduced male foraging times and a decreased energy intake (Alberts et al., 1996; Sparkes et al., 1996), a reduction in male body weight or condition (Komdeur, 2001; Prenter et al., 2003), a lower growth rate (Robinson and Doyle, 1985), or a reduction in stored energy reserves because of increased energy expenditure (Plaistow et al., 2003). These costs or trade-offs are important to understand as they may alter the duration, and hence effectiveness, of mate guarding (Plaistow et al., 2003; Saeki et al., 2005). The energetic cost of mate guarding is of particular interest because under conditions where it results in a negative energy balance, this demonstrates that mate guarding is extremely important to the animal under those circumstances: indeed, it has a greater fitness benefit than seeking additional food. In such cases, a version of consumer demand theory (Dawkins, 1983) could be used to indicate the strength of selection acting to produce such a choice.
Commonly, the energetic cost of mate guarding has been inferred from observations that males trade-off foraging opportunities for mate guarding, thereby reducing their potential energy intake (Alberts et al., 1996; Bryant and Tatner, 1988; Westneat, 1994). However, in these situations the possibility remains that males compensate for shorter foraging times by being more efficient during their foraging bouts (Bryant and Tatner, 1988) or by moving less, thereby limiting energy expenditure (Alberts et al., 1996; Sparkes et al., 1996). Even when experimental food supplementation or better body condition increases mate-guarding behavior (Cuthill and MacDonald, 1990; Westneat, 1994), this only demonstrates that one behavior may be traded-off against the other, not that mate guarding is necessarily energetically costly (as males may simply modify their levels of mate guarding to maintain the same energy input). Because it is usually impractical to measure all variables associated with energy intake and energy expenditure, one approach has been to take a direct measure of net energy utilization during mate guarding, by measuring glycogen and lipid reserves (Plaistow et al., 2003; Sparkes et al., 1996), measuring condition (Prenter et al., 2003), or weighing the animal (Askenmo et al., 1992; Komdeur, 2001). While this has the advantage of allowing a direct measure of energy cost to be related to mate-guarding effort, the relationship between traditional measures of mate guarding, such as mate-following behavior, and cost are not necessarily straightforward. Costs could be modified by the energetic consequences of chasing or repelling extrapair male intruders. Thus, a male closely following his mate during her fertile period may show a smaller energy deficit than one who, instead, engages in repelling extraterritorial intruders. To test this possibility, I directly measured the energetic cost of mate guarding in the stitchbird, or hihi Notiomystis cincta, a species with intense mate guarding and variable levels of extrapair intruders during the mate-guarding period (Low, 2005a,b).
The stitchbird is a medium-sized (28–43 g), sedentary passerine, which is currently restricted in its distribution to three islands off the coast of New Zealand. While stitchbirds generally form long-term socially monogamous bonds, there is considerable evidence that sperm competition is intense in this species. Testicular and cloacal protuberance volumes are among the largest recorded for any passerine species (Castro et al., 1996; Low et al., 2005), and extrapair offspring are a common feature of their mating system (35–46% of all chicks, Castro et al., 2004; Ewen et al., 1999). The male stitchbird actively mate guards his female during her fertile period (Low, 2005b), but once his mate has laid her eggs he largely ignores her and begins seeking extrapair copulations by intruding into other males' territories (Castro et al., 1996; Ewen et al., 2004; Low, 2005a,b). Extrapair copulations are almost always forced by the male and resisted to some degree by the female (Low, 2005a) and usually involve a unique face-to-face copulatory position that the female actively and aggressively avoids (Anderson, 1993; Castro et al., 1996; Low, 2005a). Mate guarding by male stitchbirds is not to prevent the female from seeking extrapair copulations but to prevent extrapair males from chasing down and forcibly inseminating the female (Low, 2005b; Low et al., 2005).
Male stitchbirds begin actively displacing other males from their territory and associating with the resident female at the beginning of the breeding season; the intensity of this behavior peaks during the few days prior to the first egg being laid by the focal female (Low, 2005b). The male maintains close proximity to his mate, and he quickly reestablishes that proximity whenever she moves away from him or he has chased off an intruder. The area from which he excludes extrapair males is contingent on the location of the female, with the male trading-off territory defense for paternity defense as the number of both intrusions and intruders increases. The resident male excludes extrapair males from 100% of his territorial area in situations of no or sporadic intrusions, whereas in extreme cases—where up to eight extrapair males may remain within the territory for extended periods—he limits his defense to a small area immediately around the female (Low, 2005b). Once the female lays her eggs the level of intruders rapidly drops to zero, mate guarding ceases, and the male leaves the territory for longer periods as he begins intruding into other males' territories whose females have since become fertile (Low, 2005a,b).
I directly measured the energetic consequences of mate guarding in this species by following male body-weight changes during the breeding season and relating this to mate guarding and the numbers of extrapair intruders being chased by the focal male. Thus, it was designed to answer two questions. First, do male weights fluctuate relative to mate-guarding intensity and their female partner's fertile period? To answer this, males were weighed on a daily basis during the breeding season using a portable weighing station. Second, can any variation in the amount of weight loss during the intense mate-guarding period be explained by the resident male chasing extraterritorial intruders? This was tested by comparing the patterns of weight loss in groups of males experiencing different levels of extrapair male intrusion and by measuring the additional distances traveled by males in order to repel intruders.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study population
Data specific to this study were collected during the 2002–2003 breeding season from the stitchbird population on Tiritiri Matangi Island (36° 36' S, 174° 53' E), located off the northeast coast of New Zealand's North Island. The island is approximately 220 ha in area, with stitchbirds restricted in their territorial distribution to the remnant forest patches comprising only 30 ha. All birds on the island were uniquely color banded and of known age and social parentage. The population was small (34 females and 41 males in 2002–2003), allowing all breeding attempts to be monitored during the breeding season from September to February. Supplementary food in the form of a 20% (w/v) sugar solution was provided from up to nine stations that were present year round and used regularly by all birds on the island. These feeding stations were necessary for the management and survival of this population (Taylor et al., 2005
). They were located at forest edges along walking paths but not within territory boundaries (distance from nest-box to nearest feeder, mean ± SD: 130 ± 92 m, n = 32, range 28–390 m). Because the stitchbird is an obligate cavity-nesting species and the island mostly comprises young regenerating forest, 110 artificial nest-boxes were provided in 2002. These were grouped in twos and threes throughout likely nesting areas and situated approximately 1.5 m off the ground with a hinged lid, which allowed easy monitoring of all nesting attempts. Based on observations of successful within-pair and extrapair copulations in this population (n = 105), the female stitchbird's fertile period is estimated to begin 6 days prior to laying of the first egg and finish the day the penultimate egg is laid (Low, 2004, 2005a).
Measuring extrapair male intrusions
Stitchbird territories were located and pairs identified by following birds in all forested areas on the island during September, when male territorial calling and female nest building began. To establish the date of nest completion and egg laying for each female, nest-boxes were monitored daily. In the period between nest completion and the third day of incubation, I took 30-min observations on focal territories and noted all extrapair intruders in 28 territories (n = 276). The timing of these observations during the day was randomly distributed among territories to control for possible temporal confounds.
To ascertain whether an extrapair male was intruding, each pair's territory boundary was determined by watching both sexes' movement and feeding patterns as well as their interactions with neighboring birds during the prefertile period. These territorial boundaries were distinct and obvious to observers and were defined as the line that the pair fed within and beyond which an extrapair male could call or be visible to the resident male without the resident male making an attempt to chase him away. This area remained generally stable for all pairs from September to February. During the female's fertile period, the focal pair utilized the entire area for feeding; however, in many cases males were found to trade-off repelling extrapair males from its outskirts in order to maintain proximity to the female (Low, 2005b). This was not a case of neighboring males expanding their territory as the focal male's area contracted as many of the intruders came from other parts of the island (Low, 2005a), and intruders were not observed feeding or calling within the focal pair's territorial boundary. For birds other than the residents entering the territory, their sex, identity, and time of entry and exit were recorded (see Low, 2004, 2005a for more details). If more than one extrapair male intruder was present in a territory at a time, then the times of each male were summed, potentially giving total male-intruder times of more than 60 min per observation hour in some territories.
Weight measurements
To determine the relationship of mate guarding and extrapair male intrusions with resident-male weight, male stitchbirds were weighed on a set of electronic scales (Weighing Systems Ltd., Nelson, New Zealand) to an accuracy of ±0.5 g once every 1–3 days from nest building (September) to chick rearing (December). The scales were attached to a hummingbird feeder containing artificial nectar so that when birds came to the supplementary feeding stations to drink, they stood on a perch linked to the weighing mechanism. An electronic readout of the bird's weight was displayed allowing the identity and weight of each bird to be recorded by the observer. Because the weight of the bird commonly increased by 0.5–1 g while drinking, only the initial weight was recorded: this was displayed within a few seconds of the bird alighting. This weight gain associated with using the feeder was temporary and reflected the ingestion of a large amount of fluid that was quickly excreted, returning the bird to its prefeeding weight before its next visit to the feeder—usually within 30 min. Males were weighed in the morning between 0800 and 1100 h to minimize the effect of diurnal weight fluctuations (Armstrong and Ewen, 2001).
Energy intake/expenditure
Because of the difficulty in accurately observing male stitchbird feeding patterns when they were in the canopy, observations of foraging were not made. Instead, I calculated the additional distance flown by males when chasing intruders from their territory as a measure of energy expenditure. While measures of energy expenditure can face similar problems to those of energy intake (Alberts et al., 1996), in birds, flying time has a highly influential effect on daily energy expenditure (Bryant and Tatner, 1988 and references therein). I contrasted two groups of males, those from 10 territories with the highest levels of extrapair intruders and those from 10 territories with zero or close to zero levels of extrapair intrusion. Resident males generally behave similarly between these two territory groupings with one exception: where intruders are present, focal males will actively fly at them and chase them out of the territory (Low, 2005a,b). Chase-flight distance was calculated for each male by multiplying the mean number of chase flights observed per hour during the mate-guarding period with the average distances of these chases. This produced a distance estimate that the males from high-intruder sites were traveling in excess of those birds at low-intruder sites.
Data analyses
General
No bird was weighed or pair observed more than once per day, and only first clutch attempts were monitored in this study. Because of the relative nesting asynchrony (mean ± SD, 5 November ± 11 days, range 52 days for onset of first egg for the 34 first clutches in 2002–2003), data collection dates were converted to a number relative to the day the first egg was laid by the female of that pair (day 0), to allow comparison of results between pairs. The periods before day –6 and after the penultimate egg was laid were labeled the prefertile and postfertile periods, respectively.
For comparisons between stages of fertility (prefertile, fertile, and postfertile), a mean weight for each male was generated from a standard interval of 6 days from each of the three time periods; this was to ensure that each male's mean weight was generated from at least three data points for each period. The prefertile period of days –12 to –7 was chosen as a time when the male typically spends a significant amount of time in the territory and with the female but does not copulate and experiences few intrusions. The fertile period of days –3 to +2 corresponded to the peak fertile period of the female (Low, 2005a), which is when the highest intensity of mate guarding (Low, 2005b) and the majority of intruder activity (Low, 2004) occur. The postfertile period of days +11 to +16 was used as it occurred 1 week after the end of the fertile period to allow for any recovery of condition by the male after the fertile period but before chick rearing began. The mean values generated for these time periods for each bird were compared using matched-pair statistical tests.
Weight data from seven males that attempted forced copulations but did not hold a territory were used for comparisons to breeding-male weights. Extrapair intruder duration and resident-male weight changes could potentially be confounded by some attribute of territory quality or the resident male and female. Thus, comparisons of levels of territorial intrusions at matched sites between years (2001–2002 and 2002–2003) and between first and second clutches within the 2001–2002 year were undertaken to determine if intrusion levels varied randomly with respect to site identity. The level of extrapair intrusions was also evaluated with respect to focal male age and condition to rule out the possibility that only poor quality males incurred intrusions and that weight changes were confounded by male quality.
Not all sites could be surveyed or birds measured in all sampling periods resulting in uneven numbers in some statistical tests. Parametric statistics were used only where data were normally distributed or could be transformed to a normal distribution (Shapiro-Wilks test: p > .05) and variances not significantly different (Levene's homogeneity of variance test: p > .05). When more than one test was performed on the same data set, a sequential Bonferroni correction was used (Rice, 1989). Means are expressed with standard errors, probability values are two tailed, and statistical significance recognized at p < .05 unless otherwise stated. With the exception of the regression tree analysis (see below), the Statistica software package (StatSoft, 1997) was used for all analyses.
Regression tree analysis
I used a regression tree analysis (De'Ath and Fabricius, 2000; Low et al., in press) to examine the relationship between changes in resident-male weight during his female's fertile period and five explanatory variables. Male weight change was calculated as a percentage of the prefertile weight; a mean weight for each male was determined for the prefertile period (between days –12 and –7) and the fertile period (days –3 to +2), and the difference between these two values was divided by the prefertile weight. The five independent variables used in the regression tree model were chosen because they were potentially important in influencing patterns of weight change during the fertile period: (1) the mean duration of extrapair male intrusions into the focal male's territory between day –3 and +2 (range 0–64 min h–1), (2) the age of the resident male in years (range 1–8), (3) the mean time the male closely associated with his female between day –3 and +2 (range 46–60 min h–1): this figure has been shown to be highly correlated with all measures of mate guarding (e.g., male-female proximity, following behavior; see Low, 2005b), (4) the distance from the nest-box to the nearest supplementary feeding station (range 28–390 m), and (5) the local population density: this was calculated by summing the total number of nest sites within a 130-m radius of the focal nest site (range 0–10). The figure of 130 m was chosen as it was the mean distance that nest-boxes were located from supplementary feeding stations in 2002–2003, and thus it was thought to be representative of the local area that birds would regularly encounter outside of their territory. Distances to supplementary feeding stations and other nest-boxes were calculated from digitized maps using global positioning system mapping software (Ozi-Explorer, 2000).
Regression trees (or classification and regression trees [CART]; Breiman et al., 1984) are a nonparametric recursive partitioning procedure, constructed by continuously dividing data into mutually exclusive groups by comparing every possible binary split in every independent variable and choosing the division that minimizes heterogeneity of the dependent variable in the resulting two groups. This process is then repeated on the next grouping level. Thus, the output resembles a tree diagram with a single node at the top containing the entire data set, with each branch a decision rule based on the values of an independent variable leading to a more homogeneous subset of the data (Rouget et al., 2004). The optimal tree size, i.e., the number of data divisions, is determined by using a cross-validation procedure that maximizes the model's prediction accuracy on data not used to build the model (De'Ath and Fabricius, 2000). For this, I used a leave-one-out cross-validation procedure and chose the model that best predicted the excluded data. This method involved excluding one observation, reconstructing the model, and then predicting the response of the excluded observation. This was repeated for the entire data set, with a correlation coefficient derived from comparing predictions to observations for each tree size. All regression tree analyses and their cross-validations were conducted using computer macros written in the MatLab programming language.
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RESULTS |
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Factors correlated with resident-male weight loss
The regression tree that best predicted changes in male weight over the female's fertile period consisted of only two terminal nodes out of a possible 14. The single decision rule used was based on intrusion rate and gave an overall R2 = .59 (Figure 1). The node occurred at an intrusion duration of 6.5 min h–1, indicating that territories with lower durations differed from those with higher durations. In the territories where extrapair male intrusions were low or nonexistent (n = 10), the resident male gained 0.96 ± 0.92% body weight during the period of intense mate guarding. This is in contrast with the territories where extrapair male intrusions were moderate to high (n = 18), in which the resident male lost 4.28 ± 0.45% body weight during the fertile period (Figure 1).
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Energetic costs as measured by male weight change
During the female's fertile period, weights for the 28 resident males dropped from a mean of 39.8 ± 0.4 g on day –6 to 38.7 ± 0.4 g on day 0. Dividing the males into two groups based on the regression tree analysis shows a clear difference in the patterns of weight change during the fertile period of the female (Figure 2).
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-) (<6.5 min h–1) or high (-•-) (>6.5 min h–1). Not all birds were weighed on all days. For "low intruder," the number of birds weighed for each mean value ranged from 7 to 10, and for "high intruder" it ranged from 15 to 18.Mean male weights during the prefertile period were similar for both groups (high intruder, n = 18: 39.9 ± 0.4 g; low intruder, n = 10: 40.0 ± 0.3 g) as were weights during the postfertile period (high intruder: 40.9 ± 0.4 g, low intruder: 41.0 ± 0.4 g), suggesting that there were no differences in the quality of these two groups. For the low-intruder group, male weights did not obviously change from the prefertile to the fertile period in contrast to the high-intruder group where they were significantly lower during the fertile period (paired t test: t = 5.39, df = 17, p < .001). Males in the high-intruder group reached their minimum weights on day –1 (38.0 ± 0.4 g) and day 0 (38.1 ± 0.4 g) (Figure 2), which corresponded to the peak in extrapair male intrusions (see also Low, 2004
). The prefertile weights of all males (regardless of intrusion duration) were significantly lower than postfertile weights (paired t test: t = 3.37, df = 26, p = .002) supporting the hypothesis that male behavior in the prefertile period, such as territorial singing and maintaining some contact with the female, involved a cost to resident males. From these results, I estimated that male behaviors aimed at securing the integrity of their territorial boundary or limiting extrapair male access to the focal female cost approximately 2.5% (1 g) of body weight, with an additional 5% (2 g) cost for males enduring significant extrapair male intrusions. By comparison, males lost 4.3 g (10.5%) during chick feeding, making the cost of chasing many intruders approximately 70% of the costs of feeding offspring (Figure 3).
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The possibility that postfertile increases in male weight were a function of the males' preparation for chick feeding rather than cessation of mate guarding was assessed by comparing breeding-male weights to the mean weights of nonpartnered males measured during the same period. Nonpartnered-male weights (mean November weights: 40.9 ± 0.3 g, n = 7) were almost identical to the weights of breeding males during their postfertile period (41.0 ± 0.3 g, n = 28) (Figure 3). Because nonpartnered males were neither mate guarding nor preparing to feed chicks, the fact that their weight mirrors that of the postfertile breeding males suggests that the postfertile weight increases are due to a reduction in mate guarding.
Extrapair male activity
Patterns of extrapair male activity and forced copulation attempts relative to the female's fertile period were very similar to that previously described in this species (Low, 2004, 2005a). Male intrusions corresponded to the day relative to egg laying and little else. Intrusions increased steadily from day –6, peaking on day 0 at 27.3 ± 8.9 min per territory per hour (n = 26), and then declined to almost zero by day 5. Intrusions varied across clutches and years. In matched comparisons on the same territory and involving the same pair, there was no correlation in intrusions between first and second clutches in 2001–2002 (11.7 ± 2.9 min h–1 versus 16.5 ± 3.1 min h–1, respectively; Pearson correlation: r = –.15, n = 30, p = .41) and were not correlated for first clutches between years (2001–2002: 8.3 ± 2.6 min h–1 versus 2002–2003: 12.4 ± 3.1 min h–1; Pearson correlation: r = –.016, n = 19, p = .94). Also, intrusion rates were not correlated with attributes of the focal male (resident-male age: Spearman rank-order correlation, rs = –.28, n = 28, p = .14; resident-male condition: Pearson correlation, r = –.32, n = 24, p = .12). Supplementary feeders did not appear to confound measures of intrusion levels. There was no significant difference between the distance of the nesting site in 2001–2002 and 2002–2003 to the nearest feeder for territories with "low" compared to "high" levels of extrapair intruders during the focal female's fertile period (144 ± 16 m versus 107 ± 16 m, respectively, t test: t = 1.6, df = 57, p = .11).
Distance traveled by resident males
In 10 territories where male intruder rates were consistently high from day –3 to +2 (23 ± 8 min h–1), resident males initiated 9.3 ± 5.1 (mean ± SD) chases h–1 of intruding extrapair males during these 6 days compared to the 0.11 ± 0.17 chases h–1 initiated by males in 10 territories with consistently low intruder rates (1 ± 0.6 min h–1). Assuming the distance traveled during each chase was approximately 60 m (30-m chase and 30-m return to the female), this equates to an additional 6.7 km being flown each day by males at sites with high intruder levels.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Few studies have directly measured the energetic cost of mate guarding, and these analyses have generally focused on invertebrates (Plaistow et al., 2003
; Prenter et al., 2003; Sparkes et al., 1996). In the only previous study where the energetic cost of mate guarding was directly measured for a vertebrate species—the Seychelles warbler Acrocephalus sechellensis—it was shown that reduced foraging during intense mate guarding was correlated with weight loss (Komdeur, 2001). My study both supports this finding and extends it; rather than the cost being correlated with the intensity of mate-guarding parameters, such as following the female, it was the energetic expenditure associated with expelling intruders from the vicinity of the female that explained much of the variance in weight loss. As intruder levels increased, males were forced to travel further in order to expel them and this was likely to have significantly increased residents' daily energy expenditure (Bryant and Tatner, 1988). However, because energy intake was not quantified, it is unclear whether these birds suffered a concurrent decrease in the quality or amount of foraging opportunities, which compounded their energy deficit.
In the current study, the termination of the regression tree after a single division indicated that duration of territorial intrusion was primarily responsible for the differences in weight loss seen in males. In cases where few or no intrusions occurred, males maintained (or even slightly increased) their weight during the fertile period. This was in contrast to territories where males lost weight when intrusions ranged from moderate to high. The fact that the model could not improve its prediction accuracy by further dividing this group of 18 males based on intrusion rates suggests that the effect of intrusions on weight loss is nonlinear: that is, higher intrusion rates result in weight loss, but the degree of weight loss cannot be predicted from relative intruder rates. One interesting aspect of this data division is that it is consistent with an observation regarding the proportion of the prefertile territory from which the resident male stitchbird can exclude extrapair males during the fertile period (Low, 2005b). Resident males could exclude extrapair males from a large part of their territory (87–100%), while concurrently mate guarding, as long as intruder levels remained below 
10 min h–1. However, as the number of both intrusions and intruders increased beyond this, a threshold was crossed where males could not simultaneously chase away all territorial intruders, resulting in a smaller defended area that centered on the position of the female. At these higher intrusion rates the defended area dropped exponentially and ranged from 0.09 to 35% of the prefertile territory (Low, 2005b). The fact that this threshold occurred at a remarkably similar level of extrapair intrusions to that highlighted by the regression tree analysis in the current study suggests that when males are forced to begin trading-off defending their territorial area from intruders because they cannot be in several places at once, this is when they are expending energy in excess of what they can consume. This switch in energy balance would explain the patterns of weight loss I observed.
During the prefertile or fertile period, breeding males might lose weight to improve their aerial performance to better expel intruders (discussed in Askenmo et al., 1992; Komdeur, 2001 and see references therein). However, such an explanation for the patterns of weight loss in the stitchbird is not supported by the findings of this study. The aerodynamic-improvement hypothesis does not account for the lower prefertile weights (compared to postfertile weights) during the period from day –18 to –6, a time when intruders are absent and females are not fertile. It also does not explain why resident males' maximum weight loss coincides with day 0, by which time most extrapair copulations have been attempted (Low, 2005a). Finally, it fails to account for why the seven nonpartnered males whose only option was to attempt forced extrapair copulations, and presumably needed good aerodynamics to do this, did not follow this weight-loss strategy. The possibility that male intrusion rates were related to factors other than the stage of fertility of the focal female also lacked support from this study. Intrusion rates were not dependent on the location or quality of the territory or the identity or quality of the focal male and female. Males did not initiate extra copulations as an additional paternity guard (see Low, 2004, 2005a,b), thus, there is no evidence that males lost weight during this time because of direct investment in copulation. Seasonal influences on male weight can be discounted due to the relative asynchrony of the female's fertile periods and the stability of nonbreeding-male weights from October to December during first clutch attempts.
While the weight loss in male stitchbirds was not as dramatic as the Seychelles warbler and did not result in males approaching their critical survival weight, this did not mean that it was of little biological relevance. Indeed, the time required for male stitchbirds to recover their weight loss was virtually the same as that seen in the Seychelles warbler (Komdeur, 2001). In populations of stitchbirds where supplementary food is not accessible (e.g., the Little Barrier Island population), weight loss during the mate-guarding period is likely to be more dramatic and may have significant consequences for the male, potentially forcing him to reduce mate-guarding intensity in favor of foraging opportunities (see Westneat, 1994).
Ethological applications of consumer demand theory (Dawkins, 1983) allow behavioral needs to be ranked based on the cost that an animal will pay in order to express them. The importance of these behaviors to the animal, and presumably selection, can then be quantified by comparing them to the cost that an animal will pay for things necessary for survival (e.g., food and water). The fact that male stitchbirds will pay a cost of up to 7.5% (3 g) of their body weight—1 g in the prefertile period and an additional 2 g in the fertile period—to expel intruders and minimize extrapair copulations suggests that there is a significant fitness benefit to the male associated with mate guarding. Indeed, this benefit is only slightly smaller than that associated with feeding offspring. It is likely that in the stitchbird, as has been found in other species, this increase in fitness is because of a reduction in extrapair copulations and fertilizations (Chuang-Dobbs et al., 2001; Komdeur et al., 1999; Pilastro et al., 2002; Westneat, 1994). This hypothesis is lent support from the fact that males will only sacrifice some of their foraging potential when the risk of sperm competition is high, i.e., during their mate's fertile period. If we also consider that the significant majority of all successful extrapair copulations are forced (Ewen et al., 1999; Low, 2005a), it is likely that forced copulation can successfully inseminate females without their cooperation in this species, an idea that is lent support from analyses of previous paternity data (Ewen et al., 1999; Low, 2005a) and an examination of the stitchbird's cloacal anatomy and unique forced copulation behaviors (Low et al., 2005). While the costs of harassment associated with forced copulation in other species have previously focused on the female (Birkhead and Møller, 1992; Foott, 1970; Olsson, 1995; Réale et al., 1996; Smuts BB and Smuts RW, 1993; Watson et al., 1998), this study shows that costs can also be significant for the female's mate when he is acting to minimize the success of forced copulation attempts. Thus, as has been recently suggested for future theoretical and empirical treatments of extrapair paternity in birds (Westneat and Stewart, 2003), assessments of reproductive costs associated with forced copulation and mate guarding need to consider their direct impact not only on females but also on both the resident male and the associated extrapair males.
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ACKNOWLEDGEMENTS |
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I thank Sally Jones, Su Sinclair, Troy Makan, Becky Lewis, Sandra Jack, Ian Fraser, Åsa Berggren, and numerous volunteers for assistance in the field and Barbara Walter, Ray Walter, Thomas-Helmig Christensen, Rachel Curtis, Ian Price, Ian McLeod, Rosalie Stamp, the New Zealand Department of Conservation, and the Supporters of Tiritiri Matangi Inc. for logistical support. Doug Armstrong kindly lent me the electronic scales and Mike Joy helped with the CART analysis. Åsa Berggren, Doug Armstrong, Ed Minot, Isabel Castro, David Westneat, and two anonymous reviewers made helpful suggestions on a previous version of this paper. This research was partly funded by the New Zealand Lottery Grants Board, the Supporters of Tiritiri Matangi Inc., and a Massey University doctoral scholarship. Nest-boxes were inspected and food provided according to Department of Conservation guidelines. All work undertaken in this study was carried out under a research permit from the New Zealand Department of Conservation and had animal ethics approval from Massey University.
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