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desertion in the Rock Sparrow Petronia petronia. M. GriGGio 1,3 and G. Venuto 2. 1 Dipartimento di Biologia, Università di Padova, Via U. Bassi 58/B, I-35131 ...
Ethology Ecology & Evolution 19: 175-182, 2007

The relationship between mate guarding and brood desertion in the Rock Sparrow Petronia petronia M. Griggio

1,3

and G. Venuto

2

1

Dipartimento di Biologia, Università di Padova, Via U. Bassi 58/B, I-35131 Padova, Italy 2 Dipartimento di Ecologia, Università della Calabria, Via P. Bucci Cubo 4/B, I-87036 Arcavacata di Rende (Cosenza), Italy Received 25 February 2006, accepted 30 May 2007

In several bird species, members of a breeding pair typically face a tradeoff between remating, and consequently deserting the brood, or continuing the original parental effort. The solution of this conflict depends, together with other factors, on the interactions between the paired birds. The Rock Sparrow Petronia petronia is an unusual species in which brood desertion occurs in both sexes and males concurrently engage in parental care and in within- or extrapair sexual behaviours. For these reasons the Rock Sparrow is an excellent species to study the behavioural interactions between pair members in this trade-off context. We studied the sexual behaviour (courtship displays, number of copulations and mate guarding) between pair members before the desertion event in order to obtain a clearer understanding of the process of brood desertion and/or to understand the factors ruling male investment in the current and future reproductive events. In particular, we compared the sexual behaviour of the pair members divided in three groups of pairs: females that cooperate with males (Biparental nests); males that deserted the brood (Female-only nests) and females that deserted (Male-only nests). During the female’s fertile period, males that will desert the brood guarded and courted their females significantly more than other males. Moreover, during the young’s care phase, males guarded their deserting females more than other males. These results indicate that pair member interactions are important in the desertion process, as assumed by recent theoretical models. This is one of the few studies to show the importance of mate guarding in the brood desertion process. key words:

birds, Alps, sexual behaviours, courtship displays, brood desertion, pair member interactions.

Introduction Methods . Results . 3

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Corresponding author: Matteo Griggio (E-mail: [email protected]).

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M. Griggio and G. Venuto Discussion . . Acknowledgements References . .

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INTRODUCTION

The mating strategy of an individual that is caring for offspring is based on a trade-off between remating, and consequently deserting the brood, or continuing the original parental effort. The solution of this conflict depends, together with other factors, also on the interactions between the members of the breeding pair (e.g. Valera et al. 1997, McNamara et al. 2002). Many studies have demonstrated that extra-pair copulations are a strategy adopted by males to increase their reproductive success and females may obtain genetic benefits (Birkhead & Møller 1992). Mate guarding, in which a male follows his mate closely to prevent opportunities for mating with extrapair males, is a common paternity assurance mechanism adopted not only by birds (e.g. Birkhead 1982, Birkhead & Møller 1992), but also by other taxa (e.g. Cuadrado 1998, Morbey 2002, Ritz & Sakaluk 2002, Rolland et al. 2003). The temporal variation in mate guarding behaviour is different between bird species: both in duration and in its intensity (Møller 1987, Birkhead & Møller 1992). In some species mate guarding is concentrated around the start of egg-laying (Arvidsson 1992), while in others it occurs during the entire egglaying period (Birkhead 1982). In Rock Sparrows, Petronia petronia it seems that this behaviour plays an important role not only in the female’s fertile period, but also during the offspring care period because within-pair, as well as extra-pair sexual behaviours, are normally observed in the population both during the fertile and the fledgling periods (Griggio et al. 2005a). So, unlike most bird species, where the sexual and parental activities are widely separated in time (Ketterson & Nolan 1994), male Rock Sparrows concurrently engage in offspring care and sexual behaviours (Griggio et al. 2005a). In recognition of this uncommon behaviour it was proposed that a male Rock Sparrow is trying to increase his reproductive success in terms of offspring number (Griggio et al. 2005a). Copulating during the nestling stage could be a means of retaining his present female for a second breeding attempt. Even if the female re-nested with another male, the first male may increase his chances of obtaining some paternity in that nest (Griggio et al. 2005a), because female birds can store viable sperm for more than one week after insemination (Birkhead & Møller 1992). This high individual variability in sexual behaviour (Pilastro et al. 2003, Griggio et al. 2005a), offers the opportunity to capture some behavioural components of sexual conflict that recent literature is seeking (e.g. McNamara et al. 2002, Houston et al. 2005). As proposed by Székely et al. (1996), the first step to answering the question of which mate’s behaviour signals its intention to desert, is to collect detailed information about behavioural dynamics between pair members. To obtain a clearer understanding of the desertion process we compared the behaviours before the desertion time among three different groups of breeding pairs in which (1) males and females collaborated in parental care (Biparental nests); (2) females deserted the first brood and re-nested (Male-only nests, for more details see Pilastro et al. 2001), and (3) males deserted the brood, stopped feeding the young and were seen in a secondary nest (Female-only nests). Throughout these comparisons, not only did we investigated the behavioural interactions between pair mem-

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177

bers, but at the same time, we looked for cues that might forecast parent desertion strategies in the three different scenarios.

METHODS Study species A north Italian alpine population of Rock Sparrow is the object of a long-term study (Mingozzi et al. 1994) concerning breeding biology, trophic and reproductive strategies, local survival and dispersal (Tavecchia et al. 2002; Griggio et al. 2003a, 2003b). This population presents a wide array of mating patterns, including monogamy, polygyny and sequential polyandry (Mingozzi et al. 1994, Pilastro et al. 2001, Griggio et al. 2003b). The Rock Sparrow exhibits a biparental care system that is highly variable. Some males cooperate with the females during the first week after hatching, then usually decrease their food provisioning rate as the nestlings age, to the extent that during the last period most of the provisioning is performed by the female alone, and females take complete care of broods when males have abandoned the brood (about 25% of entire male population). Less frequently some males may take exclusive care of the nestlings when their females begin to lay a second clutch (about 10% of the females that have successfully raised their first brood, Pilastro et al. 2001). When males do not feed the young, they often remain at the nest and regularly court and copulate with their mate, probably because double-brooding females become fertile again before the young of the first brood fledge (Pilastro et al. 2003, Griggio et al. 2005a). In our population polygynous males seem to have a higher annual fledgling success than monogamous males, but an elevated extrapair paternity rate causes polygynous males to suffer a higher proportion of extrapair young in their broods than monogamous males (Pilastro et al. 2002). So, when corrected for paternity, the fledgling success does not seem to differ significantly with male mating status, despite the fact that monogamous males guard their mates more intensely than polygynous males. This indicates a male trade-off between attracting a new mate and protecting paternity (Pilastro et al. 2002) and underlines the importance of mate guarding as an anti-cuckoldry tactic in this species, as well as frequent courtship displays (Pilastro et al. 2003, Matessi et al. 2005). In the Rock Sparrow both sexes possess the yellow patch (a carotenoid-based trait) which is sexually selected by females and males (Griggio et al. 2005b, 2007). In females the yellow patch size is positively correlated with body mass (Pilastro et al. 2003) and in males it is used as a badge of status (Griggio et al. 2007).

Study area The study was carried out in the upper Susa valley, Western Italian Alps (44°56’N 6°48’E) in an area, close to the French border, of about 12.8 km2 including the three small villages of San Sicario (1570 m a.s.l.), Champlas Seguin (1780 m) and Champlas Janvier (1784 m). A mean of 40 nest boxes each year were set up in the area (Venuto et al. 2005). Nest boxes were designed also to work, when necessary, as trapping devices and adults trapped within the nest were individually colour-ringed and measured (Mingozzi et al. 1994). The population included about 20 breeding pairs each year (Pilastro et al. 2003).

Field work During the whole breeding season, from 1998 to 2000, and from 2002 to 2004 we made 1 hr behavioural observation per pair every 2-3 days, in order to determine the pair bond and to study reproductive behaviour (Pilastro et al. 2003, Griggio et al. 2003a). We carried out

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observations on 55 nests (1998 = 11, 1999 = 10, 2000 = 12, 2002 = 6, 2003 = 7, 2004 = 9) for a total of 525 hr. Mean observation time per nest ± SE was 9.54 ± 0.36 hr (range: 7-17 hr). We observed nest entrance with × 20-60 spotting scopes while sitting in the open, 30-50 m from the nest. Each nest was observed during the morning and late afternoon (06:00-10:30 and 15:30-19:00 hr), when the level of activity at the nest is highest (Griggio et al. 2003a). We recorded the rate of courtship displays (min/hr) and the copulation rate (copulations/hr). A mate-guarding index was calculated as the proportion of arrivals to, and departures from the nest in which the male was following the female (Griggio et al. 2005a). Brood desertion was determined by observing families in which one parent was no longer present at the nest and was observed in a second nest (for more details see Pilastro et al. 2001). Desertion was assumed to have taken place midway between the date the partner was seen for the last time and the subsequent observation (Székely & Lessells 1993). We recorded the sexual behaviours in two breeding periods: the female’s fertile period and the offspring care period before the desertion date of one partner. We assumed that the female’s fertile period starts 6 days before the first egg is laid and finishes the day of the penultimate egg deposition (Birkhead & Møller 1992, Pilastro et al. 2002). After hatching the chicks stay into the nest for about 18 days (offspring care period). Finally, we distinguished three types of breeding pairs according to the desertion pattern. The first group was represented by pairs in which females laid only one clutch during a given breeding season and both parents cooperate in parental activity (Biparental nests, N = 30). A second group includes pairs where males deserted the brood, stopped feeding the young in the first nest and were seen in a second nest (Female-only nests, N = 16). Finally, the group in which females deserted the first brood (stopped feeding the young) to breed in a second nest (Male-only nests, N = 9). The breast patch size was measured by placing a strip of transparent acetate on the patch and drawing the contour of the yellow area. We used the major axis as an index of patch size. A detailed description of the patch measurements can be found in Pilastro et al. (2003) or Griggio et al. (2005b). We obtained data on breast patch sizes for 36 males and 39 females.

Statistical analyses Statistical analyses were performed using SPSS 13.0 (Norušis 1993). Proportions were arcsine transformed and log transformation was used where appropriate. Where normality and homogeneity of variances were not met even after transformation, we used nonparametric statistics (Zar 1974). Unless otherwise stated, means ± 1 SE are given, and all probabilities are two-tailed. We compared the behaviours of Rock Sparrows among the three groups before the date of desertion, with day 9 after hatching considered to be the ‘date of desertion’ in biparental pairs. This time represents the average date between male’s and female’s date of desertion. We compared the behaviour of male and female Rock Sparrows using ANOVA or repeated measures ANOVA. For all the analyses, we entered the group (male-only, female-only or biparental) and the year of observation as factors and the date in which the female started to lay as a covariate. We checked for differences among years in laying date. Neither laying date or brood size (either before or after desertion) differed significantly among years (all F6,54 < 0.8, P > 0.57). Neither year (entered as a factor) or laying date (entered as a covariate), or their interaction, were significant at P < 0.05 in any ANOVA in which sexual behaviours of Rock Sparrow pairs were compared among groups, so they were removed from the models.

RESULTS

The sexual behaviour (courtship display and copulation rate) of males did not differ significantly among the three groups, both during the female’s fertile period

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179 Table 1.

Sexual behaviour of the three groups of breeding pairs (Biparental, Female-only and Male-only) of Rock Sparrow at their nest during the female’s fertile period (from 10 days before the female started to lay her clutch until the last egg was laid) and during the offspring care period (from hatching to desertion or to day 9 after hatching in biparental pairs). Three groups of pairs are distinguished in relation to the occurrence of male and female desertion. Means and (SE) are given (repeated measure ANOVA, within groups: variation between periods; between groups: interaction between period and group).

Period

Courtship display (min/hr)

Copulation rate (copulations/hr)

Mate guarding index *

Biparental Female-only Male-only (N = 30) (N = 16) (N = 9)

Repeated measure ANOVA Within groups

Between groups

Female’s fertile

1.01 (0.19)

1.80 (0.40)

1.29 (0.30) F1,52 = 25.52 F2,52 = 3.21

Offspring care

0.48 (0.10)

0.34 (0.17)

0.53 (0.11)

Female’s fertile

0.56 (0.09)

0.49 (0.11)

0.50 (0.15) F1,52 = 37.62 F2,52 = 0.18

Offspring care

0.07 (0.03)

0.09 (0.43)

0.11 (0.05)

Female’s fertile

0.54 (0.04)

0.74 (0.05)

0.48 (0.10) F1,52 = 47.47 F2,52 = 5.40

Offspring care

0.16 (0.03)

0.18 (0.05)

0.37 (0.03)

P < 0.001

P < 0.001

P < 0.001

P = 0.049

P = 0.84

P = 0.007

* Proportion of flights (arrivals to and departures from the nest) initiated by the female in which the pair male followed the mate.

and during the offspring care period (all P > 0.33, Table 1). One exception was the intensity of mate guarding: during the female’s fertile period those males that later deserted their brood guarded significantly more intensely their females than the males of the other two groups (Table 1, F2,54 = 4.17, P = 0.021, Dunnett two-way t test, biparental pairs set as control). In addition, during the female’s fertile period those males that later abandoned their nests courted their females less intensely, although not significantly, than the males of the other two groups, (Table 1, F2,54 = 2.28, P = 0.072, Dunnett two-way t test, biparental pairs set as control). Male sexual activity (courtship rate, mate guarding and copulation rate) significantly decreased during the offspring care period in all three groups (Table 1). The males in the male-only group also decreased their mate guarding, but to a lesser degree compared to the other three groups, resulting in a significant interaction effect in the repeated measure ANOVA (Table 1). Lastly, the breast patch size of males did not differ significantly between groups (Biparental nests: X ± SE = 13.9 ± 0.5 mm, N = 17; Female-only nests: 15.3 ± 0.9 mm, N = 12 ; Male-only nests: 14.3 ± 0.9 mm, N = 7; Kruskal-Wallis ANOVA: χ22,35 = 1.96 P = 0.375). Also the breast patch size of

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females did not differ significantly between groups, although the sample size, as in the case of males, is not large (Biparental nests: X ± SE = 11.8 ± 0.6 mm, N = 22; Female-only nests: 13.1 ± 0.8 mm, N = 11; Male-only nests: 12.2 ± 0.7 mm, N = 6; Kruskal-Wallis ANOVA: χ 22,38 = 3.09 P = 0.213).

DISCUSSION

The two key results of this study are (i) males that would subsequently desert the brood, during the fertile period guarded their mates more than males of the other two groups; (ii) males paired with females that would subsequently desert the brood, during the young’s care period guarded their females more than males of the other two groups. In passerine birds females rearing nestlings exhibit lower body mass compared with laying and pre-laying females (Ricklefs & Hussell 1984, Jones 1986, Griggio et al. 2005a). A recent experiment on Rock Sparrow (Griggio et al. 2005a) investigated the relationship between female weight, and male variation in sexual behaviour during offspring care: loading of the female with weights to simulate her readiness to lay a new clutch and to simulate so an imminent desertion. Males paired with weighted females performed more mate guarding than other males (as in the case of real desertion). Moreover, these males reduced the time spent in attracting a second mate on a secondary nesting box (Griggio et al. 2005a). Males probably remain with “deserting” females in order to ensure their paternity of the subsequent brood, or to persuade females to stay and re-mate with them. The correlative information provided here allows us to reasonably conclude that the male normally utilises the female’s weight increment (as well as other signals), to acquire information about the female’s strategy. The interpretation of why males that will desert the brood do so much mate guarding during female’s fertile period is more complex. One explanation may be that during the female’s fertile period the males increase mate guarding in order to be sure of the female’s fidelity and to discourage occasional extra pair copulations. This could serve as a basis for males to decide whether to desert the brood or not. A male will desert the brood only if he is sure that his female is not contacting a new male. So, there are few probabilities that both parents will desert the brood with a consequent death of the young. In fact, contrary to what has been observed in other species in which both parents may desert the brood (e.g. Valera et al. 1997), in this alpine population of Rock Sparrow few nests failed as a result of contemporary abandonment by both of the parents (M. Griggio pers. obs.). A male’s investment in paternity guards depends on his condition (Møller 1987), but also on the quality of his female (Pilastro et al. 2003). For example, in the Penduline Tit Remiz pendulinus males that deserted their fertile females (at the beginning of egg-laying) do not loose paternity, whereas males that guard their females suffer from paternity loss (Schleicher et al. 1997). There is great deal of evidence that the occurrence of extra-pair young in the Penduline Tit’s nest might be related to male attractiveness. Indeed, poor quality males should invest more in mate guarding, in order to reduce the risk of losing paternity because their females are more active in seeking extra-pair copulations in order to acquire genetic benefits through them (Schleicher et al. 1997). Therefore, another non-mutually exclusive explanation for the difference observed in mate guarding investment in this

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study could be based on differences in the partners’ ornamentation. We found no difference in male and female attractiveness (at least for yellow patch size) between the three groups. Anyway, the small sample size on sexual ornamentation does not allow us to discard this hypothesis and further investigations are necessary to study the possible relationship between mate guarding intensity and partners’ attractiveness (see also Pilastro et al. 2003). Our study provides new information about the behaviour of pair members that is needed in order to understand the complicated desertion process. The need for field studies such as this one has been long advocated by theoreticians (Székely et al. 1996; Webb et al. 1999, 2002; Barta et al. 2002; McNamara et al. 2002). In particular, this is one of the few studies to show the importance of mate guarding in the brood desertion process.

ACKNOWLEDGEMENTS We thank the many assistants who helped with the fieldwork. We are very grateful to Andrea Pilastro for his suggestions and to Toni Mingozzi for comments and practical help, and to Francisco Valera, Marco Girardello and an anonymous referee for their constructive comments on an earlier version of the manuscript.

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