Nest decorations: an ‘extended’ female badge of status?

Animal Behaviour 99 (2015) 95e107 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Nest decorations: an ‘extended’ female badge of status? Vicente García-Navas a, b, Francisco Valera a, Matteo Griggio c, * a

n Experimental de Zonas Aridas Department of Functional and Evolutionary Ecology, Estacio EEZA-CSIC, Almería, Spain Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland c Department of Biology, University of Padova, Padova, Italy b a r t i c l e i n f o Article history: Received 7 July 2014 Initial acceptance 13 August 2014 Final acceptance 20 October 2014 Published online MS. number: 14-00553R Keywords: feather carrying female competition nest ornamentation Petronia petronia sexual selection signalling Extended phenotypes as signals are widely distributed among animal taxa. For example, many bird species build eye-catching nests or structures, which can potentially mirror the quality or ability of the builder. Rock sparrow, Petronia petronia, nests are usually overly decorated with feathers belonging to different species. Feather carrying in this and other species seems to play a role beyond their supposed thermoregulatory function, that is, to provide insulation to eggs and developing chicks. In this study, we documented for the first time this intriguing pattern of behaviour in the rock sparrow and experimentally tested its potential role as a sexually selected or status signal by means of a feather supplementation experiment carried out in two distinct populations from Italy and Spain. We found that females were responsible for feather carrying, laid larger clutches and provisioned their young at a lower rate in those nests with experimentally added feathers. Decorated nests sustained fewer intrusions by floater individuals and were defended with greater intensity by both parents than control nests, which supports the role of nest ornamentation as a status signal to conspecifics. Presence of experimental feathers did not significantly increase the frequency with which males provisioned their young but males tended to desert their brood less often and spent more time guarding the brood in experimental nests, indicating that feather presence may also play a role in an intersexual context. Overall, our results allow us to exclude the thermoregulation hypothesis as a likely explanation for the occurrence of these decorations and provide partial evidence for the idea that feather carrying conveys information to the partner and potential competitors. Our study thus supports the notion that nonbodily traits serving a direct (naturally selected) function can also evolve a signalling component. © 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Many animals transfer information to conspecifics through morphological or behavioural traits such as gaudy plumages, extravagant body ornaments (antlers, horns) or courtship displays (Maynard Smith & Harper, 2003). From these conspicuous signals, receivers can assess the quality of the bearer (e.g. the fighting ability of a rival or the quality of a potential mate). Some species go further, collecting different materials to build complex structures or decorate their nests, which are used as an extension of their phenotype (‘extended phenotype’ sensu Dawkins, 1982). The extended phenotype concept refers to the potential effects of genes on the environment beyond the individual's body (reviewed in Schaedelin & Taborsky, 2009). For example, certain orb web spiders add extra silk structures to their capture webs whose function may be to deter predators or provide a warning signal for organisms that might destroy the web (Herbestein, Craig, Coddington, & Elgar,
ry & Casas, 2009; Walter & Elgar, 2012). Thus, the 2000; The * Correspondence: M. Griggio, Department of Biology, University of Padova, U. Bassi, 35100 Padova, Italy. E-mail address: matteo.griggio@unipd.it (M. Griggio). contemporary signal effect of such decorations is different from their original function (i.e. entangle unsuspecting prey). In some cases, a novel trait can acquire a signalling effect and may explain, for example, the occurrence of odd items such as flowers, stones, snake skins, scats or human-derived material (foil, plastics) in the € & breeding structures of many species (e.g. Ostlund-Nilsson Holmlund, 2003; Schuetz, 2005; Trnka & Prokop, 2011). The presence of this unusual nest-building material may indicate the builder's vigour, technical or harvesting ability and capacity to deter rivals (Mainwaring et al., 2014; Moreno, 2012). Thus, nests not only provide a protective environment for developing eggs and offspring but may also constitute an important signalling device to reveal information for members of the opposite sex (Barber, Nairn, & Huntingford, 2001; Brouwer & Komdeur, 2004; Hoi, Schleicher, &Valera, 1996; Schaedelin & Taborsky, 2006) or potential competitors (Penteriani & Delgado, 2008). In this sense, on the basis of the existing literature, we can discern two main functions of nest (or similar structures) decorations as visual cues: (1) to act as a pre- or postmating sexual signal (intersexual context) and (2) to advertise social status to potential intruders (intrasexual context). http://dx.doi.org/10.1016/j.anbehav.2014.10.024 0003-3472/© 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 96 V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 Regarding the former (maleefemale communication), a wellunderstood example is the case of birds of the family Ptilonorhynchidae (bowerbirds). Males of most of these species build and decorate stick structures (called bowers) to attract the females with which they mate (Borgia, 1985; Endler, Endler, & Doerr, 2010; Madden, 2003). The use of nest-building activity as a sexual signal has been observed in other taxa as well. For example, in many species of African cichlids, males build sand craters to attract females for spawning (Barber, 2013; Schaedelin & Taborsky, 2010). Pebble heaps of wheatears, Oenanthe leucura, or multiple nests of Australian reed warblers, Acrocephalus australis, and Eurasian wrens, Troglodytes troglodytes, seem to play a similar role as a source of information to current or potential partners (Berg, Beintema, Welbergen, & Komdeur, 2006; Garson, 1980; Soler,
n, 1996). Such information can be Soler, Møller, Moreno, & Linde used by females to ascertain male condition and obtain cues about future paternal investment in their brood (Soler, Møller, & Soler, 1998; Soler, de Neve, Martínez, & Soler, 2001). Evidence for social status signalling has been provided by two recent studies on territorial raptors (eagle owl, Bubo bubo: Penteriani & Delgado, 2008; black kite, Milvus migrans: Sergio et al., 2011). Penteriani and Delgado (2008) reported that owls use their own faeces and prey feathers, deposited on posts and plucking sites in proximity to the nest, to mark their territory and signal current reproductive status to potential trespassers. Sergio et al. (2011) found that nest decorations (mainly human rubbish such as plastic bags) observed in most (80%) black kite nests can serve as a signal of the builder's physical prowess and thus as a threat against conspecifics. However, these two alternatives are not mutually exclusive and nest ornamentation may have multiple functions. Next to plant matter and fur, feathers are one of most common nest-building materials (Hansell, 1995, 2000). Many passeriformes use downy feathers from other species for lining their nests. Feathers are generally deposited within the nest cup, in contact with the eggs, and therefore it has been traditionally considered that these possess a thermoregulatory function (Dawson, O'Brien, & Mlynowski, 2011; Lombardo, Bosman, Faro, Houtteman, & Kluisza, 1995; McGowan, Sharp, & Hatchwell, 2004). Some species carry flight or contour feathers to their nests with a merely ornamental purpose, not to provide insulation, placed outside the nest cup in very visible locations (Veiga & Polo, 2005). Feathers constitute a limiting resource because they usually come from dead or killed birds (Hansell, 1995) and thus feather gathering may be indicative of good physical condition or high predisposition to devote time and energy to reproduction. Observational and experimental evidence for this comes from a study by Sanz and García-Navas (2011), which showed that female blue tits, Cyanistes caeruleus, use nest decoration as a source of information about male quality, and, accordingly, modulate their level of parental investment. However, feather carrying is not a male-exclusive behaviour as it has also been described in females of the spotless starling, Sturnus unicolor (Polo & Veiga, 2006; Veiga & Polo, 2011). Rock sparrows, Petronia petronia, like other Old World sparrows (Spanish sparrow, Passer hispaniolensis: Alonso, 1982; tree sparrow, Passer montanus: Pinowski et al., 2006; house sparrow, Passer
pez de Hierro, Moleo
n, & Ryan, 2013), usually domesticus: García-Lo carry feathers from other species (hoopoe, Upupa epops, wood pigeon, Columba palumbus, azure winged-magpie, Cyanopica cyanus, Eurasian jay Garrulus glandarius and raptors) to their nests. Feathers are placed on the nest rim, stacked in the straw like ‘hunting trophies’ in a conspicuous manner (Fig. 1, see also Fig. S1 in the Supplementary Material). In the present study, we documented this previously undescribed behaviour and tested the possible function of feather delivery by means of a feather addition experiment carried out in two separate Mediterranean populations. Specifically, we predicted that (1) if feather carrying is primarily for Figure 1. Examples of rock sparrow nests exaggeratedly decorated with feathers belonging to different species including Eurasian black vulture, Aegypius monachus, common buzzard, Buteo buteo, Eurasian jay, Garrulus glandarius, azure-winged magpie, Cyanopica cyanus, red-legged partridge, Alectoris rufa, and golden oriole, Oriolus oriolus. Note that feathers are not embedded within the nest matrix but they are arranged to maximize its visibility. Photos: Vicente García-Navas. V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 thermoregulation, first, feathers should be in close contact with eggs, second, its presence should decrease with the progress of the season (as temperatures rise) and third, we should expect a shorter incubation period, a higher hatching rate and enhanced offspring growth in experimental nests; (2) if feather carrying constitutes a male or female sexual signal, we expected a greater investment in reproduction by the partner in response to the feather addition treatment; and (3) if feather carrying plays a role as a signal of current reproductive status to potential competitors, receivers should respond to the signal in a way that benefits signallers and thus we expected fewer visits by intruders or ‘floating’ individuals in those nests in which we added feathers experimentally. Meanwhile, from the signaller's point of view, the presence of foreign feathers may be indicative of a high risk of usurpation (i.e. he/she may infer the presence of a potential competitor) and this may increase the signaller's investment in nest defence. METHODS Study Species The rock sparrow is a hole-nesting passerine whose distribution ranges from southern Europe to central Asia (Cramp, 1998). Rock sparrows are monomorphic birds; both sexes have a yellow spot on the upper breast, which contrasts with their earth-coloured plumage. Previous studies have suggested that this ornament is maintained by mutual sexual selection as it has been shown that males also prefer more ornamented females (Griggio, Matessi, et al., 2005; Griggio, Serra, Licheri, Monti, & Pilastro, 2007; Griggio, Devigili, Hoi, & Pilastro, 2009; Griggio, Valera, et al., 2005; Pilastro, Griggio, & Matessi, 2003). This trait also plays a role in an intrasexual context (like an ‘armament’) as an indicator of individual quality and social status to conspecifics (Griggio et al., 2007; Griggio,
th & Griggio, 2011). Rock sparrows have a Zanollo, & Hoi, 2010; To flexible mating system unusual among birds, in which sequential polygyny and polyandry regularly occur (García-Navas, García del
n, Ferrer, & Fathi, 2013a; Griggio & Pilastro, 2007; Griggio, Rinco Tavecchia, Biddau, & Mingozzi, 2003). Probably as a result of sexual conflict (i.e. the conflicting evolutionary interests of males and females) both sexes can desert their brood and thus it is not uncommon to find nests in which parental care is carried out by a single parent (Griggio & Venuto, 2007). Therefore, any information relative to mate quality conveyed through body or other ornaments may be especially valuable in this context. Rock sparrows incorporate feathers into their nests (an untidy structure built by the female using straw and grass), mostly during the early breeding period, but it is not clear which sex is responsible for this behaviour. Before the onset of egg laying, males often sing on top of their nestbox (some of them defend more than one box at the same time) and they are visited by different females, which usually inspect the box (Matessi, McGregor, Peake, & Dabelsteen, 2005; Nemeth, Kempenaers, Matessi, & Brumm, 2012; our personal observation). Such prospecting behaviour continues even during the laying phase when more than one female usually visit the nest. The rock sparrow is a semicolonial species and can occupy adjacent nesting sites (e.g. nest holes built by bee-eaters, Merops apiaster, in sandy cliffs). Rock sparrows become very territorial at a small scale (4e5 m around the nest) during the breeding period and intruders or floaters are chased out quickly by the owners. In addition, agonistic interactions are frequent between neighbours, such as individuals destroying clutches or removing nest-building material from nests located in adjacent territories (our personal observation). During the offspring-rearing period, males spend much time in the vicinity of their nest. In some cases males do not feed the young but remain in their territory (they do not abandon the nest) courting, 97 and trying to copulate with their partner (Griggio, Matessi, et al., 2005; Griggio, Mingozzi, Bortolin, & Pilastro, 2008). Study Area This study was carried out during the 2013 breeding season in two distant colonies of rock sparrow: one located in ‘Las Navas’ (Quintos de Mora, Montes de Toledo, central Spain, 39 240 230 N, 4 40190 W) and another in ‘Barbagia’ (central Sardinia, Italy, 40 230 300 N, 9120120 E). ‘Las Navas’ (hereafter, Quintos de Mora) consists of 45 nestboxes distributed in a grid pattern in a young woodland of zeen oak, Quercus faginea, with Mediterranean scrubland surrounded by a shrubby riverside and stony open areas. In Quintos de Mora, breeding density is very high (occupation rate: 100%; all but five nests occupied by rock sparrows) and thus there is strong competition for nesting sites. This colony is expanding and rock sparrows have recently colonized a nearby nestbox plot (‘Gil García’, 1.5 km away) previously only occupied by tits (see GarcíaNavas et al., 2013a for more details). Some rock sparrow nests from ‘Gil García’ were also included in the present study (see below). ‘Barbagia’ consists of 36 nestboxes installed from 2008 in a woodland of cork oak, Quercus suber, with Mediterranean scrubland and stony open areas with short grass. It holds approximately 20 breeding pairs each year. The climate in both areas is Mediterranean, with hot and dry summers and mean annual temperatures of around 16  C (Kottek, Grieser, Beck, Rudolf, & Rube, 2006). Field Methods and Basic Reproductive Parameters We monitored the breeding activity of rock sparrows in both populations from the nest-building period (mid-May) until the last chicks fledged (mid-July). The following reproductive parameters were recorded: laying date, clutch size, hatching date, hatching and fledging success (proportion of eggs hatched and proportion of hatchlings that resulted in fledged young, respectively). On day 6e7 posthatching, parents were captured when feeding the young by means of spring-traps. Trapped birds were identified with metal and coloured rings to allow individual identification. A small blood sample was taken from the brachial vein of adult birds and stored on FTA reagent-loaded paper (Whatman Bioscience, Florham Park, NJ, U.S.A.) for sex determination using molecular methods (see García-Navas et al., 2013a). Nestlings were measured (tarsus length ± 0.01 mm) and weighed (±0.1 g) with a digital calliper and a portable electronic balance, respectively, at the age of 13 days following the protocol described in Svensson (1992). Observational Data During the two previous breeding seasons (2011e2012) we collected information about the presence of natural feathers in the nests in order to determine to what extent such behaviour constitutes a widespread characteristic in this species or a specific trait of certain populations. We recorded the number of feathers present in each nest and these were grouped into two categories: nests with or without feathers. We paid attention to the seasonal trend in the appearance of feathers to test for an association between feather presence and calendar date. We also tested for the existence of differences in clutch size and male desertion rate between adorned and unadorned nests. Experimental Design We randomly allocated nests, found before egg laying, to a control or experimental treatment. Once the nest was complete, we checked it daily until the laying of the first egg. On the first-egg day 98 V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 (day 0) we supplied five blue commercial feathers (Almacenes
n SA, Madrid, Spain) at those nests assigned to the feather Cobia supplementation treatment (experimental nests). Feathers were arranged outside the nest cup, such as they are found naturally. We chose blue feathers because we have previously observed that rock sparrows have a preference for ornamental feathers or flowers with this colour such as feathers of azure-winged magpie, tail feathers of blue tit, striped feathers of Eurasian jay and petals of blueweed, Echium vulgare. Nests were checked daily during the laying sequence to record the number of feathers present in each. We replaced or uncovered feathers in those nests in which they were removed or buried by the owner birds to ensure that all experimental nests contained the same number of supplemented feathers. Some experimental and some control nests contained natural feathers (mean ± SE; experimental: 3.6 ± 0.6, range 0e13; control: 1.1 ± 0.2, range 0e4). Control nests were also visited on a daily basis until clutch completion in order to disturb both treatments equally, but we did not remove feathers from these nests. So our manipulation increased the differences in the degree of nest ornamentation between individuals. We added feathers in a total of 31 nests (Quintos de Mora N ¼ 17, Barbagia N ¼ 14) and 35 others (Quintos de Mora N ¼ 29, Barbagia N ¼ 6) served as controls. Thus, including both study sites, a total of 66 rock sparrow nests were considered in the present study. Some breeding attempts (ca. 20%), particularly in Quintos de Mora, did not reach the nestling stage because of nest usurpation by conspecifics or abandonment. Specifically, five nests (three experimental and two control, all from Quintos de Mora) failed, presumably because of interference by other females, given that we found signs of conspecific intrusions (stolen nest-building material, destroyed nests) and we sometimes observed a new clutch laid by a different female a few days later. Nine nests (three experimental and six control) were (apparently) naturally deserted by both parents prior to (N ¼ 1) or after (N ¼ 8) hatching. This left us with a total of 52 nests in which nestlings fledged successfully. If feather presence produces adequate nest insulation, it would reduce the cooling rates of eggs, therefore reducing the costs of incubation and allowing parents to cope with longer incubation bouts in (warmer) experimental nests (Reid, Monaghan, & Ruxton, 2000). Once chicks hatch they are faced with a trade-off between allocating energy to growth or thermoregulation (Dawson, Lawrie, & O'Brien, 2005; Dawson, O'Brien, & Mlynowski, 2011). If feather supplementation reduces maintenance costs, nestlings may be able to devote more resources to growth in experimental broods. Determination of the Sex Responsible for Feather Carrying A subsample of nests (Quintos de Mora N ¼ 8, Barbagia N ¼ 6) not included in the experiment was supplied with a pile of coloured feathers deposited in the nest surroundings (within a ca. 3 m radius around the nestbox) in order to determine the sex responsible for this behaviour. In Quintos de Mora such observations were carried out on nests belonging to ‘Gil García’, that is, outside the main (experimental) study area (‘Las Navas’). Feathers were placed directly on the ground, and they were surrounded with stones and branches to impede wind disturbance. The rock sparrows' reaction to the presence of feathers was observed directly with a spotting telescope (30 magnification) or filmed using camouflaged video cameras mounted on tripods and situated about 2e3 m away from the feather pile. Parental Care Estimates: Offspring Provisioning and Nest Defence We filmed or directly observed the parental behaviour of adult rock sparrows on day 8e9 posthatching in 52 nests. We recorded the number of feeding events made by each parent, whose sex was identified from ringing details, during a period spanning 64 to 280 min (mean observation time per nest ± SD was 3.17 ± 0.99 h for a total of 165 h). Provisioning rates were calculated by dividing the number of feeding visits made by the adults by both brood size and duration of the observation period or taping session to yield provisioning visits/nestling per h. Relative provisioning effort (male/female share of provisioning) was calculated as the proportion of provisioning visits made by one sex in relation to the total number of visits (i.e. both sexes combined) observed in each nest. We also noted the number of visits without prey delivery by each parent, which is relatively frequent in this species (Griggio et al., 2003; García-Navas et al., 2013a; Matessi, Carmagnani, Griggio, & Pilastro, 2009). The number of nonprovisioning visits and the total time (min) spent near the nest (1e2 m radius) were used as an index of defence intensity. In addition, we noted the incidence of intruders trying to access the nestbox. Potential trespassers were easily detectable from ring details or the nest owner's reaction to their presence (intruders are violently expelled from the nest vicinity). From our observations of parental activity, we distinguished between monoparental and biparental nests. We considered as biparental nests those in which we observed both parents attending the nest irrespective of whether they fed their young or not (four males, two from experimental nests and two from controls defended their nest but they did not contribute to offspring provisioning). We refer to monoparental nests (N ¼ 13) as those in which only one parent, usually the female (92% of cases), provided care (i.e. the partner was not present). Data Analysis From a merely functional point of view, we tested the effect of feather supplementation on clutch size, length of the incubation period, hatching success, fledging success and offspring quality (nestling size and body mass) of rock sparrows using generalized linear models (GLMs). The effect of the treatment on hatching/ fledging success (hatchlings/fledglings as a numerator and clutch size as a denominator, respectively) was analysed using GLMs with binomial distribution and logit function. For the remaining variables we employed GLMs with normal distribution. Full models included treatment, our focal variable, and study area (and its interaction) as categorical variables and a series of potential covariates as necessary: standardized laying date (to correct for a possible calendar effect), brood size on day 8 (to correct nestling measurements for differences in brood demand) or nestling tarsus length (to correct body mass for differences in skeletal size). In an intersexual context, we tested (1) whether feather supplementation is used to deter a partner from seeking a new mate, and (2) whether this behaviour is employed as a means to stimulate investment of the partner in the current brood; that is, if the receivers adjust parental effort in response to the perceived quality of the builder as the differential allocation hypothesis posits (Burley, 1986). To test the former, we compared the frequency of monoparental nests (nests in which one pair member deserted the brood) in the experimental and control groups using contingency tables. Regarding the latter, we first tested for sex differences in provisioning effort between treatments using a matched-pair test. We then constructed another GLM including total, male or female provisioning rate as a dependent variable in order to test for the effect of our experiment on adult provisioning investment. We also controlled for the provisioning rate of the partner because parents usually respond to changes in each other's effort (Harrison, Barta,
kely, 2009). This aspect is particularly important in Cuthill, & Sze species with intense sexual conflict such as rock sparrows or penduline tits, Remiz pendulinus (van Dijk, 2009; Valera, Schleicher, & V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 Hoi, 1997). In addition, we constructed a model including relative provisioning effort as a dependent variable in order to determine whether males increased their share of provisioning in response to the treatment. To avoid potential confounding effects of compensatory care, only biparental nests (39 nests; experimental N ¼ 22, control N ¼ 17) were included in these analyses. In an intrasexual context, we tested whether experimental nests were visited less by neighbouring or ‘floater’ birds, which would imply that ornamental feathers can be used to discourage or deter potential trespassers. We constructed a model fitting the number of observed intrusions as the dependent variable (Poisson distribution) and treatment as the predictor. Intruder rate may also be affected by the nest defence behaviour of parents. Consequently, we also tested whether the builders' willingness to defend their nests (which is a form of parental care) was affected by the presence of experimental feathers. Accordingly, females may exhibit a higher propensity to invest in nest defence in those cases in which they perceive a high risk of nest usurpation by competing individuals (i.e. experimental nests). To that end, we constructed GLMs similar to those mentioned above but including the number of guarding visits (Poisson distribution) and time spent performing nest defence behaviour (log10 þ 1 transformed to attain a normal distribution) as the dependent variable. All statistical analyses were performed using SAS 9.1 (SAS Institute, Cary, NC, U.S.A.). Sample sizes vary where incomplete data forced the exclusion of some observations. Unless otherwise stated, all tests were two tailed, the level of significance (a) was set to 0.05 and means ± SE are given. Ethical Note Nine broods (from which only three belonged to the experimental group) were deserted by both parents (see above) and the chicks belonging to these broods died. The desertion rate was not higher than usual in these two populations (Griggio et al., 2003, 2005; García-Navas et al., 2013a) and this proportion was similar in both treatments (experimental: 10%; control: 17%; c ¼ 0.78, P ¼ 0.38). Spring-traps were constantly monitored by means of binoculars. and no bird remained trapped in the nest for more than 10 min. Captured parents resumed their feeding activity after 20e25 min. Nestlings were kept in either a plastic container or a lightweight bag during the handling process. The entire procedure of nestling measuring lasted less than 10 min. Our broad experience with the study species and results obtained in previous experimental studies allow us to confirm that handled birds and their offspring do not suffer any detectable reduction in welfare or survival as a consequence of this procedure. We manipulated, bled (20e30 ml) and banded birds under licence from the respective
n General del Medio Natinstitutional authorities (Spain: Direccio ural of Junta de Comunidades de Castilla-La Mancha and Ringing Office of the Spanish Society of Ornithology SEO/BirdLife, licence no. 520030; Italy: permits issued by the Istituto Superiore per la Protezione e la Ricerca Ambientale, ex-Istituto Nazionale Fauna Selvatica, licence no. 19828). RESULTS The Sex Responsible for Feather Carrying In all cases in which we observed rock sparrows using the feathers we supplied (nine of 14), the behaviour was carried out by females (five in Quintos de Mora, four in Barbagia). Upon arrival to the nest surroundings, birds were attracted by the presence of feathers. Within a few minutes, the rock sparrows had gathered the 99 feathers until none remained on the ground (see Fig. S2 and the video recording in the Supplementary Material). In two cases we observed that the feathers we supplied were added to the nest by an individual (probably a ‘floater’) other than the nest owners (one of them was resighted trying to access the nest during the broodrearing period). In those cases (N ¼ 5) in which feathers were not used, we did not observe any individual in the vicinity of the nest during the observation period. This indicates that the resource was not detected and therefore could not be exploited. Supplementary video related to this article can be found at http://dx.doi.org/10.1016/j.anbehav.2014.10.024. Behavioural observations collected during the 2011 and 2012 breeding seasons on the incidence of feather carrying in rock sparrow nests indicate that this behaviour is frequent at both sites; we found ornamental feathers in more than half of the nests (Quintos de Mora: 62.2% N ¼ 53; Barbagia: 67.6% N ¼ 34). Nest decorations usually appeared before laying, declined slightly during the incubation period and markedly so thereafter, so that when nestlings were ringed (day 13 posthatching) very few feathers were found in the nest (our personal observation). Feather delivery did not show any seasonal pattern (Pearson correlation: r87 ¼ 0.22, P ¼ 0.20), which is in disagreement with what the thermoregulation hypothesis predicts. Clutch size did not differ significantly between nests adorned naturally and nests without feathers (with feathers: 5.57 ± 0.18; without feathers: 5.37 ± 0.14; F1,85 ¼ 0.88, P ¼ 0.35). Male desertion rate was lower in nests decorated with feathers than in those without feathers (11% versus 20%, respectively) but the difference was not statistically significant (P ¼ 0.33). There was a significant relationship between the number of feathers present in the nest and male provisioning rate in Barbagia (Pearson correlation: r34 ¼ 0.34, P ¼ 0.047; see Fig. A1), but not in Quintos de Mora (P > 0.05). Breeding Parameters and Offspring Performance Feather supplementation had a significant effect on clutch size; females laid larger clutches in experimental nests (Table 1, Fig. 2a; F1,61 ¼ 8.59, P < 0.01). However, there was a significant study site*treatment interaction (F1,61 ¼ 4.30, P ¼ 0.04) and post hoc analysis revealed that the difference in clutch size between groups was only significant in Barbagia (Tukey test: P < 0.01 for Barbagia, P ¼ 0.27 for Quintos de Mora), where females' productivity was lower than at Quintos de Mora (Quintos de Mora: 6.13 ± 0.11; Barbagia: 4.98 ± 0.20; F1,61 ¼ 24.10, P < 0.001). However, this did not result in a higher food demand for parents of experimental nests because there were no differences in brood size between treatments (Table 1; F1,61 ¼ 1.84, P ¼ 0.18). Feather supplementation did not affect the length of the incubation period, hatching success or fledging success (see Table 1; all P > 0.25). Both hatching and fledging success differed significantly between sites (hatching success in Quintos de Mora: 77.68 ± 4.32%; hatching success in Barbagia: 92.98 ± 5.30%; F1,61 ¼ 4.21, P ¼ 0.04; fledging success in Quintos de Mora: 58.16 ± 5.77%; fledging success in Barbagia: 87.19 ± 5.26%; F1,61 ¼ 9.40, P < 0.01). Feather supplementation had no significant effect on nestling size or nestling body mass either when considering all nests (Table 1; both P > 0.1) or considering only those with biparental care (Table 1; both P > 0.25). However, offspring quality was affected by the number of provisioning parents and the relative importance of each sex in this task (see below). Probability of Mate Desertion In Quintos de Mora, we found a marginally lower proportion of nests with monoparental care (all ‘female-care’ nests except one) in 100 V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 Table 1 Differences (mean ± SE) in reproductive parameters between experimental (feather-supplemented) and control nests applied to two data subsets: one considering all nests and the second only considering those with biparental care ‘Quintos de Mora’ ‘Barbagia’ Experimental Control Experimental Control All nests (N¼66) Clutch size Incubation period (days) Number of hatchlings Brood size (day 8) No. fledged young Nestling tarsus length (mm) Nestling body mass (g) 6.18±0.18 11.78±0.25 4.73±0.39 4.27±0.50 3.87±0.61 18.20±0.13 27.63±0.92 6.03±0.14 12.47±0.49 4.64±0.33 3.96±0.42 3.53±0.43 18.96±0.10 29.22±0.73 5.57±0.23 12.42±0.14 5.14±0.44 5.07±0.44 4.85±0.43 18.10±0.12 27.89±0.88 4.40±0.24 12.40±0.24 4.40±0.24 4.20±0.20 4.00±0.45 18.12±0.20 28.41±1.42 Only biparental nests (N¼39) Clutch size Incubation period (days) Number of hatchlings Brood size (day 8) No. fledged young Nestling tarsus length (mm) Nestling body mass (g) 6.20±0.25 11.89±0.35 5.20±0.27 5.20±0.28 4.70±0.44 18.35±0.11 28.59±0.98 5.92±0.17 12.10±0.33 5.23±0.24 5.15±0.24 4.77±0.38 18.46±0.10 30.39±0.89 5.75±0.22 12.41±0.30 5.58±0.25 5.50±0.25 5.25±0.40 18.11±0.10 27.93±0.85 4.50±0.29 12.25±0.52 4.50±0.43 4.25±0.44 4.00±0.69 18.14±0.17 28.27±1.47 the experimental group (chi-square test: c21 ¼ 2.08, P ¼ 0.079). That is, male desertion rate tended to be lower in those nests that were manipulated (percentage of nests with monoparental care: control: 41% of 22; experimental: 17% of 12). The percentage of nests with female-only care did not differ significantly between groups in Barbagia (control: 0% of 5; experimental: 8% of 13; P > 0.20). Adult Provisioning Effort Females without male assistance in nestling provisioning tended to feed at a higher rate than females aided by their partner (female provisioning rate/chick per h; without male assistance: 1.22 ± 0.13; with male assistance: 0.95 ± 0.08; F1,48 ¼ 3.13, P ¼ 0.08). This indicates that females were able to compensate for the shortfall in food provisioning. When only considering nests with biparental care, we found that females fed their young more often than males irrespective of the treatment (feeding events/ nestling per h; female: 1.03 ± 0.08; male: 0.54 ± 0.06; Z38 ¼ 3.57, P < 0.001). However, sex differences were less pronounced in the experimental group (females from experimental nests: 0.87 ± 0.42; males from experimental nests: 0.58 ± 0.33; Z22 ¼ 2.22, P ¼ 0.01; females from control nests: 1.25 ± 0.48; males from control nests: 0.49 ± 0.48; Z16 ¼ 2.72, P ¼ 0.002). Feather supplementation had a significant effect on total provisioning rates: provisioning rates per nestling were lower in experimental than in control nests (experimental: 1.44 ± 0.13; control: 1.70 ± 0.09; Table 2, Fig. 2b). Total (per pair) provisioning rates also differed significantly between sites (Table 2) being higher in Barbagia than in Quintos de Mora (1.70 ± 0.06 versus 1.46 ± 0.12, respectively). When examining provisioning rates by sex, we found a significant effect of treatment on female provisioning rates: females fed their young at a lower rate in those nests in which we supplied feathers (experimental: 0.87 ± 0.09; control: 1.25 ± 0.12; Table 2). Female provisioning effort also differed between sites; females breeding at Barbagia fed their young at a higher rate than females from Quintos de Mora (1.19 ± 0.09 versus 0.91 ± 0.11, respectively). Regarding males, treatment had no significant overall effect on the frequency at which they fed their young (Table 2). The male's share of provisioning effort increased with brood size, but it did not differ significantly between experimental and control nests (Table 2). Thus, it seems that, first, males did not compensate for reduced female assistance in experimental nests and, second, they were more likely to invest in offspring provisioning as brood demand increased. In fact, both male total and per nestling provisioning rate were positively related to brood size on day 8 posthatching (Pearson correlations: r38 ¼ 0.56, P < 0.001 and r38 ¼ 0.38, P ¼ 0.02, respectively; Fig. A2). Total female provisioning rate was not associated with brood size on day 8 (Pearson correlation: r38 ¼ 0.06, P ¼ 0.68) and female per nestling provisioning rate was negatively related to nestling demand (Pearson correlation: r38 ¼ 0.49, P < 0.01), suggesting that they worked at their maximum level. The number of care-giving parents significantly affected nestling size (F1,46 ¼ 4.11, P ¼ 0.048), but not nestling mass (F1,46 ¼ 2.01, P ¼ 0.16). Nestling rock sparrows were larger in those nests in which both parents contributed to nestling care (tarsus length: monoparental: 18.01 ± 0.11 mm; biparental: 18.28 ± 0.06 mm). Nestling body mass was associated positively with female provisioning rate (Pearson correlation: r36 ¼ 0.47, P < 0.01; Fig. 3) and negatively with male provisioning rate (Pearson correlation: r35 ¼ 0.36, P ¼ 0.03; Fig. 3). Consequently, the relative contribution of each parent predicted mean nestling mass; we found heavier chicks in those nests in which the female's contribution to nestling provisioning was higher (Pearson correlation: r35 ¼ 0.51, P < 0.01; Fig. A3). Nest Defence Behaviour We detected the presence of ‘floating’ or intruder individuals in 37% (19/51) of nests. Five of six nests that were visited by conspecifics more than once were control nests. Intruder pressure was significantly lower for those nests in which we added feathers; experimental broods were less frequently visited by intruders than control ones (mean number of intrusions per nest: experimental: 0.40 ± 0.11; control: 0.96 ± 0.33; GLM: c2 ¼ 6.39, P ¼ 0.01). The number of nest-guarding visits did not differ significantly between treatments for males or for females (Table 2). In males the number of nest-guarding visits declined as brood size increased whereas for females this variable was positively correlated with laying date (Table 2). Males engaging in nest defence behaviour were less likely to invest in nestling provisioning (Pearson correlation: r38 ¼ 0.46, P < 0.01) whereas there was no significant relationship between nest guarding and nestling provisioning rate in females (Pearson correlation: r38 ¼ 0.12, P ¼ 0.45). Both males and females from experimental nests spent more time guarding their nest than those from the control nests (experimental males: 7 min 9 s; experimental females: 7 min 41 s; control males: 1 min 34 s; control females: 1 min 11 s; Table 2). V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 Table 2 Generalized linear models to the effect of the experimental treatment on different estimates of parental care 7 (a) 6.5 Estimate±SE 6 Clutch size 5.5 5 4.5 4 3.5 3 Total provisioning rate (per nestling per h) 2.6 101 Control Experimental (b) 2.4 2.2 2 1.8 1.6 1.4 1.2 1 0.8 0.6 Control Experimental Figure 2. Differences in (a) clutch size and (b) total provisioning rate (feeding visits/ chick per h) between experimental (N ¼ 32 for clutch size and N ¼ 22 for provisioning rates) and control nests (N ¼ 34 for clutch size and N ¼ 17 for provisioning rates). Mean ± SE values, calculated jointly (both populations combined: circles) and separately (‘Quintos de Mora’: diamonds; ‘Barbagia’: squares) are given. DISCUSSION Our main findings provide partial support for the idea that nest ornamentation in the rock sparrow can act as both a sexual and a status signal. We observed that our experimental treatment elicited specific behavioural reactions: (1) females laid larger clutches (in Italy), (2) fed the nestlings less and spent more time guarding the nest; (3) males were less likely to abandon the nest and invested more in passive nest defence and intruders less often prospected those nests in which we supplied feathers. Overall, we detected a general effect of the experiment on the studied variables although there were differences in several reproductive traits (fledging success, provisioning rate) between study sites. The different ecological conditions (e.g. nest site availability, operational sex ratio) to which birds are presumably subjected in these populations could explain the existence of an interaction between treatment and study site for Parental provisioning behaviour Total provisioning rate Study site 0.17±0.08 Treatment 0.17±0.07 Treatmentstudy site Laying date Female provisioning rate Study site 0.19±0.06 Treatment 0.23±0.06 Treatmentstudy site Laying date Mate provisioning rate 0.43±0.15 Male provisioning rate Study site Treatment Treatmentstudy site 0.15±0.16 Laying date Mate provisioning rate 0.41±0.15 Male proportion of feedings Study site Treatment Treatmentstudy site Laying date Brood size on day 8 10.31±3.76 Parental defence behaviour Female guarding visits Study site 1.36±0.65 Treatment Laying date 0.87±0.30 Brood size on day 8 Male guarding visits Study site Treatment Laying date Brood size on day 8 0.83±0.12 Female guarding time Study site 0.07±0.01 Treatment 0.04±0.01 Treatmentstudy site 0.04±0.01 Laying date Brood size on day 8 Male guarding time Study site 0.05±0.01 Treatment 0.03±0.01 Treatmentstudy site Laying date Brood size on day 8 df Test P 1.36 1.36 1.34 1.34 5.08 5.33 2.50 3.69 0.03 0.03 0.12 0.06 1.34 1.34 1.28 1.28 1.34 8.78 12.72 0.27 1.72 7.86 <0.01 0.001 0.60 0.20 0.01 1.33 1.33 1.33 1.33 1.28 1.86 0.41 5.47 2.75 7.47 0.18 0.53 0.03 0.11 0.01 1.32 1.32 1.32 1.32 1.36 2.91 2.27 0.17 0.31 7.51 0.09 0.14 0.68 0.58 <0.01 1.35 1.35 1.29 1.29 4.32 0.83 8.06 0.29 0.04 0.36 <0.01 0.61 1.36 1.36 1.29 1.29 0.95 0.01 2.84 44.77 0.33 0.99 0.09 <0.01 1.35 1.35 1.35 1.29 1.29 44.79 11.17 11.73 0.01 1.69 <0.001 <0.01 <0.01 0.99 0.20 1.36 1.36 1.35 1.29 1.29 21.45 6.14 3.19 0.63 3.65 <0.01 0.02 0.08 0.43 0.06 We were unable to distinguish the sex of parents in one nest and to determine accurately the date of the first egg in four nests, and consequently degrees of freedom can differ among analyses. Significant results are marked in bold. some parameters. However, our observations conducted in two very distant localities allow us to assert that this previously undescribed behaviour of feather carrying constitutes a distinctive feature of this species rather than a locally adaptive behaviour. ‘Thermoregulatory Function’ Hypothesis The primary function of feather carrying, to provide insulation for eggs or young, was not supported by our results; we did not find evidence that feather presence conferred direct benefits to experimental pairs. Experimental broods did not have shorter incubation periods or higher hatching success and nestlings from feathered nests were not larger or in better condition than those from the control nests. Observational data on temporal and seasonal patterns of feather occurrence also do not fit the predictions for an insulation role of feather addition. We failed to find a seasonal decline in feather delivery, which is in contrast to the 102 V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 Mean nestling mass on day 13 (g) 36 34 32 30 28 26 24 22 20 0 0.5 1.5 1 2 2.5 Male/female provisioning rate (feeding events/nestling per h) Figure 3. Mean nestling mass on day 13 in relation to female (grey circles and dotted line) and male (empty circles and continuous line) provisioning rate. Only biparental nests (N ¼ 39) are included. We refer to biparental nests as those in which both parents were present during the brood-rearing period irrespective of whether they fed their young or not (one female and four males visited the nest more than once during the sampling session but they were never observed provisioning the nestlings). thermoregulation hypothesis because if feathers grant thermal benefits, this behaviour should be more frequent in early nests (when ambient temperatures are lower) and less common later in the season, when the risk of hyperthermia increases. In addition, this species shows a high breeding synchrony (more than 70% of clutches are concentrated within a 5-day period), and therefore the existence of internest variability in feather presence can scarcely be explained by changes in weather conditions. Our results contrast with those reported for other sparrow species. For example, the use of feathers as nest-lining material seems to be clearly linked to a thermoregulatory function in the tree sparrow (Pinowski et al., 2006). Tree sparrows show a marked preference for downy feathers especially during their autumnal display when they build nests that are used for roosting at night in winter (García-Navas,
pez de Arroyo, & Sanz, 2008). In the house sparrow, García-Lo Hierro et al. (2013) reported that the amount of feathers inside nests peaked during incubation and with newly hatched chicks, when the maintenance of a thermally stable microenvironment may be more important. None the less, they suggested that feather carrying could also form part of the male courtship display as they found that one-third of the feathers were deposited at the nest entrance and females paired with those males that collected more
pez de Hierro feathers invested more in reproduction (García-Lo et al., 2013). In rock sparrows, whose genus (Petronia) constitutes a separate lineage from the genus Passer and has been postulated as a possible ancestral group (Allende et al., 2001), feather carrying may have totally lost its primitive (thermal) function and may have evolved to serve as an aesthetic trait (i.e. as a signal, see Fig. 1). This is a very likely scenario given that most of the Petronia species are found in Africa and/or are characteristic of arid zones. ‘Sexual Signalling’ Hypothesis A common finding in studies that looked for the significance of feather carrying with an ornamental purpose is the existence of a positive relationship between feather presence and clutch size (Table 3). We found that the experimental addition of feathers to nests caused an increase in clutch size, a similar result to that reported by Veiga and Polo (2011) in spotless starlings. Since in both species (rock sparrows, spotless starlings) feather carrying is mostly a female trait, it is likely that the presence of feathers has a positive effect per se on female prospects, triggering a differential response in the form of increased egg production (Veiga & Polo, 2011). In this sense, anecdotal evidence suggests that male rock sparrows can also gather feathers sporadically (our personal observation; see also Veiga & Polo, 2011). Therefore, we cannot discard the possibility that experimental females perceived that feathers were brought by their partner, which could have induced them to increase their reproductive investment according to pre
pez de dictions of the differential allocation hypothesis (García-Lo Hierro et al., 2013; Sanz & García-Navas, 2011). Alternatively, or additionally, and also from the female's perspective, female rock sparrows may perceive the presence of feathers as a cue of increased female competition (i.e. increased risk of losing the partner) and they may opt to lay larger clutches in order either to advertise their individual quality or to increase brood demand, and thereby prevent male abandonment. This latter scenario is certainly plausible since we observed that females did not willingly accept the presence of feathers in their nests; these were buried or, in some cases, covered with faeces or removed from the nestbox. Thus, it is reasonable to think that rock sparrows just perceived the experimental feathers as being introduced by female rivals (see also García-Navas, Ortego, Ferrer, & Sanz, 2013b). It implies that our manipulation successfully mimicked the presence of an intruder, which is a common circumstance in this study system. In fact, we occasionally observed that feathers supplied by us were carried to the nest by ‘floater’ birds, probably as a means to urge the owner to abandon the nest (some nests are occupied by two different females within the same breeding season; our personal observation). If the presence of foreign feathers is perceived as a threat or a sign of increased nest vulnerability to competitors by females, it could explain their higher investment in nest defence in those nests in which we added feathers (see more below). Regarding the males, we found a greater investment by the partner in response to the feather addition treatment; males in the experimental group tended to desert less frequently and spent on average more time at the nest. These results support the sexual signalling hypothesis and are in agreement with previous studies showing that male rock sparrows can strategically allocate their parental investment in response to their partner's quality or attractiveness, advertised through bodily ornaments (Griggio et al., 2003; Pilastro et al., 2003). Furthermore, this hypothesis is certainly plausible given the strong intensity of sexual conflict over parental care in this species, in which each pair member tries to reduce its workload urging the other to work harder (Griggio & Pilastro, 2007). Thereby, the antagonistic interests of both sexes may lead to the appearance of mechanisms intended to promote greater investment by the partner. In fact, we observed a positive relationship between male provisioning effort and the number of feathers added naturally to the nest (in the years prior to the experiment) in one of the study areas. However, the fact that male rock sparrows did not fully compensate for the reduced care by females in experimental nests is not surprising since male rock sparrows usually play a secondary role in nestling provisioning (Griggio & Pilastro, 2007). Similarly, in an experimental study with this species, Pilastro et al. (2003) manipulated the yellow spot size of females and found that ornament reduction resulted in a decrease in male nest attendance whereas ornament enlargement had no effect on provisioning effort. This suggests that male rock sparrows may be less willing to increase their investment above a certain threshold, except when there is no choice (i.e. female brood desertion). However, in species like this in which both pair members appear to be constantly assessing one another and ‘negotiating’ over care, it is difficult to determine to what extent the observed effect may be a consequence of a pure effect of the Table 3 Studies providing observational (C) or experimental data (E) on feather carrying or petal carrying behaviour with an ornamental purpose in different avian species Species Material* Sex Experimental or correlative data Hypothesis Outcomes/Observations Source Satin bowerbird Ptilonorhynchus violaceus Feathers (bower) Male C: Observational data Intersexual communication Borgia and Gore (1986) Archbold's Bowerbird Archboldia papuensis Feathers (bower) Male C: Observational Intersexual communication Tree swallows Tachycineta bicolor Feathers (nest, display) Male Female C: Observational data Intersexual communication Spotless starling Sturnus unicolor Feathers (nest) Female Intersexual communication Feathers (nest) Female E: Green plant (_ display) addition C: observational data E: Feathers addition Eagle owl Bubo bubo Feathers (territory) Male C: Observational data Blue tit Cyanistes caeruleus Feathers (nest) Male Feathers (nest) Male E: Feather addition and feather removal C: observational data E: Feather addition _ decorates the avenue bowers with rare blue feathers of Psittacidae (which can be stolen from other bowers) _ uses feathers from bird of paradise Pteridophora alberti as bower decoration Aerial pursuits and battles for feathers are fierce and may indicate competitive ability and individual quality \ carries feathers in response to a _ courtship behaviour (addition of green material) Increase of clutch size, no change in provisioning effort Prey feathers and faeces deposited on plucking sites in proximity to the nest may be used as territorial marks Increase of clutch size, no change in provisioning effort House sparrow Passer domesticus Feathers (nest, display) Male Rock sparrow Petronia petronia Feathers Flowersy (nest) Feathers (display) Female E: Feather addition and feather removal C: Correlative data E: Feathers addition Male C: Observational data Flowers (display) Male C: Observational data Flowers (display) Male C: Observational data Flowers (display) Male C: Observational data Flowers (display) Male C: Observational data Black-throated weaver Ploceus benghalensis Flowers (nest) Male C: Observational data Intersexual communication Striated weaver-bird Ploceus manyar Flowers (nest) Male C: Observational data Intersexual communication * y Intersexual communication Intrasexual communication (decreases the male's certainty of paternity) Intersexual communication Intersexual communication Intersexual communication Intersexual communication Intersexual communication Intersexual communication Intersexual communication Lombardo (1995); Dawson et al. (2011) Polo and Veiga (2006) Veiga and Polo (2011) Penteriani and Delgado (2008) Sanz and García-Navas (2011) _ reduced parental care (provisioning effort, nest defence) García-Navas et al. (2013b) Increase of clutch size and \ provisioning effort
pez de Hierro García-Lo et al. (2013) Increase of clutch size, no change in provisioning effort (but _ deserted less often) _ holds a feather in the bill while courting the \ _ carries flowers from Lantana sp. during intrusions into nearby territories _ carries yellow petals and displays them to conspecifics (mainly \) _ carries pink or purple petals and display them to conspecifics (mainly \) _ carries blue petals and displays them to conspecifics (mainly \) Present study Nest decorated with orange or scarlet flowers cemented to the nest with cow dung Nests decorated with Acacia flowers cemented to the nest with cow dung or wet mud Immelmann (1980) V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 African waxbill Estrilda astrild Red-backed fairy wren Malurus melanocephalus Superb fairy wren Malurus cyaneus Splendid fairy wren Malurus splendens White-winged fairy wren Malurus leucopterus Intersexual communication Intrasexual communication Frith and Frith (1990) Karubian and Alvarado (2003) Mulder (1997); Rowley and Russell (1997) Rowley (1991); Rowley and Russell (1997) Rowley and Russell (1997); Rathburn and Montgomerie (2003) Ali and Ripley (1974) Ali and Ripley (1974) In parenthesis is indicated if the material is deposited in the nest/bower/territory or if this behaviour is part of a display. Rock sparrows also add blue flowers (but to a lesser extent) in Quintos de Mora, but not in Barbagia, suggesting the existence of local preferences for nest decorations in this species. 103 104 V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 treatment on the individual's decision making or a response to the change in provisioning behaviour of the partner. Nevertheless, although nestlings from experimental nests were fed less frequently than those from control nests, they were not smaller or lighter than the latter. This suggests that experimental females may take advantage of their longer time lags between provisioning visits to increase the size and/or quality of prey (e.g. Grieco, 2002). That is, the reduction in female provisioning rate did not result in nestlings being in worse condition. Feather presence (perceived by females as territorial intrusions) may have reduced females' level of maternal care through hormonal pathways and, therefore, explain why females fed their young less often in those nests that were artificially ornamented. For example in an experiment with spotless starlings, whose males usually add green material to their nests, researchers supplied some nests with this material and found that female partners increased their testosterone levels compared with control females
pez-Rull, Gil, & Veiga, 2010; Veiga & Polo, 2011). The (Polo, Lo presence of green plants thus may have induced female spotless starlings to increase their level of aggressiveness, which may in turn have reduced their investment in caring for the young as a consequence of the existence of a trade-off between territorial aggression and parental care (e.g. McGlothlin, Jawor, & Ketterson, 2007; Schwagmeyer, Schwabl, & Mock, 2005). Regarding this, several studies in which females were implanted with testosterone found an increase in female aggression at the expense of maternal care (e.g. Rosvall, 2013; Veiga & Polo, 2008). In our case, however, the decrease in provisioning effort observed in experimental females cannot be totally explained as a result of an increase in female aggressive behaviour because we only found a significant negative association between nest guarding and provisioning effort in males. That is, females did not spend more time defending the nest, in lieu of provisioning. At this point, we can raise two likely explanations for this result. First, female rock sparrows may decrease their provisioning frequency in response to the increase in femaleefemale competition that might be inferred from the presence of foreign feathers. In other words, females may change their priorities in response to the simulated challenge. Second, females may decrease their level of parental investment in response to the perceived increase in the males' propensity to contribute to offspring care (see above). That is, an increased predisposition of males to contribute to brood care may relax the demand put on the opposite sex (Parker, Royle, & Hartley, 2002). ‘Social Status’ Hypothesis Nest decorations may also function as an effective deterrent to neighbouring individuals or potential intruders because of their high visibility and effectiveness in the absence of the signaller (Penteriani & Delgado, 2008; Sergio et al., 2011). In this way, a territory owner can inform passing receivers about his vigour and willingness to invest in nest defence, even when they are not present, and may deter potential intruders from contending for the nest. In this sense, we found that experimental nests were visited less by intruders, which suggests that trespassers avoided decorated nests; that is, receivers responded to the signal. In spite of that, there was an effect of the treatment on the mean time that females spent guarding the nest; females from experimental nests invested more in passive nest defence, indicating that feather supplementation could have resulted in an increase in females' perception of the risk of nest usurpation (which may have forced them to keep guard against potential intruders). In addition, there are several lines of evidence in support of the intrasexual signalling hypothesis. First, suitable nesting sites for rock sparrows in our study system are scarce, and nestboxes constitute a valuable resource. As a consequence, damage inflicted by conspecifics during nest intrusions (egg destruction, removal of nesting material and, ultimately, nest eviction) is the major cause of nesting failure in these colonies, especially in Quintos de Mora (where it affected ca. 15% of the nests). We observed that 37% of nests were visited by conspecific intruders during the brood-rearing period and probably visiting frequency is higher in the early stages of the breeding period (nest building, egg laying; our personal observation). Second, we have observed that rock sparrows sometimes place feathers in the nestbox before the start of the nest-building period (it is relatively common to find empty boxes with some new feathers added in April or early May, see Supplementary Material). Therefore, it is reasonable to think that feather presence may work as a sort of ‘nestbox booking’ or ‘nestbox claiming’. Third, female rock sparrows are prone to retaining their breeding territory; they often lay in the same nestbox with different partners in different years. We observed that 22 of 35 recaptured females (63%) occupied the same nestbox used in the previous breeding season whereas this was the case in 51% (15/29) of males. This is in contrast with the common finding of female-biased dispersion in birds (Greenwood, 1980). A similar pattern has been reported in tree swallow, Tachycineta bicolor, populations, where there is strong competition for nesting cavities and aggressive behaviour to defend the nesting territory from female floaters is an essential component of reproductive success (e.g. Leffelaar & Robertson, 1985; Rosvall, 2008). In contrast, female site fidelity is relatively frequent in tropical passerines with year-round
nez, 2009; territoriality, such as hummingbirds (Illes & Yunes-Jime Tobias, Gamarra-Toledo, García-Olaechea, Pulgarín, & Seddon, 2011). Most of these species bear ornaments that are expressed in both sexes, as is the case in the rock sparrow, which is consistent with the notion that mutual ornamentation often goes hand-in-hand with territoriality by both sexes (Kraaijeveld, Kraaijeveld-Smit, & Komdeur, 2007; Tobias, Montgomerie, & Lyon, 2012; West-Eberhard, 1983). Thus, it is reasonable to argue that processes leading to female ornamentation can be better understood in a social selection framework, since not only male mate choice but also femaleefemale competition over nonsexual resources (social competition sensu West-Eberhard, 1983) may be a source of selection for such traits, especially in species in which breeding pairs form dense groups or colonies (Clutton-Brock & Huchard, 2013; LeBas, 2006; Rosvall, 2011). Conclusions The outcome of our experiment and observational data allows us to speculate that females add feathers to the nest to inform about their status or quality to prospecting females in search of a nesting site (and/or a partner), and to their current partners to persuade them to invest more in the care of the brood. This suggests that this female ornament may be under direct sexual selection by males and selection via reproductive competition over nonsexual resources among females. To the best of our knowledge, this is the first study showing that males can differentially allocate their reproductive investment according to nonbodily female ornamentation. Our results also add to increasing evidence that resource defence may be an important function of female ornamental traits (including extended phenotype signals), a neglected topic in the field of sexual selection (Tobias, Montgomerie, & Lyon, 2012). In particular, feather carrying may represent an overlooked but widespread tool for communicating current reproduction to conspecifics (Penteriani & Delgado, 2008; see also Table 3). However, we must highlight the speculative nature of our work and, consequently, these findings should be interpreted cautiously. Our results provide a baseline for further testing of the function of nest ornamentation as a female signal of resource-holding potential. Further studies focused on patterns of competitive interactions among females (e.g. femaleefemale contests) are necessary to elucidate the importance of V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 access to resources, such as territories or feeding sites, as a driving force in the evolution of female ornaments. Acknowledgments We are indebted to the board of ‘Centro Quintos de Mora’ (Spain) for the facilities offered to work and live there. Sebastiano Secchi generously allowed us to work on his beautiful land ‘Agriturismo Testone’ (Italy). We warmly thank Conchi C
aliz for her help with molecular sexing. We thank Herbert Hoi and Giorgio Massaro for practical help and constant support. Vincenzo Penteriani and two anonymous referees provided valuable comments. Funding was provided by a career development bursary for V.G.N. by the British Ornithologists' Union (BOU). Supplementary Material Supplementary material associated with this article is available, in the online version, at http://dx.doi.org/10.1016/j.anbehav.2014. 10.024. References Ali, S., & Ripley, S. D. (1974). Handbook of the birds of India and Pakistan. Oxford, U.K.: Oxford University Press.
n, J., Martínez-Laso, J., Lowy, E., et al. Allende, L. M., Rubio, I., Ruíz-del-Valle, V., Guille (2001). The Old World Sparrows (Genus Passer) phylogeography and their relative abundance of nuclear mtDNA pseudogenes. Journal of Molecular Evolution, 53, 144e154.
n a la biología del Gorrio
n Moruno, Passer hispanioAlonso, J. C. (1982). Contribucio
gicas con el Gorrio
n lensis (Temm.), en la Península Ib
erica y sus relaciones ecolo común, Passer domesticus (L.) (Unpublished doctoral thesis). Madrid, Spain: Universidad Complutense de Madrid. Barber, I. (2013). The evolutionary ecology of nest construction: insight from recent fish studies. Avian Biology Research, 6, 83e98. Barber, I., Nairn, D., & Huntingford, F. A. (2001). Nests as ornaments: revealing construction by male sticklebacks. Behavioral Ecology, 12, 390e396. Berg, M. L., Beintema, N. H., Welbergen, J. A., & Komdeur, J. (2006). The functional significance of multiple nest-building in the Australian Reed Warbler Acrocephalus australis. Ibis, 148, 395e404. Borgia, G. (1985). Bower quality, number of decorations and mating success of male satin bowerbirds (Ptilonorhynchus violaceus): an experimental analysis. Animal Behaviour, 33, 266e271. Borgia, G., & Gore, M. A. (1986). Feather stealing in the Satin Bowerbird (Ptilonorhynchus violaceus): male competition and the quality of display. Animal Behaviour, 34, 727e738. Brouwer, L., & Komdeur, J. (2004). Green nesting material has a function in mate attraction in the European Starling. Animal Behaviour, 67, 539e548. Burley, N. (1986). Sexual selection for aesthetic traits in species with biparental care. American Naturalist, 127, 415e445. Clutton-Brock, T. H., & Huchard, E. (2013). Social competition and selection in males and females. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 368, 20130074. Cramp, S. (1998). The complete birds of the Western Paleartic (CD-Rom). Oxford, U.K.: Optimedia. Dawkins, R. (1982). The extended phenotype: the long reach of the gene. Oxford, U.K.: Oxford University Press. Dawson, R. D., Lawrie, C. C., & O'Brien, E. L. (2005). The importance of microclimate variation in determining size, growth and survival of avian offspring: experimental evidence from a cavity nesting passerine. Oecologia, 144, 499e507. Dawson, R. D., O'Brien, E. L., & Mlynowski, T. J. (2011). The price of insulation: costs and benefits of feather delivery to nests for male tree swallows Tachycineta bicolor. Journal of Avian Biology, 42, 93e102. van Dijk, R. E. (2009). Sexual conflict over parental care in penduline tits (Unpublished doctoral thesis). Bath, U.K.: University of Bath. Endler, J. A., Endler, L. C., & Doerr, N. R. (2010). Great bowerbirds create theaters with forced perspective when seen by their audience. Current Biology, 20, 1679e1684. Frith, C. B., & Frith, D. W. (1990). Archbold's Bowerbird Archboldia papuensis (Ptilonorhynchidae) uses plumes from King of Saxony Bird of Paradise Pteridophora alberti (Paradisaeidae) as bower decoration. Emu, 90, 136e137.
pez de Hierro, L., Moleo
n, M., & Ryan, P. G. (2013). Is carrying feathers a García-Lo sexually selected trait in house sparrows? Ethology, 119, 1e13. García-Navas, V., Arroyo, L., & Sanz, J. J. (2008). Nestbox use and reproductive parameters of Tree Sparrows Passer montanus: are they affected by the presence of old nests? Acta Ornithologica, 43, 32e42.
n, A., Ferrer, E. S., & Fathi, H. (2013a). Mating García-Navas, V., García del Rinco strategies, parental investment and mutual ornamentation in Iberian Rock Sparrows Petronia petronia. Behaviour, 150, 1641e1663. 105 García-Navas, V., Ortego, J., Ferrer, E. S., & Sanz, J. J. (2013b). Feathers, suspicions and infidelities: an experimental study on certainty of paternity and parental care in the blue tit. Biological Journal of the Linnean Society, 109, 552e561. Garson, P. J. (1980). Male behaviour and female choice: mate selection in the wren. Animal Behaviour, 28, 491e502. Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour, 28, 1140e1162. Grieco, F. (2002). Time constraint on food choice in provisioning blue tits, Parus caeruleus: the relationship between feeding rate and prey size. Animal Behaviour, 64, 517e526. Griggio, M., Devigili, A., Hoi, H., & Pilastro, A. (2009). Female ornamentation and directional male mate preference in the Rock Sparrow. Behavioral Ecology, 20, 1072e1078. Griggio, M., Matessi, G., & Pilastro, A. (2005). Should I stay or should I go? Female brood desertion and male counter strategy in Rock Sparrows. Behavioral Ecology, 16, 435e441. Griggio, M., Mingozzi, T., Bortolin, F., & Pilastro, A. (2008). Trade-off between sexual activities and parental care: An experimental test using handicapped mates. Ethology, Ecology & Evolution, 20, 155e164. Griggio, M., & Pilastro, A. (2007). Sexual conflict over parental care in a species with female and male brood desertion. Animal Behaviour, 74, 779e785. Griggio, M., Serra, L., Licheri, D., Monti, A., & Pilastro, A. (2007). Armaments and ornaments in the Rock Sparrow: a possible dual utility of a carotenoid-based feather signal. Behavioral Ecology and Sociobiology, 61, 423e433. Griggio, M., Tavecchia, G., Biddau, L., & Mingozzi, T. (2003). Mating strategies in the Rock Sparrow Petronia petronia: the role of female quality. Ethology, Ecology & Evolution, 15, 389e398. Griggio, M., Valera, F., Casas, A., & Pilastro, A. (2005). Males prefer ornamented females: a field experiment of male choice in the Rock Sparrow. Animal Behaviour, 69, 1243e1250. Griggio, M., & Venuto, G. (2007). The relationship between mate guarding and brood desertion in the Rock Sparrow Petronia petronia. Ethology, Ecology & Evolution, 19, 175e182. Griggio, M., Zanollo, V., & Hoi, H. (2010). Female ornamentation, parental quality, and competitive ability in the rock sparrow. Journal of Ethology, 28, 455e462. Hansell, M. H. (1995). The demand for feathers as building material by woodland nesting birds. Bird Study, 42, 240e245. Hansell, M. H. (2000). Bird nests and construction behaviour. Cambridge, U.K.: Cambridge University Press.
kely, T. (2009). How is sexual conflict over parental Harrison, F., Barta, Z., Cuthill, I., & Sze care resolved: a meta-analysis. Journal of Evolutionary Biology, 22, 1800e1812. Herbestein, M. E., Craig, C. L., Coddington, J. A., & Elgar, M. A. (2000). The functional significance of silk decorations of orb-web spiders: a critical review of the empirical evidence. Biological Reviews, 75, 649e669. Hoi, H., Schleicher, B., & Valera, F. (1996). Nest size variation and its importance for mate choice in penduline tits, Remiz pendulinus. Animal Behaviour, 51, 464e466.
nez, L. (2009). A female songbird out-sings male conspeIlles, A. E., & Yunes-Jime cifics during simulated territorial intrusions. Proceedings of the Royal Society of London B: Biological Sciences, 276, 981e986. Immelmann, K. (1980). Introduction to ethology. New York, NY: Plenum Press. Karubian, J., & Alvarado, A. (2003). Testing the function of petal-carrying in the Redbacked Fairy wren (Malurus melanocephalus). Emu, 103, 87e92. € ppenKottek, M., Grieser, J., Beck, C., Rudolf, B., & Rube, F. (2006). World Map of the Ko Geiger climate classification updated. Meteorologische Zeitschrift, 15, 259e263. Kraaijeveld, K., Kraaijeveld-Smit, F. J. L., & Komdeur, J. (2007). The evolution of mutual ornamentation. Animal Behaviour, 74, 657e677. LeBas, N. R. (2006). Female finery is not for males. Trends in Ecology & Evolution, 21, 170e173. Leffelaar, D., & Robertson, R. J. (1985). Nest usurpation and female competition for breeding opportunities by tree swallows. Wilson Bulletin, 97, 221e224. Lombardo, M. P. (1995). Nest architecture and reproductive performance in tree swallows (Tachycineta bicolor). Auk, 111, 814e824. Lombardo, M. P., Bosman, R. M., Faro, C. A., Houtteman, S. G., & Kluisza, T. S. (1995). Effect of feathers as nest insulation on incubation behavior and reproduction performance of Tree Swallows (Tachycineta bicolor). Auk, 112, 973e981. Madden, J. R. (2003). Male spotted bowerbirds preferentially choose, arrange and proffer objects that are good predictors of mating success. Behavioral Ecology and Sociobiology, 53, 263e268. Mainwaring, M. C., Hartley, I. R., Lambrechts, M. M., & Deeming, D. C. (2014). The design and function of birds' nests. Ecology and Evolution, 20, 3909e3928. http://dx.doi.org/10.1002/ece3.1054. in press. Matessi, G., Carmagnani, C., Griggio, M., & Pilastro, A. (2009). Male Rock Sparrows differentially allocate nest defence but not food provisioning to offspring. Behaviour, 146, 209e223. Matessi, G., McGregor, P. K., Peake, T. M., & Dabelsteen, T. (2005). Do male birds intercept and use rival courtship calls to adjust paternity protection behaviours? Behaviour, 142, 507e524. Maynard Smith, J., & Harper, D. G. C. (2003). Animal signals. Oxford, U.K.: Oxford University Press. McGlothlin, J. W., Jawor, J. M., & Ketterson, E. D. (2007). Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist, 170, 864e875. McGowan, A., Sharp, S. P., & Hatchwell, B. J. (2004). The structure and function of nests of long-tailed tits Aegithalos caudatus. Functional Ecology, 18, 578e583. V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 Trnka, A., & Prokop, P. (2011). The use and function of snake skins in the nests of Great Reed Warblers Acrocephalus arundinaceus. Ibis, 153, 627e630. Valera, F., Schleicher, B., & Hoi, H. (1997). Egg burial in Penduline tits (Remiz pendulinus): its role in nest desertion and female polyandry. Behavioral Ecology, 8, 20e27. Veiga, J. P., & Polo, V. (2005). Feathers at nests are potential female signals in the spotless starling. Biology Letters, 1, 334e337. Veiga, J. P., & Polo, V. (2008). Fitness consequences of increased testosterone levels in female spotless starlings. American Naturalist, 172, 42e53. Veiga, J. P., & Polo, V. (2011). Feathers in the spotless starling nests: a sexually selected trait? Behaviour, 148, 1359e1375. Walter, A., & Elgar, M. A. (2012). The evolution of novel animal signals: silk decorations as a model system. Biological Reviews, 87, 686e700. West-Eberhard, M. J. (1983). Sexual selection, social competition, and speciation. Quarterly Review of Biology, 58, 155e183. Appendix Number of male provisioning visits/h 9 8 7 6 5 4 3 2 1 0 2 4 6 8 10 Number of feathers 12 14 16 Figure A1. Male provisioning effort (number of feeding visits/h) in relation to the number of natural feathers found in the nest for the Barbagia population (2011e2012; N ¼ 34, seven overlapping data points). 9 1.8 8 1.6 7 1.4 6 1.2 5 1 4 0.8 3 0.6 2 0.4 1 0.2 0 Number of male provisioning visits/chick per h Moreno, J. (2012). Avian nests and nest-building as signals. Avian Biology Research, 5, 238e251. Mulder, R. A. (1997). Extra-group courtship displays and other reproductive tactics of Superb Fairy-Wrens. Australian Journal of Zoology, 45, 131e143. Nemeth, E., Kempenaers, B., Matessi, G., & Brumm, H. (2012). Rock sparrow song reflects male age and reproductive success. PLoS One, 7, e43259. € Ostlund-Nilsson, S., & Holmlund, M. (2003). The artistic three-spined stickleback (Gasterosteus aculeatus). Behavioral Ecology and Sociobiology, 53, 214e220. Parker, G., Royle, N. J., & Hartley, I. R. (2002). Intrafamilial conflict and parental investment: a synthesis. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 357, 295e307. Penteriani, V., & Delgado, M. M. (2008). Owls may use faeces and prey feathers to signal current reproduction. PLoS One, 3, e3014. Pilastro, A., Griggio, M., & Matessi, G. (2003). Male Rock Sparrows adjust their breeding strategy according to female ornamentation: parental or mating investment? Animal Behaviour, 66, 265e271. Pinowski, J., Andrzej, H., Leszek, J., Pinowska, B., Barkowska, M., Grodzki, A., et al. (2006). The thermal properties of some nests of the Eurasian Tree Sparrow Passer montanus. Journal of Thermal Biology, 31, 573e581.
pez-Rull, I., Gil, D., & Veiga, J. P. (2010). Experimental addition of green Polo, V., Lo plants to the nest increases testosterone levels in female spotless starlings. Ethology, 116, 129e137. Polo, V., & Veiga, J. P. (2006). Nest ornamentation by female spotless starlings in response to a male display: an experimental study. Journal of Animal Ecology, 75, 942e947. Rathburn, M. K., & Montgomerie, R. (2003). Breeding biology and social structure of White-winged Fairy-wrens (Malurus leucopterus): comparison between island and mainland subspecies having different plumage phenotypes. Emu, 103, 295e306. Reid, J. M., Monaghan, P., & Ruxton, G. D. (2000). Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation. Proceedings of the Royal Society of London B: Biological Sciences, 267, 37e41. Rosvall, K. A. (2008). Sexual selection on aggressiveness in females: evidence from an experimental test with tree swallows. Animal Behaviour, 75, 1603e1610. Rosvall, K. A. (2011). Intrasexual competition in females: evidence for sexual selection? Behavioral Ecology, 22, 1131e1140. Rosvall, K. A. (2013). Life history trade-offs and behavioral sensitivity to testosterone: an experimental test when female aggression and maternal care cooccur. PLoS One, 8, e54120. Rowley, I. (1991). Petal-carrying by the Red-backed Fairy-wren. Sunbird, 21, 112e113. Rowley, I., & Russell, E. (1997). Fairy-wrens and Grasswrens. Oxford, U.K.: Oxford University Press. Sanz, J. J., & García-Navas, V. (2011). Nest ornamentation in blue tits: Is feather carrying ability a male status signal? Behavioral Ecology, 22, 240e247. Schaedelin, F. C., & Taborsky, M. (2006). Mating craters of Cyathopharynx furcifer (Cichlidae) are individually specific, extended phenotypes. Animal Behaviour, 72, 753e761. Schaedelin, F. C., & Taborsky, M. (2009). Extended phenotypes as signals. Biological Reviews, 84, 293e313. Schaedelin, F. C., & Taborsky, M. (2010). Female choice of a non-bodily ornament: an experimental study of cichlid sand craters in Cyathopharynx furcifer. Behavioral Ecology and Sociobiology, 64, 1437e1447. Schuetz, J. G. (2005). Common waxbills use carnivore scat to reduce the risk of nest predation. Behavioral Ecology, 16, 133e137. Schwagmeyer, P. L., Schwabl, H. G., & Mock, D. W. (2005). Dynamics of biparental care in house sparrows: hormonal manipulations of paternal contributions. Animal Behaviour, 69, 481e488.
pez, L., Lemus, J., et al. (2011). Raptor nest Sergio, F., Blas, J., Blanco, G., Tanferna, A., Lo decorations are a reliable threat against conspecifics. Science, 331, 327e330. Soler, J. J., Møller, A. P., & Soler, M. (1998). Nest building, sexual selection and parental investment. Evolutionary Ecology, 12, 427e441. Soler, J. J., de Neve, L., Martínez, J. J., & Soler, M. (2001). Nest size affects clutch size and the start of incubation in magpies: an experimental study. Behavioral Ecology, 12, 301e307.
n, M. (1996). An experimental Soler, M., Soler, J. J., Møller, A. P., Moreno, J., & Linde analysis of the functional significance of an extreme sexual display: stonecarrying in the black wheatear Oenanthe leucura. Animal Behaviour, 51, 247e254. Svensson, L. (1992). Identification guide to European passerines. Stockholm, Sweden: Svensson.
ry, M., & Casas, J. (2009). The multiple disguises of spiders: web colour and The decorations, body colour and movement. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 471e480. Tobias, J. A., Gamarra-Toledo, V., García-Olaechea, D., Pulgarín, P. C., & Seddon, N. (2011). Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments. Journal of Evolutionary Biology, 24, 2118e2138. Tobias, J. A., Montgomerie, R., & Lyon, B. E. (2012). The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367, 2274e2293.
th, Z., & Griggio, M. (2011). Leaders are more attractive: Birds with bigger yellow To breast patches are followed by more group-mates in foraging groups. PLoS ONE, 6, e26605. Number of male provisioning visits/h 106 0 0 3 4 5 6 7 Brood size on day 8 Figure A2. Relationship between nestling demand (brood size on day 8) and male provisioning rate (feeding visits/h: filled circles and continuous line; feeding visits/ chick per h: empty circles and dotted line). V. García-Navas et al. / Animal Behaviour 99 (2015) 95e107 36 Mean nestling mass on day 13 (g) 34 32 30 28 26 24 22 20 0 40 60 80 20 Male’s share of provisioning effort (%) 100 Figure A3. Mean nestling mass on day 13 in relation to the male’s contribution to nestling provisioning (proportion of provisioning visits to the nest by the male divided by the total number of visits by the male and the female). Only biparental nests (i.e. those in which both parents were present) were considered. The relationship remained significant (r ¼ 0.39, P ¼ 0.02) after excluding the point indicated with an arrow. 107