Access the full text.
Sign up today, get DeepDyve free for 14 days.
Revista Brasileira de Ornitologia 25(1): 12–19. ARTICLE March 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil 1 1 1 1 1,2 Christian Beier , Márcio Repenning , Maurício da Silveira Pereira , André Pereira & Carla Suertegaray Fontana PUCRS – Pontifícia Universidade Católica do Rio Grande do Sul, Programa de Pós-Graduação em Zoologia, Museu de Ciências e Tecnologia, Laboratório de Ornitologia. Avenida Ipiranga, 6681, CEP 90619-900, Porto Alegre, RS, Brazil. Corresponding author: firstname.lastname@example.org Received on 18 August 2016. Accepted on 10 May 2017. ABSTRACT: We studied demography, territoriality and social/mate system of the Brazilian population of Yellow Cardinal (Gubernatrix cristata). The study was conducted in the municipality of Barra do Quaraí, western Rio Grande do Sul, Brazil, during two breeding seasons (October to February, 2013–2015). We ringed 35 (seven females, 14 males and 14 young) out of 53 individuals found, and by September 2015, the Brazilian population of Yellow Cardinal had 38 remaining individuals. Adult sex ratio was 1.5:1 and the lifespan was at least 8 years. Pairs are socially monogamous and territorial, with male-biased philopatry and female-biased dispersal. The mean territory size was 18 ha, and mean home range was 27.7 ha. Some pairs and nests (23%) were attended by one or two nest helpers, which contributed on nest and territory defense, and provisioning of nestlings and fledglings. Presence of helpers is a key new finding for this species. Parental care was biparental or cooperative, and t he pair had high frequency of visits to the nest than helpers. Mean nest productivity was two fledglings/successful nest attended by helpers, and one fledgling/successful nest not attended by helpers. We recorded second broods after a successful attempt, only when helpers were present. Overall Mayfield nesting success was 18%, 40% for nests with and 13% without helpers. We recorded a case of inbreeding, between father and daughter. The species need for large home ranges and factors that may adversely affect the breeding success such as inbreeding, predation, and parasitism can exacerbate the status of the threatened Brazilian population and the species. It reinforces the importance of autecology studies and their contribution to the conservation schemes. KEY-WORDS: breeding territory, home range, nest helpers, small population, threatened species. INTRODUCTION breeding behavior affect the territorial and home range dynamics, such as their sizes, boundaries, acquisition, The Yellow Car dinal, Gubernatrix cristata, is a passerine dispersal, among others. Because natural habitats are of temperate South America and its natural history is usually fragmented to some degree, small patches may relatively unknown. It occurs in the savannas of Argentina, not have sufficient area for home ranges and a lso increase predation and parasitism near edges (Beier et al. 2002), Uruguay and southern Brazil (Jaramillo 2011). Due to their color and song, they are often captured for illegal as well as the patch isolation may have negative effects on trade in wildlife (Martins-Ferreira et al. 2013). Illegal dispersal (Pavlacky-Jr. et al. 2012). trapping and wildlife trade, along with habitat loss, were Cooperative breeding is a social system characterized the main causes of the great population decline for this by a breeding pair and one or more individuals that did not breed, but collaborate to rear a brood (Woolfenden species, now considered as globally “Endangered” and regionally threatened (BirdLife International 2015), & Fitzpatrick 1984, Burt et al. 2007). These individuals “Endangered” in Argentina and Uruguay (López- are called nest helpers (hereafter, helpers). Why some Lanús et al. 2008, Azpiroz et al. 2012), and “Critically individuals tend to postpone their own reproduction Endangered” in Brazil (Martins-Ferreira et al. 2013). and help to rear a brood from others has intrigued scientists for decades. Studies have tried to explain how Home range is an area where an individual restricts its activities during the year or period (Odum & Kuenzler the cooperative breeding evolved (Poiani & Jermiin 1955). When part of or all home range is defended against 1994, Du Plessis et al. 1995, Arnold & Owens 1998, other conspecifics it is defined as a territory (Nice 1941, Heinsohn & Legge 1999, Doerr & Doerr 2006, Russell Odum & Kuenzler 1955). Home range is a cognitive et al. 2007, Hatchwell 2009, Cockburn & Russell 2011, Jetz & Rubenstein 2011, Feeney et al. 2013, Downing et map of resources that individuals keep up-to-date to fulfil their requirements (Powell & Mitchell 2012). Social and al. 2015, Drobniak et al. 2015), but life-histories differ Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. considerably between species and there is not a one-size- ring (standard CEMAVE/ICMBio; the Brazilian Banding fits-all hypothesis (Cockburn 1998, Berg et al. 2012, Agency) and a unique combination of colored plastic Gamero et al. 2014). There are more than 10,000 extant rings. Ten days old nestlings or chicks that just fledged bird species in the world, and 9% are estimated to present were also marked. We measured birds following Eck et cooperative breeding (Cockburn 2006), and among the al. (2011): wing chord, tail length, tarsus length, bill oscines 18.5% (Cockburn 2003). The Neotropics is the and culmen length, nostril to bill tip, and total length, region with highest biodiversity on Earth, but it is the using a precision caliper (0.1 mm) and a ruler (1.0 mm). relatively less studied in terms of bird behavior (Stutchbury Body mass was measured using a precision dynamometer & Morton 2001). It is estimated that 6% (218 species) (0.5 g) of kind Pesola Swiss Micro 20060. Plumage of all Neotropical birds have cooperative breeding (Jetz categorization follows Wolfe et al. (2010). & Rubenstein 2011), but the effective number of species Individual behavior was recorded ad libitum while that breed cooperatively may be slightly higher as the monitoring nests and when away from the nest (Altmann breeding systems and natural histories of more birds are 1974). Observations of parental care were mainly in the being described. morning, from sunrise until 11:00 h, or afternoon, from Here, we describe cooperative breeding in the 17:00 h until sunset, using binoculars (12 × 50 mm) and Yellow Cardinal for the first time. We compare breeding spotting telescope (25–60×). We used a camcorder at one and success between pairs with and without helpers to nest, with mean recording time of 72 ± 21.7 min (50– determine the potential benefits of cooperation. We also 100 min; n = 5) every 2–3 days. We divided nestling stage examine demography of the Brazilian population of the in two nestling phases: initial (1–8 days) and final (9–16 cardinal, and place cooperation in terms of social system days), and calculated the visit rate for each individual and and breeding territories. We then interpret these new phase. findings in the context of conservation of this threatened We considered breeding territory as the maximum species. area that a male defended and where it nested (Nice 1941, Welty & Baptista 1988) and home range as the area frequently used but not necessarily defended (Odum & METHODS Kuenzler 1955, Powell & Mitchell 2012). When found, we noted the coordinates of family groups or individuals Study area using a handheld GPS. Encounters that ended without chasing or fight and individuals gone on opposing The study was carried out in Barra do Quaraí, state of Rio directions, we considered as territory boundaries. We Grande do Sul. From four study sites, three are located estimated the area of breeding territories using Minimum at Espinilho State Park (ESP; 30°12'S; 57°30'W), and Convex Polygon at 95% confidence (MCP 95%) (O dum one at São Marcos Ranch (SMR), adjacent to the ESP. & Kuenzler 1955). We estimated home range size using Only one site at ESP was not grazed by livestock. The Fixed Kernel Density Estimation at 95% probability of mean annual rainfall is 1300 mm and it is highly variable occurrence (KDE 95%), and kernel bandwidth calculated between years. Mean annual temperature is 24.3°C, with by Least Squares Cross Validation (LSCV) (Seaman et al. occurrence of < 0°C in winter, and occasionally > 40°C 1999, Jacob & Rudran 2006). We used only data from in summer. The vegetation is a savanna dominated by individuals with more than 25 locations due to minimum Prosopis affinis and Vachellia caven (Fabaceae) and is the sample size limitations of KDE (Seaman et al. 1999). largest among the last remnants of that type of savanna in Breeding territory and home range estimations were southern Brazil (Marchiori & Alves 2011). calculated using package adehabitatHR (Calenge 2006) in R (R Core Team 2015). Data collection Productivity was calculated as the mean number of fledglings by all successful nests. We calculated the We began with a pilot study from November 2012 until apparent success (Marini et al. 2010), as the ratio between January 2013. We then carried out observations from the number of successful nests and all monitored nests. October to February, during two breeding seasons (2013– Complementarily, we calculated Mayfield nesting success 2015) of the only known population of Yellow Cardinal (Mayfield 1975), with modifications to compare nests in Brazil. Population size, sex ratio, and longevity were with and without helpers (Hensler & Nichols 1981). estimated using banded birds, and unmarked individuals when it was possible to identify them by unique marks Statistical analysis on plumage. We searched for Yellow Cardinals at the beginning of each breeding season (October) and captured To assess differences on morphometric measurements adults using mist nets and marked with an aluminum between sexes and parental care between nestling phases Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. we used the non-parametric Mann-Whitney U-test nest was lost to predation and a second female divorced. (Wilcoxon rank-sum test). Comparison of the frequency All other pairs remained together. The divorced female of of visits to the nest of each group member (male, female 2014 was later found paired in a neighboring territory in 2015. On a territory where both individuals of the pair and helper) were run with Kruskal-Wallis H tests, followed by post-hoc pairwise Mann-Whitney U-tests. Values were marked, we ringed a nestling at the nest in January are presented as mean ± SD and considered statistically 2013. In May 2013, the female disappeared, but the significant when P < 0.05. young was observed with the male. In October 2013, we found father and daughter on their territory and apparently paired, which was confirmed in December RESULTS 2013 when we found a nest with nestlings. This male remained alone during the second breeding season. It is Capture, morphometric and demographic data the first recor d of inbreeding in the Yellow Cardinal. A fledgling from t his pair was ringed, but all young and the female were not seen since January 2014. We captured and marked 35 birds (7 adult females, 14 adult males, and 14 young). We also recognized 18 unmarked individuals (seven females, four males, and seven young). Nest helpers Of the 53 birds found in this study, 15 disappeared, and the remaining 38 were the known population of Yellow In 2012, we found a group with an adult male, an adult female and a male helper in formative plumage with some Cardinal in Brazil at that time. We found a secondary sex ratio of 1.5:1 (21/14). A male captured as adult in 2008 grey patches. We observed three pairs accompanied by was last seen in February 2015 and so was at least 8 years male helpers from December 2012 to January 2013. We old. There was no difference in body mass between sexes found 30 nests in two breeding seasons (2013–2015), of (males: 47.8 ± 2.8 g, n = 9; females: 47.9 ± 3.5 g, n = which helpers attended seven. A female helper attended one mating pair in the first season (2013). Two male 4), and we found sexual dimorphism only in wing chord (males: 94.9 ± 2.9 mm, n = 9; females: 89.9 ± 2.5 mm, n helpers attended a mating pair in the second season = 4; U = 2.5, P = 0.02) and tarsus length (males: 27.0 ± (2014–2015), but apparently, only one of them fed the 0.8 mm, n = 9; females: 25.4 ± 1.0 mm, n = 4; U = 4.5, nestlings. P = 0.04) (Table 1). Helpers were observed contributing in territory and nest defense, feeding nestlings and caring of fledglings. Table 1. Morphometric measurements of marked adults Yellow In the latter case, a mating pair had a successful nesting Cardinal (Gubernatrix cristata) grouped by sex. Values presented as attempt in December 2012 and re-nested in January mean ± 1 SD (n). 2013. The helper attended t he first nest but not the re- Measurement Male Female nesting attempt, as it was taking care of fledglings. Body mass (g) 47.8 ± 2.8 (9) 47.9 ± 3.5 (4) Fledglings may stay in the natal territory for up to 10 Total length (mm) 200.5 ± 4.8 (8) 195.3 ± 6.0 (3) months (n = 1 female). Apparently, helpers are offspring Wing cord (mm) 95.0 ± 2.9 (9) 89.9 ± 2.5 (4) of the mating pair, and it was confirmed in one case Tail length (mm) 89.0 ± 3.9 (9) 87.4 ± 2.7 (4) where helpers were marked as nestlings. In other cases, Tarsus length (mm) 27.0 ± 0.8 (9) 25.4 ± 1.0 (4) helpers were in formative plumage, which we assume that they were offspring of the previous bree ding season of the Bill length (mm) 18.2 ± 1.1 (9) 19.2 ± 0.6 (4) Culmen length (mm) 15.6 ± 2.1 (7) 16.1 ± 0.1 (2) breeding pair. Nostril to bill tip (mm) 11.5 ± 0.4 (9) 11.5 ± 0.3 (4) A male was found in October 2013 defending a small territory. It budded off part of its natal territory, where it was helper in the previous breeding season (2012–2013). Social/mate system This male did not mate, and then it returned to its natal territory as helper, where it stayed at least until February The Yellow Car dinal is socially monogamous and 2014. In October 2014, this male was found alone on the mated pairs may stay together for more than one its previous territory. Later in the season (November breeding season, and only two divorces were observed. 2014), we found it in another territory and paired with Additionally, two males lost their mates and mated again. an unmarked female, where it had two breeding attempts. In 2013, from nine mating pairs, one female disappeared and one divorced. After a successful nest, the divorced Productivity and nesting success female and her two offspring disappeared in December 2013, but all three were seen again in October 2014. At Mean productivity per successful nest was 1.6 ± 0.74 that time, the female had found another male, and the fledglings (n = 8). Successful nests without helpers fledged two offspring became helpers. In 2014, one female at a Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. a mean of one chick (4 fledglings/4 nests), and with 0.02) between helpers and females (3.71 ± 1.38 vs. 7.29 ± helpers fledged two (8 fledglings/4 nests). The apparent 2.69 visits/h; U = 5; P = 0.01). success of nests with and without helpers was 57% (4/7) and 31% (4/13), respectively. The Mayfield Nesting Success was 40% and 13% for nests with and without helpers, respectively (18% for all nests pooled). There was no difference between nests with and without helpers in probability of survival for incubation (0.544 ± 0.239 vs. 0.403 ± 0.117; Z = 0.53; P = 0.60), nor nestling stage (0.732 ± 0.231 vs. 0.318 ± 0.125; Z = 1.58; P = 0.11). Parental care We observed about 12 h of parental care at three nests and recorded 6 h at one nest. The total frequency of visits to the nest was 12.28 ± 5.26 visits/h and we found a significant difference between initial and final nestling phases (9.91 Figure 1. Frequency of visits to the nest of male (grey bars), female ± 3.88 vs. 16.0 ± 5.16 visits/h; U = 14, P = 0.03, n = (black bars), and helper (white bars) on nestling age of the Yellow Cardinal (Gubernatrix cristata). Bars represent mean ± 1 SD. 18). Males made 4.39 ± 1.69 visits/h, females 5.06 ± 3.13 visits/h and helpers 2.83 ± 1.72 visits/h (Figure 1). There was a significant difference on visit rate between family Breeding territories members during the complete nestling period (H = 7.92; P = 0.02), especially between helpers and females (2.83 Mean estimated breeding territory size was 17.9 ± 5.6 ± 1.72 vs. 5.06 ± 3.13 visits/h; U = 89.5; P = 0.02), and ha (11.9–28.4 ha; n = 9). Mean home range size was helpers and males (2.83 ± 1.72 vs. 4.39 ± 1.69 visits/h; 27.7 ± 9.1 ha (14.5–41.9 ha; n = 9; Figure 2). Breeding U = 84; P = 0.01). Only females increased significantly territories were relatively stable and defended year-round. their visit rate from initial to final nestling phase (3.64 ± A yearling female was marked in October 2013 and 2.58 vs. 7.29 ± 2.69 visits/h; U = 12.5; P = 0.02). There found later paired with a male two territories away from was no difference between frequency of visits per group her natal territory in November 2013. The mean distance member on initial phase (H = 4.32; P = 0.12), but there between simultaneous nests of different breeding pairs/ was significant difference on final p hase (H = 7.75; P = territories was 443 ± 155 m (215–628 m; n = 6). Figure 2. Distribution of home ranges (polygons) of 13 breeding pairs of Yellow Cardinal (Gubernatrix cristata), in the municipality of Barra do Quaraí, state of Rio Grande do Sul, Brazil. Shaded area represents the protected area of Espinilho State Park. Polygon lines (grey, continuous black, dotted, dashed) are only for visual differentiation purposes. Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. Birds were territorial, with both sexes defending the occurrence of the species. Small populations are likely to territory. Encounters between individuals of different have genetic and demographic problems through time, territories were noted (n = 8), where at least 50% (n = such as inbreeding (Lande 1988, Stacey & Taper 1992, 4) resulted on agonistic interactions and chasing. In one Pimm et al. 1993), which we observed in this population. case (January 2012), two males stepped into another Unmarked individuals that appear in definitive basic pair's territory, where it had an active nest, and they plumage may be immigrants from Argentina (about 4 were readily chased and expelled by the breeding pair. In km) or Uruguay. another case, a mating pair with two juveniles came into a The small bias towards males on adult sex ratio neighbor territory. Agonistic interactions occurred inside (1.5:1) that we found, despite the small sample and not the invaded territory, where only adults engaged in fight, being significant, may be caused by the tendency for accompanied by juveniles from safe distance. Three days males to become helpers (Doerr & Doerr 2006) and later, we found these two pairs fighting in the same site. female-biased adult mortality (Székely et al. 2014). For Breeding territories increased from nine during the White-banded Tanager, Neothraupis fasciata, a close- first season to 12 in the second season. The main cause was related species, the primary sex ratio was 1:1, including all males that were helpers or were alone on the first season, nestlings of all clutches (Gressler et al. 2014). Apparently, but that found females to mate on the second season. Yellow Cardinal is a species with female-biased dispersal, Two of these males were alone on isolated territories and and males tend to be philopatric. Dispersal is a critical moved into larger available areas. Other two males were event in the life of an individual, with high inherent risks helpers on a prior season, moved to other areas (a territory that tend to reduce the survival of dispersing birds. In far from natal ground) by territorial budding and paired addition, the opposite is true for philopatric individuals, with unmarked females (November 2014). which tend to have higher survival rates. White-banded We noted some movements outside territories for Tanager have female-biased dispersal (Soares 2007) with some individuals. One case was in winter (July 2015), slightly lower survival rates for females when fledglings when a pair was found alongside a vicinal dirty road, where (less than 2 months old) and small biases on sex ratio they gone about 700 m far from their territory. The pair towards males as a result of higher survival rates of the was apparently foraging on rice seeds of a harvested fie ld, philopatric sex, being 15% higher for subadult males with other bird species, as Red-crested Cardinal (Paroaria than for subadult females (Gressler 2012). Female-biased coronata), Saffron Finch ( Sicalis flaveo la), Shiny Cowbird adult sex ratios are also associated to higher divorce rates (Molothrus bonariensis) and Grayish Baywing (Agelaioides (Liker et al. 2014). We found a relatively low divorce rate badius). Other case was noted during the second breeding (14%), which corroborates this proposition. season at a stream between two territories (about 200 Mortality rates are unknown for the Yellow m from both territorial boundaries). There was a tree Cardinal, and in our study, it was not possible to estimate with dark purple and ellipsoid fruits (Chrysophyllum adult survival rates due to difficulties to distinguish marginatum, Sapotaceae) at the stream bank. In 12 between mortality and dispersal, and the short-term November 2014, we observed a widowed male feeding monitoring. However, adult survival seems to be high in on those fruits, and the tree was east of its territory. In 15 the Brazilian population, whereas all nine adults marked November 2014, we encountered two males of a territory in the first bree ding season were found and monitored south of the tree. In both situations, the individuals did in the second season. We estimated the age for a male not show any territorial behavior. (about 8 years old) based on ringing data and plumage, but this individual may be older as we do not know how old it was when it was marked. A wild female of Northern DISCUSSION Cardinal (Cardinalis cardinalis), a passerine with similar body size, was reported to survive more than 15 years We present here the first study about the Brazilian old (Klimkiewicz & Futcher 1987). Birds marked as population of the Yellow Cardinal. We report that the nestlings are excellent opportunities to obtain precise data remaining population is very small in Brazil and we on lifespan, as for other life-history traits, by means of confirmed a case of inbree ding, the first in the wild. continuous monitoring. We also found that the Yellow Cardinal defends large While there was no sexual dimorphism with respect territories, fledglings show delayed dispersal and with to body mass (as in Argentina, Domínguez et al. 2015), male-biased philopatry. Moreover, we show that the we did find differences in wing and tarsus measurements. species may breed cooperatively with nest helpers. In Thraupidae, most species exhibit slight or no sexual We are confident that the entire Brazilian dimorphism in body mass (Hilty 2011). Sexual size population of Yellow Cardinal from Espinilho savanna dimorphism is reported more frequently for species with was monitored by searching all potential areas of monomorphic plumage (Faria et al. 2007, Chiarani & Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. Fontana 2015). Székely et al. (2007) suggests that wing especially for home ranges estimates. Other grassland and tarsus lengths may be related to mating competition, birds have smaller territories and home ranges. It was where larger individuals have an advantage. estimated that mean territory size for Lesser Grass-finch (Emberizoides ypiranganus, 20 g) is 1.1 ha (maximum Parental care is unknown in nearly half (4313 species) of the 9456 species of birds for which parental 2.4 ha) (Chiarani & Fontana 2015), 3.7 ha for White- care was summarized (Cockburn 2006). This is the case banded Tanager (Soares 2007). Chiarani & Fontana for the Yellow Cardinal, which we can now say is an (2015) found that 83% of Lesser Grass-finch territories occasional cooperative breeder. Phylogeny may play a had the same males defending it in both breeding seasons. Pereira (2015) found a density of one territory/100 ha for role alongside environmental conditions on cooperative breeding occurrence (Edwards & Naeem 1993), and Yellow Cardinal in the same study site, reflecting its large it could emerge or disappear within a lineage (Berg et territories. Dardanelli et al. (2006) studied the minimum al. 2012). Recent molecular phylogenies found that area requirements of a bird community in Argentina, Gubernatrix, Hedyglossa (Diuca) and Neothraupis compose and they found that, from 54 woodland species, 80% needed no more than 3 ha. However, they also found a monophyletic clade (Barker et al. 2013, Burns et al. 2014), and cooperative breeding was already reported for that nine species needed fragments of 80 ha or more, Neothraupis (Alves 1990, Manica & Marini 2012). six of which also occur in our study site: Sharp-shinned We noted that individuals could begin the season Hawk (Accipiter striatus), White-fronted Woodpecker alone on their own territory and become helpers later in the (Melanerpes cactorum), T ufted Tit-Spinetail (Leptasthenura platensis), Scimitar-billed Woodcreeper (Drymornis same season. Nests with helpers had twice the productivity as those with only the pair. Since we do not have data bridgesii), Narrow-billed Woodcreeper (Lepidocolaptes for parental care in nests without helpers, we were not angustirostris), and Suiriri Flycatcher (Suiriri suiriri). able to identify the cause of increase in productivity by Delayed and female biased dispersal is reported for helper presence. The White-banded Tanager had similar other cooperatively breeding birds (e.g. Florida Scrub- jay Aphelocoma coerulescens, Woolfenden & Fitzpatrick productivity with and without helpers, but with helpers, parental effort b y the adult male decreased (Manica & 1984 and White-banded Tanager Soares 2007). Delayed Marini 2012). Load lightening hypothesis predicts that dispersal is also commonly associated with cooperative one or both parents could reduce their contribution to the breeding (Koenig et al. 1992), but some species delay nest due to the extra food delivered by helpers, increasing dispersal without helpers (e.g. Siberian Jay Perisoreus infaustus, Ekman & Griesser 2016). Some cooperatively parent survival (Manica & Marini 2012). Other possible effects of helper presence are reduced maternal allocation breeding species are able to expand and defend larger of resources on eggs (Paquet et al. 2013), and reduced territories due to increased group size. Consequently, rates of nest predation (Schaub et al. 1992) and brood groups with larger territories increase the chances of parasitism (Canestrari et al. 2009). We observed post- territory budding by helpers (Woolfenden & Fitzpatrick 1984). fledging care b y helpers, which allows breeders to perform more breeding attempts, as well as it might increase their survival (Langen 2000). More data on parental care for Conservation actions Yellow Cardinal is needed to understand how helpers affect productivity and survival. Some findings of our study are of conservation concern for this species: small population size, inbreeding, We found that breeding territories were close together on park-like vegetation, with almost no unoccupied area relatively large breeding territories, and saturated between them, which may indicate habitat saturation. habitat. A captive-breeding program of Yellow Cardinal High adult survival rates and habitat saturation are is underway in Brazil, with planned releases of captive- potential causes of cooperative breeding (Arnold & bred individuals in sites with historical occurrence of the species (Martins-Ferreira et al. 2013). Habitat loss Owens 1998), as it is for White-banded Tanager (Alves 1990, Manica & Marini 2012). Also, the presence of and fragmentation due to land use conversion (e.g. from helpers may reduce nest parasitism (Feeney et al. 2013). livestock to monocultures and forestry) and bird trapping Nevertheless, the Brazilian population of Yellow Cardinal still being main conservation problems for the Yellow is suffering with high rates of brood parasitism by Shiny Cardinal in some regions. Demographic parameters, such as adequate home range needs, must be considered Cowbird, including nests with helpers (CB, MR and CSF, pers. obs.). when defining how and where to release captive-bred Breeding territory and home range sizes may Yellow Cardinals. We highly recommend further studies be considered large for a passerine of its size (~47 g). on habitat selection by Yellow Cardinal, as well as studies However, our estimations could be biased due to small to understand the role of helpers and the continuous monitoring of the Brazilian population. sampling effort, and may be considered with caution, Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. Chiarani E. & Fontana C.S. 2015. Breeding biology of the Lesser ACKNOWLEDGEMENTS Grass-Finch (Emberizoides ypiranganus) in southern Brazilian upland grasslands. Wilson Journal of Ornithology 127: 441–456. We like to thank Secretaria do Meio Ambiente do Rio Cockburn A. 1998. Evolution of helping behavior in cooperatively Grande do Sul (SEMA-RS) and Parque Estadual do breeding birds. Annual Review of Ecology and Systematics 29: 141– Espinilho staff for permitting to research on a protected 177. Cockburn A. 2003. Cooperative breeding in Oscine passerines: does area, and Fazenda São Marcos owners for granting access sociality inhibit speciation? Proceedings of the Royal Society of to a study site. We also thank Condomínio Agropecuário London B: Biological Sciences 270: 2207–2214. Ceolin, Fazenda São João and Granja Santo Ângelo for its Cockburn A. 2006. Prevalence of different modes of parental care huge support. M.S. Borba, E. Chiarani, and C.B. Andretti in birds. Proceedings of the Royal Society of London B: Biological Sciences 273: 1375–1383. for their fieldwork assistance and i deas. We are grateful Cockburn A. & Russell A.F. 2011. Cooperative breeding: a question to A.B. Azpiroz, A.S. Di Giacomo, J.J. Roper, H. Beier, of climate? Current Biology 21: R195–R197. A.L. Boesing, and anonymous reviewers for suggestions Dardanelli S., Nores M.L.M. & Nores M. 2006. Minimum area and comments. C.B. and C.S.F. were supported by requirements of breeding birds in fragmented woodland of central Argentina. Diversity and Distributions 12: 687–693. a studentship and a research fellowship, respectively, Doerr E.D. & Doerr V.A.J. 2006. Comparative demography from Conselho Nacional de Desenvolvimento Científico e of treecreepers: evaluating hypotheses for the evolution and Tecnológico (CNPq). Our study was substantially financed maintenance of cooperative breeding. Animal Behaviour 72: by Fundação Grupo Boticário de Proteção à Natureza (grant 147–159. number 0975_20131). Domínguez M., Reboreda J.C. & Mahler B. 2015. Impact of Shiny Cowbird and botfly parasitism on the reproductive success of the globally endangered Yellow Cardinal Gubernatrix cristata. Bird Conservation International 25: 294–305. REFERENCES Downing P.A., Cornwallis C.K. & Griffin A.S. 2015. Sex, long life and the evolutionary transition to cooperative breeding in birds. Altmann J. 1974. Observational study of behaviour: sampling Proceedings of the Royal Society of London B: Biological Sciences 282: methods. Behaviour 49: 227–267. Alves M.A.S. 1990. Social system and helping behavior in the White- Drobniak S.M., Wagner G., Mourocq E. & Griesser M. 2015. Family banded Tanager (Neothraupis fasciata). Condor 92: 470–474. living: an overlooked but pivotal social system to understand the Arnold K.E. & Owens I.P.F. 1998. Cooperative breeding in birds: a evolution of cooperative breeding. Behavioral Ecology 26: 805– comparative test of the life history hypothesis. Proceedings of the Royal Society of London B: Biological Sciences 265: 739–745. Du Plessis M.A., Siegfried W.R. & Armstrong A.J. 1995. Ecological Azpiroz A.B., Alfaro M. & Jiménez S. 2012. Lista roja de las aves del and life-history correlates of cooperative breeding in South African Uruguay. Montevideo: Dirección Nacional de Medio Ambiente. birds. Oecologia 102: 180–188. Barker F.K., Burns K.J., Klicka J., Lanyon S.M. & Lovette I.J. 2013. Eck S., Fiebig J., Fiedler W., Heynen I., Nicolai B., Töpfer T., van Going to extremes: contrasting rates of diversification in a recent den Elzen R., Winkler R. & Woog F. 2011. Measuring birds/Vögel radiation of New World passerine birds. Systematic Biology 62: Vermessen. Wilhelmshaven: Deutsche Ornithologen-Gesellschaft. 298–320. Edwards S.V & Naeem S. 1993. The phylogenetic component of Beier P., van Drielen M. & Kankam B.O. 2002. Avifaunal collapse cooperative breeding in perching birds. American Naturalist 141: in west African forest fragments. Conservation Biology 16: 1097– 754–789. Ekman J. & Griesser M. 2016. Siberian jays: delayed dispersal in Berg E.C., Aldredge R.A., Peterson A.T. & McCormack J.E. 2012. the absence of cooperative breeding, p. 6–18. In: Koenig W.D. New phylogenetic information suggests both an increase and at & Dickinson J.L. (eds.). Cooperative breeding in vertebrates: least one loss of cooperative breeding during the evolutionary studies of ecology, evolution, and behavior. Cambridge: Cambridge history of Aphelocoma jays. Evolutionary Ecology 26: 43–54. University Press. BirdLife International. 2015. Species factsheet: Gubernatrix cristata. Faria L.P., Carrara L.A. & Rodrigues M. 2007. Dimorfismo sexual http://www.birdlife.org/datazone/speciesfactsheet.php?id=9078 de tamanho no Fura-barreira Hylocryptus rectirostris (Wied) (Aves, (acessado em 21 December 2015). Furnariidae). Revista Brasileira de Zoologia 24: 207–212. Burns K.J., Shultz A.J., Title P.O., Mason N.A., Barker F.K., Feeney W.E., Medina I., Somveille M., Heinsohn R., Hall M.L., Klicka J., Lanyon S.M. & Lovette I.J. 2014. Phylogenetics and Mulder R.A., Stein J.A., Kilner R.M. & Langmore N.E. 2013. diversification of tanagers (Passeriformes: Thraupidae), the largest Brood parasitism and the evolution of cooperative breeding in radiation of Neotropical songbirds. Molecular Phylogenetics and birds. Science 342: 1506–1508. Evolution 75: 41–77. Gamero A., Székely T. & Kappeler P.M. 2014. Delayed juvenile Burt D.B., Coulter P.F. & Ligon J.D. 2007. Evolution of parental care dispersal and monogamy, but no cooperative breeding in White- and cooperative breeding, p. 295–326. In: Jamieson B.G.M. (ed.). breasted Mesites (Mesitornis variegata). Behavioral Ecology and Reproductive biology and phylogeny of birds, Part B: sexual selection, Sociobiology 68: 73–83. behavior, conservation, embryology and genetics. Enfield: Science Gressler D.T. 2012. Razão sexual e sobrevivência em Neothraupis Publishers. fasciata. Ph.D. Thesis. Brasília: Universidade de Brasília. Calenge C. 2006. The package “adehabitat” for the R software: a tool Gressler D.,T., Pereira Z.P. & Marini M.Â. 2014. Brood sex allocation for the analysis of space and habitat use by animals. Ecological in the Neotropical cooperative White-banded Tanager Neothraupis Modelling 197: 516–519. fasciata. Journal of Ornithology 155: 713–719. Canestrari D., Marcos J.M. & Baglione V. 2009. Cooperative breeding Hatchwell B.J. 2009. The evolution of cooperative bree ding in birds: in Carrion Crows reduces the rate of brood parasitism by Great kinship, dispersal and life history. Philosophical Transactions of the Spotted Cuckoos. Animal Behaviour 77: 1337–1344. Royal Society of London B: Biological Sciences 364: 3217–3227. Revista Brasileira de Ornitologia 25(1): 2017 Cooperative breeding and demography of Yellow Cardinal Gubernatrix cristata in Brazil Beier et al. Heinsohn R. & Legge S. 1999. The cost of helping. Trends in Ecology occupancy in a spatially structured bird population. Journal of and Evolution 14: 53–57. Animal Ecology 81: 940–952. Hensler G.L. & Nichols J.D. 1981. The Mayfield method of estimating Pereira M.S. 2015. Assembleia de aves territorialistas na formação nesting success: a model, estimators and simulation results. Wilson Espinilho: densidade e seleção de habitat reprodutivo. MSc. Bulletin 93: 42–53. Dissertation. Porto Alegre: Pontifícia Universidade Católica do Hilty S. 2011. Tanagers (Thraupidae), p. 46–155. In: del Hoyo J., Rio Grande do Sul. Elliott A. & Christie D. (eds.). Handbook of the birds of the world, Pimm S.L., Diamond J., Reed T.M., Russell G.J. & Verner J. v. 16 (tanagers to New World blackbirds). Barcelona: Lynx Edicions. 1993. Times to extinction for small populations of large birds. Jacob A.A. & Rudran R. 2006. Radiotelemetria em estudos Proceedings of the National Academy of Sciences of the United States populacionais, p. 285–342. In: Cullen-Jr. L., Rudran R. & of America 90: 10871–10875. Valladares-Padua C. (eds.). Métodos de estudos em biologia da Poiani A. & Jermiin L.S. 1994. A comparative analysis of some conservação e manejo da vida silvestre. Curitiba: Ed. Universidade life-history traits between cooperatively and non-cooperatively Federal do Paraná. breeding Australian passerines. Evolutionary Ecology 8: 471–488. Jaramillo A. 2011. Yellow Cardinal, p. 641. In: del Hoyo J., Elliott A., Powell R.A. & Mitchell M.S. 2012. What is a home range? Journal of & Christie D. (eds.). Handbook of the birds of the world: tanagers to Mammalogy 93: 948–958. New World blackbirds. Barcelona: Lynx Edicions. R Core Team. 2015. R: a language and environment for statistical Jetz W. & Rubenstein D.R. 2011. Environmental uncertainty and computing. https://www.r-project.org (access on 15 December the global biogeography of cooperative breeding in birds. Current 2015). Biology 21: 72–78. Russell A.F., Langmore N.E., Cockburn A., Astheimer L.B. & Kilner Klimkiewicz M.K. & Futcher A.G. 1987. Longevity records of North R.M. 2007. Reduced egg investment can conceal helper effects in American birds: Coerebinae through Estrildidae. Journal of Field cooperatively breeding birds. Science 317: 941–944. Ornithology 58: 318–333. Schaub R., Mumme R.L. & Woolfenden G.E. 1992. Predation on Koenig W.D., Pitelka F.A., Carmen W.J., Mumme R.L. & Stanback the eggs and nestlings of Florida Scrub Jays. Auk 109: 585–593. M.T. 1992. The evolution of delayed dispersal in cooperative Seaman D.E., Millspaugh J.J., Kernohan B.J., Brundige G.C., breeders. Quarterly Review of Biology 67: 111–150. Raedeke K.J. & Gitzen R.A. 1999. Effects of sample size on Lande R. 1988. Genetics and demography in biological conservation. kernel home range estimates. Journal of Wildlife Management 63: Science 241: 1455–1460. 739–747. Langen T.A. 2000. Prolonged offspring dependence and cooperative Martins-Ferreira C., Bencke G.A., Fontana C.S., Dias R.A., breeding in birds. Behavioral Ecology 11: 367–377. Repenning M., Damiani R.V., Mauricio G.N., Gianuca A.T., Liker A., Freckleton R.P. & Székely T. 2014. Divorce and infidelity are Krügel M.M., Franz I., Rovedder C.E., Rupp A.E., Pereira M.S., associated with skewed adult sex ratios in birds. Current Biology Vizentin-Bugoni J., Joenck C.M., Straube F.C., Reinert B.L., 24: 880–884. Bornschein M.R., Dias D., Vieira B.P & Serafini, P.P. 2013. P lano López-Lanús B., Grilli P., Di Giacomo A.S., Coconier E.E. & Banchs de Ação Nacional para a conservação dos Passeriformes ameaçados R. (eds.). 2008. Categorización de las aves de la Argentina según su dos Campos Sulinos e Espinilho. Brasília: Instituto Chico Mendes estado de conservación. Buenos Aires: Informe de Aves Argentinas/ de Conservação da Biodiversidade. Série espécies ameaçadas 31. AOP y Secretaría de Ambiente y Desarrollo Sustentable. Soares, C.G.D. 2007. Biologia e conservação de Neothraupis fasciata Manica L.T. & Marini M.Â. 2012. Helpers at the nest of White- (Aves: Thr aupidae) no cerrado do Brasil central. Ph.D. Thesis. banded Tanager Neothraupis fasciata benefit male breeders but Brasília: Universidade de Brasília. do not increase reproductive success. Journal of Ornithology 153: Stacey P.B. & Taper M. 1992. Environmental variation and the 149–159. persistence of small populations. Ecological Applications 2: 18–29. Marchiori J.N.C. & Alves F.S. 2011. O Inhaduvá (Prosopis affinis Stutchbury B.J.M. & Morton E.S. 2001. Behavioral ecology of tropical Spreng.) no Rio Grande do Sul. 8 - Aspectos fitogeográficos. birds. London: Academic Press. Balduinia 29: 13–20. Székely T., Liker A., Freckleton R.P., Fichtel C. & Kappeler P.M. 2014. Marini M.Â., Duca C. & Manica L.T. 2010. Técnicas de pesquisa Sex-biased survival predicts adult sex ratio variation in wild birds. em biologia reprodutiva de aves, p. 295–312. In: von Matter Proceedings of the Royal Society of London B: Biological Sciences 281: S., Straube F.C., Accordi I.A., Piacentini V.Q. & Cândido-Jr., 20140342. J.F. (eds.). Ornitologia e conservação: ciência aplicada, técnicas de Székely T., Lislevand T. & Figuerola J. 2007. Sexual size dimorphism pesquisa e levantamento. Rio de Janeiro: Technical Books. in birds, p. 27–37. In: Fairbairn D.J., Blanckenhorn W.U. & Mayfield H.F. 1975. Suggestions for calculating nest success. Wi lson Székely T. (eds.). Sex, size and gender roles: evolutionary studies of Bulletin 87: 456–466. sexual size dimorphism. Oxford: Oxford University Press. Nice M.M. 1941. The role of territory in bir d life. American Midland Welty J.C. & Baptista L.F. 1988. The life of birds. New York: W. B. Naturalist 26: 441–487. Saunders. Odum E.P. & Kuenzler E.J. 1955. Measurement of territory and Wolfe J.D. Ryder T.B., Pyle P. 2010. Using molt cycles to categorize home range size in birds. Auk 72: 128–137. the age of tropical birds: an integrative new system. Journal of Paquet M., Covas R., Chastel O., Parenteau C. & Doutrelant C. 2013. Field Ornithology 81: 186–194. Maternal effects in relation to helper presence in the cooperatively Woolfenden G.E. & Fitzpatrick J.W. 1984. The F lorida Scrub Jay: breeding Sociable Weaver. PLoS ONE 8: e59336. demography of a cooperative-breeding bird. Princeton: Princeton Pavlacky-Jr. D.C., Possingham H.P., Lowe A.J., Prentis P.J., Green University Press. D.J. & Goldizen A.W. 2012. Anthropogenic landscape change promotes asymmetric dispersal and limits regional patch Associate Editor: Cristiano S. Azevedo. Revista Brasileira de Ornitologia 25(1): 2017
Ornithology Research – Springer Journals
Published: Mar 1, 2017
Keywords: breeding territory; home range; nest helpers; small population; threatened species
Access the full text.
Sign up today, get DeepDyve free for 14 days.