Introduction
The Yellow Cardinal Gubernatrix cristata (Aves: Thraupidae) is a passerine from southern South America categorised as ‘Endangered’ by IUCN (BirdLife International 2020). Historically, Yellow Cardinals were distributed throughout the southern tip of Brazil (Rio Grande do Sul), Uruguay, and central and northern Argentina (BirdLife International 2020). Habitat loss and the capture of individuals for the illegal cage bird market are reportedly the biggest threats that have led to the species’ decline (BirdLife International 2020). Currently, its distribution is discontinuous with the largest populations found in Argentina (Reales et al. Reference Reales, Sarquis, Daradanelli and Lammertink2019, Domínguez et al. Reference Domínguez, Lapido, Gorrindo, Archuby, Correa, Llanos, Reales, Piantanida, Marateo, Meriggi, Andreani, Encabo, Gomez Vinasa, Bertini, Perelló, Banchs, Crignoli, Verón and Mahler2020), mainly in non-modified areas within the Espinal ecoregion. Natural habitats of this ecoregion are characterized by patches of thorny trees and shrub forests, interspersed with pastures as well as woodlands and more open savanna-like habitats (Cabrera Reference Cabrera and Kugler1976). Even though habitat loss and illegal wildlife trafficking are the main threats to the species, Domínguez et al. (Reference Domínguez, Reboreda and Mahler2015) reported the negative impact of brood parasitism by Shiny Cowbirds Molothrus bonariensis as an additional threat for Yellow Cardinals. Puncturing of host eggs by parasite females resulting in brood reduction and often in nest abandonment was identified as the main impact of Shiny Cowbird parasitism on the reproductive success of Yellow Cardinals (Domínguez et al. Reference Domínguez, Reboreda and Mahler2015). Brood parasitism by cowbirds has been suggested to compromise the viability of populations of threatened species by negatively affecting the reproductive success of hosts (Brittingham and Temple Reference Brittingham and Temple1983, DeCapita Reference DeCapita, Smith, Cook, Rothstein, Robinson and Sealy2000, Rothstein and Cook Reference Rothstein, Cook, Smith, Cook, Rothstein, Robinson and Sealy2000, Oppel et al. Reference Oppel, Schaefer, Schmidt and Schroder2004).
As part of a conservation plan for Yellow Cardinals in Argentina, a reintroduction programme for individuals rescued from the illegal wildlife trade has been carried out for the past three years. Rescued individuals went through a sanitary rehabilitation at the Fundación Temaikèn recovery centre and were subsequently released back into areas with suitable habitat within their area of provenance, previously determined by the use of molecular markers (Domínguez et al. Reference Domínguez, Pizzarello, Atencio, Scardamaglia and Mahler2019).
Information on the breeding biology of released individuals along survival and persistence are the main demographic parameters needed to evaluate the success of a reintroduction programme (Seddon Reference Seddon1999, Parker et al. Reference Parker, Ewen, Seddon and Armstrong2013). In this contribution we report the impact of Shiny Cowbird parasitism on the recruitment of released and wild Yellow Cardinals in La Pampa province, Argentina.
Methods
Study site
The study took place in a private livestock ranch in La Pampa province, Argentina (36°48’S; 64°37’W) from early October to late December 2019, covering almost the entire breeding season of the species (late September–early January; Domínguez et al. Reference Domínguez, Reboreda and Mahler2015, Segura et al. Reference Segura, Perelló, Gress and Ontiveros2019). The ranch contains thorny shrubland forests with different vegetation densities, dominated by calden mesquite Prosopis caldenia, within the Espinal ecoregion (Morello et al. Reference Morello, Matteucci and Rodríguez2012), covering a total area of 1,320 ha.
Data collection
Nine Yellow Cardinal reproductive pairs were followed during the 2019 breeding season within the private ranch and surrounding areas (1–2 km into the neighbouring ranches). Six of these pairs were composed of (either one or both) individuals recovered from illegal wildlife traffic, released in the study site in 2017, 2018 or 2019. The remaining three pairs were wild Yellow Cardinals found within the study site. In order to identify and follow the wild reproductive pairs, they were captured with mist nets and banded on the tarsus with a numbered aluminium ring and a combination of two-coloured plastic rings. The released Yellow Cardinals had been banded before release.
We monitored the activity of the reproductive pairs and determined their territories. We searched for nests within these territories and followed reproductive attempts by visiting the nest every 1–4 days until the reproductive attempt concluded. During nest localizations and nest visits, disturbance of the brood was minimised by following standardized techniques described in Martin and Geupel (Reference Martin and Geupel1993). During each visit, the content of the nest was examined, and eggs were marked with waterproof ink. Yellow Cardinal nests have a modal clutch size of three eggs (range 2–4) of a bluish background colour with black spots (Dominguez et al. 2015), and are easily distinguishable from brood parasite eggs since Shiny Cowbirds do not lay eggs with such characteristics (Ortega Reference Ortega1998, de la Colina et al. Reference De la Colina, Mahler and Reboreda2011, Hanley et al. Reference Hanley, Lopez, Fiorini, Reboreda, Grim and Hauber2019).
To estimate the frequency of brood parasitism we calculated the proportion of nests with Shiny Cowbird eggs. Intensity of parasitism was estimated by averaging the number of parasite eggs in parasitized nests that were found during construction, laying, or incubation after laying had been completed.
Results
We found 17 nests during the study period, three during construction, six during laying and eight during incubation corresponding to nine reproductive pairs. We followed 15 of these nests, until the reproductive attempt ceased (from now on “monitored nests”). Six of the nine reproductive pairs had re-nesting attempts, five of them with one re-nesting attempt and one with three. The frequency of Shiny Cowbird parasitism was 100% (n = 17) and its intensity was 4.5 ± 3.4 (mean ± SD) eggs per parasitized nest (range 1 – 13; n = 15; Fig. 1A). All monitored nests lost Yellow Cardinal eggs. In 13 nests, we found convincing evidence that eggs were lost as a consequence of Shiny Cowbird parasitism. In most cases (n = 10) Yellow Cardinal eggs were found punctured (Fig. 1B) or ejected from the nest (broken eggs found on the ground; Fig. 1C), most likely as a consequence of the egg punctures. In three nests, Yellow Cardinal eggs had disappeared by the time of appearance of parasite eggs. Since these nests were not found empty or abandoned, predation was not a likely cause for host egg losses. The remaining two nests were found with parasite eggs only and therefore we cannot draw conclusions on the mechanism that led to the loss of host eggs. These two nests were found active.
Figure 1. Nest and eggs of Yellow Cardinals in La Pampa province, Argentina. (A) Nest with eight parasite eggs and one host egg; (B) Punctured Yellow Cardinal egg; (C) Broken Yellow Cardinal egg.
All monitored nests failed to fledge Yellow Cardinals. Seven showed a complete loss of host eggs. In two of these cases, Yellow Cardinals managed to rear parasite chicks (one fledged and the other was depredated 10 days after hatching), whereas in the other five cases nests were abandoned. In the remaining eight nests, egg losses were not total (one host egg remained). Three of these nests were abandoned, four were depredated (nest content disappeared between consecutive visits with no parental activity near the nest) and one failed for unknown reasons.
Discussion
This is the first study on the reproductive success of a mixed population of wild and released Yellow Cardinals. The population of Yellow Cardinals monitored in this study had zero recruitment since none of the reproductive pairs were able to fledge their own chicks. Because of the conspicuous territorial behaviour of this species (mainly during the early stages of nesting), it is unlikely that we have overlooked nesting attempts of already identified breeding pairs. However, due to the large size of the study site, we could have possibly overlooked a reproductive pair or nesting attempt that occurred before the reproductive pairs were found. Nevertheless, since none of the breeding pairs were found with fledglings, we assume that if they had prior nesting attempts, these were not successful.
Yellow Cardinal breeding failures occurred mainly as a consequence of brood parasitism by Shiny Cowbirds. The Yellow Cardinal has been reported as a host of the Shiny Cowbird in Uruguay (Azpiroz Reference Azpiroz2015), Brazil (Beier and Fontana Reference Beier and Fontana2019) and Argentina (Domínguez et al. Reference Domínguez, Reboreda and Mahler2015). Domínguez et al. (Reference Domínguez, Reboreda and Mahler2015) and Beier and Fontana (Reference Beier and Fontana2019) published data on the negative impact of Shiny Cowbird parasitism on Yellow Cardinals’ reproductive success. The frequencies and intensities of parasitism reported in these two studies (33% and 67%, and 1.09 ± 0.09 and 1.9 ± 1.3 eggs per parasitized nest, respectively) were much lower than those presented in the current study (100% and 4.5 ± 3.4 eggs per parasitized nest). The high parasitism rates we recorded might be a consequence of a higher density of Shiny Cowbirds in our study site. Due to agricultural and livestock farming expansion, this area has been subject to habitat transformation (Arturi Reference Arturi, Brown, Martinez Ortiz, Acerbi and Corcuera2005, Brown and Pacheco Reference Brown, Pacheco, Brown, Martínez Ortiz, Acerbi and Corchera2006, Matteucci Reference Matteucci, Morello, Matteucci, Rodriguez and Silva2012). More open habitats and external food provisioning generate favourable conditions for Shiny Cowbirds, thus increasing their populations (Robinson et al. Reference Robinson, Rothstein, Brittingham, Petit, Grzybowski, Martin, Finch, Martin and Finch1995, Mermoz et al. Reference Mermoz, Cruz, Chace, Reboreda, Downs and Hart2020). Increased parasitism in this area has also been recorded for the Fork-tailed Tyrant Tyrannus savanna, which was observed feeding Shiny Cowbird fledglings (A. Jahn pers. comm.). In other areas, this species rejects Shiny Cowbird eggs and is rarely a host of the Shiny Cowbird (D. Tuero pers. comm.). Parasite densities and host use throughout the area should be studied in order to clarify the causes of the high parasitism rates we observed.
The parasitism rates presented in this study are of great conservation concern. The absence of recruitment calls for a modification in the conservation actions that have been implemented until now. In particular, the release sites chosen for the reintroduction programmes should receive special attention. Despite being a livestock ranch, the site chosen for releases contained natural habitats over almost all its extent, suitable for Yellow Cardinals. Besides habitat suitability, release sites were also determined by the abundance of conspecifics (in order to avoid possibly negative Allee effect consequences; Deredec and Courchamp Reference Deredec and Courchamp2007) and the surveillance capacity by local authorities preventing individuals from being recaptured for illegal trafficking.
It is possible that the release area (habitat in which released organisms are expected to remain; Seddon Reference Seddon2013) is exhibiting a source-sink dynamic, in which the release site (the smaller location within the release area where actual releases occur; Seddon Reference Seddon2013) chosen for the past three releases is a sink habitat. Sink habitats are those where mortality exceeds reproductive rates, hence the population is not able to persist without immigration (Pulliam Reference Pulliam1988). Releases into sink habitats will not be successful and will sooner or later fail, as conditions are inadequate for reproduction. In this case, the cause of failure was the high impact of brood parasitism on the population’s reproductive success. However, data on demographic parameters of other populations within the release area are needed in order to calculate lambda, a finite rate of population increase, that allows determining whether the populations are in fact exhibiting a source-sink dynamic (Pidgeon et al. Reference Pidgeon, Radeloff and Mathews2006). Habitat suitability plays a major role in the outcome of reintroduction projects (Osborne and Seddon Reference Osborne, Seddon, Ewen, Armstrong, Parker and Seddon2012). In an ideal scenario, the quality of the release sites should be evaluated prior to the release (IUCN/SSC 2013). However, in a threatened species scenario, natural populations tend to be very small, thereby posing a challenge to the collection of demographic and habitat-use data required for an adequate assessment. Hence, the information gathered in post-release monitoring programmes is of utmost importance and should be used for planning future releases (Letty et al. Reference Letty, Marchandeau and Aubineau2007, Sutherland et al. Reference Sutherland, Armstrong and Butchart2010, Parker et al. Reference Parker, Ewen, Seddon and Armstrong2013).
Currently, the populations with the highest densities of Yellow Cardinals are found in the north-eastern, central, and southern areas of its distribution in Argentina (Domínguez et al. Reference Domínguez, Lapido, Gorrindo, Archuby, Correa, Llanos, Reales, Piantanida, Marateo, Meriggi, Andreani, Encabo, Gomez Vinasa, Bertini, Perelló, Banchs, Crignoli, Verón and Mahler2020). These areas have also suffered loss and transformation of natural habitats as a consequence of the intensification of agricultural activities and livestock ranching (Arturi Reference Arturi, Brown, Martinez Ortiz, Acerbi and Corcuera2005, Matteucci Reference Matteucci, Morello, Matteucci, Rodriguez and Silva2012). Therefore, high densities of Shiny Cowbirds are expected (Mermoz et al. Reference Mermoz, Cruz, Chace, Reboreda, Downs and Hart2020), making brood parasitism a major threat for the species. Hence, evaluating Shiny Cowbird densities and eventually controlling Shiny Cowbird populations might be considered in future conservation plans for Yellow Cardinals. Control strategies on brood parasites have improved the reproductive success of threatened species in the past (Cruz et al. Reference Cruz, Lopez-Ortiz, Ventosa-Febles, Wiley, Nakamura, Ramos-Alvarez and Post2005, Krabbe et al. Reference Krabbe, Juina and Sornoza2011, Hartmann et al. Reference Hartmann, Oppel, Segelbacher, Juiña and Schaefer2017). These studies have shown that trapping cowbirds near host nesting areas and cowbird feeding areas, as well as shooting cowbirds, resulted in marked population increases of the threatened host species. Reducing Shiny Cowbird densities in areas where the main populations of Yellow Cardinals reside, or rescued individuals are planned to be released, could result in higher recruitment and help in the recovery of this species. Moreover, a long-term management plan for agricultural-livestock practices could outline the best ways to avoid habitat modification and implement practices that avoid a drastic increase in cowbird numbers.
Acknowledgements
We thank Steffen Oppel, Steven Rothstein and one anonymous referee for their constructive comments and suggestions on a previous version of this manuscript. We also thank Fundación Temaikèn, especially M. A. de la Colina, for collaboration in conducting Yellow Cardinal recoveries and releases, and M. Domínguez for her comments on the manuscript. We also thank research assistants F. Ciperiani, M. D’Occhio and P. Fracas for their aid in field work, and J. C. Padilla and F. Bruno for their support at the release site. Funding was provided by Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación to BM [PICT-2015-0569].
