Genetic monogamy in burrowing parrots Cyanoliseus patagonus?
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1 Wilson, R. P. In press. Determination of foraging behaviour of free-ranging endotherms at sea: geographical position, local movements and ingestion. Proc. V European Conf. Wildl. Telemetry. Wilson, R. P., Hustler, K., Ryan, P. G., Burger, A. E. and Nöldeke, E. C Diving birds in cold water: do Archimedes and Boyle determine energetic costs? Am. Nat. 140: Wilson, R. P., Nagy, K. A. and Obst, B. S Foraging range of penguins. Polar Rec. 25: Wilson, R. P., Ropert-Coudert, Y. and Kato, A. In press. Rush and grab strategies in foraging marine endotherms: the case for haste in penguins? Anim. Behav. Yoda, K., Sato, K., Niizuma, Y., Kurita, M., Bost, C.-A., Le Maho, Y. and Naito, Y Precise monitoring of porpoising behaviour of Adélie Penguins determined using acceleration data loggers. J. Exp. Biol. 202: JOURNAL OF AVIAN BIOLOGY 33: , 2002 Genetic monogamy in burrowing parrots Cyanoliseus patagonus? Juan F. Masello, Institut für O kologie, Friedrich-Schiller-Uni ersität Jena, Dornburger Str. 159, D Jena, Germany. b8maju@excite.com Anna Sramko a, Institut für E olutionsbiologie und O kologie, Rheinische Friedrich-Wilhelms-Uni ersität Bonn, An der Immenburg 1, D Bonn, Germany Petra Quillfeldt, Institut für O kologie, Friedrich-Schiller-Uni ersität Jena, Dornburger Str. 159, D Jena, Germany Jörg Thomas Epplen, Molekulare Humangenetik, Ruhr-Uni ersität Bochum, D Bochum, Germany Thomas Lubjuhn, Institut für E olutionsbiologie und O kologie, Rheinische Friedrich-Wilhelms-Uni ersität Bonn, An der Immenburg 1, D Bonn, Germany We report on a first DNA fingerprinting study of paternity in a Psittaciform bird, the burrowing parrot Cyanoliseus patagonus. In two consecutive breeding seasons, a total of 49 families was sampled, of which 11 breeding pairs were investigated each of two years. Extra-pair paternity was not encountered suggesting that burrowing parrots are socially as well as genetically monogamous. Strict genetic monogamy is comparatively rare in birds and occurs predominantly in some groups of non-passeriformes all of which exhibit long reproductive lifespans and essential paternal care. Psittaciformes fit this pattern. We conclude that paternal care plays a crucial role in the evolution and maintenance of genetic monogamy in the study species. Cases of intraspecific brood parasitism are rarely observed. Extra-pair copulations (EPCs) are widespread among socially monogamous birds (e.g. Birkhead 1998), but a large interspecific variation in levels of extra-pair paternity (EPP) has been observed (Petrie and Kempenaers 1998). While in some species over half of the chicks are extra-pair young (EPY), e.g. in tree swallows Tachycineta bicolor (Kempenaers et al. 1999), there are some groups of birds where EPY are rarely found. Especially in Sphenisciformes (e.g. Moreno et al. 2000) and Procellariiformes among seabirds (summarised in Quillfeldt et al. 2001), as well as Strigiformes and Falconiformes among raptors (summarised in Müller et al. 2001), EPP seems to occur infrequently or may even be absent. The life histories of these non-passeriform groups of birds exhibit some striking similarities such as indispensable male parental care and long reproductive lifespans, which have been proposed as the causes for the low rates of EPP. If male care is essential, females should refrain from seeking EPCs if they risk losing their partner s investment in the brood. In particular, males of long-lived species should withdraw care to a brood if any doubt of parentage exists, as suggested by a model of male parental decisions (Mauck et al. 1999). Psittaciformes (parrots and cockatoos) are another group of long-lived birds exhibiting very high levels of parental investment, but to our knowledge no analyses of EPP have been performed in this group of birds. Thus, the following study on paternity in the burrowing parrot Cyanoliseus patagonus represents the first DNA fingerprint study on paternity in a Psittaciform bird. Methods The burrowing parrot is one of the most southern Neotropical parrots. Burrowing parrots breed colonially excavating their own nest burrows by tunnelling into the faces of sandstone, limestone or earth cliffs. Nesting pairs use burrows dug in previous seasons but they enlarge the burrows every year (J. F. Masello and P. Quillfeldt unpubl. data). Each burrow is occupied by 99
2 a single pair. Burrowing parrots do not use nesting material but, rather, deposit their eggs on the sandy nest bottom. The clutch of two to five eggs (J. F. Masello and P. Quillfeldt unpubl. data) is incubated by the female alone while the male provides food (de Grahl 1985). Burrowing parrots exhibit intensive biparental care. Chick feeding is shared between the sexes. The chicks remain in the nest for about 60 days (J. F. Masello and P. Quillfeldt unpubl. data). After fledging, the young are fed by the adults for approximately four months (Westen 1995). The study was carried out from October 1998 to February 1999 and November 1999 to January 2000 in the largest and most important colony of burrowing parrots, located in a sandstone cliff at the Atlantic coast in the province of Río Negro, Patagonia, Argentina. The colony covers 5 to 10 km of cliffs (Yorio and Harris 1997); the westernmost kilometre of the colony (41 3 S, W) is by far the most densely populated with 6750 active nests (J. F. Masello unpubl. data). For this study, we selected and marked nests in the dense sector of the colony. All the nests were inspected every five days by climbing. Burrowing parrots have the tendency to desert in response to disturbances during the incubation period (de Grahl 1985, J. F. Masello and P. Quillfeldt unpubl. data) and during the first week after hatching of nestlings (J. F. Masello and P. Quillfeldt unpubl. data). To reduce observer disturbance, nests were not visited until about five days after the estimated hatching date of the last chick of a clutch. Birds were captured in the nest chambers between November and January during chick rearing. A total of 49 families with 166 chicks was sampled in two consecutive breeding seasons (1998/99: 22; 1999/ 2000: 27). For 11 breeding pairs, chicks were sampled in both seasons, while all other families were only sampled in a single season. Blood samples (approximately 50 l) were taken by puncture of the brachial vein. Samples were immediately suspended in 70% ethanol (Arctander 1988) and stored at 4 C for four to twelve weeks and thereafter at 20 C until processing. DNA was extracted using standard procedures modified according to Miller et al. (1988); for additional details see Lubjuhn and Sauer (1999). For each sample, approximately 5 to 10 g DNA was digested with 50 U of Alu I following the instructions of the manufacturer. Digests were separated by agarose gel electrophoresis (gel size: cm, 0.8% agarose, 1 2 V/cm) for 49 50hin1 TBE buffer (89 mm Tris, 89 mm boric acid, 2 mm EDTA). After drying, gels were hybridized with the 32 P-labelled oligonucleotide probe (CA) 8. Detailed procedures are given in Epplen (1992). All DNA samples of the members of a family were run in adjacent gel lanes. Bands were scored by eye within a range from approximately 30 to 3 KB and were evaluated according to the criteria proposed in Westneat (1990). Fingerprint bands of nestlings that were not attributable to either putative parent were scored. Band-sharing coefficients were calculated according to the formula given in Wetton et al. (1987) as =2N AB / (N A +N B ), where N AB is the number of fragments shared between individuals A and B and N A and N B are the total number of fragments in individuals A and B, respectively. Background band-sharing was obtained by comparing the banding patterns of breeding partners. The informativity of DNA fingerprint patterns for assigning parentage depends on their variability. This in turn is determined by the restriction enzyme/oligonucleotide probe combination used and the proportion of bands that individuals share by chance. Alu I digestion of DNA followed by hybridization with the oligonucleotide (CA) 8 produced banding patterns that were sufficiently variable to be individual-specific. A mean of SD (n=242) bands per individual was scored with a background band-sharing of SD (n=38). An informativity index I (Krawczak and Lubjuhn 1995) was calculated from these values to quantify the evidential power of the used enzyme/probe combination and to make this study comparable to others. The value of I=33.8 ranges high in a comparative list of informativity indices of 14 DNA fingerprint studies in birds (Lubjuhn and Sauer 1999). The probability p of falsely assigning parentage to one or both putative parents was calculated following Burke et al. (1989) as p= and p= respectively. Therefore, the enzyme/probe combination used produces sufficiently variable banding patterns to assign parentage in burrowing parrots unambiguously. Results In 151 of 166 chicks investigated, all bands could be attributed to the putative parents. Twelve additional chicks showed one novel fragment, and the remaining three chicks had two, 17 and 19 novel fragments that were not attributable to either parent. The cases of one or two novel fragments were interpreted to have resulted from mutations for several reasons. (i) The mean band-sharing coefficient between putative parents and chicks with no novel fragments in their banding patterns ( SD, n=302) did not differ from that between putative parents and chicks with one or two novel fragments in their banding patterns ( SD; n=26; t-test: t=1.091, df=326, p=0.28; see also Fig. 1), but both values differed significantly from the mean band-sharing coefficient of breeding partners ( SD, n=38; Mann-Whitney U-test, putative parents and chicks without novel fragments: U= 834.5, p 0.001; putative parents and chicks with one or two novel fragments: U=1329.0, p 0.001; see also Fig. 1). (ii) For the restriction enzyme/oligonucleotide 100
3 Fig. 1. Distributions of band-sharing coefficients between putative parents and chicks (separated for chicks with no [302 values] and chicks with one or two [26 values] novel fragments) and between breeding partners (38 values). probe combination used here, the mean expected number of novel fragments can be estimated at 7.1 per chick if one of the putative parents was not the genetic parent (for calculation see Jeffreys et al. 1985, Burke and Bruford 1987). The calculation of this value is based on the background band-sharing found for pair partners. (iii) Estimating the mutation rate per fragment under the assumption that a single novel fragment is due to mutation, we obtained a value of This value is within the range of other DNA fingerprint studies in birds (for calculation and a range from to see Burke and Bruford 1987, Kempenaers et al. 1992, Decker et al. 1993). Regarding the two chicks with a total of 17 and 19 novel fragments, we obtained low band-sharings with both putative parents of between 0.20 and Therefore, and because the number of novel fragments by far exceeds that expected if only one putative parent is not the genetic parent (see above), we concluded that in these instances none of the two adults was related to the respective chick. Thus, in summary no cases of EPP occurred in the 49 families investigated. Interestingly, two chicks seem to have resulted from intraspecific brood parasitism. Discussion Extra-pair paternity Our results show that in a sample of 166 nestlings of burrowing parrots from two years, no EPP occurred. Thus, burrowing parrots appear to be not only socially but also genetically monogamous. The probability that EPPs were missed on the basis of our sample can be calculated following Mauck et al. (1995). If the true level of EPPs was 5, 10 or 15%, we could have missed EPPs in our sample of 49 families with a probability of 0.08, and , respectively. Our results are in accordance with other studies on birds with a similar life history (see Introduction). Psittaciformes have generally a high probability of survival to the next breeding season. Thus the offspring of a single breeding season represent a small proportion of the potential lifetime reproductive success. Any reduction of adult survival by investment in current offspring has a larger influence on lifetime reproductive success than in short-lived bird species. Therefore, long-lived birds such as parrots should not invest in broods of doubtful paternity (Mauck et al. 1999) and this is supported by our data. A female burrowing parrot engaging in EPCs might thus face reduced, or even be denied paternal care, which is thought to be of paramount importance for reproductive success in burrowing parrots, because the female incubates (de Grahl 1985) while the male provides food (David Clarke pers. comm.). Alternative explanations for the absence of EPP involve males having highly effective paternity guards, because males that invest intensely in the brood are expected to be under particularly strong selection to protect their paternity. Two main paternity guards have been proposed for birds, namely mate guarding and frequent within-pair copulations (Birkhead and Møller 1992). Burrowing parrots are usually observed flying in pairs (J. F. Masello pers. observ.), possibly a way of mate guarding by males. Information on copulation frequencies in burrowing parrots, however, is lacking. Unrelated chicks Two of 166 chicks were not related to either parent. The DNA fingerprints identified one unrelated chick each year in a total of 22 and 27 nests, respectively. In one of the cases, we found a connection between the nest chamber and that of a neighbouring nest (which we could not access) late in the breeding season, suggesting that the broods were mixed at the time of blood sampling. Cases of brood mixing by the collapse of the wall between two nest chambers were also observed in some other nests not included in the present study. However, the second case of an unrelated chick cannot be explained by brood mixing, and therefore most likely resulted from intraspecific brood parasitism. DNA fingerprinting has revealed that intraspecific brood parasitism is not as rare in birds as presumed earlier (Petrie and Møller 1991, Lyon 1993) it has been demonstrated in many groups of birds. Lyon (1993) suggested that the benefits of a mixed strategy of parasitism and breeding depend on the length of the breeding season and on the seasonal variation in reproductive success. Burrowing parrots in the study colony have a long egg-laying period of 32 days (J. F. Masello and P. Quillfeldt unpubl. data) with sufficient time to produce an own clutch as well as to identify active nests 101
4 for parasitism. On the other hand, chick survival declines later in the season (J. F. Masello unpubl. data). This fact favours early breeding and increases the costs of delayed laying which may be associated with a mixed strategy of parasitism and breeding. The latter reason may explain the infrequent occurrence of intraspecific brood parasitism observed here. However, alternative explanations for this infrequent occurrence must also be considered. For example, a best of a bad job strategy of a single female that had lost her clutch during the laying period may explain our results as well. Further implications The finding of zero to low values of EPP in colonial birds has important ramifications for the discussion on the evolution of coloniality. Nesting density has been proposed to enhance the opportunities for EPCs (Møller and Birkhead 1993), and it has been proposed that the evolution of coloniality might be driven by sexual selection (Morton et al. 1990, Wagner 1993). This is based on comparative evidence showing that birds living in colonies had increased rates of EPCs compared with dispersed breeders (Wittenberger and Hunt 1985, Birkhead and Møller 1996). Wagner (1993) suggested for razorbills Alca torda that colonies may be formed when males are drawn to colonies as a result of females pursuing EPCs ( hidden-lek hypothesis ). This mechanism is a potentially powerful factor contributing to the evolution of colonial breeding and there is some evidence for it from a study of bearded tits Panurus biarmicus (Hoi and Hoi-Leitner 1997). However, the absence of EPP in colonial seabirds, colonial parrots and colonial raptors, does not support the assumptions of the hidden lek hypothesis at least for these groups of birds. Acknowledgements We wish to thank K. P. Sauer, Adrián Pagnossin, María Luján Pagnossin, Mara Marchesan, Vicky Temperton and Maike and Günther Grabs for their contributions to this work. This study was partly supported by the City Council of Viedma (province of Río Negro, Argentina), a research grant of the German Research Foundation DFG (LU 572) and a grant of the state of Thuringia, Germany (Landesgraduiertenstipendium). The present study was carried out under permission of the Dirección de Fauna de la Provincia de Río Negro, Argentina (Exp. n DF-98). References Arctander, P Comparative studies on avian DNA restriction fragment length polymorphism analysis: Convenient procedures based on blood samples from live birds. J. Ornithol. 129: Birkhead, T. R Sperm competition in birds: Mechanisms and function. In: Birkhead, T. R. and Møller, A. P. (eds). Sperm competition and sexual selection. Academic Press, London, pp Birkhead, T. R. and Møller, A. P Sperm competition in birds; evolutionary causes and consequences. Academic Press, San Diego, California. Birkhead, T. R. and Møller, A. P Monogamy and sperm competition in birds. In: Black, J. M. (ed.). Partnerships in birds: the study of monogamy. Oxford University Press, Oxford, pp Burke, T. and Bruford, M DNA fingerprinting in birds. Nature 327: Burke, T., Davies, N. B., Bruford, M. W. and Hatchwell, B. J Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNAfingerprinting. Nature 338: Decker, M. D., Parker, P. G., Minchella, D. J. and Rabenold, K. N Monogamy in Black Vultures: Genetic evidence from DNA fingerprinting. Behav. Ecol. 4: de Grahl, W Papageien: Lebenweise, Arten, Zucht. Eugen Ulmer, Stuttgart. Epplen, J. T The methodology of multilocus DNA fingerprinting using radioactive or nonradioactive oligonuecleotide probes specific for simple repeat motifs. In: Chrambach, A., Dunn, M. J. and Radola, B. J. (eds). Advances in electrophoresis. Vol. 5. VCH, Weinheim, Germany, pp Hoi, H. and Hoi-Leitner, M An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilisations. Behav. Ecol. 8: Jeffreys, A. J., Wilson, V. and Thein, S. L Individualspecific fingerprints of human DNA. Nature 314: Kempenaers, B., Verheyen, G. R., van den Broeck, M., Burke, T., van Broeckhoven, C. and Dhondt, A. A Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357: Kempenaers, B., Congdon, B., Boag, P. and Robertson, R. J Extrapair paternity and egg hatchability in tree swallows: Evidence for the genetic compatibility hypothesis? Behav. Ecol. 10: Krawczak, M. and Lubjuhn, T An informativity index for multilocus DNA fingerprinting. Electrophoresis 16: Lubjuhn, T. and Sauer, K. P DNA fingerprinting and profiling in behavioural ecology. In: Epplen, J. T. and Lubjuhn, T. (eds). DNA profiling and DNA fingerprinting. Birkhäuser Verlag, Basel, Switzerland, pp Lyon, B. E Conspecific brood parasitism as a flexible female reproductive tactic in American coots. Anim. Behav. 46: Mauck, R. A., Waite, T. A. and Parker, P. 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5 Quillfeldt, P., Schmoll, T., Epplen, J. T. and Lubjuhn, T Genetic monogamy in Wilsons Storm-petrel. Auk 118: Wagner, R. H The pursuit of extra-pair copulations by female birds: a new hypothesis of colony formation. J. theor. Biol. 163: Westen, K Felsensittiche Cyanoliseus p. patagonus nicht jedermanns Sache. Papageien 8: Westneat, D. F Genetic parentage in the indigo bunting: a study using DNA fingerprinting. Behav. Ecol. Sociobiol. 27: Wetton, J. H., Carter, R. E., Parkin, D. T. and Walters, D Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327: Wittenberger, J. F. and Hunt, G. L The adaptive significance of coloniality in birds. Avian Biol. 8: Yorio, P. and Harris, G Distribución de aves marinas y costeras coloniales en Patagonia: relevamiento aéreo Bahía Blanca-Cabo Vírgenes, noviembre Informe Técnico del Plan de Manejo Integrado de la Zona Costera Patagónica 29: JOURNAL OF AVIAN BIOLOGY 33: , 2002 Beha ioural and physiological effects of absence of ultra iolet wa elengths on European starlings Sturnus vulgaris Sam A. Maddocks, Arthur R. Goldsmith and Innes C. Cuthill (correspondence), Centre for Beha ioural Biology, School of Biological Sciences, Uni ersity of Bristol, Woodland Road, Bristol, BS8 1UG, UK. i.cuthill@bris.ac.uk As ultraviolet wavelengths are used in normal avian colour perception, the maintenance of captive birds under artificial lighting (which is normally UV-deficient) may have welfare implications. European starling Sturnus ulgaris juveniles kept in UV-deficient light environments had significantly higher basal plasma corticosterone concentrations than those kept under full spectrum lighting, in the second of two experimental blocks. UV-deficient conditions also led to significant changes in behaviour indicative of escape (less perching and more hanging on the cage and pecking at it). However, the birds from the first block, where the interval between transfer to the experimental set-up from the wild was short (2 days), showed significantly higher basal and maximum plasma corticosterone concentrations than those in the second block and no additional effect of light environment on either corticosterone or behaviour. We hypothesise that this difference between blocks was due to the overriding initial stress of being in captivity swamping any treatment effects. Capture stress had declined in the second set of birds, which entered the experiment after 7 14 days in captivity. Stress effects of UV-deficient lighting appear small relative to the overall impact of captivity, but may nevertheless become apparent after the initial effects of capture subside. There is evidence that birds use ultraviolet cues in foraging and intra-specific signalling (reviewed in Cuthill et al. 2000c). However, captive birds tend to be housed under lighting designed to human specifications, which is usually poor in ultraviolet emissions (Lewis and Morris 1998). This could have welfare implications due to the direct loss of information utilised in individual recognition or foraging, which could increase aggression (Sherwin et al. 1999) or re-directed feather pecking (Huber-Eicher and Wechsler 1997). Unnatural wavelength compositions are also likely to affect general colour perception, since UV is a part of normal avian colour space (see e.g. Cuthill et al. 2000c). This may lead to chronic effects of impaired general visual performance and, in addition to welfare, affect the interpretation of laboratory experiments (Cuthill et al. 2000a, b). UV-deficient light environments increase basal plasma corticosterone levels and lead to a tendency to show less exploratory behaviour in domestic chicks Gallus g. domesticus, implying that the lack of UV wavelengths could be deleterious (Maddocks et al., in press b). Chickens sense UV via a cone type that is maximally sensitive to violet wavelengths (VS cone, max approximately 418 nm; Bowmaker et al. 1997). However, passerines possess a cone type that is maximally sensitive to ultraviolet (e.g. starling UVS cone, max 362 nm; Hart et al. 1998) so UV-deficient environments may be more deleterious for passerines than galliformes. We sought to determine whether starlings maintained in UV-deficient environments exhibited signs of compromised welfare compared with those under full spectrum lighting. We used juveniles as they lack the UV-iridescent plumage of adults (Bennett et al. 1997, Cuthill et al. 1999) and had no experience of mate choice using natural UV cues (Bennett et al. 1997, Maddocks et al. in press a). In this sense they are a conservative test of the stress effects of UV-deficient lighting on this species. We used a combination of behavioural (focal animal observation) and physiological measures (plasma corticosterone stress response). In birds, increased secretion of corticosterone occurs in 103
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