SUCESSO REPRODUTIVO DE CURICACA ( caudatus) (: ) NO PLANALTO DAS ARAUCÁRIAS, RIO GRANDE DO SUL, BRASIL.

BREEDING SUCCESS OF BUFF-NECKED (Theristicus caudatus) (PELECANIFORMES: THRESKIORNITHIDAE) IN ARAUCARIA PLATEAU, RIO GRANDE DO SUL, .

DAL CORNO, Renata De Boni1,2*; AVER, Gustavo Francisco3; PETRY, Maria Virginia4;

1 Universidade de Caxias do Sul, Área das Ciências da Vida, Rua Francisco Getúlio Vargas, 1130. Petrópolis. cep 95070-560 – Caxias do Sul – RS, Brasil (fone:+55 54 3218 2100)

2,3,4 Universidade do Vale do Rio dos Sinos, Programa de Pós Graduação em Biologia, Av. Unisinos, 950. Cristo Rei. Cep 93020-190 – São Leopoldo – RS, Brasil (fone: +55 51 3591 1122) * Autor correspondente e-mail: [email protected]

Received 02 November 2020; received in revised form 16 November 2018; accepted 31 December 2018

RESUMO

A história de vida de uma espécie pode ser considerada a principal fonte de informações acerca desta, parâmetros como comportamento de corte, período de incubação, número de ovos e filhotes, podem representar a aptidão dos indivíduos em relação ao meio, alterado ou não. Dessa maneira ao se obter informações do sucesso reprodutivo de uma espécie é possível avaliar a relação dos indivíduos com as modificações do ambiente. A Curicaca, (Theristicus caudatus) ocupa preferencialmente áreas secas campestres e utilizam áreas de cultivo como sítios de alimentação. Dentro da família Threskiornithidae, é considerada a espécie mais adaptável às perturbações ambientais e por isso ela pode ocupar diversos ambientes, inclusive antropizados, nidificando próximo a residências, e até em torres de transmissão. Este trabalho teve como objetivo avaliar o sucesso reprodutivo de três diferentes populações de Theristicus caudatus nos Campos de Cima da Serra. Foram acompanhados na estação reprodutiva de 2011, três locais de nidificação nas cidades de Bom Jesus (A e C) e São José dos Ausentes (B), que possuíam características ambientais diferentes entre si. Utilizaram-se três métodos para determinação do sucesso reprodutivo: o sucesso aparente, a taxa de eclosão dos ovos e o protocolo de Mayfield (1961,1975), considerando as modificações sugeridas por Hensler & Nichols (1981). Nas 600 horas de observação durante período reprodutivo, evidenciou-se uma média de 1,87 ± 0,74 ovos por ninho. O sucesso aparente e o protocolo de Mayfield apresentaram diferenças proporcionais entre os grupos, sendo o grupo B o que obteve maior sucesso reprodutivo, seguido por C e A. O ambiente onde os indivíduos do grupo B se encontravam pode ser considerado um meio termo entre as características dos outros grupos, possuindo características antrópicas que afastam predadores dos ninhos e das áreas de alimentação, enquanto os locais de alimentação têm reduzida influencia externa.

Palavras-chave: reprodução, ornitologia, comportamento, aves.

ABSTRACT

The life history of a can be considered the main source of information about it, parameters such as incubation period, number of and chicks, may represent the aptitude of individuals in relation to the environment, modified or not. Thus information from the reproductive success of a species allows evaluating the relationship of individuals to environmental changes. This study aimed to assess the reproductive success of three different populations of Buff-necked ibis, Theristicus caudatus, in Araucaria Plateau. The groups were followed in the reproductive season of 2011, three breeding which had environmental characteristics different from each other. We used three methods to determine the reproductive success: apparent success, hatching rate of eggs and protocol of Mayfield. In 600 hours of observation during the reproductive period, approximately 200 hours for each group, there was an average of 1.87 ± 0.74 eggs per nest. The apparent success and the

PERIÓDICO TCHÊ QUÍMICA • www.periodico.tchequimica.com • Vol. 16 N. 31. • ISSN 1806-0374 (impresso) • ISSN 1806-9827 (CD-ROM) • ISSN 2179-0302 (meio eletrônico) © 2019. Porto Alegre, RS. Brasil 831 protocol of Mayfield showed proportional differences between the groups. The environment where individuals were nesting in group B can be considered a compromise between the characteristics of other groups, with anthropogenic characteristics that draw predators away from nests and feeding areas, while feeding sites has reduced external influences.

Keywords: breeding, ornithology, behavior, .

INTRODUCTION MATERIAL AND METHODS

The Buff-necked ibis, Theristicus Sampling caudatus (Boddaert, 1783), belongs to Pelecaniform Order and occurs in , Three nesting sites were monitored distributed from to Tierra del Fuego. In (Figure 1), which were classified by natural Brazil these birds occupy countryside areas like environmental characteristics and/or the Cerrado, croplands and humid fields anthropogenic relating to land use. Group A was (Hancock et al. 1992), and its diet consists of located in Bom Jesus, and nesting occurred in arthropods, soil and some small Eucalyptus sp. who were near habitations. In the such as and lizards (Scherer- surrounding area was forestation of exotic Neto, 1982; Matheu and Del Hoyo, 1992; Belton, species Pinus sp. and pastures for cattle. Group 1994; Sick, 1997). B was found in São José dos Ausentes, nesting was held on Araucaria Angustifolia on the edge of Within the of Threskiornithidae, the a forest fragment modified without understory, Buff-necked ibis is considered the most due to cattle trampling. Its surroundings had adaptable species to disturbances, which may modified the native field. Group C, also located in occupy many environments, including Bom Jesus and the subjects performed nesting anthropogenic locations, nesting close to on individuals of A. angustifolia near housing, residences, and even transmission towers (Olive, associated with native pasture and native forest 2008), resulting in a higher abundance of in adjacent areas. Thus, they considered that the individuals. However, even abundant, this groups were at different levels of anthropogenic species has few studies on its ecology and pressure. biology (Scherer-Neto, 1982; Matheu and Del Hoyo, 1992; Hancock et al. 1992; Lorenzetto et al. 2003; Lorenzetto et al. 2004; Oliveira, 2008). The understanding of the ecological patterns of the species is a limiting factor for developing appropriate conservation and management strategies, both for wildlife and the environment in which they are held. In addition, several studies conclude on the importance to know the aspects of basic biology of these species, including information on reproductive biology, and these data are key in setting priorities for conservation of the same (Boyce, 1992; Reed et al. 1998; Quader, 2005, Velevski et al. 2014, Machado et al. 2017). In this sense, this study aimed to evaluate the reproductive success of three different populations of T. caudatus in Araucaria Plateau using different environments, such as native and impacted by agriculture and forestry areas. Figure 1. Map of the study area showing the location of the three groups: a) in relation to Brazil, b) in relation to the state of Rio Grande do Sul; c) distribution of the three groups.

PERIÓDICO TCHÊ QUÍMICA • www.periodico.tchequimica.com • Vol. 16 N. 31. • ISSN 1806-0374 (impresso) • ISSN 1806-9827 (CD-ROM) • ISSN 2179-0302 (meio eletrônico) © 2019. Porto Alegre, RS. Brasil 832 The groups were followed during the predators that larger groups can offer (Martins breeding season of the year 2011 for the months and Donatelli, 2001; Santos, 2009). Monitored from July to December, in monthly campaigns, groups of T. caudatus maintained the density lasting fifteen days, being that each group was throughout the study, even outside the breeding observed for five days. During each campaign, season. The subjects performed movements for the group was observed daily and observations the feed sites in smaller flocks or pairs as were performed in the active period of subjects, described by Oliveira (2008), returning to the nest ranging from 05:00 to 19:00. Totalizing a sites. The formation of aggregations were sampling effort of 600 hours of observation during related to the reduction of losses in the the reproductive period, each group had about reproduction (Master et al ., 1993) allowing to 200 hours. conclude that over time the groups remain The observation was directed at aggregated even after the breeding seasons, due individuals in reproductive behavior, possible to the better utilization of the resource, as well as breeding pairs, as well as individuals in the nest. possible protection against predators that larger At the end of each campaign was carried out the groups can offer (Martins and Donatelli, 2001; count of the eggs with the aid of mirrors and rods Santos, 2009). in order to avoid further interference in the It was observed that some couples used reproductive process of birds. existing nests, and this strategy has been

observed for seven nests, three for the A site, Statistical analysis four for site B and C. Three methods were used to determine The estimated average incubation time the reproductive success: the apparent success was 25 ± 3.018 days. About 45 days after (number of successful nests / number of active hatching period the first pups started to come out nests x 100), the hatching rate of eggs (number of the nest. The last puppy held the nest out of pups that have flown / number of eggs laid x about 60 days after hatching. 100) and the Mayfield protocol (1961, 1975), The reduction of the brood, a whereas the modifications suggested by Hensler phenomenon where two or more eggs are laid, and Nichols (1981). Within the Mayfield, protocol but usually only one develops, was present in the was possible to calculate the daily survival rate three groups and is widely observed in many (DSR), Daily mortality and survival probability of groups of birds (Martins and Dias, 2003; Roberts, nesting in each group. DSR represents the 2009; Rodriguez, 2009) inclusive may indicate a probability of the nest remain active from one day form of adaptation in response to low food to another, while the survival of the nest nests is conditions (Rodriguez, 2009). the probability to generate at least one offspring at a period. In this sense, the laying of more than one may be interpreted as a mechanism to

ensure the success of at least one young per RESULTS AND DISCUSSION: nest. Even with a reduction of 87% of the eggs, the mortality rate of the less efficient group (A) In the study, sites were observed a total of was 0.6%. In work by Hass et al. (1999) with 93 individuals who formed 19 couples during the individuals from ( ruber - reproductive period (Table 1). Threskiornithidae) had mortality rates of 4% of Monitored groups of T. caudatus eggs. In this study, it is reported that this maintained the density throughout the study, reduction may be mainly associated with even outside the breeding season. The subjects predation, an event that was not observed in any performed movements for the feed sites in of the following groups. smaller flocks or pairs as described by Oliveira In addition, the loss of chicks and nests (2008), returning to the nest sites. The formation has been reported in other species of the same of bird aggregations were related to the reduction family in the state of Rio Grande do Sul. Petry of losses in the reproduction (Master et al., 1993) and Fonseca (2005) found varying rates of loss of allowing to conclude that over time the groups nests, and the highest was 26.92% to Bared- remain aggregated even after the breeding faced ibis ( Phimosus infuscatus ) and 34.12% for seasons, due to the better utilization of the White-faced ibis ( chihi ). resource, as well as possible protection against

PERIÓDICO TCHÊ QUÍMICA • www.periodico.tchequimica.com • Vol. 16 N. 31. • ISSN 1806-0374 (impresso) • ISSN 1806-9827 (CD-ROM) • ISSN 2179-0302 (meio eletrônico) © 2019. Porto Alegre, RS. Brasil 833 The average of the hatching success of (Sigrist, 2009) may be related to using of different eggs between groups was 42.47 ± 4.33%, with environmental and/or anthropogenic features only the group A having a rate below the average found, influencing their reproductive success (37.5%), while B (45.45%) and C (42.86%) had rates. above-average rates. In turns, the apparent success was 79.44% ± 4.19 among the three groups. Group A had the apparent success of CONCLUSIONS: 75%, while B was 83.33% and C 79.44%. The hatching rate of the eggs showed no The reproductive success of Theristicus big difference between the groups. In all of them caudatus was influenced by the environment in the number of eggs remained close to the already with the nests wore build. The presence of reported average (Belton, 1994; Sick., 1997; anthropic characteristics does not induce Lorenzetto et al., 2003), ranging from 1 to 3 eggs differences in egg hatching, although, only one per nest, but resulting in all cases in only one site wave 100% probability of survival. young per nest. Daily survival rate excelled in This survival tax and the reproductive group B with 100% probability of survival of a success was higher in the area here the birds nest overnight. This was because since, even have access to food, but a minimum of with the reduction of the clutch, all couples who disturbance in the environmental, that reduce the lay eggs in this group had a puppy who flew from presence of predators on nesting or feeding the nest. spots.

Calculations using the Mayfield protocol ACKNOWLEDGMENTS: showed differences between breeding groups. DSR and the probability of survival of nests for We would like to thank the owners of the group A were 0.993 and 60.55%, respectively. study areas that allowed us access and remain in While the C group had DSR 0.997 and 81.85% their areas to carry out this study. probability of survival of nests and for the B group, the values were 0.1 and 100%, as all nests obtained reproductive success. REFERENCES: Regarding the apparent success and Mayfield protocol is observed that, in both tests, 1. Belton, W. Aves do Rio Grande do Sul, group B stands with the greatest reproductive distribuição e biologia. Universidade do success, followed by C and A. The environment Vale do Rio dos Sinos, São Leopoldo, where the B group was found, showed RS, Brasil. 1994. 584p. intermediate environmental characteristics 2. Boyce, M.S. Population viability analysis. compared to other groups. This site has anthropic Annual Review of Ecology and features that shy away from approaching Systematics , 1992. 23: 481-506. predators of nests and feeding areas (Donazár et 3. Donazár, J.A.; Ceballos, O.; Travaini, A.; al. , 1994). On the other hand, the dirty fields used Rodriguez, A.; Funes, M. & Hiraldo, F. as feeding areas do not receive any anthropic Breeding performance in relation to nest- influence, which can make the site as well as site substratum in a Buff-necked Ibis safe and less impacted with reduced external (Theristicus caudatus ) population in influence (Donazár et al., 1994). Patagonia. Condor , 1994. 96: 992-1102. The partial reduction of the clutch was 4. Gantz, A., & Yañez, M.. Breeding biology high, being approximately 87% of the nest of the black-faced Ibis (Theristicus reduced the clutch size, both in the incubation (10 melanopis) in Southern Chile. Waterbirds , occurrences) and in nestling phase (6 2016. 39(4), 346-355. occurrences). It is noteworthy that only three 5. Hass, A.; Matos, R. H. R. & Marcondes- nests become inactive with reduced litter size. Machado, L. O. Ecologia reprodutiva e The mortality rate to group A was 0.6% and C distribuição espacial da colônia de 0.26%, and in group B the value was zero Eudocimus ruber (Ciconiiformes, because there were no losses of nests. Threskiornithidae) na Ilha do Cajual, Maranhão. Revista Brasileira de So with this study, we can confirm that the Ornitologia , 1999. 7(1): 41-44. high adaptability of the species T. caudatus 6. Hensler, G.L. & Nichols, J.D. The Mayfield

PERIÓDICO TCHÊ QUÍMICA • www.periodico.tchequimica.com • Vol. 16 N. 31. • ISSN 1806-0374 (impresso) • ISSN 1806-9827 (CD-ROM) • ISSN 2179-0302 (meio eletrônico) © 2019. Porto Alegre, RS. Brasil 834 method of estimating nesting success: a Theristicus caudatus em linhas de model, estimators and simulation results. transmissão de alta tensão. Dissertação Wilson Bulletin, 1981. 93(1): 42-53. de Mestrado. Universidade de Brasília. 7. Lorenzetto, A. Lindoso, G. Russel, J.; Brasília, BR. 2008. Serbena, A.; Pichorim, M.; Reinert, B. L. & 17. Mortensen, J. L., & Reed, J. M. Population Salvo, L. Padrão de atividade diária em Viability and Vital Rate Sensitivity of an dois ninhos de curicacas (Theristicus Endangered Avian Cooperative Breeder, caudatus, Threskionithidae) no Parque the White-Breasted Thrasher Estadual de Vila-Velha – PR. In: (Ramphocinclus brachyurus). PloS one, Sociedade Brasileira de Ornitologia. Anais 2016. 11(2), e0148928. do XII Congresso Brasileiro de 18. Petry, M.V. & Fonseca, V.S.D.S. Breeding Ornitologia. Blumenau – SC. 2004. success of the colonist species Bubulcus 8. Lorenzetto, A.; Pichorim, M.; Reinert, B.L.; ibis (Linnaeus, 1758) and four native Salvo, L.M.; Muller, C. & Lindoso, G. species. Acta Zoologica, 2005. 86(3): Aspectos da ecologia da curicaca, 217-221. Theristicus caudatus (Threskionithidae), 19. Quader, S. Mate choice and its no Parque Estadual de Vila Velha – PR. implications for conservation and In: Anais do XII Congresso Brasileiro de management. Current Science, 2005. 89: Ornitologia. Blumenau – SC. 2003. 1220-1229. 9. Machado, T. L. D. S. S., Lombardi, V. T., 20. Reed, J.M.; Elphick, C.S. & Oring, L.W. de Meireles, R. C., Teixeira, J. P. G., Life-history and viability analysis of the Solar, R. R. D. C., & Lopes, L. E. endangered Hawaiian Stilt. Biological Breeding biology of the threatened Conservation, 1998. 84:35-45. Campo Miner Geositta poeciloptera 21. Rodrigues, S.S. Biologia e sucesso (Aves: Scleruridae), a Neotropical reprodutivo de Mimus saturninus (aves: grassland specialist. Journal of Natural Mimidae) no cerrado. Dissertação de History, 2017. 51(41-42), 2551-2563. Mestrado. Universidade de Brasília, 10. Martins, F.C. & Donatelli, R.J. Estratégia Brasília. 2009. alimentar de Guira guira (Cuculidae: 22. Rodriguez, M.N. Assincronia e sincronia Crotopahginae) na região centro-oeste do de eclosão: um teste experimental de estado de São Paulo. Revista Brasileira reprodução em Furnarius rufus. de Ornitologia, 2001. 9(2): 89-94. Dissertação de Mestrado. Universidade 11. Martins, F.C. & Dias, M.M. Cuidado Federal do Paraná. 2009. parental de Sula leucogaster (Boddaert) 23. Santos, E.S.A. Biologia reprodutiva de (Aves, Pelecaniformes, ) nas Ilhas Vanellus chilensis (Aves: Charadriidae): dos Currais, Paraná, Brasil. Revista por que reproduzir em grupo? Brasileira de Zoologia. 2003. 20(4): 583- Dissertação de Mestrado. Universidade 589. de Brasília, Brasília. 2009. 12. Master, T.L.; Frankel, M, & Russell, M. 24. Scherer-Neto, P. Aspectos bionômicos e Benefits of foraging in mixed-species desenvolvimento de Theristicus caudatus agregations in a sol New-Jersey. (Boddaert 1783). Dusenia 1982. 13 (4): Waterbirds, 1993. 14: 176 179. 145- 149. 13. Matheu, E. & Del Hoyo, J. Family 25. Sick, H. Ornitologia Brasileira. 2 ed. Rio Threskiornithidae ( and ). de Janeiro: Editora Nova Fronteira. 1997. Pp. 472–506 In: del Hoyo J, Elliott A, 26. Sigrist, T. Guia de campo Avis Brasilis – Sargatal J (eds). Handbook of the birds of Avifauna brasileira: descrição das the world. Volume 1. Ostrich to Ducks. espécies. 1 ed. Vinhedo: AvisBrasilis Lynx Edicions. Barcelona, Spain. 1992. Editora. 2009 14. Mayfield, H.F. Nesting success calculated 27. Velevski, M., Grubac, B., & Tomovic, L. from exposure. Wilson Bulletin, 1961. Population viability analysis of the 73(3): 255-261. Egyptian Vulture Neophron percnopterus 15. Mayfield, H.F. Suggestions for calculating in Macedonia and implications for its nest success. Wilson Bulletin, 1975. conservation. Acta Zoologica Bulgarica, 87(4): 456-466. 2014. 66: 43-58. 16. Oliveira, A.C.. Ocupação ambiental e características populacionais de curicacas

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A B C Total Number of 43 27 23 93 individuals Breeding pairs 7 (36,84%) 6 (31,58%) 6 (31,58%) 19 Average number 2 ± 0,82 1,83 ± 0,75 1,8 ± 0,84 1,87 ± 0,74 of eggs per nest Built nests 6 (35,29%) 6 (35,29%) 5 (29,42%) 17 Active nests 4 (26,67%) 6 (40%) 5 (33,33%) 15

PERIÓDICO TCHÊ QUÍMICA • www.periodico.tchequimica.com • Vol. 16 N. 31. • ISSN 1806-0374 (impresso) • ISSN 1806-9827 (CD-ROM) • ISSN 2179-0302 (meio eletrônico) © 2019. Porto Alegre, RS. Brasil 836