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Cannibalism by Brown Booby (Sula leucogaster) at a small tropical archipelago

Cannibalism by Brown Booby (Sula leucogaster) at a small tropical archipelago Revista Brasileira de Ornitologia, 23(3), 299-304 ARTICLE September 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago 1 1,2,3 1,2 1,2 Felipe Machado Neves , Patrícia Luciano Mancini , Fernanda Pinto Marques , Guilherme Tavares Nunes 1,2,4 and Leandro Bugoni Waterbirds and Sea Turtles Laboratory, Institute of Biological Sciences, Universidade Federal do Rio Grande - FURG, CP 474, CEP 96203-900, Rio Grande, RS, Brazil. Graduate Program in Biological Oceanography, Universidade Federal do Rio Grande - FURG, CP 474, CEP 96203-900, Rio Grande, RS, Brazil. Current address: Seção de Aves, Museu de Zoologia da Universidade de São Paulo, CP 42694, CEP 04263-000, São Paulo, SP, Brazil. Corresponding author: lbugoni@pq.cnpq.br Received on 1 January 2015. Accepted on 15 September 2015. ABSTRACT: Cannibalism is the total or partial consumption of a conspecifi c’s body or eggs, and it has been reported for many bird taxa, particularly carnivorous, colonial species, and those species that ingest fragmented prey. Here we report cannibalism by Brown Booby (Sula leucogaster r r) at Saint Peter and Saint Paul Archipelago, offshore Brazil. We discussed possible causes for this behavior such as opportunistic feeding, colony sanitation and space competition for nesting places. KE E EY Y Y-WORDS: chick mortality, opportunistic feeding, Saint Peter and Saint Paul Archipelago, seabirds, Sulidae. INTRODUCTION Similarly to some other Sulidae species, the Brown Booby shows obligate siblicide (Anderson 1990, Drummond 2001, Nelson 2005, but see Tershy et alll. 2000). Only one Direct cannibalism refers to the consumption of a living conspecifi c or its eggs (Stanback & Koenig 1992) and chick fled ges, either because the parents only feed one indirect cannibalism refers to scavenging on a conspecific chick or because the first-hatched chick or the parents whose death was due to other causes, including the action eventually ejects the younger chick from the nest. Here we provide evidence for direct and indirect cannibalism of predators (Riehl 2006). Cannibalism occurs in a wide involving chicks and adults Brown Booby at Saint Peter range of animal taxa, from Protozoa to mammals, and has been reported for nearly every major vertebrate group, and Saint Paul Archipelago (SPSPA breeding colony), but it is infrequent in most species in which it occurs offsho re Brazil. (Stanback & Koenig 1992, Pfennig 1997). Cannibalism in birds occurs primarily in species that are carnivorous, METHODS colonial, and that feed on fragments of prey rather than the whole prey (Stanback & Koenig 1992). Therefore, among wild birds, raptors and seabirds are the groups Study Area more prone to cannibalism (Stanback & Koenig 1992, Th e SPSPA (00°55'10"N, 29°20'33"W) is about 1,100 Markham & Watts 2007, Andrew & Munro 2008). km from the Northeastern mainland Brazilian coast. It Among seabirds, cannibalism has been reported in gulls, originates from a Meso-Atlantic elevation based at 4,000 pelicans, terns, frigatebirds and boobies (Stanback & Koenig 1992, Humphries et alll. 2006, Gubiani et alll. m depth and comprises 15 rocky islets covering an area 2012, Hayward et alll. 2014). of 17,500 m . Belmonte is the largest islet, about 100 m long, 50 m wide and the highest point of the archipelago The Brown Boob y (Sula leucogaster r r) is the most is 18 m above sea level (Vaske-Jr et alll. 2010). SPSPA widely distributed Sulidae species, occurring in tropical is located in an oligotrophic area, directly influenced and subtropical seas around the world (Nelson 2005). Typically, Brown Boobies capture fi sh and squids by by the South Equatorial Current, fl owing from east to plunge-diving (Harrison et alll. 1983, Naves et alll. 2002), west, and the Equatorial Undercurrent, which flows in the opposite direction and with core located about 80 but also feed on fishery discards (Krul 2004). The m depth (Travassos et alll. 1999). Approximately 580 Brown Booby is monogamous and usually lays two eggs. Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni Brown Boobies, 390 Brown Noddies ( ( (Anous stolidus s) without eggs or chicks. We carried out experimental trials and 320 Black Noddies ( ( (A. minutus s) breed in SPSPA opportunistically whenever a dead chick was found, and (Both & Freitas 2004, Neves et alll. 2013). The number observed and recorded with photography and video the of Brown Boobies is fairly constant year round and about reaction of the receiving pairs towards the dead chick. 90% of these birds occur on Belmonte Islet, in a dense We paid particular attention to whether receiving birds monospecific colony (Barbosa-Filho & Vooren 2010) swallowed the chick carcass, and the age and sex of while other islets are used mainly for roosting by this cannibals. We determined sex of adults by vocalizations species (Naves et alll. 2002, Both & Freitas 2004, Barbosa- or the colors of the head, skin or bill, and determined age Filho & Vooren 2010). Flyingfi shes are key prey species by plumage colors (Harrison 1983). Finally, we estimated for tuna, sharks and seabirds (Mancini & Bugoni 2014), the age of the dead chicks following Barbosa-Filho & while the abundant fishery resources are explored by a Vooren (2010), and then used age to estimate body mass commercial fishery of regional importance based on the of ingested chicks (Coelho et alll. 2004). mainland (Vaske-Jr et al. 2005). RESULTS Observations Research expeditions to SPSPA occurred in August 2011, Experimental Trials January 2012, May-June 2014 and July 2015. Initially, we observed two Brown Booby pairs (including the parents of Trial 1 (19 August 2011). We collected one 3-week old a dead chick) pecking rapidly and repeatedly on the dead chick (~300 g) found dead close to its original nest and nestling, although we did not notice consumption of the placed it on the ground, in front of a Brown Booby pair body. Th is aggressive behavior suggested that cannibalism that was defending an empty nest. Both birds observed the could occur at this colony and, therefore, a behavioral chick for a few seconds. Th e male approached the chick experiment was developed to study the occurrence of and moved it closer to the female, which immediately cannibalism. We collected fresh chick carcasses resulting swallowed the chick. from natural mortality in their original nests or close to Trial 2 (19 August 2011). We found a dead 3-week old them. To assess propensity for cannibalism, we carried chick (~300 g) and placed it on the ground next to a pair, out seven experimental trials. We placed a dead chick different from the previous pair. The pair soon approached next to paired Brown Boobies defending a nest site the chick and the female swallowed it (Figure 1). FIGURE 1. Cannibalism of a dead chick by a female Brown Booby (Sula leucogaster r r) at Saint Peter and Saint Paul Archipelago, Northeastern Brazil. (Photo: F. M. Neves) Revista Brasileira de Ornitologia, 23(3), 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni Trial 3 (11 January 2012). We observed a breeding by a pair without chick or egg. Both adults pecked and male Brown Booby at 10:10 h (GMT-2), close to its own shook the chick vigorously for 2 min, the female acting 4-week old dead chick (~400 g). Th is male continually more aggressively, and then set it aside without trying to moved soil, small stones, and the chick around the nest swallow it. in a manner similar to nest-building behavior. With the Trial 6 (15 May 2014). We placed an adult Brown chick out of the nest, this behavior continued and a small Booby carcass on the other side of booby nests, away from hole was dug in the ground. By 12:00 h, the pair was in birds. About 2 min later a female grabbed the carcass and the nest and the dead chick was at the same place, close tried to swallow it repeatedly, but was unsuccessful due to to the nest. Shortly after, we removed the chick from the gape limitation. She left the carcass on the ground and a vicinity of the pair. The parents became restless, as did the wave washed it away from the colony. neighboring boobies. Trial 7 (31 May 2014). We found a dead chick (~300 Trial 4 (11 January 2012). We placed the dead chick g) and placed it near a nest occupied by a pair without (the same specimen used for trial 3) in a nearby nest chick or egg. A female pecked at the chick and tried to occupied by a pair without chick or egg. The receivin g swallow it, but was unsuccessful due to gape limitation. pair began to peck at the chick as soon as they perceived Male and female continued pecking the dead nestling, its presence. A nearby nearly-fled ged, fli ghtless chick but lost interest over time. got involved and exhibited aggressive behavior towards Apart from the trials explained above, during a the receiving pair and other birds around, including 1-month expedition, two spontaneous cannibalistic the parents of the dead chick. The nearly-fled ged chick events were recorded. On 20 July 2015, a female pushed persistently attempted to swallow the dead chick for out their younger nestling (3 days old; <100 g) and about 10 min (Figure 2), but was unsuccessful due to its promptly, an adjacent breeding pair caught the still alive small size relative to the dead chick and its gape width chick, and the male swallowed it (Figure 3). On 27 July limitation. When the nearly-fl edged chick fi nally stopped 2015, a breeding male caught and swallowed a 1-week its attempts, the juvenile’s mother immediately grabbed old nestling (<100 g) from the adjacent nest, while the dead chick and tried to swallow it for about 1 min, researchers were sampling the adult attending the nest, again unsuccessful due to gape limitation. The dead chic k which did not last more than 5 minutes. was then left on the ground. Overall, from seven trials and two spontaneous Trial 5 (11 January 2012). We moved the dead observations, we report seven cannibalistic events by chick (from trials 3 and 4) to another nest occupied Brown Booby individuals at SPSPA. FIGURE 2. A nearly-fledged Brown Booby ( Sula leucogaster r r) attempting to swallow a dead chick from an adjacent nest at Saint Peter and Saint Paul Archipelago, Brazil. (Photo: F. P. Marques) Revista Brasileira de Ornitologia, 23(3), 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni FIGURE 3. Brown Booby (Sula leucogaster r r) breeding pair fighting for a 3-days old chick, which was pushed out of the nest by the adjacent breeding female. Th e fi ght ends with the male swallowing the chick. Chronological sequence of the events from left to right. (Photo: G. T. Nunes) DISCUSSION Booby chicks were consumed or there was attempted consumption, a possible explanation could be an Cannibalism in sulid species was recorded a single time opportunistic feeding behavior by females to restore in the Nazca Booby (Sula granti) in more than 15 years energy during breeding. In seabirds, including sulids, males and females generally share breeding duties equally of research at Galapagos Islands (Humphries et alll. 2006). However, Brown Booby cannibalism at SPSPA was (Nelson 2005, Lormee et alll. 2005, Weimerskirch et alll. reported previously in two unpublished sources. The 2006). However, at SPSPA, female Brown Boobies are fi rst report was part of a Ph.D. thesis, which included mostly responsible for feeding chicks (80% of the time, a Brown Booby diet study at SPSPA and one chick was compared to males, Kohlrausch 2003). In the SPSPA, the Brown Booby breeds throughout the year and there has observed in a female regurgitate, sampled between 1999- 2001 (Kohlrausch 2003). Th e second report was from been no report of yearly variation in the occurrence of expedition diaries (Expedition No. 164, and report by breeding (Both & Freitas 2001, Barbosa-Filho & Vooren C.J.A. Costa-Jr., A. Cavalcante and C.M. Vooren), which 2010). Furthermore, in SPSPA, seabirds and marine described a female with a broken wing that ate a live chick pelagic fish rely on the same prey species (flyin gfish), but the overlap in their trophic niches was limited, most when it was ejected from the nest by its parents in August 2004. Thus, cannibalistic behavior had been previously likely due to an overabundant food resource (Mancini & observed at our study site, apparently under natural Bugoni 2014). circumstances, i.e. without an intentional delivery to Th e availability of food for seabirds at the SPSPA potential cannibals as in our trials. is probably constant and predictable through the year (Barbosa-Filho & Vooren 2010). SPSPA slows the Many hypotheses have been suggested to explain cannibalism in birds. In the broken winged female case, Equatorial Undercurrent, increasing residence time cannibalism could have occurred due to acute food of nutrients around the archipelago and generating limitation (Ingram 1959, Stanback & Koenig 1992, subsurface vortices (Araujo & Cintra 2009). Th is process Nishimura 2010), because the female was fli ghtless and increases local primary productivity and allows a great abundance of flyin gfish, lar ge pelagic fishes and intense food deprived. Cannibalism has been associated with food shortage in other species, such as the Long-tailed fi sheries around the SPSPA (Vaske-Jr et alll. 2003, 2008, Jaeger (Stercorarius longicaudus s s) (Vooren & Chiaradia Viana et alll. 2012). Thus, food shortage does not seem to 1989), the Australian Pelican (Pelecanus conspicillatus s s), be driving cannibalistic behavior. Th e ‘icebox hypothesis’ the Australian White Ibis (Threskiornis molucca) (Andrew (Alexander 1974), alternatively, considers that a marginal offsprin g is a potential feeding resource and that its & Munro 2008), the Peruvian Pelican (P. thagus s s) (Daigre et alll. 2012), and the Socotra Cormorant (Phalacrocorax consumption confers breeding advantage to the parents nigrogularis s s) (Gubiani et alll. 2012). (Ingram 1959). Filial cannibalism (consumption of all In our observations (trials 1, 2, 4, 6, 7, and the two or part of the young by the parents) may be an adaptive events of spontaneous cannibalism), as well as in the strategy where energetic requirements trigger cannibalism (Klug & Bonsall 2007). However, cannibalism seems to case reported by Kohlrausch (2003), in which Brown Revista Brasileira de Ornitologia, 23(3), 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni contribute only a marginal increment to the breeding established by the Brazilian Navy, may be influencing this success of the Nazca Booby, and Humphries et al. (2006) behavior. Since then, the island has been permanently did not observe family members consuming chicks inhabited by small groups of researchers and mariners because the similar size of siblings precludes such behavior. (usually four). Additionally, researchers, sailors and At SPSPA, most cannibalistic birds were females, and in fishermen often feed boobies left-over fish parts, and one instance (trial 1), the male offered the dead chick to individuals with a propensity for cannibalistic behavior the female, in line with the food deprivation hypothesis, may have interpreted the dead chicks thrown close to which could help offset energetic costs of egg production. the nests (our trials) as a food off er by humans, despite Th e exceptions were the two spontaneous cannibalism this does not explain the spontaneous cannibalism events recorded in July 2015, when males swallowed events reported. In summary, explanations for the chicks, which suggests that this hypothesis does not natural cannibalism reported previously, as well as our explain all cannibalistic events at SPSPA. ‘unnatural’ trials, which result in cannibalistic attempts, Furthermore, cannibalism may be a density- remain elusive, and further experimental studies should dependent behavior (Fox 1975, Nishimura 2010). At be carried out to address why Brown Boobies from this high nest densities, egg cannibalism and social stress area differ from s ulids elsewhere. increase in gulls (Burger 1980, Brouwer & Spaans 1994), and disputes over territories are frequent in ACKNOWLEDGMENTS booby colonies (Alves et alll. 2004, Nelson 2005). The SPSPA Brown Booby population increased from 334 We thank the Brazilian Navy and Comissão Interministerial birds in 2000-2001 (Barbosa-Filho & Vooren 2010) to para os Recursos do Mar r (CIRM/SECIRM) for logistic 588 birds in 2011-2014 (Neves et alll. 2013, Mancini support for the SPSPA expeditions, the Brazilian et alll. unpublished data) and no emigration has been Research Council (CNPq - Grant No. 557152/2009-7 documented (Barbosa-Filho & Vooren 2010). In this and 405497/2012-1) for funding the project. P.L.M. colony there is an average distance between nests of acknowledges CAPES Foundation for providing grants 1 m, while in the Rocas Atoll, northeastern Brazil, for (No. 9733/2011-6). L.B. is a research fellow from the instance, nests are 11 m apart on average (Kohlrausch Brazilian CNPq (Proc. No. 308697/2012-0). Authors are 2003). Furthermore, average nest diameter of SPSPA is also grateful to L. C. Naves and R. H. Macedo for a critical ~20% smaller than Rocas Atoll nests (Kohlrausch 2003). revision and insightful comments on an earlier version. Some additional observations of the authors on the Brown Boobies at SPSPA also suggest space limitation. Fights over territory in the nest surroundings are intense REFERENCES and common, resulting in injured adults or chick death. Furthermore, boobies frequently establish nests in low, Alexander, R. D. 1974. Th e evolution of social behaviour. Annual marginal areas, close to the area of wave action, i.e., low Review of Ecology, Evolution and Systematics, 5: 325-383. quality areas with reduced breeding success. In both Alves, V. S.; Soares, A. B. A. & Couto, G. S. 2004. Aves marinhas spontaneous events reported here, cannibalized chicks e aquáticas das ilhas do litoral do Rio de Janeiro, p. 83-100. In: Branco, J. O. (Ed.). Aves marinhas e insulares brasileiras: bioecologia belonged to nests adjacent to cannibals. All this suggests e conservação. 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Cannibalism by Brown Booby (Sula leucogaster) at a small tropical archipelago

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Revista Brasileira de Ornitologia, 23(3), 299-304 ARTICLE September 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago 1 1,2,3 1,2 1,2 Felipe Machado Neves , Patrícia Luciano Mancini , Fernanda Pinto Marques , Guilherme Tavares Nunes 1,2,4 and Leandro Bugoni Waterbirds and Sea Turtles Laboratory, Institute of Biological Sciences, Universidade Federal do Rio Grande - FURG, CP 474, CEP 96203-900, Rio Grande, RS, Brazil. Graduate Program in Biological Oceanography, Universidade Federal do Rio Grande - FURG, CP 474, CEP 96203-900, Rio Grande, RS, Brazil. Current address: Seção de Aves, Museu de Zoologia da Universidade de São Paulo, CP 42694, CEP 04263-000, São Paulo, SP, Brazil. Corresponding author: lbugoni@pq.cnpq.br Received on 1 January 2015. Accepted on 15 September 2015. ABSTRACT: Cannibalism is the total or partial consumption of a conspecifi c’s body or eggs, and it has been reported for many bird taxa, particularly carnivorous, colonial species, and those species that ingest fragmented prey. Here we report cannibalism by Brown Booby (Sula leucogaster r r) at Saint Peter and Saint Paul Archipelago, offshore Brazil. We discussed possible causes for this behavior such as opportunistic feeding, colony sanitation and space competition for nesting places. KE E EY Y Y-WORDS: chick mortality, opportunistic feeding, Saint Peter and Saint Paul Archipelago, seabirds, Sulidae. INTRODUCTION Similarly to some other Sulidae species, the Brown Booby shows obligate siblicide (Anderson 1990, Drummond 2001, Nelson 2005, but see Tershy et alll. 2000). Only one Direct cannibalism refers to the consumption of a living conspecifi c or its eggs (Stanback & Koenig 1992) and chick fled ges, either because the parents only feed one indirect cannibalism refers to scavenging on a conspecific chick or because the first-hatched chick or the parents whose death was due to other causes, including the action eventually ejects the younger chick from the nest. Here we provide evidence for direct and indirect cannibalism of predators (Riehl 2006). Cannibalism occurs in a wide involving chicks and adults Brown Booby at Saint Peter range of animal taxa, from Protozoa to mammals, and has been reported for nearly every major vertebrate group, and Saint Paul Archipelago (SPSPA breeding colony), but it is infrequent in most species in which it occurs offsho re Brazil. (Stanback & Koenig 1992, Pfennig 1997). Cannibalism in birds occurs primarily in species that are carnivorous, METHODS colonial, and that feed on fragments of prey rather than the whole prey (Stanback & Koenig 1992). Therefore, among wild birds, raptors and seabirds are the groups Study Area more prone to cannibalism (Stanback & Koenig 1992, Th e SPSPA (00°55'10"N, 29°20'33"W) is about 1,100 Markham & Watts 2007, Andrew & Munro 2008). km from the Northeastern mainland Brazilian coast. It Among seabirds, cannibalism has been reported in gulls, originates from a Meso-Atlantic elevation based at 4,000 pelicans, terns, frigatebirds and boobies (Stanback & Koenig 1992, Humphries et alll. 2006, Gubiani et alll. m depth and comprises 15 rocky islets covering an area 2012, Hayward et alll. 2014). of 17,500 m . Belmonte is the largest islet, about 100 m long, 50 m wide and the highest point of the archipelago The Brown Boob y (Sula leucogaster r r) is the most is 18 m above sea level (Vaske-Jr et alll. 2010). SPSPA widely distributed Sulidae species, occurring in tropical is located in an oligotrophic area, directly influenced and subtropical seas around the world (Nelson 2005). Typically, Brown Boobies capture fi sh and squids by by the South Equatorial Current, fl owing from east to plunge-diving (Harrison et alll. 1983, Naves et alll. 2002), west, and the Equatorial Undercurrent, which flows in the opposite direction and with core located about 80 but also feed on fishery discards (Krul 2004). The m depth (Travassos et alll. 1999). Approximately 580 Brown Booby is monogamous and usually lays two eggs. Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni Brown Boobies, 390 Brown Noddies ( ( (Anous stolidus s) without eggs or chicks. We carried out experimental trials and 320 Black Noddies ( ( (A. minutus s) breed in SPSPA opportunistically whenever a dead chick was found, and (Both & Freitas 2004, Neves et alll. 2013). The number observed and recorded with photography and video the of Brown Boobies is fairly constant year round and about reaction of the receiving pairs towards the dead chick. 90% of these birds occur on Belmonte Islet, in a dense We paid particular attention to whether receiving birds monospecific colony (Barbosa-Filho & Vooren 2010) swallowed the chick carcass, and the age and sex of while other islets are used mainly for roosting by this cannibals. We determined sex of adults by vocalizations species (Naves et alll. 2002, Both & Freitas 2004, Barbosa- or the colors of the head, skin or bill, and determined age Filho & Vooren 2010). Flyingfi shes are key prey species by plumage colors (Harrison 1983). Finally, we estimated for tuna, sharks and seabirds (Mancini & Bugoni 2014), the age of the dead chicks following Barbosa-Filho & while the abundant fishery resources are explored by a Vooren (2010), and then used age to estimate body mass commercial fishery of regional importance based on the of ingested chicks (Coelho et alll. 2004). mainland (Vaske-Jr et al. 2005). RESULTS Observations Research expeditions to SPSPA occurred in August 2011, Experimental Trials January 2012, May-June 2014 and July 2015. Initially, we observed two Brown Booby pairs (including the parents of Trial 1 (19 August 2011). We collected one 3-week old a dead chick) pecking rapidly and repeatedly on the dead chick (~300 g) found dead close to its original nest and nestling, although we did not notice consumption of the placed it on the ground, in front of a Brown Booby pair body. Th is aggressive behavior suggested that cannibalism that was defending an empty nest. Both birds observed the could occur at this colony and, therefore, a behavioral chick for a few seconds. Th e male approached the chick experiment was developed to study the occurrence of and moved it closer to the female, which immediately cannibalism. We collected fresh chick carcasses resulting swallowed the chick. from natural mortality in their original nests or close to Trial 2 (19 August 2011). We found a dead 3-week old them. To assess propensity for cannibalism, we carried chick (~300 g) and placed it on the ground next to a pair, out seven experimental trials. We placed a dead chick different from the previous pair. The pair soon approached next to paired Brown Boobies defending a nest site the chick and the female swallowed it (Figure 1). FIGURE 1. Cannibalism of a dead chick by a female Brown Booby (Sula leucogaster r r) at Saint Peter and Saint Paul Archipelago, Northeastern Brazil. (Photo: F. M. Neves) Revista Brasileira de Ornitologia, 23(3), 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni Trial 3 (11 January 2012). We observed a breeding by a pair without chick or egg. Both adults pecked and male Brown Booby at 10:10 h (GMT-2), close to its own shook the chick vigorously for 2 min, the female acting 4-week old dead chick (~400 g). Th is male continually more aggressively, and then set it aside without trying to moved soil, small stones, and the chick around the nest swallow it. in a manner similar to nest-building behavior. With the Trial 6 (15 May 2014). We placed an adult Brown chick out of the nest, this behavior continued and a small Booby carcass on the other side of booby nests, away from hole was dug in the ground. By 12:00 h, the pair was in birds. About 2 min later a female grabbed the carcass and the nest and the dead chick was at the same place, close tried to swallow it repeatedly, but was unsuccessful due to to the nest. Shortly after, we removed the chick from the gape limitation. She left the carcass on the ground and a vicinity of the pair. The parents became restless, as did the wave washed it away from the colony. neighboring boobies. Trial 7 (31 May 2014). We found a dead chick (~300 Trial 4 (11 January 2012). We placed the dead chick g) and placed it near a nest occupied by a pair without (the same specimen used for trial 3) in a nearby nest chick or egg. A female pecked at the chick and tried to occupied by a pair without chick or egg. The receivin g swallow it, but was unsuccessful due to gape limitation. pair began to peck at the chick as soon as they perceived Male and female continued pecking the dead nestling, its presence. A nearby nearly-fled ged, fli ghtless chick but lost interest over time. got involved and exhibited aggressive behavior towards Apart from the trials explained above, during a the receiving pair and other birds around, including 1-month expedition, two spontaneous cannibalistic the parents of the dead chick. The nearly-fled ged chick events were recorded. On 20 July 2015, a female pushed persistently attempted to swallow the dead chick for out their younger nestling (3 days old; <100 g) and about 10 min (Figure 2), but was unsuccessful due to its promptly, an adjacent breeding pair caught the still alive small size relative to the dead chick and its gape width chick, and the male swallowed it (Figure 3). On 27 July limitation. When the nearly-fl edged chick fi nally stopped 2015, a breeding male caught and swallowed a 1-week its attempts, the juvenile’s mother immediately grabbed old nestling (<100 g) from the adjacent nest, while the dead chick and tried to swallow it for about 1 min, researchers were sampling the adult attending the nest, again unsuccessful due to gape limitation. The dead chic k which did not last more than 5 minutes. was then left on the ground. Overall, from seven trials and two spontaneous Trial 5 (11 January 2012). We moved the dead observations, we report seven cannibalistic events by chick (from trials 3 and 4) to another nest occupied Brown Booby individuals at SPSPA. FIGURE 2. A nearly-fledged Brown Booby ( Sula leucogaster r r) attempting to swallow a dead chick from an adjacent nest at Saint Peter and Saint Paul Archipelago, Brazil. (Photo: F. P. Marques) Revista Brasileira de Ornitologia, 23(3), 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni FIGURE 3. Brown Booby (Sula leucogaster r r) breeding pair fighting for a 3-days old chick, which was pushed out of the nest by the adjacent breeding female. Th e fi ght ends with the male swallowing the chick. Chronological sequence of the events from left to right. (Photo: G. T. Nunes) DISCUSSION Booby chicks were consumed or there was attempted consumption, a possible explanation could be an Cannibalism in sulid species was recorded a single time opportunistic feeding behavior by females to restore in the Nazca Booby (Sula granti) in more than 15 years energy during breeding. In seabirds, including sulids, males and females generally share breeding duties equally of research at Galapagos Islands (Humphries et alll. 2006). However, Brown Booby cannibalism at SPSPA was (Nelson 2005, Lormee et alll. 2005, Weimerskirch et alll. reported previously in two unpublished sources. The 2006). However, at SPSPA, female Brown Boobies are fi rst report was part of a Ph.D. thesis, which included mostly responsible for feeding chicks (80% of the time, a Brown Booby diet study at SPSPA and one chick was compared to males, Kohlrausch 2003). In the SPSPA, the Brown Booby breeds throughout the year and there has observed in a female regurgitate, sampled between 1999- 2001 (Kohlrausch 2003). Th e second report was from been no report of yearly variation in the occurrence of expedition diaries (Expedition No. 164, and report by breeding (Both & Freitas 2001, Barbosa-Filho & Vooren C.J.A. Costa-Jr., A. Cavalcante and C.M. Vooren), which 2010). Furthermore, in SPSPA, seabirds and marine described a female with a broken wing that ate a live chick pelagic fish rely on the same prey species (flyin gfish), but the overlap in their trophic niches was limited, most when it was ejected from the nest by its parents in August 2004. Thus, cannibalistic behavior had been previously likely due to an overabundant food resource (Mancini & observed at our study site, apparently under natural Bugoni 2014). circumstances, i.e. without an intentional delivery to Th e availability of food for seabirds at the SPSPA potential cannibals as in our trials. is probably constant and predictable through the year (Barbosa-Filho & Vooren 2010). SPSPA slows the Many hypotheses have been suggested to explain cannibalism in birds. In the broken winged female case, Equatorial Undercurrent, increasing residence time cannibalism could have occurred due to acute food of nutrients around the archipelago and generating limitation (Ingram 1959, Stanback & Koenig 1992, subsurface vortices (Araujo & Cintra 2009). Th is process Nishimura 2010), because the female was fli ghtless and increases local primary productivity and allows a great abundance of flyin gfish, lar ge pelagic fishes and intense food deprived. Cannibalism has been associated with food shortage in other species, such as the Long-tailed fi sheries around the SPSPA (Vaske-Jr et alll. 2003, 2008, Jaeger (Stercorarius longicaudus s s) (Vooren & Chiaradia Viana et alll. 2012). Thus, food shortage does not seem to 1989), the Australian Pelican (Pelecanus conspicillatus s s), be driving cannibalistic behavior. Th e ‘icebox hypothesis’ the Australian White Ibis (Threskiornis molucca) (Andrew (Alexander 1974), alternatively, considers that a marginal offsprin g is a potential feeding resource and that its & Munro 2008), the Peruvian Pelican (P. thagus s s) (Daigre et alll. 2012), and the Socotra Cormorant (Phalacrocorax consumption confers breeding advantage to the parents nigrogularis s s) (Gubiani et alll. 2012). (Ingram 1959). Filial cannibalism (consumption of all In our observations (trials 1, 2, 4, 6, 7, and the two or part of the young by the parents) may be an adaptive events of spontaneous cannibalism), as well as in the strategy where energetic requirements trigger cannibalism (Klug & Bonsall 2007). However, cannibalism seems to case reported by Kohlrausch (2003), in which Brown Revista Brasileira de Ornitologia, 23(3), 2015 Cannibalism by Brown Booby (Sula leucogaster r r) at a small tropical archipelago Felipe Machado Neves, Patrícia Luciano Mancini, Fernanda Pinto Marques, Guilherme Tavares Nunes, and Leandro Bugoni contribute only a marginal increment to the breeding established by the Brazilian Navy, may be influencing this success of the Nazca Booby, and Humphries et al. (2006) behavior. Since then, the island has been permanently did not observe family members consuming chicks inhabited by small groups of researchers and mariners because the similar size of siblings precludes such behavior. (usually four). Additionally, researchers, sailors and At SPSPA, most cannibalistic birds were females, and in fishermen often feed boobies left-over fish parts, and one instance (trial 1), the male offered the dead chick to individuals with a propensity for cannibalistic behavior the female, in line with the food deprivation hypothesis, may have interpreted the dead chicks thrown close to which could help offset energetic costs of egg production. the nests (our trials) as a food off er by humans, despite Th e exceptions were the two spontaneous cannibalism this does not explain the spontaneous cannibalism events recorded in July 2015, when males swallowed events reported. In summary, explanations for the chicks, which suggests that this hypothesis does not natural cannibalism reported previously, as well as our explain all cannibalistic events at SPSPA. ‘unnatural’ trials, which result in cannibalistic attempts, Furthermore, cannibalism may be a density- remain elusive, and further experimental studies should dependent behavior (Fox 1975, Nishimura 2010). At be carried out to address why Brown Boobies from this high nest densities, egg cannibalism and social stress area differ from s ulids elsewhere. increase in gulls (Burger 1980, Brouwer & Spaans 1994), and disputes over territories are frequent in ACKNOWLEDGMENTS booby colonies (Alves et alll. 2004, Nelson 2005). The SPSPA Brown Booby population increased from 334 We thank the Brazilian Navy and Comissão Interministerial birds in 2000-2001 (Barbosa-Filho & Vooren 2010) to para os Recursos do Mar r (CIRM/SECIRM) for logistic 588 birds in 2011-2014 (Neves et alll. 2013, Mancini support for the SPSPA expeditions, the Brazilian et alll. unpublished data) and no emigration has been Research Council (CNPq - Grant No. 557152/2009-7 documented (Barbosa-Filho & Vooren 2010). In this and 405497/2012-1) for funding the project. P.L.M. colony there is an average distance between nests of acknowledges CAPES Foundation for providing grants 1 m, while in the Rocas Atoll, northeastern Brazil, for (No. 9733/2011-6). L.B. is a research fellow from the instance, nests are 11 m apart on average (Kohlrausch Brazilian CNPq (Proc. No. 308697/2012-0). Authors are 2003). Furthermore, average nest diameter of SPSPA is also grateful to L. C. Naves and R. H. Macedo for a critical ~20% smaller than Rocas Atoll nests (Kohlrausch 2003). revision and insightful comments on an earlier version. Some additional observations of the authors on the Brown Boobies at SPSPA also suggest space limitation. Fights over territory in the nest surroundings are intense REFERENCES and common, resulting in injured adults or chick death. Furthermore, boobies frequently establish nests in low, Alexander, R. D. 1974. Th e evolution of social behaviour. Annual marginal areas, close to the area of wave action, i.e., low Review of Ecology, Evolution and Systematics, 5: 325-383. quality areas with reduced breeding success. In both Alves, V. S.; Soares, A. B. A. & Couto, G. S. 2004. Aves marinhas spontaneous events reported here, cannibalized chicks e aquáticas das ilhas do litoral do Rio de Janeiro, p. 83-100. In: Branco, J. O. (Ed.). Aves marinhas e insulares brasileiras: bioecologia belonged to nests adjacent to cannibals. All this suggests e conservação. 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Journal

Ornithology Research – Springer Journals

Published: Sep 1, 2015

Keywords: chick mortality; opportunistic feeding; Saint Peter and Saint Paul Archipelago; seabirds; Sulidae

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