Predation of Greater Crested Tern (Thalasseus bergii) Eggs by Juvenile Brown Boobies (Sula leucogaster) on Ashmore Reef

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1 Predation of Greater Crested Tern (Thalasseus bergii) Eggs by Juvenile Brown Boobies (Sula leucogaster) on Ashmore Reef Author(s): Jennifer L. Lavers, Ashley Herrod and Rohan H. Clarke Source: Waterbirds, 37(2): Published By: The Waterbird Society DOI: URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and noncommercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 Predation of Greater Crested Tern (Thalasseus bergii ) Eggs by Juvenile Brown Boobies (Sula leucogaster ) on Ashmore Reef JENNIFER L. LAVERS *, ASHLEY HERROD AND ROHAN H. CLARKE School of Biological Sciences, Monash University, Building 17, Clayton, Victoria, 3800, Australia * Corresponding author; Jennifer.Lavers@monash.edu Abstract. As young seabirds approach independence, a range of tactics are sometimes employed in an attempt to secure additional food items prior to departing the nest. Detailed here are previously unreported kleptoparasitic and predatory behaviors of juvenile Brown Boobies (Sula leucogaster) on Ashmore Reef in the Timor Sea. From November 2013, the number of Greater Crested Terns (Thalasseus bergii) breeding adjacent to a Brown Booby colony was reduced from 128 adults attending the colony to 59 adults. During this time, two juvenile Brown Boobies were observed depredating the eggs of the Greater Crested Terns and ingesting prey regurgitated by Greater Crested Terns. The factors that lead to this unusual foraging behavior in juvenile Brown Boobies are not known; however, low body mass and hunger may play a role. Repeated years of predation of Greater Crested Tern eggs by Brown Boobies could lead to the abandonment of this colony. Received 2 February 2014, accepted 28 February Key words. Brown Booby, egg predation, Greater Crested Tern, interspecific kleptoparasitism, Sula leucogaster, Thalasseus bergii. Waterbirds 37(2): , 2014 Due to the significant time and energy required to raise a chick (up to 10 months), most seabird species produce only one offspring annually (Brooke 2004). In the Sulidae (gannets and boobies), the chick fledges (leaves the nest but remains on the island) after ~100 days (Nelson 1978; Guo et al. 2010). Juvenile boobies (Sula sp.) return to the nest site for many weeks to be fed by their parents, but as the adults prepare for the next breeding season and encourage their chicks to seek independence, the frequency of feeding events is reduced (Simmons 1967; Nelson 1978; Guo et al. 2010). Fledglings respond to growing hunger by increasing their begging effort (Harper 1986; Schreiber and Norton 2002). Young boobies also attempt to obtain their own food by foraging in waters adjacent to their nesting islands, though like many seabirds they are less successful at catching prey than adults (van Bemmel and Hoogerwerf 1940; Guo et al. 2010). Juvenile boobies will also occasionally resort to kleptoparasitising (stealing food from) frigatebirds (Fregata sp.) or other boobies by intercepting adult birds when they are feeding their own chicks (Nelson 1978; Schreiber and Norton 2002). Predation by adult seabirds (especially the Laridae) on eggs and chicks of other seabird species is frequently reported, often in relation to reduced prey availability (Stenhouse and Montevecchi 1999; Massaro et al. 2000). Here, we report the occurrence of juvenile Brown Boobies (Sula leucogaster) in the post-fledgling stage depredating the eggs of Greater Crested Terns (Thalasseus bergii; hereafter Crested Terns) and eating their regurgitated prey on Ashmore Reef in the Timor Sea. Study Area METHODS Ashmore Reef Commonwealth Marine Reserve (12 20' S, ' E) is located approximately 630 km north of Broome, Western Australia, and is home to some of the most important seabird rookeries on the North West Shelf (Fig. 1; Clarke et al. 2011). The Brown Booby is the most abundant of three species of Sulidae breeding at Ashmore Reef with a count of 6,085 pairs breeding in April 2013 (Clarke and Herrod 2013a). Two small colonies of Crested Terns have been recorded breeding on areas of bare sand on Middle Island, Ashmore Reef, each November between 2010 and 2013 (total for both colonies: 382 ± 130 adults in the period ). These colonies are invariably adjacent to breeding Brown Boobies, which nest over much of the island (Clarke and Herrod 2013b). Observations Interactions between juvenile Brown Boobies and Crested Terns were observed opportunistically during seabird surveys (visual counts using spotting scopes) on Middle Island during November Targeted observations were undertaken on 20 November 2013 during which the behavior of the birds along with any items ingested were recorded and photographed with a digital camera from a distance of approximately 15 m. 215

3 216 WATERBIRDS Figure 1. Map showing the location of Middle Island, Ashmore Reef, Western Australia (W.A.). RESULTS On 14 November 2013, the Crested Tern breeding colony located at the southeastern end of Middle Island contained 128 adult birds attending nests that were occupied by either an egg or chick. Chicks were 1-2 days old. Between November 2013, the number of adults at the breeding colony declined from 128 adults to only 59 adults (Table 1). Although day-old chicks were Table 1. Number of adult Greater Crested Terns in attendance at the breeding colony and nest contents between November 2013, Middle Island, Ashmore Reef. Date Adults in Colony Contents of Nests 14 Nov Eggs and day-old chicks 16 Nov 2013 Not recorded Eggs 18 Nov Eggs 20 Nov Eggs present on 14 November, no chicks were recorded from November. Daily circumnavigating of the shoreline on foot, combined with seabird surveys on land, did not reveal any Crested Tern chicks (which form crèches along the shoreline; Davies and Carrick 1962), leading us to conclude that the chicks had been depredated. Two juvenile Brown Boobies were regularly observed along the periphery of the Crested Tern colony from November The adult Crested Terns became agitated when Brown Boobies approached and would vocalize and briefly take flight. As the boobies were not banded, it is not clear whether the same individuals were recorded on subsequent days although we suspect this to be the case. At 8:00 am on 20 November 2013, two juvenile Brown Boobies were observed approaching the Crested Tern colony. Those Crested Terns nearest to the Brown Boo-

4 BROWN BOOBY PREDATION OF TERN EGGS 217 bies left their nests, taking flight, and flying in an agitated manner above the nesting colony. Prior to flying, one Crested Tern regurgitated a harlequin snake eel (Myrichthys colubrinus), which was ingested by one of the Brown Boobies (Fig. 2a). This Brown Booby then moved further into the Crested Tern colony, and, while amongst the incubating terns, it punctured a Crested Tern egg with its beak before swallowing the egg. This was repeated with an egg from another nest (Fig. 2b). The behavior of the Brown Boobies was documented for another 30 min. During this time, both juvenile Brown Boobies remained in close proximity to the Crested Tern colony, occasionally charging into the colony to flush the Crested Terns, but no additional eggs were consumed. The behavior of the Brown Boobies following 20 November and the fate of the remaining Crested Tern eggs are not known. This behavior was not observed during three previous November seabird surveys ( ) on Middle Island. DISCUSSION Juvenile Brown Boobies on Middle Island, Ashmore Reef, were recorded depredating Crested Tern eggs and kleptoparasitising an adult Crested Tern in November 2013, behavior that has not been reported in other Sulid colonies and was not recorded during three prior trips to Ashmore Reef at the same time of year. Brown Boobies were not observed depredating Crested Tern chicks; however, the disappearance of dayold chicks from the island soon after hatching, in tandem with the behavior displayed by the Brown Boobies, suggests the Crested Tern chicks may have been depredated by the juvenile Brown Boobies. Gulls (Larus sp.) are absent from Ashmore Reef (Clarke 2011). While other reported predators of waterbird young present on Ashmore Reef, such as the Eastern Reef Egret (Ardea sacra; Recher and Recher 1972), Nankeen Night- Heron (Nycticorax caledonicus; Le Souef 1922) and Ruddy Turnstone (Arenaria interpresl; Smith 1986), were not observed interacting with the Crested Tern colony, predation by these species cannot be excluded as a possible cause of the disappearance of some Crested Tern eggs and chicks. The factors driving the unusual foraging behavior of juvenile Brown Boobies on Ashmore Reef reported here are uncertain. Mature aged Brown Booby chicks (some down remaining on neck and flanks) were recorded on Middle Island on 26 August 2013 (R. Mott, pers. commun.), which suggests the juvenile Brown Boobies in fresh plumage interacting with Crested Terns on 20 November 2013 were in the late post-fledgling period. The length of the post-fledging feeding stage is thought to be influenced by the individual abilities of chicks to secure food from their parents, as well as the ability of the parents to provision their chicks with food (i.e., prey availability; Schreiber and Norton 2002). Changes in environmental conditions (e.g., El Niño events) have led to reduced Brown Booby productivity and more variable diet (Simmons 1967; Jahncke and Goya 2000; Schreiber and Norton 2002), and could also contribute to altered behavior, though no such event was recorded in 2013 (National Oceanic and Atmospheric Administration 2013). Hunger and perhaps curiosity drive some juvenile seabirds, including Brown Boobies, to consume unusual items such as vegetation (Hindwood 1946; J. L. Lavers, pers. obs.). The body condition of the two juvenile Brown Boobies involved in the Crested Tern interactions is not known. While measurement data are only available for a single individual, the mass of a juvenile Brown Booby from the same cohort (467 g) suggests at least some of the juveniles present on Middle Island were underweight, as similarly aged juvenile Brown Boobies on Ascension Island and Gorgona Island weighed 973 ± 127 g ( days old; n = 6) and 1,162 ± 150 g (91-95 days old; n = 4), respectively (Dorward 1962; Ospina-Álvarez 2014). The juvenile Brown Boobies that were observed ingesting Crested Tern eggs and regurgitated Crested Tern prey may have been driven by hunger caused by early parental abandonment. Alternatively, given their late post-fledging development stage,

5 218 WATERBIRDS Figure 2. Juvenile Brown Booby ingesting (A) harlequin snake eel regurgitated by an adult Greater Crested Tern and (B) Greater Crested Tern egg. they may have been supplementing dwindling parental food provisions. Whatever the cause, the behavior contributed to disturbance and mortality of the Crested Terns. Common Terns (Sterna hirundo) have abandoned breeding attempts on islands due to predation by mink (Mustela vison) and Shorteared Owls (Asio flammeus), with breeding

6 BROWN BOOBY PREDATION OF TERN EGGS 219 attempts shifted to new or existing colonies elsewhere (Holt 1994; Craik 1997). It is interesting to speculate as to whether the behavior of juvenile Brown Boobies will be repeated throughout the adult life of these individuals, and, if so, if other Brown Boobies will learn this behavior. Such a behavioral shift could conceivably lead to the failure of future Crested Tern breeding events on Middle Island. ACKNOWLEDGMENTS Parks Australia granted permission for our work on Ashmore Reef (Permit No. AU-COM ). Research was undertaken with approval from the Monash University Animal Ethics Committee (Permit No. BSCI/2012/21). We thank Diversity Charter Company, M. Carter, R. Mott, and G. Swann for assistance with surveys and A. Bond, J. Coffey, and two anonymous reviewers for providing comments on earlier drafts of the manuscript. LITERATURE CITED Brooke, M Albatrosses and petrels across the world. Oxford University Press, Oxford, U.K. Clarke, R. H Seabirds and shorebirds at Ashmore Reef and Cartier and Browse Islands: monitoring program for the Montara Well release. Third post-impact field survey: unpublished progress report May Department of the Environment, Water, Heritage and the Arts, Melbourne, Australia. Clarke, R. H. and A. Herrod. 2013a. Seabirds and shorebirds at Ashmore Reef, Cartier Island and Browse Island. Monitoring program for the Montara Well release. Seventh post impact survey: unpublished progress report May Monash University, Melbourne, Australia. Clarke, R. H. and A. Herrod. 2013b. Seabirds and shorebirds at Ashmore Reef, Cartier Island and Browse Island. Monitoring program for the Montara Well release. Eighth post-impact survey: unpublished progress report December Monash University, Melbourne, Australia. Clarke, R. H., M. J. Carter, G. Swann and J. Thomson The status of breeding seabirds and herons at Ashmore Reef, off the Kimberley coast, Australia. Journal of the Royal Society of Western Australia 94: Craik, C Long-term effects of North American mink Mustela vison on seabirds in western Scotland. Bird Study 44: Davies, S. and R. Carrick On the ability of Crested Terns, Sterna bergii, to recognize their own chicks. Australian Journal of Zoology 10: Dorward, D. F Comparative biology of the White Booby and the Brown Booby Sula spp. at Ascension. Ibis 103b: Guo, H., L. Cao, L. Peng, G. Zhao and S. Tang Parental care, development of foraging skills, and transition to independence in the Red-Footed Booby. Condor 112: Harper, A. B The evolution of begging: sibling competition and parent-offspring conflict. American Naturalist 128: Hindwood, K. A The stomach contents of young mutton-birds. Emu 46: Holt, D. W Effects of Short-Eared Owls on Common Tern colony desertion, reproduction, and mortality. Colonial Waterbirds 17: 1-6. Jahncke, J. and E. Goya Responses of three Booby species to El Niño Waterbirds 23: Le Souef, W. H. D Nankeen Night-Herons and young ducks. Emu 21: Massaro, M., J. W. Chardine, I. L. Jones and G. J. Robertson Delayed capelin (Mallotus villosus) availability influences predatory behaviour of large gulls on Black-legged Kittiwakes (Rissa tridactyla), causing a reduction in kittiwake breeding success. Canadian Journal of Zoology 78: National Oceanic and Atmospheric Administration Forecast forum: December Climate Diagnostics Bulletin. National Oceanic and Atmospheric Administration, Silver Spring, Maryland. Nelson, J. B The Gannet. Buteo Books, Vermillion, South Dakota. Ospina-Álvarez, A Breeding ecology of Brown Booby in Gorgona Island, eastern tropical Pacific Ocean. Notornis 61: Recher, H. F. and J. A. Recher The foraging behaviour of the Reef Heron. Emu 72: Schreiber, E. A. and R. L. Norton Brown Booby (Sula leucogaster). No. 649 in The Birds of North America Online (A. Poole, Ed.). Cornell Lab of Ornithology, Ithaca, New York. accessed 3 September Simmons, K. E. L Ecological adaptations in the life history of the Brown Booby at Ascension Island. Living Bird 6: Smith, G. C Eagle Island, Great Barrier Reef, Queensland. Seabird Islands Series No Corella 10: Stenhouse, I. J. and W. A. Montevecchi Indirect effects of the availability of capelin and fishery discards: gull predation on breeding storm-petrels. Marine Ecology Progress Series 184: van Bemmel, A. C. V. and A. Hoogerwerf The birds of Goenoeng Api. Treubia Deel 17: