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Predation of Greater Crested Tern (Thalasseus bergii) Eggs byJuvenile Brown Boobies (Sula leucogaster) on Ashmore ReefAuthor(s): Jennifer L. Lavers, Ashley Herrod and Rohan H. ClarkeSource: Waterbirds, 37(2):215-219. 2014.Published By: The Waterbird SocietyDOI: http://dx.doi.org/10.1675/063.037.0210URL: http://www.bioone.org/doi/full/10.1675/063.037.0210

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215

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; E-mail: 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 14-20 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 Boo-bies 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 2014.

Key words.—Brown Booby, egg predation, Greater Crested Tern, interspecific kleptoparasitism, Sula leucogaster, Thalasseus bergii.

Waterbirds 37(2): 215-219, 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 fre-quency of feeding events is reduced (Sim-mons 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 occasion-ally resort to kleptoparasitising (stealing food from) frigatebirds (Fregata sp.) or other boo-bies by intercepting adult birds when they are feeding their own chicks (Nelson 1978; Sch-reiber 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.

METHODS

Study Area

Ashmore Reef Commonwealth Marine Reserve (12° 20' S, 123° 00' 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 breed-ing at Ashmore Reef with a count of 6,085 pairs breed-ing in April 2013 (Clarke and Herrod 2013a). Two small colonies of Crested Terns have been recorded breed-ing 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 2010-2012). These colonies are invariably adjacent to breed-ing 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 13-19 November 2013. Targeted observations were undertaken on 20 November 2013 dur-ing 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.

216 WATERBIRDS

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 14-20 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

present on 14 November, no chicks were re-corded from 16-20 November. Daily circum-navigating of the shoreline on foot, com-bined with seabird surveys on land, did not reveal any Crested Tern chicks (which form crèches along the shoreline; Davies and Car-rick 1962), leading us to conclude that the chicks had been depredated.

Two juvenile Brown Boobies were regu-larly observed along the periphery of the Crested Tern colony from 18-20 November 2013. The adult Crested Terns became agi-tated 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 ap-proaching the Crested Tern colony. Those Crested Terns nearest to the Brown Boo-

Figure 1. Map showing the location of Middle Island, Ashmore Reef, Western Australia (W.A.).

Table 1. Number of adult Greater Crested Terns in at-tendance at the breeding colony and nest contents be-tween 14-20 November 2013, Middle Island, Ashmore Reef.

Date Adults in Colony Contents of Nests

14 Nov 2013 128Eggs and “day-old” chicks

16 Nov 2013 Not recorded Eggs18 Nov 2013 90 Eggs20 Nov 2013 59 Eggs

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 re-gurgitated 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. Dur-ing 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 ad-ditional eggs were consumed. The behavior of the Brown Boobies following 20 Novem-ber and the fate of the remaining Crested Tern eggs are not known. This behavior was not observed during three previous Novem-ber seabird surveys (2010-2012) on Middle Island.

DISCUSSION

Juvenile Brown Boobies on Middle Is-land, Ashmore Reef, were recorded depre-dating Crested Tern eggs and kleptoparasi-tising 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 day-old chicks from the island soon after hatch-ing, 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 inter-presl; Smith 1986), were not observed inter-

acting with the Crested Tern colony, preda-tion 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 Ash-more Reef reported here are uncertain. Ma-ture aged Brown Booby chicks (some down remaining on neck and flanks) were record-ed on Middle Island on 26 August 2013 (R. Mott, pers. commun.), which suggests the juvenile Brown Boobies in fresh plumage in-teracting with Crested Terns on 20 Novem-ber 2013 were in the late post-fledgling pe-riod. The length of the post-fledging feeding stage is thought to be influenced by the indi-vidual 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 vari-able 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 Admin-istration 2013). Hunger and perhaps curios-ity 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 pres-ent on Middle Island were underweight, as similarly aged juvenile Brown Boobies on As-cension Island and Gorgona Island weighed 973 ± 127 g (107-133 days old; n = 6) and 1,162 ± 150 g (91-95 days old; n = 4), respec-tively (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 pa-rental abandonment. Alternatively, given their late post-fledging development stage,

218 WATERBIRDS

they may have been supplementing dwin-dling parental food provisions. Whatever the cause, the behavior contributed to dis-turbance and mortality of the Crested Terns.

Common Terns (Sterna hirundo) have aban-doned breeding attempts on islands due to predation by mink (Mustela vison) and Short-eared Owls (Asio flammeus), with breeding

Figure 2. Juvenile Brown Booby ingesting (A) harlequin snake eel regurgitated by an adult Greater Crested Tern and (B) Greater Crested Tern egg.

BROWN BOOBY PREDATION OF TERN EGGS 219

attempts shifted to new or existing colonies elsewhere (Holt 1994; Craik 1997). It is in-teresting to speculate as to whether the be-havior of juvenile Brown Boobies will be repeated throughout the adult life of these individuals, and, if so, if other Brown Boo-bies will learn this behavior. Such a behavior-al 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-COM2012-138). Re-search 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 re-viewers for providing comments on earlier drafts of the manuscript.

LITERATURE CITED

Brooke, M. 2004. Albatrosses and petrels across the world. Oxford University Press, Oxford, U.K.

Clarke, R. H. 2011. Seabirds and shorebirds at Ash-more Reef and Cartier and Browse Islands: moni-toring program for the Montara Well release. Third post-impact field survey: unpublished prog-ress report May 2011. Department of the Environ-ment, Water, Heritage and the Arts, Melbourne, Australia.

Clarke, R. H. and A. Herrod. 2013a. Seabirds and shore-birds at Ashmore Reef, Cartier Island and Browse Island. Monitoring program for the Montara Well release. Seventh post impact survey: unpublished progress report May 2013. Monash University, Mel-bourne, Australia.

Clarke, R. H. and A. Herrod. 2013b. Seabirds and shore-birds at Ashmore Reef, Cartier Island and Browse Island. Monitoring program for the Montara Well release. Eighth post-impact survey: unpublished progress report December 2013. Monash University, Melbourne, Australia.

Clarke, R. H., M. J. Carter, G. Swann and J. Thomson. 2011. The status of breeding seabirds and herons at Ashmore Reef, off the Kimberley coast, Australia. Journal of the Royal Society of Western Australia 94: 365-376.

Craik, C. 1997. Long-term effects of North American mink Mustela vison on seabirds in western Scotland. Bird Study 44: 303-309.

Davies, S. and R. Carrick. 1962. On the ability of Crested Terns, Sterna bergii, to recognize their own chicks. Australian Journal of Zoology 10: 171-177.

Dorward, D. F. 1962. Comparative biology of the White Booby and the Brown Booby Sula spp. at Ascension. Ibis 103b: 174-220.

Guo, H., L. Cao, L. Peng, G. Zhao and S. Tang. 2010. Parental care, development of foraging skills, and transition to independence in the Red-Footed Boo-by. Condor 112: 38-47.

Harper, A. B. 1986. The evolution of begging: sibling competition and parent-offspring conflict. Ameri-can Naturalist 128: 99-114.

Hindwood, K. A. 1946. The stomach contents of young mutton-birds. Emu 46: 71-73.

Holt, D. W. 1994. Effects of Short-Eared Owls on Com-mon Tern colony desertion, reproduction, and mor-tality. Colonial Waterbirds 17: 1-6.

Jahncke, J. and E. Goya. 2000. Responses of three Booby species to El Niño 1997-1998. Waterbirds 23: 102-108.

Le Souef, W. H. D. 1922. Nankeen Night-Herons and young ducks. Emu 21: 312-313.

Massaro, M., J. W. Chardine, I. L. Jones and G. J. Robert-son. 2000. Delayed capelin (Mallotus villosus) avail-ability influences predatory behaviour of large gulls on Black-legged Kittiwakes (Rissa tridactyla), causing a reduction in kittiwake breeding success. Canadian Journal of Zoology 78: 1588-1596.

National Oceanic and Atmospheric Administration. 2013. Forecast forum: December 2013. Climate Diagnostics Bulletin. National Oceanic and Atmo-spheric Administration, Silver Spring, Maryland.

Nelson, J. B. 1978. The Gannet. Buteo Books, Vermil-lion, South Dakota.

Ospina-Álvarez, A. 2014. Breeding ecology of Brown Booby in Gorgona Island, eastern tropical Pacific Ocean. Notornis 61: 10-18.

Recher, H. F. and J. A. Recher. 1972. The foraging be-haviour of the Reef Heron. Emu 72: 85-90.

Schreiber, E. A. and R. L. Norton. 2002. Brown Booby (Sula leucogaster). No. 649 in The Birds of North America Online (A. Poole, Ed.). Cornell Lab of Or-nithology, Ithaca, New York. http://bna.birds.cor-nell.edu/bna/species/649/articles/introduction, accessed 3 September 2013.

Simmons, K. E. L. 1967. Ecological adaptations in the life history of the Brown Booby at Ascension Island. Living Bird 6: 187-212.

Smith, G. C. 1986. Eagle Island, Great Barrier Reef, Queensland. Seabird Islands Series No. 161. Corella 10: 81-83.

Stenhouse, I. J. and W. A. Montevecchi. 1999. Indirect effects of the availability of capelin and fishery dis-cards: gull predation on breeding storm-petrels. Ma-rine Ecology Progress Series 184: 303-307.

van Bemmel, A. C. V. and A. Hoogerwerf. 1940. The birds of Goenoeng Api. Treubia Deel 17: 421-472.