Seabird surveys of globally important populations in the British Virgin Islands

The British Virgin Islands is home to two globally important and eight regionally important populations of breeding seabirds, distributed across the 60 islands that make up the territory. Here, we re-survey key sites within the islands to assess breeding numbers of the globally important Magnificent Frigatebird ( Fregata magnificens ) and Roseate Tern ( Sterna dougallii ) populations. Our 2013–2014 surveys suggest that both these populations have declined since 1995, with the Roseate Tern population showing the steepest declines. We identify potential threats facing these populations, including those from invasive species and entanglement with fishing line. This study highlights the need for regular, systematic seabird surveys across the territory and the neighboring territories of the U.S. Virgin Islands and Puerto Rico, to ensure any population declines or threats facing populations are identified, and appropriate conservation management practices implemented.

populations (Table 1).At its closest point, the BVI is less than 5 km away from the United States Virgin Islands (USVI), which consists of 50 islands.Despite political separation, the islands share similar biogeography, and the local foraging ranges of many BVI seabird species and other marine species likely span both BVI and USVI territorial waters.The last complete seabird survey for the BVI was conducted in 2004-2005(McGowan et al. 2006)), and reported globally significant populations of Magnificent Frigatebirds (Fregata magnificens) and Roseate Terns (Sterna dougallii), in addition to eight regionally significant populations.The BVI has three designated Important Bird Areas (IBAs; Wege and Anadón-Irizarry 2008), of which Green Cay and Great Tobago were designated primarily for breeding colonies of Roseate Terns and Magnificent Frigatebirds, respectively.
Magnificent Frigatebirds are distributed on the Pacific and Atlantic coasts of the Americas, from California (USA) to Ecuador (including the Galapagos), and from Florida to southern Brazil (BirdLife International 2018a).The BVI colony represents one of the largest in the Caribbean region, and the only colony within the Virgin Islands.Roseate Terns are present on all continents except Antarctica (BirdLife International 2018b), however they have declined in many regions.In 1987, Roseate Terns were listed as Endangered in the USA and are currently red-listed in the UK after suffering the greatest population decline of any seabird species between 1970 and 1988 (Mitchell et al. 2004).It is therefore of particular importance for the BVI to effectively monitor these globally important populations.
Seabirds typically exhibit a high degree of breeding site fidelity, returning to the same colony year after year (González-Solís et al. 1999, Zador et al. 2009, Gauthier et al. 2010, Braby et al. 2012).However, environmental conditions such as food supply, disturbance, and predation can cause abandonment of breeding sites, particularly for smaller seabird species which are more vulnerable to effects of predation and disturbance (Crawford 2003).Despite suitable breeding habitat being available on other cays within the BVI, Great Tobago is the only cay to support a breeding colony of Magnificent Frigatebirds, indicating high breeding site fidelity for this species.Likewise, breeding site fidelity for over 30 yr has been demonstrated for Roseate Terns in the USA and Europe (Burger et al. 1996, Mavor et al. 2008).However, the Caribbean Roseate Tern populations are reported to be less con-sistent in their breeding site selection.Movement of color-banded birds among three key breeding areas in Puerto Rico and the USVI ranged from 2% to 50% over 3 yr (Shealer et al. 2005).In addition, two color-banded Roseate Terns which bred in the USVI in 1993 bred in the BVI in 1994 (Saliva and Pierce 1996).Roseate Terns have been reported breeding at 12 different cays in the BVI since 1976, making regular surveys of this species a large undertaking.
Here, we review previous information on the breeding populations of Magnificent Frigatebirds and Roseate Terns in the BVI, and compare with survey data collected during 2013 and 2014.We also present data on the status of other summer breeding seabirds, and present a review of the threats facing the BVI's seabirds.

Magnificent Frigatebirds
Two complete colony counts of Magnificent Frigatebirds were conducted on Great Tobago (18°26'45"N, 64°49'30"W) during 2013 and 2014.Magnificent Frigatebirds on Great Tobago nest on the crowns of trees and bushes, primarily in a few large stands of seagrape (Coccoloba uvifera) trees.In recent years, birds have begun nesting on the slopes on the outer edges of the colony in loblolly (mapoo) trees (Pisonia subcordata), and even in a few prickly pear tree cacti (Opuntia rubescens).On 10 April 2013, active nests were counted by moving systematically through the colony counting active nests in each individual tree.
A second count was undertaken on 27 January 2014 by taking photographs of the colony from a high vantage point in the middle of the island and counting incubating adults and chicks by examining the photographs using Microsoft Office Picture Manager software (Microsoft, Redmond, WA, USA).

Roseate Terns and Other Summer Breeding Seabirds
Twenty islands within the BVI were surveyed from 10 to 22 June 2014 by Jost Van Dykes Preservation Society (JVDPS) staff and volunteers from their sailing and education vessel Endeavour II.All sites with previous breeding records of Roseate Tern were surveyed (with the exception of Guana Island and Virgin Gorda).In many cases, the small rocks and cays of the BVI have no suitable landing points, and so islands were circumnavigated by sailing boat or dingy to check for breeding activity.In addition to recording Roseate Terns, the presence of Laughing Gulls (Leucophaeus atricilla), Brown Noddies (Anous stolidus), Bridled Terns (Onychoprion anaethetus), and Sandwich Terns (Thalasseus sandvicensis) was also recorded.As surveys could not be conducted by foot, it was not possible to record actual breeding numbers.Instead, we recorded the presence of seabirds as either (1) breeding (adults flying up from or landing in the vegetation, adults carrying fish into the colony, or protective display behavior at the colony); (2) likely breeding (birds flying from the ground or cliff faces but breeding not confirmed); or (3) present (no signs of breeding observed).
In addition to seabird surveys on board Endeavour II, the IBA of Green Cay was surveyed on foot on 10 June 2014.Roseate Tern nests were located, but a total count was not made in an attempt to minimize disturbance to the breeding site.

Tropicbirds
Red-billed Tropicbirds (Phaethon aethereus) and White-tailed Tropicbirds (P.lepturus) were also recorded during these summer seabird surveys, although peak breeding for these species occurs during the winter months.

Previous Survey Data
Previous survey data for Magnificent Frigatebirds and Roseate Terns were compiled to allow comparisons with this survey.Two previous studies reported the number of breeding Magnificent Frigatebirds on Great Tobago in 1995, 2004, and 2005(McGowan et al. 2006, Wege and Anadón-Irizarry 2008).Past Roseate Tern data were compiled by JP, who coordinated annual Roseate Tern counts in the BVI between 1993 and 2003.These counts were undertaken by circumnavigation of cays by boat with the exception of the more accessible islands (Cockroach, Seal Dogs, and Green Cay) where direct nest counts were undertaken.In addition, McGowan et al. (2006) recorded Roseate Tern numbers in surveys undertaken between 2004 and 2005.

Results
A total of 903 breeding pairs of Magnificent Frigatebirds were recorded in 2013, and 925 breeding pairs in 2014.This represents a decline from the 3,000 breeding pairs reported in 1995 (Table 2), but is higher than numbers recorded in 2004-2005, and still qualifies as a globally important population (Wege and Anadón-Irizarry 2008).
Three Roseate Tern breeding sites were recorded during the 2014 surveys: Green Cay, West Seal Dog, and Broken Jerusalem (Table 3).All sites had been previously used by Roseate Terns, although breeding had not been reported on Broken Jerusalem since 2005 (Table 4).On the 10 June visit to Green Cay, the majority of nests located contained two eggs.We estimated 50-200 adults breeding at each of the three colonies (Table 4).Data on the presence of other summer breeding seabird species and tropicbirds are shown in Table 3.

Discussion
While infrequency in survey data may prevent the detection of all population trends, it appears that since the early 1990s the two globally important breeding seabird populations in the BVI have declined significantly in number.

Magnificent Frigatebirds
Magnificent Frigatebird numbers declined from c. 3,000 pairs in 1995 to 500 pairs in 2005, but have since increased to 903 pairs in 2013 and 925 pairs in 2014 (Table 2).While the decline since 1995 may be attributable to differences in count method, incompleteness of survey, or the time of year the count was undertaken (Ratcliffe et al. 2008), the decline could equally be due to reduction in nesting habitat due to the presence of goats (Capra aegagrus hircus) on the island and also to a landslide X which occurred in July 2011 (caused by overgrazing leading to erosion) which destroyed the seagrape trees and a number of nests within a section of the colony.(Campbell and Donlan 2005).Entanglement with fishing line has also been identified to be a major threat for this breeding colony, with 60 birds found dead at the breeding colony in 2012 either entangled with fishing line in the vegetation or found with hooks and line in their throats (SZ pers.obs.).

Restoring and Protecting Seabird Populations
There are many examples of successful restoration programs for seabirds, which include measures such as prevention of human disturbance, predator removal, provision of nest shelters to reduce predation by aerial predators, and restoration of natural vegetation (Avery et al. 1995, Jones andKress 2012).Indeed the BVI Government, BVI National Parks Trust, and JVDPS, in collaboration with global partners, have already conducted a successful rat eradication program on Sandy Cay, and are in the process of eradicating feral goats from Great Tobago, as well as producing feasibility studies for the eradication of rats from Great Toba-go and Green Cay.In addition to these efforts, other cays should be prioritized for seabird restoration work, and measures such as artificial nest boxes, decoys, and call-playback may be useful to encourage re-establishment of populations once predators have been removed.
An education program is already underway to reduce negative interactions with fisheries (coordinated by JVDPS), both for local and visiting fishers, to inform them of the measures they should take if a seabird is caught by hook and line.Further investigation of appropriate measures that can be taken, e.g., fast sinking lures and bird scarers on lines, should also be investigated (Bull 2007, Bugoni et al. 2008).
However, the immediate priority for seabird conservation in the BVI is to establish a long-term monitoring plan for seabirds to ensure complete and systematic surveys are conducted regularly.Cross territorial surveying is also encouraged; both measures will allow for a better understanding of seabird population trends and provide valuable information to address any observed declines and inform conservation measures.

Fig. 1 .
Fig. 1.Location of the British Virgin Islands relative to the U.S. Virgin Islands and Puerto Rico (map produced in ArcMap 10.0 [Esri, Redlands, CA, USA]).
b McGowan et al. (2006) c This study