4. DISCUSSION

Through our observations at sea in the Chagos Archipelago we have identified spatio-temporal trends in seabird distribution. Our multiyear survey spanned a broad range of environmental conditions and has enabled us to identify geomorphic and oceanographic conditions driving seabird distribution, including a possible association between regional abundance and the IO Dipole oscillation.  Accounting for unbalanced sampling effort, we have identified seabird hotspots within the BIOT MPA, complementing previous investigations in the southwest and southern IO (Mannocci, Laran, et al., 2014; Hyrenbach et al., 2007). We have modelled the spatially explicit impact of islands with and without rats on seabird distribution, and have identified areas of net increase in abundance under an archipelago-wide rat eradication scenario. Information on seabird hotspots, sensitivity to climate oscillation, and how eradication can result in distribution shifts has critical implications for tropical seabird conservation and for island restoration strategies.

4.1 Drivers of seabird distribution within the Chagos Archipelago

The distribution of the Laridae, dominated by the brown noddy, was strongly related to depth and chlorophyll-a, with modelled abundance concentrated around islands, and over shallow water (<100 m). Laridae in the Chagos Archipelago have previously been observed to be mostly lagoonal foragers (Carr, pers. comm), consistent with their modelled distribution here. Our results are also consistent with previous observations of the brown noddy and lesser noddy leaving and returning to islands during the same day in the breeding season, suggesting they are not long-distance or multiday foragers (Surman, Nicholson, & Ayling, 2017; Jaquemet, Le Corre, & Weimerskirch, 2004). In line with theoretical expectations due to their small size (Harper & Bunbury, 2015), the Laridae were the group most sensitive to rats, resulting in elevated abundance near rat-free islands.
The Sulidae showed a primarily oceanic distribution, with pronounced hotspots east of the Diego Garcia and west of the Peros Banhos atolls, and along the Lakshadweep-Maldives-Chagos ridge. Sulidae distribution has traditionally been thought to be positively associated with areas of high productivity and elevated chl-a concentration (Ballance, Pitman, & Reilly, 1997; Jaquemet, Le Corre, Marsac, Potier, & Weimerskirch, 2005; Weimerskirch, Le Corre, Jaquemet, & Marsac, 2005). In contrast, Mendez et al. (2017) identified a negative correlation between red-footed boobies and chl-a. Mendez et al. (2017) collected data on the foraging behaviour of red-footed boobies using tracking devices in five colonies along the equator (Galapagos Islands, Mozambique Channel, New Caledonia and the IO) permitting a more robust understanding of factors that determines distribution. They concluded that across the pantropical range of the red-footed booby, distribution is closely driven by intra and interspecific competition for prey. As chl-a concentration was not prognostic here, our results were consistent with Mendez et al. (2017). Sulidae were sensitive to rats although less so than Laridae, aggregating in greater abundance near rat-free islands.
Procellariidae were evenly distributed across the BIOT marine protected area, preferring warmer (>30° C), and less productive waters (<0.20 mg. m-3 chl-a). Our observations were consistent with those of Mannocci, Laran, et al. (2014) in the western IO, reporting greater number of shearwater in warmer waters (>29.5° C) and lower number in productive areas (> 0.37 mg m-3). The Procellariidae were the group the least sensitive to island proximity and, in contrast to the Laridae and Sulidae, appeared to increase in abundance with distance from islands. A potential reason for this is that Procellariidae typically have a wider foraging range from nesting colonies (i.e. 480 km; King 1974) than both Sulidae (i.e. 67.5 km; Young et al. 2010) and Laridae (i.e. 80 km; Harrison & Stone-Burner, 1981; King, 1974). Procellariidae return to burrows only at night; that their distribution appears independent from islands may be due to a predominantly scattered and remote distribution during the day (Dias, Alho, Granadeiro & Catry, 2015). Although we found no significant effect of rat presence on Procellariidae distribution, many Procellariidae species are particularly vulnerable to invasive land predators (Smith, Polhemus, & Vaderwerf, 2002), because they nest in ground burrows (i.e. shearwaters). The pelagic behaviour and large foraging range of this family (up to 3500 km in the Seychelles; Catry, Ramos, Le Corre & Phillips, 2009), which our sampling range could have failed to capture, may mask any distribution shift related to rat presence.
Constant competition over prey is expected to lead to a prey depredation zones around colonies, otherwise known as The Ashmole’s Halo (Ashmole, 1963). The Halo is expected to vary as a function of colony proximity, size, and bird foraging range (Birt, Birt, Goulet, Cairns & Montevecchi, 1987). Within the Chagos Archipelago, many islands are less than 100 km apart and are clustered close together (< 20 km between islands) within atolls. The range to which both the abundant Laridae and Sulidae distribution radiates out from islands (i.e. 100.7 km and 176.0 km respectively), makes it therefore very likely that neighbouring colonies overlap in distribution and therefore compete (in line with Mendez et al. 2017), unless individuals from different colonies express different behaviour to minimise foraging overlap (Wakefield et al. 2013). The wide distribution range and lower abundance of the Procellariidae makes it likely that the competition pressure resulting from colony proximity is less pronounced than for the other families (Gaston, Ydenberg & Smith, 2007).

4.2 Implication for rat eradication programmes

Past eradication efforts in the Chagos Archipelago include a failed attempt on Eagle Island (Meier, 2006) and successful attempts on Îles Vache Marine, du Sel and Jacobin (Harper et al., 2019). The latter attempts focussed on small islands to test the feasibility of eradication and appropriate methodologies on a small scale. Island rodent eradication is increasingly recognized as a powerful strategy for the preservation and recovery of avian populations (Brooke, et al., 2018; Jones et al., 2016; Lavers, Wilcox, & Donlan, 2010). However, eradication is technically challenging and expensive (Warren, 2018), requiring the application of toxic rodenticide posing a risk to humans, livestock, pets, and wildlife (Pickrell, 2019; Van den Brink, Elliott, Shore & Rattner, 2017). Eradication is more likely to fail in the tropics, with high mean annual temperatures and constant precipitation (Russell & Holmes, 2015), and in the presence of land crabs and coconut palms (Holmes, et al., 2015), making a programme in the Chagos Archipelago challenging. Eradication on the largest island of Diego Garcia is likely to be particularly complex and expensive as it is inhabited (Harper & Carr, 2015).
Our analysis has revealed that gains in seabird distribution at sea following eradication are spatially and family-specific, and that eradication on larger islands will yield greater distribution gain. This, combined with the presence of thresholds in distribution, suggests that prioritising remote islands (> 50 km from nearest bird colonies) will impose less spatial competition at sea to the recolonizing seabirds. From the perspective of our study, we propose that eradication should prioritise Île Sud-Est and Île Lubine in Egmont Islands, Île du Coin and Île Pierre in Peros Banhos Atoll, Île Boddam in Salomon Islands and Eagle Island in the Great Chagos Bank, in order to minimise potential overlap in distribution, and therefore competition, between recovering colonies. We note that these recommendations are on the basis of factors explored in this study only and that there are multiple factors that dictate the feasibility, success and approach to rodent eradication. Our results here aim to be useful to feed into a far wider set of considerations, with the ultimate aim of eradicating rats from all islands in the archipelago, in order to achieve full conservation impact.

4.3 Influence of Climate Oscillation

Our multiyear time series enable us to test for distribution effect of climatic oscillations at the inter-annual scale. We observed similar abundance trends for Sulidae and Procellariidae during the six years of sampling, with both families decreasing initially, followed by an increase. The abundance of both families appeared therefore to closely match the strength of the Dipole Mode Index, with the Procellaridae doing so to a lesser degree. We detected no correspondence between seabird and the ENSO index. Our results are consistent with current understanding regarding the influence of the dipole of higher trophic levels in the Indian Ocean. For example, Kumar, Pillai & Ushadevi (2016), identified a positive association between IO tuna productivity and the Dipole Index. While in the southern IO, Albatross breeding-success has been correlated with the Dipole Index (Rivaland et al., 2010). While knowledge of mechanisms driving these patterns is at present limited, our results add to a fledgling body of research on the importance of the Dipole on IO megafauna.
Previous studies may give some clues to possible mechanisms why seabird abundance in the Chagos Archipelago is higher during positive Dipole events, although these must remain speculative. There is, for example, evidence that equatorial upwelling in the IO are more pronounced and that westerly winds decrease in intensity during positive Dipole events (Du & Zhang, 2015). In the Chagos Archipelago, it is possible that a drop in regional upwelling require seabirds to forage further afield, leading to a drop in regional abundance. This would be consistent with understanding regarding other climate oscillations such as ENSO, which is known to influence forage species productivity (Lehodey, Bertignac, Hampton, Lewis, & Picaut, 1997), with implications for the demography and foraging behaviour of higher trophic levels (Champagnon, Lebreton, Drummond & Anderson, 2018). For example, Sprogis et al. (2018), found that the common bottlenose dolphin (Tursiuops trunctatus ) migrated offshore during strong ENSO years, possibly due to a lack of inshore prey. Use of telemetry and satellite tracking is currently being deployed on red-footed boobies in BIOT (Carr, pers. comm.), which will enable mechanisms to be explored in more detail. The greater sensitivity of Procellaridae to both oceanographic variables and to the Dipole suggests this family may be the most vulnerable to global environmental change.
Any linkage between the Dipole and mobile megafauna are likely mediated by multiple trophic links (Oro, 2014). As foragers commensal with subsurface predators, seabirds could be impacted by the Dipole both directly, for example, by a reduction in forage species abundance, and indirectly, by an increase in tuna abundance (Maxwell & Morgan, 2013; Kumar et al., 2016). It is beyond our scope to distinguish these processes here, however we are currently expanding our analysis of seabird distribution to include data on subsurface prey and predator abundance collected simultaneously to the seabird observations, using midwater baited videography (Letessier, Bouchet & Meeuwig, 2017; Letessier et al., 2019).

4.4 Concluding remarks

Seabird abundance and distribution at sea in BIOT is driven by geomorphology and oceanographic conditions. Our modelled distribution complements previous efforts elsewhere in the IO and our time-series has enabled us to identify potential interannual variability related to climate oscillation. Seabird populations are vulnerable to both climatic variability and interactions with human activities (Paleczny et al., 2015). Environmental variability is predicted to increase globally under climate change scenarios (Allen et al., 2014), and evidence suggest that global warming variability may decouple the Dipole from upwelling in the western IO (Watanabe, Watanabe, Yamazaki, Pfeiffer & Claereboudt, 2019). Identifying how inter-annual processes like the IO Dipole drives seabird distribution, where human activities are limited, is valuable for identifying long-term strategies for seabird protection.
To our knowledge, this is the first attempt at predicting the response of seabird distribution to a rat-eradication scenario. We have demonstrated areas of net gain in distribution and have predicted new hotspots at sea after a rat-eradication programme. There is considerable impetus for eradicating invasive species on islands (Brooke et al., 2018; Jones et al., 2016; Lavers et al., 2010). In addition to practical considerations such as cost and probability of success, eradication programmes should identify where eradication can have the greatest conservation impact and ecological footprint. We have successfully identified multiple factors that should influence conservation activities, which is particularly important for seabirds, whose niche extends beyond terrestrial breeding colonies.