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Ruler of the atoll: the world's largest land invertebrate

2017; Wiley; Volume: 15; Issue: 9 Linguagem: Inglês

10.1002/fee.1730

1540-9309

Mark E. Laidre,

Pacific and Southeast Asian Studies

Predation can exert life-or-death selection pressures on prey over evolutionary time. Even when the observed frequency of predation is low, predators may induce widespread avoidance behavior in prey, thereby creating “landscapes of fear” (Laundré et al. 2014), which indirectly transform species abundance and community composition. For some animals, especially in remote areas, we know little about their predatory capacities or their potential impact on communities. The coconut crab (Birgus latro) inhabits remote coral atolls and is the world's largest terrestrial invertebrate, growing to what Charles Darwin described as “a monstrous size” (Darwin 1845), with a leg span exceeding 1 m and a weight of up to 4 kg. Following a brief larval stage in the ocean, these crabs spend the rest of their life on land, first as juveniles wearing remodeled gastropod shells (Laidre 2012) – like their closest evolutionary relatives, the terrestrial hermit crabs (Laidre 2014) – and then as adults living shell-free. Historically, coconut crabs were distributed across the Indo-Pacific on islands that for millions of years lacked any human presence. However, due to anthropogenic impacts, especially harvesting by humans, coconut crabs have been driven to local extinction in many parts of their original range. Few studies of this remarkable animal's behavior have been undertaken since Darwin's Beagle voyage, but anecdotes abound, including rumors that the crabs ate Amelia Earhart (Nuwer 2013; though see Krieger et al. 2016 for well-documented predation on invertebrates). A review of the biology of coconut crabs emphasized that “behavioral ecology studies are few” and stressed “the need for further systematic research” (Drew et al. 2010). From January to March 2016, I undertook a 2-month field expedition to study the behavior and natural history of coconut crabs on the Chagos Archipelago (British Indian Ocean Territory), the Earth's largest coral atoll and one of the biggest protected areas in the world. In contrast to other sites where coconut crabs’ natural behavior has likely been substantially modified by human activities, no indigenous humans have been present on Chagos for almost half a century. Chagos therefore provides arguably the most pristine existing environment to study the natural behavior of these animals. Before leaving for Chagos, I wondered what coconut crabs would eat. I had undertaken studies of foraging in terrestrial hermit crabs for almost a decade, in Costa Rica, the Dominican Republic, and Mexico, and these revealed an omnivorous and often carnivorous diet, one of the most diverse of any crustacean (Laidre 2010, 2013). Yet only twice in all those years have I observed predation by terrestrial hermit crabs, in both cases on another invertebrate (hymenopterans that fell on the beach in their final death throes). All other carnivory involved scavenged dead carcasses. In Chagos, the first hint of predation on vertebrates by coconut crabs came when I inventoried a crab's underground lair on 5 Feb 2016. Deep inside the crab's burrow was the carcass of a nearly full-grown red-footed booby (Sula sula), one of the largest birds on Chagos (Carr 2011). Then on 2 Mar 2016, in the middle of the night, I observed a coconut crab attack and kill an adult red-footed booby. The booby had been sleeping on a low-lying branch, less than a meter up the tree. The crab slowly climbed up and grabbed the booby's wing with its claw, breaking the bone and causing the booby to fall to the ground, where it was unable to fly. The crab then approached the bird, grabbing and breaking its other wing (Figure 1). The booby struggled and pecked at the crab, but the crab retained its grip with both claws, kicking at the bird with its ambulatory legs (https://youtu.be/XIRfCoauxbo). Five more coconut crabs came to the site within 20 minutes, likely cueing in on the blood with their neurologically acute olfactory sense (Stensmyr et al. 2005). The attacker responded by dragging the booby several meters away, and then released its grip. As the booby lay paralyzed, the crabs fought, eventually tearing the bird apart over several hours, carrying it away, and consuming it. A daytime attack had been witnessed 2 years before by M Luchmun (pers comm). An adult red-footed booby had landed near the entrance to a coconut crab's burrow. As the bird stood there, the crab slowly emerged from its underground lair, approaching the bird from behind. The crab then grabbed the bird by one leg and dragged it, struggling, back into its burrow. The bird never remerged. Although observations of crab predation on red-footed boobies are scarce, these attacks may still have an important ecological impact by stimulating fear in prey, potentially influencing boobies’ and other bird species’ choice of islands, especially where they nest. On the island of Diego Garcia, Chagos’ largest land mass (2719 hectares), where both attacks on adult boobies where observed, I counted over 1000 coconut crabs in single 15-km transects but did not observe even one ground-nesting bird. The eggs of all the bird species I encountered were in nests high in the trees, never on the ground. To explore whether this nesting pattern might be due to coconut crabs, I surveyed three small islands (West, Middle, and East) in the mouth of the Diego Garcia lagoon (WebFigure 1). These islands represented side-by-side “natural experiments”, each covering a few hectares. In contrast to Diego Garcia, all three lacked invasive rats, which are known nest predators. It was therefore possible to explore whether the pattern of bird nesting behavior across these three islands was related exclusively to the presence or absence of coconut crabs. While birds can fly from island to island, adult coconut crabs cannot travel between islands with the same frequency or accuracy, having lost their ability to breathe underwater. Even as larvae, they may fail to reach certain islands in an archipelago due to the uncertainty inherent in oceanic dispersal. I myself experienced a similar challenge when leaping out of a boat and swimming against strong currents till I made it ashore to each of the islands. The pattern I found across these islands was pronounced, suggesting a strong relationship between coconut crabs and nesting birds. On Middle and East islands, there were no ground-nesting birds, nor any eggs on the ground, but in both cases I counted dozens of coconut crabs. By contrast, as I stepped onto West Island, many nesting noddies (Anous spp) took flight (WebFigure 1, top) and continued circling overhead as I undertook my transect along the island's length. While moving across my transect I did not find a single coconut crab but here, every few strides, I encountered an egg (Figure 2) and had to be careful where I stepped. I counted over a hundred ground nests on West Island, every nest containing one intact egg. Noddies nest colonially on the ground and the adults are much smaller than red-footed boobies, so adult noddies and their eggs may be highly susceptible to predation. Indeed, compared to coconuts (which I regularly observed coconut crabs crack open), noddy eggs are extremely fragile and could easily be broken by the crab's powerful claws. For birds on archipelagoes with heterogeneous distributions of coconut crabs, the decision of which island to nest on may therefore be a crucial one. Surveying further islands of different sizes will help to determine the generality of the natural history patterns observed here. At present, the patterns in bird nesting behavior, together with the observations of predation by coconut crabs on one of the largest bird species on Chagos, raise an intriguing hypothesis for future testing: coconut crabs could act as “ruler of the atoll” for terrestrial communities, inducing fear, particularly in vulnerable, ground-nesting species. Coconut crabs’ influence might be particularly strong on small islands of the size I inventoried (on larger islands, enormous colonies of breeding birds in the tens of thousands could swamp predation). This “island of fear” hypothesis predicts that in areas where humans have locally eradicated coconut crabs, there should be measurable impacts on prey behavior, species abundance, and community composition (Estes et al. 2011). An added twist might be “priority effects”, with bird communities on some islands perhaps preempting coconut crabs from ever colonizing, for instance by preying upon small recently dispersed individuals before they reach the enormous size needed to pose a danger. In other words, a juvenile coconut crab placed on West Island might be eaten by birds and have no impact, whereas an adult crab may wreak havoc. Further research could experimentally test these ideas, although important ethical considerations would obviously arise if coconut crabs were translocated, even temporarily, between islands, and the birds would need to be protected. From a conservation standpoint, humanity should be mindful that if our destructive impact on coconut crabs continues, we risk losing the species that may once have ruled the atoll. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.