Received: 8 October 2018 | Revised: 20 February 2019 | Accepted: 1 March 2019 DOI: 10.1002/ece3.5105 ORIGINAL RESEARCH Intricate trophic links between threatened vertebrates confined to a small island in the Atlantic Ocean Ricardo J. Lopes1 | Catarina J. Pinho1,2 | Bárbara Santos1,2 | Mariana Seguro2 | Vanessa A. Mata1,2 | Bastian Egeter1 | Raquel Vasconcelos1 1CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Abstract Laboratório Associado, Universidade do Trophic networks in small isolated islands are in a fragile balance, and their distur‐ Porto, Vairão, Portugal bance can easily contribute toward the extinction vortex of species. Here, we show, 2Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, in a small Atlantic island (Raso) in the Cabo Verde Archipelago, using DNA metabar‐ Portugal coding, the extent of trophic dependence of the Endangered giant wall gecko Correspondence Tarentola gigas on endemic populations of vertebrates, including one of the rarest Ricardo J. Lopes and Raquel Vasconcelos, bird species of the world, the Critically Endangered Raso lark Alauda razae. We found CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO that the Raso lark (27%), Iago sparrow Passer iagoensis (12%), Bulwer's petrel Bulweria Laboratório Associado, Universidade do bulwerii (15%), and the Cabo Verde shearwater Calonectris edwardsii (10%) are the Porto, Vairão, Portugal. Emails: [email protected] (RJL); raquel. most frequent vertebrate signatures found in the feces of the giant wall gecko. This [email protected] (RV) work provides the first integrative assessment of their trophic links, an important Funding information issue to be considered for the long‐term conservation of these small and isolated is‐ This work was funded by grants from Fondation Ensemble (MP/ land ecosystems. EAM/2016/06) and Club 300 Foundation for Bird Protection, and fellowships KEYWORDS SFRH/BPD/84141/2012, SFRH/ birds, Cabo Verde, DNA metabarcoding, endemics, reptiles, trophic networks BPD/79913/2011, PD/BD/113462/2015, PD/BD/106055/2015, funded by FCT/MEC and POPH/QREN/FSE and NORTE2020/ PORTUGAL funds (NORTE‐01‐0145‐ FEDER‐AGRIGEN). Monaco Explorations also partially funded the laboratory work. B.E. and V.A.M. were supported via the European Union's Horizon 2020 research and innovation programme under grant agreement No 668981. 1 | INTRODUCTION large impact on the viability of populations (Holt, 2010), since tro‐ phic networks in small islands can be more unstable than in conti‐ Small islands, due to their size, long‐lasting barriers to dispersal and nental grounds or in larger islands (Novosolov, Rodda, Gainsbury, & occurrence of small populations adapted to these atypical environ‐ Meiri, 2018). Indeed, there is a trend toward smaller food networks ments, are particularly exposed to climatic, environmental and an‐ (Roslin, Varkonyi, Koponen, Vikberg, & Nieminen, 2014) also facili‐ thropogenic pressures that increase the probability of extinction of tated by the fact that smaller islands usually hold lower species di‐ native populations (Whittaker & Fernández‐Palacios, 2007). Species versity than larger islands (Whittaker & Fernández‐Palacios, 2007). relationships, especially competition and predation, can also have a These factors may lead to a higher probability of collapse of trophic This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;1–9. www.ecolevol.org | 1 2 | LOPES ET AL. networks due to trophic cascades or stochastic environmental pro‐ presently restricted to Raso (BirdLife International, 2017; Hirschfeld, cesses, such as drought or hurricanes (Massol et al., 2017). On the Swash, & Still, 2013). With <1,500 individuals, this resident popu‐ other hand, these smaller trophic networks can provide better an‐ lation is subject to substantial size fluctuations, mostly due to the alytical frameworks to test alternative hypothesis concerning the stochasticity of environmental conditions but also due to predation impact of biogeographical gradients on trophic metrics, due to their (Brooke, n.d.). In some years, a considerable egg predation was re‐ simplicity, lower number of confounding variables, and the possible corded, without a clear identification of the predator(s), although replication of food webs in multiple islands (Gravel, Massol, Canard, the researchers hypothesize the giant wall gecko T. gigas as being Mouillot, & Mouquet, 2011; Matias et al., 2017; Roslin et al., 2014; the most likely candidate (Donald et al., 2005; Donald, Ponte, Groz, Spiller & Schoener, 1996). However, while the impact of new invasive & Taylor, 2003). This large nocturnal gecko, with an average snout‐ vertebrate species on these small food webs (McCreless et al., 2016; vent length >10 cm (Vasconcelos, Perera, Geniez, Harris, & Carranza, Medina et al., 2011; Zarzoso‐Lacoste et al., 2016) or on vertebrate 2012) presently only occurs on Raso and nearby Branco islets. It is diets based on invertebrates or plants (Kartzinel & Pringle, 2015) has classified as Endangered due to the small population size and re‐ been extensively documented, the analysis of insular food webs with stricted range of occupancy (Vasconcelos, 2013). a strong component of vertebrate predation is less frequent. This is a Previous studies of the diet of this nocturnal gecko, relying on result of the natural lack of secondary vertebrate consumers in many traditional methodologies, have already shown evidence of a gener‐ small islands and also from the difficulty of retrieving data concern‐ alist diet. Morphological analysis of gecko feces and gut content, ef‐ ing these links in these remote, small, and vulnerable communities. fective for identifying diet items with nondigestible parts, recorded Cabo Verde (Figure 1b) has been recognized as one of the the presence of plants, invertebrates, fish scales and seabird, and most important areas for conservation within the Mediterranean small bird feathers (Mateo, Geniez, Hernández‐Acosta, & Jurado, Basin Biodiversity Hotspot, and is the only tropical member of 2016; Schleich, 1980). Observations also confirm that this gecko the Macaronesian Region (Mittermeier, Turner, Larsen, Brooks, & often eats regurgitated food, egg remains, whole eggs and possibly Gascon, 2011; Myers, Mittermeier, Mittermeier, Fonseca, & Kent, chicks and feces from some of the most abundant seabirds, the Near 2000). Here, we focus on the small and threatened vertebrate com‐ Threatened Cabo Verde shearwater Calonectris edwardsii, and the munity of Raso, a protected uninhabited islet in this archipelago Least Concern Bulwer's petrel Bulweria bulwerii (den Hartog, 1990; (Figure 1c). It comprises six colonial seabird species, nine terrestrial Schleich & Wutke, 1983; Schleich, 1980). The importance of pas‐ breeding bird species, and four species of reptiles (Table 1). serines as diet items is of special concern, since geckos may feed on Of special concern are the populations of the Raso lark Alauda eggs and possibly nestlings. The evidence to date lead to the hypoth‐ razae and the giant wall gecko Tarentola gigas, that coexist in this islet esis that this gecko is the major (and perhaps only) natural predator since its origin, a couple of million years ago. Considered one of the of eggs of the Raso lark (Donald et al., 2005, 2003), and possibly of rarest bird species of the world (Donald, Collar, Marsden, & Pain, the Iago sparrow Passer iagoensis, the other abundant resident pas‐ 2013), the Raso lark is a Critically Endangered ground‐nesting bird serine species. (a) (c) 1,840,000 Cabo N Verde 1,839,500 Africa 1,839,000 1,838,500 500km N (b) Raso 1,838,000 Islet Sal São UTM26Q 756,000 756,500 757,000 757,500 758,000 758,500 759,000 Vicente FIGURE 1 (a) Geographic location of Fecal samples (N = 41) 15 11 the Cabo Verde Archipelago and (b) Raso 7 5 Islet; (c) The surveyed areas in Raso, in a 11 1 100km 17 24 500 m grid. White circles show the areas JunJul AugSep Oct Nov Dec where no gecko was found or sampled. Inland N Santiago Coastal Dry season Wet season Colored circles show the areas with (d) positive fecal sampling (violet: coastal; green: inland). Also, shown is the spatial and monthly discrimination of the number of feces analyzed; (d) Panoramic view of the main plateau of Raso and the highest elevations during the dry season LOPES ET AL. | 3 TABLE 1 Vertebrate species known to Group Common name Scientific name Raso breed in Raso Islet, according to Vasconcelos, Brito, Carranza, & Harris Marine birds Cabo Verde Calonectris edwardsii (Oustalet, 1883) • (2013) and Hazevoet (2015). The symbol shearwater "•" represents a species with confirmed Boyd's shearwater Puffinus boydi Mathews, 1912 • breeding records while "?" represents a Bulwer's petrel Bulweria bulwerii (Jardine and Selby, 1828) • species suspected to breed or have bred Cabo Verde storm Oceanodroma jabejabe (Bocage, 1875) • petrel Red‐billed tropicbird Phaethon aethereus (Linnaeus, 1758) • Brown booby Sula leucogaster (Boddaert, 1783) • Terrestrial birds Little egret Egretta garzetta (Linnaeus, 1866) ? Osprey Pandion haliaetus (Linnaeus, 1758) • Neglected kestrel Falco neglectus Schlegel, 1873 • Quail Coturnix coturnix (Linnaeus, 1758) • Cream‐colored Cursorius cursor (Latham, 1787) ? courser Cabo