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Endemic Shearwaters Are Increasing in the Mediterranean in Relation to Factors That Are Closely Related to Human Activities

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Endemic Shearwaters Are Increasing in the Mediterranean in Relation to Factors That Are Closely Related to Human Activities Global Ecology and Conservation 20 (2019) e00740 Contents lists available at ScienceDirect Global Ecology and Conservation journal homepage: http://www.elsevier.com/locate/gecco Original Research Article Endemic shearwaters are increasing in the Mediterranean in relation to factors that are closely related to human activities * Beatriz Martín a, , Alejandro Onrubia a, Miguel Ferrer b a Fundacion Migres, CIMA, ctra. N-340, Km.85, Tarifa, E-11380, Cadiz, Spain b Applied Ecology Group, Donana~ Biological Station, CSIC, Seville, Spain article info abstract Article history: The aim of this study was to estimate global population trends of abundance of two Received 20 March 2019 endemic migratory seabird species breeding in the Mediterranean Sea, Balearic and Received in revised form 22 July 2019 Scopoli's shearwaters, from migration counts at the Strait of Gibraltar. Specifically, we Accepted 31 July 2019 assessed how regional environmental conditions (i.e. sea surface temperature, chlorophyll a concentration, NAO index and fish catches), as proxies of climate change, prey availability Keywords: and human-induced mortality factors, modulate the interannual variation in shearwater Chlorophyll numbers. The change in the migratory population size of both shearwater species was Climate change fi Fisheries estimated by tting Generalized Additive Models (GAM) to the annual counts against the fi Seabird year of observation. Speci cally, we modelled daily counts of migrant shearwaters during Monitoring the post-breeding season. Contrary to current estimates at breeding colonies, coastal-land based counts of migrating birds provide evidence that Baleric and Scopoli's shearwaters have been recently increasing in the Mediterranean Sea. Our results highlight that de- mographic patterns in these species are complex and non-linear, suggesting that most of the increases have happened recently and intimately bounded to environmental factors, such as chlorophyll concentration and fisheries, that are closely related to human activ- ities. Counts of migrating birds at strategic coastal points may provide useful estimates of the global population trend, as well as an efficient and rapid assessment of these and other seabird species in the Mediterranean. © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction Seabirds are top predators at the end of the aquatic trophic chain thus they are of main interest for monitoring the marine environments, since they are good indicators of the status of pelagic ecosystems and the changes therein (Zacharias and Roff, 2001). Therefore, the standardized long-term monitoring of these species may be a useful tool to detect alterations in fisheries and/or changes in marine environments due to climate and other human-induced changes (Martín et al., 2016). In addition, many of these species are endangered thus they require accurate estimates of population trends to detect any change in their conservation status (IUCN, 2001; Paleczny et al., 2015). In this sense, many of the efforts made to date to monitoring seabird populations have been devoted to census of breeding numbers with some exceptions (e.g., Aunins et al., 2013; Karris et al., 2017). The main reason is because it is easier, both logistically and in terms of the costs required to survey and monitor, to * Corresponding author. E-mail address: [email protected] (B. Martín). https://doi.org/10.1016/j.gecco.2019.e00740 2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). 2 B. Martín et al. / Global Ecology and Conservation 20 (2019) e00740 make accurate counts of breeding birds or nests, than it is to count all birds in seabird populations (Furness et al., 2003). However, changes in breeding numbers may not reflect overall population trends, since they do not provide information on the non-breeding part of the population (i.e., immature birds and mature non-breeding birds; Arroyo et al., 2014; Weimerskirch et al., 1997). In addition, changes in the timing of breeding can be misinterpreted as changes in population numbers when counts are carried out on a particular same date during the breeding period. Moreover, even when monitoring is focused on breeding numbers, surveillance of seabirds is still logistically costly, thus long-term monitoring of seabird populations is scarce (Becker and Chapdelaine, 2003), and the available information about population trends of seabird species is frequently incomplete or inaccurate (Carboneras et al., 2013). However, many seabirds are migratory species, thus sampling their numbers during migration may offer a cost-effective and efficient method for monitoring overall populations of these species (Arroyo et al., 2014) compared to more direct methods such as nest surveys or sampling breeding numbers (Lewis and Gould, 2000). The Strait of Gibraltar (southern Spain) is a bottleneck used by many seabird species breeding in the Mediterranean Sea, since it is the only connection between the Atlantic Ocean and the Mediterranean Sea (Tellería, 1981). Consequently, this area is a key point for monitoring seabird populations during their migratory trips, moving in or out the Mediterranean throughout their annual cycle (Hashmi, 2000) by means of visual observation of migration (Arroyo et al., 2014). Most of the population of Balearic shearwater (Puffinus mauretanicus) and the entire population of Scopoli's shearwater (Calonectris diomedea) leave the Mediterranean each year after breeding, passing along the Strait of Gibraltar (Guilford et al., 2012; Reyes- Gonzalez et al., 2017) and spend the non-breeding season in the Atlantic. The Balearic shearwater only breeds in the Balearic Islands (Spain) and it is considered as one of the most threatened seabirds in the world, included as ‘Critically Endangered’ on the IUCN Red List (BirdLife International, 2018a). Scopoli's shearwater is globally considered as “least concern” (BirdLife International, 2018b) but it is an endemic breeding species in the Mediterranean included as ‘Endangered’ in the Bird Red Data Book for Spain (Carboneras, 2004) because their populations are believed to be declining (Carboneras et al., 2013; Derhe, 2012). Both shearwater species are also considered as threatened birds at the European level (i.e., rare or vulnerable bird species as listed in Annex I of the EU Bird Directive). However, there is no systematic global monitoring scheme for any of these species (BirdLife International, 2018b, 2018b). Estimates of population trends for Scopoli's shearwater are based on data from only 6% of the population (Carboneras et al., 2013; Derhe, 2012). In the case of Balearic shearwater, counts at the breeding sites rely on indirect sampling methods (e.g. counts of rafts, vocalizations) due to the inaccessibility of the breeding sites, and therefore the population estimates are highly inaccurate, not allowing to derive reliable population trends (BirdLife International, 2018a). Counts of migrating birds at bottlenecks may allow us to detect overall population trends of these two seabird species and these trends can be used as an early warning system to identify conservation concerns at regional level related to environ- mental changes such as global warming or fisheries, among others (Martín et al., 2014; Paleczny et al., 2015). The aim of this study was to estimate global population trends of abundance of two endemic migratory seabird species breeding in the Mediterranean Sea, Balearic and Scopoli's shearwaters, from migration counts at the Strait of Gibraltar. Previous studies support the relationship between food availability and population size in seabirds, through effects on the reproductive output and the survival of these species (Croxall and Rothery, 1991; Oro and Furness, 2002). In addition, since migrating birds need to replenish energy reserves during stopover periods at key locations where maximize their refueling opportunities (McKnight et al., 2013), fluctuations in migration are also related to changes in food resources (Wynn et al., 2007). Moreover, in some seabird species, such as Scopoli's shearwaters, it is known the relationship of survival and breeding success with climate indexes such as NAO and SOI (Genovart et al., 2013b), likely through effects of these indexes on fish stocks (Tsikliras et al., 2018). Therefore, to better understand the fluctuations observed in migration counts, we collected information on the annual variation of shearwater food resources. Specifically, we assessed how regional environmental conditions (i.e. sea surface temperature, chlorophyll a concentration, NAO index and fish catches), as proxies of climate change, prey availability and human-induced mortality factors, modulate the interannual variation in shearwater numbers. Finally, we fully discuss our findings in relation to changes in the global population of shearwaters. 2. Methods 2.1. Study area The Strait of Gibraltar is a short sea-crossing point for pelagic seabirds (14 km between Europe and Africa) where migrants are constrained from both shorelines into a narrow front. Since the Strait is the only connection between the Atlantic Ocean and the Mediterranean Sea (Fig. 1), it funnels seabirds moving in or out the Mediterranean throughout their annual cycle (Hashmi, 2000). Therefore, this site records east-west oriented movements of seabirds passing
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