Habitat suitability and environmental factors affecting

Environ Biol Fish DOI 10.1007/s10641-015-0413-5

Habitat suitability and environmental factors affecting whale shark (Rhincodon typus) aggregations in the Mexican Caribbean Ana Hacohen-Domené & Raúl O. Martínez-Rincón & Felipe Galván-Magaña & Natalí Cárdenas-Palomo & Rafael de la Parra-Venegas & Beatriz Galván-Pastoriza & Alistair D. M. Dove

Received: 21 May 2014 / Accepted: 10 April 2015 # Springer Science+Business Media Dordrecht 2015

Abstract The Mexican Caribbean is considered one of the most important sites for whale shark aggregations. Whale shark groups of over 300 individuals have been recorded frequently. There is little published information regarding the ecology of the whale shark in Mexico, and the role that the Mexican Caribbean plays as habitat for this species. This area has been recognized as important for the whale shark and therefore it is necessary to determine the environmental factors that shape the distribution of these animals. The aim of this study was to identify key environmental factors associated with A. Hacohen-Domené : F. Galván-Magaña (*) Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Av. IPN s/n. Col. Playa Palo de Santa Rita, Apartado Postal 592, La Paz, BCS, Mexico e-mail: [email protected] R. O. Martínez-Rincón Centro de Investigaciones Biológicas del Noroeste CONACYT, Avenida IPN s/n, La Paz, Baja California Sur 23096, México N. Cárdenas-Palomo Centro de Investigación y Estudios Avanzados del IPN, México, Mexico R. de la Parra-Venegas : B. Galván-Pastoriza Ch’ooj Ajauil AC, Av. Xelha N° 1-311, SM 28, Cancún, Quintana Roo 77500, México A. D. M. Dove Georgia Aquarium Research Center, 225 Baker Street NW, Atlanta, GA 30313, USA

whale shark feeding aggregations and to determine the patterns in habitat suitability for whale sharks in the Mexican Caribbean through the modeling approach of maximum entropy. Whale shark data obtained for this study included 250 records during April to September (2008–2012). The MaxEnt model performed better than random and produced an area under the curve (AUC) score of 0.946. Primary productivity and sea surface temperature were the variables most strongly related to whale shark sightings. The model predicted a high suitability in areas located to the north of Isla Contoy and the offshore area east of Isla Contoy named BAfuera^ (>0.75), with medium suitability north of Cabo Catoche (>0.5) and lower suitability for the northeast of Cabo Catoche (0.75) with medium suitability north of Cabo Catoche (>0.5) and lower suitability for the northeast of Cabo Catoche (0.75) and are in fact areas with highest encounter rates in the field. Contrastingly, the model predicted medium

suitability north of Cabo Catoche (>0.5) and lower suitability for the northeast of Cabo Catoche (100 organisms) in Qatar have also been related to Euthynnus affinis spawing (Robinson et al. 2013). In the Afuera area, to date, it is still unknown where and when the little tunny spawing event occurs and the little tunny population size. It is also unknow what environmental conditions are associated with the spawning event or the factors that trigger this event. It has been suggested that the tuna may Bsearch^ for optimal temperature to spawn. By the time the eggs have hatched (16 h later), they have drifted northwest on prevailing currents into the plankton rich waters around Cabo Catoche, where the fry will have plenty of food to eat (A. Dove, pers. comm.). Future research efforts should be made regarding the spawning event in this area, in order to have a more complete understanding of the whale shark aggregation in the study area. The presence of the whale shark in the Mexican Caribbean is related to high productivity present in the study area. Whale shark aggregations around the world suggest that shark abundance and distribution depends on food availability, since whale shark seasonal aggregation sites correspond to areas of high productivity and therefore massive concentrations of plankton (Norman 1999; Heyman et al. 2001; Graham et al. 2006; Nelson and Eckert 2007; Taylor 2007; Motta et al. 2010; Cárdenas-Palomo et al. 2010; Ketchum et al. 2012; Cárdenas-Palomo et al. 2014), as with other large marine planktivores (Sims and Quayle 1998; Croll et al. 2005). The second key environmental determinant, of whale shark distribution our MaxEnt model identified was SST. Our model predicts the probabilities of whale shark sightings, and would be associated at water temperatures higher than 26 °C (predicted value of 0.2). The SST values varied during May to September (2005– 2012) ranging from 25.2- 27.8 °C, prevailed within the optimal range of temperature for this species (Hoffman et al. 1981; Ketchum 2003; Wilson et al. 2006; Graham and Roberts 2007; Nelson and Eckert 2007). Our results agree with Cárdenas-Palomo et al. (2010) recorded SST during the whale shark season in the area during 2005 and 2006 (27.8 °C±1.5), which were higher values compared with the absence of whale sharks in the area (25 °C±0.96). The whale sharks in the pelagic waters of the western Indian Ocean have been correlated with SST (Sequeira

et al. 2012). In the coastal waters of the Seychelles, the SST and wind speed have been correlated with whale shark numbers in an aerial survey (Rowat et al. 2009), as well as Chl-a concentration, distance from the coast and fish schools, possibly as a direct indication of zooplankton abundance. In the northern Gulf of Mexico, the whale shark presence is mostly related to their distance from the continental shelf edge, distance to adjacent petroleum platforms, and chlorophyll-a which McKinney et al. (2012), suggested an association of these variables with high food availability. Whale shark studies in the area have shown aggregations in coastal waters, as they do in other aggregation sites (Pravin 2000; Nelson and Eckert 2007; Robinson et al. 2013). Satellite tag studies of whale sharks in the Gulf of Mexico (Hueter et al. 2013), have shown that individual sharks remained in the area for an estimated mean duration of 24–33 days with maximum residency up to about 6 months as determined by photo-identification. When they leave the feeding area, the sharks showed horizontal movements in multiple directions throughout the Gulf of Mexico basin, the northwestern Caribbean Sea, and the Straits of Florida (Hueter et al. 2013). Whale shark sightings in the area correspond to warmer weather seasons: dry and rainy, which agrees with the seasonal suitability map (Fig. 5). The results show that the spatial patterns changed seasonally (Fig. 5), as a result of seasonal changes in the environment, which agrees with what the sighting trend has been observed in the last years (Cárdenas-Palomo et al. 2010, de la ParraVenegas et al. 2011; Hueter et al. 2013). Our seasonal maps indicated that the environment was most suitable for the whale shark during the rainy season. The SST during the whale shark season is higher in the area, as a result of the dry and rainy season. In October, the water temperature decreases, and whale sharks start to leave the area. Hueter et al. (2013) suggested that decreasing water temperatures may be one of the reasons for the whale sharks leaving the Mexican Caribbean in September–October, as well as declining the productivity in the area. This agrees with our seasonal analysis. Habitat suitability maps showed that the environment was not suitable for the whale shark during the north and cold fronts seasons (Fig. 5). Primary productivity decreases as the upwelling weakens during the winter and northern winds. As a result Cabo Catoche and Isla Contoy are no longer suitable habitats for the whale shark. In the Afuera area,

Environ Biol Fish

it is unknown if whale sharks leave because it’s too cold for them or because it’s too cold for the tuna, but aerial surveys in the area show the absence of whale sharks after October (de la Parra-Venegas et al. 2011). Robinson et al. (2013) reported whale sharks actively feeding on several occasions in water temperatures of 30 °C and up to 33.8 °C, which contradicts Sequeira et al. (2012) that whale sharks may avoid higher temperatures, and shows whale sharks actively able to tolerate greater temperature range than previously thought. SST has also proved to help predict whale shark occurrences in the Azores, where timing of whale sharks sightings in this region coincides with a period of highest SST (Afonso et al. 2014). It has been found that migratory species are particularly vulnerable to increased temperatures, changes in food availability, mismatch in timing, the loss of breeding habitat and reduced migratory abilities (Robinson et al. 2009). Also, the results of the vulnerability assessment to large-scale threats suggest that global climate change could have a significant impact on the size and distribution of whale shark aggregations in the future (Ziegler 2010). Results obtained in this study show a good fit with known areas of whale shark feeding aggregations, and provide information regarding the environmental factors affecting whale shark habitat use. This is a first step to understand the whale shark habitat use with the help of species distribution models in the Mexican Caribbean. It is recommended that future analysis with longer time series should be applied, as to investigate if models can be used to explain the changes in occurrence from previous locations within the Mexican Caribbean to the Afuera area. Further, whale sharks are often seen with large wounds or scars clearly derived from maritime traffic accidents, such as collision with boats or ship propellers (Speed et al. 2008; Ramírez-Macías et al. 2012), as a result of sharks spending long periods on the surface while in coastal aggregations. Predicting a possible habitat distribution for this species in an area can be used to restrict access of large vessels as well as imposing speed limits in the area. In general, understanding habitat utilization is essential for management decisions. Studies in this area, suggest this region is favorable for the whale shark as a trophic habitat due to the environmental conditions, such as enhanced seasonal high primary and secondary productivity. Due to the high aquatic productivity in the upwelling area, it is common to observe abundant marine fauna during spring and summer. So, maintaining the

whale shark feeding habitat is of great importance because besides the whale shark, this area is home to many other species.

Acknowledgments This work was supported by MEX-US (University of California-CONACYT) in the project BDetermination of movement, habitat use, filtration mechanics and diet/food preference of manta rays off the Yucatan peninsula^. Also thanks to CONACYT and PIFI- IPN for fellowships to AHD, and Instituto Politécnico Nacional (COFAA, EDI) granted to FGM. Thank to MVZ Francisco Remolina Suárez, Director Reserva de la Biosfera Tiburón Ballena to develop this project in the protected area.

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