INTRODUCTION
Albinism is a genetic anomaly that produces a reduction in melanin pigment biosynthesis. There are two kinds of albinism: complete albinism is the total absence of integumentary pigmentation, and partial albinism or leucism is the partial or complete loss of integumentary pigments but with retinal pigments present (Goto et al., Reference Goto, Sato-Matsumur, Sawamura, Yolota, Nakamura and Shimizu2004). This phenomenon has been reported in mammals, reptiles, fish, sharks and invertebrates (Fertl et al., Reference Fertl, Barros, Rowlett, Estes and Richlen2004; Sandoval-Castillo et al., Reference Sandoval-Castillo, Mariano-Melendez and Villavicencio-Garayzar2006; Modesti et al., Reference Modesti, Aguzzi and Manenti2011; Zhao et al., Reference Zhao, Yang, Zhao, Liu and Wang2012; Muto et al., Reference Muto, Noda, Kai and Nakabo2013). This mutation is also present in the Holothuroidea class; nevertheless, information about the occurrence of albinism in these kinds of echinoderms is scarce and refers to species from temperate to cold regions of the ocean (Casellato et al., Reference Casellato, Massiero and Soresi2006).
The brown sea cucumber, Isostichopus fuscus (Ludwig, 1875), can be found on the Pacific coast of Mexico (including the Gulf of California) and off the coast of Central and South America, from subtidal areas to depths of 39 m (Solis et al., 2009). Brown sea cucumber fishery is intense and is conducted in several countries, which makes this species the most important commercial holothurian in the eastern Pacific (Purcell et al., Reference Purcell, Mercier, Conand, Hamel, Toral-Granda, Lovatelli and Uthicke2013). However, the species is considered as ‘Endangered’ in the Red List of the International Union for Conservation of Nature (IUCN) because of the reported reduction in population density (Mercier et al., Reference Mercier, Hamel, Toral-Granda, Alvarado, Paola-Ortiz and Benavides2013). A number of papers have described the basic aspects of its ecology (Herrero-Perezrul et al., Reference Herrero-Perezrul, Reyes-Bonilla, Garcia-Dominguez and Cintra-Buen Rostro1999; Hamel et al., Reference Hamel, Ycaza Hidalgo and Mercier2003; Reyes-Bonilla et al., Reference Reyes-Bonilla, Herrero-Perezrul, Fernandez-Rivera Melo, Urciaga-Garcia, Beltran-Morales and Lluch Belda2009), but there are still many aspects to be addressed (e.g. genetic variation and connectivity). In this article, we report the first documented observation of albinism in the brown sea cucumber found in the Gulf of California, Mexico, as a way of improving our knowledge of this important holothurian species.
MATERIALS AND METHODS
In 2013, we observed two albino individuals of Isostichopus fuscus: the first one at Loreto Bay National Park, caught by hand at a depth of 16 m (25°45′54″N, 111°14′36″W), and the second one at a depth of 10 m at the Los Angeles Bay Biosphere Reserve (29°02′54″N, 113°29′49″W, Figure 1). The specimens were identified following Gotshall (Reference Gotshall1998) and Solís-Marín et al. (Reference Solís-Marín, Arriaga-Ochoa, Laguarda-Figueras, Frontana-Uribe and Durán-González2009) by means of the presence of papillae on the back as their diagnostic characters.
Geographic distribution of Isostichopus fuscus in the Pacific (grey line in corner of the map) and records of albinism in the Gulf of California, Mexico (red circles).
To quantify the incidence of albinism at Loreto Bay, a total of 137 surveys were conducted, using the technique of belt transects (30 × 2 m2). We calculated the average abundance and standard error of the brown sea cucumber, then we estimated the population density (D = average abundance/area of census) and, finally, we estimated the population density by multiplying the average density by the study area. The latter was calculated using bathymetric maps of the study area and a type of substrate census following the unit point contact method developed by Freiwald et al. (Reference Freiwald, Wisniewski, Wehrenberg, Shuman and Dawson2013). With the estimated population, the percentage of albinism in the brown sea cucumber was calculated using the formula p(%) = (P/T) × 100.
RESULTS
The sea cucumbers' body showed a total absence of integumentary pigmentation (Figure 2). The total length and weight of the individuals were 230 mm and 570 g in Loreto Bay, respectively; while in Los Angeles Bay, the total length and weight were 292 mm and 840 g. According to the data, the mean number of holothurians per 60 m2 transect was 1.14 ± 0.11, and the total number in the census was 137. With those figures, the potential total number of individuals was 909,463 ± 84,787, and the percentage of albino Isostichopus fuscus obtained was 1.10 × 10−4%.
Isostichopus fuscus albino in the Gulf of California, Mexico (scale 10 cm).
DISCUSSION
Although albinism has been reported in different species of marine animals, information on its occurrence in holothurians is scarce. Reports for only two species were available: Apostichopus japonicus (Selenka, 1867) and Ocnus planci (Brant, 1835) in the north-western Pacific Ocean and the Mediterranean Sea, respectively (Casellato et al., Reference Casellato, Massiero and Soresi2006; Zhao et al., Reference Zhao, Yang, Zhao, Liu and Wang2012).
Albinism in Isostichopus fuscus from Loreto Bay (less than 1 × 10−4% of the population) might be linked to a recessive gene or genes, as is the case in humans (Grønskov et al., Reference Grønskov, Ek and Brondum-Nielsen2007) and in other species (Browder, Reference Browder1972; Bensch et al., Reference Bensch, Hansson, Hasselquist and Nielsen2000). In addition, the loss of coloration in the brown sea cucumber may represent a selective disadvantage for the organisms because predators could detect them more easily. Both factors might be contributing to the extremely low incidence of albinism in this species on the Gulf of California.
Although the fishery of I. fuscus has been active in several countries since the early 1990s, and a number of papers have analysed the biological aspects of this species (Hearn et al., Reference Hearn, Martinez, Toral-Martinez, Murillo and Polovina2005; Herrero-Pérezrul & Reyes-Bonilla, Reference Herrero-Pérezrul and Reyes-Bonilla2008; Reyes-Bonilla et al., Reference Reyes-Bonilla, Herrero-Pérezrul, González-Romero, González-Peralta and Ramírez-Hernández2008; Alvarado & Solis-Marin, Reference Alvarado and Solis-Marin2013; Purcell et al., Reference Purcell, Mercier, Conand, Hamel, Toral-Granda, Lovatelli and Uthicke2013), our work is the first documented record of albinism in this species, not only in the region, but also in the entire eastern Pacific. Specifically for the Gulf of California, the annual catch has exceeded 120,000 organisms per year in any single area of capture of the eight recorded in the Gulf of California (Reyes-Bonilla et al., Reference Reyes-Bonilla, Herrero-Perezrul, Fernandez-Rivera Melo, Urciaga-Garcia, Beltran-Morales and Lluch Belda2009). Nevertheless, the presence of albinism had never been reported for this species before.
Finally, it is noteworthy that the specimens were found at two different locations separated by 400 km on the Gulf of California during the same year. As albinism is genetically determined, our observations point to a possible substantial connection between the bays of Loreto and Los Angeles. Because both areas are under federal protection, our findings can be considered as a positive argument for the creation of a network of protected areas in the Gulf.
ACKNOWLEDGEMENTS
The first author (FJFRM) was supported by a Master's Scholarship from Consejo Nacional de Ciencia y Tecnología de Mexico (register 274238). We thank Sara Melo, Maria Martínez, Violeta Martínez and Israel Sánchez for their support and participation in the monitoring of this work. Members of the fishing cooperative ‘Mujeres del Golfo’ and ‘Ligüi’ provided invaluable help in the field and Diana Dorantes Salas provided important editorial services.
