Bull Mar Sci. 92(2):285–290. 2016 note http://dx.doi.org/10.5343/bms.2015.1051 First record of albinism in three-rowed sea cucumber, Isostichopus badionotus Centro Regional de Investigación Armando T Wakida-Kusunoki * Pesquera de Yucalpetén, Instituto Nacional de Pesca, Alicia Poot-Salazar Carretera a Chelem, Boulevard Richard Juan de Dios Mena-Loria del Pescador S/N Puerto de Abrigo, C.P. 97320, Yucaltepén, Yucatán, Mexico. ABSTRACT.—The first case of albinism in the three- * Corresponding author email: <[email protected]. rowed sea cucumber, Isostichopus badionotus (Selenka, mx>. 1867), is reported here through the study of two specimens caught by commercial divers fishing off the Yucatán coast of Mexico. The dorsal lengths of the albino sea cucumber specimens were 24.5 and 25.5 cm, with gutted weights of 350 and 400 g, respectively. The entire sea cucumber bodies were completely white in color and devoid of pigmentation. Additional sampling and monitoring is necessary to evaluate Date Submitted: 3 August, 2015. the causes and incidence of albinism in I. baniodotus off the Date Accepted: 23 February, 2016. Yucatán coast. Available Online: 23 March, 2016. Albinism is a hereditary lack of pigmentation caused by an enzyme deficiency in- volving the metabolism of melanin during prenatal development and may involve part of or the entire body of an organism (Boncinelli 1998). Albinism has been re- ported in aquatic organisms, such as marine mammals, bony fishes, sharks and rays, and invertebrates (Hatler 1974, Hain and Leatherwood 1982, Wakida-Kusunoki and Amador-del-Ángel 2013, Wakida-Kusunoki 2015). The three-rowed sea cucumber, Isostichopus badionotus (Selenka, 1867), is wide- spread throughout the Caribbean region (Guzman et al. 2003). It also occurs from the southern United States (North Carolina) to northern Brazil, and east to the mid- Atlantic including Ascension Island, and the Gulf of Guinea, western Africa (Hendler et al. 1995). It is found at depths of 0–55 m (Miller and Pawson 1984). This species is subject to intense fishing off the coast of the state of Yucatán, Mexico, where fishing quotas and closed seasons apply (DOF 2015a). Here we describe the first record of albinism in the three-rowed sea cucumber I. badionotus, found off the coast of Yucatán, Mexico. Materials and Methods In May 2015, the commercial catch of the small-scale fleet operating via hookah diving was monitored from Dzilam de Bravo to Lagartos River, Yucatán, in the sou- thern Gulf of Mexico (21°21´08˝N, 89°10´20˝W to 21°29´21˝N, 87°32´00˝W). The catch depth ranged from 10 to 20 m. The albino specimens were collected and trans- ported to the laboratory where they were identified according to Deichmann (1930) Bulletin of Marine Science 285 © 2016 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 286 Bulletin of Marine Science. Vol 92, No 2. 2016 and Pawson et al. (2010). The morphometric characteristics of the specimens were recorded to the nearest millimeter. Body measurements were made according to Poot-Salazar et al. (2014) before fixation in formalin. After 2 d, the specimens were preserved in 70% alcohol. One of the specimens was deposited in the National Echinoderms Collection of the Universidad Nacional Autónoma de México under catalog number ICML- UNAM 11094. Data from the sea cucumber fishery monitoring program of the Instituto Nacional de Pesca (INAPESCA) was used to quantify the incidence of albinism off the Yucatán coast. These data consisted of information on distribution sizes and yields of sea cucumber by commercial small-scale fisheries, and of daily surveys of the commer- cial catch conducted in Dzilam de Bravo (21°21´08˝N, 89°10´20˝W to 21°31´17˝N, 88°37´00˝W), and San Felipe and Lagartos River (21°31´17˝N, 88°37´00˝W to 21°29´21˝N, 87°32´00˝W) during the short fishing season of April 24–28 and May 14–25, 2015 (17 d in total). The percentage of albino organisms in the commercial catch was calculated by: (1) estimating the total number of organisms caught, which is obtained by dividing the total catch of the surveyed vessels by the average weight of the organism (Nt = total weight of surveyed vessels/average weight of the surveyed organisms); (2) calculating the percentage of albinism of the number of sea cucumbers lacking pigmentation divided by the total number of organisms in the catch. Results and Discussion During the sea cucumber fishery monitoring in May 2015, two albino I. badionotus were landed. The entire sea cucumber bodies were completely white in color and devoid of pigmentation; thus, we concluded that the specimens were total albino (Fig. 1A). The total lengths and gutted weights of the albino specimens were 245 and 255 mm, and 350 and 400 g, respectively. The sex of the specimens could not be determined because they were gutted when collected. A total of 426,492 kg of I. badionotus was inspected from the commercial catch. The specimens had an average weight of 0.331 (SD 0.002) kg. Thus, the estimated total number of sea cucumbers was Nt = 1,288,495, and the percentage of albino I. badionotus obtained was 0.00015%, which is very similar to the percentage of albinism of Isostichopus fuscus found in the Gulf of California (Fernández-Rivera Melo et al. 2015). These two species have been under great pressure from fishing; I. fuscus is a protected species under Mexican environmental laws (DOF 2002). Off the Yucatán Peninsula, I. badionotus is regulated with closure periods by the Official Mexican Standard (NOM-009-PESC-1993) (DOF 2015b). Prior to the fishing season (February 24–March 22), to determine the biomass of sea cucumbers off the Yucatán coast, the Instituto Nacional de Pesca (INAPESCA) conducted scuba surveys to count sea cucumbers along line transects. For the 500 stations monitored, there were no reports of albino I. badionotus, which indicates the low incidence of albinism in this species. In pigmented specimens of I. badionotus, body coloration is extremely variable, ranging from light brown to blackish, with numerous spots and blotches often present (Pawson et al. 2010) (Fig. 1B). Color mutation is one of the most significant characteristics of sea cucumbers (Kang et al. 2011) and can improve the flavor and market price in China (Ma et al. Note 287 Figure 1. Three-rowed sea cucumber, Isostichopus badionotus, collected in May 2015 off Yucatán, Mexico, exhibiting (A) total albinism and (B) full pigmentation. Photographs were taken while fresh by A Poot-Salazar. 2014a). Albinism appears to be rare in the class Holothuroidea although it is reported in at least four species (Table 1); however, the mechanism by which albinism occurs in sea cucumbers remains poorly understood. Completely white albino sea cucumbers are rare in nature, possibly because of predation and sensitivity to their surroundings (Ma et al. 2014a). Studies of Apostichopus japonicus (see Table 1 for species authorities) showed albinism occurs due to lower expression of microphthalmia-associated transcription factor (MITF), which is implicated as an important regulator of the expression of the tyrosinase gene family involved in the melanin biosynthetic pathway (Zhao et al. 2012). According to Ma et al. (2014b), albinism in A. japonicus could result in the interruption of melanogenesis-related pathways caused by the inactive transcription of internal key genes together with abnormal tyrosine metabolism. One of these key genes is protein kinase C (PKC), which can expand protein kinase A (PKA) promotion of melanin synthesis by up-regulating the MITF gene (Park et al. 2006). Although the chromatic anomaly events might be the result of random events, an interaction between genes and the environment could not be excluded. Low oxygen and the presence of metals at oviposition sites may cause scoliosis in larval fishes and amphibians (Unrine et al. 2004, Sanabria et al. 2010). Because sea cucumbers have larval developmental stages, there is a risk that the larvae are exposed to environmental changes that could trigger albinism. Almost every year, in July and August, when I. badionotus are in their main reproductive periods (Poot-Salazar 2015), upwelling processes and groundwater discharges push in cold and nutrient-rich water near Dzilam de Bravo and Río Lagartos; these conditions provide for the development of algal blooms (Enriquez et Table 1. Cases of albinism that have been reported in the class Holothuroidea. Family/species Location Reference Cucumariidae Cucumaria frondosa (Gunnerus, 1767) Maine, USA Feindel 2002 Ocnus planci (Brandt, 1835) Gulf of Venice, Italy Casellato et al. 2006 Stichopodidae Apostichopus japonicus (Selenka, 1867) China Ma et al. 2014a,b Isostichopus fuscus (Ludwig, 1875) Gulf of California Fernández-Rivera Melo et al. 2015 288 Bulletin of Marine Science. Vol 92, No 2. 2016 al. 2010). Algal blooms can increase the organic matter content in sediment naturally and reduce oxygen levels. This condition could favor the presence of albinism in sea cucumbers. With regard to the spread of albinism, some researchers argue that overfishing can lead to a reduction of the effective population size, favoring inbreeding and the ex- pression of the gene for albinism (Sanabria et al. 2010, Leal et al. 2013). Although the fishing of I. badionotus has been active in several countries of the Caribbean region in Central and South America since the 1990s (Toral-Granda 2008), the presence of albinism has never been reported for this species. For the recessive albino trait to appear in an animal, the offspring must inherit a recessive gene from both parents (Kaneko 2001). Fertilization of gametes is external in sea cucumbers; therefore, the presence of hermaphroditic individuals could also facilitate inbreeding and the com- bination of recessive genes; and hermaphroditism in I.