INTRODUCTION
The Indo-Pacific lionfish Pterois volitans, introduced in the Western Atlantic (Whitfield et al., Reference Whitfield, Gardner, Vives, Gilligan, Courtenay, Ray and Hare2002; Schofield, Reference Schofield2010) 30 years ago, invaded a large portion of the region posing a serious threat to the marine ecosystem (Côté et al., Reference Côté, Green and Hixon2013). In the southern Gulf of Mexico, invasive lionfish was detected late in 2009 (Aguilar-Perera & Tuz-Sulub, Reference Aguilar-Perera and Tuz-Sulub2010) and now is considered established in coral reefs of Alacranes Reef, northern Yucatan Peninsula, Mexico (López-Gómez et al., Reference López-Gómez, Aguilar-Perera and Perera-Chan2014).
In the Western Atlantic, 24 taxa have been recorded parasitizing invasive lionfish including digeneans, monogeneans, cestodes, nematodes, isopods, a copepod and an acanthocephalan (Bullard et al., Reference Bullard, Barse, Curan and Morris2011; Fernández-Osorio et al., Reference Fernández Osorio, Corrada Wong, Chevalier Monteagudo, Caballero Aragón and Cabrera Sanson2014; Sikkel et al., Reference Sikkel, Tuttle, Cure, Coile and Hixon2014; Ramos-Ascherl et al., Reference Ramos-Ascherl, Williams, Bunkley-Williams, Tuttle, Sikkel and Hixon2015) in the Cayman Islands, Puerto Rico, The Bahamas and Cuba. The most common and abundant parasite recorded in the invasive lionfish is the digenean, Lecithochirium floridense (Ramos-Ascherl et al., Reference Ramos-Ascherl, Williams, Bunkley-Williams, Tuttle, Sikkel and Hixon2015). In general, invasive lionfish has shown a low susceptibility to parasites in its invaded environment (Ruiz-Carus et al., Reference Ruiz-Carus, Matheson, Roberts and Whitfield2006; Bullard et al., Reference Bullard, Barse, Curan and Morris2011; Loerch et al., Reference Loerch, McCammon and Sikkel2015; Ramos-Ascherl et al., Reference Ramos-Ascherl, Williams, Bunkley-Williams, Tuttle, Sikkel and Hixon2015; Sellers et al., Reference Sellers, Ruiz, Leung and Torchin2015). In fact, Tuttle et al. (Reference Tuttle, Sikkel, Cure and Hixon2017) argued that the escape from parasites hypothesis may have contributed to the success of lionfish invasion.
Isopod species (Isopoda) have also been recorded parasitizing invasive lionfish, including Aegiochus tenuipes, Carpias serricaudus, Eurydice convexa, Excorallana quadricornis, Gnathia sp. and Rocinela signata in coral reefs of the Cayman Islands, Puerto Rico and The Bahamas (Ramos-Ascherl et al., Reference Ramos-Ascherl, Williams, Bunkley-Williams, Tuttle, Sikkel and Hixon2015). Additional records include Anilocra haemuli in Cuba (Fernández-Osorio et al., Reference Fernández Osorio, Corrada Wong, Chevalier Monteagudo, Caballero Aragón and Cabrera Sanson2014), Excorallana spp. in Bonaire (Poole, Reference Poole2011) and R. signata in Panama (Simmons, Reference Simmons2014).
Cymothoa excisa (Cymothoidae), a parasitic isopod that attaches in the buccal cavity of fish hosts (Bunkley-Williams et al., Reference Bunkley-Williams, Williams and Bashirullah2006), has been recorded in 16 fish species of five families in the Caribbean Sea (Bunkley-Williams et al., Reference Bunkley-Williams, Williams and Garzon-Ferreira1999, Reference Bunkley-Williams, Williams and Bashirullah2006; Joca et al., Reference Joca, Leray, Zigler and Brusca2015). However, only nine fish species are currently recorded as hosts of C. excisa in the Gulf of Mexico (Kensley & Schotte, Reference Kensley and Schotte1989; Joca et al., Reference Joca, Leray, Zigler and Brusca2015).
In the southern Gulf of Mexico, off the northern Yucatan Peninsula, Mexico, C. excisa has been found parasitizing mainly snappers, such as the yellowtail Ocyurus chrysurus and mutton, Lutjanus analis (Kensley & Schotte, Reference Kensley and Schotte1989), and recently the pinfish Lagodon rhomboides (Sparidae) (Bonilla-Gómez et al., Reference Bonilla-Gómez, Ramírez-Rojas, Badillo-Alemán and Chiappa-Carrara2014). In the present study, while not a parasitological study, we document the occurrence of the snapper-choking isopod Cymothoa excisa parasitizing invasive lionfish Pterois volitans in Alacranes Reef.
MATERIALS AND METHODS
Alacranes Reef (22°21′44–22°35′12 N 89°36′30–89°48′00 W) is located 130 km off the northern coast of the Yucatan Peninsula, Mexico, and is the largest reef complex in the southern Gulf of Mexico. Local diver-fishermen participated in collections of invasive lionfish in Alacranes reef and provided specimens. In the laboratory, lionfish were measured for morphometric data, such as total length (TL) in millimetres and weight in grams, and for meristic data (e.g. fin rays number, spines counting, etc.) (López-Gómez et al., Reference López-Gómez, Aguilar-Perera and Perera-Chan2014). In 2016, during routine examinations we noticed isopods in the buccal cavity of two lionfish collected in November 2015 at 10 m deep. In previous routine examinations conducted since 2010 to present in more than 1000 lionfish specimens, no isopods were noticed.
Isopods were removed from lionfish with forceps, preserved in 95% ethanol, placed in labelled containers, and later identified under the dissecting microscope following Kensley & Schotte (Reference Kensley and Schotte1989) and Thatcher et al. (Reference Thatcher, Jost and Souza-Conceição2003). Additionally, isopods were measured with a calliper for body length (BL) in millimetres and deposited in the invertebrate collection of the Universidad Autonoma de Yucatan, Merida, Mexico.
RESULTS AND DISCUSSION
Isopods were identified as Cymothoa excisa by characters that distinguish them from other cymothoid isopods, including the anterolateral angles of pleonite one reaching to half-length of cephalon or less, eyes or eye traces present, and anterolateral angles of pleonite one narrow and subacute (Kensley & Schotte, Reference Kensley and Schotte1989). Isopod specimens were adult females attached to the lionfish buccal cavity. The smaller specimen (11 mm in BL, Figure 1A) was attached at the base of the buccal cavity of one lionfish (294 mm TL) posterior to the tongue, with the head of the isopod facing anteriorly toward the mouth of the lionfish. The larger specimen (14 mm BL, Figure 1B) was attached upside down on the roof of the buccal cavity of the other lionfish (301 mm TL), with the head of the isopod oriented anteriorly facing the mouth of the lionfish. There was no evidence of tissue deterioration in the buccal cavity of the lionfish due to isopod attachment or presence of blood content in the isopods.
Fig. 1. Two snapper-choking isopod Cymothoa excisa recorded parasitizing invasive lionfish Pterois volitans. (A) 11 mm body length, (B) 14 mm body length. Scale bar = 5 mm.
The invasive lionfish Pterois volitans, as a new host for C. excisa, represents a new record in the Western Atlantic. In general, introduced species arrive in the invaded region without their natural parasites (Torchin et al., Reference Torchin, Lafferty, Dobson, McKenzie and Kuris2003) and local parasites opportunistically infect invasive species. In this case, there is not any evidence that suggests invasive lionfish brought parasites with them from the Pacific Ocean (Ruiz-Carus et al., Reference Ruiz-Carus, Matheson, Roberts and Whitfield2006; Bullard et al., Reference Bullard, Barse, Curan and Morris2011; Tuttle et al., Reference Tuttle, Sikkel, Cure and Hixon2017). In fact, Tuttle et al. (Reference Tuttle, Sikkel, Cure and Hixon2017) proposed that low infection rates of invasive lionfish indicate that parasites are not, and have not been likely, sources of biotic resistance to the lionfish invasion. Sellers et al. (Reference Sellers, Ruiz, Leung and Torchin2015) found that lionfish accumulate native parasites in the introduced range with patterns of parasitism varying regionally, but the absence of an association between lionfish condition and parasite abundance suggests that parasites probably do not have a substantial direct effect on lionfish.
Interestingly, infective free-swimming juveniles of C. excisa always attach on top of the tongue of their hosts and develop into females. In this case, neither specimen in Alacranes Reef appeared to be attached to the tongue or feeding on the lionfish host. Williams & Bunkley-Williams (Reference Williams, Bunkley-Williams, Bruce and Smitin press) described juvenile prey-predator transfers as a new life cycle strategy in Cymothoa oestrum. This latter transfer was previously documented in adult Anilocra acuta to King Mackerel Scomberomorus cavalla (Williams & Bunkley-Williams, Reference Williams and Bunkley-Williams1994). We suggest the possibility that C. excisa infected invasive lionfish in Alacranes Reef through adult prey-predator transfer.
In Alacranes Reef, Cymothoa excisa either infected lionfish as free-swimming juveniles or as adults through prey-predator transfer (probably ingesting a yellowtail snapper Ocyurus chrysurus, recorded in lionfish stomach content analyses in various locations of the Western Atlantic; Morris & Akins, Reference Morris and Akins2009). Our findings, and the rarity of infections, suggest the latter. Monitoring should continue to further elucidate the infection method as well as prevalence of other parasite species in invasive lionfish. Additionally, we recommend determining the degree of susceptibility of lionfish to parasite species by comparing the parasite prevalence between native and invasive lionfish populations (as in Sikkel et al., Reference Sikkel, Tuttle, Cure, Coile and Hixon2014) or between invasive lionfish and ecologically similar native fish species (as in Sellers et al., Reference Sellers, Ruiz, Leung and Torchin2015).
ACKNOWLEDGEMENTS
We thank Jorge Canché-Jiménez, Damaris Camargo-Saavedra and Jessica Valle-Nava for helping in many ways in the lionfish processing. We also thank lobster fishermen from Alacranes Reef for providing lionfish samples. Cristian Aguilar-Perera generously helped assembling Figure 1.
