Annotated checklist of marine fishes from the Sanctuary of Bahía Chamela, Mexico with occurrence and biogeographic data

Abstract An annotated checklist of marine fishes of the Sanctuary of Islands and Islets of Bahía Chamela in the central Mexican Pacific is presented. Records of fish species were obtained by different methods including visual census, sampling with anesthetics, fisherman-nets, and trawling with a biological dredge. Additional records were obtained from natural history collections and publications. The list comprises 196 species in 64 families and 141 genera. The Carangidae is the most speciose family with 11 species, followed by the Labridae with 10 and the Pomacentridae with nine. Fourteen species are endemic in Mexican Pacific waters, but none is restricted to Bahía Chamela. The most dominant species recorded during underwater surveys were Epinephelus labriformis, Stegastes flavilatus, and Halichoeres dispilus. Most species are of tropical affinities distributed throughout the tropical eastern Pacific (123), eastern Pacific (23), and Mexican Pacific (14). Other species are known from the eastern and Indo-Pacific regions (18), eastern Pacific and western Atlantic oceans (2), and some are circumtropical (9). A new record of the Gulf Brotula Ogilbia ventralis is provided for the Bahía Chamela and its geographical distribution is extended to Mexican central Pacific.


Introduction
The study of fish diversity along the Mexican Pacific coasts started two centuries ago by naturalists and scientists who studied rich collections from some now-memorable expeditions (Gilbert 1890, Jordan et al. 1895, Breder 1926, 1927, 1928, 1936, Fowler 1944. Today the estimated number of recorded marine species along these coasts is 1,121, with the Gulf of California exhibiting the highest species richness (van der Heiden and Findley 1988, Espinosa-Pérez 2014. However, there are still many areas and habitats (bays, estuaries, mangroves, reefs, littoral zones, deepwater realm) in the Mexican tropical Pacific where proper fish inventories are missing.
Fishes are an important marine group from an ecological and economic point of view. The destruction and pollution of many habitats and the overexploitation of fishes have affected marine ecosystems with the consequent loss of environmental services. For this reason, the implementation of Marine Protected Areas (MPAs) has begun to be a common practice in conservation and a useful fisheries management tool (Roberts et al. 2001, Edgar 2011. However, the design of an effective MPA requires information about the diversity of species inhabiting an area and its connectivity with other areas (Halpern andWarner 2003, Costello et al. 2010).
In  (Ramírez-Gutiérrez et al. 2007, López-Pérez et al. 2010, Juárez-Hernández et al. 2013 in the central and southern Mexican Pacific. However, many of the MPAs from the Mexican central Pacific are lacking inventories of marine fishes. One of these is the Sanctuary of Bahía Chamela located along the coast of Jalisco; it comprises eight islands and four islets dispersed along the bay.
The Sanctuary of Bahía Chamela was the first marine sanctuary in Mexico and has been protected since 2002 (Miranda et al. 2011). This sanctuary is home to species of restricted distribution and endemic fauna and flora. However, scarce information about fish diversity of the sanctuary is available. Only two previous lists of fishes of this bay are found reporting 59 and 80 species for the mainland coastline and for the two largest islands in the bay, respectively (Espinosa-Pérez et al. 2002, Galván-Villa 2015. In the current study, a comprehensive checklist of fish species from the Sanctuary of Bahía Chamela Islands has been compiled based on sampling work from 2007 to 2014, review of material from ichthyological collections, and critical analysis of selected references. A biogeographic and occurrence characterization of all species is also provided.

Material and methods
Study area. The Bahía Chamela is located in the middle coastline area of Jalisco state on the central Mexican Pacific (19°32'N; 105°06'W) (Figure 1). The bay is located between two major oceanic systems: the Gulf of Tehuantepec and the Gulf of California. The extent of the bay is 28 km from Punta Chamela to Punta Rivas (south to north). The sanctuary includes eight islands called as Pajarera, Cocinas, Mamut, Colorada, San Pedro, San Agustín, San Andrés, and La Negra, and four islets as Los Anegados, El Novillo, La Mosca, and Submarino (CONANP 2008). All of these islands and islets are included in the Marine Priority Region No. 38 of sites for conservation of the National Commission for Knowledge and Use of Biodiversity of Mexico (CONABIO). The continental coast of the bay presents sandy beaches to the northern side and shallow plains and rocky beaches to the south. The islands and islets are of continental origin with similar age and composition throughout the region (possibly from the Cretaceous) (Schaaf 2002). The two larger islands have rocky and sandy beaches, while the smaller islands and the islets have rocky intertidal zones sometimes with vertical steep slopes. The depth of the bay varies between 10 and 25 m, decreasing dramatically in the proximity of the coastline and the islands.
Sampling effort and data analysis. Records of fish species were made by visual census and obtained from analyses of collection reports and materials and available publications. Records in situ were made using underwater visual census from 2007 to 2012 according to the technique described by English et al. (1994). Each transect covered an area of 100 m 2 (50 m × 2 m) and was conducted by a single diver. Cryptic fishes and other specimens were collected from 2007 to 2015 with a 10% anaesthetic solution of clove oil diluted in ethanol, with a fisherman-net, and with a biological dredge. All collected specimens were deposited in the fish collection of the Laboratory of Marine Ecosystems and Aquaculture (LEMA-CPE), Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara (Zapopan, Mexico), except specimen of Chaenopsis sp. that was deposited in the Marine Vertebrate Collection (SIO), Scripps Institution of Oceanography, University of California (San Diego, USA). Records obtained from publications included only those that were identified to species level and excluded any questionable records that we could not confirm as species known to occur in the Mexican Pacific.
The nomenclature for species level, family designations, and systematic were updated following Eschmeyer (2015). Distributions and biogeographic affinities for species are based on Thomson et al. (2000), Hastings and Springer (2009, and Robertson and Allen (2015), using the following categories: CT = Circumtropical (distributed throughout the tropics of the world), EP = eastern Pacific (including tropical and temperate regions), EP+ATL = eastern Pacific and western Atlantic oceans (occurs in both oceans), EP+IP = eastern Pacific and Indo-Pacific regions (occurs in both regions), MEX = Mexican waters of the Pacific (including the Gulf of California and outer coast of Baja California), and TEP = tropical eastern Pacific (extends from south of Magdalena Bay, Baja California to Cabo Blanco in northern Peru, includes the Gulf of California and offshore islands as Revillagigedo, Clipperton, Cocos, Malpelo, and the Galápagos). For a description of the structure of fish assemblages, the species recorded between 2007 and 2012 through visual census were classified in five categories using the frequency of occurrence: D = Dominant (> 80% of census), A = Abundant (61-80%), C = Common (41-60%), U = Uncommon (21-40%), and R = Rare (< 21%).

Results and discussion
Species richness. A list of 196 species, 141 genera, and 64 families of marine fishes from the Bahía Chamela is presented (Table 1). In comparison with previous studies by Pfeiler (2008). ‡ These individuals represent juveniles too small to be accurately identified. § This individual is an undescribed species previously found in Costa Rica. (Espinoza-Pérez et al. 2002, Galván-Villa 2015, the richness of the bay increased in this study by more than 240% (by 117 species). The jacks (Carangidae) represent the most diverse family, with 11 species and 8 genera, followed by the wrasses (Labridae) with 10 species and 5 genera, and damselfishes (Pomacentridae) and grunts (Haemulidae) each with 9 species and 4 genera. Eighteen families are represented by only one species. No endemic species for Bahía Chamela were found but 14 endemic species for the Mexican Pacific are recorded here. The fish species richness of Bahía Chamela (196 species) is greater than in other surveyed MPAs of the Mexican Pacific, including Bahía de Los Ángeles (93 species), Bahía Loreto (66) (Table 1).
Fifty-four percent of the species was recorded using visual census. The composition of the fish assemblage of the bay is characterized mainly by rare species (72%). Three species are categorized as dominant: Epinephelus labriformis, Stegastes flavilatus, and Halichoeres dispilus; these species are widely distributed along the Mexican Pacific and are recognized as important in the reef-fish assemblage structure for this bay and other MPAs of the Mexican Pacific because of their high abundance and biomass (Galván-Villa 2015). Another four species are categorized as abundant: Chaetodon humeralis, Microspathodon dorsalis, Stegastes acapulcoensis, and Halichoeres nicholsi; nine as common, and 13 as uncommon. The number of species inhabiting the bay may increase after checking additional details of some of the collected specimens and published records. Additions may include undescribed species, juvenile stages from different species, or records from publications with erroneous determinations. For example, a single female individual of chaenopsid pike-blenny (Chaenopsis sp.) that was collected from sandy bottom of the bay corresponds to an undescribed species distributed from Mexico to Costa Rica (Hastings pers obs). Also three individuals of Pontinus (sp. 1 and sp. 2) were collected, but due to their small size (< 2 cm), the identification of species was not possible. They probably correspond to P. furcirhinus or P. sierra, as both species have been recorded in the area (Robertson and Allen 2015). Another five juvenile individuals of flounders (Paralichthyidae) and eight tonguefishes (Cynoglossidae) collected by the biological dredge from sandy bottoms were not identified to species level. Future careful taxonomic work on these and other specimens would increase the number of species recorded from the bay.
Biogeographic affinity. Most fish species recorded in Bahía Chamela are widely distributed in the tropical eastern Pacific (123 spp = 66%) (Figure 2). Twenty-three species occur in the eastern Pacific, and 18 occur in both eastern and Indo-Pacific waters. Fourteen species are endemic in Mexican waters of the Pacific. One specimen of the Gulf Brotula, Ogilbia ventralis, was collected with clove oil anesthetic from under rocks, depth 6 m at the islet Novillos (Figure 3). This record represents a southern range extension for this species, known previously from the Gulf of California and southern part of the outer Baja peninsula. Bahía Chamela is the type locality for a second Ogilbia species, O. boydwalkeri (Møller et al. 2005). The festive drum fish, Pareques fuscovitattus, is the only endemic species in the Mexican Province (Robertson and Allen 2015). Nine species are circumtropical, and another two (Mugil curema and Etropus crossotus) occur in both the eastern Pacific and western Atlantic regions. Seven undetermined or nondescribed species were excluded from the analysis of biogeographic affinity.
Previous studies considered Haemulon steindachneri (Haemulidae) to occur in both eastern Pacific and western Atlantic oceans, although recently molecular analysis found that these two populations belong to different species, so the valid distribution of this nominal species is the TEP (Rocha et al. 2008). Future review of other species that reportedly occur in both oceans is important to define valid distributions. Finally, according to Robertson and Cramer (2009), the fish richness of Bahía Chamela is most similar to that of the Panama biogeographic province, but there is an important contribution of species from the Gulf of California and outer Baja peninsula and a few species from other oceans.