Annotated checklist of the coastal ichthyofauna from Michoacán State, Mexico

Abstract This study is the first to complete an intensive and comprehensive list of the ichthyofauna of nearly all ecosystems of the Michoacán coast, Mexico. The resulting systematic checklist, supplemented with information from the literature and scientific collections, comprises 440 species belonging to two classes, 31 orders, 104 families, and 264 genera. The families with the highest number of species were Sciaenidae (30 spp.), Carangidae (26), Haemulidae (24), Serranidae (21), Paralichthyidae, and Gobiidae (13). Of the total species list, 134 represent first records for the Michoacán State, and one is a first record for Mexico. The results expand the number of known fish species of the Michoacán coast by almost one third and will help to develop conservation and management plans for this coastal zone.


Introduction
differing markedly in the marine ecosystems and consequently in the fish species present: (1) the municipalities of Lazaro Cardenas and Coahuayana, which are characterized by coastal plains, with a wide sandy coastline, mangroves, and estuary zones, (2) and the municipality of Aquila comprising numerous cliffs extending into the sea and forming wide zones of rocky reefs, coralline patches, and intertidal pools; estuaries in the last zone are scarce and differ in size and dynamism from those found in Lazaro Cardenas and Coahuyana (Correa and Gómez 2003).
Such heterogeneity in a transitional zone potentially produces high fish species richness. Nevertheless, information on the ichthyofauna of the Michoacán coast is limited, including two study focused on artisanal fishery species (Amezcua-Linares 2009, Sánchez-Aguilar 2007, two on estuarine fishes (Madrigal-Guridi 2006, Sandoval-Huerta et al. 2014) and one including all habitats (Medina-Nava et al. 2001). Madrid-Vera et al. (1998) published the previously most extensive list of the fish fauna of the Michoacán coast, with 257 species, 157 genera, and 76 families recorded in a wide variety of environments. This limited knowledge of the fish fauna contrasts with the importance of the fishery to the economy of the region as the main economic activity, with about 11,931 fishermen producing 6525 tons with an estimated economic value of 145,255,860 MXN (CONAPESCA 2014).
The main goal of this study was to provide an updated checklist of the ichthyofauna from the Michoacán coast including information on fish of local commercial importance and their biogeographic affinity. This knowledge will increase the understanding of regional fish diversity and could be of usefulness for conservation and management strategies of the littoral zone of the Central Mexican Pacific and particularly for the Michoacán State.

Materials and methods
The study area encompassed the coastline of Michoacán state, with 110 locations directly sampled (Fig. 1) and information on 50 additional sites obtained from published literature or scientific collections. These data were obtained through extensive review of the biological material deposited at the Colección de Peces de la Universidad Michoacana de San Nicolás de Hidalgo (CPUM), the Colección Nacional de Peces (UNAM), the Colección Ictiológica del Instituto de Ciencias del Mar y Limnología (UNAM) and the Marine Vertebrate Collection, Scripps Institute of Oceanography (SIO). In addition, records from the data base of the fish collection of the California Academy of Sciences (CAS) were reviewed. These investigation also included an extensive review of specialized publications (books, catalogues, and field guides) and reports of specimens deposited in ichthyological collections recognized by the Secretaria de Medio Ambiente y Recursos Naturales, México, or specimens of which identification was corroborated by experts.
Field sampling was conducted bimonthly from February 2010 to February 2011, with intermittent sampling in the ensuing year. Sampling was carried out in estuarine zones, rocky intertidal pools, rocky reefs, sandy areas, coralline communities, artificial reefs, and the demersal-pelagic area. Methods were tailored to the ecosystem. Reef species were collected via SCUBA diving using elastic band harpoons. Ecologically cryptic (sensu Viesca-Lobatón 2005) and intertidal pool species were collected using eugenol (clove oil) anesthetic at a ratio of 1:5 (eugenol:ethanol) for reef and 0.25:9.75 for intertidal pool species. When the organisms were sedated, they were captured with a slurp gun or hand net. For estuarine locations, nocturnal sampling was done using gill nets (12 × 1.8 m and 0.7 to 1.2 cm mesh) and cast nets. For sandy-bottomed sites, a small fishing net (2 × 1.8 m, 1 cm mesh and 3 m bag) was used using a dragging period of 20 min. Captures from a shrimp fishing boat were also analyzed. Aggregations of debris in the open sea were investigated to collect ocean species rarely found in coastal areas. Cooperation with local artisanal fishermen was established to review incidental and commercial catches. Fishermen used lines of 50, 100, and 200 m at 5, 20, and 40 m depth, with hooks of various sizes, fishing with fishhook at a maximum depth of 80 m and gillnets of 7 to 12 cm mesh size. Information about the commercial value and uses of the species also was recorded.
The systematic arrangement followed Nelson et al. (2016). The current taxonomic status of each species was corroborated in Eschmeyer et al. (2016). The arrangement of the genera and species was in alphabetical order. In the systematic list, the habitattype from which each species was collected and the scientific collection by which the specimen was identified, or the scientific document from which information of the specimen was obtained, are indicated.
Finally, a zoogeographical affinity analysis of the species, based on the biogeographical regionalization proposed by Briggs (1974Briggs ( , 1995, was made. Accordingly, the Tropical Eastern Pacific was divided into three provinces. The San Diegan province was also included, since some species tended to have a northern distribution.

Results
Sampling was performed in 13 intertidal pool sites, 20 rocky reef sites, three coralline communities, two artificial reefs, 22 estuarine ecosystems, and 50 soft bottom and open sea sites, collecting 6963 fishes.

Discussion
The present checklist represents the most updated and comprehensive systematic list of fishes recorded from the coast of the Mexican State of Michoacán. Of the species cataloged, 30% were first records for this State. The highest proportion of cataloged species was collected in reefs (40%). The pelagic zone accounted for 24% of the species collected, indicated a requirement for future studies of the demersal and pelagic zones with increased sampling effort (Fig. 2). The highest number of new records for Michoacán was found in reefs, chiefly species exhibiting cryptic behavior (Table 1). This could be related to the sampling methods employed, which had not been previously used; the few previously reported species with cryptic behavior were primarily bycatch (Madrid-Vera 1998, Chávez-Comparan 2008, Márquez-Espinoza 2012. Another source of new species records from Michoacán was the intertidal zone (Table 1), for which no published records are available. In general, the number of species in the area may be increased if sampling effort is expanded and records from shrimp and tuna bycatches are included. A new record was obtained for Mexico, two specimens of C. janthinoptera (Bleeker, 1855) were collected from Barco Hundido del Faro de Bucerias (CPUM 4532, N 18°21'8.82'W -103°31'18.71'), which identification was corroborated by BLAST (http://www.ncbi.nlm.nih.gov/genbank) and by boldsystems (http://www. boldsystems.org), searches showing 99% similarity in the cytochrome oxidase subunit 1 gene (COX-1) to specimens identified as C. janthinoptera from the south Tropical Eastern Pacific and the Indo-Pacific Ocean (GenBank accession numbers: KX505745 and KX505746). One specimen of Bathygobius andrei (Sauvage, 1880) (Gobiidae) was also reported in the Chuta estuary (CPUM 3296, 18°2'1"N and 102°33'33"W), representing an extension of its previously known northern distribution limit of the coast of Chiapas (Gómez-González et al. 2012). One specimen of Calotomus carolinus (Valenciennes, 1840) was collected from rocky reef in Faro de Bucerias location (18°20'50"N and 103°30'37"W), extending its extension range in the TEP.
In artisanal fishing (Fig. 3), the species considered to have the highest economic value belong chiefly to Carangidae (e.g. Alectis ciliaris, (Bloch, 1787)), Lutjanidae (e.g. Lutjanus guttatus, (Steindachner, 1869)), Paralichthyidae (e.g. Cyclopsetta querna, (Jordan & Bollman, 1890)), Centropomidae (e.g. Centropomus armatus, Gill, 1863), and Serranidae (e.g. Epinephelus labriformis, (Jenyns, 1840)) ( Table 1). Most of the elasmobranch capture, with the exception of the fins, is considered of low economic value. A high number of neonatal and juvenile hammerhead sharks (Sphyrna sp.), were captured, as well as pregnant Rhinobatos glaucostigma Jordan & Gilbert, 1883, Gymnura marmorata (Cooper, 1863, and Urotrygon spp. In general, the elasmobranchs, due to their unique biological and ecological characteristics, present low population growth and are considered highly vulnerable (Frisk et al. 2005, Hutchings et al. 2012. We accordingly recommend review and enforcement of the relevant legislation. Bycatch in commercial fishing is frequently used for personal consumption, bait (~50%), or discarded (Fig. 3). Species with no current market value may have high nutrient value; hence the number of species with potential to be commercialized is underestimated. In offshore fisheries, these species often have commercial value. For instance, Scorpaena mystes (Jordan & Starks, 1895) reaches 35.6 cm and is marketed in regions such as Baja California. Trichiurus nitens Garman, 1899 supports a small fishery in the central portion of the littoral zone of Ecuador (pers. obs. Romero-Gallardo), whereas, in Michoacán, this species is not used for human consumption.
It was observed that 49% of the listed species are reported as also occurring throughout the three TEP provinces, with 8% of the species reported only in the Panamic and Mexican provinces, being mostly of tropical affinity, agreeing with previous fish fauna surveys in the area . The presence of 81 species (19%) with affinity to the San Diegan province (Fig. 4), a temperate-warm zone, reflects the dynamics of the current flow system of the Michoacán coast, reaffirming this region as a transition zone.
Although visual censuses and photo identification of fish species is widely used for the study of richness, diversity, and ecology of marine habitats (Aguilar-Palomino 2002, Palacios-Salgado 2005, Galván-Villa 2016, it is necessary to rely on reference organisms for taxonomic corroboration. A high proportion of small, nocturnal, or ecologically cryptic species may not be counted in a visual census, especially when the fish fauna of the area under study is not well known, as is the case for the Michoacán State. The collections obtained in the present study enriched the records of the CPUM collection by 19%, since the majority of marine species previously collected remain in collections outside of Michoacán. Many species reported in this study as new records (Table 1) were included by Robertson and Allen (2015), although these authors listed them in the littoral zone of Michoacán coastline only as potential distribution based on habitat suitability. We have confirmed the distribution of such fish, as exemplified by the first formal record of 24 ecologically cryptic species. Our work expanded on the most complete fish fauna checklist previously available for the area by 32.5% (Madrid et al. 1998) and will undoubtedly represent important input for decisions about conservation and management of the coastal area of Michoacán State.