ENDEMIC FISHES OF THE CORTEZ BIOGEOGRAPHIC PROVINCE ( EASTERN PACIFIC OCEAN )

1 Escuela Nacional de Ingeniería Pesquera, Universidad Autónoma de Nayarit, Bahía de Matanchén, San Blas Nayarit, México 2 IIK’KAKNAB A.C. Bahía Asunción 181, Col. Fovissste, 23060, La Paz, Baja California Sur, Mexico 3 Secretaria de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA). 4Centro de Investigaciones Biológicas del Noroeste, S.C. (CIBNOR), Mexico 5Facultad de Ciencias Marinas, Universidad Autónoma de Baja California (UABC), Ensenada, Baja California, Mexico 6 Instituto de Investigaciones Oceanológicas (IIO), UABC, Ensenada, Baja California, Mexico


INTRODUCTION
The Gulf of California (GC) represents one of the world's most productive sea areas including an important diversity of marine environments (e.g., rocky-and coraline reefs, oceanic trenches, lagoons, and wetlands) (Thomson et al. 2000, Thomson and Gilligan 2002, Brusca et al. 2005).The GC oceanographic conditions, geographic location, and geological history have deeply influenced speciation processes and species accumulation, which may explain why this area includes the second highest peak in species richness within the Tropical Eastern Pacific (TEP) (Mora andRobertson 2005, Robertson andAllen, 2008).Its location in the transitional warm-temperate and subtropical biogeographic region allows the fishes inhabiting to be a mixture of elements from different affinities: tropical, subtropical, temperate, and arctic-boreal or warm-temperate (Walker 1960, Castro-Aguirre et al. 1995, Hastings et al. 2010).
Given the high number of reported endemisms from different taxonomic groups, Briggs (1974) recognized the inner sea of the Baja California Peninsula as a biogeographic province different from the San Diegan and Mexican Provinces, naming it the Cortez Province (CP).The latter author determined the southern limits to be at La Paz Bay on the west coast of the Gulf of California, and Topolobampo Bay on the east coast.This province together with the San Diegan Province constitutes the warm-temperate Californian region.Currently, the northern limit of the CP is known to be located at Bahía Magdalena, Baja California Sur, and the southern boundary in the Topolobampo region, Sinaloa (Fig. 1) (Hastings 2000, Robertson andCramer 2009).This province is delimited to the north by strong temperature gradients (Robertson et al. 2004, Mora andRobertson 2005) and to the south by the Sinaloa gap, a coastline of 370 km, which includes wide extensions of sandy and muddy bottoms, with estuarine lagoons and wide mangrove areas that separate it from the Mexican Province (Springer 1959, Dawson 1975, Hastings 2000).This gap has been considered a 'faunistic filter' given that it does not have the same isolation effects for all fish elements (Castro-Aguirre et al. 1995).Walker (1960) made the first evaluation of the endemic fishes of the Gulf of California reporting 92 species.In subsequent studies, Findley et al. (1996aFindley et al. ( , b, 1997Findley et al. ( , 1999) ) initially recognized the existence of 77, and ended up with 86, endemic species.Castro-Aguirre et al. (2005a) evaluated fish species from the Gulf of California with amphipacific, boreal, endemic, and amphipeninsular distributions and reported 50 endemic species.Nevertheless, despite these studies mention endemic species of the GC, none of them present a complete systematic list.Our study presents an amendment of the fish component from the CP, including the most relevant ecological attributes of species, plus an updated taxonomic list.

MATERIAL AND METHODS
A comprehensive literature review was made, considering current biological knowledge and taxonomic status of the endemic species from the Cortez Province (CP) (sensu Hastings 2000).Those fish species with restricted distribution ranges, falling within the limits of this province, were considered endemic.An updated systematic list is presented excluding species being a subject of any stage of taxonomic review.Family designations and higher hierarchical ranks follow Nelson (2006).Genera and their respective species are presented alphabetically.The spelling of scientific and common names is based on FishBase (Froese and Pauly 2012).
Additionally, and to recognize the dominant ecological attributes of CP endemic species, the preferential habitat, bathymetric distribution, reproduction strategy, and the maximum total length (TL) were recorded.According to their habitat, species were classified as follows: reef species (R); soft bottom demersal (SBD); mixed bottom demersal (MBD); pelagic-demersal (PD), species that being demersal also break-into the water column; neriticpelagic (NP), those species associated to the upper part of the water column by the coastal zone; mesopelagic (MP); and bathybenthic (BB).Classification in bathymetric distribution was made using minimum and maximum depth limits in which species are distributed.
Reproductive strategies for each species were grouped according to Balon (1989) and Elliot and Dewailly (1995), as following: viviparous (V), those species who give birth to complete juveniles and whose embryos obtain nutrients from yolk or directly from their mother; ovoviviparous (W), those with internal fertilization, embryonic development is produced inside the ovary until larvae are formed, and nutrition of embryo does not depend on the mother but on egg yolk; and oviparous, in those fishes, eggs are spawned directly to the environment and fertilization is external although in some uncommon instances internal fertilization events may occur before spawning.Within the oviparous group, a sub-classification was considered: oviparous with pelagic eggs (OP), oviparous with benthic eggs and pelagic phase (OBPP), oviparous with benthic eggs without pelagic phase (OBWPP), oviparous with oral gestation (OOG), and oviparous with gestation in the vascularized ventral sac (OGVVS).
Regarding size, species were classified by 10 cm length intervals.Biological information was obtained from specific published sources (e.g., Thomson et al. 2000, Robertson andAllen 2008).

RESULTS
Seventy-nine endemic species were recognized and grouped into 29 families, and 59 genera (Table 1).A total of 75 species belong to the class Actinopterygii (94.9%), three to the class Chondrichthyes (3.8%), and one to the class Myxini (1.3%).Gobiidae, Chaenopsidae, and Labrisomidae were the best represented families in terms of number of species with 12, 8, and 7, respectively.On the other hand, Sebastes and Ogilbia (with six and four species, respectively) were the genera with the highest richness.From the overall taxonomic composition, five genera appeared to be endemic to the CP (Colpichthys, Totoaba, Crocodilichthys, Xenomedea, and Aruma).
Fishes associated to coralline-and rocky reef systems were the dominant group with 36 species (45.6%).Nineteen (24.05%) species were grouped in the soft bottom demersal group; the demersal-pelagic and demersalneritic groups were represented by eight species each (Fig. 2).Twenty-seven species (35.5%) can be found within the first 10-m depth layer of water (Fig. 3).Six species reach depths > 200 m, of which, only two exceed 1000 m.The dominant reproduction strategies were oviparous with benthic eggs and pelagic phase (38 species, 48.7%), and oviparous species with pelagic eggs (20 species, 25.6%) (Fig. 4).Regarding adult length, more than half of the endemic species (39 species, 52%) are between 1 and 10 cm total length (TL) and only six exceed 50 cm of TL (Fig. 5).

DISCUSSION
The 79 endemic species considered in this study constitute 8.67% of the total fish fauna reported for the Gulf of California (911 species; Hastings et al. 2010) and 6.14% of the total shore species of the Tropical Eastern Pacific (1285 species) (Robertson and Allen 2008).The number of reported endemic fish species has not drastically changed within the past 50 years, from the 92 species documented by Walker (1960), or the 77-86 found by Findley et al. (1996aFindley et al. ( ,b, 1997Findley et al. ( , 1999)).However, the taxonomic list of species that take part of this endemic assemblage has indeed been modified.Since 1960, a total of 31 endemic new species have been described as species new to science in the CP.Ten of these new species were described after Findley et al. (1996aFindley et al. ( , b, 1997Findley et al. ( and 1999)) The greatest percentage of endemic species corresponded to the families Gobiidae (13 species), Chaenopsidae (8 species), Labrisomidae (7 species), Scorpaenidae (6 species), Gobiesocidae (5 species), Sciaenidae (5 species), Bythitidae (4 species), and Dactyloscopidae (3 species).Highly diversified families in the Tropical Eastern Pacific such as Serranidae (56 species), Ophichthidae (41 species), Haemulidae (37 species), Labridae (36 species), Carangidae (35 species), and Muraenidae (33 species), do not have endemic representatives in the CP and/or are poorly represented.The same pattern can be identified at a genus level; e.g., anchovies (Anchoa: 19 species), tonguefishes (Symphurus: 18 species), wrasses and moray eels (Halichoeres and Gymnothorax, respectively; both with 12 autochthonous species), among others.Walker (1960) recognized four endemic genera from the CP, while Findley et al. (1997) only found two (Totoaba and Xenomedea).According to the presently reported study, five genera, four of them currently monotypic, are endemic to the CP (Colpichthys, Totoaba, Crocodilichthys, Xenomedea, and Aruma).
From the endemic species, three belong to the family Atherinopsidae: the false grunion, Colpichthys regis, a common species in the Sonora coastal hypersaline (values > pss 50) lagoons; and Colpichthys hubbsi and Leuresthes sardine, both autochthonous to the northern part of the Gulf of California, and restricted to the delta and mouth of the Colorado River, Sonora (Castro-Aguirre and Espinosa-Pérez 2006).The Panamic flashlightfish, Phthanophaneron harveyi, is the only species of the family Anomalopidae present in the Tropical Eastern Pacific and it is endemic to the CP (Thomson et al. 2000).
Some species of this endemic component support or even keep supporting important fishery pressure.The Gulf weakfish, Cynoscion othonopterus, forms reproductive aggregations from February to May; a period during which it is captured in great numbers.In 2009, the Gulf weakfish capture reached a profit of more than 30 million Mexican pesos (Paredes et al. 2010).The Gulf croaker, Micropogonias megalops, represents almost 27% of the total fish capture in the Upper Gulf of California (Aragón-Noriega et al. 2009).The totoaba, Totoaba macdonaldi, supported one of the most important fisheries in the region; nevertheless, uncontrolled fisheries and the decrease of Colorado River flow and thus spawning, breeding, and reproduction of this species brought this fishery to collapse (Cisneros-Mata et al. 1995).Currently, the totoaba is included in NOM-059-SEMARNAT-2010 regulation in the category of risk of extinct, and as Critically Endangered by the IUCN red list of threatened Species.According to Berdegue (1955), during the 1950s, totoaba fisheries at San Felipe were composed of 25 shrimp fishing ships, each capturing an average of five to six tons of totoaba weekly.
The number of endemic species presented in this study may vary given that there are non-validated records, such as the spiny guitarfish, Rhinobatos spinosus, that was described from a 26 cm total length specimen, and considered  Van, 1938) Cortez rockfi sh F 25.5 W Sebastes exsul Chen, 1971 Buccaneer rockfi sh D 31 W Sebastes peduncularis Chen, 1975 Gulf rockfish F 440-450 4.7 AJ W as a possible juvenile of a different species by Compagno (2005).However, Castro-Aguirre and Espinosa-Pérez (1996) collected and confirmed the existence of this species off the La Paz Bay.A similar situation is that of the mystery anchovy, Anchoviella parri, described from specimens collected in 1926 on board of the Pawnee research cruise off San Felipe.Based on morphological characters Whitehead et al. (1988) proposed that Anchoviella parri might instead be the Upper Gulf of California Anchoa lucida.Similarly, the Gulf rockfish, Sebastes peduncularis, is only known from two juvenile specimens collected with midwater trawls between the southern end of Tiburon Island and Angel de la Guarda Island, at 440-450 m depths (Chen 1975).However, given the overlapping characters with the Cortez rockfish, S. cortezi, Chen (1975) himself discussed the option of this species being a junior synonym of the Cortez rockfish or even of any other species of Sebastes (see Chen 1975, Love et al. 2002).Additionally, three species were described and are currently known only from their holotypes.The ordinary eel, Ethadophis byrnei, was sampled during low tide at Puertecitos, western coast of the Gulf of California.The Cortez searobin, Peristedion paucibarbiger, was collected by bottom trawling at 60 m depth north of La Paz bay, BCS.Lastly, the cape wrasse, Pseudojuloides inornatus, is known only from a juvenile collected near Cabo San Lucas, BCS.Common names follow those in FishBase (Froese and Pauly 2012); Habitat: A = reef species, B = soft bottom demersal, C = mixed bottom demersal, D = pelagic-demersal (species that being demersal also break-into the water column), E = neritic-pelagic (those associated to the upper part of the water column by the coastal zone), F = mesopelagic, G = bathybenthic; Depth (minimum and maximum depth limits in which species are distributed); TL = maximum total length, (AJ = all juveniles); RS = reproduction strategy (V = viviparous, W = ovoviviparous, OP = oviparous with pelagic eggs, OBPP = oviparous with benthic eggs and pelagic phase, OBWPP = oviparous with benthic eggs without pelagic phase, OOG = oviparous with oral gestation, OGVVS = oviparous with gestation in the vascularized ventral sac).

Class, family, and species Common name Habitat Depth [m] TL [cm] RS
A smoothhound shark, Mustelus albipinnis, was described from six captured specimens in 2000, at Puerto Adolfo Lopez Mateos, BCS.The same species was also described, in the same year, under the name M. hacat, from 36 collected specimens across the Gulf of California; nevertheless, M. albipinnis is considered as the valid name according to priority principle (Anonymous 1999).Considering both descriptions, the distribution range of this species comprises the inner parts of the Gulf of California: from north of Isla Angel de la Guarda, to the south-western coast of the Gulf of California including Santa Cruz and Monserrat Islands, and La Ventana Bay, and the Western coast of BCS on the shelf in front of Bahía Magdalena (Castro-Aguirre et al. 2005b, Perez-Jimenez et al. 2005).This species can be kept as an endemic component of CP; however, according to Perez-Jimenez et al. (2005), it is possible that M. albipinnis distribution extends southward to the coasts of Ecuador including Galapagos Islands.Bussing and Lavenberg (2003), in a review of the genus Opistognathus, concluded that Opistognathus mexicanus Allen et Robertson, 1991, considered endemic to the Gulf of California, was instead a juvenile of O. punctatus Peters, 1869, which has a wide distribution across the Tropical Eastern Pacific.An opposite case is that of delta mudsucker, Gillichthys detrusus (Gobiidae), this species was erroneously placed in the synonymy of G. mirabilis Cooper, 1864, in 1907 (see Swift et al. 2011).
A study on several species complexes done by Hastings and Springer (2009), resulted in recognition of existing morphological differences among subspecies of Dactyloscopus pectoralis (fallax, insulatus, and pectoralis) and Malacoctenus hubbsi (hubbsi and polyporosus) evidence used to guarantee at least the existence of D. pectoralis and M. hubbsi as endemic species to the CP.Similar studies were made by Rosenblatt andParr (1967, 1969) for the genus Paraclinus; Stepien and Rosenblatt (1991) for Gibbonsia and Heterostichus; and Bath (2008) for the genus Parablennius, where some subspecies were raised to species and some others were recognized as synonyms (Hastings and Springer 2009).Nonetheless, the use of additional tools is required (e.g., geometric morphometrics and genetic or molecular analyses) to come to any further conclusions on these particular cases.
Additionally, 21 species described as endemics of the Gulf of California have been found outside the CP expanding their distribution ranges (e.g., Castro-Aguirre et al. 2006).Those species are: Raja cortezensis  On the other hand, ecological characteristics of the CP endemic species revealed that the component associated with coralline and rocky reef systems is dominant, mainly represented by small fishes from the families Gobiidae, Chaenopsidae, Labrisomidae, Gobiesocidae, and Bythitidae, among others.These groups are common off the islands of the Gulf of California, and in the central and south-western coasts of it (Thomson et al. 2000, Thomson andGilligan 2002).Demersal, demersal-pelagic, and neritic-pelagic species from the families Paralichthyidae, Sciaenidae, Engraulidae, and Atherinopsidae are related mainly to soft bottom ecosystems in the eastern coast and Upper Gulf of California (Hastings andFindley 2007, Robertson andAllen 2008).Concerning deep-water ichthyofauna from the Gulf of California, Castro-Aguirre and Balart (1996) denoted the importance of further studies on the great basins, trenches, and ocean depressions from where specimens like the Cortez hagfish, Eptatretus sinus, were obtained.Robertson and Cramer (2009) without counting this deep-water component validated the existence of only 62 fish species endemic to the PC.
From the endemic ichthyofauna, 12 species reach a maximum length of 5 cm, 39 are shorter than 10 cm, and only the totoaba reaches a total length exceeding 2 m.Small-sized species belong mainly to the families Gobiidae, Chaenopsidae, Labrisomidae, Gobiesocidae, Dactyloscopidae, and Tripterygiidae.The dominant reproduction strategy of these families is oviparous with benthic eggs and pelagic phase.These families are considered primary residents given the limited movility of larvae and adults (Thomson and Gilligan 2002).Eggs are relatively large and fixed to the substratum, while adults have a short lifetime (one or two years of generation time), becoming  territorial and therefore limiting genetic flow and favouring species fragmentation (Rosenblatt 1963, Thomson andGilligan 2002).TEP biogeographic gaps (e.g., Sinaloa and Central America) have a considerable impact on these families.Conversely oviparous species with pelagic eggs and long planktonic larval stage (secondary residents) have great potential for dispersal, which is enhanced by the currents (Leis and McCormick 2002), keeping species genetic homogeneity.In the TEP just 30% of species are oviparous with benthic eggs and pelagic phase, most of the species are oviparous with pelagic eggs (56%) (Robertson and Allen 2008).
Some models have demonstrated that ecological differences may cause partial or total reproductive barriers in just hundreds of generations (Hendry et al. 2007).Reproductive isolation may evolve rapidly when populations are settled and adapted to ecologically different environments (Palumbi 1994).In the presently reported study, 26 species with disjunct population distribution have been detected; these species are found on the Pacific Coast and in the northern part of the Gulf of California, but are absent from the southern (Cabo San Lucas) region (Walker 1960, Castro-Aguirre et al. 2005a, Hastings et al. 2010) Some studies (e.g., Bernardi et al. 2003, Sandoval-Castillo and Rocha-Olivares 2011) have detected subtle morphological differences and, in some species, significant genetic distance (Table 2), which in turn could be derived in increasing ichthyodiversity endemism in this province.In addition, according to Robertson and Allen (2008), three species (Chriolepis (2) and Enneanectes (1)) have not yet been described in the Gulf of California.
There is a general consensus that the limits of biogeographic provinces are identified by the occurrence of species distribution and that these limits generally correspond with the existence of environmental discontinuities.Established limits for the CP have been extensively discussed (e.g., Hendrickx 1992, Hastings 2000, Erisman et al. 2011).Based on geological evidence several authors (Thomson et al. 2000, Brusca and Findley 2005, Brusca et al. 2005, Hendrickx et al. 2005, 2007, and Hastings et al. 2010) have included in the limits of the Gulf of California an extended fringe from the Baja California Peninsula towards the Mexican mainland territory, in other words from Cabo San Lucas, BCS towards Cabo Corriente, Jalisco.The southern CP limit extension allows the inclusion of three endemic species from Islas Marías: the scaly-belly blenny, Starksia lepidogaster Rosenblatt et Taylor, 1971, described from 11 specimens collected at Cleopatra Island; the leastfoot blenny, Paraclinus ditrichus Rosenblatt et Parr, 1969, known only from three specimens; and the lonely clingfish, Gobiesox marijeanae Briggs, 1960, known from eleven specimens.The latter two species were sampled at San Juanito Island.This addendum would increase endemic species number to 82.
A great number of studies have pointed out the importance of the CP in terms of conservation, and although recent meaningful efforts for its conservation have been developed (e.g., World heritage Islands and protected areas of the Gulf of California, Natural protected areas: Biosphere reserves of the Upper Gulf of California and Colorado River delta; San Pedro Martir Island; Bahia de los Angeles, Ballenas and Salsipuedes Channels; Gulf of California islands; and Cabo San Lucas; National parks of Loreto bay, Cabo Pulmo, Espiritu Santo Archipelago, and San Lorenzo Archipelago), over the past two decades the existence of a complex web of threats to this large marine ecosystem have being noted (Sala et al. 2004, Enríquez-Andrade et al. 2005, Sáenz-Arroyo et al. 2005, Cudney-Bueno et al. 2009, Hastings et al. 2010, Erisman et al. 2011).
It is generally known that nomenclature ambiguity, and incomplete diversity lists may represent a problem for species and therefore area conservation (Rojas 1992, Hey et al. 2003, Isaac et al. 2004, Mace 2004).Hence, the importance of clarifying species taxonomic status and updating the knowledge of endemism might help in the development of objective conservation strategies (Kerr 1997).

Table 1
Taxonomic list of the endemic fishes from Cortez Province (Eastern Pacific Ocean)