The fish fauna of three lagoon-estuarine systems in the northeastern Gulf of Tehuantepec, Mexican south Pacific

Emilio I. Romero-Berny(a)(b)(*), Ernesto Velázquez-Velázquez(c), Manuel de Jesús Anzueto-Calvo(c),
Eduardo Urbina-Trejo(b), Juan J. Schmitter-Soto(d)

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Figure 1. Maps of the Gulf of Tehuantepec (upper left), Mar Muerto (A), La Joya-Buenavista (B) and Los Patos-Solo Dios (C) lagoon-estuarine systems, with sampling sites of the fish fauna.

La Joya-Buenavista (47.5 km²) is a shallow and seasonally polyhaline system with restricted oceanic exchange. Interconnected lagoons (La Joya, Cabeza de Toro, Buenavista) communicate with the GT through a dredged channel 2.4 km long (San Marcos) that leads into the inlet of the estuarine channel (Boca del Cielo). The system shows a high concentration of nutrients; therefore, it is considered one of the most productive coastal lagoons in the Mexican Pacific (Contreras, 2010; Contreras-Espinosa & Zabalegui-Medina, 1991). Here, we established 15 sampling sites (#11-25; Fig. 1B). The samples were collected between May 2013 and June 2016.

Los Patos-Solo Dios (113 km²) comprises several small and shallow lagoons (Los Patos, El Mosquito, La Balona, Pampita) interconnected by narrow channels, and connected to the GT through the dredged channel Joaquín Amaro (12 km). A greater number of ephemeral streams drain into the system, so mesohaline conditions prevail seasonally. Because the Barra de Santiago-Iolomita inlet is closed, the main tidal influence occurs through channels that are connected to adjacent systems. Nine sampling sites (#26-34) were established (Fig. 1C). In this system, collections were made between August 2014 and October 2015.

Fish were collected with a 20-m long by 2-m deep and 56-mm-mesh-size gill net, a 4-m diameter and 15 mm-mesh-size casting net, a 5- and 10-m long by 2-m deep and 5 mm-mesh-size seine nets, spoon net, cod-end net, harpoon, and some complementary samples from local fishermen. At most sampling events, salinity at mid-water was measured with a refractometer or a multiprobe meter (to the nearest 0.1 psu). The fish specimens were fixed in a 10% formalin solution during 1 week, then washed in water during 1 day, and finally preserved in 70% ethanol. Then they were deposited in the fish collection (CHIS-PEC-210-03-09) of the Museum of Zoology, Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas (UNICACH, Tuxtla Gutiérrez, Chiapas, Mexico; see museum vouchers in
Appendix).

Fish were identified to species level with the taxonomic keys of Bussing and López (2011), Castro-Aguirre et al. (1999), Fischer et al. (1995), and Miller et al. (2009), original descriptions, and recent systematic reviews. The systematic checklist was arranged by order and family following the classification of Nelson (2006); genera and species within families were arranged in alphabetical order. Nomenclature of taxonomic units follows Eschmeyer et al. (2016). For a general description of the fish community structure, the species recorded between 2013 and 2015 through standardized sampling (with cast net, gill net, and seine net) were classified by their residency status in lagoon-estuarine systems using the relative frequency of occurrence as: Permanent resident (> 80%), Seasonal/Recurrent visitor (50-80%), Transient/Occasional visitor (20-49%), and Rare (< 19%).

The ecogeographical affinity classification according to salinity tolerance was based on criteria of Castro-Aguirre et al. (1999), Miller (1966), and Myers (1949). The species were classified into 4 groups: estuarine resident, euryhaline, stenohaline, and freshwater (primary or secondary). The biogeographical affinities and distributional ranges of the species were based on Briggs (1974, 1995), Castro-Aguirre et al. (2006), and Robertson and Cramer (2009), using the following categories: San Diegan Province, Cortés Province, Mexican Province, Panamic Province, Circumtropical, Amphi-Pacific, Amphi-American, and Freshwater. The global conservation status and risk categories were based on the IUCN Red list (IUCN, 2016) and Mexican
law NOM-059-SEMARNAT-2010 (Semarnat, 2010).

Results

This study recorded 120 species belonging to 87 genera, 52 families, 19 orders and 2 classes. The order Perciformes is the most diverse, with 66 species, representing 56% of the total recorded species. The most speciose families were Carangidae (9 spp.), Gerreidae (7), and Engraulidae (6), whereas Poeciliidae, Lutjanidae, Haemulidae, Sciaenidae, and Gobiidae had 5 species each. Twenty-six families had only 1 species. The checklist (Table 1) shows the presence of species in each system.

The most frequent species in the studied systems were Gerres simillimus (62% of the sampling stations), Astatheros macracanthus (62%), Diapterus brevirostris (59%), Eucinostomus currani (56%), Centropomus robalito (56%), Lile gracilis (53%), and Gobionellus microdon (50%). Fifty-three percent of the species were recorded using the standardized methods. The structure of the fish assemblages based on the residency status is characterized mainly by rare species (82%). Only 1 species is categorized as permanent resident: L. gracilis. Another 3 species are categorized as seasonal or recurrent visitors: A. macracanthus, C. robalito, and Mugil curema; 7 are classified as transient or occasional visitors.

Values and ranges of salinity are presented here for 97 species collected at sites with conditions ranging from limnetic (0.6 psu) to hyperhaline (45 psu) in all 3 systems. The specific richness according to ecological affinity based on salinity tolerance is shown in Figure 2.

Zoogeographically, the ichthyofauna was mainly related to 3 provinces: Panamic (80.7%), Mexican (79.8%), and Cortés (73.1%). A few fish are related to Circumtropical (3.4%), Amphi-Pacific (1.7%), or Amphi-American (0.8%) distributional patterns. The Freshwater component is represented by families Lepisosteidae (Atractosteus tropicus), Characidae (Astyanax aeneus), Anablepidae (Anableps dowei), Poeciliidae (Poecilia nelsoni, Poecilia sphenops, Poeciliopsis fasciata, P. pleurospilus, P. turrubarensis), and Cichlidae (Amphilophus trimaculatus, Astatheros macracanthus). The only exotic component is the cichlid Oreochromis niloticus. Four species were recorded with some national or international risk category (Table 1).

Discussion

The fish composition recorded in this study is similar to that reported in other coastal lagoons in the GT (Gómez-González et al., 2012; Tapia-García et al., 1998). This represents 21.7% of the continental components (548 spp.) and 8.6% of all the shore-fish fauna (1,358 spp.) known for the Tropical Eastern Pacific (Robertson &

Allen, 2015). Likewise, the checklist contains 66% of continental fishes recorded in the coastal basins of Chiapas (165 spp.; Pacific Subprovince; Velázquez-Velázquez et al., 2013). Additionally, this study reports 10 species that had not been previously recorded in inland waters of Chiapas: Atherinella panamensis, Fistularia commersonii, Epinephelus labriformis, Pseudupeneus grandisquamis, Stegastes flavilatus, Halichoeres dispilus, Nicholsina denticulata, and Acanthurus xanthopterus.

Differences in species richness among the 3 systems may be associated with factors such as seasonal pattern, rainfall, diversity of habitats, lagoon area, width and dynamics of inlets, substrate, and mangrove cover (González-Acosta et al., 2005; Mendoza et al., 2009; Raz-Guzmán & Huidobro, 2002). The highest richness was found in the MM system with 89 species, which is higher than the 66 reported by Tapia-García et al. (1998) in the same locality, although in our study fewer stations were sampled. This system has the highest diversity of euryhaline and stenohaline marine components, reflecting a strong marine influence. Lower richness and diversity of marine species in PSD are due to a limited oceanic exchange, because the main inlet of the system remained closed during the sampling period. Checklists for the JB and PSD systems are documented for the first time here.

Species richness in both MM and JB systems was higher than reported for other coastal lagoons of the GT, such as Superior-Inferior (47 spp.; Tapia-García & Mendoza-Rodríguez, 2005), Oriental-Occidental (72 spp.; Chávez, 1979), or Carretas-Pereyra (67 spp.; Gómez-González et al., 2012). At a regional scale, the area of the lagoon-estuarine system and the width of the adjacent continental shelf may be critical to determine the fish richness (Passos et al., 2012; Vasconcelos et al., 2015). Area partly explains the high richness in MM, which is more extensive (720 km²) than other South Pacific estuarine systems with fewer species: Carretas-Pereyra (36 km²), Chacahua (6 km²; Mendoza et al., 2009), Chautengo (34 km²), and Tres Palos (50 km²; Yáñez-Arancibia, 1978). However, this variable is not sufficient to explain the high richness of systems, which are small in surface, but display great environmental heterogeneity, e.g., Chantuto-Panzacola (143 spp., 180 km²; Gómez-González et al., 2012). Also, a part of such differences among ichthyofaunas may be due to incomplete sampling in all the diversity of estuarine habitats, and a lack of standardization in the use of fishing gear for surveys (Blaber, 2002).

In this study, elasmobranchs were represented by order Myliobatiformes, with 4 species. Castro-Aguirre et al. (1999) mentioned unpublished records of 18 species (8 families) with presence in MM at the locality of Paredón. Most species of elasmobranchs are stenohaline, and their incursion into brackish waters can be associated with high salinity during the dry season.

The high diversity of Engraulidae, Carangidae, and Gerreidae is commonly found in coastal lagoons of the GT (e.g., Tapia-García et al., 1998; Tapia-García & Mendoza-Rodríguez, 2005; Gómez-González et al., 2012). The euryhaline capacity of many species in these families is key to explain the structure of demersal fish communities, related to the heterogeneity of intertidal environments (Martínez-Muñoz et al., 2016).

Marine ichthyofauna in estuarine-lagoons of the GT is composed of many species widely distributed between the provinces Cortés and Panamic, dominating species of tropical derivation over those of temperate origin. Although the GT is located at a critical point of the Central American gap, this has a limited effect on the fish fauna at the regional level in the Mexican tropical Pacific (Palacios-Salgado et al., 2014; Robertson & Cramer, 2009). From the standpoint of the continental biogeography, the Pacific slope provinces in northern and nuclear Central America are characterized by a low representation of primary derivation species (Cichlidae and Poeciliidae are the most speciose families), dominating components of marine and neotropical origin (Lozano-Vilano & Contreras-Balderas, 1987; Matamoros et al., 2015; Myers, 1966).

The exotic cichlid O. niloticus was found in JB; this is its third record in estuarine localities in Chiapas (Gómez-González et al., 2012). Although the species is not widely distributed in these environments, their presence implies a potential impact on native communities, considering the constant release of organisms, deliberate or incidental, as part of public policies for aquaculture development.

This work provides a data set relevant for assessing the composition of estuarine fish fauna in a poorly studied region. While the high number of species found reflects the extent of the inventoried area and the sampling effort with multiple fishing gears, it is also due to the complexity of their coastal lagoons. The list may be increased by sampling in other habitats, such as mangroves, marshes, and swamps. Intertidal environments in the GT could be among the most diverse in the Mexican Pacific (Gómez-González et al., 2012). Although it has been suggested that the Tropical Eastern Pacific fish fauna is well studied (Allen & Robertson, 1998; Robertson & Allen, 2015), information specific to most coastal lagoons is still scant. Increased knowledge of the fish fauna can generate inputs for a more precise regionalization of coastal areas. Annotated checklists represent an essential component for the development of management strategies in a priority region for artisanal fisheries and coastal ecosystems conservation.

Acknowledgements

We thank all the students of the Biology and Marine Biology & Watershed Management academic programs at UNICACH for their assistance during fieldwork and Adán Gómez-González for his expertise in species identification. Also thanks to the fishing cooperatives of Santa Brígida (La Gloria, Arriaga), Miguel Hidalgo y Costilla (La Polka, Tonalá), Unión y Trabajo (Joaquín Amaro, Pijijiapan), and El Madresal Ecotourism Center (Ponteduro, Tonalá), especially to Juan Flores, Mauricio Ovando, Nahum Ordóñez, Jesús Villalobos, Fabián Ordóñez, and their families. Anonymous reviewers provided useful suggestions. The collection of endangered species was performed under permit SGPA/DGVS/00488/16. This paper constitutes a partial fulfillment by the first author of the requirements to obtain a Doctor of Science degree within the Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México. El Consejo Nacional de Ciencia y Tecnología granted a scholarship to the first author.

Appendix. Museum vouchers of specimens from 3 lagoon-estuarine systems in the northeastern Gulf of Tehuantepec, deposited in the ichthyological collection at the Museo de Zoología of the Universidad de Ciencias y Artes de Chiapas (#MZ-P-UNICACH). Numbers in parentheses indicate the number of sampling station where the specimen was collected (see Fig. 1). Species are arranged in alphabetical order.

Aboma etheostoma: 5462(14), 5730(11), 6940(24); Abudefduf troschelli: 7108(22); Acanthurus xanthopterus: 7103(22), 7110(10); Achirus mazatlanus: 5460(19), 5476(21), 5483(24), 6055(25), 6115(27), 6117(28), 6126(30), 6144(31), 6155(33), 6168(34),  6170(1), 6780(3), 6785(4), 7088(9); Achirus scutum: 3352(10), 5488(21); Albula esuncula: 3324(4), 6041(22); Alphestes multiguttatus: 6093(4); Amphilophus trimaculatus: 5250(11), 5731(14), 5774(15), 5787(18), 5794(23), 5815(26), 5853(27), 5860(30), 5867(31), 6059(32), 6095(33), 6164(34), 6193(2), 6996(4), 7015(7);  Anableps dowei: 5254(17), 5461(19), 5793(21), 5891(27), 6047(31), 6066(33), 6150(1); Anchoa curta: 6986(4); Anchoa ischana: 6161(33); Anchoa lucida: 5219(13), 5463(18), 5766(19), 5898(20), 6143(31), 6965(3); Anchoa mundeola: 5225(14), 5468(12), 5720(13), 5742(11), 5744(15), 5749(16), 5803(26), 5825(27), 5852(28), 5859(29), 5886(2), 6173(3), 6177(7), 6774(8); Anchoa starksi: 6232(33); Anchovia macrolepidota: 5224(14), 5265(15), 6050(28), 6114(31), 6771(32), 6773(34), 6939(4); Astatheros macracanthus: 5036(11), 5216(13), 5230(14), 5253(15), 5258(16), 5470(17), 5471(18), 5723(19), 5734(23), 5776(24), 5780(27), 5785(28), 5796(29), 5822(30), 5850(31), 5896(32), 6057(33), 6122(34), 6172(4), 6969(6), 6974(7); Astyanax aeneus: 5777(12), 6189(33), 6795(29); Atherinella guatemalensis: 5261(11), 5733(12), 5750(17), 5812(18), 5858(26), 5871(30), 5892(31), 6068(1), 6154(2), 6190(7), 6779(8); Atherinella panamensis: 6227(1); Atractosteus tropicus: 5789(31), 6800(34); Awaous trasandeanus: 6044(1); Bairdiella armata: 7030(2); Bathygobius andrei: 6181(22), 7105(21), 7107(24); Batrachoides boulengeri: 3332(1); Batrachoides waltersi: 3333(2), 6231(1); Caranx caninus: 5257(13), 5485(16), 5758(17), 5820(21), 5864(22), 6054(27), 6128(1), 6153(3), 6978(4), 7033(10); Cathorops liropus: 5740(19), 5849(31), 5875(33), 6051(34), 6163(4); Cathorops steindachneri: 5259(17), 5851(19), 5874(31), 6165(33), 6963(34), 7031(7); Centropomus armatus: 5843(23); Centropomus nigrescens: 5255(17), 5835(23), 5842(24), 5846(28), 5897(31), 6069(34); Centropomus robalito: 5037(11), 5228(14), 5264(17), 5472(18), 5728(19), 5775(23), 5795(24), 5837(26), 5841(27), 5847(28), 5857(29), 5869(30), 5895(31), 6063(32), 6141(33), 6174(34), 6176(2), 6995(3), 7003(5); Centropomus viridis: 5479(18), 5762(19), 5879(28), 6121(4); Chaetodipterus zonatus: 7029(2), 7097(4); Chaetodon humeralis: 6180(10), 7100(22), 7114(21); Chanos chanos: 7091(2); Chloroscombrus orqueta: 6097(4); Citharichthys gilberti: 5243(21), 5475(22), 6111(10); Ctenogobius sagittula: 6941(21); Cyclopsetta panamensis: 6160(4); Cynoscion albus: 6132(2); Dactyloscopus amnis; 6810(32); Dactyloscopus lunaticus: 6187(10); Diapterus brevirostris: 5215(11), 5242(13), 5738(14), 5739(15), 5751(16), 5798(17), 5799(18), 5863(19), 6116(25), 6129(26), 6137(27), 6184(31), 6775(33), 6783(34), 6957(1), 6960(3), 6973(4), 6976(5), 6983(5), 7006(7); Diodon hystrix: 5477(22); Dormitator latifrons: 5227(11), 5480(12), 5732(19), 5755(23), 5772(24), 5790(26), 5887(27), 6065(30), 6112(31), 6782(32), 6788(33), 6798(34); Eleotris picta: 5724(21), 5873(22), 6166(25), 7112(31), 7113(34); Elops affinis: 5725(11), 6099(4), 6188(21), 6943(22); Epinephelus labriformis: 6102(22), 7012(21); Erotelis armiger: 5877(34); Etropus crossotus: 6151(1); Eucinostomus currani: 5229(11), 5241(13), 5251(14), 5490(15), 5759(16), 5764(17), 5801(18), 5813(19), 5824(22), 5832(23), 5833(25), 5838(32), 6064(33), 6109(34), 6139(1), 6140(3), 6159(5), 6778(8), 7000(10); Eucinostomus dowii: 5233(3), 6984(22); Eucinostomus gracilis: 6228(5); Eugerres axillaris: 5034(11), 5260(12), 5718(13), 5721(14), 5746(15), 5767(16), 5817(17); Eugerres lineatus: 5469(13), 5482(14), 5781(18), 5810(19), 6106(4), 6961(5), 7008(33); Fistularia commersonii: 5894(21); Genyatremus pacifici: 6101(2), 6135(4); Gerres simillimus: 5040(11), 5214(12), 5220(13), 5252(14), 5473(15), 5491(16), 5805(17), 5809(18), 5836(19), 5840(22), 5865(23), 5870(30), 6052(33), 6110(1), 6113(2), 6157(3), 6959(4), 6970(5), 6975(6), 7002(7), 7034(10); Gobiomorus maculatus: 5226(23), 5783(24), 5829(26), 5855(28), 5861(29), 6049(30), 6060(31), 6169(32), 6171(33), 6175(1), 6967(6), 6992(7); Gobionellus microdon: 5018(11), 5035(13), 5039(15), 5717(16), 5747(17), 5839(19), 6125(25), 6136(26), 6149(27), 6167(29), 6178(30), 6185(31), 6229(32), 6781(34), 6786(1), 6794(2), 7090(5); Haemulopsis axillaris: 5223(21); Haemulopsis leuciscus: 6124(2); Halichoeres dispilus: 7101(22); Hemicaranx zelotes: 6226(10); Hippocampus ingens: 7092(22); Hoplopagrus guentherii: 4632(4), 7098(25); Hyporhamphus naos: 3387(10), 5757(22), 6956(8), 7016(9); Hyporhamphus rosae: 6100(10); Kyphosus analogus: 6120(10); Lile gracilis: 5221(11), 5467(12), 5716(13), 5722(14), 5743(15), 5760(16), 5768(17), 5779(18), 5788(19), 5816(29), 5823(30), 5845(31), 6162(32), 6770(33), 6772(34), 6977(7), 6979(10), 7024(1); Lile nigrofasciata: 5756(22); Lutjanus argentiventris: 4633(20), 5474(21), 5792(22), 5802(25), 5808(32), 6972(4), 7085(7); Lutjanus colorado: 4631(4), 5806(21), 6158(2); Lutjanus guttatus: 6105(2); Lutjanus novemfasciatus: 4634(18), 5763(21), 5834(23), 5868(4), 6966(6), 7104(22); Membras gilberti: 5240(21), 5459(22), 6108(10); Menticirrhus nasus: 7096(25); Microdesmus dorsipunctatus: 5263(22), 7094(21); Micropogonias altipinnis: 6230(2); Mugil cephalus: 5489(12), 5804(15), 5827(16), 5828(18), 7109(31); Mugil curema: 5212(11), 5262(12), 5466(13), 5486(16), 5769(17), 5800(18), 5811(19), 5814(21), 5821(22), 5824(26), 5899(27), 6067(31), 6119(32), 6131(34), 6138(1), 6142(3), 6152(6), 6182(10); Mugil hospes: 5232(21), 5245(22), 5807(15) 5807(18), 6043(2), 7001(5); Nematistius pectoralis: 7093(2); Nicholsina denticulata: 5244(22); Oligoplites altus: 5038(13), 5217(14), 5266(15), 5478(16), 5819(19), 5830(22), 6045(27), 6094(28), 6127(4), 6183(5), 6969(6), 6971(7), 7004(8), 7014(10); Oligoplites saurus: 5487(19), 5791(20), 5831(21), 5854(22), 5862(26), 6118(33), 6186(5), 7007(10); Ophichthus zophochir: 0081(2); Opisthonema libertate: 5484(4), 6053(2), 6103(21), 6179(22), 6980(10); Orthopristis chalceus: 5222(21); Oreochromis niloticus: 5481(12); Paralonchurus goodei: 7028(2); Poecilia nelsoni: 5231(11), 5256(12), 5736(17), 5784(23), 5797((27), 5893(28), 6061(31), 6146(32), 6148(33), 6191(34), 6789(1), 6797(2), 6994(6), 7020(7); Poecilia sphenops: 5773(12), 5876(27), 6058(28), 6062(30), 6156(31), 6787(33), 6791(34), 6799(1), 6998(2); Poeciliopsis fasciata: 5735(11), 5771(12), 6790(28), 6793(33), 7018(7), 7025(8); Poeciliopsis pleurospilus: 5737(11), 5888(26), 6769(27), 6777(28), 6792(31), 6988(33), 7023(7); Poeciliopsis turrubarensis: 5463(19), 5786(20), 5872(27), 5890(31), 6147(32), 6776(33), 6964(34), 6991(1), 6993(6), 7019(7), 7021(8); Polydactylus approximans: 6225(21), 6945(10); Polydactylus opercularis: 6133(2); Pomadasys macracanthus: 6145(3), 7005(4), 7027(5), 7035(7), 7099(9); Pseudobalistes naufragium: 7111(10), 7164(22); Pseudophallus starksii: 6192(7), 7012(8); Pseudupeneus grandisquamis: 6130(2); Rhinoptera steindachneri: 7116(10); Sciades guatemalensis: 5465(13), 5818(16), 5844(18), 5848(19), 5889(27), 6167(31),6962(33), 6989(3); Sciades seemanni: 5782(21), 6042(26), 6134(33), 6981(4); Scomberomorus sierra: 6096(4); Selene orstedii: 6123(2); Selene peruviana: 6104(2); Sphoeroides annulatus: 5213(21), 6046(10), 7106(22); Sphoeroides rosenblatti: 6098(22); Sphyraena ensis: 7117(22); Stegastes flavilatus: 7095(22); Strongylura exilis: 7009(8); Styracura pacifica: 6942(21), 7163(1); Symphurus elongatus: 7165(1); Synodus scituliceps: 7118(9); Trachinotus kennedyi: 6056(4); Trachinotus rhodopus: 6946(10), 7032(21); Urotrygon chilensis: 6944(10); Urotrygon nana: 6048(10).

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