Occurrence of Holacanthus clarionensis (Pomacanthidae), Stegastes leucorus, and Stegastes acapulcoensis (Pomacentridae) at Magdalena Bay, B.C.S., Mexico
© Hernandez Velasco et al. 2016
Received: 7 June 2016
Accepted: 8 June 2016
Published: 27 July 2016
Pomacanthids and Pomacentrids are mainly distributed in tropical and subtropical regions, and inhabit shallow rocky and coral reefs. Due to their colorful patterns and unusual body shapes, they have been widely targeted by aquarium fish trade; these species are of great commercial interest. Here we document the occurrence of one Pomacanthid (Holacanthus clarionensis), and two Pomacentrids (Stegastes acapulcoensis, and S. leucorus) north of their reported distribution range during the 2014 warm water period in the eastern Tropical Eastern Pacific. Sightings took place at Magdalena-Almejas Bay complex, located in the western margin of the Baja California Peninsula. Using a series of abiotic data for the Tropical Eastern Pacific, we created a maximum entropy model for each species and identified that high probability of occurrence at Magdalena-Almejas Bay complex was only denoted for S. leucorus. Here we report the occurrence of H. clarionensis, S. acapulcoensis and S. leucorus 70 km, 300 km, and 300 km north of the northernmost reported limits.
KeywordsReef fish Pomacanthidae Pomacentridae Zoogeography Occurrence
Pomacanthids (angelfishes) and Pomacentrids (damselfishes) are mainly distributed in tropical and subtropical regions, and inhabit rocky and coral reefs between 1 and 30 m deep; a few species range to depths of 80 m or more (Thomson et al., 2000; Robertson & Allen 2008). Eschmeyer & Fong (2015) and Nelson (2006) report a total of 89 angelfish, and 387 damselfish species distributed around the world’s oceans. Along the Mexican coast, in the Eastern Tropical Pacific, registered species of this family include four angelfishes: Pomacanthus zonipectus (Gill, 1862), Holacanthus passer (Valenciennes, 1846), H. limbaughi (Baldwin, 1963), and H. clarionensis (Gilbert, 1891), and 13 damselfishes: Abudefduf troschelii (Gill, 1862), A. declivifrons (Gill, 1862), Azurina hirundo (Jordan & McGregor in Jordan & Evermann, 1898), Chromis alta (Greenfield & Woods, 1980), C. atrilobata (Gill, 1862), C. limbaughi (Greenfield & Woods, 1980), Hypsypops rubicundus (Girard, 1854), Microspathodon bairdii (Gill, 1862), M. dorsalis (Gill, 1862), Stegastes acapulcoensis (Fowler, 1944), S. flavilatus (Gill, 1862) S. leucorus (Gilbert, 1892) S. rectifraenum (Gill, 1862), and S. redemptus (Heller & Snodgrass, 1903).
Due to their colorful patterns and unusual body shapes, angelfish and damselfish have been widely targeted by aquarium fish trade, thus many species are of great commercial interest. In fact, damselfishes hold the world’s first place in such trade, while angelfishes are rated as fifth (Wabnitz et al. 2003). Piña-Espallargas et al. (2001) have pointed that H. clarionensis, S. leucorus and S. acapulcoensis are considered as commercially important fish in Mexico’s ornamental fishery.
Internationally, H. clarionensis and S. leucorus are listed as “Vulnerable” species in the International Union for Conservation of Nature (IUCN) red list, as their already limited distribution is likely to be affected by the ongoing climate change, resulting in reduction of actual population sizes (Pyle et al., 2010; Allen et al. 2010a, 2010b). In addition, these three species are not listed in any appendix of the Convention of International Trade of Endangered Species of Wild Fauna and Flora (CITES). Nevertheless, at a national level the only species with a degree of vulnerability is H. clarionensis, listed as needing “Special protection” due to their great demand by aquarium trade industry and their limited range of distribution to the Mexican Pacific (Diario Oficial de la Federación, 2010).
In this paper we document the occurrence of H clarionensis, S. acapulcoensis, and S. leucorus north of their reported range of distribution. Given the ecological and economic importance of such species, this information should be taken into account for future decisions making in conservation and management subjects.
Materials and methods
Sampling effort for five monitoring sites at Isla Magdalena from 2010 to 2014
To determine the currently accepted geographical range of the species we used specialized literature (Allen 1998; Robertson & Allen 2008), and looked at information about specimens housed in over 20 collections of Mexico and the United States, available in the Global Biodiversity Information Facility webpage (GBIF, 2015), the Ocean Biogeographic Information System (OBIS, 2015), FishBase (Froese & Pauly, 2014), and VerNet (2015).
We used the maximum entropy software MaxEnt ver. 3.3.3 k (Phillips et al., 2006) to develop an ecological niche model of the species on the basis of occurrence records and on yearly average, annual range, maximum and minimum surface values of a series of oceanographic factors (9 × 9 km pixel resolution). Temperature (°C), chlorophyll a concentration (mg/m3), photosynthetic active radiation (Einstein/m2/day), and water transparency (1/m) were obtained from the Ocean Color Radiometry Online Visualization and Analysis Tool (GIOVANNI) of the National Aeronautics and Space Administration of the United States (NASA; http://gdata1.sci.gsfc.nasa.gov/daac-bin/G3/gui.cgi?instance_id=ocean_month). Salinity (PSU), dissolved oxygen (ml/l), and concentration of nitrate, phosphate, and silicate (μmol/l) were obtained from the World Ocean Atlas 2009 of the National Oceanic and Atmospheric Administration (NOAA; http://www.nodc.noaa.gov/OC5/SELECT/woaselect/woaselect.html). Calcite concentration and pH were estimated using the program CO2SyS (http://carboocean.iopan.gda.pl/co2sys.htm), from data on temperature, salinity, silicate, nitrate and atmospheric concentration of carbon dioxide (obtained from the Scripps Institution of Oceanography CO2 Program; http://scrippsco2.ucsd.edu/). Bathymetry (m) and coastal type (soft or hard bottom) were obtained from the Global Bathymetric Chart of the Oceans (www.gebco.net), and Google Earth, respectively. The modeling area was defined considering the known geographic range of the species, from 39.5°N to −10.5°S of latitude, and from −130.5°W to −77°W of longitude for S. acapulcoensis and S. leucorus; and from 27°N to 17°N of latitude, and from −116.5°W to −105°W of longitude for H. clarionensis. For modeling, in MaxEnt we used a maximum iteration value of 1000 and the logistic output to evaluate probability of occurrence of the species in each pixel in a scale of 0 to 1 representing the suitability of each pixel, being 0 unsuitable and 1 very suitable. By consensus, values of 0.5 and higher represent presence of the species at that pixel (Peterson et al., 2011). Model accuracy was determined with the area under the curve (AUC) of the threshold independent receiver operating characteristic analysis (ROC). Occurrence data were randomly partitioned into 75 % for training and 25 % for testing (Franklin, 2009).
Previously reported northern endpoints for Holocanthus clarionensis, Stegastes acapulcoensis, and S. leucorus and records of this study
Northernmost limit in Baja California’s Pacific Coast
This is the first occurrence of H. clarionensis, S. leucorus y S. acapulcoensis at Bahia Magdalena. Presence of these species in the northern limit of the Tropical Eastern Pacific Province and previous records in Pacific islands might indicate a tendency in which tropical fish species are extending their ranges towards temperate environments. This tendency, also reported for species in the Gulf of California (González-Cuéllar et al., 2013; Martínez-Torres et al., 2014; Fernández-Rivera Melo et al., 2015), might be explained by the warm water intrusions into northern regions reported for 2014 (Peterson et al. 2015).
The model outputs showed that bathymetry and coastal type were the most important variables limiting the distribution of the three species, in agreement with the preferred habitat characteristics preferred by Pomacanthids and Pomacentrids: rocky and coral reefs in shallow tropical and subtropical waters (Robertson & Allen 2008). Nevertheless, the potential niche is determined by a series of biotic (e.g., food availability, predator abundance, competition) and abiotic (e.g., temperature, depth, salinity) factors, which allow a species to maintain a stable population (Peterson et al., 2011). Even though coast bathymetry and coast type requirements were met, other factors such as temperature, food availability and competition with native species may not allow these species to increment their abundances, and establish viable populations.
In conclusion, the results of this paper extend the currently known distribution northern endpoints for H. clarionensis, S. acapulcoensis, and S. leucorus. Low densities along with the absence of juveniles suggest that their reproductive populations have not established in Magdalena-Almejas Bay Complex. Nevertheless, currently rising temperatures and the confirmation of positive temperature anomalies during the possible 2015 El Niño event might promote their establishment.
AUC, area under the curve; CITES, Convention of International Trade of Endangered Species of Wild Fauna and Flora; GBIF, Global Biodiversity Information Facility; GIOVANNI, Ocean Color Radiometry Online Visualization and Analysis Tool; IUCN, International Union for Conservation of Nature; NASA, National Aeronautics and Space Administration of the United State; NOAA, National Oceanic and Atmospheric Administration; OBIS, Ocean Biogeographic Information System; PSU, Practical Salinity Units; ROC, receiver operating characteristic analysis
We thank Roger Romero, Ernesto Romero, Norberto Estala, Raul Romero, Daniel Valdez, Ulises Gomez, Alberto de la Toba, Christian Alducin, and Alfonso Romero for their support and participation in the monitoring of this work. Members of the fishing cooperative “Magdalena” provided invaluable help in the field.
This study was funded by David and Lucile Packard Foundation and Walton Family Foundation.
Availability of data and materials
Authors do not wish to share data used in this project, as it represents a subset of databases of private-owned (by fishers) no-take marine reserves. Nevertheless, data may be available upon contact of the main author, AHV.
AHV and FJFRM performed field surveys, SMMM performed the MaxEnt models, and JCVD managed the database and performed other analysis. All authors contributed equally to writing the paper. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Allen G, Robertson R. Fishes of the Tropical Eastern Pacific. University of Hawaii Press. Honolulu, Hawaii, USA. 1994. p. 335.Google Scholar
- Allen G, Robertson R, Zapata F. Stegastes leucorus, The IUCN Red List of Threatened Species. (version 2014.3.). 2010a. Available at www.iucenredlist.org (Accessed 21 Feb 2015).Google Scholar
- Allen G, Robertson R, Rivera R, Edgar G, Merlen G, Zapata F, Barraza E. Stegastes acapulcoensis, The IUCN Red List of Threatened Species. (version 2014.3.). 2010b. Available at www.iucenredlist.org (Accessed 21 Feb 2015).Google Scholar
- Allen GR. Damselfishes. In: Paxton J, Eschmeyer W, editors. The world encyclopedia of fishes. 2nd ed. San Diego: Academic; 1998. p. 205–8.Google Scholar
- Álvarez-Borrego S, Galindo-Bect LA, Chee-Barragán A. Características hidroquímicas de Bahía Magdalena, BCS. Cienc Mar. 1975;2:94–110.Google Scholar
- Diario Oficial de la Federación. Norma Oficial Mexicana. México: NOM-059-ECOL-2010; 2010. p. 78.Google Scholar
- Eschmeyer WN, Fong JD. Species by family/subfamily, Catalog of fishes, California Academy of Sciences. (version 03/2015). 2015. Available at: http://research.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp. (Accessed 21 Feb 2015).Google Scholar
- Fernández-Rivera Melo FJ, Reyes-Bonilla H, Campos-Dávila L, Balart EF. Extension of range of Lutjanus inermis (Peters, 1896) (Perciformes: Lutjanidae) to the central region of the Gulf of California, Mexico. J Appl Ichthyol. 2015.
- Franklin J. Mapping species distributions: spatial inference and prediction. Cambridge: Cambridge University Press; 2009. p. 320.Google Scholar
- Froese R, Pauly D, editors. FishBase. 2014 (version 11/2014).Available at: http://www.fishbase.org (Accessed 21 Feb 2015).Google Scholar
- Galván-Magaña F, Gutiérrez-Sánchez F, Abitia-Cárdenas LA, Rodríguez-Romero J. The distribution and affinities of the shore fishes of the Baja California Sur lagoons. In: Manuwar M, Lawrence SG, Manuwar IF, Malley DF, editors. Aquatic Ecosystems of Mexico: Status and Scope, Ecovision World Monograph Series. Backhuys Publishers; 2000. p. 383–98
- Gardner SC, Chávez‐Rosales S. Changes in the relative abundance and distribution of gray whales (Eschrichtius robustus) in Magdalena Bay, Mexico during an El Niño event. Mar Mamm Sci. 2000;16:728–38.View ArticleGoogle Scholar
- Global Biodiversity Information Facility. 2015. (version 2/2015). Available at: http://data.gbif.org (Accessed 21 Feb 2015).
- González-Cuéllar OT, Reyes-Bonilla H, Fourriére M, Rojo M, Hernández-Velasco A, Sánchez-Alcántara I, Pfister T. Range extensions of four species of parrotfishes (Scaridae) in the northern Gulf of California, Mexico. Cybium. 2013;37:223–6.Google Scholar
- Humann P, de Loach N. Reef fish identification: Baja to Panama. Jacksonville: New World Publications; 2004.Google Scholar
- Martínez-Torres M, Reyes-Bonilla H, Fernández-Rivera Melo FJ, Sánchez-Alcántara I, González-Cuellar OT, Morales-Portillo CD. Range extension of the blue and yellow damselfish Chromis limbaughi (Pomacentridae) to the northern Gulf of California, Mexico. Mar Biodiversity Rec. 2014;7:e43. doi:10.1017/S1755267214000281.View ArticleGoogle Scholar
- Nelson JS. Fishes of the world. 4th ed. Hoboken: Wiley; 2006. p. 601.Google Scholar
- Ocean Biogeographic Information System. 2015. 2015 (version 02/2015). Available at: http://www.iobis.org/ (accessed 21 Febrary 2015).Google Scholar
- Peterson AT, Soberón J, Pearson RG, Anderson R, Martínez-Meyer E, Nakamura M, Araújo M. Ecological niches and geographic distributions. Princeton: Princeton University Press; 2011.Google Scholar
- Peterson W, Robert M, Bond N. The warm blob - Conditions in the northeastern Pacific Ocean. PICES Press23.1; 2015. p. 36–8. Winter 2015. http://search.proquest.com/openview/481857b39c09789c693933a903bbde8a/1?pq-origsite=gscholar.
- Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distribution. Ecol Model. 2006;190:231–59.View ArticleGoogle Scholar
- Piña-Espallargas R, Reyes-Bonilla H, Ortuño-Manzanares G, Garcáa-Náñez NE, Mendoza-Vargas L, González-Ania LV. Especies marinas de ornato del Golfo de California. In: Sustentabilidad y pesca responsable en México: evaluación y manejo. Mexico: INP-SAGARPA; 2001. p. 878–914.Google Scholar
- Pyle R, Myers R, Rocha LA, Robertson R. Holacanthus clarionensis, The IUCN Red List of Threatened Species. (version 2014.3.). 2010. Available at www.iucenredlist.org (Accessed 21 Feb 2015).Google Scholar
- Robertson RR, Allen GR. Shorefishes of the tropical eastern Pacific online information system. 2008 (version 184.108.40.206). Availble at: http://biogeodb.stri.si.edu/sftep/intro1.php (Accessed 21 Feb 2015).Google Scholar
- Thomson DA, Findley LT, Kerstitch AN. Reef fishes of the Sea of Cortez. University of Texas Press, Austin, TX. 2000.Google Scholar
- VerNet. 2015. (version 09/2014). Available at: http http://www.vertnet.org/ (Accessed 21 Feb 2015)
- Wabnitz C, Taylor M, Green E, Razak T. From Ocean to Aquarium. 2003. UNEP-WCMC.Google Scholar
- Zaitsev O, Sánchez-Montante O, Saldivar-Reyes M. Seasonal variations of the thermohaline structure in the Magdalena-Almejas Bay lagoon system and adjacent sea. Cienc Mar. 2010;36(4):413–32.View ArticleGoogle Scholar
- Zarate-Ovando B, Palacios E, Reyes-Bonilla H, Amador E, Saad G. Waterbirds of the Lagoon Complex Magdalena Bay-Almejas, Baja California Sur, Mexico. Waterbirds. 2006;29:350–64.View ArticleGoogle Scholar