Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2017 | 9(8): 10571–10576

 

 

 

 

 

A new record of Harlequin Shrimp (Malacostraca: Decapoda: Palaemonidae: Hymenocera picta Dana, 1852) in the southern Mexican Pacific Reefs

 

 

Omar Valencia-Mendez 1, Andres Lopez-Perez 2, Betel Martinez-Guerrero 3, Virgilio Antonio-Perez 4 & Eduardo Ramirez-Chavez 5

 

 

1 Programa de Doctorado en Ciencias Biológicas y de la Salud, 2 Departamento de Hidrobiología, Universidad Autónoma Metropolitana, San Rafael Atlixco 186, Col. Vicentina CP09340, Ciudad de México, México

3,5 Universidad del Mar, Campus Puerto Ángel, Carretera a Zipolite Km. 1.5, Col. Puerto Ángel, San Pedro Pochutla, Oaxaca, 70902, México

4 Buceo Huatulco, Ocotillo # 206, La Crucecita, Bahías de Huatulco, Oaxaca, 70989, México

1 ovalenciam@outlook.com, 2 alopez@xanum.uam.mx (corresponding author), 3 alpheusb@hotmail.com, 4 hoy.bucea@gmail.com, 5 eduardo@angel.umar.mx

 

 

 

 

 

doi: http://doi.org/10.11609/jott.3238.9.8.10571-10576 | ZooBank: urn:lsid:zoobank.org:pub:4BF4E504-DBFB-4CFE-9603-D8B4943DC5D2

 

Editor: Mary K. Wicksten, Texas A&M University, College Station, USA. Date of publication: 26 August 2017 (online & print)

 

Manuscript details: Ms # 3238 | Received 29 December 2016 | Final received 28 July 2017 | Finally accepted 30 July 2017

 

Citation: Mendez, O.V., A.L. Perez, B.M. Guerrero, V.A. Perez & E.R. Chavez (2017). A new record of Harlequin Shrimp (Malacostraca: Decapoda: Palaemonidae: Hymenocera picta Dana, 1852) in the southern Mexican Pacific Reefs. Journal of Threatened Taxa 9(8): 10571–10576; http://doi.org/10.11609/jott.3238.9.8.10571-10576

 

Copyright: © Mendez et al. 2017. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use of this article in any medium, reproduction and distribution by providing adequate credit to the authors and the source of publication.

 

Funding: Buceo Huatulco, and CONACYT to ALP (#236654)

 

Competing interests: The authors declare no competing interests.

 

Acknowledgements: We wish to express our gratitude to Fernando Álvarez Noguera (IB, UNAM, México), Arthur Anker (Universidade Federal do Ceará, Fortaleza, Ceará, Brazil) and Prakash Sanjeevi (Sathyabama University, Chennai, India) for confirming species identification. We appreciate the help in the field by Jorge Segoviano. Support was provided by Buceo Huatulco, and by grants from CONACYT to ALP (#236654) and doctoral fellowship to OVM (#401738). We want to express our gratitude to two anonymous reviewers.

 

 

 

 

Abstract: The Harlequin Shrimp Hymenocera picta is abundant in the Indo-Pacific and Central Pacific regions, but there are few reports of it from the eastern Pacific. Two pairs of the Harlequin Shrimp were observed feeding on the Sea Star Phataria unifascialis (Gray, 1840) in the reefs of Huatulco National Park, Mexican Pacific. This paper reports the occurrence of H. picta in Mexican Pacific waters and extends its previous distribution by 1,270km north of El Ocotal, Costa Rica in the eastern Pacific equatorial zone. In addition, we evaluate the potential distribution of H. picta along the tropical eastern Pacific using the Maximum-Entropy modelling algorithm.

Keywords: Caridea, coral reefs, harlequin shrimp, Huatulco National Park, sea star predator.

 

 

 

 

 

 

Hymenocera Latreille, 1819 is a monospecific genus that contains Hymenocera picta Dana, 1852, commonly known as “Harlequin Shrimp” or “Painted Shrimp”. Hymenocera is a small decapod crustacean (~5cm in TL) belonging to the superfamily Palaemonoidea Rafinesque, 1815 sensu De Grave & Fransen (2011). Due to its amazing coloration, it is one of the most in-demand decapod crustacean species in the marine ornamental trade, reaching up to 80 USD per pair (Calado et al. 2003).

Hymenocera picta was first described by Dana based on a specimen collected in Raraka, Tuamotu, French Polynesia. Dana’s figures were made from a living specimen; however, holotype specimens were lost in the wreck of the “Peacock” (Edmondson 1923). This event led to the complex and problematic taxonomy for the species (Edmondson 1923). Previously, two nominal species were recognized: Hymenocera elegans Heller, 1862 was described as a species with a white or creamy body with blue or brown blotches with a distribution within the Indo-west Pacific (Debelius 1999), while H. picta differed in the colour of its blotches (wine or red) and with a distribution in the central and eastern Pacific (Hoover 1998). Kawamoto & Okuno (2003) found both colour patterns in Okinawa, Japan suggesting the blotch colour changes according to the species’ diet. As a consequence, H. elegans was re-designated as a junior synonym of H. picta (De Grave & Fransen 2011).

The Harlequin Shrimp is a monogamous and territorial species that typically live in pairs inhabiting shallow waters and associated with holes, crevices and caves in coral reefs (Wickler 1973). The most particular characteristic of the species is its unique coloration (red or blue blotches in the body), and the morphology of the chela (Debelius 1999). Feeding habits of the Harlequin Shrimp are based exclusively on starfish of the Class Asteroidea Blainville, 1830 (Wickler 1973; Prakash & Kumar 2013), being currently referred to as an important biological control of Fromia monilis (Perrier, 1869), Linckia laevigata (Linnaeus, 1758), Mithrodia fisheri Holly, 1932, Asteropsis carinifera (Lamarck, 1816), Nidorellia armata (Gray, 1840), and Acanthaster planci (Linnaeus, 1758) populations (Wickler 1973; Juncker & Poupin 2009; Prakash & Kumar 2013).

Although Hymenocera picta is abundant in the Indo-Pacific regions (Wickler 1973; Seibt & Wickler 1979; Prakash & Kumar 2013), it has also been recorded in the eastern tropical Pacific in the Galapagos Island (Hickman & Zimmerman 2000), Gorgona Island, Colombia (Juan Felipe Lazarus Agudelo, pers. comm. 17 August 2016), Panamá Islands (Canal de Afuera, Pedro González, Uva and Toboga) (Glynn 1977, 1982; Wicksten & Hendrickx 2003), El Ocotal, Costa Rica (Wicksten & Hernández 2000) and Clipperton Island, France (Debelius 1999; Poupin et al. 2009). In this paper, we report the presence of H. picta in Cacaluta Island and Punta Maguey, Mexican Pacific for the first time, therefore extending its distribution 1, 270km north from its previous record in Central America.

 

 

Material and Methods

The present record is based on field observations in Huatulco National Park (HNP) of H. picta at two different times. While conducting biological censuses of reef associated invertebrates and vertebrates in HNP, we (OVM and VAP) observed a pair of Harlequin Shrimps in Cacaluta Island (15.71888889 N & -96.16194444 W) on March 2014, and another in Punta Maguey (15.73011 N & -96.14611 W) in July 2016 (Fig. 1). Specimens were observed between 10–15 m depth and recorded with video (GoPro Hero 3) and digital photography (Nikon Coolpix Aw120). No specimens were collected since both sites are part of a Natural Protected Area (NPA) and collecting is forbidden without the adequate scientific collecting permit granted by Mexican federal agencies.

Specimens were further identified by taxonomist (Fernándo Álvarez Noguera, Universidad Nacional Autónoma de México; Arthur Anker, Universidade Federal do Ceará, Brazil, and Sanjeevi Prakash, Sathyabama University, India). Finally, the taxonomic validity of the species name was addressed after verification by WoRMS (World Register of Marine Species http://www.marinespecies.org) and ITIS (Integrated Taxonomic Information System http://www.itis.gov) databases.

Furthermore, information of 13 environmental variables (minimum, maximum and average values of sea surface temperature, primary productivity, particulate organic carbon, particulate inorganic carbon and bathymetry) and historical records of occurrence of H. picta around the tropical eastern Pacific (TEP), were used to predict the potential geographic distribution of the species in cells of 4km latitude/longitude in the area. Environmental variables were downloaded from NASA’s Ocean Color Web (http://oceancolor.gsfc.nasa.gov) and processed using the program WIM (Windows Image Manager http://www.wimsoft.com; Kahru 2007). The distribution data of H. picta were gathered from online databases such as Invertebrate Zoology Collections (http://collections.mnh.si.edu/) and Global Biodiversity Information Facility (http://www.gbif.org/). Maximum entropy (Maxent) modelling algorithm version 3.3.3k (Phillips et al. 2006) was used employing default settings. Among the different species distribution model algorithms, Maxent is extensively used for projecting current species distributions (Elith & Leathwick 2009) due to its better predictive performance relative to other modelling algorithms (Elith et al. 2006) even with low sample sizes (Pearson et al. 2007), and its applicability when presence-only data are available (Phillips et al. 2006). Maxent has been described as a modelling method able to fit overly complex environmental response curves (Elith & Leathwick 2009), particularly when using default parameters (Merow et al. 2013); default settings of Maxent have been tested successfully over a wide range of species and environmental conditions (Phillips & Dudík 2008). Finally, probability predictions were interpreted as habitat suitability index (HSI) for H. picta for exploratory purposes only, rather than as the probability of species presence in each cell.

Results

Two pairs of Harlequin Shrimp Hymenocera picta of ~4.5cm in TL, were recorded at Cacaluta Island and Punta Maguey respectively, Huatulco National Park, Mexican Pacific (Image 1). Specimens were observed feeding on the sea star Phataria unifascialis (Gray, 1840) in shallow coral reef waters (at ~10m) dominated by Pocillopora damicornis (Linnaeus, 1758) corals. Specimens were identified on the basis of their coloration (white body with blue and wine coloured blotches), and unique morphologic characteristics such as antennule with lateral flagellum greatly expanded, the 3rd maxilliped with penultimate segment wider than the antepenultimate and 2nd pereopod greatly expanded following the criteria of Wickler (1973) and Mitsuhashi et al. (2005).

A total of 47 historical bibliographic references indicate that the harlequin shrimp have a wide geographical distribution in the Pacific Ocean (Fig. 2). In particular, in the eastern Pacific, literature and museum records indicate that H. picta inhabit the oceanic islands of Galapagos, Gorgona, Malpelo, Perlas and Clipperton; but also in coastal zone as El Ocotal, Costa Rica (Fig. 2). The new record for Cacaluta Island and Punta Maguey (Fig. 1) was located about 1, 279km north from El Ocotal, Costa Rica and 1, 529km northeast from Clipperton Atoll. According to the species distribution model (Fig. 3), the TEP may represent a highly suitable habitat for the occurrence of H. picta. At large spatial scale, high habitat suitability (>0.92) for H. picta may be found between the Gulf of California and Ecuador, including the eastern Pacific oceanic islands, but suitability predicted by the model decrease (<0.85) on the western part of the Baja California peninsula and south of mainland Ecuador. Likewise, bathymetry along with minimum and average sea surface temperature across the TEP is mainly involved in predicting habitat suitability for the species. In particular, habitat suitability for the harlequin shrimp reaches its maximum when minimum sea surface temperature is 250C in shallow waters (<20m), but suitability decreases exponentially when depth increases, or when minimum sea surface temperature is below 250C.

 

 

 

 

 

Discussion

Specimens of H. picta were easily identified because they displayed the typical coloration pattern, which is unique to Hymenocera species. In addition, morphological characteristics observed in Cacaluta Island and Punta Maguey specimens match with those originally addressed by Dana (1852), and in the reviews performed by Wickler (1973) and Mitsuhashi et al. (2005) for specimens recorded in the Indian Ocean, Western and Central Pacific. The new record of H. picta at Cacaluta Island and Punta Maguey, increase the number of new records of crustacean species (García-Madrigal & Andreu-Sánchez 2010; Cortés-Carrasco & García-Madrigal 2013) in the area, but most importantly extends the former distribution of the species by 1, 270km north from Costa Rica (Wicksten & Hernández 2000) and 1, 529km northeast from Clipperton (Debelius 1999; Poupin et al. 2009). The record of H. picta in Mexican Pacific waters, is part of a long list of new records of species previously known to occur in Central America in taxonomic groups as varied as echinoderms (Granja-Fernández et al. 2013), fish (López-Pérez et al. 2010; Zepeta-Vilchis et al. 2013), polychaeta (Bastida-Zavala & Guevara-Cruz 2012) and crustaceans (García-Madrigal & Andréu-Sánchez 2010; Cortés-Carrasco & García-Madrigal 2013). The new record of H. picta presented here along with the above-mentioned records, reinforces the faunal connectivity hypothesis between Central America and southwestern Mexico via the Costa Rica Coastal Current (Fiedler & Talley 2006; Pineda et al. 2007).

Considering the new record presented here, H. picta is distributed as north as southern Mexican Pacific. Species distribution model (Fig. 3) suggest that, at large spatial scale, habitat suitability for the species may extend as far north as the Gulf of California and as far south as the frontier between Ecuador and Peru, corresponding to the full extension of the TEP, whose the most northern and southern distribution limits was defined by the minimum sea surface temperature. According to the model the entire TEP is suitable to harbour H. picta populations, but at small spatial scale that may depend upon the distribution of coral reefs communities and prey availability. Several studies indicate that Harlequin Shrimps inhabit holes and crevices of coral reefs (Glynn 1977, 1982) and prey exclusively upon on starfish of the Class Asteroidea (Wickler 1973; Prakash & Kumar 2013), not only in the eastern Pacific (Glynn 1977, 1982) but across its entire distribution (Prakash & Kumar 2013). During the current study, we observed the harlequin shrimp feeding on the starfish P. unifascialis, while field observations on coral reefs in the Gulf of Chiriquí (Panamá) showed that H. picta feeds on A. planci (Ormond & Campbell 1974; Glynn 1977, 1982). Regardless of the biology (feeding habits), ecology (distribution), and prediction model (Maxent) of H. picta, future detailed prospecting of coral communities and reefs from the eastern Pacific may render more insights on new species records in this area.

 

 

References

 

Bastida-Zavala, J.R. & C. Guevara-Cruz (2012). Estado del conocimiento de los poliquetos (Annelida: Polychaeta) del Pacífico sur de México, pp. 335–355. In: Sánchez, A.J., X. Chiappa-Carrara & R. Brito-Pérez (eds.). Recursos acuáticos costeros del sureste, Vol. I. Conciytey, Fomix, Siidetey, Unacar, Conacyt, UNAM, UJAT, Ecosur, Promep, Recorecos, Mérida, 1106pp.

Calado, R., J. Lin, A.L. Rhyne, R. Araújo & L. Narciso (2003). Marine ornamental decapods-popular, pricey, and poorly studied. Journal of Crustacean Biology 23(4): 963–973; http://doi.org/10.1651/C-2409

Cortés-Carrasco, F. & M.S. García-Madrigal (2013). New records of three brachyuran crabs (Crustacea: Decapoda) from the southern Pacific of Mexico. Marine Biodiversity Records 6: e104; http://doi.org/10.1017/S1755267213000754

Dana, J.D. (1852). Crustacea. Part I. United States Exploring Expedition during the years 1838, 1839, 1840, 1841, 1842, under the Command of Charles Wilkes, U.S.N. Sherman: Philadelphia 1: 1–658.

De Grave, S. & C.H.J.M. Fransen (2011). Carideorum Catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and Caridean Shrimps (Crustacea, Decapoda). Zoologische Mededelingen 85(9): 195–589.

Debelius, H. (1999). Crustacea. Guide of the world. IKAN, Jahr-Verla, Hamburg, 318pp.

Edmondson, C.H. (1923). Crustacea from Palmyra and Fanning Islands. Bishop Museum 5: 1-43.

Elith, J., C.H. Graham, R.P. Anderson, M. Dudík, S. Ferrier, A. Guisan, R.J. Hijmans, F. Huettmann, J.R. Leathwick, A. Lehmann, J. Li, L.G Lohmann, B.A. Loiselle, G. Manion, C. Moritz, M. Nakamura, Y. Nakazawa, J.McC.M. Overton, A. Townsend Peterson, S.J. Phillips, K. Richardson, R. Scachetti-Pereira, R.E. Schapire, J. Soberón, S. Williams, M.S. Wisz & N.E. Zimmermann (2006). Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29: 129–151; http://doi.org/10.1111/j.2006.0906-7590.04596.x

Elith, J. & J.R. Leathwick (2009). Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40: 677–697; http://doi.org/10.1146/annurev.ecolsys.110308.120159

Fiedler, P.C. & L.D. Talley (2006). Hydrography of the eastern tropical Pacific: a review. Progress in Oceanography 69(2-4): 143–180; http://doi.org/10.1016/j.pocean.2006.03.008

García-Madrigal, M.S. & L.I. Andreu-Sánchez (2010). Los cangrejos porcelánidos (Decapoda: Anomura) del Pacífico sur de México, lista de especies y clave de identificación para todas las especies del Pacífico Oriental Tropical. Ciencia y Mar 13(39): 23–54.

Global Biodiversity Information Facility (2014). http://www.gbif.org/occurrence/search?taxon_key= 2225510&HAS_COORDINATE=true&HAS_GEOSPATIAL_ISSUE=false Electronic version accessed 10 July 2016.

Glynn, P.W. (1977). Interactions between Acanthaster and Hymenocera in the field and laboratory. Proceedings of the Third International Coral Reef Symposium 1: 209–215.

Glynn, P.W. (1982). Acanthaster population regulation by a shrimp and a worm. Proceedings of the 4th International Coral Reef Symposium 2: 607–612.

Granja-Fernández, R, V. Antonio-Pérez & R.A. López-Pérez (2013), Euapta godeffroyi (Holothuroidea: Synaptidae): filling the distribution gap between Mexico and Costa Rica, eastern tropical Pacific. Hidrobiológica 23(1): 130–132.

Hickman, C.P. & T.L. Zimmerman (2000). A Field Guide to Crustaceans of Galápagos. Sugar Spring Press, Virginia, 156pp.

Hoover, J.P. (1998). Hawaii sea creatures, a guide to Hawaii marine invertebrates. Mutual Publishing, Honolulu, 366pp.

Invertebrate Zoology Collections (2016). http://collections.nmnh.si.edu/search/iz/. Electronic version accessed 10 July 2016.

ITIS (2016). http://collections.nmnh.si.edu/search/iz/?qn=Hymenocera+picta. Electronic version accessed 10 July 2016.

Juncker, M. & J. Poupin (2009). Crustacés de Nouvelle-Calédonie (Décapodes and Stomatopodes): Illustration des espèces et liste documentée des espèces terrestres et des récifs. Rapport Scientifique du CRISP, 20pp.

Kawamoto, T. & J. Okuno (2003) Shrimps and Crabs of Kume Island, Okinawa. Hankyu Communication, Tokyo, 174pp.

Kahru, M. (2007). Windows Image Manager (WIM). Image Display and analysis program for Microsoft Windows Software. WIMSoft 6.25 software.

López-Pérez, R.A., I. López Pérez-Maldonado, A.M. López-Ortiz, L.M. Barranco-Servín, J. Barrientos-Villalobos & G.E. Leyte-Morales (2010). Reef fishes of the Mazunte-bahías de Huatulco reef track, Oaxaca, Mexican Pacific. Zootaxa 2422: 53–62.

Merow, C., M.J. Smith & J.A. Silander Jr. (2013). A practical guide to Maxent for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36(10): 1–12; http://doi.org/10.1111/j.1600-0587.2013.07872.x

Mitsuhashi, M., T.Y. Chan & M.S. Jeng (2005). First records of the two Caridean Families, Gnathophyllidae Dana, 1852 and Hymenoceridae Ortmann, 1890 (Decapoda, Palaemonoidea) from Taiwan. Crustaceana 78(8): 987–1000.

Ormond, R.F.G. & A.C. Campbell (1974). Formation and breakdown of Acanthaster planci aggregations in the Red Sea. Proceedings of the Second International Coral Reef Symposium. Brisbane, Australia, 1: 595–619.

Pearson, R.G., C.J. Raxworthy, M. Nakamura & A. Townsend-Peterson (2007). Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography 34(1): 102–117; http://doi.org/10.1111/j.1365-2699.2006.01594.x

Phillips, S.J. & M. Dudík (2008). Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31(2): 161–175; http://doi.org/10.1111/j.0906-7590.2008.5203.x

Phillips, S.J., R.P. Anderson & R.E. Schapire (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling 190(3–4): 231–259; http://doi.org/10.1016/j.ecolmodel.2005.03.026

Pineda, J., J.A. Hare & S. Sponaugle (2007). Larval dispersal and transport in the coastal ocean and consequences for population connectivity. Oceanography 20(3): 22–39; http://doi.org/10.5670/oceanog.2007.27

Poupin, J., J.M. Bouchard, L. Albenga, R. Cleva, M. Hermozo-Salazar & V. Solís-Weiss (2009). Les Crustacés décapodes et stomatopodes, inventaire, écologie, et zoogéographie, pp. 163–216. In: Charpy, L. (ed.). Clipperton: environnement et biodiversité d’un microcosme océanique. Muséum National d’ Histoire Naturelle, Paris, 420pp.

Prakash, S. & T.T.A. Kumar (2013). Feeding behavior of Harlequin Shrimp Hymenocera picta Dana, 1852 (Hymenoceridae) on Sea Star Linckia laevigata (Ophidiasteridae). Journal of Threatened Taxa 5(13): 4819–4821; http://doi.org/10.11609/JoTT.o3506.4819-21

Seibt, U. & W. Wickler (1979) The biological significance of the pair bond in the shrimp Hymenocera picta. Zeitschrift für Tierpsychologie 50(2): 166–179; http://doi.org/10.1111/j.1439-0310.1979.tb01024.x

Wickler, W. (1973). Biology of Hymenocera picta Dana. Micronesica 9(2): 225–230.

Wicksten, M.K. & M.E. Hendrickx (2003). An updated checklist of benthic marine and brackish water shrimps (Decapoda: Penaoidea, Stenopodidea, Caridea) from the Eastern Tropical Pacific, pp. 49–76. In: Hendrickx, M.E. (ed.). Contributions to the Study of East Pacific Crustaceans 2. [Contribuciones al Estudio de los Crustáceos del Pacífico Este 2] Instituto de Ciencias del Mar y Limnología, UNAM, 303pp.

Wicksten, M.K. & L. Hernández (2000). Range extensions, taxonomic notes and zoogeography of symbiotic caridean shrimps of the Tropical Easter Pacific (Crustacea: Decapoda: Caridea). Bulletin of the Southern California Academy of Sciences 99(2): 91–100.

WoRMS (2016). World Register of Marine Species. http://www.marinespecies.org/aphia.php?p=taxdetails&id=210554. Electronic version accessed 10 July 2016.

Zepeta-Vilchis, R.C., A. Ayala-Bocos, O. Valencia-Méndez & R.A. López-Pérez (2013) First record and range extension of the jawfish Opistognathus panamaensis (Perciformes: Opistognathidae) from Western Mexico. Marine Biodiversity Records 6: e132; http://doi.org/10.1017/S1755267213001139