Abstract

Several fishes of the family Poeciliidae are commonly produced in ornamental aquaculture and also used for pest control, leading to their introduction in numerous countries. Many of these species exhibit tolerance and invasiveness, as exemplified by Xiphophorus maculatus (Günther, 1866). This report documents the presence of X. maculatus in a Caribbean coastal stream in Venezuela. Quizandal Creek has experienced significant human intervention in its lower drainage and channel area. In the final segment of the creek the fish were captured using hand nets and beach seines. The specimens were transported alive to the laboratory for evaluation and subsequently preserved according to standard methods and later were cataloged in the fish collection. 16 males ♂ and 8 females ♀ (16.6-29.4 mm SL. CPUCLA-3630) from the Quizandal Creek, part of the coastal drainage of the Borburata River, were analyzed. This is the first report on the occurrence of Xiphophorus maculatus in natural environments of Venezuela. These coastal streams are situated in a zoogeographic transition zone between regional freshwater ichthyofaunas that have a limited number of species, primarily secondary and amphidromous, which could be susceptible to the presence of introduced species. Xiphophorus fish demonstrate the ability to thrive in highly degraded environments, promoting their dispersion and amplifying the impact on the habitat and local fish, particularly small endemic fish, such as the Rivulidae and Poeciliidae.

Keywords:
Poeciliidae; ornamental fish; invasive species; coastal rivers; environmental stressors

Resumo

Vários peixes Poeciliidae são comumente empregados na aquicultura ornamental e no controle de pragas, levando à sua introdução em vários países. Muitas dessas espécies exibem tolerância e invasividade, exemplificadas por Xiphophorus maculatus (Günther, 1866). Esta nota documenta a presença de X. maculatus em um riacho costeiro na encosta do Caribe, Venezuela. O riacho Quizandal sofreu intervenção humana significativa na drenagem inferior e na área do canal. No trecho final do riacho os peixes foram capturados com redes de mão e arrastos. Os espécimes foram transportados vivos ao laboratório para avaliação e posteriormente preservados segundos métodos padronizados para posterior catalogação na coleção de peixes. Foram analisados 16 machos ♂ e 8 fêmeas ♀ (16,6-29,4 mm SL. CPUCLA-3630) provenientes do Córrego Quizandal, associado à drenagem costeira do Rio Borburata. Este é o primeiro relato da ocorrência de Xiphophorus maculatus em ambientes naturais da Venezuela. Estes riachos costeiros estão situados numa zona de transição zoogeográfica entre ictiofaunas regionais de água doce e apresentam um número limitado de espécies, principalmente secundárias e anfidromas, que podem ser suscetíveis à presença de espécies introduzidas. Os peixes Xiphophorus demonstram a capacidade de prosperar em ambientes altamente degradados, promovendo a sua dispersão e amplificando o impacto no habitat e nos peixes locais, particularmente pequenos peixes endêmicos, como os Rivulidae e Poeciliidae.

Palavras-chave:
Poeciliidae; peixes ornamentais; espécies invasivas; rios costeiros; estressores ambientais

The family Poeciliidae (274 species) is mainly characterized by small-sized individuals with distinctive sexual dimorphism and ovoviviparity (Fricke et al., 2023Fricke, R., Eschmeyer, W.N., & van der Laan, R., eds., 2023. Catalog of fishes: genera, species, references (Online). Retrieved in 2023, September 30, from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
http://researcharchive.calacademy.org/re... ). The males often display vibrant colors, and have the anal fin modified into a gonopodium, used to introduce sperm into the female reproductive tract (Rosen & Bailey, 1963Rosen, D.E., & Bailey, R.M., 1963. The poeciliid fishes (Cyprinodontiformes), their structure, zoogeography, and systematics. Bull. Am. Mus. Nat. Hist. 126, 1-176.). In Poeciliinae, one of the subfamilies, the genus Xiphophorus Heckel 1848 has 26 species (Fricke et al., 2023Fricke, R., Eschmeyer, W.N., & van der Laan, R., eds., 2023. Catalog of fishes: genera, species, references (Online). Retrieved in 2023, September 30, from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
http://researcharchive.calacademy.org/re... ) that were originally distributed in Gulf of Mexico drainages from northeastern Mexico to Caribbean drainages of northeastern Honduras (Kallman & Kazianis, 2006Kallman, K.D., & Kazianis, S., 2006. The genus Xiphophorus in Mexico and Central America. Zebrafish 3(3), 271-285. PMid:18377209. http://dx.doi.org/10.1089/zeb.2006.3.271.
http://dx.doi.org/10.1089/zeb.2006.3.271... ). Many Xiphophorus species, known for their exceptional beauty, have become popular choices for ornamental aquariums and have been utilized for the biological control of mosquitoes. Consequently, numerous species are now invasive in various aquatic ecosystems worldwide (Froese & Pauly, 2023Froese, R., & Pauly, D., eds., 2023. FishBase, version 10/2023 (Online). Retrieved in 2023, September 30, from www.fishbase.org
www.fishbase.org... ).

Fishes of the genus Xiphophorus are popularly known as platyfish and swordtails by aquarists and can be found in ornamental aquaculture operations and pet stores in most South American countries. Moreover, their introduction and established populations in natural environments have already been reported from Brazil (Ottoni et al., 2021Ottoni, F.P., Guimarães, E.C., Santos, J.P., Brito, P.S., South, J., & Bragança, P.H.N., 2021. First record of non-native Xiphophorus maculatus (Günther, 1866) (Cyprinodontiformes, Poeciliidae) in the state of Maranhão, northeastern Brazil. Check List 17(6), 1615-1622. http://dx.doi.org/10.15560/17.6.1615.
http://dx.doi.org/10.15560/17.6.1615... ), Colombia (Albornoz-Garzón & Villa-Navarro, 2017Albornoz-Garzón, J.G., & Villa-Navarro, F.A., 2017. Range extension of the invasive fish Xiphophorus maculatus (Günther, 1866) (Cyprinodontiformes: Poeciliidae) in the upper Magdalena river basin, Colombia. Check List 13(3), 2149. http://dx.doi.org/10.15560/13.3.2149.
http://dx.doi.org/10.15560/13.3.2149... ) and Peru (Cossíos, 2010Cossíos, E.D., 2010. Vertebrados naturalizados en el Perú: historia y estado del conocimiento. Rev. Peru. Biol. 17(2), 179-189. http://dx.doi.org/10.15381/rpb.v17i2.25.
http://dx.doi.org/10.15381/rpb.v17i2.25... ). The presence in captivity of Xiphophorus helleri Heckel 1848, X. maculatus (Günther, 1866Günther, A., 1866. Catalogue of fishes in the British Museum: catalogue of the Physostomi, containing the families Salmonidae, Percopsidae, Galaxidae, Mormyridae, Gymnarchidae, Esocidae, Umbridae, Scombresocidae, Cyprinodontidae, in the collection of the British Museum. London: British Museum, vol. 6.) and X. variatus (Meek 1904) in Venezuela has been documented (Ojasti, 2001Ojasti, J., 2001. Estrategia regional de biodiversidad para los países del trópico andino: convenio de cooperación técnica no reembolsable ATN/JF-5887-RG. Estudio sobre el estado actual de las especies exóticas: estudio nacional. Caracas: Comunidad Andina, Banco Interamericano de Desarrollo.) but there are no reports of its occurrence in natural environments. While monitoring of coastal drainages in Venezuela and surveying fish, we surprisingly found a population of X. maculatus. In this study, we provide a description of the characteristics of X. maculatus and the aquatic and riparian habitat. Additionally, we discuss the threats posed by the introduction of this alien species to the local ichthyofauna.

The Borburata River (5661 ha. mouth: 10°28'23” N; 67°57'34” W) is a small drainage on the Caribbean slope of the Coastal Range of Venezuela (Figure 1). The climate in its headwaters (1975 meters above sea level) is humid, with 800-1200 mm precipitation and cool, temperatures 10-14 °C. Close to the mouth, the climate is semiarid with low precipitation of 500-600 mm and hot temperatures of 24-26 °C (Rodríguez-Olarte et al., 2018Rodríguez-Olarte, D., Marrero, C.J., & Taphorn, D.C., 2018. Ríos en riesgo al Mar Caribe y al Golfo de Venezuela. In: Rodríguez-Olarte, D., ed. Ríos en riesgo de Venezuela. Barquisimeto, Lara: Universidad Centroccidental Lisandro Alvarado, 71-102, Colección Recursos Hidrobiológicos de Venezuela, no. 2.). The San Esteban National Park (43,500 ha) covers most of this drainage and allowed the preservation of humid and cloud forests in the mountains and dry forests in the lower areas. In the plains human activities prevail in a mosaic with deforestation, agriculture, villages (Borburata and Gañango, ~6000 people) and beaches with permanent tourism. The above conditions of the Borburata River drainage are common to most of the coastal rivers in this region of Venezuela.

Figure 1
Locality record of species Xiphophorus maculatus from Quizandal Creek (black dot) in the Borburata River drainage, Western Caribbean Province of Venezuela. Double arrow indicates a change in fish richness: few species of freshwater fishes have been found towards the east but over 70 have been collected in west.

Quizandal Creek is a tributary in the plains with severe intervention of its drainage and channel. The habitat was characterized and quantified using a standard method developed by Rodríguez-Olarte et al. (2006)Rodríguez-Olarte, D., Amaro, A., Coronel, J., & Taphorn, D.C., 2006. Integrity of fluvial fish communities is subject to environmental gradients in mountain streams, Sierra de Aroa, north Caribbean coast, Venezuela. Neotrop. Ichthyol. 4(3), 319-328. http://dx.doi.org/10.1590/S1679-62252006000300003.
http://dx.doi.org/10.1590/S1679-62252006... . In a section of this creek about 30 m long the fish were collected with hand nets and seines with different mesh sizes (1-5 mm). In the laboratory, all individuals of X. maculatus were maintained alive; subsequently, the fishes were euthanized with ice, fixed in formalin [10%], preserved later in ethanol [70%], and catalogued in the Colección Regional de Peces (CPUCLA), Museo de Ciencias Naturales of Universidad Centroccidental Lisandro Alvarado (UCLA, Barquisimeto, Lara). The taxonomic identification was made with diagnosis and keys (Rosen, 1960Rosen, D.E., 1960. Middle-American poeciliid fishes of the genus Xiphophorus. Bull. Fla. State Mus. Biol. Sci. 5(4), 57-242. http://dx.doi.org/10.58782/flmnh.bnrr6484.
http://dx.doi.org/10.58782/flmnh.bnrr648... ; Rosen & Bailey, 1963Rosen, D.E., & Bailey, R.M., 1963. The poeciliid fishes (Cyprinodontiformes), their structure, zoogeography, and systematics. Bull. Am. Mus. Nat. Hist. 126, 1-176.). The counts and measurements were made with a digital caliper and were expressed in 0.1 mm increments.

The aquatic habitat in Quizandal Creek was surrounded and shaded by a patch of secondary forest with profuse understory (Figure 2). The channel had a width of 0.4-2.3 m and a maximum depth of 0.5 m, while the substrate was a mixture of mud and sand covered by dense debris of branches and leaves. The flow was low (~5 l/s), with waters crystalline and slightly tinted. The water parameters were: pH: 7.5, conductivity: 81 μS/cm, total dissolved solids 34 mg/l. The contamination of the water was evident and caused by sewage coming from nearby agricultural and urban areas. The density for X. maculatus was 2.1 ind/m², calculated from a littoral transect long of the locality and before sampling. A few small individuals of Gobiomorus dormitor Lacepède 1800 and Eleotris sp. (Gobiiformes: Eleotridae) were also collected. No other species was observed at the site.

Figure 2
Sampling site in the Quizandal creek corresponding to voucher collection (CPUCLA-3630) of Xiphophorus maculatus.

The specimens examined of Xiphophorus maculatus were 16 males (♂) and 8 females (♀) (16.6-29.4 mm SL CPUCLA-3630) all of Quizandal Creek in Borburata drainage (10°28′09″ N; 67°58′07″ W; 5 meters above sea level), June 2022, coll. D. Rodríguez-Olarte and C. J. Marrero. All specimens were identified as X. maculatus because they have 22-25 scales in the lateral line and 7-11 rays in the dorsal fin. They are small fish, the body is compressed laterally, with a maximum body depth close to half the standard length (SL) and below the origin of the dorsal fin. The head is small, and less compressed than the body. The mouth is superior and somewhat protrusible, and the eyes are of medium size. The maximum length is for males 40 mm and females 60 mm. The caudal peduncle is long, very deep and compressed laterally. The caudal fin is round. They are sexually dimorphic fish: the males have a modified anal fin (gonopodium) that does not reach the base of the caudal fin. Due to the polymorphism of the species the meristics vary, but the usual values are dorsal fin with 7-11 rays (usually 8-10) and lateral scales 22 to 25 (usually 23-24, 26 in other platys).

The individuals of X. maculatus introduced in Quizandal Creek showed color patterns and combinations of black spots as follows (Figure 3): (a) on the body sides above the midline and before the origin of the dorsal fin; (b) covering most of the caudal peduncle and (c) at the base of the upper and lower external rays of the caudal fin or black lines extended only on the external rays. The literature reports wild populations with colors between silvery and pale olive, with iridescences in a reticulated pattern and eventually with melanic spots (Günther, 1866Günther, A., 1866. Catalogue of fishes in the British Museum: catalogue of the Physostomi, containing the families Salmonidae, Percopsidae, Galaxidae, Mormyridae, Gymnarchidae, Esocidae, Umbridae, Scombresocidae, Cyprinodontidae, in the collection of the British Museum. London: British Museum, vol. 6.; Rosen 1960Rosen, D.E., 1960. Middle-American poeciliid fishes of the genus Xiphophorus. Bull. Fla. State Mus. Biol. Sci. 5(4), 57-242. http://dx.doi.org/10.58782/flmnh.bnrr6484.
http://dx.doi.org/10.58782/flmnh.bnrr648... ). With a roundish black spot on the middle of the caudal base and another on the middle of the side of the trunk. The dorsal fin has small dark spots on the interradial membranes and often has the color of the body or black. A mid-lateral stripe is absent. Ornamental individuals have intense or iridescent colors, principally orange, red, yellow and black. Often, they have pure colors or mixtures with patterns of spots and varied lines. The variety of color pattern observed in Quizandal Creek indicates a possible mix of ornamental varieties (Figure 3).

Figure 3
Live specimens of Xiphophorus maculatus from Quizandal Creek (Borburata drainage) in Coastal Range of Venezuela. All specimens preserved (CPUCLA 3630. (a) 27.5 mm SL; (b) 25.5 mm SL; (c) 28.5 mm SL; (d) 27.0 mm SL). Scale bar 10 mm.

Most species of Xiphophorus have a notable physiological tolerance and are capable of living in environments with low water quality; moreover, they have rapid growth, possible sex reversal, ovoviviparity and high abundance (Meffe & Snelson, 1989Meffe, G.K., & Snelson, F.F., 1989. Ecology and evolution of livebearing fishes (Poeciliidae). Englewood Cliffs: Prentice Hall.; Balon, 2004Balon, E.K., 2004. About the oldest domesticates among fishes. J. Fish Biol. 65(s1), 1-27. http://dx.doi.org/10.1111/j.0022-1112.2004.00563.x.
http://dx.doi.org/10.1111/j.0022-1112.20... ). These attributes explain the high success in the colonization and invasion of different aquatic ecosystems by X. maculatus, however there is little evidence available on specific ecological impacts. The contamination in regional coastal rivers could also favor X. maculatus due to their tolerance to living in disturbed habitats, because these rivers are in risk mainly to pollution by urban and industrial effluents, transformation and loss of channels, deforestation of riparian zones and watersheds, and water extraction (Rodríguez-Olarte et al., 2018Rodríguez-Olarte, D., Marrero, C.J., & Taphorn, D.C., 2018. Ríos en riesgo al Mar Caribe y al Golfo de Venezuela. In: Rodríguez-Olarte, D., ed. Ríos en riesgo de Venezuela. Barquisimeto, Lara: Universidad Centroccidental Lisandro Alvarado, 71-102, Colección Recursos Hidrobiológicos de Venezuela, no. 2.). Thus, the invasive condition of X. maculatus could have a detrimental effect on the local ichthyofauna in coastal drainages, such as the killifish Austrofundulus leohoignei Hrbek, Taphorn & Thomerson (Rivulidae), an endemic and highly restricted species to local coastal floodplains and which is threatened by the loss of its habitat (Rodríguez-Olarte et al., 2011Rodríguez-Olarte, D., Taphorn, D.C., & Lobón-Cerviá, J., 2011. Do protected areas conserve neotropical freshwater fishes? A case study of a biogeographic province in Venezuela. Anim. Biodivers. Conserv. 34(2), 273-285. http://dx.doi.org/10.32800/abc.2011.34.0273.
http://dx.doi.org/10.32800/abc.2011.34.0... ), but also several Poeciliidae fishes species, which include Poecilia dauli, P. koperi, P. reticulata and P. heterandria, this last is endemic and restricted to local drainages toward in the Caribbean Sea (Rodríguez-Olarte et al., 2009Rodríguez-Olarte, D., Taphorn, D.C., & Lobón-Cerviá, J., 2009. Patterns of freshwater fishes of the Caribbean versant of Venezuela. Int. Rev. Hydrobiol. 94(1), 67-90. http://dx.doi.org/10.1002/iroh.200711070.
http://dx.doi.org/10.1002/iroh.200711070... ). Poecilia fish are common in a wide range of habitats, principally in creeks, swamps, lagoons and estuaries; they are omnivores with a tendency to insectivory (Zandonà et al., 2015Zandonà, E., Auer, S.K., Kilham, S.S., & Reznick, D.N., 2015. Contrasting population and diet influences on gut length of an omnivorous tropical fish, the Trinidadian guppy (Poecilia reticulata). PLoS One 10(9), e0136079. PMid:26360601. http://dx.doi.org/10.1371/journal.pone.0136079.
http://dx.doi.org/10.1371/journal.pone.0... ). These features are very similar to those of X. maculatus, which usually is twice the size of the majority of local poeciliids. In consequence, the introduction of an invasive competitor such southern platyfish could displace certain species due to similar requirements of habitat. Furthermore, in Quizandal Creek juveniles and pregnant females of X. maculatus were collected, suggesting reproductive success and populations of relative permanence.

The zoogeographic patterns of the regional ichthyofauna in combination with human intervention of rivers can limit or favor the permanence of alien species and increase the risk for the local fishes. In this province, the richness of freshwater fishes in the western drainages reaches about 70 species (Rodríguez-Olarte et al., 2009Rodríguez-Olarte, D., Taphorn, D.C., & Lobón-Cerviá, J., 2009. Patterns of freshwater fishes of the Caribbean versant of Venezuela. Int. Rev. Hydrobiol. 94(1), 67-90. http://dx.doi.org/10.1002/iroh.200711070.
http://dx.doi.org/10.1002/iroh.200711070... ), the majority of which are primary species living mostly in freshwaters; but in small rivers to the east, no more than 10 freshwater species occur, all are secondary, amphidromous or catadromous (Figure 1). This longitudinal gradient in the fish richness can favor the establishment of alien species such as X. maculatus in drainages to the east, because there could be less competition for resources and a lower chance of predation by other fishes.

Although the fish of the genus Xiphophorus are the most commercialized ornamental fish in Venezuela (Salazar et al., 2008Salazar, S.K., Pérez, J., & Alfonsi, C., 2008. Introducción y extracción de peces ornamentales y especies de invertebrados acuáticos en Venezuela. Saber 20(2), 139-148.) and have already been observed in artificial environments and creeks of some cities, the species X. maculatus has not been reported formally as living in natural environments of the country. In Venezuela two aspects may be added to the list of possible causes leading to the dissemination of ornamental fish: electronic commerce and the economic crisis. The commercialization of ornamental fish on social networks is very common, even more so in post-pandemic conditions, because contact is direct between private breeders and enthusiasts, thus avoiding government controls and commercial records on the sales or trafficking of ornamental fish. On the other hand, the economic crisis has limited the ability to maintain ornamental fish, mainly due to the exaggerated increase in the cost of equipment, food and veterinary services. This could explain in recent years the many cases where fish have been abandoned or released into both natural and artificial environments.

An evaluation of factors promoting the introduction and spread ornamental freshwater fishes in coastal drainages of Venezuela is a priority. There are observations of alien species (e.g. Cichla, Metynnis, Prochilodus) and some biological collections have museum records, but there is no adequate and updated data on the status of those introductions (Rodríguez-Olarte et al., 2018Rodríguez-Olarte, D., Marrero, C.J., & Taphorn, D.C., 2018. Ríos en riesgo al Mar Caribe y al Golfo de Venezuela. In: Rodríguez-Olarte, D., ed. Ríos en riesgo de Venezuela. Barquisimeto, Lara: Universidad Centroccidental Lisandro Alvarado, 71-102, Colección Recursos Hidrobiológicos de Venezuela, no. 2.). Consequently, the first step is to apply periodic monitoring in rivers and lakes where the state and integrity of aquatic habitats and native fish communities can be recognized. The second step involves the development of citizen science training and outreach programs, which will allow the effects associated with the introduction of exotic fish to regional freshwater ecosystems to be recognized and assessed. At the same time, it is necessary to facilitate procedures to develop and adapt legislation that regulates aquaculture and the management of ornamental fish species.

Acknowledgements

This report is a partial result of projects of The Mohamed Bin Zayed Species Conservation Found (212528182, 230531876), Idea Wild (rodrvene1221), CDCHT-UCLA (1081-AG-2017, 1209-RAG-2022), MINCYT-FONACIT Venezuela (2023000 79) and ONCC-MINEC Venezuela (DGD-SP-NC-23-002) support by Museum of Natural Sciences, UCLA. The INSOPESCA (MPPPA-Venezuela) provided the scientific permit (N°PC/0001-0006-2022).

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