An island invaded by exotics: a review of freshwater fish in Puerto Rico

ABSTRACT The introduction of exotic fishes in streams and water reservoirs has modified autochthonous freshwater fish communities in Puerto Rico. There are approximately 46 fish species in inland waters, and most of them were introduced during the last century. We here summarize relevant information on 46 freshwater fish species reported for the island. Approximately 80% of the species are non-native. An evaluation of the local trade revealed another 128 freshwater fish species are sold locally as pets. This raises serious concerns, as we detected a potential pool of non-native species that are either considered invasive elsewhere, or that, based on their ecology, could become invasive on the island in the near future. We also found that cichlids as a group pose the highest risk to freshwater ecosystems, with 13 species established in the wild, and another 38 potential invaders in the local pet trade. This study may be used as a baseline for the conservation and management purposes of both native and non-native fish species, including the development of strategies for preventing the release of live fish pets into the wild. More specific management for non-native fish, especially those identified here that pose significant threats to Puerto Rico’s native fish and their ecosystems, are warranted.


Introduction
The Neotropical realm has the highest diversity of freshwater fish, with more than 5,160 recorded species worldwide [1]. Native freshwater fish communities on tropical islands usually have low species diversity and are composed entirely of species with catadromous or amphidromous life histories [2,3]. Puerto Rico has nine native freshwater fish species, all of which require contact with marine environments during some phase of their life cycle [4]. These native species include representatives within the families Anguillidae, Eleotridae, Gobiidae, and Mugilidae [5,6]. Today, however, there are about 77 reported freshwater fish species that inhabit the inland waters of Puerto Rico [3].
Unsustainable human development has considerably impacted freshwater ecosystems globally, and native freshwater fish face a variety of threats [7]. Catchment-scale modifications (i.e. altered movement pathways of sediments in water systems due to landuse changes or increased imperviousness) and stream channelization projects in urban areas, often employed as a strategy to control flooding, have a strong impact on the distribution and composition of fish species and their communities [8]. Hence, the migratory patterns and life cycles associated with the development of a species are modified or broken, and thus the native species assemblages become overtaxed, while the establishment of exotic species remains rampant [5,9].
Highly urbanized areas degrade freshwater ecosystems due to the interplay between the loss of appropriate habitat for native fish species and the proliferation of introduced non-native species (which are often more tolerant to disturbed ecosystems), resulting in a decrease of native freshwater fish diversity [10], and in the loss of the ecological services they provide [11]. In Puerto Rico, over the last century, anthropogenic disturbances such as the modification of watersheds through the alteration of river courses, construction of dams, channelization of reaches, deforestation, road crossings, water pollution, and changes in the species compositionwhich includes the introduction of non-native fishhave greatly modified the inland freshwater ecosystems [12]. For example, dam construction and some channel modifications serve as barriers to Puerto Rico's native fish species, affecting their migratory patterns and species assemblages of native fish. Most the major rivers of Puerto Rico have some degree of damming (i.e. water retention structures), which has negatively impacted freshwater fish communities through habitat fragmentation [13].
With the establishment of Biological Invasion as a discipline, we now know, without a doubt, that the detrimental effects of biological invasions have intensified greatly during the last decades [14]. The ever-present threat of new introductions on non-native fish to indigenous ecosystems represents a serious threat to freshwater systems, especially on island ecosystems. The introduction of non-native fish in the inland freshwater systems of Puerto Rico has severely impacted native fish communities, with local depletion or local extinction of native species [3,8,15]. Currently, freshwater habitats are mostly composed of fish species introduced from America, Africa and Asia [15]. Although the introduction of non-native fish into the water reservoirs of Puerto Rico began in the early 1900s, most of the non-native species present in the wild today are the result of both accidental and intentional releases during the last decades. Nonnative fishes were brought for aquaculture and the sport fishing industries, and some escaped from fish hatcheries and fishponds that were mainly established in the 1930s [16]. Hence, species such as goldfish (Carassius auratus), swordtails (Xiphophorus hellerii), sailfin catfish (Pterygoplichthys sp.), algae-eater (Gyrinocheilus aymonieri), and several cichlid species have been released to the wild by their owners and have become common throughout the island [17]. What ecological impacts these non-native fish may have on native species is a shared concern amongst scientists that study freshwater ecosystems in Puerto Rico. For example, predation by introduced non-native freshwater fish upon native snail and bird species has been reported in Puerto Rico [18].
Early studies of freshwater fish communities in Puerto Rico focused on biological aspects of native species [19,20,], and they gradually shifted to include species distributions, the biology and management of non-native species, and the impacts of these on native freshwater fish communities [15]. More recently, studies have focused on the effects of ecological factors influencing freshwater fish populations and communities (e.g. parasitization), genetics, and urban fish assemblages [8,17,21,22]. However, and although Puerto Rican freshwater ecosystems are relatively well studied when compared to other islands, biologists keep recording new species established in the wild. For example, just in 2018, Rodríguez-Barreras and Zapata-Arroyo [23] recorded the occurrence of an established population of the highly invasive African catfish Clarias gariepinus in Puerto Rico, a species considered harmful to native species elsewhere, which raised grave concerns amongst state and federal agencies tasked with the management of the native and sport fish resources of the island.
The availability of scientific information on the identity of both native and non-native fish species that currently inhabit the island, and on locally traded non-native freshwater fish is critical to effectively manage the freshwater fish resources. However, there is currently no updated list of freshwater species to accomplish this. To fill this gap, here we present a comprehensive list of native and nonnative freshwater fish species established in Puerto Rico, and the species that have not yet been reported in the wild, but that are traded locally. For the freshwater fish fauna that are present in the wild, we synthesize the most relevant information, which includes aspects of their biology, ecology, and their geographic distribution. Additionally, we provide information about freshwater fish species that are sold through the aquarium pet trade in Puerto Rico and their potential invasiveness.

Site description
The Puerto Rican Archipelago is located in the Caribbean Sea, and composed of three main populated-islands (Puerto Rico, Vieques, and Culebra), and numerous other islands, islets and cays, which, together with the US and UK Virgin Islands (except for St. Croix) form the biogeographic area known as the Puerto Rican Bank. This study focuses on the main island of the Puerto Rican Archipelago, Puerto Rico, which is the smallest of the Greater Antilles, with an area of approximately 8,870 km 2 . Puerto Rico currently has a human population of approximately 3.2 million inhabitants with a humanpopulation density of ca. 351 inhabitants per km 2 , after experiencing a dramatic decrease in population (of ca. −0.5 million, or a 15.3% decrease) in just 8 years [24]. Geologically, Puerto Rico is of volcanic origin, but possesses karst regions [17], and has diverse climatic zones [25]. The climatic zones of the freshwater systems of the island vary from perennial streams in areas of high precipitation, to intermittent streams in areas of low precipitation [26]. The Central Cordillera is the main mountainous chain that runs east-west through the center of Puerto Rico. It reaches 1,340 m at its highest point and is the origin of most of the rivers and streams on the island. The rivers and streams draining towards the north include many underground systems flowing through the Karst Region and include the longest river systems on the island, whereas there are fewer and shorter length rivers and streams draining towards the south [27,28]. When compared to the other Greater Antilles, the rivers and streams of Puerto Rico are generally small and flashy, and composed of mainly rocky substrates of volcanic origin (e.g. pebbles, gravel, boulders) and sand.

Compilation of fish species present in puerto rico
To generate a comprehensive and updated list of freshwater fish species present in Puerto Rico that may be used to inform conservation and management strategies, we focused on identifying: i) species present in the wild, and ii) locally traded species, especially those present only in captivity (i.e. that may be potentially released into the wild).

Fish species present in the wild
To compile a list of fish species present in the wild, we reviewed the literature (which included published and unpublished scientific articles and technical reports of government agencies), performed a survey of specimens collected and deposited in zoological collections, and carried out sampling in-situ.
To identify the species of fish present in the wild, we considered species with life histories recognized as catadromous, amphidromous and stream resident. We excluded fish species with life histories dominated primarily by phases inhabiting marine, estuarine and brackish water habitats. To compile a list of fish species present in the wild, we reviewed the literaturewhich included published and unpublished scientific articles and technical reports of government agencies, performed a survey of specimens collected and deposited in zoological collections, and carried out sampling insitu. Local distribution for all species was not uniform due to differences in information sources.
To perform the literature review, we used the institutional database of the library in the University of Puerto Rico, and search engines using the keywords: "freshwater", "fish", "exotic species", and "Puerto Rico". To complement the information extracted from the literature, we surveyed the specimens deposited in the Zoological Museum of the University of Puerto Rico -Río Piedras Campus. For each collection, we recorded the following information: sample identification number (ID), species identity, number of individuals, and collection date.
We conducted fish surveys in four locations in the metropolitan area of San Juan, which includes Guaynabo River (18°21ʹ59,78 . Sites were selected because these are areas of high suspected invasion potential due to proximity to aquaria owners and have not been frequently sampled. Fish species were identified visually by snorkeling or by capturing them using a hand net. All captured individuals were released immediately after identification.

Locally traded fish species
To identify locally traded fish species, primarily through the aquarium (ornamental) and pet trade markets, and to identify those species that have invasive potential, we followed Falcón and Tremblay [29]. Briefly, during April of 2019, we conducted surveys in situ, focusing on petand aquarium shops in the Metropolitan Area of San Juan. Moreover, we surveyed online community groups covering topics related to biodiversity, pet trade, aquarium fish, and collected available posted data (e.g. location, species, photographs). Surveyed Facebook (http://www.facebook.com) groups included The fish outlet, Nativos Ciclids fish shop, Adictos a los peces, Báez Aquarium and more, Aquarium Xtra, and Pet Ways (see Supplemental Information). We also surveyed the pet section of local online classified (user-generated ads) webpage Clasificados Online.

Scientific name nomenclature
After taxonomic identification (at the lowest possible level), we followed the nomenclature established by the Integrated Taxonomic Information System to assign the corresponding scientific name for each identified taxon, and updated the scientific name of fish reported in the literature or preserved in zoological collections, as needed [30]. We provide common names for fish currently present in the wild in Puerto Rico in both English and Spanish in Table 1.

Results
We report 46 freshwater fish for Puerto Rico freshwater systems, belonging to 7 orders, 14 families, and 32 genera (Table 1, Figure 1). The Order Perciformes was the best represented with 26 species, whereas the Orders such as Anguilliformes and Characiformes were represented only by one species (Table 1). The family Cichlidae was the best represented with 13 species followed by Poeciliidae with 7 species, both families include only non-native species ( Figure 2). Most fish species found in Puerto Rico's streams and water reservoirs are non-native; only 9 species of this list are native, which represents 19.6% of the total number of freshwater fish species reported for Puerto Rico. We also found another 128 freshwater fish species commercialized in stores and local websites. The most represented families were Cichlidae with 39 species, Cyprinidae with 16 species and Characidae with 11 species (Figure 2). See Appendix 1 for more details.
The following list includes all freshwater fish species with established populations on the island: Order Anguilliformes Family Anguillidae Rafinesque, 1810 Anguilla rostrata (Lesueur, 1817)

Distribution
Northwest to western Central Atlantic: Greenland south along the Atlantic coast of Canada and the USA to Panama and throughout much of the south Caribbean to Trinidad. References [35,36].

Order Cypriniformes
Family Arcticidae Newton, 1891 Carassius auratus (Linnaeus, 1758) Distribution Worldwide distributed, but originally from Asia: central Asia and China and Japan.

Poecilia reticulata Peters, 1859
Distribution South America: Venezuela, Barbados, Trinidad, northern Brazil and the Guyanas. Widely introduced and established elsewhere, mainly for mosquito control, but had rare to non-existing effects on mosquitoes, and negative to perhaps neutral effects on native fish. Africa: Feral populations reported from the coastal reaches of Natal river from Durban southwards, as well as in the Kuruman Eye and Lake Otjikoto in Namibia.

Xiphophorus hellerii Heckel, 1848
Distribution North and Central America: Rio Nantla, Veracruz in Mexico to northwestern Honduras. Africa: Feral populations reported from Natal and eastern Transvaal as well as in Lake Otjikoto, Namibia.

Distribution
North and Central America: Ciudad Veracruz, Mexico to northern Belize. Puerto Rico localities: found in several drainages around the island.

Distribution
Western Atlantic from North Carolina south along the USA, Bahamas, throughout the Gulf of Mexico and the Caribbean Sea to southeastern Brazil.
Puerto Rico localities: Widespread throughout the island, but only in rivers, not present in freshwater reservoirs.

Discussion
We review the freshwater fish fauna of Puerto Rico and present an updated list of the species present in the island. We report all known sites occupied by each fish species that inhabit streams and freshwater reservoirs in the island (georeferenced when possible). Although 77 fish species have been reported for Puerto Rico [3], we include only those species considered freshwater residents or species that spend most of their life cycle in freshwater. Consequently, we have excluded native fish such as Bathygobius soporator, Dormitor maculatus, Gerres cinereus, Kryptolebias marmoratus, Microphis brachyurus, Mugil cephalus, Mugil liza, Megalops atlanticus and Strongylura marina, all of which are occasionally found in freshwater streams, but primarily inhabit marine or estuarine ecosystems [16]. One of the highlights of our study, and a source of concern, is the number of introduced species inhabiting streams and water reservoirs in Puerto Rico, compared to the pool of native species currently present on the islands. Less than 20% of the freshwater fish species are native. The fast development of freshwater aquaculture in the past century has been a major factor responsible for the introduction of many exotic fish in mainland areas, and some islands [66]. However, the dominance of aquarium species in our list and the lack of an established aquaculture industry in Puerto Rico indicate that the pet trade has been critical in the introduction of exotic freshwater fish. In the past, there were short-lived commercial tilapia farms established in Puerto Rico. For example, the Lajas Aquaculture Station and the Maricao Fish Hatchery operated for years [67], with the Maricao Fish Hatchery still being operated today by the Department of Natural and Environmental Resources (D.N.E.R.). The introduction of most (62.6%) non-indigenous resident species in Puerto Rico is associated with the local aquarium and pet trade business, while the vector for the remainder non-native species is equivocal; however, we suspect the aquarium and pet trade market as the likely culprit.
The international fish trade is currently growing and represents an important source of revenue for many countries [68,69]. However, this brings with it the risk of release of live non-native freshwater fish outside their native range, which may have negative impacts on the populations of native species and the ecosystem services they provide. As with many introduced invasive species, the introduction of non-native freshwater fish may have unintended and unpredictable negative effects on local environments and currently represents one of the main threats against the survivorship and genetic integrity of native species populations [70,71]. Moreover, established exotic fish may introduce parasites and diseases, compete for or alter food resources and habitat dynamics, and prey upon native fish [72]. The current freshwater fish community's composition in Puerto Rico is not only a direct consequence of irresponsible and uninformed attitudes of pet owners but it is also due to the illegal introduction by local aquaculture farms. For example, the Jaguar Guapote Cichlid was introduced to Puerto Rico without the permission of the D.N.E.R by aquaculture farms to control tilapia overpopulation in the culture ponds. Once discovered, the D. N.E.R ordered the eradication of the fish, which was supposedly completed. However, the Jaguar Guapote appeared later in the Loiza Reservoir, which indicates other (geographic) sources are supplying the species into freshwater ecosystems.
The existence of another 128 freshwater fish sold locally as pets represents a serious threat and serves as a "potential pool" of non-native species that could be added to natural freshwater ecosystems in the future (See Appendix 1). Of all the species, those that belong to the family Cichlidae represent the most aggressive invaders, with 13 species established on the island and another 38 potential invasive species sold as pets ( Figure 2). The 2010 D.N.E.R Fisheries Regulations [73] published a table with the aquarium species which are allowed for import into Puerto Rico. When we compare this list with our potential invasive species list, we noticed differences. For example, the Family Anguillidae has only one species in the D.N.E.R. list, but we also found another species of eel, Anguilla marmorata, sold as pets. Most alarming is that the Family Cichlidae has 113 species authorized by D.N.E. R to be sold as pets. Thirteen of those have escaped and established while another 39 potential cichlid invaders are still in the local market.
The negative impacts of exotic fish have not yet been thoroughly documented in Puerto Rico, but there are indications that impacts may be, indeed, serious. For example, Red devil cichlids (Amphilophus spp.) are known to be extremely aggressive predators and competitors. D.N.E.R has documented an inverse relationship between non-native sunfish (Lepomis sp.) and red devil abundances, but attributing sunfish decline to the introduction of invasive red devil cichlids is speculative since the evidence may be circumstantial [74]. However, if there is such a relationship between the two nonindigenous species, then we could expect that if the red devil invades Puerto Rican rivers, they will potentially negatively impact the native freshwater fish community. Another species of concern is the armored catfish (Pterygoplichthys spp.) which could compromise shoreline stability by increasing riverbank erosion and suspended sediment loads in the reservoirs as a result of excavating nest burrows at high densities along shorelines [75]. Armored catfish may also pose a threat to endangered brown pelicans (Pelecanus occidentalis), some of which have died from having catfish lodged in their throat by their spines [18].
There are many different approaches to managing existing invasive species and avoiding new introductions. For example, managers and politicians should create an administrative bill that would establish public education programs and campaigns about the importance of avoiding the release of freshwater fish from aquaria and aquaculture in streams, channels, and reservoirs. New laws could also penalize releasing potential invasive fish with fines. More specific management of current populations of introduced fish, especially those that pose significant threats to Puerto Rico's native fish and their ecosystems, should be prioritized. In order for management efforts to succeed, further research must be done to fill in the knowledge gaps in the distribution and ecology of introduced species. Efforts should prioritize native ecosystems with higher native fish diversity such as lowland streams and introduced species that are found at high abundances in these environments.