Metazoan Marine Parasites of Costa Rica: A Review
1
Centro de Investigación en Enfermedades Tropicales, Universidad de Costa Rica, San Jose 11501, Costa Rica
2
Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San Jose 11501, Costa Rica
*
Author to whom correspondence should be addressed.
Parasitologia 2023, 3(2), 116-141; https://doi.org/10.3390/parasitologia3020014
Submission received: 2 March 2023
/
Revised: 14 March 2023
/
Accepted: 21 March 2023
/
Published: 1 April 2023
/
Corrected: 20 November 2023
Abstract
:Many new marine parasite species are added every year. Still, in some places, mainly tropical regions, marine parasites have been little studied. An exhaustive review of the indexed publications where species of parasites are reported in the marine environments of Costa Rica was carried out. The history of research on marine parasites in this region is also reviewed. A total of 146 species of marine parasites have been reported in Costa Rica as parasites of 61 different species of hosts. Most of these parasites correspond to trematodes and cestodes, found mainly in the digestive tract of their vertebrate hosts. In Costa Rica, marine parasites have been studied mainly in sea turtles, elasmobranchs, fish, and dolphins. Most marine parasites have been reported based on morphological identifications of adult stages, and most of the work done so far consists of taxonomic identifications (species reports), with little contribution to the pathology and other aspects of the parasites–hosts interactions. The technical difficulties for research in marine parasitology, the lack of sampling in certain groups of hosts, and the lack of a consolidated research group in marine wildlife parasitology in Costa Rica are factors that have prevented a greater and faster advance in the knowledge of the biodiversity of marine parasites in this country.
1. Introduction
The parasitic lifestyle is successful. An initial estimation of nearly 40% of known species to be parasitic was made by Rhode [1]. New data have made researchers change their minds about the diversity of parasite fauna. The awareness of the numbers of potential hosts, cryptic species, and the exponential growth in the discovery rate of new parasite species is increasingly revealing the actual numbers, which now are thought to be more than half of all organisms known [2,3,4,5]. In marine environments, many new parasitic species or new reports are added every year. Still, even so, marine parasites of certain diverse groups, like fish, have been under-sampled worldwide, especially in the tropics [3]. Sampling effort is known to be positively correlated to parasite species richness [5].
Several factors have been proposed as determinants of parasite richness. One of them, apart from sampling effort, is latitude. As latitude values become lower, overall species richness increases, and parasite species richness is also predicted to increase. Interestingly, that has been demonstrated only for microparasites (virus, bacteria, protozoans) from primates and rodents. It has been hypothesized that this could result from comparatively little sampling effort of the many other groups of hosts that are harder to sample [5]. Such a gradient in parasite species could tell us about the importance of factors such as temperature variation, humidity, rainfall, and biodiversity of potential hosts as determinants of parasite species richness [6]. The analysis of parasite richness becomes more complex as many parasites in aquatic systems have significant seasonal variations depending on the taxonomic group and the specific environment [7].
Hosts and their parasites communities have complex relationships; the characteristics of the hosts, parasites, and environment affect each other. For one species of host, the environment could be a powerful predictor of the diversity and abundance of parasites, whereas, in other situations, biological variables of hosts and parasites might be more important in determining how these communities are shaped [8]. Parasites also help shape community structure by reducing host fitness. They not only have a role in organizing a given community structure, but they also influence interspecific interactions and destabilize community dynamics when certain environmental conditions change considerably [9]. In a global climate change era, this is of major concern.
The information on marine parasites of the neotropical regions is dispersed. In Costa Rica, there have been some prolific moments of studies on marine parasites in the past, led by just a few enthusiastic researchers, mostly foreigners, who described several new species and contributed many new species reports for the region. Nevertheless, research on this topic has been scarce in the last decade. This review aims to provide a comprehensive overview of the research that has been done so far on the marine parasites of Costa Rica. We present a list of the metazoan marine parasites reported for Costa Rica and point out gaps in research of parasite groups, geographic regions, and hosts.
2. Results
2.1. Brief History of Marine Parasites Research in Costa Rica
More than 50 papers have been published with information on marine parasites of Costa Rica, 43 of them from the Pacific waters and eight from the Caribbean, starting in the 1930s, with peaks of publication in the 1990s, 2000s, and 2010s decades (Figure 1; Appendix A, Table A1). The first reports were based on collections by Harold W. Manter, done at Bahía Culebra on 24–25 February 1934, during the third Allan Hancock Expedition to the Galápagos Islands (and the neighboring Pacific) [10]. The first paper was on parasitic copepods of fish by Charles B. Wilson in 1937 [11], followed by the description of a new species of a monogenean by Frank G. Meserve [12], while Manter (1940) reported and described new species of digenetic trematodes of fishes [13]. Harley J. Van Cleave (1940) described a new species of acanthocephalan from the stomach of a fish [14]. Schmitt (1939) visited Isla del Coco during the US Presidential Cruise of 1938 and collected parasitic copepods from fish and a fleshy cirripedian [15].
The next set of publications was in the late 1950s and early 1960s by Rodrigo R. Brenes-Madrigal, of the Universidad de Costa Rica (UCR) and his Mexican colleagues of the Universidad Nacional Autónoma de México (UNAM). They published on helminth parasites of fish [16,17,18]. Only one paper was published in the 1970s on monogenean parasites of the skin of Carcharhinus leucas and elasmobranch trematodes in Barra del Colorado, north Caribbean [19]. Two papers were published in the 1980s, one that mentions parasitic copepods of scombrids (mackerel and tuna) [20], and another is a thesis on trematodes of marine fishes [21].
The 1990s was the most productive decade with 13 papers, most by research groups headed by Daniel R. Brooks and Fernando Marques, University of Toronto, and UNAM, on parasites of elasmobranchs and teleost fish. Six of these papers are on cestodes, and a total of 15 new species and two new genera were described, including all groups of helminth parasites [22,23,24,25,26,27,28]. Not only vertebrate parasites were found in this decade. Patricia Jiménez and Mario Vargas of UCR (1990) reported the presence of an isopod in a shrimp [29], while V.A. Zullo found an ectoparasitic barnacle on a lobster [30], and J.C. Markham found new ectoparasitic bopyrid isopods on porcellanid crabs [31]. Finally, Lamothe-Argumedo and collaborators listed 11 marine parasitic species from Costa Rica in the Mexican National Helminth Collection Catalogue [32].
The decade between 2001 and 2020 was very productive, with 81 new marine parasite reports in 21 publications, mainly from sea turtles and dolphins. Research groups headed by Dr. Mario Santoro reported the presence of 41 marine parasite species in sea turtles from Costa Rica. They published four papers on parasites of the green turtle Chelonia mydas from Tortuguero, in the Caribbean of Costa Rica, and synthesized this information in a book about the digenetic trematode community in nesting green turtles of this region. These contributions included the description of a new species of digenean parasite [33,34,35,36,37]. Majewska, Robinson, and Santoro, each in a different collaboration, contributed to studying parasites associated with nesting olive ridley turtles Lepidochelys olivacea in the north Pacific of Costa Rica [38,39,40] and parasites of the hawksbill turtle Eretmochelys imbricata were also studied by Santoro [41]. In the book on Costa Rica’s marine biodiversity, Santoro and Mattiucci published a synthesis of the knowledge on marine turtle parasites of Cost Rica [42].
Other publications during these decades included one on an ectoparasitic copepod of a shark [43], another on fish-parasite isopods [44], and isopod parasites of crabs [45]. Rodriguez-Ortiz, in 2004 [46,47], compiled a checklist of helminth parasites of vertebrates in Costa Rica, including several marine vertebrate parasite species, while Cortés (2009) published a list of marine fish parasites [48]. In 2011 Oliveira and collaborators published on parasites of stranded cetaceans on the Pacific coast of Costa Rica [49]. In the late 2010s, there were two publications on fish parasites, one on monogenean parasites of marine fishes in the Gulf of Nicoya and one on acanthocephalan parasites of mullet fish that included material from Costa Rica [50,51].
The last publications regarding Costa Rica’s marine parasites were published in 2021 and 2022. In one of these publications, the authors used molecular approaches to study the diversity of haploporid trematodes from mugilid fish in Central America and found two new species of these trematodes, including the new genus Ekuarhuni [52].
Finally, Angulo and Sibaja-Cordero made the most recent addition to the marine parasite fauna of Costa Rica by reporting the presence of an interesting parasitic cirripedian in the ninja lantern shark (Etmopterus benchleyi) [53]. By the end of 2022 and the beginning of February 2023, no more recent additions, or studies on the marine parasitic fauna of Costa Rica have been made.
2.2. Costa Rican Marine Parasite Diversity
A total of 146 species of marine parasites, belonging to 113 genera in five animal phyla, have been reported in Costa Rican marine and brackish water animals (Appendix A, Table A1). Thirty-two were reported as new species and described from material collected in Costa Rica. Three species were described as new genera, and 38 species were new reports for the eastern tropical Pacific when reported (Appendix A, Table A1). Of all these species, 47 (32%) are deposited as voucher specimens in any Costa Rican biological collection (Colección Helmintologica de Costa Rica or Museo de Zoología UCR), with more than two-thirds of the collected material deposited as voucher specimens in biological collections in other countries, mainly in the United States and México (Supplemental Figures S1 and S2).
More researchers have sampled sites in the Pacific in search of marine parasites than on the Caribbean coast (Appendix A, Figure 2). The number of species reported from each coast reflects this differential sampling effort, with more species reported in the Pacific of Costa Rica and significantly fewer marine parasite species reported for the Caribbean Sea (Figure 2 and Figure S1). These efforts had rendered a total of 51 species reported for the Caribbean, 101 for the Pacific, and five species present on both coasts (Figure 2). Most species have been sampled from coastal and brackish waters.
Santoro and collaborators, during several years in the 2000–2015 period, and Watson and Thorson (1976) did most of the work that resulted in new reports for the Caribbean, while, in the Pacific, several authors (F. Marques, J.B Oliveira, M. Santoro, G. Ponce de León, and R. Majeuska) lead the description of new species of marine parasites for Costa Rica. Neodermata flatworms (Trematoda, Monogenea, and Cestoda) dominate the metazoan parasitic fauna known for Costa Rica, representing 71.9% of all the marine parasite species, all of which are parasites of vertebrates (Figure 3). Within Neodermata, 42.5% of the total reported species are trematodes, and most of them (55 out of 62) are classified in the order Plagiorchiida. Most trematodes reported were found in turtles (64.5%), and fish (29%), parasitic or epibiont crustaceans were found mainly in fish (32.2%), and cestodes have been found mainly in elasmobranchs (mostly in rays) (82.8%) (Figure 3).
Sixty-one different marine or brackish water species have been identified as hosts for this marine parasite diversity in Costa Rica. Sea turtle species (L. olivacea, C. mydas, and Eretmochelys olivacea) and fish species are the hosts for most of the marine parasites reported (Figure 4A). The rest of the species have been reported in elasmobranchs, dolphins, and a few species as parasites of some crustaceans, such as crabs, lobsters, or barnacles. Most parasites were obtained as adults from the digestive tract, while other common parasite collection sites were the gills of fish (Figure 4B).
2.3. Platyhelminthes
Most marine parasites reported in Costa Rica are intestinal neodermatan platyhelminths, mostly trematodes and Cestodes.
2.3.1. Trematodes
Most of the reports on marine parasites of Costa Rica are trematodes (Figure 3). Digenean trematodes have been the most reported marine parasites in the Caribbean and the Pacific (Appendix A, Table A1). They have been found parasitizing bony fishes, sea turtles, and dolphins. Several families of the order Plagiorchiida are present as parasites of Costa Rica’s marine vertebrates, and 7 out of these 62 reports were new species when reported (Supplementary Table S1). The digestive tract of hosts was the most frequent localization. Even when no marine trematode parasites have been reported in elasmobranchs (rays and sharks), 62 marine trematode species are informed for Costa Rica: 40 species in sea turtles, 18 species in fish, and 4 species in dolphins. These trematodes belong mainly to the order plagiorchiida and are classified into 21 different families. Families Pronocephalidae and Hemiuridae are the most diverse in sea turtles and fish, respectively, while the Brachycladidae family has been the only found up to now in dolphins from Costa Rica.
2.3.2. Trematdoes from Sea Turtles
The biodiversity and other aspects of trematode infections in turtles of Costa Rica are better known today thanks to the work of Mario Santoro and his collaborators. They devoted much of their work over several years investigating these aspects, mainly in the north Caribbean and North Pacific [29,30,31,32,33,36,37,38]. Thanks to their work, they described one new species and six new reports of marine parasites of sea turtles of the Caribbean and the Eastern Tropical Pacific (ETP) as a part of the reports of 40 marine turtle parasites not previously known for Costa Rica (Appendix A, Table A1).
A total of 33 species of plagiorchiid and 7 diplostomid trematode parasites have been reported in Costa Rican sea turtles: 20 species in the family Pronocephalidae, 6 species in Spirorchiidae, 5 in the family Microscaphidiidae; and the rest are in the families Cladorchiidae, Opecoelidae, Gorgoderidae, Pachypsolidae, and Plagiorchiidae (Figure 5). Such diversity has been recorded from only three out of the seven sea turtle species arriving on Costa Rican coasts: the green turtle C. mydas (mostly from Tortuguero National Park, in the north Caribbean), the olive ridley turtle Lepidochelys olivacea (mostly from Ostional beach, in the north Pacific), and E. imbricata (also from Ostional beach). Pleurogonius tortugeroi sp.n was described from material collected from the lower intestine of C. mydas from Tortuguero National Park in 2007 [30].
Five more trematode species (four in Pronocephalidae and one in Spirorchiidae) found in E. imbricata were new reports for sea turtle parasites in the Eastern Pacific [37]. Up to now, research on sea turtle parasites has revealed that Pronocephalidae is a very common family of digenean sea turtle parasites in Costa Rica and that there is a significant overlap among digenean parasite species of sea turtles in the Pacific of Costa Rica and other places of the Pacific coast of the American continent [33,34,35,36,37,38,39,40,41,42,54,55,56]. Within the trematodes, only partial genetic sequences of some ribosomal genes have been published for Homalometron lesliorum, Ekuarhuni papillatus, and Forticulcita isabelae (Appendix A, Table A1).
Using histopathological analyses, Santoro and collaborators have additionally provided information on the pathological changes caused by the parasites on its hosts, mainly at Tortuguero (Caribbean Coast) and Gulf of Nicoya (Pacific Coast). They found lesions in the heart and great vessels caused by spirorchiids in nesting C. mydas, killed by jaguars Panthera onca, at Tortuguero National Park. Lesions were caused mainly by Learedius learedi, Hapalotrema postorchis, and Monticellius indicum. Eggs of these parasites were found affecting other tissues and organs like the digestive tract, spleen, gall bladder, urinary bladder, and other sites in the host [37].
Most studies on sea turtle parasites have been performed on relatively few stranded or nesting individuals. Santoro [42] pointed out that it is difficult to clarify how ontogenetic and ecological factors such as diet, foraging habits, habitat, or population density influence the helminth community of a given turtle species with a such scarcity of data. Many of the previously cited factors are also affected by global warming and habitat loss [5]. Still, there is no data on what is happening with parasites of sea turtles concerning those changes.
2.3.3. Monogeneans
Fourteen species of monogeneans in nine families have been reported for Costa Rica. Four of them were reported as new species (Appendix A, Table A1). Adult monogeneans are inhabitants of the gills of fish or cloacal membranes of aquatic turtles or amphibians. In marine environments of Costa Rica, they have been found in 12 different species of hosts, mainly carangid fish in the Gulf of Nicoya and the north Pacific coast [12,50], bull sharks in brackish environments of Barra del Colorado [18], and one species, Jaliscia caballeroi, was found parasitizing the skin of olive ridley turtles in the Pacific coast [46]. All monogenean marine parasites of Costa Rica have been found parasitizing their hosts’ gills or skin (Appendix A, Table A1). The latest additions of monogenean species for Costa Rica were made by Aguilar-Aguilar and collaborators in 2018 [50]. Their reports increased the marine monogenean reports by adding three species to the list. The family Microcotylidae is represented by three species, one in the skin of the olive ridley turtle, L. olivacea, one in the red snapper fish Lutjaus colorado, and one in the bull shark Carcharhinus leucas. Hexabothriidae, Diclidophoridae, and Chauaneidae (each with two species reported) have been found in fish and elasmobranchs (Figure 6).
2.3.4. Cestodes
A total of 29 species of cestode parasites of marine Costa Rican fauna have been reported since 1976 [19]. Tetraphyllideans (15 spp.) accounted for 51.7% of the cestode species found up to now, followed by Phyllobothriideans (5 spp.). The Tetraphyllidean family Onchobothriidae is the one with more species reported, all in elasmobranchs, mainly rays (Figure 7). Cestode parasites in marine environments of Costa Rica have been found parasitizing mainly rays of the Dasyatidae, Myliobatidae, Urotrygonidae, Narcinidae, and Pristidae; the bull shark Charcharhinus leucas and dolphins (three spp. in the tetrabothriidae family found in several Stenella species) (Appendix A, Table A1). All of them but two were found in the digestive tract (intestine, spiral valve, rectum) one species, Phyllobothrium delphini, was extracted from a subcutaneous blubber in the dolphin Stenella coeruleoalba, and one species, Monorygma grimaldii, was found in the intestine, testis, and uterine ligaments (Appendix A, Table A1).
No cestode parasites have been reported in Costa Rican sea turtles or fish. The most diverse cestode genus of marine cestodes in Costa Rica is Acanthobothrium (Onchobothriidae), with eight species described in the 1990s in three papers published by the group headed by Marques; in these papers, they reported new species being those eight Acanthobotrhium species, plus one Acanthobothrioides species (A. pacificus, also in the Onchobothriidae family) while sampling different species of rays [22,23,24,25]. Cestoda is the parasite group where more new marine helminth parasites have been discovered and described as new species, with 15 species reported as new, including one new genus, Escherbothrium, represented by the species E. molinae found in a ray, Urotrygon chilensis, described by Berman and Brooks [57] (Appendix A, Table A1). DNA sequences from the r28S gene of Escherbothrium sp. were identified from a sample in Urotrygon aspidura, but morphological details were not annotated by the author [58], within cestode marine parasites of Costa Rica; this is the only genetic sequences available. The latest additions to the list of marine cestode parasites were made by Oliveira and collaborators in dolphins in 2011 [49]. Besides the study by Oliveira, all other additions to the list of marine cestode parasitic fauna were made before 1998.
2.4. Nematodes
Five species of nematode worms in four families have been reported as parasites of marine animals in Costa Rica, all of them in the Pacific [49]. Four of them were found to be endoparasites of dolphins (stranded), and one species in the spiral valve of a dasyatid ray (Himantura pacifica), which resulted in being a new species [59] (Appendix A, Table A1). Anisakis sp., the most prevalent, was found in the digestive tract of dolphins, causing gastritis [49], while Halocercus lagenorhynchi was collected from the lungs and air passage of dolphins causing granulomatous pneumonia [49], and individuals of Crassicauda anthonyi were collected from the kidneys of Ziphius cavirostris with partial destruction of these organs [49]. All those nematode parasites were new geographic records for the Pacific coast of Central America and increased the reported occurrence of the parasites in new hosts [49]. Even though sea turtle parasites have been thoroughly investigated in Costa Rica, no parasitic nematodes from sea turtles have been reported in Costa Rica. Furthermore, nematodes are the most diverse group of parasitic helminths; however, to date, very few species have been identified as parasites of Costa Rican marine fauna.
2.5. Acanthocephalans
Only three species in two families of acanthocephalan marine parasites have been reported for Costa Rica, all from the Pacific coast, each in the digestive tract of a different teleost fish species (Appendix A, Table A1). No acanthocephalan species in marine animals have been reported in the Caribbean. Koronacantha pectinaria (originally described as Tegorhynchus pectinarius) was described by Van Cleave in 1940 based on material obtained from an uncertain host in Bahía Culebra, Pacific coast of Costa Rica, with no other publications on this species since then [60]. Further investigations on parasites of marine fishes from Charmela Bay, México [61] found several specimens later identified as T. pectinarius. To make a comparison with the original material, researchers realized that the original material from Van Cleave was lost, so they collected more material in the type locality in Bahía Culebra. These specimens were redescribed based on 16 male and 32 female specimens from Costa Rica and México found in the fish Microlepidotus brevipinnis (Perciformes: Haemulidae) and assigned this parasite to the species Koronacantha pectinaria. The site of infection for all these specimens was the intestine and caecum. This one was the first report of males of this parasite, and until 2015, it was also the only report of an acanthocephalan parasitizing Costa Rica’s marine fauna [60]. In 2015 Pinacho-Pinacho and collaborators found the species Neoechinorhynchus mamesi parasitizing the intestines of sleeper fish (Dormitator maculatus, Dormitator latifrons), and in 2020, Rosas-Valdés reported Floridosentis pacifica in the intestines of a mullet Mugil curema, collected during their research about the genetic variation of the genus Floridosentis in mullets from the Americas [51,62]. To our knowledge, studies on K. pectinaria other than taxonomic are lacking; the species has been used to explore molecular phylogeny within the Neodermata group [62], and genetic sequences (LSU, ITS, and cox 1) from Floridosentis specimens from this study are the only genetic sequences of any costarican marine acanthocephalan known up to now [51].
2.6. Hirudinean Annelids
Santoro and collaborators described lesions on the skin of sea turtle C. mydas from Tortuguero, Caribbean coast of Costa Rica, produced by leeches, Ozobranchus branchiatus [63]. They found traumatic purulent and ulcerative dermatitis lesions in more than 50% (n = 47) of turtles sampled associated with O. branchiatus and eggs of this leech on the surface of the carapace of 39 of those turtles. That information is relevant as O. branchiatus is one of the candidates to be a mechanical vector of fibropapilloma-associated turtle herpesvirus in sea turtles [63,64]. Majewska and collaborators, in 2015, found a high prevalence of O. branchiatus in L. olivacea sea turtles from Ostional, Guanacaste, and found a much less prevalent presence of another Ozobranchus species, O. margoi also in the olive ridley turtle from Ostional [40].
2.7. Parasitic Crustaceans
Thirty-one species of marine crustaceans living as ectoparasites or as epibionts have been recorded for Costa Rica. Most of them are copepods (12 spp.) and cirripedes (12 spp.), and seven other species are isopods, amphipods, or decapods. Figure 8 illustrates the diversity of crustacean marine parasites at the family level in each type of host (Figure 8). Only two parasitic crustacean species have been recorded from the Caribbean, one cirripede and one copepod; the rest are reports from the Pacific (Appendix A, Table A1).
2.7.1. Parasitic Malacostracan Crustaceans
Five species of isopods have been found as parasites of marine animals in Costa Rica. Most of them (four) are in the family Bopyridae and are parasites of palaemonid and porcellanid crabs. One more species, Cymothoa exigua (Cymothoidae), has been found in snapper fish (several species of Lutjanus). The material of Aporobopyrus trilobatus collected from Costa Rica was found in a new host for this parasite species, the crab Petrolisthes ortmanni [45]. In the same paper, Markham reports the presence of a new species in the genus Aporobopyrus, A. bourdonis, in Petrolisthes edwardsi, also collected in Costa Rica. Cymothoid isopods are parasites represented in Costa Rica by the species Cymothoa exigua, which is distributed from the Gulf of California to southern Ecuador and Islas Galápagos. This species was first collected from Golfo de Nicoya, between Isla Jesucita and Islas Negritos, between 1979 and 1981 as a parasite of Pomadasys maculatus; this fish does not occur in the ETP), so the identification of the host is uncertain. Later in 1990, three new host species for this parasite were reported in Costa Rica (Lutjanus colorado, L. jordani, and L. peru). Two of these hosts, L. colorado and L. jordani, from Costa Rica, were also new host reports for C. exigua in the eastern tropical Pacific [44]. Only one species of parasitic amphipod has been reported for Costa Rica, Podocerus chelonophilus in sea turtles, L. olivacea, from the Pacific [48]. Finally, one unidentified grapsid crab in the genus Planes was found on the carapace of L. olivacea; this is the only report of a decapod as a marine epibiont of sea turtles in Costa Rica [39].
2.7.2. Copepodes
Twelve species of marine parasitic copepods, most of them in the family Caligidae, have been reported to be present in Costa Rica (Figure 8, Appendix A, Table A1). These species were found mainly on the gills and fins of Scombrid and Carangid fishes [11,15,20,65], although one species was found on the pectoral fins of bluefin sharks [43], and one harpacticoid balenophilid copepod, Balaenophilus manatorum was found in the olive ridley turtle, L. olivacea [39]. One additional new species of Caligid, Lepeophtheirus alvaroi, was found in a plankton sample in Isla del Coco and was found unattached to its host [65]. Three of the copepod species reported for Costa Rica were newly described species. One of the copepod species, Pennella instructa (Pennelidae), was found parasitizing the barnacle Conchoderma virgatum [15].
2.7.3. Cirripedians
Twelve species of ectoparasitic cirripedes have been reported for Costa Rica, most of them in the families Lepadidae and Coronulidae, mainly as ectoparasites of the olive ridley turtle L. olivacea. Also in sea turtles, two chelonibiid cirripedes were reported, Stepnaholepas muricata (on C. mydas and E. imbricata), and Chelonibia testudinaria (on L. olivacea) [40,66]. Two species of cirripedes were reported as ectoparasites of other crustaceans; one of them was a new species of sacculinid Ptychascus barnwelli, which was found under the abdomen of Ocypodid crabs (genus Minuca) in the Caribbean of Costa Rica [67]. The description of this new species was based on the ultrastructural study of the cyprid larval stage. The other is Paralepas quadrata which was found on the lobster Panulirus penicillatus [30]. Another Coronulid species, Xenobalanus globicipitis, was found over the caudal fluke of the dolphin Stenella attenuata in the Pacific of Costa Rica (Appendix A, Table A1) [49]. All but one of these reports were made after 2010; before this year, only the new species Ptychaschus barnwelli had been described for Costa Rica.
3. Discussion
To our knowledge, this is the first comprehensive list (all taxonomic groups recorded) of metazoan marine parasite species published for a country. In general, these types of reviews focus on listing the parasites of some group of hosts, in the case of the Americas, mainly marine fish parasites of North and South America [68,69]. Most reports are species lists made by a singular group of researchers that studied in a relatively short time a particular group of hosts (e.g., fish, elasmobranchs, dolphins, sea turtles). This list, therefore, provides information that will serve as a baseline for future research on the diversity of parasites in the marine environments of Costa Rica.
Few authors who have studied marine parasites in Costa Rica have been working in this country for a prolonged period and published more than one paper reporting marine parasite species for Costa Rica, as seen in Figure 1. Although marine parasitology in Costa Rica started in the decade of 1930s, the decades of the late 1970s, 1990s, and the years after 2000 have been the most productive in terms of new reports. This can be since marine biodiversity, in the early years of research, was performed mostly by expeditions that used to collect within a very large range of distance, in several countries, with the only objective of describing new species but not focusing on a particular place, with little time of sampling effort in each location [10,11,12,13,14,15]. Research groups that focused more on a particular type of host and in particular locations came to Costa Rica in the 1970s, 1990s, and after, and so made more additions to the marine parasites fauna than in the early years; this is the case of the works by Watson and Thorson with elasmobranchs, Oliveira and collaborators with stranded dolphins, and Santoro and collaborators with sea turtles [19,22,23,24,25,33,34,35,36,37,38,49]. In addition, marine biological sciences in Costa Rica did not begin to develop until around 1971 [70].
Since then, no research group, with its base in Costa Rica, has dedicated systematic efforts to marine wildlife parasitology in this country, and throughout the history of marine parasitology in Costa Rica, it can be concluded that this topic, has been studied mainly by foreign researchers on very specific groups of parasites and hosts (from all the reported species, only 2 out of 146 reports come from a group headed by Costa Rican Scientists). These foreign researchers have made important contributions during limited periods without the emergence or consolidation of an autochthonous marine parasitology research group in the country. Because of the above, in Costa Rica, there is a lack of material deposited in the national scientific collections of parasitology or zoology; most of the comparison material is deposited in other collections, mainly in México, the United States of America, and Switzerland. This is a global problem regarding natural history collections in Latin America, and that continues today, with several groups of researchers that come to Latin American countries, collect biological samples, and take them to other countries, leaving neither specimen deposited in the local biological collections, nor a strengthen capability in Costa Rican researchers to make further advances in the field. Undoubtedly, this harms the pace of progress in the knowledge of the marine parasite biodiversity of Costa Rica [71].
Among the marine parasite groups, helminth parasites have been the most reported parasites in Costa Rica and around the world [2,72]. This can be explained as helminth parasites are more diverse than other marine animal groups that have developed a parasitic style of life [2]. Additionally, their specific identification based on morphology is usually plausible, and sampling methods are easier to gather the specimens; while protozoans, bacteria, and viruses are difficult to sample and identify without using several immunological and molecular techniques.
Most of the parasitic helminths of marine hosts described or reported so far for Costa Rica correspond to trematodes and cestodes, and the identifications were mostly based on the morphology of the adult (for most species, other stages of the life cycle remain undetermined). A simpler morphology-based taxonomy in adult trematodes and cestodes in contrast to nematodes could explain why so few marine parasitic nematodes have been identified in marine environments of Costa Rica, even though parasitic nematodes are very abundant and diverse in vertebrates living in other environments [72,73,74].
Despite advances in molecular techniques for the identification of nematodes, genetic information for many marine parasitic nematodes is still scarce [73,74]. Only 61 of the nearly 6700 marine species have been reported as hosts for marine parasites in Costa Rica; these are extremely poor numbers in a country with 3.5% of the marine biodiversity of the world [75]. Most marine parasites found in Costa Rica have been collected from relatively near shore habitats, even in brackish waters, so places further from the coast and deeper water environments have been little sampled in search of these organisms. In addition, research has focused on turtles, elasmobranchs, and teleost fish; researchers have found marine parasites only in 35 marine fish of Costa Rica; that number represents very little in comparison to the nearly 800 fish species estimated to be in Costa Rican marine environments between 0 and 200 m depth [75]. There is lacking a more comprehensive search of parasites in the widest range of hosts. For all the above, the 146 species of marine parasites found so far probably represent a very small percentage of the actual diversity.
The difference in marine parasite species between the Caribbean and the Pacific is remarkable, with 51 species reported for the Caribbean and 101 species reported in the Pacific. This is, in part, a consequence of the lower amount of research carried out in the Caribbean on the subject of marine parasites (11 papers published) in comparison to the Pacific, where 41 papers have been published, 78.4% of the marine parasite species from the Caribbean of Costa Rica have been recorded from one single study with the bull shark Carcharhinus leucas [19] and one principal study on the digenean parasites of the green turtle C. mydas [33]. The active search for marine parasites is a difficult task, and much of it relay on searching in nesting turtles or stranded mammals. Stranded mammals are more prevalent on the Pacific coast of Costa Rica than on the Caribbean coast and so in other parts of Central America as well [76,77]. In terms of sea turtle nesting sites, the North Caribbean and North Pacific are the sites with the highest numbers of nesting sea turtles, Lepidochelys olivacea in the Pacific and C. mydas in the Caribbean. However, less research has been done on the rest of the Costa Rican Caribbean coast (e.g., the parasites of the nesting leatherback turtle Dermochelys coriacea have not been investigated). In general, in both the Pacific and the Caribbean, the other sea turtle species that nest in much lower numbers in Costa Rica, Caretta caretta, Dermochelys coriacea, and the Pacific Green Turtle (Chelonia agazzisi), have not been investigated for parasites.
Digenean trematodes are diverse in sea turtles; these types of helminths were found in several fish and dolphin species in Costa Rica. Among digenean trematodes, the family Pronocephalidae is diverse in the marine trematode parasitic fauna of Costa Rica. This family of parasites is primarily found in the intestines of marine reptiles, with few species occurring in fish and other marine vertebrates [78]. In Costa Rica, these parasites have been recorded mainly from the green turtle C. mydas and the endangered hawkbill turtle E. imbricata. Several of the species found in Costa Rica have been previously recorded in the same host species in other studies. In Brazil, species found in hawksbill turtle E. imbricata, like Cricocephalus albus, Carettacola stunkardi, Hapalotrema postorchis, and Monticellius indicum have been found in the same host [54]. No digenean trematodes have been reported from Costa Rican elasmobranchs; this group is, by far, a less diverse group in this type of host. The extensive adaptive radiation of cestodes in elasmobranchs has “muted” the trematode diversity in this vertebrate group; on the contrary, in fish and sea turtles, trematodes have had a bigger adaptive radiation that exceeds greatly that of cestodes [79,80].
There is little information other than taxonomic about pathology caused by trematodes in marine animal hosts. Regarding spirorchiid-derived pathology in C. mydas, one study was the first to investigate parasites in non-stranded Caribbean sea turtles of Costa Rica and the only study in marine turtles of Costa Rica, up to now, revealing the effects of those parasites on the host [37]. In this work, they found the species Learedius learedi, Hapalotrema postorchis, Monticellius indicus, and Amphiorchis solus parasitizing the hearth and great vessels of C. mydas in the North Caribbean of Costa Rica [37]. The parasites were present in 39 out of 40 turtles in Tortuguero and caused aneurysms, nodular thickening of the vessels’ walls, thrombi, and other complications; all these complications are common in the cases of sea turtle spirorchidiasis. All genera found in Costa Rican sea turtles have been found to cause similar pathologies in other studies, being Learedius species the most prevalent [81]. In other countries, recent research has determined that heavy helminth infections on C. mydas and E. imbricata generate significant health complications in individuals with significant intestinal damage, in the case of the microascaphidiid parasite Octangium sp., or at the level of other organs such as the myocardium, e.g., the case of spirorchiid trematodes [81,82]. More research is needed to determine other effects of helminth parasitic infestations on turtles in Costa Rica.
Regarding cestodes diversity, most parasites have been reported in the digestive system of elasmobranchs, and most of them are in the family Onchobothriidae [19,22,23,24,25]. The family Onchobothriidae contains mainly parasitic species of elasmobranchs [83,84]. The genus Acanthobothrium is one of the most diverse in the family and is associated with various species, mainly rays [83,84]. Many of the new species described in Costa Rica are cestodes placed in this genus studied in the 1990s. Other cestode species found in the marine fauna of Costa Rica were Tetrabothriid and Phyllobothriid cestodes collected in the digestive system of stranded dolphins; in Central America, the study by Oliveira on parasites of stranded dolphins in the Pacific is the only study that reported parasites of these mammals of Costa Rica [49]. Major tetraphyllidean cestodes that are parasites of dolphins worldwide are Phyllobothrium delphini and Monorygma grimaldi, both reported by Oliveira in Costa Rica. The role of dolphins in the life cycle of these parasites is as intermediate hosts, no adult stages of these species are known to occur in dolphins. Large sharks that prey on dolphins are thought to be the definitive hosts for these parasites [85]. As there is no data on endoparasites of costarican sharks other than the bull shark, it is not surprising that these parasites in their adult forms have not been reported yet in Costa Rica.
Monogenean parasites of Costa Rica have been found mostly on the gills of several species of carangid fish, tuna, and puffer fish. Mazocraeidan monogeneans are common in fish as ectoparasites that feed on mucus and epithelial cells on the surface of the body of the fish hosts, causing morbidity and mortality usually when they are in great numbers in the gills. Some studies have hypothesized the possibility that these parasites could also act as vectors of viruses [86]. The species found so far in Costa Rica have been reported previously in South America [87]. In lists published about marine monogeneans of Asia (China, Japan), several families of monogeneans are represented [88,89]. It would be expected a high diversity of monogeneans in tropical marine environments as predicted by a greater diversity of hosts [90]. However, the search for this type of parasite in Costa Rica is also scarce; they have been searched only in a limited group of hosts, mainly carangid fishes.
Marine biologists have also made important contributions to the knowledge of Costa Rican marine parasites belonging to several groups of crustaceans. After the 1990s, a greater number of reports of parasitic or epibiont crustacean species have been made for Costa Rica [29,30,31]. Bopyrid isopods are a well-represented isopod family around the world. Probopyrus pandalicola had been previously reported in the Eastern Pacific from the branchial cavity of several species of decapods, including the genus Palaemon; in Costa Rica, it was found in the branchial cavity of Palaemon hiltoni [29]. In the Gulf of California, this species was registered as a parasite of Palaemon pandaliformis, Palaemon ritteri, and Palaemon nortropi [91]. Aporobopyrus trilobatus was previously known from the Caribbean and Pacific coast of Mexico, and Petrholistes edwardsi was already known to be a host of A. bourdonis from the Pacific of Mexico [31,45,92].
The role of some crustacean species as parasites or simply epibionts is still difficult to establish. For some families, such as the Caligidae copepods, their role as ectoparasites is clearer [93]; also, for some large cirripedes [94], that can cause certain limitations to their hosts if they are small, but for others, it is not yet clear if they cause any harm to the host. Whatever the case, research on marine metazoans parasites other than helminths is still widely an unexplored terrain, as is the search for marine parasites in invertebrate hosts; in Costa Rica, this is not an exception.
Basic questions like the richness and abundance of parasites in a given marine zone in Costa Rica cannot be answered yet, nor how these species interact with other community components or how those interactions between different hosts can favor the transmission of a given group of parasites. For many marine parasites, their specific role as parasites in the health and sickness of the host has not been determined. Of course, sampling some alive marine hosts is very challenging. For example, feces or serum samples, even today, are not very useful in the morphological identification of most marine parasites (because eggs or larval stages that can be found in those samples have not been described), and molecular identification is not available for most of them, and very few sequences of the Costa Rican marine parasites are deposited in the main genetic databases.
Additionally, maintaining living individuals from the marine environment in controlled conditions to study their parasites employing experimental infections to describe their life cycles and pathology is hardly possible because of numerous technical difficulties, research permits, and several other ethical and technical issues.
The last checklist of the helminth fauna of Costa Rica was published in 2004 [46], and after that, only a few additions have been made to the list, and the Colección Helmintológica de Costa Rica [47]. Only four holotypes out of the 32 marine parasite species described from material of Costa Rica are deposited in Costa Rican Collections, and, in the case of voucher specimens, only 32% of the reported species of marine parasites of Costa Rica have voucher specimens deposited in local biological collections (Supplementary Table S1).
There is a need for more research on marine wildlife parasites in Costa Rica. Research lines followed by new parasitologists in Costa Rica have focused mostly on human parasitology and molecular diagnosis of medical and veterinary important parasites with a clinical and epidemiological approach, while other basic research on wildlife parasitology has been left behind for several years. Since the diversity and other aspects of the ecology of the parasites in the marine environment are important indicators of the ecosystem’s health, it is necessary that the interest in basic research in marine parasitology arises again in the country and that this is supported by the sources of the research funding of public universities, research institutions, and other entities inside and outside of Costa Rica.
Scientific knowledge on marine parasites of Costa Rica, other than taxonomic, is very scarce. Many of the reports have depended upon the finding of stranded dead or nearly dead hosts. That situation, together with the scarcity of voucher specimens that represent our metazoan marine parasite fauna, does not allow us to infer the dynamics of parasites at the population level and higher, given that systematic research has not been carried out to fully understand the diversity of marine parasites in Costa Rica, and little work have been done regarding the parasite communities and their interactions. Climate change and macroenvironmental disturbances could be making many parasite species silently disappear. In some contexts, the biological traits of some parasite species make them highly vulnerable to these disturbances, e.g., complex life cycles, host specificity, and narrow climatic tolerances [95]. Conversely, in other contexts, pollution and climate change are making parasites more abundant and a cause of important diseases for their hosts [96].
4. Materials and Methods
An exhaustive search of publications about metazoan marine parasite species reported in Costa Rica was performed. The keywords “Costa Rica” and “Central America” were used together with the words “marine parasites”, “marine helminths”, “marine acanthocephalan”, “marine trematodes”, “marine fish parasites”, “marine turtle parasites”, “parasitic copepods”, “parasitic crustaceans”, “monogenean”, “marine epibionts”, “marine parasitic Mollusca” in the scientific search engines Google Scholar, Microsoft Academic, and BASE. Additionally, the “Colección Helmintológica de Costa Rica” databases and archives were analyzed to supplement the information. The WORMS database was also consulted to guarantee the accepted names are being used. The list of species of metazoan marine parasites known for Costa Rica was obtained, along with other information about the research that has been carried out on some of these species as well as the expeditions and history of the collections of marine parasites in different species since the first quarter of the twentieth century. All metazoan marine or brackish water parasites reported for Costa Rica were included, and protozoans and other microorganisms were excluded from this review. Figures were elaborated using the software Microsoft PowerBI and Microsoft Excel, while the map was created using QGIS 3.0 and Google Earth Pro applications.
5. Conclusions
A total of 146 species of marine parasites have been reported in Costa Rica; of them, 32 new species were described from Costa Rica material. Three species of sea turtles and elasmobranchs (mainly rays) have been the hosts most thoroughly studied in the search for parasites in Costa Rica, in total 61 marine species have been recorded as hosts of at least one metazoan marine parasite, which is very few compared to the enormous diversity of marine wildlife. Helminths from the Trematoda and Cestoda constitute the groups better represented, in inside these groups, few families are associated mainly with the most sampled hosts. Studies other than taxonomic about marine parasites in Costa Rica are also lacking, as well as ecological studies. This review points out the importance of enhancing the science of marine parasitology in Costa Rica because of its implications for the knowledge of marine biodiversity, the ecological importance of parasites in marine biological communities, and conservation.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/2673-6772/3/2/14/s1, Figure S1: Number of voucher specimens and country where they have been deposited, Figure S2: Number of type specimens and country where they have been deposited, Table S1: Open database of the list of metazoan marine parasites reported for Costa Rica from 1937 to 2022.
Author Contributions
Conceptualization, A.S.-B. and J.C.; methodology, J.C.; formal analysis, A.S.-B.; investigation, A.S.-B., and J.C.; resources, A.S.-B. and J.C.; data curation, A.S.-B.; writing—original draft preparation, A.S.-B.; writing—review and editing, J.C. and A.R.; funding acquisition A.R. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
The core database that reunited all information on marine parasites of Costa Rica (gathered from the published papers and the “Colección Helmintológica de Costa Rica”) is an open Database and is part of the Supplementary archives of this publication.
Acknowledgments
J.C. thanks the Universidad de Costa Rica for supporting basic research in marine biodiversity. A.S.B. and A.R. thanks to Universidad de Costa Rica for supporting the project “Colección Helmintologica de Costa Rica”, a biological reference collection of helminth parasites of Costa Rica and other countries.
Conflicts of Interest
The authors declare no conflict of interest.
Appendix A
Table A1.
List of marine parasites reported for Costa Rica from 1937 to 2022.
| Parasite Species | Class/Order | Host Species | Reporting Reference | Location |
|---|---|---|---|---|
| Acanthobothrium nicoyaensea | Cestoda: Tetraphyllidea | Aetobatus narinari | [22] | Punta Morales, Pacific Coast |
| Acanthobothrium costarricensea | Cestoda: Tetraphyllidea | Dasyatis longus | [23] | Punta Morales, Pacific Coast |
| Acanthobothrium cimari a | Cestoda: Tetraphyllidea | Dasyatis longus | [23] | Punta Morales, Pacific Coast |
| Acanthobothrium puntarenasense a | Cestoda: Tetraphyllidea | Dasyatis longus | [23] | Punta Morales, Pacific Coast |
| Acanthobothrium vargasi a | Cestoda: Tetraphyllidea | Dasyatis longus | [23] | Punta Morales, Pacific Coast |
| Acanthobothrium campbelli a | Cestoda: Tetraphyllidea | Urotrygon chilensis | [23] | Punta Morales, Pacific Coast |
| Acanthobothrium franus a | Cestoda: Tetraphyllidea | Narcine entemedor | [25] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Acanthobothrium inbiorium a | Cestoda: Tetraphyllidea | Narcine entemedor | [25] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Acanthobothroides pacificus a | Cestoda: Tetraphyllidea | Himantura pacifica | [24] | Playa Panamá, Guanacaste |
| Scalithrium geminum a | Cestoda: Tetraphyllidea | Himantura pacifica | [24] | Playa Panamá, Guanacaste |
| Cylindrophorus hypoprioni | Cestoda: Tetraphyllidea | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Triloculatum triloculatum | Cestoda: Tetraphyllidea | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Escherbothrium molinae a,b | Cestoda: Tetraphyllidea | Urotrygon chilensis | [57] | Punta Morales, Puntarenas |
| Anthobothrium pristis | Cestoda: Tetraphyllidea | Pristis perotteti | [19] | Barra del Colorado, Caribbean Coast |
| Anthobothrium laciniatum | Cestoda: Tetraphyllidea | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Pterobothrioides carvajali a,b | Cestoda: Trypanorhyncha | Dasyatis longus | [26] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Dasyrhynchus varioucinnatus | Cestoda: Trypanorhyncha | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Callitetrarhynchus gracilis | Cestoda: Trypanorhyncha | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Heteronybelinia estigmena | Cestoda: Trypanorhyncha | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Otobothrium penetrans | Cestoda: Trypanorhyncha | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Cathetocephalus thatcheri | Cestoda: Cathetocephalidea | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Tetrabothrius forsteri | Cestoda: Tetrabothriidea | Stenella coeruleoalba Stenella attenuata | [49] | Playa hermosa, Guanacaste |
| Strobilocephalus triangularis | Cestoda: Tetrabothriidea | Stenella coeruleoalba | [49] | undefined location |
| Trigonocotyle sp. | Cestoda: Tetrabothriidea | Stenella longirostris | [49] | Tamarindo, Guanacaste |
| Phyllobothrium delphini | Cestoda: Phyllobothridea | Stenella coeruleoalba | [49] | undefined location |
| Phyllobothrium pristis a | Cestoda: Phyllobothridea | Pristis perotteti | [19] | Barra del Colorado, Caribbean Coast |
| Paraorygmatobothrium nicaraguensis a | Cestoda: Phyllobothridea | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Monorygma grimaldii | Cestoda: Phyllobothridea | Stenella coeruleoalba Stenella attenuata Tursiops truncatus | [49] | undefined location |
| Scyphophyllidium leuci a | Cestoda: Phyllobothridea | Charcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Hargicola oligoplites | Monogenea: Mazocraeidea | Oligoplites altus | [50] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Mazocraes sp. | Monogenea: Mazocraeidea | Anchovia macrolepidota | [50] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Neohexostoma euthynni | Monogenea: Mazocraeidea | Euthynnus lineatus | [50] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Ahpua piscicola | Monogenea: Mazocraeidea | Caranx Caballus, Oligoplites altus | [32] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Pseudomazocraes monsivaisae | Monogenea: Mazocraeidea | Selene peruviana | [32] | Puntarenas |
| Cemocotylella elongata a | Monogenea: Mazocraeidea | Caranx caballus | [12] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Hargicotyle louisianensis | Monogenea: Mazocraeidea | Menticirrhus sp. | [32] | Puntarenas |
| Heterobothrium ecuadori | Monogenea: Mazocraeidea | Sphoeroides sp. | [18] | Puntarenas |
| Polymicrocotyle manteri | Monogenea: Mazocraeidea | Lutjanus colorado | [32] | Puntarenas |
| Jaliscia caballeroi | Monogenea: Mazocraeidea | Lepidochelys olivacea | [46,47] | undefined location |
| Dermophthirius maccallumi a | Monogenea: Mazocraeidea | Carcharhinus leucas | [19] | Barra del Colorado, Caribbean |
| Neomicrocotyle pacifica | Monogenea: Mazocraeidea | Caranx sexfasciatus | [14] | Bahía Culebra, Guanacaste |
| Heteronchocotyle leucas a | Monogenea: Diclybothriidea | Carcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Erpocotyle carcharhini a | Monogenea: Diclybothriidea | Carcharhinus leucas | [19] | Barra del Colorado, Caribbean Coast |
| Alloinfundiburictus costaricae a | Trematoda: Plagiorchiida | Haemulopsis axillaris | [13] | Bahía Culebra, Guanacaste |
| Bucephalus gorgon a | Trematoda: Plagiorchiida | Caranx hippos and Seriola | [13] | Bahía Culebra, Guanacaste |
| Prosorhynchoides sp. | Trematoda: Plagiorchiida | Caranx caballus | [46,47] | undefined location |
| Manteria brachyderus | Trematoda: Plagiorchiida | Caranx caballus/Oligoplites altus | [21] | undefined location |
| Brachycladium palliatum | Trematoda: Plagiorchiida | Stenella coeruleoalba | [49] | undefined location |
| Brachycladium pacificum | Trematoda: Plagiorchiida | Stenella longirostris | [49] | undefined location |
| Nasitrema globicephalae | Trematoda: Plagiorchiida | Stenella attenuata | [49] | undefined location |
| Oschmarinella albamarina | Trematoda: Plagiorchiida | Ziphius cavirostris | [49] | undefined location |
| Homalometron lesliorum a | Trematoda: Plagiorchiida | Eucinostomus currani | [28] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Theletrum lamothei a | Trematoda: Plagiorchiida | Echidna nocturna | [27] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Ectenurus virgula | Trematoda: Plagiorchiida | Fistularia commersonii | [27] | Ocotal, Guanacaste |
| Lecithochirium microstomum | Trematoda: Plagiorchiida | Fistularia commersonii | [27] | Ocotal, Guanacaste |
| Lecithochirium monticelli | Trematoda: Plagiorchiida | Syhodus sp. | [18] | Ocotal, Guanacaste |
| Mecoderus oligoplitis | Trematoda: Plagiorchiida | Oligoplites altus, Oligoplites refulgens, Oligoplites sp. | [21] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Ekuarhuni papillatus a,b | Trematoda: Plagiorchiida | Mugil curema | [52] | Punta Dominical, Puntarenas |
| Forticulcita isabelae a | Trematoda: Plagiorchiida | Mugil curema | [52] | Punta Dominical, Puntarenas |
| Trifoliovarium sp. | Trematoda: Plagiorchiida | Echidna nocturna | [27] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Bianium plicitum | Trematoda: Plagiorchiida | Arothron hispidus, Sphoeroides sp. | [16] | Bahía prieta, Guanacaste and Mata de Limón, Puntarenas |
| Hypocreadium myohelicatum | Trematoda: Plagiorchiida | Epinephelus itajara | [27] | Cuajiniquil, Gulf of Santa Elena, Guanacaste |
| Stephanostomum casum | Trematoda: Plagiorchiida | Caranx caballus | [27] | Playa Ocotal, Guanacaste, Pacific Coast |
| Tergestia laticollis | Trematoda: Plagiorchiida | Caranx caballus | [27] | Playa Ocotal, Guanacaste, Pacific Coast |
| Plesiochorus cymbiformis | Trematoda: Plagiorchiida | Lepidochelys olivacea | [38] | Ostional National Wildlife Refuge, Nicoya Peninsula, North Pacific Coast |
| Enodiotrema megachondrus | Trematoda: Plagiorchiida | Lepidochelys olivacea | [38] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Enodiotrema reductum | Trematoda: Plagiorchiida | Eretmochelys imbricata | [41] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Pachypsolus irroratus | Trematoda: Plagiorchiida | Lepidochelys olivacea | [38] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Microscaphidium reticulare | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Microscaphidium warui | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Deuterobaris intestinalis | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Polyangium linguatula | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Octangium hyphalum | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Schizamphistomum scleroporum | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Schizamphistomum erratum | Trematoda: Plagiorchiida | Chelonya mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Helicometra fasciata | Trematoda: Plagiorchiida | Muraena sp. | [13] | Bahía Culebra, Guanacaste |
| Cricocephalus resectus | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Cricocephalus megastomus | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Cricocephalus albus | Trematoda: Plagiorchiida | Chelonia mydas, Eretmochelys imbricata | [33,41] | Tortuguero National Park, North Caribbean Coast, Gulf of Nicoya |
| Desmogonius desmogonius | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pronocephalus obliquus | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Charaxicephaloides polyorchis | Trematoda: Plagiorchiida | Chelonia mydas | [36] | Tortuguero National Park, North Caribbean Coast |
| Charaxicephalus robustus | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pleurogonius longiusculus | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pleurogonius sindhii | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pleurogonius sp. | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pleurogonius tortugueroi a | Trematoda: Plagiorchiida | Chelonia mydas | [34] | Tortuguero National Park, North Caribbean Coast |
| Pleurogonius linearis c | Trematoda: Plagiorchiida | Chelonia mydas, Eretmochelys imbricata | [33] | Tortuguero National Park, North Caribbean Coast, Gulf of Nicoya |
| Pleurogonius solidus | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pleurogonius lobatus | Trematoda: Plagiorchiida | Chelonia mydas, Eretmochelys imbricata | [33,41] | Tortuguero National Park, North Caribbean Coast, Gulf of Nicoya |
| Pleurogonius trigonocephalus c | Trematoda: Plagiorchiida | Eretmochelys imbricata | [41] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Rameshwarotrema uterocrescens | Trematoda: Plagiorchiida | Chelonia mydas | [35] | Tortuguero National Park, North Caribbean Coast |
| Adenogaster serialis c | Trematoda: Plagiorchiida | Eretmochelys imbricata | [41] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Pyelosomum crassum c | Trematoda: Plagiorchiida | Eretmochelys imbricata | [41] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Pyelosomum cochlear | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Pyelosomum posterorchis c | Trematoda: Plagiorchiida | Eretmochelys imbricata | [41] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Rhytidodoides similis | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Rhytidodoides intestinalis | Trematoda: Plagiorchiida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Clinostomum complanatum | Trematoda: Diplostomida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Learedius learedi | Trematoda: Diplostomida | Chelonia mydas | [33,37] | Tortuguero National Park, North Caribbean Coast |
| Hapalotrema postorchis | Trematoda: Diplostomida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Monticellius indicus | Trematoda: Diplostomida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Amphiorchis solus | Trematoda: Diplostomida | Chelonia mydas | [33] | Tortuguero National Park, North Caribbean Coast |
| Carettacola stunkardi c | Trematoda: Diplostomida | Eretmochelys imbricata | [41] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Neospirorchis sp. | Trematoda: Diplostomida | Chelonia mydas | [37] | Tortuguero National Park, North Caribbean Coast |
| Halocercus lagenorhynchi | Nematoda: Strongylida | Stenella coeruleoalba | [49] | Playa Panamá, Guanacaste |
| Halocercus sp. | Nematoda: Strongylida | Stenella attenuata Stenella longirostris | [49] | undefined location |
| Echinocephalus janzeni a | Nematoda: Rabditida | Himantura pacifica | [59] | undefined location |
| Crassicauda anthonyi | Nematoda: Rhabditida | Ziphius cavirostris | [49] | Matapalo, Puntarenas, Pacific Coast |
| Anisakis spp. | Nematoda: Rhabditida | Stenella coeruleoalba Stenella attenuata Stenella longirostris Ziphius cavirostris | [49] | undefined location |
| Koronacantha pectinaria | Palaeoacanthocephala: Echinorhynchida | Microlepidotus brevipinnis | [60] | Bahía Culebra, Guanacaste |
| Floridosentis pacifica | Eoacanthocephala: Neoechinorhynchida | Mugil curema | [51] | Punta Dominical, Puntarenas and Gulf of Nicoya |
| Neoechinorhynchus mamesi | Eoacanthocephala: Neoechinorhynchida | Dormitator maculatus, Dormitator latifrons | [62] | Playa Grande, Guanacaste |
| Ozobranchus branchiatus | Hirudinea: Rhynchobdellida | Chelonia mydas, Lepidochelys olivacea | [37,39,40] | Tortuguero National Park, North Caribbean Coast, Ostional wildlife refuge, Nicoya penninsula, north Pacific coast |
| Ozobranchus margoi | Hirudinea: Rhynchobdellida | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Cymothoa exigua | Crustacea: Isopoda | Lutjanus colorado, L. jordani and L. peru | [44] | undefined location |
| Probopyrus pandalicola | Crustacea: Isopoda | Palaemon hiltoni | [29] | Gulf of Nicoya, Puntarenas, North Pacific Coast |
| Aporobopyrus bourdonis a | Crustacea: Isopoda | Petrolisthes edwardsii | [45] | Junquillal, Area of conservation, Guanacaste |
| Aporobopyrus aduliticus | Crustacea: Isopoda | Petrolisthes sp. | [31] | Punta Dominical, Puntarenas and Gulf of Nicoya |
| Aporobopyrus trilobatus | Crustacea: Isopoda | Petrolisthes ortmanni | [45] | Punta Dominical, Puntarenas and Gulf of Nicoya |
| Podocerus chelonophilus | Crustacea: Amphipoda | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Planes sp. | Crustacea: Decapoda | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Anelasma squalicola c | Crustacea-Cirripedia: Pollicipedomorpha | Etmopterus benchleyi | [53] | Off Pacific Coast |
| Paralepas quadrata | Crustacea-Cirripedia: Scalpellomorpha | Panulirus penicillatus | [30] | Chatam Bay, Isla del Coco |
| Conchoderma auritum | Crustacea: Cirripedia:Scalpellomorpha | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Conchoderma virgatum | Crustacea: Cirripedia:Scalpellomorpha | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Lepas hilli | Crustacea: Cirripedia:Scalpellomorpha | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Ptychascus barnwelli a | Crustacea: Cirripedia:Kentrogonidae | Minuca burgersi, Minuca mordax & Minuca vocator | [67] | Limón, Moin. |
| Stephanolepas muricata | Crustacea: Cirripedia:Balanomorpha | Eretmochelys imbricata, Chelonya mydas | [63] | Golfo Dulce, Pacific Coast and Gulf of Nicoya |
| Chelonibia testudinaria | Crustacea: Cirripedia:Balanomorpha | Lepidochelys olivacea | [39,40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Platylepas decorata | Crustacea: Cirripedia:Balanomorpha | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Platylepas hexastylos | Crustacea: Cirripedia:Balanomorpha | Lepidochelys olivacea | [40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Stomatolepas elegans | Crustacea: Cirripedia:Balanomorpha | Lepidochelys olivacea | [39,40] | Ostional National Wildlife Refuge, Nicoya Peninsula |
| Xenobalanus globicipitis | Crustacea: Cirripedia:Balanomorpha | Stenella attenuata | [49] | Bajamar Puntarenas |
| Pandarus satyrus | Crustacea: Copepda: Siphonostomatoida | Prionace glauca | [43] | undefined location |
| Pennella instructa | Crustacea: Copepda: Siphonostomatoida | Conchoderma virgatum | [15] | Chatam Bay, Isla del Coco |
| Gloiopotes ornatus | Crustacea: Copepda: Siphonostomatoida | sailfish (SNI) | [15] | Chatam Bay, Isla del Coco |
| Caligus mutabilis | Crustacea: Copepda: Siphonostomatoida | Scomberomorus brasiliensis | [20] | undefined location |
| Caligus omissus a | Crustacea: Copepda: Siphonostomatoida | Scomberomorus sierra | [20] | undefined location |
| Caligus chorinemi | Crustacea: Copepda: Siphonostomatoida | Seriola lalandi | [20] | Bahía Culebra, Guanacaste |
| Lepeophtheirus alvaroi a | Crustacea: Copepda: Siphonostomatoida | Unknown | [65] | Bahía Wafer, Isla del Coco |
| Unicolax collateralis a | Crustacea: Copepda: Siphonostomatoida | Euthynnus lineatus | [20] | undefined location |
| Pseudocycnus appendiculatus | Crustacea: Copepda: Siphonostomatoida | Thunnus albacares | [20] | undefined location |
| Cybicola buccatus | Crustacea: Copepda: Siphonostomatoida | Scomberomorus sierra, Scomberomorus brasiliensis | [20] | undefined location |
| Lernanthropus micropterygis | Crustacea: Copepda: Siphonostomatoida | Seriola sp. | [11] | Bahía Culebra, Guanacaste |
| Balaenophilus manatorum | Crustacea: Copepoda:Harpacticoida | Lepidochelys olivacea | [39] | Ostional National Wildlife Refuge, Nicoya Peninsula |
a was reported as a new species (sp.nov), b was described as a new genus, and c report is new for the Eastern Tropical Pacific.
References
- Rohde, K. Ecology of marine parasites. Helgol. Meeresunters 1984, 37, 5–33. [Google Scholar] [CrossRef]
- Carlson, T.A.; Dallas, T.A.; Alexander, L.W.; Phelan, A.L.; Phillips, A.J. What would it take to describe the global diversity of parasites? Proc. R. Soc. B 2020, 287, 20201841. [Google Scholar] [CrossRef] [PubMed]
- Dobson, A.; Lafferty, K.D.; Kuris, A.M.; Hechinger, R.F.; Jetz, W. Homage to Linnaeus: How many parasites? How many hosts? Proc. Natl. Acad. Sci. USA 2008, 105, 11482–11489. [Google Scholar] [CrossRef]
- Poulin, R. Parasite biodiversity revisited: Frontiers and constraints. Int. J. Parasitol. 2014, 44, 581–589. [Google Scholar] [CrossRef] [PubMed]
- Morand, S. (macro-) Evolutionary ecology of parasite diversity: From determinants of parasite species richness to host diversification. Int. J. Parasitol. Parasites Wildl. 2015, 4, 80–87. [Google Scholar] [CrossRef] [PubMed]
- Gaston, K.J. Global patterns in biodiversity. Nature 2000, 405, 220–227. [Google Scholar] [CrossRef]
- Poulin, R. Meta-analysis of seasonal dynamics of parasite infections in aquatic ecosystems. Int. J. Parasitol. 2020, 50, 501–510. [Google Scholar] [CrossRef]
- Santoro, M.; Laccarino, D.; Bellisario, B. Host biological factors and geographic locality influence predictors of parasite communities in sympatric sparid fishes off the southern Italian coast. Sci. Rep. 2020, 10, 13283. [Google Scholar] [CrossRef]
- Hudson, P.J.; Dobson, A.P.; Lafferty, K.D. Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 2006, 21, 381–385. [Google Scholar] [CrossRef]
- Cortés, J. Historia de la investigación marino-costera en Bahía Culebra, Pacífico Norte, Guanacaste, Costa Rica. Rev. Biol. Trop. 2012, 60, 19–37. [Google Scholar] [CrossRef]
- Wilson, C.B. Parasitic copepods taken during the Third Hancock Expedition to the Galapagos Islands. Allan Hancock Pac. Exped. 1937, 2, 24–30. [Google Scholar]
- Meserve, F. Some monogenetic trematodes from Galapagos Islands and the neighbouring Pacific. Rep. Hancock Pac. Exped. 1938, 2, 31–89. [Google Scholar]
- Manter, H.W. Digenetic trematodes of fishes from the Galapagos Islands and the neighboring Pacific. Allan Hancock Pac. Exped. 1940, 2, 329–496. [Google Scholar]
- Van Cleave, H.J. The Acanthocephala collected by the Allan Hancock Pacific Expedition, 1934. Rep. Collect. Obtained Allan Hancock Pac. Exped. 1932–1948 1940, 2, 501–527. [Google Scholar]
- Schmitt, W.L. Decapod and other Crustacea collected on the presidential cruise of 1938. Smithson. Misc. Collec. 1939, 98, 1–29. [Google Scholar] [CrossRef]
- Caballero, E.; Brenes, R.R.; Jiménez-Quirós, O. Helmintos de la República de Costa Rica IV. Algunos trematodos de animales domésticos y silvestres. Rev. Biol. Trop. 1957, 5, 135–155. [Google Scholar]
- Brenes, R.R. Catálogo de los helmintos parásitos de Costa Rica. Rev. Biol. Trop. 1961, 9, 67–95. [Google Scholar] [CrossRef]
- Bravo-Hollis, M.; Arroyo, G. Helmintos de peces costarricenses. An. Inst. Biol. Univ. Nal. Autón. Méx. Ser. Zool 1962, 33, 79–95. [Google Scholar]
- Watson., D.E.; Thorson, T.B. Helminths from elasmobranchs in Central American fresh waters. In Investigations of the Ichthyofauna of Nicaraguan Lakes; Thorson, T.B., Ed.; University of Nebraska-Lincoln: Lincoln, NE, USA, 1976; pp. 629–640. [Google Scholar]
- Cressey, R.F.; Cressey, H.B. Parasitic copepods of mackerel-and tuna-like fishes (Scombridae) of the world. Smithson. Contrib. Zool. 1980, 311, 1–186. [Google Scholar] [CrossRef]
- Ponciano, R.G. Estudio Taxonómico de Trematodos de Peces Marinos y Dulceacuícolas de México y América Central. Licenciatura; Facultad de Ciencias, Universidad Autónoma de México: México, Mexico, 1986. [Google Scholar]
- Brooks, D.R.; McCorquodale, S. Acanthobothrium nicoyaense n. sp. (Eucestoda: Tetraphyllidea: Onchobothriidae) in Aetobatus narinari (Euphrasen) (Chondrichthyes: Myliobatiformes: Myliobatidae) from the Gulf of Nicoya, Costa Rica. J. Parasitol. 1995, 81, 244–246. [Google Scholar] [CrossRef]
- Marques, F.; Brooks, D.R.; Monks, S. Five new species of Acanthobothrium van Beneden, 1849 (Eucestoda: Tetraphyllidea: Onchobothriidae) in stingrays from the gulf of Nicoya, Costa Rica. J. Parasitol. 1995, 81, 942–951. [Google Scholar] [CrossRef] [PubMed]
- Marques, F.; Brooks, D.R.; Ureña, H.M. Two new species of Tetraphyllidean cestodes in Himantura pacifica (Chondrichthyes: Myliobatiformes: Dasyatididae) from the northwest coast of Costa Rica. J. Parasitol. 1996, 82, 302–306. [Google Scholar] [CrossRef] [PubMed]
- Marques, F.; Centritto, R.; Stewart, S.A. Two new pecies of Acanthobothrium in Narcine entemedor (Rajiformes: Narcinidae) from the northwest coast of Guanacaste Peninsula, Costa Rica. J. Parasitol. 1997, 83, 927–931. [Google Scholar] [CrossRef]
- Campbell, R.A.; Beveridge, I. Pterobothrioides, a new genus of tapeworms (Cestoda: Trypanorhyncha: Pterobothriidae) from dasyatid stingrays in the Eastern Atlantic and Pacific Oceans. Syst. Parasitol. 1997, 38, 81–91. [Google Scholar] [CrossRef]
- Ponce de León, G.P.P.; León-Règagnon, V.; Scott, M. Theletrum lamothei sp. nov.(Digenea), parasite of Echidna nocturna from cuajiniquil, Guanacaste, and other digenes of marine fishes from Costa Rica. Rev. Biol. Trop. 1998, 46, 345–354. [Google Scholar]
- Parker, J.H.; Curran, S.S.; Overstreet, R.M.; Tkach, V.V. Examination of Homalometron elongatum Manter, 1947 and description of a new congener from Eucinostomus currani Zahuranec, 1980 in the Pacific ocean off Costa Rica. Comp. Parasitol. 2010, 77, 154–163. [Google Scholar] [CrossRef]
- Jiménez, P.; Vargas, M. Probopyrus pandalicola (Isopoda: Bopyridae) infesting Palaemonetes hiltonii (Crustacea: Caridea), along the Pacific coast of Costa Rica. Rev. Biol. Trop. 1990, 38, 457–462. [Google Scholar]
- Zullo, V.A. Zoogeography of the shallow-water cirriped fauna of the Galápagos Islands and adjacent regions in the tropical eastern Pacific. In Galápagos Marine Invertebrates; James, M.J., Ed.; Springer: Boston, MA, USA, 1991; pp. 173–192. [Google Scholar] [CrossRef]
- Markham, J.C. The Isopoda Bopyridae of the eastern Pacific–missing or just hiding. Proc. San Diego Soc. Natl. His. 1992, 17, 1–4. [Google Scholar]
- Brooks, D.R.; Lamothe-Argumedo, R.; Garcia-Prieto, L.; Osorio-Sarabia, D.; de León, G.P.P. Catalogo de la Coleccion Nacional de Helmintos. J. Parasitol. 1998, 84, 907. [Google Scholar] [CrossRef]
- Santoro, M.; Greiner, E.C.; Morales, J.A.; Rodríguez-Ortíz, B. Digenetic trematode community in nesting sea turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. J. Parasitol. 2006, 92, 1202–1206. [Google Scholar] [CrossRef]
- Santoro, M.; Greiner, E.C.; Morales, J.A.; Rodríguez-Ortíz, B. A new pronocephalid, Pleurogonius tortugueroi n. sp. (Digenea), from the intestine of green sea turtles (Chelonia mydas) in Costa Rica. Parassitologia 2007, 49, 97–100. Available online: https://pubmed.ncbi.nlm.nih.gov/18412051/ (accessed on 13 November 2022). [PubMed]
- Santoro, M.; Morales, J.A.; Stacy, B.; Greiner, E.C. Rameshwarotrema uterocrescens trematode parasitism of the oesophageal glands in green sea turtles (Chelonia mydas). Vet. Rec. 2007, 160, 59–60. [Google Scholar] [CrossRef] [PubMed]
- Santoro, M.; Brandmayr, P.; Greiner, E.C.; Morales, J.A.; Rodríguez-Ortíz, B. Redescription of Charaxicephaloides polyorchis Groschaft and Tenora 1978 (Digenea: Pronocephalidae) from the green turtle Chelonia mydas in Costa Rica. Helminthologia 2009, 46, 97–99. [Google Scholar] [CrossRef]
- Santoro, M.; Morales, J.A.; Rodríguez-Ortíz, B. Spirorchiidiosis (Digenea: Spirorchiidae) and lesions associated with parasites in Caribbean green turtles (Chelonia mydas). Vet. Rec. 2007, 161, 482–486. [Google Scholar] [CrossRef] [PubMed]
- Santoro, M.; Morales, J.A. Some digenetic trematodes of the olive ridley sea turtle, Lepidochelys olivacea (Testudines, Cheloniidae) in Costa Rica. Helminthologia 2007, 44, 25–28. [Google Scholar] [CrossRef]
- Robinson, N.J.; Lazo-Wasem, E.M.; Butler, B.O.; Lazo-Wasem, E.A.; Zardus, J.D.; Pinou, T. Spatial distribution of epibionts on olive ridley sea turtles at Playa Ostional, Costa Rica. PLoS ONE 2019, 14, e0218838. [Google Scholar] [CrossRef]
- Majewska, R.; Santoro, M.; Bolaños, F.; Chaves, G.; De Stefano, M. Diatoms and Other Epibionts Associated with Olive Ridley (Lepidochelys olivacea) Sea Turtles from the Pacific Coast of Costa Rica. PLoS ONE 2015, 10, e0130351. [Google Scholar] [CrossRef]
- Santoro, M.; Morales, J.A.; Bolaños, F.; Chaves, G.; De Stefano, M. Helminths of hawksbill turtle (Eretmochelys imbricata) from the Pacific coast of Costa Rica. Helminthologia 2015, 52, 67–70. [Google Scholar] [CrossRef]
- Santoro, M.; Mattiucci, S. Sea Turtle Parasites. In Marine Biodiversity of Costa Rica, Central America; Wehrtmann, I.S., Cortés, J., Eds.; Springer Netherlands: Dordrecht, The Netherlands, 2009; Volume 86, pp. 507–519. [Google Scholar] [CrossRef]
- Rojas, J.R.; Rodríguez Solano, O.; Morales-Ramírez, A. Size and distribution of Pandarus satyrus (Copepoda: Pandaridae) on the blue shark Prionace glauca (Carcharhiniformes: Carcharhinidae) in Costa Rica. Rev. Biol. Trop. 2001, 49, 199–201. [Google Scholar]
- Williams, E.H.; Bunkley-Williams, L. New records of fish-parasitic isopods (Cymothoidae) in the eastern Pacific (Galápagos and Costa Rica). Not. Galapagos 2003, 2003, 21–23. [Google Scholar]
- Markham, J.C. New Records of Pseudionine Bopyrid isopods, including two new species and one new genus, infesting porcellanid Crabs (Decapoda: Anomura) on the Pacific coast of North and Central America. Bull. South. Calif. Acad. Sci. 2008, 107, 145–157. [Google Scholar] [CrossRef]
- Rodriguez-Ortíz, B.; García-Prieto, L.; de León, G.P.P. Checklist of the helminth parasites of vertebrates in Costa Rica. Rev. Biol. Trop. 2004, 52, 313–353. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Ortíz, B.; García-Prieto, L.; Herrera-Vázquez, J.; de León, G.P.P. Addendum to the Checklist of the helminth parasites of vertebrates in Costa Rica. Rev. Biol. Trop. 2004, 52, 355–361. [Google Scholar] [CrossRef] [PubMed]
- Cortés, J. Marine Fish Parasites. In Marine Biodiversity of Costa Rica, Central America; Wehrtmann, I.S., Cortés, J., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 521–533. [Google Scholar] [CrossRef]
- Oliveira, J.B.; Morales, J.A.; González-Barrientos, R.C.; Hernández-Gamboa, J.; Hernández-Mora, G. Parasites of cetaceans stranded on the Pacific coast of Costa Rica. Vet. Parasitol. 2011, 182, 319–328. [Google Scholar] [CrossRef] [PubMed]
- Aguilar-Aguilar, R.; Marcotegui, P.; Martorelli, S.; García-Prieto, L. New records for three species of monogeneans (Platyhelminthes) of marine fishes in the Gulf of Nicoya, Costa Rica. Bol. Soc. Zool. Urug. 2018, 27, 7–10. [Google Scholar] [CrossRef]
- Rosas-Valdez, R.; Morrone, J.J.; Pinacho-Pinacho, C.D.; Domínguez-Domínguez, O.; García-Varela, M. Genetic diversification of acanthocephalans of the genus Floridosentis Ward 1953 (Acanthocephala: Neoechinorhynchidae), parasites of mullets from the Americas. Infect. Genet. Evol. 2020, 85, 104535. [Google Scholar] [CrossRef]
- Andrade-Gómez, L.; García-Varela, M. Unexpected morphological and molecular diversity of trematode (Haploporidae: Forticulcitinae) parasites of mullets from the ocean Pacific coasts in Middle America. Parasitol. Res. 2021, 120, 55–72. [Google Scholar] [CrossRef]
- Angulo, A.; Sibaja-Cordero, J.A. First record of the parasitic barnacle Anelasma squalicola Darwin, 1852 (Pollicipedomorpha: Pollicipedidae) in the eastern Pacific Ocean and a new host report: Eretmopterus benchleyi Vásquez, Ebert & Long, 2015 (Squaliformes: Etmopteridae). Zootaxa 2021, 5072, 165–172. [Google Scholar] [CrossRef]
- Meira-Filho, M.R.C.; Andrade, M.F.; Domit, C.; Silva-Souza, A.T. A review of helminths of the green turtle (Chelonia mydas) in Brazil. Oecologia Aust. 2017, 21, 17–26. [Google Scholar] [CrossRef]
- Werneck, M.R.; Lima, E.H.S.M.; Pires, T.; Silva, R.J. Helminth parasites of the juvenile Hawksbill turtle Eretmochelys imbricata (Testudines: Cheloniidae) in Brazil. J. Parasitol. 2015, 101, 500–503. [Google Scholar] [CrossRef]
- Werneck, M.R.; Baldassin, P.; D’Azeredo, F.; Trazi, A.; Berger, B. The Hawksbill Sea Turtle Eretmochelys imbricata Linnaeus 1758 (Testudines, Cheloniidae) as new host of Hapalotrema postorchis Rao, 1976 (Digenea: Spirorchiidae). Comp. Parasitol. 2014, 81, 75–78. [Google Scholar] [CrossRef]
- Berman, R.; Brooks, D.R. Escherbothrium molinae n. gen. et n. sp. (Eucestoda: Tetraphyllidea: Triloculariidae) in Urotrygon chilensis (Chondrichthyes: Myliobatiformes: Urolophidae) from the Gulf of Nicoya, Costa Rica. J. Parasitol. 1994, 80, 775–780. [Google Scholar] [CrossRef] [PubMed]
- Ruhnke, T.R.; Caira, J.N.; Cox, A. The cestode order Rhinebothriidea no longer family-less: A molecular phylogenetic investigation with erection of two new families and description of eight new species of Anthocephalum. Zootaxa 2015, 3904, 51–81. [Google Scholar] [CrossRef] [PubMed]
- Hoberg, E.P.; Brooks, D.R.; Molina-Ureña, H.; Erbe, E. Echinocephalus janzeni n. sp. (Nematoda: Gnathostomatidae) in Himantura pacifica (Chondrichthyes: Myliobatiformes) from the Pacific coast of Costa Rica and Mexico, with historical biogeographic analysis of the genus. J. Parasitol. 1998, 84, 571–581. [Google Scholar] [CrossRef]
- Monks, S.; Marques, F.; Leon-Regagnon, V.; de León, G.P.P. Koronacantha pectinaria n. comb. (Acanthocephala: Illiosentidae) from Microlepidotus brevipinnis (Haemulidae) and Redescription of Tegorhynchus brevis. J. Parasitol. 1997, 83, 485–494. [Google Scholar] [CrossRef]
- García-Varela, M.; Nadler, S.A. Phylogenetic relationships among Syndermata inferred from nuclear and mitochondrial gene sequences. Mol. Phylogenet. Evol. 2006, 40, 61–72. [Google Scholar] [CrossRef]
- Pinacho-Pinacho, C.D.; Sereno-Uribe, A.L.; De León, G.P.P.; García-Varela, M. Checklist of the species of Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) in fishes and turtles in Middle-America, and their delimitation based on sequences of the 28S rDNA. Zootaxa 2015, 3985, 98–116. [Google Scholar] [CrossRef]
- Greenblatt, R.J.; Work, T.M.; Balazs, G.H.; Sutton, C.A.; Casey, R.N.; Casey, J.W. The Ozobranchus leech is a candidate mechanical vector for the fibropapilloma-associated turtle herpesvirus found latently infecting skin tumors on Hawaiian green turtles (Chelonia mydas). Virology 2004, 321, 101–110. [Google Scholar] [CrossRef]
- Rittenburg, L.; Kelley, J.; Mansfield, K.; Savage, A. Marine leech parasitism of sea turtles varies across host species, seasons, and the tumor disease fibropapillomatosis. Dis. Aquat. Organ. 2021, 143, 1–12. [Google Scholar] [CrossRef]
- Suárez-Morales, E.; Gasca, R.A. A new Lepeophtheirus (Copepoda: Siphonostomatoida: Caligidae) from Isla del Coco National Park, Costa Rica, Eastern Tropical Pacific. Rev. Biol. Trop. 2012, 60, 235–242. [Google Scholar] [CrossRef]
- Corrales-Gómez, N.; Herrera-Ulloa, A. first record of the turtle barnacle Stephanolepas muricata from the Pacific coast of Costa Rica. Mar. Turt. Newsl. 2012, 135, 9–10. [Google Scholar]
- Andersen, M.L.; Bohn, M.; Høeg, J.T.; Jensen, P.G. Cyprid ultrastructure and adult morphology in Ptychascus barnwelli, new species, and P. glaber (cirripedia: Rhizocephala), parasites on semiterrestrial crabs. J. Crustac. Biol. 1990, 10, 20–28. [Google Scholar] [CrossRef]
- Holmes, J.C. Helminth communities in marine fishes. In Parasite Communities: Patterns and Processes; Esch, G.W., Bush, A.O., Aho, J.M., Eds.; Springer: Dordrecht, The Netherlands, 1990; pp. 101–130. [Google Scholar] [CrossRef]
- Kohn, A.; Cohen, S.C.; Salgado-Maldonaldo, G. Checklist of Monogenea Parasites of Freshwater and Marine Fishes, Amphibians and Reptiles from Mexico, Central America and Caribbean; Magnolia Press: Auckland, New Zealand, 2006; pp. 1–114. [Google Scholar]
- Cortés, J. Historia del desarrollo de las ciencias del mar en la Escuela de Biología, Universidad de Costa Rica. Rev. Biol. Trop. 2009, 57, 16–18. [Google Scholar]
- Duarte, R.H. Between the national and the universal: Natural history networks in Latin America in the nineteenth and twentieth centuries. ISIS 2013, 104, 777–787. [Google Scholar] [CrossRef]
- Moravec, F.; Gibbons, L.M. Keys to the nematode parasites of vertebrates: Supplementary volume. Par. Vec. 2010, 3, 9. [Google Scholar] [CrossRef]
- Hernández-Orts, J.S.; Paso-Viola, M.N.; García, N.A.; Crespo, E.A.; González, R.; García-Varela, R.; Kuchta, R. A checklist of the helminth parasites of marine mammals from Argentina. Zootaxa 2015, 3936, 301–334. [Google Scholar] [CrossRef]
- Pereira, F.; González-Solís, D. Review of the parasitic nematodes of marine fishes from off the American continent. Parasitology 2022, 149, 1928–1941. [Google Scholar] [CrossRef]
- Bussing, W.A.; López, M. Marine Fish. In Marine Biodiversity of Costa Rica, Central America; Wehrtmann, I.S., Cortés, J., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 453–458. [Google Scholar] [CrossRef]
- Rodríguez-Fonseca, J.; Cubero-Pardo, P. Cetacean strandings in Costa Rica (1966–1999). Rev. De Biol. Trop. 2001, 49, 667–672. [Google Scholar]
- De Weerdt, J.; Ramos, E.A.; Pouplard, E.; Kochzius, M.; Clapham, P. Cetacean strandings along the Pacific and Caribbean coasts of Nicaragua from 2014 to 2021. Mar. Biodivers. Rec. 2021, 14, 13. [Google Scholar] [CrossRef]
- Blair, D. Keys to the Trematoda; CABI Publishing and The Natural History Museum: London, UK, 2002; Volume 2, p. 521. [Google Scholar]
- Olson, P.D.; Crib, T.H.; Tkach, V.V.; Bray, R.A.; Littlewood, D.T.J. Phylogeny and classification of the digenea (platyhelminthes: Trematoda). Int. J. Parasitol. 2003, 33, 733–755. [Google Scholar] [CrossRef]
- Cribb, T.H.; Cutmore, S.C.; Bray, R.A. The biodiversity of marine trematodes; then, now and in the future. Int. J. Parasitol. 2021, 51, 1085–1097. [Google Scholar] [CrossRef]
- Adnyana, W.; Ladds, P.W.; Blair, D. Prevalence and clinic-pathological studies on trematodiasis in marine turtles in Indonesia. Int. J. Sci. Res. Pub. 2020, 10, 274–295. [Google Scholar] [CrossRef]
- Oliveira, R.E.M.; Rossi, S.; Attademo, F.L.N.; Santoro, T.A.; Revoredo, R.A.; de Farias, D.S.D.; Lima, M.A.; Batista, J.S.; Silva, F.J.L.; Gavilan, S.A.; et al. Colocolic intussusception associated with Octangium sp. (Digenea: Microscaphidiidae) in a green sea turtle Chelonia mydas. J. Aquat. Anim. Health 2021, 33, 17–23. [Google Scholar] [CrossRef]
- Fyler, C.A.; Caira, J.N. Five new species of Acanthobothrium (Tetraphyllidea: Onchobothriidae) from the freshwater stingray Himantura chaophraya (Batoidea: Dasyatidae) in Malaysian Borneo. J. Parasitol. 2006, 92, 105–125. [Google Scholar] [CrossRef]
- Campbell, R.A.; Beveridge, I. The genus Acanthobothrium (Cestoda : Tetraphyllidea : Onchobothriidae) parasitic in Australian elasmobranch fishes. Invertebr. Syst. 2002, 16, 237–344. [Google Scholar] [CrossRef]
- Aznar, F.J.; Agustí, C.; Littlewood, D.T.J.; Raga, J.A.; Olson, P.D. Insight into the role of cetaceans in the life cycle of the tetraphyllideans (Platyhelminthes: Cestoda). Int. J. Parasitol. 2007, 37, 243–255. [Google Scholar] [CrossRef]
- Justine, J.L.; Bonami, J.R. Virus-like particles in a monogenean (platyhelminthes) parasitic in a marine fish. Int. J. Parasitol. 1993, 23, 69–75. [Google Scholar] [CrossRef]
- Kohn, A.; Cohen, S.C. South American Monogenea—List of species, hosts and geographical distribution. Int. J. Parasitol. 1998, 28, 1517–1554. [Google Scholar] [CrossRef]
- Jianying, Z.; Tingbao, Y.; Lin, L.; Xuejuan, D. A list of monogeneans from Chinese marine fishes. Syst. Parasitol. 2003, 54, 111–130. [Google Scholar] [CrossRef]
- Dyer, W.G.; Williams, E.H., Jr.; Williams, L.B. Monogeneans from marine fishes of Okinawa, Japan. Proc. Helminthol. Soc. Wash. 1989, 56, 64–68. [Google Scholar]
- Rohde, K. Diversity gradients of marine Monogenea in the Atlantic and Pacific Oceans. Experientia 1980, 36, 1368–1369. [Google Scholar] [CrossRef]
- Campos, E. Epicarídeos de Baja California : Distribution y notas ecologicas de Probopyrus pandalicola (Packard, 1879) en el Pacifico oriental. Rev. Biol. Trop. 1989, 37, 29–36. [Google Scholar]
- Romero-Rodríguez, J.; Álvarez, F. Bopyrid isopods of the genus Aporobopyrus infesting porcellanid crabs (Decapoda: Anomura) in the Gulf of California, Mexico: New host and parasite records. Proc. Biol. Soc. 2019, 132, 99–118. [Google Scholar] [CrossRef] [PubMed]
- Dojiri, M.; Ho, J.S. Systematics of the Caligidae, Copepods Parasitic on Marine Fishes; Brill: Leiden, The Netherlands; Boston, MA, USA, 2013; p. 460. [Google Scholar]
- Williams, E.H. Conchoderma virgatum (Spengler) (Cirripedia Thoracica) in association with Dinemoura latifolia (Steenstrup & Lutken) (Copepoda, Caligidea), a parasite of the shortfin mako, Isurus oxyrhynchus Rafinesque (Pisces, Chondrichthyes). Crustaceana 1978, 34, 109–110. [Google Scholar]
- Cizauskas, C.A.; Carlson, C.J.; Burgio, K.R.; Clements, C.F.; Dougherty, E.R.; Harris, N.C.; Phillips, A.J. Parasite vulnerability to climate change: An evidence-based functional trait approach. R. Soc. Open Sci. 2017, 4, 160535. [Google Scholar] [CrossRef]
- Rogalski, M.A.; Gowler, C.D.; Shaw, C.L.; Hufbauer, R.A.; Duffy, M.A. Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems. Philos. Trans. R. Soc. 2017, 372, 20160043. [Google Scholar] [CrossRef]
Figure 1.
Number of new marine parasite reports for Costa Rica over the decades. The first parasite collection was done in the early 1930s, and the last one in November 2022. More species have been reported in any decade in the Pacific. For the Pacific, the most productive decade was 2011–2020 and 2001–2010 for the Caribbean. The orange line represents species reported as new; most species reported as new were reported in the 1991–1980 decade. The period between 2001 and 2020 has been highly productive. Four species of marine parasites, three new, have been published for Costa Rica in the first two years of 2021–2030.
Figure 1.
Number of new marine parasite reports for Costa Rica over the decades. The first parasite collection was done in the early 1930s, and the last one in November 2022. More species have been reported in any decade in the Pacific. For the Pacific, the most productive decade was 2011–2020 and 2001–2010 for the Caribbean. The orange line represents species reported as new; most species reported as new were reported in the 1991–1980 decade. The period between 2001 and 2020 has been highly productive. Four species of marine parasites, three new, have been published for Costa Rica in the first two years of 2021–2030.
Figure 2.
Map showing the main locations (S-1 to S-17) where marine parasites have been collected and identified in Costa Rica. The number of species per site (red dots, different sizes, exact number in black numbers) and the total number of species per coast (blue dots). Santa Elena Bay (S-1), Gulf of Papagayo (S-2), Prieta Bay (S-3), Tamarindo Bay (S-4), Ostional (S-5), Gulf of Nicoya (S-6), Mata Palo (S-7), Punta Dominical (S-8), Golfo Dulce (S-9), 60 km off Quepos (S-10), species with no exact location reported in the Pacific (S-11), Isla del Coco (S-12), Barra del Colorado (14), Tortuguero (S-15), Moín (S-16), Species with no exact location reported in the Caribbean (S-17). Total number of species reported in the Caribbean (S-18), total number of species reported in the Pacific (S-13).
Figure 2.
Map showing the main locations (S-1 to S-17) where marine parasites have been collected and identified in Costa Rica. The number of species per site (red dots, different sizes, exact number in black numbers) and the total number of species per coast (blue dots). Santa Elena Bay (S-1), Gulf of Papagayo (S-2), Prieta Bay (S-3), Tamarindo Bay (S-4), Ostional (S-5), Gulf of Nicoya (S-6), Mata Palo (S-7), Punta Dominical (S-8), Golfo Dulce (S-9), 60 km off Quepos (S-10), species with no exact location reported in the Pacific (S-11), Isla del Coco (S-12), Barra del Colorado (14), Tortuguero (S-15), Moín (S-16), Species with no exact location reported in the Caribbean (S-17). Total number of species reported in the Caribbean (S-18), total number of species reported in the Pacific (S-13).
Figure 3.
Number of marine parasite species reported for Costa Rica according to the taxonomic group (left side labels) in which they are classified and according to the type of marine host. The main groups of parasites are trematodes parasitizing sea turtles and fish, and cestodes parasitizing elasmobranchs.
Figure 3.
Number of marine parasite species reported for Costa Rica according to the taxonomic group (left side labels) in which they are classified and according to the type of marine host. The main groups of parasites are trematodes parasitizing sea turtles and fish, and cestodes parasitizing elasmobranchs.
Figure 4.
(A) Number of parasite species per type of host species. (B) number of parasite species per anatomical localization.
Figure 4.
(A) Number of parasite species per type of host species. (B) number of parasite species per anatomical localization.
Figure 5.
Diversity of families of marine trematodes reported for Costa Rica and type of host in which they were reported, data from 1937 to 2022. The Plagiorchiida order is the most diverse; only one other order has been reported, the order Diplostomida. Family Pronocephalidae (20 spp.) from sea turtles represents the majority of the species reported for Costa Rica.
Figure 5.
Diversity of families of marine trematodes reported for Costa Rica and type of host in which they were reported, data from 1937 to 2022. The Plagiorchiida order is the most diverse; only one other order has been reported, the order Diplostomida. Family Pronocephalidae (20 spp.) from sea turtles represents the majority of the species reported for Costa Rica.
Figure 6.
Diversity of Monogenea families reported for Costa Rica and type of host they were reported, data from 1937 to 2022. The circular axis represents the number of species.
Figure 6.
Diversity of Monogenea families reported for Costa Rica and type of host they were reported, data from 1937 to 2022. The circular axis represents the number of species.
Figure 7.
Diversity of marine parasitic cestodes families reported for Costa Rica and type of host they were reported, data from 1937 to 2021. The circular axis represents the number of species.
Figure 7.
Diversity of marine parasitic cestodes families reported for Costa Rica and type of host they were reported, data from 1937 to 2021. The circular axis represents the number of species.
Figure 8.
Diversity of marine parasitic crustacean families reported for Costa Rica and type of host where they were reported, data from 1937 to 2021. The circular axes represent the number of species. Caligid copepods are better represented in fish, while bopyrid isopods are in porcellanid crabs.
Figure 8.
Diversity of marine parasitic crustacean families reported for Costa Rica and type of host where they were reported, data from 1937 to 2021. The circular axes represent the number of species. Caligid copepods are better represented in fish, while bopyrid isopods are in porcellanid crabs.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Solano-Barquero, A.; Rojas, A.; Cortés, J. Metazoan Marine Parasites of Costa Rica: A Review. Parasitologia 2023, 3, 116-141. https://doi.org/10.3390/parasitologia3020014
AMA Style
Solano-Barquero A, Rojas A, Cortés J. Metazoan Marine Parasites of Costa Rica: A Review. Parasitologia. 2023; 3(2):116-141. https://doi.org/10.3390/parasitologia3020014
Chicago/Turabian StyleSolano-Barquero, Alberto, Alicia Rojas, and Jorge Cortés. 2023. "Metazoan Marine Parasites of Costa Rica: A Review" Parasitologia 3, no. 2: 116-141. https://doi.org/10.3390/parasitologia3020014
APA StyleSolano-Barquero, A., Rojas, A., & Cortés, J. (2023). Metazoan Marine Parasites of Costa Rica: A Review. Parasitologia, 3(2), 116-141. https://doi.org/10.3390/parasitologia3020014
