Marine nematodes of Costa Rica: state of the art

Alcides Sánchez-Monge; Jorge Cortés

doi:10.3897/neotropical.19.e115345

Abstract

Nematoda is the fourth most diverse animal phylum and is widely distributed. Marine nematodes are generally the most speciose group of meiofauna, yet there are relatively few studies on the taxonomy and biodiversity of free living marine nematodes. Here we present a review of the existing scientific literature and data in international databases on marine nematodes of Costa Rica. Most of the papers currently available mentioned Nematoda as the most abundant phylum in terms of the number of individuals within sand samples, nonetheless, only three publications included taxonomic data such as the description of new species or new records. Most publications are for the Pacific coast and we found only one paper for the Caribbean coast of Costa Rica. Large sections of the coasts and almost all the Exclusive Economic Zone remain unexplored in terms of nematode diversity, abundance and ecological role. Ten species, five free-living and five parasitic species, have been reported from the coasts of Costa Rica. Several reports indicate the presence of nematodes without further identification. More effort should be dedicated to the taxonomic identification of nematodes since, in addition to being the most abundant group, they can also be used as biological indicators.

Key words

Caribbean, eastern Pacific, Isla del Coco, marine biodiversity, Nematoda

Introduction

Nematodes are the most abundant animal phylum in terms of the number of individuals, accounting for around 1% of the total animal biomass (Bar-On et al. 2018), and the fourth most speciose phylum with 25,043 described species (Zhang 2013). They are also ubiquitous and can be found in most ecosystems, even the Polar regions (Caruso et al. 2019), where they can represent several niches ranging from free-living species to plant and animal parasites. Nematodes can even be important as bioindicators of environmental quality in a broad range of natural and agro-ecosystems (Savin et al. 2015; Moura and Franzener 2017), including estuarine and marine ecosystems (de la Cruz and Vargas 1987; Geetanjali et al. 2002; Losi et al. 2013; Semprucci 2013; Ridall and Ingels 2021). The few taxonomic studies from tropical areas indicate that marine nematodes can be very diverse; for example, Armenteros et al. (2020) identified 215 species, 138 genera, 35 families, seven orders and two classes of marine nematodes in seagrass beds in Cuba.

The biodiversity of Costa Rica has been studied for a long time and some groups are relatively well known (Cortés and Wehrtmann 2009; Wehrtmann et al. 2009; Avalos 2019). However, nematological data is mainly focused on species of economic, veterinary or medical relevance whereas soil and marine nematode diversity is mostly unknown, especially free-living taxa. Several studies on Costa Rican marine ecosystems report the presence of nematodes from several environments such as beaches (Dexter 1974; Sibaja-Cordero et al. 2019), mud flats (de la Cruz and Vargas 1986, 1987; Vargas 1988, 2016; Dittmann and Vargas 2001), coral reefs (Guzmán et al. 1987), sandy bottoms (Sibaja-Cordero et al. 2016) and deep-waters (Neira et al. 2018; Gracia et al. 2020). Nonetheless, their taxonomic status is usually not assessed despite nematodes comprising up to 75% of the meiofauna of a muddy beach in the Gulf of Nicoya. Moreover, only three papers include taxonomic details of parasitic and free-living species (Cobb 1920; Hoberg et al. 1998; Oliveira et al. 2011).

In this paper we present a review of current knowledge of the marine nematodes of Costa Rica to highlight the lack of data on the diversity of the group as well as some limitations and gaps in their study and characterization.

Methods

To compile the information on marine nematodes of Costa Rica, we searched what has been published and what is recorded in international databases: OBIS (http://www.obis.org), GBIF (https://www.GBIF.org), Nemys (World Database of Nematodes http://nemys.ugent.be/) and WoRMS (World Register of Marine Species http://www.marinespecies.org/index.php). From the publications we extracted the level of taxonomic identification, sampling locality and the year. The international databases were searched using the key words “Nematoda” and “Costa Rica”. Reported localities were plotted on a map made with GMT (Wessel et al. 2013).

Results

From the 14 papers where marine nematodes of Costa Rica are mentioned, only one has information on the Caribbean coast (Table 1, Fig. 1) and all but three refer to nematodes as a group with no further identification. All ten identified species were found on the Pacific coasts, five of them being described by Cobb (1920).

Figure 1.

Sampling sites on the Caribbean and Pacific of Costa Rica where free-living and parasitic nematodes have been reported in literature. Dotted oval on the north side of Isla del Coco corresponds to more than 20 sampling points.

Table 1.

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Published reports of marine nematodes of Costa Rica.

Habitat	Locality	Coordinates	Years sampled	References
Caribbean coast
Sandy beach	Puerto Viejo, Limón	9°40'N, 82°44'W (9°39'N, 82°45'W)*	1971	Dexter 1974
Pacific coast
Unknown	Puntarenas, Puntarenas	Unknown	Unknown	Cobb 1920
Sandy beach	Playita Blanca, Guanacaste	10°34'N, 85°42'W (10°33'N, 85°42'W)*	1971	Dexter 1974
Muddy beach	Punta Morales, Golfo de Nicoya	10°04'N, 84°58'W	1983	de la Cruz and Vargas 1986
Muddy beach	Punta Morales, Golfo de Nicoya	10°04'N, 84°58'W	1984	de la Cruz and Vargas 1987
Coral reef	Isla del Caño, Puntarenas	8°43'N, 83°52'W	1984	Guzmán et al. 1987
Muddy beach	Punta Morales, Golfo de Nicoya	10°04'N, 84°58'W	1984–1985	Vargas 1988
Parasite	Playa Panamá, Guanacaste	10°15'N, 86°00'W	1992	Hoberg et al. 1998
Parasite	Along the Pacific coast, Guanacaste and Puntarenas	Several beaches along the Pacific coast	2001–2009	Oliveira et al. 2011
OMZ**	Off the central Pacific coast, Puntarenas	Several points between 400 and 1800 m depth	2009	Neira et al. 2018
Methane seep	Off the central Pacific coast, Puntarenas	8°55.778'N, 84°18.730'W	2010	Gracia et al. 2020
Methane seep	Off the central Pacific coast, Puntarenas	~1,000 m depth	2010	Gracia et al. 2020
Sandy bottom	Isla del Coco, Pacific Ocean	24 sampling stations around the island	2010	Sibaja-Cordero et al. 2016
Sandy beach	Golfito, Golfo Dulce	8°64.26'N, 83°17.40'W	2014–2017	Sibaja-Cordero et al. 2019
	Punta Morales, Golfo de Nicoya Junquillal, Guanacaste	10°06.30'N, 84°95.68'W
	Punta Morales, Golfo de Nicoya Junquillal, Guanacaste	10°96.86'N, 85°68.84'W

The most recent description is that of the parasitic species Echinocephalus janzeni from a sting ray (Hoberg et al. 1998). Four additional parasitic taxa were found in stranded cetaceans, mainly dolphins (Solano-Barquero et al. 2023).

Discussion

Several taxonomical changes and occurrence reports are available for these 10 species, and a summary of their status and related literature is given below.

Free-living taxa

The following free-living nematodes were all described by Cobb (1920) from samples collected from Puntarenas, on the Pacific coast of Costa Rica. It is important to point out that the locality name is misspelled in the descriptions and should be read “Puntarenas” instead of “Punta Arenas”.

Antomicron pellucidum Cobb, 1920

According to WoRMS, ten species comprise the genus Antomicron, the type species being A. pellucidum. Nonetheless, Holovachov (2012) recognizes only six valid species pointing out that several taxa in the genus were never found again; A. pellucidum remains valid despite the illustrations in the original description being insufficient for comparisons (Holovachov 2012). Remarkably, the specimen studied by Holovachov (2012) was found 274 m offshore at Turkey Point, Florida, Gulf of Mexico while the species was described from specimens from the Pacific coast off Costa Rica.

Hypodontolaimus punctulatus (Cobb, 1920) Filipjev 1934

= Iotadorus punctulatus Cobb, 1920.

WoRMS and Nemys register 27–30 species in the genus Hypodontolaimus but only 26 are regarded as valid by Venekey et al. (2019), including H. punctulatus. Three years earlier, Huang and Gao (2016) questioned the validity of H. punctulatus because only females were known; however, males are present in the original description (Cobb 1920) as stated by Venekey et al. (2019). No more details about H. punctulatus (including geographic distribution) were found.

Pseudochromadora quadripapillata Daday, 1899

= Desmodora cephalata (Cobb, 1920).

= Desmodora luticola (Timm, 1952).

= Desmodora quadripapillata (Daday, 1899).

= Micromicron cephalatum Cobb, 1920.

= Micromicron luticola Timm, 1952.

Pseudochromadora comprises thirteen species worldwide (WoRMS), but only five species are valid according to Muthumbi et al. (1995). P. quadripapillata was listed as P. luticola in a biodiversity survey in Brazil (Venekey et al. 2010) and reported as M. cephalatum from Vietnam (Gagarin and Thanh 2015). Current georeferenced records include the Caribbean coast of Belize, the Bay of Fundy on the Atlantic coast of Canada and the Maldives (GBIF). This species was reported by Cobb (1920) as a new marine taxon, however, WoRMS includes freshwater as a plausible environment. According to Verschelde et al. (2006), P. quadripapillata has been reported from New Guinea, Costa Rica, Brazil, two sites in USA, Nil Kamal, Bay of Bengal, Canada, Solomon Islands and Australia.

Pseudolella cephalata Cobb, 1920

Pseudolella cephalata remains valid within a dozen Pseudolella species (GBIF; Nemys) while Wang and Huang (2016) list fourteen species and provide a key to 11 valid species. No further information was found for this species except for “benthos” as its functional group (Nemys) which was not mentioned in the original description. Geographic distribution data are not available.

Zygonemella striata Cobb, 1920

= Daptonema matrona Neres, Fonseca-Genevois, Torres, Cavalcanti, Castro, Silva, Rieger & Decraemer, 2010.

Zygonemella striata is the only species of the genus Zygonemella. The synonymy of Z. striata and D. matrona was settled by Cunha et al. (2013). Interestingly, there are georeferenced records of new specimens from the Atlantic coast of Brazil (OBIS, Venekey et al. 2014) while the genus was described based upon samples from the Pacific coast of Costa Rica. More recently, a metabarcoding approach of Antarctic sediments found Operational Taxonomic Units (OTUs) with BLAST identity percentages matching Z. striata’s sequences in more than 90%, suggesting that this species may be present in that region (Fonseca et al. 2017).

Parasitic taxa

All parasitic species were found off the Pacific coast of Costa Rica.

Anisakis spp. Dujardin, 1845

= Conocephalus Diesing, 1860.

= Filocapsularia Deslongchamps, 1824.

= Peritrachelius Diesing, 1851.

= Stomachus Goeze, 1800.

Despite the number of valid species in databases varying from six (OBIS) or 12 (Nemys; WoRMS), or up to 16 (GBIF), the most recent review on the family Anisakidae registers only 10 valid species in this genus (Ángeles-Hernández et al. 2020). There is ample information since infection of human hosts, i.e. anisakiasis, is not uncommon (Patiño and Olivera 2019).

Several unidentified species of Anisakis were found in the digestive tracts of stranded cetaceans: three species of dolphins — Stenella coeruleoalba (Meyen, 1833), pantropical spotted dolphin, Stenella attenuata (Gray, 1846), striped dolphin and Stenella longirostris (Gray, 1828), spinner dolphin— and in Ziphius cavirostris (Cuvier, 1823), Cuvier’s beaked whale (Oliveira et al. 2011; Solano-Barquero et al. 2023). Records from freshwater fish are available (see Choc et al. 2018) but these are beyond the scope of this paper. As marine parasites, the family Anisakidae has a worldwide distribution (Ángeles-Hernández et al. 2020) as is the case for Anisakis spp. according to Cipriani et al. (2022).

Crassicauda anthonyi Chabaud, 1962

Thirteen species belong to the genus Crassicauda Leiper & Atkinson, 1914 (WoRMS). European coasts account for most of the georeferenced localities (GBIF). The specimens reported from Costa Rica were found in the kidneys of a stranded Cuvier’s beaked whale (Oliveira et al. 2011; Solano-Barquero et al. 2023), and they can be fatal according to Febronio et al. (2021). The distribution of C. anthonyi includes the Bay of Biscay, European waters and Costa Rican North Pacific Ocean (WoRMS); in addition, it has been reported from Australia and Brazil (Febronio et al. 2021) as well as Aguada, Aguadilla, Hatillo and Vieques Island in Puerto Rico and St. Thomas in the U.S. Virgin Islands (Colón-Llavina et al. 2009).

Echinocephalus janzeni Hoberg, Brooks, Molina-Ureña & Erbe, 1998

E. janzeni was described from Costa Rican and Mexican specimens collected in 1992 and 1997, respectively (Hoberg et al. 1998), and these specimens were isolated from the intestine of the sting ray Himantura pacifica (Beebe & Tee-Van, 1941). Hoberg et al. (1998) recognized only nine species in the genus but the number in databases ranges from ten (Nemys) to 18 (GBIF). More recently, Moravec and Justine (2021) and Saad et al. (2022) presented a key for only 12 valid species including E. janzeni. We also found that E. spinosus Müller, Adriano, Oliveira, Corrêa (2022), a parasite of freshwater stingrays, is absent from the lists and keys, probably due to its recent description.

Halocercus lagenorhynchi Baylis & Daubney, 1925 and Halocercus sp

= Delamurella Gubanov in Skrjabin 1952.

= Halocercus (Posthalocercus) Delyamure in Skrjabin 1942.

= Halocercus (Prohalocercus) Delyamure in Skrjabin 1942.

= Skrjabinalius Delyamure, 1942.

Halocercus comprises 13 valid species, the most recent being described in 2020 (WoRMS). Costa Rican Halocercus sp. were collected from the lungs of pantropical spotted dolphins and spinner dolphins, while H. lagenorhynchi was collected from air passages and lungs of stranded pantropical spotted dolphins (Oliveira et al. 2011; Solano-Barquero et al. 2023). As a side remark, Alfaro-Shigueto et al. (2022) omitted the findings of Halocercus lagenorhynchi in dolphins from the Pacific Ocean by only listing the Atlantic and Indian Oceans as reported localities. Nonetheless, this omission is in a non-peer-reviewed version of the on-line posted document and the information should therefore be used cautiously. Similarly, John et al. (2023) reported an infected dolphin off the Southwest coastline of India but the publishing platform of this information is also not peer-reviewed.

Abundance and unidentified taxa

The other papers on Costa Rican marine nematodes treat them as an important group of the meiofauna with no further details. They have been reported from both coasts of Costa Rica (Cortés and Wehrtmann 2009); several studies on the Pacific coasts have been performed since the 1970s, while only one paper, Dexter (1974), presents information on the Caribbean side focused on the diversity of macroscopic infauna of sandy beaches (Table 1, Fig. 1). In the late 1980s, the studies by de la Cruz and Vargas (1986, 1987) and Vargas (1988) on intertidal mud flat samples from the Gulf of Nicoya found that nematodes represented, respectively, 74.9%, 88.1% and 82% of the total organisms. Furthermore, the vertical distribution estimated by de la Cruz and Vargas (1987) showed that 82.7% of the nematodes were found in the top 2 cm of sediments and decreased to 5.3% at 4–9 cm depth. More recently, Sibaja-Cordero et al (2016) found that nematodes represented the second highest relative abundance (21.95%) from 24 out of 27 sampling points around Isla del Coco, totalling 3382 individuals. Unfortunately, all nematodes were treated as “Adenophorea spp. indet.” and no further information on their identity was given.

Abundance can be very different according to the sampling locality, as Guzmán et al. (1987) found in sediments of a coral reef at Isla del Caño Biological Reserve, with nematodes representing 19.12%. Furthermore, the numbers can fluctuate significantly between months, and also depending on sampling methodology, equipment and preservation of specimens in diversity studies (Vargas 1988).

Neira et al. (2018) assessed the distribution of meiofauna at different depths (400 and 1800 m) off the central Pacific coast. Nematodes had an overall mean relative abundance of 79.7%, ranging from 64.97% at 1800 m to a maximum of 99.9% in the Oxygen Minimum Zone (OMZ) at 400 m. The density of nematodes in Costa Rica’s OMZ (~3688 ind. 10 cm⁻²) is the highest reported compared to other OMZs in the eastern Pacific, but in terms of species richness it was one of the lowest (Neira et al. 2018). Gracia et al. (2020) studied the meio-epifaunal organisms that colonized woodblocks deployed at Mound 12, central Pacific coast, at ~1,000 m water depth. Woodblocks were placed at active methane seeps and inactive sites nearby. In such conditions, nematodes made up to 9.8% of the individuals, being more abundant in wood located in inactive sites.

There are no data of nematodes from other marine habitats, e.g., seagrasses or coral reefs in the Caribbean of Costa Rica. Interestingly, Dexter (1974) only reported nematodes in one out of five and eight Caribbean and Pacific beaches, respectively. Similarly, Sibaja-Cordero et al. (2019) found nematodes on the Pacific coast but not on the Caribbean side after sampling 16 and 12 sandy beaches, respectively.

Conclusion

Despite decades of research on Costa Rican biodiversity (Avalos 2019) marine nematodes from Costa Rica are practically unknown. Fourteen publications have mentioned Costa Rican marine nematodes but only three present taxonomic data for ten species; undoubtedly, there are far more species.

The diversity of marine nematodes is high in the tropics, for example in Cuban marine ecosystems (Armenteros et al. 2009, 2020); they are also the most abundant taxa in methane seeps in the Gulf of Cádiz (Pape et al. 2011). Similar coastal ecosystems do exist on both coasts of Costa Rica (Cortés 2016a, b) and there are also numerous methane seeps on the Pacific coast (Sahling et al. 2008; Levin et al. 2015). Regarding parasitic nematodes of marine organisms, there must be many more in Costa Rica (Solano-Barquero et al. 2023); for example, parasitic nematodes in the Mediterranean Sea have been found in edible scallops (Marcer et al. 2020) and in sea turtles (Santoro et al. 2019) such as the loggerhead turtle Caretta caretta (Linnaeus, 1758); the same, or similar, species are present in Costa Rica.

It is evident that taxonomic studies should be carried out to explore the actual diversity of marine nematodes in Costa Rica. More research is needed since ecological studies have highlighted the importance of this group in marine ecosystems and the potential of nematodes as biondicators (Geetanjali et al. 2002; Semprucci and Balsamo 2012; Losi et al. 2013; Savin et al. 2015; Ridall and Ingels 2021).

Acknowledgements

ASM thanks Daniel Apolonio Silva de Olivera (Nederlandse Voedsel- en Warenautoriteit, Wageningen) for sharing key taxonomic literature and Wilfrida Decraemer (Ghent University, Belgium) for sharing her passion on nemas, both, terrestrial and aquatic. JC thanks the Vicerrectoría de Investigación, Universidad de Costa Rica for the financial support over many years to maintain marine biodiversity studies. We also thank Ivonne Arroyo (Programa de Investigación Red Sismológica Nacional, Universidad de Costa Rica) for her help with the GMT for the map elaboration and Paul Hanson for his suggestions to the final version.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

No funding was reported.

Author contributions

ASM and JC conceived the review and searched for related data in literature and databases. ASM edited the map to plot reports. Both authors wrote the manuscript and made improvements to every version of it. Both authors read and approved the manuscript.

Author ORCIDs

Alcides Sánchez-Monge https://orcid.org/0000-0002-6884-0175

Jorge Cortés https://orcid.org/0000-0001-7004-8649

Data availability

The datasets analysed during the current study are available in the following URLs: OBIS (http://www.obis.org), GBIF (https://www.GBIF.org), Nemys (World Database of Nematodes http://nemys.ugent.be/) and WoRMS (World Register of Marine Species http://www.marinespecies.org/index.php).

References

Alfaro-Shigueto J, Van Waerebeek K, Reyes JC, Van Bressem M, Samaniego J, Félix F, Fraija-Fernández N (2022) Checklist of helminth parasites and epizoites in common dolphins from coastal Peru and Ecuador. Preprints, 2022100095. https://doi.org/10.20944/preprints202210.0095.v1

Ángeles-Hernández JC, Gómez-De Anda FR, Reyes-Rodríguez NE, Vega-Sánchez V, García-Reyna PB, Campos-Montiel RG, Calderón-Apodaca NL, Salgado-Miranda C, Zepeda-Velázquez AP (2020) Genera and species of the Anisakidae family and their geographical distribution. Animals 10(12): 1–23. https://doi.org/10.3390/ani10122374

Armenteros M, Ruiz-Abierno A, Fernández-Garcés R, Pérez-García JA, Díaz-Asencio L, Vincx M, Decraemer W (2009) Biodiversity patterns of free-living marine nematodes in a tropical bay: Cienfuegos, Caribbean Sea. Estuarine, Coastal and Shelf Science 85(2): 179–189. https://doi.org/10.1016/j.ecss.2009.08.002

Armenteros M, Rodríguez-García P, Pérez-García JA, Gracia A (2020) Diversity patterns of free-living nematode assemblages in seagrass beds from the Cuban archipelago (Caribbean Sea). Biodiversity Data Journal 8: e58848. https://doi.org/10.3897/BDJ.8.e58848

Avalos G (2019) Still searching the rich coast: Biodiversity of Costa Rica, numbers, processes, patterns, and challenges. In: Pullaiah T (Ed.) Global Biodiversity. Apple Academic Press, Oakville, 101–135. https://doi.org/10.1201/9780429433634-4

Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on Earth. Proceedings of the National Academy of Sciences of the United States of America 115(25): 6506–6511. https://doi.org/10.1073/pnas.1711842115

Baylis HA, Daubney R (1925) A revision of the lungworms of Cetacea. Parasitology 17(2): 201–216. https://doi.org/10.1017/S0031182000004595

Caruso T, Hogg ID, Nielsen UN, Bottos EM, Lee CK, Hopkins DW, Cary SC, Barrett JE, Green TGA, Storey BC, Wall DH, Adams BJ (2019) Nematodes in a polar desert reveal the relative role of biotic interactions in the coexistence of soil animals. Communications Biology 2(1): е63. https://doi.org/10.1038/s42003-018-0260-y

Chabaud AG (1962) Description de Crassicauda anthonyi n.sp, nématode parasite rénal de Mesoplodon mirus True. Bulletin du Muséum National d’Histoire Naturelle 34(5): 397–403.

Choc L, Arguedas Cortés D, Dolz G, Jiménez-Rocha AE (2018) Presencia de parásitos (Nematoda: Anisakidae) en peces de agua dulce destinados al consumo humano en Costa Rica. Ciencias Veterinarias (Heredia) 36(3): е47. https://doi.org/10.15359/rcv.36-3.34

Cipriani P, Palomba M, Giulietti L, Marcer F, Mazzariol S, Santoro M, Alburqueque RA, Covelo P, López A, Santos MB, Pierce GJ, Brownlow A, Davison NJ, McGovern B, Frantzis A, Alexiadou P, Højgaard DP, Mikkelsen B, Paoletti M, Nascetti G, Levsen A, Mattiucci S (2022) Distribution and genetic diversity of Anisakis spp. in cetaceans from the Northeast Atlantic Ocean and the Mediterranean Sea. Scientific Reports 12(1): е13664. https://doi.org/10.1038/s41598-022-17710-1

Cobb NA (1920) One Hundred New Nemas (Type Species of 100 New Genera). Contributions to a Science of Nematology IX. Waverly Press, Baltimore, 217–343. https://doi.org/10.5962/bhl.title.20608

Colón-Llavina MM, Mignucci-Giannoni AA, Mattiucci S, Paoletti M, Nascetti G, Williams Jr EH (2009) Additional records of metazoan parasites from Caribbean marine mammals, including genetically identified anisakid nematodes. Parasitology Research 105(5): е1239. https://doi.org/10.1007/s00436-009-1544-4

Cortés J (2016a) The Pacific coastal and marine ecosystems. In: Kappelle M (Ed.) Costa Rican Ecosystems. University of Chicago Press, Chicago, 97–138. https://doi.org/10.7208/chicago/9780226121642.003.0005

Cortés J (2016b) The Caribbean coastal and marine ecosystems. In: Kappelle M (Ed.) Costa Rican Ecosystems. University of Chicago Press, Chicago, 591–617. https://doi.org/10.7208/chicago/9780226121642.003.0017

Cortés J, Wehrtmann IS (2009) Diversity of marine habitats of the Caribbean and Pacific of Costa Rica. In: Wehrtmann IS, Cortés J (Eds) Marine Biodiversity of Costa Rica, Central America. Springer, Dordrecht, 1–45. https://doi.org/10.1007/978-1-4020-8278-8_1

Cunha BP, Brito S, Fonseca G (2013) Zygonemella: The forgotten genus of the family Xyalidae (Nematoda). Zootaxa 3669(2): 179–183. https://doi.org/10.11646/Zootaxa.3669.2.10

Daday J (1899) Uj-guineai szabadon elö nematodok. Mathematikai És Természettudományi Értesitö 17: 557–572.

de la Cruz E, Vargas JA (1986) Estudio preliminar de la meiofauna de la playa fangosa de Punta Morales, Golfo de Nicoya, Costa Rica. Brenesia 25/26: 89–97.

de la Cruz E, Vargas JA (1987) Abundancia y distribución vertical de la meiofauna en la playa fangosa de Punta Morales, Golfo de Nicoya, Costa Rica. Revista de Biología Tropical 35: 363–367.

Dexter DM (1974) Sandy-beach fauna of the Pacific and Atlantic coasts of Costa Rica and. Colombia. Revista de Biología Tropical 22: 51–66.

Dittmann S, Vargas JA (2001) Tropical tidal flat benthos compared between Australia and Central America. Ecological Studies: 275–293. https://doi.org/10.1007/978-3-642-56557-1_14

Dujardin F (1845) Histoire Naturelle des Helminthes ou vers intestinaux. Libraire Encyclopédique de Roret, Paris, XVI, 654 pp. https://doi.org/10.5962/bhl.title.10123

Febronio AMB, Boos GS, Batista RLG, Amorim DB, Guimarães JP, Bianchi MV, Mariani DB, Koproski L, Mari C, Parente Jociery EV, Sonne L, Werneck MR, Marques SMT, Driemeier D, Kolesnikovas CKM, Groch KR, Sobotyk C, Verocai GG, Groch KR, Díaz-Delgado J (2021) Crassicaudiasis in three geographically and chronologically distant Cuvier’s beaked whales (Ziphius cavirostris) stranded off Brazil. International Journal for Parasitology. Parasites and Wildlife 16: 262–269. https://doi.org/10.1016/j.ijppaw.2021.10.010

Filipjev IN (1934) The classification of the free-living nematodes and their relation to the parasitic nematodes. Smithsonian Miscellaneous Collections 89(6): 1–63.

Fonseca VG, Sinniger F, Gaspar JM, Quince C, Creer S, Power DM, Peck LS, Clark MS (2017) Revealing higher than expected meiofaunal diversity in Antarctic sediments: A metabarcoding approach. Scientific Reports 7(1): 1–11. https://doi.org/10.1038/s41598-017-06687-x

Gagarin VG, Thanh NV (2015) Subsphaerolaimus minor sp. n. and Micromicron cephalatum Cobb, 1920 (Nematoda) from the Yen River Estuary of Vietnam. Zootaxa 3994(3): 396–410. https://doi.org/10.11646/zootaxa.3994.3.4

Geetanjali , Malhotra SK, Malhotra A, Ansari Z, Chatterji A (2002) Role of nematodes as bioindicators in marine and freshwater habitats. Current Science 82: 505–507. https://drs.nio.res.in/drs/bitstream/handle/2264/281/Curr_Sci_82_505.pdf?sequence=1&isAllowed=y

Gracia AA, Levin LA, Zea S (2020) Meio-epifaunal wood colonization in the vicinity of methane seeps. Marine Ecology 41(1): 1–14. https://doi.org/10.1111/maec.12573

Guzmán HM, Obando VL, Cortés J (1987) Meiofauna associated with a Pacific coral reef in Costa Rica. Coral Reefs 6: 107–112. https://doi.org/10.1007/BF00301379

Hoberg EP, Brooks DR, Molina-Urena H, Erbe E (1998) 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. The Journal of Parasitology 84(3): е571. https://doi.org/10.2307/3284726

Holovachov O (2012) Swedish Plectida (Nematoda). Part 2. The genus Antomicron Cobb, 1920. Zootaxa 3380(1): 1–39. https://doi.org/10.11646/zootaxa.3380.1.3

Huang Y, Gao Q (2016) Two new species of Chromadoridae (Chromadorida: Nematoda) from the East China Sea. Zootaxa 4144(1): 89–100. https://doi.org/10.11646/zootaxa.4144.1.4

John S, Morris S, Geethambika SB, Muraleedharan M, Thomas JA, Savitha G, Joseph P (2023) Halocercus lagenorhynchi infection in a stranded striped dolphin Stenella coeruleoalba (Meyen, 1833) on the Southwest Coastline of India. https://doi.org/10.21203/rs.3.rs-3132599/v1

Leiper RT, Atkinson EL (1914) Helminthes of the British Antarctic Expedition, 1910–1913. Proceedings of the Zoological Society 1914: 222–226.

Levin LA, Mendoza GF, Grupe BM, Gonzalez JP, Jellison B, Rouse G, Thurber AR, Waren A (2015) Biodiversity on the rocks: Macrofauna inhabiting authigenic carbonate at Costa Rica methane seeps. PLOS ONE 10: e0131080. https://doi.org/10.1371/journal.pone.0131080

Losi V, Ferrero TJ, Moreno M, Gaozza L, Rovere A, Firpo M, Marques JC, Albertelli G (2013) The use of nematodes in assessing ecological conditions in shallow waters surrounding a Mediterranean harbour facility. Estuarine, Coastal and Shelf Science 130: 209–221. https://doi.org/10.1016/j.ecss.2013.02.017

Marcer F, Tosi F, Franzo G, Vetri A, Ravagnan S, Santoro M, Marchiori E (2020) Updates on Ecology and Life Cycle of Sulcascaris sulcata (Nematoda: Anisakidae) in Mediterranean Grounds: Molecular Identification of Larvae Infecting Edible Scallops. Frontiers in Veterinary Science 7: 1–64. https://doi.org/10.3389/fvets.2020.00064

Moravec F, Justine J (2021) Echinocephalus inserratus sp. n. (Nematoda: Gnathostomatidae) from the stingray Pastinachus ater (Dasyatidae) and new records of congeneric and some other nematode larvae from teleost fishes off New Caledonia. Folia Parasitologica 68: 1–14. https://doi.org/10.14411/fp.2021.014

Moura GS, Franzener G (2017) Biodiversity of nematodes biological indicators of soil quality in the agroecosystems. Arquivos do Instituto Biológico 84(0): 1–8. https://doi.org/10.1590/1808-1657000142015

Müller MI, Adriano EA, Oliveira MSB, Corrêa LL (2022) Integrative taxonomy suggests that South American freshwater nematodes Echinocephalus and their host stingrays co-originated in late Oligocene to early Miocene. Journal of Helminthology 96: e68. https://doi.org/10.1017/S0022149X22000554

Muthumbi A, Verschelde D, Vincx M (1995) New desmodoridae (Nematoda : Desmodoroidea): three new species from Ceriops mangrove sediments (Kenya) and one related new species from the North Sea. Cahiers de Biologie Marine 36: 181–195.

Neira C, Ingels J, Mendoza G, Hernandez-Lopez E, Levin LA (2018) Distribution of meiofauna in bathyal sediments influenced by the oxygen minimum zone off Costa Rica. Frontiers in Marine Science 5: 1–17. https://doi.org/10.3389/fmars.2018.00448

Neres PF, da Fonseca-Gnevois VG, Torres RA, da Fonseca-Cavalcanti M, de Castro FJV, Da Silva NRR, Rieger TT, Decraemer W (2010) Morphological and molecular taxonomy of a new Daptonema (Nematoda, Xyalidae) with comments on the systematics of some related taxa. Zoological Journal of the Linnean Society 158(1): 1–15. https://doi.org/10.1111/j.1096-3642.2009.00528.x

Oliveira JB, Morales JA, González-Barrientos RC, Hernández-Gamboa J, Hernández-Mora G (2011) Parasites of cetaceans stranded on the Pacific coast of Costa Rica. Veterinary Parasitology 182(2–4): 319–328. https://doi.org/10.1016/j.vetpar.2011.05.014

Pape E, Nara Bezerra T, Vanneste H, Heeschen K, Moodley L, Leroux F, van Breugel P, Vanreusel A (2011) Community structure and feeding preference of nematodes associated with methane seepage at the Darwin mud volcano (Gulf of Cádiz). Marine Ecology Progress Series 438: 71–83. https://doi.org/10.3354/meps09278

Patiño JA, Olivera MJ (2019) Anisakiasis gastro-alérgica, primera descripción de un caso en Colombia y revisión bibliográfica. Biomédica 39(2): 241–246. https://doi.org/10.7705/biomedica.v39i2.3936

Ridall A, Ingels J (2021) Suitability of Free-Living Marine Nematodes as Bioindicators: Status and Future Considerations. Frontiers in Marine Science 8: 1–16. https://doi.org/10.3389/fmars.2021.685327

Saad CB, Suthar J, Theisen S, Palm HW, Gargouri L (2022) Echinocephalus caniculus n. sp. (Nematoda: Gnathostomatidae Railliet, 1895) from the lesser spotted dogfish Scyliorhinus canicula (L.) (Elasmobranchii: Scyliorhinidae Gill, 1862) off Tunisia, with a key to species of the genus Echinocephalus. Systematic Parasitology 99: 299–307. https://doi.org/10.1007/s11230-022-10027-7

Sahling H, Masson DG, Ranero CR, Hühnerbach V, Weinrebe W, Klaucke I, Bürk D, Brückmann W, Suess E (2008) Fluid seepage at the continental margin offshore Costa Rica and southern Nicaragua. Geochemistry, Geophysics, Geosystems 9(5): е2008GC001978. https://doi.org/10.1029/2008GC001978

Santoro M, Marchiori E, Iaccarino D, Uberti B, Cassini R, Di Nocera F, Cerrone A, Galiero G, Marcer F (2019) Epidemiology of Sulcascaris sulcata (Nematoda: Anisakidae) ulcerous gastritis in the Mediterranean loggerhead sea turtle (Caretta caretta). Parasitology Research 118(5): 1457–1463. https://doi.org/10.1007/s00436-019-06283-0

Savin MC, Wolf DC, Davis KJ, Gbur EE, Thoma GJ (2015) Nematodes as Bioindicators of Ecosystem Recovery During Phytoremediation of Crude Oil Contaminated Soil. International Journal of Phytoremediation 17(2): 182–190. https://doi.org/10.1080/15226514.2013.876964

Semprucci F (2013) Marine Nematodes from the Shallow Subtidal Coast of the Adriatic Sea: Species List and Distribution. International Journal of Biodiversity 2013: 1–9. https://doi.org/10.1155/2013/187659

Semprucci F, Balsamo M (2012) Key role of free-living nematodes in the marine ecosystem. In: Boari F, Chung JA (Eds) Nematodes: Morphology, Functions and Management Strategies. Nova Science Publishers, Hauppauge, New York, 109–134.

Sibaja-Cordero JA, Troncoso JS, Cortés J, Moreira J, Vargas JA, Benavides-Varela C (2016) Biodiversity and density of subtidal benthos of an oceanic tropical island (a comparison within the Pacific Ocean). Journal of Sea Research 115: 47–58. https://doi.org/10.1016/j.seares.2016.07.004

Sibaja-Cordero JA, Camacho-García YE, Azofeifa-Solano JC, Alvado-Arranz B (2019) Ecological patterns of macrofauna in sandy beaches of Costa Rica: A Pacific-Caribbean comparison. Estuarine, Coastal and Shelf Science 223: 94–104. https://doi.org/10.1016/j.ecss.2019.04.032

Solano-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

Timm RW (1954) A survey of the marine nematodes of Chesapeake Bay, Maryland. Dissertation. The Catholic University of America. Solomons Island, Maryland.

Vargas JA (1988) A survey of the meiofauna of an Eastern Tropical Pacific intertidal mud flat. Revista de Biología Tropical 36(2B): 541–544. https://doi.org/10.15517/rbt.v36i2B.23894

Vargas JA (2016) The Gulf of Nicoya: estuarine ecosystem. In: Kappelle M (Ed.) Costa Rican Ecosystems. University of Chicago Press, Chicago, 139–161.

Venekey V, Fonseca-Genevois VG, Santos PJP (2010) Biodiversity of free-living marine nematodes on the coast of Brazil: A review. Zootaxa 2568(1): 1–39. https://doi.org/10.11646/zootaxa.2568.1.2

Venekey V, Gheller PF, Maria TF, Brustolin MC, Kandratavicius N, Vieira DC, Brito S, Souza GS, Fonseca G (2014) The state of the art of Xyalidae (Nematoda, Monhysterida) with reference to the Brazilian records. Marine Biodiversity 44(3): 367–390. https://doi.org/10.1007/s12526-014-0226-3

Venekey V, Gheller PF, Kandratavicius N, Cunha BP, Vilas-Boas AC, Fonseca G, Maria TF (2019) The state of the art of Chromadoridae (Nematoda, Chromadorida): A historical review, diagnoses and comments about valid and dubious genera and a list of valid species. Zootaxa 4578(1): 1–67. https://doi.org/10.11646/zootaxa.4578.1.1

Verschelde D, Nicholas W, Vincx M (2006) A review of the genera Croconema Cobb, 1920 and Pseudochromadora Daday, 1899 (Nematoda, Desmodoroidea): New species from the Coasts of Kenya and Australia. Hydrobiologia 571(1): 17–40. https://doi.org/10.1007/s10750-006-0194-0

Wang C, Huang Y (2016) Pseudolella major sp. Nov. (Axonolaimidae, Nematoda) from the intertidal zone of the East China Sea. Chinese Journal of Oceanology and Limnology 34(2): 295–300. https://doi.org/10.1007/s00343-015-4395-0

Wehrtmann IS, Cortés J, Echeverría-Sáenz S (2009) Marine Biodiversity of Costa Rica: Perspectives and Conclusions. Marine Biodiversity of Costa Rica, Central America: 521–533. https://doi.org/10.1007/978-1-4020-8278-8_49

Wessel P, Smith WHF, Scharroo R, Luis J, Wobbe F (2013) Generic Mapping Tools: Improved Version Released. Eos 94(45): 409–410. https://doi.org/10.1002/2013EO450001

Zhang ZQ (2013) Animal biodiversity: An update of classification and diversity in 2013. Zootaxa 3703(1): 5–11. https://doi.org/10.11646/zootaxa.3703.1.3

﻿Abstract

Key words

﻿Introduction

﻿Methods

﻿Results

﻿Discussion

﻿Free-living taxa

﻿Antomicron pellucidum Cobb, 1920

﻿Hypodontolaimus punctulatus (Cobb, 1920) Filipjev 1934

﻿Pseudochromadora quadripapillata Daday, 1899

﻿Pseudolella cephalata Cobb, 1920

﻿Zygonemella striata Cobb, 1920

﻿Parasitic taxa

﻿Anisakis spp. Dujardin, 1845

﻿Crassicauda anthonyi Chabaud, 1962

﻿Echinocephalus janzeni Hoberg, Brooks, Molina-Ureña & Erbe, 1998

﻿Halocercus lagenorhynchi Baylis & Daubney, 1925 and Halocercus sp

﻿Abundance and unidentified taxa

﻿Conclusion

﻿Acknowledgements

﻿Additional information