1. Introduction

Diatoms are unicellular microscopic algae that belong to the class Bacillariophyta. With over 100,000 known species, are a major group of algae, specifically a type of phytoplankton, characterized by their unique silica cell walls, known as frustules [1, 2]. These microscopic, photosynthetic organisms play a crucial role in aquatic ecosystems, contributing significantly to the primary production of oxygen and forming the base of the food chain in marine and freshwater environments [1, 2]. These phytoplankton are ubiquitous in aquatic environments, whether marine or freshwater, and serve as significant biomarkers [2–4]. Some species exhibit pharmaceutical properties due to their diverse components, which have been reported to control bacteria and parasites. Additionally, they are valuable as a source of essential fatty acids like Eicosapentaenoic Acid (EPA) and Docosahexaenoic Acid (DHA), as well as various bioactive molecules, making them relevant to the nutraceutical industry [1, 5–9].

Marine fish parasites encompass a wide array of species, comprising both protozoan and metazoan parasites [10, 11]. These parasites present significant economic burdens, with costs related to parasitic infections in finfish aquaculture, reaching up to 10% of the projected fish yield worldwide [12], but also, they represent a threat to both marine and freshwater fish, exacerbating challenges such as habitat loss, pollution, invasive species, and overfishing. The emergence of these parasites has been further fueled by global warming [5, 13–15]. In South America, and specifically Colombia, various parasites have been documented to impact human health, with clinical cases, as a consequence of global tourism and consuming exotic foods. Individuals can inadvertently become infected by sampling ethnic dishes, traditional cuisine, or unique culinary preparations [16–19].

The association study between parasites and diatoms has shown promise as an innovative approach to controlling parasitic infections in fish, particularly in aquaculture, where resistance to traditional treatments is a growing concern [5, 8, 20–23]. Despite extensive research, there is a significant knowledge gap regarding these associations in the tropical ecosystems of Colombia’s Pacific coast [1]. This region possessses significantive species richness, especially within its aquatic ecosystems, where diatoms from the Bacillariophyta order thrive.

Colombia is a unique tropical country in South America, having coasts on both the tropical Pacific Ocean and the Caribbean Sea with a total shoreline of nearly 3,000 km, is recognized by its rich biodiversity within its aquatic ecosystems, including a variety of microorganisms such as algae, particularly diatoms from the Bacillariophyta order [2–4, 24].

In order to contribute to the discussion regarding how fish manage endoparasites disease, and considering that there is minimal study on this field [25], we hypothesize that diatoms are important elements for fish diet and plays a significant role, probably to treat or minimize the endoparasite charges. The main objective of this research was to investigate the association between diatoms genus and parasites within the gastrointestinal compartments (GICs) of commercial fish in fisheries of the marine pacific coast of Colombia (Buenaventura). This aimed to better understand the zoo pharmacognosy in commercial fish, the self-medication behavior of fishes in this region, as well as to analyze the structure and vulnerability of the host-parasite networks field using diatoms as biomarkers [26, 27].

2. Materials and methods

2.2 Description of the study area

We sampled in the Piñal Bridge in Buenaventura in the Department of Valle del Cauca, Colombia, following these parameters: first, it is the one of the main fisheries centers that distribute and merchandise the product to inhabitants, and supplies restaurants and markets in Buenaventura; secondly, it is a significant species richness center, with cultural practices and traditional sanitary regulation. Thirdly, the Buenaventura harbor is one of the leading international markets in Colombia [31, 32]. Buenaventura is in the estuary of Buenaventura Bay, at the Tropical Eastern Pacific (3° 52′ 59,7” N to 77° 3´ 20”). The estuary spans approximately 70 km² and has a 16-km-long and 5-m-deep central canal field (Fig 1) [33].

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Fig 1. Samples were collected from Puente el Piñal, and San Antonio.

Ranging in elevation from 0 to 7 m.a.s.l. (A, B) Platonera in Puente el Piñal, preparing and selling market fish products; (C) fishing boat arriving after fishing at Puente el Piñal; (D) fishermen, eviscerating fish; (E) pelicans in the Puente el Piñal; (F), cat eating gastrointestinal compartments of fish. Created in BioRender. Benavides, J. (2024) BioRender.com/e10g125.

https://doi.org/10.1371/journal.pone.0312015.g001

3. Results

From 104 gastrointestinal compartments acquired from marine fish, this study identified different species of diatoms and parasites. 14 genus of diatoms were found: Actinoptychus spp., Aulacoseira spp., Biddulphia spp., Botrydiopsis spp., Cyclotella spp., Cymbella spp., Coscinodiscus spp., Gyrosigma spp., Melosira spp., Navicula spp., Paralia spp., Skeletonema spp., Torodinium spp., and Unruhdinium spp. Coscinodiscus emerged as the most prevalent diatom, appearing in 58/104 analyzed compartments. This diatom was present in eight species, and it was most frequently identified in Mugil curema in all sampling (Fig 2, Table 1, S1 Fig and S1 Table). Cyclotella spp. also had a high prevalence, 28/104 (26.9%) in Anisotremus spp. and in the last sampling. In the case of Paralia spp., it was found in 26/104, 25%; Centropomus unionensis and Mugil curema were identified in all samples. Gyrosigma spp. at 11/104, 10.6%; was present in three species Mugil curema, Oreochromis niloticus, Parapsettus panamensis in two sampling times. Navicula spp. at 11/104, 10.6%, (Fig 2, Table 1, S1 Fig and S1 Table.)

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Fig 2. Species of diatoms present in marine fish intestine from the pacific of Colombia.

A) Actinoptychus spp.; B) Aulacoseira spp.; C) Biddulphia spp; D) Botrydiopsis spp; E) Coscinodiscus spp.; F) Cyclotella spp; G) Cymbella spp.; H, I) Gyrosigma spp.; J, K) Melosira spp.; L) Navicula spp.; M) Paralia spp.; N) Skeletonema spp.; O) Torodinium spp.; P) Unruhdinium spp. Created in BioRender. Created in BioRender. Benavides, J. (2024) BioRender.com/z47t234.

https://doi.org/10.1371/journal.pone.0312015.g002

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Table 1. Diatoms found in the gastrointestinal compartments of fish population in Buenaventura port of Colombia.

https://doi.org/10.1371/journal.pone.0312015.t001

Endoparasites associated with diatoms, specifically Anisakis spp. and Contracaecum spp., were detected in the intestines of Mugil curema (commonly known as Lisa) at a prevalence ranging from 3.9% to 12.5%. Mugil curema, Anisakis spp. and Contracaecum spp. exhibited associations with various diatom species, including Botrydiopsis spp., Coscinodiscus spp., Gyrosigma spp., Navicula spp., Paralia spp., and Unruhdinium spp. Notably, during the third sampling, the species of diatoms decreased to a single species, Coscinodiscus spp., at a prevalence of 3.9%, while Anisakis spp. and Contracaecum spp. persisted (Figs 3 and 4 and Table 2, S2 Fig).

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Fig 3.

Parasites found from various Pacific fish species: Anisakidae eggs (A); Contracaecum spp. (B), Anisakis spp. (C), Cyst of a cilliated from Cynoscion albus (D), Eimeria spp. (E, F), Macrostomorpha spp. (G), Metagonimus spp. (H), Paragonimus spp. (I). Created in BioRender. Benavides, J. (2024) BioRender.com/u24c141.

https://doi.org/10.1371/journal.pone.0312015.g003

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Fig 4.

Helminths from Mugil curema, Thunnus alalunga and Notarious armbrusteri. Nematodes located on cerose gastric (A), Anisakidae family teeth observed 40X t: (B) Confocal, lateral view (C), Anisakis simplex sensu lato. anterior region (D), posterior or tail observed by confocal microscopy (E), SEM tail (F), Acanthocephalus spp. (G), Acanthocephalus spp. head with hooks (H), Acanthocephalus spp. tail (I). Created in BioRender. Benavides, J. (2024) BioRender.com/h00l150.

https://doi.org/10.1371/journal.pone.0312015.g004

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Table 2. Endoparasites found in the gastrointestinal compartments of fish population in Buenaventura port of Colombia.

https://doi.org/10.1371/journal.pone.0312015.t002

Eimeria spp. and Methagonimus spp. were found in Centropomus unionensis at a prevalence of 12.5%, associated with Biddulphia spp. during the first sampling on March 19, 2023 (Table 2). However, this trend was not prominent during the subsequent sampling in October, where Coscinodiscus spp., Navicula spp., and Paralia spp. were present, and parasites were notably absent (Table 2, Figs 3, S2).

Interestingly, Menticirrhus panamensis, which tested negative for diatoms, was found parasitizing Acanthocephalus spp., whereas Parapsettus panamensis, Bagre panamensis, and Lutjanus guttatus tested negative for parasites, and exhibited associations with various diatoms, including Coscinodiscus spp., Cymbella spp., Gyrosigma spp., Botrydiopsis spp., Melosira spp., and Torodinium spp. (Table 2, Figs 4 and S2).

During the second sampling on October 07, 2023, samples from Bagre pinnimaculatus revealed infection with Anisakis eggs., along with the occurrence of ameboid cysts in association with Aulacoseira spp., Botrydiopsis spp., Coscinodiscus spp., and Cyclotella spp., at a prevalence of 20.7%. Cynoscion albus tested positive for parasites such as Anisakis spp. and Balantidium spp., and exhibited association with Coscinodiscus spp. Interestingly, Mugil curema showed the highest susceptibility to parasites across all samplings, with Anisakis spp., Contracaecum spp., and ameboid cysts (Table 2). Additionally, Cynoscion albus exhibited positivity for both Anisakis spp. and cilliated cyst., coinciding with the presence of Coscinodiscus spp. In contrast, Cynoscion squamipinnis and Eugerres periche were positive for Coscinodiscus spp. and Navicula spp., respectively. These showed negativity for parasites in the first and second samplings; however, Eugerres periche was present in diatoms such as Aulacoseira spp., Coscinodiscus spp, and Paralia spp. associated with Paragonimus spp, during the third sampling (Table 2, Figs 3 and 4 and S2).

Notarius armbrusteri, (Ñato sea-catfish) tested negative for parasites in October 2023, during the second samplings. However, it exhibited positivity for diatoms and parasites during the third sampling in March 2024, as it was Infected with Acanthocephalus spp., Eimeria spp., and ameboid cysts (Table 2, Figs 3 and 4 and S2).

Thunnus alalunga (longfin tuna), collected during the third sampling, exhibited a high prevalence of Anisakis spp. and Contracaecum spp. without any association with diatoms. Conversely, Caranx sexfasciatus, Caranx vinctus, Caranx caninus, Lutjanus colorado, Nematistius pectoralis, Peprilus snyderi, and Strongylura fluviatilis tested negative for diatoms and parasites across all samplings (Table 2, Figs 4, S2).

The association level between parasites and diatoms in each sampling was >1, with a 45.83% prevalence of parasites associated to diatoms (11 digestive compartments were positive for both), on March 19^th, 2023. Only one (4.17%) gastrointestinal compartment was positive for parasites and negative for diatoms. Diatoms were present without parasites (16.67%). Conversely, digestive compartments without diatoms and parasites were 8 (33.3%). That means a factor association odds ratio with a value of 22.0, superior to >1. The presence of diatoms in the gastrointestinal compartments of fish is associated with a higher likelihood of parasitic infection. This is evident from the higher odds ratio (OR = 2.8) for compartments with diatoms, indicating that these compartments are significantly more likely to be associated to parasites compared to compartments without diatoms. Conversely, compartments without diatoms have a much lower likelihood of parasitic association (OR = 0.1), suggesting a protective effect or simply a lower association between the absence of diatoms and the presence of parasites. This analysis supports the conclusion that diatoms are correlated with an increased risk of parasitic infections in the gastrointestinal compartments of fish. (Fig 5, Table 3, S2 Fig).

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Fig 5. Contingency table.

Parasites ‐ Diatoms association in Gastrointestinal Compartments (CGIs) in fish from harbor of Buenaventura–Colombia. First sampling 19 march 2023 (A), Second sampling 07 october 2023 (B), Third sampling 09 march 2024 (C), Total sampling (D). Significant differences using Fisher test P ≤0,0035, **. P≤0.0001****.

https://doi.org/10.1371/journal.pone.0312015.g005

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Table 3. Measures of association, retrospective study cohort with percentage of grand total, relative risk and odds ratio.

https://doi.org/10.1371/journal.pone.0312015.t003

On October 7th, 2023, second sampling, the association between parasites and diatoms had a prevalence of 41.38%., in 12 compartments. No digestive compartments examined lacked both parasites and diatoms. Conversely, 24.14% (7) of the compartments harbored diatoms without parasites. The negative digestive compartments for diatoms and parasites were 34.48% (10). That means a factor association (Odds ratio) with a value of 1.7. The presence of diatoms in the gastrointestinal compartments of fish is associated with a higher likelihood of parasitic infection. However, the odds ratio of 1.7 suggests a moderate association compared to the first table, where the OR was 2.8. In contrast, compartments without diatoms showed no cases of parasitic infection (OR = 0.0), indicating that the absence of diatoms is strongly associated with the absence of parasitic infection. Overall, this data suggests that the presence of diatoms is associated to parasitic infection. (Table 3). In the last sampling, on March 9th, 2024, we found an association between parasites and diatoms in 30 digestive compartments from the total sampling (51), with a prevalence of 58.82%. 7 gastrointestinal compartments were positive for parasites and negative for diatoms (13.73%). There were 7 (13.73%) with diatoms present but without parasites. Finally, 7 digestive compartments were negative for diatoms and parasites (13.73%). Significant differences with high percentage of compartments with diatoms are positive for parasites compared to those without diatoms and a higher percentage of compartments without diatoms are negative for parasites. The presence of diatoms is strongly associated with a higher likelihood of parasitic infections using Fisher test P ≤0,0035, **. P≤0.0001****. (Fig 5, Table 3, S2 Fig).

4. Discussion

The presence of diatoms in the gastrointestinal compartments with strong associated with parasitic infection was demonstrated, as indicated by the high odds ratio of (OR:2,8; OR:1,7; OR:4,3; OR:2,94), this means that fishes with parasites are more likely to have compartments with diatoms compared to compartments without diatoms. In contrast, the compartments without diatoms have an equal likelihood of being infected or not infected by parasites (OR ≤ 1.0), suggesting no strong association between the absence of diatoms and parasitic infection. Overall, the data indicates a significant relationship between the presence of diatoms and parasitic infections in the fish’s gastrointestinal compartments and suggests that diatoms could be a contributing factor or an indicator of environments that is present when the parasitic infections are introduced.

The presence of diatoms in the gastrointestinal compartments of fish is associated with a higher likelihood of parasitic infection. An OR of 2.94 indicates that fish probably use diatoms when they become infected by parasites and parasites without parasitic infections has less probability to use diatoms, as indicated by the OR of 0.32. This suggests that the absence of diatoms is correlated with a reduced risk of parasitic infection (Fig 5). This data is associated to previous studies reporting the use of diatoms to control parasitic diseases in fish and reduce the use chemical treatments [5, 23]. Diatoms could play a role in facilitating or indicating environments where parasitic infections are more likely to occur and that the zoopharmacognosy might be a common phenomenoa in the ocean fish [25].

Nematodes of the Anisakidae family (genera Anisakis, Pseudoterranova and Contracaecum) are common fish parasites. Among these, Anisakis simplex, sensu stricto (s.s), and Anisakis pegreffii have been reported as causative agents infecting humans [51, 52]. This study identified various morphotypes of Anisakis simplex sensu lato, a larvae type I with an elongated ventricle and a mucron at the caudal end in Lisa (Mugil curema). This is consistent with previous reports of nematode larvae isolated in Cartagena (Colombia) from Mugil incilis, identified as Contracaecum spp., with a prevalence of 60.49% [37].

In Tumaco, Colombia, there have been reports of a type II Pseudoterranova larva, with a prevalence of 94%, identified as A. physeteris and Pseudoterranova decipiens [31]. Contracaecum sp. infection in Hoplias malabaricus (moncholo) were documented in rivers and marshes of Colombia, with a high intensity of 77.82% and a prevalence of 100%. Although the morphological and molecular diagnosis of parasites and diatoms was not incorporate [53].

Anisakidae eggs were found under coprology, ascarid nematodes divided into two distinct clades (families), the Anisakidae (which includes species of Anisakis, Pseudoterranova and Contracaecum) and the Raphidascarididae (which includes species of Hysterothylacium and Raphidascaris) [54]. The egg size of A. simplex was 41.3 μm ‐ 45.6 μm; Pseudoterranova decipiens: 45.2μm ‐ 41 μm; Contracaecum osculatum: 72.6 μm -80.9 μm [55]. Other studies had reported egg measures for Contracaecum multipapillatum s.l. of 53 × 43 μm, although after the larvae had developed inside, egg size increased to 66 × 55 μm [56], the egg of Anisakis pegreffii measure 40–60 μm in perimeter of egg oviposited [57] However, the size of the embryonated eggs can vary from one genus to another, so the morphological characteristics may present variations that make identification difficult [58]. This research found various Anisakidae eggs of varying sizes. These are compatible with Contracaecum spp. and Anisakis spp., considering the morphological description of adult L4 stages. Future molecular studies are required to identify the parasites at the level of specie.

Ciliated protozoa type Balantidium spp., primarily infects terrestrial animals, particularly pigs, and its presence in marine environments is not well-documented [34, 50]; However, there are other species within the Balantidium genus, such as Balantidium polyvacuolum and Balantidium fulinensis, which have been identified in fish [59, 60]. For example, Balantidium polyvacuolum has been observed in the hindgut of the fish species Xenocypris davidi, where it plays a role in energy metabolism by digesting plant material within the fish’s intestines [59, 60]. Here, we found a prevalence of ciliated type Balantidium spp. in fish gastrointestinal compartments of 6.7%, which is higher than previous reports in domestic and wild animals (0.89% to 4.17%) [34, 50]. Interestingly, 13 species of Balantidium spp., have been reported in fish, 4 of them in marine fish [61]. In South America, sea lions have been reported in Otaria flavescens with a prevalence of 13.8%, which represents an important biological component considering surveys on anthropozoonotic pathogens circulating in wild free-living sea lions and their possible impact on public health issues and marine wildlife [62]. The B. ctenopharyngodoni parasite was increasingly associated with bacterial diversity, a higher relative abundance of Clostridium, and a lower abundance of Enterobacteriaceae in grass carp, suggesting that the presence of Balantidium ctenopharyngodoni may improve intestinal health through changes in microbiota and metabolites [63]. Balantidium piscicola has been discovered parasitizing caranha Piaractus brachypomus and mandi catfish Synodontis clarias [64]. These findings suggest that while Balantidium coli may not commonly infect marine fish, other Balantidium species are adapted to aquatic environments and can be found in fish. This underscores the importance of accurately identifying the specific ciliate species involved when cysts are observed in marine fish using accurate molecular techniques.

Other parasites found in this study were three types of trematodes: Methagonimus spp. (with a prevalence of 7.7%), Paragonimus spp. (4.8%) and Macrostomorpha spp. (1%). Intestinal trematodes are taxonomically diverse and consist of more than 60 species worldwide. Macrosotomorpha spp., is a free-living flatworm, whose eggs are around 100 microns in diameter [65], with more than 100 marine species reported in fresh and brackish water. Species are contained in the genus Macrostomum, and some of them have worldwide distribution patterns [66]. They are an essential component of marine and freshwater ecosystems as top predators and secondary producers [67]. Among them, Metagonimus spp. is a source of human infection due to ingesting raw or improperly cooked fish. Its eggs are ovoid, pyriform, or elliptical with a size range of 21–35×12–21 μm [68, 69].

Paragonimus spp. constitutes a group of trematode parasites that infect humans throughout the world. Between 5 and 10% of Asia’s human population is infected. The areas with the highest possibility of infection are Asia, Central and South America, and Africa. An estimated 293 million people are at risk of infection [70]. These parasites have been reported in Colombia in Embera Indian communities located at the Colombian Pacific Coast and investigated in 1993–1998 [71]. Paragonimosis, is a lung disease characterized by symptoms such as coughing, haemoptysis, thoracic pain, and light dyspnea [71]. They are normally associated with the consume of undercooked freshwater crustaceans such as crab (Moreirocarcinus emarginatus) and primarily affect the lungs, but may ectopically migrate to other organs to produce a multisystemic clinical presentation [72]. In the present study Paragonimus spp. in fish are generally not considered common hosts; However, the polluted water in Buenaventura harbor could explain the unusual findings of these parasites, as contamination with fecal matter might contribute to their presence and Paragonimus as paratenic host [73–76].

In marine fishes, over 100 species of coccidians have been identified across 60 different fish families. These species are classified into five genera: Calyptospora and Crystallospora, each with one described species; Epieimeria, which includes four species; Eimeria, comprising 64 species; and Goussia, with 30 species [77].

The genus Eimeria consists of apicomplexan parasites primarily known for infecting terrestrial animals, especially birds and mammals, and causing coccidiosis. These parasites have a complex life cycle that includes both sexual and asexual reproduction phases, and they produce oocysts, which are excreted in the host’s feces. Eimeria is predominantly known for its impact on terrestrial animals, there are documented cases of various Eimeria species in fish, both freshwater and marine. Numerous species of Eimeria have indeed been identified in fish, including marine species. Some examples include: Eimeria adioryxi (reported in marine fish), Eimeria anguillae (found in eels), Eimeria dingleyi (found in marine fish), Eimeria dicentrarchi (documented in marine environments), Eimeria catalina and others. This diversity suggests that while Eimeria is more commonly associated with terrestrial hosts, it also has representatives in aquatic environments, including marine fish [77].

In the present study, coccidias type Eimerias spp. was identified in Notarius armbrusteri and Centropomus unionensis, at a prevalence of 10.6%. Multiple species of coccidians (Apicomplexa: Eimeriorina) from the Epieimeria, Calyptospora, and Crystallospora genera have been reported in marine teleosts; some of them have contribuited to high mortality [77, 78]. The presence of coccidia species in Centropomus unionensis, Notarious armbrusteri, in Colombia represents an important field of study that needs to be understood. In some of these species, parasites’ intestinal epithelial cells are temperature dependent, where their development is complete at 20°C in 9 to 10 d post-exposure (PE), but the metabolism is reduced at low temperatures, at 8 to 10°C 37 d (PE). Probably, the presence of these parasites is related to temperature averages (March 2023, 26,6^o; March 2024, 28°C). Future studies incorporating molecular techniques will help to elucidate accurately the genus and species of Eimerias in this ecosystems.

Acanthocephalus spp. had a prevalence of 8.7%, associated to Notarius armbrusteri (Spanish common name: ñato), and Menticirrhus panamensis (Spanish common name: botellona). Acanthocephalus spp. are endoparasites of the vertebrate intestine and have a heteroxenous life cycle with at least one arthropod intermediate host In their larval stages. They comprise 1200 species that measure a few millimeters in length; others are larger in size, such as Macracanthorhynchus hirudinaceus (7–15 cm). Some reported species in fish are Echinorhynchus truttae (0,7–2,2 mm) Salmo sp., with Gammarus sp. (Amphipoda) as intermediate host; Pomphorhynchus laevis (1–3.5 mm) (Gammarus sp.—Amphipoda—intermediate host); and Neoechinorhynchus rutili 0.5–1 in Cyprinus carpio as definitive host, and Ostracoda as intermediate host [79–82]. More than 50 Acanthocephalan species have been reported in the Pacific Oceans from freshwater and marine fish, amphibians, reptiles, birds, and mammals such as Rhadinorhynchus circumspinus n. sp., Rhadinorhynchus pacificus n. sp., Rhadinorhynchus multispinosus n. sp. [83].

In Mexico, Acanthocephalus amini n. sp. (Palaeacanthocephala: Echinorhynchidae) has been documented in the intestine of Cichlasoma urophthalmus (Günther) (Pisces: Cichlidae), collected in Río Champotón, a river in Campeche State, Mexico [84]. In Peru, there have been 71 described species in fish [85], whereas the literature documents 23 genera in Brazil, comprising 34 named species and 13 undetermined species of acanthocephalans, parasitizing Brazilian fishes [86]. Unfortunately, Costa Rica, Venezuela, Colombia, Chile, and Uruguay exhibited the lowest publication numbers, resulting in gaps in the distribution of acanthocephalans [87].

Regarding diatoms, we found 14 genus of diatoms in the intestinal compartments of 22 fish species. This is a normal value, but it is also lower than those expressed In previous reports in the Coast zones of Caribbean oceans, which have reported 337 taxon, 312 species [88]. In the Pacific Ocean coast of Colombia, San Andres de Tumaco, has been reported 101 genus and 262 species of diatoms [89]. This is the first report of diatoms in gastrointestinal compartments in various species of fish on the Pacific coast of Colombia. There are several studies covering phytoplankton species, especially regarding diatoms in the Buenaventura harbor. Usually, Buenaventura reports less species than Tumaco, which can be likely attributed to salinity, port harbor activity, and contamination levels [90]. These findings can explain why the species of diatoms in the present study was lower than in previous reports.

Diatoms are unicellular algae made of siliceous skeletons called frustules and are found in almost every aquatic environment, including fresh and marine waters [91]. Here, we found a strong association of parasites and diatoms, a value of 9.2, which is >1. (Table 3). Of 104 digestive compartments, 53 tested positives for diatoms and parasites, indicating a prevalence rate of 51%. Parasites were detected in 8 compartments, but in these Instances diatoms were absent, accounting for 7.7% of the cases. Conversely, 18 compartments tested positive for diatoms but negative for parasites, representing 17.3% of the total. Additionally, 25 compartments showed negative results for both diatoms and parasites, making up 24% of the samples.

Among the identified diatoms, Coscinodiscus spp. exhibited the highest prevalence, at 55.8%, indicating its dominance in the dietary diatom frequency within the gut content. These findings suggest that the genus Coscinodiscus significantly contributes to the composition of diatoms in the gut. Moreover, previous studies support our results by identifying four distinct species of Coscinodiscus and confirming their taxonomic classification based on SEM-based characters [7].

Some diatoms groups usually form colonies [92]. Free-living diatoms are covered by a siliceous skeleton (frustule) composed of SiO2 and H2O [92]. The structure of the frustule is the main feature used to identify species [93].

Marine diatoms have diverse bioactive molecules and have a great value for the nutraceutical industry, with compounds such as carotenoids, proteins, vitamins, essential amino acids, and omega-rich oils [8, 94]. Marine diatoms have shown promising potential as agents with anti-parasitic effects. These effects stem from various bioactive compounds produced by diatoms, which exhibit cytotoxic, anti-inflammatory, and immunomodulatory properties. Silica shells produce a mechanical disruption, provide structural support and possess abrasive properties. The rigid silica shells of diatoms can mechanically disrupt parasites, including protozoa and helminths, upon contact. This mechanical disruption can interfere with the attachment, feeding, and reproduction of parasites, thereby limiting their ability to establish infections [95].

Diatoms also produce a diverse array of bioactive compounds, including polyunsaturated fatty acids (PUFAs), sterols, alkaloids, and phenolic compounds, which exhibit anti-parasitic activity. For example, PUFAs such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) have been shown to disrupt the lipid metabolism of parasites, leading to membrane damage and impaired viability. Similarly, sterols present in diatoms can interfere with parasite cell membrane integrity, disrupting essential physiological processes [96].

Some diatom-derived compounds also possess immunomodulatory properties, which can enhance the host’s immune response against parasitic infections. For instance, polysaccharides isolated from certain diatom species have been shown to stimulate macrophage activity and cytokine production, thereby promoting the clearance of parasites by the host immune system. Furthermore, diatom-derived antioxidants can mitigate inflammation associated with parasitic infections, reducing tissue damage and facilitating the resolution of infection [97]. Additionally, some diatom species produce antimicrobial peptides (AMPs) as part of their defense mechanisms against microbial pathogens, which may also exhibit activity against parasitic organisms. These peptides can disrupt parasite cell membranes, interfere with essential metabolic pathways, or modulate host immune responses to combat parasitic infections. Research in this area is ongoing, with efforts focused on identifying and characterizing novel diatom-derived AMPs with potent anti-parasitic properties [98]. Diatomaceous earth has been found useful in the prevention of worm infestation in purebred pigeons [99]. Recent studies have supported its use as animal growth promoter, vaccine adjuvant in livestock, water purifier, mycotoxin binder, inert dust applications in stored-pest management, pesticide, animal feed additive, as a natural source of silicon in livestock, and as natural anthelmintic [100]. Fossil shell flour has the potential to supplement traditional crops in beef cattle rations in response to complex global challenges, since it Is cheap, readily available, and eco-friendly. However, it has not gained much attention from scientists, researchers, and farmers, and its use has not yet been adopted in most countries [101]. For the past two decades, fossil shell flour (FSF) has been used to naturally deworm animals, as 2% inclusion rate of FSF can be used with positive results in the destruction of internal parasites and worms [100].

In the present study, we did not capture fish for our research methodology. To collect the gastrointestinal tracts, we followed the cultural fish practice developed by artisanal fisheries of the municipality of Buenaventura (Pacific of Colombia). This cultural practice is characterized by species that inhabit coastal habitats such as mangroves and a limited number of pelagic species (tuna, sawfish, billfish, pipefish). These fisheries represent >21% of all fishery landings in the region. Normally, communities capture around 12 species exclusively by trammel net. Some of the captured species are herbivorous and therefore can only be caught with this process. Trammel nets also have the ability to capture a more diverse collection of species, although not necessarily those of commercial value [46]. The most common species caught using trammel nets in the artisanal fisheries of Buenaventura are Bagre pannamensis, Caulolatilus affinis, Cyncoscion albus, Notarius troscheli, Centropomus viridis, Bagre pinnimaculatus, Centropomus medius, Cynoscion reticulatus, Oligoplites altus, Centropomus sp. Some areas have reported up to 38 species of fish richness [46]. In the present research, we found 22 species of fish in the area, This implies that means a diverse array of present species within the community or ecosystem. This also indicates a healthy and varied environment, supporting a wide range of organisms.

The individuals within the community are distributed relatively evenly among the different species. This means that not only there are a significant amount of present species, but they are also well-balanced in terms of population sizes. Higher number of species often correlates with ecosystem stability. That mean that the ecosystem is resilient to disturbances due to the fact that it has a variety of species that can fulfill different roles and functions. This resilience can help the ecosystem withstand environmental changes and maintain its structure and function over time, which is often considered desirable for conservation and ecological sustainability.

Species of fish such as Cynoscion albus were positive for Anisakis spp. Balantidium spp. and diatoms such as Coscinodiscus spp. This species is distributed from Mexico to Ecuador and it is an important meat predator of second order; however, there is minimal information about its food habits [102]. This species live between 0–41 m. of depth [103]. The yellow croaker Cynoscion albus is a species that is distributed in the eastern Pacific from Baja California to Peru. It inhabits coastal waters, while juveniles enter shallow bays, estuaries, and river mouths. It is a bento-pelagic species. It feeds on shrimp, crabs, cephalopods and fish. It reaches sizes of up to 130 cm total length (TL) [104].

The lisa fish (Mugil Curema) is distributed in the Pacific ocean and inhabis water coasts at a depth rangin from 0 to 15 m. It is an omnivorous fish that consumes insects and algae; for this reason, they are an intermediate parasite host, contributing to the development of anisakis stages. In this species has been found the presence of abundant diatoms such as Gyrosigma, Navicula, Cymbella, Fragilaria, and Nitzschia [105]. This study found other additional diatoms such as Coscinodiscus, Botrydiopsis, Cyclotella, Melosira, Paralia, Skeletonema, and Unruhdinium. We confirmed the presence of Gyrosigma and Navicula. Other studies developed in Mexico reported 130 taxa dominating Nitzschia, Navicula, Amphora, and Cocconeis dominated [106]. To our knowledge, there are no previous reports of diatoms for these species associated to parasites. Therefore, we present the first study reporting the association of diatoms and parasites in gastrointestinal GI tracts.

Although species such as Tuna Thunnus alalunga did not report the presence of diatoms, fish that are primarily carnivorous or piscivorous (fish-eating) may not actively seek out diatoms as a significant portion of their diet. Instead, they may prefer other prey such as small fish, crustaceans, or insects. Interestingly, we found a significant parasitic charge of parasites that may be associated to the carnivorous and migratory habits as pelagic fish which is distributed in most tropical and temperate oceans [107, 108]. In Colombia, Thunnus alalunga has a wide distribution in the Colombian Caribbean (depth range: 0 to 600 m.). The diet of adults comprises a variety of fish, squid and crustaceans, while the diet of juveniles comprises mainly fish (anchovies, saury, sardines, juvenile hake) [109]. In the case of parasites, at least 14 valid species parasitizing T. alalunga have been reported as metazoan gill parasite species, isopods, copepods, nematodes, trematodes, and acanthocephalans (Echinorhynchus sp.) [110–112]. In Brazil, the presence of nematodes of the Anisakidae family is recorded: A. simplex in T. albacares, T. atlanticus and T. obesus, of A. physeteris in T. albacares, of Contracaecum sp. in T. atlanticus and T. obesus and Raphidascaris sp. in T. albacares and T. obesus. [113].

Lutjanus guttatus is a fish that we found harboring eggs of Metagonimus spp., in its gastrointestinal tracts, but was negative for diatoms, which is consistent with its carnivorous diet. It acts as final or intermediate host for several parasite species, throughout its life cycle [114].

Lutjanus guttatus ranges from the Gulf of California to northern Peru, encompassing the Galapagos Islands. Despite being subject to high levels of exploitation, it is categorized by the International Union for Conservation of Nature (IUCN) as being in the least concern category [115]. It is a benthopelagic species, present in marine and brackish habitats, associated with reefs and shallow waters. It is a carnivorous species, feeding on invertebrates and fish. As an adult it lives in coastal reefs, up to about 30 m. deep, and during its youth in estuaries and river mouths. It is a carnivorous species that feeds on fish and invertebrates [116]. It is an important resource for artisanal fishermen on the Mexican Pacific coast. In this fish there have been identified 32 taxa of metazoan parasites: four species of Digenea, four Monogenea, one Cestoda, two Acanthocephala, seven Nematoda (the nematodes Anisakis sp., Hysterothylacium sp. and Procamallanus sp.), one Hirudinea and nine Crustacea (six Copepoda and three Isopoda).

The outcomes of our study were impacted by climatic conditions, including global warming and phenomena like El Niño and La Niña. We concur with Villalba’s perspective that the dynamics of regional and local marine parasites could be influenced by these factors [114]. Changes in dietary preferences, such as increased consumption of raw fish and undercooked fish products, alongside evolving food habits and tastes, may elevate the likelihood of consumers being exposed to parasitic risks [61]. The risk can be mitigated by storing the fish at temperatures of −20°C or below for a total of seven days, or at −35°C or below for 15 hours. Additionally, ensuring proper preparation of dishes by thoroughly cooking the food at a temperature of 60°C for at least 10 minutes can help reduce the risk. However, these practices are not consistently followed in various communities [17, 117, 118].

The widespread occurrence and significant correlation of certain diatoms, including species like Cymbella spp., Aulacoseira spp., Coscinodiscus spp., Gyrosigma spp., Navicula spp., and Paralia spp., alongside the presence of parasites in various fish species, lead us to hypothesize that fish might acquire these diatoms as a form of nutraceutical treatment. This speculation arises from observations such as the application of P. tricornutum as an antiparasitic remedy for monogenean diseases in aquaculture [5, 8]. Coscinodiscus spp., along with other diatoms mentioned in this research, are promising subjects for further investigation, as previous studies have noted that Coscinodiscus is a prevalent component of the diet in the gut content studies [7].

Finally, this work consider that this research delved into the intricate relationship between diatoms and parasites in the gastrointestinal tracts of various fish species inhabiting the Buenaventura harbor along the Pacific Ocean. Through coprological techniques and microscopic examinations, we were able to identify a diverse array of diatoms and parasites, shedding light on their associations and prevalence rates. Notably, we observed zoonotic parasites like Anisakis spp., Acanthocephalus spp., and Contracaecum spp., alongside protozoa like Balantidium spp. Furthermore, we found several species of trematodes and coccidians, enriching our understanding of the parasite diversity within these fish populations. Our study also revealed insights into the dietary habits and ecological roles of these fish species, with some showing preferences for specific prey items and habitats. Additionally, the presence of certain diatom species in the gut content suggests a potential role in fish nutrition and health, which warrants further investigation.

Climate change and phenomena such as El Niño and La Niña were identified as factors influencing the dynamics of marine parasites, highlighting the need for ongoing monitoring and adaptation strategies [119]. Moreover, the risks associated with consuming raw or undercooked fish underscore the importance of proper food handling and preparation practices to mitigate parasitic infections. Overall, our findings hope to contribute to the broader understanding of marine species richness and ecosystem dynamics, emphasizing the interconnectedness of species within these complex environments. Future research incorporating morphological and molecular techniques could provide deeper insights into the interactions between diatoms, parasites, and their hosts, paving the way for enhanced strategies in parasite management and ecosystem conservation.

5. Conclusions

The GICs analysis of fish provided useful insights regarding its diatoms associated with parasites as a first report in Colombia. The genus Coscinodiscus spp. and Gyrosigma spp. dominated the diatom frequency during the study in different compartments associated with a diversity of fish using optical microscopy and SEM. Diatoms not only have nutritional profiles for fish but also, in some trophic levels, they are strongly associated with parasites, especially Mugil curema. This study also opens an avenue for research in searching for diatoms as preferential fish feed and their further screening for the purpose of identifying a commercially viable bioactive compounds for formulating potential value-added nutraceuticals and supplementary food for various dietary requirements of humans, livestock, and in aquaculture. Finally, future studies need to incorporate morphological and molecular diagnosis of parasites and diatoms.

Supporting information

Acknowledgments

We thank the community of Puente el Piñal–Buenaventura Colombia, particularly the “Platoneras,” the afro-descendant women who sell market fish products derived from the bycatch of this fishery and who play an integral role in the trawl fishery. We are also thankful to the research group investigating PARINEI. Special thanks to Andres Camacho, Yiseth Xiomara Hermoza, and Harby Leandro Pizo for their assistance in the collection and processing of samples. I extend my sincere thanks to the PLOS editors and Dr. Florence Jhun Almadin for their invaluable critical feedback.