First report of the parasite Perkinsus marinus (Myzozoa: Perkinsidae) in the marine snail Hexaplex nigritus (Gastropoda: Muricidae) from a coastal lagoon in the southeastern Gulf of California

Primeiro registro do parasita Perkinsus marinus (Myzozoa: Perkinsidae) no gastrópode marinho Hexaplex nigritus (Gastropoda: Muricidae) de uma lagoa costeira no sudeste do Golfo da Califórnia

Abstract

Perkinsus marinus is a myzozoa parasite native to the eastern coast of the United States, where it has been associated with significant mortalities in bivalve mollusk populations. Over the past two decades, its presence has been documented in various shellfish species—including oysters, clams, mussels, and scallops—along the Gulf of California (GC), leading to its classification as a widely distributed exotic invasive species. To assess the occurrence of P. marinus in the marine gastropod Hexaplex nigritus, thirty specimens were collected monthly from the Navachiste lagoon (NL, southeastern GC) between February 2022 and January 2023 (n = 360). The presence of presumptive hypnospores was detected using Ray’s thioglycolate fluid medium, while polymerase chain reaction analysis confirmed P. marinus in the digestive gland of H. nigritus. The pathogen was detected at a prevalence of 6.66% in October (annual prevalence = 0.6%), exhibiting low infection intensity (<10⁴ hypnospores g⁻¹ of tissue), indicative of a non-pathogenic or subclinical condition. Sequencing of the amplified product revealed 99.34% similarity with P. marinus sequences available in GenBank (accession number OR936656.1). This study represents the first record of the parasite P. marinus infecting the marine snail H. nigritus in NL, Sinaloa, Mexico. The finding broadens the known host range of this parasite and suggests that H. nigritus may play a potential role in its dispersal and transmission within the local food web, with possible implications for regional biodiversity and fisheries management.

Keywords:
invasive parasite; gastropod mollusks; host; in vitro incubation and molecular technique; horizontal transmission

Resumo

Perkinsus marinus é um parasita mizozoário nativo da costa leste dos Estados Unidos, onde tem sido associado a mortalidades significativas em populações de moluscos bivalves. Nas últimas duas décadas, sua presença foi documentada em várias espécies de moluscos – incluindo ostras, amêijoas, mexilhões e vieiras –ao longo do Golfo da Califórnia (GC), levando à sua classificação como uma espécie exótica invasora amplamente distribuída. Para avaliar a ocorrência de P. marinus no gastrópode marinho Hexaplex nigritus, trinta espécimes foram coletados mensalmente na lagoa Navachiste (NL, sudeste do GC) entre fevereiro de 2022 e janeiro de 2023 (n = 360). A presença de hipnósporos presumíveis foi detectada utilizando o meio fluido de tioglicolato de Ray, enquanto a análise por reação em cadeia da polimerase confirmou a presença de P. marinus na glândula digestiva de H. nigritus. O patógeno foi detectado com uma prevalência de 6.66% em outubro (prevalência anual = 0.6%), apresentando baixa intensidade de infecção (<10⁴ hipnósporos g⁻¹ de tecido), indicativa de uma condição não patogênica ou subclínica. O sequenciamento do produto amplificado revelou 99.34% de similaridade com sequências de P. marinus disponíveis no GenBank (número de acesso OR936656.1). Este estudo representa o primeiro registro do parasita P. marinus infectando o gastrópode marinho H. nigritus na NL, Sinaloa, México. A descoberta amplia a gama de hospedeiros conhecidos desse parasita e sugere que H. nigritus pode desempenhar um papel potencial em sua dispersão e transmissão na cadeia alimentar local, com possíveis implicações para a biodiversidade regional e o manejo da pesca.

Palavras-chave:
parasita invasor; moluscos gastrópodes; hospedeiro; incubação in vitro e técnica molecular; transmissão horizontal

1. Introduction

Parasitic diseases constitute one of the major threats to marine mollusk populations, particularly those of economic importance in fisheries and aquaculture. Among these diseases, perkinsosis is notable, being caused by myzozoa parasites of the genus Perkinsus (Villalba et al., 2004). Perkinsus marinus is native to the eastern coast of the United States, where it has been linked to mass mortalities in cultured populations of the American oyster Crassostrea virginica (Burreson and Ragone-Calvo, 1996). The species was introduced into the Pacific Ocean via the transfer of infected oysters from the Gulf of Mexico and the U.S. Atlantic coast to the Gulf of California (GC) (Cáceres-Martínez and Vásquez-Yeomans, 2013), where it is now recognized as an invasive exotic pathogen (García-Ulloa et al., 2023).

In the GC, P. marinus has been associated with severe mortalities in farmed Pacific oysters (Crassostrea gigas) (Enríquez-Espinoza et al., 2010) and has been detected in wild populations of Crassostrea corteziensis (Cáceres-Martínez et al., 2008) and Saccostrea palmula (Cáceres-Martínez et al., 2012). More recently, this parasite has been reported in additional bivalve hosts, including the mussels Modiolus capax (Góngora-Gómez et al., 2021) and Mytella strigata (García-Ulloa et al., 2023), as well as in the clams Chionista fluctifraga (Góngora-Gómez et al., 2022), Leukoma grata, and Larkinia grandis (Góngora-Gómez et al., 2024). Despite these findings, infections in these species have not been associated with apparent pathological effects or compromised health status.

Although the prevalence of P. marinus varies according to the host species and environmental conditions —proliferating mostly at temperatures and salinities above 22 °C and 15 PSU (practical salinity units), respectively (Cáceres-Martínez et al., 2008; Enríquez-Espinoza et al., 2010; Bushek et al., 2012)— its presence in mollusks from the coasts of the GC categorizes it as an invader and potential vector stationed in a latent propagation phase, demonstrating its physiological plasticity in a wide spectrum of geographic dispersion and transmission between hosts (García-Ulloa et al., 2023).

Most studies on Perkinsus infection are related to filter-feeding bivalves that acquire it by feeding directly from the water column, such as oysters (Carnegie et al., 2021), mussels (Zhang et al., 2024), clams (Fernández-Boo et al., 2023), and scallops (Góngora-Gómez et al., 2016). However, there are reports indicating that the parasite could be indirectly transmitted, as in the case of herbivorous gastropods —such as abalones— that consume substrates that presumably contain parasite trophozoites (Lester and Davis, 1981), or even through host-to-host transmission facilitated by ectoparasitic carnivorous snails, such as Boonea impressa, which disperses P. marinus among oyster populations (White et al., 1987). To date, there is no information on the presence of this parasite within carnivorous marine snails as hosts.

The “black chinese” snail Hexaplex nigritus, is native to the GC and highly valued for the flavor of its meat, the ornamentation of its shell for handicrafts (Escamilla-Montes et al., 2018), and the medicinal and religious uses of its operculum (Potorti et al., 2024). It is harvested year-round without strict regulation (México, 2023), resulting in gaps in information regarding the ecological and biological aspects of its population, including its health status. As a benthic organism with predatory habits, H. nigritus feeds primarily on clams (Cudney-Bueno et al., 2008), which are known hosts of P. marinus. Therefore, it is possible to infer that the parasite can survive and proliferate within this gastropod.

The objective of this study was to evaluate the occurrence (prevalence, density, and infection intensity) of P. marinus in the “black chinese” snail from Navachiste lagoon (NL), Sinaloa, México, and its possible tissue damage through histological analysis. Based on previous reports on the presence of the parasite in various clams from the region, it was hypothesized that H. nigritus would be an additional host of P. marinus. Monitoring this myzozoa in H. nigritus would provide information on its potential role in transmission dynamics within the food web, as well as anticipate its impact on marine biodiversity and species of commercial interest.

2. Material and Methods

Sampling of H. nigritus was conducted in NL (25°29′14″ N, 108°50′22″ W), located in the north-central region of Sinaloa, southeastern GC, Mexico (Figure 1). The lagoon is part of a protected natural area designated as a RAMSAR site (# 1826) and encompasses approximately 14,000 ha. From February 2022 to January 2023, 30 individuals were collected monthly by free diving at an average depth of 1.53 ± 0.58 m (n = 360; average shell height: 101.35 ± 13.71 mm). Sampled organisms were transported alive to the laboratory in seawater-filled plastic containers following the protocol described by Sotelo-González et al. (2021). During each sampling, in situ physicochemical parameters were recorded. Water temperature and dissolved oxygen concentration were measured using a portable oximeter (YSI 55/12 FT, Ohio, USA), salinity was determined with a precision refractometer (ATAGO S/Mill), and pH was measured using a portable potentiometer (Hanna HI 8314, USA), following the methodology described by Góngora-Gómez et al. (2024).

Figure 1
Geographic location of the study area in Navachiste lagoon, Sinaloa, located in the southeastern Gulf of California, Mexico.

In the laboratory, the snails were shelled, and the tissues (mantle, gill, gonad, and digestive gland) were divided into two subsamples. One subsample was fractionated and homogenized for incubation (7 days in the dark at room temperature) in Ray's fluid thioglycolate medium (RFTM) to detect hypnospores of the pathogen, following the guidelines of the International Office of Epizootics (OIE, 2023). The observed structures were stained with Lugol, and hypnospores were identified as blue-black spherical cells measuring 20–70 µm. Prevalence [(number of individuals with hypnospores/total snails) × 100] (Thrusfield, 2018), parasite density (hypnospores g⁻¹ of tissue, wet weight), and infection intensity (Bushek et al., 1994) were calculated. RFTM-positive samples were analyzed with the polymerase chain reaction (PCR) test to confirm the presence of P. marinus.

From the second tissues subsample, DNA was extracted —by tissue— using the 3% CTAB method (Zhang et al., 1998). Molecular detection was performed by PCR using the specific oligonucleotides PmarITS-70F (5’-CTT-TTG-YTW-GAG-WGT-TGC-GAG-ATG-3’) and its reverse oligonucleotide PmarITS-600R (5’-CGA-GTT-TGC-GAG-TAC-CTC-KAG-AG-3’), which amplify a 509-base pairs (bp) fragment (Audemard et al., 2004). A positive control (DNA from infected C. corteziensis; Villanueva-Fonseca et al., 2020) and a negative control (ultrapure water) were included. The products were separated on a 1% agarose gel, purified using the Wizard SV Gel and PCR Clean-Up System commercial kit (Promega), and sent for sequencing (Macrogen, South Korea). The percentage identity was confirmed by BLAST (Camacho et al., 2009) in the GenBank (NCBI, 2025), and the results obtained were deposited in that database.

The fragments derived from this analysis were aligned with reference sequences of the genus Perkinsus available in the GenBank database, selecting those that represent species reported in host mollusks from different geographic regions (P. marinus, P. mediterraneus, P. olseni, P. atlanticus, P. beihaiensis, P. chesapeaki, and P. andrewsi). The multiple alignment was performed using the MEGA v12.0.11 program (Molecular Evolutionary Genetics Analysis; Kumar et al., 2024) through the ClustalW algorithm, and a phylogenetic tree was constructed with the maximum likelihood method, applying 1000 bootstrap replicates to evaluate the robustness of the branches.

The H. nigritus sequence obtained was incorporated into a set of reference sequences to determine its evolutionary relationship and visualize its clustering with the closest strains. The resulting tree was visualized and edited using the Interactive Tree of Life (iTOL) v7.2.2 platform (Letunic and Bork, 2024), which allowed for a graphical representation of the genetic affinity between the analyzed sequences.

Finally, to evaluate possible tissue damage, histological analysis of digestive tissue was performed in sections stained with hematoxylin-eosin-phloxine (Humason, 1979) to determine the degree of infection proposed by Cáceres-Martínez et al. (2008).

3. Results

Surface water temperature in NL, ranged between 19 and 32 °C throughout the sampling year. Dissolved oxygen fluctuated between 2.66 and 10.23 mg L⁻¹, while salinity ranged between 33 and 39 PSU. The pH ranged from 7.53 to 8.60. No seasonal trends were observed, except for an increase in temperature during the summer months.

The thioglycolate culture technique showed the presence of dark-colored spherical cells (≈ 50 µm in diameter) in the mantle and digestive tissues of H. nigritus, characteristic of P. marinus hypnospores (Figure 2).

Figure 2
Microscopic detection (40X) of Perkinsus sp. hypnospores (arrow) in RFTM, isolated from Hexaplex nigritus from the Navachiste lagoon (southeastern GC).

Of the 360 ​​snails analyzed during the year, two tested positive for P. marinus using RFTM in October 2022, with two hypnospores observed per H. nigritus specimen. The prevalence, parasite density, and monthly infection intensity were 6.66%, 0.53 hypnospores g⁻¹ of wet weight (ww) tissue and light (<10⁴ hypnospores g⁻¹ of ww tissue), respectively; while, considering the annual sampling period, the average parasite prevalence and density were 0.6% and 0.00147 hypnospores g⁻¹ (ww).

Of the snails that tested positive for RFTM, the presence of P. marinus was confirmed in one of the two H. nigritus specimens by PCR, obtaining a 509 bp fragment of the ITS region in the digestive tissue (Figure 3).

Figure 3
Detection of Perkinsus marinus in Hexaplex nigritus by PCR and visualization on a 1% agarose gel. M, molecular weight marker (1 kb Ladder); lane 1, mantle sample; lane 2, gill sample; lane 3, digestive gland sample (509 bp); lane 4, gonad sample; C-, negative control for P. marinus; C+, positive control for P. marinus (509 bp).

The 480-bp sequence of the pathogen obtained from the digestive tissue of H. nigritus showed 99.34% identity with P. marinus isolates previously reported in the southern oyster (C. corteziensis) from the same NL region and in C. gigas in South Korea (OR936656.1). Phylogenetic alignment showed that the obtained sequence clusters consistently with these isolates (Figure 4), confirming the presence of P. marinus in H. nigritus.

Figure 4
Phylogenetic tree constructed from the alignment of the Perkinsus marinus sequence ―obtained from Hexaplex nigritus― with homologous sequences deposited in GenBank (NCBI, 2025).

Histological sections showed an intact tissue structure, with no evidence of necrosis, abnormal inflammatory infiltration, phagocytic activity, brown cells, or cellular alterations that could be associated with the different stages of the parasite's life cycle.

4. Discussion

The water temperature (32 °C) and salinity (35 PSU) recorded in the NL during October 2022, when hypnospores were detected, fall within the environmental ranges previously reported as favorable for the proliferation of P. marinus under both experimental conditions (Villalba et al., 2004) and natural estuarine and marine environments (Bushek et al., 2012; Bidegain et al., 2017). Despite these apparently suitable conditions, parasite prevalence in H. nigritus was remarkably low, being detected in only two individuals out of the 360 examined. Such findings indicate that P. marinus may persist at low infection intensities that remain below the detection threshold of conventional histopathological methods or that vary seasonally according to environmental conditions. Hypnospores were observed exclusively during autumn, coinciding with the highest recorded temperature and salinity values. A comparable pattern was reported by Góngora-Gómez et al. (2016), who found a markedly higher prevalence (90%) of Perkinsus sp. in the pen shell Atrina maura from areas adjacent to the present study site, indicating that infection outcomes can vary substantially even among sympatric molluscan hosts exposed to similar environmental conditions. Similarly, low infection levels have persisted in other bivalve species from the same region despite favorable temperature and salinity regimes (Góngora-Gómez et al., 2021, 2022, 2024). Taken together, these observations indicate that, beyond temperature and salinity, host-related factors such as species-specific susceptibility and immune competence, together with ecological drivers including environmental variability and anthropogenic disturbance, may substantially influence parasite establishment and transmission dynamics (Bidegain et al., 2017; Gignoux-Wolfsohn et al., 2020).

Recent studies conducted in other geographic regions under contrasting environmental conditions have likewise demonstrated that Perkinsus spp. infections can elicit highly variable responses among bivalve hosts, ranging from subclinical infections to severe disease and mortality. For example, Chan et al. (2021) demonstrated that C. virginica develops a pronounced but ultimately maladaptive immune response against P. marinus, characterized by excessive inflammatory activation that fails to clear the parasite and instead contributes to the tissue damage underlying the extensive mortalities frequently reported in natural populations. In contrast, C. gigas exhibited a comparatively attenuated immune response, which has been associated with greater tolerance to infection rather than resistance, underscoring that interspecific differences in Perkinsus susceptibility depend on the regulation and outcome of the immune response, not merely on its magnitude. Likewise, Kim et al. (2025) reported that infections caused by P. olseni and P. honshuensis in wild oyster populations induced relatively weak immune responses and were associated with lower mortality rates than those observed in oysters experimentally challenged with P. marinus. Similarly, Rocha et al. (2023) documented the occurrence of P. marinus hypnospores in mangrove oysters (Crassostrea sp.) from Brazil, with prevalence values ranging from 18% to 34% and no evidence of significant mortality. Collectively, these studies indicate that the presence of this parasite does not necessarily translate into measurable physiological impairment of the host, with infection outcomes largely determined by the interplay between host-specific immune capacity and local environmental conditions.

Consistent with this pattern, the RFTM results obtained in the present study suggest that H. nigritus may function primarily as an incidental carrier of P. marinus rather than as a susceptible host supporting active infection. Comparable patterns of apparent bioinvasion without detectable adverse effects have been documented for other Perkinsus species in several molluscan hosts worldwide. For example, P. chesapeaki and P. olseni have been reported in Crassostrea rhizophorae, C. gasar, Anomalocardia brasiliana, Mytilus platensis, and Mytella falcata from South America, exhibiting variable prevalence levels but without associated mortality or significant pathological alterations (Cremonte et al., 2005; Dantas-Neto et al., 2016; Silva et al., 2024). Similarly, Ye et al. (2022) detected P. olseni, P. beihaiensis, and P. chesapeaki in oysters, clams, and abalones from China, with low to moderate prevalence (<30%) and no apparent impacts on host health. In New Zealand, Lane et al. (2023) reported prevalences ranging from 0% to 3% for P. olseni in the green-lipped mussel Perna canaliculus, whereas Carella et al. (2023) recorded prevalences between 10% and 40% in the Mediterranean mussel Mytilus galloprovincialis; neither study identified significant consequences for population health. Together, these reports suggest that Perkinsus infections frequently occur as subclinical events, allowing infected mollusks to potentially act as reservoirs that contribute to parasite persistence and dispersal within marine ecosystems.

PCR-based molecular diagnosis provided the first definitive evidence of P. marinus in the digestive tissue of H. nigritus. This technique, widely employed for Perkinsus detection and identification (Góngora-Gómez et al., 2024), confirmed the presence of the parasite through the amplification of species-specific DNA markers. Although the overall annual prevalence was low (0.6%), the molecular evidence is consistent with previous reports of P. marinus in bivalve species from the GC (Villanueva-Fonseca et al., 2020). These results support the hypothesis that the participation of H. nigritus in the life cycle of the parasite is likely incidental (White et al., 1987; García-Ulloa et al., 2023), possibly reflecting its trophic behavior rather than a true host–parasite association. Given the predominantly carnivorous feeding habits of this gastropod, acquisition of the parasite may occur through the consumption of infected bivalves or other susceptible hosts.

Sequencing and phylogenetic analysis of the 480-bp fragment recovered from the digestive tissue of H. nigritus confirmed the identity of P. marinus, revealing 99.34% sequence identity and clustering of the isolate within the corresponding species clade together with sequences previously reported from C. corteziensis in the GC (Villanueva-Fonseca et al., 2020) and C. gigas from South Korea (OR936656.1; Kim et al., 2024), as well as with records from Crassostrea sp. in Brazil (Rocha et al., 2023). This clustering pattern, accompanied by only slight genetic divergence among isolates from different geographic regions, corroborates the taxonomic identity of the parasite and indicates a remarkable capacity to colonize diverse hosts and environments, consistent with the widespread distribution of a dominant haplotype potentially facilitated by host-mediated dispersal along coastal environments and its persistence across broad biogeographic scales (Pysěk and Richardson, 2010). These findings highlight the need for future studies addressing the genetic diversity, population structure, and dispersal pathways of P. marinus among different host species and ecosystems.

Histological examination of H. nigritus revealed no tissue damage, inflammatory responses, or pathological alterations attributable to P. marinus infection. Similar observations were reported by Kim et al. (2024) in C. gigas, in which the parasite was not detected through histology or RFTM but was identified by PCR at low frequencies (13–27%). This apparent tolerance may be related to specific biological and trophic characteristics of H. nigritus. Unlike filter-feeding bivalve hosts, in which P. marinus transmission is direct and dose-dependent, driven by the continuous uptake of waterborne trophozoites, prezoosporangia, and zoospores during feeding (Audemard et al., 2004; Bidegain et al., 2017), H. nigritus is a strictly carnivorous, non-filter-feeding gastropod that preys primarily on bivalves, including clams (Cudney-Bueno et al., 2008; Escamilla-Montes et al., 2018). Its exposure to the parasite would therefore be expected to occur indirectly and intermittently, through the occasional ingestion of infected prey tissue—a trophic route of acquisition comparable to that previously described for other carnivorous or ectoparasitic gastropods implicated in Perkinsus transmission, such as abalones consuming trophozoite-contaminated substrates (Lester and Davis, 1981) and the ectoparasitic snail B. impressa feeding on infected oysters (White et al., 1987). This predation-based mode of acquisition would plausibly result in a lower and more sporadic infective dose than the continuous filtration characteristic of bivalve hosts. Although the immune response of H. nigritus to P. marinus has not yet been characterized, gastropods in general rely on an innate immune system mediated primarily by circulating hemocytes capable of phagocytosis and encapsulation of foreign particles and parasites (Pila et al., 2016; Al-Khalaifah, 2022); such a defense mechanism, if present in H. nigritus, could plausibly contain the parasite at subclinical levels before it proliferates within host tissues, contributing to the absence of detectable histopathological lesions. Together with the low prevalence and low infection intensity detected in the present study, these trophic and immunological considerations support the hypothesis that H. nigritus functions as a tolerant or accidental host, in which limited trophic-level exposure and a potentially effective innate immune containment jointly restrict parasite proliferation and the development of overt pathology.

5. Conclusion

This study confirmed the occurrence of P. marinus in H. nigritus, representing the first record of this parasite in this marine gastropod, broadening the known host range of this invasive parasite within the GC. The combined application of RFTM, PCR, DNA sequencing, and phylogenetic analysis confirmed low prevalence, sporadic occurrence, and low infection intensity, with no associated histopathological alterations, indicating that H. nigritus functions as an incidental or opportunistic host rather than a primary reservoir sustaining parasite populations, and that the parasite currently poses little immediate risk to snail populations or associated fisheries. As a predatory, non-filter-feeding gastropod, H. nigritus highlights trophic transmission as an additional pathway for P. marinus dispersal beyond traditional bivalve hosts, underscoring the need for expanded surveillance of Perkinsus spp. in non-bivalve species to better understand its ecology and transmission dynamics within coastal food webs of the GC.

Acknowledgements

The authors thank the Instituto Politécnico Nacional (IPN) and Secretaría de Ciencia, Humanidades, Tecnología e Innovación (SECIHTI) Mexico, for their logistical and economic support. COMP, YLGB and ALA (PhD) and CHS (Postdoc) are grateful to the SECIHTI for supporting their studies at the Interdisciplinary Research Center for Integral Regional Development (IPN-CIIDIR-Sinaloa). This research was funded by the Instituto Politécnico Nacional (IPN), through the projects: IPN-SIP-20230821 Presencia de Perkinsus marinus en dos poblaciones silvestres de la almeja pata de mula Anadara mazatlanica en el sureste del Golfo de California; IPN-SIP-20240017 Análisis de metales pesados de la "almeja negra", Larkinia grandis, del sureste del Golfo de California y su implicación en la salud humana.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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*

e-mail: [e-mail]

Editor:

Takako Matsumura Tundisi

Publication Dates

• Publication in this collection
  25 Sept 2026
• Date of issue
  2026

History

• Received
  12 Dec 2025
• Accepted
  24 July 2026