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Hidden hosts: Limpets as key players in trematode transmission

Published online by Cambridge University Press:  23 February 2026

C.-H. Li Open the ORCID record for C.-H. Li [Opens in a new window] ,
J. Bennett Open the ORCID record for J. Bennett [Opens in a new window]  and
R. Poulin Open the ORCID record for R. Poulin [Opens in a new window]
C.-H. Li*
Affiliation:
Department of Zoology, University of Otago , Dunedin, New Zealand
J. Bennett
Affiliation:
Department of Zoology, University of Otago , Dunedin, New Zealand
R. Poulin
Affiliation:
Department of Zoology, University of Otago , Dunedin, New Zealand
*
Corresponding author: C.-H. Li; Email: cillialichen@hotmail.com
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Abstract

Limpets are abundant and ecologically important gastropods in intertidal and some riverine ecosystems, yet their role in trematode transmission remains comparatively understudied. We investigated trematode infection in intertidal limpets from Otago Harbour, New Zealand, using a molecular approach. Two species were identified: the avian schistosome Gigantobilharzia cf. patagonensis in Siphonaria australis and Acanthoparyphium sp. A metacercariae in Notoacmea sp. Gigantobilharzia cf. patagonensis was detected at all five sampling sites, with prevalence ranging from 2.6% to 100%. Haplotype network analysis using cox1 revealed high haplotype diversity and a star-like topology, suggesting a recent population expansion. This study expanded the known diversity of marine schistosomes in the region and raises potential public health concerns with cercarial dermatitis. We also conducted a literature synthesis further demonstrating that limpets contribute to trematode transmission across 12 superfamilies and 23 families, with distinct parasitism profiles between freshwater and marine environments. These findings highlight limpets as overlooked but significant hosts in trematode ecology and emphasize the need for broader surveys and definitive host screening to resolve incomplete life cycles and assess epidemiological risks in coastal ecosystems.

Keywords

Digeneamarine schistosomesSiphonariidaelimpet hostshaplotype diversity

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 100 , 2026 , e21
Creative Commons
Creative Common License - CCCreative Common License - BYCreative Common License - NCCreative Common License - ND
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives licence (http://creativecommons.org/licenses/by-nc-nd/4.0), which permits non-commercial re-use, distribution, and reproduction in any medium, provided that no alterations are made and the original article is properly cited. The written permission of Cambridge University Press or the rights holder(s) must be obtained prior to any commercial use and/or adaptation of the article.
Copyright
© The Author(s), 2026. Published by Cambridge University Press

Introduction

Limpets are ubiquitous and abundant invertebrates in aquatic environments, yet they remain comparatively understudied for parasitological research relative to other gastropod taxa. As molluscs, limpets play important roles in the transmission of digenean trematodes, serving either as first intermediate hosts harbouring sporocysts, rediae, and cercariae, or as second intermediate hosts harbouring metacercariae (Koppel et al. Reference Koppel, Leung and Poulin2011). Given their wide distribution and potential role in parasite transmission, investigating the diversity of trematodes infecting limpets can help resolve partially understood life cycles and provide predictive insights into the parasite diversity of local vertebrate hosts.

In New Zealand, fewer than 0.5% of marine gastropod taxa have documented helminth parasites (Bennett et al. Reference Bennett, Presswell and Poulin2022b). Although knowledge of marine helminth diversity has expanded in recent years (Bennett et al. Reference Bennett, Poulin and Presswell2022a), many life cycles remain incomplete (Bennett et al. Reference Bennett, Presswell and Poulin2023). The Otago Harbour mudflats, in New Zealand’s South Island, are known to support a rich diversity of trematode parasites (Leung et al. Reference Leung, Donald, Keeney, Koehler, Peoples and Poulin2009b). While previous biodiversity surveys in Otago’s coastal marine ecosystem have successfully matched various larval stages to adult parasites (Bennett et al. Reference Bennett, Presswell and Poulin2023), limpets (here including limpet-shaped gastropods) have been overlooked. Koppel et al. (Reference Koppel, Leung and Poulin2011) examined only one limpet species (Notoacmea scapha) and recovered metacercariae from three trematode species in Otago Harbour, highlighting limpets’ potential role as viable intermediate hosts and transmitters of parasites.

Of particular interest is the role of siphonariids (false limpets), which are known to host marine schistosomes (Digenea: Schistosomatidae) in Argentina, Australia, and Kuwait (Abdul-Salam and Al-Khedery Reference Abdul-Salam and Al-Khedery1992; Brant et al. Reference Brant, Loker, Casalins and Flores2017; Ewers Reference Ewers1961; Lorenti et al. Reference Lorenti, Brant, Gilardoni, Diaz and Cremonte2022). Schistosomes are dioecious blood flukes of birds and mammals. Unlike most trematodes, they lack a metacercarial stage, and cercariae leave the molluscan host and penetrate the definitive host (Gabrielli and Garba Djirmay, Reference Gabrielli and Garba Djirmay2023). Some species cause schistosomiasis in humans, while others can induce human cercarial dermatitis (HCD, or swimmer’s itch) when non-human schistosome cercariae accidentally penetrate human skin (Gabrielli and Garba Djirmay Reference Gabrielli and Garba Djirmay2023; Horak et al. Reference Horak, Mikes, Lichtenbergova, Skala, Soldanova and Brant2015). In New Zealand, outbreaks of HCD have been reported from freshwater avian schistosomes in the genus of Trichobilharzia (Davis et al. Reference Davis, Blair and Brant2022), but the diversity and zoonotic potential of marine schistosomes remain poorly understood. Recently, a schistosome (Schistosomatidae gen. sp. 1) was reported from the limpet Patelloida corticate in New Zealand (Bennett et al. Reference Bennett, Poulin and Presswell2022a). However, this host may have been misidentified and is likely Siphonaria australis. This represents only the second marine schistosome species recorded in New Zealand, the first being Ornithobilharzia canaliculata from the gull Larus dominicanus (Bennett et al. Reference Bennett, Presswell and Poulin2023; Rind Reference Rind1984). Therefore, examining these gastropods in greater depth could reveal the diversity, distribution, and public health potential of marine schistosomes in New Zealand.

In this study, we adopt a morphological definition of ‘limpet’, encompassing gastropods with a patelliform (limpet-shaped) shell regardless of taxonomic lineage. Our aims are to investigate the limpet species of Otago Harbour and molecularly identify the trematode parasites they harbour. We also conducted a comprehensive review of available information on trematode parasites infecting limpets in both marine and freshwater ecosystems worldwide, to provide an up-to-date synthesis of the trematode taxa using these molluscs as hosts.

Methods

Field collection and dissection

Limpets were collected by hand at low tide from five sites along Otago Harbour, South Island, New Zealand, between December 2024 and March 2025. These sampling sites include Lower Portobello Bay (latitude, longitude: −45.832203, 170.672795), Wellers Rock (−45.797962, 170.715378), Macandrew Bay (−45.868997, 170.596806), Broad Bay (−45.848534, 170.619328), and Company Bay (−45.856851, 170.598893). Sample sizes vary across sampling sites (Table 1). Prior to dissection, limpets were maintained in aerated containers with fresh seawater. Each limpet was removed from its shell using forceps, and internal organs were examined under a dissection microscope. Muscle tissue was firmly pressed between two glass plates and examined under the dissection microscope for parasites. All parasites recovered were preserved in 70% ethanol for subsequent DNA sequencing. Limpets were identified to species or genus using published keys (Carson and Morris Reference Carson and Morris2017; Jones et al. Reference Jones, Marsden, Holdaway and Jones2005), and through personal communication with expert molluscan taxonomist Prof. Hamish Spencer (Zoology Department, University of Otago, Dunedin, New Zealand).

Table 1.

Parasite prevalence from the limpets collected at five Otago Peninsula sites facing the Otago Harbour

Parasite identification and haplotype network

Genomic DNA was extracted from individual cercariae or metacercariae using the DNeasy® Blood &Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol. Two genetic markers were targeted for amplification: a partial region of the 28S rRNA gene and the cytochrome c oxidase subunit I (cox1) gene. For the 28S rRNA gene, primers T16 and T30 (Harper and Saunders 2001) were used under the following thermal cycling conditions: initial denaturation at 94°C for 5 min; 38 cycles of denaturation at 94°C for 30 s, annealing at 45°C for 30 s, and extension at 72°C for 2 min; followed by a final extension at 72°C for 7 min. For the cox1 gene, primers JB3 (Bowles 1993) and Trem.cox1.rrnl (Kralova-Hromadova 2008) were used with the following protocol: initial denaturation at 95°C for 2 min; 40 cycles of denaturation at 95°C for 30 s, annealing at 48°C for 40 s, and extension at 72°C for 1 min; followed by a final extension at 72°C for 10 min. PCR products were cleaned using ExoSAP-ITTM Express PCR Product Cleanup Reagent (USB Corporation, Cleveland, OH, USA) following the manufacturer’s instructions. Sanger sequencing by capillary electrophoresis was performed by the Genetic Analysis Service, Department of Anatomy, University of Otago, New Zealand.

Raw sequences were trimmed using default parameters and manually curated to correct ambiguous bases in Geneious Prime® version 2025.2.2. Depending on the parasite, we either used the 28S gene or a combination of 28S and cox1 genes to identify species to the lowest taxonomic level possible through BLASTn (Basic Local Alignment Search Tool for nucleotides) searches against the NCBI GenBank database (https://blast.ncbi.nlm.nih.gov/). To examine the genetic structure of the schistosome, we constructed a haplotype network from aligned cox1 sequence data. Approximately 33 bp downstream of the cox1 stop codon were retained in the alignment due to their high sequence quality. Some sequences were shorter in length compared to others, but still included in the haplotype network with the assumption that they matched 100% to longer haplotype representatives. Sequences were aligned using the ClustalW algorithm implemented in the msa package (version 1.38.0) (Bodenhofer et al. Reference Bodenhofer, Bonatesta, Horejs-Kainrath and Hochreiter2015) within R Statistical Software (version 4.2.2; R Core Team, 2022). The haplotype network was constructed using the pegas package (version 1.3) (Paradis Reference Paradis2010) to visualize genetic relationships among haplotypes.

Literature review

To survey trematodes parasitising limpets, a topic search was conducted in Web of Science in July, 2025 using the following query: ‘(Trematod* OR Digenea OR Fluke OR Redia* OR Cercaria* OR Sporocyst* OR Metacercaria*) AND (Limpet* OR Patellogastropod* OR Patellid* OR Fissurellid* OR Lepetelloid* OR Siphonariid* OR Phenacolepadid* OR Tylodinid* OR Latiid* OR Latia OR Trimuscul* OR Ancylid*)’. For completeness, besides the ‘true limpets’ (family Patellidae), we also included in our review all major gastropod groups commonly referred to as ‘limpets’ in the literature (e.g., family Fissurellidae – keyhole limpets; family Siphonariidae – false limpets; family Calyptraeidae – slipper limpets). The title and abstract of all publications retrieved by the search were checked, and all relevant publications were retained. From each publication, we extracted the host species name, the trematode family and (if given) species name, the sampling locality, and (if available) the prevalence of infection.

Results

Trematode survey and molecular identification

We collected and examined four limpet taxa (Siphonaria australis Quoy & Gaimard, 1833, Cellana ornata Dillwyn, 1817, Cellana strigilis Hombron & Jacquinot, 1841, Notoacmea sp.) from five intertidal sites in Otago Harbour and identified two trematode species (Table 1). Siphonaria australis was the most common and abundant species, occurring at all five sites. Schistosome infections were detected in S. australis at every site, with a prevalence of sporocysts ranging from 2.6% to 100%, though the 100% prevalence was based on a sample size of only two limpets from Lower Portobello Bay. Notoacmea sp. were found at four sites, but only individuals from Lower Protobello Bay hosted metacercaeriae of Acanthoparyphium sp. A. (11.4% prevalence). No parasites were detected in any of the Cellana ornata and C. strigilis examined.

Cercariae from the false limpet S. australis were identified as Gigantobilharzia cf. patagonense (Figure 1). The 28S rRNA sequence obtained (~560 bp, GenBank accession PX833732) differed by a single nucleotide (99.83% identity) from Gigantobilharzia patagonense (syn. Marinabilharzia patagonense) described from the kelp gull Larus dominicanus in Argentina (GenBank accessions OK338634-OK338636) (Lorenti et al. Reference Lorenti, Brant, Gilardoni, Diaz and Cremonte2022). It also shared a 99.83% identity with Schistosomatidae sp. recorded from L. dominicanus (KX302891) and Siphonaria lessonii (KX302889) in Argentina (Brant et al. Reference Brant, Loker, Casalins and Flores2017), and a 99.81% identity (89% query coverage) with a sequence from Patelloida corticata in New Zealand (ON661331) (Bennett et al. Reference Bennett, Poulin and Presswell2022a). Additionally, the sequence shared 98.91% identity with Schistosomatidae sp. from penguin Spheniscus demersus from South Africa (KM023789) (Aldhoun and Horne Reference Aldhoun and Horne2015). For the cox1 gene, our consensus sequence shared 96.69% identity (44% query coverage) with G. patagonensis from the brown-hooded gull Chroicocephalus maculipennis (OK338770) and 95.83% identity (55% query coverage) with G. patagonense from L. dominicanus (OK338769) (Lorenti et al. Reference Lorenti, Brant, Gilardoni, Diaz and Cremonte2022).

Figure 1.

Photomicrographs of the cercaria of Gigantobilharzia cf. patagonensis showing (A) dorsal view and (B) lateral view.

Metacercariae found infecting Notoacmea sp. at Lower Portobello (Table 1) were identified as Acanthoparyphium sp. A. Our 28S rRNA sequence was identical (100% match) to various representatives of Acanthoparyphium sp. A of (Leung et al. Reference Leung, Keeney and Poulin2009a) recorded from New Zealand intertidal species, including cockle Austrovenus stutchburyi (OQ407748), the green chiton Chiton glaucus (OQ407746), and the limpet Notoacmea scapha (OQ407744) (Bennett et al. Reference Bennett, Presswell and Poulin2023). It also shared 98.72% identity with isolates of another unidentified Acanthoparyphium sp. from N. scapha (ON661320) (Bennett et al. Reference Bennett, Poulin and Presswell2022a).

Haplotype network analysis of Gigantobilharzia cf. patagonensis

We identified nine unique G. cf. patagonensis haplotypes based on cox1 sequences (Figure 2A, accessions PX910024-PX910034). The network displayed a star-like topology dominated by haplotype I, which was the most common lineage and present in four of the five sampling locations (absent only from Lower Portobello) across Otago Harbour, New Zealand. Haplotypes III, V, and VI differed from haplotype I by 1bp, while haplotypes II, IV, and VII differed by 2 bp. Broad Bay exhibited the highest genetic diversity, containing all nine identified haplotypes. This included two divergent lineages found exclusively at this site: Haplotype VIII (8 mutational steps from haplotype I) and haplotype IX (a further 19 mutational steps away). Despite the variation, haplotypes were mixed among sites (Figure 2B), showing random sorting with no clear geographic structuring across the Otago Peninsula.

Figure 2.

Haplotype network of Gigantobilharzia cf. patagonensis recovered from Siphonaria australis, based on cox1 sequences from five Otago Harbour sites (A) and the distribution of haplotypes by location (B). BB, Broad Bay; CB, Company Bay; LP, Lower Portobello; MB, Macandrew Bay; WR, Wellers Rock.

Literature survey of limpet-associated trematodes

The bibliographical survey recovered trematodes from 12 superfamilies and 23 families utilising marine or freshwater limpets as first or second intermediate hosts (Table 2). In the freshwater environment, trematode superfamilies included the Paramphistomoidea, Diplostomoidea, Schistosomatoidea, Echinostomatoidea, Monorchioidea, and Gorgoderoidea. In the marine environment, trematodes belonged to the superfamilies Gymnophalloidea, Hemiuroidea, Lepocreadioidea, Pronocephaloidea, Microphalloidea, and Opecoeloidea, as well as the Schistosomatoidea and Echinostomatoidea. Although the Schistosomatoidea and Echinostomatoidea superfamilies were found in both environments, no trematode families were shared between freshwater and marine systems. These trematodes utilised limpet-shaped hosts from nine families: three freshwater families (Planorbidae, Bumupiidae, Acroloxidae), and six marine families (Siphonariidae, Lottidae, Patellidae, Fissurellidae, Nacellidae, Calyptraeidae).

Table 2.

Summary of trematode taxa reported from limpet hosts from previous publications

* IH-1 = First intermediate host; IH-2 = second intermediate host; DH = definitive host.

** FW, Freshwater; MR, marine.

The prevalence of trematode infection in freshwater environments ranged from 0 to 20%, with all recorded trematodes using limpets as first intermediate hosts. In marine environments, prevalence ranged from 0.1 to 100%, and many trematode species also use limpets as second intermediate hosts. Trematodes of the genus Proctoeces (family Fellodistomidae) can mature into egg-producing adult worms in their molluscan host, and thus also use limpets as their definitive host. Records of limpet-associated trematodes are most numerous in the United States for freshwater systems and in Argentina and Ireland for marine systems.

Discussion

The role of limpets (in the broad sense) in trematode life cycles remains poorly documented. Here, we identified two trematode species in intertidal limpets from Otago Harbour. The first is the avian schistosome, Gigantobilharzia cf. patagonensis, which uses Siphonaria australis as its first intermediate host. The second is Acanthoparyphium sp. A metacercaria, recovered from Notoacmea sp., used as a second intermediate host. Gigantobilharzia cf. patagonensis was recovered from all five sampling sites, with prevalence reaching up to 100%. Genetic analyses revealed considerable diversity of cox1 sequences within the Otago Harbour population. In addition, our literature review highlights the broad diversity of trematodes infecting limpets in both marine and freshwater systems around the world.

We report Siphonaria australis as a new first intermediate host record for Gigantobilharzia cf. patagonensis. Previous studies in Otago recovered matching sequences (Bennett et al. Reference Bennett, Poulin and Presswell2022a), but the host was identified as the true limpet Patelloida corticata. Given that schistosomes within the Gigantobilharzia clade are known to infect pulmonate gastropods (Siphonariidae) (Brant et al. Reference Brant, Loker, Casalins and Flores2017; Ewers Reference Ewers1961; Lorenti et al. Reference Lorenti, Brant, Gilardoni, Diaz and Cremonte2022), the earlier record likely reflects host misidentification, with S. australis representing the intermediate host in this region.

The Otago Harbour isolate is closely related to Gigantobilharzia patagonensis, which infects S. lessoni in Argentina (Brant et al. Reference Brant, Loker, Casalins and Flores2017; Lorenti et al. Reference Lorenti, Brant, Gilardoni, Diaz and Cremonte2022). Definitive hosts of G. patagonensis include the kelp gull Larus dominicanus in Argentina and the African penguin Spheniscus demersus in South Africa (Aldhoun and Horne Reference Aldhoun and Horne2015). In New Zealand, the life cycle involves the black-backed gull L. dominicanus (Bennett et al. Reference Bennett, Presswell and Poulin2023). As these gulls are non-migratory, introduction via bird migration is unlikely.

Analysis of the mitochondrial cox1 gene of G. cf. patagonensis revealed high haplotype diversity within the Otago Harbour population. The haplotype network displayed a star-like topology dominated by a single common lineage (haplotype I), suggesting a potential recent population expansion. Broad Bay exhibited the highest diversity, containing unique, divergent lineages. This genetic diversity suggests a large, stable parasite population within the harbour, likely maintained by the constant movement of avian definitive hosts dropping schistosome eggs across different coastal sites. Prevalence in S. australis (2.6–100%) was notably higher than that reported for G. patagonensis in S. lessoni from Argentina (0.9–6.1%) (Alda and Martorelli Reference Alda and Martorelli2009; Brant et al. Reference Brant, Loker, Casalins and Flores2017). However, extreme values in our dataset may result from small sample sizes (e.g., 100% prevalence at Lower Portobello Bay was based on only two limpets, and our highest number of haplotypes came from Broad Bay, which has the highest number of limpets examined).

Avian schistosomes can cause HCD when their cercariae penetrate human skin. While freshwater outbreaks associated with Trichobilharzia are well documented (Davis et al. Reference Davis, Blair and Brant2022; Horak et al. Reference Horak, Mikes, Lichtenbergova, Skala, Soldanova and Brant2015), marine species also pose risks to humans (Ewers Reference Ewers1961). Compared with freshwater schistosomes, marine taxa remain less studied worldwide (Brant and Loker Reference Brant and Loker2013; Khosravi et al. Reference Khosravi, Thieltges, Shamseddin and Georgieva2022); however, genera such as Ornithobilharzia have previously been reported in New Zealand (Bennett et al. Reference Bennett, Presswell and Poulin2023; Rind Reference Rind1984). The molecular confirmation of Gigantobilharzia in five bays within Otago Harbour expands the known diversity of marine schistosomes in the region. Its presence in intertidal zones highlights a potential public health concern if this species has zoonotic potential, and underscores the need for monitoring schistosome populations in recreational coastal environments. In the context of climate change, swimmer’s itch is likely to become increasingly prevalent in cool, temperate areas like New Zealand (Soleng et al. Reference Soleng, Gundersen and Lindstedt2025), reinforcing the importance of clinical awareness and improved knowledge of parasite distribution and host knowledge.

Metacercariae recovered from Notoacmea sp. were identified as Acanthoparyphium sp. A of Leung et al. (Reference Leung, Keeney and Poulin2009a) (Echinostomatoidea: Himasthlidae). The 28S rRNA sequences matched 100% with isolates previously recorded from the New Zealand cockle Austrovenus stutchburyi and the chiton Chiton glaucusi (Bennett et al. Reference Bennett, Presswell and Poulin2023). Acanthoparyphium sp. A was also reported in Notoacmea scapha from Lower Protobello Bay in 2010, where limpets were suggested to act as dead-end hosts unlikely to transmit metacercariae to suitable definitive hosts, such as oystercatchers, due to their small body size (Koppel et al. Reference Koppel, Leung and Poulin2011). Finally, we found no trematode infection in either of the other two limpet species examined from Otago Harbour, Cellana ornata and C. strigilis; however, the numbers of specimens of these species that could be collected and examined were too low to conclude that they are not used as hosts by trematodes.

Our literature survey revealed that limpets play important roles in trematode life cycles across 12 superfamilies and 23 families. Ecological roles of limpets differ between freshwater and marine environments. Freshwater limpets (Planorbidae, Burnupiidae, Acroloxidae) serve exclusively as first intermediate hosts, whereas marine limpets (Siphonariidae, Lottidae, Patellidae, Fissurellidae, Nacellidae, Calyptraeidae) can serve as both first and second intermediate hosts. No trematode families exploit both marine and freshwater limpets, although members of superfamilies Echinostomatoidea and Schistosomatoidea occur in both environments. Prevalence tends to be higher in limpets serving as second intermediate hosts, likely resulting from accumulating metacercarial encystment, whereas first intermediate host infections, which often result in castration and increased mortality due to cercariae asexual amplification, occur at much lower prevalences.

Different limpet families exhibit distinct parasitism profiles. For example, Siphonariidae (air-breathing false limpets) are key first intermediate hosts for marine Schistosomatidae and Hemiuridae, and second intermediate hosts for Microphallidae (Gilardoni et al. Reference Gilardoni, Etchegoin, Diaz, Ituarte and Cremonte2011). In contrast, the Fissurellidae (keyhole limpets) are often exploited by Fellodistomidae, specifically the genus Proctoeces. Notably, Proctoeces lintoni is reported to exhibit progenesis (precocious maturity) in Fissurellidae in Chile, whereby limpets act as alternative definitive hosts alongside clingfish (George-Nascimento et al. Reference George-Nascimento, Balboa, Aldana and Olmos1998).

Although sample size varied among limpet species and sampling sites and may influence prevalence estimates or the likelihood of detecting rare haplotypes, this study provides important insights into the diversity and ecology of marine schistosomes in New Zealand. We documented high G. cf. patagonensis prevalence and genetic diversity in Otago Harbour, thus highlighting potential public health risks of the zoonotic disease HCD. Future work can expand geographic sampling and incorporate definitive host screening to resolve life cycles fully and assess the distribution of G. cf. patagonensis and the risk of HCD in recreational coastal environments.

Acknowledgements

We would like to acknowledge Priscila Salloum and Lilou Mayeur for their assistance with field collections. We also thank Hamish Spencer for sharing his expertise in limpet identification.

Financial support

This work was supported by a Ministry of Business, Innovation and Employment Endeavour Fund Emerging Aquatic Diseases: A novel diagnostic pipeline and management framework, Award no: CAWX2207, recipient: Cawthron Institute.

Competing interests

The authors declare no conflict of interest.

References

Abdul-Salam, J and Al-Khedery, B (1992) The occurrence of larval Digenea in some snails in Kuwait Bay. Hydrobiologia 248, 161–165.10.1007/BF00006083CrossRefGoogle Scholar
Alda, P and Martorelli, SR (2009) Larval digeneans of the Siphonariid pulmonates Siphonaria lessoni and Kerguelenella lateralis and the flabelliferan isopod Exosphaeroma sp. from the intertidal zone of the Argentinean Sea. Comparative Parasitology 76, 267–272.10.1654/4381.1CrossRefGoogle Scholar
Aldana, M, Pulgar, J, Hernández, B, George-Nascimento, M, Lagos, NA and García-Huidobro, MR (2020) Context-dependence in parasite effects on keyhole limpets. Marine Environmental Research 157, 104923.10.1016/j.marenvres.2020.104923CrossRefGoogle ScholarPubMed
Aldana, M, Pulgar, JM, Orellana, N, Patricio Ojeda, F and García-Huidobro, MR (2014) Increased parasitism of limpets by a trematode metacercaria in fisheries management areas of central Chile: Effects on host growth and reproduction: Management areas and parasitism. EcoHealth 11, 215–226.10.1007/s10393-013-0876-9CrossRefGoogle ScholarPubMed
Aldhoun, JA and Horne, EC (2015) Schistosomes in South African penguins. Parasitology Research 114, 237–246.10.1007/s00436-014-4185-1CrossRefGoogle ScholarPubMed
Appleton, CC (2003) The avian Schistosomatidae of sub-Saharan Africa with particular reference to Cercaría herinU a cause of dermatitis in people. Proceedings of Workshop on African Freshwater Malacology, Kampala, Uganda, 9–12 September 2003, 213–233.Google Scholar
Bagnato, E, Gilardoni, C, Lauthier, JJ and Cremonte, F (2022) Paramonostomum deseado n. sp. (Digenea: Notocotylidae) parasitizing the South American Black Oystercatcher and their atypical life cycle from the Patagonian coast. Parasitology 149, 1642–1651.10.1017/S0031182022001159CrossRefGoogle Scholar
Bennett, J, Poulin, R and Presswell, B (2022a) Annotated checklist and genetic data for parasitic helminths infecting New Zealand marine invertebrates. Invertebrate Biology 141, e12380.10.1111/ivb.12380CrossRefGoogle Scholar
Bennett, J, Presswell, B and Poulin, R (2022b) Biodiversity of marine helminth parasites in New Zealand: What don’t we know? New Zealand Journal of Marine and Freshwater Research 56, 175–190.10.1080/00288330.2021.1914689CrossRefGoogle Scholar
Bennett, J, Presswell, B and Poulin, R (2023) Tracking life cycles of parasites across a broad taxonomic scale in a marine ecosystem. International Journal for Parasitology 53, 285–303.10.1016/j.ijpara.2023.02.004CrossRefGoogle Scholar
Bodenhofer, U, Bonatesta, E, Horejs-Kainrath, C and Hochreiter, S (2015) msa: An R package for multiple sequence alignment. Bioinformatics 31, 3997–3999.10.1093/bioinformatics/btv494CrossRefGoogle Scholar
Brant, SV and Loker, ES (2013) Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends in Parasitology 29, 449–459.10.1016/j.pt.2013.06.004CrossRefGoogle ScholarPubMed
Brant, SV, Loker, ES, Casalins, L and Flores, V (2017) Phylogenetic placement of a Schistosome from an unusual marine snail host, the false limpet (Siphonaria lessoni) and gulls (Larus dominicanus) from Argentina with a brief review of marine Schistosomes from snails. Journal for Parasitology 103, 75–82.10.1645/16-43CrossRefGoogle ScholarPubMed
Bretos, M and Chihuailaf, RH (1993) Studies on the reproduction and gonadal parasites of Fissurella pulchra (Gastropoda: Prosobranchia). The Veliger 36, 245–251.Google Scholar
Cable, RM and Peters, LE (1986) The cercaria of Allocreadium ictaluri Pearse (Digenea: Allocreadiidae). The Journal of Parasitology 72, 369–371.10.2307/3281675CrossRefGoogle Scholar
Carson, S and Morris, R (2017) Collins Field Guide to the New Zealand Seashore. Auckland, New Zealand: Harper Collins Publishers.Google Scholar
Ching, HL and Grosholz, E (1988) Occurrence of a Metacercaria (Trematoda: Gymnophallidae) in Acmaeid gastropods, Lottia digitalis and Collisella scabra. Proceedings of the Helminthological Society of Washington 55, 104–105.Google Scholar
Cremonte, F, Pina, S, Gilardoni, C, Rodrigues, P, Chai, J.-Ya nd Ituarte, C (2013) A new species of Gymnophallid (Digenea) and an amended diagnosis of the genus Gymnophalloides Fujita, 1925. The Journal of Parasitology 99, 85–92.10.1645/GE-2909.1CrossRefGoogle Scholar
Davis, NE, Blair, D and Brant, SV (2022) Diversity of Trichobilharzia in New Zealand with a new species and a redescription, and their likely contribution to cercarial dermatitis. Parasitology 149, 380–395.10.1017/S0031182021001943CrossRefGoogle Scholar
Ewers, WH (1961) A new intermediate host of schistosome trematodes from New South Wales. Nature (London) 190, 283–284.10.1038/190283b0CrossRefGoogle ScholarPubMed
Feiler, K (1986) Eine neue Gymnophallus-Metacercarie und ihre Haufigkeitsverteilung in Patinigera polaris der Sudshetlands (Antarktis). Angewandte Parasitologie 27, 227–240.Google Scholar
Firth, LB, Grant, LM, Crowe, TP, Ellis, JS, Wiler, C, Convery, C and O’Connor, NE (2017) Factors affecting the prevalence of the trematode parasite Echinostephilla patellae (Lebour, 1911) in the limpet Patella vulgata (L.). Journal of Experimental Marine Biology and Ecology 492, 99–104.10.1016/j.jembe.2017.01.026CrossRefGoogle Scholar
Flores, K, López, Z, Levicoy, D, Muñoz-Ramírez, CP, González-Wevar, C, Oliva, ME and Cárdenas, L (2019) Identification assisted by molecular markers of larval parasites in two limpet species (Patellogastropoda: Nacella) inhabiting Antarctic and Magellan coastal systems. Polar Biology 42, 1175–1182.10.1007/s00300-019-02511-6CrossRefGoogle Scholar
Gabrielli, AF and Garba Djirmay, A (2023) Schistosomiasis in Europe. Current Tropical Medicine Reports 10, 79–87.10.1007/s40475-023-00286-9CrossRefGoogle Scholar
García-Huidobro, MR, Reyes, M, Fuentes, NC, Bruna, T, Guzmán-Rivas, F, Urzúa, Á, Pulgar, J and Aldana, M (2024) Host-parasite dialogue: Fecundity compensation mechanisms of Fissurella crassa. Frontiers in Marine Science 10:1266405.10.3389/fmars.2023.1266405CrossRefGoogle Scholar
George-Nascimento, M, Balboa, L, Aldana, M and Olmos, V (1998) The key-hole limpets Fissurella spp, (Mollusca: Archaeogastropoda) and the clingfish Sicyases sanguineus (Pisces: Gobiesocidae) are sequential hosts of Proctoeces lintoni (Digenea: Fellodistomidae) in Chile. Revista Chilena Chilena De Historia Natural 71, 169–176.Google Scholar
Geraghty, A-C (2018) Variation in Parasitism of Intertidal Invertebrates, With a Focus on Trematodes on the Southwest of Ireland. PhD thesis, School of Biological, Earth and Environmental Sciences, National University of Ireland, Cork.Google Scholar
Gilardoni, C, Di Giorgio, G, Bagnato, E, Pina, S, Rodrigues, P and Cremonte, F (2020) A potential zoonotic parasite, the digenean Gymnophalloides nacellae, on the Magellanic coast in the Southwestern Atlantic Ocean: Its life cycle and geographical distribution. Polar Biology 43, 725–734.10.1007/s00300-020-02674-7CrossRefGoogle Scholar
Gilardoni, C, Di Giorgio, G, Ituarte, C and Cremonte, F (2018) Atypical lesions and infection sites of larval trematodes in marine gastropods from Argentina. Diseases of Aquatic Organisms 130, 241–246.10.3354/dao03273CrossRefGoogle ScholarPubMed
Gilardoni, C, Etchegoin, J, Diaz, JI, Ituarte, C and Cremonte, F (2011) A survey of larval digeneans in the commonest intertidal snails from Northern Patagonian coast, Argentina. Acta Parasitologica 56, 163–179.10.2478/s11686-011-0021-2CrossRefGoogle Scholar
Horak, P, Mikes, L, Lichtenbergova, L, Skala, V, Soldanova, M and Brant, SV (2015) Avian schistosomes and outbreaks of cercarial dermatitis. Clinical Microbiology Reviews 28, 165–190.10.1128/CMR.00043-14CrossRefGoogle ScholarPubMed
Jones, MB, Marsden, ID, Holdaway, RN and Jones, MB (2005) Life in the Estuary: Illustrated Guide and Ecology. Christchurch, New Zealand: Canterbury University Press.Google Scholar
Khosravi, M, Thieltges, DW, Shamseddin, J and Georgieva, S (2022) Schistosomes in the Persian Gulf: Novel molecular data, host associations, and life-cycle elucidations. Scientific Reports 12, 13461.10.1038/s41598-022-17771-2CrossRefGoogle ScholarPubMed
Kollien, AH (1996) Cercaria patellae Lebour, 1911 developing in Patella vulgata is the cercaria of Echinostephilla patellae (Lebour, 1911) n. comb. (Digenea, Philophthalmidae). Systematic Parasitology 34, 11–25.10.1007/BF01531206CrossRefGoogle Scholar
Koppel, EM, Leung, TL and Poulin, R (2011) The marine limpet Notoacmea scapha acts as a transmission sink for intertidal cercariae in Otago Harbour, New Zealand. Journal of Helminthology 85, 160–163.10.1017/S0022149X10000404CrossRefGoogle ScholarPubMed
Laamrani, H, Boelee, E and Madsen, H (2005) Trematode infection among freshwater gastropods in Tessaout Amont irrigation system, Morocco. African Zoology 40, 77–82.10.1080/15627020.2005.11407312CrossRefGoogle Scholar
Leung, TLF, Donald, KM, Keeney, DB, Koehler, AV, Peoples, RC and Poulin, R (2009b) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: Life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research 43, 857–865.10.1080/00288330909510044CrossRefGoogle Scholar
Leung, TL, Keeney, DB and Poulin, R (2009a) Cryptic species complexes in manipulative echinostomatid trematodes: When two become six. Parasitology 136, 241–252.10.1017/S0031182008005374CrossRefGoogle Scholar
Loot, G, Aldana, M and Navarrete, SA (2005) Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conservation Biology 19, 203–212.10.1111/j.1523-1739.2005.00396.xCrossRefGoogle Scholar
López-Hernández, D, Locke, SA, ALd, Melo, Rabelo, ÉML and Pinto, HA (2018) Molecular, morphological and experimental assessment of the life cycle of Posthodiplostomum nanum Dubois, 1937 (Trematoda: Diplostomidae) from Brazil, with phylogenetic evidence of the paraphyly of the genus Posthodiplostomum Dubois, 1936. Infection, Genetics and Evolution 63, 95–103.10.1016/j.meegid.2018.05.010CrossRefGoogle ScholarPubMed
López-Hernández, D, Valadão, MC, de Melo, AL, Tkach, VV and Pinto, HA (2023) Elucidating the life cycle of opossum parasites: DNA sequences reveal the involvement of planorbid snails as intermediate hosts of Rhopalias spp. (Trematoda: Echinostomatidae) in Brazil. PloS One 18, e0279268.10.1371/journal.pone.0279268CrossRefGoogle ScholarPubMed
Lorenti, E, Brant, SV, Gilardoni, C, Diaz, JI and Cremonte, F (2022) Two new genera and species of avian schistosomes from Argentina with proposed recommendations and discussion of the polyphyletic genus Gigantobilharzia (Trematoda, Schistosomatidae). Parasitology 149, 675–694.Google Scholar
Martin, WE (1982) A renicolid trematode developing in the limpet, Collisella digitalis (Rathke, 1833). Proceedings of the Helminthological Society of Washington 49, 19–21.Google Scholar
Martin, S and Vazquez, R (1984) Biology and behaviour of the cercariae of a Sanguinicola sp. in the river Cilloruelo (Salamanca, Spain). Annales de parasitologie humaine et comparée 59, 231–236.10.1051/parasite/1984593231CrossRefGoogle ScholarPubMed
Martorelli, SR and Morriconi, E (1998) A new gymnophallid metacercaria (Digenea) in Nacella (P.) magellanica and N. (P.) deaurata (Mollusca, Patellidae) from the Beagle Channel, Tierra del Fuego, Argentina. Acta Parasitologica 43, 20–25.Google Scholar
Mattos, A.Cd, Boaventura, MFF, Fernandez, MA and Thiengo, SC (2013) Larval trematodes in freshwater gastropods from Mato Grosso, Brazil: Diversity and host-parasites relationships. Biota Neotropica 13, 34–38.10.1590/S1676-06032013000400003CrossRefGoogle Scholar
Mekhraliev, A (1978) Ozernaia chashechka Acroloxus lacustris (sem. Ancylidae) kak novyĭ promezhutochnyĭ khoziain trematod v SSSR [Acroloxus lacustris (fam. Ancylidae) as a new intermediate trematode host in the USSR]. Parazitologiia 12, 121–125.Google ScholarPubMed
Oliva, ME (1992) Parasitic castration in Fissurella crassa (Archaeogastropoda) due to an adult Digenea, Proctoeces lintoni (Fellodistomidae). Memórias do Instituto Oswaldo Cruz 87, 37–42.10.1590/S0074-02761992000100007CrossRefGoogle Scholar
Oliva, ME (1993) Effect of an adult trematode, Proctoeces lintoni (Fellodistomidae), on the gonadosomatic index of Fissurella limbata (Archaeogastropoda). Acta Parasitologica 38, 155–156.Google Scholar
Oliva, ME and Alvarez, C (2011) Is a vertebrate a better host for a parasite than an invertebrate host? Fecundity of Proctoeces cf lintoni (Digenea: Fellodistomidae), a parasite of fish and gastropods in northern Chile. Parasitology Research (1987) 109, 1731–1734.10.1007/s00436-011-2489-yCrossRefGoogle ScholarPubMed
Oliva, M and Diaz, M (1988) Quantitative aspects of the infection by Proctoeces humboldti (Trematoda: Fellodistomidae) in the key-hole limpet Fissurella crassa (Mollusca: Archaeogastropoda). Revista Chilena De Historia Natural 61, 27–33.Google Scholar
Oliva, ME and Diaz, MA (1992) An ecological approach to the study of infection of Proctoeces lintoni (Digenea, Fellodistomidae) in the key hole limpet, Fissurella limbata Sowerby, 1835 (Archaeogastropoda) from northern Chile. Acta Parasitologica 37, 115–118.Google Scholar
Oliva, ME and Huaquin, LG (2000) Progenesis in Proctoeces lintoni (Fellodistomidae), a parasite of Fissurella crassa (Archaeogastropoda) in a latitudinal gradient in the Pacific Coast of South America. The Journal of Parasitology 86, 768.10.1645/0022-3395(2000)086[0768:PIPLFA]2.0.CO;2CrossRefGoogle Scholar
Oliva, ME, Valdivia, IM, Cárdenas, L, Muñoz, G, Escribano, R and George-Nascimento, M (2018) A new species of Proctoeces and reinstatement of Proctoeces humboldti George-Nascimento and Quiroga 1983 (Digenea: Fellodistomidae) based on molecular and morphological evidence. Parasitology International 67, 159–169.10.1016/j.parint.2017.10.004CrossRefGoogle ScholarPubMed
Oliva, ME and Vásquez, AM (1999) Effects of the Digenea Proctoeces lintoni (Fellodistomidae) in the proportion of hemolymphatic cells in Fissurella crassa (Mollusca: Archaeogastropoda). Memórias do Instituto Oswaldo Cruz 94, 827–828.10.1590/S0074-02761999000600021CrossRefGoogle ScholarPubMed
Oliva, ME and Vega, AA (1994) Effect of Proctoeces lintoni (Digenea) on the fecundity of Fissurella crassa (Archaeogastropoda). Memórias do Instituto Oswaldo Cruz 89, 225–225.10.1590/S0074-02761994000200020CrossRefGoogle Scholar
Oliva, MM and Zegers, LJ (1988) Variaciones intraespecíficas del adulto de Proctoeces lintoni Siddiqi & cable, 1960 (Trematoda: Fellodistomidae) en hospedadores vertebrados e invertebrados. Studies on Neotropical Fauna and Environment 23, 189–195.10.1080/01650528809360760CrossRefGoogle Scholar
Outa, JO and Avenant-Oldewage, A (2024) Underreported and taxonomically problematic: Characterization of sanguinicolid larvae from freshwater limpets (Burnupiidae), with comments on the phylogeny and intermediate hosts of sanguinicolids. Parasitology 151, 108–124.10.1017/S003118202300121XCrossRefGoogle ScholarPubMed
Outa, JO and Avenant-Oldewage, A (2025) Echinostomatids from South African freshwater limpets: Phylogenetic analyses and diagnostic morphological features for cercariae of Petasiger. Journal of Helminthology 98, e91.10.1017/S0022149X24000749CrossRefGoogle ScholarPubMed
Paradis, E (2010) pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics 26, 419–420.10.1093/bioinformatics/btp696CrossRefGoogle Scholar
Prinz, K, Kelly, TC, O’Riordan, RM and Culloty, SC (2010) Temporal variation in prevalence and cercarial development of Echinostephilla patellae (Digenea, Philophthalmidae) in the intertidal gastropod Patella vulgata. Acta Parasitologica 55, 39–44.10.2478/s11686-010-0002-xCrossRefGoogle Scholar
Quinn, EA, Thomas, JE, Malkin, SH, Eley, MJ, Coates, CJ and Rowley, AF (2022) Invasive slipper limpets Crepidula fornicata are hosts for sterilizing digenean parasites. Parasitology 149, 1–9.10.1017/S0031182022000257CrossRefGoogle ScholarPubMed
Rind, S (1984) The blood fluke Ornithobilharzia canaliculata (Rudolphi, 1819) (Trematoda: Schistosomatidae) from the gull Larus dominicanus at Lyttelton, New Zealand. Mauri Ora 11, 71–75.Google Scholar
Simon-Martin, F and Gomez-Bautista, M (1986) Preliminary SEM observations of the cercaria of a Sanguinicola sp. (Digenea: Sanguinicolidae). Annales de parasitologie humaine et comparée 61, 529–531.10.1051/parasite/1986615529CrossRefGoogle ScholarPubMed
Smith, RJ (1967) Ancylid snails as intermediate hosts of Megalodiscus temperatus and other digenetic trematodes. The Journal of Parasitology 53, 287–291.10.2307/3276577CrossRefGoogle ScholarPubMed
Smith, RJ (1968) Ancylid snails as first intermediate hosts of Lissorchis mutabile comb. n. (Trematoda: Lissorchiidae). The Journal of Parasitology 54, 283–285.10.2307/3276936CrossRefGoogle Scholar
Soleng, A, Gundersen, T and Lindstedt, H (2025) Cercarial dermatitis in Norway – an emerging zoonotic disease. Acta Parasitologica 70, 143.10.1007/s11686-025-01083-2CrossRefGoogle ScholarPubMed
Turner, HM and Beasley, SM (1982) Ancylid snails as hosts for Posthodiplostomum minimum (MacCallum, 1921) (Digenea: Diplostomatidae). Proceedings of the Helminthological Society of Washington 49, 143–143.Google Scholar
Turner, HM and Corkum, KC (1977) New snail host for Spirorchis scripta Stunkard, 1923 (Digenea: Spirorchiidae) with a note on seasonal incidence. Proceedings of the Helminthological Society of Washington 44, 225–226.Google Scholar
Valdivia, IM, Criscione, CD, Cárdenas, L, Durán, CP and Oliva, ME (2014) Does a facultative precocious life cycle predispose the marine trematode Proctoeces cf. lintoni to inbreeding and genetic differentiation among host species? International Journal for Parasitology 44, 183–188.10.1016/j.ijpara.2013.10.008CrossRefGoogle ScholarPubMed
Wood, CL, Micheli, F, Fernández, M, Gelcich, S, Castilla, JC, Carvajal, J and Boots, M (2013) Marine protected areas facilitate parasite populations among four fished host species of central Chile. The Journal of Animal Ecology 82, 1276–1287.10.1111/1365-2656.12104CrossRefGoogle ScholarPubMed
Figure 0

Table 1. Parasite prevalence from the limpets collected at five Otago Peninsula sites facing the Otago Harbour

Figure 1

Figure 1. Photomicrographs of the cercaria of Gigantobilharzia cf. patagonensis showing (A) dorsal view and (B) lateral view.

Figure 2

Figure 2. Haplotype network of Gigantobilharzia cf. patagonensis recovered from Siphonaria australis, based on cox1 sequences from five Otago Harbour sites (A) and the distribution of haplotypes by location (B). BB, Broad Bay; CB, Company Bay; LP, Lower Portobello; MB, Macandrew Bay; WR, Wellers Rock.

Figure 3

Table 2. Summary of trematode taxa reported from limpet hosts from previous publications