Larval Digeneans Research Articles

Ecological consequences of hidden pathology by larval digeneans in South American mollusks

The study of digeneans and their association with mollusks commenced in Europe and South America during the mid-19th to early 20th centuries. Digenean infestation can severely degrade host tissue, leading to diminished energy resources and eventual host mortality. However, these parasites can also induce various non-lethal effects, including changes in growth rates, survival rates, and reproductive capabilities, alongside physiological and behavioral alterations. While numerous studies have explored the ecological effects of digeneans on hosts in Europe and North America, our understanding of these dynamics in South America, particularly in first intermediate hosts, remains limited. Therefore, this paper aims to provide an overview of ecological investigations into digenean-mollusk systems in South America, emphasizing the importance of robust sampling designs and statistical analyses to address key ecological inquiries. Although fascinating examples exist of parasitism influencing different hierarchical levels of digenean-mollusk systems, particularly at the individual, population, and community levels, documentation of their ecosystem-level impacts is comparatively sparse. As South American studies of digenean-mollusk systems from an ecological perspective are still in their early stages, there is immense potential for uncovering unique ecological patterns in this largely unexplored region, propelling us toward further developmental strides in the parasite ecology.

Larval Digenean Parasitizing Amphibian Hosts from the Argentinian Chaco Region.

The diversity of larval digenetic trematodes can provide information on one or more intermediate hosts prior to maturation into the definitive host; on host activity and distribution; and in some cases, on environmental perturbations. In this context, the goal of the present study was to analyse the trematode larvae found in adult amphibians collected from the Argentinian Chaco Region. Few studies have been reported on the systematics of larval digeneans in amphibians. A total of 167 specimens of frogs (Leptodactylus macrosternum, Leptodactylus latinasus, Lepidobatrachus laevis, Lepidobatrachus llanensis and Lysapsus limellum) and toads (Rhinella bergi) were examined for larval digeneans. Frogs and toads were collected in two Argentinian ecoregions (Dry Chaco and Humid Chaco); between June 2002 and December 2019. Morphology of each taxon was studied in detail using light microscopy and scanning electron microscopy (SEM). Fourteen different taxa of the families Diplostomidae (Alariinae gen sp., Didelphodiplostomum sp., Pharingostomoides sp. and Tylodelphys sp.), Proterodiplostomidae (Heterodiplostomum lanceolatum), and Strigeidae (Strigea spp.) were found infecting the body cavity, mesentery, muscle, fluid in the spinal cord canal, and cranial cavity of amphibians. All species are described and illustrated, and their life cycles are briefly discussed. These infections provide new information on the morphology, morphometry, and composition of the diversity of mesocercariae and metacercariae in amphibians, thus contributing to the knowledge of potential intermediate hosts. In addition, our results serve as an indicator of parasite and host biodiversity in different ecoregions of the Gran Chaco.

A checklist of larval Digenea (Platyhelminthes: Trematoda) in molluscs from inland waters of Argentina: one hundred years of research.

A checklist of larval digeneans parasitising molluscs from inland waters of Argentina is presented here. Based on the bibliographical survey of 113 scientific articles and nine theses published between 1930 and 2021, 213 digeneans were found, which were distributed within 13 superfamilies and 35 families. The parasites were identified in 102 locations, encompassing eight of the sixteen biogeographical provinces in Argentina. Digeneans were found in 34 mollusc species (31 gastropods and three bivalves) belonging to 17 genera. The available data are presented for each digenean species, and included host information, localities, prevalence values, type of habitat, life cycle information (natural or experimental host), and information on material and genetic sequences deposited in repositories. Only 21.1% of individuals were identified to species level, and 8.5% to genus level. In addition, the genetic sequences of only 10 species (4.7%) were available at GenBank. This survey constitutes the first checklist of parasitic helminths in molluscs from inland waters of Argentina.

Diversity and dynamics in larval digenean assemblages parasitizing Heleobia parchappii in a freshwater shallow lake from the Southeastern Pampa plain, Argentina.

Digeneans have important roles within ecosystems; however, it is estimated that only 14% of the species have been described. Therefore, before being able to detail their role, digenean species’ identification and the diversity present in the ecosystems must be known. In this study, the diversity and the temporal-spatial dynamics of larval digeneans in the freshwater snail Heleobia parchappii were analysed in a shallow lake. Specimens of H. parchappii were collected seasonally at three points during one year and a total of 2871 molluscs were analysed. A total of 23 species of digenea were registered and both the overall prevalence and the composition of the assemblages presented temporal and spatial variations, responding to the differential environmental conditions characteristics (anthropic effect, presence of native forests, and differential use of the habitat by the definitive hosts) of three sampled sites. The assemblages of larval digenean in their first intermediate host support the idea that this area is of great importance in biodiversity, and could be endemic areas of some species of digenean that use reptiles, amphibians and bats as hosts, groups that are at risk of conservation. Protection of these environments is a fundamental pillar in the policies for the conservation of wild flora and fauna.

Morphological and molecular characterization of larval digenean trematodes (Parvatrema: Gymnophallidae) and their pathological effects on the clam Leukoma thaca (=Protothaca thaca) (Bivalvia:Veneridae) (Molina, 1782) from northern Chile.

Trematodes are one of the largest taxa of mollusk parasites. The clam Leukoma thaca is an economically exploited bivalve found along the south-eastern Pacific coast of Peru and Chile. This bivalve is parasitized by various unidentified larval stages of digeneans in the mantle, gonads and digestive gland. The aims of this study were to determine and describe the different larval stages of the digeneans based on morphological characteristics, to identify them at the species level by performing molecular analyses, and to evaluate pathologies associated with the parasites of this clam. Individuals of L. thaca were collected in San Jorge Bay (23°S), Chile, between November 2018 and February 2019. Morphological description was carried out using in vivo and fixed specimens, and analyses including histological and scanning electron microscopy were performed. Individuals were also isolated for molecular analysis using nuclear ribosomal internal transcribed spacer 1 (ITS1), including partial subunit 18S rDNA (18S) and small subunit 5.8S gene (5.8S). Morphological characteristics indicated that the metacercaria larval stage belongs to the family Gymnophallidae, genus Parvatrema, which was supported by molecular analysis. Molecular results revealed that metacercaria, sporocysts and cercaria stages found in this clam belong to the same species of Parvatrema (genetic distance 0%), evidencing that this species uses L. thaca as the first and second intermediate host. Pathologies examined in the host were similar in nature to those reported in other gymnophallids in bivalves, but high prevalence of cercariae (20%) in gonads suggested an important castrator effect on the host.

Discrimination of Red Mullet Populations (Teleostean, Mullidae) Off the Sicilian Coasts (Mediterranean Sea) on the Basis of Metazoan Parasites

Knowledge on fish stock units and their boundaries is still poor in the Mediterranean despite the relevance of this information for developing accurate stock assessment and effectively managing fisheries. The aim of this work is to identify parasite species that might serve as biological tags for discrimination of red mullet stocks Mullus barbatus and M. surmuletus, off the northern and southern coasts of Sicily (central Mediterranean). Stephanostomum sp. metacercariae were selected as good biological tags for M. barbatus and M. surmuletus. Specimens caught in the Strait of Sicily showed a high level of metacercariae infections while no infected fish was found in the Southern Tyrrhenian Sea. Furthermore, cestode larvae (order Trypanorhyncha), and adult and larval digeneans were considered suitable as biological tags for stock discrimination in M. surmuletus, presenting statistically different epidemiological levels between the two areas. Results suggest a likely occurrence of distinct populations of red mullets in two areas of the central Mediterranean on the basis of parasite infestations.

Spatio-temporal variations in larval digenean assemblages of Heleobia parchappii (Mollusca: Cochliopidae) inhabiting four human-impacted streams.

In the last years, a growing number of studies have focused on the search for biological indicators of human impact in freshwater environments. Given their susceptibility to different types of impact, larval digeneans have been considered as useful tools for the study of temporal variations in parasite communities. However, few studies have been carried out in lotic environments. For that reason, the spatio-temporal variations of the larval digenean assemblages parasitizing the gastropod Heleobia parchappii were analysed in four human-impacted streams, located on the coast of Argentina. In total, 4800 specimens of H. parchappii were collected seasonally, and 12 digenean species belonging to eight families were registered. Three of the streams showed similar species presence but, during spring and summer, the streams located within the city presented lower species presence than the streams located in the urban periphery. By contrast, the spatial prevalence values evidenced a higher variation between the environments. Streams located in the urban periphery showed higher prevalence values throughout the year, compared to those calculated for streams located within the city. The spatio-temporal variations of larval digenean assemblages parasitizing H. parchappii seem to be mainly influenced by the diversity and vagility of definitive hosts, the types of digenean life cycles and habitat characteristics. However, environmental disturbances derived from anthropogenic activities are highlighted as the probable main factors that may affect the composition and dynamic of these parasite assemblages.

Phylogenetic studies of larval digenean trematodes from freshwater snails and fish species in the proximity of Tshwane metropolitan, South Africa.

The classification and description of digenean trematodes are commonly accomplished by using morphological features, especially in adult stages. The aim of this study was to provide an analysis of the genetic composition of larval digenean trematodes using polymerase chain reaction (PCR) and sequence analysis. Deoxyribonucleic acid (DNA) was extracted from clinostomatid metacercaria, 27-spined echinostomatid redia, avian schistosome cercaria and strigeid metacercaria from various dams in the proximity of Tshwane metropolitan, South Africa. Polymerase chain reaction was performed using the extracted DNA with primers targeting various regions within the larval digenean trematodes’ genomes. Agarose gel electrophoresis technique was used to visualise the PCR products. The PCR products were sequenced on an Applied Bioinformatics (ABI) genetic analyser platform. Genetic information obtained from this study had a higher degree of discrimination than the morphological characteristics of seemingly similar organisms.

Helminth parasites of Xiphophorus birchmanni (Pisces: Poeciliidae) from two localities of the Pánuco River drainage, Mexico

Specimens of Xiphophorus birchmanni (Teleostei: Poeciliidae) (55 individuals) (Sheepshead swordtail) were collected from 2 localities in the Panuco River drainage from Hidalgo and Veracruz [at Atlatipa (n = 26) and Benito Juarez (n = 29), respectively], Mexico. The structure of the parasite communities of fish from the 2 localities was examined and compared. Helminths from 10 taxa were recovered: 6 species of larval digeneans ( Posthodiplostomum sp., Uvulifer sp., Centrocestus formosanus, Ascocotyle sp., Haplorchis pumilio , and Echinostomatidae gen. sp.); 2 adult monogeneans ( Urocleidoides vaginoclastrum and Gyrodactylus sp.); 1 larval cestode (metacestode stage; Glossocercus auritus ); and 1 larval nematode, Eustrongylides sp. Urocleidoides vaginoclastrum and C. formosanus were the most frequent and abundant species. The remaining taxa were rare and found at low mean abundance. Component community and infracommunity differences observed in this study could be attributed to abiotic and biotic environmental factors resulting from the geographic separation of these localities during the orogeny of the Sierra Madre Oriental that restricted fish to isolated localities.

Temporal variations of larval digenean assemblages parasitizing Heleobia parchappii (Mollusca: Cochliopidae) in two shallow lakes from the Buenos Aires province, Argentina

ABSTRACT The larval digenean assemblages in snail hosts are influenced by biotic and abiotic factors and by environmental disturbances due to human activities. Given their susceptibility to different types of impact, they can be useful tools for the study of temporal variations in parasite communities. The study of temporal dynamics in prevalence and species richness of larval digenean assemblages of Heleobia parchappii (D’Orbigny, 1835), in two Pampean lakes, provides a good opportunity to test the supposition that seasonal variations in digenean assemblages are determined by a series of biotic and abiotic factors that operate interdependently. To analyze the temporal variations, and to evaluate how local factors influence these digenean assemblages in Los Padres and La Brava lakes (Buenos Aires province, Argentina), 2,400 specimens of H. parchappii were collected seasonally, during one year. The digenean assemblages in Los Padres and La Brava lakes were composed of 13 and 12 species respectively. These larval digenean assemblages showed similarities in the number and in the seasonal frequency of occurrence of species (eight of which were present in both lakes). However, despite these similarities, the assemblages showed different temporal dynamics in La Brava and Los Padres lakes and, also, different correlations with the abiotic and biotic factors analyzed during this study (temperature, high of the water column and snail relative abundance). Temporal dynamics in prevalence and species richness of larval digenean assemblages of H. parchappii in both lakes seems to be influenced by a series of factors (diversity and abundance of definitive hosts, intermediate and definitive host location, snail relative abundance and anthropogenic disturbances). Our results highlight the importance of analyzing the role and interaction of local factors, especially in studies dealing with spatiotemporal fluctuations or with distance decay of similarities in species richness of parasite assemblages.

Larval digenean communities in Biomphalaria species in two contrasting wetlands from South America.

A key factor in the colonization probabilities of parasites is the host's characteristic habitat. Considering that rice fields are simple habitats compared with natural wetlands, we comparatively analyzed the composition of the cercariae communities in Biomphalaria snails in an agricultural and a nonagricultural habitat of Corrientes Province, Argentina. We collected 2998 Biomphalaria snails from November 2011 to May 2012: B. tenagophila, B. occidentalis, B. peregrina, and B. orbignyi in the nonagricultural habitat and B. straminea in the agricultural habitat. Nine cercaria species were found in the nonagricultural habitat and 12 in the agricultural habitat, with overall parasite prevalence of 9.27 and 7.69%, respectively. The overall prevalence and mean species richness of cercariae showed no significant differences between habitats. The cercariae communities of the 2 habitats showed low similarity (38%), sharing 4 species. The mean species diversity of cercariae was higher in the nonagricultural habitat. Our results suggest that rice fields provide conditions for the hosts and cercariae that are somewhat similar to those of nonagricultural wetlands, although the contrasting characteristics of habitats can influence the presence of different intermediate and definitive hosts and consequently impact parasite diversity.

Use of qPCR-Based Cercariometry to Assess Swimmer\u2019s Itch in Recreational Lakes

Swimmer’s itch (cercarial dermatitis) is a nuisance encountered by bathers and recreational water users worldwide. The condition is caused by the penetration of larval digenean trematodes (cercariae) of the family Schistosomatidae, into the skin, following their release into freshwater from pulmonate snails that serve as the intermediate hosts for these parasites. This study utilizes qPCR-based cercariometry to monitor and quantify cercariae from water samples collected at 5 lakes in northern Michigan. The resolution provided by qPCR facilitated assessment of the environmental and biological drivers of swimmer’s itch-causing cercariae concentrations, allowing us to demonstrate that cercarial abundance is greatest at the top of the water column, in locations with prevailing on- and alongshore winds.

Invasive parasites are detectable by their abundance-occupancy relationships: the case of helminths from Liza haematocheilus (Teleostei: Mugilidae)

The biogeographic patterns of abundance and prevalence of helminths from Liza haematocheilus were studied across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. Abundance-occupancy relationships (AORs) were tested for the core-satellite and enemy release (ERH) species hypotheses in eight and 14 host samples from the native and introduced host ranges, respectively. The AOR model fitted parasite data extremely well, irrespective of whether the host or the parasite species were native or invasive. Except for co-introduced monogeneans, species were less abundant and prevalent in the introduced host population than in the native one, which agrees well with the ERH. Two occupancy patterns were observed. A unimodal, right-skewed distribution of prevalence frequency was common for the acquired groups of helminth parasites in the introduced range, whereas a bimodal distribution was more common in the native range. Core species in the native range were monogeneans, adult and larval digeneans, whereas host-specific, co-introduced monogeneans were the only core species in the introduced range. Acquired grey-mullet specialists and host generalists infected only a small portion of the introduced host population with low mean abundance. These results indicate that strict host specificity, together with a direct life cycle, are the traits that enabled helminth species to entirely occupy the invasive host population. The AORs showed that parasite individuals tend to accumulate in a relatively small fraction of susceptible introduced hosts, probably as an adaptation to enhance mating opportunities, thereby providing a mechanistic explanation of the ERH. All this evidence suggests that co-introduced and acquired species use the introduced host population in very different ways. Therefore, we posit that the examination of AORs can be instrumental in understanding the role of co-introduced parasites in invasion theory.

Testing the enemy release hypothesis: abundance and distribution patterns of helminth communities in grey mullets (Teleostei: Mugilidae) reveal the success of invasive species

The abundance and aggregation patterns of helminth communities of two grey mullet hosts, Liza haematocheilus and Mugil cephalus, were studied across 14 localities in Atlantic and Pacific marine areas. The analysis matched parasite communities of (i) L. haematocheilus across its native and introduced populations (Sea of Japan and Sea of Azov, respectively) and (ii) the introduced population of L. haematocheilus with native populations of M. cephalus (Mediterranean, Azov-Black and Japan Seas). The total mean abundance (TMA), as a feature of the infection level in helminth communities, and slope b of the Taylor’s power law, as a measure of parasite aggregation at the infra and component-community levels, were estimated and compared between host species and localities using ANOVA. The TMA of the whole helminth community in the introduced population of L. haematocheilus was over 15 times lower than that of the native population, but the difference was less pronounced for carried (monogeneans) than for acquired (adult and larval digeneans) parasite communities. Similar to the abundance pattern, the species distribution in communities from the invasive population of L. haematocheilus was less aggregated than from its native population for endoparasitic helminths, including adult and larval digeneans, while monogeneans showed a similar pattern of distribution in the compared populations of L. haematocheilus. The aggregation level of the whole helminth community, endoparasitic helminths, adult and larval digeneans was lower in the invasive host species in comparison with native ones as shown by differences in the slope b. An important theoretical implication from this study is that the pattern of parasite aggregation may explain the success of invasive species in ecosystems. Because the effects of parasites on host mortality are likely dose-dependent, the proportion of susceptible host individuals in invasive species is expected to be lower, as the helminth distribution in the invasive host was featured by a higher number of uninfected hosts and a shorter distribution tail when compared with native species.

Stunting of the penis in Heleobia parchappii (Mollusca: Cochliopidae) and its relationship with parasitism.

Penis anatomy is used to discriminate species of gastropods belonging to the family Cochliopidae; however, this characteristic may be affected by the presence of parasites. To evaluate the possible effect of parasites on penis length and number of papillae in Heleobia parchappii, 195 males were collected from the Nahuel Rucá Lagoon, Argentina. Male snails were only infected by trematode digeneans (total prevalence 45.13%). Three out of 9 species of digeneans registered showed prevalence values higher than 10%: Microphallus szidati, M. simillimus, and Notocotylidae sp. 1. The penis length of non-parasitized males and those parasitized by M. szidati and M. similimus increased with increased snail length; however, this increase was lower in infected snails. In the case of snails infected with Notocotylidae sp. 1, no relationship between shell length and penis length was apparent. Differences in the life cycles of these 3 digeneans could explain the null or lower penis growth rate in relation to host body growth. In contrast, no change was observed in the number of penial papillae of H. parchappii when these snails were infected by larval digeneans compared to those that were not infected. This indicates that penial papillae may be a more stable characteristic than penis length to discriminate between species within the Cochliopidae. The study of penial papillae should be central in the taxonomy and identification of new species within the Cochliopidae, as well as in previously described species.

Larval digenean preferences in two sympatric snail species at differing tidal levels off the Atlantic coast of Patagonia.

Larval stages of the trematodes Maritrema madrynense and Hemiuroidea fam. gen. et sp. differentially parasitized Siphonaria lessonii and S. lateralis, two sympatric pulmonate snail species on the rocky intertidal shore at Puerto Deseado, south-western Atlantic coast of Patagonia, Argentina. Snail specimens were collected at two sampling sites with contrasting physical-chemical characteristics. One site, in the upper intertidal, was exposed to sewage from fish-processing plants, greater hydrodynamic forcing and desiccation, a wider temperature range, longer exposure to ultraviolet radiation and higher abundance of birds. The second site, in the lower intertidal, was generally characterized by less stressful environmental conditions. At both sites, S. lateralis showed a markedly higher density than S. lessonii (55.13 vs. 5.87 snails/m2, respectively). Despite this, the prevalence of both digeneans was higher in S. lessonii (17.37% and 3.52% for M. madrynense and Hemiuroidea, respectively) than in S. lateralis (0.09% and 0% for M. madrynense and Hemiuroidea, respectively). This study demonstrates high parasite specificity for the host. Low densities of S. lessonii are attributed to castration of parasitized hosts and reduction of their physiological condition. The prevalence and intensity of infection of both digenean parasites were higher at the more stressful, upper intertidal site, thus suggesting that a higher abundance of birds and exposure to sewage pollution may promote the transmission of trematodes.

A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta, Canada.

Digenean trematode distributions, compatibility profiles with their snail hosts, and complete life cycles remain mysteries in many parts of the world. Surveys of digenean biology and ecology provide further insight and perspective into just how incredibly diverse and important helminth parasites are in shaping local ecosystems. Past surveys have provided substantial characterizations of adult digeneans within their definitive hosts, and many now have contributed toward furthering our understanding of larval digeneans within their intermediate host communities. However, much information about the diversity of digeneans and their relationships with their snail intermediate hosts are lacking in many locations across the globe. This is certainly true in Canada, where few records related to digenean-snail relationships exist. Currently, there is a need for more information about the presence and distribution of digeneans across Canada, and how this compares to other parts of North America and beyond. To address this diversity gap in Western Canada, six lakes within central Alberta were surveyed for the presence of snails and larval digenean species and their associations. This investigation into the diversity of digeneans utilized a combined approach of morphological and molecular tools to identify 39 digenean species among five snail host species, from biweekly collections, taken over the course of 2years (2013-2014). Here, digenean-snail combinations, presence, and distribution across sampling sites and lakes are reported. Overall, this survey contributes new information toward digenean-snail compatibility, life cycles, and distribution in Northern lake ecosystems within North America.

Endogenous growth factor stimulation of hemocyte proliferation induces resistance to Schistosoma mansoni challenge in the snail host

Digenean trematodes are a large, complex group of parasitic flatworms that infect an incredible diversity of organisms, including humans. Larval development of most digeneans takes place within a snail (Gastropoda). Compatibility between snails and digeneans is often very specific, such that suitable snail hosts define the geographical ranges of diseases caused by these worms. The immune cells (hemocytes) of a snail are sentinels that act as a crucial barrier to infection by larval digeneans. Hemocytes coordinate a robust and specific immunological response, participating directly in parasite killing by encapsulating and clearing the infection. Hemocyte proliferation and differentiation are influenced by unknown digenean-specific exogenous factors. However, we know nothing about the endogenous control of hemocyte development in any gastropod model. Here, we identify and functionally characterize a progranulin [Biomphalaria glabrata granulin (BgGRN)] from the snail B. glabrata, a natural host for the human blood fluke Schistosoma mansoni Granulins are growth factors that drive proliferation of immune cells in organisms, spanning the animal kingdom. We demonstrate that BgGRN induces proliferation of B. glabrata hemocytes, and specifically drives the production of an adherent hemocyte subset that participates centrally in the anti-digenean defense response. Additionally, we demonstrate that susceptible B. glabrata snails can be made resistant to infection with S. mansoni by first inducing hemocyte proliferation with BgGRN. This marks the functional characterization of an endogenous growth factor of a gastropod mollusc, and provides direct evidence of gain of resistance in a snail-digenean infection model using a defined factor to induce snail resistance to infection.

Influence of Microphallus szidati Martorelli, 1986 (Trematoda) on the fecundity of the second intermediate host, Palaemonetes argentinus Nobili, 1901 (Decapoda: Natantia)

Fil: Merlo, Matias Javier. Consejo Nacional de Investigaciones Cientificas y Tecnicas; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Departamento de Biologia. Laboratorio de Parasitologia; Argentina

Prevalence of Haematoloechus pulcher metacercariae (Digenea: Plagiorchioidea) in the crayfish Cambarellus montezumae in Salazar Lagoon, Estado de México

Crayfish can be intermediate hosts of larval digeneans. Cambarellus montezumae is a crustacean endemic of the Mexican plateau and is part of the diet of the inhabitants of Lerma; nonetheless, this municipality lacks parasitological studies on the species of hosts. This work is an analysis of 13 samples collected monthly proceeding from the lakeshore. Two hundred and twenty one crayfish were examined externally and internally. The metacercariae number per crayfish and per anatomical unit was registered. The prevalence, intensity and abundance were recorded each month. Ninety four crayfish were parasitized by metacercariae encysted mainly in the gills. The highest prevalence was observed in March, May and June. In spite of the slight difference in abundance between females (2.6) and males (2.4), there was no significant difference (U-Mann–Whitney test). The highest parasite burden was 26, with an average of 6 metacercariae per crayfish. In addition, all specimens with a size larger than 14mm presented metacercariae, the only larval stage detected. C. montezumae could be considered a second intermediate host of the digenean Haematoloechus pulcher in the Salazar Lake in Mexico due to the prevalence and presence of this parasite throughout the year.