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International Journal for Parasitology: Parasites and Wildlife logoLink to International Journal for Parasitology: Parasites and Wildlife
. 2025 Aug 28;28:101130. doi: 10.1016/j.ijppaw.2025.101130

Disproportionate infection by Eustrongylides sp. (Nematoda: Dioctophymatoidea: Dioctophymatidae) in the imperiled Harter's watersnake, Nerodia harteri

Cory C McKinstry 1, Wesley J Neely 1, David Rodriguez 1,⁎
PMCID: PMC12433484  PMID: 40955297

Abstract

Describing host-parasite dynamics in natural systems is a priority for hosts of conservation concern. Harter's watersnake (Nerodia harteri ssp.) is one such species, endemic to north-central Texas and impacted by habitat alteration, low genetic diversity, and emerging infectious diseases. In this study, we report new records of Eustrongylides sp. infections in three watersnake species (N. harteri ssp., N. erythrogaster, and N. rhombifer) from five artificial reservoirs in the Brazos and Colorado River watersheds in north-central Texas. Nematodes were contained within subcutaneous nodules on the midbody of sampled snakes, and we quantified nodule presence as a proxy for infection prevalence. From seven individuals, we extracted nematodes from nodules for molecular analysis. Phylogenetic analyses on the mitochondrial cytochrome c oxidase subunit I and 18S rRNA genes of excised nematodes confirmed the identity as Eustrongylides sp. and resolved our samples into a single well supported clade divergent to previously accessioned lineages from Asia. The imperiled N. harteri had a higher risk of infection than sympatric watersnakes. Snakes were more frequently infected in Lake Granbury, a stronghold for N. harteri. Though observed infection rates were low, Eustrongylides sp. infections can induce severe pathologic responses in intermediate hosts, and our findings highlight the need for assessments of fitness implications and further parasitological surveillance in N. harteri to inform management.

Keywords: Helminths, Host-parasite dynamics, COI, 18S, Harter's watersnake, Serpentes

Graphical abstract

Image 1

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Highlights

  • •

    Subcutaneous nodules in north-central Texas snakes contained nematodes.

  • •

    Molecular analyses identified nematodes as a Eustrongylides sp.

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    Eustrongylides samples from Texas were divergent to samples from Asia.

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    Infection prevalence varies significantly between reservoirs.

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    The imperiled species Nerodia harteri had higher infection rates than congeners.

1. Introduction

Nematodes of the genus Eustrongylides ((Jägerskiöld, 1909); Nematoda: Dioctophymatidae) are cosmopolitan parasites often found in wetland habitats (Honcharov et al., 2022). Species in this genus are transmitted through the trophic chain, using oligochaetes as a first intermediate host, fish, amphibians and reptiles as second or third intermediate hosts, and piscivorous birds as definitive hosts (Friend et al., 1999; Karmanova, 1986; Measures, 1988; Melo et al., 2016; Spalding et al., 1993). Infection by Eustrongylides spp. can cause negative impacts on hosts, leading to inflammation, septicemia, and occasional mass mortality events in birds (Dezfuli et al., 2015; Wiese et al., 1977) and severe granulomatous inflammatory responses in intermediate hosts (Coyner et al., 2001; Guagliardo et al., 2019; Mihalca et al., 2007).

Owing to their broad distribution and complex life cycles, host-parasite dynamics of Eustrongylides spp. are poorly understood for several host taxa and geographic regions. While studies from South America, North America, Europe, and Australia, have reported larval Eustrongylides in piscivorous herpetofauna (Bursey, 1986; Jones, 1978; McAllister et al., 2015; Veiga Pereira et al., 2021; Yildirimhan et al., 2007), only one record of Eustrongylides infection exists from reptiles in Texas, a single larval specimen infecting Thamnophis proximus orarius from Harris County (McAllister et al., 2015). However, many snake taxa may act as hosts of this genus in Texas snake communities, and previous work has documented susceptibility to infection in captive individuals of Agkistrodon contortrix, Coluber constrictor, Masticophis flagellum, Pituophis melanoleucus, and Thamnophis sirtalis (Lichtenfels and Lavies, 1976; Winsor, 1948). Additionally, wild Nerodia spp. have suffered from severe Eustrongylides infections in Virginia, though no such infections have been reported in the common Nerodia species native to Texas (Bursey, 1986).

Here, we document new host records of Eustrongylides sp. in wild Nerodia rhombifer, Nerodia erythrogaster, and both subspecies of Nerodia harteri (N. h. harteri and N. h. paucimaculata), a Texas endemic currently considered threatened by the Texas Parks and Wildlife Department (State Wildlife Action Plan: Texas, 2023 Comprehensive Revision, 2023). Specifically, we detected parasite infection through the presence of nodules on the body of infected snakes and used molecular techniques to identify nematodes excised from nodules. This work expands our understanding of Eustrongylides host use and life cycle, revealing high prevalence of a previously undocumented helminth in imperiled populations of N. harteri.

2. Material and methods

2.1. Specimen collection and nodule detection

For four weeks in September and October 2023, four weeks in April and May 2024, and four weeks in September and October 2024, we surveyed N. harteri (N. h. harteri and N. h. paucimaculata), N. erythrogaster, and N. rhombifer populations occupying reservoirs in the Brazos and Colorado River watersheds. Surveys were conducted at seven reservoirs across the two drainages in central Texas: Lake Granbury, Possum Kingdom Lake, Lake Fort Phantom Hill, and Lake Stamford in the Brazos drainage and Lake O.H. Ivie, Ballinger City Lake, and E.V. Spence Reservoir in the Colorado drainage (Fig. 1). All sites were surveyed twice during each four-week sampling effort. We captured snakes using visual encounter surveys and partially submerged minnow traps, and subsequently collected morphometric data and PIT tagged unique individuals to identify recaptures. We quantified the presence of subcutaneous nodules, granulomatous capsules surrounded by an outer fiber layer and containing one or more nematodes, on the body of Nerodia spp. Nodules were identified as firm, oval-shaped swellings roughly 5–20 mm in length in the lateral and dorsal regions of the midbody. These nodules show slight mobility upon palpitation and were typically around lateral regions of the midbody.

Fig. 1.

Fig. 1

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Map of survey locations for subcutaneous nodules in Nerodia spp. in north-central Texas, USA. White circles represent locations where captured snakes were surveyed for nodule presence and red triangles indicate locations where a nematode was excised from a nodule.

From seven snakes captured at O.H. Ivie (n = 1) and Granbury (n = 6) reservoirs, we collected a single nematode from subcutaneous nodules characteristic of Eustrongylides infection (Table 1). Hosts of collected nematodes were non-neonates with masses ranging from 45.3 to 194.4 g. Excised specimens were placed in a 1.5 mL screwcap tube with 70–95 % ethanol, then stored in a refrigerator at 4 °C. Snake capture and processing was approved by the Texas State University Institutional Animal Care and Use Committee under Animal Use Protocol 8246 and collections were carried out under Texas Parks and Wildlife Department permit number SPR-0823-101.

Table 1.

Accession number, host species, and geographic origin of parasite taxa used for phylogenetic comparisons within this study. An asterisk indicates that the information is not available.

GenBank Accession No. Target Locus Molecular ID Host Species Locality Study
PV423508 18S Eustrongylides sp. Nerodia rhombifer Granbury Lake, Texas This study
PV423507 18S Eustrongylides sp. Nerodia erythogaster Granbury Lake, Texas This study
PV423506 18S Eustrongylides sp. Nerodia rhombifer Granbury Lake, Texas This study
PV423505 18S Eustrongylides sp. Nerodia erythogaster Granbury Lake, Texas This study
PV423503 18S Eustrongylides sp. Nerodia harteri harteri Granbury Lake, Texas This study
PV423504 18S Eustrongylides sp. Nerodia erythogaster Granbury Lake, Texas This study
PV423502 18S Eustrongylides sp. Nerodia harteri paucimaculata O. H. Ivie Lake, Texas This study
AY277895 18S Soboliphyme baturini Martes zibellina Kolyma Province, Russia Rusin et al. (2003)
OM772690 18S Dioctophyme renale Canis lupus familiaris Poland unpublished
LC389872 18S Dioctophyme renale Rattus norvegicus Tokyo, Japan Banzai et al. (2018)
MT241888 18S Dioctophyme sp. Felis catus Peru Gomez-Puerta et al. (2021)
PP934436 18S Eustrongylides sp. ∗ Barvi Reservoir, Mumbai, India Iqbal et al. (2024)
PP236907 18S Eustrongylides sp. Alligator sinensis Anhui Province, China Shuai et al. (2025)
PP989425 18S Eustrongylides sp. ∗ Barvi Reservoir, Mumbai, India Iqbal et al. (2024)
PP934668 18S Eustrongylides sp. ∗ Barvi Reservoir, Mumbai, India Iqbal et al. (2024)
MG696303 18S Eustrongylides sp. Channa punctata India unpublished
MG696298 18S Eustrongylides sp. Channa gachua India unpublished
PV427049 COI Eustrongylides sp. Nerodia harteri paucimaculata O. H. Ivie Lake, Texas This study
PV427044 COI Eustrongylides sp. Nerodia erythogaster Granbury Lake, Texas This study
PV427045 COI Eustrongylides sp. Nerodia rhombifer Granbury Lake, Texas This study
PV427046 COI Eustrongylides sp. Nerodia erythogaster Granbury Lake, Texas This study
PV427048 COI Eustrongylides sp. Nerodia harteri harteri Granbury Lake, Texas This study
PV427047 COI Eustrongylides sp. Nerodia erythogaster Granbury Lake, Texas This study
EU394166 COI Soboliphyme baturini Sorex unguiculatus Sakhalin Island, Sakhalin Oblast, Russia Koehler et al. (2009)
OP208291 COI Dioctophyme renale Chrysocyon brachyurus Argentina Arce et al. (2024)
OP208330 COI Dioctophyme renale Canis lupus familiarus Argentina Arce et al. (2024)
MT246537 COI Dioctophyme sp. Felis silvestris catus Peru Gomez-Puerta et al. (2021)
KJ925005 COI Eustrongylides sp. Monopterus albus China unpublished
MK013341 COI Eustrongylides excisus Sander lucioperca Turkey Pekmezci and Bolukbas (2021)
GQ215580 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215581 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215582 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215583 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215584 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215585 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215586 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215587 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215588 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215589 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215590 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215591 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215592 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215593 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215594 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215595 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215596 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215597 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215598 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215599 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215600 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215601 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215602 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215603 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215604 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215605 COI Eustrongylides sp. Odontobutis obscura China Xiong et al. (2013)
GQ215640 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215641 COI Eustrongylides sp. Monopterus albus China Xiong et al. (2013)
GQ215642 COI Eustrongylides sp. Pelteobagrus fulvidraco China Xiong et al. (2013)
GQ215643 COI Eustrongylides sp. Pelteobagrus fulvidraco China Xiong et al. (2013)
GQ215644 COI Eustrongylides sp. Siniperca chuatsi China Xiong et al. (2013)
GQ215645 COI Eustrongylides sp. Coila nasus China Xiong et al. (2013)
GQ215646 COI Eustrongylides sp. Acanthogobius flavimanus China Xiong et al. (2013)
GQ215647 COI Eustrongylides sp. Acanthogobius flavimanus China Xiong et al. (2013)
GQ215648 COI Eustrongylides sp. Acanthogobius flavimanus China Xiong et al. (2013)
GQ215649 COI Eustrongylides sp. Acanthogobius flavimanus China Xiong et al. (2013)
GQ215650 COI Eustrongylides sp. Channa argus China Xiong et al. (2013)
GQ215651 COI Eustrongylides sp. Channa argus China Xiong et al. (2013)
GQ215652 COI Eustrongylides sp. Channa argus China Xiong et al. (2013)
GQ215653 COI Eustrongylides sp. Channa asiatica China Xiong et al. (2013)
GQ215654 COI Eustrongylides sp. Coila nasus China Xiong et al. (2013)
GQ215655 COI Eustrongylides sp. Coila nasus China Xiong et al. (2013)
GQ215656 COI Eustrongylides sp. Coila nasus China Xiong et al. (2013)
GQ215657 COI Eustrongylides sp. Hemibarbus maculatus China Xiong et al. (2013)
GQ215658 COI Eustrongylides sp. Hemibarbus maculatus China Xiong et al. (2013)
GQ215659 COI Eustrongylides sp. Elopichthys bambusa China Xiong et al. (2013)
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2.2. Statistical analysis

Using nodule presence as a proxy of parasite occurrence, we calculated the prevalence and binomial 95 % confidence intervals (95 % CI) of nodules for each host species and sampling locality. We used logistic regression with Firth's bias correction to estimate whether nodule prevalence differed between these groups. Nodule prevalence was modeled as a binary response variable using a ‘logit’ link function. For predictors showing evidence of an effect on the model, subsequent pairwise comparisons were assessed using the package “emmeans” (Lenth, 2025). In statistical analyses, we only included samples from Lake Granbury and Possum Kingdom Lake, two reservoirs where we consistently documented nodule occurrence and represented the majority of N. harteri captures (95/103, 92.2 %). For snakes that were captured more than once, we included only assessment data from the initial capture. We assessed statistical significance at p = 0.05 and conducted all statistical analyses in JMP Pro version 17 (SAS Institute Inc. , 2021) and R version 4.2.2 (R Core Team, 2022).

2.3. Molecular identification

We extracted DNA from the midsection of seven nematodes (Fig. 2C) using the GeneJET Genomic DNA Purification Kit (Thermo Scientific) following a modified version of the manufacturer's protocol with an incubation time of 2 h and a final elution volume of 100 μL. For genetic identification, we amplified a portion of the nuclear 18S rRNA gene and the mitochondrial cytochrome c oxidase subunit I (COI) gene using the extracted DNA as a template for PCRs. Previous studies have demonstrated the effectiveness of such molecular genetic markers for larval nematode identification (Gasser and Hoste, 1995; Xiong et al., 2013; Zhang et al., 2021). We visualized amplicons on a 1 % Tris-Acetate-EDTA (TAE) agarose gel to confirm DNA amplification, then performed purification using EMnetic PCR Cleanup Kit (Beckman Coulter). For the 18S rRNA gene, we used primers Nem_18S_F (5′-CGCGAATRGCTCATTACAACAGC-3′) and Nem_18S_R (5′-GGGCGGTATCTGATCGCC-3′) (Floyd et al., 2005) to amplify DNA from all seven excised individuals. For the COI gene, we used primers L6625 (5′-TGRTTYTTYGGNCAYCC-3′) and H7005 (5′-ACNACRTARTANGTRTCRTG-3′) (Hafner et al., 1994) to amplify the region in six individuals. PCR reaction mixes (12.5 μL) contained 6.25 μL of DreamTaq MasterMix (Themo Scientific), 0.125 μl of forward and reverse primer (10 μM) each, 0.5 μL of MgCl2 (25 mM), 5.0 μL of ddH2O, and 0.5 μL of template DNA. We ran PCR reactions in duplicate on a Mastercycler® thermal cycler (Eppendorf), following a program consisting of two cycle sets. The first set of 20 cycles includes 30s denaturation at 94 °C, 30s annealing at 55 °C (−1 °C per cycle), and 45s extension at 72 °C. The second set of 14 cycles includes 30s denaturation at 94 °C, 30s annealing at 45 °C, and 45s extension at 72 °C. We conducted sequencing on a MinION 10.4.1 flow cell (Oxford Nanopore Technologies) following the Ligation sequencing amplicons – Native Barcoding Kit 96 V14 (SQK-NBD114.96) protocol. We imported raw demultiplexed reads into Geneious version 9.1.6 and generated consensus sequences for each individual with the ‘De Novo Assemble’ option using default parameters for the ‘Geneious’ assembler under the ‘Medium Sensitivity/Fast’ setting.

Fig. 2.

Fig. 2

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Representative images of subcutaneous nodules in Nerodia harteri harteri (A and B). An excised Eustrongylides sp. nematode (C) and a partially excised Eustrongylides nematode (D) from Nerodia rhombifer.

We inferred a phylogenetic tree to evaluate the relationship of our collected nematodes to representative members of the family Dioctophymatidae available on GenBank (Table 1). We aligned reference sequences to those from our samples using the MAFFT web server (Katoh et al., 2019), then trimmed the alignments (941 bp for 18S and 381 bp for COI) and calculated pairwise distances in MEGA version 11 (Tamura et al., 2021). Lastly, we constructed maximum likelihood phylogenetic trees using the IQ-Tree web server (Trifinopoulos et al., 2016) with 10,000 ultrafast bootstrap replicates (Minh et al., 2020).

3. Results

We captured 551 snakes and documented nodule presence on individuals at five of the seven reservoirs (i.e. O.H. Ivie, Ballinger, E.V. Spence, Granbury, and Possum Kingdom). For assessments of nodule prevalence, we compared 332 individuals collected at Lake Granbury and Possum Kingdom Lake, including 98 N. harteri harteri (Granbury, n = 23; Possum Kingdom, n = 75), 111 N. erythrogaster (Granbury, n = 70; Possum Kingdom, n = 41), and 123 N. rhombifer (Granbury, n = 73; Possum Kingdom, n = 50). We estimated nodule prevalence at 18.4 % (95 % CI: 11.3–27.5 %), 7.2 % (95 % CI: 3.2–13.7 %), and 4.1 % (95 % CI: 1.3–9.2 %) for N. harteri, N. erythrogaster, and N. rhombifer, respectively. Our regression analysis revealed that nodules were significantly different between species and geographic localities (Fig. 3), and post-hoc tests confirmed that nodules were more prevalent on N. harteri than congeners (N. harteri/N. rhombifer; odds ratio = 11.23, SE = 9.02, p = 0.008, N. erythogaster/N. harteri; odds ratio = 0.13, SE = 0.10, p = 0.027), as well as on individuals from Lake Granbury than Possum Kingdom Lake (odds ratio = 11.5, SE = 8.32, p = 0.001).

Fig. 3.

Fig. 3

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Variation in nematode infection between host species and locality at statistically analyzed reservoirs in Texas, USA. Bars show nodule prevalence ± standard error of host species and are grouped according to the two reservoirs with the majority of N. harteri samples.

Nematodes were excised from three N. erythrogaster, two N. rhombifer, and a N. harteri harteri at Granbury Lake, as well as a N. h. paucimaculata from Lake O.H. Ivie. All excised parasites were encapsulated and alive. Nematodes were red or pink in color and coiled within the nodule. Molecular analyses revealed that the specimens clustered into a moderately well-supported monophyletic clade with other Eustrongylides (Bootstrap Support, BS = 80 for 18S and BS = 87 for COI). Both 18S and COI trees grouped our samples into a distinct clade within the larger Eustrongylides clade, with relatively high levels of sequence divergence between this and other Eustrongylides clades (18S: 0.6–3.1 %; COI: 30.2–36.0 %), but relatively low sequence divergence within the Texas clade (18S: 0-0 %, COI: 0–0.01 %, Fig. 4). Newly generated sequences were accessioned in GenBank: PV423502-PV423508 (18S) and PV427044-PV427049 (CO1) (see Table 1 for details).

Fig. 4.

Fig. 4

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Phylogeny of collected parasites using the ribosomal 18S gene and mitochondrial cytochrome oxidase 1 gene. Colors indicate the host taxa (i.e., reptile, fish, mammal, or unreported) and sequences generated by this study are indicated by a star. Major Eustrongylides clades are indicated by vertical black bars, and maximum likelihood bootstrap values are shown at the corresponding nodes (10,000 replicates), with values under 80 % removed.

4. Discussion

Assessing infection dynamics for species of conservation concern is essential to understand the breadth of risks that these species are facing (McCallum and Dobson, 1995). Our study expands the known host range of Eustrongylides spp. to include N. harteri, a threatened species in Texas (State Wildlife Action Plan: Texas, 2023 Comprehensive Revision, 2023), as well as two wide ranging sympatric congeners, N. erythrogaster and N. rhombifer. Visual assessments of nodule prevalence suggest variation in infection prevalence, indicating that N. harteri exhibits higher rates of infection than sympatric congeners, particularly at Lake Granbury, which was shown to be a stronghold for this imperiled species in a previous study (Harding et al., 2022). Molecular analyses confirmed the identity of these nodule-forming nematodes within the genus Eustrongylides and revealed genetic divergence from previously sequenced specimens accessioned in GenBank (Fig. 4). Our findings demonstrate the complexity of host-parasite relationships and underscore the need for further research on the ecology and taxonomy of this genus in North American snake populations, raising timely considerations for conservation efforts such as captive breeding and reintroduction programs.

Eustrongylides spp. are generalist parasites with a high level of ecological plasticity allowing them to use many different hosts and habitats (Honcharov et al., 2022). Despite this, our results indicate that across this range of viable hosts, there are geographic and taxonomic associations for infection. Variation in natural histories may drive infection differences between taxa, with species predating on oligochaete-eating fish having an increased risk of exposure and infection with Eustrongylides spp. (Coyner et al., 2003). Nerodia harteri is one such dietary specialist, feeding almost exclusively on small fish, whereas congeners N. rhombifer and N. erythrogaster are more generalist and prey on larger fish and anurans, respectively (Greene et al., 1994; Mushinsky and Hebrard, 1977; Mushinsky et al., 1982; O'Brien and Evermann, 1988; Rodriguez et al., 2012). Alternatively, N. harteri, N. rhombifer, and N. erythrogaster may exhibit differential immunogenetic resistance to parasitism. While our comparative understanding of immune processing is limited, some Nerodia species appear to vary in their susceptibility to a fungal pathogen, Ophidiomyces ophidiicola (Haynes et al., 2020), suggesting innate differences in immune response to infectious agents. Inbreeding depression may limit the genetic resistance of N. harteri to infection, as they appear to have small population sizes in isolated reservoir populations, particularly at Lake Granbury (O'Brien and Evermann, 1988; Rodriguez et al., 2012). Additional data on host immunogenetics (e.g., Major Histocompatibility Complex gene diversity) are still needed to parse out these effects.

Across sites, the prevalence of Eustrongylides sp. seems to vary greatly. While some comprehensive surveys of wild populations report extremely high prevalences (Yermolenko et al., 2022), others report no infection despite large sampling efforts, including surveys of 46 watersnakes in Alabama, 202 watersnakes in Louisiana, 31 watersnakes in North Carolina, and 20 watersnakes in Ohio (Collins, 1969; Detterline et al., 1984; Fontenot and Font, 1996; Gibson and Rabalais, 1973). In this study, we found that nodules were more prevalent in snakes at Lake Granbury than at Possum Kingdom Lake, suggesting the potential for variable parasite prevalence within a single river drainage. Interestingly, previous studies of E. ignotus have indicated that highly disturbed sites have increased prevalences of this nematode (Hirshfield et al., 1983; Spalding et al., 1993), as organic enrichment and thermal discharge create conditions favorable for rapid population growth and sustained high densities of intermediate hosts (Frederick et al., 1996). Lake Granbury is distinctively more urbanized than Possum Kingdom Lake (Alsulaiman, 2017), which may account for the higher prevalence of Eustrongylides parasites and sheds light on how habitat modification may indirectly pose threats to host species by increasing exposure or susceptibility to parasite communities.

While impacts of Eustrongylides infection on snake fitness are not well understood, studies have reported that these nematodes can have severe pathologic or fatal effects on intermediate hosts, and parasite encapsulation is known to induce eosinophilia associated tissue responses such as inflammation and necrosis in snakes (Bursey, 1986; Mihalca et al., 2007). In one study, Mihalca et al. (2007) described parasitic granulomas surrounding nematode larvae on the organs of Natrix tessellate, and Lichtenfels and Lavies (1976) reported mortality due to high Eustrongylides loads in seven of 20 captive T. sirtalis, though no histopathologic evaluation was completed. We speculate that the parasitic loads of snakes captured in this study were relatively low, as we did not observe greater than four nodules on any single individual. Other studies have reported far greater nodule loads, with one study reporting up to 22 nodules visible on a single N. sipedon (Bursey, 1986). Perhaps due to a low parasitic load in captured individuals, we did not observe any noticeable behavioral or pathological effects in infected snakes, though such effects were not systematically evaluated. Despite a lower number of nodules per individual, infection prevalence is likely underreported in this study as only nematodes in visible subdermal nodules were scored, and worms in the coelomic cavity, musculature, or deeper tissues remain undocumented. Further, all removed parasites were encapsulated and alive; although unencapsulated, encapsulated and dead, and encapsulated and sclerotic nematodes likely also occur in Brazos reservoir snake communities due to the frequency of apparent infection (Bursey, 1986).

It is well documented that parasites have a direct impact on their hosts as agents of pathogenicity and disease vectors. Not only can parasites directly endanger the host by causing disease or compromising the immune system, mechanical abrasions created as an effect of parasite infection can facilitate secondary infection with bacterial, fungal, and viral pathogens (Oranges et al., 2022). Severe dermal lesions and scarring from encapsulated and sclerotic nematodes might pose a conservation risk to highly infected species by providing a point of entry for secondary infections, such as the fungal pathogen Ophidiomyces ophidiicola (Lorch et al., 2015, 2016) that is disproportionately prevalent in Nerodia harteri (Harding et al., 2022). Alternatively, parasites may benefit the host by priming the immune system to protect against subsequent infections or beneficially modulating host behavior (Salgame et al., 2013; Weinersmith and Earley, 2016).

More broadly, the abundance of Eustrongylides sp. in snakes may be indicative of high environmental abundance. Environments facing a high abundance of Eustrongylides may be disrupted by epizootics and large-scale mortality in piscivorous birds (Wiese et al., 1977; Xiong et al., 2009), and non-piscivorous birds may experience novel infections after preying upon infected snakes, including birds native to the Brazos and Colorado River watersheds like the Red-shouldered Hawk, Swainson's Hawk, and Loggerhead Shrike (Giovanni et al., 2007; Strobel and Boal, 2010; Tyler, 1991). Additionally, frequently captured and consumed game fish from Possum Kingdom Lake and Granbury Lake may be experiencing heavy parasite burdens, impacting human health (Beaver and Theis, 1979; Guerin et al., 1982; Narr et al., 1996; Wittner et al., 1989) and sportfishing; a $14 billion dollar industry in Texas (TPWD News Release, 2025). More research is required to determine the frequency of infection in the fish of Granbury and Possum Kingdom, lakes that are regularly stocked with game species and are commonly fished for recreation (Stocking History for Granbury; Stocking History for Possum Kingdom). Efforts to study the complete lifecycle and all potential competent hosts in an ecosystem would be similarly useful for potential mitigation strategies.

5. Conclusion

In this study, we document the presence of Eustrongylides sp. in three new host species: Nerodia harteri, N. erythrogaster, and N. rhombifer, and in watersnake populations at five of seven artificial reservoirs along the Brazos and Colorado River watersheds in Central Texas. These data improve our knowledge of host associations and geographic range for this parasite. Using nodule presence as a proxy, we further report distinct differences in infection prevalence between sites and species, and our results indicate that the imperiled species N. harteri is disproportionately infected with Eustrongylides sp. in the Brazos River system. Experimental studies in these host taxa are still needed to analyze behavioral or pathological effects of infection, and additional field surveys in Brazos and Colorado River watersheds would contribute to better estimates of infection. We expect that as helminth surveys continue in Texas herpetofaunal communities, more hosts of Eustrongylides sp. will be described. Continued monitoring in Nerodia harteri populations will further unravel the implications of Eustrongylides infections on conservation efforts for this threatened endemic, such as a captive propagation and reintroduction program initiated by the Houston Zoo in 2025. Given the multidimensional effects Eustrongylides parasites may have on host health, future research into parasite-host associations and fitness implications is essential, particularly in fauna such as reptiles which are broadly understudied for parasite infections.

CRediT authorship contribution statement

Cory C. McKinstry: Writing – review & editing, Writing – original draft, Visualization, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Wesley J. Neely: Writing – review & editing, Writing – original draft, Visualization, Validation, Methodology, Investigation, Formal analysis, Data curation. David Rodriguez: Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Resources, Project administration, Methodology, Investigation, Funding acquisition, Formal analysis, Data curation, Conceptualization.

Ethics Statement

Animal sampling was carried out under the permission of the Texas Parks and Wildlife Department (SPR-0823-101) and Texas State University's Institutional Animal Care and Use Committee (Rodriguez: 8246)

Funding

This work was supported by the Texas Comptroller of Public Accounts, USA (7549BG) and the Texas State University Run to R1 Postdoctoral Fellowship Program.

Conflicts of Interest

We declare no conflicts of interest.

Acknowledgements

We would like to thank the Brazos River Authority and the Colorado River Municipal Water District for facilitating this work, and Jacob Jackson, Paul Crump, and Nathan Rains for logistical advice. For their assistance in the field, we would like to thank Royce Voss-Heflin, Melanie Sheppard, Monica Argueta, Maria del Mar Moretta Urdiales, Toriann Rogalski, Carly Naundorff, Madison Nadler, Madison P. Gover, Maria A. Ramirez, and Elibardo Leal.

Contributor Information

Cory C. McKinstry, Email: corymckinstry0@gmail.com.

Wesley J. Neely, Email: wesleyjneely@gmail.com.

David Rodriguez, Email: drdz@txstate.edu.

Data availability

Newly generated sequence data are available from GenBank under accession numbers PV423502-PV423508 (18S) and PV427044-PV427049 (CO1). Sequence alignments used for phylogenetic analyses and raw data for statistical tests are available from https://doi.org/10.5281/zenodo.15832097.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Newly generated sequence data are available from GenBank under accession numbers PV423502-PV423508 (18S) and PV427044-PV427049 (CO1). Sequence alignments used for phylogenetic analyses and raw data for statistical tests are available from https://doi.org/10.5281/zenodo.15832097.

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