Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy

Abstract

Trematodes of the genus Alaria develop into an arrested stage, known as mesocercariae, within their amphibian second intermediate host. The mesocercariae are frequently transmitted to a non-obligate paratenic host before reaching a definitive host where further development and reproduction can occur. Snakes are common paratenic hosts for Alaria spp. with the mesocercariae often aggregating in the host’s tail. In the current study, we used morphological examination and molecular analyses based on partial sequences of nuclear large ribosomal subunit gene and mitochondrial cytochrome C oxidase subunit 1 gene to identify larvae in the tails of red-sided garter snakes (Thamnophis sirtalis parietalis) as mesocercariae of Alaria marcianae, Alaria mustelae, and Alaria sp. as well as metacercariae of Diplostomidae sp. of unknown generic affiliation. We assessed infection prevalence, absolute and relative intensity, and associated pathological changes in these snakes. Infection prevalence was 100% for both male and female snakes. Infection intensity ranged from 11 to more than 2,000 mesocercariae per snake tail, but did not differ between the sexes. Gross pathological changes included tail swelling while histopathological changes included mild inflammation and the presence of mucus-filled pseudocysts surrounding mesocercariae, as well as the compression and degeneration of muscle fibers. Our results indicate that mesocercariae can lead to extensive muscle damage and loss in both sexes which likely increases the fragility of the tail making it more prone to breakage. As tail loss in garter snakes can affect both survival and reproduction, infection by Alaria mesocercariae clearly has serious fitness implications for these snakes.

Current and time‐lagged effects of climate on innate immunity in two sympatric snake species

“…Snout‐to‐vent length (SVL) was also collected and can be considered a proxy for snake age since body length is correlated with age in this system (Bronikowski & Arnold, 1999). We also recorded presence/absence of tail trematode infection by looking for swelling, pinkness, or other abnormalities on the tail (Uhrig et al., 2015).…”

Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis

“…The rDNA operon of A. americana assembled from genomic data differs by 2.2-13.5% from 13 sequences from A. mustelae, A. marcianae, A. alata and three unidentified species of Alaria (comparisons of various regions of the rDNA array, limited to sequences overlapping > 500 bp, AF184263, AY222091, JF769477-8, JF769480, JF769482, JF769484, JF820605, JF820607, JF820609, KT254014, KT254021, KT254023). Notably, A. americana differs from A. marcianae by 6.1% in partial 28S rDNA (914/973 identities with KT254021-2, Uhrig et al, 2015)) and by 8.4-8.9% in partial CO1 (KT254037-9, Uhrig et al 2015).…”

“…Adults of this species occur in canid definitive hosts, while A. marcianae mainly matures in felid and mustelid hosts (Pearson and Johnson, 1988). The adult A. marcianae sequenced in Uhrig et al (2015) was collected from Taxidea taxus (Mustelidae).…”

“…In A. americana and other Alaria spp., intraspecific CO1 distances range from 0 to 2.9% and interspecific distances from 8.4 to 13.1% (total 53 CO1 sequences from A. americana, A. mustelae, and A. marcianae; A. marcianae includes Alaria sp. 2 of Locke et al (2011) as noted by Uhrig et al (2015), who recorded the sequence match but mistakenly referred to Alaria sp. 1 of Locke et al (2011)).…”

A review of the role of parasites in the ecology of reptiles and amphibians

“…cause extensive muscle damage (Uhrig et al . ). The fungal chytrid genus Batrachochytrium damages the permeable skin of amphibians, causing loss of water and electrolyte equilibrium (Voyles et al .…”