Jackson R. Roberts

Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites

Significance Within eastern North America, distributions of vector-transmitted haemosporidian blood parasites of birds, commonly known as “avian malaria parasites,” are associated with the distributions of their host species independently of direct effects of climate on potential vectors. Spatial analyses additionally indicated an absence of dispersal limitation for these parasites. Finally, host-breadth, ranging continuously from specialist to generalist, varies among parasite lineages and is dynamic within parasite assemblages over space and time. The distributions of avian haemosporidian parasites emphasize the ability of parasites to disperse across broad regions and to switch readily between hosts to become emerging infectious diseases. The drivers of regional parasite distributions are poorly understood, especially in comparison with those of free-living species. For vector-transmitted parasites, in particular, distributions might be influenced by host-switching and by parasite dispersal with primary hosts and vectors. We surveyed haemosporidian blood parasites (Plasmodium and Haemoproteus) of small land birds in eastern North America to characterize a regional parasite community. Distributions of parasite populations generally reflected distributions of their hosts across the region. However, when the interdependence between hosts and parasites was controlled statistically, local host assemblages were related to regional climatic gradients, but parasite assemblages were not. Moreover, because parasite assemblage similarity does not decrease with distance when controlling for host assemblages and climate, parasites evidently disperse readily within the distributions of their hosts. The degree of specialization on hosts varied in some parasite lineages over short periods and small geographic distances independently of the diversity of available hosts and potentially competing parasite lineages. Nonrandom spatial turnover was apparent in parasite lineages infecting one host species that was well-sampled within a single year across its range, plausibly reflecting localized adaptations of hosts and parasites. Overall, populations of avian hosts generally determine the geographic distributions of haemosporidian parasites. However, parasites are not dispersal-limited within their host distributions, and they may switch hosts readily.

New Genus of Blood Fluke (Digenea: Schistosomatoidea) from Malaysian Freshwater Turtles (Geoemydidae) and its Phylogenetic Position Within Schistosomatoidea

Abstract Baracktrema obamai n. gen., n. sp. infects the lung of geoemydid turtles (black marsh turtle, Siebenrockiella crassicollis [type host] and southeast Asian box turtle, Cuora amboinensis) in the Malaysian states of Perak, Perlis, and Selangor. Baracktrema and Unicaecum Stunkard, 1925 are the only accepted turtle blood fluke genera having the combination of a single cecum, single testis, oviducal seminal receptacle, and uterine pouch. Baracktrema differs from Unicaecum by having a thread-like body approximately 30−50× longer than wide and post-cecal terminal genitalia. Unicaecum has a body approximately 8−12× longer than wide and terminal genitalia that are anterior to the distal end of the cecum. The new genus further differs from all other accepted turtle blood fluke genera by having a cecum that is highly convoluted for its entire length, a spindle-shaped ovary between the cirrus sac and testis, a uterine pouch that loops around the primary vitelline collecting duct, a Laurers canal, and a dorsal common genital pore. Phylogenetic analysis of the D1–D3 domains of the nuclear large subunit ribosomal DNA (28S) revealed, with high nodal support and as predicted by morphology, that Baracktrema and Unicaecum share a recent common ancestor and form a clade sister to the freshwater turtle blood flukes of Spirorchis, paraphyletic Spirhapalum, and Vasotrema and that, collectively, these flukes were sister to all other tetrapod blood flukes (Hapalorhynchus + Griphobilharzia plus the marine turtle blood flukes and schistosomes). Pending a forthcoming emended morphological diagnosis of the family, the clade including Spirorchis spp., paraphyletic Spirhapalum, Vasotrema, Baracktrema, and Unicaecum is a likely placeholder for “Spirorchiidae Stunkard, 1921” (type genus Spirorchis MacCallum, 1918; type species Spirorchis innominatus Ward, 1921). The present study comprises the 17th blood fluke known to infect geoemydid turtles and the first proposal of a new genus of turtle blood fluke in 21 yr.

Prevalence of avian haemosporidian parasites is positively related to the abundance of host species at multiple sites within a region.

Parasite prevalence is thought to be positively related to host population density owing to enhanced contagion. However, the relationship between prevalence and local abundance of multiple host species is underexplored. We surveyed birds and their haemosporidian parasites (genera Plasmodium and Haemoproteus) at multiple sites across eastern North America to test whether the prevalence of these parasites in a host species at a particular site is related to that host’s local abundance. Prevalence was positively related to host abundance within most sites, although the effect was stronger and more consistent for Plasmodium than for Haemoproteus. In contrast, prevalence was not related to variation in the abundance of most individual host species among sites across the region. These results suggest that parasite prevalence partly reflects the relative abundances of host species in local assemblages. However, three nonnative host species had low prevalence despite being relatively abundant at one site, as predicted by the enemy release hypothesis.

Blood flukes of Asiatic softshell turtles: revision of Coeuritrema Mehra, 1933 (Digenea: Schistosomatoidea) and a new species infecting Chinese softshell turtles, Pelodiscus sinensis (Trionychidae), from Vietnam

Coeuritrema Mehra, 1933, previously regarded as a junior subjective synonym of Hapalorhynchus Stunkard, 1922, herein is revised to include Coeuritrema lyssimus Mehra, 1933 (type species), Coeuritrema rugatus (Brooks et Sullivan, 1981) comb. n., and Coeuritrema platti Roberts et Bullard sp. n. These genera are morphologically similar by having a ventral sucker, non-fused caeca, two testes, a pre-testicular cirrus sac, an intertesticular ovary, and a common genital pore that opens dorsally and in the sinistral half of the body. Phylogenetic analysis of the D1-D3 domains of the nuclear large subunit ribosomal DNA (28S) suggested that Coeuritrema and Hapalorhynchus share a recent common ancestor. Coeuritrema is morphologically most easily differentiated from Hapalorhynchus by having ventrolateral tegumental papillae and a definitive metraterm that is approximately 3-7× longer than the uterus. Coeuritrema comprises species that reportedly infect Asiatic softshell turtles (Testudines: Trionychidae) only, whereas Hapalorhynchus (as currently defined) comprises blood flukes that reportedly infect those hosts plus North American musk turtles (Sternotherus Bell in Gray) and mud turtles (Kinosternon Spix), both Kinosternidae, North American snapping turtles (Chelydridae), Asiatic hard-shelled turtles (Geoemydidae) and African pleurodirans (Pelomedusidae). Coeuritrema platti sp. n. infects the blood of Chinese softshell turtles, Pelodiscus sinensis (Wiegmann), cultured in the Da Rang River Basin (Phu Yen Province, Vietnam). It differs from C. lyssimus by having a narrow hindbody (< 1.6× forebody width), ventrolateral tegumental papillae restricted to the hindbody, a short cirrus sac (< 10% of corresponding body length), a transverse ovary buttressing the caeca, a short, wholly pre-ovarian metraterm (~ 10% of corresponding body length), and a submarginal genital pore. It differs from C. rugatus by having small ventrolateral tegumental papillae, testes without deep lobes, and a Laurers canal pore that opens posterior to the vitelline reservoir and dorsal to the oviducal seminal receptacle. The new species is only the second turtle blood fluke reported from Vietnam.

Revision and New Species of Vasotrema Stunkard, 1926 (Digenea: Schistosomatoidea): Turtle Blood Flukes of North American Softshell Turtles (Testudines: Trionychidae: Apalone spp.)

Abstract Gulf Coast spiny softshell turtles, Apalone spinifera aspera (Agassiz, 1857) (Testudines: Trionychidae) from Canoe Lake (33°47′56.16″N, 86°29′25.02″W; Springville, Alabama) and Round Lake (32°41′50.91″N, 87°14′30.39″W; Perry Lakes State Park, Marion, Alabama), were infected by V. robustum Stunkard, 1928, Vasotrema longitestis Byrd, 1939, and Vasotrema rileyae n. sp. The new species differs from its congeners by having papillate suckers, a short testis, an ovary dextral to the oviduct, and a pre-ovarian genital pore that is lateral to the ventral sucker. We studied the newly collected specimens and museum specimens of all congeners to revise the diagnosis of Vasotrema Stunkard, 1926 and redescribe and provide an updated dichotomous key to all species of the genus.

A new genus and species of turtle blood fluke (Digenea: Schistosomatoidea) from the Mekong snail-eating turtle, Malayemys subtrijuga (Schlegel & Müller) (Testudines: Geoemydidae) in Vietnam, with a reassessment of related Asiatic turtle blood flukes and molecular phylogeny

Platt sinuosus Roberts & Bullard n. g., n. sp. (type-species) infects the kidney and mesenteric blood vessels of Mekong snail-eating turtles, Malayemys subtrijuga (Schlegel & Müller), in the Mekong River Basin. Species of Platt Roberts & Bullard n. g. are unique by the combination of having a papillate ventral sucker, vasa efferentia that are dorsal to the gonads, a massive cirrus-sac that is directed anteriad or laterad, and a vitellarium that surrounds the intestinal caeca. The new species resembles Platt ocadiae (Takeuti, 1942) Roberts & Bullard n. comb. but differs from it by having an external seminal vesicle that overlaps with or is immediately posterior to the level of the ventral sucker. Seven species previously of Hapalorhynchus Stunkard, 1922 are reassigned herein to Platt: P. odhnerensis (Mehra, 1933) Roberts & Bullard n. comb.; P. yoshidai (Ozaki, 1939) Roberts & Bullard n. comb.; P. ocadiae; P. oschmarini (Belous, 1963) Roberts & Bullard n. comb.; P. sutlejensis (Mehrotra, 1973) Roberts & Bullard n. comb.; P. synderi (Platt & Sharma, 2012) Roberts & Bullard n. comb.; and P. tkachi (Platt & Sharma, 2012) Roberts & Bullard n. comb. A dichotomous key to Platt spp. is provided. Hapalorhynchus sheilae (Mehrotra, 1973) Bourgat, 1990 and Hapalorhynchus mica (Oshmarin, 1971) Bourgat, 1990 are considered as species inquirendae, and Hapalorhynchus indicus (Thapar, 1933) Price, 1934 and Hapalorhynchus macrotesticularis (Rohde, Lee, & Lim, 1968) Brooks & Sullivan, 1981 are considered as species incertae sedis. Phylogenetic analysis of the large subunit rDNA (28S) showed P. sinuosus and P. snyderi to be sister taxa distinct from a monophyletic Hapalorhynchus and Coeuritrema platti Roberts & Bullard, 2016.

Acipensericola glacialis n. sp. (Digenea: Aporocotylidae) from heart of lake sturgeon Acipenser fulvescens Rafinesque (Acipenseriformes: Acipenseridae) in the Great Lakes Basin, Lake Winnebago System, USA

AbstractAcipensericola glacialis n. sp. infects the heart of lake sturgeon, Acipenser fulvescens (Rafinesque), in the Lake Winnebago System and differs from its only congener, Acipensericola petersoni Bullard, Snyder, Jensen & Overstreet, 2008, by having a dendritic intestine, deeply-lobed testes, a post-ovarian oötype, and a common genital pore that is medial to the dextral caecum. Acipensericola petersoni has a non-dendritic intestine, testes that are not deeply lobed, an oötype that is at level of the ovary (ventral to the ovary), and a common genital pore that is dorsal to the dextral caecum. Comparison of the large (28S) and small (18S) sub-unit ribosomal DNA and internal transcribed spacer 2 (ITS2) regions between specimens of A. glacialis n. sp. and A. petersoni revealed 13 (of 1,621 nt; 99.2% similarity in the 28S), 8 (of 1,841 nt; 99.9% similarity in the 18S), and 11 (of 442 nt; 97.5% similarity in the ITS2) nucleotide differences. Collectively, these results comprise an unexpectedly high degree of morphological and molecular similarity given the geographical (Mississippi River Basin vs Great Lakes Basin) and phylogenetic (Polyodontidae vs Acipenseridae) separation of these hosts but seemingly did not reject a previous hypothesis concerning lake sturgeon dispersal from the Mississippi Refugium following the Wisconsin glaciation ~18,000 years ago. The new species is the first nominal blood fluke described from a sturgeon.

Exotic “Gill Lice” Species (Copepoda: Lernaeopodidae: Salmincola SPP.) Infect Rainbow Trout (Oncorhynchus mykiss) and Brook Trout (Salvelinus fontinalis) in the Southeastern United States

Abstract Salmincola californiensis infected 25 of 31 (prevalence 0.8; intensity 2–35 [mean 6.6 ± standard deviation 7.7; n = 25]) rainbow trout, Oncorhynchus mykiss, from a private trout farm connected to the Watauga River, North Carolina. Salmincola edwardsii infected all of 9 (1.0; 2–43 [9.3 ± 13.0; 9]) brook trout, Salvelinus fontinalis, from Big Norton Prong, a tributary of the Little Tennessee River, North Carolina. Both lernaeopodids are well-known salmonid pathogens, but neither is native to, nor has been previously taxonomically confirmed from, the southeastern United States. Herein, we (1) use light and scanning electron microscopy to identify and provide supplemental morphological observations of these lernaeopodids, (2) furnish complementary molecular sequence data from the 28S rDNA (28S), and (3) document the pathological effects of gill infections. We identified and differentiated these lernaeopodids by the second antenna (exopod tip with large [S. californiensis] vs. slender [S. edwardsii] spines; endopod terminal segment with subequal ventral processes shorter than [S. californiensis] vs. longer than or equal to [S. edwardsii] dorsal hook), maxilliped palp (length typically ≤1/3 [S. californiensis] vs. 1/3–1/2 [S. edwardsii] subchela length exclusive of claw), and bulla (sub-circular and concave on manubriums side [S. californiensis] vs. non-stellate [S. edwardsii]). Analysis of the 28S rDNA sequences confirmed our taxonomic assignments as demonstrated by 100% sequence similarity among the sympatric, morphologically-conspecific isolates. Histopathology revealed focal gill epithelial hyperplasia, obstruction of interlamellar water channels, lamellar fusion, and crypting of gill filaments. High intensity infections by either lernaeopodid are surveillance-worthy because they are potentially pathogenic to trout in the southeastern United States.

Morphological and molecular confirmation of Myxobolus cerebralis myxospores infecting wild‑caught and cultured trout in North Carolina (SE USA)

We used microscopy and molecular biology to provide the first documentation of infections of Myxobolus cerebralis (Myxozoa: Myxobolidae), the etiological agent of whirling disease, in trout (Salmonidae) from North Carolina (USA) river basins. A total of 1085 rainbow trout Oncorhynchus mykiss, 696 brown trout Salmo trutta, and 319 brook trout Salvelinus fontinalis from 43 localities across 9 river basins were screened. Myxospores were observed microscopically in pepsin-trypsin digested heads of rainbow and brown trout from the Watauga River Basin. Those infections were confirmed using the prescribed nested polymerase chain reaction (PCR; 18S rDNA), which also detected infections in rainbow, brown, and brook trout from the French Broad River Basin and the Yadkin Pee-Dee River Basin. Myxospores were 9.0-10.0 µm (mean ± SD = 9.6 ± 0.4; N = 119) long, 8.0-10.0 µm (8.8 ± 0.6; 104) wide, and 6.0-7.5 µm (6.9 ± 0.5; 15) thick and had polar capsules 4.0-6.0 µm (5.0 ± 0.5; 104) long, 2.5-3.5 µm (3.1 ± 0.3; 104) wide, and with 5 or 6 polar filament coils. Myxospores from these hosts and rivers were morphologically indistinguishable and molecularly identical, indicating conspecificity, and the resulting 18S rDNA and ITS-1 sequences derived from these myxospores were 99.5-100% and 99.3-99.8% similar, respectively, to published GenBank sequences ascribed to M. cerebralis. This report comprises the first taxonomic circumscription and molecular confirmation of M. cerebralis in the southeastern USA south of Virginia.