Meta-analysis of cyathostomin species-specific prevalence and relative abundance in domestic horses from 1975–2020: emphasis on geographical region and specimen collection method

Abstract

Background Cyathostomins infect virtually all horses, and concomitant infections with 10 or more species per horse is standard. Species-specific knowledge is limited, despite potential species bias in development of disease and anthelmintic resistance. This is the first meta-analysis to examine effects of geographical region and cyathostomin collection method on reported composition of cyathostomin communities. Methods Thirty-seven articles published in English in 1975 or later, in which adults of individual species were systematically enumerated, were included. Seven regions; North America, South America, eastern Europe, western Europe, northern Europe, southern Africa, and Oceania, and three cyathostomin collection methods; (i) standard necropsy recovery from the large intestine, (ii) critical test collection from post-treatment feces and necropsy, and (iii) diagnostic deworming recovery solely from post-treatment feces, were considered. Generalized mixed linear models analyzed the effects of region and collection method on species-specific prevalence and relative abundance. Species richness was analyzed by mixed linear models. Results Definitively, the most prevalent and relatively abundant species were Cylicocyclus nassatus (prevalence = 93%, relative abundance = 20%), Cylicostephanus (Cys.) longibursatus (93%, 20%), and Cyathostomum catinatum (90%, 16%). A bias toward horses with high infection intensities and cyathostomin collection from feces resulted in North American critical tests and eastern European diagnostic deworming overestimating the species-specific prevalence and underestimating the relative abundance of rare/uncommon species compared to respective intra-regional standard necropsies. North American critical tests underestimated species richness due partially to identification key errors. Inter-regional standard necropsy comparisons yielded some species-specific regional differences, including a significantly higher Cys. longibursatus prevalence and relative abundance in North America (92%, 33%) than in eastern Europe (51%, 7%) (P > 0.0001). Localization of critical tests to North America and diagnostic deworming to Eastern Europe precluded expansive ‘region by collection method’ interaction analyses. Conclusion We provide substantial data to inform study design, e.g. effect and study size, for cyathostomin research and highlight necessity for method standardization and raw data accessibility for optimal post-factum comparisons.

Species turnover between age groups of horses and positive network of co-occurrences define the structure of horse strongylid communities: a meta-analysis

“…At the anatomical scale, strongylid 15 communities are structured around positive co-occurrences fluctuating across anatomical niches. As such, our results complement and expand the past work by Bellaw and Nielsen (Bellaw and Nielsen, 2020) with additional horse-based data and different approaches and interpretations of the findings.…”

“…Reliance on this binary matrix defined at the regional level also prevented the use of other statistics like the effective number of species (Chase and Knight, 2013) or individual based rarefaction (Chase et al, 2018) to better account for differences in scales (geographical and temporal) across the considered species sets. As a result, the significant species turnover across the recovery methods that we observed as other authors (Bellaw and Nielsen, 2020) may simply reflect scale differences between studies. We took care to correct for differences in sampling effort and restricted the analysis to the same geoclimatic conditions.…”

“…At the anatomical scale, strongylid species sets. As a result, the significant species turnover across the recovery methods that we observed as other authors (Bellaw and Nielsen, 2020) may simply reflect scale differences between studies. We took care to correct for differences in sampling effort and restricted the analysis to the same geoclimatic conditions.…”

“…However, these reports remain often descriptive and limited exploration of the relationship between community structure and host and environmental variables been conducted. For instance, variation in species richness and diversity along the intestinal tract of horses has been reported (Collobert-Laugier et al, 2002;Gawor, 1995;Ogbourne, 1976) and recent meta-analysis reported the impact of parasite recovery method and geographical region on cyathostomin abundance or prevalence (Bellaw and Nielsen, 2020). These studies however did not address how community structure, richness and diversity varied with environmental factors of interest.…”

Evaluation of the nemabiome approach for the study of equine strongylid communities

“…Despite their worldwide distribution and relevance for stakeholders in the field, little knowledge has been gathered on the mechanisms driving their assemblage. Recent meta-analyses found that strongylid community structure was little affected by geo-climatic factors (Bellaw and Nielsen, 2020; Boisseau et al, 2021; Louro et al, 2021) and a few observations exist on the relationship between cyathostomin assemblage structure and environmental factors like temperature (Kuzmina et al, 2006; Nielsen et al, 2007), horse age (Bucknell et al, 1995; Kuzmina et al, 2016; Torbert et al, 1986) or the host sex (Kornaś et al, 2010; Sallé et al, 2018). The tedious and delicate process of species identification by morphological keys (Lichtenfels et al, 2008) is a major hurdle to study further the mechanisms of species assemblage, their turnover and the respective impacts of the host and their environment.…”