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Gastrointestinal Parasite Community in the Critically Endangered West African Lion

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Gastrointestinal Parasite Community in the Critically Endangered West African Lion bioRxiv preprint doi: https://doi.org/10.1101/2020.06.09.136176; this version posted June 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Manuscript currently “in review” at Ecohealth (updated June 2020) 1 Gastrointestinal parasite community in the critically endangered West African lion 2 Sofia Kruszka1, Nyeema C. Harris1,2 3 1Applied Wildlife Ecology Lab, Ecology and Evolutionary Biology, University of Michigan 4 1105 N. University Ave, Ann Arbor, Michigan 48106 5 2 Corresponding author: [email protected] (NCH) 6 7 8 Abstract 9 Large carnivores of Africa, such as lions (Panthera leo), suffer from prey depletion and habitat 10 fragmentation, that possibly impact the composition of the gastrointestinal parasite community. 11 West African lions are particularly important, as this population is critically endangered and yet 12 little is known of their gastrointestinal parasite community, which can reflect the health and 13 resilience of the host population. From fecal samples collected in the W-Arly-Pendjari (WAP) 14 transboundary protected area complex in Burkina Faso and Niger, we identified 309 oocysts of at 15 least five different species using fecal flotation and sedimentation tests. We also compared these 16 gastrointestinal parasites to other results from surveys of lions from Southern and East African 17 regions and found similar taxa to previous surveys, but lower species richness across West 18 African samples. 19 20 Word Count = 1,491 (excluding references, table and figure) 21 22 23 24 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.09.136176; this version posted June 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Manuscript currently “in review” at Ecohealth (updated June 2020) 25 Large carnivores are in jeopardy (Dirzo et al., 2014; Ripple et al., 2014). Reductions in their 26 population sizes and geographic ranges have broad ecological ramification in structuring 27 communities and ecosystem processes through consumptive and non-consumptive pathways 28 (Schmitz et al., 2010; Abdala-Roberts et al., 2019). One such consequence includes variation in 29 parasite communities emergent from changing host densities that affect disease dynamics and 30 health attributes (Colwell et al., 2012; Hatcher et al., 2012; DeCandia et al., 2019). For example, 31 fragmentation and other land degradations coupled with pollution can alter micro- and 32 macroparasite diversity (Altizer et al., 2003; Chakraborty et al., 2019), which in turn impairs the 33 host’s ability to digest nutrients and defend itself against more harmful pathogens (Amato et al., 34 2013). Therefore, we underscore that studying parasite composition and diversity are important 35 for assessing health particularly in threatened populations. 36 37 Studies of parasites in threatened carnivores provide essential ecological information that can aid 38 in promoting their recovery and persistence. In the endangered Iberian lynx (Lynx pardinus), 39 Ancylostoma tubaeforme was significantly more prevalent in juveniles than adults in Doñana 40 National Park in Southwest Spain, and the authors highlight investigating the clinical 41 consequences of hookworm burdens (Vicente et al., 2004). Intestinal parasites detected in feces 42 or other parasites found on the host can reflect nutritional requirements and dietary preferences. 43 A gastrointestinal survey of scat from endangered Croatian wolves (Canis lupus) indicated 44 consumption of fish, wild boar (Sus scrofa), roe deer (Capreolus capreolus), and deer (Cervus 45 elaphus) based on the detection of Diphyllobothrium sp. and Opisthorchis sp. helminths and a 46 high prevalence of Sarcocystis sp. protozoa (Hermosilla et al. 2017). In a survey of ectoparasites 47 for endangered black-footed ferrets (Mustela nigripes) in South Dakota, Harris and colleagues bioRxiv preprint doi: https://doi.org/10.1101/2020.06.09.136176; this version posted June 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Manuscript currently “in review” at Ecohealth (updated June 2020) 48 (2014) observed parasites associated with common prey species including prairie dogs (Cynomys 49 sp.). 50 51 Africa’s iconic apex predator, the African lion (Panthera leo), faces a tenuous future with 52 persistent threats from prey depletion, human conflict, and habitat loss (Bauer et al., 2015). As 53 such, different populations may harbor a unique parasite community with varying implications 54 for the host’s health and spatial patterns of biodiversity, more broadly. To date, several studies 55 have investigated intestinal parasites found in feces from free-ranging lions in East and South 56 Africa. (Müller-Graf 1995; Berensten et al. 2012; Lajas et al., 2015). Here, we present the first 57 survey of the gastrointestinal parasite community for lions in West Africa. This critically 58 endangered population now occupies only 1% of historic range and continues to decline 59 (Henschel et al., 2014). Our work: 1) validates methods to confirm host identity from fecal 60 samples through kit and primer testing; 2) describes the gastrointestinal parasite community of 61 lions in West Africa; and 3) conducts regional comparisons of the gastrointestinal community 62 across lion populations through literature searches. Overall, we expect a parasite community 63 comprised of generalist parasites for West African lions due to their lower population sizes and 64 increased vulnerability to extinction. 65 66 Specifically, we investigated the gastrointestinal parasites of lions in the largest West African 67 population located in the W-Arly-Penjari (WAP) transboundary protected area complex. WAP is 68 a UNESCO World Heritage site and the largest protected area complex in West Africa, 69 comprising 26,515 km2 across Niger, Benin, and Burkina Faso. Lions coexist with other large 70 carnivores, namely spotted hyenas (Crocuta crocuta) and leopards (Panthera pardus) and a bioRxiv preprint doi: https://doi.org/10.1101/2020.06.09.136176; this version posted June 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Manuscript currently “in review” at Ecohealth (updated June 2020) 71 myriad of ungulate prey in a network of national parks and hunting concessions (Mills et al., 72 2020). However, human pressures persist, as livestock grazing is pervasive, which may 73 exacerbate disease risks for sympatric wildlife (Harris et al., 2019). 74 75 From 2016-2018, we collected feces presumed to be lion in WAP and preserved samples in 76 ethanol (EtOH), N,N-diethyltryptamine (DET) buffer, or RNAlater for subsequent molecular 77 confirmation and analysis. We extracted DNA by testing protocols from three different 78 manufacturer kits: Qiagen© QIAmp (MoBio) PowerFecal DNA Kit, MP© FastDNA SPIN Kit 79 for Feces, and Qiagen© QIAmp DNA Stool Mini Kit. DNA were amplified through PCR using 80 three different primers for target genes: 16S (Tessler et al., 2017), 12S (Kitano et al., 2007), and 81 CytB (Kocher et al., 1989; Farrell et al., 2000). Samples were then matched to known sequences 82 in the NCBI database with 98% or higher identity and 90% or higher query cover being 83 confirmed as African lion. We used 2g of feces for fecal flotation tests using a ZnSO4 solution 84 diluted to a specific gravity of 1.2 with centrifugation to isolate and observe lighter intestinal 85 parasites such as nematodes and cestodes. Additionally, to detect heavier parasites such as 86 trematodes, we used sedimentation test in ZnSO4 solution without centrifugation. We used 87 measurements obtained through microscopy and morphology described by Zajac et al (2012) to 88 complete identifications. 89 90 We conducted a literature search through Web of Science to compile known gastrointestinal 91 parasites reported from wild, free-ranging African lions. Keywords included: “gastrointestinal”, 92 “helminth”, “macroparasite”, “gut”, “parasite”, “disease”, “Panthera leo”, and “African lion”. 93 We filtered search results to remove any experimental manipulations or studies occurring in bioRxiv preprint doi: https://doi.org/10.1101/2020.06.09.136176; this version posted June 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Manuscript currently “in review” at Ecohealth (updated June 2020) 94 captive populations. From resultant papers, we also conducted backwards and forward searches 95 to identify any additional gastrointestinal papers found for African lions. 96 97 Of the three extraction kits tested, we recommend the Qiagen © QIAmp DNA Stool kit, which 98 required the least amount of sample and was relatively easy to train personnel to implement. Of 99 the three universal genes, the 16S primers produced the highest quality amplicons, allowing for 100 the highest percent of host identifications for the Qiagen © QIAmp DNA Stool kit (85%). We 101 found CytB performed the worst in amplification of lion samples across all kits with only 11- 102 22% confirmation of lion samples. 103 104 We identified 309 oocysts of at least five different gastrointestinal
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