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Efficiency and composition of vertebrate scavengers at the land-water interface in the Chernobyl Exclusion Zone
Accepted Manuscript Efficiency and composition of vertebrate scavengers at the landwater interface in the Chernobyl Exclusion Zone
Peter E. Schlichting, Cara N. Love, Sarah C. Webster, James C. Beasley PII: DOI: Article Number: Reference:
S2352-2496(18)30033-8 https://doi.org/10.1016/j.fooweb.2018.e00107 e00107 FOOWEB 107
To appear in:
Food Webs
Received date: Revised date: Accepted date:
8 June 2018 4 October 2018 30 October 2018
Please cite this article as: Peter E. Schlichting, Cara N. Love, Sarah C. Webster, James C. Beasley , Efficiency and composition of vertebrate scavengers at the land-water interface in the Chernobyl Exclusion Zone. Fooweb (2018), https://doi.org/10.1016/ j.fooweb.2018.e00107
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ACCEPTED MANUSCRIPT Efficiency and composition of vertebrate scavengers at the land-water interface in the Chernobyl Exclusion Zone
Peter E. Schlichting1, Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA
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Cara N. Love, Savannah River Ecology Laboratory, Odum School of Ecology, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA
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Sarah C. Webster, Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA
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James C. Beasley, Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA 1
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Corresponding author, current address: College of Integrative Sciences and Arts, Arizona State University, Polytechnic campus, 6073 South Backus Mall, Mesa, Arizona 85212, USA
ACCEPTED MANUSCRIPT Abstract
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Scavenging increases the connectivity of food webs yet scavenging links between adjacent ecosystems are poorly characterized. Here we explored the movement of aquatic carrion into terrestrial food webs by vertebrate scavengers across two habitat types in the Chernobyl Exclusion Zone (CEZ). We used motion activated cameras to monitor experimentally placed fish carcasses to quantify the composition and efficiency of vertebrate scavengers of canal and river communities in the CEZ. We conducted 83 trials that were scavenged by 10 mammalian and 5 avian species. Species diversity, percentage consumed, scavenging efficiency, and time until scavenged differed between canal and river trials. Mesocarnivores were the predominant scavengers in both habitats, and we observed greater scavenger efficiency and higher diversity (but lower richness) among river trials. Variation in scavenging among habitats was attributed to the interplay of higher detection rates in the river habitats and differences in scavenger community, as canals intersected a greater diversity of habitat types. Our data suggest the CEZ supports a highly diverse and efficient vertebrate scavenging community with important implications for the redistribution of scavenging-derived nutrients and the connectivity of adjacent ecosystems. Future studies should focus on species-specific patterns of nutrient redistribution and ultimate carcass deposition sites to further our understanding of the mechanisms connecting aquatic and terrestrial systems via scavenging of aquatic nutrients by terrestrial scavengers.
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Keywords: aquatic-terrestrial interface, Chernobyl Exclusion Zone, fish carrion, food webs, mesocarnivore, scavenging links
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1. Introduction
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Vertebrate scavengers play an important role in maintaining healthy ecosystems and fulfill several ecological functions including the creation of biodiversity hotspots (Smith and Baco 2003; Bump et al. 2009), containment of disease (Markandya et al. 2008), and formation of critical linkages in food webs (DeVault et al. 2003; Wilson and Wolkovich 2011). The patchiness of carrion resources means there are few obligate vertebrate scavengers (Ruxton and Houston 2004), and this spatiotemporal unpredictability of carrion has important implications for promoting both scavenging species diversity and the importance of facultative scavenging (Cortés-Avizanda et al. 2012). There is growing awareness of the impact of facultative scavenging (DeVault et al. 2003; Pereira et al. 2014; Beasley et al. 2015) and including facultative scavenging in food web analyses can result in as much as a 16-fold increase in linkages (Wilson and Wolkovich 2011). The formation of these linkages results in more connected, and thus stable, food webs (Polis 1991; Polis and Strong 1996; McCann et al 1998; McCann 2000). However, many scavenging links remain poorly understood, particularly linkages involving the transfer of nutrients between adjacent ecosystems (Vander Zanden and Sanzone 2004; Beasley et al. 2012).
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Most food web studies have focused on linkages within a single ecosystem due to the inherent complexities of biological systems, yet nutrients commonly flow among ecosystems through both biotic and abiotic processes (Polis et al. 1996; Vander Zanden, and Sanzone 2004; Witman et al. 2004; Beasley et al. 2012; Benbow et al. 2018). The flow of aquatic-derived nutrients into terrestrial habitats can be detected beyond their physical boundaries (Muehlbauer et al. 2014), and the movement of aquatic nutrients by animal vectors has the potential to increase the spatial redistribution of nutrients and augment terrestrial system productivity (Nakano and Murakami 2001; Henschel 2004; Helfield and Naiman 2006; Gratton et al. 2008). Mechanisms of nutrient transfer across the land-water interface include terrestrial defecation by semi-aquatic foragers (Fariña et al. 2003; Crait and Ben-David 2007), terrestrial consumers moving aquatic resources into terrestrial systems (Rose and Polis 1998; Quinn et al. 2009), and the non-consumptive deposition of nutrients (e.g. shells, feathers) (Polis and Hurd 1995; Vander Zanden et al. 2012). Scavenging is another important mechanism facilitating the transfer of nutrients between adjoining ecosystems (Beasley et al. 2012), although inter-ecosystem linkages via scavenging have received comparatively little attention.
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Scavenging across the land-water interface has been documented in marine and freshwater systems. Allochthonous marine resources can subsidize coastal carnivores enough to yield a numerical response (Holling 1959) and sustain higher densities than inland populations (Rose and Polis 1998). Similarly, sea turtle carrion may be a key seasonal resource for numerous terrestrial mammals, reptiles, and birds (Escobar-Lasso et al. 2016). Feeding by dingos (Canis lupus dingo) on recreational fishing remains has been shown to alter their activity patterns (Déaux et al. 2018) and this common type of provisioning can have important implications for food webs (Newsome et al. 2015). At the land-ocean interface, the scavenging of fish by a diverse community suggests scavenging shapes food web dynamics by supplementing several trophic levels via facultative scavenging (Schlacher et al. 2013; Huijbers et al. 2016).
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One of the most notable examples of inter-ecosystem nutrient exchange is the annual migration of anadromous fish from pelagic to inland freshwater systems. This process deposits vast amounts of nutrients from marine ecosystems into inland riverine and stream systems, enriching those systems, as well as adjacent terrestrial ecosystems (Willson et al. 1998; Cederholm et al. 1999). While many anadromous fish carcasses are decomposed or scavenged within the aquatic system, 20-89% of salmon carcasses may become available to terrestrial scavengers (i.e. not deposited on streambed or carried downstream) and potentially transported into the adjoining terrestrial environment (Cederholm et al. 1989; Hewson 1995). This spatial redistribution of salmon carcasses by a diverse guild of terrestrial scavengers (Cederholm et al. 1989; Hewson 1995; Quinn et al. 2009) can have direct effects on riparian forests (Helfield and Naiman 2006) and lake productivity (Payne and Moore 2006). The scavenging of fish carcasses not subject to mass mortality events is rarely documented even though annual non-predatory mortality is estimated around 20-25% (Reznick et al. 2002). While many carcasses are undoubtedly consumed by aquatic scavengers or are deposited in sediment (Chidami and Amyot
ACCEPTED MANUSCRIPT 2008), the fate and scavenging rate of carcasses available to terrestrial vertebrate scavengers is unknown.
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Scavenging species diversity and scavenging rate have important implications for how nutrients move within terrestrial systems and these can vary with the habitats where carcasses occur. The observed differences in diversity and scavenging rate due to habitat can generally be accounted for by differences in scavenger guild and detection rates. Carcasses in open habitats have higher detection rates and tend to be consumed faster (Houston 1988; Selva et al. 2003; Abernethy et al. 2017). This may also be true for carcasses placed along habitat features with hard edges, such as water bodies, that are used as travel corridors by many facultative scavenging carnivores (Whittington et al 2005; Abernethy et al. 2017). Habitat can influence the guild of scavengers likely to utilize carcasses and, in turn, their efficiency of carrion removal (Sebastián‐ González et al. 2016; Turner et al. 2017). Intuitively, carcasses in habitats with a greater number of scavenging species present are expected to have greater diversity and efficiency in scavenging (Olson et al. 2012; Huijbers et al. 2016).
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Our study explores the movement of aquatic carrion resources (fish) into terrestrial food webs by vertebrate scavengers in the Polesie State Radiation Ecological Reserve (PSRER) portion of the Chernobyl Exclusion Zone (CEZ). The CEZ is an ideal system to study scavenging communities due to the limited human presence, diverse vertebrate community (Deryabina et al. 2015; Webster et al. 2016), and juxtaposition of distinct habitats where aquatic (i.e. riverine and abandoned irrigation canals) and terrestrial systems interact. We hypothesized that 1) a diverse vertebrate community including both semi-aquatic and terrestrial consumers would utilize carrion placed at the interface of aquatic and terrestrial systems, 2) the abundance and diversity of vertebrate scavengers in the CEZ would result in highly efficient scavenging, and 3) both scavenger efficiency and community composition would vary by habitat type (riverine vs. irrigation canals). We expected scavenging species richness and diversity to be higher in canal trials because canals are juxtaposed with a greater variety of habitats. However, we predicted a greater efficiency of vertebrate scavengers among river trials because carcasses along rivers are more visually exposed thus potentially more easily detected by both mammalian and avian species. 2. Materials and Methods 2.1. Study site Established after the Chernobyl power plant explosion in 1986, the PSRER is a 2,600 km² human exclusion area located in present day southern Belarus (Fig. 1). Historically, this region was predominantly used for agriculture, with government-owned farms and cooperative farms comprising the largest land use. To aid in agricultural production, irrigation canals were constructed during the early 20th century throughout the landscape. These canals were fed by local rivers/water sources and were constructed to hold water year-round. These canals have
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been abandoned since the Chernobyl accident, although most still retain water. Agricultural fields were either abandoned or planted with Scots pine (Pinus sylvestris) to prevent radionuclide re-suspension and soil erosion (Yoshenko et al. 2012). At the time of our study, approximately 51% of the PSRER was forested, with the remaining 49% comprised of seasonal wetlands, open fields, and abandoned agricultural and developed land (deserted villages, farms, and transportation systems). The PSRER is bisected by the Pripyat River, a large braided river with many adjacent oxbow lakes. These numerous open water bodies, along with the abandoned irrigation canals, provide ample opportunity for nutrient transfer between aquatic and terrestrial ecosystems. Access to the PSRER is highly restricted and the lack of human inhabitants has resulted in abundant, diverse wildlife populations, including numerous facultative vertebrate scavengers (Deryabina et al. 2015, Webster et al. 2016). 2.2. Trial Design
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Scavenging trials were conducted along irrigation canals and the Pripyat River from October 24 to November 18, 2016; our sampling unit consisted of single trials in either habitat type. Trials occurred during fall when invertebrate activity was limited as we were specifically focused on vertebrate use of carrion in this study. For bait we used whole domestic common carp (Cyprinus carpio) carcasses, purchased fresh from a local market, because the species is present in the CEZ along with nine other native and introduced species in the family Cyprinidae (Kaglyan et al. 2016). We measured carcass length (mouth to tip of tail) and height (widest ventral to dorsal point) before placing each fish in front of a motion-activated camera (Moultrie M-1100i Mini Game Camera, Calera, Alabama, U.S.A.) set to take a burst of three photos with a one second delay between photos and a one minute quiet period between bursts. We mounted cameras roughly 0.75 m above the ground and recorded photographs for 7-9 days or until the carcass was wholly removed, whichever came first. We placed carcasses at the edge of open water along either abandoned irrigation canals or the Pripyat River to mimic the natural deposition of fish carcasses. Sites categorized as “river” included both natural oxbow lakes and the main channel of the Pripyat, where access was possible. Active trial sites were a minimum of 1,000 m apart and subsequent trials were a minimum of 500 m from previous sites to ensure scavengers did not become conditioned to visit trial sites. To minimize disturbance of irradiated soil, carcasses were not staked into the ground, but were attached to large debris, usually tree branches of enough mass to prevent carcasses from being moved out of frame by scavengers not expected to wholly consume carcasses (e.g., mice, small avian scavengers). We attached carcasses to branches with braided 14 kg test fishing line by sewing the line through the body cavity. Stitches were made so that the fishing line passed at the base of scales to minimize the impact to carcass integrity. 2.3 Scavenger species composition – At the conclusion of each trial, camera images were analyzed to identify all vertebrate scavenging species and determine elapsed time between the start of the trial and each scavenging event. A “scavenging event” was defined as any time a vertebrate consumed any portion of the carcass. Species were identified as the “final scavenger”
ACCEPTED MANUSCRIPT when they consumed the entirely of the remaining carcass, irrespective of the amount of carcass that remained. When carcasses were moved out of frame, the final scavenger was identified as the last species shown manipulating the carcass. Trials where a carcass was taken but the scavenging species was indistinguishable were classified as “Unknown”. Scavenger diversity and scavenging species richness was estimated for all scavenging events at canal and river sites using the Shannon Diversity Index (Shannon and Weaver 1949) and compared using a Hutcheson t-test (Hutcheson 1970).
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For carcass trials in which there were multiple scavengers, camera images were further analyzed to determine the percentage of each carcass that was consumed by each species. For each species observed scavenging on a carcass, two independent observers estimated the percentage consumed with a minimum value of 5% assigned. When carcasses were removed from camera the final scavenger was assumed to have consumed the remainder of the carcass. Although subjective, we believe our estimates of the percentage of each carcass scavenged by a species accurately reflects the amount consumed given the lack of carcass utilization by invertebrates (due to low temperatures), the simple body shape of common carp, and the large proportion of carcasses that were entirely consumed by a single vertebrate (see results). Consumption percentages by species were averaged across all trials and by habitat type. Species specific differences in consumption were compared by habitat with a χ² test of independence in package “FactoMineR” (Le et al. 2008) in Program R (R Core Team 2016).
3. Results
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2.4 Scavenging efficiency - Scavenging efficiency was evaluated by determining the scavenging rate (the proportion of carcasses scavenged) and persistence time. Scavenging rate was determined for all trials and by habitat type for completely and partially scavenged carcasses. To assess differences in persistence time between habitats we first recorded the number of hours it took for a scavenger to find the carcass and the number of hours until it was completely consumed. We used the package “survival” (Therneau 2015) in Program R (R Core Team 2016) to calculate probability of a carcass persisting through time. Carcasses were considered available until a final scavenger consumed the carcass or the trial ended. We used a log-rank test which calculates a χ² value for observed and expected events for each time step to test for differences in persistence time between habitat types.
We conducted 83 scavenging trials in the CEZ, 16 of which were unusable due to camera failure or a flooding event with subsequent freezing that rendered carcasses inaccessible to vertebrate scavengers. Cameras deployed during the first round of trials were programmed to only take photos on a 15 minute time lapse, resulting in 12 trials with the scavenging species classified as unknown; these trials were included in assessments of carcass persistence time and scavenging efficiency. Carcasses were placed an average of 1.04 ± 0.02 m from open water. Fish averaged 10.88 ± 0.88 cm in height and 32.49 ± 0.57 cm in length.
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3.1 Scavenger species composition – Fifty-five scavenging trials allowed for identification of scavenging species and estimation of the percentage consumed by species. Carp carcasses were scavenged by 15 vertebrate species composed of 10 mammalian and 5 avian species (Table 1). Three mouse species (striped field mouse, Apodemus agrarius; yellow necked mouse, Apodemus flavicollis; harvest mouse, Micromys minutus), Eurasian jays (Garrulus glandarius, Fig.e 2a.), and common magpies (Pica pica) were among the most common scavengers, although they rarely completely consumed a carcass. These species tended to consume fleshy portions of the carcass until removal by larger scavengers. The average biomass consumed by mice and corvids was less than 8% (Table 1). Larger scavengers, including raccoon dogs (Nyctereutes procyonoides, Fig. 2b.), American mink (Neovison vison), Eurasian otter (Lutra lutra, Fig. 2c.), wolves (Canis lupus, Fig. 2d.), raven (Corvus corax), and white-tailed eagle (Haliarrtus albicilla), completely consumed carcasses when found. Raccoon dogs and American mink were the predominant final scavengers and consumed 48.73% of carcass biomass (Table 1).
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Scavenging community varied between canal and river trials (p= 0.03) with canal trials having a lower Shannon’s Diversity Index than river trials (1.56 vs. 1.86). A greater number of scavenging visits were documented per canal trial (canal =4.5, river = 3.68) though this is mainly due to visits from smaller scavengers before a larger scavenger found the carcass. Species specific scavenging proportions differed significantly between canal and river sites (p < 0.001). Canal locations had greater species richness with 14 documented species, but 13.71% of biomass remained unscavenged at the end of trials (Table 1). Fewer scavenger species (n=11) were recorded at river trials but all river trials were scavenged completely (Table 1). Several species had greater than 5% differences in the proportion of carcasses scavenged between habitat types. Scavenging events and percentage consumption by mice and Eurasian otters was greater in canal trials, whereas mink, raccoon dog, and wolf consumption was greater among river trials. No bird species showed a greater than 5% change in scavenging between habitat types. Several species including tawny owls (Strix aluco), red fox (Vulpes vulpes), least weasel (Mustela nivalis), and pine marten (Martes martes) were not documented scavenging at river trials and wolves were never documented scavenging along canals.
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3.2 Scavenging efficiency - Of the 67 usable trials, 66 (98.51%) were partially scavenged, of which 60 (89.55%) ultimately were completely scavenged over the ~1 week carcasses were monitored during our study. Vertebrate scavengers were more efficient along the river as every trial (n=25) was completely scavenged. Scavengers were slightly less efficient at removing carrion along canals (n=42), with 33 complete scavenging events, 8 partial scavenging events, and 1 trial with no documented scavenging. For all trials, elapsed time until the first scavenging event averaged 34.99 ± 6.21 hours and ranged between 0.57 and 201.87 hours (n=54). Persistence time until the carcass was completely scavenged averaged 53.02 ± 6.98 hours and ranged between 2.08 and 201.87 hours (n=48). Persistence times were significantly different between canal and river trials (Fig. 3, X²1 = 6.3, p = 0.012) with carcasses along rivers being removed faster. The elapsed time from carcass
ACCEPTED MANUSCRIPT placement to the first scavenging event did not differ between habitat types (X²1 = 1.9, p = 0.167). 4. Discussion
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Results of our study revealed a highly efficient community of vertebrate scavengers utilizing fish carrion, with all but one carcass scavenged by vertebrates within ~1 week. Such scavenging rates (>98%) are high, but within the range reported in the literature for other taxa (reviewed in DeVault et al. 2003) and the few published accounts of fish scavenging (Cederholm et al. 1989; Hewson 1995). Similar to other studies, we found a diverse assemblage of mammalian and avian species consuming small carrion, with the majority of carcass biomass consumed by mesocarnivores (DeVault et al. 2011; Villegas-Patraca et al. 2012; Turner et al. 2017). Mesocarnivores were the predominant scavengers in both river and canal habitats, but we observed subtle differences in scavenging dynamics between these habitats, with greater scavenger efficiency and higher diversity (but lower richness) for carcasses placed along rivers. Collectively, these data suggest the CEZ supports a highly diverse and efficient vertebrate scavenging community, providing further evidence of abundant wildlife populations in the CEZ (Deryabina et al. 2015; Webster et al. 2016). Further, the efficient utilization of aquatic resources by a diverse guild of terrestrial and semi-aquatic scavengers has important implications for the redistribution of scavenging-derived nutrients and the connectivity of adjacent ecosystems.
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Scavengers of fish carcasses in the CEZ included a diverse group of both semi-aquatic and terrestrial species that were highly efficient at locating and consuming carcasses. Such prolific scavenging rates suggest fish carrion is a valuable resource that is utilized when available, and thus vertebrate scavenging likely plays a role in the transfer of nutrients between aquatic and terrestrial systems. The majority of scavenging species were mammals (n=10) that could move nutrients into upland habitats through defecation, transfer of carcass remains, and eventual death. Although mammals were more likely to consume the entirety of carcasses once found, birds were observed scavenging at 33% of carcasses in our study. Given their mobility, birds have the potential to disseminate carrion nutrients extensive distances from carcasses, as well as facilitate the redistribution of scavenged resources among ecosystems (Payne and Moore 2006; Fujita and Koike 2009). In addition to vertebrates, invertebrates undoubtedly play an important role in the transfer of nutrients among systems (Gende et al. 2002; Laidre 2013). Scavenging trials in our study were conducted in Oct-Nov when invertebrate activity was limited due to cold temperatures. During warmer months when invertebrate scavengers are active we anticipate a more complex pattern of nutrient redistribution exists among vertebrate and invertebrate scavengers (Beasley et al. 2015). However, consumption of carrion by invertebrates would further increase the proportional biomass of carrion nutrients transferred from aquatic to terrestrial ecosystems. Several species groups were notable in presence and absence in these trials. The dominance of mesocarnivores at carcasses in the CEZ is not surprising given that fish carcasses
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are small, easy to open, and mesocarnivores are efficient scavengers even in degraded systems (Olson et al. 2012; Turner et al. 2017). Among mesocarnivores, raccoon dogs and American mink were the dominant scavengers, both of which are non-native to the region and compete with native species that occupy similar niche space (Selva et al. 2005; Brown et al. 2015). American mink are particularly detrimental to the critically endangered European mink (Mustela lutreola, Maran et al. 1998). European mink populations have been so reduced, however, that American mink may have functionally replaced them in the CEZ community with limited changes to nutrient flow or total diversity (Dornelas et al. 2014; Huijbers et al. 2016). Jays and magpies were the most common avian scavengers and generally opened the carcass before larger species removed it. Other avian species including ravens, tawny owls, and white-tailed eagles removed carcasses once found. Several other mammalian and avian scavengers are present in the CEZ but were not detected during our trials (e.g., Eurasian lynx – Lynx lynx, wild boar – Sus scrofa, brown bear – Ursus arctos). The non-detection of these species at our carcasses likely is a result of the limited number of trials performed, low density, or limited use of small carcasses, as larger carcasses are available for longer periods and thus available to a broader diversity of scavengers (Moleón et al. 2015; Turner et al. 2017).
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Habitat played an important role in scavenging diversity and efficiency in this study by influencing detection rates and determining the scavenging community present. Thirty years after abandonment, the canals in the CEZ are still channelized but highly vegetated. Conversely, the oxbow lakes and river banks are less sloped and have comparatively little vegetation at the water’s edge. The reduced cover could make fish carcasses more conspicuous to scavengers; reducing detection time and increasing the likelihood that scavenging will occur. Canals in the CEZ bisect a greater diversity of microhabitats than the river because they run through both upland and lowland habitats with varying degrees of human impacts (i.e. forestry and abandoned farmland). Scavenging communities vary along this gradient of habitat types and several species (least weasel, pine marten, red fox, and tawny owl) were only documented scavenging along canals. Other species, including raccoon dogs and wolves, were expected to occur at higher rates in the riverine habitats (Webster et al. 2016) and indeed we found they scavenged at higher rates or exclusively in riverine habitats. Variation seen between habitat types is likely due to the interplay of detection rates and community differences. Because detection rates were lower in canal trials it allowed carcasses to persist longer in the environment and allowed species with more limited search efficiency to detect carcasses. Given the greater persistence time of carrion placed along canals, we observed increased scavenging by smaller species (e.g., mice, birds) that were unable to completely remove carcasses. These smaller species often utilized carcasses on consecutive nights until the carcass was consumed by a larger vertebrate; in some cases mice and birds were able to completely consume carcasses in canals before arrival of larger scavengers. The movement of nutrients between ecosystems via scavenging of fish carcasses is prevalent and deserves further investigation. Specifically, quantifying spatial redistribution of nutrients would increase our understanding of how scavenging promotes inter-linkages among
ACCEPTED MANUSCRIPT ecosystems. Scavengers vary in their ability to transport nutrients based on their habitat preferences and movement capabilities yet no study has documented species specific patterns of fish carcass redistribution or locations where carcasses are deposited. Unconsumed portions of fish carcasses that are deposited in upland habitats would be available to a different guild of scavengers, adding further complexity to food webs. Future work that identifies both scavenging species communities and the ultimate fate of carcasses remains would illuminate this process.
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Previous work has highlighted the flow of nutrients across the land-water interface due to vertebrate redistribution during mass die-off events involving hundreds of fish carcasses (Hewson 1995; Cederholm et al. 1989). Here we presented evidence that individual deaths of aquatic organisms due to natural and anthropogenic causes may be an important pathway for aquatic derived nutrients to move into terrestrial systems. Although the CEZ is a large intact system with little human disturbance, the high scavenging rate and efficiency of vertebrate scavengers was within the range reported in the literature (DeVault et al. 2003), including landscapes highly degraded from human land use (Olson et al. 2012). Thus, our results may be broadly applicable, as landscapes supporting robust mesocarnivore populations appear to be highly efficient at assimilating small carrion resources, irrespective of human land use, but this relationship remains to be examined across the land-water interface.
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Acknowledgements
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We thank the Polesie State Radioecological Reserve staff as well as the Ministry of Education and Research for their support. We additionally thank J. Smith, V. Dombrovski, and D. Shamovich for assistance with this manuscript and collection of field data. Funding for this study was provided by the U.S. Department of Energy under Award No. DE-EM0004391 to the University of Georgia Research Foundation.
ACCEPTED MANUSCRIPT Table 1. Summary table of scavenging events and percentage of carcasses consumed in 55 scavenging trials in the Chernobyl Exclusion Zone carried out during October-November 2016. Scavenging event totals are included for canal and river trials as well as a total for all trials. For 48 trials where the final scavenger was identified they are totaled in the column “Final Scav.”. The average percentage of carcasses consumed by species is also included for canal and river trials, as well as for all trials.
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% of All Carcasses Scav. 7.18 0.27 15.64 10.00 1.82 33.09 1.82 3.64 3.73 5.27 3.18 1.64 4.00 8.73 100
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Final Scav. 0 0 10 6 1 20 1 2 1 1 2 1 3 48
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Total Scav. Events 111 3 21 7 1 23 1 2 17 37 4 1 4 232
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River Scav. Events 23 0 8 1 0 11 0 2 7 13 3 0 2 70
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Species Mouse sp. (3) Least weasel, Mustela nivalis American Mink, Neovison vison Eurasian Otter, Lutra lutra Pine Marten, Martes martes Raccoon Dog, Nyctereutes procyonoides Red Fox, Vulpes vulpes Wolf, Canis lupus Eurasian Jay, Garrulus gladarius Common Magpie, Pica pica Raven, Corvus corax Tawny Owl, Strix aluco White-Tailed Eagle, Haliarrtus albicilla None Total
Canal Scav. Events 88 3 13 6 1 12 1 0 10 24 1 1 2 162
% of Canal Carcasses Scav. 10.00 0.43 12.71 12.86 2.86 24.57 2.86 5.14 5.43 2.86 2.57 4.00 13.71 100
% of River Carcasses Scav. 2.25 20.75 5.00 48.00 10.00 1.25 5.00 3.75 4.00 100
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ACCEPTED MANUSCRIPT Fig. 1. The Belarusian Polesie State Radiation Ecological Reserve portion of the Chernobyl Exclusion Zone (black in inset). Irrigation canals, Pripyat River, and trial locations are shown.
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Fig. 2. Ten mammalian and five avian species were documented scavenging fish carcasses in the Chernobyl Exclusion Zone including raccoon dogs (Nyctereutes procyonoides, a.), wolves (Canis lupus, b.), Eurasian otters (Lutra lutra, c.), and Eurasian jay (Garrulus glandarius, d.).
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Fig. 3. Persistence probability of common carp carcasses placed at the intersection of aquatic and terrestrial habitats in the Polesie State Radiation Ecological Reserve. Persistence varied significantly (p = 0.0118) by habitat type trials were censored after complete removal by vertebrate scavengers.
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Author’s name
Savannah River Ecology Laboratory, UGA, Aiken, SC
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Peter E. Schlichting
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James C. Beasley
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Cara N. Love Sarah C. Webster
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Savannah River Ecology Laboratory, UGA, Aiken, SC
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Peter E. Schlichting, Cara N. Love, Sarah C. Webster, James C. Beasley PII: DOI: Article Number: Reference:
S2352-2496(18)30033-8 https://doi.org/10.1016/j.fooweb.2018.e00107 e00107 FOOWEB 107
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Food Webs
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Please cite this article as: Peter E. Schlichting, Cara N. Love, Sarah C. Webster, James C. Beasley , Efficiency and composition of vertebrate scavengers at the land-water interface in the Chernobyl Exclusion Zone. Fooweb (2018), https://doi.org/10.1016/ j.fooweb.2018.e00107
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ACCEPTED MANUSCRIPT Efficiency and composition of vertebrate scavengers at the land-water interface in the Chernobyl Exclusion Zone
Peter E. Schlichting1, Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA
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Cara N. Love, Savannah River Ecology Laboratory, Odum School of Ecology, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA
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Sarah C. Webster, Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA
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James C. Beasley, Savannah River Ecology Laboratory, Warnell School of Forestry and Natural Resources, University of Georgia, P.O. Drawer E, Aiken, SC 29802, USA 1
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Corresponding author, current address: College of Integrative Sciences and Arts, Arizona State University, Polytechnic campus, 6073 South Backus Mall, Mesa, Arizona 85212, USA
ACCEPTED MANUSCRIPT Abstract
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Scavenging increases the connectivity of food webs yet scavenging links between adjacent ecosystems are poorly characterized. Here we explored the movement of aquatic carrion into terrestrial food webs by vertebrate scavengers across two habitat types in the Chernobyl Exclusion Zone (CEZ). We used motion activated cameras to monitor experimentally placed fish carcasses to quantify the composition and efficiency of vertebrate scavengers of canal and river communities in the CEZ. We conducted 83 trials that were scavenged by 10 mammalian and 5 avian species. Species diversity, percentage consumed, scavenging efficiency, and time until scavenged differed between canal and river trials. Mesocarnivores were the predominant scavengers in both habitats, and we observed greater scavenger efficiency and higher diversity (but lower richness) among river trials. Variation in scavenging among habitats was attributed to the interplay of higher detection rates in the river habitats and differences in scavenger community, as canals intersected a greater diversity of habitat types. Our data suggest the CEZ supports a highly diverse and efficient vertebrate scavenging community with important implications for the redistribution of scavenging-derived nutrients and the connectivity of adjacent ecosystems. Future studies should focus on species-specific patterns of nutrient redistribution and ultimate carcass deposition sites to further our understanding of the mechanisms connecting aquatic and terrestrial systems via scavenging of aquatic nutrients by terrestrial scavengers.
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Keywords: aquatic-terrestrial interface, Chernobyl Exclusion Zone, fish carrion, food webs, mesocarnivore, scavenging links
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1. Introduction
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Vertebrate scavengers play an important role in maintaining healthy ecosystems and fulfill several ecological functions including the creation of biodiversity hotspots (Smith and Baco 2003; Bump et al. 2009), containment of disease (Markandya et al. 2008), and formation of critical linkages in food webs (DeVault et al. 2003; Wilson and Wolkovich 2011). The patchiness of carrion resources means there are few obligate vertebrate scavengers (Ruxton and Houston 2004), and this spatiotemporal unpredictability of carrion has important implications for promoting both scavenging species diversity and the importance of facultative scavenging (Cortés-Avizanda et al. 2012). There is growing awareness of the impact of facultative scavenging (DeVault et al. 2003; Pereira et al. 2014; Beasley et al. 2015) and including facultative scavenging in food web analyses can result in as much as a 16-fold increase in linkages (Wilson and Wolkovich 2011). The formation of these linkages results in more connected, and thus stable, food webs (Polis 1991; Polis and Strong 1996; McCann et al 1998; McCann 2000). However, many scavenging links remain poorly understood, particularly linkages involving the transfer of nutrients between adjacent ecosystems (Vander Zanden and Sanzone 2004; Beasley et al. 2012).
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Most food web studies have focused on linkages within a single ecosystem due to the inherent complexities of biological systems, yet nutrients commonly flow among ecosystems through both biotic and abiotic processes (Polis et al. 1996; Vander Zanden, and Sanzone 2004; Witman et al. 2004; Beasley et al. 2012; Benbow et al. 2018). The flow of aquatic-derived nutrients into terrestrial habitats can be detected beyond their physical boundaries (Muehlbauer et al. 2014), and the movement of aquatic nutrients by animal vectors has the potential to increase the spatial redistribution of nutrients and augment terrestrial system productivity (Nakano and Murakami 2001; Henschel 2004; Helfield and Naiman 2006; Gratton et al. 2008). Mechanisms of nutrient transfer across the land-water interface include terrestrial defecation by semi-aquatic foragers (Fariña et al. 2003; Crait and Ben-David 2007), terrestrial consumers moving aquatic resources into terrestrial systems (Rose and Polis 1998; Quinn et al. 2009), and the non-consumptive deposition of nutrients (e.g. shells, feathers) (Polis and Hurd 1995; Vander Zanden et al. 2012). Scavenging is another important mechanism facilitating the transfer of nutrients between adjoining ecosystems (Beasley et al. 2012), although inter-ecosystem linkages via scavenging have received comparatively little attention.
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Scavenging across the land-water interface has been documented in marine and freshwater systems. Allochthonous marine resources can subsidize coastal carnivores enough to yield a numerical response (Holling 1959) and sustain higher densities than inland populations (Rose and Polis 1998). Similarly, sea turtle carrion may be a key seasonal resource for numerous terrestrial mammals, reptiles, and birds (Escobar-Lasso et al. 2016). Feeding by dingos (Canis lupus dingo) on recreational fishing remains has been shown to alter their activity patterns (Déaux et al. 2018) and this common type of provisioning can have important implications for food webs (Newsome et al. 2015). At the land-ocean interface, the scavenging of fish by a diverse community suggests scavenging shapes food web dynamics by supplementing several trophic levels via facultative scavenging (Schlacher et al. 2013; Huijbers et al. 2016).
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One of the most notable examples of inter-ecosystem nutrient exchange is the annual migration of anadromous fish from pelagic to inland freshwater systems. This process deposits vast amounts of nutrients from marine ecosystems into inland riverine and stream systems, enriching those systems, as well as adjacent terrestrial ecosystems (Willson et al. 1998; Cederholm et al. 1999). While many anadromous fish carcasses are decomposed or scavenged within the aquatic system, 20-89% of salmon carcasses may become available to terrestrial scavengers (i.e. not deposited on streambed or carried downstream) and potentially transported into the adjoining terrestrial environment (Cederholm et al. 1989; Hewson 1995). This spatial redistribution of salmon carcasses by a diverse guild of terrestrial scavengers (Cederholm et al. 1989; Hewson 1995; Quinn et al. 2009) can have direct effects on riparian forests (Helfield and Naiman 2006) and lake productivity (Payne and Moore 2006). The scavenging of fish carcasses not subject to mass mortality events is rarely documented even though annual non-predatory mortality is estimated around 20-25% (Reznick et al. 2002). While many carcasses are undoubtedly consumed by aquatic scavengers or are deposited in sediment (Chidami and Amyot
ACCEPTED MANUSCRIPT 2008), the fate and scavenging rate of carcasses available to terrestrial vertebrate scavengers is unknown.
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Scavenging species diversity and scavenging rate have important implications for how nutrients move within terrestrial systems and these can vary with the habitats where carcasses occur. The observed differences in diversity and scavenging rate due to habitat can generally be accounted for by differences in scavenger guild and detection rates. Carcasses in open habitats have higher detection rates and tend to be consumed faster (Houston 1988; Selva et al. 2003; Abernethy et al. 2017). This may also be true for carcasses placed along habitat features with hard edges, such as water bodies, that are used as travel corridors by many facultative scavenging carnivores (Whittington et al 2005; Abernethy et al. 2017). Habitat can influence the guild of scavengers likely to utilize carcasses and, in turn, their efficiency of carrion removal (Sebastián‐ González et al. 2016; Turner et al. 2017). Intuitively, carcasses in habitats with a greater number of scavenging species present are expected to have greater diversity and efficiency in scavenging (Olson et al. 2012; Huijbers et al. 2016).
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Our study explores the movement of aquatic carrion resources (fish) into terrestrial food webs by vertebrate scavengers in the Polesie State Radiation Ecological Reserve (PSRER) portion of the Chernobyl Exclusion Zone (CEZ). The CEZ is an ideal system to study scavenging communities due to the limited human presence, diverse vertebrate community (Deryabina et al. 2015; Webster et al. 2016), and juxtaposition of distinct habitats where aquatic (i.e. riverine and abandoned irrigation canals) and terrestrial systems interact. We hypothesized that 1) a diverse vertebrate community including both semi-aquatic and terrestrial consumers would utilize carrion placed at the interface of aquatic and terrestrial systems, 2) the abundance and diversity of vertebrate scavengers in the CEZ would result in highly efficient scavenging, and 3) both scavenger efficiency and community composition would vary by habitat type (riverine vs. irrigation canals). We expected scavenging species richness and diversity to be higher in canal trials because canals are juxtaposed with a greater variety of habitats. However, we predicted a greater efficiency of vertebrate scavengers among river trials because carcasses along rivers are more visually exposed thus potentially more easily detected by both mammalian and avian species. 2. Materials and Methods 2.1. Study site Established after the Chernobyl power plant explosion in 1986, the PSRER is a 2,600 km² human exclusion area located in present day southern Belarus (Fig. 1). Historically, this region was predominantly used for agriculture, with government-owned farms and cooperative farms comprising the largest land use. To aid in agricultural production, irrigation canals were constructed during the early 20th century throughout the landscape. These canals were fed by local rivers/water sources and were constructed to hold water year-round. These canals have
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been abandoned since the Chernobyl accident, although most still retain water. Agricultural fields were either abandoned or planted with Scots pine (Pinus sylvestris) to prevent radionuclide re-suspension and soil erosion (Yoshenko et al. 2012). At the time of our study, approximately 51% of the PSRER was forested, with the remaining 49% comprised of seasonal wetlands, open fields, and abandoned agricultural and developed land (deserted villages, farms, and transportation systems). The PSRER is bisected by the Pripyat River, a large braided river with many adjacent oxbow lakes. These numerous open water bodies, along with the abandoned irrigation canals, provide ample opportunity for nutrient transfer between aquatic and terrestrial ecosystems. Access to the PSRER is highly restricted and the lack of human inhabitants has resulted in abundant, diverse wildlife populations, including numerous facultative vertebrate scavengers (Deryabina et al. 2015, Webster et al. 2016). 2.2. Trial Design
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Scavenging trials were conducted along irrigation canals and the Pripyat River from October 24 to November 18, 2016; our sampling unit consisted of single trials in either habitat type. Trials occurred during fall when invertebrate activity was limited as we were specifically focused on vertebrate use of carrion in this study. For bait we used whole domestic common carp (Cyprinus carpio) carcasses, purchased fresh from a local market, because the species is present in the CEZ along with nine other native and introduced species in the family Cyprinidae (Kaglyan et al. 2016). We measured carcass length (mouth to tip of tail) and height (widest ventral to dorsal point) before placing each fish in front of a motion-activated camera (Moultrie M-1100i Mini Game Camera, Calera, Alabama, U.S.A.) set to take a burst of three photos with a one second delay between photos and a one minute quiet period between bursts. We mounted cameras roughly 0.75 m above the ground and recorded photographs for 7-9 days or until the carcass was wholly removed, whichever came first. We placed carcasses at the edge of open water along either abandoned irrigation canals or the Pripyat River to mimic the natural deposition of fish carcasses. Sites categorized as “river” included both natural oxbow lakes and the main channel of the Pripyat, where access was possible. Active trial sites were a minimum of 1,000 m apart and subsequent trials were a minimum of 500 m from previous sites to ensure scavengers did not become conditioned to visit trial sites. To minimize disturbance of irradiated soil, carcasses were not staked into the ground, but were attached to large debris, usually tree branches of enough mass to prevent carcasses from being moved out of frame by scavengers not expected to wholly consume carcasses (e.g., mice, small avian scavengers). We attached carcasses to branches with braided 14 kg test fishing line by sewing the line through the body cavity. Stitches were made so that the fishing line passed at the base of scales to minimize the impact to carcass integrity. 2.3 Scavenger species composition – At the conclusion of each trial, camera images were analyzed to identify all vertebrate scavenging species and determine elapsed time between the start of the trial and each scavenging event. A “scavenging event” was defined as any time a vertebrate consumed any portion of the carcass. Species were identified as the “final scavenger”
ACCEPTED MANUSCRIPT when they consumed the entirely of the remaining carcass, irrespective of the amount of carcass that remained. When carcasses were moved out of frame, the final scavenger was identified as the last species shown manipulating the carcass. Trials where a carcass was taken but the scavenging species was indistinguishable were classified as “Unknown”. Scavenger diversity and scavenging species richness was estimated for all scavenging events at canal and river sites using the Shannon Diversity Index (Shannon and Weaver 1949) and compared using a Hutcheson t-test (Hutcheson 1970).
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For carcass trials in which there were multiple scavengers, camera images were further analyzed to determine the percentage of each carcass that was consumed by each species. For each species observed scavenging on a carcass, two independent observers estimated the percentage consumed with a minimum value of 5% assigned. When carcasses were removed from camera the final scavenger was assumed to have consumed the remainder of the carcass. Although subjective, we believe our estimates of the percentage of each carcass scavenged by a species accurately reflects the amount consumed given the lack of carcass utilization by invertebrates (due to low temperatures), the simple body shape of common carp, and the large proportion of carcasses that were entirely consumed by a single vertebrate (see results). Consumption percentages by species were averaged across all trials and by habitat type. Species specific differences in consumption were compared by habitat with a χ² test of independence in package “FactoMineR” (Le et al. 2008) in Program R (R Core Team 2016).
3. Results
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2.4 Scavenging efficiency - Scavenging efficiency was evaluated by determining the scavenging rate (the proportion of carcasses scavenged) and persistence time. Scavenging rate was determined for all trials and by habitat type for completely and partially scavenged carcasses. To assess differences in persistence time between habitats we first recorded the number of hours it took for a scavenger to find the carcass and the number of hours until it was completely consumed. We used the package “survival” (Therneau 2015) in Program R (R Core Team 2016) to calculate probability of a carcass persisting through time. Carcasses were considered available until a final scavenger consumed the carcass or the trial ended. We used a log-rank test which calculates a χ² value for observed and expected events for each time step to test for differences in persistence time between habitat types.
We conducted 83 scavenging trials in the CEZ, 16 of which were unusable due to camera failure or a flooding event with subsequent freezing that rendered carcasses inaccessible to vertebrate scavengers. Cameras deployed during the first round of trials were programmed to only take photos on a 15 minute time lapse, resulting in 12 trials with the scavenging species classified as unknown; these trials were included in assessments of carcass persistence time and scavenging efficiency. Carcasses were placed an average of 1.04 ± 0.02 m from open water. Fish averaged 10.88 ± 0.88 cm in height and 32.49 ± 0.57 cm in length.
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3.1 Scavenger species composition – Fifty-five scavenging trials allowed for identification of scavenging species and estimation of the percentage consumed by species. Carp carcasses were scavenged by 15 vertebrate species composed of 10 mammalian and 5 avian species (Table 1). Three mouse species (striped field mouse, Apodemus agrarius; yellow necked mouse, Apodemus flavicollis; harvest mouse, Micromys minutus), Eurasian jays (Garrulus glandarius, Fig.e 2a.), and common magpies (Pica pica) were among the most common scavengers, although they rarely completely consumed a carcass. These species tended to consume fleshy portions of the carcass until removal by larger scavengers. The average biomass consumed by mice and corvids was less than 8% (Table 1). Larger scavengers, including raccoon dogs (Nyctereutes procyonoides, Fig. 2b.), American mink (Neovison vison), Eurasian otter (Lutra lutra, Fig. 2c.), wolves (Canis lupus, Fig. 2d.), raven (Corvus corax), and white-tailed eagle (Haliarrtus albicilla), completely consumed carcasses when found. Raccoon dogs and American mink were the predominant final scavengers and consumed 48.73% of carcass biomass (Table 1).
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Scavenging community varied between canal and river trials (p= 0.03) with canal trials having a lower Shannon’s Diversity Index than river trials (1.56 vs. 1.86). A greater number of scavenging visits were documented per canal trial (canal =4.5, river = 3.68) though this is mainly due to visits from smaller scavengers before a larger scavenger found the carcass. Species specific scavenging proportions differed significantly between canal and river sites (p < 0.001). Canal locations had greater species richness with 14 documented species, but 13.71% of biomass remained unscavenged at the end of trials (Table 1). Fewer scavenger species (n=11) were recorded at river trials but all river trials were scavenged completely (Table 1). Several species had greater than 5% differences in the proportion of carcasses scavenged between habitat types. Scavenging events and percentage consumption by mice and Eurasian otters was greater in canal trials, whereas mink, raccoon dog, and wolf consumption was greater among river trials. No bird species showed a greater than 5% change in scavenging between habitat types. Several species including tawny owls (Strix aluco), red fox (Vulpes vulpes), least weasel (Mustela nivalis), and pine marten (Martes martes) were not documented scavenging at river trials and wolves were never documented scavenging along canals.
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3.2 Scavenging efficiency - Of the 67 usable trials, 66 (98.51%) were partially scavenged, of which 60 (89.55%) ultimately were completely scavenged over the ~1 week carcasses were monitored during our study. Vertebrate scavengers were more efficient along the river as every trial (n=25) was completely scavenged. Scavengers were slightly less efficient at removing carrion along canals (n=42), with 33 complete scavenging events, 8 partial scavenging events, and 1 trial with no documented scavenging. For all trials, elapsed time until the first scavenging event averaged 34.99 ± 6.21 hours and ranged between 0.57 and 201.87 hours (n=54). Persistence time until the carcass was completely scavenged averaged 53.02 ± 6.98 hours and ranged between 2.08 and 201.87 hours (n=48). Persistence times were significantly different between canal and river trials (Fig. 3, X²1 = 6.3, p = 0.012) with carcasses along rivers being removed faster. The elapsed time from carcass
ACCEPTED MANUSCRIPT placement to the first scavenging event did not differ between habitat types (X²1 = 1.9, p = 0.167). 4. Discussion
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Results of our study revealed a highly efficient community of vertebrate scavengers utilizing fish carrion, with all but one carcass scavenged by vertebrates within ~1 week. Such scavenging rates (>98%) are high, but within the range reported in the literature for other taxa (reviewed in DeVault et al. 2003) and the few published accounts of fish scavenging (Cederholm et al. 1989; Hewson 1995). Similar to other studies, we found a diverse assemblage of mammalian and avian species consuming small carrion, with the majority of carcass biomass consumed by mesocarnivores (DeVault et al. 2011; Villegas-Patraca et al. 2012; Turner et al. 2017). Mesocarnivores were the predominant scavengers in both river and canal habitats, but we observed subtle differences in scavenging dynamics between these habitats, with greater scavenger efficiency and higher diversity (but lower richness) for carcasses placed along rivers. Collectively, these data suggest the CEZ supports a highly diverse and efficient vertebrate scavenging community, providing further evidence of abundant wildlife populations in the CEZ (Deryabina et al. 2015; Webster et al. 2016). Further, the efficient utilization of aquatic resources by a diverse guild of terrestrial and semi-aquatic scavengers has important implications for the redistribution of scavenging-derived nutrients and the connectivity of adjacent ecosystems.
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Scavengers of fish carcasses in the CEZ included a diverse group of both semi-aquatic and terrestrial species that were highly efficient at locating and consuming carcasses. Such prolific scavenging rates suggest fish carrion is a valuable resource that is utilized when available, and thus vertebrate scavenging likely plays a role in the transfer of nutrients between aquatic and terrestrial systems. The majority of scavenging species were mammals (n=10) that could move nutrients into upland habitats through defecation, transfer of carcass remains, and eventual death. Although mammals were more likely to consume the entirety of carcasses once found, birds were observed scavenging at 33% of carcasses in our study. Given their mobility, birds have the potential to disseminate carrion nutrients extensive distances from carcasses, as well as facilitate the redistribution of scavenged resources among ecosystems (Payne and Moore 2006; Fujita and Koike 2009). In addition to vertebrates, invertebrates undoubtedly play an important role in the transfer of nutrients among systems (Gende et al. 2002; Laidre 2013). Scavenging trials in our study were conducted in Oct-Nov when invertebrate activity was limited due to cold temperatures. During warmer months when invertebrate scavengers are active we anticipate a more complex pattern of nutrient redistribution exists among vertebrate and invertebrate scavengers (Beasley et al. 2015). However, consumption of carrion by invertebrates would further increase the proportional biomass of carrion nutrients transferred from aquatic to terrestrial ecosystems. Several species groups were notable in presence and absence in these trials. The dominance of mesocarnivores at carcasses in the CEZ is not surprising given that fish carcasses
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are small, easy to open, and mesocarnivores are efficient scavengers even in degraded systems (Olson et al. 2012; Turner et al. 2017). Among mesocarnivores, raccoon dogs and American mink were the dominant scavengers, both of which are non-native to the region and compete with native species that occupy similar niche space (Selva et al. 2005; Brown et al. 2015). American mink are particularly detrimental to the critically endangered European mink (Mustela lutreola, Maran et al. 1998). European mink populations have been so reduced, however, that American mink may have functionally replaced them in the CEZ community with limited changes to nutrient flow or total diversity (Dornelas et al. 2014; Huijbers et al. 2016). Jays and magpies were the most common avian scavengers and generally opened the carcass before larger species removed it. Other avian species including ravens, tawny owls, and white-tailed eagles removed carcasses once found. Several other mammalian and avian scavengers are present in the CEZ but were not detected during our trials (e.g., Eurasian lynx – Lynx lynx, wild boar – Sus scrofa, brown bear – Ursus arctos). The non-detection of these species at our carcasses likely is a result of the limited number of trials performed, low density, or limited use of small carcasses, as larger carcasses are available for longer periods and thus available to a broader diversity of scavengers (Moleón et al. 2015; Turner et al. 2017).
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Habitat played an important role in scavenging diversity and efficiency in this study by influencing detection rates and determining the scavenging community present. Thirty years after abandonment, the canals in the CEZ are still channelized but highly vegetated. Conversely, the oxbow lakes and river banks are less sloped and have comparatively little vegetation at the water’s edge. The reduced cover could make fish carcasses more conspicuous to scavengers; reducing detection time and increasing the likelihood that scavenging will occur. Canals in the CEZ bisect a greater diversity of microhabitats than the river because they run through both upland and lowland habitats with varying degrees of human impacts (i.e. forestry and abandoned farmland). Scavenging communities vary along this gradient of habitat types and several species (least weasel, pine marten, red fox, and tawny owl) were only documented scavenging along canals. Other species, including raccoon dogs and wolves, were expected to occur at higher rates in the riverine habitats (Webster et al. 2016) and indeed we found they scavenged at higher rates or exclusively in riverine habitats. Variation seen between habitat types is likely due to the interplay of detection rates and community differences. Because detection rates were lower in canal trials it allowed carcasses to persist longer in the environment and allowed species with more limited search efficiency to detect carcasses. Given the greater persistence time of carrion placed along canals, we observed increased scavenging by smaller species (e.g., mice, birds) that were unable to completely remove carcasses. These smaller species often utilized carcasses on consecutive nights until the carcass was consumed by a larger vertebrate; in some cases mice and birds were able to completely consume carcasses in canals before arrival of larger scavengers. The movement of nutrients between ecosystems via scavenging of fish carcasses is prevalent and deserves further investigation. Specifically, quantifying spatial redistribution of nutrients would increase our understanding of how scavenging promotes inter-linkages among
ACCEPTED MANUSCRIPT ecosystems. Scavengers vary in their ability to transport nutrients based on their habitat preferences and movement capabilities yet no study has documented species specific patterns of fish carcass redistribution or locations where carcasses are deposited. Unconsumed portions of fish carcasses that are deposited in upland habitats would be available to a different guild of scavengers, adding further complexity to food webs. Future work that identifies both scavenging species communities and the ultimate fate of carcasses remains would illuminate this process.
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Previous work has highlighted the flow of nutrients across the land-water interface due to vertebrate redistribution during mass die-off events involving hundreds of fish carcasses (Hewson 1995; Cederholm et al. 1989). Here we presented evidence that individual deaths of aquatic organisms due to natural and anthropogenic causes may be an important pathway for aquatic derived nutrients to move into terrestrial systems. Although the CEZ is a large intact system with little human disturbance, the high scavenging rate and efficiency of vertebrate scavengers was within the range reported in the literature (DeVault et al. 2003), including landscapes highly degraded from human land use (Olson et al. 2012). Thus, our results may be broadly applicable, as landscapes supporting robust mesocarnivore populations appear to be highly efficient at assimilating small carrion resources, irrespective of human land use, but this relationship remains to be examined across the land-water interface.
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Acknowledgements
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We thank the Polesie State Radioecological Reserve staff as well as the Ministry of Education and Research for their support. We additionally thank J. Smith, V. Dombrovski, and D. Shamovich for assistance with this manuscript and collection of field data. Funding for this study was provided by the U.S. Department of Energy under Award No. DE-EM0004391 to the University of Georgia Research Foundation.
ACCEPTED MANUSCRIPT Table 1. Summary table of scavenging events and percentage of carcasses consumed in 55 scavenging trials in the Chernobyl Exclusion Zone carried out during October-November 2016. Scavenging event totals are included for canal and river trials as well as a total for all trials. For 48 trials where the final scavenger was identified they are totaled in the column “Final Scav.”. The average percentage of carcasses consumed by species is also included for canal and river trials, as well as for all trials.
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% of All Carcasses Scav. 7.18 0.27 15.64 10.00 1.82 33.09 1.82 3.64 3.73 5.27 3.18 1.64 4.00 8.73 100
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Final Scav. 0 0 10 6 1 20 1 2 1 1 2 1 3 48
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Total Scav. Events 111 3 21 7 1 23 1 2 17 37 4 1 4 232
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River Scav. Events 23 0 8 1 0 11 0 2 7 13 3 0 2 70
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Species Mouse sp. (3) Least weasel, Mustela nivalis American Mink, Neovison vison Eurasian Otter, Lutra lutra Pine Marten, Martes martes Raccoon Dog, Nyctereutes procyonoides Red Fox, Vulpes vulpes Wolf, Canis lupus Eurasian Jay, Garrulus gladarius Common Magpie, Pica pica Raven, Corvus corax Tawny Owl, Strix aluco White-Tailed Eagle, Haliarrtus albicilla None Total
Canal Scav. Events 88 3 13 6 1 12 1 0 10 24 1 1 2 162
% of Canal Carcasses Scav. 10.00 0.43 12.71 12.86 2.86 24.57 2.86 5.14 5.43 2.86 2.57 4.00 13.71 100
% of River Carcasses Scav. 2.25 20.75 5.00 48.00 10.00 1.25 5.00 3.75 4.00 100
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ACCEPTED MANUSCRIPT Fig. 1. The Belarusian Polesie State Radiation Ecological Reserve portion of the Chernobyl Exclusion Zone (black in inset). Irrigation canals, Pripyat River, and trial locations are shown.
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Fig. 2. Ten mammalian and five avian species were documented scavenging fish carcasses in the Chernobyl Exclusion Zone including raccoon dogs (Nyctereutes procyonoides, a.), wolves (Canis lupus, b.), Eurasian otters (Lutra lutra, c.), and Eurasian jay (Garrulus glandarius, d.).
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Fig. 3. Persistence probability of common carp carcasses placed at the intersection of aquatic and terrestrial habitats in the Polesie State Radiation Ecological Reserve. Persistence varied significantly (p = 0.0118) by habitat type trials were censored after complete removal by vertebrate scavengers.
ACCEPTED MANUSCRIPT Conflict of Interest and Authorship Conformation Form
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Author’s name
Savannah River Ecology Laboratory, UGA, Aiken, SC
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Peter E. Schlichting
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James C. Beasley
Savannah River Ecology Laboratory, UGA, Aiken, SC
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Cara N. Love Sarah C. Webster
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Savannah River Ecology Laboratory, UGA, Aiken, SC
Savannah River Ecology Laboratory, UGA, Aiken, SC
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