Publications by authors named "Paolo Ciucci"

13 Publications

  • Page 1 of 1

Multiple species-specific molecular markers using nanofluidic array as a tool to detect prey DNA from carnivore scats.

Ecol Evol 2021 Sep 1;11(17):11739-11748. Epub 2021 Aug 1.

Grimsö Wildlife Research Station Department of Ecology Swedish University of Agricultural Sciences Riddarhyttan Sweden.

Large carnivore feeding ecology plays a crucial role for management and conservation for predators and their prey. One of the keys to this kind of research is to identify the species composition in the predator diet, for example, prey determination from scat content. DNA-based methods applied to detect prey in predators' scats are viable alternatives to traditional macroscopic approaches, showing an increased reliability and higher prey detection rate. Here, we developed a molecular method for prey species identification in wolf () scats using multiple species-specific marker loci on the cytochrome gene for 18 target species. The final panel consisted of 80 assays, with a minimum of four markers per target species, and that amplified specifically when using a high-throughput Nanofluidic array technology (Fluidigm Inc.). As a practical example, we applied the method to identify target prey species DNA in 80 wolf scats collected in Sweden. Depending on the number of amplifying markers required to obtain a positive species call in a scat, the success in determining at least one prey species from the scats ranged from 44% to 92%. Although we highlight the need to evaluate the optimal number of markers for sensitive target species detection, the developed method is a fast and cost-efficient tool for prey identification in wolf scats and it also has the potential to be further developed and applied to other areas and large carnivores as well.
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http://dx.doi.org/10.1002/ece3.7918DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8427573PMC
September 2021

First core microsatellite panel identification in Apennine brown bears (Ursus arctos marsicanus): a collaborative approach.

BMC Genomics 2021 Aug 18;22(1):623. Epub 2021 Aug 18.

Department for the Monitoring and Protection of the Environment and for Biodiversity Conservation, Unit for Conservation Genetics (BIO-CGE), Italian Institute for Environmental Protection and Research (ISPRA), Via Ca' Fornacetta, 9 - 40064 Ozzano dell'Emilia, Bologna, Italy.

Background: The low cost and rapidity of microsatellite analysis have led to the development of several markers for many species. Because in non-invasive genetics it is recommended to genotype individuals using few loci, generally a subset of markers is selected. The choice of different marker panels by different research groups studying the same population can cause problems and bias in data analysis. A priority issue in conservation genetics is the comparability of data produced by different labs with different methods. Here, we compared data from previous and ongoing studies to identify a panel of microsatellite loci efficient for the long-term monitoring of Apennine brown bears (Ursus arctos marsicanus), aiming at reducing genotyping uncertainty and allowing reliable individual identifications overtimes.

Results: We examined all microsatellite markers used up to now and identified 19 candidate loci. We evaluated the efficacy of 13 of the most commonly used loci analyzing 194 DNA samples belonging to 113 distinct bears selected from the Italian national biobank. We compared data from 4 different marker subsets on the basis of genotyping errors, allelic patterns, observed and expected heterozygosity, discriminatory powers, number of mismatching pairs, and probability of identity. The optimal marker set was selected evaluating the low molecular weight, the high discriminatory power, and the low occurrence of genotyping errors of each primer. We calibrated allele calls and verified matches among genotypes obtained in previous studies using the complete set of 13 STRs (Short Tandem Repeats), analyzing six invasive DNA samples from distinct individuals. Differences in allele-sizing between labs were consistent, showing a substantial overlap of the individual genotyping.

Conclusions: The proposed marker set comprises 11 Ursus specific markers with the addition of cxx20, the canid-locus less prone to genotyping errors, in order to prevent underestimation (maximizing the discriminatory power) and overestimation (minimizing the genotyping errors) of the number of Apennine brown bears. The selected markers allow saving time and costs with the amplification in multiplex of all loci thanks to the same annealing temperature. Our work optimizes the available resources by identifying a shared panel and a uniform methodology capable of improving comparisons between past and future studies.
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http://dx.doi.org/10.1186/s12864-021-07915-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8371798PMC
August 2021

Cross-continental comparison of parasite communities in a wide-ranging carnivore suggests associations with prey diversity and host density.

Ecol Evol 2021 Aug 13;11(15):10338-10352. Epub 2021 Jul 13.

Department of Geography University of Victoria Victoria BC Canada.

Parasites are integral to ecosystem functioning yet often overlooked. Improved understanding of host-parasite associations is important, particularly for wide-ranging species for which host range shifts and climate change could alter host-parasite interactions and their effects on ecosystem function.Among the most widely distributed mammals with diverse diets, gray wolves () host parasites that are transmitted among canids and via prey species. Wolf-parasite associations may therefore influence the population dynamics and ecological functions of both wolves and their prey. Our goal was to identify large-scale processes that shape host-parasite interactions across populations, with the wolf as a model organism.By compiling data from various studies, we examined the fecal prevalence of gastrointestinal parasites in six wolf populations from two continents in relation to wolf density, diet diversity, and other ecological conditions.As expected, we found that the fecal prevalence of parasites transmitted directly to wolves via contact with other canids or their excreta was positively associated with wolf density. Contrary to our expectations, the fecal prevalence of parasites transmitted via prey was negatively associated with prey diversity. We also found that parasite communities reflected landscape characteristics and specific prey items available to wolves.Several parasite taxa identified in this study, including hookworms and coccidian protozoans, can cause morbidity and mortality in canids, especially in pups, or in combination with other stressors. The density-prevalence relationship for parasites with simple life cycles may reflect a regulatory role of gastrointestinal parasites on wolf populations. Our result that fecal prevalence of parasites was lower in wolves with more diverse diets could provide insight into the mechanisms by which biodiversity may regulate disease. A diverse suite of predator-prey interactions could regulate the effects of parasitism on prey populations and mitigate the transmission of infectious agents, including zoonoses, spread via trophic interactions.
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http://dx.doi.org/10.1002/ece3.7837DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8328421PMC
August 2021

Broadening the toolset for stakeholder engagement to explore consensus over wolf management.

J Environ Manage 2021 Oct 9;296:113125. Epub 2021 Jul 9.

Istituto di Ecologia Applicata di Roma, Via B. Eustachio 10, 00161, Rome, Italy. Electronic address:

Facilitating coexistence between people and large carnivores is critical for large carnivore conservation in human-dominated landscapes, when their presence impacts negatively on human interests. Such situations will often require novel ways of mediating between different values, worldviews and opinions about how carnivores should be managed. We report on such a process in an agricultural area of recent wolf recovery in central Italy where unsolved social tensions over wolf presence have radicalized opinions on either side of the wolf debate, resulting in a stalemate. Where previous mitigation policies based on top-down damage compensation have failed, we tested the potential for applying a participatory approach to engage different stakeholder groups in a dialogue aimed at sharing a deep understanding of the problem and co-creating potential solutions. We based our approach on the theory of meta-consensus, using a decision support tool known as Multi Criteria Decision Analysis (MCDA). Over the course of three months, we carried out five workshops with stakeholder representatives from farming, hunting and environmental associations, and one biologist. Stakeholders shared several objectives and agreed over many management interventions, including the management of free-ranging dogs, the implementation of damage prevention measures, and a damage compensation system suitable for farmers. The process facilitated agreement over actions aimed at improving relations between stakeholders and enhancing the state of knowledge on the issues at stake. Most importantly, we recorded positive social and relationship outcomes from the workshops, and observed a willingness from participants to engage in further discussions over disputed management preferences. Overall, we found MCDA to be a useful tool for laying the groundwork for further participatory and deliberative processes on wolf management. However, challenges ahead included the involvement of a larger number of representatives of different social sectors, and a simplification of the methodology which some participants found too complicated and time consuming.
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http://dx.doi.org/10.1016/j.jenvman.2021.113125DOI Listing
October 2021

Gaining insight into the assimilated diet of small bear populations by stable isotope analysis.

Sci Rep 2021 Jul 8;11(1):14118. Epub 2021 Jul 8.

Department of Environmental Biology, Sapienza University of Rome, Rome, Italy.

Apennine brown bears (Ursus arctos marsicanus) survive in an isolated and critically endangered population, and their food habits have been studied using traditional scat analysis. To complement current dietary knowledge, we applied Stable Isotope Analysis (SIA) to non-invasively collected bear hairs that had been individually recognized through multilocus genotyping. We analysed carbon (δC) and nitrogen (δN) stable isotopes of hair sections and bear key foods in a Bayesian mixing models framework to reconstruct the assimilated diet on a seasonal basis and to assess gender and management status effects. In total, we analysed 34 different seasonal bear key foods and 35 hair samples belonging to 27 different bears (16 females and 11 males) collected during a population survey in 2014. Most bears showed wide δN and δC ranges and individual differences in seasonal isotopic patterns. Vegetable matter (herbs, fleshy fruits and hard mast) represented the major component of the assimilated diet across the dietary seasons, whereas vegetable crops were rarely and C4 plants (i.e., corn) never consumed. We confirmed an overall low consumption of large mammals by Apennine bears consistently between sexes, with highest values in spring followed by early summer but null in the other seasons. We also confirmed that consumption of fleshy fruits peaked in late summer, when wild predominated over cultivated fleshy fruits, even though the latter tended to be consumed in higher proportion in autumn. Male bears had higher δ N values than females in spring and autumn. Our findings also hint at additional differences in the assimilated diet between sexes, with females likely consuming more herbs during spring, ants during early summer, and hard mast during fall compared to males. In addition, although effect sizes were small and credibility intervals overlapped considerably, management bears on average were 0.9‰ lower in δ C and 2.9‰ higher in δ N compared to non-management bears, with differences in isotopic values between the two bear categories peaking in autumn. While non-management bears consumed more herbs, wild fleshy fruits, and hard mast, management bears tended to consume higher proportions of cultivated fruits, ants, and large mammals, possibly including livestock. Although multi-year sampling and larger sample sizes are needed to support our findings, our application confirms that SIA can effectively integrate previous knowledge and be efficiently conducted using samples non-invasively collected during population surveys.
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http://dx.doi.org/10.1038/s41598-021-93507-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8266819PMC
July 2021

Cost of Coexisting with a Relict Large Carnivore Population: Impact of Apennine Brown Bears, 2005-2015.

Animals (Basel) 2021 May 19;11(5). Epub 2021 May 19.

Department of Biology and Biotechnologies, University of Rome La Sapienza, 00185 Rome, Italy.

Human-carnivore conflicts are a major conservation issue. As bears are expanding their range in Europe's human-modified landscapes, it is increasingly important to understand, prevent, and address human-bear conflicts and evaluate mitigation strategies in areas of historical coexistence. Based on verified claims, we assessed costs, patterns, and drivers of bear damages in the relict Apennine brown bear population in the Abruzzo Lazio and Molise National Park (PNALM), central Italy. During 2005-2015, 203 ± 71 (SD) damage events were verified annually, equivalent to 75,987 ± 30,038 €/year paid for compensation. Most damages occurred in summer and fall, with livestock depredation, especially sheep and cattle calves, prevailing over other types of damages, with apiaries ranking second in costs of compensation. Transhumant livestock owners were less impacted than residential ones, and farms that adopted prevention measures loaned from the PNALM were less susceptible to bear damages. Livestock farms chronically damaged by bears represented 8 ± 3% of those annually impacted, corresponding to 24 ± 6% of compensation costs. Further improvements in the conflict mitigation policy adopted by the PNALM include integrated prevention, conditional compensation, and participatory processes. We discuss the implications of our study for Human-bear coexistence in broader contexts.
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http://dx.doi.org/10.3390/ani11051453DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8158715PMC
May 2021

A deepening understanding of animal culture suggests lessons for conservation.

Proc Biol Sci 2021 04 21;288(1949):20202718. Epub 2021 Apr 21.

Sea Mammal Research Unit, School of Biology, University of St Andrews, St Andrews KY16 8LB, UK.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.
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http://dx.doi.org/10.1098/rspb.2020.2718DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8059593PMC
April 2021

Correlates of parasites and pseudoparasites in wolves () across continents: A comparison among Yellowstone (USA), Abruzzo (IT) and Mercantour (FR) national parks.

Int J Parasitol Parasites Wildl 2019 Dec 12;10:196-206. Epub 2019 Sep 12.

Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, CH-2000, Neuchâtel, Switzerland.

Little is known about the impact of infectious diseases on large carnivores. We investigated factors structuring the helminth and protozoan infections of wolves () by using coprological analyses. Faecal samples (n = 342) were analysed from 11 wolf packs belonging to three different geographical and ecological settings in Italy (Abruzzo, Lazio e Molise National Park, PNALM: 4 packs, 88 samples), in France (Mercantour National Park, PNM: 4 packs, 68 samples) and in the U.S.A. (Yellowstone National Park, YNP: 3 packs, 186 samples). Parasites were found in 29.4%-88.6% of the samples and parasite taxa ranged from four to ten in each study area. Taeniidae (), spp and were most common in faecal samples from YNP, whereas spp., Taeniidae and were predominant in PNALM. We used generalised linear mixed models to assess the relationship between parasite infection or the number of parasite taxa and selected ecological drivers across study areas. Significant effects illustrated the importance of the ecological factors such as occurrence of free-ranging dogs, diet composition and wolf density, as well as the ancestry of the wolf populations, in shaping parasite-wolf communities. Additional investigations are needed to elucidate the impact of parasitic infections on wolf populations, as well as the role of anthropogenic factors in facilitating parasitic diffusion to apex predators.
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http://dx.doi.org/10.1016/j.ijppaw.2019.09.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6812024PMC
December 2019

Use of hidden Markov capture-recapture models to estimate abundance in the presence of uncertainty: Application to the estimation of prevalence of hybrids in animal populations.

Ecol Evol 2019 Jan 5;9(2):744-755. Epub 2019 Feb 5.

CEFE, CNRS University of Montpellier, University Paul Valéry Montpellier 3, EPHE, IRD Montpellier France.

Estimating the relative abundance (prevalence) of different population segments is a key step in addressing fundamental research questions in ecology, evolution, and conservation. The raw percentage of individuals in the sample (naive prevalence) is generally used for this purpose, but it is likely to be subject to two main sources of bias. First, the detectability of individuals is ignored; second, classification errors may occur due to some inherent limits of the diagnostic methods. We developed a hidden Markov (also known as multievent) capture-recapture model to estimate prevalence in free-ranging populations accounting for imperfect detectability and uncertainty in individual's classification. We carried out a simulation study to compare naive and model-based estimates of prevalence and assess the performance of our model under different sampling scenarios. We then illustrate our method with a real-world case study of estimating the prevalence of wolf () and dog () hybrids in a wolf population in northern Italy. We showed that the prevalence of hybrids could be estimated while accounting for both detectability and classification uncertainty. Model-based prevalence consistently had better performance than naive prevalence in the presence of differential detectability and assignment probability and was unbiased for sampling scenarios with high detectability. We also showed that ignoring detectability and uncertainty in the wolf case study would lead to underestimating the prevalence of hybrids. Our results underline the importance of a model-based approach to obtain unbiased estimates of prevalence of different population segments. Our model can be adapted to any taxa, and it can be used to estimate absolute abundance and prevalence in a variety of cases involving imperfect detection and uncertainty in classification of individuals (e.g., sex ratio, proportion of breeders, and prevalence of infected individuals).
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http://dx.doi.org/10.1002/ece3.4819DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6362442PMC
January 2019

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers.

Proc Natl Acad Sci U S A 2017 11 24;114(45):E9589-E9597. Epub 2017 Oct 24.

Department of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles () can be an important driver of divergence in isolation, () can be tolerated when balancing selection prevents random loss of variation at important genes, and () is followed by or results directly in favorable behavioral changes.
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http://dx.doi.org/10.1073/pnas.1707279114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5692547PMC
November 2017

Environmental and Intrinsic Correlates of Stress in Free-Ranging Wolves.

PLoS One 2015 23;10(9):e0137378. Epub 2015 Sep 23.

Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.

Background: When confronted with a stressor, animals react with several physiological and behavioral responses. Although sustained or repeated stress can result in severe deleterious physiological effects, the causes of stress in free-ranging animals are yet poorly documented. In our study, we aimed at identifying the main factors affecting stress levels in free-ranging wolves (Canis lupus).

Methodology/principal Findings: We used fecal cortisol metabolites (FCM) as an index of stress, after validating the method for its application in wolves. We analyzed a total of 450 fecal samples from eleven wolf packs belonging to three protected populations, in Italy (Abruzzo), France (Mercantour), and the United States (Yellowstone). We collected samples during two consecutive winters in each study area. We found no relationship between FCM concentrations and age, sex or social status of individuals. At the group level, our results suggest that breeding pair permanency and the loss of pack members through processes different from dispersal may importantly impact stress levels in wolves. We measured higher FCM levels in comparatively small packs living in sympatry with a population of free-ranging dogs. Lastly, our results indicate that FCM concentrations are associated with endoparasitic infections of individuals.

Conclusions/significance: In social mammals sharing strong bonds among group members, the death of one or several members of the group most likely induces important stress in the remainder of the social unit. The potential impact of social and territorial stability on stress levels should be further investigated in free-ranging populations, especially in highly social and in territorial species. As persistent or repeated stressors may facilitate or induce pathologies and physiological alterations that can affect survival and fitness, we advocate considering the potential impact of anthropogenic causes of stress in management and conservation programs regarding wolves and other wildlife.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0137378PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4580640PMC
May 2016

Recovery of large carnivores in Europe's modern human-dominated landscapes.

Science 2014 Dec;346(6216):1517-9

University of Ljubljana, Biotechnical Faculty, Jamnikarjeva 101, 1000 Ljubljana, Slovenia.

The conservation of large carnivores is a formidable challenge for biodiversity conservation. Using a data set on the past and current status of brown bears (Ursus arctos), Eurasian lynx (Lynx lynx), gray wolves (Canis lupus), and wolverines (Gulo gulo) in European countries, we show that roughly one-third of mainland Europe hosts at least one large carnivore species, with stable or increasing abundance in most cases in 21st-century records. The reasons for this overall conservation success include protective legislation, supportive public opinion, and a variety of practices making coexistence between large carnivores and people possible. The European situation reveals that large carnivores and people can share the same landscape.
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http://dx.doi.org/10.1126/science.1257553DOI Listing
December 2014
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