European Journal of Wildlife Research (2023) 69:79 https://doi.org/10.1007/s10344-023-01700-3 BRIEF REPORT The synzootic potential of common epidemics in chamois populations Cristina Garrido‑Amaro1,2 · Anna Jolles3 · Roser Velarde1,2 · Jorge Ramón López‑Olvera1,2 · Emmanuel Serrano1,2 Received: 2 March 2023 / Revised: 27 May 2023 / Accepted: 6 June 2023 / Published online: 18 July 2023 © The Author(s) 2023 Abstract Southern chamois (Rupicapra pyrenaica) is a medium-sized and gregarious mountain ungulate with populations affected by periodic outbreaks of border disease virus (BD), infectious keratoconjunctivitis (IKC), and sarcoptic mange (SM). Even though the impact of each disease on chamois populations has been described in detail, there is a lack of information about the potential impact of concomitant epidemics and the synzootic potential (co-occurring enzootic or epizootic processes producing worse health outcomes in wildlife) on chamois populations. Furthermore, whether a specific order of appari- tion of epidemics is more or less harmful for the host population is practically unknown not only for chamois but also for most mammal populations. Using a population viability analysis (PVA), we studied the consequences of multiple disease outbreaks with synzootic potential on growth rates and probabilities of extinction of virtual populations exposed to hard winters, density dependence, and co-occurring BD, IKC, and SM outbreaks. Such infections are not under cross-immunity nor density-dependent processes and thus are supposed to affect population demography independently. Heavy snowfalls are also likely to occur in our simulated populations. Our simulations showed that a second outbreak, even caused by a low virulent pathogen, causes an increase in the probability of extinction of the host population with regard to the first outbreak. IKC-BD- and SM-BD-affected populations had a higher risk of becoming extinct in 50 years confirming the extra risk of multiple outbreaks on the viability of the affected populations. Keywords Emerging infectious diseases · Epidemics · Population viability analysis · Rupicapra pyrenaica pyrenaica · Vortex For more than four decades now, infectious diseases have lions (Panthera leo) (Roelke-Parker et al. 1996) or Ebola in been recognized as a major demographic driver of wild African apes (Leroy et al. 2004) are good examples of such populations. Virus (Sillero-Zubiri et al. 1996), bacteria deleterious impacts. Pathogens have the potential to affect (Foreyt and Jessup 1982), fungi (Berger et al. 1998), or almost every life-history trait of mammals including energy helminth (Goodman and Johnson 2011) outbreaks increase storage (Carvalho et al. 2015), fecundity and fertility rates the extinction risk of wildlife (Pedersen et al. 2007), threat- (Rhyan et al. 2001; Sarasa et al. 2011), to fetus development ening global biodiversity (Daszak et al. 2000). Population (Aleuy et al. 2020), juvenile recruitment (Rossi et al. 2011,) collapses caused by canine distemper virus in Serengeti or adult survival (Pedersen et al. 2007). Further, the main mechanisms for disease-induced extinctions in wildlife are * Cristina Garrido‑Amaro the pre-epidemic population size and the presence of reser- cristinagarridoa@gmail.com voirs (Castro and Bolker 2005). * Emmanuel Serrano Even though outbreaks caused by different pathogens are emmanuel.serrano@uab.cat not rare in the wild (Barnett et al. 2018), our knowledge about the impact of synzootics (i.e., co-occurring wildlife 1 Wildlife Ecology & Health Group (WE&H, www.weh. diseases) on mammal population demography is scarce. This cat), and Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat synzootic concept derives from the term “syndemic”, used Autònoma de Barcelona (UAB), Bellaterra, Barcelona, Spain in human medicine to assess the consequences of multiple 2 Departament de Medicina i Cirurgia Animals, Facultat de diseases acting in tandem in a given socio-economic and Veterinària, Universitat Autònoma de Barcelona (UAB), environmental conditions on human populations (Singer Edifici V, E‑08193 Bellaterra, Barcelona, Spain et al. 2017). This syndemic point of view has barely been 3 Department of Biomedical Sciences, Oregon State applied to wildlife (Sweeny et al. 2021), although the risk of University, Corvallis, OR, USA 13 Vol.:(0123456789) 79 Page 2 of 7 European Journal of Wildlife Research (2023) 69:79 suffering from multiple infections in variable environments decided to not include the density dependence in mange out- is the norm (Bordes and Morand 2011; Munson et al. 2008) breaks in our viability modelling due to a lack of information and thus the likelihood of potential synzootic interactions for density dependence transmission parameters. is great. Knowledge about the impact of infectious diseases SM outbreaks duration is 5 years on average (Serrano on wildlife demographics is mainly based on outbreaks by et al. 2015). Mortality rates associated with SM are roughly single pathogens. Information about the impact of synzoot- 10.5% for kids, 14% for yearlings, 52.5% for adult females, ics on wildlife is limited and often restricted to the impact and 60% for adult males (Fernando-Morán et al. 1997; Rossi of comorbidities. Only a few cases such as European wild et al. 2007). rabbit (Oryctolagus cuniculus) populations affected by rab- IKC, on the other hand, is a highly contagious bacterial bit hemorrhagic disease (RHD) but previously exposed to disease of the eye characterized by inflammation of the con- myxoma virus (Mutze et al. 2002) are a good example of junctiva and cornea (Nicholas and Giacometti 2012). Myco- the potential of co-occurring epidemics on host population plasma conjunctivae is considered the major cause of IKC in dynamics. With regard to synzootics, the unprecedented caprine species (Giacometti et al. 2002). IKC outbreaks are mortalities of African lion populations affected by canine characterized by a short duration (1–2 years), high morbid- distemper virus (CDV) and Babesia spp. in very dry years ity, low mortality (around 30%), and spontaneous recovery are an excellent case (Munson et al. 2008). (Loison et al. 1996). After an IKC epizootic episode, the Southern chamois (Rupicapra pyrenaica) is a medium- number of kid and adult females typically decreases between sized mountain ungulate classified as a least concern species 10 and 19% (Arnal et al. 2013), recovering 1 year after the by the International Union for the Conservation of Nature, outbreak. Mortality rates associated with IKC are in 6% of with a global population number of around 50,000 (Herrero kids, 70% of yearlings, 20% of females, and 9% of males (% et al. 2020). Nevertheless, outbreaks of diseases such as sar- of kids, 52% of yearlings) (Loison et al. 1996; Arnal et al. coptic mange (SM), infectious keratoconjunctivitis (IKC), 2013). and border disease (BD) affect and have caused dramatic On the other hand, BD is caused by a pestivirus (Frölich declines in local populations of the Pyrenean (Rupicapra p. et al. 2012) and in chamois curses emaciation, depression, pyrenaica) and Cantabrian (Rupicapra p. parva) subspecies weakness and difficulties in locomotion (Marco et al. 2007). (Fernández-Morán et al. 1997; Marco et al. 2007; Fernán- Pyrenean chamois population in the Pyrenees decreased by dez-Aguilar et al. 2017). 30% due to disease outbreaks (Frölich et al. 2012), which SM is caused by the burrowing mite Sarcoptes scabiei are considered important drivers for chamois population and is a contagious disease of mammals that induces an demography (Serrano et al. 2015). Published reports (Marco allergic-type skin reaction resulting in visible hypersensi- et al. 2007; Fernández-Sirera et al. 2012) suggest that mor- tive lesions and pruritus (Walton et al. 2004). Although tality rates associated with BD outbreaks are 50.5% for kids, sarcoptic mange epizootics usually do not affect long-term 51.8% for yearlings, 45.7% for females, and 47% for males. population dynamics, the net effect of mange can have seri- The consequences of BD are easily observed 5 years after ous conservation consequences in remnant or fragmented the first clinical case is detected. The three aforementioned populations of threatened or endangered species including diseases do not induce cross-immunity, and there is no clear mountain ungulates (Pence and Ueckermann 2002). Apart evidence for their density-dependent regulation (Fernández- from the Cantabrian Mountains, SM has been reported to Sirera et al. 2012). cause mortality in Alpine chamois (Rupicapra rupicapra In this work, we aimed to simulate the impact of multiple rupicapra) in the Dolomite Alps in Italy (Rossi et al. 2007). outbreaks on chamois population demography. Our objec- Contrary to the typical assumptions of epidemiological mod- tives are (I) to explore the consequences of consecutive out- els, SM dynamics in carnivores seem to be frequency- rather breaks of SM, IKC, and BD on chamois population viabil- than density-dependent. In other words, disease transmis- ity and (II) to determine the specific outbreak pair with the sion is mainly driven by behaviors mediating contact rates greater demographic impact on the viability of our virtual (Devenish-Nelson et al. 2014). chamois population. To achieve these objectives, we mod- In Rupicapra species, social interactions (e.g., contact elled the consequences of single (SM, IKC and BD) and spe- rates) depend more on social affinities than on any other cific disease outbreak combinations (SM + IKC, SM + BD factors (Crampe et al. 2021). However, in the last work on and IKC + SM) on the viability of a virtual chamois popula- Sarcoptes scabiei transmission (Browne et al. 2022), the tion using a stochastic population viability analysis (PVA, authors stated that high population densities and local popu- Lacy 1993). Since the impact of chronic BD epidemics is lation sizes would be key factors for Sarcoptes transmission not well understood (Fernandez-Sirera et al. 2012), we have in chamois, but they also argued that the rates of contact decided not to include a secondary outbreak in BD-affected within each species are poorly understood. So, this density- populations. We expect that multiple outbreaks will have dependent transmission issue is unclear, and thus, we have greater negative effects than single outbreaks, but more 13 European Journal of Wildlife Research (2023) 69:79 Page 3 of 7 79 particularly, those combinations involving the more viru- disease outbreak for each simulation is 0.2 for IKC (the com- lent pathogens such as BD or SM. From now on, when we monest disease in chamois populations) and 0.1 for SM and discussed about the extinction of the population in the simu- BD. Two diseases can occur simultaneously or sequentially lation, we refer to the probability that a chamois population at the given probabilities. Since there is a likelihood of heavy can become extinct locally rather than globally after a poten- winters during disease outbreaks, we consider our modelling tial combination of different disease outbreaks. might reflect the effect of synzootics (comorbidity + adverse Population viability analysis was performed in VORTEX environmental conditions, see Sweeny et al. (2021). 10.1.6.0 (Lacy and Pollak 2015). This computer program Each model scenario was run for 50 years, 1000 itera- simulates the effects of deterministic forces and stochastic tions, and 20 initial population sizes proportional to the events (demographic, environmental, and genetic) to model carrying capacity (from 5 to 100%, with an increment of the growth rate (stoch-r), the final population size (N-all), 5% each time). The Vortex software, however, does not and the mean probability of extinction (PE). To compare the provide population-size-specific outputs (see Table 1 and impact of different simulations, we created a control sce- Fig. 1 for a summary). We used non-parametric Mann- nario (pristine population), only affected by winter condi- Whitney U tests to compare the mean growth rate (stoch- tions (Serrano et al. 2015). The effects of heavy winters have r), the average population size of a given scenario at also been included in our population viability modelling. the end of the simulation (averaging both surviving and This winter effect strongly relies on the local orography, but extinct iterations, N-all), and the probability of extinction on average, population reduction due to this natural phenom- (PE) between specific outbreak pairs. We performed all the enon could reach 40% every 10 years (Rughetti et al. 2011). statistical analyses using the statistical software R 4.2.1 (R In this scenario, the carrying capacity was fixed at 4000 Development Core Team 2022). individuals. We also recreated seven disease scenarios rep- The probability of extinction in the pristine scenario was resenting single outbreaks (IKC, SM, and BD), and outbreak equal to zero, and the final population size was stabilized combinations using the IKC-, SM-, and BD-associated mor- around the carrying capacity as expected in populations talities at specific age classes. In brief, we modelled age and with density dependence regulation (Akçakaya and Burg- sex-specific mortalities based on the descriptions found in man 1999). The effect of a single outbreak causes a sig- the published reports (Serrano et al. 2015). The likelihood of nificant decrease in the growth rate of our virtual chamois Table 1  Mean, minimum (min), and maximum (max) stochastic growth rates of the population, probabilities of extinction, and final population sizes of a hypothetical chamois population of an initial size of 600 individuals and limited by a carrying capacity of 4000 individuals Scenario Population Probability Final growth rate of extinction population size Mean Interval Mean Interval Mean Interval (min–max) (min–max) (min-max) Pristine 0.0635 0.0620–0.0650 0 - 3723.57 3282.24–3795.69 population Single disease outbreaks IKC outbreak 0.0463 0.0440/0.0540 0.25 0.241–0.263 2782.79 2180.39–2857.37 SM outbreak −0.0065 −0.0090/0.0080 0.229 0.217–0.780 1441.52 597.53–1594.47 BD outbreak −0.0326 −0.0370/−0.003 0.534 0.524–0.571 767.86 345.47–865.86 Combined disease outbreaks IKC + SM out- −0.0349 −0.0410/−0.0090 0.47 0.370–0.549 619.67 245.59–711.92 breaks IKC + BD out- −0.0533 −0.0610/−0.0160 0.634 0.594–0.700 343.22 126.57–430.72 breaks SM + IKC out- 0.0323 0.0290/0.0410 0.253 0.241–0.264 1288.04 1590.07–1398.56 breaks SM + BD out- −0.0400 −0.0460/−0.0100 0.559 0.537–0.617 585.72 213.31–667.66 breaks Simulations were estimated for 50 years and 1000 iterations. The pristine population (control) was only affected by the carrying capacity, the IKC, SM, and BD single outbreaks of infectious keratoconjunctivitis (IKC), sarcoptic mange (SM), and border disease (BD), and the IKC + SM, IKC + BD, SM + IKC, and SM + BD combined disease outbreaks 13 79 Page 4 of 7 European Journal of Wildlife Research (2023) 69:79 Fig. 1  a Mean stochastic growth rates (stoch-r) and b mean probabilities of extinction (PE), of a hypothetical chamois population of an initial size of 600 individuals and limited by a carrying capacity of 4000 individuals. Our modelling scenarios were the following: pristine population (population only limited by the carrying capacity in light green), the single outbreak scenarios (in blue color), and combined disease outbreaks (dark green). Infectious keratoconjunctivitis (IKC), sarcoptic mange (SM), and border disease (BD). In b, sqrtPE of our pristine chamois population was equal to zero. A, B and C respresnt Sarcoptes scabiei Mycoplasma spp and a pestiviurs respectively 13 European Journal of Wildlife Research (2023) 69:79 Page 5 of 7 79 population. Compared to pristine populations, the mean Author contribution CGA, RV, AJ, and ES conceived and designed the probability of extinction after a single disease outbreak modelling; CGA performed the analytic calculations and performed numerical simulations; CGA and ES wrote the manuscript with the increased from 0.22 for SM to 0.53 for BD epidemics that support from JRLO, RV, and AJ. All authors discussed the results and means that 22% and 53% of the simulated populations get contributed to the final manuscript. extinct, respectively. IKC outbreaks resulted in an intermedi- ate probability of extinction value (0.25, see Table 1). Funding Open Access Funding provided by Universitat Autonoma de Barcelona. E. Serrano was supported by the Spanish Ministerio Our population viability modelling clearly shows the de Economía y Competitividad (MINECO) through a Ramón y Cajal negative impacts of a second disease outbreak. PE increased agreement (RYC-2016-21120). after a second disease outbreak but in particular after BD epidemics. Along the same lines, the growth rate and popula- Data Availability The data that support the findings of this study are available from the corresponding author, (CGA, ES), upon reasonable tion size decreased after the second outbreak. For example, request. SM or BD outbreaks in chamois populations initially affected by IKC resulted in lower growth rate ­(WIKC vs IKC-SM = 400, Declarations p value = 5.8 e-10, ­WIKC vs IKC-BD = 400, p value = 6.02 e-10) and final population size ­(WIKC vs IKC-SM = 400, p Conflict of interest The authors declare no competing interests. value = 1.45 e-11, ­WIKC vs IKC-BD = 400, p value = 1.5 e-10), Open Access This article is licensed under a Creative Commons Attri- but higher PE (­WIKC vs IKC-SM = 400, p value = 6.73 e-08, bution 4.0 International License, which permits use, sharing, adapta- ­WIKC vs IKC-BD = 400, p value = 6.76 e-08) than those only tion, distribution and reproduction in any medium or format, as long affected by IKC. The same happened in SM-affected pop- as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes ulations suffering BD outbreaks, where the growth rate were made. The images or other third party material in this article are ­(WSM vs SM-BD = 400, p value = 5.1 e-08) and final population included in the article's Creative Commons licence, unless indicated sizes ­(WSM vs SM-BD = 336, p value = 9.2 e-07) are lower than otherwise in a credit line to the material. If material is not included in in populations only affected by SM. Final population sizes the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will in mixed epizootics decreased in 59% ­(WSM vs SM-BD = 400, need to obtain permission directly from the copyright holder. To view a p value = 6.7 e-08). For example, the mean probability of copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. extinction for IKC + SM outbreaks is 0.47, whereas = 0.25 or 0.22 for single IKC or SM epizootics. 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