Threats to Site Occupation of Carnivores: A Spatiotemporal Encroachment of Non-native Species on the Native Carnivore Community in A Human-dominated Protected Area

© 2021 Academia Sinica, Taiwan Open Access Threats to Site Occupation of Carnivores: A Spatiotemporal Encroachment of Non-native Species on the Native Carnivore Community in A Human-dominated Protected Area Kasereka Vitekere1,4 , Luc Mumbere Lango2, Jiao Wang1, Mengyan Zhu1, Guangshun Jiang1,*, and Yan Hua3,* 1Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin, Heilongjiang, 150040, P.R. China. *Correspondence: E-mail: [email protected] (Jiang). E-mail: [email protected] (Vitekere); [email protected] (Wang) 2Research Center for Environmental Planning, Goma, Democratic Republic of Congo. E-mail: [email protected] (Lango) 3Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou 510520, China. *Correspondence: E-mail: [email protected] (Hua) 4University of Goma, Faculty of Sciences, Goma, North-Kivu, 204, Democratic Republic of Congo. Received 4 January 2021 / Accepted 6 June 2021 / Published 16 September 2021 Communicated by Jian-Nan Liu Interspecific interactions of commensal non-native species such as domestic dogs and livestock with native wildlife are evident issues in protected areas (PAs). We studied spatiotemporal interactions by combining camera trap photographic sampling over three years. We used a generic multiseason occupancy and cooccurrence analysis and kernel density estimates of temporal activity. We accumulated a total of 1,305 and 1,557 independent photo-captures respectively for non-native and carnivore species during 26,216 trap nights. We found that non-native and carnivore species did not show substantial changes in occupancy rate over time. Yet both kinds of species were frequently detected. Carnivores had lower values of occupancy equilibrium than non-native species in seasons one and two. Domestic dogs directly occurred with native carnivores (except with leopards in season one), while the human and livestock presence displayed direct (Species Interaction Factors > 1) and indirect (Species Interaction Factors close to 1) cooccurrence, respectively, with the leopard and two mesocarnivores. The leopard cat was the least spatially influenced carnivore by the non-native species interactions. Furthermore, the leopard had higher temporal overlap (high Δ4) with all non-native species than the leopard cat and red fox (low Δ4). Our study exposes the negative impact of free-ranging non-native species across this protected area on native carnivore occupancy. An evaluation of the interconnections among non-native and carnivore species across diverse PA management regimes is crucial to develop robust landscape-scale conservation strategies. Key words: Conservation and management, Non-native and carnivore species, Overlap, Protected area, Spatiotemporal patterns. BACKGROUND Protected Areas (PAs) are the most widely-known and well-accepted strategy for protecting ecosystems and biodiversity (Chape et al. 2005; Dudley 2008; Mwakatobe et al. 2013). Protected areas have proven to be effective in protecting species’ habitats from landuse changes occurring outside of the protected areas (Andam et al. 2008). They represent one of the most significant global surface areas dedicated to a common Citation: Vitekere K, Lango LM, Wang J, Zhu M, Jiang G, Hua Y. 2021. Threats to site occupation of carnivores: a spatiotemporal encroachment of non-native species on the native carnivore community in a human-dominated protected area. Zool Stud 60:52. doi:10.6620/ZS.2021.60-52. Zoological Studies 60:52 (2021) doi:10.6620/ZS.2021.60-52 1 © 2021 Academia Sinica, Taiwan goal (after areas used for food production), that of preserving global biodiversity (Palomo et al. 2014). In their regular management, PAs typically face many difficulties (Cromsigt et al. 2013; Zaman et al. 2020). One of the most common issues is human interactions with wildlife, which can manifest in different forms (Treves and Karanth 2003; Okello et al. 2014) and often generates misunderstandings between PA managers and the local population. Carnivores need large living spaces for their daily activities, which include hunting and walking (Treves and Karanth 2003). To meet these needs, large carnivores typically use resources outside of PAs (Hansen et al. 2002; Treves and Karanth 2003), potentially bringing them into contact with human landuse activities such as livestock and crop production (Morehouse and Boyce 2017). Conflicts between nonnative and native carnivore species can lead to largescale ecosystem disturbances. The presence of non-native species in PAs poses a threat to native carnivorous species in both space usage and temporal activities. The human activities within and around PAs within landscapes lead to the presence of domestic dogs (Farris et al. 2017) and livestock species (Vanak and Gompper 2010), which have harmful consequences on wildlife. The most cited effects of this include carnivores preying upon invasive livestock (Treves and Karanth 2003), causing non-native species to destabilise (Morehouse and Boyce 2017), and spreading diseases to native carnivore species in the PAs (Okello et al. 2014). They also create edge effects and habitat fragmentation (Gerber et al. 2012a; Sleeman 2013; Vanak et al. 2013; Brodie et al. 2015; Chanchani et al. 2016). Non-native species (especially carnivores) often significantly increase pressure on native carnivores by modifying their spatiotemporal activity patterns and habitat use (Gerber et al. 2012b; Farris et al. 2015) and decreasing prey availability (Young et al. 2011). When non-native species are livestock, native carnivores can alter their natural diet because herds will seem like easy prey (Okello et al. 2014; Ciucci et al. 2018). Cited effects (disease transmission, spatio-temporal destabilisation, prey decrease, preying on livestock) can lead to decreased carnivore survival within the habitat and generate negative consequences on the whole landscape with the reduction of the carrying capacity in the ecosystem. Carnivores are greatly sensitive to disturbances inside and outside of PAs and are negatively affected by edge effects and human presence (poaching or human-wildlife conflict) occurring around PAs (Wearn et al. 2012; Sleeman 2013; Hua et al. 2020). Therefore, carnivore population wellbeing is expected to be driven by species-specific tolerance to microenvironment change, habitat fragmentation and PA edge effects, human presence, non-native species density, and prey availability. All these facts are essential in and around PAs and must be well managed to ensure species sustainability (Farris et al. 2017). The Tieqiaoshan Provincial Nature Reserve (TPNR) contains some of the largest North China leopard (Panthera pardus japonensis, Gray 1862) populations in China (Vitekere et al. 2020a; Zhu et al. 2021). Most of the North China leopard populations are within 22 Nature Reserves situated in the Taihang Mountains and some nearby regions (Song et al. 2014), but most of these PAs have not been surveyed and accurate population estimates are lacking. Thus, little is known about this leopard subspecies living in a guild with two mesocarnivores, the leopard cat (Prionailurus bengalensis, Kerr 1792) and the red fox (Vulpes vulpes, Linnaeus 1758), within the TPNR ecosystem (Hua et al. 2020). This landscape hosts a considerable human population density (local people), with livestock activities facilitating the invasion of the integral conservation zone of the TPNR by dogs, livestock, and humans (e.g., Farris et al. 2017). Few studies have examined the conservation status of these carnivores and the effects of non-native species introduced by the shepherds in the PAs. Hua et al. (2020) highlighted the effect of human presence on the detectability of these carnivores. Still, the longterm effects and the coexistence with non-native species remain unstudied within the TPNR landscape. We carried out a multi-year study on the coexistence between non-native species—the domestic dog (dog), livestock and herdsmen (human)—and native carnivores—North China leopard (leopard), leopard cat and red fox (fox)—within TPNR, one of the Taihang Mountains landscapes. We first hypothesized that carnivores would not depict the stability of occupancy contrarily to non-native species’ over the years. We also hypothesized that all three native carnivores would have a real coexistence defined as “apparent co-occurrence” or “direct interaction” with non-native species, and they would portray increasing Species Interaction Factors (SIF: a parameter describing the spatial interactions of two species in an area, previously computed by Alexander et al. (2016) and Farris et al. (2020)) over the years. Human detection, particularly, would markedly affect native species since the two others (livestock and dog) are human presence-dependent. We finally hypothesized that non-native and carnivore species would not temporally overlap, since non-native and native carnivore species diurnal and nocturnal, respectively. Studying these multi-year spatiotemporal interactions in a landscape with human invasion (bringing invasive species) will help assess the effectiveness of management policies for the page 2 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan conservation of these carnivores in TPNR. The findings of this work will provide further suggestions to improve strategies for sustainably managing PAs that host nonnative species. MATERIALS AND METHODS Study Area The TPNR is a reserve in China that hosts the North China leopard sub-species. This PA has GPS coordinates: 111°25'E to 114°17'E and 36°39'N to 38°06'N (Fig. 1), with an elevation ranging from 1300 to 1827 m. The TPNR is a Protected Area, approved by the provincial administration by document No. 124. Officially established in 2009, this PA was assigned a total of 353.52 km2 (Zhu et al. 2021) divided into an area of integral protection (139.5 km2), a buffer zone (74.2 km2), and a multi-use zone. The annual average of rainfall varied from 500 mm to 700 mm, with heavy rains in the period July-September (Hua et al. 2020). This area did not present high daily and yearly thermal amplitude, with mean temperatures of 10°C and 6°C, respectively (Zheng et al. 2009). One of the principal characteristics of this PA is that it hosts humans (Zhu et al. 2021), an estimated 2,000 of them, meaning that the PA had always experienced disturbances from humans (Hua et al. 2020). A significant part of the area is a mixture of primary and secondary forests, and the remaining parts are shrubs. Wildlife is abundant within the PA, including mammals (carnivores: leopard, leopard cat, fox, badger, etc.; artiodactyl: many kinds of deer and the wild boar), and a diversified fauna of reptiles, amphibians, and birds (Song et al. 2014). Methods Data Collection We collected data on the presence and absence of three native carnivore species and three non-native species for a total of 383 days over 3 years: 130 (March– July 2017), 119 (September–December 2018) and 134 (March–June 2019), comprising three sampling periods (SP1, SP2, and SP3) and two interseasons (IS1 and IS2), according to Farris et al. (2017). We used two brands of cameras: the Eastern Red Hawk E1B 6210M (Shenzhen Ereagle Technology Co. Ltd, Shenzhen, China) and the LTL6210MM (LTL Acorn Trail Camera, United Fig. 1. The data collection sites within the Tieqiaoshan Provincial Nature Reserve and villages housing herdsmen in and around the Protected Area. N page 3 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan Kingdom). Both brands were triggered remotely by an infrared sensor to record animal activity, following Karanth et al. (2003) and Swann et al. (2011). SP1 contained 81 cameras while SP2 and SP3 contained 62 cameras. Cameras were deployed within 27 4 km × 4 km quadrants in the study area, attached to trees at an average height of 0.5 m. Each data collection site had two or three cameras installed to face each other. Where possible, cameras were placed on trails, but otherwise they were placed at points thought to maximise the visibility of the animals. Cameras were set to capture data with the time and date automatically displayed on the photos (e.g., Barrull et al. 2014). Each camera operated for at least 100 consecutive days in each sampling period. Data Analysis Spatial patterns We first aggregated data from more than 100 days of capture within each sampling period into multiple shorter intervals. In SP1 and SP3, each survey (sampling occasion) was two weeks long, while in SP2 is was 10 days. This data aggregation allowed standardisation of the three sampling periods (e.g., Bu et al. 2016; Farris et al. 2017) and provided multiple surveys within each sampling period, as required for occupancy modelling (Alexander et al. 2016; MacKenzie et al. 2006). We considered a species to be detected if it was present at a site in an interval of aggregated days. Otherwise, it was not detected. We then performed two different occupancy analyses to investigate interactions between native carnivore and non-native species: the multiseason occupancy and the multiseason co-occurrence analyses. Occupancy analysis is based on collecting occurrence data for studied species within data collection sites. Species can be imperfectly detected; therefore, n sites are visited on t sampling occasions, and the presence/ absence of each targeted species is recorded on each occasion (MacKenzie et al. 2003). We used the software PRESENCE (version 5.8 < 130315.0823 > by James E Hines). This modelling using presence/absence data for different species allowed us to estimate changes in occupancy for all species over three years to test if there is an apparent spatial co-occurrence between native carnivores and non-native species, and finally to assess the influence of non-native species on the occupancy and detection probabilities of native species. In the first step (multiseason occupancy), parameters estimated can depict variations across time: the probability of occupancy (ψ), the probability of detection (p), the colonisation rate (γ), and the local extirpation rate (ε); all estimate values were accompanied by their standard errors. We estimated these parameters to determine the general trend of site occupation of species across years. Following MacKenzie et al. (2006), two derived parameters were also computed for the interpretation of the occupancy dynamics: (1) the rate of change in occupancy: λ't = ψt+1/(1-ψt+1) ψt/(1-ψt) (eq1 MacKenzie et al. 2006) (2) the occupancy equilibrium: ψequilibrium = γ ⁄ (γ + ε) (eq2 MacKenzie et al. 2006) In the second step (multiseason co-occurrence), we computed the co-occupancy and co-detection parameters (Table 1), and the SIF (φ). This latter parameter describes the species’ interactions in an area, where φ < 1 indicates no interaction or avoidance, φ > 1 indicates direct interaction or apparent co-occurrence and φ = 1 indicates independent or indirect cooccurrence (Alexander et al. 2016; Farris et al. 2020). We then used the Chi-squared test of independence to verify if the occupancy of a carnivore computed as single species is independent from the same species’ occupancy in a co-occurrence (two species) pattern. Temporal patterns The time that a species was captured was automatically stamped on species photographs. We removed any subsequent photos of the same species at the same site that occurred within 30 minutes to minimize pseudo-replication biases (e.g., Monterroso et al. 2013; Sunarto et al. 2015; Farris et al. 2017). All photos of a species remaining in the dataset after the application of this filter were considered to be independent observations. We compared the day and night visibility of species by calculating the proportion of detections that occurred in two intervals: 06:00–18:00 for daytime and 18:00–06:00 for night-time to test the species’ “nocturnality.” A species was categorized to prefer night-time or daytime when its detection rate was ≥ 70%, respectively, in the 06:00–18:00 and 18:00–6:00 time interval (e.g., Dias et al. 2018; Hua et al. 2020). To analyze the temporal activity overlap between non-native species and native carnivore, we calculated the kernel density estimates (KDEs) using the R package overlap (Oliveira-Santos et al. 2013; Meredith and Ridout 2014). We assessed the temporal overlap coefficient (Δ4) to compare activity patterns of all pairwise species combinations of non-native species and native carnivores. The overlap coefficient is a metric that ranges from zero, meaning the absence page 4 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan of overlap, to one, meaning complete overlap (Linkie and Ridout 2011; Meredith and Ridout 2014). As our sample was large (n > 75), we estimated the overlap coefficient using the estimator Dhat4 (e.g., Guerisoli et al. 2019) denoted Δ4. We computed the 95% confidence interval (hereafter, 95% CI) from 999 bootstrap samples to obtain this estimator’s precision (Dias et al. 2019; Mori et al. 2020). The species’ overlap coefficient was considered low if Δ4 < 0.50, intermediate if 0.50 < Δ4 < 0.70, and high if Δ4 > 0.70 (e.g., Monterroso et al. 2014). The spatiotemporal value (STV) for species’ interactions We wanted to use an approach that explore species’ spatiotemporal overlap, which was depicted with both non-native species and native carnivores within the study area. At this end, we made a combination of results from spatial patterns; multiseason two-species co-occurrence analysis and the temporal activity overlap between these two kinds of species. The first parameter used was the SIF. We combined it to the temporal overlap coefficient (Δ4) performed from the kernel density estimator. Both SIF and Δ4 are probabilities, thus the probability of SIF “and” Δ4 implies multiplication. Therefore, we computed the STV by multiplying the SIF value by the Δ4 value i.e., STV = SIF * Δ4, as previously used by Farris et al. (2020). These two parameters (SIF and Δ4) varied between the different paring species (non-native species and native carnivores). This combination was useful as sites that have a temporal activity overlap among species are not clearly defined. Also the spatial co-occurrence analyses of species can display bias, particularly when considering that investigated sites may be occupied by one or both species (for the paring species used), but these two species can be undetected. Such cases can imply the imperfection detection concept of MacKenzie et al. (2006). Accordingly, the STV shows a degree of overlap for each species pairing, thus 0 designates no overlap for both spatial and temporal patterns and as the STV rises this confirms the aggregation of spatial and temporal overlap, which depicts direct interactions between species (Farris et al. 2020). RESULTS Overall Trend in Capture and Multi-Year Changes in Species Estimates For non-native species, investigations in the TPNR produced over the three seasons a total of 526, 631, and 145 independent photographs of human, livestock, and dog, respectively. For carnivore species, there were 128, 154, and 412 independent photos of leopard, leopard cat, and fox, respectively. In total, the survey lasted 383 days, used 205 cameras, and yielded 26,216 trap nights. The overall trap success rates (which is the total number Table 1. Parameters computed in the multiseason co-occurrence models to verify the effect of the invasive species’ presence on the occupancy, detection, colonization, and local extirpation of carnivores in the Tieqiaoshan Provincial Natural Reserve (Par: Parameters) Par Definitions ψBA The probability that species B initially occupies the area, given that species A is also present ψBa The probability that species B initially occupies the area, given that species A is not present γBAA The probability that the area is colonised by species B in the interval t, t+1, given that species A is present in survey t and species A persists in the interval t, t+1 γBAa The probability that the area is colonised by species B in the interval t, t+1, given that species A is present in survey t and species A goes extinct in the interval t, t+1 γBaa The probability the area is colonised by species B in the interval t, t+1, given that species A is not present in survey t and species A does not colonise in the interval t, t+1 εBAA The probability that species B becomes extinct in the area in the interval t, t+1, given that species A is present in survey t and species A persists in the interval t, t+1 εBAa The probability that species B becomes extinct in the area in the interval t, t+1, given that species A is present in survey t and species A goes extinct in the interval t, t+1 εBaa The probability that species B becomes extinct in the area in the interval t, t+1, given that species A is not present in survey t and species A does not colonise in the interval t-t+1 rBA The probability of detecting species B, given that both are present and species A detected rBa The probability of detecting species B, given that both are present and species A not detected φSpecies Interactions Factor (SIF) page 5 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan of independent captured photographs for a species divide by the total number of night-traps) for non-native species were 2.01%, 2.40% and 0.55% for human, livestock, and dog, respectively; and 0.48%, 0.58%, and 1.57% for leopard, leopard cat, and fox, respectively. Spatial Multi-Year Patterns For the multi-year occupancy estimates for nonnative species, livestock had the highest occupancy of 0.78 ± 0.06 in SP2 followed by human with 0.61 ± 0.03 in the SP1, which also had the lowest site occupation among all non-native species (0.43 ± 0.09) in SP2. Dog had 0.53 ± 0.10 as the highest site occupation estimates in SP3 (Fig. 2). The leopard cat showed the highest probability of site occupation for carnivores, particularly SP3, with 0.82 ± 0.11. The fox had the second-highest site occupation probability of 0.74 ± 0.08 in SP1. In the previous study (Vitekere et al. 2020b), the leopard depicted an average site occupation probability with its highest estimate found in SP1 (0.54 ± 0.09). The lowest value found was for the leopard (0.44 ± 0.10) in SP2 (Fig. 2). Neither non-native nor native carnivore species showed a substantial rate of change in occupancy (all values < 2, Table 2). However, carnivores had lower occupancy equilibrium values than non-native species in IS1 (Table 2), except human, which represented the lowest value (0.22) (Table 2) when the pattern in IS2 was different. The dog was the only species found at equilibrium in both IS according to its equilibrium occupancy values. The fox also showed an equilibrium in the SP2 (Table 2). In general, the fox had the highest detection probability, followed by human. The lowest detection pertained to the dog (Fig. 3). The human presence in the SP1 (0.47 ± 0.03) was the highest detection probability among non-native species, followed by livestock (0.32 ± 0.03) in the SP1. The lowest detection was for the dog (0.20 ± 0.03) in the SP2. For the carnivore, the fox had the highest detection probability (0.64 ± 0.03) followed by the leopard with 0.36 ± 0.05 in the SP1. The lowest detection was for the leopard cat (0.24 ± 0.03) in the SP2 (Vitekere et al. 2020b). The highest colonisation rates were 0.54 ± 0.15, Table 2. The occupancy equilibrium and rate of change in occupancy of non-native species (human, livestock, and dog) and carnivore species (leopard, cat, and fox), computed as derived parameters from equation one (eq1) and equation two (eq2), respectively, to show trends in species occupancy from 2017 to 2019 in the Tieqiaoshan Provincial Natural Reserve Species OE1RC1OE2RC2 human 0.22 0.48 0.52 1.68 livestock 0.58 1.82 0.45 0.72 dog 0.70 1.08 0.79 1.17 leopard 0.55 0.96 0.45 1.08 leopard cat 0.36 0.88 0.56 1.28 fox 0.49 0.5 0.69 1.41 OE: occupancy equilibrium and RC: rate of change in occupancy, one and two are IS1 and IS2. Fig. 2. Estimated site occupation probability across three years (2017–2019) of non-native species (human, livestock and dog) and carnivore species (leopard, cat and fox) in the Tieqiaoshan Provincial Natural Reserve; outputs of multi-year analysis computed in PRESENCE software. Carnivores’ data have been previously used by Vitekere et al. (2020b). page 6 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan 0.42 ± 0.12, respectively, for fox and dog in IS2 and 0.32 ± 0.06 for livestock in the IS1 (Fig. 4). The lowest colonisation rates were in the IS1 for both native carnivores and non-native species (0.15 ± 0.09 for leopard cat and 0.13 ± 0.08 for human). Two non-native species had the highest extirpation rates (Fig. 5) for both categories of species, human in IS1 and livestock in the IS2, with 0.45 ± 0.09 and 0.30 ± 0.05, respectively. The lowest extirpation rate was for the dog in the IS2 (0.11 ± 0.09). The fox had the highest extirpation rate among carnivore species, followed by the leopard cat both in the IS1 (0.29 ± 0.10 and 0.26 ± 0.15, respectively). The lowest extirpated carnivore was leopard in the IS1 (0.21 ± 0.15). Multi-Year Co-occurrence Estimates For all comparisons, there were no significant differences between the occupancy of a single species’ analysis and the two species co-occurrence analysis as all p-values were greater than 0.05. In the humancarnivores coexistence (Table 3A), the leopard occupancy remained almost the same with human absence except in the SP2. The leopard cat’s site occupation was low in human presence except in SP3. The fox depicted unchanged estimates for occupancy in human presence except in SP2. Human absence positively and negatively influenced colonisation and local extirpation of the leopard and the leopard cat, respectively (except the local extirpation in the IS2). For the fox, the colonisation slightly diminished in both presence and absence of human, and the extirpation rate remains unchanged in the human absence in both IS. Its occupancy did not change in human presence and absence for the first two SPs. The human presence influenced the detectability of the leopard in all three SPs. Simultaneously, the detection of the leopard cat did not markedly change in human presence, and human Fig. 4. Estimated colonisation rates across three years (2017–2019) of non-native species (human, livestock and dog) and carnivore species (leopard, cat and fox) in the Tieqiaoshan Provincial Natural Reserve; outputs of multi-year analysis performed in PRESENCE software, col1: colonisation in interseason 1 and col2: colonisation in interseason 2. Carnivores’ data have been previously used by Vitekere et al. (2020b). Fig. 3. Estimated detection probabilities across three years (2017–2019) of non-native species (human, livestock and dog) and carnivore species (leopard, cat and fox) in the Tieqiaoshan Provincial Natural Reserve; outputs of multi-year analysis performed in PRESENCE software. Carnivores’ data have been previously used by Vitekere et al. (2020b). page 7 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan presence did not influence the fox’s detectability. Referring to the livestock-carnivore interaction (Table 3B), livestock presence brought a lesser influence to the occupancy of leopard and the occupancy of the leopard cat was modified (except the SP1) and the fox occupancy changed in the SP3. The colonisation rates of carnivores were influenced by livestock presence; as for the leopard and the fox, their occupancy slightly changed, especially in IS2. Surprisingly, livestock absence positively influenced the leopard’s local extirpation when for leopard cat and fox, they were negatively influenced. Detection probability of leopard was lesser with livestock absence, for leopard cat and fox did not markedly change with livestock presence. For dog-carnivore coexistence (Table 3C) the leopard and leopard cat occupancies slightly changed with dog presence when it markedly changed for the fox, especially in the SP3. In general, the dog presence influenced the colonization rates of the leopard and fox in both IS. The dog absence impacted negatively the leopard’s local extirpation, while its presence changed the local extirpation for leopard cat and fox. The detection was slightly less for all species with the dog presence. Temporal Patterns All the non-native species portrayed a marked preference for daytime, with very low nocturnalities (proportion of observations between 18:00 and 06:00) of 0.11, 0.12 and 0.16 for human, livestock, and dog, respectively. The leopard was crepuscular with a broad peak of activity in the morning and a more sharply defined evening peak around 18:00–19:00, with a nocturnality of 0.41; the leopard cat and the fox preferred night-time with nocturnalities of 0.71 and 0.69, respectively, and peak activity around midnight. Non-native species had noteworthy peaks of activity in the morning (7:00) and in the early evening (18:00), whereas they were observed less frequently around noon (Fig. 6). The activity time overlap coefficients (Δ4) were low for all pairwise species combinations of non-native species with the leopard cat and the fox (the highest value was 0.48 between livestock and fox). However, overlap of non-native species with the leopard was higher (human-leopard: 0.73; livestock-leopard: 0.75 and dog-leopard: 0.74, Table 4). The spatiotemporal value (STV) (Table 4) concomitantly indicates the spatial and the temporal overlapping in one value, with the highest value for the species pairing livestockleopard (0.97) and the lowest for the pair humanleopard cat (0.41). DISCUSSION Overall Species’ Site and Time Occupation Patterns Among all non-native species, livestock depicted the highest occupancy across all SPs, followed by human in SP1 and SP3 and dog. The non-native species were predominantly diurnal with very low nocturnality (close to 10%). Except for the leopard, which intensely selected crepuscular time, carnivore species preferred the night for their diel activity time. As is well known, humans always prefer daytime for their activities (Mori et al. 2020), inducing some invasive species (dog and livestock mainly) to have a similar pattern of time Fig. 5. Estimated extirpation rates across three years (2017–2019) of non-native species (human, livestock, and dog) and carnivore species (leopard, cat, and fox) in the Tieqiaoshan Provincial Natural Reserve; outputs of multi-year analysis performed in PRESENCE, ext1: local extirpation in interseason 1 and ext2: local extirpation interseason 2. Carnivores’ data have been previously used by Vitekere et al. (2020b). page 8 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan activity as they are mostly human-dependent (Vanak and Gompper 2010; Farris et al. 2015 2016 2017). The presence of the non-native species was quantified by their occupancy estimates (> 0.40 for all species), which indicated how these species are permanent in PAs, although human activities are forbidden in most declared conservation ecosystems (Chape et al. 2005; Dudley 2008). Non-native species remain real threats Table 3. Co-occurrence results for non-native species (species A) and carnivores (species B)—including the species interaction factor (SIF)—within the Tieqiaoshan Provincial Nature Reserve (2017–2019) A: human-carnivores ψBA ψBa γBAA γBAa γBaa εBAA εBAa εBaa rBA rBa φ SP human-leopard one 0.46 ± 0.09 0.58 ± 0.05 0.23 ± 0.07 0.26 ± 0.09 0.30 ± 0.10 0.29 ± 0.08 0.27 ± 0.13 0.15 ± 0.05 0.19 ± 0.08 0.30 ± 0.02 1.16 ± 0.03 two 0.42 ± 0.15 0.39 ± 0.01 0.15 ± 0.03 0.18 ± 0.06 0.22 ± 0.08 0.32 ± 0.10 0.21 ± 0.08 0.18 ± 0.14 0.20 ± 0.10 0.14 ± 0.12 1.18 ± 0.09 three 0.44 ± 0.11 0.50 ± 0.07 NA NA NA NA NA NA 0.18 ± 0.09 0.25 ± 0.03 1.21 ± 0.10 human-leopard cat one 0.78 ± 0.07 0.81 ± 0.09 0.11 ± 0.04 0.20 ± 0.06 0.19 ± 0.06 0.31 ± 0.16 0.25 ± 0.08 0.23 ± 0.05 0.29 ± 0.11 0.36 ± 0.05 1.05 ± 0.11 two 0.63 ± 0.13 0.71 ± 0.04 0.14 ± 0.08 0.18 ± 0.12 0.22 ± 0.07 0.22 ± 0.11 0.19 ± 0.09 0.20 ± 0.04 0.33 ± 0.08 0.49 ± 0.14 1.08 ± 0.15 three 0.78 ± 0.11 0.67 ± 0.08 NA NA NA NA NA NA 0.31 ± 0.10 0.30 ± 0.12 1.11 ± 0.05 human-fox one 0.70 ± 0.01 0.76 ± 0.08 0.21 ± 0.10 0.19 ± 0.11 0.26 ± 0.02 0.36 ± 0.06 0.31 ± 0.02 0.28 ± 0.13 0.50 ± 0.14 0.55 ± 0.10 1.05 ± 0.09 two 0.42 ± 0.09 0.58 ± 0.11 0.28 ± 0.07 0.36 ± 0.05 0.48 ± 0.03 0.32 ± 0.01 0.32 ± 0.04 0.23 ± 0.02 0.35 ± 0.13 0.48 ± 0.05 1.11 ± 0.05 three 0.64 ± 0.09 0.66 ± 0.05 NA NA NA NA NA NA 0.26 ± 0.11 0.28 ± 0.09 1.17 ± 0.02 B: livestock-carnivores ψBA ψBa γBAA γBAa γBaa εBAA εBAa εBaa rBA rBa φ SP livestock-leopard one 0.46 ± 0.09 0.49 ± 0.05 0.44 ± 0.02 0.24 ± 0.07 0.20 ± 0.13 0.16 ± 0.08 0.29 ± 0.02 0.28 ± 0.05 0.24 ± 0.15 0.25 ± 0.17 1.29 ± 0.02 two 0.48 ± 0.10 0.41 ± 0.09 0.39 ± 0.05 0.32 ± 0.12 0.18 ± 0.09 0.21 ± 0.05 0.24 ± 0.03 0.30 ± 0.08 0.20 ± 0.10 0.25 ± 0.08 1.34 ± 0.09 three 0.56 ± 0.08 0.45 ± 0.07 NA NA NA NA NA NA 0.47 ± 0.08 0.19 ± 0.13 1.27 ± 0.11 livestock-leopard cat one 0.81 ± 0.07 0.78 ± 0.08 0.14 ± 0.08 0.28 ± 0.13 0.28 ± 0.10 0.14 ± 0.05 0.13 ± 0.08 0.10 ± 0.03 0.28 ± 0.11 0.36 ± 0.12 1.32 ± 0.07 two 0.67 ± 0.02 0.52 ± 0.08 0.17 ± 0.04 0.19 ± 0.11 0.23 ± 0.09 0.28 ± 0.07 0.23 ± 0.09 0.15 ± 0.08 0.19 ± 0.08 0.31 ± 0.10 1.08 ± 0.03 three 0.57 ± 0.10 0.46 ± 0.06 NA NA NA NA NA NA 0.33 ± 0.10 0.32 ± 0.09 1.06 ± 0.08 livestock-fox one 0.76 ± 0.08 0.70 ± 0.03 0.27 ± 0.08 0.25 ± 0.05 0.30 ± 0.08 0.32 ± 0.09 0.29 ± 0.11 0.23 ± 0.07 0.66 ± 0.05 0.60 ± 0.07 1.04 ± 0.04 two 0.60 ± 0.01 0.47 ± 0.05 0.48 ± 0.03 0.50 ± 0.03 0.55 ± 0.11 0.27 ± 0.13 0.25 ± 0.08 0.18 ± 0.10 0.50 ± 0.01 0.57 ± 0.11 1.14 ± 0.09 three 0.75 ± 0.10 0.49 ± 0.09 NA NA NA NA NA NA 0.32 ± 0.04 0.39 ± 0.06 1.10 ± 0.09 C: dog-carnivores ψBA ψBa γBAA γBAa γBaa εBAA εBAa εBaa rBA rBa φ SP dog-leopard one 0.43 ± 0.04 0.48 ± 0.01 0.36 ± 0.08 0.39 ± 0.07 0.33 ± 0.01 0.25 ± 0.10 0.23 ± 0.05 0.18 ± 0.02 0.29 ± 0.07 0.33 ± 0.02 0.93 ± 0.02 two 0.61 ± 0.01 0.32 ± 0.05 0.20 ± 0.03 0.25 ± 0.09 0.23 ± 0.04 0.28 ± 0.08 0.27 ± 0.08 0.16 ± 0.06 0.19 ± 0.04 0.22 ± 0.08 1.36 ± 0.03 three 0.55 ± 0.08 0.31 ± 0.03 NA NA NA NA NA NA 0.23 ± 0.08 0.37 ± 0.10 1.29 ± 0.07 dog-leopard cat one 0.83 ± 0.05 0.78 ± 0.01 0.16 ± 0.06 0.13 ± 0.10 0.20 ± 0.09 0.19 ± 0.07 0.23 ± 0.11 0.25 ± 0.08 0.24 ± 0.07 0.31 ± 0.08 1.17 ± 011 two 0.78 ± 0.08 0.60 ± 0.09 0.19 ± 0.04 0.28 ± 0.03 0.17 ± 0.05 0.20 ± 0.02 0.18 ± 0.05 0.21 ± 0.01 0.21 ± 0.06 0.28 ± 0.03 1.16 ± 0.05 three 0.81 ± 0.03 0.77 ± 0.07 NA NA NA NA NA NA 0.25 ± 0.12 0.32 ± 0.09 1.13 ± 0.04 dog-fox one 0.83 ± 0.10 0.66 ± 0.09 0.42 ± 0.08 0.38 ± 0.08 0.29 ± 0.06 0.36 ± 0.08 0.29 ± 0.01 0.15 ± 0.06 0.58 ± 0.10 0.50 ± 0.08 1.32 ± 0.03 two 0.60 ± 0.08 0.35 ± 0.11 0.49 ± 0.03 0.56 ± 0.07 0.32 ± 0.01 0.29 ± 0.05 0.24 ± 0.03 0.21 ± 0.07 0.51 ± 0.07 0.48 ± 0.11 1.64 ± 0.08 three 0.84 ± 0.11 0.54 ± 0.13 NA NA NA NA NA NA 0.49 ± 0.12 0.43 ± 0.08 1.47 ± 0.01 Estimates are accompanied by standard errors, SP: sampling period and NA: not applicable because colonization and local extirpation rates are only present in IS. page 9 of 16Zoological Studies 60:52 (2021) © 2021 Academia Sinica, Taiwan Xu H, Tang X, Liu J, Ding H, Wu J, Zhang M, Yang Q, Cai L, Zhao H, Liu Y. 2009. 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