Wildlife can adaptively respond to their environment by modifying their diel activity and partitioning time to maximize survival and limit exposure to risks, producing a species’ temporal niche (Bennie et al., 2014; Vinne et al., 2019). Prey commonly employ predator avoidance strategies along the temporal niche axis (Kohl et al., 2019), which is contrasted by predators selecting for temporal activity patterns that maximize hunting success and minimize competitive encounters (Cozzi et al., 2012; Dröge et al., 2017). As a result, large carnivores are predominantly nocturnal while ungulates often exhibit more diurnal behavior, although neither exclusively so. However, pervasive human pressures disrupt individual behaviors that facilitate coexistence of predator and prey populations alike (Wolf and Ripple, 2016; Shamoon et al., 2018; Xiao et al., 2018; Sévêque et al., 2020). How human-induced responses of many species cascade to alter the dynamics of predation and other ecological interactions at the community level remains understudied (Guiden et al., 2019).

The fear of humans can suppress spatiotemporal activity in both carnivores and herbivores with cascading impacts to lower trophic levels (Dorresteijn et al., 2015; Gaynor et al., 2018; Suraci et al., 2019a). Specifically, human presence engenders shifts in diel activity patterns across guilds, altering their temporal niche to incorporate avoidance of human encounters (Gaynor et al., 2018; Frey et al., 2020). Human activities concentrated in the day and predator activity at night reduce the availability of temporal refugia for prey from risky encounters, and can constrain species’ abilities to optimize activity along the temporal niche axis (Kohl et al., 2019; Vinne et al., 2019). As predator and prey species alter their diel activity to adaptively respond to human presence, predator-prey temporal overlap and resulting encounter rates are likely to be changed (Patten et al., 2019), thus altering predator access to a suite of prey resources (Figure 1). Such perturbations to predator-prey dynamics can have cascading impacts that alter population regulation, habitat structure, and various ecosystem processes, such as carbon storage, herbivory, and seed dispersal (Pringle et al., 2007; Terborgh et al., 2008; Asner et al., 2009; Schmitz et al., 2018; Atkins et al., 2019).

Figure 1

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If wildlife modify their temporal niche to avoid pressures associated with human presence, predators and prey will exhibit increased nocturnal activity at both the species and guild levels (Gaynor et al., 2018). If all species respond to humans similarly, human avoidance further predicts: (1) intensified predator-prey overlap overall and (2) a greater diversity of prey species available to predators as previously diurnal species adopt nocturnal behaviors. Increasing the diversity of accessible prey would likely result in diminished predation rates on individual species, given that prey selection by carnivores is influenced in part by prey species’ availability relative to other sympatric prey and the diversity of the prey community (Sinclair et al., 2003; Owen-Smith and Mills, 2008). However, avoidance of humans may not be ubiquitous across species given that species have different vulnerabilities to humans (Tablado and Jenni, 2017). Thus, the prevalence of human avoidance among species is likely to determine the nature of community-level predator-prey outcomes.

Here, we evaluated the effects of human presence on the diel activity of predators and prey and consequential differences in predator-prey relationships using a novel method to assess predator-prey overlap at a community scale. We executed a systematic camera survey spanning 13,100 km² of the W-Arly-Pendjari (WAP) complex in West Africa across 21,430 trap-nights, obtaining detections of both wildlife and humans. We used occupancy modeling to determine areas of low and high human use within the study area and evaluate spatially explicit responses in species’ behavior and potential alterations to trophic interactions. Specifically, we tested for differences in diel activity patterns and nocturnal behaviors for 3 large carnivores (African lions, spotted hyenas, and African leopards) and 11 ungulate species between areas of low and high human presence. We also evaluated the effects of human presence on the overall temporal overlap (Δ) between each predator and its prey, as well as assessed differences in the relative overlap between predators and each individual prey species. We determined: (i) how carnivores and ungulates adjusted their temporal niche in response to human presence and (ii) how apex predator access to prey species was influenced by human presence.

Previous works often investigate temporal overlap of predators and prey in a pairwise manner (Linkie and Ridout, 2011; Ramesh et al., 2012; Patten et al., 2019). However, such an approach does not consider the overall composition of resources available to predators and the relative contributions of individual prey species. Higher order interactions beyond pairwise predator-prey relationships likely contribute to determining community structure and coexistence among species (Levine et al., 2017). We combatted these limitations by extending beyond pairwise comparisons to consider predator-prey interactions at the community level. We aggregated temporal activity among ungulates, providing a more ecologically realistic depiction of overlap between predators and their prey. Specifically, we used bootstrapped kernel density distributions of predator and prey diel activity to calculate the overlap between each predator-prey pair relative to the overall available prey (percent area under the predator diel curve, PAUC). PAUC values were generated by aggregating prey activity curves and then scaling the prey activity (kernel density estimates) to each predator. PAUC represents a metric of relative prey access for the apex predator, as it provides insight into the times of day that encounters between the predator and prey species are most likely to occur based on the temporal activity of both. In this new approach to assess the spatially explicit temporal responses of predators and their prey to humans, we elucidate the community-level effects of humans on trophic interactions and their implications for ecosystem regulation by large carnivores.

Our camera survey yielded 786 and 10,325 detections of apex predators and ungulates, respectively, over 21,430 trap-nights throughout our West African study system (Supplementary file 1). Spotted hyenas are the dominant predator in the system with six times more detections than either African lions or leopards. Warthog, reedbuck, and bushbuck were the most commonly observed ungulates, each detected over 1000 times.

We obtained 350 detections of humans in 69 out of 204 surveyed 10-km² grid cells, leading to a naive human occupancy of 0.34. Accounting for imperfect detection, model selection resulted in four competing top models (ΔAICc < 2) for human occupancy (Supplementary file 2). Detection of humans primarily varied among years and sites and was higher in non-savanna habitat (top model goodness-of-fit p-value = 0.327). Human occupancy was pervasive, but heterogeneous within the study area (Figure 2a; $\stackrel{-}{\mathrm{\Psi }}$ = 0.54 SE 0.41), ranging from 0.0006 to 1 with highest frequencies near these extremes (Figure 2b). Using the mean value of occupancy as a pressure threshold, we designated 108 of 204 grid cells as having high human use (occupancy > 0.54). Humans exhibited mostly diurnal activity with 80.3% of detections occurring between sunrise and sunset (Figure 2c).

Figure 2 with 1 supplement see all

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Human avoidance responses

Human presence generated marked modifications in the temporal niches of sympatric wildlife, with both guilds exhibiting human avoidance behaviors overall. Carnivores and ungulates showed significantly different diel activity patterns between low and high human use (carnivores p-value=0.017; ungulates p-value<0.001; Figure 3). Over two-thirds (10 out of 14) of the mammal species in the study exhibited significant differences in their diel activity patterns in response to human presence (African leopards, spotted hyenas, and eight ungulates; Figure 3). Ungulates overall were 7.1% (95% CI ± 1.7%) more active at night in high human areas, while carnivores showed a slight but non-significant increase in night-time activity of 3.9% (±5.7%). Specifically, we observed significantly higher nocturnal activity with high human use for reedbuck (+12.3 ± 4.8%), duiker (+7.4 ± 4.4%), bushbuck (+6.9 ± 3.6%), and warthog (+4.5 ± 1.9%); and significant decreases for kob (−5.3 ± 4.2%) and aardvark (−15.0 ± 8.1%; Figure 4). In contrast, five ungulate species and all three carnivores showed no significant differences in nocturnality. After testing the sensitivity of our results to the human occupancy threshold selected, we found that increasing or decreasing the low vs. high human occupancy threshold by ±0.1 did not alter our interpretation of species’ differences in diel activity (Supplementary file 3). The only change we observed was detecting significance when reducing the threshold from 0.54 to 0.44 for two species: African leopard and roan antelope. Our results highlight that most species respond to human occurrence by modifying their behaviors and reducing their realized temporal niche to incorporate more night-time activity, potentially altering predator-prey encounter rates.

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Figure 4

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Human occurrence restructures access to specific prey

African lions and spotted hyenas experienced similarly distinct differences in the composition of accessible prey due to human presence using the 95% CIs of the average difference in percent area under the predator activity curve (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}\mathrm{C}}$), our novel method for assessing predator-prey temporal overlap in a community context (Figure 5a). Specifically, humans generated significant differences in overlap of these predators with 4 out of 11 prey species: bushbuck (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{i}\mathrm{o}\mathrm{n}}}$ = +1.49, 95% CI ± 1.14%; ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{h}\mathrm{y}\mathrm{e}\mathrm{n}\mathrm{a}}}$ = +1.51 ± 0.73%), reedbuck (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{i}\mathrm{o}\mathrm{n}}}$ = +1.99 ± 1.34%; ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{h}\mathrm{y}\mathrm{e}\mathrm{n}\mathrm{a}}}$ = +1.88 ± 0.87%), duiker (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{i}\mathrm{o}\mathrm{n}}}$ = +1.56 ± 1.31%; ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{h}\mathrm{y}\mathrm{e}\mathrm{n}\mathrm{a}}}$ = +0.84 ± 0.73%), and kob (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{i}\mathrm{o}\mathrm{n}}}$ = -2.24 ± 1.58%; ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{h}\mathrm{y}\mathrm{e}\mathrm{n}\mathrm{a}}}$ = -1.45 ± 0.88%) (Figure 5b). All three species to which predator access increased significantly also exhibited increased night-time activity as a human avoidance strategy. In contrast, kob was less active at night in high human areas and experienced lower overlap with African lions and spotted hyenas (Figure 4). Additionally, African lion and spotted hyena access to two prey species showed near significant differences (buffalo ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{i}\mathrm{o}\mathrm{n}}}$ = +1.33 ± 1.41%; ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{h}\mathrm{y}\mathrm{e}\mathrm{n}\mathrm{a}}}$ = +0.87 ± 0.97%; and waterbuck ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{i}\mathrm{o}\mathrm{n}}}$ = -1.66 ± 1.73%; ${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{h}\mathrm{y}\mathrm{e}\mathrm{n}\mathrm{a}}}$ = -1.67 ± 1.71%).

Figure 5

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All three apex predators showed comparable differences in access to all prey between human use levels (Figure 5b). However, differences in African leopard access to prey items were not significant based on 95% CIs, with only aardvark (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{e}\mathrm{o}\mathrm{p}\mathrm{a}\mathrm{r}\mathrm{d}}}$ = -4.6 ± 4.7%) and bushbuck (${\displaystyle \stackrel{-}{\mathrm{\Delta }}\mathrm{P}\mathrm{A}\mathrm{U}{\mathrm{C}}_{\mathrm{l}\mathrm{e}\mathrm{o}\mathrm{p}\mathrm{a}\mathrm{r}\mathrm{d}}}$ = 1.7 ± 1.8%) access nearing significance (Figure 5). We suspect this is due to leopards’ differential response to human presence (-4.6 ± 19.1% change in nocturnality) compared to African lions (+11.9 ± 16.3%) and spotted hyenas (+3.7 ± 6.5%; Figure 4), although these differences are non-significant.

Although overlap with total available prey did not differ for any predator, human presence increased the variation in species-specific prey accessibility (PAUC estimates) for African lions (Fligner-Killeen test, p-value=0.03), indicating lower diversity of available prey and therefore more access to certain prey species compared to others where human presence was high (Figure 5b). African leopards and spotted hyenas showed no significant differences in access variability as a response to humans.

Wildlife responses to human activities have the potential to reshape natural ecological processes and trophic dynamics (Hebblewhite et al., 2005; Dorresteijn et al., 2015; Suraci et al., 2019a). When anthropogenic pressures are heterogeneous, the resultant dynamism promotes many adaptive strategies to manage and mitigate threats including behavioral shifts in diel activity that redefine species’ temporal niches (Muhly et al., 2011; Carter et al., 2012; Gaynor et al., 2018; Frey et al., 2020). Such shifts in diel activity may lead to increased prey vulnerability to nocturnal predators, thus altering probabilities of encounter and diets in consumers (Figure 1). We found that over two-thirds of the assessed species exhibited different overall diel activity patterns as a response to humans in the study area. Most species showed more nocturnal activity, consistent with previous works and supporting our hypothesis of human avoidance (Carter et al., 2012; Gaynor et al., 2018). Valeix et al., 2012 and Suraci et al., 2019b similarly found reduced diurnal activity near human settlements in African lions in Makgadikgadi Pans National Park, Botswana, and Laikipia, Kenya, respectively, likely to reduce risks of human encounters. Human presence appears to be limiting temporal refugia from risks for many species and driving increases in ungulate activity when predators are also active, possibly decoupling anti-predator behaviors from predation risks (Dröge et al., 2019; Smith et al., 2019). Patten et al., 2019 also presented evidence of human avoidance driving increased predation risks in North American white-tailed deer (Odocoileus virginianus).

Heterogeneity in species’ responses to human presence, however, indicates different sensitivities to humans among the carnivores and ungulates in our study system. Some species did not exhibit differences in nocturnality as expected (e.g. kob and aardvark). These species may be benefitting from the observed human avoidance in many sympatric species that potentially reduces risks of predation and competition, commonly referred to as a human shield response (Berger, 2007; Muhly et al., 2011). For example, Atickem et al., 2014 reported mountain nyala (Tragelaphus buxtoni) leveraging predator avoidance of humans during the day as a temporal refuge in Ethiopia. The ability to exploit human presence as a shield from predatory or competitive encounters may be due to the life history traits of a species that reduce sensitivity to humans, such as body size, energetic requirements, dispersal abilities, social structure, or foraging strategies (Blumstein et al., 2005; Tablado and Jenni, 2017). Similarly, these species’ temporal niches may be constrained by inherent characteristics that were evolved for diurnal activity, making night-time activity more costly despite refuge from human pressures and limiting their adaptive capacity to avoid humans (Monterroso et al., 2013). In contrast, the amount of wildlife persecution (i.e. trophy hunting and poaching) in the system may induce stronger human-avoidance behaviors in hunted species. For instance, Vanthomme et al., 2013 attributed the negative associations of 10 mammals with human disturbances in Gabon to hunting avoidance behaviors, contrasted by six species in the study showing positive associations. Although the mechanisms driving differential responses to humans were not explicitly investigated here, our study demonstrates non-uniform responses of large mammals to human presence. As such, future work can assess the drivers of species-specific responses and sensitivities to humans.

We showed that human presence modified the availability of prey species relative to the overall pool of available prey, which is an important driver of prey selection in apex predators, and thus provide new insights into community-level repercussions of human sympatry with wildlife (Sinclair et al., 2003; Owen-Smith and Mills, 2008). While we expected overall predator-prey overlap and the diversity of available prey to be higher due to human avoidance, the combination of human avoidance and human shield strategies observed in our system resulted in little difference in overall overlap but substantial differences in apex predator access to individual prey species. Specifically, our new community-level approach to predator-prey temporal overlap revealed that prey species experienced intensified overlap with predators when they increased their nocturnal temporal niche (e.g. duiker, reedbuck, bushbuck) to avoid humans, while overlap was lessened for species that did not (e.g. kob). For African lions, this resulted in a lower diversity of available prey, likely intensifying predation pressures on a smaller subset of species which could contribute to destabilizing trophic dynamics (Gross et al., 2009). This highlights increasing concerns for the persistence of the now Critically Endangered West African lions that are suffering from prey depletion (Henschel et al., 2014). The predators in our study are largely opportunistic night-time hunters, and temporal overlap is often strongest between predators and their preferred prey species (Hayward and Slotow, 2009; Linkie and Ridout, 2011; Ramesh et al., 2012; Dou et al., 2019). Thus, we expect that species experiencing the highest overlap with apex predators relative to other prey to be integrated into the predators’ diets in higher proportions, and consequently expect varied prey selection by predators between low and high human use areas. Buffalo are a common prey item of African lions in other systems, and our results suggest they may be vulnerable to intensified selection by lions due to human presence increasing access to buffalo in our study area (Davidson et al., 2013). Our approach implemented in this study may therefore be useful for anticipating herbivore population declines as a result of intensified predation pressures, as well as potential resulting feedbacks into predator population stability especially for endangered species such as the West African lion (Owen-Smith et al., 2005). Additionally, human disturbance can increase the predation rates and carcass abandonment by large carnivores as well as alter mesopredator foraging behaviors, potentially increasing mortality rates on preferred prey species and providing augmented carrion resources that may be detrimental to scavenger populations (Smith et al., 2015; Prugh and Sivy, 2020). As such, disturbances to predator-prey relationships potentially lead to alterations in predators’ diets with consequences for ungulate and mesopredator community regulation and nutrient distribution (Schmitz et al., 2010; Owen-Smith, 2019).

Although protected areas are the primary strategy for biodiversity conservation worldwide, human exploitation of protected areas is pervasive and in many cases, necessary for the sustenance of human populations (Jones et al., 2018; Geldmann et al., 2019). By accounting for imperfect detection to understand human space use, we contribute to a more comprehensive understanding of human impacts within coupled human-natural ecosystems that is imperative to effectively manage for the conservation of ecological processes, biodiversity, and human needs. However, human activities observed in our study system may not impact species uniformly. Because we aggregated a variety of human activities to depict human use, there might be activity-specific responses by wildlife that were not captured. Humans exploit resources in national parks in many ways including livestock herding, resource gathering, subsistence poaching, hunting, and recreation, all of which impact the system and wildlife to varying degrees (Everatt et al., 2019; Geldmann et al., 2019; Harris et al., 2019). Indeed, Harris et al., 2019 found differential impacts of human activities on wildlife behavior in WAP, suggesting species in this system do not respond to all humans uniformly. However, limited sample sizes of many human activity categories currently preclude more detailed analyses using an occupancy framework. Overall, human impacts encompass a variety of disturbances that impact ecosystems, both in our study and more broadly, and thus disentangling the responses of wildlife to specific human pressures may facilitate designing more effective conservation interventions (Jones et al., 2018; Nickel et al., 2020). Our results are also suggestive of the potential ecological effects of changes to human activity in natural areas, which could result from fluctuations in tourism, infrastructure development, policy changes, and other local or global processes.

Our results demonstrate prevalent disruptions to wildlife temporal activity patterns from human presence, leading to overall reductions in diurnal activity and modified community dynamics. Because both carnivores and ungulates serve fundamental roles in regulating African ecosystems via predation and herbivory, respectively, the pervasiveness of their responses to human occurrence demonstrates the capacity for humans to disrupt essential ecological processes that facilitate coexistence among wildlife, in this case reshaping predator-prey interactions. As the human footprint continually expands, spatial refugia from anthropogenic disturbance become more limited, stimulating an increasing need to exploit temporal partitioning to avoid human pressures. We show that the community-level implications of these behavioral modifications must be considered in light of complex higher-order interactions that govern mechanisms of coexistence among predators and their prey.

Occupancy model data (human detection histories and model covariates) are available on Dryad. Wildlife detection data have been provided as a supporting file (Source Data 1).

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Author details

1. Kirby L Mills

   Applied Wildlife Ecology Lab, Ecology and Evolutionary Biology Department, University of Michigan, Ann Arbor, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing, Processed and curated camera trap images

   For correspondence

   kimills@umich.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7693-9629

2. Nyeema C Harris

   Applied Wildlife Ecology Lab, Ecology and Evolutionary Biology Department, University of Michigan, Ann Arbor, United States

   Contribution

   Conceptualization, Resources, Data curation, Supervision, Funding acquisition, Investigation, Visualization, Project administration, Writing - review and editing, Processed and curated camera trap images

   For correspondence

   nyeema@umich.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5174-2205

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