Introduction

The categorization of wildlife activity tends to be constrained to traditional day-night niches, strictly classifying species as diurnal or nocturnal [1–3]. Less frequently, the term crepuscular is used, since many diurnal species are active at dawn and dusk as well as in full daylight [4]. Identification of distinct adaptations to either a diurnal or nocturnal life history strategy (e.g. larger orbits in nocturnal primate species improving night vision [5]) may contribute to the tendency by some to view species’ activity patterns as more of a binary trait, rather than extending across a spectrum of temporal activity types [2, 6]. The characterization of a species to an activity pattern may translate into a methodological approach where evaluation extending beyond the dominant activity period is never attempted.

This more simplistic approach, however, was questioned in the 1970s with the characterization of the activity patterns of the presumed diurnal Mayotte lemur (Lemur fluvus mayottensis). This species was observed to apportion its behavior equally between day and night periods [7]. As a consequence, the term cathemerality was developed to capture this temporal activity type, adding to the previously established, and mutually exclusive categories of nocturnal and diurnal. As a behavioral strategy, cathemerality is thought to allow considerable advantages, identifying the ability for the species to engage in diurnal and/or nocturnal activity periods in response to varying ecological conditions [3]. Factors such as temperature, access to food resources, and predation risk are all thought to be important in promoting cathemerality [3]. At least eight species of Madagascar lemur exhibit cathemeral activity patterns [1, 8, 9]. This new term was initially met with skepticism and even rejected by a reviewer in the peer review process as it was considered to be “unnecessary new jargon” [2]. This initial rejection illustrates the commitment to the notion that animal activity cycles can be viewed as if they are a binary trait, rather than extending across a spectrum of temporal activity types. Where behavioral activity is identified outside of the expected time period, these events are often considered unusual and, therefore, of potentially limited ecological significance. However, these events may provide information critical to understanding a species diel behavior and ecology in a given landscape.

A prominent hypothesis for diurnal species expanding activity into the night is that nighttime activity occurs due to elevated light levels [10–12]. Singing at night was typical of unmated northern mockingbirds (Mimus polyglottos) and regularly occurred during full moon periods and less frequently during other lunar phases [13]. For carnivores, more recent studies reveal that nocturnal activity may be more pronounced than previously thought (14,15). For traditionally perceived diurnal species such as the African wild dog (Lycaon pictus [14, 15]) and cheetahs (Acinonyx jubatus [15]), nocturnal activity for both species comprised roughly 25% of their overall activity budget [15]. Nocturnal activity was associated with the lunar cycle and restricted to brighter nights, potentially allowing these species to avoid stronger competitors such as lions (Panthera leo) and hyenas (Crocuta crocuta), which are active at night [15].

We used camera traps to study behavior among banded mongooses (Mungos mungo), a diurnal mesocarnivore [16], at den sites in Northern Botswana. Systematic studies of banded mongoose ecology and behavior previously have only been undertaken during daylight hours (e.g. [16–22]). Here, we report nocturnal activity for this presumed exclusively diurnal species. We characterize behavior type and test whether observed nocturnal activity patterns are associated with brighter lunar phases as observed in other species. We discuss our findings in the light of our current approach to activity pattern classification and methodological approaches for ecological and behavioral studies of wildlife.

Methods

Results

From January to November 2016, nighttime activity was identified for 3% of the trap days (SD = 18%, n = 7/215) and across five of the 11 months of the study. Night trap events occurred between 2000 and 2400 hours (n = 7). The nighttime activity was observed in 29% of study troops (n = 5/17 study troops, S1 Table). There was no significance between land classification of the den site (town or park) and the occurrence of night activity (Fisher’s exact test p = 1). However, the limited number of park troops might have influenced our ability to detect an effect.

Banded mongoose nighttime activity was seen across all moon phases with no significant difference between the nights with no light (i.e., the new moon) and the phases (i.e. waning, waxing, full) that did provide moonlight (Fisher’s exact test p = 0.638; S1 Dataset for trap days and associated moon phases).

Discussion

Like other social mongooses, banded mongooses are considered diurnal species [24] and, across studies, ecological and behavioral investigations have been restricted to daylight periods [16–22]. However, this limited temporal approach may fail to capture data critical to understanding the ecology, biology of a species, and the temporal nature of space use. Here, we report nocturnal behavior and space use for banded mongooses. Our observed nocturnal behaviors were both vigilant and non-vigilant in nature (S2 Table for ethogram). Where vigilance behaviors were identified, they were followed by fleeing and den relocation, which is unique for nighttime study periods in banded mongoose. Photos from the cameras traps did not, however, provide information as to what prompted these behaviors. Fleeing behavior in this species had only been previously been reported in association with intergroup aggression events [25].

Non-vigilant behaviors were also observed and included individuals walking towards an active den site, investigating a den site, and in one situation, an individual emerges from the den to chase a mongoose. In that last scenario, only one mongoose returns to the den hours later. In each of these events, photographic evidence of mongooses emerging from the den is absent (with exception of the mongoose chasing a putative intruder). Indeed in two of the instances, there was only one entrance to the den and photographic evidence of den emergence would have been necessary if the mongoose was from the resident troop. These data suggest that non-resident mongoose may make forays at night into the home range of other troops. Further research is needed to fully understand the ecological purpose of these behaviors.

When evaluating the lunar phases and nighttime activity, night trap events were identified across both the moonlight and dark nights. Nocturnal behavior in banded mongoose did not appear to be influenced by availability of light. Lack of association with moon phase suggests other important ecological factors or stimuli are encountered at night and influence the occurrence of these behaviors.

Fitness advantages for nocturnal behavior in diurnal species have been previously identified [26, 27], and signal the importance of identifying diel behavior patterns rather than focusing on the dominant activity period. For example, the diurnal yellow breasted chat (Icterina virens) will move outside of their territories at night with fertile females engaging in extrapair copulations, potentially allowing them to go undetected by their social mate [26]. While being primarily diurnal, brown bears (Ursus arctos) forage equally between daylight and darkness during salmon migrations, with capture success increasing during the night [27]. Restricting data collection for diurnal species to expected daytime activity periods might hinder or limit our ability to gain further insight into important aspects of the biology and ecology of wildlife species.

Focusing effort toward dominant activity periods may also result in erroneous conclusions when restricting data collection to a particular activity time. For example, non-invasive fecal glucocorticoids are often used to evaluate stress responses in wildlife [28] and results are often interpreted in conjunction with behavioral data collected during the same diurnal time period of collection or the diurnal period the day before collection [29]. Here, stress levels are interpreted and aligned with observed daytime movements and behaviors when, in fact, the stress response may reflect the occurrence of unobserved nocturnal events. Failure to account for variation in activity periods might not only undermine study objectives, but also the veracity of our understanding of a species’ ecology and behavior.

Considering that heterogeneity is a fundamental underlying phenomena of ecology [30], temporal variation in activity patterns should be explicitly accounted for in methodological approaches. Our observations of banded mongooses illustrate the importance of including observations during low activity times when studying a wildlife species. Initially, ecology assumed spatial homogeneity for convenience and simplicity, with heterogeneity an unwelcome but necessary complication [31]. Study approaches and theoretical frameworks in the field of landscape ecology that have embraced heterogeneity and complexity have provided new and critical insights into key ecological processes (e.g. community dynamics or succession, the role of edges, patch dynamics)[31]. A similar inclusion of heterogeneity into our consideration of activity periods and associated behaviors is called for and will likely lead to a new era of ecological discovery.

Supporting information

Acknowledgments

We thank the Government of Botswana’s Ministry of Environment Wildlife and Tourism, and the Department of Wildlife and National Parks for permission to conduct this study. We thank Dr. Mark Vandewalle and CARACAL staff for their assistance with fieldwork and the undergraduate volunteers at Virginia Tech for analyzing photographs.