Activity patterns and burrowing ecology of the giant pouched rat (Cricetomys emini) in Tshuapa Province, D. R. Congo

1 Introduction

Giant-pouched rats of the genus Cricetomys are native to much of Sub-Saharan Africa, ranging from far West Africa and across the Congo Basin to the Indian Ocean (Kingdon 2015; Rosevear 1969). These rodents have been documented to be associated with a variety of zoonotic diseases such as leptospirosis, bartonellosis, trypanosomiasis, capillariasis and monkeypox (Centers for Disease Control and Prevention 2003; Gretillat et al. 1981; Herder et al. 2002; Hutin et al. 2001; Machang’u et al. 2004; Malekani et al. 1994). Monkeypox (MPX) is of particular concern in this region as the vast majority of MPX cases are reported from the Democratic Republic of the Congo (DRC) where there is an estimated infection rate of 5.53 cases per 10,000 people (Rimoin et al. 2010). MPX is endemic in the Tshuapa Province of DRC where an average of 661 suspected human cases were reported each year from 2011 to 2014 (Osadebe et al. 2017). Anti-orthopoxvirus antibodies have been found in samples collected from giant-pouched rats and other small mammals in this province and elsewhere in central Africa (Doty et al. 2017; Doshi et al. 2019), indicating some animals examined in these studies had possible exposure to Monkeypox virus (MPXV) or another Orthopoxvirus (OPXV). Additionally, giant-pouched rats are commonly hunted for meat and therefore pose a risk to human health in Tshuapa Province.

The taxonomy of this genus varies within the literature, either two (Van der Straeten and Peterhans 2008; Van der Straeten et al. 2008), four (Carleton and Musser 2005) or five species (Kingdon 2015) are currently recognized. The two species arrangement includes C. emini and Cricetomys gambianus, whereas others concur Cricetomys kivuensis and Cricetomys ansorgei are sufficiently divergent from C. emini and C. gambianus, respectively, to warrant species-level recognition. Recent molecular data has indicated both arrangements likely underestimate the true diversity within the genus (Olayemi et al. 2012), but further research is needed to appropriately connect taxonomy (subspecies and species), linked to morphologically identified type-specimens stored in natural history museums, to the recently identified genetic lineages. Clearly, additional research into the genetic variation within this group is warranted. Animals captured for this study were from the area south of the Congo River, as were animals sampled from lineage sp2 as described by Olayemi et al. (2012); however, because this area is within the geographic range of C. emini as currently recognized, animals are referred to as C. emini. Furthermore, captured specimens displayed a slender shape with a short, grey and soft fur coat, as which is indicative of the species C. emini (Olayemi et al. 2012).

Giant-pouched rats are primarily terrestrial and use underground burrows (Malekani 1990). Previous reports indicate burrows of C. emini can be found in dense forest as well as in open areas such as farmlands, fallow fields, and near abandoned houses in forest villages (Malekani 1987). Most burrows have been observed in elevated places (mounds, deserted termitaries or beneath large trees), with at least two entrances, of which one is primarily used (Malekani 1987, 1990). The second entrance is typically closed by ground cover or located inside a hollow making it difficult to locate. As a result, in some cases the burrow may seem to have only one entrance (Malekani 1990). Additional evidence suggests one individual occupies one burrow at a time; females with juveniles have been observed to occupy one burrow for several months (Malekani 1987). Rosevear (1969) reported that these animals change burrows frequently and that old burrows are left vacant. A recent study suggests that Cricetomys rodents utilize multiple borrows within the core areas of their home range, which may aid escaping predators (Yadok et al. 2019).

In general, Cricetomys rodents are considered to be solitary and nocturnal; with two peaks of activity (bimodal activity pattern), generally within the limits of dusk until dawn, with a reduction/cessation of activity during the few hours following midnight (Ewer 1967; Majer 1973; Rosevear 1969; Yadok et al. 2019). Some studies have additionally observed limited diurnal activity of Cricetomys spp. (Ewer 1967; Majer 1973; Rosevear 1969; Yadok et al. 2019). No study to date has addressed activity patterns of C. emini using radio-telemetry. Previous studies relating to the activity patterns of these rodents were either conducted in captivity (ex-situ) or focused on either nocturnal or diurnal activity only but not both. The use of radio transmitters allowed us to assess the behavior of these animals during the entire 24 h cycle. The purpose of this study was to gain a better understanding of burrow site selection and the temporal activity patterns of C. emini in the equatorial forest of DRC.

2 Materials and methods

2.5 Spatial analysis

The burrow sites were analyzed spatially in ArcGIS for proximity to developed areas (man-made structures, roads, pathways), and evaluation of spatial movements and distribution. Distances between burrow sites and man-made structures or paths were calculated as Euclidean distance using ArcGIS. Due to the paucity of spatial information on C. emini, den sites were spatially overlaid in ArcGIS with the documented home range of the congeneric C. gambianus, 4.95 ha (range = 2.23–11.10 ha) to serve as a proxy (Skinner and Chimimba 2005). This provides some insights into the dispersal and interaction potential between individual Cricetomys, as well as interactions with human activity and development. Structures, boundaries, and roadway data were sourced from OpenStreetMap contributors (https://www.openstreetmap.org). Specific imagery in Figure 1 was sourced from Maxar Technologies Inc., published in ESRI World Imagery basemap, accessed using ArcGIS software version 10.5 (ESRI, Redlands, California).

Figure 1:

Satellite imagery and location of the den sites of Cricetomys emini that were identified in tshuapa province, DR Congo, 2016. The den sites are buffered by a circular crosshatched area approximately equivalent to the home range of the congeneric C. gambianus reported by Skinner and Chimimba (2005).

3 Results

We captured and telemetry collared 5 giant-pouched rats (2 males and 3 females). Based on their weight and reproductive status, 1 animal was determined to be a juvenile and 4 were adults. During examination of reproductive conditions, one (animal 3) of the three females was pregnant and the other two females had evidence of past reproductive events (i.e., enlarged nipples). One of the two males was reproductively active, whereas the other was a juvenile (410 g). The weights of the adult animals ranged from 750 – 900 g with the pregnant female being the largest (Table 1).

3.1 Activity patterns

For each hour of the 24 h cycle, data were collected 5 times per animal during the study period allowing for sufficient time between data points to be considered as independent readings. Animal 1 was captured by local hunters who returned the radio-collar of the animal two days after its disappearance. Therefore, Animal 1 was only observed for 3 full cycles prior to its removal from the study. Animal 1, a female, was observed to be the most active animal, averaging 1.67 h of inactivity with a maximum observed inactive period of 2 h while her normal activity averaged 22.33 h with a maximum period of 23 h of observed activity (Table 1). Animal 3, the pregnant female, was found to be the least active animal; average duration of inactivity was 5 h with a maximum period of 8 h, and normal activity duration averaged 19 h with a maximum period of 21 active hours (Table 1). The observed average inactivity period for all animals was 3.01 h and average normal activity period was 20.86 h.

Nocturnal activity appeared to range between the hours of 18:00 and 05:00 with a probable cessation or reduction of activity between 20:00–23:00 and around 04:00. Diurnal activity ranged between 06:00 and 17:00 h with a probable cessation of activity between 11:00 and 14:00 (Figure 2, Figure 3).

Figure 2:

Percentage of active observations recorded for each 1 h period for five (5) Cricetomys emini in tshuapa province, DR Congo, 2016.

Figure 3:

Most frequently observed daily activity of individual Cricetomys emini in tshuapa province, DR Congo, 2016. The most common (modal value) activity parameter (active or inactive) recorded for each 1 h period is graphed. Breaks in the animal-specific lines denote periods where inactivity was the most common parameter of the individual among all observations.

4 Discussion

Only 5 telemetry collars were available for this study, therefore the sample size was limited to 5 animals. In addition to the small sample size, the short observation period of 37 days limits the conclusions that can be made from this data. Despite these constraints, this work provides new information as the only study to address activity patterns or burrow sites of Cricetomys rodents using radio telemetry (Ewer 1967; Majer 1973; Rosevear 1969; Yadok et al. 2019). The data presented here suggest that C. emini spends more time being active (maximum period of 20.86 h) than inactive (maximum period of 3.01 h). This suggests a different pattern than what was reported in C. gambianus (maximum activity period of 5.7 h) by Ewer (1967). These differences may be due to the fact that Ewer (1967) studied a captive animal colony in an unnatural setting. In the present study, Animal 3 was observed to have the most hours of inactivity (maximum period of 8 h) compared to the other animals (Table 1); this could potentially be due to pregnancy.

C. emini appears to have a bimodal activity pattern, active during multiple periods of the day and night. Nocturnal activity ranged between the hours of 18:00 and 05:00 with a probable reduction of activity between 20:00–23:00 and around 04:00 (Figure 2). This nocturnal activity is similar to that observed for C. gambianus by Ewer (1967) and for C. emini by Majer (1973), but differs from Cricetomys sp. as reported by Yadok et al. (2019) who described a bimodal activity pattern during nocturnal hours only. Yadok et al. (2019) suggests that this bimodal pattern may be due to the fact that these animals have a temporal strategy to avoid predators and reduce competition. We also found that diurnal activity for C. emini ranged between 06:00 and 17:00 h with a probable cessation of activity between 11:00 and 14:00 h (Figure 2). Rosevear (1969) states that Cricetomys is primarily nocturnal but has occasionally been seen hunting for food in the daytime. In the present study, Cricetomys were observed to be active during the day inside their burrows.

Rosevear (1969) reports that Cricetomys change burrows frequently, leaving the old burrow vacant and Yadok et al. (2019) suggests that Cricetomys rodents utilize multiple borrows within the core areas of their home range, which may be useful in aiding escape from predators. The present study suggests that C. emini may change burrows less frequently than previously reported, since only one among 5 animals (Animal 5) was found to regularly move between burrows (Figure 1). A giant pouched rat can only use one burrow at a time and unoccupied burrows may therefore be available for use by other individuals.

Burrows of this species have been commonly reported in dense forest habitats, in farmlands, near deserted houses in forest villages, and near riparian areas (Genest-Villard 1967; Malekani 1990; Misonne 1971; Yadok et al. 2019). De Balsac and Lamotte (1958) report this species is particularly fond of oil palm fruits. Burrow habitats observed in this study support these previous findings, as most burrow sites for C. emini were located in disturbed sites such as mixed agricultural areas, including cassava and palm farms with few old growth trees.

Given the low sample size and high burrow fidelity observed in this study, the home range estimate of 5,527 m² we generated is limited and core use areas cannot be identified. This estimate is based solely on burrow sites and therefore would underestimate the actual home range of the animal as data on the movements of C. emini while active were not collected. This serves as the first C. emini den selection and movement study to provide a home range estimate. However, it is likely that the home range is more similar to that documented for C. gambianus, given the similarity between the habitat usage and activity patterns of these congeners (Majer 1973). There was no observed overlap between home range buffered den sites (Figure 2). This is likely due to our low sample size, as we cannot assume that every animal in the area was captured and therefore overlap between undetected animals may have occurred. Another possibility is home range estimation error due to the methods described here, but is worth noting that this could be the result of territoriality between individuals, as both male and female Cricetomys are known to be territorial (Ajayi et al. 1978).

In the present study, we observed C. emini burrows with entrances between 6 and 15 cm in diameter and the mean maximum diameter of burrow entrances was 11 cm (n = 27). This is similar to burrows reported by Ajayi (1977) who observed entrances between 4.5 and 15 cm in diameter for C. gambianus in a savanna area. Additionally, Ajayi (1977) reported that C. gambianus are known to have a maximum of four burrow exits in the savanna and human modified landscapes. We observed that the average number of entrances per burrow was 2.7 with a range of 1–5 entrances for C. emini. The number of burrow exits may be higher for C. emini in Thsuapa because the risk of predation may be higher due to human activities.

There are multiple paths and roads that connect Boende with surrounding villages and farms. The five C. emini individuals observed during this study were, on average, 123 m away from these paths, which were routinely used by human traffic (Figure 1). Given that we observed den site movements of up to 164.8 m during the study period, co-occurrence with humans and human activity is evident. This is concerning as giant pouched rats are a potential reservoir of MPXV (Doty et al. 2017; Drake 2005; Hutin et al. 2001) and other zoonotic pathogens. Additionally, the activity patterns observed here suggest a higher degree of diurnal activity than previously described for Cricetomys species (Ewer 1967; Majer 1973; Rosevear 1969; Yadok et al. 2019). It is possible that this result was impacted by our short observation period or our limited sample size, however, one explanation may be a lack of resources in the area, as Rosevear (1969) states that Cricetomys can be seen foraging for food in the daytime. Another explanation may be an increase in predator avoidance behavior caused by human disturbance. Hunters reportedly dig into burrows to catch these animals as a source of protein (Ajayi 1977; Assogbadjo et al. 2005; Kingdon 1997), and the proximity of the observed burrows to human activity means these animals are relatively convenient to be captured. In fact, one animal (Animal 1) observed in this study was captured by local hunters who returned the radio-collar to the authors during the study period and reported consuming the animal.