Rodent Assemblages in the Mosaic of Habitat Types in the Zambezian Bioregion

Home , Aethomys, Dendromus, Fat mouse, Grammomys, Gray climbing mouse, Gray tree rat

diversity

Article Rodent Assemblages in the Mosaic of Habitat Types in the Zambezian Bioregion

Vincent R. Nyirenda 1,* , Ngawo Namukonde 1 , Matamyo Simwanda 2 , Darius Phiri 2, Yuji Murayama 3 , Manjula Ranagalage 3,4 and Kaula Milimo 5 1 Department of Zoology and Aquatic Sciences, School of Natural Resources, Copperbelt University, P.O. Box 21692, Kitwe 10101, Zambia; [email protected] 2 Department of Plant and Environmental Sciences, School of Natural Resources, Copperbelt University, P.O. Box 21692, Kitwe 10101, Zambia; [email protected] (M.S.); [email protected] (D.P.) 3 Faculty of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba City, Ibaraki 305-8572, Japan; [email protected] (Y.M.); [email protected] (M.R.) 4 Department of Environmental Management, Faculty of Social Sciences and Humanities, Rajarata University of Sri Lanka, Mihintale 50300, Sri Lanka 5 Department of National Parks and Wildlife, Ministry of Tourism and Arts, Private Bag 1, Chilanga 10100, Zambia; [email protected] * Correspondence: [email protected]; Tel.: +260-977-352035

Received: 12 July 2020; Accepted: 21 September 2020; Published: 23 September 2020

Abstract: Rodent assemblages have ecological importance in ecosystem functioning and protected area management. Our study examines the patterns of assemblages of rodents across four habitat types (i.e., Miombo woodland, Acacia woodland, grasslands and farmlands) in the savanna environment. Capture-mark-recapture (CMR) methods were applied for data collection across the Chembe Bird Sanctuary (CBS) landscape. The Non-metric Multi-Dimensional Scaling (NMDS) was used for exploratory data analysis, followed by Analysis of Variance (ANOVA) and Tukey–Kramer’s Honestly Significant Difference (HSD) post-hoc tests. The rodent assemblages in CBS significantly differed between the non-farmlands (i.e., Miombo woodland, Acacia woodland and grasslands) and farmlands. There were: (1) zero rodent diversity in farmlands, dominated completely by a pest species, M. natalensis; and (2) different rodent assemblages in three non-farmland habitat types. We suggest that rodent assemblages should be mediated by conservation planning and multi-stakeholder collaboration beyond the protected area boundaries to contribute to a working CBS landscape positively.

Keywords: habitat preferences; habitat types; multiple rodent species; savanna; Zambia

1. Introduction Small mammals, defined as mammalian fauna with body mass less than 200 g, such as rodents [1], play an important ecological role in shaping the structure, composition and diversity of landscapes [2]. Rodents (Order: Rodentia) contribute positively to plant cover, and soil chemical and physical properties [3,4], and impact on landscapes through pollination and dispersal of seeds and fungal spores [5,6]. The rodents form a prey base to predators, such as snakes and birds of prey [7] and insects [8]. The rodents play a critical role in the food web in the savanna, as numerous predators depend on them as a source of food [9]. The rodent assemblage may be affected by the amount of vegetation cover protecting rodents from predators, and food availability for their survival in different habitat types, including farmlands [10–12]. The rodent diversity would be affected by the functional spatial heterogeneity of habitats they explore and occupy [13]. Such environmental factors, such as fire, vegetation types, and season, may proffer cues to rodents to utilise, or not, a particular space in time for food and denning [14–17]. Seasons may affect the availability of dietary items, such as seeds, flowers,

Diversity 2020, 12, 365; doi:10.3390/d12100365 www.mdpi.com/journal/diversity Diversity 2020, 12, 365 2 of 14 and fruits, for rodents [12]. Therefore, the use of different habitat types by rodents may be indicative of the landscape integrity [18] or ecosystem changes [19], based on the species assemblages [20]. Human-dominated landscapes can potentially reduce the assemblages and diversity of fauna [21], through the land conversion of natural landscapes to agriculture [22]. However, small mammals in agricultural areas may utilise vegetation remnants [23], and available food, which contribute to increased biodiversity across the landscapes [24,25]. At a landscape level, consisting of several ecosystems, such as wetland/grasslands, woodland and agro-ecosystems, rodents are expected to adapt their behaviour to avoid predation, and effectively search for food, mates, shelter and a suite of environmental conditions for their survival [26], thereby affecting their distribution. For instance, the rodents will endeavour to maximise their foraging benefits under given conditions in the landscapes, as predicted by Optimum Foraging Theory (OFT) [27], in combination with predation risk avoidance suggested by Optimal Escape Theory [28]. In the case of anti-predator responses of rodents, they are expected to increase during the breeding seasons (i.e., wet seasons) or during the post-parturient period when adult females are caring for their offspring, facing elevated predation risks for their progeny and themselves [29]. There is still a dearth of information on small mammal assemblages in tropical Africa, particularly for habitats in the Zambezian bioregion [30]. In this study, our focus was on the patterns of rodent assemblages across the CBS landscapes. Knowledge of rodent assemblages in an ecologically sensitive landscape, such as CBS, can be useful to conservation planning across conservation–agricultural interfaces. Anthropogenic activities, such as natural land (e.g., natural forested areas) conversions to various land uses, including agriculture, are ever-increasing and contributing to habitat fragmentation and biodiversity loss [22,31]. Nevertheless, in some cases, the conversion of natural lands to agricultural fields leads to increased biodiversity (e.g., [32]). We assumed that differences in rodent assemblages could be associated with seasonal variations in food availability (i.e., food deprivation or abundance) and vegetation cover [14,33–35]. Seasonal differences in physiognomic vegetation in various habitat types may also affect the rodent assemblages [36]. Other factors that may affect rodent assemblages include lunar phases and illumination, influencing prey–predator relationships [37] and wildfires [15]. Our key research question was: what are the patterns of rodent assemblages across CBS landscape? We hypothesise that rodent assemblages vary between farmlands and non-farmlands.

2. Data and Methods

2.1. Study Area

This study was conducted in CBS (27.9955◦ E, 12.8302◦ S; 539 ha) and its adjacent area, located in Kalulushi District, Zambia (Figure1). The study site lies in the Zambezian bioregion [ 30,38]. The area’s mean rainfall is 1200 mm per annum, and temperatures range between 18 and 30 ◦C[39]. Inside the CBS, there is Lake Chembe and outside the CBS are many wetlands, in the form of streams and ponds. The CBS is fenced and kept natural, precluding several anthropogenic activities, such as land clearing. The area is predominately Miombo woodland, characterised by Julbenadia, Brachystegia and Isobelinia tree species. The other vegetation types are Acacia woodland, mostly comprising Acacia tortilis and A. polyacantha, and open grasslands, constituting Setaria spp. and Hyparrhenia spp. Several termite (Macrotermes) mounds characterise both Miombo and Acacia woodlands. In addition, there are farmlands outside the CBS and these are owned by subsistence farmers. These farmers commonly cultivate maize (Zea mays). However, they also occasionally grow other crop varieties inter alia; sorghum (Sorghum bicolor), cassava (Manihot esculenta), sweet potatoes (Ipomoea batatas), beans (Phaseolus vulgaris) and groundnuts (Arachis hypogaea). These crops are among the dietary items consumed by some rodents. In the study area, there are a number of birds of prey, such as Barn owls, Tyto alba; spotted eagle owls, Bubo africanus; pearl spotted owls, Cilaucidium perlatum; and giant eagle owls, Bubo lacteus [40], which predate on rodents. The rodent-predator snakes known to inhabit the CBS landscape include Diversity 2020, 12, x FOR PEER REVIEW 3 of 14

DiversityTyto alba2020; spotted, 12, 365 eagle owls, Bubo africanus; pearl spotted owls, Cilaucidium perlatum; and giant eagle3 of 14 owls, Bubo lacteus [40], which predate on rodents. The rodent-predator snakes known to inhabit the CBS landscape include Puff adders (Bitis arietans arietans), Cape vine snakes (Thelotornis Pucapensisoatesiiﬀ adders (Bitis), Stripped arietans arietansgrass ),snakes Cape vine(Psammophylax snakes (Thelotornis tritaeniatus capensisoatesii) and Common), Stripped house grass snakes snakes (Psammophylax(Lamprophis fuliginosus tritaeniatus). ) and Common house snakes (Lamprophis fuliginosus).

FigureFigure 1.1. Locational map of the study area of Chembe Bird Sanctuary, Kalulushi, Zambia.

2.2.2.2. DataData CollectionCollection ProtocolsProtocols DataData werewere collected and and recorded recorded on on assemblages assemblages of ofrodents rodents across across four four habitat habitat types types of the of CBS the CBSlandscape landscape (Figure (Figure 2; Table2; Table 1), under1), under ethical ethical approval approval code codenumber number DNPW/101/9/77, DNPW /101 issued/9/77, issuedon 3 June on 32018 June by 2018 Departmentby Department of National of National Parks and Parks Wildlife and Wildlife (DNPW). (DNPW). The habitat The habitat types were types classified were classified based basedon the on vegetation the vegetation cover cover characteristics. characteristics. The Thecapture-mark-recapture capture-mark-recapture (CMR) (CMR) method method adopted adopted as asa aproxy proxy method method for for deriving deriving abundance abundance [41], [41], was was applied applied in in four four different different habitat habitat types types (i.e., (i.e., Miombo Miombo woodland,woodland, Acacia Acacia woodland,woodland, grasslandsgrasslands andand farmlands),farmlands), alongalong ten (10) transects, using 336 Sherman Sherman livelive trapstraps overover 3,3, 360360 traptrap nightsnights duringduring wetwet (December)(December) andand drydry (July–August) seasons of of 2018 2018 and and 2019,2019, respectively.respectively. TheThe habitathabitat typestypes werewere consideredconsidered asas stratastrata forfor datadata collection.collection. Both grids and transects (Figure2) were used for specific purposes: (1) the 200 m 200 m grids [42] were laid out for transects (Figure 2) were used for specific purposes: (1) the 200 m ×× 200 m grids [42] were laid out for determinationdetermination ofof wherewhere toto samplesample fromfrom inin thethe landscape;landscape; (2) transects (lines) were applied to guide thethe systematicsystematic settingsetting ofof traps.traps. The transects comprisedcomprised either 42 or 28 traps, resulting in transect lengthslengths of of 420 420 m orm 280or 280 m, totalling m, totalling 840 trap 840 nights trap fornights each for habitat each types habitat in 2018types and in 2019, 2018 respectively and 2019, (Tablerespectively1). Due (Table to Acacia 1). woodlandDue to Acacia mosaics woodland in the Miombo mosaics woodland in the Miombo on the south-western woodland on part the ofsouth- CBS, onewestern transect part was of CBS, longer one than transect others was to longer compensate than others for Acacia to compensate woodland for mosaics Acacia (Figure woodland2). Transects mosaics in(Figure the landscape 2). Transects originated in the landscape from random originated positions from within random the randomlypositions within selected the grids randomly and proceeded selected ingrids random and proceeded directions (Figurein random2). directions (Figure 2). Diversity 2020, 12, 365 4 of 14

Table 1. Numbers of captured rodents in wet and dry seasons across habitat types in Chembe Bird Sanctuary landscape, Zambia, in 2018–2019.

Mean Diversity Total No. Rodents Mean Total No. Rodents Captured * Equitability of Captured * Diversity (H’) Habitats No. Transects Trap Nights Pielou (J’) Mastomys Mus Saccostomus Steatomys Gerbilliscus Grammomys Dendromus Natalensis Minutoides Campestris Pratensis Leucogaster Surdaster Melanotis Miombo 0.611 0.12 3 840 27 (15) [34] 13 (0) [13] 0 (6) [6] 0 (0) [0] 16 (0) [16] 0 (0) [0] 0 (0) [0] 56 (21) [69] 0.856 (0.881) woodland (0.274 ± 0.18) 0.653 ± 0.11 Acacia woodland 2 840 59 (7) [61] 10 (0) [10] 24 (0) [24] 0 (0) [0] 0 (0) [0] 0 (8) [8] 0 (0) [0] 93 (15) [103] 0.799 (0.998) (0.250 ± 0.15) 0.688 ± 0.15 Grasslands 3 840 14 (13) [19] 8 (7) [11] 0 (0) [0] 20 (10) [23] 0 (0) [0] 0 (0) [0] 0 (7) [7] 42 (37) [60] 0.086 (0.980) (0.280 ± 0.18) Farmlands 2 840 85 (28) [94] 0 (0) [0] 0 (0) [0] 0 (0) [0] 0 (0) [0] 0 (0) [0] 0 (0) [0] 85 (28) [94] 0 (0)± 0 (0) 185 (63) Total 10 3360 31 (7) [34] 24 (6) [30] 20 (10) [23] 16 (0) [16] 0 (8) [8] 0 (7) [7] 276 (101) [326] - - [208] No. & percentage n = 14; 7.0% n = 3; 8.8% n = 3; 11.1% n = 1; 4.8% n = 2; 11.1% NA (n = 1; NA (n = 1; of rodents -- --- (n = 2; 3.1%) (n = 1; 12.5%) (n = 1; 14.3%) (n = 1; 9.1%) (NA) 11.1%) 12.5%) recaptured * Wet season captures, rodent counts and equitability values are shown outside the parentheses, (), and dry season related values inside the parentheses. In square brackets, [], are respective Minimum Number Alive (MNA). NA-Not applicable: no initial captures of individuals yielded. DiversityDiversity2020 2020,,12 12,, 365 x FOR PEER REVIEW 7 5of of 14 14

FigureFigure 2.2. Distribution of rodents and their abundance in dry and wet wet seasons seasons across across four four habitat habitat types types inin thethe ChembeChembe BirdBird SanctuarySanctuary landscape,landscape, Zambia,Zambia, 2018,2018, and 2019. Points Points in in Figure Figure 22 representrepresent thethe traptrap sitessites wherewhere capturescaptures (samples)(samples) werewere made,made, andand the sizes of points signify the number number of of rodent rodent captures.captures. TheThe transectstransects alongalong whichwhich samplessamples werewere collected are shown as solid brown lines.

AA traptrap session session per per season season consisted consisted of 5-trap of 5-trap nights, nights, conducted conducted in wet and in drywet seasons, and dry respectively, seasons, acrossrespectively, the four across habitats the infour 2018 habitats and 2019. in 2018 The and number 2019. ofThe Sherman number live of Sherman traps per live transect, traps andper transect, numbers ofand transects numbers per of habitat transects are depictedper habitat in Tableare depicted1. Sherman in Table live traps 1. Sherman on each live transect traps were on each separated transect by 10were m from separated each other,by 10 consideringm from each the other, local considerin scale heterogeneityg the local [ 43scale]. As heterogeneity baiting is commonly [43]. As baiting practised is ascommonly an effective practised way of rodentas an effective captures way due of to rodent its olfactory captures effect due [42 to], peanutits olfactory butter effect mixed [42], with peanut maize mealiebutter mealmixed in thewith form maize of a pastemealie was meal used in for the rodent form baitingof a paste in the was Sherman used livefor rodent traps. Being baiting nocturnal in the animals,Sherman the live traps traps. for Being rodents nocturnal were laid animals, at sunset the and trap inspecteds for rodents for catches were laid at sunrise at sunset the and next inspected morning. Byfor laying catches them at sunrise late in the the next day, morning. tampering Byby laying vervet them monkeys late in the (Chlorocebus day, tampering pygerythrus by vervet) was monkeys avoided. When(Chlorocebus inspected, pygerythrus only two) was of avoided. the empty When traps inspected, had each only at a singletwo ofinstance, the empty attracted traps had ants each (Order: at a Hymenoptera)single instance, in attracted them after ants laying (Order: them Hymenopter overnight ona) thein them transects. after laying them overnight on the transects.Further, the captured rodents were marked with ear-notches, followed by determination of their sex, age,Further, body the weights captured and rodents morphometrics were marked prior with to ear-notches, releasing them followed [44,45 by], determination and were considered of their susex,ffi cientage, tobody aid identificationweights and morphometrics of the recaptured prior individuals to releasing in the them subsequent [44,45], captures. and were The considered captured rodentssufficient were to aid weighed identification in-situ using of the Pesola recaptured spring individuals balances with in the a specification subsequent of captures. a maximum The captured specimen massrodents of 300were g allowable.weighed in-situ The target using rodents Pesola weighspring less balances than 300 with g(mean a specification= 40.58 of2.24 a g;maximumn = 377). ± Inspecimen addition, mass tail, of ear 300 and g allowable. hindfoot The lengths target of rodents rodents weigh were less measured than 300 using g (mean callipers = 40.58 and ± 2.24 applied g; n to= 377). ascertain In addition, the identity tail, ofear the and recaptured hindfoot rodents.lengths of The rodents visual were sex determinationmeasured using was callipers conducted and byapplied examining to ascertain the genital the organsidentity of of captured the recapt rodentsured visuallyrodents. whileThe visual age was sex determined determination by visual was examinationconducted by of examining fur colour, the texture genital and organs body of size. captured The Garmin-ETrex rodents visually 30 Globalwhile age Positioning was determined System (GPS)by visual sets examination were used to of collect fur colour, geographic texture data. and body size. The Garmin-ETrex 30 Global Positioning System (GPS) sets were used to collect geographic data. 2.3. Data Analysis 2.3. Data Analysis To derive patterns (i.e., similarities and differences) among rodent communities, we conducted a multivariateTo derive analysis patterns of Bray–Curtis(i.e., similarities dissimilarity and differences) matrices among by Non-metric rodent communities, Multi-Dimensional we conducted Scaling (NMDS)a multivariate ordination. analysis The of input Bray–Curtis data were dissimil the transectarity IDs,matrices habitat by typesNon-metric and counts Multi-Dimensional of captures per species.Scaling There(NMDS) were ordination. 5 and 6 taxa The used input in the data analysis were for the the transect wet and IDs, dry season,habitat respectively. types and counts Data were of

Diversity 2020, 12, 365 6 of 14 normalised a priori by conversion from absolute abundance to relative abundance to maintain their robustness. NMDS analyses were conducted using Vegan package in R-statistical software, version 3.6.1 [46]. Stress values were generated for model validation. We assumed homogeneity of multivariate dispersion of rodents, and tested it using distance-based ANOVA test to reveal deviations of rodent assemblages from individual habitat types [47,48]. Comparison of derived Shannon–Weiner indices of the diversity of rodents was conducted by converting to their diversity equitability ([49,50]; Equations (1) and (2)). In Equation (1), the Shannon–Weiner index (H’) was derived from sample species of rodents, where Pi is the proportion of captured rodents in the samples of a particular number, i, of individuals per habitat type, lnPi is the natural logarithm of the proportion of the captured rodents while S is the number of sampling units. In Equation (2), diversity equitability of Pielou (J’) is used to enable comparisons of the diversity of rodents between habitat types, where H’max is the natural logarithm of the number of species [ln(S)]. The diversity and its equitability values were calculated using 5-night trap sessions per season. A one-way Analysis of Variance (ANOVA) was based on a completely randomised design, established on randomly selected grids used in the setting of transects for data collection [51]. Further, the Minimum Number Alive (MNA) was determined from the rodent capture counts. MNA referred to the number of individual rodents caught in a 5-night trap session, plus those that were not caught during that particular session but were caught both previously and subsequently [52]. The number of recaptured rodents was not considered in the analyses of assemblages and diversity. The ANOVA was followed by Tukey–Kramer’s Honestly Significant Difference (HSD) post-hoc tests at α = 0.05 for multiple comparisons of means to determine which habitat types had significantly different rodent assemblages across seasons. Data analyses were performed in R statistical software, version 3.6.1 [46].

XS H0 = Piln(Pi) (1) i=1

J0 = H0/H0max (2)

3. Results A total of 377 individuals of seven sympatric rodent species were captured during the wet and dry surveys (Figure2; Table1). The captured rodent species include five murids (family: Muridae): Natal multimammate rat, Mastomys natalensis; Southern African pygmy mouse, Mus minutoides; Fat mouse, Steatomys pratensis; Bushveld gerbil, Gerbilliscus leucogaster; and African woodland thicket rat, Grammomys surdaster. The other two rodent species were nesomyids (family: Nesomyidae): Southern African pouched mouse, Saccostomus campestris; and Gray climbing mouse, Dendromus melanotis. M. natalensis was the most abundant species (n = 248; 65.8%) across seasons and habitat types. Most of the rodent captures were observed in the wet seasons (n = 276; 73.2%). In dry seasons, the rodent assemblages appear to be more clumped (i.e., the concentration of species in particular habitat types) than in the wet seasons across habitat types, except in farmlands dominated by M. natalensis (Figure3a). On the other hand, the rodent assemblages seem random (i.e., pattern assortment with no particular order across habitat types) during dry seasons (Figure3b). For the rodent assemblages in both wet and dry seasons, the stress values are <0.1 with dimensions k = 2, lying within acceptable limits as an indication of well-preserved original dissimilarities in a reduced number of dimensions (Figure4a,b). There seem to be higher variability in rodent assemblages in wet seasons [F(3,38) = 3.659, p = 0.021] compared to dry seasons when the dispersion is very weak [F(3,21) = 0.499, p = 0.687] (Figure3). In both wet and dry seasons, all species except M. natalensis showed avoidance of the farmlands. Further, in the wet season, 52.9% (n = 146) were associated with flood-prone spaces, while in the dry season, all captured rodents were captured in flood-prone spaces. Several captured rodents (n = 65; 84.4%) in Miombo woodland were in proximity with termite mounds (<10 m). The number of recaptured rodents Diversity 2020, 12, x FOR PEER REVIEW 9 of 14 Diversity 2020, 12, x FOR PEER REVIEW 9 of 14 The diversity of rodents varied significantly between farmlands and other habitat types in wet The diversity of rodents varied significantly between farmlands and other habitat types in wet and dry seasons, respectively [F(3,38) = 5.127, p = 0.004; F(3,21) = 0.758, p = 0.035]. Comparison of Figure and dry seasons, respectively [F(3,38) = 5.127, p = 0.004; F(3,21) = 0.758, p = 0.035]. Comparison of Figure Diversity5a,b depict2020, 12higher, 365 mean diversity in the wet seasons than in the dry seasons, depicting similar7 of 14 5a,bpatterns depict across higher habitat mean types. diversity The diversity in the wet of rodeseasonsnt species than invaried the drysignificantly seasons, depictingbetween out-CBS similar patternsfarmlands across and counterparthabitat types. in-CBS The diversityhabitat types, of rode whntile species there were varied insignificant significantly variations between among out-CBS in- ranged from 4.8% to 11.1% in wet seasons and 3.1% to 14.3% in dry seasons (Table1). There were farmlandsCBS habitats and (Figure counterpart 5a,b). in-CBS habitat types, while there were insignificant variations among in- varyingCBS habitats minimum (Figure numbers 5a,b). of rodents across seasons and habitat types (Table1).

Figure 3. Species–habitat associations of rodent community in the Chembe Bird Sanctuary landscape, Figure 3. Species–habitat associations of rodent community in the Chembe Bird Sanctuary landscape, FigureZambia, 3. inSpecies–habitat 2018–2019 in associationswet (a) and ofdry rodent (b) seasons, community respectively, in the Chembe derived Bird from Sanctuary Non-metric landscape, Multi- Zambia, in 2018–2019 in wet (a) and dry (b) seasons, respectively, derived from Non-metric Zambia,Dimensional in 2018–2019 Scaling. Thein wet terminal (a) and points dry (inb) Figureseasons, 3a,b respectively, reveal networks derived of differentfrom Non-metric rodent samples Multi- Multi-Dimensional Scaling. The terminal points in Figure3a,b reveal networks of di ﬀerent rodent Dimensionalin particular Scaling.habitats. The Line terminal colours pointsshow thein Figure similari 3a,bty ofreveal species networks presence of differentin a particular rodent habitat samples in samples in particular habitats. Line colours show the similarity of species presence in a particular inrelation particular to other habitats. habitats. Line In colours Figure show 3b, Sc the in similariMiomboty woodland of species representspresence in S .a campestris particular, whilehabitat Dm in habitat in relation to other habitats. In Figure3b, Sc in Miombo woodland represents S. campestris, relationand Mm to in other grasslands habitats. represent In Figure D. melanotis3b, Sc in andMiombo M. minutoides woodland, respectively. represents S . campestris, while Dm whileand Mm Dm in and grasslands Mm in grasslands represent D represent. melanotisD .andmelanotis M. minutoidesand M. minutoides, respectively., respectively.

Figure 4. Stress plots (Shepard’s diagrams) showing the fitfit of configurationconfiguration inin twotwo dimensionsdimensions ((kk == 2)2) withFigurewith originaloriginal 4. Stress data data plots patterns patterns (Shepard’s of countsof countsdiagrams) in the in rodent theshowing ro communitiesdent the communities fit of inconfiguration the Chembe in the in BirdChembe two Sanctuary dimensions Bird landscape,Sanctuary (k = 2) withZambia,landscape, original in 2018–2019Zambia, data patterns in in 2018–2019 wet (ofa) andcounts in dry wet in (b ()thea seasons,) androdent dry respectively. communities(b) seasons, The respectively.in hollow the Chembe circles The (points)Bird hollow Sanctuary and circles red landscape,lines(points) (i.e., and monotonic Zambia, red lines in step 2018–2019(i.e., lines) monotonic represent in wet rodentstep(a) and lin counts es)dry represent (b and) seasons, the modelrodent respectively. fits,counts respectively. and The the hollow model circles fits, (points)respectively. and red lines (i.e., monotonic step lines) represent rodent counts and the model fits, respectively.The diversity of rodents varied significantly between farmlands and other habitat types in wet and dry seasons, respectively [F(3,38) = 5.127, p = 0.004; F(3,21) = 0.758, p = 0.035]. Comparison of Figure5a,b depict higher mean diversity in the wet seasons than in the dry seasons, depicting similar patterns across habitat types. The diversity of rodent species varied significantly between out-CBS farmlands and counterpart in-CBS habitat types, while there were insignificant variations among in-CBS habitats (Figure5a,b).

Diversity 2020, 12, 365 8 of 14 Diversity 2020, 12, x FOR PEER REVIEW 10 of 14

FigureFigure 5. 5. MeanMean diversity diversity of of rodents rodents across across different different habi habitattat types types in in Chembe Chembe Bird Bird Sanctuary Sanctuary landscape, landscape, Zambia,Zambia, in 2018–20192018–2019 in in wet wet (a )( anda) and dry dry (b) seasons,(b) seasons, respectively. respectively. The error The bars error represent bars represent the standard the standarderrors in errors the mean in the diversity mean ofdivers rodents.ity of Lettersrodents. a, Letters b, and aba, b, above and theab above bar graphs the bar denote graphs significant denote significantdifferences differences of mean diversity of mean of diversity rodents amongof rodents diff amongerent habitat different types. habitat types. 4. Discussion 4. Discussion This study reveals dynamic patterns of rodent assemblages across seasons and habitats in the This study reveals dynamic patterns of rodent assemblages across seasons and habitats in the CBS landscape (Figures3 and5; Table1). Although specific behavioural (activity) data per species CBS landscape (Figures 3 and 5; Table 1). Although specific behavioural (activity) data per species is is outside the scope of this study, it can be speculated based on patterns of rodent assemblages in outside the scope of this study, it can be speculated based on patterns of rodent assemblages in CBS CBS landscape in this study that seasonality in the rodent assemblages might have been affected by a landscape in this study that seasonality in the rodent assemblages might have been affected by a number of factors, inter alia: (1) vegetation cover for protection from predators and food availability, number of factors, inter alia: (1) vegetation cover for protection from predators and food availability, which are usually more abundant in wet seasons than in dry seasons [14,53]; (2) as a result of food which are usually more abundant in wet seasons than in dry seasons [14,53]; (2) as a result of food availability and vegetation cover, rodents prefer breeding and raising offspring in the wet seasons availability and vegetation cover, rodents prefer breeding and raising offspring in the wet seasons to to the dry seasons [54–56]; (3) rodents may experience torpor during the dry seasons to conserve the dry seasons [54–56]; (3) rodents may experience torpor during the dry seasons to conserve energy energy [57,58]; (4) rodents would also cache food for use when in short supply in the dry seasons [57,58]; (4) rodents would also cache food for use when in short supply in the dry seasons or food or food deficient years, which could further limit demand for foraging [59,60]; and (5) some species, deficient years, which could further limit demand for foraging [59,60]; and (5) some species, such as such as D. melanotis would prefer dry grasses to fresh ones [9]. D. melanotis would prefer dry grasses to fresh ones [9]. Compared with their conspecifics, M. natalensis is most abundant in this study and occurring in all Compared with their conspecifics, M. natalensis is most abundant in this study and occurring in the habitat types, probably due to their being an omnivorous species and generalists [61]. M. natalensis all the habitat types, probably due to their being an omnivorous species and generalists [61]. M. was dominant in all habitats except in grasslands where it was less common, probably due to it natalensis was dominant in all habitats except in grasslands where it was less common, probably due being a generalist forager [62] and the presence of other environmental resources, such as vegetation to it being a generalist forager [62] and the presence of other environmental resources, such as cover for protection from predators. Apart from M. natalensis, all the other rodents in CBS depicted vegetation cover for protection from predators. Apart from M. natalensis, all the other rodents in CBS some form of habitat specialisation (Table1) and, thus, spatial niche partitioning. However, rodents depicted some form of habitat specialisation (Table 1) and, thus, spatial niche partitioning. However, other than M. natalensis have also been recorded to occur in human-modified rural agricultural-fallow rodents other than M. natalensis have also been recorded to occur in human-modified rural mosaic landscapes in Africa [63]. Spatial niche partitioning is an important means of co-occurrence agricultural-fallow mosaic landscapes in Africa [63]. Spatial niche partitioning is an important means of rodent species in a landscape [64]. In particular, the diversity of specialized species is likely to of co-occurrence of rodent species in a landscape [64]. In particular, the diversity of specialized be negatively impacted upon by farmlands due to the limited choice of food and homogeneity of species is likely to be negatively impacted upon by farmlands due to the limited choice of food and habitat that limits their survival across time and space [65]. For instance, S. pratensis specialised in homogeneity of habitat that limits their survival across time and space [65]. For instance, S. pratensis utilising the grasslands, similar to the observation by [66], and they were relatively many during the specialised in utilising the grasslands, similar to the observation by [66], and they were relatively dry seasons when they were supposed to be hibernating. This could be indicative of some behavioural many during the dry seasons when they were supposed to be hibernating. This could be indicative change worth further study. Similarly, M. minutoides was recorded in all habitats except on farmlands, of some behavioural change worth further study. Similarly, M. minutoides was recorded in all habitats while S. campestris utilised the woodland (i.e., Miombo and Acacia) and can be evolutionarily linked to except on farmlands, while S. campestris utilised the woodland (i.e., Miombo and Acacia) and can be such environments [67]. G. leucogaster, G. surdaster, and D. melanotis exclusively utilised the Miombo evolutionarily linked to such environments [67]. G. leucogaster, G. surdaster, and D. melanotis woodland, Acacia woodland and grasslands, respectively. Though Aethomys chrysophilus were expected exclusively utilised the Miombo woodland, Acacia woodland and grasslands, respectively. Though Aethomys chrysophilus were expected to be abundant in the African miombo woodland [38], none were captured and recorded during this study. G. surdaster appears to prefer thickets, such as Acacia

Diversity 2020, 12, 365 9 of 14 to be abundant in the African miombo woodland [38], none were captured and recorded during this study. G. surdaster appears to prefer thickets, such as Acacia woodland for their vegetation cover from predation and nesting sites [68]. As rodents respond to seasonal changes in the habitat types by adjusting their foraging behaviours, captures could also reduce in dry seasons as also observed by [64]. Further, the increase in diversity of rodents in the wet seasons coincides with the heightened food caching activity during the food abundant seasons [69]. The hoarding behaviour in rodents would be linked to productivity in a particular landscape (e.g., [70]), and available suitable food types [59]. Further, the rodent MNA seemed to vary across species, habitat types and seasons (Table1). Like in other studies on rodents in Africa [71,72], M. natalensis had the highest populations, which peaked in the wet season. Acacia and farmlands had relatively higher M. natalensis populations than other habitat species, probably due to supportive habitat attributes, such as food availability. Varying conditions in particular habitat type might lead to changing rodent populations, which would also manifest from sporadic movements of rodents from one habitat to another [50]. The diversity of rodents in the Miombo woodland in CBS can be attributed to several factors, such as vegetation cover and a variety of food items across seasons [73,74]. While ordinarily Miombo woodland is expected to have relatively low fauna productivity, the resource-rich termite mounds in Miombo woodland could have contributed to increased abundance and richness of rodents [75], as food abundance facilitates breeding and survival in rodents [76]. The lower diversity in farmlands than in different habitat types in CBS could be a result of mono-specific cropping which favours generalist species [61], and usually seasonal cereal crops, which form restrictive single food types to specialised rodent species. Temporal variations in food availability can have negative effects on rodents and their predators [77]. While vegetation cover could have attracted rodents to Acacia woodland, grasslands with massive ground vegetation cover were interspersed by some flood areas, which are potentially resource and food-rich areas capable of attracting rodents as well [78].

5. Conservation Implications Conservation of rodent populations is critical in small ecologically compressed and isolated sanctuaries, embedded in a human-dominated landscape, such as CBS where several predators, such as snakes, and birds of prey depend on them. Such an ecologically isolated sanctuary has the potential to conserve dwindling biodiversity [79]. The responsible wildlife agency and land owners around the CBS can benefit from the insights unravelled in this study, where rodents can be used as a general model group for the proposition of management steps towards protection of diversity in the area by (1) not increasing the area of farmlands into CBS and (2) protecting the mosaic of all present natural habitats. For instance, to sustain high rodent assemblages and diversity, more mosaics of natural and non-natural, agricultural and fallow, different habitat types are needed beyond CBS boundaries while land owners integrate practices that encourage balancing rodent conservation and crop protection [63,80,81]. This requires the broad-based participation of multiple stakeholders to assist with conservation planning and maximising expanses of natural areas under a form of protection to increase the potential for species persistence [82,83]. Foraging behaviour can also provide vital information for pest management, as in the case of M. natalensis that may be utilising the nearby farmlands as sink areas, and as such future research could comprehensively focus on the effects of farmlands and fallow fields on rodent assemblages in comparison with non-farmlands. Previously, ecological based rodent management has been proposed to eradicate rodents, such as M. natalensis, by trappings and the removal of vegetation cover and food sources [72], but we counter-propose that while methods of achieving food security need to be further explored or implemented, care should be taken in employing such methods in agrarian areas adjoining conservation areas. In return, local communities living adjacent to the protected area should be sufficiently supported to benefit from wildlife utilisation through various ecotourism businesses to sustain their support over wildlife conservation [84]. Diversity 2020, 12, 365 10 of 14

6. Conclusions Our study has demonstrated that even small isolated conservation areas are important for maintaining terrestrial small mammal assemblages and diversity. Seasons and habitat types seem to be among the key factors aﬀecting the rodent assemblages and diversity in the CBS, inﬂuencing the species co-existence and habitat preferences. The suppressed rodent assemblages and diversity could negatively be impacted upon by stochastic factors, such as environmental changes, leading to species extirpation. Therefore, we propose that such interactions should be mediated by conservation planning and multi-stakeholder collaboration, through dialogue and sensitisation of landowners/farmers bordering the conservation areas.

Author Contributions: Conceptualization, V.R.N. and N.N.; Methodology, V.R.N. and N.N.; Analysis, V.R.N.; Investigation, V.R.N., N.N., M.S., D.P. and K.M.; Resources, V.R.N., N.N., M.S., D.P., and Y.M.; Draft Preparation, V.R.N.; Internal Review and Editing, V.R.N., N.N., M.S., D.P., Y.M., M.R., and K.M.; Visualization, V.R.N., M.S., and D.P.; Project Administration, V.R.N. and N.N.; Funding Acquisition, Y.M., and M.S. All authors have read and agreed to the published version of the manuscript. Funding: This study was partly supported by the JSPS grant 18H00763 (2018-20). Acknowledgments: The Copperbelt University (CBU), and DNPW authorised this study. The anonymous reviewers are thanked for their contribution to the improvement of manuscript quality. We are also grateful to Conrald Kunda, Remmy Kopeka and Clausin Chulu for their participation in the data collection. Conﬂicts of Interest: The authors declare no conﬂict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; and in the decision to publish the results.

References

1. Kurten, E.L. Cascading effects of contemporaneous defaunation of tropical forest communities. Biol. Conserv. 2013, 163, 22–32. [CrossRef] 2. Johnson, S.; Burgoyne, P.; Harder, L.D.; Dotterl, S. Mammal pollinators lured by the scent of a parasitic plant. Proc. R. Soc. B 2011, 278, 2303–2310. [CrossRef][PubMed] 3. Galiano, D.; Kubiak, B.B.; Overbeck, G.E.; de Freitas, T.R.O. Effects of rodents on plant cover, soil hardness, and soil nutrient content: A case study on tuco-tucos (Ctenomys minutes). Acta Theriol. 2014, 59, 583–587. [CrossRef] 4. Yong, S.K.; Jalaludin, N.H.; Brau, E.; Shamsudin, N.N.; Heo, C.C. Changes in soil nutrients (ammonia, phosphate and nitrate) associated with rat carcass decomposition under tropical climate conditions. Soil Res. 2019, 57, 482–488. [CrossRef] 5. Flores-Peredo, R.; Sánchez-Velásquez, L.; Galindo-González, J.; Morales-Mávil, J. Post-dispersed pine seed removal and its effect on seedling establishment in a Mexican Temperate Forest. Plant. Ecol. 2011, 212, 1037–1046. [CrossRef] 6. Stephens, R.B.; Rowe, R.J. The underappreciated role of rodent generalists in fungal spore-dispersal networks. Ecology 2020.[CrossRef][PubMed] 7. Labuschagne, L.; Swanepoel, L.H.; Taylor, P.J.; Belmain, R.R.; Keith, M. Are avian predators effective biological control agents for rodent pest management in agricultural systems? Biol. Control 2016, 101, 94–102. [CrossRef] 8. Moretti, T.; Benedito, R.O.; Thyssen, P.; Russ Solis, D. Insects on decomposing carcasses of small rodents in a secondary forest in Southeastern Brazil. Eur. J. Entomol. 2008, 105, 691–696. [CrossRef] 9. Byrom, A.; Ruscoe, W.; Nkwabi, A.; Metzger, K.; Forrester, G.; Craft, M.; Durant, S.; Makacha, S.; Bukombe, J.; Mchetto, J.; et al. Small mammal diversity and population dynamics in the greater Serengeti ecosystem. In Serengeti IV: Sustaining Biodiversity in a Coupled Human-Natural System; Sinclair, A.R.E., Metzger, K.L., Mduma, S.A.R., Fryxell, J.M., Eds.; University of Chicago Press: Chicago, IL, USA, 2015; pp. 323–357. [CrossRef] 10. Manning, J.; Edge, W. Small mammals responses to fine woody depris and forest fuel reduction in southwest Oregon. J. Wildl. Manag. 2008, 72, 625–632. [CrossRef] Diversity 2020, 12, 365 11 of 14

11. Mulungu, L.S.; Borremans, B.; Ngowo, V.; Mdangi, M.E.; Katakweba, A.S.; Tesha, P.; Mrosso, F.P.; Mchomvu, M.; Kilonzo, B.S. Comparative study of movement patterns of Mastomys natalensis in irrigated rice and fallow fields in eastern Tanzania. Afr. J. Ecol. 2015, 53, 473–479. [CrossRef] 12. Sellers, L.; Long, R.; Baldwin, R.A.; Jay-Russell, M.; Li, X.; Atwill, E.R.; Engeman, R.M. Impact of field border plantings on rodents and food safety concerns. Proc. Vertebr. Pest. Conf. 2016, 27, 150–155. [CrossRef] 13. Zhang, S.; Zhu, M.; Zhang, H.; Yao, N.; Wang, Y.; Zhang, Y.; Wang, Z. Complex spatial patterns delay the food discovery and locating of rodents. Integr. Zool. 2020.[CrossRef] 14. Flores-Peredo, R.; Vázquez-Domínquez, Y.G. Influence of vegetation type and season on rodent assemblage in a Mexican temperate forest mosaic. Therya 2016, 3, 357–369. [CrossRef] 15. Namukonde, N.; Daniel, K.; Jörg, U.G. Differential effects of fire on small mammal communities in Busanga plain, Zambia. Trop. Conserv. Sci. 2017, 10, 1–13. [CrossRef] 16. Babale, A.; Joshua, A.; Elena, M.; Pierre-Michel, F. Forest disturbance and seasonal food availability influence a conditional seed dispersal mutualism. Biotropica 2018, 50, 750–757. [CrossRef] 17. Garrido-García, J.A.; Nieto-Lugilde, D.; Alba-Sánchez, F.; Soriguer, R.C. Agricultural intensification during the late Holocene rather than climatic aridification drives the population dynamics and the current conservation status of Microtus cabrerae, an endangered Mediterranean rodent. J. Biogeogr. 2018, 45, 448–460. [CrossRef] 18. Avenant, N. The potential utility of rodents and other small mammals of indicators of ecosystem integrity of South African grasslands. Wildl. Res. 2011, 38, 626–639. [CrossRef] 19. Ofori, B.Y.; Attuquayefio, D.K.; Owusu, E.H.; Musah, Y.; Ntiamoa-Baidu, Y. Spatio-temporal variation in small mammal species richness, relative abundance and body mass reveal changes in a coastal wetland ecosystem in Ghana. Environ. Monit. Assess. 2016, 188, 1–10. [CrossRef][PubMed] 20. Milstead, B.; Meserve, P.; Campanella, A.; Previtali, K.; Gutierrez, R. Spatial ecology of small mammals in north-central Chile: Role of precipitation and refuges. J. Mammal. 2007, 88, 1532–1538. [CrossRef] 21. Hurst, Z.M.; McCleery, R.A.; Collier, B.A.; Fletcher, R.J., Jr.; Silvy, N.J.; Taylor, P.J.; Monadjem, A. Dynamic edge effects in small mammal communities across a conservation-agricultural interface in Swaziland. PLoS ONE 2013, 8, e74520. [CrossRef][PubMed] 22. Balestrieri, A.; Remont, L.; Morotti, L.; Saino, N.; Prigioni, C.; Guidali, F. Multilevel habitat preferences of Apodemus syvaticus and Clethrionomys glareolus in an intensively cultivated agricultural landscape. Ethol. Ecol. Evol. 2017, 29, 38–53. [CrossRef] 23. Ellis, E.; Ramankutty, N. Putting people in the map: Anthropogenic biomes of the world. Front. Ecol. Environ. 2008, 6, 439–447. [CrossRef] 24. Monadlem, A.; Mahlaba, T.; Dlamini, N.; Eiscb, S.; Belmain, S. Impact of crop cycle on movement patterns of pest rodent species between fields and houses in Africa. Wildl. Res. 2011, 38, 603–609. [CrossRef] 25. Nikolić, T.; Radišić, D.; Cosić,´ N.; Díaz-Delgado, R.; Milić, D.; Vujić, A.; Cirović,´ D. Landscape heterogeneity effects on keystone rodent species: Agro-ecological zoning for conservation of open grasslands. Biodivers. Conserv. 2019.[CrossRef] 26. Yadok, B.G.; Pech, R.; Chapman, H. Perception of predation risk by African giant pouched rats (Cricetomys sp. nov) is higher in forest-edge microhabitats. Behav. Process. 2019, 168, 103953. [CrossRef][PubMed] 27. Pyke, G.H. Optimal foraging theory: A critical review. Annu. Rev. Ecol. Evol. Syst. 1984, 15, 523–575. [CrossRef] 28. Cooper, W.E., Jr.; Frederick, W.G. Optimal flight initiation distance. J. Theor. Biol. 2007, 224, 59–67. [CrossRef] [PubMed] 29. Ciuti, S.; Pipia, A.; Ghiandai, F.; Grignolio, S.; Apollonio, M. The key role of lamb presence in affecting flight response in Sardinian mouflon (Ovis orientalis musimon). Behav. Process. 2008, 77, 408–412. [CrossRef] 30. Linder, H.P.; de Klerk, H.M.; Born, J.; Burgess, N.D.; Fjeldsa, J.; Rahbek, C. The partitioning of Africa: Statistically defined biogeographical regions in sub-Saharan Africa. J. Biogeogr. 2012, 39, 1189–1205. [CrossRef] 31. Millennium Ecosystem Assessment. Ecosystems and Human Well-Being: Biodiversity Synthesis; World Resources Institute: Washington, DC, USA, 2005. 32. Koneˇcný, A.; Koubek, P.; Bryja, J. Indications of higher density and abundance of small rodents in human-influenced Sudanian savannah than in the Niokolo Koba National Park (Senagal). Afr. J. Ecol. 2010, 48, 718–726. [CrossRef] 33. Nicolas, V.; Colyn, M. Seasonal variations in population and community structure of small rodents in a tropical forest of Gabon. Can. J. Zool. 2003, 81, 1034–1046. [CrossRef] Diversity 2020, 12, 365 12 of 14

34. Addisu, A.; Bekele, A. Habitat preferences, seasonal abundance and diets of rodents in Alage, southern Ethiopia. Afr. J. Ecol. 2013, 52, 284–291. [CrossRef] 35. Ramírez-Bautista, A.; Williams, J.N. The importance of productivity and seasonality for structuring small rodent diversity across a tropical elevation gradient. Oecologia 2019, 190, 275–286. [CrossRef][PubMed] 36. Magige, F.; Senzota, R. Abundance and diversity of rodents at the human-wildlife interface in Western Serengeti, Tanzania. Afr. J. Ecol. 2006, 44, 371–378. [CrossRef] 37. Johnson, M.; De León, Y. Effect of an invasive plant and moonlight on rodent foraging behavior in a coastal dune ecosystem. PLoS ONE 2015, 10, e0117903. [CrossRef][PubMed] 38. Mazoch, V.; Mikula, O.; Bryja, J.; Konviˇcková, H.; Russo, I.-R.; Verheyen, E.; Šumbera, R. Phylogeography of a widespread sub-Saharan murid rodent Aethomys chrysophilus: The role of geographic barriers and paleoclimate in the Zambezian bioregion. Mammalia 2018, 82, 373–387. [CrossRef] 39. Conservation Farming Unit. Conservation Farming and Conservation Agriculture Handbook for Hoe Farmers in Agro-Ecological Regions I and IIa; Conservation Farming Unit: Lusaka, Zambia, 2009. 40. Nyirenda, V.R.; Musonda, F.; Kambole, S.; Tembo, S. Peasant farmer–raptor conflicts around Chembe Bird Sanctuary, Zambia, Central Africa: Poultry predation, ethno–biology, land use practices and conservation. Anim. Biodivers. Conserv. 2017, 40, 121–132. [CrossRef] 41. Anthony, N.M.; Ribic, C.A.; Bautz, R.; Garland, T., Jr. Comparative effectiveness of Longworth and Sherman live traps. Wildl. Soc. Bull. 2005, 33, 1018–1026. [CrossRef] 42. Andrzejewski, R. The home-range concept in rodents revised. Acta Theriol. 2002, 47, 81–101. [CrossRef] 43. Foord, S.H.; Swanepoel, L.H.; Evans, S.W.; Schoeman, C.S.; Erasmus, B.; Schoeman, M.C.; Keith, M.; Smith, A.; Mauda, E.V.; Maree, N.; et al. Animal taxa contrast in their scale-dependent responses to land use change in rural Africa. PLoS ONE 2018, 13, e0194336. [CrossRef] 44. Bergeron, P.; Réale, D.; Humphries, M.M.; Garant, D. Anticipation and tracking of pulsed resources drive population dynamics in eastern chipmunks. Ecology 2011, 92, 2027–2034. [CrossRef] 45. Hansen, N.; Hughes, N.K.; Byrom, A.E.; Banks, P.B. Population recovery of alien black rats Rattus rattus: A test of reinvasion theory. Austral. Ecol. 2020, 45, 291–304. [CrossRef] 46. R Core Development Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2019. 47. Anderson, M.J. Distance-based test for homogeneity of multivariate dispersions. Biometrics 2006, 62, 245–253. [CrossRef] 48. Gijbels, I.; Omelka, M. Testing for homogeneity of multivariate dispersions using dissimilarity measures. Biometrics 2013, 69, 137–145. [CrossRef][PubMed] 49. Brady, M.J.; Slade, N.A. Diversity of a grassland rodent community at varying temporal scales: The role of ecologically dominant species. J. Mammal. 2001, 82, 974–983. [CrossRef] 50. Mortelliti, A.; Boitani, L. Patterns of rodent species diversity and abundance in a Kenyan relict tropical rainforest. Biodivers. Conserv. 2006, 15, 1425–1440. [CrossRef] 51. Dag, O.; Dolgun, A.; Konar, N.M. Onewaytests: An R package for one-way tests in independent group designs. R J. 2018, 10, 175–199. [CrossRef] 52. Krebs, C.J. Demographic changes in fluctuating populations of Microtus californicus. Ecol. Monogr. 1966, 36, 239–273. [CrossRef] 53. Sunyer, P.; Munoz, A.; Mazerolle, M.; Bonal, R.; Espelta, J.M. Wood mouse population dynamics: Interplay among seed abundance seasonality, shrub cover and wild boar interference. Mamm. Biol. 2016, 81, 372–379. [CrossRef] 54. Massawe, A.W.; Makundi, R.H.; Mulungu, L.S.; Katakweba, A.; Shayo, T.N. Breeding dynamics of rodent species inhabiting farm–fallow mosaic fields in Central Tanzania. Afr. Zool. 2012, 47, 128–137. [CrossRef] 55. Gasperini, S.; Mortelliti, A.; Bartolommei, P.; Bonacchi, A.; Manzo, E.; Cozzolino, R. Effects of forest management on diversity and survival in three forest rodent species. For. Ecol. Manag. 2016, 382, 151–160. [CrossRef] 56. Hoset, K.S.; Villers, A.; Wistbacka, R.; Selonen, V. Pulsed food resources, but not forest cover, determine lifetime reproductive success in a forest-dwelling rodent. J. Anim. Ecol. 2017, 86, 1235–1245. [CrossRef] [PubMed] Diversity 2020, 12, 365 13 of 14

57. Ellison, G.T.H.; Skinner, J.D. The influence of ambient temperature on spontaneous daily torpor in pouched mice (Saccostomus campestris: Rodentia: Cricetidae) from southern Africa. J. Therm. Biol. 1992, 17, 25–31. [CrossRef] 58. Smith, S.E.; Ramos, F.A.; Refinetti, R.; Farthing, J.P.; Paterson, P.G. Proteinenergy malnutrition induces an aberrant acute-phase response and modifies the circadian rhythm of core temperature. Appl. Physiol. Nutr. Metab. 2013, 38, 844–853. [CrossRef] 59. Charron, I.; Cabanac, M. Influence of pellet size on rat’s hoarding behaviour. Physiol. Behav. 2004, 82, 447–451. [CrossRef] 60. Yadok, B.G.; Forget, P.-M.; Gerhard, D.; Chapman, H. Low fruit-crop years of Carapa oreophila drive increased seed removal and predation by scatter hoarding rodents in a West African forest. Acta Oecol. 2019, 99, 103448. [CrossRef] 61. Mamba, M.; Fasel, N.; Mahlaba, T.A.M.; Austin, J.D.; McCleery, R.A.; Monadjem, A. Influence of sugarcane plantations on the population dynamics and community structure of small mammals in a savanna-agricultural landscape. Glob. Ecol. Conserv. 2019, 82, 250–260. [CrossRef] 62. Mulungu, L.S.; Mahlaba, T.; Massawe, A.; Kennis, J.; Crauwels, D.; Eiseb, E.; Monadjem, A.; Makundi, R.; Katakweba, A.; Leirs, H.; et al. Dietary preferences of the multimammate mouse (Mastomys natalensis, Smith 1832) across different habitats and seasons in Tanzania and Swaziland. Wildl. Res. 2011, 38, 640–646. [CrossRef] 63. Taylor, P.J.; Downs, S.; Monadjem, A.; Eiseb, S.J.; Mulungu, L.S.; Massawe, A.W.; Mahlaba, T.A.; Kirsten, F.; Maltitz von, E.; Malebane, P.; et al. Experimental treatment-control studies of ecologically based rodent management in Africa: Balancing conservation and pest management. Wildl. Res. 2012, 39, 51–61. [CrossRef] 64. Püttker, T.; Barros, C.S.; Pinotti, B.T.; Bueno, A.A.; Pardini, R. Co-occurrence patterns of rodents at multiple spatial scales: Competitive release of generalists following habitat loss? J. Mammal. 2019, 100, 1229–1242. [CrossRef] 65. Rocha, C.R.; Ribeiro, R.; Marinho-Filho, J. Influence of temporal variation and seasonality on population dynamics of three sympatric rodents. Mamm. Biol. 2017, 84, 20–29. [CrossRef] 66. Plavsic, M.J. Seasonal dynamics of macrohabitat use by small mammals in the Okavango Delta, Boswana: Implications for landscape-level disturbance resilience. Afr. J. Ecol. 2015, 53, 44–53. [CrossRef] 67. Mikula, O.; Šumbera, R.; Aghová, T.; Mbau, J.S.; Katakweba, A.S.; Sabuni, C.A.; Bryja, J. Evolutionary history and species diversity of African pouched mice (Rodentia: Nesomyidae: Saccostomus). Zool. Scripta 2016, 45, 595–617. [CrossRef] 68. Bryja, J.; Šumbera, R.; Peterhans, J.C.K.; Aghová, T.; Bryjová, A.; Mikula, O.; Nicholas, V.; Denys, C.; Verheyen, E.K. Evolutionary history of the thicket rats (genus Grammomys) mirrors the evolution of African forests since the late Miocene. J. Biogeogr. 2017, 44, 182–194. [CrossRef] 69. Rusch, U.D.; Midgley, J.J.; Anderson, B. Seasonal fluctuations in rodent seed catching and consumption behavior in fynbos shrublands: Implications for fire management. S. Afr. J. Bot. 2014, 93, 217–221. [CrossRef] 70. McCain, C.M.; King, S.R.B.; Szewczyk, T.; Beck, J. Small mammal species richness is directly linked to regional productivity, but decoupled from food resources, abundance, or habitat complexity. J. Biogeogr. 2018, 45, 2533–2545. [CrossRef] 71. Makundi, R.H.; Massawe, A.W.; Mulungu, L.S. Breeding seasonality and population dynamics of three rodent species in the Magamba Forest Reserve, Western Usambara Mountains, north-eastern Tanzania. Afr. J. Ecol. 2006, 45, 17–21. [CrossRef] 72. Massawe, A.W.; Mulungu, L.S.; Makundi, R.H.; Dlamini, N.; Eiseb, S.; Kirsten, F.; Mahlaba, T.; Malebane, P.; von Maltitz, E.; Monadjem, A.; et al. Belmain. Spatial and temporal population dynamics of rodents in three geographically different regions: Implications for ecologically-based rodent management. Afr. Zool. 2011, 46, 393–405. [CrossRef] 73. Adams, A.; Yihune, M. Species composition, relative abundance and habitat association of rodents in Yekoche Forest, East Gojjam, Ethiopia. Int. J. Biodivers. Conserv. 2016, 8, 216–223. [CrossRef] 74. Larsen, A.L.; Homyack, J.A.; Bently-Wigley, T.; Miller, D.A.; Kalcounis-Rueppell, M.C. Effects of habitat modification on cotton rat population dynamics and rodent community structure. For. Ecol. Manag. 2016, 376, 238–246. [CrossRef] 75. Fleming, P.A.; Loveridge, J.P. Miombo woodland termite mounds: Resource islands for small vertebrates? J. Zool. 2003, 259, 161–168. [CrossRef] Diversity 2020, 12, 365 14 of 14

76. Mlyashimbi, E.C.M.; Marien, J.; Kimaro, D.N.; Tarimo, A.J.P.; Isabirye, M.; Makundi, R.H.; Massawe, A.W.; Mdangi, M.E.; Kifumba, D.; Nakiyemba, A.; et al. Relationships between seasonal changes in diet of Multimammate rat and its breeding patterns in sermi-arid areas in Tanzania. Cogent Food Agric. 2018, 4, 1507–1553. [CrossRef] 77. Martin, J.M.; Branch, L.C.; Rain, R.N.; Beyeler, S.C. Temporal instability of agricultural habitat reduces reproductive success of Barn owls (Tyto alba). Auk 2010, 127, 909–916. [CrossRef] 78. Madsen, T.; Ujvari, B.; Shine, R.; Buttemer, W.; Olsson, M. Size matters: Extraordinary rodent abundance on an Australian tropical ﬂood plain. Austral. Ecol. 2006, 31, 361–365. [CrossRef] 79. Damschen, E.I.; Brudvig, L.A.; Burt, M.A.; Fletcher, R.J.; Haddad, N.M.; Levey, D.J.; Orrock, J.L.; Resasco, J.; Tewksbury,J.J. Ongoing accumulation of plant diversity through habitat connectivity in an 18-year experiment. Science 2019, 365, 1478–1480. [CrossRef][PubMed] 80. Rosenzweig, M.L. Species Diversity in Space and Time; Cambridge University Press: Cambridge, UK, 1995. 81. MacArthur, R.H.; Wilson, E.O. The Theory of Island Biogeography; Princeton University Press: Princeton, NJ, USA, 2001; Volume 1. 82. Allan, J.R.; Possingham, H.P.; Atkinson, S.C.; Waldron, A.; Di Marco, M.; Adams, V.M.; Butchart, S.H.M.; Venter, O.; Maron, M.; Williams, B.A.; et al. Conservation attention necessary across at least 44% of Earth’s terrestrial area to safeguard biodiversity. bioRxiv 2019, 839977. [CrossRef] 83. Dinerstein, E.; Vynne, C.; Sala, E.; Joshi, A.R.; Fernando, S.; Lovejoy, T.E.; Mayorga, J.; Olson, D.; Asner, G.P.; Baillie, J.E.M. A global deal for nature: Guiding principles, milestones, and targets. Sci. Adv. 2019, 5, eaaw2869. [CrossRef][PubMed] 84. Snyman, S. The role of ecotourism employment in poverty reduction and community perceptions of conservation and tourism in Southern Africa. J. Sustain. Tour. 2012, 20, 395–416. [CrossRef]

© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).