Persistence of mammals in a selectively logged forest in Malaysian Borneo

Accepted Manuscript Title: Persistence of mammals in a selectively logged forest in Malaysian Borneo Author: Alys Granados Kyle Crowther Jedediah F. Brodie Henry Bernard PII: DOI: Reference:

S1616-5047(16)30015-5 http://dx.doi.org/doi:10.1016/j.mambio.2016.02.011 MAMBIO 40814

To appear in: Received date: Revised date: Accepted date:

4-7-2015 26-2-2016 26-2-2016

Please cite this article as: Granados, Alys, Crowther, Kyle, Brodie, Jedediah F., Bernard, Henry, Persistence of mammals in a selectively logged forest in Malaysian Borneo.Mammalian Biology http://dx.doi.org/10.1016/j.mambio.2016.02.011 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Persistence of mammals in a selectively logged forest in Malaysian Borneo Alys Granados1*, Kyle Crowther1, Jedediah F. Brodie 1,2, and Henry Bernard 3 1

Department of Zoology and Biodiversity Research Centre, University of British Columbia,

Vancouver, BC, Canada 2

Department of Botany, University of British Columbia, Vancouver, BC, Canada

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Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Jalan UMS, 88400

Kota Kinabalu, Sabah, Malaysia

*Corresponding author: [email protected] Present address: University of British Columbia, #4200-6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada

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Abstract Many tropical mammals with important functional roles in forest ecosystems are threatened with extinction, yet how they respond to increasingly prevalent habitat disturbance, such as selective logging, is not well understood. We deployed 43 motion-triggered camera traps in 2013 and 2014 in unlogged forest and in a forest logged three decades previously in Malaysian Borneo. We used camera trap photographs to assess whether selective logging influenced the local abundance of medium to large-bodied ground-dwelling mammals. We focused our study on six locally common species: sambar deer, (Rusa unicolor), yellow muntjac (Muntiacus atherodes), chevrotains (Tragulus spp.), banded civet (Hemigalus derbyanus), Malay civet (Viverra tangalunga), and pig-tailed macaque (Macaca nemestrina). Occupancy models were used to estimate local abundance. None of the mammals in our study exhibited decreased abundance in logged forest, although yellow muntjac and pig-tailed macaque were associated with canopy height. Contiguous forest connects these two areas, allowing animal movement between them, potentially explaining the lack of responses. The elapsed time since logging may have further influenced our findings. The effects of logging on mammal local abundance may no longer detectable after 30 years. Overall, our results demonstrate the importance of regenerating forest as habitat for medium- to large-sized mammal species.

Keywords: Borneo; camera traps; logging; mammals; occupancy

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Introduction Quantifying how species respond to human-induced habitat disturbance is integral to wildlife conservation efforts and can provide valuable insight into the consequences of human activity for forest communities. Selective logging (the targeted removal of trees of particular taxa or size) is the principal method of timber extraction in the tropics and a major cause of habitat degradation that alters forest structure (e.g. by reducing sapling abundance, reducing canopy height, and reducing seed production, as well as changing microclimate conditions) (Drigo et al., 2009; Edwards et al., 2014; Hall et al., 2003; Johns, 1988; Okuda et al., 2003; Simard and Fryxell, 2003; Wilcove et al., 2013). Though it is known that many tropical species can be quite vulnerable to human-induced habitat disturbances (Edwards et al., 2014), our understanding of how logging impacts tropical forest communities is complicated by the complex webs of species inteactions in those systems (Chazdon et al., 2009; Foody and Cutler, 2003). Animals may be affected by habitat disturbance decades after logging has stopped (Chapman et al., 2000). However, species can also adapt to the conditions of secondary forest, and be unaffected, or more abundant than in intact forest (Berry et al., 2008; Clark et al., 2009; Meijaard and Sheil, 2008). Generalizing our understanding of which tropical animals are impacted by selective logging is critical given that many are threatened with extinction by various forms of anthropogenic activity including hunting (Corlett, 2007) and habitat degradation (Sodhi et al., 2004). Further, impacts on particular species can indirectly affect additional taxa via species interactions. For example, terrestrial mammals can act as important seed dispersers (Brodie et al., 2009) and seed predators (Markl et al., 2012). Variation in body size affects their ability to manipulate and consume large fruits or break through hard seed coats, with consequences for seed dispersal (Corlett, 1998).

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The lowland dipterocarp forests of Sabah, Malaysian Borneo are home to several vertebrate species that interact with trees as herbivores, seed dispersers, and seed predators, yet many of these animals are threatened by habitat degradation and the loss of primary forest habitat. As one of the few remaining areas of primary forest left in Sabah, the Danum Valley Conservation Area (DVCA) provides important habitat for many species. Historically, Borneo was predominantly covered by tropical rainforest that supported exceptionally high biodiversity (Ashton, 2010) but according to recent estimates, just 28% of Borneo remains as intact forest (Bryan et al., 2013). Within Sabah, 25% of the landscape is intact forest yet only 8% of that area occurs within protected areas (Bryan et al., 2013). Selective logging for adult dipterocarp trees is the most prevalent form of timber extraction in Borneo and has played a major role in the loss of primary forest habitat (Bryan et al., 2013). Repeated cycles of logging are common: 86% of logged forests in Borneo have been logged at least twice, impeding the forest regeneration process (Bryan et al., 2013). In this study, we used motion-triggered camera traps to assess the impact of past selective logging on the occupancy of several ground-dwelling, medium- to large-bodied mammals in Malaysian Borneo. Our focal species occur in different feeding guilds, representing omnivores, herbivores, and frugivores, providing insight into how differences in foraging ecology may affect responses to habitat disturbance.

Methods Study Sites We collected data in the Danum Valley Conservation Area (DVCA) (N5.10189°/ E117.688°) and the Sabah Biodiversity Experiment (SBE) (N5.16727°/E117.564°) in eastern

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Sabah, Malaysian Borneo (Fig. 1). This region is part of the Yayasan Sabah Forest Management Area (YFSMA) and consists of mixed lowland dipterocarp forest, characterized by dominance of trees in the family Dipterocarpaceae. The DVCA (438 km2) is a Class I ("Totally protected") reserve and is protected from resource extraction. It represents the largest expanse of intact primary lowland dipterocarp forest in Sabah and has remained relatively undisturbed by human activity, with no accounts of logging or agriculture (Hazebroek et al., 2012). The Malua Forest Reserve (MFR) (335 km2) is located 25 km north of the DVCA and was logged for dipterocarps greater than 60 cm dbh in the 1980s with the use of tractors and high lead cables (Berry et al., 2010; Hector et al., 2011). The SBE is found within that area that was previously logged. In 2007, parts of the MFR were re-logged, although the SBE itself was not (Hector et al., 2011). This area (SBE and MFR) is classified as a Class II reserve and commercial timber extraction is permitted. Much remains unclear about how mammals in Southeast Asia may be affected by past logging, and even locally common species may show different responses. In our study region, locally common species include chevrotains (Tragulus napu and Tragulus javanicus.), yellow muntjac (Muntiacus atherodes), and Malay civet (Viverra tangalunga). Species of conservation concern occur there as well, including sambar deer (Rusa unicolor, Vulnerable), pig-tailed macaque (Macaca nemestrina, Vulnerable), and banded civet (Hemigalus derbyanus, Near Threatened), all of which are exhibiting decreasing population trends (IUCN, 2015).

Data collection We used motion-triggered Reconyx HC500 camera traps to monitor animal presence at our field sites. In 2013, we established 22 camera trap stations at DVCA and 20 in SBE. We used 5 

the same camera trap locations in 2014. One of our cameras in the DVCA was not used in 2014, but a new site was added elsewhere in DVCA so the number of active cameras in each year remained the same. At our unlogged forest site (DVCA), camera traps were set up near the Field Centre on a 1 × 1 km grid created using Garmin Basecamp (Tobler et al., 2008). We then navigated to UTM coordinates for potential camera trap stations determined using Garmin Basecamp (Tobler et al., 2008). Upon arriving within 100 m of each potential location, we searched for suitable locations for camera traps, taking into account the terrain and ease of access, as camera trap stations were to be revisited every few weeks for a concurrent study on animal occupancy and fruiting phenology. Each location was at least ~1 km apart (Fig. 1). At our logged forest site (all cameras in the SBE and around the MFR), we placed nine cameras within the SBE near the SBE Research Centre. The remaining eleven cameras were at least 100 m from forestry roads around the MFR. Camera trap stations in “logged forest” therefore refer to cameras in either the SBE or those around the MFR. Directions from the road were determined by random compass bearings and stations spanned an elevation gradient of 200 m. As in the unlogged forest, camera trap stations in the logged forest were at least ~1 km apart. Cameras remained in place from May to September 2013 in the DVCA and from June to August 2013 in SBE and MFR. In 2014, camera traps were set up in the same locations as 2013 and were active from May to September. In 2013, camera traps were deployed at approximately 60 cm tree height but were moved down to 30 cm after three weeks and remained at this height for the rest of the 2013 field season. Cameras placed higher on the tree (e.g. 60 cm) may have reduced the likelihood of detecting smaller species, but likely did not affect our ability to detect the medium- to large-sized mammals that were our focus. In 2014, cameras were deployed at 30 cm tree height and

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remained at this height throughout the field season. At each camera trap station, we visually estimated canopy height in meters to determine whether this affected the prevalence of mammals. Camera traps were set to ‘high’ trigger sensitivity and programmed to take three photographs in rapid-fire succession upon triggering, with a 30 second delay before a subsequent trigger. Camera traps were active 24 hours/day. We did not use baits or lures.

Data Analysis Photos from camera traps were date- and time-stamped, allowing us to quantify animal presence at each camera station for sambar deer, yellow muntjac, chevrotains, banded civet, Malay civet, and pig-tailed macaque. Detection data were assembled into a matrix with an integer of 0 or 1, representing animal presence (1) or absence (0) at each camera station. We used these data in site occupancy-models to compare species occupancy, which can be used as a metric of local abundance, between a previously logged forest and intact, primary forest. We estimated whether canopy height (m) influenced these occupancy estimates, while also incorporating detectability (MacKenzie and Nichols, 2004; MacKenzie et al., 2002). Specifically, we performed our analyses using Royle-Nichols site occupancy models that estimate detectability, r, and local abundance, λ (Royle and Nichols, 2003). This modelling approach takes into account that our ability to detect species at camera stations is influenced by the abundance of those species at camera stations (Royle and Nichols, 2003). We pooled our camera trap data from both years, treating this larger sample as a single season. The Royle-Nichols models operate under the assumption of closure (Royle and Nichols, 2003) but we assumed that occupancy did not change between our sampling periods. We used day as the temporal unit for sampling and tested whether the number of hours that camera traps 7 

were active each day as well as forest type (logged vs. unlogged forest) affected detectability for all species. We examined twelve different occupancy models representing all possible combinations of two occupancy covariates and two detectability covariates. Continuous covariates (camera hours and canopy height) were standardized to have a mean = 0 and a variance = 1 and “forest type” was our categorical variable with two levels (logged and unlogged forest). Occupancy analyses were done using the occuRN function in the R “Unmarked” package (Royle and Nichols, 2003). We used model selection and model averaging to obtain estimates of r and λ in each habitat. The best models were defined as those with the highest AIC (Akaike Information Criterion) weight.

Results Our cameras were active for 3709 camera trap days in the unlogged forest and 2886 camera trap days in the logged forest. During this time, we recorded 26 medium- to large-bodied mammal species but focused our analysis on six species that had more than 20 detections each: sambar, yellow muntjac, chevrotains (data pooled for greater chevrotain, Tragulus napu and lesser chevrotain, T. javanicus due to difficulty in distinguishing between species), banded civet, Malay civet, and pig-tailed macaque (Table 1). Species exhibited different responses to logging. However, local abundance did not significantly differ between logged and unlogged forest for any species (Table 2, Fig. 2). Canopy height ranged from 10 to 30 m at camera traps in the unlogged forest (mean = 18.6 m, SD = 3.7) and 13 to 25 m in the logged forest (mean = 17.5 m, SD = 3.3). Canopy height did not affect the local abundance of most species, except for pig-tailed macaques and yellow muntjac, which were positively associated with canopy height (Table 2). The number of hours that camera traps were

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active did not significantly influence detectability for any of the species. We included forest as a detectability covariate to determine whether differences in forest structure influenced our ability to detect species, which could influence occupancy estimates (Royle and Nichols, 2003). Detectability was associated with forest type for banded civets and sambar, whereby individuals were more likely to be detected in unlogged forest (Table 2).

Discussion Logging alters forest structure and resource availability for mammals (Johns, 1988), which has been associated with changes in abundance for several species (Bicknell and Peres, 2010; Chapman et al., 2000; Heydon, 1994; Sodhi et al., 2010). However, the mammals in our study did not show significant differences in local abundance between unlogged forest and a forest selectively logged 30 years prior. Southeast Asian ungulates may show density reductions after logging (Davies et al., 2001; Heydon and Bulloh, 1997), but we found ungulate abundances to be similar in our study sites. Conclusions from previous research on responses of muntjac to logging are mixed: Johns (1997) found muntjac in peninsular Malaysia to be more common in logged forest, whereas Heydon (1994) found muntjac density to be similar between forests logged 2 to 12 years previously and unlogged areas. Brodie et al. (2015) found that muntjac were less abundant in forest logged in the 1990s. Yellow muntjac consume fruit and browse; we found their local abundance to be only slightly positively associated with canopy height. This may be indicative of the importance of browse in their diet, consistent with previous work by Heydon (1994) where both species of muntjac (M. atherodes and M. muntiacus) were associated with increased canopy height. 9 

Sambar deer showed no significant response to logging, as in Davies (2001), whereas elsewhere in Borneo, sambar were more abundant in logged forest (Brodie et al., 2015; Heydon, 1994), particularly in forests logged >10 years previously (Brodie et al., 2014). Together, these studies illustrate the ability of sambar to persist in disturbed habitat. The creation of forest gaps caused by the removal of adult trees for logging promotes fast growing pioneer species. This provides an abundant food source for ungulates whose primary food source is understory foliage, as is the case among sambar, who can therefore take advantage of the secondary growth gaps created by logging (Kuijper et al., 2009). Other characteristics associated with regenerating forest may be beneficial for chevrotains, possibly explaining their use of disturbed habitat. Chevrotains were previously found to be relatively common in recently logged forest (Johns, 1997). We found chevrotian abundances to be similar between intact and logged forest, consistent with findings by Brodie et al. (2015) but contrary to those of Heydon and Bulloh (1997) who found that densities were reduced in primary forest. Chevrotains are frugivorous, heavily relying on fallen fruit for food, but their similar use of both forest types suggests they might exploit browse or the fruit from pioneer tree species in regenerating forest to a greater degree (Meijaard and Sheil, 2008). It may also be that the thick understory vegetation typical of secondary growth forests provides refuge, as suggested by Nummelin (1990), for red and blue duikers. Though many tropical forest vertebrates consume fruit to some degree (Gautier-Hion et al., 1985), the ability to consume non-plant food resources may explain the use of logged forest in civets and pig-tailed macaques. Our results for Malay and banded civets were contrary to previous findings suggesting that civets are more abundant in unlogged forest (Brodie et al., 2015; Colón, 2002). Heydon and Bulloh (1996) found that both Malay and banded civets were

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more negatively affected by logging than other civet species. Similarly, elsewhere in Borneo, Malay civets were not detected in camera trap surveys of logged forest (Brodie and Giordano, 2010). These trends may be attributed to the importance of fruit in the civet diet, as fruit production can decline after logging (Heydon, 1994). However, findings by Brodie et al. (2014) were consistent with our own, where banded civets showed no difference in local abundance between logged and unlogged habitat, suggesting that fruit availability did not limit civet persistence in logged habitat. Malay and banded civets both consume a large proportion of invertebrates and small vertebrates in their diet, which might instead explain their similar occurrence between disturbed and undisturbed habitat. This was especially true among Malay civets, where beetles, crabs, millipedes, and scorpions dominated their diet (Colón and Sugau, 2012). Like civets, pig-tailed macaques are omnivorous (Payne and Francis, 2007) and occurred at similar local abundances in the logged and unlogged forest. This is similar to findings in Sabah and Sarawak (Brodie et al., 2014) and elsewhere in Southeast Asia (Plumptre and Johns, 2001). Dipterocarps are targeted for removal in selective logging, but macaques are generalists and dipterocarp fruits are typically not an important part of their diet, which could explain their similar abundance between our study areas (Plumptre and Johns, 2001). Our findings differed from other studies investigating how taxa are affected by logging. This emphasizes that we cannot generalize how species respond to logging and that other factors should be considered when trying to assess how logging affects mammals, such as species’ foraging ecology. We found no difference in the local abundance of the mammals in our study between the unlogged and logged forest. However, this may be attributed to the elapsed time since our study site was logged (~30 years) and any immediate impacts of logging on local 11 

abundance may no longer detectable. Tree species composition in logged forests in Kalimantan, Indonesia, resembled that of nearby intact forest less than a decade after logging (Cannon et al., 1998), and assembalages of locally common mammal species in logged areas may resemble those of intact forest within several years (Johns, 1992; Wells et al., 2007). The difficulty in access of both our study sites may have also played a role in the patterns we observed: aside from being relatively remote, road access points into the region have guarded gates. With limited access and a halt to logging practices, anthropogenic pressures in this logged forest may have lessened over time, suggesting that forest conditions became more similar between sites (Hall et al., 2003). The lack of significant differences in mammal abundance between our logged and unlogged forest may further be attributed to the proximity of the SBE to the DVCA. The SBE lies adjacent to DVCA at its southern range, facilitating a direct access point for species to move from the primary forest to the logged forest, and vice versa. This was the case in Gabon, where distance to unlogged forest was a primary factor determining how mammals were affected by logging (Clark et al., 2009). Activities associated with logging, such as the clearing of forest to create logging roads, often facilitate hunting in logged areas (Wilkie et al., 2000). Indeed, hunting is viewed as a more serious threat to wildlife compared to logging (Brodie et al., 2015), yet it can be difficult to separate the impacts of logging and hunting on wildlife [but see (Poulsen and Clark, 2011)]. The reduced threat of poaching in our study area allowed us to quantify the impacts of selective logging on local mammal abundances in isolation from hunting. Our findings show that when left to regenerate, logged forests can provide valuable habitat that is used by vulnerable species. As tropical forests continue to be cleared, secondary forests are becoming more important in forest conservation (Chazdon et al., 2009). This is particularly true in Sabah, where the majority

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of forests have already been logged, so conservation efforts for many forest fauna will inevitably depend on previously logged sites. The use of logged forest by multiple medium- and largebodied mammal species and the limited effect of logging on occupancy implies that these forests are of relevant conservation value, and management practices should accommodate their persistence. Additional research into the use of logged forests by tropical mammals, particularly in forests varying in degree of logging intensity, would assist in identifying the forest conditions under which various species can best survive.

Acknowledgments We thank Yayasan Sabah, the Sabah Biodiversity Council (SaBC), and the Danum Valley Management Committee (DVMC) for permission to collect data. We are especially grateful for assistance at DVFC and SBE from G. Reynolds, A. Karolus, P. Ulok, A. Karolus, U. Jami, M. Bernadus, R. Murus, M. Markus, and E. Lee. We thank our all project volunteers, particularly A. Sorokin and T. Ferrel. This study was part of Southeast Asian Rainforest Research Programme (SEARRP) and was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) post-graduate doctoral award (PGS-D) to A. Granados, an NSERC USRA fellowship to K. Crowther, an NSERC Discovery Grant to J. Brodie, and the Canadian Foundation for Innovation.

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Figure captions

Fig. 1. Map of Sabah, Malaysian Borneo, showing the location of our study sites and our camera trap array in unlogged [Danum Valley Conservation Area (DVCA)] and logged [Sabah Biodiversity Experiment (SBE)] forest.

Fig. 2. Estimates of local abundance, λ, for mammal species at camera trap stations in unlogged (Danum Valley Conservation Area) and logged (Sabah Biodiversity Experiment) forest in Sabah, Malaysian Borneo. None of the species showed significant differences in local abundance between logged and unlogged forest. Standard error bars are shown.

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Fig 1

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Fig 2

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Tables Table 1. Number of detections by camera traps and conservation status (as defined by the World Conservation Union, IUCN) of mammal species in unlogged forest (Danum Valley Conservation Area) and in a forest logged 30 years previously (Sabah Biodiversity Experiment) in Sabah, Malaysian Borneo. Species

Common name

IUCN Status Number of stations with ൒1 detection

Mean (SE) number of detections per station

Rusa unicolor

Sambar

VUa

40

3.46 (0.51)

Muntiacus atherodes

Yellow Muntjac

LCb

39

7.07 (1.16)

Tragulus spp.

Chevrotains

LCc, DDd

41

15.17 (2.18)

Hemigalus derbyanus

Banded civet

NTe

27

2.07 (0.39)

Viverra tangalunga

Malay civet

LCf

25

1.74 (0.33)

Macaca nemestrina

Pig-tailed macaque

VUg

38

3.58 (2.04)

a

Timmins et al., (2015). Timmins et al., (2008). c Timmins and Duckworth (2015). d Duckworth et al., (2015). e Ross et al., (2015). f Azlan et al., (2008). g Richardson et al., (2008). b

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Table 2. Mean model coefficient estimates for site covariates from occupancy model selection results for six locally common species in Sabah, Malaysian Borneo. Estimated 95% confidence intervals (CI) that overlap zero indicate which model coefficients significantly affected local species abundances at camera trap stations. Coefficients are forest type (unlogged or logged) and estimated canopy height (ch) in meters at each camera trap station. Detectability coefficient estimates are also presented for forest type [forest (det)] and camera hours (camhours). Species

Model coefficient

Mean estimate of model coefficient

Lower CI

High CI

Sambar

canopy height (ch) forest forest*ch forest (det) camhours

0.04 0.14 -0.02 0.11 0.00

-0.04 -0.05 -0.06 -0.02 -0.03

0.13 0.32 0.01 0.24 0.01

Yellow muntjac

canopy height forest forest*ch forest (det) camhours

0.17 -0.02 0.00 -0.01 0.01

0.00 -0.16 -0.02 -0.04 -0.01

0.35 0.12 0.02 0.02 0.03

Chevrotains

canopy height forest forest*ch forest(det) camhours

-0.04 -0.01 0.00 -0.05 -0.05

-0.13 -0.10 -0.01 -0.12 -0.01

0.04 0.09 0.02 0.03 0.02

Banded civet

canopy height forest forest*ch forest (det) camhours

-0.01 0.12 -0.00 0.32 0.00

-0.09 -0.04 -0.02 0.02 -0.03

0.06 0.27 0.01 0.64 0.01

Malay civet

canopy height forest forest*ch

0.05 0.25 -0.04

-0.08 -0.10 -0.10

0.18 0.60 0.03

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forest (det) camhours Pig-tailed macaque

canopy height forest forest*ch forest (det) camhours

0.03 0.00

-0.07 -0.03

0.12 0.03

0.17 -0.02 0.01 -0.01 0.01

0.00 -0.16 -0.03 -0.04 -0.01

0.34 0.11 0.03 0.02 0.03

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