Mammal Diversity at Artificial Saltlicks in Malaysia: A Targeted Use - Frontiers
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BRIEF RESEARCH REPORT
published: 16 November 2020
doi: 10.3389/fenvs.2020.556877
Mammal Diversity at Artificial
Saltlicks in Malaysia: A Targeted Use
Boyd K. Simpson 1,2* , Noraini Nasaruddin 3 , Carl Traeholt 1 and Shukor Md. Nor 2
1
Copenhagen Zoo, Copenhagen, Denmark, 2 Faculty of Science and Technology, National University of Malaysia, Bangi,
Malaysia, 3 Department of Wildlife and National Parks, Kuala Lumpur, Malaysia
Natural mineral licks are used by many species throughout the world but information
relating to the use of artificial saltlicks for wildlife conservation and management is scant.
The Department of Wildlife and National Parks in Peninsular Malaysia has established
more than 30 artificial saltlicks intended to enrich the habitat with additional mineral
resources for wildlife. We used automated camera traps to assess mammal diversity
and visitation rates at 14 artificial saltlicks across three wildlife reserves, and compared
these metrics to those from nearby (300 m) forest sites. Cameras were operational for
Edited by:
Tsitsi McPherson, an average of 65.3 trap nights (TN), providing 846 TN at artificial saltlicks and 916 TN in
State University of New York at forest areas. At artificial saltlicks we recorded 159.7 independent mammal encounters
Oneonta, United States
(100 TN−1 ), significantly higher (p < 0.0001) than from forest sites at 31.1 100 TN−1 .
Reviewed by:
Emiliano Mori,
Twenty-three species were recorded at artificial saltlicks while 19 species were detected
University of Siena, Italy from forest sites. Of the seven most frequent species to visit the artificial saltlicks, only
Attila D. Sándor,
wild pig (p = 0.012), Malayan tapir (p = 0.033), red muntjac (p = 0.008), and Malayan
University of Agricultural Sciences
and Veterinary Medicine porcupine (p = 0.007) showed significantly higher encounter rates over forest sites,
of Cluj-Napoca, Romania indicating a specific preference and targeted use of artificial saltlicks for these species.
Wanlop Chutipong,
King Mongkut’s University
Artificial saltlick sites successfully attracted a wide range of species, possibly because
of Technology Thonburi, Thailand they provided valuable resources that would otherwise be absent in the study area.
*Correspondence: Such areas may be beneficial in diversifying and enriching habitats, particularly where
Boyd K. Simpson
natural mineral licks have been lost or habitats necessitate restoration or rehabilitation.
boydsimpson@gmail.com
Keywords: mineral lick, camera trap, biodiversity, rehabilitation, mammal, natural lick, man-made saltlick,
Specialty section: conservation
This article was submitted to
Conservation and Restoration
Ecology, INTRODUCTION
a section of the journal
Frontiers in Environmental Science
Mineral licks are naturally occurring sites found throughout much of the world where the
Received: 29 April 2020 substrate and/or water contains numerous and various mineral elements. Commonly known as
Accepted: 16 October 2020
salt-licks, these areas are spatially limited, but essential to a variety of wildlife species. Herbivores,
Published: 16 November 2020
in particular, frequently engage in geophagy at these sites, consuming the soil or water from
Citation: these mineral-rich areas (Kreulen, 1985). While the exact reason for the deliberate ingestion of
Simpson BK, Nasaruddin N,
mineralized water or soil has yet to be fully ascertained, it is likely mineral licks serve multiple
Traeholt C and Nor SM (2020)
Mammal Diversity at Artificial Saltlicks
functions that may vary for different species, sexes, or at different temporal scales (Kreulen, 1985;
in Malaysia: A Targeted Use. Atwood and Weeks, 2002). Natural mineral licks provide essential nutrients that are lacking in the
Front. Environ. Sci. 8:556877. diet (Weeks and Kirkpatrick, 1976; Jones and Hanson, 1985; Heimer, 1988; Ceacero et al., 2009;
doi: 10.3389/fenvs.2020.556877 Flueck et al., 2012) or buffering compounds against dietary toxins, diarrhea, endoparasites or to
Frontiers in Environmental Science | www.frontiersin.org 1 November 2020 | Volume 8 | Article 556877Simpson et al. Mammal Diversity at Artificial Saltlicks
adjust gut pH (Mahaney et al., 1995; Knezevich, 1998; a Peninsular Malaysian context. However, predator diversity
Krishnamani and Mahaney, 2000; Ayotte et al., 2006). is moderate and species abundance for large mammals is
Mineral licks are considered a crucial micro-habitat and low (DWNP, 2001), indicating considerable limiting factors.
are key to supporting, especially, a high herbivore diversity Indigenous communities live within and around KWR and
(Montenegro, 2004). However, these areas must be protected if undertake subsistence hunting. Other nearby local communities
they are to remain an integral part of a functioning ecosystem are also thought to engage in activities that impact negatively on
(Matsubayashi et al., 2011). With natural forests continuing to mammal densities (DWNP, 2001).
decline (Potapov et al., 2017; Watson et al., 2018), the destruction The Sungai Dusun Wildlife Reserve (SDWR) in Selangor
or loss of natural mineral licks continues too. The continuing covers an area of 4,330 ha of secondary dipterocarp and peat-
expansion of road networks, logging areas, agricultural and urban swamp forest (DWNP, 2004), with an elevation of less than 250
land developments often obliterate these small important micro- m. At the Sungai Dusun conservation center (which undertakes
habitats. breeding and rehabilitation of the Malayan tapir), three artificial
Whereas natural mineral licks have received considerable saltlicks were assessed. All saltlicks were within 1km of the
scientific attention, the development and use of artificial saltlicks conservation center. Hunting pressure in SDWR is unknown.
for wildlife conservation and management has received very little The mammal diversity is believed to be lower than that of an
attention. Deer and moose are known to visit and consume equal size primary forest, although a comprehensive assessment
salt deployed for de-icing roads in north America (Fraser and at the SDWR has not been undertaken.
Thomas, 1982; Grosman et al., 2009), whilst also being attracted The Sungkai Wildlife Reserve (SWR) in Perak covers an area
to salt or mineral blocks placed by game hunters (DIY hunting, of 2,468 ha comprising mostly lowland secondary dipterocarp
2019). The use of artificial licks in the United States was also forest, with an elevation reaching 1,000 masl in the northeast
studied by burying commercially available deer mineral blocks where it adjoins the Titiwangsa mountain range. At the Sungkai
at ground level (Schultz, 1990; Schultz and Johnson, 1992). conservation center, three artificial saltlicks were assessed and
These ‘licks’ were very successful in attracting white-tailed deer all located within 2 km of the center. The conservation center
which licked and consumed the mineral blocks and granulated undertakes wildlife breeding programs for guar, sambar, and
mineral. Animal viewing hides can also be baited with salt various bird species. An assessment of local threats has not
to attract wildlife for photography and enhance the wildlife been undertaken, although a biodiversity inventory recorded a
viewing experience. Several viewing hides in Malaysia’s Taman moderate mammal diversity (DWNP, 2009) including the rare
Negara National Park have salt and mineral blocks added to dhole (Magintan et al., 2014).
attract wildlife. All Wildlife Reserves share borders with forested areas, local
In Peninsular Malaysia, the Department of Wildlife and communities and large agricultural developments of oil palm
National Parks (DWNP) has established more than 30 artificial and rubber. Elephants, guar, Sumatran rhino and probably tiger
saltlicks throughout various National Parks and protected areas. are no longer found in any of these Reserves. All artificial
These were specifically aimed at enriching the natural forest saltlicks were established at elevations from 40 to 140 masl. Most
habitat by providing additional mineral resources for wildlife. artificial saltlicks were situated further than 1 km apart, but we
In a preliminary investigation Magintan et al. (2015) found acknowledge four artificial saltlicks were situated within 500–700
20 mammal species visiting these artificial saltlicks over an 18 m of another artificial saltlick. As we were not estimating species
months period and concluded that these sites were successful density, but rather comparative visitation rates between forest
in attracting wildlife. In this study, we used camera traps to and saltlick sites, we feel results should still reflect preferences (or
quantify and assess species richness, diversity and patterns of use otherwise) for artificial saltlicks.
at artificial saltlicks in Malaysia, and compared these metrics to
wildlife in nearby forested areas. Artificial Saltlicks
The DWNP developed the artificial saltlicks used in this study
in 2011 and 2012 (Magintan et al., 2015) by digging a shallow
METHODS pit at an appropriate location in the forest. Typically, these pits
were 2–3 m long, 1.5–2 m wide, and 30–50 cm deep. Several
Study Site artificial lick sites were also formed within natural depressions in
Fifteen (15) artificial saltlicks were assessed from six sites across the forest. The size and depth of these artificial saltlicks could also
three wildlife reserves in Peninsular Malaysia (Figure 1). change over time due to erosion by animals and weather. An area
The Krau Wildlife Reserve (KWR) in Pahang comprises an of 1–3 m around the edge of the pit was cleared of vegetation to
area of 62,395 ha of lowland primary forest with the highest peak form a small clearing of approximately 20–40 m2 , including the
reaching 2,100 masl. Nine (9) artificial saltlicks were assessed saltlick itself. Approximately 1,000 kg of common, commercially
from four areas. At Perlok station (unmanned) one artificial available course-grain salt (NaCl) (purchased in 40 kg bags) was
saltlick. At Lompat station (unmanned) two artificial saltlicks. added to newly dug pits, together with 5–15 domestic-stock
At Jenderak guar conservation center, three artificial saltlicks. mineral blocks (Phos Rich 2% Rockie mineral blocks, Rockies
At Bukit Rengit operations center, three artificial saltlicks. All Tithebarn Ltd., United Kingdom). These commercial mineral
artificial saltlicks were situated within 1km of a ranger station blocks provide essential macro and micro-nutrients for domestic
or center. Mammal richness in KWR is particularly high within livestock, and were enriched in sodium, phosphorous, calcium,
Frontiers in Environmental Science | www.frontiersin.org 2 November 2020 | Volume 8 | Article 556877Simpson et al. Mammal Diversity at Artificial Saltlicks
FIGURE 1 | Location of the Sungkai, Sungai Dusun, and Krau wildlife reserves (WR) in Peninsular Malaysia.
magnesium, iron, cobalt, iodine, manganese, selenium and zinc. forest. Paired lick-forest cameras were placed at an average
The artificial saltlicks were typically replenished with additional distance of 315 m apart. Forest cameras were set on animal
salt (∼200–300 kg) and numerous mineral blocks 2–4 times a trails or at small clearings used by wildlife, while cameras at
year, although such regimes were not regimented. Rainfall would artificial saltlick sites were typically set 6–10 m from the focal
fill the saltlick pits and dissolve the salt, leaving small pools of artificial saltlick area. Camera-trapping started on 25 July 2017
salty water, from which animals could drink. and ended in mid-October 2017, with two cameras operational
As Malaysia is situated close to the equator, it has an ever- until December 2017.
wet tropical climate and rain falls throughout the year. The All cameras were set to record two pictures per trigger event
country typically receives rain 10–20 days each month, with a and were operational 24 h/day. The trigger event interval was set
mean monthly rainfall of 259 mm and an annual total exceeding at 2 min. Cameras were generally positioned at a height of 50–80
3,000 mm (for the 1991–2016 period) (World Bank, 2019). Such cm above the ground, and all had a small transparent plastic cover
consistent rainfall usually results in the artificial saltlick pits being attached to the top to help protect against rain. Cameras were
saturated with water, resulting in the formation of “wet” lick deployed to specifically detect medium-large sized terrestrial
pools. Many of the natural mineral licks in Malaysia are “wet” mammals, although other species were also photographed. All
licks (where animals drink the pooled or seeping mineral-rich locations were recorded with a 60CSx Garmin GPS.
water), as opposed to “dry” licks which are often excavated into
the side of a bank by animals consuming the mineral-rich soil. Data Analysis
The camera trapping software CameraSweet (see Sanderson and
Camera Trapping Harris, 2013) was used to organize and analyze camera trap
The wildlife use of artificial saltlicks and surrounding forested pictures. All mammals were identified to species where possible.
area was assessed using automated camera traps (Scoutguard SG With the exception of the conspicuous moonrat, Echinosorex
565FV and Bestguarder SG 990V, Guangdong, China). A total of gymnurus, pictures of smaller mammal species such as rats,
30 camera traps were deployed in pairs at each site. One camera mice, treeshrews or squirrels were grouped into “superfamily-
of each pair was set at each of the 15 artificial saltlick sites, type” groups due to difficulties in accurate identification.
and a further 15 cameras were placed within the surrounding The Lesser mousedeer (Tragulus kanchil), and the Greater
Frontiers in Environmental Science | www.frontiersin.org 3 November 2020 | Volume 8 | Article 556877Simpson et al. Mammal Diversity at Artificial Saltlicks
mousedeer (T. napu) were grouped together as mousedeer spp. Species richness was not significantly different for pooled
due to difficulties in distinguishing between the species in site mammal data (T-test, p = 0.076) between artificial
some photographs. People, domestic animals, “ghost” shots and lick sites (X̄= 7.2 ± 2.5 species, n = 14) and forest sites
animals that could not be identified due to poor image quality or (X̄ = 5.4 ± 2.7 species, n = 13). Sampling completeness at each
partial shots were excluded. site (artificial licks 77%; forest sites 95%) however, indicates
Pictures of the same species at the same site were considered that further camera trapping should result in the detection
to be independent after a period of 60 min (an Independent of more species.
Encounter, IE). The Encounter Rate (ER) for a species (or group) Shannon diversity indices, however, indicate significantly
was determined as Independent Encounters per 100 trap nights. higher mammal diversity at forest sites (H0 = 2.342 forest vs.
The persistence of a species at a camera site was calculated as 1.767 at lick sites, p < 0.0001). This translates to an effective
the time between the first and last picture of an independent number of species (ENS) of 10.4 mammal species at forest
encounter, and rounded to 1 min. A single photograph was sites while only 5.9 mammal species at artificial lick sites. The
recorded as a visit of less than 2 min. lower ENS of mammals was a result of the targeted use of
Comparisons between artificial saltlicks and forest sites were the artificial saltlicks by some species. This results in a highly
analyzed using pooled data from the two sampling groups with skewed species abundance visitation profile, and a lower species
a T-test for unequal variance. Paired T-tests were used for evenness index at artificial saltlick sites (Shannon E = 0.564),
species comparisons from paired cameras. Means (± SD) were when compared to forested sites (Shannon E = 0.796). Simpson
expressed for pooled data, while statistical significance levels were dominance indices (D) also support skewed visitation toward
set at p ≤ 0.05. Species diversities were assessed using Shannon artificial lick sites by mammals (D = 0.262 artificial licks vs.
diversity indices (H0 ), Shannon Evenness metric (E) and the D = 0.135 forest)—that is, some mammal species were targeting
Simpson dominance index (D) for pooled data from all cameras artificial saltlicks, resulting in a higher species dominance index
from saltlick and forest sites, and assessed with T-tests. Sampling and a lower diversity index; as diversity is the function of species
completeness and the equivalent number of species (or “true richness and evenness.
diversity”) for sites were based on Hill numbers described by
Chao et al. (2016). Species similarity was assessed with Jaccard’s Frequent Visitors
similarity coefficient. The majority of the 23 mammal species detected at the 14 artificial
lick sites and forest sites were seen infrequently (Table 1). Due
to such low encounter rates with large variations between sites,
RESULTS comparisons between the two sampling groups would not be
statistically meaningful. The most common mammals to visit
From the 30 cameras deployed (15 at artificial lick sites, 15 in the artificial saltlicks were wild pigs (45.7% of all lick visits),
forests), two were stolen from the Jenderak site, while another Malayan tapirs (13.9%), mousedeer spp. (13.7%), red muntjac
malfunctioned completely. The 27 operational cameras (14 at (9.2%), and Malayan porcupines (7.3%). These five species alone
licks and 13 at forest sites, i.e., 13 paired sites) where active for an represented 90% of all encounters at artificial saltlick sites. By
average of 65.3 trap nights (TN) per camera. Trap effort was not comparison the five most common species photographed in
equal across sites with 846 TN recorded at the artificial saltlicks, forest areas were wild pigs (28.3% of forest photographs), pig-
while 916 TN were recorded in the forest. tailed macaques (14.5%), mousedeer spp., (13.4%), red muntjac
More than 11,000 pictures were recorded in all, of which 6,431 (6.3%), and Malayan porcupine (6.3%), representing 69% of
were identified visitors to the camera site locations. From these, forest encounters.
1,775 independent encounters were made of various species. The Only seven species visiting the artificial saltlicks had encounter
vast majority of encounters were of medium and large-sized rates of ≥ 3.0 100 TN−1 , which we consider as “frequent”
mammals (93.1%), followed by birds (3.0%), small mammals visitors. Only four of these species showed significantly higher
(2.3%), people (1.0%), and reptiles (0.6%). mean encounter rates at the artificial saltlicks over forest sites,
when assessed with paired T-tests. The wild pig (p = 0.012),
Mammal Diversity Malayan tapir (p = 0.033), red muntjac (p = 0.008), and
Capture rates for all mammals were significantly higher (T-test, Malayan porcupine (p = 0.007) all had significantly higher visit
p < 0.0001) at artificial saltlick sites (159.7 ± 60.6 encounters rates at artificial saltlicks, indicating a specific preference and
100 TN−1 ) than from forest sites (31.1 ± 18.9 encounters 100 targeted use of artificial saltlicks over forest sites (Table 1).
TN−1 ), indicating a targeted use of the artificial saltlicks by some Mean encounter rates for mousedeer spp. (p = 0.253), sambar
(or all) mammal species. deer (p = 0.136) and pig-tailed macaque (p = 0.318), which
Overall, 29 mammal species (or mammal groups) were were also “frequent” visitors at the artificial saltlicks, were
recorded during the study; 23 species from artificial lick not significantly different from encounter rates at forest
sites, and 19 species from forest areas (Table 1). Thirteen sites (Figure 2).
species were common to both artificial lick and forest sites, If the four “close-proximity” artificial saltlicks were removed
resulting in a Jaccard similarity coefficient of 0.45 (or 45%). from analysis (see Study site), the results for “frequent” visitors
Ten species were only recorded at artificial lick sites while remained unchanged. The same seven species were identified
six species were only recorded at forest sites (Table 1). as “frequent” visitors with encounter rates of ≥ 3.0 100
Frontiers in Environmental Science | www.frontiersin.org 4 November 2020 | Volume 8 | Article 556877Simpson et al. Mammal Diversity at Artificial Saltlicks
TABLE 1 | Mammal species (or groups) detected visiting artificial saltlicks and forest sites with camera traps.
IUCN Sites Artificial Lick Forest
Common name Scientific name status IE ER IE ER
Species recorded at artificial saltlick and forest sites
Wild pig Sus scrofa LC DSK 651 77.0 76 8.3
Malayan tapir Tapirus indicus EN DK 198 23.4 2 0.2
Mousedeer spp. Tragulus spp. LC DSK 195 23.0 36 3.9
Southern red muntjac Muntiacus muntjac LC SK 131 15.5 17 1.9
Malayan porcupine Hystrix brachyura LC DSK 104 12.3 17 1.9
Pig-tailed macaque Macaca nemestrina VU DSK 38 4.5 39 4.3
Sambar deer Rusa unicolor VU SK 27 3.2 3 0.3
Short-tailed mongoose Herpestes brachyurus NT DK 21 2.5 3 0.3
Malay civet Viverra tangalunga LC DK 21 2.5 2 0.2
Long-tailed porcupine Trichys fasciculata LC DS 4 0.5 17 1.9
Squirrels – – DSK 2 0.2 11 1.2
Rats/mice – – DSK 1 0.1 12 1.3
Banded civet Hemigalus derbyanus NT K 1 0.1 4 0.4
Species recorded only at artificial saltlick sites
White-thighed langur Presbytis siamensis NT DSK 11 1.3 0 0.0
Long-tailed macaque Macaca fascicularis LC DK 8 0.9 0 0.0
Sun bear Helarctos malayanus VU K 2 0.2 0 0.0
Common palm civet Paradoxurus hermaphroditus LC D 2 0.2 0 0.0
Large Indian civet Viverra zibetha LC SK 2 0.2 0 0.0
Masked palm civet Paguma larvata LC K 1 0.1 0 0.0
Small-clawed otter Aonyx cinerea VU K 1 0.1 0 0.0
Marbled cat Pardofelis marmorata NT K 1 0.1 0 0.0
Golden cat Catopuma temminckii NT K 1 0.1 0 0.0
Leopard Panthera pardus VU D 1 0.1 0 0.0
Species recorded only at forest sites
Moonrat Echinosorex gymnurus LC S 0 0.0 11 1.2
Brush-tailed porcupine Atherurus macrourus LC DK 0 0.0 10 1.1
Tree shrews – – K 0 0.0 4 0.4
Banded linsang Prionodon linsang LC SK 0 0.0 3 0.3
Sunda pangolin Manis javanica CR S 0 0.0 1 0.1
Yellow throated marten Martes flavigula LC K 0 0.0 1 0.1
Total 1424 168.3 269 29.4
IE, independent encounter; ER, encounter rate (number of independent encounters 100TN−1 ); IUCN status: CR, critically endangered; EN, endangered; VU, vulnerable;
NT, near threatened; LC, least concern. Sites: wildlife reserves where species detected, D, Sungai Dusun; S, Sungkai; K, Krau.
TN−1 , with only the wild pig, Malayan tapir, red muntjac and Tapirs only spent about a quarter of their time (27%) on short
Malayan porcupine maintaining significantly higher visit rates at (< 2 min) visits to artificial lick sites, with an average site
artificial saltlick sites. persistence of 16.9 (± 18.3) min/visit. This was significantly
(p < 0.0001) longer than at forest sites (1 min). Tapirs would
Site Persistence spend considerable time drinking the mineralized water, and, at
The four “frequent” visitors showing significantly higher visit one deeper saltlick, swimming. Red muntjac spent an average of
rates at the artificial saltlicks (wild pig, Malayan tapir, red 14.1 (± 21.1) min at the artificial saltlicks, significantly longer
muntjac and Malayan porcupine) all varied in the time spent (p < 0.0001) than at forest sites (1.5 ± 2.2 min). The time
at the artificial saltlick sites. Wild pigs (with group sizes up spent at artificial saltlicks (8.4 ± 15.0 min) by the Malayan
to 23 individuals) were the most frequent visitors to artificial porcupine was not significantly longer (p = 0.219) than at forest
lick sites, but more than half of the time (55%) they were sites (4.3 ± 11.4 min). However, this was exclusively due to
simply passing by, or spending less than 2 min at the site (a a single forest visit represented by two photographs 49 min
single photograph only). Pigs spent an average of 7.4 (± 13.2) apart, which considerably increased average persistence time and
min at the artificial lick site, often wallowing at some sites, or standard deviation for forest cameras. Whether this was the
rooting in the surrounds. This was significantly longer (T-test, same individual remaining at the forest site or two different
p < 0.0001) than the 2.6 (± 5.2) min spent at forest cameras. individuals is unknown.
Frontiers in Environmental Science | www.frontiersin.org 5 November 2020 | Volume 8 | Article 556877Simpson et al. Mammal Diversity at Artificial Saltlicks
artificial saltlick site itself. Small patches of cleared forest such as
these may be beneficial in helping to diversify the forest habitat.
Further research will be beneficial for comparing species visiting
artificial saltlicks to those of forest clearings, wallows and natural
licks. The results may help further clarify the attractiveness of
artificial lick sites for some species.
The main users targeting these artificial sites showed typical
encounter rates of ∼10–70 visits per 100 trap nights. These high
visitation rates were comparable to frequent visitors utilizing
natural mineral licks in tropical forests. Bearded pigs from
Borneo were recorded at rates of 14–20 visits 100 TN−1
(Matsubayashi et al., 2007a; Matsuda et al., 2015), sambar deer
9–40 visits 100 TN−1 (Matsubayashi et al., 2007b; Matsuda et al.,
FIGURE 2 | Mean encounter rates for frequent species visiting artificial 2015), lesser mouse deer 8 visits 100TN−1 (Matsubayashi et al.,
saltlicks and forest sites. Frequent species were considered those with artificial 2007a), red muntjac 13 visits 100TN−1 (King et al., 2016) and
lick-site encounter rates of ≥ 3 visits 100TN−1 . Error bars are standard errors. lowland tapirs 55–98 visits 100TN−1 (Blake et al., 2012; Link
Encounter rates are independent pictures 100TN−1 . Star denotes significantly et al., 2012). Natural mineral licks from Peninsular Malaysia
different encounter rates (p ≤ 0.05) assessed with paired T-tests.
showed encounter rates (100 TN−1 ) of 6–47 for Malayan tapir,
3–25 for wild pig, 4–46 for red muntjac and 2–6 for Malayan
porcupine (Simpson unpublished data). Artificial saltlicks are
DISCUSSION therefore attracting a similar suite of species at rates similar to
those of natural mineral licks, and may be seen as an alternative
It is clear from this study that mammals were using the to natural licks, at least in terms of behavioral activities. How
artificial saltlicks, with 23 mammal species (groups) detected artificial saltlicks compare to natural mineral licks in terms of
over the approximate 2-month sampling period. This was slightly their chemical properties or their implied health benefits has
higher than the 19 species detected in nearby forest areas, yet to be ascertained, however, several studies have shown that
albeit with a somewhat different species composition. Sampling natural mineral licks provide a wide variety of macro and micro
completeness, however, indicates that both artificial lick and minerals and gut buffering properties beneficial to wildlife health
forest sites were yet to reach species saturation. Tobler et al. (Jones and Hanson, 1985; Kreulen, 1985; Mahaney et al., 1995;
(2005) suggests that trap effort is more important than trap Ayotte et al., 2006).
placement for recording a larger number of species, and thus Comparisons of visit rates for a particular species between
further trapping would no doubt result in more species being the different artificial saltlicks sites can be compounded
detected at both sites. by numerous sampling biases. Mean encounter rates were
Not all species detected at the artificial saltlicks were sometimes accompanied by large standard deviations. Not all
specifically targeting the area, with many species also found camera sites were subjected to the same disturbance levels,
in forest sites at similar encounter rates. As these small forest cover, structure, substrate or species densities, with the
artificial sites form an integral part of the larger forested effects of such factors being highlighted in studies on species
landscape, many species seen at the saltlicks will simply be distributions and modeling (Blom et al., 2005; Fahrig and
passing through another micro-habitat within their habitat or Rytwinski, 2009; Vanthomme et al., 2013; Whitworth et al.,
range. The effectiveness of artificial saltlicks to attract wildlife 2019). While some artificial saltlicks were located in dense
therefore cannot be evaluated by species richness alone, as forest, others were situated in proximity to built-up areas, which
indicated by Magintan et al. (2015), but through additional may then affect species encounter rates, especially for more
indicators which may assess comparative frequencies, persistence timid species. Hunting pressures and general human disturbance,
at site or activities undertaken. Such indicators may also be which were unknown for all areas, could have an effect on
affected by biotic, abiotic, behavioral or biological factors or be mean encounter rates, resulting in large standard deviations for
impacted at different temporal scales. White-tailed deer in the species-specific means. Underlying these factors are also species
United States, for example, were seen to utilize artificial licks densities and distributions, which are no doubt heterogeneous
to varying extents, depending on location, month and season across wildlife reserves. Schultz and Johnson (1992) also found
(Schultz and Johnson, 1992). large variations in artificial saltlick use by white-tailed deer, and
It is clear that some species were deliberately targeting suggest dietary needs may influence artificial saltlick use. It is
the artificial saltlicks. Wild pigs, tapirs, muntjac and Malayan possible that species like the sambar deer may actually target
porcupines all showed significantly higher visit rates to artificial artificial saltlicks under favorable conditions. Although not borne
saltlicks than to forest areas, and were targeting these sites to out in this study, sambar deer were the second most common
engage in geophagy, or wallowing as was the case for the wild pig. visitor to artificial saltlicks in an earlier study in Malaysia
Forest clearings such as these may also provide useful hunting, (Magintan et al., 2015).
basking, feeding or browsing areas, and thus prove attractive to In the Krau wildlife reserve, for example, sambar deer were
a suite of species seeking the more open terrestrial habitat of the recorded at both areas in the Jenderak and Lompat sites, yet not
Frontiers in Environmental Science | www.frontiersin.org 6 November 2020 | Volume 8 | Article 556877Simpson et al. Mammal Diversity at Artificial Saltlicks
at all around the more-disturbed Bukit Rengit site. Proximity DATA AVAILABILITY STATEMENT
to noise and other disturbance at Bukit Rengit may have
precluded the species from cameras in this area. Wild pigs spent The raw data supporting the conclusions of this article will be
considerable time wallowing at some of the artificial saltlicks made available by the authors, without undue reservation, to any
where deep mud was formed. At other lick sites, feeding (rooting qualified researcher.
in the soil) was a major activity. A small pond-type artificial
saltlick which attracted a large number of tapirs for drinking
and swimming, had few wild pig visits. It is also interesting ETHICS STATEMENT
to note that tapir was recorded in all areas except for the
six camera sites (3 lick and 3 forest) at the Sungkai wildlife Ethical review and approval was not required for the study.
reserve—and this may relate to tapir distribution, rather than The manuscript presents results of an observational study of
any association with artificial saltlicks. Magintan et al. (2014) forest and forest resources. Cameras were used to record forest
did however, record tapir in this Wildlife Reserve. The white activities, which included images of forest animals. Animals were
thighed langur is known to utilize natural mineral licks in the not captured, handled, restrained or disturbed. No animal or
Krau wildlife reserve (pers. obs., BS), but was only recorded animal products were collected, handled or sampled. Activities
drinking from three artificial saltlicks in this study. Whether this comply with the legal and ethical requirements of Department of
was due to the unsuitability of the other artificial saltlicks, or Wildlife and National Parks, Malaysia.
because artificial saltlick sites were unknown to langurs, or due
to other biological or behavioral aspects is unknown. Typically,
primate species utilize natural mineral licks with specific physical
or chemical characteristics, and incorporate anti-predator and AUTHOR CONTRIBUTIONS
ranging behaviors when descending to mineral lick sites (Link
BS and SN conceived and designed the research. BS and NN
et al., 2011; Matsubayashi et al., 2011; Ampeng et al., 2016).
conducted the fieldwork. BS conducted the data analysis and all
With natural forest estates declining due to increasing forestry
authors contributed to writing and editing the manuscript.
and agricultural practices (Potapov et al., 2017), natural mineral
licks will also come under increasing risk of annihilation.
Natural mineral licks are known to attract numerous wildlife
species that often engage in geophagy, or drink the mineralised FUNDING
water (Jones and Hanson, 1985). Ungulates seem particularly
attracted, although other herbivores (primates, sloths) and Fieldwork was undertaken with funding from Copenhagen Zoo’s
birds have also been recorded using natural mineral licks Southeast Asia Programme. Universiti Kebangsaan Malaysia
(Krishnamani and Mahaney, 2000; Brightsmith et al., 2008; provided funds for open access publication.
Mosquera et al., 2019). Such natural licks, which are often
small, non-descript and spatially limited, are considered crucial
micro-habitats (Montenegro, 2004). They are key to supporting ACKNOWLEDGMENTS
healthy biodiversities and are integral to functioning ecosystems
(Matsubayashi et al., 2011). The effect on ecological functions This work was carried out under a Memorandum of
from the loss of natural mineral licks is unknown, but may impact Understanding between Copenhagen Zoo, Denmark and the
on certain species’ population distribution, health or vigor. Department of Wildlife and National Parks (DWNP), Malaysia.
Although the effectiveness of artificial saltlicks to supplement All activities comply with the legal and ethical requirements of
the nutrition of wild species on native ranges has yet to be DWNP. We thank the Director General of DWNP, YBhg. Dato’
fully ascertained (Schultz and Johnson, 1992), artificial saltlicks Abdul Kadir bin Abu Hashim and Dr. Pazil bin Abdul Patah,
may deliver an avenue to rehabilitate degraded landscapes by DWNP Director of Biodiversity Conservation for facilitating
providing a range of species access to essential dietary needs. this work. We thank Adrian Jawing for assisting with fieldwork
Developing artificial saltlicks to support wildlife populations and also DWNP staff at Bukit Rengit, Jenderak, Kuala Lompat,
should be considered where natural sites have been degraded or Perlok, Sungai Dusun and Sungkai for their assistance. Three
where areas will benefit from additional mineral resources and reviewers and provided comments that improved earlier drafts
diversified micro-habitats. of the manuscript.
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visitation by lowland tapir (Tapirus terrestris) and lowland paca (Cuniculus Conflict of Interest: The authors declare that the research was conducted in the
paca) in a western Amazonian rainforest in Ecuador. Mastozool. Neotropical absence of any commercial or financial relationships that could be construed as a
19, 63–70. potential conflict of interest.
Link, A., Galvis, N., Fleming, E., and Di Fiore, A. (2011). Patterns of mineral
lick visitation by spider monkeys and howler monkeys in Amazonia: are licks Copyright © 2020 Simpson, Nasaruddin, Traeholt and Nor. This is an open-access
perceived as risky areas? Am. J. Primatol. 73, 386–396. doi: 10.1002/ajp. article distributed under the terms of the Creative Commons Attribution License
20910 (CC BY). The use, distribution or reproduction in other forums is permitted, provided
Magintan, D., Ahmad, M. A., Ismail, A., and Rasdi, I. (2014). Observation of dhole the original author(s) and the copyright owner(s) are credited and that the original
(Cuon alpinus) at Sungkai wildlife reserve, Perak, Malaysia. J. Wildlife Parks 29, publication in this journal is cited, in accordance with accepted academic practice. No
69–72. use, distribution or reproduction is permitted which does not comply with these terms.
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