Next Article in Journal
Native Carnivore Diversity and Relative Abundance in Landscapes of the Coast Range in Central Chile: Insights for Conservation Decision-Making
Previous Article in Journal
Land Use Change and the Structural Diversity of Affem Boussou Community Forest in the Tchamba 1 Commune (Tchamba Prefecture, Togo)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Conservation
Volume 3
Issue 3
10.3390/conservation3030025
conservation-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Leaping Forward or Crawling Backward? Efforts and Biases in Amphibian and Reptile Research on a Megadiverse Faunal Region in the Philippines

by
Sumaira S. Abdullah
1,2,
Kier Celestial Dela Cruz
1,2,
Lothy F. Casim
3,
Angelo Rellama Agduma
1,2,4,5 and
Krizler Cejuela Tanalgo
1,2,*
1
Ecology and Conservation Research Laboratory (Eco/Con Lab), Department of Biological Sciences, College of Science and Mathematics, University of Southern Mindanao, Kabacan 9407, Philippines
2
Mindanao Open Biodiversity Information (MOBIOS+) Project, Ecology and Conservation Research Laboratory (Eco/Con Lab), Department of Biological Sciences, College of Science and Mathematics, University of Southern Mindanao, Kabacan 9407, Philippines
3
Molecular Parasitology Research Laboratory, Department of Biological Sciences, College of Science and Mathematics, University of Southern Mindanao, Kabacan 9407, Philippines
4
State Key Laboratory for Conservation and Utilization of Subtropical Agrobioresources, Guangxi University, Nanning 530004, China
5
Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning 530004, China
*
Author to whom correspondence should be addressed.
Conservation 2023, 3(3), 363-378; https://doi.org/10.3390/conservation3030025
Submission received: 6 June 2023 / Revised: 10 July 2023 / Accepted: 14 July 2023 / Published: 18 July 2023
Browse Figures
Versions Notes

Abstract

:
Research efforts to protect Philippine biodiversity have increased significantly. However, there is an imbalance in the distribution of published studies, with specific territories receiving more attention than others. Mindanao, a southern Philippine group of islands, is known for its high levels of endemism for amphibians and reptiles. Despite this, research on these groups remains scattered. To address this gap, we conducted a literature review focusing on amphibians and reptiles in the Mindanao faunal region. We found an increasing effort towards herpetofauna over the two decades, yet there is a clear bias in the effort towards amphibians compared to reptiles. Furthermore, we found that amphibians have a significantly higher species threat index than reptiles and all other vertebrate groups, regardless of species endemism and conservation status. Yet, threatened herpetofauna species and those facing greater threats are poorly studied in general. Understanding the factors driving research biases in Mindanao and the Philippines is essential to allow us to redirect research efforts to the most needed areas, particularly understudied and neglected taxa in Mindanao. This is especially urgent in the face of a changing climate, where diverse herpetofauna communities are at an increased risk of extinction. Consequently, by bridging these gaps in biodiversity information, we can effectively contribute to the conservation and understanding of biodiversity in the region.

1. Introduction

Human societies are widely dependent on healthy ecosystems and biodiversity; yet, numerous species and populations are declining as a result of increasing human pressures [1,2]. The current estimate shows that the pace of species extinction could be up to a thousand times higher than in the pre-industrialized period [3]. Among tetrapods, amphibians and reptiles are particularly susceptible to environmental changes due to their traits that are sensitive to rapidly changing ecological conditions, such as increased temperature and changes in precipitation [4,5,6]. Land use changes, disease, and alien species have negatively affected amphibian and reptile populations for many years [7]. Additionally, direct anthropogenic activities, including hunting, trade, and pollution, negatively impact the ability of populations to recover from declines [5]. The extreme sensitivity of amphibians to environmental changes makes them ideal bioindicators of the health of their environment and would help indicate conservation prioritization [6,7].
The Philippine archipelago, consisting of more than 7000 islands, supports high herpetofaunal biodiversity [8]. This high species diversity makes the country one of the main hotspots in southeast Asia for herpetofauna biodiversity [4,9]. However, many species and habitats in the Philippines are threatened, mainly by the growing human population and deforestation in lowland areas [10,11]. Therefore, identifying species and habitats at a higher risk of loss and extinction is crucial to prioritize conservation efforts and reduce further negative impacts on biodiversity [12,13,14]. One of the approaches to identifying conservation priorities is to examine the proportion of threatened and endemic species, assess the extent of threats they face, evaluate ongoing conservation efforts directed towards these species, and analyze how threats interact with species traits [15]. Unfortunately, valuable information for comprehensive synthesis remains scattered in many regions in the Philippines [16]. Moreover, some current biodiversity syntheses aimed at understanding extinction risks are often too broad, which makes it challenging to reflect on local or national policy integration.
The amount of research on Philippine biodiversity has increased significantly in recent years, commonly driven by concerns about the state of its biodiversity and natural resources, which have spurred funding and conservation efforts [11,17]. However, there is a noticeable imbalance in the research focus, with certain territories and organisms receiving disproportionate attention. Mindanao supports unusually high levels of endemism for both amphibians and reptiles [9,18,19]. Nevertheless, like any other taxonomic group, data for herpetofauna species in Mindanao remain sparse and scattered, impeding the effective identification of key species and conservation priorities [8,20,21]. To address this gap, we have developed a literature review as the basis of a biodiversity synthesis aimed at understanding the progress, patterns, and distribution of herpetofauna in Mindanao, Philippines. Specifically, our objective was to determine (i) the levels of effort and factors toward amphibians and reptiles, (ii) the relationship between species extinction risk and endemism, (iii) the diversity and distribution of amphibians and reptiles across biodiversity sites in Mindanao faunal region, and (iv) the key threatening processes and levels of threats to amphibians and reptiles.
By identifying and addressing these issues, our goal is to bolster the overall understanding of herpetofauna’s biodiversity in Mindanao. Furthermore, we intend to prioritize conservation efforts towards species in Mindanao that are threatened and understudied.

2. Materials and Methods

2.1. Study Area and Synthesis Framework

The focus of this study was on biodiversity hotspots in the Mindanao faunal region (MFR), which comprises the entire Mindanao archipelago, the Leyte and Samar islands, Bohol, Basilan, and the nearby minor islands (Figure 1). We adopted a framework to develop the review and synthesis of the literature by integrating the literature from 2000 to 2022 to assess the efforts of species research and threat levels [22].

2.2. Literature Search and Databasing

We used the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) approach to search key databases, including Google Scholar (https://scholar.google.com), ResearchGate (https://www.researchgate.net), and personal correspondence (e.g., for natural history papers not available in both repositories) to create a database of amphibian and reptile literature from January 2000 to June 2022. We used the following keywords: (amphibian* or frog* or newt* or caecilian* or toads*) AND reptile OR snake* OR lizard* OR turtle* OR squamate*) AND (Philippine* OR Mindanao*) to search for the literature [23]. Most Philippine academic institutions do not have an accessible online library or thesis repository [24]. Therefore, we excluded unpublished theses and dissertations from the analysis to standardize and reduce the bias of data sampling for the literature review. All publications collated from the search results were screened and classified by taxonomic group, year of publication, site, and thematic areas using standardized criteria [25].
We curated and updated species names from the recent literature (e.g., [18,19], the International Union for the Conservation of Nature (IUCN) Red List (version 2022-2), the Amphibia Web database (https://amphibiaweb.org/search/) (accessed on 5 November 2022) [26], and the Reptile Database (https://reptile-database.reptarium.cz/) (accessed 14 October 2022) [27]. We determined the species endemism and conservation using the IUCN Red List (v. 2022-2).

2.3. Diversity and Distribution of Amphibians and Reptiles

We investigated the relationship between species diversity, endemism, and species binomial extinction risk (threatened and non-threatened). To determine the risk of extinction, we used the IUCN red list classification [28]. We classified the species as ‘threatened’ when the species is ‘vulnerable’, ‘endangered’, or ‘critically endangered’. On the other hand, we classified species as ‘least threatened’ if they were categorized as ‘least concern’ or ‘near threatened’. Additionally, we included species classified as ‘data deficient’ in the same category as ‘threatened’ when comparing species diversity. We made this assumption because species lacking information may have limited occurrences and are likely to be endangered [29,30]. We compared the species richness per site based on the number of species recorded.
The Chi-square test of independence (χ2) was then applied to assess the relationship between extinction risk, taxonomic groups, and endemism and conservation status. We also employed this analysis to compare endemism and conservation between biodiversity hotspots or sites.

2.4. Research Effort and Threat Assessment

We analyzed species research efforts at the taxonomic level using the Species Research Effort Allocation (SREA) following [25]. We calculated the SREA using the following equation: SREA (x) = R°/y, where x is the species or taxonomic level, R° is the number of times the species or taxonomic group (x) was recorded from the overall publications, and y° is the total assessment coverage. We used Mann–Whitney U or Kruskal–Wallis tests to compare SREA between taxonomic groups, extinction risk, and geopolitical endemism.
To standardize the comparison of threats between endemism and conservation status, and to determine the priority level of each species, we used the species threat index (STI (s)) [14]. Species threats were classified using the standard lexicon [31] and the IUCN classification scheme, with direct, indirect, and natural threats represented [22]. The species threat index (STIspecies = (ƩT/N° T) was calculated as the quotient of the total absolute threat of all species (Tdir,ind,nat) and the number of threats assessed (N° T). Using a non-parametric Kruskal–Wallis test, the species threat index STI (Tdir,ind,nat) was then compared between the threatened category and endemism.
We correlated SREA and STI using Kendall’s Tauτ B to determine if there was a congruence between the research effort and the conservation status among amphibians and reptiles. We used generalized linear mixed models (GLMM) with Poisson distribution to assess the predictor of research efforts toward amphibians and reptiles. We used the relative frequency of species recorded in the literature (%R°) as dependent variables, the risk of species binomial extinction, endemism, body size (log10), and species threat index (STI) as fixed factors, and families as random factors.

2.5. Site-Level Comparison

We compared species diversity distribution, endemism, and conservation status across sites using the Chi-square test of independence (χ2). We estimated the distance and density of species recorded from terrestrial protected areas, which were then calculated using Quantum GIS.
Deforestation is a significant threat to terrestrial ecosystems in the Philippines, including key biodiversity sites. To assess the extent of deforestation and land use change and its relationship with species diversity, endemism, and conservation, we used data from Daipan (2021) [32] to obtain measurements of tree cover loss and remaining forests. Kendall’s Tauτ B was used to examine the relationship between estimated species richness at the site level, percent endemism and percent threatened species, and the rate of change (e.g., rate of deforestation in protected areas). We used a generalized linear model (GLM) with Poisson distribution to determine the link between %remaining forest cover to %endemism and %threatened species in each key biodiversity site.

2.6. Statistical Software

All statistical tests and modeling were performed using the open and free software JAMOVI 2.3.2. [33]. GraphPad Prism 8 was used for data visualization [34], and QGIS 3.16 [35] was used for all spatial analyses. The level of significance was established at p < 0.05.

3. Results

3.1. Diversity and Distribution of Herpetofauna in Mindanao

A total of 42 articles were collated that were published between 2000 and 2022. We found that some studies had classifications that overlapped with other taxonomic groups, and most of the studies included in the review focused on ‘diversity’ studies, particularly in community surveys. Regarding the number of studies per taxonomic group, there were 36 for amphibians and 26 for reptiles. The mean annual number of studies was higher among amphibians (mean = 1.48/yr.) compared to reptiles (mean = 1.09/yr.) (Figure 2a). Research in both taxonomic groups experienced an overall increase, albeit irregularly. Although we did not find significant differences in the number of studies between amphibians and reptiles (Mann–Whitney U test = 229.5, p = 0.431), there was a notable peak in growth in 2015, followed by an inconsistent trend with peaks in 2020 and 2021 (Figure 2b). Furthermore, the correlation analysis showed that amphibians and reptiles were studied extensively together, as shown in their positive and significant correlation in terms of the number of species recorded per year (Kendall’s τ B = 0.845, p < 0.001).
Based on the database we built from the published literature, we recorded 160 species of herpetofauna from the MFR (Table S1). This includes 52 species of amphibians belonging to nine families and two orders and 108 species of reptiles belonging to sixteen families of two orders. Among amphibians, Rhacophoridae and Dicroglossidae were the most species-rich families recorded (n = 12 spp., 23%), followed by Microhylidae (n = 7 spp., 13%), Ranidae (n = 6 spp., 11.5%), Bufonidae (n = 5 spp., 10%), Ceratobatrachidae (n = 4 spp., 8%), Megophyridae (n = 3 spp., 6%), and Eleutherodactylidae and Ichthyophiidae, each represented by single species recorded (n = 1 spp., 2%). Among reptiles, Scinidae was the most species-rich (n = 35 spp., 32%), followed by Gekkonidae (n = 15 spp., 14%), Colubridae (n = 13 spp., 12%), and Agamidae (n = 11 spp., 10%). At the same time, other families were represented by fewer than 10 species. Regarding species endemism, we found more endemic species among reptiles (58%, n = 63 spp.), but a higher percentage of endemics among amphibians (63%, n = 33 spp.).
Species Research Effort Allocation (SREA) was significantly different and higher among amphibians than among reptiles and all other taxonomic groups (Figure 3). Within amphibians, we found that non-threatened species (mean = 0.356 ± 0.299) a had higher SREA compared to threatened groups (mean = 0.145 ± 0.145), but not statistically significant (H = 3.169, df = 1, p = 0.075). In terms of geopolitical endemism, we found a significantly higher SREA among Philippine-endemic species (mean = 0.395 ± 0.316) versus non-endemic species (mean = 0.232 ± 0.220) (H = 4.186, df = 1, p = 0.041). However, among reptiles, we found that the SREA did not differ significantly in terms of endemism but was higher between species endemic to the Philippines (mean = 0.183 ± 0.137) compared to their more widespread counterparts (Figure 3).

3.2. Conservation Status across Endemism and Conservation

Twenty percent of all herpetofauna species were considered in the threatened category (VU = 4 spp., EN = 3 spp., and DD = 14 spp.). The conservation status between taxonomic groups differed, with 14.8% and 9.6% of reptiles and amphibians being threatened, respectively. Among nine amphibian families, Dicroglossidae (25%, n = 3 spp.) and Ceratobatrachidae (20%, n = 1 spp.) had the highest proportions of threatened species (χ2 = 7.317, df = 8, p = 0.503). Although no significant differences were found in the distribution of threatened species between the 17 families of reptiles (χ2 = 22.458, df = 16, p = 0.129), we documented that at least 6 families had a remarkably higher proportion of threatened species, particularly Geomydidae (100%, n = 1 spp.), Elapidae (50%, n = 2 spp.), Typhlopidae (50%, n = 1), Agamidae (36.4%, n = 4), and Calamariidae (33.33%, n = 1). Furthermore, the proportion of threatened species between endemic species only differed significantly among reptiles (χ2 = 4.058, df = 1, p = 0.044) and was highest among those endemic to the Philippines (20.6%, n = 13 spp.). Although we did not find a significant relationship in the proportion of threatened species among amphibians (χ2 = 3.185, df = 1, p = 0.074), it was higher among Philippine-endemic species (15.2%, n = 5 spp.) compared to those that are widespread (Figure 4a).
Among the key threats, bushmeat hunting, deforestation, and other changes in land use are the major threats to amphibians and reptiles (Figure 4b). Bushmeat consumption threatens 74% of amphibians and 55% of reptiles. Land use changes such as agriculture and aquaculture are the subsequent significant threats, threatening 64% of amphibians and 51% of reptiles (Figure 4b). Interestingly, urbanization (52%) and pollution (35%) threaten a high proportion of amphibians compared to reptiles.
We used the species threat index (STI) to determine the level of threat each species faces according to its endemism and conservation status. Amphibians exhibited a significantly higher species threat index (STI) compared to other taxonomic groups, such as birds and mammals, while reptiles showed an exceptionally low STI (Figure 5). Among endemism and conservation status, STI was generally higher among threatened amphibian species (0.500 ± 0.204) (H = 0.012, df = 1, p = 0.911) and reptiles (0.313 ± 0.175) (H = 6.285, df = 1, p = 0.012), but only statistically significant in the latter. We observed similar patterns of threat levels between Philippine-endemic amphibians (0.556 ± 0.211) (H = 7.145, df = 1, p = 0.008) and reptiles (0.227 ± 0.166) (H = 4.534, df = 1, p = 0.033).

3.3. Relationship between Threat Index and Research Effort

We did not find a significant correlation between SREA and STI among amphibians (Kendall’s τ B = 0.007, p = 0.472) and reptiles (Kendall’s τ B = 0.062, p = 0.425). On the contrary, a positive and significant correlation between body mass and STI was specifically observed among reptiles (Figure 5). More importantly, our analysis revealed significant trends in the research focus on herpetofauna of Mindanao. Our findings revealed a negative correlation (β = −0.646, p < 0.001) between the allocation of the research effort and its threat status, indicating that more efforts were directed toward non-threatened species (Table 1). Similarly, herpetofauna species with lower threat levels are studied more but were only significant for amphibians (β = −0.355, p < 0.001). Furthermore, Philippine-endemic herpetofauna species exhibited a positive association with increased research effort (β = 0.415, p < 0.001), as did larger-bodied species (β = 0.272, p < 0.001). These trends were consistent in separate models for reptiles and amphibians, indicating an overall pattern in the relationship between the research effort and the endemism and conservation status of the species (Table 1).

3.4. Site-Level Priorities

We recorded a total of 1060 (51%) amphibian and 1031 (49%) reptile occurrences at 28 biodiversity hotspot sites in Mindanao (Figure 6). Within this dataset, 44% of the amphibian and 49% of the reptile records were within 10 km of protected areas. Among the 27 sites for amphibians, Mount Hibok-Hibok (n = 26 spp.) and Mount Hilong-Hilong (n = 25 spp.) had the highest number of recorded species. While Mount Balatukan (100%, n = 25 spp.), Mount Lumot (77.4%, n = 24 spp.), and Mount Magdiwata (78.1%, n = 25 spp.) had the highest number of Philippine-endemic species (n = 30 spp.). However, we observed a lower proportion of threatened amphibian species among the sites included in our analysis. Specifically, only two sites had a percentage of threatened amphibian species that exceeded 10%. Although 20 biodiversity hotspots for reptiles were studied, Mount Hamiguitan (n = 96 spp.) and Mount Magdiwata (n = 58 spp.) were the sites that had the highest species. Likewise, Mount Hamiguitan had the highest recorded endemic species (n = 63 spp., 66%), followed by Mount Magdiwata (n = 37 spp., 78%). In contrast, reptile species exhibited a higher proportion of threatened species among the analyzed sites. Specifically, three sites had more than 20% of their reptile species classified as threatened, while in five sites, at least 10% of the reptile species were in the threatened category (Figure 6). In general, the number of threatened amphibians (χ2 = 17.40, df = 26, p = 0.897) and reptiles (χ2 = 17.415, df = 19, p = 0.562) did not show a significant difference between biodiversity sites.
Furthermore, we found a strong concordance between the species richness of amphibians and reptiles across sites (Kendall’s τ B = 0.626, p < 0.001). Similarly, we found a positive correlation between the percentage of endemism and threatened species among amphibians (Kendall’s τ B = 0.468, p = 0.007) and reptiles (Kendall’s τ B = 0.715, p < 0.001). Furthermore, we found that a higher proportion of threatened (β = 0.005, p = 0.034) and endemic (β = 0.006, p = 0.002) amphibian species, but not among reptiles, are related to the higher amount of forest remaining within biodiversity sites.

4. Discussion

Mindanao is home to a diverse range of unique and endangered taxa that provide valuable ecosystem services to humans. This study represents the first attempt to synthesize and analyze biodiversity conservation initiatives that specifically target amphibians and reptiles in the megadiverse region of the Philippines. Our literature review allowed us to synthesize our understanding of the diversity and distribution of herpetofauna and their research gaps in the region.
In our study, we recorded the presence of 160 species and have shown that various studies and efforts in Mindanao increased available herpetological knowledge. Based on our literature review, the number of species we recorded represents approximately 46% of the total herpetofauna species in the Philippines [18,19]. Our synthesis of the available data generally indicates that Mindanao has a high diversity of amphibians and reptiles. This is congruent with the broader patterns of distribution observed throughout the Philippines [8]. Herpetofaunal endemism is as high as 85%, with up to 23% of native amphibians endemic to Mindanao [18,19,36]. Furthermore, our study showed a positive correlation between research efforts (i.e., the number of studies) and the number of herpetofauna species recorded in the last two decades. This growing record is due to recent comprehensive biodiversity assessments conducted in various ecosystems of Mindanao that have provided evidence of the exceptional levels of diversity and endemism of herpetofauna in the region. Consequently, these assessments have shed light on the remarkable richness and unique composition of amphibians and reptiles found in Mindanao [19,37]. For example, in Northeast Mindanao and the surrounding islands, Sanguila et al. [19] recorded at least 126 amphibian and reptile species, including 40 species of frogs and 1 species of caecilian for amphibians, and 49 species of lizards, 35 species of snakes, 1 species of freshwater turtle, and 1 species of crocodile for reptiles. Furthermore, in the southern part of Mindanao, for example, at Mount Busa, which was poorly explored before, 68 species of herpetofauna were discovered, including 28 amphibians and 40 reptiles [38].
Despite increasing research efforts, data are still lacking for a large number of amphibian and reptile species, hampering conservation efforts toward many of these species. While amphibians and reptiles are often studied in tandem, we found a greater research focus on the former. A comparison of effort allocation measures between taxonomic groups revealed that amphibian species received more attention than birds and mammals [20]. Still, reptiles remain the most poorly studied group among terrestrial vertebrates. Our findings are consistent with a previous analysis showing that amphibians are studied and represented more in the literature than reptiles [39,40]. Although both groups are confronting comparable threats, the growing focus on amphibians can be attributed to a greater demand to prioritize them. This increasing attention comes from persistent reports of declining amphibian populations around the world, mainly due to their vulnerability to climate and land use changes [2,41].
The observed bias in research between amphibians and reptiles may also be explained by species traits and their probability of detection during field studies. Amphibians are generally more readily detectable due to their distinctive breeding patterns, making them potentially easier to locate [42,43,44]. During rainy periods, amphibians often become more visible, emerge from concealment, and can even be identified by their audible calls [42,45]. On the other hand, reptiles exhibit less predictable patterns compared to amphibians, and unlike frogs, they do not vocalize or produce distinct calls, further complicating their detection and observation [46]. In addition, some recorded reptiles are often fossorial, making them more challenging to collect and study than those living aboveground, and this can lead to poor representation in scientific collections and records relative to other groups [40,47,48]. On the contrary, arboreal species, such as most amphibians, are easier to find and capture during visual surveys [49]. However, there is a clear lack of trait information available for many herpetofaunal species in Mindanao, thus certainly pinpointing the fact that the relationships of traits and their detectability need further exploration.
Furthermore, our analysis revealed a bias in research allocation toward larger herpetofauna species. This bias can be attributed to the practicality of detecting and studying larger species during fieldwork [40,50]. Their size and visibility make them more accessible and easier to observe and document than smaller, cryptic species. The preference to study larger herpetofauna species can inadvertently overlook the ecological importance and conservation needs of smaller species [51].
Contrary to our expectations, endemic and rare species were more frequently studied for both groups. However, we showed that threatened herpetofauna species were poorly studied in general. This is likely because threatened species generally have narrower ranges and are therefore difficult to observe and study [52,53]. In addition, research on threatened species is often subject to more stringent regulations and permits, making research more difficult, costly, and time-consuming. Our analysis also showed that amphibians face more threats than reptiles or any other group of vertebrates, regardless of their endemism and conservation status. Among the threats to the herpetofauna are pollution and habitat loss, likely driven by deforestation, shifting agriculture, and wildlife collection for consumption. Globally, amphibians and reptiles are especially susceptible to environmental changes and direct human activities [5,6]. However, amphibians are declining much more rapidly than other terrestrial vertebrates, and multiple factors are attributed to this trend [54,55]. Amphibians, in addition to being ectothermic, have complex life cycles, which makes them usually more sensitive to rapid environmental disturbance and threats such as habitat modification, pollution, and climatic change [7,56].
Furthermore, increasing levels of pollutants in freshwater ecosystems are also associated with direct mortality and physiological impacts on the decline of the amphibian population [57]. Although there is limited research on reptiles, they are expected to be just as vulnerable to the same threats as amphibians [6,58,59], especially since the two groups share and occupy similar ecological requirements and habitats. A recent global analysis showed that 21% of global reptiles are in threatened categories and face significant threats similar to those of other tetrapods, including agriculture, logging, urban development, and invasive species [59]. Furthermore, our analysis showed that the increase in forest cover in key biodiversity sites supports more ecologically important species of herpetofauna. Tropical forest species of reptiles and amphibians, such as those of Mindanao forests, are more threatened and susceptible to many threats and population declines compared to species in other ecosystems [8,58,59]. This suggests that allocating more protection efforts in forest areas, especially in lowlands where threats are greater, will conserve more species and avoid loss [20]. However, the potential impact of climate change on Mindanao’s herpetofauna remains unclear due to the lack of studies and investigations dedicated to the impacts of such threats [60]. Together with the environmental changes, the records of invasive species of amphibians such as the Asiatic painted toad (Kaloula pulchra), cane toad (Rhinella marina), Chinese bullfrog (Hoplobatrachus rugulosus), and greenhouse frog (Eleutherodactylus planirostris) may also pose a threat to native populations of amphibians in the region, and should be given careful attention [61].
The current state of herpetofauna research in Mindanao highlights important trends and knowledge gaps that require attention, but also presents an opportunity for current and future conservation efforts. By recognizing threats and their impacts on different species, we can strategically directly apply research efforts to identify the mechanisms driving these risks. Given the cryptic behavior of amphibians and reptiles, long-term monitoring efforts and the effective integration of available information will be required to guide conservation efforts and mitigate and address the many environmental threats to native Philippine herpetofauna. Likewise, by understanding research biases toward different taxonomic groups in Mindanao, we can direct limited conservation funding to research efforts where they are most needed, that is, toward understudied and neglected taxa that may likely face more threats. Furthermore, considering the changing climate and the increasing human alteration of habitats, the need to address the issue becomes increasingly urgent, primarily due to the increased susceptibility of diverse herpetofauna communities to extinction [62,63]. Finally, efforts to increase knowledge and improve species inventory are being made by promoting integrative taxonomic studies and building collaborative networks. Lastly, making biodiversity assessment data more accessible and open is one of the few initiatives that should be pursued to further advance herpetofauna research not only in Mindanao but throughout the Philippines.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/conservation3030025/s1, Table S1: List of herpetofauna included in the analysis based from literature published from 2000 to 2022. References [64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95] are cited in the supplementary materials.

Author Contributions

Conceptualization, K.C.T., S.S.A. and K.C.D.C.; methodology, K.C.T., S.S.A. and K.C.D.C.; validation, K.C.T., S.S.A., A.R.A., L.F.C. and K.C.D.C.; formal analysis, K.C.T., S.S.A., A.R.A. and K.C.D.C.; investigation, S.S.A.; resources, K.C.T.; data curation, K.C.T., S.S.A., A.R.A., L.F.C. and K.C.D.C.; writing—original draft preparation, S.S.A., A.R.A. and K.C.T.; writing—review and editing, K.C.T., S.S.A., A.R.A., L.F.C. and K.C.D.C.; visualization, S.S.A., K.C.D.C. and K.C.T.; supervision, K.C.T., A.R.A. and L.F.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research is self-funded and received no external funding from any institutions.

Data Availability Statement

Data associated with this manuscript are available in the supplementary files.

Acknowledgments

We would like to thank the editors and the four anonymous reviewers for their rigorous and insightful feedback, which substantially improved this article.

Conflicts of Interest

The authors declare that the research was conducted without any commercial or financial relationships that could be construed as a potential conflicts of interest.

References

  1. Ceballos, G.; Ehrlich, P.R.; Barnosky, A.D.; García, A.; Pringle, R.M.; Palmer, T.M. Accelerated Modern Human–Induced Species Losses: Entering the Sixth Mass Extinction. Sci. Adv. 2015, 1, e1400253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Wake, D.B.; Vredenburg, V.T. Are We in the Midst of the Sixth Mass Extinction? A View from the World of Amphibians. Proc. Natl. Acad. Sci. USA 2008, 105, 11466–11473. [Google Scholar] [CrossRef]
  3. Pimm, S.L.; Jenkins, C.N.; Abell, R.; Brooks, T.M.; Gittleman, J.L.; Joppa, L.N.; Raven, P.H.; Roberts, C.M.; Sexton, J.O. The Biodiversity of Species and Their Rates of Extinction, Distribution, and Protection. Science 2014, 344, 1246752. [Google Scholar] [CrossRef]
  4. Bickford, D.; Howard, S.D.; Ng, D.J.J.; Sheridan, J.A. Impacts of Climate Change on the Amphibians and Reptiles of Southeast Asia. Biodivers. Conserv. 2010, 19, 1043–1062. [Google Scholar] [CrossRef]
  5. Hoffmann, M.; Hilton-Taylor, C.; Angulo, A.; Böhm, M.; Brooks, T.M.; Butchart, S.H.M.; Carpenter, K.E.; Chanson, J.; Collen, B.; Cox, N.A.; et al. The Impact of Conservation on the Status of the World’s Vertebrates. Science 2010, 330, 1503–1509. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Böhm, M.; Collen, B.; Baillie, J.E.M.; Bowles, P.; Chanson, J.; Cox, N.; Hammerson, G.; Hoffmann, M.; Livingstone, S.R.; Ram, M.; et al. The Conservation Status of the World’s Reptiles. Biol. Conserv. 2013, 157, 372–385. [Google Scholar] [CrossRef] [Green Version]
  7. Hof, C.; Araújo, M.B.; Jetz, W.; Rahbek, C. Additive Threats from Pathogens, Climate and Land-Use Change for Global Amphibian Diversity. Nature 2011, 480, 516–519. [Google Scholar] [CrossRef]
  8. Diesmos, A.; Brown, R.; Alcala, A.; Sison, R.; Afuang, L.; Gee, G. Philippine Amphibians and Reptiles: An Overview of Species Diversity, Biogeography, and Conservation. In Philippine Biodiversity Conservation Priorities: A Second Iteration of the National Biodiversity Strategy and Action Plan; Department of the Environment and Natural Resources, Conservation International, University of the Philippines Center for Integrative and Developmental Studies, and Foundation for the Philippine Environment: Quezon City, Philippines, 2002; pp. 26–44. [Google Scholar]
  9. Das, I.; van Dijk, P.P. Species richness and endemicity of the herpetofauna of South and Southeast Asia. Raffles Bull. Zool. 2013, 9, 269–277. [Google Scholar]
  10. Alcala, E.L.; Alcala, A.C.; Dolino, C.N. Amphibians and Reptiles in Tropical Rainforest Fragments on Negros Island, the Philippines. Environ. Conserv. 2004, 31, 254–261. [Google Scholar] [CrossRef]
  11. Posa, M.R.C.; Diesmos, A.C.; Sodhi, N.S.; Brooks, T.M. Hope for Threatened Tropical Biodiversity: Lessons from the Philippines. BioScience 2008, 58, 231–240. [Google Scholar] [CrossRef] [Green Version]
  12. Hoffmann, M.; Brooks, T.M.; da Fonseca, G.A.B.; Gascon, C.; Hawkins, A.F.A.; James, R.E.; Langhammer, P.; Mittermeier, R.A.; Pilgrim, J.D.; Rodrigues, A.S.L.; et al. Conservation Planning and the IUCN Red List. Endanger. Species Res. 2008, 6, 113–125. [Google Scholar] [CrossRef]
  13. Rondinini, C.; Rodrigues, A.S.L.; Boitani, L. The Key Elements of a Comprehensive Global Mammal Conservation Strategy. Philos. Trans. R. Soc. B Biol. Sci. 2011, 366, 2591–2597. [Google Scholar] [CrossRef] [Green Version]
  14. Tanalgo, K.C.; Oliveira, H.F.M.; Hughes, A.C. Mapping Global Conservation Priorities and Habitat Vulnerabilities for Cave-Dwelling Bats in a Changing World. Sci. Total Environ. 2022, 843, 156909. [Google Scholar] [CrossRef] [PubMed]
  15. Cooper, N.; Bielby, J.; Thomas, G.H.; Purvis, A. Macroecology and Extinction Risk Correlates of Frogs. Glob. Ecol. Biogeogr. 2008, 17, 211–221. [Google Scholar] [CrossRef]
  16. Heberling, J.M.; Miller, J.T.; Noesgaard, D.; Weingart, S.B.; Schigel, D. Data Integration Enables Global Biodiversity Synthesis. Proc. Natl. Acad. Sci. USA 2021, 118, e2018093118. [Google Scholar] [CrossRef] [PubMed]
  17. Mercado, D. Compilation & Synthesis of Valuation Studies on Philippine Biodiversity; UNDP: New York, NY, USA, 2016. [Google Scholar]
  18. Diesmos, A.; Watters, J.; Huron, N.; Davis, D.; Alcala, A.; Crombie, R.; Afuang, L.; Gee-Das, G.; Sison, R.; Sanguila, M.; et al. Amphibians of the Philippines, Part 1: Checklist of the Species. Proc. Calif. Acad. Sci. 2015, 62, 457–539. [Google Scholar]
  19. Sanguila, M.B.; Cobb, K.A.; Siler, C.D.; Diesmos, A.C.; Alcala, A.C.; Brown, R.M. The Amphibians and Reptiles of Mindanao Island, Southern Philippines, II: The Herpetofauna of Northeast Mindanao and Adjacent Islands. Zookeys 2016, 624, 1–132. [Google Scholar] [CrossRef] [Green Version]
  20. Dela Cruz, K.C.; Abdullah, S.S.; Agduma, A.R.; Tanalgo, K.C. Early Twenty-First Century Biodiversity Data Pinpoint Key Targets for Bird and Mammal Conservation in Mindanao, Southern Philippines. Biodiversity 2023, 1–18. [Google Scholar] [CrossRef]
  21. Agduma, A.R.; Garcia, F.G.; Cabasan, M.T.; Pimentel, J.; Ele, R.J.; Rubio, M.; Murray, S.; Hilario-Husain, B.A.; Dela Cruz, K.C.; Abdullah, S.; et al. Overview of Priorities, Threats, and Challenges to Biodiversity Conservation in the Southern Philippines. Reg. Sustain. 2023, 4, 203–213. [Google Scholar] [CrossRef]
  22. Tanalgo, K.C.; Hughes, A.C. Priority-Setting for Philippine Bats Using Practical Approach to Guide Effective Species Conservation and Policy-Making in the Anthropocene. Hystrix 2019, 30, 74–83. [Google Scholar] [CrossRef]
  23. McInnes, M.D.F.; Moher, D.; Thombs, B.D.; McGrath, T.A.; Bossuyt, P.M.; Clifford, T.; Cohen, J.F.; Deeks, J.J.; Gatsonis, C.; Hooft, L.; et al. Preferred Reporting Items for a Systematic Review and Meta-Analysis of Diagnostic Test Accuracy Studies: The PRISMA-DTA Statement. JAMA 2018, 319, 388–396. [Google Scholar] [CrossRef] [PubMed]
  24. Guerrero, J.; Tanalgo, K.; Abante, C. Role of Academic Institution to Inform Local and Regional Scale Biodiversity in the Eastern Philippines. J. Trop. Life Sci. 2021, 11, 241–250. [Google Scholar] [CrossRef]
  25. Tanalgo, K.C.; Hughes, A.C. Bats of the Philippine Islands—A Review of Research Directions and Relevance to National-Level Priorities and Targets. Mamm. Biol. 2018, 91, 46–56. [Google Scholar] [CrossRef]
  26. AmphibiaWeb Database. AmphibiaWeb Database Search. Available online: https://amphibiaweb.org/search/ (accessed on 5 November 2022).
  27. The Reptile Database. The Reptile Database. Available online: https://reptile-database.reptarium.cz/ (accessed on 14 October 2022).
  28. Atwood, T.B.; Valentine, S.A.; Hammill, E.; McCauley, D.J.; Madin, E.M.; Beard, K.H.; Pearse, W.D. Herbivores at the Highest Risk of Extinction among Mammals, Birds, and Reptiles. Sci. Adv. 2020, 6, eabb8458. [Google Scholar] [CrossRef] [PubMed]
  29. Bland, L.M.; Collen, B.; Orme, C.D.L.; Bielby, J. Predicting the Conservation Status of Data-Deficient Species: Predicting Extinction Risk. Conserv. Biol. 2015, 29, 250–259. [Google Scholar] [CrossRef] [PubMed]
  30. Tanalgo, K.C.; Tabora, J.A.G.; Hughes, A.C. Bat Cave Vulnerability Index (BCVI): A Holistic Rapid Assessment Tool to Identify Priorities for Effective Cave Conservation in the Tropics. Ecol. Indic. 2018, 89, 852–860. [Google Scholar] [CrossRef]
  31. Salafsky, N.; Salzer, D.; Stattersfield, A.J.; Hilton-Taylor, C.; Neugarten, R.; Butchart, S.H.M.; Collen, B.; Cox, N.; Master, L.L.; O’Connor, S.; et al. A Standard Lexicon for Biodiversity Conservation: Unified Classifications of Threats and Actions. Conserv. Biol. 2008, 22, 897–911. [Google Scholar] [CrossRef]
  32. Daipan, B.P. Patterns of Forest Cover Loss in the Terrestrial Key Biodiversity Areas in the Philippines: Critical Habitat Conservation Priorities. J. Threat. Taxa 2021, 13, 20019–20032. [Google Scholar] [CrossRef]
  33. Jamovi, Version 2.3.22; The Jamovi Project: Sydney, Australia, 2023.
  34. GraphPad Prism, GraphPad Software, Inc.: San Diego, CA, USA, 2022.
  35. QGIS Development Team QGIS Geographic Information System. Open Source Geospatial Foundation Project. 2022. Available online: http://qgis.osgeo.org (accessed on 14 October 2022).
  36. Diesmos, A.C. Ecology and Diversity of Herpetofaunal Communities in Fragmented Lowland Rainforests in the Philippines. Ph.D. Thesis, National University of Singapore, Singapore, 2009. [Google Scholar]
  37. Plaza, J.; Sanguila, M. Preliminary Report on the Anurans of Mount Hilong-Hilong, Agusan Del Norte, Eastern Mindanao, Philippines. Asian Herpetol. Res. 2015, 6, 18–33. [Google Scholar] [CrossRef]
  38. Pitogo, K.M.; Saavedra, A.J.; Afuang, L. Amphibians and Reptiles of Mount Busa, Sarangani Province: A Glimpse of the Herpetological Community of Southern Mindanao, Philippines. Philipp. J. Sci. 2021, 150, 1279–1306. [Google Scholar] [CrossRef]
  39. Christoffel, R.A.; Lepczyk, C.A. Representation of Herpetofauna in Wildlife Research Journals. J. Wildl. Manag. 2012, 76, 661–669. [Google Scholar] [CrossRef]
  40. Guedes, J.J.M.; Moura, M.R.; Alexandre, F.; Diniz-Filho, J. Species out of Sight: Elucidating the Determinants of Research Effort in Global Reptiles. Ecography 2023, 2023, e06491. [Google Scholar] [CrossRef]
  41. Lötters, S.; Plewnia, A.; Catenazzi, A.; Neam, K.; Acosta-Galvis, A.; Vela, Y.A.; Allen, J.; Segundo, J.A.; Cabezas, A.A.; Alvarado, G.; et al. The Amphibian Extinction Crisis Is Still an Emergency. Res. Sq. 2023. preprint. [Google Scholar] [CrossRef]
  42. Dubos, N.; Morel, L.; Crottini, A.; Freeman, K.; Honoré, J.; Lava, H.; Noël, J.; Porton, I.; Rendrirendry, G.; Rosa, G.M.; et al. High Interannual Variability of a Climate-Driven Amphibian Community in a Seasonal Rainforest. Biodivers. Conserv. 2020, 29, 893–912. [Google Scholar] [CrossRef]
  43. Aide, T.M.; Corrada-Bravo, C.; Campos-Cerqueira, M.; Milan, C.; Vega, G.; Alvarez, R. Real-Time Bioacoustics Monitoring and Automated Species Identification. PeerJ 2013, 1, e103. [Google Scholar] [CrossRef] [Green Version]
  44. Segniagbeto, G.H.; Dekawole, J.K.; Ketoh, G.K.; Dendi, D.; Luiselli, L. Herpetofaunal Diversity in a Dahomey Gap Savannah of Togo (West Africa): Effects of Seasons on the Populations of Amphibians and Reptiles. Diversity 2022, 14, 964. [Google Scholar] [CrossRef]
  45. Larsen, A.S.; Schmidt, J.H.; Stapleton, H.; Kristenson, H.; Betchkal, D.; McKenna, M.F. Monitoring the Phenology of the Wood Frog Breeding Season Using Bioacoustic Methods. Ecol. Indic. 2021, 131, 108142. [Google Scholar] [CrossRef]
  46. Hoefer, S.; McKnight, D.T.; Allen-Ankins, S.; Nordberg, E.J.; Schwarzkopf, L. Passive Acoustic Monitoring in Terrestrial Vertebrates: A Review. Bioacoustics 2023, 1–26. [Google Scholar] [CrossRef]
  47. Colli, G.R.; Fenker, J.; Tedeschi, L.G.; Barreto-Lima, A.F.; Mott, T.; Ribeiro, S.L.B. In the Depths of Obscurity: Knowledge Gaps and Extinction Risk of Brazilian Worm Lizards (Squamata, Amphisbaenidae). Biol. Conserv. 2016, 204, 51–62. [Google Scholar] [CrossRef]
  48. Moura, M.R.; Costa, H.C.; Abegg, A.D.; Alaminos, E.; Angarita-Sierra, T.; Azevedo, W.S.; Cabral, H.; Carvalho, P.; Cechin, S.; Citeli, N.; et al. Unwrapping Broken Tails: Biological and Environmental Correlates of Predation Pressure in Limbless Reptiles. J. Anim. Ecol. 2023, 92, 324–337. [Google Scholar] [CrossRef]
  49. Petrovan, S.O.; Al-Fulaij, N.; Christie, A.; Andrews, H. Why Link Diverse Citizen Science Surveys? Widespread Arboreal Habits of a Terrestrial Amphibian Revealed by Mammalian Tree Surveys in Britain. PLoS ONE 2022, 17, e0265156. [Google Scholar] [CrossRef]
  50. Bonnet, X.; Shine, R.; Lourdais, O. Taxonomic Chauvinism. Trends Ecol. Evol. 2002, 17, 1–3. [Google Scholar] [CrossRef]
  51. Ruggieri-Mitchell, C. The More Things Changed, the More They Stayed the Same: Trends in Conservation Focus 2010–2019. J. Nat. Conserv. 2023, 73, 126403. [Google Scholar] [CrossRef]
  52. Ducatez, S.; Shine, R. Drivers of Extinction Risk in Terrestrial Vertebrates. Conserv. Lett. 2017, 10, 186–194. [Google Scholar] [CrossRef]
  53. Chen, C.; Chen, C.; Wang, Y. Ecological Correlates of Extinction Risk in Chinese Amphibians. Divers. Distrib. 2019, 25, 1586–1598. [Google Scholar] [CrossRef]
  54. Catenazzi, A. State of the World’s Amphibians. Annu. Rev. Environ. Resour. 2015, 40, 91–119. [Google Scholar] [CrossRef]
  55. Harfoot, M.B.J.; Johnston, A.; Balmford, A.; Burgess, N.D.; Butchart, S.H.M.; Dias, M.P.; Hazin, C.; Hilton-Taylor, C.; Hoffmann, M.; Isaac, N.J.B.; et al. Using the IUCN Red List to Map Threats to Terrestrial Vertebrates at Global Scale. Nat. Ecol. Evol. 2021, 5, 1510–1519. [Google Scholar] [CrossRef] [PubMed]
  56. Stuart, S.N.; Chanson, J.S.; Cox, N.A.; Young, B.E.; Rodrigues, A.S.L.; Fischman, D.L.; Waller, R.W. Status and Trends of Amphibian Declines and Extinctions Worldwide. Science 2004, 306, 1783–1786. [Google Scholar] [CrossRef] [Green Version]
  57. Polo-Cavia, N.; Burraco, P.; Gomez-Mestre, I. Low Levels of Chemical Anthropogenic Pollution May Threaten Amphibians by Impairing Predator Recognition. Aquat. Toxicol. 2016, 172, 30–35. [Google Scholar] [CrossRef] [PubMed]
  58. Gibbons, J.W.; Scott, D.E.; Ryan, T.J.; Buhlmann, K.A.; Tuberville, T.D.; Metts, B.S.; Greene, J.L.; Mills, T.; Leiden, Y.; Poppy, S.; et al. The Global Decline of Reptiles, Déjà Vu Amphibians: Reptile Species Are Declining on a Global Scale. Six Significant Threats to Reptile Populations Are Habitat Loss and Degradation, Introduced Invasive Species, Environmental Pollution, Disease, Unsustainable Use, and Global Climate Change. BioScience 2000, 50, 653–666. [Google Scholar] [CrossRef] [Green Version]
  59. Cox, N.; Young, B.E.; Bowles, P.; Fernandez, M.; Marin, J.; Rapacciuolo, G.; Böhm, M.; Brooks, T.M.; Hedges, S.B.; Hilton-Taylor, C.; et al. A Global Reptile Assessment Highlights Shared Conservation Needs of Tetrapods. Nature 2022, 605, 285–290. [Google Scholar] [CrossRef] [PubMed]
  60. Alcala, A.; Bucol, A.; Diesmos, A.; Brown, R. Vulnerability of Philippine Amphibians to Climate Change. Philipp. J. Sci. 2012, 141. [Google Scholar]
  61. Pili, A.N.; Supsup, C.E.; Sy, E.Y.; Diesmos, M.L.L.; Diesmos, A.C. Spatial Dynamics of Invasion and Distribution of Alien Frogs in a Biodiversity Hotspot Archipelago; International Union for Nature Conservation (IUCN): Gland, Switzerland, 2019. [Google Scholar]
  62. Iglesias-Carrasco, M.; Medina, I.; Ord, T.J. Global Effects of Forest Modification on Herpetofauna Communities. Conserv. Biol. 2023, 37, e13998. [Google Scholar] [CrossRef]
  63. Tan, W.C.; Herrel, A.; Rödder, D. A Global Analysis of Habitat Fragmentation Research in Reptiles and Amphibians: What Have We Done So Far? Biodivers. Conserv. 2023, 32, 439–468. [Google Scholar] [CrossRef]
  64. Almeria, M.L.; Nuñeza, O.M. Diet of seven anuran species (Amphibia: Anura) in Agusan Marsh, Mindanao, Philippines. Anim. Biol. Anim. Husb. 2013, 5, 116–126. [Google Scholar]
  65. Ates, F.B.; Delima, E.M.M. Assemblage and microhabitats of anurans from Mt. Sinaka, Arakan, Cotabato and Mt. Hamiguitan, Davao Oriental, Mindanao Island, Philippines. J. Nat. Stud. 2008, 7, 101–107. [Google Scholar]
  66. Balmores, M.N.; Nuñeza, O.M. The reptiles of Bega watershed of the province of Agusan Del Sur in the Philippines. World J. Environ. Biosciences 2015, 4, 50–61. [Google Scholar]
  67. Baron, E.M.D.; Marin, M.O.D.; Logramonte, B.A.; Mohagan, A.B. Species Account of Anurans from the Western Slope of Mt. Kitanglad, Mindanao Island, Philippines. Asian Herpetol. Res. 2021, 12, 76–87. [Google Scholar]
  68. Belleza, B.G.D.; Nuneza, O.M. Herpetofaunal diversity and endemism in selected caves of Sarangani Province and Lanao del Sur, Philippines. Adv. Environ. Biol. 2014, 8, 411–418. [Google Scholar]
  69. Beukema, W. Herpetofauna of disturbed forest fragments on the lower Mt. Kitanglad Range, Mindanao Island, Philippines. Salamandra 2011, 47, 90–98. [Google Scholar]
  70. Calo, T.J.V.; Nuñeza, O.M. Species richness and endemism of anurans in Bega Watershed, Prosperidad, Agusan del Sur, Philippines. J. Biodivers. Environ. Sci. 2015, 7, 1–14. [Google Scholar]
  71. Coritico, F.B.; Sinamban, E.B.; Mohagan, A.B.; Amoroso, V.B. Preliminary report on the anurans of Mt. Pantaron Range, Bukidnon, Central Mindanao, the Philippines. J. Nat. Stud. 2018, 17, 9–23. [Google Scholar]
  72. Coronel, J.; Gomez, R.; Allado, A.; Bravo, R.; Montero, J. Gaynawaan 2004: Conservation of Threatened Vertebrates at Mount Sinaka, Mindanao. Available online: https://www.conservationleadershipprogramme.org/media/2014/11/000704_Philippines_FR_Gaynawaan.pdf (accessed on 11 October 2022).
  73. Dela Torre, V.C.; Nuneza, O.M. Species Diversity, Distribution, and Microhabitats of Anurans on Mt. Kalo-Kalo of the Mt. Kalatungan Range Natural Park, Bukidnon, Philippines. Asian Herpetol. Res. 2021, 12, 58–75. [Google Scholar]
  74. Delima, E.M.M.; Ates, F.B.; Ibañez, J.C. Species composition and microhabitats of frogs within Arakan Valley Conservation Area, Cotabato, Mindanao Island, Philippines. Banwa 2006, 3, 16–30. [Google Scholar]
  75. Delima, E.M.M.; Diesmos, A.C.; Ibañez, J.C. The herpetological importance of Mt. Hamiguitan Range, Mindanao Island, Philippines. Banwa 2007, 4, 27–40. [Google Scholar]
  76. Galolo, A.R.V.; Demayo, C.G.; Raganas, C.D.; Paz, S.L. Amphibian diversity, endemism and habitat associations within and outside the selected mining sites in Caraga Region, Philippines. Proc. Int. Acad. Ecol. Environ. Sci. 2001, 11, 159–187. [Google Scholar]
  77. Hingco, J.T.; Manapsal, M.A. Reptilian Diversity in Clarin River, Misamis Occidental, Philippines. J. Multidiscip. Stud. 2018, 7, 224–236. [Google Scholar]
  78. Labajo-Villantes, Y.; Hingco, J.T.; Manapsal, M.A.M. Species Richness and Endemism of Herpetofauna in Kapatagan Watershed, Philippines. J. Multidiscip. Studies. 2015, 4, 153–175. [Google Scholar]
  79. Mapi-ot, E.F.; Bendoy, C.P.; Palacio, M.M.D.S. Species richness and endemism of amphibians along the riparian system of Clarin River, Misamis Occidental, Philippines. J. Multidiscip. Studies. 2015, 4, 86–107. [Google Scholar] [CrossRef]
  80. Medina, M.N.D.; Cabras, A.A.; Ponce, R.G. List of Threatened Fauna in Mt. Hamiguitan Range Wildlife Sanctuary, Davao Oriental, Mindanao Island, Philippines. Asian J. Biodivers. 2019, 10, 14–25. [Google Scholar] [CrossRef]
  81. Mohagan, A.B.; Nuñeza, O.M.; Alcala, A.C.; Escarlos, J.A., Jr.; Gracia, A.G., Jr.; Selpa, E.C.T.; Baguhin, L.J.B.; Coritico, F.P.; Amoroso, V.B. Species richness and endemism of Reptilian Fauna in four Long-Term Ecological Research sites in Mindanao, Philippines. Biodivers. J. 2019, 10, 237–248. [Google Scholar] [CrossRef]
  82. Mohagan, A.B.; Nuñeza, O.M.; Diesmos, A.C.; Escarlos, J.A., Jr.; Gracia, A.G., Jr.; Selpa, E.C.T.; Baguhin, L.J.B.; Coritico, F.P.; Amoroso, V.B. Anuran Species Richness and Endemism in Four Long-Term Ecological Research Sites in Mindanao, Philippines. Asian J. Conserv. Biol. 2018, 7, 83–91. [Google Scholar]
  83. Nuñeza, O.M.; Ates, F.B.; Alicante, A.A.; Calizo-Enguito, M.R.; Toledo-Bruno, A.G.; Labajo, Y.I.; Dejarme, S.M. Vertebrate Faunal Diversity and Relevant Interrelationships of Critical Resources in Mt. Malindang; SEARCA: Laguna, Philippines, 2006; pp. 37–65. [Google Scholar]
  84. Nuñeza, O.M.; Calizo-Enguito, M.R.; Labajo-Villantes, Y.; Ponce, A.G. Species richness and endemism of cave herpetofauna in Northern Mindanao, Philippines. Extrem. Life Biospeology Astrobiol. 2015, 7, 10–24. [Google Scholar]
  85. Obeña, R.D.R.; Tolentino, P.J.S.; Villanueva, E.L.C.; Fernandez, D.A.P.; Delos Angeles, M.D.; Buot, I.E., Jr. Flora and fauna inventory of limestone forests in Taft, Eastern Samar, Philippines. Thail. Nat. Hist. Mus. J. 2021, 15, 1–20. [Google Scholar]
  86. Patindol, T. Post Biological Assessment of Faunal Resources in The Samar Island Natural Park. Ann. Trop. Res. 2016, 38, 52–73. [Google Scholar] [CrossRef] [Green Version]
  87. Quibod, M.N.R.M.; Alcantara, K.N.L.; Bechayda, N.A.; Estropia, C.J.C.; Guntinas, J.B.; Obin, M.A.H.A.; Raymundo, R.M.; Soniega, E.P. Terrestrial vertebrates in modified landscapes in northeastern Mindanao, Philippines. J. Anim. Divers. 2021, 3, 72–85. [Google Scholar] [CrossRef]
  88. Relox, R.E.; Leano, E.P.; Bates-Camino, F.R.I.T.Z.I.E. Herpetofaunal endemism and diversity in tropical forests of Mt. Hamiguitan in the Philippines. Herpetol. Conserv. Biol. 2011, 6, 107–113. [Google Scholar]
  89. Salo, J.V.B.; Solania, C.L. Preliminary Survey and Diet Analysis of Anurans in The Riparian Zone of Calayagon Watershed, Agusan Del Norte, Philippines. J. Bioresour. Manag. 2022, 9, 2. [Google Scholar]
  90. Solania, C.L.; Fernandez-Gamalinda, E.V. Species composition and habitat association of anurans within water systems of Andanan Watershed, Agusan del Sur, Caraga Region, Philippines. Environ. Exp. Biol. 2018, 16, 159–168. [Google Scholar]
  91. Solania, C.L.; Cuadrado, J.T.; Galolo, A.R.V.; Gamalinda, E.F. Species Richness and Community Structure of Amphibians and Reptiles in Andanan Watershed Forest Reserve, Caraga Region, Philippines. Biodivers. J. 2021, 12, 673–694. [Google Scholar] [CrossRef]
  92. Sularte, R.P.; Boyles, L.Z.; Calomot, N.H.; Demetillo, M.T.; Ombat, L.A.; Ngilangil, M.C.; Binag, G.M. Species distribution and abundance of amphibians in two vegetation types of Agusan Marsh, Philippines. Adv. Environ. Sci. 2015, 7, 20–34. [Google Scholar]
  93. Supsup, C.E.; Guinto, F.M.; Redoblado, B.R.; Gomez, R.S. Amphibians and reptiles from the Mt. Hamiguitan Range of eastern Mindanao Island, Philippines: New distribution records. Check List 2017, 13, 2121. [Google Scholar] [CrossRef] [Green Version]
  94. Toledo-Bruno, A.G.; Macas, D.G.; Buenavista, D.P.; Medina, M.A.P.; Forten, R.R.C. Amphibian and reptile diversity in Mt. Kalatungan Range Natural Park, Philippines. Environ. Exp. Biol. 2017, 15, 127–135. [Google Scholar] [CrossRef]
  95. Venturina, R.E.L.; Del Prado, Y.L.C.; Kamir, R.A.C.; Balmores, M.N.; Diesmos, A.C. A revised checklist of amphibians and reptiles in Camiguin Sur, Misamis Oriental, Mindaanao, Philippines. Asian Herpetol. Res. 2020, 11, 28–43. [Google Scholar]
Conservation 03 00025 g001 550
Figure 1. Map of the Mindanao faunal region (outlined in red) (hereafter ‘MFR’).
Figure 1. Map of the Mindanao faunal region (outlined in red) (hereafter ‘MFR’).
Conservation 03 00025 g001
Conservation 03 00025 g002 550
Figure 2. Annual trends in the number (a) and average study (b) of amphibian and reptile research published in journals between 2000 and 2022, compared to other taxonomic groups. The broken lines indicate the average number of studies per year for birds (mean = 1.62) and mammals (mean = 1.30). Note: Amp-co-cumulative trend for amphibians; Rept-co-cumulative trend for reptiles.
Figure 2. Annual trends in the number (a) and average study (b) of amphibian and reptile research published in journals between 2000 and 2022, compared to other taxonomic groups. The broken lines indicate the average number of studies per year for birds (mean = 1.62) and mammals (mean = 1.30). Note: Amp-co-cumulative trend for amphibians; Rept-co-cumulative trend for reptiles.
Conservation 03 00025 g002
Conservation 03 00025 g003 550
Figure 3. Comparison of Species Research Effort Allocation (SREA) between the endemism and conservation status of amphibians and reptiles. Whiskers represent SD values. The broken lines indicate the mean SREA for all birds (SREA = 0.28) and mammals (SREA = 0.20).
Figure 3. Comparison of Species Research Effort Allocation (SREA) between the endemism and conservation status of amphibians and reptiles. Whiskers represent SD values. The broken lines indicate the mean SREA for all birds (SREA = 0.28) and mammals (SREA = 0.20).
Conservation 03 00025 g003
Conservation 03 00025 g004 550
Figure 4. Distribution and proportion of endemic and threatened amphibian and reptile species (a). Sankey plot showing the distribution of threats according to taxonomic group, endemism, and threatened categories (b).
Figure 4. Distribution and proportion of endemic and threatened amphibian and reptile species (a). Sankey plot showing the distribution of threats according to taxonomic group, endemism, and threatened categories (b).
Conservation 03 00025 g004
Conservation 03 00025 g005 550
Figure 5. Comparison of species threat index (STI) between the endemism and conservation status of amphibians and reptiles. Whiskers represent SD values. Broken lines indicate mean STI for all birds (STI = 0.12) and mammals (STI = 0.27).
Figure 5. Comparison of species threat index (STI) between the endemism and conservation status of amphibians and reptiles. Whiskers represent SD values. Broken lines indicate mean STI for all birds (STI = 0.12) and mammals (STI = 0.27).
Conservation 03 00025 g005
Conservation 03 00025 g006 550
Figure 6. Species occurrence and distances (km) of amphibians (a) and reptiles (b) from different sites in MFR. The dots represent the presence-only distribution of species recorded based on the literature. Proportion of amphibians and reptiles recorded across key biodiversity sites in Mindanao faunal region (c).
Figure 6. Species occurrence and distances (km) of amphibians (a) and reptiles (b) from different sites in MFR. The dots represent the presence-only distribution of species recorded based on the literature. Proportion of amphibians and reptiles recorded across key biodiversity sites in Mindanao faunal region (c).
Conservation 03 00025 g006
Table
Table 1. Results of generalized linear mixed modelling (GLMM) predicting the relationship of species endemism and conservation status, and traits and threats to research efforts toward herpetofauna species.
Table 1. Results of generalized linear mixed modelling (GLMM) predicting the relationship of species endemism and conservation status, and traits and threats to research efforts toward herpetofauna species.
(A)
All Herpetofauna
VariablesβSEzp
(Intercept)2.390.20311.758<0.001
Threatened—Non threatened–0.6460.077–8.42<0.001
Philippine-endemic—Non-endemic0.4170.0488.69<0.001
Body size (log10)0.2730.0644.256<0.001
Species Threat Index (STI)–0.020.116–0.1720.863
(B)
Amphibians
(Intercept)1.9610.355.604<0.001
Threatened—Non threatened–1.4240.16–8.916<0.001
Philippine-endemic—Non-endemic0.8580.08110.614<0.001
Body size (log10)0.5440.1523.591<0.001
Species Threat Index (STI)–0.3550.158–2.2430.025
(C)
Reptiles
(Intercept)2.4270.2529.641<0.001
Threatened—Non threatened–0.3510.092–3.811<0.001
Philippine-endemic—Non-endemic0.1730.0612.8210.005
Body size (log10)0.2930.074.2<0.001
Species Threat Index (STI)0.1990.1791.1090.267
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Abdullah, S.S.; Dela Cruz, K.C.; Casim, L.F.; Agduma, A.R.; Tanalgo, K.C. Leaping Forward or Crawling Backward? Efforts and Biases in Amphibian and Reptile Research on a Megadiverse Faunal Region in the Philippines. Conservation 2023, 3, 363-378. https://doi.org/10.3390/conservation3030025

AMA Style

Abdullah SS, Dela Cruz KC, Casim LF, Agduma AR, Tanalgo KC. Leaping Forward or Crawling Backward? Efforts and Biases in Amphibian and Reptile Research on a Megadiverse Faunal Region in the Philippines. Conservation. 2023; 3(3):363-378. https://doi.org/10.3390/conservation3030025

Chicago/Turabian Style

Abdullah, Sumaira S., Kier Celestial Dela Cruz, Lothy F. Casim, Angelo Rellama Agduma, and Krizler Cejuela Tanalgo. 2023. "Leaping Forward or Crawling Backward? Efforts and Biases in Amphibian and Reptile Research on a Megadiverse Faunal Region in the Philippines" Conservation 3, no. 3: 363-378. https://doi.org/10.3390/conservation3030025

Article Metrics

Back to TopTop