Review Article
Print
Review Article
Amphibian fauna of Pakistan with notes on future prospects of research and conservation
expand article infoMuhammad Rais, Waseem Ahmed, Anum Sajjad§, Ayesha Akram, Muhammad Saeed, Hannan Nasib Hamid, Aamina Abid
‡ Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, Pakistan
§ International Islamic University, Islamabad, Pakistan
Open Access

Abstract

Research on amphibians and their conservation have gained worldwide attention, as the group includes the highest number of threatened and Data Deficient species when compared to other vertebrates. However, amphibians have long been neglected in wildlife conservation, management decisions, policy making, and research agendas in Pakistan. In this paper, an annotated checklist of the 21 amphibian species of Pakistan, a key to their identification, and detailed discussions on variation in species, including the genera Minervarya and Sphaerotheca, are provided. We found a statistically significant difference in the morphometric measurements of males but non-significant difference in the females of the two forms (rusty dorsum and dotted dorsum) of S. maskeyi. Some genera, such as Microhyla, Uperodon, Minervarya, Allopaa, Chrysopaa, Euphlyctis, Nanorana, and Sphaerotheca, in Pakistan are in need of additional data for molecular and morphological comparisons with taxa in other South Asian countries. The predicaments of amphibian research in Pakistan are discussed, gaps identified, and suggestions are made. Although the occurrence of chytrid fungus in Pakistan is predicted of low likelihood, a lack of data merits studying the prevalence of the fungus, particularly in the northern regions of the country which exhibit complex and dynamic ecosystems. It is recommended that systematic and coordinated surveys are conducted throughout the country to build a database of species occurrences and distributions. Additionally, the monitoring of wild populations and threat mitigation, as well as appropriate legislation, are suggested as long-term measures. By adopting an inclusive wildlife conservation approach in Pakistan, amphibians could be integrated into wildlife conservation and management efforts.

Keywords

Black-spined toad, Data Deficient, chytrid, endemism, extinction, inclusive conservation, intrinsic value, South Asia

Introduction

Amphibians are bioindicators of an ecosystem’s health and may also serve as a biological control of crop and forest pests (Attademo et al. 2005; Kanagavel et al. 2017). Additionally, various important compounds have also been extracted from their skin and eggs for medical applications (Erspamer 1971; Clarke 1997). Amphibians are sometimes kept as pets (Gerson 2012) and are also a source of food (protein) for people in many regions of the world (Marineros 2007). The number of currently described amphibian species is 8378 (Frost 2021).

The First Herpetological Congress, organized in 1989, presented alarming findings about the decline in amphibian populations which was presumed to have started in the early 1970s in the United States, certain Central American countries, and in northeastern Australia (Czechura and Ingram 1990; Drost and Fellers 1996; Burrowes et al. 2004). Amphibians include the highest number of Data Deficient species (>1500 species) (Morais et al. 2013) and the highest percentage (>40 %) of threatened species among all vertebrate groups. Bishop et al. (2012) categorized threats to amphibians into two groups. The first group of threats included habitat destruction and fragmentation, exotic invasive species, and over-exploitation. The second group, which is more poorly understood, includes the threats of infectious diseases and global climate change. Approximately 700 amphibian species are known to have been affected globally by the chytrid fungus, Batrachochytrium dendrobatidis. This fungus has extirpated about 90 amphibian species and has caused population declines of over 500 species (Rosenblum et al. 2010; Lips 2016; Scheele et al. 2019).

This paper provides an annotated checklist of the 21 amphibian species of Pakistan and keys to their identification. The predicaments of amphibian research in Pakistan are discussed and knowledge gaps identified. Suggestions are made on how to proceed with research and conservation of amphibians in the country.

Materials and methods

The available historical as well as recent literature on the amphibians of Pakistan was critically reviewed. We collected data on the morphology of 10 amphibian species (N = 158) (Suppl. material 1, Table S1) beginning in 2015 from the areas of Rawalpindi, Islamabad, and Gilgit-Baltistan. We used published literature (Murray 1884; Khan and Tasnim 1989; Auffenberg and Rehman 1997; Dutta 1997; Stöck et al. 1999; Khan 2006; Dufresnes et al. 2019; Ali et al. 2020) on other species in the development of the identification keys.

We studied morphological differentiation of the two forms of Sphaerotheca maskeyi: uniform rusty-colored dorsum (n = 9, Fig. 3F) and dorsum olive with dotted pattern (n = 29, Fig. 3E). We performed a principal components analysis (PCA) on 23 morphometric measurements separately on males and females (Borzée et al. 2013) in XLSTAT to reduce the studied measurements into fewer significant variables (r > 0.90) (see variable 1–23 in Suppl. material 1, Table S2a, S2b). Principal components analysis (PCA) is a variable-reduction technique that shares many similarities to exploratory factor analysis. The aim is to reduce a larger set of variables into a smaller set of “artificial” variables, called “principal components”, which account for most of the variance in the original variables. We then conducted a multivariate generalized linear model (one-way MANOVA) to examine if there were any differences (a = 0.05) between categorical predictor variables in the two forms (in males and females separately) on continuous response variables (obtained after PCA with r > 0.90) in SPSS 22.

Results

There are 21 species of amphibians (order Anura) in Pakistan, belonging to four families: Bufonidae Gray, 1825, Megophryidae Bonaparte, 1850, Microhylidae Günther, 1858, and Dicroglossidae Dubois, 1987. The identification keys of amphibian families and species of Pakistan are as follows:

Key to amphibian families of Pakistan

1 Parotid glands present Bufonidae
Parotid glands absent 2
2 Pupil vertical 3
Pupil horizontal Dicroglossidae
3 Head and mouth narrow, body smooth with few smooth small tubercles Microhylidae
Head and mouth broad, body heavily warty, a distinct elevated post orbital ridge Megophryidae

Key to species

Bufonidae

1 Head with cranial crest 2
Head without cranial crest 3
2 Only supraorbital crest, tympanum indistinct Duttaphrynus himalayanus (Günther, 1864) (Fig. 1C)
Supraorbital, canthal, post orbital, orbitotympanic crest, tympanum distinct Duttaphrynus melanostictus (Schneider, 1799) (Fig. 2A)
3 Interorbital space is smaller or nearly equal to the internarial space 4
Interorbital space a little wider than the upper eyelid 6
4 Parotid glands are inconspicuous, subarticular tubercles single under toes; often double on first, second, and, in some, third finger Bufotes baturae (Stöck et al., 1999) (Fig. 1B)
Parotid glands conspicuous, toes with double subarticular tubercles 5
5 Dorsal pattern of longitudinal stripes, three on each side Bufotes latastii (Boulenger, 1882) (Fig. 1D)
Dorsum gray, with greenish spotting, a dark blotch on the upper eyelid Bufotes surdus (Boulenger, 1891) (Fig. 1A)
6 Tibial gland absent 7
Tibial gland present, tarsal fold indicated by weak spinulated line Duttaphrynus stomaticus (Lütken, 1864) (Fig. 2C)
7 Dorsum uniformly olive, interorbital space slightly concave, parotids depressed Duttaphrynus olivaceus (Blanford, 1874) (Fig. 2B)
Dorsum with green pattern 8
8 Dorsum with scattered green spots Bufotes zugmayeri (Eiselt and Schmidtler, 1973) (Fig. 1E)
Dorsum heavily green with occasional light spots, Dorsal tubercles are not so prominent, rather they are flat Bufotes pseudoraddei (Mertens, 1971) (Fig. 1F)
Figure 1. 

A Iranian Toad (Bufotes surdus) B Batura Toad (Bufotes baturae) C Himalayan Toad (Duttaphrynus himalayanus) D Ladakh Toad (Bufotes latastii) E Baloch Green Toad (Bufotes zugmayeri) F Swat Green Toad (Bufotes pseudoraddei). Photographers: Dr Spartak Litvinchuk (A–D, F); Muhammad Sharif Khan (E).

Figure 2. 

A Asian Common Toad or Black-spined Toad (Duttaphrynus melanostictus)B Olive Toad (Duttaphrynus olivaceus) C Indus Valley Toad (Duttaphrynus stomaticus) D Kashmir Torrent Frog (Allopaa barmoachensis) E Hazara Torrent Frog (Allopaa hazarensis) F Indus Valley Bull Frog (Hoplobatrachus tigerinus). Photographers: Dr Muhammad Rais (A, C, E); Dr Spartak Litvinchuk (B); Muhammad Sharif Khan (D); Janis Czurda (F).

Figure 3. 

A Skittering Frog (Euphlyctis cyanophlyctis) B Skittering Frog (Euphlyctis kalasgramensis) C Pierrei’s Cricket Frog (Minervarya pierrei) D Murree Hills Frog (Nanorana vicina) E, F Burrowing Frog (Sphaerotheca maskeyi). Photographers: Dr Muhammad Rais (A, C–F); Waqas Ali (B).

Megophryidae

1 Head and mouth broad, body heavily warty, a distinct elevated post orbital tuberculate ridge, tympanum indistinct Scutiger occidentalis (Dubois, 1978) (Fig. 4B)

Microhylidae

1 Tongue elliptical, adult <30 mm, body dorsum with elongated, light brown, large, branched blotch Microhyla nilphamariensis (Howlader et al., 2015a) (Fig. 4C)
Tongue oval, adult 50–60 mm, dorsum with brown reticulation Uperodon systoma (Schneider, 1799) (Fig. 4D)
Figure 4. 

A Karez Frog (Chrysopaa sternosignata) B Ladakh Pelobatid Toad (Scutiger occidentalis) C Ant Frog (Microhyla nilphamariensis) D Marbled Balloon Frog (Uperodon systoma). Photographers: Dr Muhammad Rais (A); Dr Matthias Stöck (B); Chaitanya Shukla (C); Peter Janzen (D).

Dicroglossidae

1 Tympanum indistinct, body dorsum brownish, smooth with a few tubercles on flanks, dark bars on forearm, thighs and shank Nanorana vicina (Stoliczka, 1872) (Fig. 3D)
Tympanum distinct 2
2 Toes partially webbed, snout pointed Minervarya pierrei (Dubois, 1975) (Fig. 3C)
Toes completely webbed 3
3 Inner metatarsal tubercle shovel-shaped Sphaerotheca maskeyi (Schleich and Anders 1998) (Fig. 3 EF)
Inner metatarsal tubercle elongate 4
4 Body dorsum with longitudinal folds and mid-dorsal line Hoplobatrachus tigerinus (Daudin, 1802) (Fig. 2F)
Body dorsum without longitudinal folds 5
5 Body pustules large, multispinulate, belly spiny Chrysopaa sternosignata (Murray, 1885) (Fig. 4A)
Body pustules small, unispinulate, belly spineless 6
6 Nuptial spines absent 7
Nuptial spines present 8
7 Ventral body spotted, relative length of fingers 4<2<1<3 Euphlyctis cyanophlyctis (Schneider, 1799) (Fig. 3A)
Ventral body whitish, relative length of fingers 1=2 < 4< 3 Euphlyctis kalasgramensis (Howlader et al., 2015b) (Fig. 3B)
8 Spinules on pustules Allopaa barmoachensis (Khan and Tasnim, 1989) (Fig. 2D)
Spinules on longitudinal ridges Allopaa hazarensis (Dubois and Khan, 1979) (Fig. 2E)

Statistical comparisons of Sphaerotheca populations

Of the studied 23 morphometric measurements in S. maskeyi, we obtained from our PCA 10 and eight significant variables (r > 0.90) in males having uniform rusty-colored dorsum and having dotted pattern, respectively. We obtained 10 and one significant variables (r > 0.90) in females, respectively. Eigen value, variability (%), cumulative variability (%), and factor loadings of the 23 morphometric measurements are given Table 1.

The multivariate generalized linear model revealed statistically significant difference (F(1, 11) = 1876.60, P = 0.018; Wilk’s Λ = 0.00, partial η2 = 0.97) in the morphometric measurements of males but non-significant in the females (F(13, 11) = 0.944, P = 0.532; Wilk’s Λ = 0.556, partial η2 = 0.444) of the two forms of S. maskeyi.

Table 1.

Eigen value, variability (%), cumulative variability (%) and factor loadings of the 23 morphometric measurements of the two forms (uniform rusty-colored dorsum and dorsum olive with dotted pattern) of Sphaerotheca maskeyi. The factor loadings with absolute correlation values greater than 0.90 were considered significant (in bold).

Male Uniform rusty-colored dorsum Dorsum olive with dotted pattern
F1 F2 F3 F1 F2 F3
Eigenvalue 10.112 7.146 5.742 14.476 2.872 1.934
Variability (%) 43.964 31.069 24.966 62.940 12.486 8.409
Cumulative % 43.964 75.034 100.000 62.940 75.425 83.835
Factor loadings
Morphometric measurements F1 F2 F3 F1 F2 F3
Snout–vent length 0.273 −0.113 0.955 0.864 0.383 −0.170
Head width −0.195 0.936 0.293 0.977 0.066 −0.142
Head length −0.224 0.845 0.486 0.984 0.014 −0.058
Distance between nostrils 0.970 −0.213 −0.114 0.736 0.333 0.383
Width of upper eyelid 0.613 0.232 −0.755 0.764 −0.522 0.237
Interorbital distance 0.868 0.056 −0.493 0.268 −0.174 0.916
Distance from the back of the mandible to the nostril 0.003 0.919 0.393 0.754 0.521 −0.286
Distance from the back of the mandible to the front of the eye 0.070 0.856 −0.513 0.826 −0.300 −0.059
Distance from the back of the mandible to the back of the eye −0.488 0.677 −0.552 0.853 −0.465 −0.174
Distance between the front of the eyes 0.811 −0.580 0.072 0.770 0.263 −0.360
Distance between back of the eyes 0.964 0.005 −0.266 0.286 0.603 0.624
Distance from the front of the eye to the nostril 0.901 0.430 −0.054 0.827 0.106 0.030
Eye length −0.924 0.384 0.006 0.953 −0.165 −0.101
Distance from the nostril to the tip of the snout −0.846 −0.158 −0.509 0.902 −0.365 −0.201
Distance from the front of the eye to the tip of the snout 0.941 −0.218 −0.261 0.950 0.084 0.064
Greatest tympanum diameter −0.660 −0.633 −0.404 0.915 −0.136 0.165
Distance from tympanum to the back of the eye −0.107 0.468 −0.877 0.807 −0.201 0.176
Forelimb length −0.641 −0.763 −0.086 0.874 −0.257 −0.002
Hand length 0.987 −0.005 0.160 0.745 0.170 0.065
Femur length 0.639 0.627 −0.446 0.829 −0.006 −0.187
Shank length −0.267 0.959 −0.095 0.783 0.088 0.216
Length of tarsus and foot 0.685 0.293 0.666 0.086 0.926 −0.074
Foot length −0.033 0.252 0.967 0.731 0.313 −0.012
Female Uniform rusty−colored dorsum Dorsum olive with dotted pattern
F1 F2 F3 F1 F2 F3
Eigenvalue 12.044 5.877 4.595 12.166 4.445 2.062
Variability (%) 52.364 25.552 19.979 52.895 19.325 8.967
Cumulative % 52.364 77.916 97.895 52.895 72.221 81.188
Factor loadings
Morphometric measurements F1 F2 F3 F1 F2 F3
Snout–vent length 0.804 0.364 0.471 0.245 0.144 −0.476
Head width 0.973 0.229 0.006 0.895 0.154 0.078
Head length 0.785 −0.164 −0.597 0.774 0.451 0.368
Distance between nostrils 0.584 0.791 0.171 0.827 0.029 −0.143
Width of upper eyelid 0.576 −0.402 0.709 0.833 −0.384 −0.190
Interorbital distance −0.244 0.127 0.961 0.603 0.095 −0.648
Distance from the back of the mandible to the nostril 0.790 0.320 −0.476 0.659 0.097 0.673
Distance from the back of the mandible to the front of the eye 0.766 −0.614 −0.190 0.786 0.160 0.412
Distance from the back of the mandible to the back of the eye 0.860 −0.509 −0.030 0.881 −0.332 0.194
Distance between the front of the eyes 0.124 0.987 −0.072 0.401 0.807 −0.124
Distance between back of the eyes −0.919 0.285 0.272 −0.045 0.897 −0.309
Distance from the front of the eye to the nostril 0.381 0.925 −0.014 0.546 0.575 0.014
Eye length 0.999 −0.034 −0.015 0.826 −0.479 0.196
Distance from the nostril to the tip of the snout 0.992 −0.083 0.094 0.879 −0.333 −0.108
Distance from the front of the eye to the tip of the snout 0.188 0.488 0.842 0.743 0.370 −0.044
Greatest tympanum diameter 0.993 0.066 0.093 0.870 −0.436 −0.032
Distance from tympanum to the back of the eye 0.845 −0.533 0.035 0.858 −0.295 −0.274
Forelimb length 0.910 −0.288 0.297 0.877 −0.431 0.028
Hand length 0.435 0.865 0.221 0.860 0.217 −0.108
Femur length 0.219 −0.156 0.961 0.731 0.154 −0.382
Shank length 0.964 −0.263 −0.011 0.804 0.277 −0.130
Length of tarsus and foot 0.051 0.606 −0.501 −0.191 0.908 0.159
Foot length 0.657 0.623 −0.422 0.672 0.442 0.344

Discussion

A number of researchers have documented the amphibian fauna of Pakistan; Pratihar et al. (2014) reported 25 species, Khan (2014) 24 species, Sarwar et al. (2016) 21 species, and Ali et al. (2018) 26 species, but these studies did not arise from any systematic survey of the country or regions of the country, nor did they employ a molecular taxonomic approach. To date, much of the difficult terrain, especially in the high-altitude northern and arid western mountains of the country, has remained unexplored.

The true toads of Pakistan are represented by two genera: Duttaphrynus Frost et al., 2006 and Bufotes Rafinesque, 1815. Duttaphrynus is characterized by prominent ridges on the head, while Bufotes lacks such ridges but bears conspicuous pattern of irregularly shaped, darker, green or greenish-olive spots.

Considering other taxa, Faiz et al. (2018) reported three amphibians, including Allopaa barmoachensis from Toli Pir National Park, Pakistan. Dubois (1992) considered A. barmoachensis synonymous with Allopaa hazarensis, but Khan (2004) regarded the two as distinct. However, Ohler and Dubois (2006) reiterated that the species is conspecific with A. hazarensis. As no molecular data exist to separate the two species, there is no evidence for separation. The species complex of Euphlyctis also needs detailed study. Dutta (1997) provided a record of Euphlyctis hexadactylus from Pakistan which needs confirmation. Murray (1884) reported and described Tomopterna strachani from Sindh, Pakistan, and Khan (2006) reported the species as Sphaerotheca breviceps. Dubois (1999) suggested that S. breviceps is a small-sized species based on the study of the name-bearing specimens. For the large-sized species of South Asia, he suggested that the names Rana variegata (Gravenhorst, 1829); Pyxicephalus fodiens (Jerdon, 1853); Pyxicephalus pluvialis (Jerdon, 1853); Sphaerotheca strigata (Günther, 1859); Rana dobsonii (Boulenger, 1882); Tomopterna strachani (Murray, 1884); Rana leuchorhynchus (Rao, 1937); and Rana swani (Myers and Leviton, 1956) are available. Dubois (1999) also regarded Tomopterna maskeyi to be a provisional synonym of these large-size taxa. Recently, Deepak et al. (2020) provided distribution records for Sphaerotheca pashchima from India and morphological descriptions of their samples of S. pashchima match samples collected for the present study. Deepak et al. (2020) reported similar morphological variation in S. pashchima among the samples collected from India. Khatiwada et al. (2021) demonstrated high similarity between topotypical material of S. maskeyi with name-bearing types of S. pashchima and considered the later name a synonym of T. maskeyi, valid as S. maskeyi. Molecular identification of our samples also confirms their identity as S. maskeyi (see Akram et al. 2021). Therefore, we conclude that Sphaerotheca maskeyi occurs in Pakistan, and not Sphaerotheca breviceps as reported by Murray (1884) and Khan (2006).

Borthakur et al. (2007) studied cricket frog species in Assam, northwest India (Fejervarya nepalensis, F. pierrei Dubois, 1975, F. syhadrensis Annandale, 1919, and F. teraiensis Dubois, 1984), which have been assigned to other genera in Nepal by Ahmed et al. (2009) and Shah and Tiwari (2004). Rawat et al. (2020) reported Minervarya species from extreme southwestern Nepal in the Shuklaphanta National Park. Molecular identification of our samples confirms their identity as Minervarya pierrei (see Akram et al. 2021). Two distinct forms of Minervarya are known, one with a mid-dorsal stripe and another without it. Dubois (1974) has reported such variation. Hence, we suggest conducting country-wide surveys and use a molecular approach to confirm presence of other species of Euphlyctis, Sphaerotheca, and Minervarya from Pakistan.

The inclusion of Uperodon systoma in the list of amphibians of Pakistan is based on two reports. Baig and Gvozdik (1998) reported this species from a torrent stream in the Shakarparian Hills, Islamabad Capital Territory (ICT), and Masroor (2011) recorded this species from a subtropical, semi-evergreen forest in Margalla Hills National Park (ICT). We consider U. systoma to be very rare in Pakistan. No historical quantitative data has been found to date. Some species assessed as Least Concern by the IUCN, such as U. systoma, are considered rare in Pakistan, compared to elsewhere in their global range. Hence, we caution the use of global conservation status for the amphibian species that occur within Pakistan.

Future prospects in amphibian research and conservation in Pakistan

Pakistan represents the westernmost limit of the geographic range of Duttaphrynus melanostictus. This species has been introduced outside its natural range into many parts of the world, and in these places it is considered a nuisance predator, a potential disease vector, and the cause of many other ecological problems (Labisko et al. 2015; Piludu et al. 2015). Studying the ecology and biology of D. melanostictus in its native range could help manage this species in Pakistan as well as elsewhere.

The chytrid fungus Batrachochytrium dendrobatidis affects amphibians worldwide. The likelihood of this fungus occurring in Pakistan is predicted to be low (<30%) (Olson et al. 2013; Rodder et al. 2010) by models which did not include samples of anurans from Pakistan. This lack of data may produce inaccurate results in models, which use no direct observational data. Therefore, the study of the prevalence of chytrid fungus in countries such as Pakistan is important to fill in these data gaps. Furthermore, the northern regions of Pakistan have complex and dynamic ecosystems (Roberts 1997) and therefore more diverse amphibian assemblages. Diversity of amphibians in an ecosystem has been linked to increased probability of the introduction and spread of chytrid fungus (Olson et al. 2013). This correlation with amphibian diversity and the lack of data in the Middle East and South Asia creates an urgency to perform risk assessments on amphibian communities in these regions.

There is also a dire need to change social attitudes towards amphibians in our society. This could be achieved by initiating community awareness by outreach, school, and citizen-science programs. While designing research projects, special attention should be given to include components of outreach. For instance, people working in agroecosystems can organize field activities with farmers and local communities. Likewise, the ongoing 10 Billion Tree Tsunami project by the Ministry of Climate Change, Government of Pakistan, should integrate consideration for herpetofauna species, particularly anuran species such as Allopaa hazarensis and Allopaa barmoachensis, which are endemic to forested montane wetlands. The development of android applications and websites could help reach out to the public. This, however, would be limited to those people who have access to the internet, but their participation would inevitably enhance the documentation of species occurrence and distribution records in the country. Collection and archiving quantitative data on anuran abundance would also help determine the current conservation status of our anuran species.

We suggest setting research priorities and to devise strategy for the conservation of amphibians of Pakistan when manageable anthropogenic threats exist, such as habitat destruction, urbanization, pollution, and unsustainable utilization, so that amphibian populations can be better controlled by utilizing less financial, administrative, and human resources. This can be achieved through short-, medium-, and long-term actions. Short-term actions could include the establishment of a network or people currently engaged in amphibian related research. A conservation assessment and management plan workshop should be organized wherein experts and researchers could provide their opinions and draft recommendations for medium- and long-term actions.

A medium-term action plan may include carrying out systematic and coordinated surveys throughout the country to establish a database on occurrence and distribution of species and the identification of their threats. It is recommended to use modern taxonomic tools, such as DNA barcoding, to determine taxonomy and initiate research on phylogenetic affinities, biogeography systematics, especially on endemic species. This approach can expect to yield additional amphibian species as a result. Some genera, such as Microhyla Tschudi, 1838, Uperodon Duméril & Bibron, 1841, Minervarya Dubois et al., 2001), Allopaa, Chrysopaa Ohler & Dubois, 2006, Euphlyctis Fitzinger, 1843, Nanorana, and Sphaerotheca Günther, 1896, which occur in Pakistan need additonal data for molecular taxonomy and detailed comparisons with taxa in other South Asian countries.

Long-term actions would entail monitoring of amphibian populations, threat mitigation, and appropriate legislation. Amphibians have been excluded from all current legislative and policy decisions of the country. The National Climate Change Policy (GoP 2012), the Pakistan National Biodiversity Strategy and Action Plan (GoP 2015), the Biodiversity Action Plan of Pakistan (GoP 2000), and the Pakistan National Conservation Strategy (GoP 1992) do not currently support the need to carry out research and conserve amphibians. Likewise, amphibians are not protected under any law (Shafiq 2005). Hence, the legislation pertaining to threatened and endemic species needs to be updated, particularly in need of revision is Schedule III, which includes protected species, of provincial and federal wildlife laws as well as the CITES appendices.

Wildlife conservation projects in Pakistan mainly focus on carnivores, ungulates, and birds. Shehzad et al. (2012) reported the occurrence of Nanorana vicina in the diet of Prionailurus bengalensis in Ayobia National Park, Khyber Pakhtunkhwa, Pakistan. Such studies usually lack the mandate of investigating whether a particular food item was eaten directly or through an alternate dietary item. Whatever the case, this explicitly signifies the role of amphibians in the food chain and could be used as an impetus to incorporate amphibians in such research projects and conservation programs. Therefore, it should be proposed to adopt an inclusive wildlife conservation approach in Pakistan. The approach would advocate the integration of poorly documented taxa, such as amphibians, in wildlife conservation and management projects to enhance the significance of their existence and the intrinsic values of all wildlife species which would eventually ensure their continued survival.

Availability of data

The data underpinning the analysis reported in this paper are deposited in the Dryad Data Repository at Dryad (https://doi.org/10.5061/dryad.mkkwh7118).

Acknowledgements

We are thankful to Paul Freed (USA) for proofreading earlier drafts of this manuscript. We wish to thank Dr Don Driscoll, Deakin University, Australia and Dr. Spartak Litvinchuk, Russian Academy of Sciences for their valuable suggestions and Russell Gray, Science Advisor. Save Vietnam’s Wildlife for improving the text on amphibian infectious diseases. We owe a deep sense of gratitude to Amphibian Survival Alliance for financial assistance through Future Leaders in Amphibian Conservation Program (https://www.amphibians.org/what-we-do/acrs/future-leaders-award/).

References

  • Ahmed MF, Das A, Dutta SK (2009) Amphibians and Reptiles of Northeast India. A Photographic Guide. Aaranyak, Guwahati, India.
  • Akram A, Rais M, Lopez K, Tarvin RD, Saeed M, Bolnick DI, Cannatella DC (2021) An insight into molecular taxonomy of bufonids, microhylids and dicroglossid frogs: first genetic records from Pakistan. Ecology and Evolution. https://doi.org/10.1002/ece3.8134
  • Ali W, Javid A, Hussain A, Bukhari SM (2018) Diversity and habitat preferences of amphibians and reptiles in Pakistan: a review. Journal of Asia-Pacific Biodiversity 11(2): 173–187. https://doi.org/10.1016/j.japb.2018.01.009
  • Ali WA, Javid A, Hussain M, Hafeez-ur-Rehman M, Chaber AL, Hemmatzadeh F (2020) First record of Euphlyctis kalasgramensis (Anura: Dicroglossidae) from Punjab, Pakistan. Mitochondrial DNA, Part B 5(2): 1227–1232. https://doi.org/10.1080/23802359.2020.1731337
  • Annandale N (1919) The fauna of certain small streams in the Bombay Presidency: some frogs from streams in the Bombay Presidency. Records of the Indian Museum 16(1): 109–161. https://doi.org/10.1016/j.agee.2004.08.012
  • Attademo AM, Peltzer PM, Lajmanovich RC (2005) Amphibians occurring in soybean and implications for biological control in Argentina. Agriculture, Ecosystems & Environment 106(4): 389–394. https://doi.org/10.1016/j.agee.2004.08.012
  • Auffenberg W, Rehman H (1997) Geographic variation in Bufo stomaticus, with remarks on Bufo olivaceus: biogeographical and systematic implications. In: Mufti SA, Woods CA, Syed AH (Eds) Biodiversity of Pakistan. Pakistan Museum of Natural History, Islamabad – Florida, Museum of Natural History, Gainsville, 351–372.
  • Baig KJ, Gvozdik L (1998) Uperodon systoma Schneider: record of a new microhylid frog from Pakistan. Pakistan Journal of Zoology 30(2): 155–156.
  • Bishop PJ, Angulo A, Lewis JP, Moore RD, Rabb GB, Moreno JG (2012) The amphibian extinction crisis—what will it take to put the action into the amphibian conservation action plan? Surveys and Perspectives Integrating Environment and Society. Version. 5.2. https://journals.openedition.org/sapiens/1406 [accessed on 30 April 2019]
  • Bonaparte CLJL (1850) Conspectus Systematum. Herpetologiae et Amphibiologiae. Editio altera reformata. E. J. Brill, Lugdini Batavorum.
  • Borzée A, Park S, Kim A, Kim HT, Jang Y (2013) Morphometrics of two sympatric species of tree frogs in Korea: a morphological key for the critically endangered Hyla suweonensis in relation to H. japonica. Animal Cells and Systems 17(5): 348–356. https://doi.org/10.1080/19768354.2013.842931
  • Boulenger GA (1882) Catalogue of the Batrachia Salientia s. Ecaudata in the Collection of the British Museum. Second Edition. Taylor and Francis, London. https://doi.org/10.5962/bhl.title.8307
  • Burrowes PA, Joglar RL, Green DE (2004) Potential causes for amphibian declines in Puerto Rico. Herpetologica 60(2): 141–154. https://doi.org/10.1655/03-50
  • Clarke BT (1997) The natural history of amphibian skin secretions, their normal functioning and potential medical applications. Biological Reviews 72(3): 365–379. https://doi.org/10.1017/s0006323197005045
  • Czechura GV, Ingram GJ (1990) Taudactylus diurnus and the case of the disappearing frogs. Memoirs of the Queensland Museum 29(2): 361–365.
  • Deepak P, Dinesh KP, Prasad VK, Das A, Ashadevi JS (2020) Distribution status of the western burrowing frog, Sphaerotheca pashchima in India. Zootaxa 4894(1): 146–150. https://doi.org/10.11646/zootaxa.4894.1.10
  • Dubois A (1974) Liste commentée d’amphibiens récoltés au Népal. Bulletin du Muséum National d’Histoire Naturelle, Série 3, Zoologie 213: 341–411.
  • Dubois A (1975) Une nouveau complexe d’espèces jumelles distinguées par le chant: les grenouilles de Népal voisines de Rana limnocharis Boie (amphibiens, anoures). Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences 281: 1717–1720.
  • Dubois A (1978) Une espèce nouvelle de Scutiger Theobald 1868 de l’Himalaya occidental (Anura: Pelobatidae). Senckenbergiana Biologica 59: 163–171.
  • Dubois A (1984) Note préliminaire sur le groupe de Rana limnocharis Gravenhorst, 1829 (Amphibiens, Anoures). Alytes 3: 143–159.
  • Dubois A (1987) Miscellanea taxinomica batrachologica. Alytes 5: 7–95.
  • Dubois A (1999) South Asian Amphibia: a new frontier for taxonomists. Journal of South Asian Natural History 4: 1–11.
  • Dubois A, Khan MS (1979) A new species of frog (genus Rana, subgenus Paa) from northern Pakistan (Amphibia, Anura). Journal of Herpetology 13(4): 403–410. https://doi.org/10.2307/1563474
  • Dubois A, Ohler A, Biju SD (2001) A new genus and species of Ranidae (Amphibia, Anura) from south-western India. Alytes 19(2): 53–79.
  • Dufresnes C, Mazepa GO, Jablonski D, Oliveira RC, Wenseleers T, Shabanov DA, Auer M, Ernst R, Koch C, Ramírez-Chaves HE, Mulder KP, Simonovo E, Tiutenko A, Kryvokhyzhar D, Wennekes PL, Zinenko OI, Korshunov AV, Al-Johany AM, Peregontsev EA, Masroor R, Betto-Colliard C, Denoël M, Borkin LJ, Skorinov DV, Pasynkova RA, Mazanaeva LFJ, Rosanov M, Dubey S, Litvinchuk SN (2019) Fifteen shades of green: the evolution of Bufotes toads revisited. Molecular Phylogenetics and Evolution 141: 1–25. https://doi.org/10.1016/j.ympev.2019.106615
  • Duméril AMC, Bibron G (1841) Erpétologie Genérale ou Histoire Naturelle Complète des Reptiles. Librarie Enclyclopedique de Roret, Paris.
  • Dutta SK (1997) Amphibians of India and Sri Lanka (Checklist and Bibliography). Odyssey Publishing House, Bhubaneswar.
  • Eiselt J, Schmidtler JF (1973) Froschlurche aus dem Iran unter Berücksichtigung ausseriranischer Poplationsgruppen. Annalen des Naturhistorischen Museums in Wien 77: 181–243.
  • Faiz AH, Hassan MU, Bagaturov MF, Tariq G, Khan FM, Faiz LZ (2018) Status and distribution of amphibians in Tolipir National Park, Pakistan. Journal of Bioresource Management 5(1): 8–11. https://doi.org/10.35691/JBM.8102.0082
  • Fitzinger LJFJ (1843) Systema Reptilium. Fasciculus Primus. Braumüller et Seidel, Vienna.
  • Frost DRT, Grant J. Faivovich RH, Bain A, Haas CFB, Haddad RO, de Sá A, Channing M, Wilkinson SC, Donnellan CJ, Raxworthy JA, Campbell BL, Blotto PE, Moler RC, Drewes RA, Nussbaum JD, Lynch DM, Green JD, Wheeler WC (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1–370. https://doi.org/10.1206/0003-0090(2006)297[0001:TATOL]2.0.CO;2
  • Gerson H (2012) International trade in amphibians: a customs perspective. Alytes 29(1–4): 103–115.
  • GOP [Government of Pakistan] (1992) The Pakistan National Conservation Strategy. Environment and Urban Affairs Division, Government of Pakistan and Pakistan and International Union for Conservation of Nature and Natural Resources, Pakistan.
  • GOP [Government of Pakistan] (2012) National Climate Change Policy. Ministry of Climate Change, Islamabad, Pakistan.
  • GOP [Government of Pakistan] (2015) National Biodiversity Strategy and Action Plan. Minister for Climate Change Government of Pakistan, and International Union for Conservation of Nature and Natural Resources, Islamabad, Pakistan.
  • GOP [Government of Pakistan] (2000) Biodiversity Action Plan of Pakistan. Ministry of Environment Government of Pakistan, World Wide Fund for Nature, and Pakistan and International Union for Conservation of Nature and Natural Resources, Islamabad, Pakistan.
  • Gravenhorst JLC (1829) Deliciae Musei Zoologici Vratislaviensis. Fasciculus primus. Chelonios et Batrachia. Leopold Voss, Leipzig.
  • Gray JE (1825) A synopsis of the genera of reptiles and Amphibia, with a description of some new species. Annals of Philosophy (Series 2) 10: 193–217.
  • Günther ACLG (1864) The Reptiles of British India. Ray Society, London.
  • Günther ACLG (1896) Report on the collections of reptiles, batrachians and fishes made by Messrs Potanin and Berezowski in the Chinese provinces Kansu and Sze-chuen. Annuaire du Musée Zoologique de l’Academie Impériale des Sciences de St. Pétersbourg 1: 199–219.
  • Jerdon TC (1853) Catalogue of reptiles inhabiting the Peninsula of India. Journal of the Asiatic Society of Bengal 22: 522–534.
  • Kanagavel A, Parvathy S, Nirmal N, Divakar N, Raghavan R (2017) Do frogs really eat cardamom? Understanding the myth of crop damage by amphibians in the Western Ghats, India. Ambio 46(6): 695–705. https://doi.org/10.1007/s13280-017-0908-8
  • Khan MS (2004) Frogs of the genus Paa Dubois, 1992, of submontane regions of Pakistan. Bulletin of the Chicago Herpetological Society 39(3): 45–47.
  • Khan MS (2006) Amphibians and Reptiles of Pakistan. Krieger Publishing, Malabar, Florida.
  • Khan MS (2014) Conservation Biology of Amphibians of Asia. Amphibians of Pakistan and their conservation status. Heatwole HF, Das I (Eds) Natural History Publications. Kota Kinabula, Borneo.
  • Khan MS, Tasnim R (1989) A new frog of the genus Rana, subgenus Paa, from southwestern Azad Kashmir. Journal of Herpetology 23(4): 419–423. https://doi.org/10.2307/1564055
  • Khatiwada JR, Wang B, Zhao T, Xie F, Jiang J (2021) An integrative taxonomy of amphibians of Nepal: an updated status and distribution. Asian Herpetological. Research 12(1): 1–35. http://dx.doi.org/10.16373/j.cnki.ahr.200050
  • Labisko J, Maddock ST, Taylor ML, Chong-Seng L, Gower DJ, Wynne FJ, Wombwell E, Morel C, French GCA, Bunbury N, Bradfield KS (2015) Chytrid fungus (Batrachochytrium dendrobatidis) undetected in the two orders of Seychelles amphibians. Herpetological Review 46(1): 41–45.
  • Lütken CF (1864) [“1863”] Nogle ny Krybyr og Padder. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjøbenhavn (Serie 2) 4: 292–311.
  • Marineros LE (2007) El consumo de anfibios y reptiles entre los maya chortí de Copán. Yaxkin 23(1): 183–193.
  • Masroor R (2011) An annotated checklist of amphibians and reptiles of Margalla Hills National Park, Pakistan. Pakistan Journal of Zoology 43(6): 1041–1048.
  • Mertens R (1971) Die Amphibien und Reptilien West-Pakistans. Senckenbergiana Biologica 52(1): 7–15.
  • Morais AR, Siqueria MN, Lemes P, Maciel NM, Marcojr PD, Brito D (2013) Unraveling the conservation status of Data Deficient species. Biological Conservation 166(2013): 98–102. https://doi.org/10.1016/j.biocon.2013.06.010
  • Murray JA (1884) The Vertebrate Zoology of Sind: A Systematic Account, with descriptions of all the known species of mammals, birds, and reptiles inhabiting the province, observations on their habits, & c., tables of their geographical distribution in Persia, Balochistan, and Afghanistan, Punjab, North-West Provinces, and the Peninsula of India generally. Richardson & Co., London; Education Society’s Press, Bombay. https://doi.org/10.5962/bhl.title.57275
  • Ohler A, Dubois A (2006) Phylogenetic relationships and generic taxonomy of the tribe Paini (Amphibia, Anura, Ranidae, Dicroglossinae) with diagnoses of two new genera. Zoosystema 28(3): 769–784.
  • Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, Fishe MC (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS ONE 8(2): e56802. https://doi.org/10.1371/journal.pone.0056802
  • Piludu N, Dubos N, Rasafimanahaka JH, Razafindraibe P, Randrianantoandro JC, Jenkins RKB (2015) Distribution, threats and conservation of a critically endangered amphibian (Mantella aurantiaca) in eastern Madagascar. Herpetology Notes 8: 119–123.
  • Pratihar S, Clark HO, Dutta S, Khan MS, Patra BC, Ukuwela KDB, Das A, Pipeng L, Jianping J, Lewis JP, Pandey BN, Razzaque A, Hassapakis C, Deuti K, Das S (2014) Diversity and conservation of Amphibians in South and Southeast Asia. Sauria Berlin 36(1): 9–59.
  • Rao CRN (1937) On some new forms of Batrachia from S. India. Proceedings of the Indian Academy of Sciences, Section B 6(6): 387–427. https://doi.org/10.1007/BF03051434
  • Roberts TJ (1997) Mammals of Pakistan. Revised edition. Ernest Benn, London.
  • Rödder D, Kielgast J, Lötters S (2010) Future potential distribution of the emerging amphibian chytrid fungus under anthropogenic climate change. Diseases of Aquatic Organisms 92(2–3): 201–207. https://doi.org/10.3354/dao02197
  • Sarwar MK, Malik MF, Hussain M, Azam I, Iqbal W, Ashi U (2016) Distribution and current status of amphibian fauna of Pakistan: a review. Electronic Journal of Biology 12(3): 243–246.
  • Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukema W, Acevedo AA, Burrowes PA, Carvalho T, Catenazzi A, De la Riva I, Fisher MC, Flechas SV, Foster CN, Frías-Álvarez P, Garner TWJ, Gratwicke B, Guayasamin JM, Hirschfeld M, Kolby JE, Kosch TA, LaMarca E, Lindenmayer DB, Lips KR, Longo AV, Maneyro R, McDonald CA, Mendelson J, Palacios-Rodriguez P, Parra-Olea G, Richards-Zawacki CL, Rödel MO, Rovito SM, SotoAzat C, Toledo LF, Voyles J, Weldon C, Whitfield SM, Wilkinson M, Zamudio KR, Canessa S (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363(6434): 1459–1463. https://doi.org/10.1126/science.aav0379
  • Schleich HH, Anders CC (1998) Tompterna maskeyi spec. nov. from Nepal (Amphibia, Anura). In: Schleich HH, Kästle W (Eds) Contributions to the Herpetology of South Asia (Nepal, India). Fuhlrott-Museum, Veröffentlichungen aus dem, 4: 57–72.
  • Schneider JG (1799) Historia Amphibiorum Naturalis et Literarariae. Fasciculus Primus. Continens Ranas, Calamitas, Bufones, Salamandras et Hydros in Genera et Species Descriptos Notisque suis Distinctos. Jena: Friederici Frommanni. https://doi.org/10.5962/bhl.title.78757
  • Shafiq M (2005) Wildlife Acts and Rules of Pakistan. Pakistan Forest Institute, Peshawar.
  • Shah KB, Tiwari S (2004) . Herpetofauna of Nepal. A Conservation Companion. The World Conservation Union, IUCN Nepal, Kathmandu.
  • Shehzad S, Riaz T, Nawaz MA, Miquel C, Poillot C, Shah SA, Pompanon FO, Coissac E, Taberlet T (2012) Carnivore diet analysis based on next-generation sequencing: application to the leopard cat (Prionailurus bengalensis) in Pakistan. Molecular Ecology 21(8): 1951–1965. https://doi.org/10.1111/j.1365-294x.2011.05424.x
  • Stöck M, Schmid M, Steinlein C, Grosse WR (1999) Mosaicism in somatic triploid specimens of the Bufo viridis complex in the Karakoram with examination of calls, morphology and taxonomic conclusions. Italian Journal of Zoology 66(3): 215–232. https://doi.org/10.1080/11250009909356259
  • Stolickza F (1872) Notes on some new species of Reptilia and Amphibia, collected by Dr. W. Waagen in North-Western Punjab. Proceedings of the Asiatic Society of Bengal 7: 124–131.

Supplementary material

Supplementary material 1 

Supplementary tables

Muhammad Rais, Waseem Ahmed, Anum Sajjad, Ayesha Akram, Muhammad Saeed, Hannan Nasib Hamid, Aamina Abid

Data type: statistical data

Explanation note: Table S1. Sample ID and Snout-vent length of samples examined. Table S2a. Descriptive statistics of morphometric measurements of Sphaerotheca maskeyi (male). Table S2b. Descriptive statistics of morphometric measurements of Sphaerotheca maskeyi (female).

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (53.79 kb)
login to comment