We present new natural history data on abundance and movements (daily and seasonal) during the pre-breeding (March-June) and breeding-post-breeding season (July-September) of two poorly studied frog species of the Himalayas, Nanorana vicina and Allopaa hazarensis. We estimated 185 Murree Hills Frogs and 90 Hazara Frogs within the study area (0.79 ha). The daily and seasonal movement data showed that the two species moved either between neighboring ponds or remained in an array of smaller ponds (within an area of 120 m²) along the stream bank. About 75% of movements were < 29.5 m in N. vicina and < 50.87 m in A. hazarensis during pre-breeding season while < 41.5 m in N. vicina and < 81 m in A. hazarensis during breeding-post-breeding season. We suggest inclusion of amphibian habitat requirements and ensuring stream connectivity in urban planning and development projects in the area to prevent the local extinction of the endemic species. In the future, more robust and long-term studies, encompassing more streams situated within a wider area, would help clarify dispersal, colonization, metapopulation structure, and dynamics of these endemic frogs of the forested montane streams in the Himalayan Foothills.

Dicroglossidae, Highland Frogs, Himalaya, Lincoln Index, Paini tribe

The temporal and spatial aspects of animal movement are considered important for population control, metapopulation dynamics and life-long sustainability of wildlife species. The impact of land use, the spread of invasive species, diseases, and responses to global climate change, can be better understood if we comprehend animal movement and dispersal (Smith and Green 2006). Movement is essential for the reproduction and survival of local populations and in a wider landscape or regional scale, mobility among populations is necessary for recolonization after local extinction and for the maintenance of metapopulations (Marsh and Trenham 2001). Young amphibians seldom disperse more than 2–3 kilometers (Petranka and Holbrook 2006) and rarely move more than five kilometers (Peter 2001). Amphibian dispersal is vital for the maintenance of amphibian populations and yet this is often significantly compromised in anthropogenically impacted landscapes (Ribeiro et al. 2019).

Currently, 21 species of amphibian (all anurans) have been documented in Pakistan (Rais et al. 2021) of which nine are believed to be endemic to Pakistan (Ali et al. 2018). Allopaa hazarensis, Family Dicroglossidae, is endemic to the springs and streams of Northern Pakistan (> 1,195 m elevation) while Nanorana vicina, Family Dicroglossidae, is endemic to Pakistan (> 1,765 m elevation) and India (Khan 2006; Ahmed et al. 2020) (Fig. 1). The two frog species are listed as Least Concern in IUCN Red List of Threatened Species. The major threats to these frog species include habitat degradation, urbanization, and climate change (Ohler and Dutta 2004; Khan et al. 2008).

Figure 1. 

Global distribution range of Murree Hills Frog (Nanorana vicina) (blue polygon) and Hazara Frog (Allopaa hazarensis) (red polygon).

The description of their adults and tadpoles is available (Dubois and Khan 1979; Khan and Malik 1979; Rais et al. 2014; Gill et al. 2020; Ikram et al. 2022). Further information about molecular taxonomy and phylogeny (Hofmann et al. 2019, 2021; Akram et al. 2021), impact of climate change (Saeed et al. 2021, 2022a), and occupancy modeling and population monitoring through eDNA (Saeed et al. 2022b) have been carried out recently. The post-breeding radiotelematry (VHF) revealed that the two species show little movement (< 3 m) (Akram et al. 2022). These two frog species breed during summer and monsoon: July-August (Saeed et al. 2021). There is no study available on what triggers them to breed and regarding their clutch size and age structure. The temperature had a positive correlation with increase in the concentrations of sex hormones (Saeed et al. 2021). Since these frogs inhabit forested streams having hard and rocky substrate (Khan 2006), these are believed to lay eggs under the heavy boulders where early development takes place. Under laboratory conditions, A. hazarensis completed metamorphosis during 12^th-18^th week while N. vicina completed metamorphosis during 18^th-22^th week with 22 °C as the most stable temperature for their growth. Although higher temperatures (>26 °C) were associated with early onset and completion of metamorphosis, they caused reduction in the body size, more frequent developmental complications or deformities such as edema and tail kinks, lower fitness and higher mortality (Saeed et al. 2021).

Since not much is known about the natural history of these two Himalayan endemics, we aimed to provide abundance data and examine daily and seasonal movements of the N. vicina (Murree Hills Frogs) and the A. hazarensis (Hazara Frogs) along a continuous habitat- montane forested freshwater stream. Our findings will help survey anurans associated with similar habitats elsewhere in the world. Our data on relative abundance and movement patterns of the two Himalayan endemics help increase understanding of their habitat requirements, metapopulation structure, dispersal, and colonization.

Of the many identified threats globally, habitat degradation, fragmentation, and loss have been recognized as the major factors responsible for the decline of many amphibian species (Brown et al. 2012). This has led to a great deal of research into understanding the ecology of amphibians, particularly their movement and dispersal capabilities, in a landscape undergoing these phenomena. Data from other regions (Nearctic, Palearctic, Neotropical, and Australian region) is available and has greatly increased our understanding of how to incorporate habitat management needs for amphibians into urban planning and development projects. Establishing the negative impact of habitat fragmentation and gathering data on movement and dispersal in amphibian populations is required for properly understanding the situation in the area in question (Funk et al. 2005). We, however, still lack scientific information about species from the Oriental region, particularly from under-developed countries, where resources are limited and smaller wildlife groups, such as amphibians, receive very little attention.

We provide new information about abundance and movement in Asian Spiny Frogs, N. vicina and A. hazarensis, endemic to Himalayas: Saeed et al. (2022) compared detection of N. vicina and A. hazarensis using eDNA surveys and visual encounter surveys for estimating occupancy. The former method accounted for higher occurrence probabilities. We report on the population of the two frog species for the first time. The two species were found to be fairly common at the study site. We, however, believe that factors such as open population structure as well as the short period of time that was available for autumn recaptures might affect the accuracy of our abundance estimates.

We found that N. vicina and A. hazarensis did not exhibit much movement in the two field sessions or during pre- and post-breeding seasons. Movement over short distances in amphibians is common. Of the 53 anuran species reviewed for their dispersal ability, 56% moved a distance of ≤ 1 km (Smith and Green 2005). About 30% of the marked individual of Physalaemus pustulosus (Tungrana Frog) moved among the ponds and covered a distance of 50 m during the period of five weeks. The majority of recorded movements were within 200 m distance (Marsh et al. 1999). Houston Toads (Bufo houstonensis) stayed within 75 m of the pond of initial capture, rarely dispersing to a distance of > 750 m (Vandewege et al. 2013). Akram et al. (2022) reported that radio tracked Murree Hills Frogs (6 ♂, 7 ♀) and five Hazara Frogs (8 ♂, 8 ♀) remained within 3 m distance during post-breeding (September, 2017 and 2018). The study was, however, conducted during breeding-post breeding season only. The mean daily movement and mean seasonal movement of the studied species were in accordance with the distances known from most amphibian species elsewhere in the world (Marsh et al. 1999; Vandewege et al. 2013).

The movement data, both daily and seasonal, showed that the frogs moved either between neighboring ponds or remained within an area of approximately 120 m², which contained a few pools on the river. The maximum linear distance from the breeding pond traveled by 11 studied female B. americanus (American Toad) ranged from 246 to 1,015 m (Forester et al. 2006). All males of B. houstonensis stayed within < 75 m of their breeding pond (Vandewege et al. 2013). Only 1% (of 10,443 individuals marked) of the adult Rana luteiventris (Columbia Spotted Frog) moved ≥ 2000 m among 21 ponds situated within 7 km distance (Funk et al. 2005). About 151 adult Water Frogs (Rana lessonae, R. ridibunda, and R. esculenta) moved among all studied ponds except the one which was separated by a road (Peter 2001). A total of 12 movements were recorded between ponds separated by 50–100 m, seven movements between 150–200 m, six movements of 150–200 m and two movements of > 200 m in P. pustulosus over a period of 5 weeks (Marsh et al. 1999). The small distance range in the movements we monitored is attributed to the presence of ponds at different elevations and with differing levels of disturbance. Pond 1 is separated from other ponds by the road, and ponds No. 1 and 2 experience a high level of human disturbance while Pond 5 had the least disturbance. The local community draws water from these ponds for household use, hence, frogs moved from ponds P1 and P2 to P5.

The majority of the movements were along the stream particularly in the upstream direction. The Ascaphus truei (Coastal Tailed Frog) is known to move upstream during low water flow in the headwater stream system whilst moving downstream to breed (Hayes et al. 2006). Our studied stream is a permanent freshwater stream. The main source is ground water, snow-melt, and drainage of rainfall from hills located in the surrounding area, especially the northern side. We suggest our species responded to disturbance level and prefer to occupy ponds in the upstream area where there are fewer disturbances.

The study area bears exceptional importance in terms of forest and biodiversity (Chawla et al. 2012). Unfortunately, the area has also been experiencing both natural and human induced changes. About 55 km² (24 km² in state-owned and 31 km² in private or community forest) reduction in the forest area of Tehsil Murree (Rawalpindi, Punjab, Pakistan) is reported (Shahzad et al. 2015). The natural areas have been degraded and the forest area has been transformed by buildings and other urban features. Climate change during the past two decades has affected many areas of Pakistan, including this study area. Over a dozen butterfly species have been lost due to changes in the climate of Murree (Saadat et al. 2016). The two endemic frog species are known to occur in sub-tropical chir pine forest (900–1,700 m) and other forest types such as Himalayan moist temperate forest (> 2000 m) further north of our study area, but do not exist in sub-tropical scrub (broad-leaved) forest (< 900 m) located in the south. The species are adapted to freshwater forested wetlands found at higher elevation with low air and water temperature and cool summers. The long-term survival of many amphibian populations or subpopulations depends on colonization from nearby wetlands (Petranka et al. 2004; Church 2008). There is an inverse relationship between colonization and distance to travel. If an amphibian species is not capable of moving from source pond to other nearby wetlands, the chances of recolonization are expected to decrease (Lehtinen and Galatowitsch 2001) which might cause local extinction. Hence, the presence of wetlands in close proximity helps attain long-term persistence in amphibian populations (Petranka and Holbrook 2006). The two studied species are unable to perform overland migration through the open forest to disperse or colonize nearby streams. Due to various anthropogenic threats or changes in climatic pattern, their movement and dispersal would be limited, resulting in the progressive decline of their populations which might eventually lead to local extinction.

Many researchers have proposed different mitigation approaches such as construction of artificial wetlands (created wetlands) and wetland restoration (Lehtinen and Galatowitsch 2001; Pechmann et al. 2001; Vasconcelos and Calhoun 2004). The natural wetlands, unlike created wetlands, undergo changes in hydrology, water regime, flow and persistence which might impact success of reproduction. Similarly, created wetlands are sometimes free of fish, all potentially negative factors for amphibian reproduction. We suggest inclusion of amphibian habitat requirements and ensuring stream connectivity in urban planning and development projects of the area.

We obtained low recaptures which could be due to the secretive nature of the studied species. These frogs may remain hidden most of the time and it was not possible for us to move the heavy rocks and boulders to check for their presence in these likely locations. The area has been experiencing rapid changes. We recommend carrying out more robust and long-term studies encompassing multiple streams situated within a wider area. This would help to understand the colonization of these frogs and establish if they are capable of moving through the forest to occupy other streams, thus providing a better picture of metapopulation structure and dynamics. Likewise, studies on the impact of water quality and quantity on these frogs would help associate water and amphibian conservation in the area.

We are indebted with thanks to Driscoll, D., Professor, Integrative Ecology, Deakin University, Melbourne, Australia, for pre-peer-review. We are thankful to Paul Freed for proof-reading the draft. We thank Mr. Wajehuddin and Mr. Bhutta, Punjab Forest Department for providing assistance during the field work. We are thankful to Dr. Ali Nawaz, Country Director, Snow Leopard Foundation, Pakistan for providing logistics.

We would like to acknowledge Higher Education Commission, Pakistan (Grant# 3170) for funding this research.