The greater part of expected mammalian extinctions will be of smaller-bodied mammals, including rats which are more generally known only as pests and carriers of pathogens. We address the long-tailed nesokia rat, which is among the least studied Palaearctic mammals. The species is known from merely five specimens, collected between March 1974 and January 1977 within a radius of 30 km around Qurna inside the seasonally flooded Mesopotamian marshes in southern Iraq. In the 1990s, this extensive aquatic habitat has been deliberately reduced to <15% of its original area and the IUCN expressed fear that such a disaster “almost certainly” caused the extinction of the long-tailed nesokia. Although the interventions after 2003 reversed the shrinking trend and marshes started to expand, the continuous presence of the long-tailed nesokia could not be unambiguously confirmed. We provide meagre evidence suggesting that the rat might be still present in the marshes. Next, our habitat modelling shows that the area of the long-tailed nesokia might be more extensive than expected with a highly suitable habitat covering 15,650 km2 of Mesopotamian marshland in Iraq (between Basra and Salah Ad Din provinces) and the Hawizeh Marshes in the adjacent Iranian Khuzestan.
Rats of the Rattus division (Murinae) are a specious rodent assemblage native to southern and south-eastern Asia. They are well-known to the lay public as pests and carriers of parasites and pathogens, and some of them pose a serious threat for human health (Aplin et al. 2003). Less known is that some rats are also listed on the IUCN Red List as species of conservation concern (IUCN 2017) and that several species were already driven to extinction during the modern history (e.g. Harper 1945, Turvey 2009). Perhaps quite surprisingly to many, the majority of mammalian extinctions over the last 400 years were not of large charismatic species but of smaller-bodied creatures (Entwistle and Stephenson 2000). Rarity is more common among rodents than would be expected in a random process (Ceballos and Brown 1995), hence the greater part of expected mammalian extinctions during the next few decades will be of smaller-bodied mammals (Entwistle and Stephenson 2000). Despite this plain evidence, rodents receive disproportionate low attention with respect to conservation activity and research (Young 1994), which translates into a lack of knowledge on their status and conservation needs. In this review, we address one of those poorly studied species, the long-tailed nesokia, Nesokia bunnii (Khajuria 1981), which is known from a handful of individuals collected in the wetlands at the confluence of the Tigris and the Euphrates Rivers, where the mythological Garden of Eden was located by most scholars (Albright 1922).
The first two individuals of the long-tailed nesokia were collected on 23 March and 16 November 1974, respectively, and served as the type and paratype for Erythronesokia bunnii, a new genus and species (Khajuria 1981). Both specimens were deposited in the mammal collection at the Natural History Research Centre and Museum, University of Baghdad, Baghdad (NHRCM), which was vandalized in 2003 during the war in Iraq (Al-Sheikhly et al. 2015). In 2016, Kryštufek et al. (2017) surveyed the still existing NHRCM small mammal collection for E. bunnii but failed in finding a single voucher specimen. It was therefore concluded that the type material of E. bunnii had been ultimately lost. Further three adults were collected between May 1974 and January 1977 and were published by Al-Robaae and Felten 1990. They are now in the Naturmuseum Senckenberg, Frankfurt, Germany (SMF), and were described by Kryštufek et al. (2017). As far as to our knowledge, no further museum vouchers are known to exist.
The description provided by Khajuria (1981) and the subsequent reclassification of E. bunnii relied entirely on morphology. The species shares with the short-tailed nesokia N. indica (Gray, 1832) all traits that distinguish Nesokia from the closely related Bandicota. The two species of nesokia rats differ in colour, size, relative length of tail, and shape of skull and mandible (Kryštufek et al. 2016, 2017). True mice and rats (Murinae) abound with cryptic species, which are so morphologically similar that they can only be discerned by molecular markers. The long-tailed nesokia rat is clearly an exception to this general similarity. It is so distinct from N. indica and the bandicoot rats that its species status was nearly unequivocally accepted by all subsequent authors (Figure 1). The generic status of Erythronesokia was retained in 1980s and more hesitantly in the 1990s. In a craniometric study, Al-Robaae and Felten 1990 demonstrated a close resemblance between the long-tailed and the short-tailed nesokia rats, concluding that Erythronesokia is “not more than – if at all – a subgenus of Nesokia, but not a separate genus.” Similar were conclusions from a geometric morphometric approach of craniodental structures (Kryštufek et al. 2016) and the species is now regarded to be one of the two extant species of Nesokia (Denys et al. 2017). The evolutionary history of the long-tailed nesokia rat can only be deduced from circumstantial evidence. The earliest appearance of Nesokia in the fossil record is at about 2 mya in Siwalik, India (Patnaik 2014), and a molecular dating suggests a divergence from Bandicota (as a sister genus) at 1.2 mya (confidence interval = 0.8–1.6 mya; Fabre et al. 2013). One can expect the origin of the long-tailed nesokia rat to have occurred in the late Middle Pleistocene or early Upper Pleistocene.
The range of the long-tailed nesokia rat is one of the smallest among the Palaearctic mammals. All reliable records of occurrence cluster within a narrow perimeter in the Basra province inside the seasonally flooded Mesopotamian marshes in southern Iraq. In the 1990s, this extensive aquatic habitat, originally covering 15–20 thousand km2, has been deliberately reduced to <15% of its original area (Al-Ansari et al. 2012). The prevailing opinion claimed that such an extensive ecosystem destruction “… almost certainly lead to the global extinction” (UNEP 2001) of two mammals, endemic to these marshes, the Iraqi smooth-coated otter Lutrogale perspicillata maxwelli Hayman, 1956, and the long-tailed nesokia rat. Attempts initiated in 2003 towards restoration of the original habitat reversed the shrinking trend and marshes started to expand at the rate of 800 km2 per year (Al-Ansari et al. 2012). While the smooth-coated otter, along with the Eurasian otter Lutra lutra (Linnaeus, 1758) escaped extinction (Al-Sheikhly et al. 2017; Moretti et al. 2017) the fate of the long-tailed nesokia rat is more perplexing. The animal was last seen in 1976, i.e. long before any drainage occurred. The IUCN Red List assessed the current conservation status of the species as Endangered (Stuart 2008).
With this study we aim to set a baseline for further work on this elusive rat in the Mesopotamia marshes of southern Iraq. Our goal is twofold. First, we assess the habitat suitability for the long-tailed nesokia rat in the marshes of Iraq to get an idea of the extension of the appropriate environment of the animal. Second, we explore all possible sources of information to trace any report which might signalize the occurrence of the animal. At last but not least, we would like to raise interest on this extremely poorly known mammal which, despite its threatened conservation status, attracts so little interest.
2 Materials and methods
2.1 Data collection
We examined existing museum vouchers of N. bunnii, i.e. three skins and skulls held in the mammal collection of the Senckenberg Forschungsinstitut und Naturmuseum Frankfurt a. M., Germany (SMF 62925, 87531, 87532). We recorded the entire information associated with these vouchers, both from specimen tags and card files. Furthermore, we performed a thorough search in literature sources and on the internet, focussing on information on marshes in general and on small mammals in particular. Over the last several years we set live traps in habitat suitable for the target species, made observations on the rodents and their tracks, and interviewed Marsh Arabs (indigenous inhabitants of the marshes) on their possible sightseeing of an unusual rat. We informed them about the animal’s appearance and encouraged them to report any encounters and, if possible, document the sightseeing with a photograph.
2.2 Habitat modelling
In order to model the habitat suitability for N. bunnii, the following methodological steps were applied: (1) identification of environmental predictor variables, (2) collection and preparation of environmental predictors, (3) species range polygon refinement and (4) habitat suitability/species distribution modelling.
By leaning on the existing literature about Nesokia bunnii’s habitat preferences, the Global Lakes and Wetlands Database Level 3 (GLWD-3) geospatial data were obtained (https://www.worldwildlife.org/pages/global-lakes-and-wetlands-database). Next, the long-time smoothed NDVI values corresponding to the mean NDVI over the period from 1999 to 2012 for summer (June 18) were purchased from the Land Cover CCI Climate Research Data Package (CRDP) which is a product developed by the Climate Change Institute of the European Space Agency (ESA CCI) (http://maps.elie.ucl.ac.be/CCI/viewer/index.php). As human interference in the study area was high, owing to wetland draining in the last decades, the NDVI variable, gathered from freely available LANDSAT satellite imagery (https://earthexplorer.usgs.gov/), was used as a proxy of landscape change. Thus, the NDVI difference between 1995 (June) and 2018 (June) was calculated and used as the next environmental predictor for the N. bunnii habitat suitability modelling. Moreover, bioclimatic data, purchased from the WorldClim database (Version 2.0), were used as well (http://www.worldclim.org/). Here the temperature and precipitation derived from bioclimatic variables were considered separately. However, all were z-standardized and PCA transformed. Three PCA components (explaining 90% of variability in temperature derived bioclimatic properties) and three PCA components (explaining 87% of variability in precipitation derived bioclimatic properties) were added to the model. The categorical wetland database was transformed to a distance variable by using the Euclidean distance algorithm, in order to meet the requirements of the habitat suitability model incorporated in the TerrSet geospatial software (Eastman 2018).
Prior to habitat suitability modelling, the above mentioned predictor variables and the IUCN range polygon were used to calculate a confidence map in the species range polygon refinement procedure. This map served in the habitat suitability/species distribution-modelling step as a weight. Finally, the Weighted Mahalonobis distance was applied to develop the final N. bunnii habitat suitability map.
3 Results and discussion
3.1 Distributional records and habitat suitability
Only four records of the long-tailed nesokia rat are known and they are positioned within a radius of 30 km around Qurna (Figure 2). These localities are: “Basra” (Khajuria 1981); Saraifa, 30 km north of Qurna; Bani Mansor, 25 km west of Qurna; 5 km north of Qurna (Kryštufek et al. 2017). According to the information on the SMF specimen tags, all vouchers were captured in the marshland. This record concurs well with the mandibular morphology of the long-tailed nesokia which is different from fossorial and Catholic species of Nesokia and Bandicota (Kryštufek et al. 2016), allegedly a consequence of its presumed aquatic life style (Al-Robaae and Felten 1990; Harrison and Bates 1991).
The IUCN polygon for the species’ range estimated the range to be more extensive, covering the Central (Qurna) and the Hammar Marshes, the Euphrates–Tigris river system, between Basra and Al Kut near Baghdad, i.e. an area of approximately 35,800 km2. Our results suggest an even more extensive suitable habitat, covering the majority of Mesopotamian marshland in Iraq, extending for approximately 600 km between Basra and Salah Ad Din provinces. A wide-ranging habitat fragment was also retrieved in the Hawizeh Marshes between the Tigris and Karun Rivers in the Iranian Khuzestan. As suggested by the habitat suitability model, the eastern border might be set by the mountain ranges of Zagros and Kabir Kuh while the western border putatively coincides with the Syrian Desert. The highly suitable habitat (habitat suitability >0.75) covers an estimated 15,650 km2, and is in two major fragments, in the north (around Samarra) and south (south-eastern Iraq and adjacent Iran). These putative fragments are separated by less suitable habitat (habitat suitability <0.25) in a distance of approximately 130 km.
Needless to say, our habitat suitability model has to be taken with caution. First, the actual sites of occurrence of the long-tailed nesokia rat are nearly half a century old. Next, their position could not be geo-referenced with a desired precision. Finally, the cluster of positive sites covers only a small proportion of potentially suitable habitat.
3.2 Is the long-tailed nesokia still present in the marshes?
As already mentioned, the last record of the long-tailed nesokia rat is from 1977. In 2007 Haba (2009) surveyed Mesopotamian marshland mammals, mainly by relying on visual observations of animals or tracks. These techniques are not the most suitable for detecting a nocturnal murine and indeed, the survey failed to confirm any evidence of the long-tailed nesokia rat. After the 2007 survey, we continued monitoring the putatively suitable habitats in the marshes by live-trapping and interviewing local inhabitants. The only large murines we recorded were the brown rat Rattus norvegicus and the short-tailed nesokia rat (Figure 3).
During this 2007 survey, Haba published a photograph of a half-eaten carcass which was not identified to the species, and it was labelled as a “Rat” (Figure 13 in Haba 2009). Only the sacral region of the body was preserved, along with hind feet and the tail (Figure 4A). The most obvious features of this leftover, clearly seen despite the low resolution of the photograph, are (i) robust feet, (ii) tail with a thick base which fairly rapidly tapers towards the tip, and (iii) the ochre red dorsal pelage which is clearly demarcated from the dirt white underside. The pelage matches that of the long-tailed nesokia rat in every detail (cf. Figures 1, 4B). The whitish underside and robust feet differ from that of the short-tailed nesokia rat which resembles its long-tailed relative in rusty dorsal fur (Figure 3A) but shows faint demarcation on flanks between the dorsal and the ventral colour and has more delicate feet. The brown rat is brownish grey (Figures 3B, 4C). The photograph by Haba is so far the strongest indication on the presence of the long-tailed nesokia rat after the last museum voucher had been captured near Bani Mansor on 2 January 1977 (Kryštufek et al. 2017). The carcass was found in the Lissan E’jeardah Marsh of the Mysan province, i.e. northward of Basra and Qurna and close to the 1970s trapping sites of the species. This leftover was unfortunately not preserved.
Another effort to record the long-tailed nesokia rat is worth mentioning. The late Jamshid Darvish, a leading rodent expert in Iran, informed us that his group searched for the long-tailed nesokia rat in the Khuzestan of Iran, but their attempts yielded no positive results (personal communication to BK, on 25 February 2011).
As shown in this study, the suitable habitat for the long-tailed nesokia rat might be much more extensive than presumed ever before (Figure 2). The proposed range is not unlikely as long as one keeps in mind that two otter-species mentioned above are widely present in this area (Al-Sheikhly and Nader 2013). We hope that the perspective of surveying a broad area will strengthen interest of conservation groups on the status of the long-tailed nesokia rat throughout the Garden of Eden.
Funding source: Slovenian Research Agency
Award Identifier / Grant number: P1-0255 and P6-0372
The authors are grateful to Irina Ruf and Katrin Krohmann (Senckenberg Forschungsinstitut und Naturmuseum Frankfurt a. M., Germany) who enabled access to specimens.
Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: Funding for this research was provided by the Slovenian Research Agency (Grant P1-0255 for B.K. and Grant P6-0372 for D.I.).
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
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