Published by Associazione Teriologica Italiana Volume 33 (2): 208–211, 2022 Hystrix, the Italian Journal of Mammalogy Available online at: http://www.italian-journal-of-mammalogy.it doi:10.4404/hystrix–00506-2021 Short Note Identification of postcranial elements of Gerbillinae (Mammalia: Rodentia) in pellet contents, with special reference to the species Meriones zarudnyi Kordiyeh Hamidi1,∗, Jamshid Darvish1 , Morteza Behnam-Rassouli1 , José Luis Copete2 1 Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran 2 Biblioteca de Ciència i Tecnologia, Servei de Biblioteques, Universitat Autònoma de Barcelona, Spain Keywords: Abstract postcranium jirds and gerbils Birds of prey feed mainly on small vertebrates and regurgitate indigestible remains, such as hair and pellet component bones of their prey, as pellet. Hence, the analysis of pellets provides valuable information on the birds of prey distribution of the prey species. In this paper, we used elements of the postcranial skeleton for the Zarudny’s jird identification of gerbilline rodents in pellets of birds of prey in Iran for the first time. These pellets were collected during several field campaigns in 11 regions of North, Razavi, and South Khorasan Article history: provinces (Iran), and supplemented with museum data from 13 regions in Razavi Khorasan, Go- Received: 23 November 2021 lestan, and Chaharmahal and Bakhtiari provinces (Iran). A total of 320 rodent individuals from 102 Accepted: 17 October 2022 different pellets were identified, of which 44 (13%) rodent specimens belong to Gerbillinae. The gerbilline species Meriones crassus, M. zarudnyi and Tatera indica were recognized based on dia- gnostic traits of their postcranium. Identification based on postcranial traits was confirmed by skull Acknowledgements and tooth identifications. Using pellet remains, the record of Zarudny’s jird (M. zarudnyi) expan- The authors would like to express their sincere gratitude to H. Moz- affari, V. Estrada-Devesa and À. Ollé for their kind assistance in this ded the distribution range of the species. We also provided some notes on the shape and size of the project. Thanks are also to anonymous researchers who have collec- pellets of birds of prey. Further studies are necessary to evaluate the role of postcranial elements in ted rodent and pellet specimens for the Zoological Museum of Ferdowsi identification of rodents. University of Mashhad (ZMFUM) over the years. This work was partially supported by the Ferdowsi University of Mashhad (FUM) [grant number: 2047267] assigned to K. Hamidi for a research project entitled “Phylo- genetic revision of subfamily Gerbillinae in Iran based on morphological characters of the postcranial skeleton”. We thank the editorial board and anonymous reviewers for their valuable comments and scientific advice which greatly improved the content. Birds of prey feed mainly on small vertebrates and regurgitate indi- target species in pellets, which usually may contain an ensemble of dif- gestible remains of prey as pellet. Generally, the diet of birds of prey is ferent species remains. related to the availability of prey species over their hunting areas, and We collected pellets of avian raptors through field campaigns from mainly depends on the habitat structure and productivity, as well as the 2010 to 2018 in 11 regions of Iran, including North, Razavi and South distribution, density and lifestyle of prey. Hence, analysis of pellets is a Khorasan provinces (Fig. 1). Most of the pellet samples were collected useful method for providing additional insight into small mammal com- from the roosting and/or breeding site of the birds of prey. We iden- munities and their distribution. Occasionally, known distribution lim- tified birds using field guides (e.g., Porter and Aspinall, 2010), and its of small mammals are expanded on pellet records (van Strien et al., carried out continuous monitoring of the bird’s activity and behavior 2015). Preys are generally killed by the breaking neck and back of the to ensure that each roost hosted only a single bird species. Finally, we skull. Thus, the skull of small mammals in pellets is rarely complete. grouped pellets according to the different species of observed birds of Although usually discarded in pellet analyses, the postcranial skeleton prey, color, shape and size. In addition to field surveys, we examined could nonetheless be an important source of prey identification, espe- pellets from museum collection of the Zoology Museum of Ferdowsi cially for those species that may not easily observed or trapped (such University of Mashhad (ZMFUM) (Iran), which include materials from as some small rodents and insectivores) (Laudet and Hamdine, 2001). Razavi Khorasan, Golestan, and Chaharmahal and Bakhtiari provinces Rodents of the subfamily Gerbillinae are distributed throughout (totally 13 regions) (Fig. 1, Tab. 1). north to south Africa and from west to central Asia. In Iran, four gen- After cleaning and washing the pellets, we referred each bone ma- era of gerbilline rodents are known: Tatera, Gerbillus, Meriones, and terial to the relevant subunit of the skeletal system (vertebral column Rhombomys (Wilson et al., 2017). There are numerous molecular and and thorax, pectoral girdle and forelimbs, and pelvic girdle and hind- morphological studies on these rodents, but the postcranial skeleton has limbs). Consequently, we examined the skeletal elements individu- been greatly ignored (Hamidi et al., 2020). ally, and identified gerbilline specimens following Hamidi et al. (2020). In this study, we intended to identify gerbilline rodents by the dia- Skulls and teeth were analysed separately according to the identifica- gnosis of postcranial material in pellets of birds of prey in Iran. We tion keys of species mentioned in Corbet (1978). The identification of aimed to evaluate our previous findings (Hamidi et al., 2020) and the postcranial bones was made by comparison with materials from refer- potential efficiency of skeletal characteristics in identification of some ence collections and literature (mainly Hamidi et al., 2020), published illustrations, and postcranial descriptions (e.g., Darvish et al., 2012; Argot, 2003; Searfoss, 1995; Berry and Searle, 1963). ∗ Corresponding author We used informative characters of the postcranial skeleton, which Email address: kordiyeh.hamidi@yahoo.com (Kordiyeh Hamidi) are considered as synapomorphies for the members of subfamily Ger- Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272 22nd December 2022 ©c b e2022 Associazione Teriologica Italiana doi:10.4404/hystrix–00506-2021 Postcranium and pellet identification Figure 2 – Postcranial skeleton of Zarudny’s jird (Meriones zarudnyi) found in pellet materials from Abravan (Sarakhs, northeast of Iran). Informative characters of vertebral column are shown with simple text for gerbilline species and in italic for M. zarudnyi. Abbreviations are as follows: C: Cervical vertebrate, Ca: Caudal vertebrate, T: Thoracic vertebrate, L: Lumbar vertebrate, D.: Dorsal view, Lt.: Lateral view, R.: Rostral view. Figure 1 – Collecting localities of pellets of birds of prey in Iran. North Khorasan province: Shirvan (1) and Bojnord (2); Razavi Khorasan province: Mashhad (3), Kalat (4), Dargaz scapula (Fig. 3C), scapula with straight coracoid process or coracoid (5), Qazqan (6), Bajgiran (7), Tandoureh (8), Sarakhs (9), Baghbagho (10), Shoorak Maleki (11), Abravan (12), Robat Sharaf (13), Mayamey (14), Khaf (15), Torbat-e Heydarieh (16) and with a curvature up to the superior ridge of glenoid fossa (Fig. 3D), Fariman (17), South Khorasan province: Qaen (18), Birjand (19) and Nehbandan (20), Golestan nonparallel anterior and posterior arcs of obturator foramen, picked province: Aliabad-e Katul (21), and Chaharmahal and Bakhtiari province: Hossein Abad pubic tuber, situation of the tip of the pubic angle in front of the 1/2 (22). Pellets collected through field campaigns are indicated by •, those provided from the Zoology Museum of Ferdowsi University of Mashhad (ZMFUM) are shown by ◦, and ♦ is superior or lower than 1/2 inferior of the anterior arc of obturator fora- used for both sources. men, and triangular shape of ischial body ridge around the tuberosity of ischium (Fig. 4A), absence of a groove along the lesser trochanter of femur (Fig. 4B), presence of an obvious posterior tuberosity in cal- caneus (Fig. 4C), and, triangular or quadrangular cuboid articular facet billinae (see Hamidi et al., 2020), for initial sorting the pellet con- in calcaneus (Fig. 4D). We used diagnostic informative characters for tents. These characters are as follows: oval shape of centrum and cir- the genera Tatera, Gerbillus, Meriones, and Rhombomys, and the rel- cular shape of transverse foramen in sixth cervical vertebrate (Fig. 2C), evant species to identify gerbilline rodents to genus and species levels crest-like neural spine of third lumbar vertebrate (Fig. 2E), no connec- following Hamidi et al. (2020). tion between neural spine of first and second sacral vertebra (Fig. 2F), A total of 320 rodent individuals were initially identified from 102 closed angle of the two prezygapophyses in the sacrum (Fig. 2G), short- pellets based on skull and teeth morphology (Tab. 1). Consecutively, broad or normal (= long) manubrium (Fig. 3A), short-broad or normal the gerbilline rodents were identified based on postcranial characterist- Table 1 – Local distribution of studied pellets of birds of prey. The most frequent rodent in pellets of each locality was identified based on the skull and teeth morphology. Numbers in parentheses for localities refer to those used in Fig. 1. Source of pellets No. of studied Average No. of Main prey Locality (birds of prey) pellets rodent remains (No.) Shirvan (1) Golden eagle 3 12 Rattus norvegicus (9) Bojnord (2) Golden eagle 2 9 Rattus norvegicus (6) Mashhad (3) unknown 1 3 Mus musculus (3) Kalat (4) Egyptian vulture 7 19 Ellobius fuscocapillus (9) Dargaz (5) Eurasian griffon vulture 6 17 Apodemus witherbyi (13) Qazqan (6) Eurasian griffon vulture 1 3 Apodemus witherbyi (3) Bajgiran (7) Eurasian griffon vulture 2 7 Mus musculus (6) Tandoureh (8) Eurasian griffon vulture 4 11 Apodemus witherbyi (5) Sarakhs (9) Common kestrel 15 51 Cricetulus migratorius (29) Baghbagho (10) Little owl 1 2 Mus musculus (2) Shoorak Maleki (11) Common kestrel 3 9 Cricetulus migratorius (6) Abravan (12) Little owl 4 12 Meriones zarudnyi (9) Robat Sharaf (13) Common kestrel 1 2 Cricetulus migratorius (2) Mayamey (14) Little owl 1 2 Mus musculus (2) Khaf (15) Little owl 30 98 Mus musculus (42) Torbat-e Heydarieh (16) Golden eagle 2 8 Rattus norvegicus (5) Fariman (17) Golden eagle 3 10 Rattus norvegicus (5) Qaen (18) Common kestrel 7 19 Meriones crassus (3) Birjand (19) Little owl 2 5 Tatera indica (2) Nehbandan (20) Common kestrel 4 13 Meriones crassus (4) Aliabad-e Katul (21) unknown 1 3 Mus musculus (3) Hossein Abad (22) unknown 2 5 Mus musculus (4) Total 102 320 209 Hystrix, It. J. Mamm. (2022) 33(2): 208–211 Table 2 – Prey features of the little owl and common kestrel as the two most frequent predators in this study. Details on the collected pellets and prey items are given. Birds of prey Little owl Common kestrel General features of pellets round, small, not compacted, with undigested bone rod-like, small, compacted, fully digested Way of identification of content skull, teeth and postcranium mainly teeth Total pellets No. of studied pellets 38 30 Average No. of rodent remains 119 94 Pellets containing No. of studied pellets 24 7 Gerbillinae Average No. of gebilline remains 33 11 Main gerbilline rodents Meriones crassus (66%) Meriones crassus (63%) Main skeletal elements most postcanium parts including: vertebral column, mainly hard bones including: humerus, ulna, helpful in identification manubrium, 1st rib, scapula, pelvic bone, humerus, femur, 3rd metatarsal, calcaneus ulna, femur, 3rd metatarsal, calcaneus ics listed in Hamidi et al. (2020) as shared characters for Gerbillinae other examined jird species). These results are incongruent with au- (Fig. 2, 3 and 4). Thirty-one pellets contained remains of 44 gerbil- thor’s previous study (Hamidi et al., 2020). line rodents with three identifiable species, including Sundevall’s jird Results showed that the main postcranial bones that were used for (Meriones crassus Sundevall, 1842) (6 out of 44 individuals: 13%), species identification were humerus, femur, ulna and pelvic bones Zarudny’s jird (Meriones zarudnyi Heptner, 1937) (9 out of 44 indi- (complete or broken parts), although these were mainly complete which viduals: 20%), and Indian gerbil (Tatera indica Hardwicke, 1807) (29 facilitated prey identification. Furthermore, scapula and calcaneus out of 44 individuals: 65%) (Tab. 2). Remains of M. zarudnyi were were as helpful as former list of skeletal parts. Other parts of the post- found in pellets from Abravan (Sarakhs, northeast of Iran) (Fig. 1, 2, 3 cranial skeleton (such as the vertebrae, manubrium, ribs, and clavicle) and 4), which was considered as a new locality record for this species. showed little or no diagnostic role, perhaps due to their fracture (dur- We confirmed results by primarily labels of cranial and dental iden- ing mechanical digestion in the buccal cavity or chemical digestion in tifications. However, this reciprocal confirmation was not possible for the digestive tract) or losing them during cleaning process of the pel- some pellet remains, when we could not find traces of skull and/or teeth let. Pellets also contained some remains of house mouse (Mus muscu- or the skull was hardly broken and teeth were not helpful due to heavy lus Linnaeus, 1758), brown rat (Rattus norvegicus Berkenhout, 1769), cusp wearing. In contrast, for some other pellets, postcranial compon- steppe field mouse (Apodemus witherbyi Thomas, 1902), grey dwarf ents were badly broken or loosed, following the effects of the digestive hamster (Cricetulus migratorius Pallas, 1773), southern mole vole (El- enzymes of birds of prey. lobius fuscocapillus Blyth, 1834), Afghan pika (Ochotona rufescens Gray, 1842), some insectivores (mainly Crocidura sp.) and birds Reconciling the results of postcranial identification with that of skull (Tab. 1). and teeth showed that several characters can be considered as inform- ative characters for Zarudny’s jird. These are including little caudal Field observations and monitoring the predators revealed that pel- extension of axial neural process in lateral view of axis (Fig. 2B), com- lets differ among birds of prey, in terms of size, shape and even color pletely flattened (not growthed) neural spine in rostral view of fourth (Tab. 2). Pellets of little owl (Athene noctua Scopoli, 1769) (38 out of caudal vertebrate (Fig. 2H), and normal (not broad or short) shape of scapula in dorsal view (Fig. 3C). However, presence of a small fossa on the olecranon in caudo-medial view of ulna (Fig. 3F) might be re- cognized as an informative character only for this species (among all Figure 3 – Postcranial skeleton of Zarudny’s jird (Meriones zarudnyi) found in pellet Figure 4 – Postcranial skeleton of Zarudny’s jird (Meriones zarudnyi) found in pellet materials from Abravan (Sarakhs, northeast of Iran). Informative characters of thorax, materials from Abravan (Sarakhs, northeast of Iran). Informative characters of pelvic pectoral girdle and forelimbs are shown with simple text for gerbilline species and in italic girdle and hindlimbs are shown with simple text for gerbilline species and in italic for M. for M. zarudnyi. Abbreviations are as follows: C.M.: Caudo-medial view, D.: Dorsal view, zarudnyi. Abbreviations are as follows: A.: Anterior view, Lt.: Lateral view, M.: Medial Lt.: Lateral view, R.: Rostral view, V.: Ventral view. view, V.: Ventral view. 210 Postcranium and pellet identification 102 pellets: 37%) were found to be generally round in shape and small pellet materials from Abravan located in northeast Iran could further in size with undigested bone components. They were not compacted corroborate the distribution range expansion of this species, towards and had several particles of plant and insect materials. According to west Turkmenistan and northeast Iran. the pellet analysis, little owls mainly fed on Mus musculus (46 out of For M. zarudnyi there is no information on home range, movement, 119 individuals: 38%) in Great Khorasan, including North, Razavi and and social organization. Previous studies showed that elongation of South Khorasan provinces. Common kestrel (Falco tinnunculus Lin- metatarsals (Fig. 4E) and femur bones (Fig. 4B) are significant indic- naeus, 1758) had small rod-like compacted pellets (30 out of 102 pel- ators of cursoriality and saltatoriality in many mammals including ro- lets: 29%) that rounded in both ends. Cricetulus migratorius (37 out dents Samuels and Van Valkenburgh (2008); Seckel and Janis (2008). of 94 individuals: 39%) was the most preferred prey for this species in Although habitat of this species is not well known, but in relation to the study areas. Large-scale uncompact pellets (10 out of 102 pellets: the morphological observations in M. zarudnyi and postcranial pattern 9%), which generally included completely broken parts of the skull, described above, one can hypothesize that probably members of this belonged to the golden eagle (Aquila chrysaetos Linnaeus, 1758). This species live in dry and arid habitats. It seems that elongation of hind- large raptor mainly captured the rodent species Rattus norvegicus (25 limbs may be an adaptation characteristic for this species, which can out of 39 individuals: 64%) as its food source in the Great Khorasan. give it the ability of running away fast in open areas (with less shelters Egyptian vulture (Neophron percnopterus Linnaeus, 1758) generally as compared with rocky areas) whenever threatened in the wild by the fed on rodent species Ellobius fuscocapillus (9 out of 19 individuals: predators. Further studies are necessary to reveal the evolution of post- 47%) and thrown up large rod-like pellets (7 out of 102 pellets: 6%), in cranial skeleton in this group of rodents and to provide new records on which some bony materials were found. Eurasian griffon vulture (Gyps the locality of Zarudny’s jird in eastern Iran to complete our limited fulvus Hablizl, 1783) regurgitated large pellets (13 out of 102 pellets: knowledge of its distribution in the Iranian Plateau. 12%) with hairs and feathers interconnected in non-regular shape. Apo- demus witherbyi (21 out of 38 individuals: 55%) was the most abund- References ant rodent prey found in the pellets for this species (Tab. 1). Therefore, Argot C.H., 2003. Functional adaptation of the postcranial skeleton of two Miocene Borhy- house mouse and grey dwarf hamster were the most frequent prey spe- aenoids (Mammalia: Metatheria) from South America. Palaeontology 46: 1213–1267. Berry R.J., Searle A.G., 1963. Epigenetic polymorphism of the rodent skeleton. Proc. Zool. cies identified in pellets of birds of prey based on cranial morphology. Soc. Lond. 140(4): 577–615. However, Egyptian and Eurasian griffon vultures are strict scavengers Corbet G.B., 1978. 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