Graomys Griseoflavus Research Articles

Correction to: Phylogeography and ecological niche modelling of the South American cricetid rodent Graomys griseoflavus, with insights into its chromosomal evolution

Correction to: Phylogeography and ecological niche modelling of the South American cricetid rodent <i>Graomys griseoflavus</i>, with insights into its chromosomal evolution

Phylogeography and ecological niche modelling of the South American cricetid rodent Graomys griseoflavus, with insights into its chromosomal evolution

Abstract The rodent Graomys griseoflavus has a wide geographical distribution in the Arid Diagonal of South America, showing variation in the diploid number (2n = 33–38) caused by three different Robertsonian (Rb) translocations. Two contrasting hypotheses have been proposed to explain the origin and evolution of this polymorphism: (i) unique and sequential events; or (ii) multiple and independent origins of Rb translocations. Here, we combined phylogeography and ecological niche modelling to elucidate the evolutionary history of G. griseoflavus and help to contrast these hypotheses. The results indicated a demographic increase that would have begun ~150 kya from the High Monte ecoregion. The spatial distributions of these populations were coincident with the areas of highest habitat suitability. The palaeoclimatic projections suggested the presence of two main glacial refugia coincident with the main genetic clusters. Graomys griseoflavus underwent two pulses of southward expansion at ~220 and ~210 kya. More recently (~20 kya), there was a secondary contact between the southern populations (Low Monte ecoregion) expanding northwards and the northern populations (High Monte ecoregion) expanding into marginal areas of the Chaco ecoregion. Combined with the cytogenetic evidence, our results support the multiple and independent origins of Rb translocations.

COMUNIDADES DE ROEDORES DE CULTIVOS DE SORGO EN LA PROVINCIA DE CÓRDOBA Y SU POSIBLE VINCULACIÓN CON LA FIEBRE HEMORRÁGICA ARGENTINA

The composition of rodent communities in fields dedicated to sorghum culture was studied in seven sites situated along two transects about 500 km long, in the SE of Córdoba Province (Argentina). Four of the sites are in the endemic area of ArgentineHemorrhagic Fever and the other three in the marginal area, free of Junin virus. The animáis were trapped during a short period in May and June, 1977. Eight Crieetidae (Calomys musculinus, Akodon azarae, Calomys laucha, Oligoryzomys flavescens, Cabreramys benefactus, Akodon dolores, Graomys griseoflavus y Calomys callosus) and one Muridae species (Mus musculus) were obtained. Comparative analysis of the species composition of the communities has been performed by using the Mountford Índex.Total number of specimens from Calomys plus Akodon represented, in all the samples, more than 80%. The most abundant species in six out of seven samples was C. musculinus, the most important reservoir of Junin virus. The structure of this species populationswas very similar for most of the endemic and marginal areas.

Tracking native small mammals to measure fine-scale space use in grazed and restored dry woodlands

The degradation of dry woodlands in South America by agricultural activities affects wildlife through a decrease in available habitat and fine-scale changes in habitat structure. The impact of land use can be perceived by small, mobile organisms as preventing or facilitating their movement through and among habitats, consequently altering ecosystem functions. By tracking with radiotelemetry we describe for the first time the pattern of movement of a small mammal (Graomys griseoflavus) that inhabits dry woodland ecosystems in South America and its relationship with environmental features that affect movement. We measured environmental variables linked to the ecological requirements of the species (e.g., plant cover and patches of forage species consumed) in restored and grazed woodlands and compared movements between seasons (dry and wet). We found that the fine-scale differences in the vegetation cover associated with livestock grazing changed the mobility and use of space of this small mammal. The step-lengths and used area for G. griseoflavus were greater under passive restoration compared to the area grazed by livestock. Small rodents moved between patches of similar mean size of forage species, avoiding large inter-patches of bare ground. Although both management conditions showed seasonal variations in plant cover, the step-lengths decreased significantly in the grazed woodland during the wet season, while step-lengths in the restored area were unaffected by season. The fine-scale spatial arrangement of plants in restored woodlands elucidated notable changes in animal movement on grazed lands, suggesting that space use by small mammals may be an important tool to identify habitat structures that facilitate the movement of animals in restoration of degraded systems.

Management of Protected Areas and Its Effect on an Ecosystem Function: Removal of Prosopis flexuosa Seeds by Mammals in Argentinian Drylands.

The ecological function of animal seed dispersal depends on species interactions and can be affected by drivers such as the management interventions applied to protected areas. This study was conducted in two protected areas in the Monte Desert: a fenced reserve with grazing exclusion and absence of large native mammals (the Man and Biosphere Ñacuñán Reserve; FR) and an unfenced reserve with low densities of large native and domestic animals (Ischigualasto Park; UFR). The study focuses on Prosopis flexuosa seed removal by different functional mammal groups: “seed predators”, “scatter-hoarders”, and “opportunistic frugivores”. Under both interventions, the relative contribution to seed removal by different functional mammal groups was assessed, as well as how these groups respond to habitat heterogeneity (i.e. vegetation structure) at different spatial scales. Camera traps were used to identify mammal species removing P. flexuosa seeds and to quantify seed removal; remote sensing data helped analyze habitat heterogeneity. In the FR, the major fruit removers were a seed predator (Graomys griseoflavus) and a scatter-hoarder (Microcavia asutralis). In the UFR, the main seed removers were the opportunistic frugivores (Lycalopex griseus and Dolichotis patagonum), who removed more seeds than the seed predator in the FR. The FR shows higher habitat homogeneity than the UFR, and functional groups respond differently to habitat heterogeneity at different spatial scales. In the FR, because large herbivores are locally extinct (e.g. Lama guanicoe) and domestic herbivores are excluded, important functions of large herbivores are missing, such as the maintenance of habitat heterogeneity, which provides habitats for medium-sized opportunistic frugivores with consequent improvement of quality and quantity of seed dispersal services. In the UFR, with low densities of large herbivores, probably one important ecosystem function this group performs is to increase habitat heterogeneity, allowing for the activity of medium-sized mammals who, behaving as opportunistic frugivores, did the most significant seed removal.

Role of small rodents in the seed dispersal process: Microcavia australis consuming Prosopis flexuosa fruits

AbstractUnderstanding the functional role of animal species in seed dispersal is central to determining how biotic interactions could be affected by anthropogenic drivers. In the Monte Desert, mammals play different functional roles in Prosopis flexuosa seed dispersal, acting as opportunistic frugivores (endozoochorous medium‐sized and large mammals) or seed hoarders (some small sigmodontine rodents). Our objective was assessing the functional role of Microcavia australis, a small hystricognathi rodent, in the fruit removal and seed deposition stages of P. flexuosa seed dispersal, compared to sympatric sigmodontine rodents. In situ, we quantified fruit removal by small rodents during non‐fruiting and fruiting periods, and determined the distance seeds were transported, particularly by M. australis. In laboratory experiments, we analysed how M. australis stores seeds (through scatter‐ or larder‐hoarding) and how many seeds are left in caches as living seeds, relative to previous data on sigmodontine rodents. To conduct field studies, we established sampling stations under randomly chosen P. flexuosa trees at the Ñacuñán Man and Biosphere Reserve. We analysed fruit removal by small rodents and seed dispersal distance by M. australis using camera traps focused on P. flexuosa fruits covered with wire screen, which only allowed entry of small animals. In laboratory trials, we provided animals with a known number of fruits and assessed seed conditions after removal. Small rodents removed 75.7% of fruit supplied during the non‐fruiting period and 53.2% during the fruiting period. Microcavia australis and Graomys griseoflavus were the main fruit removers. Microcavia australis transported seeds to a mean distance of 462 cm and cached seeds mainly in scatter‐hoards, similarly as Eligmodontia typus. All transported seeds were left in fruit segments or covered only by the endocarp, never as predated seeds. Microcavia australis disperses P. flexuosa seeds by carrying fruits away from a source to consume them and then by scatter‐hoarding fruits and seeds.

Distribution of Telomeric Sequences (TTAGGG)n in Rearranged Chromosomes of Phyllotine Rodents (Cricetidae, Sigmodontinae)

Phyllotines are sigmodontine rodents endemic to South America with broad genetic variability, Robertsonian polymorphisms being the most frequent. Moreover, this taxon includes a species with multiple sex chromosomes, which is infrequent in mammals. However, molecular cytogenetic techniques have never been applied to phyllotines to elucidate their karyotypic evolution. We studied the chromosomes of 4 phyllotine species using FISH with a pantelomeric probe (TTAGGG)_n. Graomys griseoflavus, Eligmodontia puerulus, and E. morgani are polymorphic for Robertsonian translocations, whereas Salinomys delicatus possesses XX/ XY₁Y₂ sex chromosomes. Telomeric signals were detected at both ends of all chromosomes of the studied species. In S. delicatus interstitial telomeric sequences (ITS) were observed in the 3 major chromosome pairs, which are equidistant from one of the telomeres in these chromosomes. These results suggest that ITS are important in the reshuffling of the highly derived karyotype of S. delicatus. Considering the phylogeny of phyllotines, the Robertsonian rearrangements of G. griseoflavus, E. puerulus, and E. morgani possibly represent chromosome fusions which have occurred independently. The pericentromeric regions of the biarmed chromosomes of these species do not contain telomeric sequences characteristic for strict fusions of recent origin, suggesting a common pattern of telomeric repeat loss during chromosomal evolution of these rodents.

Agricultural land-use intensity and its effects on small mammals in the central region of Argentina

Agriculture intensification is one of the main threats to biodiversity in agricultural systems. The effectiveness of conservation strategies in these systems depends mainly on the compromise between biodiversity conservation and agricultural land use. The aim of this study was to assess the effect of land-use intensity, characteristics of linear habitats (field borders) and their surrounding fields (landscape) on small mammal richness and abundance in agricultural systems of Argentina. In autumn 2009, we performed a removal sampling in 60 traplines located in the field borders of high or low land-use intensity regions. In traplines under high land-use intensity we found seven species while under low land-use intensity we found ten. Characteristic species of grasslands and woodlands such as Monodelphis dimidiata, Thylamys pallidior, Necromys lasiurus and Graomys griseoflavus were only captured in traplines under low land-use intensity. Higher numbers of Calomys musculinus species (habitat generalist) were observed under high land-use intensity while Akodon azarae and Oxymycterus rufus species, known as habitat specialists, were more frequently found in the low land-use intensity region. Border width and height, as well as land use of both sides of the border, were major variables for explaining small mammal abundances. Our results suggest that conservation of wide field borders with characteristics similar to those of natural habitats would be crucial for sustainable management of Pampean agricultural systems which hold high richness and abundance of small mammal species.

Association of cellular and molecular alterations in Leydig cells with apoptotic changes in germ cells from testes of Graomys griseoflavus × Graomys centralis male hybrids

Spermatogenesis is disrupted in Graomys griseoflavus×Graomys centralis male hybrids. This study was aimed to determine whether morphological alterations in Leydig cells from hybrids accompany the arrest of spermatogenesis and cell death of germ cells and whether apoptotic pathways are also involved in the response of these interstitial cells. We used three groups of 1-, 2- and 3-month-old male animals: (1) G. centralis, (2) G. griseoflavus and (3) hybrids obtained by crossing G. griseoflavus females with G. centralis males. Testicular ultrastructure was analyzed by transmission electron microscopy. TUNEL was studied using an in situ cell death detection kit and the expression of apoptotic molecules by immunohistochemistry. The data confirmed arrest of spermatogenesis and intense apoptotic processes of germ cells in hybrids. These animals also showed ultrastructural alterations in the Leydig cells. Fas, FasL and calbindin D28k overexpression without an increase in DNA fragmentation was detected in the Leydig cells from hybrids. In conclusion, the sterility of Graomys hybrids occurs with ultrastructural changes in germ and Leydig cells. The enhancement of Fas and FasL is not associated with cell death in the Leydig cells. Probably the apoptosis in these interstitial cells is inhibited by the high expression of the antiapoptotic molecule calbindin D28k.

Hoarding patterns of sigmodontine rodent species in the Central Monte Desert (Argentina)

AbstractHoarding food is an important strategy of rodents in desert environments characterized by unpredictable and poor food resource availability. In the Monte Desert, Prosopis produces abundant food, unevenly in time and space, in the form of pods and seeds. Sigmodontine rodents (Graomys griseoflavus, Akodon molinae, Eligmodontia typus and Calomys musculinus) use Prosopis propagules extensively, and they could be predators or dispersers depending on how they handle and where they leave the propagules. The objectives of this study were: (1) to know what rodent species transported propagules; (2) to evaluate what hoarding pattern was used by species that transport propagules (larder and scatterhoarding); and (3) to analyse in which condition were propagules left by the rodent species, both at the food source and in caches. Our results showed that all four species transported propagules, with G. griseoflavus and E. typus being the species that carried more seeds. Our study supported the evidence that food caching is common among species and that many species both larderhoard and scatterhoard food. Graomys griseoflavus and A. molinae, the largest species, larderhoarded more than did the smaller E. typus. These results uphold the hypothesis that larger species will show greater propensity to larderhoard than smaller species. Considering the interaction between seed‐hoarding patterns and plants, E. typus was the species that could most improve germination because it scatterhoarded propagules and left seeds out of pods. In contrast, G. griseoflavus could have a negative impact on plant populations because this was the species that predated more seeds and larderhoarded a high percentage of them. The smallest C. musculinus was the species that transported propagules least, and left them as seeds inside pods or pod segments mainly at the food source, which makes seeds more vulnerable to predation.

Small mammals (Didelphimorphia, Rodentia and Chiroptera) from Pampean Region, Argentina

We studied small mammal assemblages recovered from owl pellets collected at 11 locations throughout the Argentina’s Pampean Region. We identified 21 species, including two marsupials, one bat, and 18 rodents. From the analysis of this dataset, we could distinguish three main groups of small mammals that currently inhabit the Pampean Region: 1) a group of taxa related to Pampean agroecosystems (Calomys spp., Akodon azarae, and Oligoryzomys flavescens); 2) a group of Brazilian species (Cavia aperea, Oxymycterus rufus, Necromys lasiurus, Necromys obscurus, Holochilus brasiliensis, and Monodelphis dimidiata); and 3) a group including species from Patagonia, Espinal and Monte phytogeographic provinces (Microcavia australis, Oligoryzomys longicaudatus, Eligmodontia typus, Graomys griseoflavus, and Akodon molinae). In addition, we documented the first record of a species of the large-bodied group of Calomys in Buenos Aires province, expanding its distribution ca. 420 km southward.

Differential use of vertical space by small mammals in the Monte Desert, Argentina

Space use in deserts usually has been considered only along the horizontal dimension; however, vertical structure could be an important variable for habitat segregation among small mammal species. Our study assessed the use of vertical space by small mammals of the Monte Desert by live-trapping animals at different heights. We recorded 1,336 captures of 4 rodent and 1 marsupial species in 27,600 trap nights. All 5 species were captured on the ground and in tree layers, but only the gray leaf-eared mouse (Graomys griseoflavus) and the desert mouse opossum (Thylamys pallidior) used vertical space appreciably. G. griseoflavus used the arboreal space independently of habitat, plant species, or branch diameter, whereas T. pallidior showed a more selective behavior, being present at greater heights and on large-diameter branches of Prosopis trees. All rodent species used lower more than higher parts of arboreal strata. They used vertical space more or only during the dry season when resource availability is low. Our study suggests that vertical structure offers greater opportunities to acquire resources when these are scarce and plays a role in the coexistence of small desert mammals.

Descripción del postcráneo de Rhipidomys austrinus y Graomys griseoflavus (Rodentia, Cricetidae, Sigmodontinae)

Se describe el esqueleto postcraneal de dos especies de roedores sigmodontinos Rhipidomys austrinus Thomas, 1921 y Graomys griseoflavus (Waterhouse, 1837). Se detalla cada estructura del esqueleto postcraneal sobre la base de la forma, tamaño, superficie y orientación de cada elemento esqueletal. La anatomía postcraneal de estas dos especies muestra caracteres asociados a patrones morfológicos diferentes, vinculados a su modo de locomoción. Es así que R. austrinus exhibe características en varios elementos del postcráneo consistente con una locomoción arborícola, mientras G. griseoflavus muestra atributos en su esqueleto relacionados a una locomoción de tipo terrestre.

Rodent selection by Geoffroy’s cats in a semi-arid scrubland of central Argentina

Small mammals usually constitute the main prey for Leopardus geoffroyi throughout its distribution. We studied the patterns of small rodent selection by this felid in a semi-arid scrubland of central Argentina, addressing whether prey choice may be related to the availability, morphology, and distribution of the different rodent species. Cat’s diet was studied during 2005–2006 through the analysis of 182 scats, along with field estimates of rodent abundances from trapping. The cricetine rodents Akodon molinae and Calomys musculinus were predated according to the availability expected by trapping, indicating that their use was opportunistic. Akodon azarae and Graomys griseoflavus, on one hand, and Eligmodontia typus, on the other hand, were consumed in lower and higher proportion than their availabilities, respectively. Our results suggest that some cricetine rodent characteristics such as abundance, escape ability, microhabitat use, and activity period, appear to be potential factors contributing to differential vulnerability to predation by Geoffroy’s cat in central Argentina.

Geographic distribution and phenetic skull variation in two close species of Graomys (Rodentia, Cricetidae, Sigmodontinae)

The interspecific differentiation of South American rodents of the genus Graomys was assayed at ecological and morphometric levels in two species. At the ecological level, niche modelling was used. At the morphometric level, the hypothesis that the size and shape of the skull vary with the geographic location was tested using geometric morphometrics by assessing the extent and spatial distribution of phenotypic skull variation within and among two species, Graomys griseoflavus and Graomys chacoensis. Our results of niche modelling indicate the spatial differentiation between the two species, with G. chacoensis inhabiting preferably the Chaco ecoregion and G. griseoflavus inhabiting mainly the Monte ecoregion. In multiple linear regressions, approximately 20% of the skull size variation is explained by latitude, altitude, and temperature seasonality. The partial least square analysis reveals strong correlation between shape and environmental variables, mainly with latitude, annual mean temperature, and annual precipitation. Discrimination between G. griseoflavus and G. chacoensis was highly reliable when using geometric morphometric tools. These results permit us to elucidate some evolutionary processes that have occurred in these species.

Small mammal remains recovered from two archaeological sites in the middle and lower Negro River valley (Late Holocene, Argentina): Taphonomic issues and paleoenvironmental implications

This paper presents the results of a taphonomic and paleoenvironmental analysis of small mammal remains recovered from the Negro Muerto and Angostura 1 archaeological sites. These sites (ca. 0.5 and 0.95 ka BP, respectively), are located in the middle and lower Negro River valley in northern Patagonia, Argentina. Based upon the presence of several types of evidence (cut marks, bone tools, and thermal alteration), it is proposed that Holochilus brasiliensis and cavies were acumulated by humans. At the Angostura 1 site, some remains also show evidence of having been generated by carnivores (digestion, breakage patterns, and relative skeletal element abundances). This indicates that carnivores (e.g., Puma concolor) could have contributed to the formation of the small mammal assemblages. Other small mammal species recovered at both sites (e.g., Galea leucoblephara, Microcavia australis, Akodon molinae, and Graomys griseoflavus) suggest semi-desert environmental conditions, similar to those found today. The presence of Reithrodon auritus and Oligoryzomys sp. indicate the development of open herbaceous steppe environments in proximity to bodies of water. However, the discovery of H. brasiliensis at both sites, an orizomyine of amphibious habitats and subtropical origin, and which is now absent in the area, suggests warmer and wetter conditions during this period.

American tripanosomiasis: a study on the prevalence of Trypanosoma cruzi and Trypanosoma cruzi-like organisms in wild rodents in San Luis province, Argentina

Chagas disease is caused by Trypanosoma cruzi. Wild and perianthropic mammals maintain the infection/transmission cycle, both in their natural habitat and in the peridomestic area. The aim of this paper was to present the results from a study on wild rodents in the central and northern regions of San Luis province, Argentina, in order to evaluate the prevalence of this infection. Sherman traps were set up in capture areas located between latitudes 32 masculine and 33 masculine S, and longitudes 65 masculine and 66 masculine W. The captured rodents were taxonomically identified and hemoflagellates were isolated. Morphological, biometric and molecular studies and in vitro cultures were performed. Infection of laboratory animals and histological examination of the cardiac muscle and inoculation area were also carried out. Parasites were detected in circulating blood in Calomys musculinus, Graomys griseoflavus, Phyllotis darwini and Akodon molinae. The parasites were identified using biological criteria. Molecular PCR studies were performed on some isolates, which confirmed the characterization of these hemoflagellates as Trypanosoma cruzi. Forty-four percent of the 25 isolates were identified as Trypanosoma cruzi, and the remaining 56% as Trypanosoma cruzi-like. These findings provide evidence that wild rats infected with Trypanosoma cruzi and Trypanosoma cruzi-like organisms are important in areas of low endemicity.

Spermatocyte apoptosis, which involves both intrinsic and extrinsic pathways, explains the sterility of Graomys griseoflavus × Graomys centralis male hybrids

Spermatogenic impairment and the apoptotic pathways involved in establishing sterility of male hybrids obtained from crossing Graomys griseoflavus females with Graomys centralis males were studied. Testes from G. centralis, G. griseoflavus and hybrids were compared at different ages. Terminal transferase-mediated dUTP nick-end labelling assay (TUNEL), Fas, Bax and cytochrome c labelling were used for apoptosis evaluation, and calbindin D(28k) staining as an anti-apoptotic molecule. In 1-month-old animals, spermatocytes were positive for all apoptotic markers, but moderate TUNEL (+) spermatocyte frequency was only found in G. centralis. At subsequent ages, the apoptotic markers were downregulated in testes from parental cytotypes, but not in hybrid testes. TUNEL (+) spermatocytes were present at 78% and 44% per tubule cross-section in 2- and 3-month-old hybrid animals, respectively. Pachytene spermatocyte death in adult hybrids occurs via apoptosis, as revealed by high caspase-3 expression. Calbindin was highly expressed in spermatocytes of adult hybrids, in which massive cell death occurs via apoptosis. Calbindin co-localisation with TUNEL or Fas, Bax and cytochrome c was very limited, suggesting an inverse regulation of calbindin and apoptotic markers. Hybrid sterility is due to breakdown of spermatogenesis at the pachytene spermatocyte stage. Both extrinsic and intrinsic pathways are involved in apoptosis of spermatocytes, which are the most sensitive cell type to apoptotic stimuli.

Ability of Murid Rodents to Find Buried Seeds in the Monte Desert

Rodents have developed a great capacity to for finding and storing seeds, and the ability of each species to find seeds in sufficient numbers could determine rodent abundance. To investigate this ability, we compared the differential ability of four murid rodents (Akodon molinae, Graomys griseoflavus, Calomys musculinus and Eligmodontia typus) to detect buried seeds. We also measured the variables (seed type, number of seeds in caches, soil depth and soil moisture) that would be affecting such ability. Results showed a differential ability to find seeds among rodents, E. typus was the most successful species, and C. musculinus and G. griseoflavus were the least successful. Conditions of wet sand and grouped seeds were the most favourable for murids to find higher number of seeds. These rodents showed preference for the sunflower seed, which is large, with good hygroscopic capacity and high in lipids, whereas millet is the opposite. The use of food storage strategies would give murid species a differential adaptive advantage, providing them with a greater ability to locate and exploit food sources more efficiently in periods of lower food abundance and after rainfall events.

Utilization of food resources by small and medium-sized mammals in the Monte Desert biome, Argentina

Theoretical models of species coexistence between desert mammals have generally been based on a combination of food and microhabitat selection by granivorous rodents. Although these models are applicable in various deserts of the world, they cannot explain resource use by mammals in Neotropical deserts. The present study examines diet composition in a mammal assemblage in the Monte desert, Argentina. The results show that two main strategies are used by these mammals: medium-sized species (hystricognath rodents: Dolichotis patagonum, Lagostomus maximus, Microcavia australis and Galea musteloides; and an exotic lagomorph: Lepus europaeus) are herbivores, whereas small-sized species (a marsupial: Thylamys pusillus; and sigmodontine rodents: Graomys griseoflavus, Akodon molinae, Calomys musculinus, Eligmodontia typus) are omnivorous. Small mammals also show a tendency towards granivory (C. musculinus), insectivory (A. molinae and T. pusillus) and folivory (G. griseoflavus).