Elephantulus Edwardii Research Articles

Associative colour learning and discrimination in the South African Cape rock sengi Elephantulus edwardii (Macroscelidea, Afrotheria, Mammalia)

Abstract Beside insects, sengis also consume plant material such as leaves, fruits, seeds and floral nectar. It is known that they use olfaction for foraging, but little is known about their vision and visual learning capabilities. Colour vision has been tested in two species, showing that they are likely dichromats (green- and blue-sensitive retinal cone-photoreceptors, meaning red-green colour blind). Our aim was to examine the learning and colour discrimination abilities of another species, Elephantulus edwardii. Using training procedures and choice experiments, we tested the hypotheses that the animals can associate a reward with trained colours and that they can discriminate between different colour hues. The sengis preferred the trained colours over the others, indicating associative learning. They could discriminate between all tested colours (blue, red, green, yellow). The sengis’ colour choice behaviour indicates that the animals can use also colour features to find food plant material. Additionally, learning abilities most likely are essential for the sengis’ foraging activities, for instance by associating floral or fruit shape, colour or scent with nectar or ripe fruit, to increase the efficiency to locate food sources.

Evolution of the mammalian insulin (Ins) gene; Changes in proteolytic processing

Disruption of insulin signaling in humans leads to diabetes yet changes in insulin function is tolerated in some species. Taking advantage of the large number of publicly available mammalian genome sequences I identified insulin gene (Ins) in the genomes of 151 of 156 mammalian species with well-annotated genomes, of which 141 had complete Ins coding sequences. Complete Ins coding sequences were identified from 8 additional species that lack complete genomes. Duplicated Ins genes were found in 12 rodents (9 with complete genomes) resulting in the identification of a total of 161 complete mammalian Ins coding sequences. While all 161 proinsulin protein sequences were predicted to have functional signal peptides, which should allow secretion of the hormone, unexpectedly, substitutions were found at prohormone convertase processing sites in sequences from 6 species, 2 from Chiroptera (Myotis brandtii and M. lucifugus) and 4 from Afrotheria (Chrysochloris asiatica, Echinops telfairi, Elephantulus edwardii, and Orycteropus afer). Both basic residues at the C-peptide-A-chain junction in the bats M. brandtii and M. lucifugas are replaced, which should prevent processing. Replacements of a single basic residue are found at the B-chain-C-peptide junction, in the two bats, and at the C-peptide-A-chain junction, in 4 species of Afrotheria, processing sites that suggest impaired processing. In addition, a large number of substitutions at sites that interact with the insulin receptor were found in the insulin sequences from M. brandtii and M. lucifugas suggesting a change in biological function.

Characterization of the complete mitochondrial genome of cape elephant shrew, Elephantulus edwardii

In this study, the complete mitochondrial genome of cape elephant shrew, Elephantulus edwardii, was determined through sequencing of PCR fragments. The complete mitochondrial genome of E. edwardii was 16,552 bp in length and and encoded 13 protein-coding genes, 22 transfer RNA (tRNA) genes, and two ribosomal RNA genes. The overall nucleotide composition is: 32.7% A, 29.5% T, 25.0% C, and 12.9% G, with a total G+C content of 37.9%. By phylogenetic analysis using Bayesian method, E. edwardii showed the closest relationship with another Elephantulus speceis (Genbank accession: AB096867.1).

Loss of RXFP2 and INSL3 genes in Afrotheria shows that testicular descent is the ancestral condition in placental mammals.

Descent of testes from a position near the kidneys into the lower abdomen or into the scrotum is an important developmental process that occurs in all placental mammals, with the exception of five afrotherian lineages. Since soft-tissue structures like testes are not preserved in the fossil record and since key parts of the placental mammal phylogeny remain controversial, it has been debated whether testicular descent is the ancestral or derived condition in placental mammals. To resolve this debate, we used genomic data of 71 mammalian species and analyzed the evolution of two key genes (relaxin/insulin-like family peptide receptor 2 [RXFP2] and insulin-like 3 [INSL3]) that induce the development of the gubernaculum, the ligament that is crucial for testicular descent. We show that both RXFP2 and INSL3 are lost or nonfunctional exclusively in four afrotherians (tenrec, cape elephant shrew, cape golden mole, and manatee) that completely lack testicular descent. The presence of remnants of once functional orthologs of both genes in these afrotherian species shows that these gene losses happened after the split from the placental mammal ancestor. These “molecular vestiges” provide strong evidence that testicular descent is the ancestral condition, irrespective of persisting phylogenetic discrepancies. Furthermore, the absence of shared gene-inactivating mutations and our estimates that the loss of RXFP2 happened at different time points strongly suggest that testicular descent was lost independently in Afrotheria. Our results provide a molecular mechanism that explains the loss of testicular descent in afrotherians and, more generally, highlight how molecular vestiges can provide insights into the evolution of soft-tissue characters.

Reproductive biology of three co-occurring, primarily small-mammal pollinated Protea species (Proteaceae)

This study investigated the role of vertebrates in the reproductive biology of a community of three co-occurring Protea species (Protea canaliculata, Protea sulphurea and Protea humiflora, Proteaceae) at Kraggashoek in the Western Cape, South Africa. Live-trapping, measures of facial and faecal pollen loads, and footage from remote cameras facing the inflorescences confirmed that all three are visited by small mammals and specialist nectarivorous birds. These plant species have bowl-shaped inflorescences that produce highly concentrated (34.1–42.9%) sucrose-rich nectar and a “yeasty” scent, typical traits of small-mammal pollinated plants. Camera footage indicated that 140 visits were made by eight small mammal species to an accumulative 19 inflorescences of the three Protea species. Small mammals thus made up 69% of total visits by all vertebrate species. Camera footage revealed that Micaelamys namaquensis visited flowers more frequently than any other vertebrate visitor (41% of total visitations by birds and mammals) but Elephantulus edwardii (10% of total visitations by birds and mammals) spent the longest time foraging on inflorescences (~28s per inflorescence). The ‘trap shy’ species, Graphiurus ocularis, was observed for the first time on camera, visiting Protea humiflora and Protea sulphurea inflorescences. Galerella pulverulenta (Cape gray mongoose) also visited inflorescences of P. canaliculata. The remaining 31% of total vertebrate visits, primarily to Protea humiflora, were by three species of specialist nectarivorous birds (the Cape sugarbird Promerops cafer, and the shorter-billed sunbirds, Anthobaphes violacea and Cinnyris chalybeus). Breeding system experiments with Protea sulphurea revealed that pollinators are needed for seed set, although exclusion of vertebrate pollinators only marginally lowered seed set of this partially self-incompatible species. These three Protea species had asynchronous flowering periods, supporting a wide range and relative abundance (overall live mammal trapping success rate of 22.7% nocturnal and 5.7% diurnal species) of vertebrate pollinators over a three month period in winter. That these Protea species co-occur suggests there is a community of vertebrate flower visitor species and primarily small mammal-pollinated plant species. The partitioning of nectar resources over a long period has conservation implications for both the plants and animals.

Nectar-drinkingElephantulus edwardiias a potential pollinator ofMassonia echinata, endemic to the Bokkeveld plateau in South Africa

Nectar-drinking<i>Elephantulus edwardii</i>as a potential pollinator of<i>Massonia echinata</i>, endemic to the Bokkeveld plateau in South Africa

The forgotten pollinators – First field evidence for nectar-feeding by primarily insectivorous elephant-shrews

Pollination of plants by non-flying mammals, such as mice (Rodentia), is a rarely observed phenomenon. Previously, elephant-shrews (Macroscelidea), small African mammals looking similar to mice, but not being related to them, were believed to be purely insectivorous and occasional flower visits of elephant-shrews in captivity were interpreted as a by-product of the search for insects. Only recently it was demonstrated that under lab conditions elephant-shrews regularly lick nectar from flowers. However, field observations of flower-visiting elephant-shrews and their role as pollinators were completely missing. Here I present the first evidence for flower visits and nectar consumption for elephant-shrews in the field. With video camcorders and infrared lights I recorded Cape rock elephant-shrews (Elephantulus edwardii) beside Namaqua rock mice (Micaelamys namaquensis) visiting flowers of the Pagoda lily (Whiteheadia bifolia, Asparagaceae) under natural conditions in the Namaqualand of South Africa. With their long tongues, the elephant-shrews visited the flowers non-destructively, definitely licking nectar, but not eating insects. The footage clearly shows that the elephant-shrews’ fur around their long noses touches the pollen-sacs and the stigmas of the flowers and that the animals’ fur is being dusted with pollen. As the elephant-shrews visited several flowers of different plants, it is obvious that they transfer pollen between the plants. This observation contributes to the knowledge about the behaviour of these representatives of a unique clade of small African mammals – especially in their natural habitat. With their behavioural and anatomical uniqueness, it is not unlikely that elephant-shrews even play a role as selective force driving floral evolution. Appendices:Additional supporting information is to be found:Appendix I. With its long tongue Elephantulus edwardii licks nectar from Whiteheadia bifolia flowers, getting dusted with pollen on its nose. Infrared video.http://www.pollinationecology.org/user-files/ JPE349_Appendix1.mp4Appendix II. Micaelamys namaquensis licking nectar from Whiteheadia bifolia flowers, getting dusted with pollen on its nose. Infrared video.http://www.pollinationecology.org/user-files/JPE349_Appendix2.aviAppendix III. Micaelamys namaquensis feeding on pollen-sacs of Whiteheadia bifolia flowers. Infrared video.http://www.pollinationecology.org/user-files/JPE349_Appendix3.avi

Nectar feeding by the Cape rock elephant-shrew Elephantulus edwardii (Macroscelidea) — A primarily insectivorous mammal pollinates the parasite Hyobanche atropurpurea (Orobanchaceae)

Cape rock elephant-shrews, Elephantulus edwardii (Macroscelidea) were found to be pollinators of Hyobanche atropurpurea (Orobanchaceae), a member of a holoparasitic plant genus, lacking up to now any detailed pollinator observations. The elephant-shrews were live-trapped near the plants in the Western Cape of South Africa. One animal was released in a terrarium, containing the plants. It licked nectar with its long and slender tongue while being dusted with pollen and touching the stigmas of the flowers with its nose and the fur above the snout. H. atropurpurea pollen was found in swabs of the fur around noses and snouts as well as in the faeces of captured animals. The occurrence of pollen in the faeces of the elephant-shrews is likely a result of grooming their fur as they visited the flowers without eating or damaging them. This is one of the first records of pollinating, nectar-drinking elephant-shrews, contributing to the very scarce knowledge about the behaviour of those primarily insectivorous animals, as well as small mammal pollination.

Does torpor of elephant shrews differ from that of other heterothermic mammals?

Torpor bouts of elephant shrews are intermediate in duration to those of daily heterotherms and hibernating mammals, but their body temperatures (Tbs) and metabolic rates are very low and similar to those of hibernating mammals. We quantified the thermal physiology of the Cape rock elephant shrew (Elephantulus edwardii), a species endemic to high-altitude regions of South Africa, where winters are cold and wet, and tested whether it displays multiday torpor characteristic of hibernators at low ambient temperature (Ta). E. edwardii regularly displayed torpor over a wide range of Tas. Occurrence of torpor and duration of torpor bouts increased with decreasing Ta. Whereas normothermic Tb was stable, Tb in torpid individuals fell with Ta. The mean Tb 2 Ta differential at the minimum Tb was 0.7uC, and the mean minimum Tb at Ta 8.9uC was 9.3uC. Duration of torpor bouts ranged from 6.5 to 44 h and was correlated negatively with Ta and Tb during torpor. Time required for the reduction of Tb to a Tb 2 Ta differential of ,2.0uC was faster for .1-day torpor bouts than those lasting 1 day, suggesting that the duration of a bout might be determined at the beginning, not during, a bout. The nature of heterothermy in E. edwardii seems qualitatively similar to that of other elephant shrews, although torpor is somewhat deeper and longer in this species. Temporal patterns of torpor in E. edwardii differ from those of most cold-climate hibernators, likely for ecological rather than physiological reasons.

Sticky snack for sengis: The Cape rock elephant-shrew, Elephantulus edwardii (Macroscelidea), as a pollinator of the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae)

Following the recent discovery of rodent pollination in the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae) in South Africa, now the Cape rock elephant-shrew, Elephantulus edwardii (Macroscelidea, Afrotheria) is reported as an additional pollinator. Elephant-shrews, live-trapped near W. bifolia plants, were released in two terraria, containing the plants. The animals licked nectar with their long and slender tongues while being dusted with pollen and touching the stigmas of the flowers with their long and flexible noses. The captured elephant-shrews had W. bifolia pollen in their faeces, likely as a result of grooming their fur as they visited the flowers without eating or destroying them. The animals mostly preferred nectar over other food. This is the first record of pollination and nectar consumption in the primarily insectivorous E. edwardii, contributing to the very sparse knowledge about the behaviour of this unique clade of African mammals, as well as pollination by small mammals.

A New Species of Elephant-shrew (Afrotheria: Macroscelidea: Elephantulus) from South Africa

Abstract Elephant-shrews (also called sengis, order Macroscelidea) are small-bodied insectivorous mammals with a strictly African distribution. Fifteen species currently are recognized, of which 9 occur in the southern African subregion. On the basis of molecular, cytogenetic, and morphological evidence, Elephantulus edwardii, the only strictly South African endemic species, is shown to comprise 2 closely related taxa. The new Elephantulus taxon described herein is from the central Nama-Karoo region of Western Cape and Northern Cape Provinces. Important genetic distinctions underpin its delimitation. Sequence data from the mitochondrial cytochrome-bgene and the hypervariable control region as well as 7th intron of the nuclear fibrinogen gene show these 2 taxa to be reciprocally monophyletic. They are separated by 13.8% sequence divergence (uncorrected) based on the 2 mitochondrial segments, and 4.2% based on the nuclear intron sequences. In addition, fixed cytogenetic differences include a centromeric shi...

Rodent assemblage in a habitat mosaic within the Valley Thicket vegetation of the Eastern Cape Province, South Africa

AbstractWe sampled small mammal assemblage in a mosaic of Valley Thicket vegetation in the Great Fish River Reserve during the summers of 2001 and 2002. Assemblage was dominated by seven rodent species with a single nonrodent species (Elephantulus edwardii) in the 357 trapped specimens. Rhabdomys dilectus was the most abundant in both years, followed by Mus minutoides (ranking 2nd in 2001) and Mastomys coucha (2nd in 2002). These three species, which are widespread generalists, made up 85.0% of the total rodent catch in 2001 and 74.3% in 2002. Individual species were captured on 2–14 sites of a total of 17 and M. minutoides was the most widespread. The majority of samples consisted of two (ten sites in a pooled sample for 2 years) or three species (ten sites). Significant morphological structuring was found only in two‐species samples. Species turnover was high both among sites and between the 2 years. We found no evidence of significant nested structure which would suggest hierarchical sets of ecological relationships among the species. Vegetation structure explained better than species interactions, the population variables in the rodent assemblage.

Coalescence methods reveal the impact of vicariance on the spatial genetic structure of Elephantulus edwardii (Afrotheria, Macroscelidea)

Within the Macroscelidea 15 species of elephant-shrews are recognized, of which nine occur in the southern African subregion. The Cape rock elephant-shrew (Elephantulus edwardii) is the only strictly endemic South African elephant-shrew species. Recent distribution data suggest that E. edwardii is continuously distributed from Namaqualand in the Western Cape Province to Port Elizabeth in the Eastern Cape Province. Molecular sequences from the mitochondrial cytochrome b gene and variable control region indicate significant substructure within the Cape rock elephant-shrew across its distribution. Our data unequivocally showed the presence of a northern Namaqua and central Fynbos clade with four evolutionary lineages identified within the latter. The geographical delimitation of the northern and central clades corresponds closely with patterns reported for other rock-dwelling vertebrate species, indicating a shared biogeographical history for these taxa in South Africa. A coalescent method revealed the effects of ancestral polymorphism in shaping the Namaqua and Fynbos populations since their divergence ~1.7 million years ago. Furthermore, our analyses uncovered a distinct Karoo lineage(s) that does not correspond to any of the previously described and/or currently recognized species, and we therefore argue for the possible recognition of a new sister taxon to E. edwardii. The taxonomic affinities of this clade were examined by sequencing corresponding regions from the type specimens of species described in the past, but which presently are synonimized within E. edwardii. Our results reveal the morphological misidentification of one of these types, accentuating the problems of field identification.

Habitat, food, and small mammal community structure in Namaqualand

The effect of habitat differences and food availability on small mammal (rodent and elephant shrew) species richness, diversity, density and biomass was investigated in Namaqualand, South Africa. Species richness in the three habitats sampled, namely Upland Succulent Karoo, Dry Riverine Shrub and North-western Mountain Renosterveld was low, with only 2–4 species per habitat. Rodents trapped were predominantly Gerbillurus paeba and Aethomys namaquensis, with fewer Mus minutoides and Petromyscus sp. The only non-rodent was the elephant shrew Elephantulus edwardii. Ten habitat features, the percentage of total plant cover, tree cover, shrub cover, grass cover, plant litter, total basal cover, sand, gravel or rock cover, and the dominant plant height were recorded at 30 randomly chosen points on five sampling grids in each habitat. Small mammal density and biomass was significantly correlated with food availability (green foliage cover, seeds, and relative density and biomass of insects). Species richness and diversity of small mammals were significantly correlated with shrub cover. Numbers and biomass of specific species correlated significantly with different habitat features in each case.

Organization of the somatosensory cortex in elephant shrews (E. edwardii)

The superorder Afrotheria consists of a diverse group of mammals, including elephants, hyraxes, dugongs, sea cows, aardvarks, tenrecs, golden moles, and elephant shrews. Recent studies suggest this clade diverged from other placental mammals 100 million years ago and thus may represent the sister group to the remaining placental mammals. Despite this important taxonomic position, relatively few studies have investigated cortical organization in these species. Here we present results of an investigation of the somatosensory cortex in the Cape elephant shrew (Elephantulus edwardii). Using multiunit electrophysiological recording techniques, we identified a topographic map of the elephant shrew's body in a location and orientation consistent with the primary somatosensory cortex (S1). The elephant shrew's elongated snout, extensive facial vibrissae, and long tongue accounted for a large portion of the somatosensory representation, located in a relatively rostral area of cortex. Evidence for an additional somatosensory area, presumed to be secondary somatosensory cortex (S2), was found just lateral to S1. Visual and auditory responsive areas were also identified and the extent of visual cortex appeared to be quite large in these highly visual mammals. Despite the elephant shrew's exceptionally well-developed eyes, ears, and vibrissae, there were no anatomical correlates to sensory areas, or body part representations (e.g., barrels), that could be identified in the flatted cortex.

Elephant shrews as hosts of immature ixodid ticks

Two hundred and seventy-three elephant shrews, consisting of 193 Elephantulus myurus, 67 Elephantulus edwardii and 13 animals belonging to other species, were examined for ixodid ticks at 18 localities in South Africa and Namibia. The immature stages of Ixodes rubicundus, Rhipicentor nuttalli, Rhipicephalus warburtoni and a Rhipicephalus pravus-like tick were the most numerous of the 18 tick species recovered. Substantial numbers of immature Rhipicephalus arnoldi, Rhipicephalus distinctus and Rhipicephalus exophthalmos were also collected from elephant shrews at particular localities. Larvae of I. rubicundus were most numerous on E. myurus in Free State Province from April to July and nymphs from June to October. Larvae of R. nuttalli were most numerous on these animals during April, May, August and September, and nymphs in February and from April to August. The immature stages of R. warburton were collected from E. myurus only in Free State Province, and larvae were generally most numerous from December to August and nymphs from April to October.

Elephant shrews as hosts of immature ixodid ticks

Two hundred and seventy-three elephant shrews, consisting of 193 Elephantulus myurus, 67 Elephantulus edwardii and 13 animals belonging to other species, were examined for ixodid ticks at 18 localities in South Africa and Namibia. The immature stages of Ixodes rubicundus, Rhipicentor nuttalli, Rhipicephalus warburtoni and a Rhipicephalus pravus-like tick were the most numerous of the 18 tick species recovered. Substantial numbers of immature Rhipicephalus arnoldi, Rhipicephalus distinctus and Rhipicephalus exophthalmos were also collected from elephant shrews at particular localities. Larvae of I. rubicundus were most numerous on E. myurus in Free State Province from April to July and nymphs from June to October. Larvae of R. nuttalli were most numerous on these animals during April, May, August and September, and nymphs in February and from April to August. The immature stages of R. warburtoni were collected from E. myurus only in Free State Province, and larvae were generally most numerous from December to August and nymphs from April to October.

How important is the relationship between Protea humiflora (Proteaceae) and its non-flying mammal pollinators?

The interaction between Protea humiflora and its non-flying mammal pollinators was investigated with the aim of quantifying the relationship for both the plants and mammals involved. We manipulated flower density by inflorescence removal and determined the effect upon mammal captures, and excluded mammals to determine their effect upon seed set. Of three mammal species captured frequently, the smallest, Acomys subspinosus (18±4SD g, Rodentia: Muridae), demonstrated the strongest relationship with P. humiflora. Breeding coincided with flowering, and pollen constituted 33.5±27.5% by volume (max 80%, n=19) of winter scats. Acomys captures on control grids were twice those on inflorescence-removal grids during flowering. Aethomys namaquensis (51±14g, Rodentia: Muridae) included flower products in its diet (pollen comprising 3.2±4.9% of winter scats, n=73), but captures were not affected by inflorescence removal. Aethomys is a seasonal breeder and juveniles entered the population 2months after flowering. Elephantulus edwardii, although an insectivore (48±7g, Macroscelidea: Macroscelididae), carried more pollen grains on its nose than the rodents, acquired while foraging in inflorescences for insects. Pollen comprised 3.1±5.4% (n=23) of winter scats. From the plant perspective, seed set was significantly reduced in caged inflorescences and in those >20cm above the ground, presumably due to limited accessibility by terrestrial animals. We conclude that small mammals are responsible for around half (56%) of the effective seed set in P. humiflora.

Small mammals in the semi-arid Karoo, South Africa: biomass and energy requirements

Small mammal communities in the semi-arid Karoo, South Africa were investigated by means of seasonal live-trapping. Eleven species were recorded, including nine Rodentia (pygmy hairy-footed gerbil Gerbillurus paeba, short-tailed gerbil Desmodillus auricularis, striped field mouse Rhabdomys pumilio, pygmy mouse Mus minutoides, multimammate mouse Mastomys natalensis, Namaqua rock mouse Aethomys namaquensis, grey climbing mouse Dendromus melanotis, bush Karoo rat Otomys unisulcatus and whistling rat Parotomys brantsii) and two Macroscelidea (round-eared elephant shrew Macroscelides proboscideus and Cape elephant shrew Elephantulus edwardii). Species richness was low (S = 3·8) but comparable to other southern African communities. Marked seasonal fluctuations in numbers, biomass and species richness were observed. Biomass of small mammals (mean = 324 g ha−1) was low in relation to Savanna communities, reflecting the low productivity of the Karoo. Despite low biomasses, the energy requirements of these largely herbivorous small mammal communities averaged 15% (maximum = 43%) of that needed to support the recommended carrying capacities of agricultural stock for these sites. The energy demands of the small mammals are highest in winter when plant production is depressed. Small mammal energy requirements need to be taken into account in ecosystem models for the Karoo, and when evaluating the impact of livestock on vegetation.

Food consumption, assimilation and rate of food passage in the cape rock elephant shrew, Elephantulus edwardii (macroscelidea: Macroscelidinae)

1. 1. Food consumption, assimilation and passage rates of an elephant shrew, Elephantulus edwardii, on three natural diets (cockroaches, locusts and termites) and one artificial cereal diet (Pronutro) were compared. 2. 2. Daily food consumption varies significantly between the diets and was partly related to % assimilation, which was highest on Pronutro and cockroaches (71%) and lowest on termites (31%). 3. 3. Throughput times were estimated using soluble ( 51 Cr-EDTA) and particulate markers in the Pronutro diet. First appearance of the soluble marker (0.5 hr) was significantly earlier than for the particulate marker (1.85 hr); 50% appeared at 3.2 and 3.35 hr for the soluble and particulate markers, respectively. 4. 4. The distribution of particulate markers in the digestive tract showed some retention in the stomach, ileum and colon, but rapid movement through the duodenum and very little entry to the caecum.