Dumpsters and other anthropogenic structures as habitat for invasive African rock agama lizards in Florida

Invasive species often use habitat differently than native species and can benefit by occupying underutilized habitats during the invasion process. The Peter’s Rock Agama (Agama picticauda)—native to savannahs of sub-Saharan Africa—is successfully invading urban habitats in Florida, USA. During a field trip in urban southern Florida, we observed apparently high A. picticauda abundance around dumpsters used for human refuse, potentially because dumpsters provide refuge, thermoregulatory opportunities, abundant arthropod prey, and harbor few competitors. In this study, we surveyed abundance and built resource selection functions to better understand habitat use of A. picticauda in urban southern Florida. We tested whether hypothesized habitat features predictably influenced the abundance and occupancy of A. picticauda among sites and whether individuals used specific habitat features within sites. Across sites, we found A. picticauda abundance was positively correlated with the number of dumpsters, and, within sites, dumpsters were preferentially selected as habitat. Similarly, we also found two other anthropogenic structures, building crevices and electrical units, were positively selected habitats at population and individual scales. We hypothesize that dumpsters, crevices, and electrical units are selected resources because they are underutilized habitats by other species and they provide refuge, beneficial thermoregulatory opportunities, and in the case of dumpsters, foraging opportunities. Our study provides the first quantitative assessment of urban habitat use by non-native A. picticauda, and supports the importance of human structures as habitat. Our results suggest the intriguing possibility that the A. picticauda invasion in Florida may be exploiting a vacant niche in urban habitats during the invasion process.

     

Six new polymorphic microsatellite loci isolated and characterized from the African savannah elephant genome

The African savannah elephant (Loxodonta africana) is a ‘keystone’ species that plays a vital role in regulating the dynamics of both plant and animal communities and yet it is endangered and its numbers have been reduced to approximately 500 000 across their entire continental range. Molecular genetic markers are important tools for providing genetic information useful in formulating effective management and conservation strategies for the surviving elephant populations. We describe the isolation and characterization of six new polymorphic microsatellite markers in the African savannah elephant and demonstrate that these loci can be PCR (polymerase chain reaction)‐multiplexed, a desirable attribute that saves costs in large‐scale microsatellite screening.     

Seasonal environments drive convergent evolution of a faster pace‐of‐life in tropical butterflies

New ecological niches that may arise due to climate change can trigger diversification, but their colonisation often requires adaptations in a suite of life‐history traits. We test this hypothesis in species‐rich Mycalesina butterflies that have undergone parallel radiations in Africa, Asia, and Madagascar. First, our ancestral state reconstruction of habitat preference, using c. 85% of extant species, revealed that early forest‐linked lineages began to invade seasonal savannahs during the late Miocene‐Pliocene. Second, rearing replicate pairs of forest and savannah species from the African and Malagasy radiation in a common garden experiment, and utilising published data from the Asian radiation, demonstrated that savannah species consistently develop faster, have smaller bodies, higher fecundity with an earlier investment in reproduction, and reduced longevity, compared to forest species across all three radiations. We argue that time‐constraints for reproduction favoured the evolution of a faster pace‐of‐life in savannah species that facilitated their persistence in seasonal habitats.     

Phylogeography of Mus (Nannomys) minutoides (Rodentia,Muridae) in West Central African savannahs: singular vicariance in neighbouring populations

We studied the phylogeography of the strict savannah pygmy mice Mus (Nannomys) minutoides in West Central Africa. A total of 846 base pairs of the cytochrome b sequence were obtained for 66 individuals collected in Gabon, Cameroon, Republic of Congo and Central African Republic. These sequences were compared to those of M. minutoides from other African countries and to eight other species of the genus Mus. We performed maximum likelihood, Bayesian and nested clade analyses, as well as neutrality tests and time estimates. We show that M. minutoides is a well‐differentiated monophyletic species that separated from other pygmy mice 1.17 Myr ago. A distinct West Central African M. minutoides clade diverged early from the other African populations of the species, with a more recent common ancestor dating 0.14 Myr. West Central African populations are globally homogeneous, despite the present fragmentation of savannahs by the rain forest. However, our analyses show an unexpected vicariance between geographically close savannahs, embedded in the rain forest in Central Gabon. One of these populations is genetically more similar to very distant peripheral populations than to three closely neighbouring populations situated on both sides of the Ogooué River. A non‐river geographical barrier probably persisted in this area, durably isolating these local populations. This hypothesis about the history of the savannah landscape should be testable through the biogeographical analysis of other strict savannah small mammal species.     

Associations of ant species to land cover types and human disturbance in south‐west Gabon

We recorded ground‐foraging ant species in forest and savannah habitats along a 52‐km‐long road planned for upgrade in the buffer zone of the Moukalaba‐Doudou National Park in south‐west Gabon. Sixty stations were established with three sampling points on each side of the future road and baited with peanut butter to record the presence of invasive Wasmannia auropunctata (Roger, 1863). We documented 46 ant species including one genus and eight species not previously reported in Gabon, but no evidence of the presence of W. auropunctata. We also found species known to have an opportunistic behaviour such as Cardiocondyla emeryi (Forel, 1881), Tetramorium simillimum (Smith, 1851) and Trichomyrmex destructor (Jerdon, 1851). Species richness in forested stations was significantly higher than in savannah. Among the most common ant species in the area, we identified 13 associated with forests, eight associated with savannahs and one generalist. Four species were highly tolerant to human disturbance. Our study, even if biased towards stress‐tolerant species, provides new insights about ant species associations with habitats and contributes to the establishment of a reference system to classify African ant species that could be used to monitor the success of restoration of areas impacted by human activities.     

Thermoregulatory differences in African mole-rat species from disparate habitats: Responses and limitations

Individuals and populations possess physiological adaptations to survive local environmental conditions. To occur in different regions where ambient temperature varies, animals must adopt appropriate thermoregulatory mechanisms. Failure to adjust to environmental challenges may result in species distributional range shifts or decreased viability. African mole-rats (Bathyergidae) occupy various habitats in sub-Saharan Africa from deserts to montane regions to mesic coastal areas. We examined thermoregulatory characteristics of three African mole-rat species originating from disparate (montane, savannah, and arid/semi-arid) habitats. Animals were exposed to various ambient temperatures, whilst core body temperature and the surface temperature of different body parts were measured. Oxygen consumption was determined as a measure of heat production. Core body temperatures of Natal (montane) mole-rats (Cryptomys hottentotus natalensis) increased significantly at ambient temperatures >24.5 °C, while those of the highveld (Cryptomys hottentotus pretoriae) (savannah) and Damaraland (Fukomys damarensis) (arid/semi-arid) mole-rats remained within narrower ranges. In terms of surface temperature variation, while pedal surfaces were important in regulating heat loss in Natal and Damaraland mole-rats at high ambient temperatures, the ventral surface was important for heat dissipation in Damaraland and highveld mole-rats. This study provides evidence of the variation and limitations of thermo-physiological mechanisms for three mole-rat species relative to their habitats. Information on physiological adaptations to particular habitats may inform predictive modelling of species movements, declines, and extinctions in response to a changing environment, such as climate change.     

Species turnover regulates leaf‐cutter ant densities in environmental gradients across the Brazilian Cerrado

Environmental changes resulting from Atta leaf‐cutter ant activities characterize them as ecosystem engineers of ecological and economic importance in multiple habitats. Although Atta effects depend strongly on colony density, there has been limited and inconsistent information available on their abundance and interspecific dominance in natural areas and across environmental gradients in the Brazilian Cerrado. Our study bridges this gap by testing the hypothesis that Atta nest density at genus level is high and relatively constant across locations regardless of vegetation type due to strong effects of dominant species turnover. To do so, we conducted a natural experiment surveying Atta nest abundance in five different vegetation types representing the environmental gradient from forest to savannah habitats found in the Cerrado. Our linear transect surveys covered 48.9 km in four well‐preserved areas across two Brazilian states in which we recorded 124 colonies. Of these, 84 nests belonged to A. laevigata and 40 to A. sexdens, the two dominant Atta species in the region. We also found no nests in 30% of the sampled area, which when combined with strong variation in density measured per transect indicates colonies tend to be aggregated in the landscape. Furthermore, we observed a strong dominant species turnover from forest habitats where 90% of nests belonged to A. sexdens to savannah habitats where 92% of nests were A. laevigata. Turnover effect was reflected in the absence of a significant difference in density between locations and vegetation types, indicating that density at genus level remains high and relatively constant regardless of nest aggregation. Our findings allow larger scale inferences about Atta effects and reveal new insights of their dynamics into natural areas that could affect plant species distribution and contribute to spatial heterogeneity of vegetation, having important implications for Cerrado conservation.     

Size and shape variability in relation to species differences and climatic gradients in the African rodent Oenomys

Aim The modern African murine rodent Oenomys is a semiarboreal genus characteristic of the rain forest zone. The size and shape geographical differentiation is studied in order to discuss the possible evolutionary patterns and constraints leading to this distribution. Location Two species of Oenomys have been previously recognized, corresponding to the West African forest block on the one hand and to the main forest block on the other hand. Both species have been sampled, and forty localities permit the study of the whole geographical range of Oenomys, from Guinea to Kenya. Methods A Fourier analysis applied to the outlines of the first upper and lower molars allows a quantification of the size and shape variations across the geographical range of Oenomys. Results This morphometrical analysis defines three morphological groups of Oenomys, corresponding to the West, Central, and East African forest zone. This result suggests the existence of an additional cryptic species. The Western group is characterized by broad asymmetrical molars and a small size. The Central African group has more elongated and larger molars while the Eastern African group displays extremely constricted molars and a small size. Main conclusion The shape can be considered as charactheristic of each group and its variations appear to be mostly related to phylogeny while size exhibits variations within each group related to climatic gradients. This discrepancy could be related to different genetic determinants for both characters, the shape being strongly genetically constrained while size can vary according to a wide range of environmental factors.     

Phylogeography of the widespread African puff adder (Bitis arietans) reveals multiple Pleistocene refugia in southern Africa

Evidence from numerous Pan‐African savannah mammals indicates that open‐habitat refugia existed in Africa during the Pleistocene, isolated by expanding tropical forests during warm and humid interglacial periods. However, comparative data from other taxonomic groups are currently lacking. We present a phylogeographic investigation of the African puff adder (Bitis arietans), a snake that occurs in open‐habitat formations throughout sub‐Saharan Africa. Multiple parapatric mitochondrial clades occur across the current distribution of B. arietans, including a widespread southern African clade that is subdivided into four separate clades. We investigated the historical processes responsible for generating these phylogeographic patterns in southern Africa using species distribution modelling and genetic approaches. Our results show that interior regions of South Africa became largely inhospitable for B. arietans during glacial maxima, whereas coastal and more northerly areas remained habitable. This corresponds well with the locations of refugia inferred from mitochondrial data using a continuous phylogeographic diffusion model. Analysis of data from five anonymous nuclear loci revealed broadly similar patterns to mtDNA. Secondary admixture was detected between previously isolated refugial populations. In some cases, this is limited to individuals occurring near mitochondrial clade contact zones, but in other cases, more extensive admixture is evident. Overall, our study reveals a complex history of refugial isolation and secondary expansion for puff adders and a mosaic of isolated refugia in southern Africa. We also identify key differences between the processes that drove isolation in B. arietans and those hypothesized for sympatric savannah mammals.     

Heterogeneity and concordance in locus‐specific differentiation and introgression between species of towhees

The maintenance or breakdown of reproductive isolation is an observable outcome of secondary contact between species. In cases where hybrids beyond the F1 are formed, the representation of each species' ancestry can vary dramatically among genomic regions. This genomic heterogeneity in ancestry and introgression can offer insight into evolutionary processes, particularly if introgression is compared in multiple hybrid zones. Similarly, considerable heterogeneity exists across the genome in the extent to which populations and species have diverged, reflecting the combined effects of different evolutionary processes on genetic variation. We studied hybridization across two hybrid zones of two phenotypically well‐differentiated bird species in Mexico (Pipilo maculatus and P. ocai), to investigate genomic heterogeneity in differentiation and introgression. Using genotyping‐by‐sequencing (GBS) and hierarchical Bayesian models, we genotyped 460 birds at over 41 000 single nucleotide polymorphism (SNP) loci. We identified loci exhibiting extreme introgression relative to the genome‐wide expectation using a Bayesian genomic cline model. We also estimated locus‐specific F_ST and identified loci with exceptionally high genetic divergence between the parental species. We found some concordance of locus‐specific introgression in the two independent hybrid zones (6–20% of extreme loci shared across zones), reflecting areas of the genome that experience similar gene flow when the species interact. Additionally, heterogeneity in introgression and divergence across the genome revealed another subset of loci under the influence of locally specific factors. These results are consistent with a history in which reproductive isolation has been influenced by a common set of loci in both hybrid zones, but where local environmental and stochastic factors also lead to genomic differentiation.     

Time,space and ecology: why some clades have more species than others

Aim We seek biotic and abiotic explanations for differences in lineage sizes of Afromontane sedges (Cyperaceae, Carex) and buttercups (Ranunculaceae, Ranunculus). Location Mountains of sub‐Saharan Africa and Madagascar. Methods We investigated differences in the species richness and diversification rates of 18 lineages of the pan‐temperate plant groups Carex and Ranunculus, established by long‐distance dispersal on African sky islands. We built generalized linear models to test the individual and the cumulative power of biotic and abiotic factors for predicting variation in the size of lineages. Tested variables were: ages of the lineages, their geographic distributions, number of mountain systems occupied, isolation/distance from ancestral areas, elevation range, number of vegetation zones and habitat types in which lineages are found, light requirement and water availability for each lineage, and the sum of the habitat factors, representing habitat heterogeneity. Habitat conservatism was measured by the overlap in habitats among the species within each lineage. Diversification rate changes were investigated using ‘laser’ in R. Results The number of Carex and Ranunculus lineages on the African mountains accumulated gradually through time. The size of these lineages could best be explained by a model combining age and distribution together with a measure of environmental heterogeneity (either elevation and water availability or habitat heterogeneity). Extensive overlap in environmental characteristics and distribution ranges among the species indicates a relatively high degree of conservatism of these characters. Main conclusions Lineages that are species‐rich are those that have the ability and time to occupy many mountain regions and a wide range of habitats. If allopatric or ecological speciation plays a role, then secondary dispersal and/or niche expansion soon obscures the patterns that may have existed at the point of speciation.     

Response of rove beetles (Staphylinidae) to various habitat types and change in Southern Mexico

We evaluated changes in levels of diversity of copro-necrophilous staphylinids attracted to piles of cattle dung and rat carrion in four contrasting habitats (continuous oak forest, oak forest patches, savannah and ravines) in southeastern Mexico during 2005 and 2006. In total, 181 morpho-species (N = 9,875 individuals) of Staphylinidae were recorded, of which 40 were coprophiles, 98 were necrophiles, and 43 were present in both substrates. Ten species accounted for 65% of the total number of individuals, 68 species were represented by singletons, whereas 103 species registered intermediate abundances. Less disturbed habitats recorded higher levels of beetle diversity. A strong seasonality effect was recorded for necrophiles, but not for coprophiles. A beta diversity analysis suggested that continuous oak forest registered the lowest fauna similarity when contrasted to other habitats; yet beetle composition among oak forest patches, savannah and ravine remained comparable. Staphylinidae body size and trophic guilds differed significantly among habitats. The results of this study suggest that key habitats such as ravines may represent a more permanent and predictable habitat for beetles in highly seasonal landscapes, even at early stages, because this habitat is characterized by a slower turnover of Staphylinidae species than in the case of tropical oak patches or savannah habitats.     

New microsatellite markers for the bush rat,Rattus fuscipes greyii: characterization and cross‐species amplification

We describe here 16 new microsatellite markers for the bush rat, Rattus fuscipes greyii, and characterize their cross‐species amplification within the Australian Rattus and at a greater level of divergence in Rattus rattus and Rattus norvegicus. Within R. f. greyii, all of the loci are highly polymorphic, with six to 24 alleles per locus across the species range and expected heterozygosity ranging from 0.48 to 0.90 per locus within a sample of 24 rats from a large population on Kangaroo Island. Cross‐species amplification rates were approximately 87% within the Australian Rattus and approximately 50% within R. rattus and R. norvegicus. These loci are highly polymorphic with a high success rate of cross‐species amplification, making them potentially useful for a wide range of genetic studies.     

Phylogeography in continuous space: coupling species distribution models and circuit theory to assess the effect of contiguous migration at different climatic periods on genetic differentiation in Busseola fusca (Lepidoptera: Noctuidae)

Current population genetic models fail to cope with genetic differentiation for species with large, contiguous and heterogeneous distribution. We show that in such a case, genetic differentiation can be predicted at equilibrium by circuit theory, where conductance corresponds to abundance in species distribution models (SDMs). Circuit‐SDM approach was used for the phylogeographic study of the lepidopteran cereal stemborer Busseola fuscaFüller (Noctuidae) across sub‐Saharan Africa. Species abundance was surveyed across its distribution range. SDMs were optimized and selected by cross‐validation. Relationship between observed matrices of genetic differentiation between individuals, and between matrices of resistance distance was assessed through Mantel tests and redundancy discriminant analyses (RDAs). A total of 628 individuals from 130 localities in 17 countries were genotyped at seven microsatellite loci. Six population clusters were found based on a Bayesian analysis. The eastern margin of Dahomey gap between East and West Africa was the main factor of genetic differentiation. The SDM projections at present, last interglacial and last glacial maximum periods were used for the estimation of circuit resistance between locations of genotyped individuals. For all periods of time, when using either all individuals or only East African individuals, partial Mantel r and RDA conditioning on geographic distance were found significant. Under future projections (year 2080), partial r and RDA significance were different. From this study, it is concluded that analytical solutions provided by circuit theory are useful for the evolutionary management of populations and for phylogeographic analysis when coalescence times are not accessible by approximate Bayesian simulations.     

Geographically widespread mitochondrial lineages of the African saw-wings inconsistent with species boundaries

The African saw-wings (genus Psalidoprocne) are a group of swallows endemic to sub-Saharan Africa. Although currently described as five species with several subspecies, the taxonomy of the saw-wings is unclear. We sequenced two mitochondrial genes (ND2 and cytb; 1 717 sites) from 20 individuals in order to investigate phylogenetic relationships across the range of Psalidoprocne. We obtained similar results from maximum likelihood (RAxML) and Bayesian (BEAST) phylogenetic analyses, which reveal multiple well-supported mitochondrial clades in the genus. The geographic overlap of distinct lineages suggests reproductive isolation, although these clades do not correspond entirely to current species designations.     

Diet overlap among three sympatric African annual killifish species Nothobranchius spp. from Mozambique

The diet patterns of three Nothobranchius species (N. furzeri, N. orthonotus and N. rachovii), small, short‐lived annual killifish from temporary pools in African savannah were investigated. Four sites with contrasting fish density and water surface area were sampled in 2008 and 2009 in southern Mozambique. Stomach content analysis showed that all the species examined were generalists, with diets largely based on aquatic invertebrates. The same invertebrate prey categories were consumed by all three species, but their relative proportions varied across species. The largest species, N. orthonotus, showed the most distinct diet and consumed vertebrates (juvenile lungfish Protopterus annectens and larval Amphibia) and a relatively high proportion of Odonata, Coleoptera and Ephemeroptera larvae. The diet of the other two species (N. furzeri and N. rachovii) showed a stronger overlap, did not include vertebrates, but was rich in small crustaceans (Cladocera, Copepoda, Ostracoda and Conchostraca). Mosquito (Diptera) larvae formed only a negligible part of the diet of all the three species.     

Population genetic structure of the malaria mosquito Anopheles arabiensis across Nigeria suggests range expansion

Ten microsatellite loci, four located within and six outside chromosome inversions, were employed to study the genetic structure of Anopheles arabiensis across the ecological zones of Nigeria (arid savannah in the north gradually turns into humid forest in the south). Regardless of location within or outside inversions, genetic variability at all loci was characterized by a reduction in both the number of alleles per locus and heterozygosity from savannah to forest. Across all loci, all but one allele in the forest also occurred in the savannah, whereas at least 78 alleles in the savannah were missing in the forest. Genetic differentiation increased with geographical distance; consequently, genetic distances between zones exceeded those within zones. The largest genetic distances were between localities at the extremes of the transect (range F(ST) = 0.196-0.258 and R(ST) = 0.183-0.468) and were as large as those between A. arabiensis and Anopheles gambiae s.s. Gene flow across the country was very low, so that Nm between the extremes of the transect was < 1. These data suggest that A. arabiensis has extended its range from the savannah into the forest during which it experienced a reduction in effective population size due to sequential founder effects. Gene flow post range expansion appears too restricted by geographical distance to homogenize the gene pool of A. arabiensis across Nigeria.     

Patterns of contact call differentiation in the panmictic East African Abyssinian White‐eye Zosterops abyssinicus (Aves: Passeriformes)

Species distribution patterns range from highly disjunct to continuous, depending on their ecological demands and the availability of respective habitats. East African savannahs are mostly interconnected and ecologically comparatively homogenous and thus provide a prerequisite for a rather panmictic distribution pattern for species occurring in this habitat. The Abyssinian white‐eye Zosterops abyssinicus is a savannah inhabiting bird species, representing such a continuous distribution. This species occurs in high abundances and is very mobile, and past population genetic studies have suggested that gene flow is high and genetic differentiation is low even across relatively large geographic distances. Further, only little morphological differences were found. In order to test for potential divergence in acoustic traits despite its interconnected geographic distribution, we analyzed 2795 contact calls of Z. abyssinicus, which were recorded at 19 sites across Kenya. Our data indicate weak, but significant differentiation in call characteristics across latitudinal gradients. We found strong changes in call characteristics in populations where Z. abyssinicus occurs in sympatry with its highland congener, Zosterops poliogaster. However, the changes in call characteristics in sympatry were in different directions and lead to strong differentiation of the sympatric populations to other conspecific populations potentially representing a case of cascade reinforcement. The detected spatial gradients likely result from ecological differences and balancing effects of natural and sexual selection.     

Characterization of tetranucleotide microsatellite loci in the African Savannah Elephant (Loxodonta africana africana)

Most African elephant (Loxodonta africana africana) populations are isolated and thus threatened by a loss of genetic diversity. As a consequence, genetic analysis of African elephant populations will play an increasing role in their conservation, and microsatellite loci will be an important tool in these analyses. Previously published sets of polymorphic microsatellites developed for African elephants are all dinucleotide repeats, which are prone to typing error. Here, we characterize 11 tetranucleotide microsatellite loci in the African elephant. All loci were polymorphic in 32 faecal samples and two tissue samples from 33 individual African savannah elephants.     

Molecular phylogeny of African hinge‐back tortoises (Kinixys): implications for phylogeography and taxonomy (Testudines: Testudinidae)

We examine the phylogeography, phylogeny and taxonomy of hinge‐back tortoises using a comprehensive sampling of all currently recognized Kinixys species and subspecies and sequence data of three mitochondrial DNA fragments (2273 bp: 12S rRNA, ND4 + adjacent DNA coding for tRNAs, cytb) and three nuclear loci (2569 bp: C‐mos, ODC, R35). Combined and individual analyses of the two data sets using Bayesian and Maximum Likelihood methods suggest that the savannah species of Kinixys are paraphyletic with respect to the rainforest species K. homeana and K. erosa, and that the rainforest species may be derived from a savannah‐living ancestor. The previously recognized savannah species K. belliana was a conglomerate of three deeply divergent clades that we treat here as distinct species. We restrict the name K. belliana (Gray, 1830) to hinge‐back tortoises ranging from Angola to Burundi, while five‐clawed hinge‐back tortoises from the northernmost part of the formerly recognized range of K. belliana, together with four‐clawed tortoises from West Africa, are assigned to the species K. nogueyi (Lataste, 1886). These two species are allied to K. spekii, whereas Southeast African and Malagasy hinge‐back tortoises formerly lumped together with K. belliana represent the distinct species K. zombensis Hewitt, 1931, which is sister to K. lobatsiana. The latter two species together constitute the sister group of the rainforest species K. homeana and K. erosa. Mitochondrial data suggest that K. natalensis has a basal phylogenetic position in a clade embracing K. belliana sensu stricto, K. nogueyi and K. spekii, while nuclear data and the two data sets combined favour a sister group relationship of K. natalensis to all other hinge‐back tortoises. Phylogeographic structure is present in all wide‐ranging species and correlates in K. homeana and K. erosa with the Dahomey Gap and former rainforest refugia. The Malagasy population of K. zombensis is weakly differentiated from its South African conspecifics and further sampling is needed to determine whether there is support for the subspecific distinctness of Malagasy tortoises.