Field collections reveal that São Tomé is the Afrotropical island with the highest diversity of drosophilid flies (Diptera: Drosophilidae)

Summary

The Drosophilid fauna has been less investigated in the Atlantic Afrotropical islands than in the Indian Ocean. Located about 250 km from the continent, the volcanic island of São Tomé has been colonized mostly by natural means, probably by the wind, since the emergence of the island about 15 million years ago, and presumably also by anthropogenic transportation of invasive and domestic species. To date, 37 different Drosophilid species have been mentioned from São Tomé. The present work extends this list to 80 species. The genera Zygothrica, Phorticella and Hypselothyrea are newly recorded from the island. Among these 80 species, only 12 are putatively introduced by human activities, suggesting the preponderance of natural arrivals. Compared to other islands, São Tomé harbours a high diversity of drosophilids. At least 14 species are supposed to be endemic. Future molecular comparisons between the island flies and their continental relatives will probably help to identify other endemic species. The high diversity observed in São Tomé is certainly due to the large size of the island, and to the presence of vast natural altitudinal forests offering a variety of possible habitats. Further collections are likely to lead to an increase of the species list. From now, São Tomé island appears as an excellent laboratory for studying the ecology and evolution of the Drosophila model.     

Freshwater snails of São Tomé, with special reference to Bulinus forskalii (Ehrenberg), host of Schistosoma intercalatum

São Tomé Island has 3 known taxa of freshwater gastropod, here identified to species for the first time; Neritina afra Sowerby, Ferrissia eburnensis Binder and a distinctive form of Bulinus forskalii (Ehrenberg). The Bulinus acts as intermediate host for the parasite Schistosoma intercalatum Fisher, the cause of human schistosomiasis in foci of infection detected in recent years on São Tomé. A morphological characterization of this snail is presented, in respect of the shell, radula and copulatory organ. It is compared with B. forskalii populations sampled on the African mainland (Nigeria, Cameroon, Gabon and Angola) and with related taxa. Despite differences in the shell from the commonly found form of B. forskalii it seems appropriate to identify the São Tomé population as an extreme conchological variant of this taxon.     

New species in the fern genus Dryopteris (Dryopteridaceae) from the islands in the Gulf of Guinea (West Africa)

Three new species of Dryopteris, D. cicatricata J.P. Roux and D. caperata J.P. Roux from São Tomé and D. aurantiaca J.P. Roux from Annobón are described. All three taxa appear to be local endemics. A key to the Dryopteris species occurring on the islands in the Gulf of Guinea is provided.     

Population estimates of the breeding birds of the Tinhosas islands (Gulf of Guinea), the only major seabird colony of the eastern tropical Atlantic

The Tinhosas islands, in São Tomé e Príncipe, host the most important seabird breeding colony in the Gulf of Guinea, but information on its conservation status was hitherto unpublished or anecdotal, the last assessment having been performed in 1997. A two-day expedition to the Tinhosas islands was undertaken to estimate the status of breeding seabirds in 2013. Four of the five seabird species known to breed in São Tomé e Príncipe, namely Brown Booby Sula leucogaster, Sooty Tern Onychoprion fuscatus, Brown Noddy Anous stolidus and Black Noddy Anous minutus, occur on the Tinhosas. A decrease of 80% in Brown Booby numbers, possibly due to occasional exploitation, and a 30% increase in Sooty Tern and Black Noddy numbers, were found compared to 1997 data although survey methods differed. Breeding of Brown Noddy and Madeiran Storm-petrel Hydrobates castro remains unconfirmed. Our estimates confirmed that BirdLife International Important Bird and Biodiversity Area criteria are met for at least one species, the Sooty Tern. The islands are not legally protected, nonetheless, apart from moderate levels of disturbance by fishermen who land on Tinhosa Grande, no alien species were seen, and no immediate threats to the Tinhosas colony were detected. Multiple visits within and between years are recommended, to census breeders, monitor threats and establish breeding phenologies.     

Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line

We have used two paralogous genes (Amyrel and Amy) of the amylase multigene family to reconstruct the phylogeny of the nine Drosophila melanogaster subgroup sister species, including D. santomea, the newly discovered endemic from São Tomé island. The evolutionary divergence of these genes is of special interest as it is suspected to result from physiological evolution via gene duplication. This paper describes the relationship between the geographical origin of the various strains and the patterns of mating and phylogeny, focusing on the evolution of D. santomea and its relationship to other species and their niches. The Amyrel and Amy data indicate that, contrary to expectations, the sympatric insular D. yakuba population is less closely related to D. santomea than allopatric mainland ones, suggesting that the extant insular D. yakuba population on São Tomé results from a recent secondary colonization. Data for sympatric and allopatric D. yakuba suggest that D. santomea arose from a mainland D. yakuba parental stock when montane habitats of the Cameroon volcanic line extended to lower altitudes during colder and less humid periods. Despite their different modes of evolution and different functions, the Amyrel and Amy genes provide remarkably consistent topologies and hence reflect the same history, that of the species.     

Occurrence and abundance of three larval codlet species (Bregmacerotidae, Teleostei) in the Southwest Atlantic Ocean (12–22°S)

There are still only a few studies related to Bregmacerotidae larvae in Brazil, although these larvae are frequently collected in oceanic ichthyoplankton samples. Thus this study analyzes the occurrence and abundance of Bregmaceros larvae along the Brazilian central coast and describes larval characteristics. During three oceanographic cruises samples were collected between the Real River (12°S) and the São Tomé Cape (22°S). Oblique hauls were conducted from a maximum depth of 200 m, using bongo nets of 330‐ and 500‐μm mesh size. Among the 951 bregmacerotids collected, three species were identified corresponding to 89%Bregmaceros atlanticus, 8%Bregmaceros cantori and 3%Bregmaceros n. sp. B. atlanticus was widely distributed along the study area and was more frequent in stations situated beyond the 200‐m isobath; this species was more abundant during the winter, showing a peak of density between Vitória and the São Tomé Cape (355 larvae per 10 m²). Bregmaceros cantori densities were very similar during the three cruises; the highest value (25.6 larvae per 10 m²) was recorded during the winter and higher concentrations were observed in neritic stations along the 200‐m isobath. Bregmaceros n. sp. was rare in collections made during the three cruises; it was concentrated along the Bahia coast (12–18°S), and was more frequent in stations situated in the oceanic region. Bregmaceros atlanticus varying from 2.0 to 6.0 mm and Bregmaceros n. sp. larvae varying from 3.0 to 6.0 mm were present in all cruises, indicating that they spawn year‐round. Bregmaceros cantori did not show a distribution pattern among the different length classes, probably associated with the fact that this species has a coastal distribution.     

Freshwater paths across the ocean: molecular phylogeny of the frog Ptychadena newtoni gives insights into amphibian colonization of oceanic islands

Aim Amphibians are a model group for studies of the biogeographical origins of salt‐intolerant taxa on oceanic islands. We used the Gulf of Guinea islands to explore the biogeographical origins of island endemism of one species of frog, and used this to gain insights into potential colonization mechanisms. Location São Tomé and Príncipe, two of the four major islands in the Gulf of Guinea, West Africa, are truly oceanic and have an exceptionally high biodiversity. Methods Mitochondrial DNA is used to test the endemic status of a frog from São Tomé and compare it with congeneric taxa from tropical Africa. Existing data on surface currents, surface salinity, atmospheric circulation and bird migration in the Gulf of Guinea are summarized to address hypotheses concerning colonization mechanisms. Results The endemic status of Ptychadena newtoni (Bocage) is supported here by mitochondrial DNA sequences, and analysis of this and other molecular data indicates that an East African species close to Ptychadena mascareniensis (Duméril and Bibron) is its nearest relative. We refute the possibility that this population was anthropogenically introduced, in favour of a natural dispersal mechanism. Main conclusions With six endemic frogs and one caecilian, the Gulf of Guinea islands harbour a diverse amphibian fauna. Five of these species appear to have their closest relatives in East Africa. Insufficient evidence exists for transportation by storms, birds or rafts alone. However, we propose a synergy of rafting, favourable surface currents and a reduction in salinity of surface waters. Catastrophic events, or wet periods in climatic history, could allow freshwater paths to open far enough to enable continental flora and fauna to reach these and other isolated oceanic islands.     

Diversity and composition of cultivable gut bacteria in an endemic island bird and its mainland sister species

The study of island biodiversity has inspired many advances in evolutionary biology. However, whether patterns of microorganism diversity are influenced by insularity is poorly understood. In particular, microorganisms that live in symbiotic association, such as the microbiota that inhabit the gastrointestinal tract of bigger animals, are subjected to demographic and coevolutionary processes that may add complexity to the common expectation of impoverished diversity on oceanic islands. Here, we explore this topic by studying the cultivable gut bacteria of two sister species of birds, from São Tomé island and nearby mainland Gabon, the endemic São Tomé thrush Turdus olivaceofuscus and the African thrush Turdus pelios. We found no differences in the diversity of cultivable gut bacteria between these thrushes, suggesting that, unlike what is commonly found for macrofauna, insularity might not represent a strong constraint for gut bacterial diversity. Although further research on complete gut bacterial communities and a broader range of species and areas is needed, our initial results suggest that the cultivable gut microbial community may bypass the diversity loss associated with island colonization. This could arise from intrinsic factors such as their large population sizes within hosts and low rates of extinction. Furthermore, as gut communities are composed mainly by mutualistic bacteria, diversifying selection (against an impoverished bacterial community), may counteract the diversity loss brought about by the stochastic and demographic effects of the founder process.     

Genetic structure of Anopheles gambiae (Diptera: Culicidae) in São Tomé and Príncipe (West Africa): implications for malaria control

The impact of a vector eradication programme, conducted in the 1980s, on Anopheles gambiae populations from the islands of São Tomé and Príncipe, was evaluated by microsatellite DNA analysis. Significant genetic differentiation was observed within and between the two islands and between the islands and a population from Gabon, suggesting a degree of isolation between them. Large estimates of long‐term N_e suggested that the control programme did not affect the effective population size of the vector. Heterozygosity tests were also not consistent with a recent bottleneck.     

Male size does not affect mating success (of Anopheles gambiae in São Tomé)

Abstract For malaria control, the utility of transgenic vector Anopheles mosquitoes (Diptera: Culicidae) refractory to Plasmodium transmission, will depend on their interbreeding with the wild vector population. In many species, larger males are more successful in obtaining mates. In São Tomé island, we determined that size did not affect mating success of male Anopheles gambiae Giles sensu stricto, the main malaria vector in tropical Africa. Also we showed that larval intraspecific competition is probably insignificant in this population of An. gambiae. Thus, the potential success of transgenic An. gambiae is unlikely to be affected by size selection under field conditions.     

Taxonomic review of Bourguyiinae,cladistic analysis,and a new hypothesis of biogeographic relationships of the Brazilian Atlantic Rainforest (Arachnida: Opiliones,Gonyleptidae)

The subfamily Bourguyiinae Mello‐Leitão, 1923 (Gonyleptidae) is revised, and both phylogenetic and biogeographic hypotheses are proposed. Bourguyiinae is monophyletic, and is the sister group of the remainder of the Gonyleptidae species used for analysis, except for the Metasarcinae, which collectively is the sister group of Metavononoides orientalis Mello‐Leitão, 1923 (Cosmetidae). Bourguyiinae is divided into two genera: Bourguyia (six species) and Asarcus (four species). The genus‐level synonyms proposed here are as follows: Caldasius, Styloleptes, and Stylopisthos are junior synonyms of Bourguyia; Bogdana, Cnemoleptes, and Opisthoplites are junior synonyms of Asarcus. The species synonyms proposed here are as follows: Afranius amarali Mello‐Leitão, 1934 is a junior synonym of Bourguyia albiornata Mello‐Leitão, 1923 ; Drastus hamatus Roewer, 1943 and Styloleptes conspersus Piza, 1943 are junior synonyms of Bourguyia trochanteralis Roewer, 1930 ; Asarcus corallipes Simon, 1879 , Asarcus lutescens Sørensen, 1884 , Asarcus pallidus Mello‐Leitão, 1923 , and Opisthoplites ypsilon Sørensen, 1884 are junior synonyms of Asarcus longipes Kollar in Koch, 1839 ; Asarcus nigriconspersus Soares & Soares, 1945 is a junior synonym of Asarcus ingenuus Melo‐Leitão, 1940. New species described are: Bourguyia bocaina sp. nov. (Serra da Bocaina, São José do Barreiro, São Paulo), Bourguyia vinosa sp. nov. (E.B. Boracéia, Salesópolis, São Paulo), and Asarcus putunaberaba sp. nov. (Parque Nacional do Caparaó, Alto Caparaó, Minas Gerais). Bourguyiinae is endemic to the Atlantic Rainforest in the Brazilian states of Minas Gerais, Rio de Janeiro, São Paulo, and Paraná. Based on the modified data matrix of Pinto‐da‐Rocha et al., we propose a new biogeographical hypothesis for the Atlantic Rainforest. We suggest that Bourguyiinae species were originally distributed from the coastal region of Paraná to the north of Rio de Janeiro and south‐east of Minas Gerais, with subsequent dispersals both to northern and southern areas. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 319–362.     

Selection of non‐target tephritids for risk evaluation in classical biocontrol programmes against the olive fruit fly

The olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), is the key pest of olives (Olea europaea L.). Classical biological control against this insect was previously attempted in Spain with Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae), with very limited success. Other parasitoids are now available for new classical biological control programmes. Before release of exotic parasitoids, an assessment of their potential impact on non‐target species is required. Surveys were conducted in different olive groves in south‐eastern Madrid to study wild tephritids associated with Asteraceae plants. We recorded plant species and their abundance and collected flower heads to identify and quantify tephritid species. Fruits from Rosa canina L. were also collected. After a multicriteria analysis (MCA), we propose Urophora hispanica Strobl, U. stylata (Fabricius) and Carpomya schineri (Loew) as candidates for further risk assessment experiments. Additional information on new associations between tephritid flies and Asteraceae plants and on autochthonous Hymenoptera parasitizing tephritids is provided.     

Synopsis of <Emphasis Type="Italic">Acalypha</Emphasis> (Euphorbiaceae) of West Tropical Africa,including Cameroon,Chad, Equatorial Guinea,Gabon, and São Tomé and Príncipe

This work features a critical review of the Acalypha species of the West Tropical Africa, including Cameroon, Chad, Equatorial Guinea, Gabon, and São Tomé and Príncipe. As a result, 15 native species, and four that appear to be naturalized, are accepted, and 17 names are considered as synonyms. Comprehensive nomenclatural information is supplied, and nine lectotypes and one neotype are designated. An identification key is also provided, as well as two original illustrations.     

Reed frog diversification in the Gulf of Guinea: Overseas dispersal,the progression rule,and in situ speciation

Oceanic islands accumulate endemic species when new colonists diverge from source populations or by in situ diversification of resident island endemics. The relative importance of dispersal versus in situ speciation in generating diversity on islands varies with a number of archipelago characteristics including island size, age, and remoteness. Here, we characterize interisland dispersal and in situ speciation in frogs endemic to the Gulf of Guinea islands. Using mitochondrial sequence and genome‐wide single‐nucleotide polymorphism data, we demonstrate that dispersal proceeded from the younger island (São Tomé) to the older island (Príncipe) indicating that for organisms that disperse overseas on rafts, dispersal between islands may be determined by ocean currents and not island age. We find that dispersal between the islands is not ongoing, resulting in genotypically distinct but phenotypically similar lineages on the two islands. Finally, we demonstrate that in situ diversification on São Tomé Island likely proceeded in allopatry due to the geographic separation of breeding sites, resulting in phenotypically distinct species. We find evidence of hybridization between the species where their ranges are sympatric and the hybrid zone coincides with a transition from agricultural land to primary forest, indicating that anthropogenic development may have facilitated secondary contact between previously allopatric species.     

Trans‐Atlantic,trans‐Pacific and trans‐Indian Ocean dispersal in the small Gondwanan Laurales family Hernandiaceae

Aim To investigate the historical biogeography of the pantropical flowering plant family Hernandiaceae (Laurales), which today comprises 62 species in five genera. Location Hernandiaceae occur in Africa (9 species), Madagascar (4), the Neotropics (25), Australia (3), southern China, Indochina, Malesia, and on numerous Pacific Islands (32). These numbers include two widespread species, Hernandia nymphaeifolia, which ranges from East Africa to the Ogasawara Islands and New Caledonia, and Gyrocarpus americanus, thought to have a pantropical range. Methods We sampled 37 species from all genera, the widespread ones with multiple accessions, for a chloroplast DNA matrix of 2210 aligned nucleotides, and used maximum likelihood to infer species relationships. Divergence time estimation relied on an uncorrelated‐rates relaxed molecular clock calibrated with outgroup fossils of Lauraceae and Monimiaceae. Results The deepest split in the family is between a predominantly African–Madagascan–Malesian lineage comprising Hazomalania, Hernandia and Illigera, and an African–Neotropical lineage comprising Gyrocarpus and Sparattanthelium; this split may be 122 (110–134) Myr old. The stem lineages of the five genera date back at least to the Palaeocene, but six splits associated with transoceanic range disjunctions date only to the Oligocene and Miocene, implying long‐distance dispersal. It is inferred that Hernandia beninensis reached the West African islands of São Tomé and Bioko from the West Indies or the Guianas; Hernandia dispersed across the Pacific; and Illigera madagascariensis reached Madagascar from across the Indian Ocean. Main conclusions The disjunct ranges and divergence times of sister clades in the Hernandiaceae are partly congruent with the break‐up of West Gondwana, but mostly with later transoceanic dispersal. An exceptional ability to establish following prolonged oceanic dispersal may be largely responsible for the evolutionary persistence of this small clade.     

Sexual isolation between two sibling species with overlapping ranges: Drosophila santomea and Drosophila yakuba

Abstract.— .Drosophila yakuba is widespread in Africa, whereas D. santomea, its newly discovered sister species, is endemic to the volcanic island of São Tomé in the Gulf of Guinea. Drosophila santomea probably formed after colonization of the island by a D. yakuba‐like ancestor. The species presently have overlapping ranges on the mountain Pico do São Tome, with some hybridization occurring in this region. Sexual isolation between the species is uniformly high regardless of the source of the populations, and, as in many pairs of Drosophila species, is asymmetrical, so that hybridizations occur much more readily in one direction than the other. Despite the fact that these species meet many of the conditions required for the evolution of reinforcement (the elevation of sexual isolation by natural selection to avoid maladaptive interspecific hybridization), there is no evidence that sexual isolation between the species is highest in the zone of overlap. Sexual isolation is due to evolutionary changes in both female preference for heterospecific males and in the vigor with which males court heterospecific females. Heterospecific matings are also slower to take place than are homospecific matings, constituting another possible form of reproductive isolation. Genetic studies show that, when tested with females of either species, male hybrids having a D. santomea X chromosome mate much less frequently with females of either species than do males having a D. yakuba X chromosome, suggesting that the interaction between the D. santomea X chromosome and the D. yakuba genome causes behavioral sterility. Hybrid F₁ females mate readily with males of either species, so that sexual isolation in this sex is completely recessive, a phenomenon seen in other Drosophila species. There has also been significant evolutionary change in the duration of copulation between these species; this difference involves genetic changes in both sexes, with at least two genes responsible in males and at least one in females.     

An updated assessment of the seabird populations breeding at Príncipe and Tinhosas

The Príncipe Autonomous Region is recognised as a marine biodiversity hotspot, although little is known about the status of its marine fauna. It holds most breeding seabirds of the tropical eastern Atlantic Ocean. Based on anecdotal accounts of increased fishing and seabird harvesting, regular monitoring of seabird populations is considered a priority. Therefore, a survey of Príncipe’s seabird colonies was conducted in 2017. The results revealed that the more accessible seabird colonies have disappeared. Around Príncipe, Boné de Joquei is the present main stronghold for Brown Boobies Sula leucogaster and White-tailed Tropicbirds Phaethon lepturus. The Tinhosas islands hold an estimated 300 000 seabirds, predominantly Sooty Terns Onychoprion fuscatus, but also Brown Boobies, Black Noddies Anous minutus and Brown Noddies Anous stolidus. Long-term multi-annual monitoring is needed to understand the breeding phenology of each species and to better assess population trends. Ensuring a protective status for both Tinhosas and the seabirds under national legislation is a key priority for future conservation policy in São Tomé and Príncipe.     

Can Management Improve the Value of Shade Plantations for the Endemic Species of São Tomé Island?

Cocoa and coffee are among the most valuable tropical crops, with much of their production in areas of high biodiversity. Although this could suggest a conflict between agricultural expansion and biodiversity conservation, these crops are normally grown in shade plantations—a more biodiversity‐friendly agroforestry system. Using São Tomé Island as a case study, we examined if shade plantation can benefit biodiversity by protecting extinction‐prone island endemic species. We found that shade plantations held rich assemblages, even in comparison with forest: we estimated 30 bird and 74 tree species occurring in plantations compared to 24 bird and 108 tree species in forests. However, the structure of the assemblages was significantly different between ecosystems, with an average dissimilarity of 33.8 percent and 87.9 percent for birds and trees, respectively. Shade plantations had consistently less endemic species than the forest; we estimated a drop from 17 to 13 in birds and from 17 to 3 in trees. We also found that despite marked differences in the response of bird species to the vegetation characteristics of shade plantations, there was a strong positive link between aboveground tree biomass and endemic species richness and abundance. These results show that shade plantations hold assemblages impoverished in endemic species, but that management can improve their value for the conservation of these species. Finally, we suggest that biodiversity‐friendly certification and carbon markets are used to implement and guarantee the long‐term economical sustainability of practices that favor the endemic species in São Tomé's shade plantations.     

Fatal toxoplasmosis in a southern muriqui (Brachyteles arachnoides) from São Paulo state,Brazil: Pathological,immunohistochemical, and molecular characterization

We report the pathological, immunohistochemical, and molecular features of fatal acute systemic toxoplasmosis in an adult, female, free‐living southern muriqui (Brachyteles arachnoides) from São Paulo state, Brazil. PCR‐RFLP genotyping analysis identified the #21 genotype of Toxoplasma gondii. This represents the first report of acute toxoplasmosis involving this genotype in humans and animals.     

Hisonotus devidei,a new species from the São Francisco basin,Brazil (Siluriformes: Loricariidae)

A recent expedition to headwaters of the Rio Pandeiros, a left‐bank tributary of the Rio São Francisco revealed the presence of a fourth species of Hisonotus from that basin. Hisonotus devidei sp. nov. differs from congeners by the presence of conspicuous dark blotches of distinct shapes irregularly arranged along lateral and dorsal surfaces of the body and scattered throughout all fins, by possessing small plates in lateral portions of the abdomen and adjacent areas between pelvic fins without development of dermal plates and by morphometric ratios. The putative phylogenetic placement of the new species is discussed based on morphological comparisons with species of related Hypoptopomatinae genera and the Hisonotus species diversity within the Rio São Francisco Basin is compared with that of adjacent basins.