RESEARCH ARTICLES
http://dx.doi.org/10.17159/ sajs.2016/20160070

 

Implications of summer breeding frogs from Langebaanweg, South Africa: Regional climate evolution at 5.1 mya

 

 

Thalassa Matthews^I; G. John Measey^II; David L. Roberts ^{† , III}

^IDST-NRF Centre of Excellence for Palaeontology, Iziko South African Museum, Cape Town, South Africa
^IICentre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University Stellenbosch, South Africa
^IIIDepartment of Geography, University of the Free State, Bloemfontein, South Africa

Correspondence

 

 

---

ABSTRACT

No direct palaeoclimatic proxies have been available to indicate the seasonality or amount of rainfall on the west coast of southern Africa during the Early Pliocene. The Benguela Upwelling System (BUS) is today one of the factors responsible for the present-day aridity on the west coast of southern Africa. The initiation of the BUS is frequently linked to the entrenchment of aridity and the establishment of the current winter rainfall pattern on the west coast; however, marine proxies are inconclusive regarding the effects of past fluctuations in the BUS and sea surface temperatures on the rainfall regime. Neither the fossil evidence nor the fact that plants using the C₃ photosynthetic pathway predominate at this time, provide direct evidence of winter rainfall at Langebaanweg. We challenge certain assumptions which are commonly made in the literature regarding the timing of inception of a winter rainfall regime on the west coast and the onset of aridity in the Langebaan region, and provide new evidence as to seasonality of rainfall at Langebaanweg in the Early Pliocene. Herein, the identification of frog species from the genus Ptychadena from Langebaanweg provides new and compelling evidence for a summer rainfall regime, or of at least significant summer rainfall, at 5.1 mya in the southwestern Cape of South Africa.
SIGNIFICANCE:
• Advances understanding of the evolution of the winter rainfall zone on the west coast of South Africa
• Assesses evidence for the inception of aridity and a winter rainfall regime on the west coast of South Africa
• Fossil Ptychadenidae from the Early Pliocene site of Langebaanweg provide evidence for a summer rainfall regime at 5.1 mya on the west coast of the southwestern Cape.

Keywords: palaeoclimate; Ptychadena; Summer Rainfall Zone; Early Pliocene; fossil frogs

---

 

 

Introduction

Southern Africa is a predominantly summer rainfall region but the Winter Rainfall Zone (WRZ) situated along the southwestern and southern tip of the African continent, lying at the boundary between southern hemisphere temperate and tropical climate systems, is an exception (Figure 1). Evidence for the inception, geographical extent, intensity and fluctuations of the WRZ prior to the last glacial period is currently fragmented through both time and space, and a coherent understanding of the evolution of this ecosystem, unique in sub-Saharan Africa, has not been attained.¹ Although progress has been made in understanding climate change and rainfall seasonality in the Late Quaternary,^2-5 the fluctuations of these variables over the Neogene are complex and incompletely understood. The Neogene terrestrial fossil record is sporadic and incomplete as a result of the lack of preservation of terrestrial organic materials and thus direct climatic proxies, deposits which are problematic in terms of dating, and a lack of understanding of the geomorphological evolution of the subcontinent.^5,6 Much therefore remains to be elucidated about the inception and evolution of the WRZ. In this paper, we challenge certain assumptions which are commonly made in the literature regarding the inception of a winter rainfall regime on the west coast and the onset of aridity in the Langebaan region, and provide new evidence for rainfall seasonality at Langebaanweg in the Early Pliocene.

The Early Pliocene (~5.1 million years ago (mya)) site of Langebaanweg (LBW) situated on the southwestern coast of South Africa (Figure 1), is a remarkably rich and world-renowned vertebrate fossil site, representing a time period when fossil assemblages are particularly rare in sub-Saharan Africa.⁷ LBW is the site of first appearance in the fossil record for numerous taxa, including large and small mammals, birds, reptiles and amphibians.^7-10 LBW sheds light on the critical period during which tectonism led to the latitudinal migration of climate belts, which resulted in widespread reorganisation in atmospheric and ocean circulation.¹¹ These events were characterised by a more humid episode, with modern aridity becoming established only in the later Pliocene, between ~4 mya and 2.8 mya.¹¹ Congruently, the fauna at LBW indicates more humid conditions than at present, but the precise nature of the vegetation in the area remains uncertain and until recent research on the frog fauna there were no effective proxies indicating the amount of rainfall, or seasonality, at the fossil site.^10,12-14

A recent study of the rich and diverse anuran (frog) community from LBW served as an effective and direct climatic proxy, and showed that this group, sensitive as they are to rainfall and moisture, supported the higher humidity inferred from studies of other faunal groups from the site, and indicated relatively high rainfall.^12,15 The huge contrast between the frog community in the Langebaanweg region today, as compared with 5.1 mya, is clearly indicated by the fact that species richness on the relatively dry west coast of South Africa is low today (1-10 species)^16,17, whereas at LBW, six families and some 19 taxa have been differentiated¹². The LBW frog fauna is put in context when compared to modern species richness elsewhere in the southwestern Cape, which varies from 11 to 30 species.^16,18

Currently, southern African Anura are distributed throughout three different rainfall zones: the Summer Rainfall Zone (SRZ), the Winter Rainfall Zone (WRZ) and the Year-round Rainfall Zone (YRZ) which is found on the South African south coast. A number of amphibian taxa from the WRZ and the SRZ overlap in the YRZ.¹⁸

All frog families and genera previously identified at LBW were ambiguous in terms of the seasonality of rainfall as all but one of the species (a SRZ taxon) identified currently occur within all three rainfall regimes (Table 1). In the present study, we take a step further, utilising the recent identification at LBW of two species of the genus Ptychadena (family Ptychadenidae) to shed further light on the seasonality of rainfall at this site. Additionally, this discovery further elucidates the biogeography of the family Ptychadenidae.

 

Climatic history of the Winter Rainfall Zone

The WRZ receives predominantly winter rainfall from eastward migrating cold fronts embedded in polar cyclonic systems originating over the South Atlantic.^19,20 During summer, the South Atlantic Anticyclone is well developed and migrates to the south, blocking both the westward propagation of easterly waves that bring summer rainfall to much of southern Africa, and the polar frontal systems. The influence of the polar frontal systems diminishes northwards and is linked to decreasing rainfall and increasing aridity.¹⁴ The cold, nutrient-rich Benguela Upwelling System (BUS) supports a diverse and rich range of marine life along the southwestern African coast.²¹ The South Atlantic Anticyclone promotes the BUS and is thus the main cause of the present aridity along the southwestern African coast, the Namib, and the dryness of the adjacent interior of the sub-continent.^5,20,22-25 In general, the climate on the west coast is determined by the complex seasonal shifts and interplay of the prevailing winds over the Benguela region.⁵ Fluctuations in summer rainfall are linked to upwelling intensity in the BUS²⁶ and along the south coast⁵. The situation is complex, as indicated by the fact that Chase et al.⁵ found that at a hyrax-midden site falling within the present WRZ, but close to the border with the SRZ, summer rainfall variability over the Holocene during the last 7000 years had the greatest impact on water availability, and was the primary determinant of humidity. Analysis of herbivore tooth enamel indicates that there were incursions of C₄ vegetation in the mid-Pleistocene,²⁷ which could be related to decreased atmospheric pCO₂ conditions during interglacial periods, or possibly to changes in rainfall seasonality.

Recent research on marine proxies for sea surface temperature (SST) in the southern Cape Basin - such as calcareous dinoflagellate cysts and alkenones - suggests the inception of the BUS at about 10.5-10 mya.^28,29 How the BUS became established is comprehensively summarised in Neumann and Bamford⁶. Some authors^29,30 have suggested that tectonic uplift in southwestern Africa would have led to a cooling in the BUS at 12 mya, and after 5 mya, but the timing and cause of such tectonic events, and even their occurrence, is controversial^6,31. The initiation of the BUS has frequently been linked in the literature to summer aridity and the entrenchment of the current winter rainfall pattern on the west coast^6,24,32,33, and this in turn has been taken to have influenced other processes, such as the diversification of plants (see Altwegg et al.³³ - although a recent analysis¹ failed to find proof that seasonal aridity at ~8 mya triggered floristic radiation and diversification in the Cape Floral Region).

The connection between the BUS and seasonality of rainfall is unclear as estimates of the evolution of SSTs are not available³⁴ and the marine record indicates that the BUS and SSTs have fluctuated considerably over time in the late Neogene. High glacio-eustatic sea levels and the presence of warm-water molluscan taxa in the middle to late Pliocene^35,36 add further complexity to deciphering the evolution of oceanic and climatic conditions in the current WRZ.

There is also evidence of an oceanic subsurface warming between 6.5 mya and 5.0 mya which may be related to variability in the strength of North Atlantic deepwater formation on the temperatures of the intermediate waters of the South Atlantic.³⁴ The climatic data during LBW times are ambiguous in terms of oceanographic conditions, with SSTs apparently in sharp decline, but with low productivity (suggesting reduced upwelling) indicated by a drop in total organic carbon.³⁴ The fossil-bearing members of the Varswater Formation present at LBW conversely contain an abundance of authigenic phosphate, which is widely interpreted as being indicative of strong upwelling (Roberts et al.¹⁴ and references therein). The presence of some mollusc taxa from LBW which are currently found northwards from East London and eastwards from False Bay suggest warmer ocean temperatures than present.³⁷

 

Identification and provenance of Ptychadena at Langebaanweg

The majority of fossils from LBW were recovered from two highly fossiliferous members which form part of the Varswater Formation, namely the Muishondfontein Pelletal Phosphate Member (MPPM) and the Langeberg Quartzose Sand Member (LQSM). See Roberts et al.¹⁴ for further details on the geology of the site.

An examination of LQSM sediments (~5.1 mya) collected from a mine dump during phosphate-mining operations several decades ago was recently undertaken. The interpretation of the LQSM in the area from which the dump derived (the so-called 'east stream') was that it represented a river floodplain.³⁸ In the course of this study, an additional anuran genus (accession number SAM-PQL-70839) was identified -Ptychadena (Family: Ptychadenidae) - on the basis of a single sacrum (Figure 2). Subsequently a further ptychadenid, which appears to belong to a relatively larger species, was recovered from MPPM deposits which were excavated from the main dig site at the West Coast Fossil Park from square G5 (accession number SAM-PQL-71524) (Figure 2). The larger Ptychadenid showed several morphological differences to the smaller taxon, including a greater distance between the anterior and posterior articular ends of the sacrum (best seen in ventral view, Figure 2b and 2f), a larger neural spine, and a wider spacing of the sacral articular condyles.

The sacrum of a modern Ptychadenid, Ptychadena mascareniensis, from the Iziko South African Museum (ZR-045512), was scanned using microcomputed tomography and then measured for comparative purposes (see Figure 2 for positioning of measurements). This species currently enjoys a wide distribution in western, eastern and central Africa, extending down into South Africa. The breadth of the sacrum was 3.27 mm and the height 1.46 mm. The modern Ptychadena thus falls in between the two fossil taxa in terms of size as the smaller of the fossil taxa (SAM-PQL-70839) measured 2.79 mm by 1.39 mm, and the larger (SAM-PQL-71524) 4.60 mm by 1.88 mm for breadth and height, respectively.

Extant Ptychadenidae comprise the genera Ptychadena, Hildebrandtia and Lanzarana, and are monophyletic.³⁹ Four unique morphological synapomorphies are noted, including the symmetrical fusion of the eighth presacral vertebra with the sacral vertebra (sacrum), forming a composite sacrum.⁴⁰ The LBW ptychadenid sacrum displays the fusion of the presacral vertebra and sacrum, together with the distinctive anterolateral orientation and morphology of the transverse processes of members of the genus Ptychadena, including a characteristic foramen above the centrum that serves as the outlet for the spinal nerve (as noted by Blackburn et al.⁴¹). In addition, Ptychadena species differ from many ranids in that the neural arches of the composite sacrum lack deep grooves and fossae on the dorsal surface and exhibit a single minute low-lying neural spine.⁴⁰ Blackburn et al.⁴¹ provide conclusive evidence, through a thorough investigation of extant and fossil taxa, that the Ptychadenidae are the only major clade of frogs with the above sacral morphologies, making the identification of the LBW taxa indisputable.

LBW extends our knowledge of the fossil distribution of ptychadenids to include the southwestern Cape at 5.1 mya, and represents the most southerly occurrence of this genus to date in the African fossil record. The fossil frog bones reported on in this paper are curated by the Iziko South African Museum, Cape Town, and each bone reported on has been allocated an identifying accession number.

Other fossil sites containing Ptychadena species

The antiquity of the Ptychadena lineage is indicated by the earliest appearance of Ptychadena in the fossil record in the late Oligocene sediments (~25 mya) from the Nsungwe Formation in southwestern Tanzania.⁴⁰ This record represents the earliest of fossil anurans from Africa below the equator, and is the earliest definitive record of any family within the diverse ranoid clade Natatanura (sensu Blackburn et al.⁴¹ and Frost et al.⁴²). Other appearances of Ptychadenidae in the fossil record include those of the Middle Miocene at Beni Mellal in Morocco⁴³ and Pleistocene deposits from Madagascar⁴⁴.

Phylogeography of Ptychadena

Extant ptychadenids comprise 55 species within the genera Hildebrandtia, Lanzarana and Ptychadena, and are widespread tropical and subtropical species distributed throughout Madagascar, sub-Saharan Africa, the Seychelles and the Mascarene islands³⁹, with the exception of two species found in the Nile Delta⁴⁰. The distribution of the genus Ptychadena in southern Africa is delimited in areas where rainfall is above 60 mm in January and the minimum temperature is above 8 °C in September. These two variables represent 36.4% and 29.0% of the distribution of the genus in southern Africa, respectively (G.J.M. unpublished data). These two parameters describe the distribution of extant species from East London to the northeast, under the influence of the SRZ and increasing temperatures (Figure 1).

In the current WRZ, all modern species breed in winter, with the exception of two invasive species from the SRZ.⁴⁵ Some genera and families are found in both the WRZ and SRZ, and the remaining southern African families and genera are found in the SRZ and breed in summer (Table 1). Six amphibian families have been identified from LBW (Hyperoliidae, Brevicipitidae, Pxyicephalidae, Pipidae, Heleophrynidae and Bufonidae), and 19 different taxa, 10 of which remain unidentified, have been differentiated.¹² Genera identified include Hyperolius, Breviceps, Tomopterna, Xenopus, Heleophryne and Amietophrynus.¹²All the frog families and genera identified from LBW¹² currently occur in all three rainfall regimes (SRZ, WRZ and YRZ), with endemism to the WRZ only existing at species level in these genera¹⁶. Matthews et al.¹² tentatively identified Kassina (a genus restricted to the SRZ) - an identification which has subsequently been confirmed by computed tomography scans of comparative material, but the family to which it belongs (Hyperoliidae) contains other genera which are found in the current WRZ. Interestingly, histological studies done on the aquatic Xenopus (Family: Pipidae; common name: the African clawed frog) femora from LBW (paper in preparation) suggest marked seasonality as clear LAGS (lines of arrested growth) are evident.

Phylogeographic structuring in the distribution of anuran taxa with respect to the winter and summer rainfall regions has been recorded,⁴⁶ but little is known about the evolution of this pattern which clearly has deep roots. In the literature, the southern African amphibian fauna is commonly divided into two main groups - the so-called 'tropical' (a term used to describe the speciose tropical frog fauna distributed widely in the northeastern parts of southern Africa) and the unique 'Cape' frog faunas of the southwestern Cape which are characterised by extremely high rates of endemism and contain a large number of species with narrow niche envelopes.^16,17,47,48 These two groups correspond to the SRZ (the tropical frog fauna) and WRZ (the Cape frog fauna), and their breeding periods are delineated by mean annual precipitation in the summer or winter rainfall months, respectively.^17,48 The two rainfall regimes have such a high turnover in species that it is evident at a global scale.⁴⁹ Nonetheless, there are some genera that straddle both rainfall zones, but the population genetics of these taxa suggest deep genetic divisions, such that populations are confined to one zone or the other.⁴⁶

 

Discussion

The palaeoenvironment at Langebaanweg

Fossil pollen is frequently used in palaeoenvironmental reconstruction to ascertain whether C₃ plants (those which fix and reduce inorganic CO₂ into organic compounds using the C₃ photosynthetic pathway) or C₄ plants (those which employ the C₄ photosynthetic pathway) dominated a palaeo-landscape. Grasses categorised as C₄ vegetation are typically associated with a summer rainfall regime, and C₃ grasses with the WRZ. Franz-Odendaal et al.'s³² research on the large mammals from LBW indicated that the expected grazers (e.g. alcelaphine, hippopotamus and rhinoceros), as well as browsing species, showed 813C values which indicated that LBW was a C₃ dominated environment. This finding was corroborated by a study of phytoliths from the site.⁵⁰ The small mammals from LBW, such as the rats and mice, suggest a fynbos component to the vegetation⁹, as does fossil pollen^51,52. The presence of cool-growing C₃ grasses at LBW during the deposition of MPPM sediments was taken to indicate that the present-day climatic regime of winter wet/summer dry was established early in the Pliocene epoch.³² Using the vegetation to establish the rainfall regime is, however, questionable, given that fynbos and C₃ grasses both have a C₃ signature, and the contribution of C₃ grasses versus that of C₃ fynbos at LBW is undetermined. In addition, there are indications that the contribution from C₃ grasses to the general C₃ signature at LBW was small, as Stynder¹⁰ suggests that fossil bovid species indicate that grass was scarce, and the environment may have been heavily wooded. The presence of woodland is supported by the presence of certain bird taxa, but arid and semi-arid landscapes are also represented.^7,9 The precise nature of the Early Pliocene vegetation at LBW remains elusive, has no modern analogue, and cannot contribute in any verifiable way to ascertaining the rainfall regime, or provide information on seasonality, at LBW. The fact that fynbos was present on the west coast during the Early Pliocene has been used as evidence of a WRZ; however, the premises on which this association is based are arguable and are discussed further in the next section.

Inception of the WRZ and aridification of the west coast

Of the eight frog genera found at LBW, six (Hyperolius, Breviceps, Tomopterna, Heleophryne, Amietophrynus and Xenopus) are found in summer, winter and year-round rainfall areas. The evidence of season-ality provided by Kassina is not clear-cut as, although this taxon is currently found in the SRZ, other members of the Hyperoliidae, such as Semnodactylus, are found in the current WRZ and YRZ. Ptychadena is, however, currently not found in the more southerly and western areas of South Africa, or in any parts of the WRZ¹⁶, suggesting that this family has evolved and adapted to live in the SRZ.

The ptychadenids are a marker SRZ species, as they are found only in this rainfall zone, and the presence of Ptychadena at LBW thus provides strong evidence of a summer rainfall regime, or at least of a rainfall regime which included summer rainfall. The faunal evidence from LBW clearly indicates that at 5.1 mya the region was still receiving a relatively high rainfall, which fell partly, if not entirely, in summer.

This finding has important implications for studies involving the evolution of west coast flora and fauna, and the interpretation of phylogenetic studies which use molecular clock estimates to interpret the timing of lineage divergence. As mentioned previously, such studies have typically used the formation of the BUS as a proxy for the inception of the winter rainfall regime along the West Coast and the beginning of aridification.^6,24,32,33 Certain fynbos taxa such as Restionaceae, Ericaceae and Proteaceae formed part of the vegetation in southwestern Africa during the Palaeogene⁵³ and fossil pollen research indicates that fynbos taxa have formed part of west coast ecosystems since well before the inception of BUS and a winter rainfall regime^{14,15,23,51,52,54}. Hoffman et al.'s¹ habitat reconstruction for the dated phylogenies of 12 plant clades from the Cape Floral Region in southern Africa indicated that they evolved in aseasonal rainfall environments. In addition, this research indicated that the initial development of aridity in the Cape Floral Region was not linked to the onset of strong rainfall seasonality - contradicting the common assumption that aridity and the development of a strongly seasonal winter rainfall regime on the west coast occurred at the same time and are effectively linked. This de-linking of these two variables indicates that commonly made assumptions in the literature are incorrect, and illustrates how much still remains to be elucidated about the evolution of the WRZ.

On a global scale, the middle Miocene is considered to have been a time of reduced seasonality and relatively stable climate with elevated temperatures and high humidity and rainfall.^1,6,52 Scisio et al.⁵² studied the pollen from cores from the Miocene age Elandsfontyn Formation at LBW, which underlies the younger, main fossil-bearing deposits at the site. A strong contribution from plants that currently occur in tropical and subtropical conditions in the summer rainfall region in eastern South Africa is noted. The climate was wetter, and probably warmer, as indicated by the presence of palms and subtropical trees, the absence of Ericaceae, and the occurrence of only two Stoebe-type pollens. The fossil pollen evidence available which pre-dates LBW thus suggests that rainfall may have been either inter-annual, or characterised by a greater contribution of summer rain.⁵²

Roberts et al.¹⁵ suggested that the current pronounced aridity gradient from south to north on the west coast may have had its inception in the earlier Miocene. Hoffmann et al.¹ suggested that the Middle Miocene (13-17 mya) saw the development of perennial to weakly seasonal arid conditions, with the strongly seasonal rainfall regime of the west coast arising ~6.5-8 mya. Neumann and Bamford⁶ suggest that aridification of the west coast began post Middle Miocene. Based on a palynology study of sediments retrieved from the Atlantic off the mouth of the Orange River, Du pont et al.⁵⁴ note that between 10 mya and 6 mya, pollen types from plants of tropical affinity disappeared, and those from the Cape flora gradually increased. The onset of aridity on the west coast has thus been postulated to pre-date the LBW fossils by 3-5 mya. This postulate has, however, been based on palaeoclimatic proxies situated much further to the north of LBW in Namibia^31,55 and the Orange River⁵⁴. The LBW frog community indicates a relatively high rainfall¹², as do some other fossil taxa¹³, and the fact that woodland appears to have been widespread¹⁰. The evidence from LBW strongly contradicts assertions that aridification of the west coast in the region was well established by 5.1 mya, although such a scenario was certainly applicable further northwards, with aridity in the Namib dating back to 16 Ma.⁵⁵ However, relatively moister conditions appear to have prevailed in the southern, as opposed to the central, Namib desert during the Miocene and the flora appears to have remained C₃ in both regions until the Pliocene.⁵⁶

The marine evidence mentioned previously is inconclusive regarding the effects of fluctuations in the BUS and SSTs on the rainfall regime during the Early Pliocene. Much uncertainty therefore exists as to the exact status of the strength, and effect, of the BUS and SSTs, and the inferences drawn from other palaeoclimatic proxies are contestable. Neither the fossil evidence, the fossil pollen data, nor the fact that C₃ plants predominate, provide direct evidence of winter rainfall at LBW, or indeed of the period of inception of the WRZ.

 

Conclusions

The majority of anuran taxa at LBW are currently found in the SRZ and WRZ, and consequently are not diagnostic in terms of the rainfall regime. However, the identification of two Ptychadena species from LBW, as well as the presence of Kassina, provides new evidence of a summer rainfall regime, or of at least some significant summer rainfall, at ~5.1 mya on the southwestern coast of southern Africa. This evidence is a significant contribution to our understanding of the evolution of seasonality on the west coast in the LBW region and challenges the commonly held assumption that the WRZ has been established on the west coast since the later Miocene/Early Pliocene. The presence of a Ptychadena species also contributes to our knowledge of the palaeo-distribution of the family, which is currently widespread in sub-Saharan Africa, and has endured since the Oligocene in Tanzania.

 

Acknowledgements

The support of the DST-NRF Centre of Excellence in Palaeosciences is hereby acknowledged. G.J.M. thanks the DST-NRF Centre of Excellence for Invasion Biology for their support. D.L.R. acknowledges support from the National Research Foundation and the Department of Geography, Faculty of Natural and Agricultural Sciences at the University of the Free State.

This paper is dedicated to the scientific contributions of Dr Dave Roberts, our co-author, who passed away during the final preparation of this manuscript. His contributions as a geologist were so wide-ranging that they spanned the interests of a great many scientific disciplines, of which this work is one such example. His insights and enthusiasm will be greatly missed.

Authors' contributions

T.M. was the project leader; undertook the fossil research and provided the first draft of the manuscript. D.L.R. provided information on climatic change and conditions over the Miocene and Pliocene and made conceptual contributions. G.J.M. made conceptual contributions and provided information on the frog taxa mentioned in the paper. All three authors contributed to writing the manuscript.

 

References

1. Hoffmann V Verboom GA, Cotterill FPD. Dated plant phylogenies resolve neogene climate and landscape evolution in the Cape Floristic Region. PLoS One. 2015;10(9), e0137847, 25 pages. Available from: http://dx.doi.org/10.1371/journal.pone.0137847        [ Links ]

2. Meadows ME, Baxter AJ. Late Quaternary palaeoenvironments of the south-western Cape, South Africa: A regional synthesis. Quat Int. 1999;57/58:193-206. http://dx.doi.org/10.1016/S1040-6182(98)00060-3        [ Links ]

3. Chase BM, Meadows ME. Late Quaternary dynamics of southern Africa's winter rainfall zone. Earth Sci Rev. 2007;84:103-138. http://dx.doi.org/10.1016/j.earscirev.2007.06.002        [ Links ]

4. Chase BM, Boom A, Carr AS, Meadows ME, Reimer PJ. Holocene climatic change in southernmost South Africa: Rock hyrax middens record shifts in the southern westerlies. Quat Sci Rev. 2013;82:199-205. http://dx.doi.org/10.1016/j.quascirev.2013.10.018        [ Links ]

5. Chase BM, Lim S, Chevalier M, Boom A, Carr AS, Meadows ME, et al. Influence of tropical easterlies in southern Africa's winter rainfall zone during the Holocene. Quat Sci Rev. 2015;107:138-148. http://dx.doi.org/10.1016/j.quascirev.2014.10.011        [ Links ]

6. Neumann FH, Bamford MK. Shaping of modern southern African biomes: Neogene vegetation and climate changes. Trans Roy Soc S Afr. 2015;70(3):195-212. http://dx.doi.org/10.1080/0035919X.2015.1072859        [ Links ]

7. Manegold AA, Louchart JC, Elaznowski A. The Early Pliocene avifauna of Langebaanweg (South Africa): A review and update. In: Gohlich UB, Koh A, editors. Paleornithological Research, Proceedings of the 8th International Meeting of the Society of Avian Paleontology and Evolution. Vienna: Natural History Museum; 2013. p. 135-152.         [ Links ]

8. Matthews T. A review of the Muridae of Langebaanweg (Mio-Pliocene, West Coast, South Africa). Published abstracts of the Langebaanweg 2006: Mini-symposium and workshop. Afr Nat Hist. 2006;2:188-189.         [ Links ]

9. Matthews T, Parkington JE, Denys C. Community evolution of Neogene micromammals from Langebaanweg 'E' Quarry and other west coast fossil sites, south-western Cape, South Africa. Palaeogeogr Palaeocl. 2007;245:332-352. http://dx.doi.org/10.1016/j.palaeo.2006.08.015        [ Links ]

10. Stynder DD. Fossil bovid diets indicate a scarcity of grass in the Langebaanweg 'E' Quarry (South Africa) late Miocene/early Pliocene environment. Paleobiology. 2011;37(1):126-139. http://dx.doi.org/10.1666/09074.1        [ Links ]

11. Diekmann B, Falker M, Kuhn G. Environmental history of the south-eastern South Atlantic since the Middle Miocene: Evidence from the sedimentological records of ODP Sites 1088 and 1092. Sedimentology. 2003;50:511-529. http://dx.doi.org/10.1046/j.1365-3091.2003.00562.x        [ Links ]

12. Matthews T, Van Dijk E, Roberts DL, Smith RMH. An early Pliocene (51 Mya) fossil frog community from Langebaanweg, south-western Cape, South Africa Afr J Herpetol. 2015;64(1):39-53. http://dx.doi.org/10.1080/21564574.2014.985261        [ Links ]

13. Hendey QB. Cenozoic geology and palaeoecology of the fynbos region. In: Deacon HJ, Hendey QB, Lambrechts JJN, editors. Fynbos palaeoecology: A preliminary synthesis. South African National Scientific Programmes Report no 75. Cape Town: Mills Litho; 1983. p. 35-60.         [ Links ]

14. Roberts DL, Matthews T, Herries AIR, Boulter C, Smith RMH, Dondo C, et al. Regional and global context of the Late Cenozoic Langebaanweg (LBW) palaeontological site: West Coast of South Africa. Earth Sci Rev. 2011;106(3):191-310. http://dx.doi.org/10.1016/j.earscirev.2011.02.002        [ Links ]

15. Roberts DL, Scisio L, Herries AIR, Scott L, Bamford MK, Musekiwa C, et al. Miocene fluvial systems and palynofloras at the southwestern tip of Africa: Implications for regional and global fluctuations in climate and ecosystems. Earth Sci Rev. 2013;124:184-201. http://dx.doi.org/10.1016/j.earscirev.2013.05.001        [ Links ]

16. Minter LR, Burger M, Harrison JA, Braak HH, Bishop PJ, Kloepfer D. Atlas and red data book of the frogs of South Africa, Lesotho and Swaziland SI/MAB Series no 9. Washington DC: Smithsonian Institution; 2004.         [ Links ]

17. Schreiner C, Rodder D, Measey GJ. Using models to test Poynton's predictions. Afr J Herpetol. 2013;62:49-62. http://dx.doi.org/10.1080/21564574.2013.794865        [ Links ]

18. Colville JC, Potts AJ, Bradshaw PL, Measey GJ, Snijman D, Picker MD, et al. Floristic and faunal Cape biochoria: Do they exist? In: Allsopp N, Colville JF, Verboom GA, editors. Fynbos: Ecology, evolution and conservation of a megadiverse region. Cape Town: Oxford University Press; 2014. p. 73-93. http://dx.doi.org/10.1093/acprof:oso/9780199679584.003.0004        [ Links ]

19. Tyson PD. Climatic change and variability in southern Africa. Cape Town: Oxford University Press; 1986.         [ Links ]

20. Chase BM, Thomas DSG. Multiphase late Quaternary aeolian sediment accumulation in western South Africa: Timing and relationship to palaeoclimatic changes inferred from the marine record. Quat Int. 2007;166(1):29-41. http://dx.doi.org/10.1016/j.quaint.2006.12.005        [ Links ]

21. Diester-Haass L, Meyers PA, Vidal L. The late Miocene onset of high productivity in the Benguela Current upwelling system as part of a global pattern. Marine Geol. 2002;180:87-103. http://dx.doi.org/10.1016/S0025-3227(01)00207-9        [ Links ]

22. Coetzee JA. Late Cainozoic palaeoenvironments of southern Africa In: Van Zinderen Bakker Sr EM, editor. Antarctic glacial history and world palaeoenvironments. Rotterdam: AA Balkema; 1978. p. 25-32. http://dx.doi.org/10.1017/S0032247400001819        [ Links ]

23. Coetzee JA, Rogers J. Palynological and lithological evidence for the Miocene palaeoenvironment in the Saldhana region (South Africa). Palaeogeogr Palaeocl. 1982;39:71-85. http://dx.doi.org/10.1016/0031-0182(82)90073-6        [ Links ]

24. Siesser WG. Aridification of the Namib Desert: Evidence from oceanic cores. Van Zinderen Bakker Sr EM, editor. Antarctic glacial history and world palaeoenvironments. Rotterdam: AA Balkema; 1978. p. 105-113. http://dx.doi.org/10.1017/S0032247400001819        [ Links ]

25. Gasse F. Hydrological changes in the African tropics since the Last Glacial Maximum. Quat Sci Rev. 2000;19:189-211. http://dx.doi.org/10.1016/S0277-3791(99)00061-X        [ Links ]

26. Farmer EC, deMenocal PB, Marchitto TM. Holocene and deglacial ocean temperature variability in the Benguela upwelling region: Implications for low latitude atmospheric circulation. Paleoceanography. 2005;20, PA2018. http://dx.doi.org/10.1029/2004PA001049        [ Links ]

27. Luyt J, Lee-Thorp J, Avery G. New light on middle Pleistocene west coast environments from Elandsfontein, western Cape, South Africa. S Afr J Sci. 2000;96:399-403.         [ Links ]

28. Heinrich S, Zonneveld KAF, Bickert T, Willems H. The Benguela upwelling related to the Miocene cooling events and the development of the Antarctic Circumpolar Current: Evidence from calcareous dinoflagellate cysts. Paleoceanography. 2011;26, PA3209. http://dx.doi.org/10.1029/2010PA002065        [ Links ]

29. Etourneau J. Tectonically driven upwelling. Nat Geosci. 2014;7:698-699. http://dx.doi.org/10.1038/ngeo2258        [ Links ]

30. Jung G, Prange M, Schultz M. Uplift of Africa as a potential cause for Neogene intensification of the Benguela upwelling system. Nat Geosci. 2014;7:741-747. http://dx.doi.org/10.1038/ngeo2249        [ Links ]

31. Roberts DL, Brink JS. Dating and correlation of Neogene coastal deposits in the Western Cape (South Africa): Implications for Neotectonism. S Afr J Geol. 2002;105(4):337-352. http://dx.doi.org/10.2113/1050337        [ Links ]

32. Franz-Odendaal T, Lee-Thorp JA, Chinsamy A. New evidence for the lack of C₄ grassland expansions during the Early Pliocene at Langebaanweg, South Africa. Paleobiology. 2002;28(3):378-388. http://dx.doi.org/10.1666/0094-8373(2002)028<0378:NEFTLO>2.0.CO;2        [ Links ]

33. Altwegg R, West A, Gillson L, Midgley GF. Impacts of climate change in the Greater Cape Floristic region. In: Allsopp N, Colville JF, Verboom GA, editors. Fynbos: Ecology, evolution and conservation of a megadiverse region. Cape Town: Oxford University Press; 2014. p. 299-320. http://dx.doi.org/10.1093/acprof:oso/9780199679584.003.0013        [ Links ]

34. Rommerskirchen F, Condon T, Mollenhauer G, Dupont L, Schefuss L. Miocene to Pliocene development of surface and sub-surface temperatures in the Benguela Current system. Paleoceanography. 2011;26, PA3216. Available from: http://dx.doi.org/10.1029/2010PA002074        [ Links ]

35. Pether J. Late Tertiary and early Quaternary marine deposits of the Namaqualand coast, Cape Province: New perspectives. S Afr J Sci. 1986;82:464-470.         [ Links ]

36. Pether J. Molluscan evidence for enhanced deglacial advection of Agulhas water in the Benguela Current, off south-western Africa. Palaeogeogr Palaeocl. 1994;111:99-117. http://dx.doi.org/10.1016/0031-0182(94)90350-6        [ Links ]

37. Kensley B. Pliocene marine invertebrates from Langebaanweg, Cape Province. Ann S Afr Mus. 1972;60:173-190.         [ Links ]

38. Hendey QB. The Pliocene occurrences in 'E' Quarry, Langebaanweg, South Africa. Ann S Afr Mus. 1976;69: 215-247.         [ Links ]

39. Frost DR. Amphibian species of the world: An online reference, Version 60 [database on the Internet]. No date [cited 2015 Sep 11]. Available from: http://researchamnhorg/herpetology/amphibia/indexhtml        [ Links ]

40. Blackburn DC, Wake DB. Class Amphibia Gray, 1825. In: Zhang ZQ, editor. Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Auckland: Magnolia Press; 2011. p. 39-55.         [ Links ]

41. Blackburn DC, Roberts EM, Stevens NJ. The earliest record of the endemic African frog family Ptychadenidae from the Oligocene Nsungwe Formation of Tanzania. J Vert Pal. 2015;35(2), Art. #e907174, 5 pages. http://dx.doi.org/10.1080/02724634.2014.907174        [ Links ]

42. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, et al. The amphibian tree of life. Bull Am Mus Nat Hist. 2006;297:1-370. http://dx.doi.org/10.1206/0003-0090(2006)297[0001:TATOL]2.0.CO;2        [ Links ]

43. Vergnaud-Grazzini C. Les amphibiens du Miocene de Beni-Mellal [Amphibians of the Miocene from Beni-Mellal]. Notes et Mémoires du Service Géologique du Maroc. 1966;27:43-74. French.         [ Links ]

44. Burney DA, Vasey N, Godfrey LR, Ramilisonina WL, Jungers M, Ramarolahy M, et al. New findings at Andrahomana Cave, southeastern Madagascar. J Cave Karst Stud. 2008;70:13-24.         [ Links ]

45. Measey GJ, Davies S. Struggling against domestic exotics at the southern end of Africa. Froglog. 2011;97:28-30.         [ Links ]

46. Tolley KA, Bowie RCK, Measey GJ, Price BW, Forest F. The shifting landscape of genes since the Pliocene: Terrestrial phylogeography in the Greater Cape Floristic Region. In: Allsopp N, Colville jF, Verboom GA, editors. Fynbos: Ecology, evolution and conservation of a megadiverse region. Cape Town: Oxford University Press; 2014. p. 142-163. http://dx.doi.org/10.1093/acprof:oso/9780199679584.003.0007        [ Links ]

47. Poynton JC. Afrotemperate amphibians in southern and eastern Africa: A critical review. Afr J Herpetol. 2013;62(1):5-20. http://dx.doi.org/10.1080/21564574.2013.794866        [ Links ]

48. Mokhatla MM, Rödder D, Measey GJ. Assessing the effects of climate change on distributions of Cape Floristic Region amphibians. S Afr J Sci. 2015;111(11-12), Art. #2014-0389, 7 pages. http://dx.doi.org/10.17159/sajs.2015/20140389        [ Links ]

49. Holt BG, Lessard JP Borregaard MK, Fritz SA, Araújo MB, Dimitrov D, et al. An update of Wallace's zoogeographic regions of the world. Science. 2013;339(6115):74-78. http://dx.doi.org/10.1126/science.1228282        [ Links ]

50. Rossouw L, Stynder D, Haarhoff P. Evidence for opal phytolith preservation in the Langebaanweg 'E' Quarry Varswater Formation and its potential for paleohabitat reconstruction. S Afr J Sci. 2009;105:223-227.         [ Links ]

51. Scott L. Pollen evidence for vegetational and climatic change in southern Africa during the Neogene and Quaternary. In: Vrba ES, Denton GH, Partridge TC, Burckle LH, editors. Paleoclimate and evolution with emphasis on human origins Yale: Yale University Press; 1995. p. 65-76.         [ Links ]

52. Scisio L, Neumann FH, Roberts DL, Tsikos H, Scott L, Bamford MK. Fluctuations in Miocene climate and sea levels along the south-western South African coast: Inferences from biogeochemistry, palynology and sedimentology. Pal Afr. 2013;48:2-18.         [ Links ]

53. Linder HP. The radiation of the Cape flora, southern Africa. Biol Rev. 2003;78(4):597-638. http://dx.doi.org/10.1017/S1464793103006171        [ Links ]

54. Dupont LM, Linder HP Rommerskirchen F, Schefuß E Climate-driven rampant speciation of the Cape flora. J Biogeog. 2011;38(6):1059-1068. http://dx.doi.org/10.1111/j.1365-2699.2011.02476.x        [ Links ]

55. Senut B, Pickford M, Ségalen L. Neogene desertification of Africa. Compt Rend Geosci. 2009;341:591-602. http://dx.doi.org/10.1016/j.crte.2009.03.008        [ Links ]

56. Senut B, Ségalen L Neogene palaeoenvironments of the Namib Desert: A brief synthesis. Trans Royal Soc S Afr. 2014;69:205-211. Available from: http://dx.doi.org/10.1080/0035919X.2014.958605        [ Links ]

 

 

Correspondence:
Thalassa Matthews
tmatthews@iziko.org.za

Received: 29 Feb. 2016
Revised: 12 May 2016
Accepted: 16 May 2016

 

 

† Deceased