Literature review of selected works by Dr. Valenti Rull.

Introduction

In my previous blog, I posted the article I wrote for the San Francisco State IR Journal in 2009. I concluded the post script of the 2009 article with the statement: “More field research needs to be undertaken to assess the realities of tepui species, and what effect global warming has on the pristine tepui ecosystems.” Happily a number of dedicated and brilliant scientists have been working on this issue, including the eminent Dr. Valenti Rull.

Dr. Valenti Rull is an extremely prolific author on the subject of tepui ecosystems and natural history. His CV, list of publications and personal interests can be found at http://www.vrull.org/ . Dr. Rulls' work was known to me at the time of my journal publication, although I did not have the leisure of delving into his work in any detail, which in retrospect would have been useful. A few selected works by Dr. Rull are being reviewed here in tandem as they have a similar purpose, methodology, and thesis. The thesis of the works is that the tepuis are not static locals of evolutionary isolation, but instead represent a combination of dynamic evolutionary processes linked to the sum totality of the natural history of South America, and indeed to the planet as a whole. His methodology is a hybrid of paleoecology and ecology a methodology which he explains in detail from a theoretical perspective in the paper “Ecology and Paleoecology: two approaches, one objective”.¹ The purpose is to establish the precise mechanisms of tepui ecosystems and the history of their establishment, and to predict their future viability under predicted global warming trends.

Summary

The 2004 short communication in Naturwissenschaften entitled “Is the 'Lost World' really lost? Paleoecological insights into the origin of the peculiar flora of the Guayana Highlands” Rull seeks to dispel the “Lost World” fantasy of the tepuis by proving that vertical migration of tepui and lowland flora has generated the current assemblages on the tepui summits.² He criticizes the notion of total isolation since the Cretaceous by stating that this theory of isolation is not supported by paleoecological evidence. By analyzing Quaternary sediments and documented vertical migrations, he infers that vertical migration must be the correct model for the establishment of tepui ecosystems. He tracks the history of the assumptions about the origin and composition of tepui biota from Doyles fictional novel “The Lost World” to the works of Berry and Huber, who demonstrated that the level of endemicity in the Guyana Highlands (GH) is 33% as opposed to the 90% levels assumed as late as the 1970s.

Rulls' basic methodology is the analysis of pollen in peat outcrops from the Chimanta tepui. The current flora assemblages are classified as tepuian meadows, shrub land and gallery forests. The composition of the meadows is mostly the Rapateaceae genus Stegolepis, which does not exist past an altitude of 2,300 meters. The shrub lands level off at 2500 meters, and are composed primarily of the Asteraceae genus Chimantaea. Gallery forests exist around waterways such as small streams and lakes, and are composed of Bonnetia roraimae. The current assemblages, as well as their altitudinal limits, can then be compared to the distributions of pollen samples taken from the peat bogs. In this way, the dynamics of the changes of vegetation, climate and ecosystems in the tepuis can be analyzed. The results of the pollen analysis show that Stegolepis was present at a lower elevation around 4000 years ago, with Chimantaea being dominant. Around 2000 years ago, as the temperature warmed up, Chimantaea dominated assemblages moved to a higher elevation, and Segolepis meadows established themselves at a higher elevation. This tracking of vertical migration of tepuian ecosystems mirrors Holocene temperature fluctuations, effectively proving that the tepui ecosystems are subject to climate trends. In the discussion section of this short paper, Rull discusses the implications for Pleistocene temperature related migrations, in which tepuian ecosystems and floral assemblages may have moved vertically downward in the magnitude of 1500 meters. This displacement would have allowed the tepui ecosystems to mix with lowland vegetation, especially during the particularly cold Long Glacial Maximum, (LGM), approximatively twenty thousand years ago. This temperature related vertical migration also limits the duration and integration of different floral assemblages, where tepuis exceeding the 1500-1000 meter elevation would have remained isolated; their altitude preventing the mixing of flora with the lowlands. Thus, Rull estimates that roughly 60% of all tepuis (those with summits 1200 meters above the surrounding terrain) would have been isolated from the lowlands even during the coldest recorded periods of the last 2.5 million years. The intermixing of tepui biota with the lowlands and other tepuis during times of temperature fluctuation is, according to Rull, the reason why the level of tepui endemics stands at roughly 33%, as opposed to the 90% estimated by other scholars. Rull concludes that the modern tepui ecosystems and their patterns of endemicity are the “result of a complex evolutionary process in which both isolation and vertical displacement due to glacial/interglacial alteration have played a role, depending on the taxa considered.” He goes further to state that more research is needed to assess the specifics of biogeographical development of the complex tepui ecosystems.

In 2006, Rull and Vegas-Vilarrubia published the work “Unexpected biodiversity loss under global warming in the neotropical Guyana Highlands: a preliminary appraisal” in the journal Global Change Biology. This work builds on previous research and publications by Rull to establish the realities of tepui natural history and ecosystem development, as well as to address new threats to the GH. The paper begins with a brief introduction regarding the trends for human caused extinction in high altitude ecosystems (begun in 1750 A.D with the start of anthropogenic climate change). The primary mechanism of this extinction is the upward migration of organisms into the global highlands in a response to this warming trend. In addressing this mechanism of extinction, the authors dispel the notion that tropical highlands are only threatened by inclement weather patterns caused by global warming and deforestation. They include the phenomena of vertical migration as a major cause of extinction in the tropical highlands, along with habitat loss and deforestation. The authors proceed to introduce the Guiana highlands and the tepui summits, mentioning key elements which make the region unique. The level of endemicity is a critical element, with a estimated 65.3% endemicity rate for the Guiana shield, a 33% endemicity rate for the highlands, and tepui summit endemicity rates with up to 60% endemic organisms. The authors dismiss the analysis of Maguire that tepui and Guiana highland endemics are the result of Cretaceous isolation, in favor of vertical biotic migrations which occur according to glacial cycles which allow for gene flow under specific temperature conditions. Although speciation in isolation and vicariance occur in the GH and the tepui summits, the patterns of species distribution and the realities of the recent paleontological record tend to disprove both Cretaceous isolation and the refuge hypothesis.

The authors describe in great detail the flora the GH, which is placed in four categories; forests, shrublands, meadows and pioneer formations. The tepui summits contain these four assemblages. The forests are composed of Bonnetia, a Thaeceae tree, as well as a variety of bromeliads. These forests are classified as being low canopy (6-12 meters in height), and are fairly homogeneous, composed of Bonnetia roraimae, tepuiensis and wurdackii. The shrub-lands are composed of members of the endemic shrub Chimantaea, such as C. mirabilis, humilis, and lanocaulis, which develop on very wet saturated soils. These shrublands are called paramoid shrublands, as they taxonomically resemble the Andean paramos shrublands. The tepui meadows are composed mostly of the genus Rapateaceae and Xyridaceae, specifically the Rapateace Stegolepis, which is prominent on the tepui summits and occur in large concentrations with a few families of shrubs. Pioneer formations are composed of cyanobacteria, algae, lichens, and other non-vascular plants.

The authors then go on to describe the conservation status of the GH, and the pantepui region. While they do not go into any great detail regarding the regions place in the scheme of global conservation, they do mention that 70% of the GH is protected under a series of reserves and parks, and is recognized by the IUCN and WWF as a Neotropical Plant diversity center. Although this conservation method is effective, and has thus far kept the GH in a comparatively pristine condition, the threat posed by global warming has not been properly addressed or researched. This is the crux of the paper: that global warming will cause significant extinctions in tepui biota unless a methodology to ameliorate its effects can be devised.

In the section entitled “Natural vs. global-warming trends and the rates of change”, Rull and Vegas-Vilarrubia detail precisely what is expected to happen to the GH if climate change continues, using Altitudinal Range Displacement analysis. This is an analysis of the niche constraints of indigenous plants, and the effect that a change in temperature would have on their altitudinal range. First, they describe the conditions during the LGM, when the temperature was 6 degrees centigrade lower then present conditions. At the peak of the LGM, tepui summit flora was distributed approximately 1100 meters below the present altitude, and made up the majority of the GH flora. At the close of the Pleistocene, the natural temperature increase of 0.025 degrees centigrade per century allowed for upward migration of flora at a rate of 5.25 meters per century. This migration due to cyclical oscillation in temperature is considered natural, with organisms being theoretically able to adapt to the gradual changes as ice ages come and go. However, human caused climate change has led to a 10 fold increase in global temperature per century, with anticipated temperature predicted to exceed the current rate of 0.24 degrees per century. The predicted temperature increase per century is estimated at between 1.5-5.8 degrees, depending on how humanity addresses its energy consumption. The authors calculate that 35% of endemic Pantepui organisms are in danger of extinction via global warming induced habitat loss. However, the authors caution that this is a tentative analysis, as the remote tepuis have not been adequately surveyed and explored to the point where the realities of climate changed based extinctions can be completely understood or predicted. What is known is that Chimantaea is in specific danger, due to the plants narrow range and high altitude habitat.

The authors utilize altitudinal range displacement analysis to examine the danger to selected taxa of vascular plants in the pantepui. The authors selected 22 endemic species, of which 11 are at high risk of extinction in the next century, as the temperature required for total habitat loss lies within the IPCC predictions for a global temperature increase of 1-5 degrees centigrade. The species under threat of extinction comprise major elements of the vegetational assemblages (such as gallery forests) include Bonnetia wurdackii, the loss of which would significantly effect the gallery forests, leading to possible parallel extinctions of dependent species. This situation of dependent and related extinctions due to the loss of keystone species also includes Stegolepis terramarensis, which dominates the meadows of Marahuaka tepui, and Stegolepis squarrosa, which is dominant on Quaiquinima tepui between 1200 and 1600 meters, the upper altitudinal limit of the species. The effect which the loss of these keystone species would have on tepui summit ecosystems is unknown. The results of the ARD analysis predict that approximately 35% of the species included in analysis by Rull and Vegas-Vilarruba are in danger of global extinction if predicted warming reaches 2-4 degrees centigrade. This prediction is subject to revision based on a variety of factors, including IPCC revision of predicted climate change, fragmentation of habitat leading to ecosystem stress, as well as reassessment of temperature thresholds for the flora which was included in the analysis. If future temperature change is stabilized at an increase of 1 degree, extinctions would be prevented to an unspecified extent. A temperature increase between 4 and 5 degrees would eliminate 70% of the GH species in the study. The effects of habitat restriction caused by lower than expected temperature increase is not known.

The establishment of temperature and altitudinal range changes which will cause extinction leads the authors to examine such events from the past. The authors hypothesize that the floral composition of the tepuis during the LGM was significantly different than what exists at present. It is hypothesized that unknown communities lacking extant representatives or modern analogues existed on the tepui summits and high altitudes during the LGM, and became extinct during the interglacial periods. The authors observe that the cumulative extinctions in the GH would have been remarkably high, as 40 cycles of glaciation have occurred over the last 2.5 million years. Our current age is the equivalent to a post glacial warming, although it compresses 20 thousand years of gradual warming into a single century. As part of this process, the upward movement of lowland organisms into the highlands is expected to occur, although the composition of this lowland invasion is stated.

In the final section of the paper, the authors recommend that a series of steps to determine what effects of global warming on the GH, as well as what to do about them. These steps are:

1. Field studies to be undertaken to specifically assess the threat that global warming posses to the GH. It is implied that collection and monitoring must be undertaken during field work.

2. Observation and monitoring of the tepuis with high resolution satellite imagery, spatial/topographical data analysis and other GIS systems.

3. Studies of upward migration rates in recent and current time, and the extrapolation of the effects that climate change has on other mountains and highlands across the world.

These steps are recommended due to the need to establish the precise realities of habitat loss and extinction in a region with a complex topography and series of micro climates which are not fully surveyed in totality. The authors state that “the case of the GH is an issue of global concern”, as the extinction of GH flora and fauna will impact global biodiversity in a significant manner. The endemic organisms of the GH comprise a significant percentage of earths biodiversity, and analogues to the GH across the planet face similar extinction scenarios.

Given the gravity of the problem, the authors recommend that the highland areas in danger of warming related extinctions be declared as biodiversity hot spots, which would assist in policy formation for their protection. An emphasis would be the conservation of critically threatened taxa, and solutions to specific problems of their conservation could be analyzed. Another solution would be massive ex situ strategies, which would identify the vulnerable species, define their tolerances and extinction potential, and then develop a way to preserve these vulnerable species outside of their present locations.

In 2009, Rull, Nogue and Vegas-Vilarrubia published the paper “Modeling biodiversity loss by global warming on Pantepui, northern South America: projected upward migration and potential habitat loss” in the Journal Climatic Change . It is an in-depth analysis of the previous work by these authors , and utilizes topographical and climatic data to model the extinction rates in the pantepui. The authors begin by introducing the problem which is being studied; global warming. The authors differentiate this work from previous analysis with a more through analysis of the species which will be effected by climate change. Where as previous publications were preliminary analysis based on a selected group of vascular plants, this analysis focuses on all known vascular plants in the GH, with an emphasis on the endemic species.

Analysis of the biodiversity in the Pantepui region was undertaken using Species-Area Relationships (SAR) Altitudinal Range Displacement (ARD) and Endemic species-Area Relationship (EAR) algorithms, in which SAR and EAR utilize the Arrhenius equation to estimate biodiversity and habitat loss. The total Pantepui area above 1,500 meters and 26 specific tepuis individually are included in the statistical analysis, comprising the majority of the total tepuis, with the omission of those with small summit areas. The areas under examination were mapped using GIS software from the Shuttle Radar Topography Mission (SRTM) at a 90 meter precision. The authors constructed 8 total scenarios using the SAR and EAR algorithms. These were SAR 1 and 2, and EAR 1 and 2, with each model set at either a 2 degree or 4 degree projected warming scenario. The four models using the SAR system produced predicted extinction results with in a similar range; from 73.2% to 83.1% estimated extinction percentages. The EAR models ranged dramatically, from a predicted 27.7% extinction under EAR 1 at 2 degrees Celsius, to a dramatic 90.2% predicted extinction with EAR 2 at 4 degrees Celsius. The ARD analysis demonstrates that 45% of the Pantepui endemics are in danger of extinction by habitat loss by 2100 AD. The discrepancies in predicted extinction are due to the different parameters in the ARD, EAR and SAR models. EAR incorporates ecological factors, where as ARD measures only shrinking habitat. As such, ARD is more a topographical and physical model while EAR includes complex biological factors. The factors of Projected Altitudinal Range (PAR) and Projected Available Area (PAA) were obtained using the ARD analysis, and when mapped out show extreme restriction in the range of tepui flora under global warming conditions. The authors state that other factors and lurking variables, such as key stone species extinction leading to secondary extinctions, soil conditions and ecosystem disintegration and fragmentation compound the potential for widespread extinction. The authors caution that the PAR and PAA modeling for extinction rates represents a “minimum expectation”. In the final analysis, the authors conclude that the SAR/EAR models predict an extinction rate on the order of 80% ( 1,700 species of vascular plants) for Pantepui species and a range of 30-50% (200-400 species of vascular plants) for Pantepui endemics. As the Pantepui is a speciation center of the Guyana and Amazon regions, these extinctions will dramatically effect future evolution in surrounding regions, and significantly compromise biodiversity in northern South America.

In the conclusion, the authors recommend that a series of steps be taken to avoid this catastrophe of biodiversity loss. The first step, which is currently being undertaken, is the classification of the endangered vascular plants according to the international conservation criteria. The second step is the utilization of precise and sophisticated modeling based on the new precision GIS and field work data. The third step is the creation of a yet to be determined ex situ conservation strategy, possibly taking the form of a reserve in the Andean mountains.

Analysis.

These three works represent a critical continuum of scholarly and scientific investigation into the natural history, current ecology, and probably future of the GH. With the first work, Rull clearly examines the history of the GH and tepui biota with quantifiable data proving that a specific hypothesis, that of vertical displacement, is the driving force behind the composition of the biodiversity observed in the GH. Thus, he establishes a theory which can be tested and used to project future movements of organisms in the region. While the paper is brief, the implications for the future of the region are clear; future climate change will result in vertical displacement. If the flora of the GH is based upon cyclical vertical migration based on the glacial cycles, what happens when those cycles are radically altered? In this paper Rull not only settles the debate about the establishment and origin of the tepui and GH ecosystems, but provides clear evidence from the paleontological record that the system of establishment is inexorably linked to climate change.

In the second paper, Rull and Vegas -Vilarrubia begin the task of assessing the habitat losses which will occur in the next 100 years, combining the theory and model of vertical migration to predict how the tepuis and GH as a whole will change. This change is expected to be defined by large scale extinctions in the vascular plants of the GH, where highland species will be replaced by lowland species as lowland habitats are displaced to the tepui summits.

In the third paper, the specifics of this predicted extinction event are analyzed in greater detail, with statistical models utilized to explore the predicted scenarios of climate change and extinction. While these models are detailed, the authors consistently call for more in-depth analysis of the region, in order to attain the specifics of the emerging extinction event in the region. This is due to the overall lack of extremely detailed field studies in the GH, a region which has not been fully explored. The authors mention that 70% of the GH is under conservation regimes, and while this is accurate it does not mean that adequate surveys of total biodiversity have been made, or that all the tepuis have been completely surveyed. Given that the GH is such a large area, and is contains borders which are under dispute ( ie the Venezuela and Guyana border dispute) the task of completely surveying the entire region is fairly daunting. Other difficulties exist, which the authors are fully aware of and have documented in Conservation Biology Volume 22 # 3, and Nature volume 453. These are difficulties involving access to the GH due to bureaucratic restrictions on exploration, specimen collection and genetic sampling. The issue is that the permit granting process is lengthy, and is controlled by a myriad of organizations starting with Fondo Nacional de Ciencia, Tecnologia e Investigacion (FONACIT) and including but not limited to such organizations as the National Tepui Commission, the Biodiversity Office, the National Institute of Parks, and the Office of Indigenous Affairs. This complicates the field work and collection possibilities, and has “prevented scientific fieldwork in the Guayana Highlands for almost 20 years”. This complex bureaucratic situation would go a long way in explaining why the tepui summits are sporadically visited by scientists, and supports anecdotes I have been told regarding the difficulty of field work on the tepui summits.

An interesting observation made by Rull and Vegas-Vularrubia in “Unexpected Biodiversity Loss” is the existence of Pliocene tepui summit communities which seem to be lost to science. Rull suggested this in his 2005 paper “Biotic diversification in the Guayana Highlands: a proposal”. If this is accurate, then the instances of extinction in the GH over the last 2.5 million years would be staggering. This situation would seem to suggest that the ecosystems established on the tepui summits would be comparatively new in a evolutionary sense, and by extension it is possible that interspecies dependence and interaction may be low. If this is true, new ecosystems would be in a relatively constant state of development, and the range of vascular plants would be in constant flux, topographically speaking.

In the 2006 work, the Rull and Vegas-Vilarrubia state that “Another element that can enhance extinction is the successful establishment of introduced and/or invasive species..., which in this case would arrive from lower altitudes pushed up by the warming trend.”. This phenomena of invasive lowland species may be presented in two scenarios: 1) under natural climate change, lowland vertical migration is would be expected over a long interglacial period, and would occur at a steady rate, allowing the potential for adaptation in highland species to the temperature change, 2) under anthropogenic climate change, the rate would be accelerated, compressing twenty thousand years of steady climate change in to a span of 100 or so years. The second scenario is cause for concern, and would be defined by rapid habitat loss for highland species, and increasing competition from invasive lowland species. What is striking about this problem of vanishing highland biota is that it should be currently observable. It should be possible, with more field work and high resolution GIS systems, to observe the process of lowland invasion into the tepuis as it occurs.

While the authors focus entirely on the flora of the GH, the question in my mind how rapid anthropogenic climate change will effect the faunal communities of the tepui summits and the highlands. What is the level of interdependence between the endemic fauna and flora? Are there symbiotic relationships which have developed between endemic arthropods and certain vascular plant communities on the tepui summits? We know very little about the history of the ecosystems on the tepuis, and in light of the vertical migration mechanism, establishing a detailed paleoecological record of the Pantepui would be necessary to plan conservation initiatives. From the three works in this review, it can be surmised that the current floral composition of the Pantepui region and the Guiana Highlands have been consistent since the end of the LGM. What remains unknown is the faunal composition of the tepuis over the last several million years. To determine the paleofaunal composition of the ancient tepuis, I suggest an analysis of the modern Pantepui endemic fauna to determine the antiquity of tepui faunal assemblages. It has been stated that the tepui summits are devoid of large faunal elements, both in terms of indigenous mammals and larger reptiles.³ By comparing the genetic drift and taxonomical differences in the herpetofauna and arthropods of the tepui summits and GH in general, one can determine their ages of establishment, and compare these dates to that of the surrounding lowlands.

I previously reviewed a paper which touched upon this issue. In “Is the 'Lost World' Lost? High endemism of amphibians and reptiles on South American Tepuis in a Changing Climate” Rodder, Schluter and Lotters attempt to use herpetofaunal endemicity rates to determine how the tepui ecosystems developed (ie vertical migration via the cool climate hypothesis), and how habitat shifts will occur if the climate continues to change. This work is in part based upon the vertical migrations ( such as those proposed by Rull in 2004,), as well as observations of the patterns of herpetofaunal endemicity on the tepui summits. In this work, a number of observations relevant to my proposed analysis are made.

1.The endemicity of amphibians and reptiles is fairtly high in the Pantepui, at 77.3% and 54.8% respectively.

2. According to the Cool climate hypothesis ( which the authors work supports), tepui biota migrate into the lowlands during glacial periods, allowing for biological exchange between isolated communities.

3. The comparisons between massifs demonstrate that the herpetofauna show limited overlap between different massifs. For example, Auyan and Chimanta, two proximal tepuis, share less than a 40% affinity between their respective herptofaunal communities. Tepuis which are far removed from each other share an average of zero percent affinity.

4. The break down of similarity is as follows: Cerro Yavi and Yutaje are most similar, followed by th eastern massifs of Los Testigos, Aprada tepui, Chimanta Tepui, Auyan tepui, and Cerro Guiaquinima, Duida-Marahuaka, Jaua Tepui, Neblina-aracamuni and the Eastern Chain tepuis are the lest similar to each other in fauna composition. The results seem to support the cool climate model, as the tepuis with higher affinities were connected during cold periods. Outliers include Cerro Guiaquinima, which has similarities with Eastern Massifs such as Auyan, but were not connected by a climate envelope during the LGM. Nor can the climate enveloped explain the uniqueness of the Eastern Chain Tepuis herpetofauna.

Thus, it would seem that the herpetofauna is subject to similar phenomena of vertical migration, although there are outliers which contradict this in some specific cases. What is important here is how distinct the endemic species in the Pantepui region are from the lowland species. Does this distinction make the tepui summit species completely different from the lowland species, or are the two groups related?

I recall a few articles mentioning that the endemic tepui toad genus Oreophrynella is somehow a “living fossil”, supposedly sharing similarities to Jurassic species, as well as West African frogs.⁴ This genus of toad and others such as the frog Pristimantis and snake Thamnodynastes are considered monophylitic highland groups, having developed in the GH. How accurate is this assessment? First, Oreophrynella is a member of the superfamily Bufonoidea, which has 35 genera, and 485 species distributed world wide.⁵ Bufonoidea is generally associated with South America, where as its sister group Ranoidea is associated with Africa.⁶ One wonders how a member of a globally distributed superfamily can be considered a living fossil. Does this particular Bufonoid, Oreophrynella, resemble members of the Ranoidea in such a way that it is taxonomically similar to African toads, and possibly a relict species? This issue of relic extant paleofauna on the tepui summits was dismissed by Havelkova et al in 2006 with the statement “ Nowadays, this dispersal scenario (ie- repeated dispersion and local speciation) in the combination with vicariant scenario is more considered than simply vicariant (refuge) scenario ...in this context, many so-called living fossils (eg the toad Oreophrynella) are now unsupported illusions.”⁷ As support for this assertion, Havelkova references the 2004 and 2005 articles of Dr. Valenti Rull, which deal with floral displacement during the Pleistocene. While this model explains the floral assemblages, it does not prove herpetofaunal dispersal or vicariant evolution.

To understand the herpetofauna of the Pantepui, it is useful to examine the composition of the known herpetofauna of the largest continuous tepui, Auyan Tepui. Myers and Donnelly have mentioned 24 species of reptiles on Auyan Tepui, (12 families, 20 genera, 24 species), which is considered diverse compared to other tepui summits. Chimanta tepui, 50 kilometers away, shares a combined 11% of its species with Auyan, 44% of genera, and 62% of families.⁸ Given this low level of overlap between the two proximal tepuis, it is possible to infer that faunal mixing does not occur on a regular basis. Reasons for this include such issues as topography, climate envelopes, and other barriers. The key question here is the date of herpetofaunal establishment. The origin of the family Bufonidea is clarified to some extent by Parmuk et al, in which the authors establish that Bufonidea originated in the Cretaceous of South America, initially displayed a post-gondwanan distribution, rapidly expanded globally, then returned to South America in a second radiation in the Oligocene.⁹ The double radiation hypothesis is what will reveal the origin of the herpeofauna of the tepui summits. If Oreophrynella is an isolated organism which existed in the GH since the initial development of Bufonoids in the Cretaceous, then it is a living fossil to some degree. This would be a unique situation as the oldest Bufonoids in the region are present in the Caribbean, and represent an ancient lineage from the initial radiation that is “consistent with colonization following the bolide impact at the K/T boundary”.¹⁰ The credible notion that Oreophrynella represents a form of paleofauna is refuted again in the paper by Santos et al (2009), in which the origin of Amazonian amphibians are demonstrated to come from the Andes during the Miocene.¹¹ While this paper focuses on poisonous frogs, it does demonstrate that the oldest lineages of poison frogs originated in the Guiana Shiled and Venezuelan Highlands, with the oldest speciation of Dendrobatidae at 40.9 mya in Venezuela. This seems to led credence to the notion that amphibians from the GH may be derived from basal lineages. The authors speculate that “The depauperate dendrobatid fauna of the Venezuelan llanos and Brazilian Shield plateau is puzzling, but might be related to Holocene aridity.”, which demonstrates that the highlands may act as a refuge for previously widespread species.¹² Thus, it seems that the vast majority of amphibians in the Venezuelan highlands represent Eocene and Miocene invasions, while some species may be outliers. In my limited attempt to find a solution to the issue of paleofauna, my search generated more questions than specific solutions. In general it can be stated that tepui herpetofauna is primarily derived from Miocene species, but further research is necessary due to possible under sampling and lack of data.

To clarify the issue of amphibian and reptile establishment in the Pantepui, an investigation to into the origin of Oreophrynella on the tepui summits may need to be conducted. As a result of the restrictions on genetic sampling and analysis of tepui biota, (as mentioned earlier), such an undertaking may prove difficult. If Oreophrynella is part of the original speciation of Bufoidea, then it is a living fossil in some respect. If it is part of a Miocene diversification and invasion from the Andes, then information will allow scientists to track the establishment to tepui herpetofauna with greater precision. In either event, this species will shed light on the origins and establishment of highland and tepui ecosystems and organisms. This may go a long way to determine exactly how global climate change will effect not only the vegetation of the tepuis, but also how animals will respond to the changing climate. Will extinctions occur across the herpetofauna of the GH, as current species die off and lowland organisms replace them? Or will organisms like Oreophrynella survive future temperature change and adapt to the changing vegetation?

Finally, the future studies and conservation methodologies recommended in these works need to be investigated. The possibility of ex situ conservation in a different, stable and analogous location needs to be taken seriously, and a plan needs to be developed. Simple seed banking is not enough, as it does not preserve ecosystem levels of biodiversity. Seed banking is analogous to keeping representatives of a species in a zoo; the complex interactions between the organisms and their native environments are not preserved.

Conclusion

These works represent some of the best investigations into the nature of the tepuis available in scholarly publications. They are concise, supported by parallel research, and predictive. They also require further investigations to support and expand on their conclusions, in order to preserve indigenous and global biodiversity. These papers form a new understanding of the dynamics of a still little explored region, and as such are the cornerstones of further research.

Several investigations based on these works come immediately to mind. First, some outstanding questions remain on the details of faunal establishment on the tepui summits. As discussed, the origin of Oreophrynella need to be determined, in order to place this genus in or out of the realm of paleofauna. As addressed in different works, the establishment of herpetofauna probably differs from the establishment of arthropods and mammals in the Highlands and tepui summits, and almost certainly differs from the methods which establish avifauna on the tepui summits. A comparative analysis of these dissimilar tepui organisms needs to be created, including phylogenetic analysis to trace the origin and development patterns of tepui fauna. Creating a phylogenetic cladogram of the Oreophrynella genus is an obvious first step, using specimens already gathered. The next step would be a comparison of all tepui to lowland heretofauna, which would reveal a great deal about the natural history of the tepuis, and their interaction with lowland species.

A similar investigation which may prove interesting would be to track the levels of lowland invasion into the highlands. In this case, critical elements that have been addressed in other works, as well as the results of the first recommended investigation, can be utilized to develop a tentative model for the rates of lowland invasion and vertical migration into the highlands. It has been noted by Michelangeli, Huber, and Havelkova as well as others that on occasion larger vertebrates invade the tepuis.¹³ This is a fairly recent observation, and needs further investigation. Thus, the second proposed investigation would be looking for anomalous biota in the Guyana Highlands. This would be a preliminary investigation, seeking to track and analyze both plants and animals which have an increased presence in the highlands, as predicted by the works of the authors reviewed in this paper. A preliminary investigation would then necessitate field work and continual monitoring of the tepuis to examine what organisms are entering the area, and if they are replacing known tepui organisms.

A third investigation needs to be undertaken to examine the possibilities of ex-situ conservation. The authors mention this as a possible strategy to preserve the biodiversity of the GH, but never go into any detail regarding its feasibility or desirability. Ex-situ conservation will need to be examined in detail; realities of seed banking, park/reserve establishment, and the technical, economic, and political hurdles which go along with such an undertaking need to bes established. The feasibility and desirability of such a project needs to be examined along with the ethical implications of housing organisms outside of their indigenous environment. In this spirit, a paper which addresses the sociological, political and economic landscape of the GH needs to be produced. I attempted a stripped down version of such a paper in 2009, and this work needs to be reformulated, expanded and updated to focus on the future of the GH.¹⁴ With the completion of these three recommended projects, a good deal of questions can be answered regarding what has been happening in the GH, what is currently occurring (both biologically and sociologically), and what must happen to avoid irreparable biodiversity loss in the near future.

1Rull, “Ecology and Paleoecology: two approaches, One objective” The Open Ecology Journal, 2010, 3, 1-5

2Rull, “Is the 'Lost World' really lost? Paleoecological insights into the origin of the peculiar flora of the Guayana Highlands” Naturwissenschaften 91, 2004

3 Havelkova et al. Brown-Nosed coati (Nasua nasus vittata) on the Roraima tepui (Carnivora: Procyonidae). Lynx (Praha) no 37. 2006.

4Specifically, National Geographics' May 1989 Article “Venezuela's Islands in Time” by Uwe George comes to mind.

5 Frost et al, “The Amphibian Tree of Life,” Bulletin of the Americna Museum of Natural History, No 297, 2006.

6Continental break up and ordinal diversification of birds and mammals. Hedges et al. Nature, vol 381, may 1996.

7 Havelkova et al. Brown-Nosed coati (Nasua nasus vittata) on the Roraima tepui (Carnivora: Procyonidae). Lynx (Praha) no 37. 2006.

8Myers and Donnelly, “The summit Herpetofauna of Auyantepui, Venezuela, Report from the Rober G. Goelet American Museum- Terramar Expedition.” Bulletin of the Amercian Museum Of Natural History, 308 1-47 2008.

9Parmuk et al “around the World in 10 million years, biogeography of the nearly cosmopolitan true toads (Anura:Bufonidea) Global Ecology and Biogeography, 2007.

10Parmuk et al “around the World in 10 million years, biogeography of the nearly cosmopolitan true toads (Anura:Bufonidea) Global Ecology and Biogeography, 2007.

11Santos, Juan C. “Amazonian Amphibian Diversity is Primarily Derived from Late Miocene Lineages”. PloS Biology, Volume 7, March 2009.

12Santos, Juan C. “Amazonian Amphibian Diversity is Primarily Derived from Late Miocene Lineages”. PloS Biology, Volume 7, March 2009.

13Huber, Otto “Guayana highlands versus Guayana Lowlands, A Reappraisal.” Taxon, 37 (3), August, 1988, Havelkova et al. Brown-Nosed coati (Nasua nasus vittata) on the Roraima tepui (Carnivora: Procyonidae). Lynx (Praha) no 37. 2006.

14Barkoczy, Laszlo. “Globalizing a Lost World: Beauty or Benefit, What drives Conservation?” The International Relations Journal, San Francisco State University, Vol 28, Spring 2009.