Fossil pollen resolves origin of the South African Proteaceae as transcontinental not transoceanic.

BACKGROUND AND AIMS: The prevailing view from the areocladogenesis of molecular phylogenies is that the iconic South African Cape Proteaceae (subfamily Proteoideae) arrived from Australia across the Indian Ocean in the Upper Cretaceous (100‒65 million years ago, Ma). Since fossil pollen indicates that the family probably arose in North-West Africa during the early Cretaceous, an alternative view is that it migrated to the Cape from North-Central Africa. The plan therefore was to collate fossil pollen records throughout Africa to determine if they are consistent with an African (para-autochthonous) origin for the Cape Proteaceae, and to seek further support from other paleo-disciplines. METHODS: Palynology (identity, date and location of records), molecular phylogeny and chronogram preparation, biogeography of plate tectonics, and paleo-atmospheric and ocean circulation models. KEY RESULTS: Our collation of the rich assemblage of Proteaceae palynomorphs stretching back to 107 Ma (Triorites africaensis) in North-West Africa showed its progressive overland migration to the Cape by 75‒65 Ma. No key palynomorphs recorded in Australia-Antarctica have morphological affinities with African fossils but specific clade assignment of the preMiocene records is not currently possible. The Cape Proteaceae encompass three molecular-based clades (tribes) whose most-recent apparent ancestors are sisters to those in Australia. However, our chronogram shows that the major Adenanthos/Leucadendron-related clade, originating 54‒34 Ma, would have 'arrived' too late as species with Proteaceae affinities were already present ~20 My earlier. The Franklandia/Protea-related clade arose 118‒81 Ma so its distinctive pollen should have been the foundation for the scores of palynomorphs recorded at 100‒80 Ma but it was not. Also, the prevailing winds and ocean currents trended away from South Africa rather than towards, as the 'out-of-Australia' hypothesis requires. Based on the evidence assembled here, we list three points favouring an Australian origin and nine against; four points favouring an Antarctic origin and seven against; and nine points favouring a North-Central African origin and three against. CONCLUSIONS: We conclude that a gradual migration of the Proteaceae from North-Central Africa southeast→south→southwest to the Cape and surrounds occurred via adaptation and speciation during the period 90‒70 Ma. We caution that incorrect conclusions may be drawn from literal interpretations of molecular phylogenies that neglect the fossil record and do not recognize the possible confounding effects of selection under matched environments leading to parallel evolution and extinction of bona fide sister clades.

Plant richness, turnover, and evolutionary diversity track gradients of stability and ecological opportunity in a megadiversity center.

Research on global patterns of diversity has been dominated by studies seeking explanations for the equator-to-poles decline in richness of most groups of organisms, namely the latitudinal diversity gradient. A problem with this gradient is that it conflates two key explanations, namely biome stability (age and area) and productivity (ecological opportunity). Investigating longitudinal gradients in diversity can overcome this problem. Here we investigate a longitudinal gradient in plant diversity in the megadiverse Cape Floristic Region (CFR). We test predictions of the age and area and ecological opportunity hypotheses using metrics for both taxonomic and phylogenetic diversity and turnover. Our plant dataset includes modeled occurrences for 4,813 species and dated molecular phylogenies for 21 clades endemic to the CFR. Climate and biome stability were quantified over the past 140,000 y for testing the age and area hypothesis, and measures of topographic diversity, rainfall seasonality, and productivity were used to test the ecological opportunity hypothesis. Results from our spatial regression models showed biome stability, rainfall seasonality, and topographic heterogeneity were the strongest predictors of taxonomic diversity. Biome stability alone was the strongest predictor of all diversity metrics, and productivity played only a marginal role. We argue that age and area in conjunction with non-productivity-based measures of ecological opportunity explain the CFR's longitudinal diversity gradient. We suggest that this model may possibly be a general explanation for global diversity patterns, unconstrained as it is by the collinearities underpinning the latitudinal diversity gradient.

Fire-mediated germination syndromes in Leucadendron (Proteaceae) and their functional correlates.

A mechanistic understanding of fire-driven seedling recruitment is essential for effective conservation management of fire-prone vegetation, such as South African fynbos, especially with rare and threatened taxa. The genus Leucadendron (Proteaceae) is an ideal candidate for comparative germination studies, comprising 85 species with a mixture of contrasting life-history traits (killed by fire vs able to resprout; serotinous vs geosporous) and seed morphologies (nutlets vs winged achenes). Individual and combined effects of heat and smoke on seed germination of 40 species were quantified in the laboratory, and Bayesian inference applied to distinguish biologically meaningful treatment effects from non-zero, but biologically trivial, effects. Three germination syndromes were identified based on whether germination was dependent on, enhanced by, or independent of direct fire cues (heat and smoke). Seed storage location was the most reliable predictor of germination syndromes, with soil-stored seeds c. 80% more likely to respond to direct fire cues (primarily smoke) than canopy-stored seeds. Notable exceptions were L. linifolium, with an absolute requirement for smoke to germinate (the third serotinous species so reported), and two other serotinous species with smoke-enhanced germination. Nutlet-bearing species, whether serotinous or geosporous, were c. 70% more likely to respond to fire cues than winged seeds, but there was no evidence for an effect of phylogeny or persistence strategy on germination. This comprehensive account of seed germination characteristics and identification of germination syndromes and their predictors, supports propagation, conservation and restoration initiatives in this iconic fynbos genus and other fire-prone shrubs with canopy or soil-stored seeds.

Foraging potential of underground storage organ plants in the southern Cape, South Africa.

Underground storage organs (USOs) serve as a staple source of carbohydrates for many hunter-gatherer societies and they feature prominently in discussions of diets of early modern humans. While the way of life of hunter-gatherers in South Africa's Cape no longer exists, there is extensive ethnographic, historical, and archaeological evidence of hunter-gatherers' use of USOs. This is to be expected, given that the Cape supports the largest concentration of plant species with USOs globally. The southern Cape is the location of several Middle Stone Age sites that are highly significant to research on the origins of behaviourally modern humans, and this provided the context for our research. Here, we evaluate the foraging potential of USOs by identifying how abundant edible biomass is in the southern Cape, how easily it is gathered, and how nutritious it is. One hundred 5 × 5 m plots were assessed in terms of USO species and abundance. Nearly all of the sites sampled (83%) contained edible USOs and some had high concentrations of edible biomass. Extrapolating from these sites suggests that the edible USO biomass falls within the range of biomass observed in areas supporting extant hunter-gatherer communities. The nutritional content for six USO species was assessed; these contained between 40 and 228 calories/100 g. Furthermore, foraging events were staged to provide an indication of the potential return rates for the same six USOs. The target species grow near the soil surface, mostly in sandy soils, and were gathered with minimal effort. Some 50% of the foraging events conducted yielded enough calories to meet the daily requirements of a hunter-gatherer within two hours. In conclusion, we demonstrate that USOs are a readily available source of carbohydrates in the southern Cape landscape and, therefore, there is a strong possibility that USOs played a critical role in providing food for early humans.

Return rates from intertidal foraging from Blombos Cave to Pinnacle Point: Understanding early human economies.

The south coast of South Africa provides the earliest evidence for Middle Stone Age (MSA) coastal resource exploitation by early Homo sapiens. In coastal archaeology worldwide, there has been a debate over the general productivity of intertidal foraging, leading to studies that directly measure productivity in some regions, but there have been no such studies in South Africa. Here we present energetic return rate estimates for intertidal foraging along the southern coast of South Africa from Blombos Cave to Pinnacle Point. Foraging experiments were conducted with Khoi-San descendants of the region, and hourly caloric return rates for experienced foragers were measured on 41 days near low tide and through three seasons over two study years. On-site return rates varied as a function of sex, tidal level, marine habitat type and weather conditions. The overall energetic return rate from the entire sample (1492 kcal h(-1)) equals or exceeds intertidal returns reported from other hunter-gatherer studies, as well as measured return rates for activities as diverse as hunting mammals and plant collecting. Returns are projected to be exceptionally high (∼ 3400 kcal h(-1) for men, ∼ 1900 kcal h(-1) for women) under the best combination of conditions. However, because of the monthly tidal cycle, high return foraging is only possible for about 10 days per month and for only 2-3 h on those days. These experiments suggest that while intertidal resources are attractive, women and children could not have subsisted independently, nor met all their protein-lipid needs from marine resources alone, and would have required substantial additional energy and nutrients from plant gathering and/or from males contributing game.

Using counterfactuals to evaluate the cost-effectiveness of controlling biological invasions.

Prioritizing limited conservation funds for controlling biological invasions requires accurate estimates of the effectiveness of interventions to remove invasive species and their cost-effectiveness (cost per unit area or individual). Despite billions of dollars spent controlling biological invasions worldwide, it is unclear whether those efforts are effective, and cost-effective. The paucity of evidence results from the difficulty in measuring the effect of invasive species removal: a researcher must estimate the difference in outcomes (e.g. invasive species cover) between where the removal program intervened and what might have been observed if the program had not intervened. In the program evaluation literature, this is called a counterfactual analysis, which formally compares what actually happened and what would have happened in the absence of an intervention. When program implementation is not randomized, estimating counterfactual outcomes is especially difficult. We show how a thorough understanding of program implementation, combined with a matching empirical design can improve the way counterfactual outcomes are estimated in nonexperimental contexts. As a practical demonstration, we estimated the cost-effectiveness of South Africa's Working for Water program, arguably the world's most ambitious invasive species control program, in removing invasive alien trees from different land use types, across a large area in the Cape Floristic Region. We estimated that the proportion of the treatment area covered by invasive trees would have been 49% higher (5.5% instead of 2.7% of the grid cells occupied) had the program not intervened. Our estimates of cost per hectare to remove invasive species, however, are three to five times higher than the predictions made when the program was initiated. Had there been no control (counter-factual), invasive trees would have spread on untransformed land, but not on land parcels containing plantations or land transformed by agriculture or human settlements. This implies that the program might have prevented a larger area from being invaded if it had focused all of its clearing effort on untransformed land. Our results show that, with appropriate empirical designs, it is possible to better evaluate the impacts of invasive species removal and therefore to learn from past experiences.

Fossil evidence for a hyperdiverse sclerophyll flora under a non-Mediterranean-type climate.

The spectacular diversity of sclerophyll plants in the Cape Floristic Region in South Africa and Australia's Southwest Floristic Region has been attributed to either explosive radiation on infertile soils under fire-prone, summer-dry climates or sustained accretion of species under inferred stable climate regimes. However, the very poor fossil record of these regions has made these ideas difficult to test. Here, we reconstruct ecological-scale plant species richness from an exceptionally well-preserved fossil flora. We show that a hyperdiverse sclerophyll flora existed under high-rainfall, summer-wet climates in the Early Pleistocene in southeastern Australia. The sclerophyll flora of this region must, therefore, have suffered subsequent extinctions to result in its current relatively low diversity. This regional loss of sclerophyll diversity occurred at the same time as a loss of rainforest diversity and cannot be explained by ecological substitution of species of one ecological type by another type. We show that sclerophyll hyperdiversity has developed in distinctly non-Mediterranean climates, and this diversity is, therefore, more likely a response to long-term climate stability. Climate stability may have both reduced the intensity of extinctions associated with the Pleistocene climate cycles and promoted the accumulation of species richness by encouraging genetic divergence between populations and discouraging plant dispersal.

Expert-derived monitoring thresholds for impacts of megaherbivores on vegetation cover in a protected area.

Monitoring is meant to inform conservation authorities, yet managers often don't know when to respond to monitoring results. One of the reasons is that management often lacks consensus on monitoring thresholds for intervention. This results in aimless monitoring without a clear directive on when monitoring indicates a trajectory towards an unacceptable state or impending change, which possibly necessitates intervention. Although experts rarely provide simple, measureable and quantifiable monitoring thresholds as required by management, they are often more comfortable expressing opinions on whether a specific area is desirable or not. This allows thresholds to be reverse engineered: by getting experts to identify sites as desirable and undesirable, field variables can subsequently be measured to derive the boundary between subjectively identified desirable and undesirable states. Such a boundary provides a defendable point for management to assess and consider intervention. Here we describe the identification of monitoring thresholds by defining the limits of desirable canopy cover, derived from expert stakeholder preferences, in the Sundays Spekboom Thicket vegetation of the Addo Elephant National Park, South Africa. The park has experienced variable utilization intensity by large herbivores, especially elephant. For years managers have grappled with the question of what percentage shrub canopy cover is desirable as a management target, but science has failed to provide this. Using experts to assess pre-selected sites as desirable or undesirable across a range of canopy covers, we showed that a canopy cover of ∼65% (±15%) would be desirable for expert stakeholders. We then used satellite imagery to map canopy cover, providing managers for the first time with a large-scale map of canopy cover, indicating desirability status. This approach was useful for facilitating joint-decision making between conservation agencies and stakeholders on tangible indicators of achieving goals, and may be useful in fostering relationships, trust, mutual understanding and transparency, characteristics critical for managing complex socio-ecological systems.

A new research strategy for integrating studies of paleoclimate, paleoenvironment, and paleoanthropology.

Paleoanthropologists (scientists studying human origins) universally recognize the evolutionary significance of ancient climates and environments for understanding human origins. Even those scientists working in recent phases of human evolution, when modern humans evolved, agree that hunter-gatherer adaptations are tied to the way that climate and environment shape the food and technological resource base. The result is a long tradition of paleoanthropologists engaging with climate and environmental scientists in an effort to understand if and how hominin bio-behavioral evolution responded to climate and environmental change. Despite this unusual consonance, the anticipated rewards of this synergy are unrealized and, in our opinion, will not reach potential until there are some fundamental changes in the way the research model is constructed. Discovering the relation between climate and environmental change to human origins must be grounded in a theoretical framework and a causal understanding of the connection between climate, environment, resource patterning, behavior, and morphology, then move beyond the strict correlative research that continues to dominate the field.

Extinction risk and diversification are linked in a plant biodiversity hotspot.

It is widely recognized that we are entering an extinction event on a scale approaching the mass extinctions seen in the fossil record. Present-day rates of extinction are estimated to be several orders of magnitude greater than background rates and are projected to increase further if current trends continue. In vertebrates, species traits, such as body size, fecundity, and geographic range, are important predictors of vulnerability. Although plants are the basis for life on Earth, our knowledge of plant extinctions and vulnerabilities is lagging. Here, we disentangle the underlying drivers of extinction risk in plants, focusing on the Cape of South Africa, a global biodiversity hotspot. By comparing Red List data for the British and South African floras, we demonstrate that the taxonomic distribution of extinction risk differs significantly between regions, inconsistent with a simple, trait-based model of extinction. Using a comprehensive phylogenetic tree for the Cape, we reveal a phylogenetic signal in the distribution of plant extinction risks but show that the most threatened species cluster within short branches at the tips of the phylogeny--opposite to trends in mammals. From analyzing the distribution of threatened species across 11 exemplar clades, we suggest that mode of speciation best explains the unusual phylogenetic structure of extinction risks in plants of the Cape. Our results demonstrate that explanations for elevated extinction risk in plants of the Cape flora differ dramatically from those recognized for vertebrates. In the Cape, extinction risk is higher for young and fast-evolving plant lineages and cannot be explained by correlations with simple biological traits. Critically, we find that the most vulnerable plant species are nonetheless marching towards extinction at a more rapid pace but, surprisingly, independently from anthropogenic effects. Our results have important implications for conservation priorities and cast doubts on the utility of current Red List criteria for plants in regions such as the Cape, where speciation has been rapid, if our aim is to maximize the preservation of the tree-of-life.