Emergent trees in Colophospermum mopane woodland: influence of elephant density on persistence versus attrition.

Colophospermum mopane (mopane) forms mono-dominant woodlands covering extensive areas of southern Africa. Mopane provides a staple foodstuff for elephants, who hedge woodland by reducing trees to small trees or shrubs, leaving emergent trees which are too large to be pollarded. Emergent trees are important for supporting faunal biodiversity, but they can be killed by ringbarking. This study first examined the influence of elephant density on woodland transformation and the height distribution of canopy volume, and, second, whether canopy volume is maintained, and tall emergent trees too large to be broken can persist, under chronic elephant utilisation. Three regimes of 0.23, 0.59 and 2.75 elephants km-2 differed in vegetation structure and the height structure of trees. Areas under the highest elephant density supported the lowest total canopy volume owing to less canopy for plants >3 m in height, shorter trees, loss of most trees 6-10 m in height, but trees >10 m in height (>45 cm stem diameter) persisted. Under eight years of chronic utilisation by elephants, transformed mopane woodland maintained its plant density and canopy volume. Plant density was greatest for the 0-1 m height class, whereas the 3.1-6 m height class provided the bulk of canopy volume, and the 1.1-3 m height layer contained the most canopy volume. Emergent trees (>10 m in height) suffered a loss of 1.4% per annum as a result of debarking. Canopy dieback of emergent trees increased conspicuously when more than 50% of a stem was debarked, and such trees could be toppled by windthrow before being ringbarked. Thus relict emergent trees will slowly be eliminated but will not be replaced whilst smaller trees are being maintained in a pollarded state. Woodland transformation has not markedly reduced canopy volume available to elephants, but the slow attrition of emergent trees may affect supported biota, especially cavity-dependent vertebrate species, making use of these trees.

Hydraulic segmentation explains differences in loss of branch conductance caused by fire.

The hydraulic death hypothesis suggests that fires kill trees by damaging the plant's hydraulic continuum in addition to stem cambium. A corollary to this hypothesis is that plants that survive fires possess 'pyrohydraulic' traits that prevent heat-induced embolism formation in the xylem and aid post-fire survival. We examine whether hydraulic segmentation within stem xylem may act as such a trait. To do so, we measured the percentage loss of conductance (PLC) and vulnerability to embolism axially along segments of branches exposed to heat plumes in two differing species, fire-tolerant Eucalyptus cladocalyx F. Muell and fire-sensitive Kiggelaria africana L., testing model predictions that fire-tolerant species would exhibit higher degrees of hydraulic segmentation (greater PLC in the distal parts of the branch than the basal) than fire-intolerant species (similar PLC between segments). Following exposure to a heat plume, K. africana suffered between 73 and 84% loss of conductance in all branch segments, whereas E. cladocalyx had 73% loss of conductance in whole branches, including the distal tips, falling to 29% in the most basal part of the branch. There was no evidence for differences in resistance segmentation between the species, and there was limited evidence for differences in distal vulnerability to embolism across the branches. Hydraulic segmentation in E. cladocalyx may enable it to resprout effectively post-fire with a functional hydraulic system. The lack of hydraulic segmentation in K. africana reveals the need to understand possible trade-offs associated with hydraulic segmentation in long-lived woody species with respect to drought and fire.

The enantiostylous floral polymorphism of Barberetta aurea (Haemodoraceae) facilitates wing pollination by syrphid flies.

BACKGROUND AND AIMS: Sexual polymorphisms of flowers have traditionally been interpreted as devices that promote cross-pollination, but they may also represent adaptations for exploiting particular pollination niches in local environments. The cross-pollination function of enantiostyly, characterized by flowers having either left- or right-deflected styles, has been uncertain in some lineages, such as the Haemodoraceae, because the positioning of stamens and styles is not always completely reciprocal among morphs. METHODS: We examined the floral biology of populations of the poorly known species Barberetta aurea (Haemodoraceae) across its native range in South Africa to establish the general features of its enanatiostylous reproductive system and the agents and mechanism of pollen transfer. RESULTS: We confirmed that B. aurea has a system of dimorphic enantiostyly. Style morph ratios varied among populations sampled, but with an overall tendency to being equal. Crossing experiments demonstrated that B. aurea is fully self-compatible, that intra- and inter-morph crosses are equally fertile and that it is wholly dependent on pollinator visits for seed production. Pollination is mainly by syrphid flies that transfer the sticky pollen via their wings, which contact the anthers and stigma precisely as they hover during approach and feeding. The majority of syrphid fly visitors feed on a film of highly concentrated nectar situated at the base of ultraviolet-absorbent 'nectar guides'. Because one of the three stamens is deflected in the same direction as the style, we predicted a high likelihood of intra-morph pollination, and this was corroborated by patterns of transfer of coloured dye particles in cage experiments involving syrphid flies. CONCLUSIONS: Barbaretta aurea exhibits dimorphic enantiostyly and, in contrast to most enantiostylous species, which are pollinated by bees, its flowers are specialized for pollination by syrphid flies. The lack of complete reciprocity of the enantiostylous arrangement of sexual organs facilitates both inter- and intra-morph pollen transfer on the wings of these flies.

Biomechanics of nectar feeding explain flower orientation in plants pollinated by long-proboscid flies.

The function of flower orientation is much debated, with adaptation to pollinator mouthparts being a particularly compelling explanation, but also one that has lacked empirical support from broad-scale comparative studies. The two families of long-proboscid fly pollinators show similar hovering behaviour while feeding on nectar but differ in the biomechanics of their proboscides which can be up to 80 mm in length: Tabanidae have a fixed forward-pointing proboscis while Nemestrinidae can swivel their proboscis downwards. We predicted that this difference has implications for the evolution of flower orientation. We established the flower angles of 156 South African plant species specialised for pollination by long-proboscid flies. Using a phylogenetically corrected analysis, we found that flowers pollinated by Tabanidae tend to be horizontally orientated, while those pollinated by Nemestrinidae tend to be more variable in orientation and more often vertically orientated. These results confirm the importance of pollinator biomechanics for the evolution of floral traits and highlight a potential mechanism of reproductive isolation between sympatric plant species pollinated by different long-proboscid fly families.

Unequal allocation between male versus female reproduction cannot explain extreme vegetative dimorphism in Aulax species (Cape Proteaceae).

Female plants not only flower but also produce resource-rich seeds, fruits, and cones. Thus, it is generally considered that female plants allocate more resources to sexual reproduction than male plants and that this allocation difference can explain vegetative dimorphism, such as greater leaf size in females. We found significant sexual vegetative differences in the dioecious and serotinous species, Aulax umbellata and A. cancellata. Plant height, annual branch length and canopy spread were greater in males whereas leaf size, branch thickness and branch number were greater in females. Sex ratios and basal stem area were, however, equal in the sexes. Equal sex ratios imply equal allocation to sexual reproduction and equal stem areas imply equal resource use and biomass, and thus allocation to vegetative growth. Given equal allocation to reproduction and resource use, we suggest that the vegetative dimorphism is driven by intra-male-competition to be more visually conspicuous to pollinators. This implies that plant architecture is both a vegetative and a reproductive trait.

Corolla stickiness prevents nectar robbing in Erica.

Floral stickiness is a rare trait with unknown function, but it is common in the mega-diverse Cape genus Erica (Ericaceae). This study investigated the role of stickiness measured as adhesive strength in Erica as protection against nectar robbing and its correlation with floral traits. We compared the incidence of nectar robbing in flowers of the same species with or without experimentally added stickiness, and amongst communities of co-occurring species with flowers differing in stickiness. Additionally, we tested the relationship between stickiness and pollination syndrome, corolla shape, corolla length and sepal-corolla ratio across the whole genus. Stickiness was correlated with lower floral damage rates within and between species, indicating it functions as an anti-nectar robbing trait. Across the genus Erica, stickiness is most strongly correlated with bird and long-proboscid fly pollination, presumably because of their larger nectar rewards. Stickiness was also correlated with floral traits that are often associated with high risk of being damaged by nectar robbers: narrow-mouthed corollas, long corollas and shorter sepals. These results show that corolla stickiness defends Erica flowers against nectar robbing and thereby potentially improves fitness.

Fairy circles in Namibia are assembled from genetically distinct grasses.

Fairy circles are striking regularly sized and spaced, bare circles surrounded by Stipagrostis grasses that occur over thousands of square kilometres in Namibia. The mechanisms explaining their origin, shape, persistence and regularity remain controversial. One hypothesis for the formation of vegetation rings is based on the centrifugal expansion of a single individual grass plant, via clonal growth and die-back in the centre. Clonality could explain FC origin, shape and long-term persistence as well as their regularity, if one clone competes with adjacent clones. Here, we show that for virtually all tested fairy circles the periphery is not exclusively made up of genetically identical grasses, but these peripheral grasses belong to more than one unrelated genet. These results do not support a clonal explanation for fairy circles. Lack of clonality implies that a biological reason for their origin, shape and regularity must emerge from competition between near neighbor individuals within each fairy circle. Such lack of clonality also suggests a mismatch between longevity of fairy circles versus their constituent plants. Furthermore, our findings of lack of clonality have implications for some models of spatial patterning of fairy circles that are based on self-organization.

Mass sterilization of a common palm species by elephants in Kruger National Park, South Africa.

Chronic herbivory by elephants rarely eliminates any species of woody savanna plants because these plants are typically vigorous basal resprouters after damage by fire or herbivory. In some instances, resprouting after elephant herbivory even increases stem numbers per unit area compared to protected areas. It is thus difficult to know whether an area has been severely degraded by elephant herbivory or not because although trees may be severely reduced in size, they will still be present and may even be relatively dense. By using an elephant exclosure in the Kruger National Park, South Africa, we demonstrate that this resprouting ability masks the fact that entire populations of a widespread African palm, Hyphaene petersiana, are prevented from reaching sexual maturity by chronic elephant herbivory. Besides sterilizing these palms and thus preventing their evolution and seed dispersal, the absence of the palm fruits, flowers and tall stems has other negative biodiversity impacts on their associated fauna. We suggest that to determine sustainable elephant impacts on savanna plants, conservation managers also use the reproductive condition of savanna plants rather than their presence, height or stem density.

Ramification has little impact on shoot hydraulic efficiency in the sexually dimorphic genus Leucadendron (Proteaceae).

Despite the diversity of branching architectures in plants, the impact of this morphological variation on hydraulic efficiency has been poorly studied. Branch junctions are commonly thought to be points of high hydraulic resistance, but adjustments in leaf area or xylem conduit abundance or dimensions could compensate for the additional hydraulic resistance of nodal junctions at the level of the entire shoot. Here we used the sexually dimorphic genus Leucadendron (Proteaceae) to test whether variation in branch ramification impacts shoot hydraulic efficiency. We found that branch ramification was related to leaf traits via Corner's rules such that more highly ramified shoots had smaller leaves, but that branch ramification had little consistent impact on shoot hydraulic efficiency, whether measured on a leaf area or stem cross-sectional area basis. These results suggest that the presumed increase in resistance associated with branching nodes can be compensated by other adjustments at the shoot level (e.g. leaf area adjustments, increased ramification to add additional branches in parallel rather than in series) that maintain hydraulic efficiency at the level of the entire shoot. Despite large morphological differences between males and females in the genus Leucadendron, which are due to differences in pollination and reproduction between the sexes, the physiological differences between males and females are minimal.

Assessing the role of dispersed floral resources for managed bees in providing supporting ecosystem services for crop pollination.

Most pollination ecosystem services studies have focussed on wild pollinators and their dependence on natural floral resources adjacent to crop fields. However, managed pollinators depend on a mixture of floral resources that are spatially separated from the crop field. Here, we consider the supporting role these resources play as an ecosystem services provider to quantify the use and availability of floral resources, and to estimate their relative contribution to support pollination services of managed honeybees. Beekeepers supplying pollination services to the Western Cape deciduous fruit industry were interviewed to obtain information on their use of floral resources. For 120 apiary sites, we also analysed floral resources within a two km radius of each site based on geographic data. The relative availability of floral resources at sites was compared to regional availability. The relative contribution of floral resources-types to sustain managed honeybees was estimated. Beekeepers showed a strong preference for eucalypts and canola. Beekeepers selectively placed more hives at sites with eucalypt and canola and less with natural vegetation. However, at the landscape-scale, eucalypt was the least available resource, whereas natural vegetation was most common. Based on analysis of apiary sites, we estimated that 700,818 ha of natural vegetation, 73,910 ha of canola fields, and 10,485 ha of eucalypt are used to support the managed honeybee industry in the Western Cape. Whereas the Cape managed honeybee system uses a bee native to the region, alien plant species appear disproportionately important among the floral resources being exploited. We suggest that an integrated approach, including evidence from interview and landscape data, and fine-scale biological data is needed to study floral resources supporting managed honeybees.

Experimental evidence for heat plume-induced cavitation and xylem deformation as a mechanism of rapid post-fire tree mortality.

Recent work suggests that hydraulic mechanisms, rather than cambium necrosis, may account for rapid post-fire tree mortality. We experimentally tested for xylem cavitation, as a result of exposure to high-vapour-deficit (D) heat plumes, and permanent xylem deformation, as a result of thermal softening of lignin, in two tree species differing in fire tolerance. We measured percentage loss of conductance (PLC) in distal branches that had been exposed to high-D heat plumes or immersed in hot water baths (high temperature, but not D). Results were compared with predictions from a parameterized hydraulic model. Physical damage to the xylem was examined microscopically. Both species suffered c. 80% PLC when exposed to a 100°C plume. However, at 70°C, the fire-sensitive Kiggelaria africana suffered lower PLC (49%) than the fire-resistant Eucalytpus cladocalyx (80%). Model simulations suggested that differences in PLC between species were a result of greater hydraulic segmentation in E. cladocalyx. Kiggelaria africana suffered considerable PLC (59%), as a result of heat-induced xylem deformation, in the water bath treatments, but E. cladocalyx did not. We suggest that a suite of 'pyrohydraulic' traits, including hydraulic segmentation and heat sensitivity of the xylem, may help to explain why some tree species experience rapid post-fire mortality after low-intensity fires and others do not.

Floral trait evolution associated with shifts between insect and wind pollination in the dioecious genus Leucadendron (Proteaceae).

Transitions between animal and wind pollination have occurred in many lineages and have been linked to various floral modifications, but these have seldom been assessed in a phylogenetic framework. In the dioecious genus Leucadendron (Proteaceae), transitions from insect to wind pollination have occurred at least four times. Using analyses that controlled for relatedness among Leucadendron species, we investigated how these transitions shaped the evolution of floral structural and signaling traits, including the degree of sexual dimorphism in these traits. Pollen grains of wind-pollinated species were found to be smaller, more numerous, and dispersed more efficiently in wind than were those of insect-pollinated species. Wind-pollinated species also exhibited a reduction in spectral contrast between showy subtending leaves and background foliage, reduced volatile emissions, and a greater degree of sexual dimorphism in color and scent. Uniovulate flowers and inflorescence condensation are conserved ancestral features in Leucadendron and likely served as exaptations in shifts to wind pollination. These results offer insights into the key modifications of male and female floral traits involved in transitions between insect and wind pollination.

A synthesis of postfire recovery traits of woody plants in Australian ecosystems.

Postfire resprouting and recruitment from seed are key plant life-history traits that influence population dynamics, community composition and ecosystem function. Species can have one or both of these mechanisms. They confer resilience, which may determine community composition through differential species persistence after fire. To predict ecosystem level responses to changes in climate and fire conditions, we examined the proportions of these plant fire-adaptive traits among woody growth forms of 2880 taxa, in eight fire-prone ecosystems comprising ~87% of Australia's land area. Shrubs comprised 64% of the taxa. More tree (>84%) than shrub (~50%) taxa resprouted. Basal, epicormic and apical resprouting occurred in 71%, 22% and 3% of the taxa, respectively. Most rainforest taxa (91%) were basal resprouters. Many trees (59%) in frequently-burnt eucalypt forest and savanna resprouted epicormically. Although crown fire killed many mallee (62%) and heathland (48%) taxa, fire-cued seeding was common in these systems. Postfire seeding was uncommon in rainforest and in arid Acacia communities that burnt infrequently at low intensity. Resprouting was positively associated with ecosystem productivity, but resprouting type (e.g. basal or epicormic) was associated with local scale fire activity, especially fire frequency. Although rainforest trees can resprout they cannot recruit after intense fires and may decline under future fires. Semi-arid Acacia communities would be susceptible to increasing fire frequencies because they contain few postfire seeders. Ecosystems dominated by obligate seeders (mallee, heath) are also susceptible because predicted shorter inter-fire intervals will prevent seed bank accumulation. Savanna may be resilient to future fires because of the adaptive advantage of epicormic resprouting among the eucalypts. The substantial non-resprouting shrub component of shrublands may decline, but resilient Eucalyptus spp. will continue to dominate under future fire regimes. These patterns of resprouting and postfire seeding provide new insights to ecosystem assembly, resilience and vulnerability to changing fire regimes on this fire-prone continent.

Faecal mimicry by seeds ensures dispersal by dung beetles.

The large brown, round, strongly scented seeds of Ceratocaryum argenteum (Restionaceae) emit many volatiles found to be present in herbivore dung. These seeds attract dung beetles that roll and bury them. As the seeds are hard and offer no reward to the dung beetles, this is a remarkable example of deception in plant seed dispersal.

Convergent and correlated evolution of major life-history traits in the angiosperm genus Leucadendron (Proteaceae).

Natural selection is expected to cause convergence of life histories among taxa as well as correlated evolution of different life-history traits. Here, we quantify the extent of convergence of five key life-history traits (adult fire survival, seed storage, degree of sexual dimorphism, pollination mode, and seed-dispersal mode) and test hypotheses about their correlated evolution in the genus Leucadendron (Proteaceae) from the fire-prone South African fynbos. We reconstructed a new molecular phylogeny of this highly diverse genus that involves more taxa and molecular markers than previously. This reconstruction identifies new clades that were not detected by previous molecular study and morphological classifications. Using this new phylogeny and robust methods that account for phylogenetic uncertainty, we show that the five life-history traits studied were labile during the evolutionary history of the genus. This diversity allowed us to tackle major questions about the correlated evolution of life-history strategies. We found that species with longer seed-dispersal distances tended to evolve lower pollen-dispersal distance, that insect-pollinated species evolved decreased sexual dimorphism, and that species with a persistent soil seed-bank evolved toward reduced fire-survival ability of adults.

Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii?

BACKGROUND AND AIMS: According to the Grant-Stebbins model of pollinator-driven divergence, plants that disperse beyond the range of their specialized pollinator may adapt to a new pollination system. Although this model provides a compelling explanation for pollination ecotype formation, few studies have directly tested its validity in nature. Here we investigate the distribution and pollination biology of several subspecies of the shrub Erica plukenetii from the Cape Floristic Region in South Africa. We analyse these data in a phylogenetic context and combine these results with information on pollinator ranges to test whether the evolution of pollination ecotypes is consistent with the Grant-Stebbins model. METHODS AND KEY RESULTS: Pollinator observations showed that the most common form of E. plukenetii with intermediate corolla length is pollinated by short-billed Orange-breasted sunbirds. Populations at the northern fringe of the distribution are characterized by long corollas, and are mainly pollinated by long-billed Malachite sunbirds. A population with short corollas in the centre of the range was mainly pollinated by insects, particularly short-tongued noctuid moths. Bird exclusion in this population did not have an effect on fruit set, while insect exclusion reduced fruit set. An analysis of floral scent across the range, using coupled gas chromatography-mass spectrometry, showed that the scent bouquets of flowers from moth-pollinated populations are characterized by a larger number of scent compounds and higher emission rates than those in bird-pollinated populations. This was also reflected in clear separation of moth- and bird-pollinated populations in a two-dimensional phenotype space based on non-metric multidimensional scaling analysis of scent data. Phylogenetic analyses of chloroplast and nuclear DNA sequences strongly supported monophyly of E. plukenetii, but not of all the subspecies. Reconstruction of ancestral character states suggests two shifts from traits associated with short-billed Orange-breasted sunbird pollination: one towards traits associated with moth pollination, and one towards traits associated with pollination by long-billed Malachite sunbirds. The latter shift coincided with the colonization of Namaqualand in which Orange-breasted sunbirds are absent. CONCLUSIONS: Erica plukenetii is characterized by three pollination ecotypes, but only the evolutionary transition from short- to long-billed sunbird pollination can be clearly explained by the Grant-Stebbins model. Corolla length is a key character for both ecotype transitions, while floral scent emission was important for the transition from bird to moth pollination.

Pollination systems of Colchicum (Colchicaceae) in southern Africa: evidence for rodent pollination.

BACKGROUND AND AIMS: Plants adapted for pollination by rodents tend to exhibit a distinct floral syndrome that includes dull coloured and geoflorous inflorescences and nocturnal anthesis and nectar production. On the basis of their floral traits, it was predicted that two African Colchicum species (C. scabromarginatum and C. coloratum) are rodent-pollinated. METHODS: Field studies were carried out in the semi-arid Succulent Karoo region of South Africa. Live trapping of rodents was conducted and pollen loads on the rodents were quantified. The daily periodicity of nectar production was determined. Selective exclusion and controlled pollination experiments were also conducted. KEY RESULTS: Live-trapped rodents were found to carry large amounts of Colchicum pollen on the fur of their snouts, and in their faeces. Birds were occasional pollinators of flowers of C. coloratum. During the evening, nectar volume and concentration increased for both species. When vertebrates were excluded from C. scabromarginatum and C. coloratum plants, there was a significant decrease in seed set compared with open control plants. By contrast, vertebrate exclusion did not significantly affect seed production of a congener, C. hantamense, which has floral traits associated with insect pollination. Breeding system experiments revealed that both C. scabromarginatum and C. coloratum require pollinators for seed production. Colchicum scabromarginatum is strictly self-incompatible, whereas C. coloratum is partially self-compatible. CONCLUSIONS: Pollination by rodents occurs in two African Colchicum species. C. scabromarginatum appears to depend exclusively on rodents for seed production, while birds and autonomous selfing may contribute to seed production in C. coloratum. These are the first records of rodent pollination in the Colchicaceae.

Density-dependent outcomes in a digestive mutualism between carnivorous Roridula plants and their associated hemipterans.

Recent studies have shown that mutualisms often have variable outcomes in space and time. In particular, the outcomes may be dependent on the density of the partners with unimodal or saturating outcomes providing stability to the mutualism. We examine density-dependent outcomes of an obligate, species-specific mutualism between a South African carnivorous plant (Roridula dentata) and a hemipteran (Pameridea) that facilitates prey digestion, but also sucks plant sap. Plants occur in sandy, leached, nitrogen-poor soils and have no digestive enzymes to digest prey. Instead they rely on obligately dependent hemipterans to supply nitrogen by digesting prey for them and defecating on their leaves. We documented the densities of Pameridea on Roridula in the field. In the greenhouse, we manipulated the hemipteran densities on Roridula and measured the mean relative growth rates of plants with differing hemipteran densities. Plants exhibited a unimodal response to the density of their mutualist partners. Those with no hemipterans had negative growth rates, suggesting that hemipterans are important in facilitating nitrogen absorption. Plants with intermediate hemipteran densities had positive growth rates but growth rates were negative under very high hemipteran densities. Our research provides support for variable and unimodal outcomes in mutualism. Unimodal outcomes may be particularly important in obligate mutualisms and this is one of the few studied outside of pollinating seed parasite mutualisms. In this system, extrinsic factors such as other predators may affect the mutualism by altering the numbers of hemipterans.