Phylogeny, biogeography, and the evolution of life-history traits in Leucadendron (Proteaceae)

Leucadendron is a moderately large genus of Proteaceae almost entirely restricted to the Cape Floristic Region of southern Africa. The genus is unusual in being dioecious and sexually dimorphic. ITS sequence data were obtained from 62 of the 96 currently recognized taxa (85 species and 11 subspecies). Phylogenetic analyses were conducted under Maximum Likelihood and parsimony and resolved nine groups of species with varying degrees of bootstrap support, but relationships between these groups are largely unsupported. The phylogeny conflicts with the current taxonomic arrangement, which is based mainly on fruit morphology. The two sections of the genus, Alatosperma and Leucadendron, and several subsections within these sections, are resolved as non-monophyletic. This means that taxonomically important characters (such as fruit shape) have evolved multiple times, as the species with nut-like fruit (resolved into two of the nine groups) appear to have evolved independently from ancestors with winged fruit. Based on the topology obtained, the life history traits of anemophily, myrmechochory, and re-sprouting have also originated multiple times. Dispersal-Vicariance (DIVA) analysis suggests that the genus had an ancestral area in the Karoo Mountain and Southeastern phytogeographic centres of endemism in the southwestern Cape.     

Genome size and polyploidy variation in the tropical hardwood genusTerminalia (Combretaceae)

Chromosome complements and 2C DNA amounts of six species ofTerminalia have been studied.Terminalia oliveri, T. myriocarpa andT. arjuna are diploid (2n = 24),T. chebula andT. bellirica are tetraploid (2n = 48),T. muelleri shows a triploid number (2n = 36). Two well demarcated groups of species are recognizable on the basis of chromosome length and 2C DNA values which range from 3.60 pg (T. oliveri) to 12.80 pg (T. bellirica) showing a 3.5-fold difference. Differences of DNA per basic genome or per chromosome are greatest (1.97-fold) betweenT. oliveri andT. arjuna. Two species groups (1)T. oliveri andT. chebula, and (2)T. myriocarpa, T. arjuna, T. muelleri, T. bellirica, therefore are well differentiated by DNA per basic genome, irrespective of polyploidy. The mean values of the two groups are 1.81 pg and 3.34 pg, respectively, showing a 1.84-fold difference. Within diploids and tetraploids there is 1.97-fold and 1.76-fold variation, respectively.     

Molecular variation and fingerprinting of Leucadendron cultivars (Proteaceae) by ISSR markers

BACKGROUND AND AIMS: There are more than 80 species of Leucadendron and most are used as cut flowers. Currently, more than 100 cultivars are used by industry and many of them are interspecific hybrids. The origin of most cultivars is unclear and their genetic diversity and relationships have not been studied. This investigation was carried out to evaluate the genetic variation and relationships among 30 Leucadendron cultivars. METHODS: ISSR markers were applied to determine the genetic variation and to discriminate Leucadendron cultivars. Sixty-four ISSR primers were screened and 25 primers were selected for their ability to produce clear and reproducible patterns of multiple bands. KEY RESULTS: A total of 584 bands of 305-2400 bp were amplified, of which 97 % were polymorphic. A dendrogram generated using the Unweighted Pair Group Method with Arithmetic Average based on a distance measure of total character difference showed that the Leucadendron cultivars clustered into two main groups. Twenty-four of the 30 cultivars can be unequivocally differentiated, but identical profiles were observed for three cultivar pairs, 'Katie's Blush' and 'Silvan Red', 'Highlights' and 'Maui Sunset', and 'Yellow Crest' and 'Yellow Devil'. CONCLUSIONS: ISSR profiling is a powerful method for the identification and molecular classification of Leucadendron cultivars. A fingerprinting key was generated based on the banding patterns produced using two ISSR primers (UBC856 and UBC857). In addition cultivar-specific ISSR bands were obtained for 17 of the 30 Leucadendron cultivars tested.     

Multivariate morphometric and allozymic analysis of theConospermum taxifolium (Proteaceae) species complex

A morphometric analysis of 18 attributes of 110 plants of theConospermum taxifolium complex suggests that it consists of three polythetically distinct taxa, corresponding to the traditional concepts ofC. taxifolium Smith s. str.,C. ericifolium Smith andC. ellipticum Smith. Discrimination is possible on the basis of leaf but not flower attributes. Analysis of allozymic variation indicates that the taxa are also genotypically differentiated.C. ericifolium andC. ellipticum are geographically isolated from each other but not fromC. taxifolium, andC. taxifolium is usually ecologically segregated from the other two taxa. Where this ecological segregation breaks down, morphological intermediates sometimes occur as the result of hybridization.     

A multivariate analysis of geographic variation in morphology inPersoonia mollis (Proteaceae)

This study highlights the utility and limitations of multivariate procedures for the analysis and taxonomic interpretation of geographic variation within a complex species. Morphological data from herbarium specimens ofPersoonia mollis (Proteceae) were analyzed by two ordination procedures, multidimensional scaling (MDS) and canonical variate analysis (CVA). Support for the earlier recognition of nine infraspecific taxa was found. However, plots of canonical variate scores against latitute or longitude across parapatric subspecies boundaries revealed unexpected phenetic homogeneity within subspecies with sharp transitions between subspecies. The geographic variation in morphology withinP. mollis can be best described as a mosaic of nine recognisably distinct and internally homogeneous allopatric or parapatric taxa, where neighbouring taxa share surprisingly narrow zones of morphological transition at ecotones. The utility of these procedures was highlighted by the recovery of unexpected patterns of variation. However, questions of rank remain unresolved by phenetic analysis alone.     

Pollination disruption by European honeybees in the Australian bird-pollinated shrubGrevillea barklyana (Proteaceae)

European honeybees (Apis mellifera) were less efficient pollinators ofGrevillea barklyana than nectar-feeding birds. Nectar-collecting honeybees did not contact reproductive parts of flowers. Pollen-collecting honeybees preferentially visited malestage flowers but rarely visited female-stage flowers. Fruit set on caged inflorescences that allowed access to honeybees but excluded birds was reduced by more than 50% compared to inflorescences that were visited by both types of visitors. Further, fruit set on caged inflorescences was less than on bagged inflorescences that excluded both birds and honeybees, indicating that pollen removal by bees decreased opportunities for delayed autonomous selfing in the absence of birds. Although fruit set was not pollen-limited at the study site, pollen removal by honeybees would decrease fruit set in small populations where birds are scarce. In addition, pollen removal by honeybees would reduce opportunities for outcrossing and reproductive success through male function. Although honeybees have been in Australia for insufficient time to have exerted selection on floral traits, evolutionary shifts in response to these animals are likely to occur in the future.     

Aspects of the reproductive ecology of four australian Hakea species (Proteaceae) in South Africa

Summary Four shrub species of the Australian Proteaceae (Hakea sericea, H. gibbosa, H. suaveolens and H. salicifolia) were introduced to South African fynbos shrublands between 1840 and 1860. H. sericea is highly invasive, H. gibbosa and H. suaveolens are moderately invasive and H. salicifolia is not invasive. The allocation of reproductive energy, germinability, the ability to survive fires and to germinate in burnt and unburnt areas, and the nutrient content of seeds were assessed for the four species. The information was used to investigate whether the success of H. sericea relative to the other three species could be explained by the superior expression of any trait. The most important trait which separates H. sericea from the other species is its ability to produce a large seed bank in its adopted environment in the absence of seed predators. Seed production in H. sericea shrubs with an above-ground dry mass of 8 kg is four times greater than H. gibbosa and more than 16 times that of H. suaveolens. Although H. salicifolia also produces a large seed bank, its seeds are unable to survive fires due to inadequate insulation by the small follicles. The results are compared to dispersal and seed bank data for indigenous South African Proteaceae, which have low dispersal and suffer high pre-dispersal seed predation. We suggest that potential invasives in the fynbos can be identified as species that have: (i) a potentially high seed production that is limited by specialized predators; (ii) an ability to disperse over long distances; and (iii) are pre-adapted to frequent fires and low soil nutrients. The data also support the current strategy of combatting H. sericea using specialized insect seed predators.     

A new species of Combretum section Ciliatipetala (Combretaceae) from southern Africa, with a key to the regional members of the section

Combretum stylesii O.Maurin, Jordaan & A.E.van Wyk, a liana or slender tree with scrambling branches from the Tugela River Valley (KwaZulu-Natal), South Africa, is described. Molecular data supports its placement in subgenus Combretum section Ciliatipetala with its closest relative Combretum edwardsii. The new species differs from C. edwardsii in having, amongst others, a single mature leaf form, leaves softly textured, with whitish hairs, often with drooping habit, shorter leaf petioles (less than 5 mm), and less complex 8-celled leaf scales. A key to the species and infraspecific taxa of section Ciliatipetala in the Flora of southern Africa region is provided.     

Causes of secondary sexual differences in plants — Evidence from extreme leaf dimorphism in Leucadendron (Proteaceae)

In extreme cases leaves in male plants of the dioecious genus Leucadendron (Proteaceae) are up to an order of magnitude smaller than female leaves. This secondary sexual dimorphism (SSD) in leaf size has previously been suggested to be due to intra-male sexual selection, leading to an increase in male allocation to reproduction in dimorphic species. After critically evaluating previous data provided to support this hypothesis, I suggest on both theoretical grounds and on re-analysis that this argument is unlikely and unsupported. Leaf size dimorphism could theoretically evolve directly due to disruptive ecological selection between genders, leading to niche dimorphism either within or between habitats. I test this ecological causation hypothesis by providing data on specific leaf area (sla) and water use efficiency (δ ¹³C) of leaves from males and females of several Leucadendron species. Results confirm the expectation of minimal gender differences. I argue that leaf dimorphism is a consequence of selection on flower size and architecture.     

Reproductive biology, variability of nectar features and pollination of Combretum fruticosum (Combretaceae) in Argentina

Flower morphology, nectary structure, nectar features (chemical composition, secretion pattern, standing crop, removal effects) and flower visitors are analysed in an Argentinian population of Combretum fruticosum. The variability of these data was examined throughout the flower lifetime. Nectar is hexose dominant. Its chemical composition and concentration are constant for all flowering stageS. Nectar volume varies as a function of flower age due to a combination of nectar secretion, cessation and resorption periods. The overall sugar production is decreased by nectar removal. The plant is self-incompatible and xenogamouS. Only 16.2% of the flowers set seedS. Inflorescences with green flowers were exclusively visited by two hummingbird and three perching bird species which transfer the pollen. A clear link was observed among nectar production pattern, standing crop of nectar, and visitors' behaviour.     

Differences in caste dimorphism among three hornet species (Hymenoptera: Vespidae): forewing size, shape and allometry

Caste shape dimorphism (CShD) has previously been studied in wasps through comparison of different body parts, originating from different imaginal discs. Using geometric morphometrics with a new protocol for measuring wings of pinned specimens from natural history collections, we tested CShD of three hornet species in an organ developed from a single imaginal disc: the forewing. Gaussian mixture models retrieved most castes and species levels, confirming that caste is an important component of wing variations in females of these hornets. Size and allometry - the influence of size on shape - contribution to wing dimorphism between castes was major, but failed to explain the entire shape dimorphism. This deviation from simple allometric scaling was not similar in the three species: in Vespa tropica, allometric directions in the shape space differed between castes, whereas in V. crabro and V. velutina, they were similar but a significant part of CShD resulted from lateral transpositions. These results clearly indicate that queens are not just enlarged workers. They also support that the different patterns of CShD may result from different developmental mechanisms. Finally, they highlight that even in a highly social group like hornets, there is still variation in caste dimorphism among species.     

Differences in pollinator effectiveness of birds and insects visiting Banksia menziesii (Proteaceae)

Summary The effectiveness of nectarivorous birds, introduced honey bees and staphylined beetles as pollinators of Banksia menziesii was assessed. Staphylinids removed substantial amounts of pollen but did not deposit any onto stigmata. Abundance of beetles on inflorescences was related to the mean number of florets opening per day. Honey bees collecting pollen were more likely to effect pollination than those collecting nectar which only contacted stigmata when arriving or leaving an inflorescence. Nectar-foraging birds probed between florets 10.2±0.8 (±SE) times, contacting 8–16 stigmata during each probe. Bees visited inflorescences ten times more frequently than birds although they deposited only 25% of the pollen that birds did on stigmata. Fruit set was ten times greater on inflorescences visited by birds than on inflorescences visited by bees. Bees were capable of removing as much pollen as birds but, because of direct pollen transfer to birds when florets opened during foraging, actual removal was probably much less. Selection for floret opening during nectar foraging by birds may have resulted from pollen removal by non-pollinating animals, such as staphylinids.     

Dynamic expansion in recently introduced populations of fire ant parasitoids (Diptera: Phoridae)

Combating invasive species requires a detailed, mechanistic understanding of the manner and speed with which organisms expand their ranges. Biological control efforts provide an opportunity to study the process of species invasions and range expansions under known initial conditions. This study examines the rate, pattern and mechanisms of spread for two populations of the biological control agent Pseudacteon tricuspis, phorid-fly parasitoids of imported fire ants. We employ a trap-based survey method that detects phorid flies in low-density populations, and provides data on abundance. This technique allows us to differentiate between continuous population spread and effective long-distance dispersal and to examine density gradients of phorid flies across the expanding population front. We find that occupied sites in front of the leading edge of continuous populations were common; forming small populations we refer to as satellite populations. Satellite populations are tens of kilometers from the nearest possible source. Wind governs the dynamics of spread in these two central Texas populations. Population edges expanding with the wind exhibited a higher frequency of effective long-distance dispersal than did populations expanding into the wind. This enhanced effective long-distance dispersal rate translated into a five times faster rate of spread for population edges traveling with the wind. This planned invasion shares many characteristics in common with unplanned species invasions including: protracted establishment phase during which densities were below detection thresholds, and slow initial spread immediately after establishment followed by rapid, accelerating spread rates as population sizes grew.     

The cost of myrmecophytism: insights from allometry of stem secondary growth

Background and Aims

Plant defence traits against herbivores incur production costs that are usually difficult to measure. However, estimating these costs is a prerequisite for characterizing the plant defence strategy as a whole. Myrmecophytes are plants that provide symbiotic ants with specialized nesting cavities, called domatia, in exchange for protection against herbivores. In the particular case of stem domatia, production of extra wood seems to be the only associated cost, making this indirect defence trait a particularly suitable model for estimating the cost of defence.

Methods

Measurements were made of growth pattern and cumulative production cost of domatia over secondary growth in the myrmecophyte Leonardoxa africana subsp. africana, whose internodes display both a solid basal segment and a hollow distal part (the domatium), thus allowing paired comparison of investment in wood.

Key Results

Previous studies showed that ‘overconstruction’ of the hollow part of internodes during primary growth is needed for mechanical support. In this study, it is shown that the relationship between the woody cross-sectional area of the solid and hollow parts of internodes is negatively allometric at the beginning of secondary growth and nearly isometric later on. Thus, in hollow stems, the first phase of slow secondary growth compensates for the ‘overconstruction’ of the ring of wood during primary growth. Moreover, the cumulative production cost of a domatium (estimated as the additional volume of wood required for a hollow stem compared with a solid one) is very high at the beginning of secondary growth and then quickly tends to zero.

Conclusions

Making domatia incurs high costs early in ontogeny, costs that are then amortized later in development of stems and of individual plants. Characterizing ontogenetic variation of the net cost of this peculiar defence mechanism will help us build more accurate theoretical models of resource allocation in myrmecophytes.     

The seed dimorphism of Spergularia marina in relation to dispersal by wind and water

Summary The seeds of the halophyte Spergularia marina differ both within and between individuals in that they either possess or lack a membranaceous border. This paper presents a morphological study of the length, weight and area of the seed types, and their dispersal characteristics under experimental conditions of wind and water dispersal. The winged seeds are shown to be larger both by length and by weight. Their rate of descent increases with wing loading. If the wing is lacking, however, the rate of descent increases with weight only. The distance of dispersal is equal for both seed types except at low wind speeds, when the winged seeds disperse farther. If the seed wing is removed, the excised seeds have shorter dispersal distances. When dispersed by water, a difference in the distance seeds are dispersed can only be detected in the presence of vegetation. The winged seeds are more frequently trapped in the vegetation as compared to the unwinged seeds. The hypothesis that the seed dimorphism is an adaptation for differential dispersal distances is discussed.     

Syringeal anatomy and allometry in murres (Alcidae: Uria)

Species and sexual differences in vocalizations and the vocal tract are widespread. We studied the vocal tract of Common (Uria aalge) and Thick-billed (U. lomvia) Murres. We predicted anatomical or allometric differences in adults between species and sexes due to vocal differences related to social behavior (Common Murres nest at higher densities; males are the more aggressive sex, etc.). The vocal tract was anatomically simple and similar between species and sexes. The trachea was mainly cartilage, but the posteriormost 4–6 tracheal rings were calcified and fused as the tympanum, as part of the syrinx. The syrinx included the (unfused) first bronchial semirings, which were enlarged and calcified beneath the insertion of M. tracheolateralis. Weak bilateral asymmetry (right side larger) occurred in widths of M. tracheolateralis and M. sternotrachealis. The trachea was ∼10% longer in Common Murres; the tympanum and M. sternotrachealis width were relatively larger in Thick-billed Murres. Vocal-tract morphology and size did not differ between the sexes in either species. In allometric analyses on adults, isometry characterized (1) tympanum size in relation to head + bill length, and to humerus length (respectively), in Thick-billed Murres, and (2) M. sternotrachealis width in relation to tarsometatarsal length in both species. Comparative field studies on species and sexes are needed to clarify the functional significance of our findings in relation to vocalization.     

The derivation, utility and implications of a divergence index for the fynbos genus Leucadendron (Proteaceae)

The derivation, utility, and implications of a divergence index for the fynbos genus Leucadendron (Proteaceae). The genus Leucadendron is useful for a phylogenetic study because it contains many species (79), is morphologically very diverse and appears to have diverged early on in the history of the family in Africa. Polarity of many characters was determined by outgroup analysis and the ontogenetic method. Exceptionally high levels of convergence made the determination of the phylogeny of the subsections problematic. An index, which is the sum of weight of all derived characters present in a species, was determined.
The genus should be removed from subfamily Aulacinae and placed closer to the Leucospermum 'alliance'. I suggest an arid temperate, shrub-like origin for the African Proteaceae, which is in contrast to some published viewS. Modifications to accepted concepts of fruit homology and evolutionary trends such as pollination and dispersal are presented for the family. The divergence index, if used as a 'morphological clock', appears to be useful for further biogeographic and ecological analyses.