Jeremy J. Midgley

Premise: Flowers that present their anthers and stigma in close proximity can achieve precise animal‐mediated pollen transfer, but risk self‐pollination. One evolutionary solution is reciprocal herkogamy. Reciprocity of anther and style positions among different plants (i.e., a genetic dimorphism) is common in distylous plants, but very rare in enantiostylous plants. We investigated the pollination and reproductive system of the enantiostylous Caribbean plant Cubanicula xanthorrhizos (Haemodoraceae). Methods: We assessed stylar orientation of flowers and conducted controlled pollination experiments. We used videography of flower visitors and pollen load analysis to determine the pollination mechanism. We also measured floral morphology, pollen production, spectral reflectance, and volatile emissions. Results: Cubanicula xanthorrhizos exhibits dimorphic enantiostyly with c. 50:50 left‐ to right‐styled morphs. Plants are self‐compatible, but pollinator dependent for seed production. Intra‐ and intermorph crosses are equally fertile. The nectarless flowers are pollinated by female carpenter bees ( Xylocopa cubaecola ) that collect pollen, often by sonication, from two centrally positioned yellow feeding anthers. An inconspicuous deflected pollinating anther deposits pollen on the side of the bee thorax, which contacts the stigma of the mirror‐image morph. A yellow‐orange “guide” on the white tepals appears to be a visual attractant. Flowers emit methoxy benzenoid volatiles that may also attract bees. Conclusions: Reciprocity of the style with a single pollinating stamen in C. xanthorrhizos appears to promote intermorph pollen export via “safe sites” on pollen‐collecting bees. This novel case of dimorphic enantiostyly contributes to understanding of the evolution of floral polymorphisms.

The frequency, size and position of the mistletoe Tapinanthus oleifolius in its dominant host's canopy were strongly correlated with the degree of exposure to herbivory by the kudu (Tragelaphus strepsiceros) and especially the giraffe (Giraffa camelopardalis). Mistletoes exposed to herbivory are less frequent and smaller compared to those deeper within the host canopy, on steeper slopes and especially where herbivores are few or absent. Where exposed to herbivores, T. oleifolius was almost entirely restricted to the spinescent host Senegalia mellifera, whereas in herbivore‐free areas, other tree species became hosts. The mistletoe Viscum rotundifolium was totally absent in areas with large herbivores. In herbivore‐free areas, it was frequently found on Ehretia alba and Boscia albitrunca, both non‐spinescent hosts. Mistletoes are thus excellent indicators of the extent of herbivory; their local absence probably indicates excessive herbivory, and a high presence indicates an absence of herbivory.

Societal Impact Statement: Seed dispersal is critical for the establishment and persistence of populations of most plant species. We investigated the seed dispersal biology of an African melon, Cucumis humifructus , which is closely related to cultivated cucumbers and watermelons but differs in that it buries its fruits deep underground. The fruits are located by antbears using olfaction; the antbears consume the fruit pulp and the seeds germinate in their faeces. Cucumis humifructus has become very rare in some parts of Africa and is vulnerable on account of its annual lifecycle combined with its dependence on a declining mammal species for establishing each new generation. Summary: Seed dispersal mutualisms between plants and animals are seldom specialized at the species level. We investigated the highly unusual case of the dispersal of seeds of a melon Cucumis humifructus by the antbear ( Orycteropus afer ), a myrmecophagous African mammal. This annual plant buries its fruits c. 20 cm underground, a depth from which seedling emergence is impossible. We asked why the fruits are buried and how they are located by animals. We investigated the seed dispersal system of C. humifructus in central Namibia using camera traps, seed germination experiments and analyses of animal faeces. Coupled gas chromatography and mass spectrometry (GCMS) was used to analyse the chemistry of fruit scent. Naturally‐buried C. humifructus fruits were excavated solely by antbears. Antbear faecal pellets often contained intact C. humifructus seeds. All of the C. humifructus plants that we examined originated in antbear pellets. Fruits placed experimentally above ground or buried shallowly were eaten by porcupines which act as seed predators as they destroy soft melon seeds with their chewing teeth. Fruits of C. humifructus emit scent with a chemical profile distinct from that of related melon species. We argue that deep burial of fruits is a strategy that C. humifructus uses to escape from mammalian seed predators, particularly porcupines. This study highlights the potential role of escape from antagonistic interactions in the evolution of specialized seed dispersal mutualisms.

Invasive species are major drivers of global ecosystem change. They often displace native species through competitive exclusion, creating novel species interactions. These interactions can lead to ecological cascades, where the presence of one invasive species enhances the fitness of another. Despite this, the mechanisms that underpin these mutualistic interactions and promote secondary invasions remain poorly understood. We assessed how the introduction of the invasive Argentine ant (Linepithema humile) alters mutualistic interactions within the recipient community, enhancing the dispersal and fitness of species of a secondary invasive plant genus (Acacia spp.). Our study examines these interactions at the community, individual species, and trait levels for a range of native and non‐native ant and plant species. Specifically, we aimed to investigate the direct and indirect effects of L. humile on seed dispersal mutualisms. We found that in L. humile invaded locations, seeds of the invasive Acacia plant species were approximately three times more likely to be dispersed than seeds of native endemic plant species. This preference is driven by indirect changes in the community structure of native seed‐dispersing ants, rather than direct interactions between the invasive ant and plant species. Moreover, we found that native ant species that co‐exist with L. humile, such as Tetramorium sericeiventre, respond to a narrower range of seed traits—traits which the invasive Acacia seeds possess. Our findings suggest that the invasion of L. humile has cascading effects on ant‐plant mutualisms, potentially increasing community permeability to secondary invasions. These results highlight that the impact of invaders like the Argentine ant may be greater than initially perceived, driving losses in both biological and functional plant diversity. Read the free Plain Language Summary for this article on the Journal blog.

Background: Spatial clumping of plants results in intense competition. Aims: We analysed the extent of clumping of Proteaceae seedlings across the Cape Floristic Region after fire. Methods: To demonstrate the extent of clumping in 23 species, we analysed the seedling and adult densities in 290 post-fire surveys each of 100 × 1 m2 plots using standard indices of clumping. Key results: We detected clumping of Cape Proteaceae seedlings, whereas parent plants were less clumped. The clumping is not due to limited safe sites for seedlings because the number of plots at a site with at least one seedling was positively related to the number of seedlings at the site. Sites with seedlings were enriched in nutrients relative to those without. Conclusions: The possible benefits of clumping are saturation of granivores and co-location of buried seeds with nutrient-rich patches of fire-derived ash and debris. A cause of clumping is seeds sticking together. Clumping, which is strongly intraspecific, has implications for trait evolution and the dominance of reseeders over resprouters. Strong clumping reduces the usefulness of the widely used seedling:parent index to determine whether fires were favourable or not. Implications: Clumping has implications for understanding seed dispersal distances, seedling versus adult traits, fire responses and demography.

We analysed nearly 31 years (1991–2022) of tree population dynamics in 108 permanent plots each 0.04 ha of the Lilyvlei Nature Reserve, a section of the Knysna Forest in South Africa which has not historically been disturbed by harvesting. The Knysna Forest is the only large piece of forest in South Africa and is marginal for tall forest, having low mean annual rainfall of only about 1000 mm and occurs on nutrient poor soils. In contrast to many studies of other forests globally, we found almost no change in overall biomass. Even at the scale of our small plots and on 10–30 year time scales, there has been little change. The forest has very low recruitment and mortality rates and thus low growth rates. Climatic changes too were minimal over this 30‐year period. The proportion of stems that died per size class was concentrated in the larger size‐classes per species, even for shorter species. This suggests that senescence rather than external disturbances determines the low mortality and thus the low dynamism and the high biomass (approx. 600 Mg ha ⁻¹ AGB or 41 m ² ha ⁻¹ basal area) of the forest. Mortality of some species exceeded conspecific recruitment, a trend accompanied by non‐significant declines in biomass. However, these trends are not significant. In conclusion, neither composition nor biomass has changed significantly in these forests over a period of 30 years. This suggests that not all Southern Hemisphere forests are in a state of decline.

Pollen transfer efficiency (PTE; the proportion of pollen removed from flowers that reaches conspecific stigmas) is expected to vary with the type of pollinator and flower morphology, and to influence male siring success. Many species in the genus Erica are pollinated by bees (which consume pollen and should thus lower PTE) but during its radiation in the Cape, several independent shifts to both sunbird and long-proboscid fly (LP fly) pollinators, which do not consume pollen have taken place. Improvements in PTE could be one of the factors driving these pollinator shifts. PTE data for 15 Erica species (five for each of the three pollinator types) were collected and compared in relation to type of pollinator and anther exsertion. LP fly- and bird-pollinated species had higher PTE in comparison with bee-pollinated species. Species with inserted anthers had higher PTE than those with exserted anthers. This suggests that sunbirds and LP flies are more efficient pollinators than bees. Additionally, the study suggests that insertion of anthers within the corolla tube can reduce pollen losses.

Carnivorous mammals have been reported to feed on fleshy fruits and disperse seeds, but these interactions are seldom observed and are poorly understood in hyper‐arid regions. Scent may play a key role in these interactions, given that most carnivores have sensitive olfactory systems and dichromatic vision. The !nara (Acanthosicyos horridus: Cucurbitaceae) in the Namib Desert produces large (10–20 cm diameter) melons that remain green while undergoing increased volatile emissions with a changing chemical profile as they ripen. Using extensive camera trapping, we found that the fruits are consumed mainly by black‐backed jackals (Canis mesomelas) and rarely also by other carnivores such as cape fox (Vulpes chama) and brown hyaena (Hyaena brunnea). We found that scent cues play a crucial role as jackals mainly sought fruits at night and easily located ripe fruits that were experimentally buried beneath the sand to remove visual cues. Seeds retrieved from jackal scat showed improved germination relative to un‐ingested seeds. This study highlights the importance of fruit scent in mediating seed dispersal mutualisms involving carnivores.

Mistletoes have much higher transpiration rates than their hosts. This is the basis for the ecological “compatibility hypothesis” for host choice. The inability of mistletoes to penetrate a host and connect to its vascular system is the competing “immunity hypothesis”. Epi‐parasites would have to transpire faster than their host mistletoe, which must transpire faster than its host. Therefore, epi‐parasites should be able to parasitise their host's host. I surveyed epi‐parasite host choice at a site and found this did not happen. Globally about a quarter of all epi‐parasites are obligate. This supports the immunity hypothesis.