Aloe pollination: floral visitors, reproductive output and gender expression
Payne, Stephanie L.
Suites of plant floral traits, such as floral colour and shape, nectar properties, scent, and timing of anthesis are important attractants and/or rewards for visitors, to ensure successful pollination events. This has resulted in a wide range of floral diversity within the angiosperms, and floral traits are often used to predict the most effective pollinators of a plant. The genus Aloe comprises of > 500 species, with the greatest concentration and diversity of species found in southern Africa. Twelve different growth forms across ~140 taxa are recognised in South Africa alone, with a wide variety of floral traits. These traits suggest specialist nectarivorous bird (e.g. sunbirds (Nectariniidae) and sugarbirds (Promeropidae), generalist (opportunistic) nectar-feeding birds (e.g. weavers (Ploceidae), thrushes (Muscicapidae), white-eyes (Zosteropidae), etc.), or insect (e.g. halictid, allodapine and honeybees) pollination. Floral colour, nectar, and pollen rewards are the most important attractants for these visitors (both predicted and unexpected), and nearly all aloes are self incompatible and reliant on pollen vectors for successful pollen transfer. This thesis investigated the role of Aloe floral traits in the attraction of multiple visitor/pollinator guilds, and the consequent effect on plant reproductive output, using three South African endemic Aloe species as model species. Aloe peglerae is a Critically Endangered, stemless aloe, which flowers during winter (June – July). Floral characteristics suggest bird pollination (red flowers that produce large amounts of nectar), although small mammals were reported as occasional nocturnal visitors to the aloes. To compare the role of diurnal bird visitors and nocturnal small mammal visitors in the pollination, and subsequent reproductive output of A. peglerae, day/night exclusion experiments were conducted during the 2013 flowering season. These experiments confirm that generalist nectar-feeding birds, especially the Cape Rock-Thrush (Monticola rupestris; 80% of all diurnal visits), are the primary pollinators of A. peglerae. Small, non-flying mammals, primarily the Namaqua Rock Mouse (Micaelamys namaquensis), successfully pollinate the aloe at night (70% of nocturnal visits), despite not being predicted by floral traits. This is the first quantification of small mammal pollination in Aloe. Over two flowering seasons with different flowering success rates (2013: a “good” flowering year, and 2014: a “poor” flowering year), day/night exclusion experiments were conducted to assess the effect of annual fluctuations in flowering success on the pollinator visitation and subsequent plant reproductive output. Small mammals are suitable, alternative pollinators, especially in years when flowering success is low. Mobile birds are able to move to more energetically viable food resources, while mice are forced to rely on their immediate surroundings. In a poorer flowering year, Aloe peglerae reproductive output was lower in bird-pollinated plants (fruit set: 2013: 23.3 ± 4.9%; 2014: 0%; mean ± S.E.), while reproductive output by small mammal pollinated plants was similar between years (2013: 8.9 ± 2.7%; 2014:4.9 ± 4.0%). This emphasizes the effectiveness of small mammals as pollinators in flowering years with low primary pollinator (bird) abundance. The production of A. peglerae nectar over a 24-hour period was measured, to assess the effect of constant nectar production on the temporal partitioning of pollinator visitation and resource use. Aloe peglerae nectar is produced continuously over 24-hours, with peaks in bird and small mammal visitation tracking periods of peak nectar production. Diurnal birds and nocturnal small mammals partition this nectar resource temporally, with overlaps in visitation at dusk and dawn. The increased nectar production during the day attracts birds, but residual and freshly secreted (albeit reduced) nectar attracts small mammals at night, ensuring pollination events throughout the flowering period of the aloes. Aloe reitzii var. reitzii flowers in summer (February – March), and flowers produce nectar throughout the day, with properties (volume and concentration) that range across both specialist- and generalist nectarivorous bird preferences. The contributions, and temporal partitioning, of both specialist- and generalist nectar feeding birds to the visitation to this aloe were investigated. Both these bird guilds regularly visit the aloes, with specialist visitation dominated by the Malachite Sunbird (Nectarinia famosa; 49% of all visits), and generalist visitation dominated by the Cape Weaver (Ploceus capensis; 41% of all visits). This may be indicative of pollinator specialisation by one generalist and one specialist nectarivore in A. reitzii var. reitzii. Visitation by these birds is temporally separated, likely due to territoriality and competition for nectar resources. Cape Weaver visitation peaks early in the morning, while Malachite Sunbirds are dominant from the late morning, and are more consistent for the rest of the day. Hawkmoths visit the aloes at night, and honeybees are regular visitors during day. Insects likely play an important role in the pollination of these aloes, as with many summer-flowering aloes. Aloe petricola is a winter flowering (July – August) aloe, with three different floral colour morphs co-existing in different proportions within the same populations (orange buds, yellow flowers (55% of sampled population); red buds, white flowers (22%); and red buds, yellow flowers (22%)). The potential influence of pollinator-mediated selection for floral colour (flower constancy) by birds, on the proportions of different floral morphs within a sub population of A. petricola, along with the resulting reproductive output of each color morph was assessed. Plant morphometrics (leaf rosette diameter and height, number of racemes, and raceme length) and nectar volume and concentration do not differ among morphs. Generalist nectar-feeding birds (six species recorded), especially the Dark-capped Bulbul (Pycnonotus tricolor; 43.2% of visits), regularly visited the aloes, with the White-bellied Sunbird (Cinnyris talatala; 10.2% of visits) making up most of the specialist nectarivore visits (four species recorded). Honeybees and butterflies were observed visiting the plants. Flower colour does not appear to confer a reproductive advantage, as bird visitors do not preferentially select among morphs and reproductive output was similar among the three morphs (fruit set/plant: orange-yellow: 21.9 ± 4.1%; red-white: 16.9 ± 2.3%, and red-yellow: 21.4 ± 5.4%) Visitors are likely foraging at any available food resources in the resource-limited winter. Interactions and functional trade-offs between biotic (pollinators, floral pigments) and abiotic factors (spatial and temporal environmental variation, resource availability and use), rather than pollinator-mediated selection and flower constancy, may be driving and maintaining polymorphism, and optimising plant fitness in this Aloe species. Despite the roles these floral characteristics play in attracting visitors and pollinators, 60% of published Aloe studies report fruit set (proportion of flowers that set fruit) of < 30%, with some plants producing no fruit at all. A review of published Aloe studies was conducted, where reports of pollinator visitation, surplus flower production and low fruit set were reviewed, and the theory of gender expression discussed in the context of Aloe. Many aloe species appear to produce surplus flowers that do not develop into fruit, likely as a result of the limited resources available, as these plants often grow in dry, resource-limited soils/environments. Fruit and seed maturation (female function) is resource-intensive, and so plants may allocate the limited resources to the “cheaper” male function of producing pollen. Therefore, these plants may be “functionally male”, with surplus flowers performing multiple functions, apart from fruit production. They may serve as additional pollinator attractants, by making inflorescences larger and more conspicuous (which is important during pollinator limitation), or providing additional nectar and pollen rewards. Surplus flowers may also compensate for flowers that are lost due to transfer of self-pollen (self-incompatibility reaction), and florivory. Structural limitations may cause low fruit set, as the infructescence cannot physically accommodate each flower as a fruit capsule; reported “low” fruit set may be the physical maximum that a plant can achieve. It appears that a trade-off between male and female function is made to optimise overall plant fitness. A broad scope for experimentation exists, as specific studies are required to define the role of surplus flowers in Aloe. Plant-pollinator interactions in Aloe are complex, and are further confounded by other factors, such as resource limitation, and climate variability. Long term studies on the variability in flowering and fruiting, as a result of resource availability, use, and storage, may prove invaluable in understanding these interactions. Further studies should avoid treating extrinsic (pollinators and resource availability) and intrinsic factors (plant size, gender expression) as mutually exclusive, but rather take the interactions into consideration. Resources are allocated to the production of pollinator attractants, and visitors of multiple guilds (specialist and generalist birds, small mammals, and insects) play a vital role in the pollination of aloes. Aloes are also important food resources for these visitors, especially in resource-limited winter months. Visitors do not appear to preferentially select plants based on specific colours or nectar properties, but rather feed at any available resource. Within each guild, there appears to be a dominant species which may be acting as the “specialist” pollinator for specific Aloe species. However, the efforts of these pollinators may be futile if remaining resources are not sufficient for fruit and seed maturation. If resources for female function are limiting, then the production of surplus flowers still ensures gene transfer. Inadequate resource supply, storage, and allocation may jeopardise the overall fitness of the plant and, ultimately, the species, many of which are sensitive to habitat transformation and land degradation.
A Thesis submitted to the Faculty of Science University of the Witwatersrand, Johannesburg, South Africa in fulfilment of the requirements for the degree Doctor of Philosophy, May 2019