SHORT COMMUNICATION

 

Notes on the flowering and pollination of the endemic grassland Aloe reitzii var. reitzii (Asphodelaceae)

 

 

Craig T. Symes

School of Animal, Plant & Environmental Sciences, University of the Witwatersrand, South Africa

Correspondence

 

 

---

ABSTRACT

BACKGROUND: Aloe reitzii var. reitzii is a succulent with a restricted distribution in the montane grassland of eastern South Africa. It is a summer (late January-March) flowering succulent that grows on rocky outcrops at 1000 m-1600 m, and the conspicuous inflorescences suggest a pollination system focused towards birds.
OBJECTIVES: To understand more about the pollination biology of A. reitzii var. reitzii.
METHODS: Nectar standing crop (flower volume and concentration) and the proportion of plants flowering were recorded. Camera traps and observations were used to record visitors to A. reitzii var. reitzii inflorescences.
RESULTS: Nectar volume was 36 μL ± 27 μL per flower (range 6 μL-93 μL; n = 27) and concentration was 16.5% ± 1.7% (range 13.5% - 19.5%). Camera trap observations, where 18.9% of all plants were observed flowering, recorded the three bird species Cape Weaver, Ploceus capensis, Malachite Sunbird, Nectarinia famosa and Greater Double-collared Sunbird, Cinnyris afer (60.4%, 27.1% and 12.5% of plant visits, respectively) visiting inflorescences.
CONCLUSION: Because birds are important pollinators for many Aloe species, it is assumed that the bird species detected visiting A. reitzii var. reitzii are similarly important pollinators. At least 10 invertebrate species and sengi (Elephantulus sp.) were also recorded as visitors to flowers, but they may be less important pollinators than specialist and generalist avian nectarivores. This study provides further insight into the pollination biology of a diverse, and ecologically important, succulent genus in Africa.

---

 

 

Introduction

Pollination systems in the genus Aloe are diverse, with numerous recent studies identifying unique and often unexpected mutualisms (Arena, Symes & Witkowski 2013; Botes, Johnson & Cowling 2009a; Botes, Wragg & Johnson 2009b; Hargreaves, Harder & Johnson 2008; Johnson 2004). While the perception remains that many Aloe species are pollinated by birds, relatively few studies have quantified the contributions of different pollinator guilds. Furthermore, in cases where a specific pollinator guild (e.g. birds) is identified as the most important contributor to pollination, fewer studies have addressed the specific roles of each species in that guild.

Many Aloe species can potentially hybridise and given the diversity of the genus it is important to understand how the species integrity of co-occurring taxa is maintained. Botes, Johnson & Cowling (2008) proposed that the problem of Aloe species coexistence may be explained by a greater diversity of bird pollination systems in the genus than previously documented. In five co-occurring Aloe species that flower together during winter there was a partitioning of pollinators, with short-billed generalist nectar feeders pollinating species with large amounts of dilute nectar in short corolla tubes, and long-billed specialist nectar feeders, that is, sunbirds, pollinating species with small amounts of concentrated nectar in long corolla tubes (Botes et al. 2008).

Many species-specific studies have provided valuable data regarding the widely distributed Afrotropical genus Aloe, where the diversity of species, with respect to (1) nectar characteristics, including volume and concentration, (2) flowering season and duration, (3) inflorescence, raceme and flower arrangement, (4) floral morphology, including structure, colour and position, (5) distribution and habitat preferences and (6) population size, is important in determining plant-pollinator associations (Botes et al. 2008, 2009a, 2009b; Hargreaves, Johnson & Nol 2004; Hargreaves, Harder & Johnson 2012; Hoffman 1988; Johnson 2004; Pailler, Warren & Labat 2002; Ratsirarson 1995; Stokes & Yeaton 1995; Wilson et al. 2009). While species-specific predictions of pollinators can be made on the basis of pollination syndromes, it is clear that determination of pollinator assemblages requires thorough field study (Fenster et al. 2004; Geerts & Pauw 2009; Johnson & Steiner 2000). An important tool in this regard is the application of camera traps, which in recent years have provided important and detailed information on plant-pollinator interactions (Melidonis & Peter 2015; Steenhuisen et al. 2015; Zoeller et al. 2016).

Aloe reitzii Reynolds (1937) var. reitzii (Asphodelaceae) is a summer-flowering (late January-March) succulent with a restricted distribution in montane grassland around Belfast and Dullstroom, northeastern South Africa (Glen & Hardy 2000; Mucina & Rutherford 2006; Reynolds 1969; Van Wyk & Smith 2003) (Figure 1a and b). It grows on rocky areas, but is by no means confined to them (Glen & Hardy 2000; Reynolds 1969). It is known from 12 to 15 locations, with most populations confined to a small area (Raimondo et al. 2005). Plants reach a height of up to 1.0 m and produce multiple racemes that can reach 2.5 m in height (Glen & Hardy 2000; Reynolds 1969; Van Wyk & Smith 2003). The immature unopened flowers are dark red, becoming orange to pale yellow when mature (Van Wyk & Smith 2003), and are incurved and relatively long (32 mm-50 mm), suggesting pollination by birds (Figure 1a and b) (Glen & Hardy 2000; Reynolds 1969; Symes, Human & Nicolson 2009; Van Wyk & Smith 2003).

The objective of this study was to investigate potential pollinators of A. reitzii var. reitzii as inferred by visitation events captured by remote camera traps, as well as by field observations.

 

Materials and methods

Study site

Field work was conducted from 19 to 21 February 2014 at two localities near Dullstroom, approximately 4 km apart, and 10 km west of Verloren Vallei Nature Reserve: (1) Houtenbek farm (~1910 m-1950 m) and (2) Klipbankspruit farm (~1930 m-1945 m). Both localities are on privately owned farms and the A. reitzii var. reitzii sites on each are currently used for extensive beef farming (landowners, pers. comm.).

Nectar characteristics

Three mature flowers (Stage 2 flowers, see Symes & Nicolson 2008) were selected from each of nine plants (six plants at Site 1 and three plants at Site 2) and nectar standing crop volume (μL) and concentration (% w/w; hand-held refractometer, Bellingham & Stanley, Tunbridge Wells, UK) measured. Site 1 was sampled during the morning (08:15-09:30) and Site 2 during the early afternoon (13:05-13:25).

Flowering biology

A single meandering transect (~1.5 km), that avoided recounting the same individual, was walked through the areas where plants occurred at Site 1, and flowering recorded. The number of racemes was counted on 109 flowering plants.

Inflorescence visitors

Nine camera traps (Bushnell, model 119456, China) were set up on tripods (ht. ~1.5 m), at least 1 m distant from each plant, to record visitors to flowering plants. Cameras were set at high sensitivity to take three photographs when motion sensors were activated, with 3-s intervals between activations. Cameras were erected on the afternoon of 19 February and collected mid-morning on 21 February. A light rain fell on the night of 20 February. Any animal perched on the inflorescence, or photographed in flight close to the inflorescence, was defined as a flower visitor. If successive photographs captured what appeared to be the same individual, these were recorded as a single visit. Visits to plants ranged from an individual perched on a raceme and captured in only one photograph to an individual moving between racemes and photographed in successive images. While the presence of a visitor does not define its role as a pollinator, the records, together with observations at the site, do provide a basis from which to make interpretations regarding pollination of A. reitzii var. reitzii. Because different sized organisms may have different effects on the triggering mechanisms, and camera trapping is less likely to record all insects, no comparisons regarding visitation rates were made between birds and insects. For birds the proportion of visits by each species was calculated by dividing the total number of visits per species by the sum of all visits. For each plant, and for each hour during the day, the accumulative number of minutes (05:00-19:00) that cameras were set was determined. The number of visits for each plant was then used to calculate an hourly visitation rate (number of visits/plant/hour). To calculate visitation rates only daylight hours were considered although cameras were active during night hours. All values are given as mean ± SD.

 

Results

Nectar characteristics

Mean nectar standing crop volume was 36 μL ± 27 μL per flower (range 6 μL-93 μL; n = 27 flowers, nine plants) and concentration was 16.5% ± 1.7%. Nectar standing crop in the early afternoon (Site 2) was lower (volume 12 μL ± 4 μL, n = 9 flowers, three plants) compared with the morning (Site 1; volume 47 μL ± 26 μL), but concentration was no different.

Flowering biology

A total of 726 plants (only sampled at Site 1) were recorded for the presence or absence of flowering. In total, 18.9% of plants were recorded flowering. The number of racemes per plant ranged from 1 to 10 (median = 3; mean = 2.9 ± 1.2; n = 109) and measured 44 cm ± 3 cm in length (n = 6 mature racemes). On all plants there were open flowers.

Inflorescence visitors and behaviour

A total of 48 visits were made by three bird species during 155 hours of camera trap observations. Most visits were by Cape Weaver, Ploceus capensis (60.4%), with fewer visits by Malachite Sunbird, Nectarinia famosa (27.1%) and Greater Double-collared Sunbird, Cinnyris afer (12.5%) (Table 1). Cape Weaver and Malachite Sunbird visited eight and six of the nine monitored plants, respectively. Greater Double-collared Sunbird only visited a single plant, located near a bush-clump in a rocky outcrop. The earliest bird visitor was at 05:40 and the latest at 18:26. Plants were visited by birds during all hours of the day except mid-afternoon.

 

 

The mean hourly visitation rate was 0.36 ± 0.19 visits/plant/hour. Cape Weaver, Malachite Sunbird and Greater Double-collared Sunbird visitation rates were 0.22 ± 0.15, 0.11 ± 0.11 and 0.03 ± 0.10 visits/plant/hour, respectively. These species were all observed probing flowers for nectar, by either perching below (Figure 1c) or above (Figure 1e) the open flowers.

At least nine invertebrate species were observed and photographed on camera traps (Figure 1) and visited throughout the day from mid-morning to late-afternoon (Table 1). The only nocturnal visitors recorded were moths (Lepidoptera) during 19:00-20:59. Invertebrates were observed drinking nectar (e.g. Camponotus sp.) or removing pollen (e.g. Apis mellifera) while others were observed simply perched on flowers (e.g. Maura sp.) or inflorescence stems (e.g. Odontomutilla sp.) (Table 1).

 

Discussion

While this study considers visitation data from only three days of a flowering season, camera traps and field observations provided information on the most likely pollinators of A. reitzii var. reitzii. In the grassland environment in which A. reitzii var. reitzii occurs there are a limited number of grassland bird species (Hockey, Dean & Ryan 2005), including specialist (e.g. sunbirds) and generalist avian nectarivores. Only a few potential bird-pollinators that are likely to visit flowering plants occur within A. reitzii var. reitzii grassland habitat and those recorded for the period of study are not unexpected (Hockey et al. 2005), given that flower and inflorescence structure in A. reitzii var. reitzii strongly suggests pollination by birds. Furthermore, nectar characteristics suggest that A. reitzii var. reitzii is more likely to be pollinated by sunbirds. Generalist avian nectarivores are predicted to prefer flowering plants with dilute (8%-12% w/w) and large volumes (40 μL-100 μL) of nectar, while specialist passerine nectarivores (i.e. sunbirds) prefer nectar of higher concentration (15%-25% w/w) with lower volumes (10 μL-30 μL) (Johnson & Nicolson 2008). With values for A. reitzii var. reitzii at the lower end of the concentrations predicted for specialist nectarivores, and volumes extending into the range expected for generalist nectarivores, it is not surprising that the majority of floral visits were by Cape Weavers, which are generalist nectarivores and are adept at feeding on nectar (Craig 2014; Johnson & Nicolson 2008). Malachite Sunbirds were recorded on as many study plants as Cape Weavers, suggesting that these two species may both be important pollinators of A. reitzii var. reitzii. Malachite Sunbirds are ubiquitous throughout southern Africa and have been identified as primary pollinators of an entire guild of plant species - the 'Malachite Syndrome' (Geerts & Pauw 2009).

Many of the study plants received significant visitation from invertebrates. While it is possible that several of these were nectar robbers (Richardson 2004), honeybees were recorded in this study and have been shown as important pollinators of other Aloe species, (Botes et al. 2009a; Symes et al. 2009). They made up by far the greatest proportion of recorded insect visitors so, like in A. greatheadii var. davyana, they may be important pollinators when they occur in large numbers (Symes et al. 2009). Interestingly, observations of a wide variety of insects visiting study flowers contrasts findings in winter-flowering Aloe species which, unless they are visited by honeybees, are less likely to be visited by insects (Botes et al. 2009a; Hoffman 1988; Kuiper et al. 2015; Payne, Symes & Witkowski 2016; Symes et al. 2009).

Aloe peglerae, an endemic grassland Aloe of the Magaliesberg Mountain Range, is pollinated mainly by Cape Rock Thrush Monticola rupestris, a diurnal generalist nectarivore, with > 60% of pollination made by this species (Arena et al. 2013; Payne et al. 2016). However, pollination is also supplemented by nocturnal mammals such as Namaqua Rock Mouse Micaelamys namaquensis and Eastern Rock Sengi Elephantulus myurus (Payne et al. 2016). Anecdotal reports from the landowner at Site 2 suggest that sengi (Elephantulus sp.) have been observed visiting flowers during the day (B. Struwig, pers. comm.). However, no photographs were obtained of small mammals visiting flowers during this study. Thus, while visits by small mammals, such as sengi (Wester 2010), may be more common in rocky areas at our study sites, this mammal-plant association remains to be investigated.

 

Conclusion

In conclusion, A. reitzii var. reitzii is visited primarily by generalist and specialist avian nectarivores, as well as by invertebrates. Although the latter cannot be confirmed as legitimate pollinators, the fact that (1) birds and insects have been shown to be successful pollinators of numerous Aloe species and (2) fruit set at the site is abundant each year (landowners, pers. obs.) suggests that these organisms are important role players in the pollination of A. reitzii var. reitzii. A generalist pollination system might contribute to fitness of A. reitzii var. reitzii, a range-restricted, summer-flowering endemic occurring in fire-dominated grasslands; this remains to be investigated further. Furthermore, this study shows the usefulness of remote camera traps in testing predictive floral syndromes in the diverse genus Aloe.

 

Acknowledgements

Zephné Bernitz and Tracy Symes assisted in the field. Bernard O'Grady (Houtenbek farm) and Bertus Struwig (Klipbankspruit farm) are thanked for access to their properties. Marcus Byrne, James Harrison (University of the Witwatersrand) and Kevin Williams (Plant Pest Diagnostics Center, Sacramento) assisted with invertebrate identification. Two anonymous reviewers are thanked for their valuable input in improving this article for publication.

Competing interests

The author declares that there are no financial or personal relationships that may have inappropriately influenced the writing of this article.

 

References

Arena, G., Symes, C. & Witkowski, E., 2013, 'The birds and the seeds: Opportunistic avian nectarivores enhance reproduction in an endemic montane aloe', Plant Ecology 214, 35-47. https://doi.org/10.1007/s11258-012-0144-z        [ Links ]

Botes, C., Johnson, S.D. & Cowling, R.M., 2008, 'Coexistence of succulent tree aloes: Partitioning of bird pollinators by floral traits and flowering phenology', Oikos 117, 875-882. https://doi.org/10.1111/j.0030-1299.2008.16391.x        [ Links ]

Botes, C., Johnson, S.D. & Cowling, R.M., 2009a, 'The birds and the bees: Using selective exclusion to identify effective pollinators of African tree aloes', International Journal of Plant Sciences 170, 151-156. https://doi.org/10.1086/595291        [ Links ]

Botes, C., Wragg, P. & Johnson, S., 2009b, 'New evidence for bee-pollination systems in Aloe (Asphodelaceae: Aloideae), a predominantly bird-pollinated genus', South African Journal of Botany 75, 675-681. https://doi.org/10.1016/j.sajb.2009.07.010        [ Links ]

Craig, A.J.F.K., 2014, 'Nectar feeding by weavers (Ploceidae) and their role as pollinators', Ostrich 85, 25-30. https://doi.org/10.2989/00306525.2014.900828        [ Links ]

Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R. & Thomson, J.D., 2004, 'Pollination syndromes and floral specialization', Annual Review of Ecology, Evolution, and Systematics 35, 375-403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347        [ Links ]

Geerts, S. & Pauw, A., 2009, 'Hyper-specialization for long-billed bird pollination in a guild of South African plants: The Malachite Sunbird pollination syndrome', South African Journal of Botany 75, 699-706. https://doi.org/10.1016/j.sajb.2009.08.001        [ Links ]

Glen, H.F. & Hardy, D.S., 2000, 'Aloaceae (first part): Aloe', in G. Germishuizen (ed.), Flora of Southern Africa, vol. 5, pp. 1-167, National Botanical Institute, Pretoria.         [ Links ]

Hargreaves, A., Harder, L. & Johnson, S., 2008, 'Aloe inconspicua: The first record of an exclusively insect-pollinated aloe', South African Journal of Botany 74, 606-612. https://doi.org/10.1016/j.sajb.2008.02.009        [ Links ]

Hargreaves, A.L., Harder, L.D. & Johnson, S.D., 2012, 'Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees', Annals of Botany 109, 761-772. https://doi.org/10.1093/aob/mcr324        [ Links ]

Hargreaves, A.L., Johnson, S.D. & Nol, E., 2004, 'Do floral syndromes predict specialization in plant pollination systems? An experimental test in an "ornnithophilous" African Protea', Oecologia 140, 295-301. https://doi.org/10.1007/s00442-004-1495-5        [ Links ]

Hockey, P., Dean, W. & Ryan, P., 2005, Roberts - Birds of southern Africa, The Trustees of the John Voelcker Bird Book Fund, Cape Town.         [ Links ]

Hoffman, M.T., 1988, 'The pollination ecology of Aloe ferox Mill', South African Journal of Botany 54, 345-350. https://doi.org/10.1016/S0254-6299(16)31300-X        [ Links ]

Johnson, S. & Nicolson, S., 2008, 'Evolutionary associations between nectar properties and specificity in bird pollination systems', Biology Letters 4, 49-52. https://doi.org/10.1098/rsbl.2007.0496        [ Links ]

Johnson, S.D., 2004, 'An overview of plant-pollinator relationships in southern Africa', International Journal of Tropical Insect Science 24, 45-54. https://doi.org/10.1079/IJT20043        [ Links ]

Johnson, S.D. & Steiner, K.E., 2000, 'Generalization versus specialization in plant pollination systems', Trends in Ecology & Evolution 15, 140-143. https://doi.org/10.1016/S0169-5347(99)01811-X        [ Links ]

Kuiper, T.R., Smith, D.L., Wolmarans, M.H.L., Jones, S.S., Forbes, R.W., Hulley, P.E. et al., 2015, 'The importance of winter-flowering Aloe ferox for specialist and generalist nectar-feeding birds', Emu 115, 49-57. https://doi.org/10.1071/mu14054        [ Links ]

Melidonis, C.A. & Peter, C.I., 2015, 'Diurnal pollination, primarily by a single species of rodent, documented in Protea foliosa using modified camera traps', South African Journal of Botany 97, 9-15. https://doi.org/10.1016/j.sajb.2014.12.009        [ Links ]

Mucina, L. & Rutherford, M.C., 2006, The vegetation of South Africa, Lesotho and Swaziland, Strelitzia 19, South African National Biodiversity Institute, Pretoria.         [ Links ]

Pailler, T., Warren, B. & Labat, J.-N., 2002, 'Biologie de la reproduction de Aloe mayottensis (Liliaceae), une espèce endémique de l'île Mayotte (Océan Indien)', Canadian Journal of Botany 80, 340-348. https://doi.org/10.1139/b02-019        [ Links ]

Payne, S.L., Symes, C.T. & Witkowski, E.T.F., 2016, 'Of feathers and fur: Differential pollinator roles of birds and small mammals in the grassland succulent Aloe peglerae', Austral Ecology 41, 952-963. https://doi.org/10.1111/aec.12387        [ Links ]

Raimondo, D., Van Staden, L., Foden, W., Victor, J.E., Helme, N.A., Turner, R.C. et al., 2005, Red list of South African plants, Strelitzia 25, South African National Biodiversity Institute, Pretoria.         [ Links ]

Ratsirarson, J., 1995, 'Pollination ecology of Aloe divaricata, Berger (Liliaceae): An endemic plant species of south-west Madagascar', South Africa Journal of Botany 61, 249-252. https://doi.org/10.1016/S0254-6299(15)30531-7        [ Links ]

Reynolds, G.W., 1937, 'Two new aloes from Zululand and two from the Transvaal', Journal of South African Botany 3, 135-137.         [ Links ]

Reynolds, G.W., 1969, The aloes of South Africa, A A Balkema, Cape Town.         [ Links ]

Richardson, S.C., 2004, 'Are nectar-robbers mutualists or antagonists?', Oecologia 139, 246-254. https://doi.org/10.1007/s00442-004-1504-8        [ Links ]

Steenhuisen, S.-L., Balmer, A., Zoeller, K., Kuhn, N., Midgley, J., Hansen, D. et al., 2015, 'Carnivorous mammals feed on nectar of Protea species (Proteaceae) in South Africa and likely contribute to their pollination', African Journal of Ecology 53, 602-605. https://doi.org/10.1111/aje.12225        [ Links ]

Stokes, C.J. & Yeaton, R.I., 1995, 'Population dynamics, pollination ecology and the significance of plant height in Aloe candelabrum', African Journal of Ecology 33, 101-113. https://doi.org/10.1111/j.1365-2028.1995.tb00786.x        [ Links ]

Symes, C.T., Human, H. & Nicolson, S.W., 2009, 'Appearances can be deceiving: Pollination in two sympatric winter-flowering Aloe species', South African Journal of Botany 75, 668-674. https://doi.org/10.1016/j.sajb.2009.08.008        [ Links ]

Symes, C.T. & Nicolson, S.W., 2008, 'Production of copious dilute nectar in the bird-pollinated African succulent Aloe marlothii (Asphodelaceae),' South African Journal of Botany 74, 598-605. https://doi.org/10.1016/j.sajb.2008.02.008        [ Links ]

Van Wyk, B.-E. & Smith, G.F., 2003, Guide to the aloes of South Africa, Briza Publications, Pretoria.         [ Links ]

Wester, P., 2010, 'Sticky snack for sengis: The Cape rock elephant-shrew, Elephantulus edwardii (Macroscelidea), as a pollinator of the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae)', Naturwissenschaften 97, 1107-1112. https://doi.org/10.1007/s00114-010-0723-6        [ Links ]

Wilson, A.-L., Ward, D., Brown, M. & Johnson, S.D., 2009, 'Seed production in a threatened Aloe is not affected by bird exclusion or population size', Plant Ecology 203, 173-182. https://doi.org/10.1007/s11258-008-9524-9        [ Links ]

Zoeller, K., Steenhuisen, S.-L., Johnson, S. & Midgley, J., 2016, 'New evidence for mammal pollination of Protea species (Proteaceae) based on remote-camera analysis', Australian Journal of Botany 64, 1-7. https://doi.org/10.1071/BT15111        [ Links ]

 

 

Correspondence:
Craig Symes
craig.symes@wits.ac.za

Received: 25 Jan. 2017
Accepted: 23 June 2017
Published: 31 Aug. 2017