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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Good times, bad times: inter-annual reproductive output in a montane endemic succulent (Aloe peglerae; Asphodelaceae) driven by contrasting visitor responses of small mammals and birds

Stephanie L. Payne A B , Ed T. F. Witkowski A and Craig T. Symes A
+ Author Affiliations
- Author Affiliations

A School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits 2050, Johannesburg, South Africa.

B Corresponding author. Email: stephanie@thepaynetribe.co.za

Australian Journal of Botany 67(2) 116-127 https://doi.org/10.1071/BT18163
Submitted: 17 August 2018  Accepted: 7 March 2019   Published: 22 April 2019

Abstract

The movements of birds and small mammals may be affected by spatial and temporal variation in resource availability. For the genus Aloe, bird abundance and diversity increase in response to increases in nectar availability during flowering. Aloe peglerae Schönland, endemic to the Magaliesberg Mountain Range, South Africa, is primarily pollinated by the Cape rock-thrush (Monticola rupestris), but the nocturnal Namaqua rock mouse (Micaelamys namaquensis) contributes to pollination. To test the independent contributions of different pollinator guilds, i.e. birds and small mammals, we conducted selective pollinator exclusion experiments during two consecutive flowering seasons – one ‘good’ year and one ‘poor’ year (14 and 7% of plants flowering respectively). Reproductive output for both years was measured for A. peglerae plants assigned to selective exclusion treatments: (i) no visitors; (ii) nocturnal visitors; (iii) diurnal visitors; and (iv) all visitors, with camera traps recording visitors to each treatment. Bird visitation rates to the ‘diurnal visitors’ treatment were higher during the good year; subsequently, reproductive output in the poor year was lower, with plants in this treatment producing no fruit in the poor flowering year. In the ‘nocturnal visitors’ treatment, nocturnal visitation rates were similar with no significant difference in reproductive output between years. Seed viability was maintained between years, although less seed was produced during the poor flowering season. Mobile birds are less abundant in the A. peglerae population during poor flowering years – years when nectar resources are less abundant than in good flowering years, resulting in reduced plant reproductive output. However, the presence of non-flying, small mammals that cannot relocate to better feeding grounds compensates for the absence of birds in poor flowering years. This aloe may be resilient against Allee effects in the absence of primary pollinators. Nonetheless, conservation of A. peglerae should still be prioritised since low flowering densities and ongoing anthropogenic disturbance could be detrimental to the species’ survival.

Additional keywords: Cape rock-thrush, inter-annual variation, Namaqua rock mouse, resource tracking.


References

Arena G (2013) The reproductive biology and habitat requirements of Aloe peglerae, a montane endemic aloe of the Magaliesberg Mountain Range, South Africa. Unpublished MSc thesis, University of the Witwatersrand, Johannesburg, South Africa.

Arena G, Symes CT, Witkowski ETF (2013) The birds and the seeds: opportunistic avian nectarivores enhance reproduction in an endemic montane aloe. Plant Ecology 214, 35–47.
The birds and the seeds: opportunistic avian nectarivores enhance reproduction in an endemic montane aloe.Crossref | GoogleScholarGoogle Scholar |

Arena G, Witkowski ETF, Symes CT (2015) Growing on rocky ground: microhabitat predictors for site-occupancy of Aloe peglerae, an Endangered endemic species with a restricted range. South African Journal of Botany 100, 174–182.
Growing on rocky ground: microhabitat predictors for site-occupancy of Aloe peglerae, an Endangered endemic species with a restricted range.Crossref | GoogleScholarGoogle Scholar |

Botes C, Johnson SD, Cowling RM (2008) Coexistence of succulent tree aloes: partitioning of bird pollinators by floral traits and flowering phenology. Oikos 117, 875–882.
Coexistence of succulent tree aloes: partitioning of bird pollinators by floral traits and flowering phenology.Crossref | GoogleScholarGoogle Scholar |

Botes C, Wragg PD, Johnson SD (2009a) New evidence for bee-pollination systems in Aloe (Asphodelaceae: Aloideae), a predominantly bird-pollinated genus. South African Journal of Botany 75, 675–681.
New evidence for bee-pollination systems in Aloe (Asphodelaceae: Aloideae), a predominantly bird-pollinated genus.Crossref | GoogleScholarGoogle Scholar |

Botes C, Johnson SD, Cowling RM (2009b) The birds and the bees: using selective exclusion to identify effective pollinators of African tree aloes. International Journal of Plant Sciences 170, 151–156.
The birds and the bees: using selective exclusion to identify effective pollinators of African tree aloes.Crossref | GoogleScholarGoogle Scholar |

Brown ED, Hopkins MJG (1996) How New Guinea rainforest flower resources vary in time and space: Implications for nectarivorous birds. Australian Journal of Ecology 21, 363–378.
How New Guinea rainforest flower resources vary in time and space: Implications for nectarivorous birds.Crossref | GoogleScholarGoogle Scholar |

Broyles SB, Wyatt R (1990) Paternity analysis in a natural population of Asclepias exaltata: multiple paternity, functional gender and the ‘pollen-donation hypothesis’. Evolution 44, 1454–1468.

Carter RV (2004) Resource tracking by bumble bees: responses to plant-level differences in quality. Ecology 85, 2764–2771.
Resource tracking by bumble bees: responses to plant-level differences in quality.Crossref | GoogleScholarGoogle Scholar |

Carter S, Lavranos JJ, Newton LE, Walker CC (2011) ‘Aloes: the definitive guide.’ (Royal Botanic Gardens: Kew: UK)

Cotton PA (2007) Seasonal resource tracking by Amazonian hummingbirds. The Ibis 149, 135–142.
Seasonal resource tracking by Amazonian hummingbirds.Crossref | GoogleScholarGoogle Scholar |

Cousins SR, Witkowski ETF (2012) African aloe ecology: a review. Journal of Arid Environments 85, 1–17.
African aloe ecology: a review.Crossref | GoogleScholarGoogle Scholar |

Craig AJFK, Hulley PE (1994) Sunbird movements: a review, with possible models. The Ostrich 65, 106–110.
Sunbird movements: a review, with possible models.Crossref | GoogleScholarGoogle Scholar |

Cunningham SA (1991) Experimental evidence for pollination of Banksia spp. by non-flying mammals. Oecologia 87, 86–90.
Experimental evidence for pollination of Banksia spp. by non-flying mammals.Crossref | GoogleScholarGoogle Scholar | 28313356PubMed |

Duffy KJ, Johnson SD, Peter C (2014) A temporal dimension to the influence of pollen rewards on bee behaviour and fecundity in Aloe tenuior. PLoS One 9, e94908
A temporal dimension to the influence of pollen rewards on bee behaviour and fecundity in Aloe tenuior.Crossref | GoogleScholarGoogle Scholar | 24755611PubMed |

Dzerefos CM, Erasmus BFN, Witkowski ETF, Guo D (2015) Modelling the current and future dry-season distribution of the edible stinkbug Encosternum delegorguei in sub-Saharan Africa. Entomologia Experimentalis et Applicata 156, 1–13.
Modelling the current and future dry-season distribution of the edible stinkbug Encosternum delegorguei in sub-Saharan Africa.Crossref | GoogleScholarGoogle Scholar |

Faegri K, van der Pijl L (1979) ‘The principles of pollination ecology.’ 3rd edn. (Pergamon Press: Oxford, UK)

Forbes RW, Craig AJFK, Hulley PE, Parker DM (2009) Seasonal variation in the avian community associated with an Aloe ferox (Asphodelaceae, Mill.) flowering event in the Eastern Cape, South Africa. In ‘Proceedings of the 12th Pan-African Ornithological Congress 2008’. (Eds DM Harebottle, AJFK Craig, MD Anderson, H Rakotomanana, M Mucha) pp. 9–17. (Animal Demography Unit: Cape Town, South Africa)

Franklin DC (1999) Opportunistic nectarivory: an annual dry season phenomenon among birds in monsoonal northern Australia. Emu 99, 135–141.
Opportunistic nectarivory: an annual dry season phenomenon among birds in monsoonal northern Australia.Crossref | GoogleScholarGoogle Scholar |

Franklin DC, Noske RA (1999) Birds and nectar in a monsoonal woodland: correlations at three spatio-temporal scales. Emu 99, 15–28.
Birds and nectar in a monsoonal woodland: correlations at three spatio-temporal scales.Crossref | GoogleScholarGoogle Scholar |

García D, Ortiz-Pulido R (2004) Patterns of resource tracking by avian frugivores at multiple spatial scales: two case studies on discordance among scales. Ecography 27, 187–196.
Patterns of resource tracking by avian frugivores at multiple spatial scales: two case studies on discordance among scales.Crossref | GoogleScholarGoogle Scholar |

Giradoux P (2018) Pgirmess: spatial analysis and data mining for field ecologists. R Package ver. 1.6.9. Available at: https://CRAN.R-project.org/package=pgirmess (accessed 6 August 2018).

Goldingay RL (1990) The foraging behaviour of a nectar feeding marsupial, Petaurus australis. Oecologia 85, 191–199.
The foraging behaviour of a nectar feeding marsupial, Petaurus australis.Crossref | GoogleScholarGoogle Scholar | 28312555PubMed |

Hargreaves AL, Harder LD, Johnson SD (2008) Aloe inconspicua: the first record of an exclusively insect-pollinated aloe. South African Journal of Botany 74, 606–612.
Aloe inconspicua: the first record of an exclusively insect-pollinated aloe.Crossref | GoogleScholarGoogle Scholar |

Hargreaves AL, Harder LD, Johnson SD (2012) Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees. Annals of Botany 109, 761–772.
Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees.Crossref | GoogleScholarGoogle Scholar | 22278414PubMed |

Hoffman MT (1988) The pollination ecology of Aloe ferox Mill. South African Journal of Botany 54, 345–350.
The pollination ecology of Aloe ferox Mill.Crossref | GoogleScholarGoogle Scholar |

ISTA (2003) Biochemical test for viability. The topographical tetrazolium test. In ‘International rules for seed testing’. (International Seed Testing Association: Bassersdorf, Switzerland)

Johnson DN, Maclean GL (1994) Altitudinal migration in Natal. The Ostrich 65, 86–94.
Altitudinal migration in Natal.Crossref | GoogleScholarGoogle Scholar |

Johnson SD, Nicolson SW (2008) Evolutionary associations between nectar properties and specificity in bird pollination systems. Biology Letters 4, 49–52.
Evolutionary associations between nectar properties and specificity in bird pollination systems.Crossref | GoogleScholarGoogle Scholar | 17999944PubMed |

Johnson CM, Pauw A (2014) Adaptation for rodent pollination in Leucospermum arenarium (Proteaceae) despite rapid pollen loss during grooming. Annals of Botany 113, 931–938.
Adaptation for rodent pollination in Leucospermum arenarium (Proteaceae) despite rapid pollen loss during grooming.Crossref | GoogleScholarGoogle Scholar | 24607723PubMed |

Johnson MD, Sherry TW (2001) Effects of food availability on the distribution of migratory warblers among habitats in Jamaica. Journal of Animal Ecology 70, 546–560.
Effects of food availability on the distribution of migratory warblers among habitats in Jamaica.Crossref | GoogleScholarGoogle Scholar |

Johnson SD, Hargreaves AL, Brown M (2006) Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87, 2709–2716.
Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant.Crossref | GoogleScholarGoogle Scholar | 17168015PubMed |

Kuiper TR, Smith DL, Wolmarans MHL, Jones SS, Forbes RW, Hulley PE, Craig AJFK (2015) The importance of winter-flowering Aloe ferox for specialist and generalist nectar-feeding birds. Emu 115, 49–57.
The importance of winter-flowering Aloe ferox for specialist and generalist nectar-feeding birds.Crossref | GoogleScholarGoogle Scholar |

Las-Casas FMG, Azevedo Júnior SM, Dias Filho MM (2012) The community of hummingbirds (Aves: Trochilidae) and the assemblage of flowers in a Caatinga vegetation. Brazilian Journal of Biology 72, 51–58.
The community of hummingbirds (Aves: Trochilidae) and the assemblage of flowers in a Caatinga vegetation.Crossref | GoogleScholarGoogle Scholar |

Letten AD, Midgley JJ (2009) Rodent pollination in the Cape legume Liparia parva. Austral Ecology 34, 233–236.
Rodent pollination in the Cape legume Liparia parva.Crossref | GoogleScholarGoogle Scholar |

Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72, 180–193.
Temporal variation in birds and fruits along an elevational gradient in Costa Rica.Crossref | GoogleScholarGoogle Scholar |

MacNally R (1996) A winter’s tale: among-year variation in bird community structure in a southeastern Australian forest. Australian Journal of Ecology 21, 280–291.
A winter’s tale: among-year variation in bird community structure in a southeastern Australian forest.Crossref | GoogleScholarGoogle Scholar |

Malizia LR (2001) Seasonal fluctuations of birds, fruits and flowers in a subtropical forest of Argentina. The Condor 103, 45–61.
Seasonal fluctuations of birds, fruits and flowers in a subtropical forest of Argentina.Crossref | GoogleScholarGoogle Scholar |

Melidonis CA, Peter CI (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.
Diurnal pollination, primarily by a single species of rodent, documented in Protea foliosa using modified camera traps.Crossref | GoogleScholarGoogle Scholar |

Mucina L, Rutherford MC (2006) ‘The vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19.’ (South African National Biodiversity Institute: Pretoria, South Africa)

Oatley TB (1964) The probing of aloe flowers by birds. Lammergeyer 3, 2–8.

Oatley TB, Skead DM (1972) Nectar-feeding by South African birds. Lammergeyer 15, 65–73.

Payne SL, Symes CT, Witkowski ETF (2016) Of feathers and fur: differential pollinator roles of birds and small mammals in the grassland succulent Aloe peglerae. Austral Ecology 41, 952–963.
Of feathers and fur: differential pollinator roles of birds and small mammals in the grassland succulent Aloe peglerae.Crossref | GoogleScholarGoogle Scholar |

Pfab MF, Scholes MA (2004) Is the collection of Aloe peglerae from the wild sustainable? An evaluation using stochastic population modelling. Biological Conservation 118, 695–701.
Is the collection of Aloe peglerae from the wild sustainable? An evaluation using stochastic population modelling.Crossref | GoogleScholarGoogle Scholar |

Pfab MF, von Staden L, Hahn N (2016) Aloe peglerae Schönland. National assessment: Red List of South African plants version 2017.1. (South African National Biodiversity Institute). Available at: http://redlist.sanbi.org/species.php?species=2206-198 (accessed 6 August 2018).

R Core Team (2018) ‘R: A language and environment for statistical computing.’ Version 3.5.1. (R Foundation for Statistical Computing: Vienna, Austria) Available at: https://www.R-project.org/ (accessed December 2018)

Reynolds GW (1950) ‘Aloes of Southern Africa.’ (Aloes of South Africa Book Fund: Johannesburg, South Africa)

Ribble DO, Perrin MR (2005) Social organisation of the eastern rock elephant shrew (Elephantulus myurus): the evidence for mate guarding. Belgian Journal of Zoology 135, 167–173.

Schmid B, Nottebrock H, Elser KJ, Pagel J, Pauw A, Böhning-Gaese K, Schurr FM, Schleuning M (2015) Reward quality predicts effects of bird-pollinators on the reproduction of African Protea shrubs. Perspectives in Plant Ecology, Evolution and Systematics 17, 209–217.
Reward quality predicts effects of bird-pollinators on the reproduction of African Protea shrubs.Crossref | GoogleScholarGoogle Scholar |

Scholes MA (1988) A population study of Aloe peglerae in habitat. South African Journal of Botany 54, 137–139.
A population study of Aloe peglerae in habitat.Crossref | GoogleScholarGoogle Scholar |

Schradin C, Pillay N (2006) Female striped mice (Rhabdomys pumilio) change their home ranges in response to seasonal variation in food availability. Behavioral Ecology 17, 452–458.
Female striped mice (Rhabdomys pumilio) change their home ranges in response to seasonal variation in food availability.Crossref | GoogleScholarGoogle Scholar |

South African Weather Service (2016) ‘Historical rainfall data for the period 2012–2014.’ (South African Weather Service) Available at: http://www.weathersa.co.za/climate/historical-rain-maps (accessed 17 March 2016)

Steenhuisen S-L, Balmer A, Zoeller K, Kuhn N, Midgley J, Hansen D, Johnson SD (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.
Carnivorous mammals feed on nectar of Protea species (Proteaceae) in South Africa and likely contribute to their pollination.Crossref | GoogleScholarGoogle Scholar |

Sutherland S (1986) Patterns of fruit-set: what controls fruit-flower ratios in plants? Evolution 40, 117–128.
Patterns of fruit-set: what controls fruit-flower ratios in plants?Crossref | GoogleScholarGoogle Scholar | 28564122PubMed |

Sutherland S, Delph LF (1984) On the importance of male fitness in plants: patterns of fruit set. Ecology 65, 1093–1104.
On the importance of male fitness in plants: patterns of fruit set.Crossref | GoogleScholarGoogle Scholar |

Symes CT (2010) The sweet option: the importance of Aloe marlothii for opportunistic avian nectarivores. Bulletin of the African Bird Club 17, 178–187.

Symes CT, Nicolson SW (2008) Production of copious dilute nectar in the bird-pollinated African succulent Aloe marlothii (Asphodelaceae). South African Journal of Botany 74, 598–605.
Production of copious dilute nectar in the bird-pollinated African succulent Aloe marlothii (Asphodelaceae).Crossref | GoogleScholarGoogle Scholar |

Symes CT, Downs CT, McLean S (2001) Seasonal occurrence of the Malachite sunbird, Nectarinia famosa, and Gurney’s sugarbird, Promerops gurneyi, in KwaZulu-Natal, South Africa. The Ostrich 72, 45–49.
Seasonal occurrence of the Malachite sunbird, Nectarinia famosa, and Gurney’s sugarbird, Promerops gurneyi, in KwaZulu-Natal, South Africa.Crossref | GoogleScholarGoogle Scholar |

Symes CT, Nicolson SW, McKechnie AE (2008) Response of avian nectarivores to the flowering of Aloe marlothii: a nectar oasis during dry South African winters. Journal of Ornithology 149, 13–22.
Response of avian nectarivores to the flowering of Aloe marlothii: a nectar oasis during dry South African winters.Crossref | GoogleScholarGoogle Scholar |

Symes CT, Human H, Nicolson SW (2009) Appearances can be deceiving: pollination in two sympatric winter-flowering Aloe species. South African Journal of Botany 75, 668–674.
Appearances can be deceiving: pollination in two sympatric winter-flowering Aloe species.Crossref | GoogleScholarGoogle Scholar |

Symes CT, McKechnie AE, Nicolson SW, Woodborne SM (2011) The nutritional significance of a winter-flowering succulent for opportunistic avian nectarivores. The Ibis 153, 110–121.
The nutritional significance of a winter-flowering succulent for opportunistic avian nectarivores.Crossref | GoogleScholarGoogle Scholar |

Tellería JL, Pérez-Tris J (2007) Habitat effects on resource tracking ability: do wintering blackcaps Sylvia atricapilla track fruit availability? The Ibis 149, 18–25.
Habitat effects on resource tracking ability: do wintering blackcaps Sylvia atricapilla track fruit availability?Crossref | GoogleScholarGoogle Scholar |

Van Wyk B-E, Smith GF (2014) ‘Guide to the aloes of South Africa.’ 3rd edn. (Briza Publications: Pretoria, South Africa)

Wesson J (2007) Aloe peglerae: On the brink of extinction? African Wildlife 61, 41

Wester P, Stanway R, Pauw A (2009) Mice pollinate the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae) – First field observations with photographic documentation of rodent pollination in South Africa. South African Journal of Botany 75, 713–719.
Mice pollinate the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae) – First field observations with photographic documentation of rodent pollination in South Africa.Crossref | GoogleScholarGoogle Scholar |

Wickham H (2016) ‘Ggplot2: Elegant graphics for data analysis.’ (Springer-Verlag: New York)

Wilmshurst JF, Fryxell JM, Farm BP, Sinclair ARE, Henschel CP (1999) Spatial distribution of Serengeti wildebeest in relation to resources. Canadian Journal of Zoology 77, 1223–1232.
Spatial distribution of Serengeti wildebeest in relation to resources.Crossref | GoogleScholarGoogle Scholar |

Wilson A-L, Ward D, Brown M, Johnson SD (2009) Seed production in a threatened Aloe is not affected by bird exclusion or population size. Plant Ecology 203, 173–182.
Seed production in a threatened Aloe is not affected by bird exclusion or population size.Crossref | GoogleScholarGoogle Scholar |

Zanjan MG, Asli DE (2012) A study of seed germination and early seedling growth of wheat genotypes affected by different seed pyridoxine-priming duration. Annals of Biological Research 3, 5687–5691.

Zoeller KC, Steenhuisen S-L, Johnson SD, Midgley JJ (2016) New evidence for mammal pollination of Protea species (Proteaceae) based on remote-camera analysis. Australian Journal of Botany 64, 1–7.
New evidence for mammal pollination of Protea species (Proteaceae) based on remote-camera analysis.Crossref | GoogleScholarGoogle Scholar |