New evidence for mammal pollination of Protea species (Proteaceae) based on remote-camera analysis
K. C. Zoeller A , S.-L. Steenhuisen A C , S. D. Johnson B and J. J. Midgley AA Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa.
B School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa.
C Corresponding author. Email: sandysteenhuisen@gmail.com
Australian Journal of Botany 64(1) 1-7 https://doi.org/10.1071/BT15111
Submitted: 14 May 2015 Accepted: 16 November 2015 Published: 12 February 2016
Abstract
Flower visitation by small mammals is difficult to observe directly on account of their sensitivity to human presence and the nocturnal activity of some species. Their role in pollination has, thus, been inferred mostly from analysis of fur and faecal pollen loads of field-trapped animals. The development of motion-activated remote cameras allows for unprecedented insights into natural behaviours of small mammals on flowers. We used remote cameras to assess the identity of flower visitors, and the frequency and timing of their visitation to flower heads of four poorly studied Protea species (P. cordata, P. decurrens P. scabra and P. subulifolia) that were predicted to be rodent-pollinated on the basis of floral traits. Camera footage revealed that small mammals (typically three to six rodent species per Protea species) were frequent visitors to flower heads over one flowering season, making up 100% of visits to P. cordata and P. subulifolia, 98% of visits to P. decurrens, and 90% of visits to P. scabra. Rodents that are known pollinators of other ground Protea species, such as Acomys subspinosus, Micaelamys namaquensis and Rhabdomys pumulio, were observed to make contact with reproductive parts of the flowers, but further work would be required to demonstrate unequivocally that they are the main pollen vectors of these species. Mus minutoides was recorded for the first time to frequently visit inflorescences of P. subulifolia. Other visitors included genets that visited P. scabra inflorescences to lick nectar off florets, and birds that were relatively infrequent visitors to all species. Together with recent literature, the present study has shown that the utilisation of remote cameras in pollination studies provides an efficient, discreet method for observing vertebrate flower-visiting behaviour.
References
Biccard A, Midgley JJ (2009) Rodent pollination in Protea nana. South African Journal of Botany 75, 720–725.| Rodent pollination in Protea nana.Crossref | GoogleScholarGoogle Scholar |
Bridges AS, Noss AJ (2011) Behavior and activity patterns. In ‘Camera traps in animal ecology: methods and analyses’. (Eds AF O’Connell, JD Nichols, KU Karanth) pp. 57–65. (Springer: New York)
Carthew SM (1993) An assessment of pollinator visitation to Banksia spinulosa. Australian Journal of Ecology 18, 257–268.
| An assessment of pollinator visitation to Banksia spinulosa.Crossref | GoogleScholarGoogle Scholar |
Carthew SM, Goldingay RL (1997) Non-flying mammals as pollinators. Trends in Ecology & Evolution 12, 104–108.
| Non-flying mammals as pollinators.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFKitQ%3D%3D&md5=41e37fcfdffb198c638488e442f240d4CAS |
Carthew SM, Slater E (1991) Monitoring animal activity with automated photography. The Journal of Wildlife Management 554, 689–692.
Chimimba CT, Bennet NC (2005) Order Rodentia. In ‘The Mammals of the southern African subregion’. (Eds JD Skinner, CT Chimimba) pp. 77–209. (Cambridge University Press: Cambridge, UK)
Fernandez-Duque E, Erkert HG (2006) Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco. Folia Primatologica 77, 123–138.
| Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco.Crossref | GoogleScholarGoogle Scholar |
Fleming P, Nicolson S (2002) How important is the relationship between Protea humiflora (Proteaceae) and its non-flying mammal pollinators? Oecologia 132, 361–368.
| How important is the relationship between Protea humiflora (Proteaceae) and its non-flying mammal pollinators?Crossref | GoogleScholarGoogle Scholar |
Goldingay RL, Carthew SM, Whelan RJ (1991) The importance of non-flying mammals in pollination. Oikos 61, 79–87.
| The importance of non-flying mammals in pollination.Crossref | GoogleScholarGoogle Scholar |
Hoole C, Oosthuizen MK, Chimimba CT, Bennett NC (2012) The locomotory activity rhythm of the spiny mouse, Acomys spinosissimus from southern Africa: light entrainment and endogenous circadian rhythms. Journal of Zoology 288, 93–102.
| The locomotory activity rhythm of the spiny mouse, Acomys spinosissimus from southern Africa: light entrainment and endogenous circadian rhythms.Crossref | GoogleScholarGoogle Scholar |
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 SD, Raguso R (2015) The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa. Annals of Botany 117, 25–36.
| The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa.Crossref | GoogleScholarGoogle Scholar | 26346719PubMed |
Johnson SD, Burgoyne PM, Harder LD, Dötterl S (2011) Mammal pollinators lured by the scent of a parasitic plant. Proceedings. Biological Sciences 278, 2303–2310.
| Mammal pollinators lured by the scent of a parasitic plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVynsb7K&md5=3c7fc8ce22dda03a53412370a5b4b8c0CAS |
Kay BJ, Twigg LE, Korn TJ, Nicol HI (1994) The use of artificial perches to increase predation on house mice (Mus domesticus) by raptors. Wildlife Research 21, 95–105.
| The use of artificial perches to increase predation on house mice (Mus domesticus) by raptors.Crossref | GoogleScholarGoogle Scholar |
Kingdon J, Happold D, Butynski T, Hoffmann M, Happold M, Kalina J (2013) ‘Mammals of Africa.’ (Bloomsbury Publishing: London)
Kleizen C, Midgley JJ, Johnson SD (2008) Pollination systems of Colchicum (Colchicaceae) in southern Africa: evidence for rodent pollination. Annals of Botany 102, 747–755.
| Pollination systems of Colchicum (Colchicaceae) in southern Africa: evidence for rodent pollination.Crossref | GoogleScholarGoogle Scholar | 18723860PubMed |
Law BS, Lean M (1999) Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest. Biological Conservation 91, 201–212.
| Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest.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 |
Rebelo AG (2001) ‘A field guide to the proteas of Southern Africa.’ (Fernwood Press: Vlaeberg, South Africa)
Rebelo AG (2006) ‘Protea atlas project.’ Available at http://protea.worldonline.co.za/default.htm [accessed 10 July 2011].
Rebelo TG, Breytenbach GJ (1987) Mammal Pollination in the Cape Flora. In ‘South African national science program report 141: preliminary synthesis of pollination biology in the Cape flora’. (Eds AG Rebelo) pp. 109–124. (South African National Scientific Programmes Unit, CSIR: Pretoria, South Africa)
Roberts PD, Somers MJ, White RM, Nel JAJ (2007) Diet of the South African large-spotted genet Genetta tigrina (Carnivora, Viverridae) in a coastal dune forest. Acta Theriologica 52, 45–53.
| Diet of the South African large-spotted genet Genetta tigrina (Carnivora, Viverridae) in a coastal dune forest.Crossref | GoogleScholarGoogle Scholar |
Rourke J, Wiens D (1977) Convergent floral evolution in South African and Australian Proteaceae and its possible bearing on pollination by non-flying mammals. Annals of the Missouri Botanical Garden 64, 1–7.
| Convergent floral evolution in South African and Australian Proteaceae and its possible bearing on pollination by non-flying mammals.Crossref | GoogleScholarGoogle Scholar |
Schradin C, Pillay N (2004) The Striped Mouse (Rhabdomys pumilio) from the succulent karoo, South Africa: a territorial group-living solitary forager with communal breeding and helpers at the nest. Journal of Comparative Psychology 118, 37–47.
| The Striped Mouse (Rhabdomys pumilio) from the succulent karoo, South Africa: a territorial group-living solitary forager with communal breeding and helpers at the nest.Crossref | GoogleScholarGoogle Scholar | 15008671PubMed |
Steenhuisen S-L, Johnson SD (2012) Evidence for beetle pollination in the African grassland sugarbushes (Protea: Proteaceae). Plant Systematics and Evolution 298, 857–869.
| Evidence for beetle pollination in the African grassland sugarbushes (Protea: Proteaceae).Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
Wiens D, Rourke JP (1978) Rodent pollination in southern African Protea spp. Nature 276, 71–73.
| Rodent pollination in southern African Protea spp.Crossref | GoogleScholarGoogle Scholar |
Wiens D, Rourke JP, Casper BB, Rickart EA, LaPine TR, Peterson CJ, Channing A (1983) Nonflying mammal pollination of southern African proteas: a non-coevolved system. Annals of the Missouri Botanical Garden 70, 1–31.
| Nonflying mammal pollination of southern African proteas: a non-coevolved system.Crossref | GoogleScholarGoogle Scholar |
