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Diurnal Pollination, Primarily by a Single Species of Rodent, Documented in Protea Foliosa Using Modified Camera Traps

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Diurnal Pollination, Primarily by a Single Species of Rodent, Documented in Protea Foliosa Using Modified Camera Traps South African Journal of Botany 97 (2015) 9–15 Contents lists available at ScienceDirect South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb Diurnal pollination, primarily by a single species of rodent, documented in Protea foliosa using modified camera traps Caitlin A. Melidonis, Craig I. Peter ⁎ Department of Botany, Rhodes University, PO Box 94, Grahamstown 6140, South Africa article info abstract Article history: Bowl-shaped inflorescences, geoflory, dull-coloured flowers and winter flowering suggest that Protea foliosa is Received 1 August 2014 adapted for rodent-pollination. To test this hypothesis, rodents were trapped in a large P. foliosa population Received in revised form 12 November 2014 near Grahamstown and examined for the presence of pollen on their snouts and in their scats. Camera traps, Accepted 10 December 2014 modified for near focus (b50 cm) by the addition of close-up filters, were used to record mammal visits to inflo- Available online xxxx rescences in situ. Two rodent species, Rhabdomys pumilio and Otomys irroratus, and a species of shrew, Crocidura Edited by CA Pauw cyanea,werecapturedandallhadP. foliosa pollen present on their snouts, but only R. pumilio was recorded on camera probing the flowers. Very little pollen was found in the scat of C. cyanea compared to the scat of Keywords: R. pumilio and none was found in the scat of O. irroratus. No camera trap footage was captured of any pollination Protea foliosa behaviour at night; however, seventeen rodent–flower interactions were recorded during the day. A bait station Diurnal rodent pollination was established near the flowers to test the efficacy of the camera traps at night by using food to attract animals Therophily into the field of view of the camera traps. All three trapped mammal species were recorded at the bait station and Rhabdomys pumilio photographed a number of times in the night, confirming the absence of nocturnal pollinator activity. Exclusion Otomys irroratus of mammals from P. foliosa inflorescences using wire cages, and the exclusion of all potential floral visitors with Crocidura cyanea nylon mesh bags resulted in a significant reduction in seed set. Unlike previous studies on rodent-pollinated Camera trap plants, we conclude that P. foliosa is pollinated almost exclusively during daylight and primarily by a single rodent species, R. pumilio. © 2014 SAAB. Published by Elsevier B.V. All rights reserved. 1. Introduction Originally described in Australian Proteaceae species, rodent pollina- tion (therophily) has, in recent years, been documented in various plant Pollination by rodents in South African Proteaceae was first de- families in the Fynbos biome in South Africa besides the Proteaceae. scribed by Rourke and Wiens (1977). However, of the approximately These species include Whiteheadia bifolia (Hyacinthaceae; Wester 35 proteoid species which have been identified as potentially rodent- et al., 2009), Cochicum scabromarginatum (Colchicaceae; Kleizen et al., pollinated (Rourke, 1980; Rebelo and Breytenbach, 1987), few have had 2008), Erica hanekomii and Erica lanuginosa (Ericaceae; Turner et al., their pollination biology investigated. To date, only Protea amplexicaulis, 2011; Lombardi et al., 2013), Massonia depressa (Hyacinthaceae; Protea humiflora (Wiens and Rourke, 1978), Protea nana (Biccard and Johnson et al., 2001), Liparia parva (Fabaceae; Letten and Midgley, Midgley, 2009) and Leucospermum arenarium (Johnson and Pauw, 2009), Cytinus visseri and Cytinus cf capensis (Cytinaceae; Johnson 2014) have been shown to be rodent-pollinated. The floral traits of Protea et al., 2011; Hobbhahn and Johnson, 2013). species that suggest pollination by rodents include: 1) bowl-shaped inflo- Protea foliosa is a dwarf species (b50 cm) with cryptic inflorescences rescences borne on short (3–4 mm) stout peduncles, often with bracts borne near ground level (geoflorous) and hidden amongst the leaves which are darkly coloured on the outside; 2) cryptic, geoflorous, axillary (Fig. 1A, Rebelo, 1995). Florets are white to cream contrasting with positioning of the inflorescences; 3) copious, sucrose-rich nectar produc- the surrounding brown-red bracts. This colouring is found in other tion with a high (ca. 36%) total carbohydrate composition; 4) often in- rodent-pollinated Protea species and was presumed by Wiens and flexed, wiry styles ca. 30–40 mm long; 5) a stigma-nectar distance of Rourke (1978) to be an adaptation to attract nocturnal rodents. approximately 10 mm to “fit” between the rostrum of the pollinating P. foliosa is therefore morphologically distinct from the well-known rodent and the stigma; 6) a distinctive ‘yeasty’ odour and 7) a winter– bird-pollinated Protea species which are tall shrubs or small trees with spring flowering period (Wiens, 1983; Rebelo and Breytenbach, 1987). large, brightly-coloured flowers borne prominently above the ground (Wiens and Rourke, 1978). Other features of P. foliosa include the pres- fl ⁎ Corresponding author. Tel.: +27 46 6038598. ence of scented in orescences that contain abundant nectar (pers. obs.), E-mail address: [email protected] (C.I. Peter). as well as winter to spring flowering which is similar to that of other http://dx.doi.org/10.1016/j.sajb.2014.12.009 0254-6299/© 2014 SAAB. Published by Elsevier B.V. All rights reserved. 10 C.A. Melidonis, C.I. Peter / South African Journal of Botany 97 (2015) 9–15 Fig. 1. Protea foliosa (A) is a dwarf shrub with dull-coloured inflorescences produced close to the ground. B) Motion-sensing camera traps, modified with the addition of closeup filters, were staked near open inflorescences to record the behaviour of visiting pollinators in situ. C) A striped field mouse, Rhabdomys pumilio,visitinganinflorescence. D) and E) R. pumilio probing inflorescences. F) Bait station in font of a modified camera (two R. pumilio individuals visiting the station). proposed rodent-pollinated Protea species (Wiens, 1983; Rebelo and subspinosus, Mus minutoides, Myomyscus verreauxi, Otomys irroratus, Breytenbach, 1987). Praomys verreauxi and Rhabdomys pumilio (Wiens and Rourke, 1978; The distribution of P. foliosa is limited to the extreme east of the Biccard and Midgley, 2009). The ranges of these rodent species overlap Fynbos biome in the Eastern Cape, South Africa, with localities between with that of P. foliosa, making them all candidate pollinators. As most Elandsberg and Port Elizabeth, as well as between Riebeek East and rodents are generalist feeders they are likely to be enticed to flowers Bushmans River Poort (Rebelo, 1995). P. foliosa was assumed by by nectar rewards during the winter periods when conventional food Rebelo (2008) to be rodent-pollinated because fresh rodent droppings resources are scarce (Wester et al., 2009). were found next to plants while surveying for the Protea Atlas. This, An initial pilot study using camera traps noted that rodents visited coupled with the similarity of the plant to other rodent-pollinated the P. foliosa inflorescences during daylight hours. This is in contrast species, has lead to the hypothesis that this species is pollinated by to previous rodent-pollination studies (Johnson et al., 2001; Kleizen rodents. et al., 2008; Wester et al., 2009; Letten and Midgley, 2009; Turner Numerous rodent species are known pollinators of several Protea et al., 2011) that have observed visits to flowers almost exclusively at species in the Western Cape including: Aethomys namaquensis, Acomys night. C.A. Melidonis, C.I. Peter / South African Journal of Botany 97 (2015) 9–15 11 On the basis of shared floral traits, we test the hypothesis that positioned 50 cm away from the plants and carefully orientated to P. foliosa is pollinated by a similar suite of rodents to other rodent- focus on an open P. foliosa inflorescence using a system of retort stand pollinated species in the west of the Fynbos. Secondly, we examined bosses attached to the stake (Fig 1B). Cameras were left in the field for the possibility that the majority of visits by rodents to flowers of periods ranging from three days to two weeks. The three camera traps P. foliosa occur during the day. were moved amongst 10 different flowering plants in the population. The three cameras totalled approximately 1000 h of observations. 2. Materials and methods Close-up (diopter) filters (2+) were attached in front of the lenses of the three camera traps with Prestik™ (equivalent to Blu-tack) to 2.1. Study site decrease the focal distance of the cameras from 1.5 m to approximately 0.5 m. The white Prestik was discoloured with carbon powder. Black in- This study was conducted in a large population of at least 200 sulation tape was placed over all but one of the infrared LEDs to prevent P. foliosa plants on an unused portion of the farm Upper Gletwyn near overexposure of nocturnal imagery (Supplementary Fig. 1). Cameras Beggars Bush, approximately 15 km east of Grahamstown, in the were configured for maximum sensitivity and to take three photo- Eastern Cape Province of South Africa (33°17′17.84″S, 26°40′44.45″E). graphs and one minute of video footage per triggering event during Field work was conducted between June and September 2013, corre- both day and night. sponding with the flowering season of P. foliosa between March and To confirm the sensitivity of the camera traps and that the absence of September (Rourke, 1980). The only co-occurring Protea species was nocturnal rodent flower visits was not an artefact of reduced camera Protea cynaroides, present in low numbers. The nearest P. cynaroides to sensitivity at night, a bait station was used to attract rodents. A mixture the study plants was approximately 50 m away. of peanut butter and rolled oats was placed in a shade-cloth bag and pegged to the ground in front of the modified camera trap's field of 2.2. Exclosure experiments view (Fig. 1F). The bait station was set up at 16:00 on the 16th of July and recorded visitations until 07:00 two days later.
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