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

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South African Journal of Botany

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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 pollination (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

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. The different mam- To determine the dependence of P. foliosa on rodents for pollination, mal species visiting the bait station were summarised as present or 20 inflorescences in bud were randomly selected and enclosed in absent for each hour of the day over the trapping period as a large num- 13 mm wire mesh which allowed access to insects once flowers ber of animals visited the station at certain times and it was not possible had opened but excluded rodents and birds (e.g. Duffy et al., 2014). to differentiate individual animals. A further 44 inflorescences were covered with stiff shade-cloth bags (ca 1 mm mesh) in the bud stage to exclude both insects and rodents. Bags were bound to the stem of the inflorescence and positioned in 2.4. Mammal trapping such a way as to preclude any contact with the florets. Finally fifty inflorescences were left unmanipulated as open controls. All inflorescences Live rodent trapping was used to assess the local occurrence and were located on separate plants. species diversity of rodents and to document pollen loads of potential After two months the inflorescences were harvested and seed set pollinators. Trapping took place on the 11th, 22nd and 23rd of July determined. Quantifying seed set in Protea species is difficult as individ- 2013 at peak flowering of P. foliosa. A total of twenty plastic Sherman- ual ovules remain attached to the inflorescence regardless of whether or type gutter traps were spread out across the study site in three 35 m not they develop into viable seed (Wiens, 1983; Biccard and Midgley, transects. The traps were spaced approximately 5 m apart and were 2009). In addition, sterile and viable achenes do not differ morphologi- baited with a mixture of rolled oats and peanut butter. cally, which makes them difficult to distinguish externally. We followed The traps were set at 16:00 and captured animals were removed the previous studies (Wiens, 1983; Biccard and Midgley, 2009) to identify following morning at 07:00, identified, inspected for pollen, marked viable, endosperm-containing seeds as being swollen and solid white using a permanent marker to determine recaptures and released at in colour, in contrast to dull-coloured and fibrous sterile seeds when the site of capture. The traps were then reset with new bait added and viewed in cross-section. Seeds were examined by cutting transverse trapping repeated during the daylight hours. sections through the achenes in place on mature infructescences. Only healthy, mature infructescences were dissected and immature infructescences and infructescences containing frass of parasitizing insects were excluded from the seed set analyses, resulting in reduced sample sizes of all treatments, particularly open controls (n = 25) and caged treatments (n = 4) but also bagged treatments (n = 33). A Kruskall–Wallis test with post-hoc Mann–Whitney pair wise comparison was used to compare treatments in the programme PAST (Hammer et al., 2001).

2.3. Camera trap observation of rodents

Remote cameras are being increasingly used to document plant- pollinator interactions. Typically this entails videography (eg. Micheneau et al., 2006; Marten-Rodriguez and Fenster, 2008; Wester et al., 2009; Letten and Midgley, 2009) and more recently, rapid time lapse photography (Yokota and Yahara, 2012; Suetsugu and Tanaka, 2013). Recent studies by Hobbhahn and Johnson (2013) and Lombardi et al. (2013) used motion activated camera traps to observe rodent visits to C. capensis and E. lanuginosa respectively. To observe plant-pollinator interactions in P. foliosa, three com- Fig. 2. Mean number of seeds produced per inflorescence for open controls exposed to all visitors (n = 26), bagged inflorescences excluding all pollinators (n = 33) and caged mercially available camera traps (Bushnell Trophy Cameras, two of inflorescences excluding vertebrates and not insects (n = 4). Boxes represent standard model 119537 and one of model 119447) were each mounted on a error of the mean and bars, standard deviation. Homogenous groups were identified metal stake hammered into the ground near the plants. Cameras were using Mann–Whitney post-hoc pairwise test and are indicated by letters. 12 C.A. Melidonis, C.I. Peter / South African Journal of Botany 97 (2015) 9–15

Table 1 self-pollination rates are low, and suggests that insects are not impor- Mammal captures in the vicinity of Protea foliosa plants. tant pollinators of this species (Fig. 2). Unbagged inflorescences had a Date & time Captured species Total Trap success mean seed set of 1.8 seeds per inflorescence, with some inflorescences captured ratea setting up to eight seeds. Natural seed set is therefore low and the R. pumilio O. irroratus C. cyanea mean number of florets per inflorescence is 96 (n = 7, SD = 6.8) in 11 July (4 pm) 3 – 2 5 25% – this population. There was only one instance of a seed being set in a 12 July (7 am) 6 1 7 35% fl fl 22 July (7 am) 7 3 2 12 60% bagged ower, while no seeds were set in owers that had been 22 July (4 pm) 2 – 2 4 20% caged although the sample sizes, particularly of the caged treatments 23 July (7 am) 6 – 1 7 35% were low as a result of seed predation. Total 24 3 8 35 35%

a Percentage of deployed traps capturing an animal. 3.2. Mammal captures

Over three 24-hour periods of trapping in July, 33 animals were 2.5. Pollen loads caught with only one recapture, totalling 34 captures (Table 1), an aver- age trapping success of 35%. Two rodent species and one shrew species To document pollen loads, the fur around the snout of the captured were caught and all had evidence of P. foliosa pollen on their rostra animals was swabbed for pollen with fuchsin gelatine (Beattie, 1971), (Fig. 3). R. pumilio was the most abundant of the captured species from the eye down to the nose and around the mouth. Cubes of fuchsin followed by O. irroratus and a species of musk shrew, thought to be gelatine where individually melted on a glass slide on a hot plate and Crocidura cyanea (Reddish-grey musk shrew, family Soricidae; Table 1). covered with a 22 mm × 50 mm cover slip. The number of P. foliosa pollen grains was counted over four length-wise scans of the cover slip (Letten and Midgley, 2009; Turner et al., 2011)at10×magnification. 3.3. Camera trap data Scats collected from the traps of each captured rodent were stored in separate 1.5 microcentrifuge tubes in a freezer. Approximately half a Camera traps recorded a total of 49 images and videos of rodents pellet of each scat sample was pulverised in 0.5 ml of distilled water interacting with P. foliosa flowers, representing seventeen visit se- in a microcentrifuge tube using a metal rod. The sample was then quences at seven different plants. Only R. pumilio probed flowers vortexed for five minutes before adding five drops of liquid fuchsin to (Fig. 1C, D and E) and all visits occurred during daylight hours, 76% be- the solution and votexing it for a further thirty seconds. Samples were tween 07:00 and 12:00 and 24% between 12:00 and 16:00 (Fig. 5). Visits then centrifuged for ten minutes at 2000 rpm to separate the heavier lasted up to 30 s, with R. pumilio individuals inserting their rostra faecal matter from the lighter pollen grains. The excess liquid was amongst florets to access nectar (Supplementary Videos 1 and 2). discarded and the top layer of the remaining faecal pellet was scraped While probing the flowers, pollen is loaded onto the rodents' rostrum off using a spatula and placed on a glass slide. The samples were then as evidenced by pollen load analysis of trapped rodents (Fig. 3). Neither covered with a 22 mm × 50 mm cover slip and scanned for pollen grains O. irroratus nor C. cyanea were recorded visiting inflorescences. as described above. Pollen loads and scat pollen content were compared All three species were present at the bait station from the time it was using Kruskall–Wallis with Mann–Whitney post-hoc pair wise compar- established (16:00) until the bait ran out (23:00). Animals continued to ison in PAST (Hammer et al., 2001). periodically visit the bait station despite the absence of bait until 15:30 two days later. Only the three species trapped with Sherman traps were 3. Results recorded at the bait station (Fig. 6), all being present between 16:00 and 16:30 (Supplementary Videos 3 and 4). The most common species 3.1. Seed set results recorded was R. pumilio particularly in the late afternoon with up to four individuals at a time (Fig. 1F). R. pumilio was also recorded in the The number of mature seeds per inflorescence from the open treat- mornings, despite the bait being exhausted. Solitary O. irroratus visited ment was significantly higher than that of the other two treatments the bait station mainly in the late afternoon (16:00 to 17:30), and only (Kruskal–Wallis: H = 14.57, p b 0.01), indicating that autonomous in one instance were two recorded feeding together (Supplementary

Fig. 3. Mean (±1 SD) number of pollen grains found on the snouts of each trapped species. Samples sizes: Rhabdomys pumilio n=19,Otomys irroratus n=2,Crocidura cyanea n=5. C.A. Melidonis, C.I. Peter / South African Journal of Botany 97 (2015) 9–15 13

Fig. 4. Mean (±1 SD) number of pollen grains present in the scats of each species trapped. Samples sizes: Rhabdomys pumilio n = 17, Otomys irroratus n=3,Crocidura cyanea n=5. Homogenous groups were identiﬁed using Mann–Whitney post-hoc pairwise test and are indicated by letters.

Video 3). C. cyanea was recorded in the late afternoon and throughout of this study in which numerous (N70) inflorescences were inspected. the night (Fig. 6, Supplementary Video 4). In addition, a camera trap recorded one very brief visit by a male malachite sunbird (Necatarina famosa)toaP. foliosa inflorescence 3.4. Pollen counts (Supplementary Fig. 2). Attempts to quantify nectar volume and concentration were Mean pollen loads of captured animals were relatively high for thwarted by the gelatinous nature of the nectar observed in small quan- R. pumilio (340.4, range 5 to 1914) and O. irroratus (231.0, range 194 tities in a number of inflorescences. The presence of glucose was con- to 268) and low for C. cyanea (63.4, range 11 to 202) (Fig. 3). No signif- firmed using glucose test strips, evidence that nectar may be the likely icant difference was found between the mean number of pollen grains reward in this species. The inflorescences were noted to have a faint on the rostra of each of the species (Kruskal–Wallis: H =2.31,p = malty scent. 0.31). Mean pollen grains present in the scat of the captured animals were highest for R. pumilio (26.6, range 0 to 164), followed by 4. Discussion C. cyanea (0.8, range 0 to 3) and O. irroratus where no pollen grains were recorded (Fig. 4). An expanded search of the scat samples for Our results support the hypothesis that P. foliosa is rodent-pollinated O. irroratus yielded only two pollen grains in one sample indicating and, unusually, we show that the majority of pollination activity occurs that this species may ingest pollen. The mean number of pollen grains during daylight hours. The presence of pollen grains on the rostra of all found in the scat of R. pumilio individuals was significantly higher than three captured mammal species (Fig. 3) and in their scats, possibly as a the number of pollen grains found in the scat of O. irroratus and result of ‘pollen-preening’ (Turner et al., 2011; Johnson and Pauw, 2014; C. cyanea individuals (H =8.76,P = 0.01). Fig 4), combined with the camera trap data, provide evidence which supports this finding. Exclusion of mammals from inflorescences result- 3.5. Additional observations ed in zero seed set (Fig. 2), suggesting that P. foliosa relies on pollinators for seed set, although sample sizes are small. Our results concur with Numerous ants were seen in the inflorescences as well as a single other studies which found that vertebrate exclusion reduced seed unidentified monkey beetle (Scarabaeidae: Hopliini) over the course set by 95% in P. amplexicaulis and 50% in P. humiflora (Rebelo and

Fig. 5. Timing of all visits by Rhabdomys pumilio to inﬂorescences of Protea foliosa recorded by camera traps (n = 17). 14 C.A. Melidonis, C.I. Peter / South African Journal of Botany 97 (2015) 9–15

Fig. 6. Presence or absence of the three species of mammals at the bait station placed in front of a camera trap over a three-day period.

Breytenbach, 1987) and that pollinators are required for seed produc- compared to continuous video capture or still images in the case of tion in these two species. time-lapse photography. Our finding that R. pumilio is the primary pollinator of P. foliosa is The use of the bait station demonstrated that the camera traps were consistent with other studies (Wiens and Rourke, 1978; Wiens, 1983; effective at night. Since the camera traps were successfully triggered by Kleizen et al., 2008; Biccard and Midgley, 2009; Wester et al., 2009; rodents at night at the bait station site, we conclude that nocturnal pol- Letten and Midgley, 2009; Johnson et al., 2011) that have documented lination is limited in this population. this rodent species as a component of the pollinator assemblages of This study expands our understanding of rodent–flower interac- other petaloid monocots and Cape Protea species. Photographs and tions, showing that at least in some populations only few rodent species video footage (Supplementary Videos 1 and 2) showed that R. pumilio interact with the flowers and it will be interesting to determine if diur- visited flowers in a manner which was non-destructive and which nal visits by the same diurnal animals occur in other populations of resulted in the rodent making contact with the anthers and stigmas. De- P. foliosa. Similarly, it will be interesting to see if other dwarf Protea spe- structive floral feeding by R. pumilio has been shown in other terrarium cies such as Protea tenax occurring in the east of the Fynbos have similar based studies where this and other rodent species have been known to interactions with diurnal mammal pollinators. We show that modified chew off and shred the flower head to obtain the nectar within (Biccard camera traps may be useful in documenting the interactions between and Midgley, 2009; Letten and Midgley, 2009). flowers and large pollinators such as rodents and birds. Importantly, The low occurrence of pollen grains in the scat of O. irroratus and camera traps allow interactions to be viewed in natural settings by un- C. cyanea relative to those of R. pumilio suggests that pollen-preening stressed animals. is reduced in these two species or that absolute pollen loads are lower Supplementary data to this article can be found online at http://dx. resulting in less pollen ingestion. Wester et al. (2009) drew similar con- doi.org/10.1016/j.sajb.2014.12.009. clusions with other rodent species based on their lack of interaction with fl the ower and lack of pollen grains found in their scat. The presence of a Acknowledgements large number of pollen grains in the scat of captured R. pumilio individ- fl uals provides evidence that this species routinely visit P. foliosa owers We thank Peter and Gill Wylie of Wylie's Dairy Farm for permission under natural conditions at this site. to work on their land, Cara-Jayne Thorne and Dylan Pons for the The camera trap data also indicates that the majority of rodent- assistance in the field, Dan Parker for the loan of gutter traps and Tony pollination activity occurs during daylight hours which stands in con- Dold for the assistance in finding populations. The NRF (National Re- trast to a number of other studies which document rodent activity in search Foundation) and Rhodes University are acknowledged for other plant species primarily at night (Johnson et al., 2001; Kleizen funding. Rhodes University ethical clearance number: ZOOL-04-2013. et al., 2008; Wester et al., 2009; Letten and Midgley, 2009; Turner et al., 2011; Lombardi et al., 2013; Johnson and Pauw, 2014). Therefore this would be one of the first examples of primarily diurnal rodent pol- References lination. Johnson et al. (2011) show that R. pumilio is one of the main Beattie, A.J., 1971. A technique for the study of insect-borne pollen. Pan Pac. Entomol. 47, pollinators of C. visseri (Cytinaceae) and R. pumilio is considered to be 82. primarily diurnal or crepuscular (de Graaff, 1981), however they ob- Biccard, A., Midgley, J.J., 2009. Rodent pollination in Protea nana.S.Afr.J.Bot.75,720–725. fl de Graaff, G., 1981. The Rodents of Southern Africa. Butterworths, Durban. served no diurnal visits to the owers despite extensive observations Duffy, K.J., Johnson, S.D., Peter, C.I., 2014. 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