scientific correspondence

Pollen transfer on birds tongues

lants are adapted for pollination by birds in diverse and intricate ways. Here I describe an extraordinary example of these adaptations. The flowers of Microloma sagittatum, a member of the milkweed family, clip parcels of pollen precisely onto the tongues of sunbirds. The pollen parcels are carried inside the birds mouth to the next flower where they are detached mechanically. This is, to the best of my knowledge, the first evidence for pollen transfer on the tongues of birds, a phenomenon that might be more widespread. Typical members of the cosmopolitan milkweed family (Asclepiadaceae) have their pollen contained in five removable parcels called pollinaria. Each pollinarium consists of two pollen-filled sacs and a mechanical clip, the corpusculum, for attachment to nectar-feeding insects. The corpusculum has a microscopic groove on one side, which catches on a bristle or other fine appendage on the body of an insect1. All documented cases of pollination in the milkweed family are by insects2. Although it is a member of the milkweed family, the common South African climber M. sagittatum has many characteristics suggestive of bird pollination. Like many bird-pollinated flowers, and unlike typical insect-pollinated flowers3, the flowers of M. sagittatum are red in colour, secrete copious quantities of dilute nectar and are odourless at all times of day. The flowers also have the unusual characteristic of remaining in a bud-like state with the petals twisted together. The only access into the flower is through five tiny slit-like pores that insects would be unable to find or stretch open. Despite observations of sunbirds visiting Microloma flowers4, previous investigators1,47 assumed insect pollination in M. sagittatum and structurally similar flowers because birds seemed to lack a suitable site for the attachment of the minutely grooved corpusculum4. However, no specific pollinator has previously been identified for M. sagittatum. I recorded visitors to the flower on 17 days and early evenings at three locations on the west coast of South Africa. No insects were seen on the flowers of M. sagittatum. Instead, lesser double-collared sunbirds (Nectarinia chalybea) were frequent visitors throughout the day (3.9 visits per plant per hour). A feeding bird probes the reinforced pores at the top the flower with the sharp tip of its bill and extends its tongue into the bottom of the flower to reach the nectar (Fig. 1a). By using flannel jackets to temporarily restrain mistnet-captured sunbirds8, I was

able to examine them under a dissecting microscope in the field, and discovered the pollinaria of M. sagittatum attached to the sunbirds tongues (Fig. 1b). The tongue is tough and flexible, and rolled up lengthways from both sides to form twin capillary

tubes through which the nectar is drawn9. At its tip the tongue bifurcates and frays, and it is onto these frayed edges that the corpusculi become attached (Fig. 1c, d). Suitable sites for the attachment of the pollinaria can also be found on the tongues of

Figure 1 Mechanism of pollen attachment to bird tongues. a, A female lesser double-collared sunbird (Nectarinia chalybea) systematically sips nectar from the flowers of Microloma sagittatum. Visits to a flowering plant lasted 21 17 s (n 43) with sunbirds probing 2.3 0.6 flowers per s (n 21). Plants bore 298 219 flowers (n 8). Flowers contained 0.61 1.14 l of nectar at sunrise, which decreased to 0.07 0.24 l after 6 h of sunbird activity (n 36). When birds were excluded using gauze bags, nectar volumes reached 14.2 6.8 l (n 19). The nectar contained 23.6 1.15 % sugar in sucrose equivalents (n 7). Scale bar, 1 cm. b, The frayed tip of the tongue (white) of N. chalybea, with two attached pollinaria (yellowbrown) from the flowers of M. sagittatum. Each pollinarium consists of a corpusculum (brown) and two pollen sacs (yellow). Scale bar, 100 m. c, Detail of a pollinarium showing the groove in the corpusculum attached to the edge of the tongue. Scale bar, 20 m. d, Cross- section through the lower quarter of the flower. Outgrowths on the petals (o) guide the tongue down bristle-lined channels (b) that lead to the nectar. When the tongue is withdrawn, the bristles push it against the anthers (a) so that one of the frayed edges of the tongue is introduced into the guide rail (g). The guide rail leads into the narrowing groove of the corpusculum (above the level of sectioning), which attaches onto the tongue. The corpusculum, with two attached pollen sacs (p), is drawn up into the birds mouth. When a bird visits the next flower with a pollinarium attached to its tongue, the row of bristles orientates the flattened pollen sac so it slides with its narrow edge into the guide rail, becomes wedged and breaks free from the clip as the tongue is withdrawn. Colours are near-natural; s, stigma; c, calyx. Scale bar, 250 m.

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New World hummingbirds and Australian honeyeaters9. Seven out of eight captured sunbirds were carrying pollinaria or partial pollinaria on their tongues, with up to four corpusculi attached at a time (median number of corpusculi per bird, 2; median number of pollen sacs per bird, 0.5). The frequent presence of corpusculi with only one or neither of their two pollen sacs attached suggests that pollen sacs were transferred successfully to other flowers. As expected from the high levels of flower visitation, a large proportion (54%) of flowers were found to be pollinated (n 48). Three times more pollen sacs were removed (2.90 2.74 per flower) than reinserted (0.96 1.01; n 48), indicating substantial losses during transfer. Seed pod production is high in plants exposed to sunbirds, whereas bagged (pollinator excluded) flowers set no seeds (n 119). A captive sunbird was used to test whether sunbirds successfully transfer pollen sacs to the intricate pollen-receiving mechanism (Fig. 1d). I exposed 37 virgin M. sagittatum flowers to the bird for a period of two minutes per flower. There were no insects in the cage. Dissection showed that the 37 experimental flowers received 39 pollen sacs, indicating that sunbirds effectively both collect and deliver pollen sacs. Plants adapted for pollen transfer on bird tongues are characterized by having: (1) tough and streamlined pollinaria with a mechanical clip; (2) morphology that excludes insects; (3) reddish coloration; (4) copious, dilute nectar; and (5) no scent. Applying these criteria to the rest of the genus Microloma5, I predict that six of the nine remaining species are pollinated in the manner described here. Outside Africa, many members of the large southeast Asian genus Dischidia 10 are among other plants that may be adapted for pollen transfer on the tongues of birds. Anecdotal accounts of sunbirds, hummingbirds and honeyeaters visiting the flowers of several genera of Asclepiadaceae2 beg investigation.
Anton Pauw
Department of Botany, University of Cape Town, Private Bag, Rondebosch 7701, Cape Town, South Africa e-mail: pauw@botzoo.uct.ac.za
1. Kunze, H. Plant Syst. Evol. 176, 227253 (1991). 2. Ollerton, J. & Liede, S. Biol. J. Linn. Soc. 62, 593610 (1997). 3. Faegri, K. & van der Pijl, L. The Principles of Pollination Ecology. (Pergamon, Oxford, 1979). 4. Vogel, S. Bot. Stud. 1, 1338 (1954). 5. Bruyns, P. & Linder, H. P. Bot. Jahrb. Syst. 112, 453527 (1991). 6. Wanntorp, H. E. Opera Bot. 98, 169 (1988). 7. Marloth, R. The Flora of South Africa, Vol. 3 (Darter, Cape Town, 1932). 8. Kearns, C. A. & Inouye, D. W. Techniques for Pollination Biologists (Univ. Press of Colorado, Niwot, 1993). 9. Paton, D. C. & Collins, B. G. Aust. J. Ecol. 14, 473506 (1989). 10. Rintz, R. E. Blumea 26, 81126 (1980).

A proxy index of ENSO teleconnections

Variations in central and eastern equatorial sea surface temperatures are linked to extratropical climate changes by atmospheric heat and moisture fluxes in so-called teleconnection patterns1,2. Estimates of sea surface temperature (SST) anomaly may be derived from the isotopic composition and minor-element chemistry of aragonite formed by annually banded reef corals. Here we reconstruct anomalies in central equatorial Pacific SSTs for 193893 from the stable oxygen isotope (18O) composition of a coral collected at Kiritimati (Christmas) Island, Republic of Kiribati (157.3 W, 2 N). We recover not only the regional anomaly in SST, but also extratropical climate information in climatically teleconnected regions. Interannual variability in the 18O composition of aragonite is a function of the temperature of the sea surface in which the coral secretes its skeleton3. This variability in coral 18O also records any changes in the 18O of sea water, which may be significant in some oceanographic settings4.
a
Coral O (s.d. units) 4 3 2 1 0 1 2 3

The strontium-to-calcium (Sr/Ca) ratio in corals is also a function of SST, but seawater Sr/Ca variability is minimal5,6. Application of these two proxies in tandem has been used to estimate both seawater 18O and SST anomalies during the 198283 El NioSouthern Oscillation (ENSO) event from measurements made on Great Barrier Reef corals7. In principle, paired Sr/Ca and 18O data from a series of temporally overlapping coral cores may yield proxy estimates of SST and seawater 18O variability extending well into the preinstrumental period. At Kiritimati, seasonal SST varies by 1.2 C, whereas ENSO-induced SST anomalies of 3 C reflect changes in wind stress and associated equatorial upwelling8. Thus, Kiritimati is an ideal location at which to monitor the thermal oceanographic signal associated with the full ENSO cycle. We measured 18O and carbon isotopic (13C) composition in a core from a living coral, collected in March 1994, at intervals of 0.5 mm along the maximal growth axis of the coral. We used the 13C record to construct an age model for analysis of the 18O record over time, on the basis of observations of the dependence of 13C levels in coralline aragonite on coralline reproductive

b
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Figure 1 Kiritimati coral proxy data. a, Kiritimati coral 18O time series normalized to the 195180 mean and standard deviation of the data. The 18O scale has been reversed for direct comparison with SST anomalies (b). Vertical error bars give uncertainty in 18O measurements (2) and horizontal error bars give decadal averages of age-model uncertainty in units of year/age-model year10. s.d. units, standard deviation units. b, Kiritimati coral 18O anomalies ( , relative to the Pee Dee Belemnite (PDB) isotopic standard) and Sr/Ca anomalies (mmol mol1) relative to the mean for the 198187 period. Reproducibility confidence intervals (estimated 2) for each tracer are as indicated. Also plotted are estimates of SST anomalies from the analysis by Reynolds and Smith14 for the 22 grid box encompassing Kiritimati. The data have been plotted on a common range so that direct comparisons of the different measurements may be made: 8 C 1.6 in 18O 0.6 mmol mol1 in Sr/Ca3,6. c, Plot of NINO-C and N INO3 indices (SST anomalies averaged over 15090 W, 5 N to 5 S) against time. Also shown are the numbers of samples analysed per year and of SST observations per year. Correlation between N INO-C and NINO3 is 0.79.

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