Anther cap retention prevents self-pollination by elaterid beetles in the South African orchid Eulophia foliosa

Abstract

Background and aims: Pollination by insects that spend long periods visiting many flowers on a plant may impose a higher risk of facilitated self-pollination. Orchids and asclepiads are particularly at risk as their pollen is packaged as pollinia and so can be deposited on self-stigmas en masse. Many orchids and asclepiads have adaptations to limit self-deposition of pollinia, including gradual reconfiguration of pollinaria following removal. Here an unusual mechanism--anther cap retention--that appears to prevent self-pollination in the South African orchid Eulophia foliosa is examined.

Methods: Visits to inflorescences in the field were observed and pollinators collected. Visitation rates to transplanted inflorescences were compared between a site where putative pollinators were abundant and a site where they were rare. Anther cap retention times were determined for removed pollinaria and atmospheric vapour pressure deficit was recorded concurrently. Anther cap anatomy was examined using light microscopy.

Key results: Eulophia foliosa is pollinated almost exclusively by Cardiophorus obliquemaculatus (Elateridae) beetles, which remain on the deceptive inflorescences for on average 301 s (n = 18). The anther cap that covers the pollinarium is retained for an average of 512 s (n = 24) after pollinarium removal by beetles. In all populations measured, anther cap dimensions are greater than those of the stigmatic cavity, thus precluding the deposition of self-pollinia until after the anther cap has dropped. An anatomical investigation of this mechanism suggests that differential water loss from regions of the anther cap results in opening of the anther cap flaps. This is supported by observations that as atmospheric vapour pressure deficits increased, the duration of anther cap retention was reduced.

Conclusions: Flowers of E. foliosa are specialized for pollination by elaterid beetles. Retention of anther caps for a period exceeding average visit times by beetles to inflorescences appears to prevent facilitated self-pollination in E. foliosa effectively.

Fig. 1.

Eulophia foliosa occurs in large populations in grasslands throughout the eastern parts of South Africa (A). The inflorescences are crowded with many apple-green flowers (B). In most populations inspected, numerous Cardiophorus obliquemaculatus (Elateridae) clickbeetles (G) were found visiting the inflorescences (C–F). Occasionally at higher altitude sites in KwaZulu-Natal we observed the much larger Atricelaphinis tigrina (Cetoniinae) visiting the inflorescences and removing the pollinaria (H). Scale bars = A, 100 mm; B, 20 mm; C–F, H, 5 mm; G, 1 mm.

Fig. 2.

Distribution of Eulophia foliosa in South Africa. Study sites include (1) Vernon Crookes Nature Reserve, (2) Camperdown, (3) Wahroonga, (4) Himeville Nature Reserve, (5) Sani Pass (all in KwaZulu-Natal) and (6) Dassie Kranz near Grahamstown in the Eastern Cape Province. Additional observations of Cardiophorus obliquemaculatus visiting E. foliosa inflorescences were made at (7) Ugie as well as Pevensy and a site east of Underberg (both indicated by point 8). Increasing altitudes are shown in darker shades of grey. Scale bar = 100 km.

Fig. 3.

Anther cap retention time decreases with increasing vapour pressure deficit (VPD), which describes the gradient of water vapour from the cells to the atmosphere. VPD is calculated from ambient temperature and relative humidity. Pollinaria were orientated in a moderate breeze of approx. 0·4 m s⁻¹ to reduce boundary layer conditions around the pollinarium. Two outliers are from one specific plant and are excluded from the regression (n = 21). Dotted line indicates the average visit times of Cardiophorus obliquemaculatus to inflorescences.

Fig. 4.

View of the proximal (rostellum side) of a pollinarium removed from the flower on the head of an insect pin. (A) Pollinarium with anther cap in place—‘flaps’ of the anther cap (arrowheads) enclose the pollinarium in the anther cap. (B) Anther cap ‘flaps’ begin to open, (C) anther cap ‘flaps’ completely open and (D) anther cap blown off 9 min after removal, exposing the pollinia for deposition. Scale bar = 0·5 mm.

Fig. 5.

(A) Anatomy of Eulophia foliosa anther cap and pollinia (p) in cross-section while still attached to the column (c). The anther cap is made up of both thick-walled (tk) and two zones of thin-walled (tn) cells. One zone of thin-walled, lightly stained cells marks the abscission layer of the anther cap from the column (tn₁); the second zone is a band of cells along the distal margin of the anther cap relative to the rest of the column (tn₂). (B) Cross-section of an anther cap dropped from the pollinarium following its natural opening sequence. Arrows are as explained in the text. Scale bar = 250 µm.