The Role of Beetles in the Pollination of Zamia furfuracea L. fil. (Zamiaceae)

A snout weevil, Rhopalotria mollis Sharp, is found to complete the reproductive phases of its life cycle upon and within male cones of the cycad, Zamia furfuracea. Larvae of this insect feed upon tissues of the male cone, pupate, and emerge as pollen-coated adults after boring through microsporangia and microsporophylls. Mature weevils visit pollen-receptive female cones but are nondestructive to ovules and seeds. Exclusion experiments show that weevils are capable of effecting the pollination of ovules of Z. furfuracea in the absence of airborne pollen. A PREVAILING ASSUMPTION exists that cycads are windpollinated plants. Charles Joseph Chamberlain, the widely recognized authority on cycad phenomena, wrote, "There have been many reports of insect pollination, but in a rather extensive field study in which all the genera have been examined, nothing has been observed which would indicate anything but wind pollination so characteristic of the whole group of gymnosperms" (Chamberlain 1935). He went on to relate that insects were found in, upon, and about male cones at the time of pollination, but considered these to be simply instances of insect predation upon the abundant pollen. Lawson (1926) found nothing to suggest that Bowenia required any agent other than wind for its pollination and remarked that pollination in some cases occurred between plants separated by "a great distance. " Nevertheless, cycad pollination has also been attributed to the agency of insects. Rattray (1913) observed the invasion of male and female cones of Encephalartos by beetles and thought they might have been involved in transfers of pollen from male to female cones. Baird (1938) considered that insects might transport pollen within cones of Macrozamia, but thought that interplant pollen transport required wind. More recently, Breckon and Ortiz (1983) have discussed the apparent pollination of Zamia pumila in Puerto Rico by fungus gnats that hovered about female cones. Niklas and Norstog (1984) have shown that airborne pollen does not preferentially settle on the ovules of some cycad species, and have implicated insects in the pollination of Dioon. Norstog and Stevenson (1980) present circumstantial evidence that some genera and species of cycads may be insect pollinated. They refer to the production of fertile seeds in cones of Z. pumila buried beneath debris in the forest floor, and to the failure of such introduced species as Encephalartos ferox and Dioon spinulosum to produce fertile seeds, even though male and female plants were in close proximity (1-2 m apart). In addition, Norstog and Stevenson (1980) report the presence of snout weevils in both male and female cones of Zamia furfuracea. These weevils were found to live for a time as larvae feeding on the tissues of male cones and to emerge as adults by boring through microsporophylls. In the course of this activity, many microsporangia were disrupted, and the insects emerged coated with pollen. Therefore, weevils would appear to be capable of transferring pollen to ovules. The following report is an extension of our observations. We present experimental evidence supporting the hypothesis that snout weevils may be facultative pollinators of Z. furfuracea. MATERIALS AND METHODS The experiments were, for the most part, done using a group of 40 plants of Zamia furfuracea L. fil. (Fairchild Tropical Garden Accession No. 66-341), grown from seeds of a plant collected in Mexico, and planted along the north wall of the Wm. J. Robbins research building at Fairchild Tropical Garden (FTG) (Fig. IA). The location is a sheltered one and not generally subjected to strong air currents. Eighteen female plants are interspersed I Received 11 April 1985, revision accepted 22 August 1985. 300 BIOTROPICA 18(4): 300-306 1986 This content downloaded from 157.55. 39.132 on Thu, 15 Sep 2016 04:56:24 UTC All use subject to http://about.jstor. org/terms FIGURE 1. Pollination of Z. furfuracea. A. Planting of Z. furfuracea at base of north wall of Win. J. Robbins building, Fairchild Tropical Garden; a similar planting, to viewer's right, is not induded in this photograph. B. Female cones (larger) and male cones (smaller). To viewer's right, male cones (arrows) bear a number of copulating weevils. Bar = 10 cm. C. Scanning electron micrograph of snout weevil, R. mollits Sharp. Bar = 0.5 mm. D. Rhopalotria copulating on surfaces of male cones. Bar = 1 cm. E. Weevil exit holes (arrows) in ends of microsporophylls of male cones. Bar = 1 cm. F. Pollen-receptive female cone; a vertical opening (arrow) between adjacent megasporophylls permits access of pollen and pollinators. Bar = 1 cm. The Role of Beetles in Zamia furfuracea Pollination 301 This content downloaded from 157.55. 39.132 on Thu, 15 Sep 2016 04:56:24 UTC All use subject to http://about.jstor. org/terms afriong the male plants, and both male and female cones (Fig. 1B) are usually well hidden among the fronds. Voucher specimens are deposited at FTG. Exclosure experiments were used to discriminate between wind and weevil pollination. Some female cones were covered with mesh bags (nylon marquisette) tied around the cone peduncles with rubber bands. (Megasporophylls of female cones become separated, usually by a vertical crack, before pollen receptivity [Fig. IFi; therefore, bagging or other treatments were done before the separation of megasporophyll to eliminate the possibility that they had already been pollinated.) The openings in the nylon mesh measured 0.6 mm across, somewhat less than the cross-sectional diameter of the suspected pollinator. We also tried other materials, including cheesecloth and cloth bags, but settled upon nylon mesh because it afforded the best possibility for insect exclusion yet permitting air transport of pollen. It should be noted, however, that when weevil-laden male cones were placed in a mesh-covered beaker, some weevils escaped through the mesh openings (ca 100 weevils were present in each cone). Nevertheless, we thought the mesh would bar the chance entry of weevils. If, on the other hand, weevils were strongly attracted to female cones, undoubtedly some might penetrate the mesh. (The possibility exists that other insects, such as ants or gnats, might also be active in pollination of Z. furfuracea, but we saw no evidence of this.) Some female cones were covered with plastic bags in order to discover if, in the absence of pollination, ovules might develop by apomixis. Other female cones were covered with cups made by cutting the mouth ends from lightweight plastic bottles. When these cups were inverted over young female cones, the cups projected approximately 5 cm below the lowermost sporophylls. We thought these devices would permit insect visitation but reduce the probability of airborne pollination. To further test this premise, detached, cup-covered cones were placed in a wind tunnel, exposed to pollen blown past at 3.2, 1. 5, and 0.5 m/sec, and pollen impact points were noted. Lastly, a number of cones were left uncovered in order to determine pollination success and fertility under "natural" conditions. The control cones were interspersed among the experimental ones. The experiments were run during a 2-month period (une and July 1982), but were monitored until January 1983, when the cones were dissected and seeds and abortive ovules counted. Two-tailed t-tests were calculated to determine significances of differences between the treatments and controls. The weevil (Fig. IC), which we suspect is the pollinator of Z. furfuracea, has been tentatively identified as Rhopalotria mollis Sharp, a Mexican form (R. E. Woodruff, pers. comm.). One of us (DWS) has found the same, or similar, snout weevils in male cones of Z. furfuracea and its close relative, Zamia loddigesii, growing in their native habitats in Mexico. In plantings of cycads at FTG, we have observed R. mollis only in Z. furfuracea and in an experimental hybrid produced by pollination of Zamia spartea with pollen of Z. furfuracea (Norstog, pers. obs.). A similar weevil, Rhopalotria slossoni Schaef. , occurs in Florida in male cones of Z. pumila, both in plantings and in nature. In this case, however, the role of the weevil in pollination does not seem quite so clear as that of R. mollis in Z. furfuracea, in part because another small beetle, Pharaxontha zamiae, also is consistently present in male cones of Z. pumila and may also be a pollinator (W. Tang, pers. comm.). We have not observed R. slossoni or P. zamiae in cones of Z. furfuracea, nor has R. mollis been found in cones of Z. pumila (W. Tang, pers.