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The Reproductive Biology of the Invasive Ferns Lygodium Microphyllum and L American Journal of Botany 90(8): 1144±1152. 2003. THE REPRODUCTIVE BIOLOGY OF THE INVASIVE FERNS LYGODIUM MICROPHYLLUM AND L. JAPONICUM (SCHIZAEACEAE): IMPLICATIONS FOR INVASIVE POTENTIAL1 MICHAEL S. LOTT,2 JOHN C. VOLIN,2 ROBERT W. P EMBERTON,3 AND DANIEL F. A USTIN4 2Department of Biological Sciences, Florida Atlantic University, 2912 College Avenue, Davie, Florida 33314 USA; 3Invasive Plant Research Laboratory, USDA-Agricultural Research Service, 3205 College Avenue, Ft. Lauderdale, Florida 33314 USA; and 4Arizona±Sonora Desert Museum, 2021 N. Kinney Road, Tucson, Arizona 85743 USA The effect of culture system and population source on sexual expression and sporophyte production was examined for two invasive fern species in Florida, USA, Lygodium microphyllum and L. japonicum (Schizaeaceae). Both species are currently spreading through Florida. Long-distance dispersal of ferns is thought to rely on successful intragametophytic sel®ng. Given the rate of spread observed in both Lygodium species, we hypothesized that both species are capable of intragametophytic sel®ng. To test this hypothesis, game- tophytes of both species were grown in vitro as isolates, pairs, and groups. Both species were capable of intragametophytic sel®ng; 78% of L. microphyllum isolates produced sporophytes and over 90% of the L. japonicum isolates produced sporophytes. Lygodium microphyllum also displayed the ability to reproduce via intergametophytic crossing, facilitated by an antheridiogen pheromone. Spo- rophyte production was rapid across mating systems for both species, an advantage in Florida's wet and dry seasonal cycles. The high intragametophytic sel®ng rate achieved by both species has likely facilitated their ability to colonize and spread through Florida. The mixed mating system observed in L. microphyllum appears to give this species the ability to invade distant habitats and then adapt to local conditions. Key words: Florida; invasive species; Lygodium; reproductive biology; Schizaeaceae; sel®ng. Homosporous ferns have two free-living generations: a hap- less mature gametophytes (e.g., Hamilton and Lloyd, 1991; loid gametophyte and a diploid sporophyte. Because homo- Hau¯er and Welling, 1994). sporous ferns have bisexual gametophytes, intragametophytic This study examines mating systems in L. microphyllum sel®ng (i.e., the union of egg and sperm from the same ga- (Cav.) R. Br. (Schizaeaceae) and L. japonicum (Thunb.) metophyte) was long held to be an important mode of repro- Swartz. The genus Lygodium is relatively small, comprised of duction in populations of homosporous ferns (Soltis et al., up to 40 species, including one, L. palmatum (Bernh.) Sw., 1988). However, in controlled growth studies to examine re- native to North America (Pemberton, 1998). Lygodium is productive strategies in homosporous ferns, only a few species mostly found in tropical regions of the world. The native range had high intragametophytic sel®ng rates (e.g., Crist and Farrar, of L. microphyllum extends into moist habitats throughout the 1983; Korpelainen, 1996, 1997). The majority of studied fern tropical Old World. Lygodium japonicum also has a large na- species reproduce through intergametophytic crossing (Hed- tive range occurring in both temperate and tropical Asia (Pem- rick, 1987; Soltis and Soltis, 1992; Korpelainen and Kolkkala, berton, 1998). 1996; Hooper and Hau¯er, 1997). Mixed mating has only been Both species have a climbing habit and are nonindigenous observed in a few species, including Onoclea sensibilis (Kle- and invasive in Florida, USA. Currently, L. microphyllum is kowski, 1982) and Dryopteris expansa (Soltis and Soltis, expanding its range in southern Florida, while L. japonicum 1987). Therefore, both intragametophytic sel®ng and outcross- is expanding its range in northern Florida (Schmitz et al., ing may represent stable mating systems in homosporous ferns 1997; Pemberton and Ferriter, 1998). For example, the total (e.g., Crist and Farrar, 1983; Peck et al., 1990; Korpelainen, area infested by L. microphyllum was estimated to have ex- 1996). In addition, homosporous ferns have evolved both mor- panded from approximately 11 200 hectares in 1993 to ap- phological (e.g., asynchronous maturation of gametophytes) proximately 43 300 hectares in 1999 (Pemberton and Ferriter, and physiological mechanisms (e.g., the pheromone antheri- 1998; A. Ferriter, South Florida Water Management District, diogen) to promote outcrossing (e.g., Tryon and Vitale, 1977; personal communication). Both species are capable of smoth- Hau¯er and Welling, 1994). Antheridiogens are pheromones ering and displacing native understory vegetation, and in ex- that promote outcrossing in fern gametophytes (e.g., DoÈpp, treme infestations, shrub and canopy vegetation. This is par- 1950; Hau¯er and Welling, 1994). These compounds are typ- ticularly notable in L. microphyllum, which can form rachis ically secreted by meristematic female gametophytes and trig- mats up to a meter thick, effectively eliminating most under- ger precocious antheridial formation on neighboring smaller, story vegetation. Several reproductive life history characteristics in plants have been proposed that may facilitate the greater competitive 1 Manuscript received 9 January 2003; revision accepted 25 March 2003. ability of nonindigenous plant species, such as self- or wind The authors thank Dr. Dianne Owen for assistance with the statistical anal- yses and Allison Snow for her help in the laboratory and ®eld. This research pollination (fertilization), rapid growth to reproductive age or was supported by grants from the Florida Department of Environmental Pro- size, high and continuous seed (spore) production, adaptations tection and the South Florida Water Management District. for short- and long-distance seed (spore) or vegetative dis- 1144 August 2003] LOTTETAL.ÐREPRODUCTIVE BIOLOGY AND INVASIVE POTENTIAL 1145 Fig. 1. Location of collection sites of spores of Lygodium microphyllum and L. japonicum in Florida, USA. persal, and vegetative as well as sexual reproduction (Baker, in June and October 2000. Fertile fronds of L. microphyllum were collected 1974; Newsome and Noble, 1986; Roy, 1990; Reichard and from Jonathan Dickinson State Park and the Big Cypress Seminole Indian Hamilton, 1997; Sakai et al., 2001). In homosporous ferns, the Reservation, located in Martin and Hendry counties, respectively, Florida, ability to reproduce through intragametophytic sel®ng pro- USA (Fig. 1). Lygodium japonicum fronds were collected from Suwannee motes long-distance dispersal (Crist and Farrar, 1983; Peck et River Water Management District land in Suwannee County and at the Ala®a al., 1990). As discussed by Peck et al. (1990), spores trans- River Corridor Preserve in Hillsborough County (Fig. 1). Fertile fronds were ported long distances would be unlikely to establish gameto- collected from at least four individual plants from each population. phytes in close enough proximity to allow for intergameto- Fronds of both species were stored in sealed plastic bags and brought back phytic sel®ng or crossing. Therefore, long-distance dispersal to the laboratory. The bags were opened and stored at ambient temperatures and colonization may be dependent upon the successful estab- and allowed to dry for several weeks, allowing the spores to be released. Each lishment of sporophytes by single spores. This ability to re- bag was kept separated from the others to prevent cross contamination. After produce through intragametophytic sel®ng would promote the the spores were released, they were sieved to remove leaf material. Following naturalization of introduced fern species, such as Lygodium. sieving, spores were sterilized in a 1% bleach solution and rinsed in sterile, Both Lygodium species are unusual among ferns in Florida distilled water. While in solution, the spores were sown with a pipette onto in that they can climb into tree canopies. Lygodium micro- 100 3 20 mm plastic petri dishes containing modi®ed Parker/Thompson's phyllum, in particular, has been observed overtopping tree can- basal nutrient medium, containing both macro- and micronutrients, and solid- opies among tree islands in the Arthur R. Marshall Loxahatch- i®ed with 1% agar (Klekowski, 1969). The petri dishes were placed in a growth chamber under cool-white ¯uorescent illumination of approximately ee National Wildlife Refuge, Boynton Beach, Florida. This 22 21 vine-like growth should theoretically promote the long-dis- 100 mmol´m ´s photosynthetic photon ¯ux with a photoperiod of 13/11 tance dispersal of these species because spores released at or hours and a temperature of 258/208C, light/dark, respectively. After approxi- above the tree canopy could potentially be carried a consid- mately 14 d, individual and pairs of asexual gametophytes were transferred erable distance by prevailing winds. Given these factors, we using a dissecting microscope and a scalpel onto fresh medium in 65 3 10 have hypothesized that both Lygodium species are capable of mm plastic petri dishes. intragametophytic sel®ng. Experimental designÐTo investigate the reproductive biology of both Ly- MATERIALS AND METHODS godium species, a series of experiments was conducted. Experiments 1±3 were Plant materialÐFertile fronds from L. microphyllum were collected in the designed to test the three potential mating types, intragametophytic sel®ng, ®eld in October 1999 and May 2000, and L. japonicum fronds were collected intergametophytic sel®ng, and intergametophytic crossing. A fourth experi-
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