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Observation of fruit production by the seagrass Halodule wrightii in the northeastern Gulf of Mexico
Aquatic Botany 87 (2007) 247–250 www.elsevier.com/locate/aquabot
Short communicationery
Observation of fruit production by the seagrass Halodule wrightii in the northeastern Gulf of Mexico Tamara M. McGovern *, Katherine Blankenhorn Dauphin Island Sea Lab, 101 Bienville Blvd, Dauphin Island, AL 36528, United States Received 30 October 2006; received in revised form 9 May 2007; accepted 15 May 2007 Available online 13 June 2007
Abstract Halodule wrightii is a highly clonal, dioecious seagrass with a wide geographic range. Though sexual reproduction has been observed in other areas of its range, we report here the first documented case of fruit production in the northeastern Gulf of Mexico. We also report on seasonal patterns of growth and biomass allocation in this region and discuss the implications of even occasional sexual reproduction for the population dynamics of this species. # 2007 Elsevier B.V. All rights reserved. Keywords: Fruit; Growth; Gulf of Mexico; Halodule wrightii; Seagrass; Sexual reproduction
1. Introduction Seagrasses are important ecosystem components in marine systems around the world (reviewed in Hemminga and Duarte, 2000). The seagrass Halodule wrightii is widely distributed, its range including the Indo Pacific, the Caribbean Sea, the Gulf of Mexico and the Atlantic as far north as North Carolina (reviewed in Ferguson et al., 1993). Though five species of sea grasses have been reported in the northeastern Gulf of Mexico (Eleuterius, 1987), H. wrightii and Ruppia maritima are the only two commonly observed in the Mobile Bay region where salinities are low (personal observations). Like most seagrasses (Duarte and Sand-Jensen, 1990; Hemminga and Duarte, 2000; Olesen et al., 2004; Rasheed, 2004), H. wrightii is highly clonal, extending and maintaining perennial beds through the growth of underground rhizomes. Sexual reproduction has been documented in other areas of its range. H. wrightii is dioecious (Ferguson et al., 1993) and flowering and/or fruit production have been observed in Texas (McMillan, 1976), the Caribbean (Johnson and Williams, 1982) and North Carolina (Ferguson et al., 1993). The past establishment of sexual recruits is also suggested by recent investigations of population structure in
* Corresponding author. Present address: Department of Biological Sciences, 132 Long Hall, Clemson University, Clemson, SC 29634-0326, United States. Tel.: +1 864 656 2638; fax: +1 864 656 0435. E-mail address: [email protected] (T.M. McGovern). 0304-3770/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2007.05.004
Texas (Angel, 2002; Travis and Sheridan, 2006) and south Florida (Angel, 2002). In this paper we report the first known observation of fruit production by H. wrightii in the northeastern Gulf of Mexico (the Alabama waters of the Mississippi Sound) and also present information on seasonal patterns of growth and biomass allocation. 2. Methods H. wrightii was collected from the western side of Pointe aux Pines, Alabama, a peninsula extending southward into Mississippi Sound west of Mobile Bay. We collected 4–8 samples on a bi-weekly basis from late February through mid September, 2006. Samples were collected using a 6 in. diameter PVC corer inserted to a depth of approximately 15 cm. Sediment was removed by sieving through a 1 mm mesh screen and samples were stored in seawater in resealable bags. Samples not processed immediately were frozen and stored at 80 8C. In the lab, we separated the above-ground (leaves) and below-ground (roots and rhizomes) fractions of the plants. Extraneous material (sediment, epifauna, shells) was removed from the roots and rhizomes, and leaves were scraped as necessary to remove epiphytes. Plant material was dried at 70 8C for a minimum of 48 h until a stable mass was obtained. When fruiting plants were found, the leaves and roots associated with the fruiting shoots were dried and weighed separately from non-fruiting shoots.
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T.M. McGovern, K. Blankenhorn / Aquatic Botany 87 (2007) 247–250
Fig. 1. Seasonal trend in biomass/m2 of Halodule wrightii. Open bars represent the biomass of roots and rhizomes, hatched bars represent the biomass of leaves, and solid bars represent reproductive biomass. Error bars represent standard errors and asterisks indicate months in which developing fruit was observed.
3. Results The total biomass of H. wrightii generally increased through late summer, then began to decline (Fig. 1). The proportion of that mass comprising roots and rhizomes generally declined from a high level in mid spring while the proportion comprising leaves generally increased (Fig. 2). The mass of below-ground structures was always greater than that of above-ground structures. Flowers were never detected, but our first observation of developing fruit (Fig. 3A and B) was in late June and we found developing fruit on three more occasions, including our last sampling trip in mid September (Fig. 1). Developing fruit was observed in 6 (or 8.0%) of the 75 total samples. The average biomass associated with reproduction in those samples (including roots and leaves attached to fruiting shoots as well as the fruits themselves) was 7.0% (range: 0.7–25.4%). The biomass of fruit alone (minus the leaves and roots associated with fruiting shoots) in the 6 samples averaged 3.8% of the total biomass (range: 0.03–13.1%). We calculated reproductive effort (RE) as the mass associated with fruit divided by total above-ground biomass in each sample (Kaldy and Dunton,
Fig. 3. (A) Photograph of developing fruit attached to rhizome and shoot. (B) Connected ramets with developing fruit.
2000). For the 6 samples in which we observed fruit, mean RE was 9.9% (0.8–30.2%, S.D. = 11.2%). Mean RE across all 75 samples was 0.7% (S.D. = 3.8%). We did not count the number of shoots, and therefore cannot calculate changes in shoot density or the proportion of shoots bearing fruit, but in the few samples with fruit, fruit-producing shoots tended to be connected (i.e. ramets of the same genet, Fig. 3B). 4. Discussion
Fig. 2. Seasonal trend of the proportion of biomass in roots and rhizomes (solid circles) and leaves (open squares). Shown are standard error bars.
As H. wrightii began to grow in the spring, there was a relative decline in the proportion of overwintering structures (roots and rhizomes) as the biomass associated with leaves increased. The proportion of biomass devoted to below-ground structures averaged across sampling dates (67%) was similar to other published reports (Pulich, 1985; Dunton, 1990) and never averaged below 54% on any given date. We never observed flowers, but other reports suggest that flowering commences in early spring in the Caribbean (Johnson and Williams, 1982) and in late spring in more northerly portions of the range (McMillan, 1976; Eleuterius, 1987; Ferguson et al., 1993). We observed developing fruit in four sampling periods in late June through mid September. Ferguson et al. (1993) observed
T.M. McGovern, K. Blankenhorn / Aquatic Botany 87 (2007) 247–250
fruit developing by the end of July in North Carolina. Our earlier observation of developing fruit may reflect an earlier start to the growing season and an earlier onset of flowering in Alabama since growth (Pulich, 1985) and flowering (McMillan, 1976, 1982) have both been tied to water temperature. Based on our observations of the biomass associated with fruiting and the number of samples with fruiting plants, sexual reproduction in H. wrightii in the Mobile Bay region appears to be uncommon and occurs at low density. Other studies on H. wrightii suggest that this may not be the case in all areas of its range. Johnson and Williams (1982) reported that flowering and fruit production in H. wrightii are a ‘‘widespread annual event’’ in the Caribbean. McMillan (1976) reported abundant flowering of H. wrightii in Texas, though neither the reproductive biomass nor proportion of flowering shoots are reported, so what is meant by ‘abundant’ is unclear. Ferguson et al. (1993) report widespread flowering of H. wrightii in North Carolina (at 14 of 16 sites), but they likewise do not present data on flower density or reproductive biomass within a site, so reproductive allocation is impossible to gauge. Studies on other species report that, similar to our observations, sexual reproduction may occur in a small, highly variable percentage of plants (Duarte et al., 1997; Inglis and Lincoln Smith, 1998; Kaldy and Dunton, 2000; Balestri, 2004), though some species and some regions are notable exceptions (e.g. Johnson and Williams, 1982; Durako and Moffler, 1987; Dunton, 1990). The low incidence and spatial patchiness of reproduction has been attributed to a variety of ‘‘local environmental and genetic factors’’ (Balestri, 2004) including clone-specific attributes (Durako and Moffler, 1987). Low reproductive allocation may reflect resource limitation since sexual reproduction is nutrient intensive (Walker et al., 2004; Gobert et al., 2005). Alternatively, low levels of fruiting could result from low pollination success. Pollination may be limited due to a low density of flowers (Reusch, 2003; Vermaat et al., 2004), restricted pollen dispersal (Ackerman, 2002) or the clonal nature of H. wrightii populations that may restrict pollination to peripheral clonemates (Handel, 1985). Though there are no genetic studies of clonal structure in H. wrightii beds in the northeastern Gulf of Mexico, the presence of developing fruits in Mississippi Sound indicates that there are multiple clones in the sampled population—at least one female and one male since H. wrightii is dioecious (Ferguson et al., 1993). Because pollen is released at the or near the sediment surface (Ferguson et al., 1993) and pollen movement is predicted to be restricted within the canopy (Ackerman, 2002), these instances of successful pollination suggest that clones are located within close proximity of one another. The presence of developing fruits also confirms that, even if sexual reproduction is not common in this region, H. wrightii may occasionally produce sexual progeny. The genetic heterogeneity of populations with ongoing sexual recruitment may increase the resistance of the seagrass community to disturbance (Hughes and Stachowicz, 2004) and stress (Williams, 2001). The production of potentially dispersive progeny (i.e. seeds) also makes possible the colonization of new and distant areas and the natural re-colonization of extinct beds
249
(Duarte and Sand-Jensen, 1990; Hemminga and Duarte, 2000; Olesen et al., 2004; Rasheed, 2004). Such colonization potential is an important attribute for a species increasingly under threat. Acknowledgements We would like to thank the staff of the Dauphin Island Sea Lab for material support and Stan Bosarge in particular for help taking photographs. This research was supported by a grant from the U.S. Environmental Protection Agency’s Science to Achieve Results (STAR) program through the Alabama Center for Estuarine Studies. The work here has not been subjected to any EPA review and therefore does not necessarily reflect the views of the Agency, and no official endorsement should be inferred. References Ackerman, J.D., 2002. Diffusivity in a marine macrophyte canopy: implications for submarine pollination and dispersal. Am. J. Bot. 89, 1119–1127. Angel, R., 2002. Genetic diversity of Halodule wrightii using random amplified polymorphic DNA. Aquat. Bot. 74, 165–174. Balestri, E., 2004. Flowering of the seagrass Posidonia oceanica in a northwestern Mediterranean coastal area: temporal and spatial variations. Mar. Biol. 145, 61–68. Duarte, C.M., Sand-Jensen, K., 1990. Seagrass colonization: patch formation and patch growth in Cymodocea nodosa. Mar. Ecol. Prog. Ser. 65, 193–200. Duarte, C.M., Uri, J.S., Agawin, N.S.R., Fortes, M.D., Vermaat, J.E., Marba, N., 1997. Flowering frequency of Philippine seagrasses. Bot. Mar. 40, 497–500. Dunton, K.H., 1990. Production ecology of Ruppia maritima L. s.l. and Halodule wrightii Aschers, in two subtropical estuaries. J. Exp. Mar. Biol. Ecol. 143, 147–164. Durako, M.J., Moffler, M.D., 1987. Factors affecting the reproductive ecology of Thalassia testudinum (Hydrocharitaceae). Aquat. Bot. 27, 79–95. Eleuterius, L.N., 1987. Seagrass ecology along the coasts of Alabama, Louisiana, and Mississippi. Fla. Mar. Res. Publ. 42, 11–24. Ferguson, R.L., Pawlak, B.T., Wood, L.L., 1993. Flowering of the seagrass Halodule wrightii in North Carolina, USA. Aquat. Bot. 46, 91–98. Gobert, S., Lejeune, P., Lepoint, G., Bouquegneau, J.M., 2005. C, N, P concentrations and requirements of flowering Posidonia oceanica shoots. Hydrobiologia 533, 253–350. Handel, S.N., 1985. The intrusion of clonal growth patterns on plant breeding systems. Am. Nat. 125, 367–384. Hemminga, M.A., Duarte, C.M., 2000. Seagrass Ecology. Cambridge University Press, Cambridge. Hughes, A.R., Stachowicz, J.J., 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl. Acad. Sci. 101, 8998– 9002. Inglis, G.J., Lincoln Smith, M.P., 1998. Synchronous flowering of estuarine seagrass meadows. Aquat. Bot. 60, 37–48. Johnson, E.A., Williams, S.L., 1982. Sexual reproduction in seagrasses: reports for five Caribbean species with details for Halodule wrightii Ashers. and Syringodium filiforme Kutz. Carib. J. Sci. 18, 61–70. Kaldy, J.E., Dunton, K.H., 2000. Above- and below-ground production, biomass and reproductive ecology of Thalassia testudinum (turtle grass) in a subtropical coastal lagoon. Mar. Ecol. Prog. Ser. 193, 272–283. McMillan, C., 1976. Experimental studies on flowering and reproduction in seagrasses. Aquat. Bot. 2, 87–92. McMillan, C., 1982. Reproductive physiology of tropical seagrasses. Aquat. Bot. 14, 245–258.
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T.M. McGovern, K. Blankenhorn / Aquatic Botany 87 (2007) 247–250
Olesen, B., Marba`, N., Duarte, C.M., Savela, R.S., Fortes, M.D., 2004. Recolonization dynamics in a mixed seagrass meadow: The role of clonal versus sexual processes. Estuaries 27, 770–780. Pulich, W.M., 1985. Seasonal growth dynamics of Ruppia maritima L. s.l. and Halodule wrightii Aschers. in southern Texas and evaluation of sediment fertility status. Aquat. Bot. 23, 53–66. Rasheed, M.A., 2004. Recovery and succession in a multi-species tropical seagrass meadow following experimental disturbance: the role of sexual and asexual reproduction. J. Exp. Mar. Biol. Ecol. 310, 13–45. Reusch, T.B.H., 2003. Floral neighbourhoods in the sea: how floral density, opportunity for outcrossing and population fragmentation affect seed set in Zostera marina. J. Ecol. 91, 610–615.
Travis, S.E., Sheridan, P., 2006. Genetic structure of natural and restored shoalgrass Halodule wrightii populations in the NW Gulf of Mexico. Mar. Ecol. Prog. Ser. 322, 117–127. Vermaat, J.E., Rollon, R.N., Lacap, C.D.A., Billot, C., Alberto, F., Nacorda, H.M.E., Wiegman, F., Terrados, J., 2004. Meadow fragmentation and reproductive output of the SE Asian seagrass Enhalus acoroides. J. Sea Res. 52, 321–328. Walker, D.I., Campey, M.L., Kendrick, G.A., 2004. Nutrient dynamics in two seagrass species, Posidonia coriacea and Zostera tasmanica, on Success Banks, Western Australia. Est. Coast. Shelf Sci. 60, 251–260. Williams, S.L., 2001. Reduced genetic diversity in eelgrass transplantations affects both population growth and individual fitness. Ecol. Appl. 11, 1472– 1488.
Short communicationery
Observation of fruit production by the seagrass Halodule wrightii in the northeastern Gulf of Mexico Tamara M. McGovern *, Katherine Blankenhorn Dauphin Island Sea Lab, 101 Bienville Blvd, Dauphin Island, AL 36528, United States Received 30 October 2006; received in revised form 9 May 2007; accepted 15 May 2007 Available online 13 June 2007
Abstract Halodule wrightii is a highly clonal, dioecious seagrass with a wide geographic range. Though sexual reproduction has been observed in other areas of its range, we report here the first documented case of fruit production in the northeastern Gulf of Mexico. We also report on seasonal patterns of growth and biomass allocation in this region and discuss the implications of even occasional sexual reproduction for the population dynamics of this species. # 2007 Elsevier B.V. All rights reserved. Keywords: Fruit; Growth; Gulf of Mexico; Halodule wrightii; Seagrass; Sexual reproduction
1. Introduction Seagrasses are important ecosystem components in marine systems around the world (reviewed in Hemminga and Duarte, 2000). The seagrass Halodule wrightii is widely distributed, its range including the Indo Pacific, the Caribbean Sea, the Gulf of Mexico and the Atlantic as far north as North Carolina (reviewed in Ferguson et al., 1993). Though five species of sea grasses have been reported in the northeastern Gulf of Mexico (Eleuterius, 1987), H. wrightii and Ruppia maritima are the only two commonly observed in the Mobile Bay region where salinities are low (personal observations). Like most seagrasses (Duarte and Sand-Jensen, 1990; Hemminga and Duarte, 2000; Olesen et al., 2004; Rasheed, 2004), H. wrightii is highly clonal, extending and maintaining perennial beds through the growth of underground rhizomes. Sexual reproduction has been documented in other areas of its range. H. wrightii is dioecious (Ferguson et al., 1993) and flowering and/or fruit production have been observed in Texas (McMillan, 1976), the Caribbean (Johnson and Williams, 1982) and North Carolina (Ferguson et al., 1993). The past establishment of sexual recruits is also suggested by recent investigations of population structure in
* Corresponding author. Present address: Department of Biological Sciences, 132 Long Hall, Clemson University, Clemson, SC 29634-0326, United States. Tel.: +1 864 656 2638; fax: +1 864 656 0435. E-mail address: [email protected] (T.M. McGovern). 0304-3770/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2007.05.004
Texas (Angel, 2002; Travis and Sheridan, 2006) and south Florida (Angel, 2002). In this paper we report the first known observation of fruit production by H. wrightii in the northeastern Gulf of Mexico (the Alabama waters of the Mississippi Sound) and also present information on seasonal patterns of growth and biomass allocation. 2. Methods H. wrightii was collected from the western side of Pointe aux Pines, Alabama, a peninsula extending southward into Mississippi Sound west of Mobile Bay. We collected 4–8 samples on a bi-weekly basis from late February through mid September, 2006. Samples were collected using a 6 in. diameter PVC corer inserted to a depth of approximately 15 cm. Sediment was removed by sieving through a 1 mm mesh screen and samples were stored in seawater in resealable bags. Samples not processed immediately were frozen and stored at 80 8C. In the lab, we separated the above-ground (leaves) and below-ground (roots and rhizomes) fractions of the plants. Extraneous material (sediment, epifauna, shells) was removed from the roots and rhizomes, and leaves were scraped as necessary to remove epiphytes. Plant material was dried at 70 8C for a minimum of 48 h until a stable mass was obtained. When fruiting plants were found, the leaves and roots associated with the fruiting shoots were dried and weighed separately from non-fruiting shoots.
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T.M. McGovern, K. Blankenhorn / Aquatic Botany 87 (2007) 247–250
Fig. 1. Seasonal trend in biomass/m2 of Halodule wrightii. Open bars represent the biomass of roots and rhizomes, hatched bars represent the biomass of leaves, and solid bars represent reproductive biomass. Error bars represent standard errors and asterisks indicate months in which developing fruit was observed.
3. Results The total biomass of H. wrightii generally increased through late summer, then began to decline (Fig. 1). The proportion of that mass comprising roots and rhizomes generally declined from a high level in mid spring while the proportion comprising leaves generally increased (Fig. 2). The mass of below-ground structures was always greater than that of above-ground structures. Flowers were never detected, but our first observation of developing fruit (Fig. 3A and B) was in late June and we found developing fruit on three more occasions, including our last sampling trip in mid September (Fig. 1). Developing fruit was observed in 6 (or 8.0%) of the 75 total samples. The average biomass associated with reproduction in those samples (including roots and leaves attached to fruiting shoots as well as the fruits themselves) was 7.0% (range: 0.7–25.4%). The biomass of fruit alone (minus the leaves and roots associated with fruiting shoots) in the 6 samples averaged 3.8% of the total biomass (range: 0.03–13.1%). We calculated reproductive effort (RE) as the mass associated with fruit divided by total above-ground biomass in each sample (Kaldy and Dunton,
Fig. 3. (A) Photograph of developing fruit attached to rhizome and shoot. (B) Connected ramets with developing fruit.
2000). For the 6 samples in which we observed fruit, mean RE was 9.9% (0.8–30.2%, S.D. = 11.2%). Mean RE across all 75 samples was 0.7% (S.D. = 3.8%). We did not count the number of shoots, and therefore cannot calculate changes in shoot density or the proportion of shoots bearing fruit, but in the few samples with fruit, fruit-producing shoots tended to be connected (i.e. ramets of the same genet, Fig. 3B). 4. Discussion
Fig. 2. Seasonal trend of the proportion of biomass in roots and rhizomes (solid circles) and leaves (open squares). Shown are standard error bars.
As H. wrightii began to grow in the spring, there was a relative decline in the proportion of overwintering structures (roots and rhizomes) as the biomass associated with leaves increased. The proportion of biomass devoted to below-ground structures averaged across sampling dates (67%) was similar to other published reports (Pulich, 1985; Dunton, 1990) and never averaged below 54% on any given date. We never observed flowers, but other reports suggest that flowering commences in early spring in the Caribbean (Johnson and Williams, 1982) and in late spring in more northerly portions of the range (McMillan, 1976; Eleuterius, 1987; Ferguson et al., 1993). We observed developing fruit in four sampling periods in late June through mid September. Ferguson et al. (1993) observed
T.M. McGovern, K. Blankenhorn / Aquatic Botany 87 (2007) 247–250
fruit developing by the end of July in North Carolina. Our earlier observation of developing fruit may reflect an earlier start to the growing season and an earlier onset of flowering in Alabama since growth (Pulich, 1985) and flowering (McMillan, 1976, 1982) have both been tied to water temperature. Based on our observations of the biomass associated with fruiting and the number of samples with fruiting plants, sexual reproduction in H. wrightii in the Mobile Bay region appears to be uncommon and occurs at low density. Other studies on H. wrightii suggest that this may not be the case in all areas of its range. Johnson and Williams (1982) reported that flowering and fruit production in H. wrightii are a ‘‘widespread annual event’’ in the Caribbean. McMillan (1976) reported abundant flowering of H. wrightii in Texas, though neither the reproductive biomass nor proportion of flowering shoots are reported, so what is meant by ‘abundant’ is unclear. Ferguson et al. (1993) report widespread flowering of H. wrightii in North Carolina (at 14 of 16 sites), but they likewise do not present data on flower density or reproductive biomass within a site, so reproductive allocation is impossible to gauge. Studies on other species report that, similar to our observations, sexual reproduction may occur in a small, highly variable percentage of plants (Duarte et al., 1997; Inglis and Lincoln Smith, 1998; Kaldy and Dunton, 2000; Balestri, 2004), though some species and some regions are notable exceptions (e.g. Johnson and Williams, 1982; Durako and Moffler, 1987; Dunton, 1990). The low incidence and spatial patchiness of reproduction has been attributed to a variety of ‘‘local environmental and genetic factors’’ (Balestri, 2004) including clone-specific attributes (Durako and Moffler, 1987). Low reproductive allocation may reflect resource limitation since sexual reproduction is nutrient intensive (Walker et al., 2004; Gobert et al., 2005). Alternatively, low levels of fruiting could result from low pollination success. Pollination may be limited due to a low density of flowers (Reusch, 2003; Vermaat et al., 2004), restricted pollen dispersal (Ackerman, 2002) or the clonal nature of H. wrightii populations that may restrict pollination to peripheral clonemates (Handel, 1985). Though there are no genetic studies of clonal structure in H. wrightii beds in the northeastern Gulf of Mexico, the presence of developing fruits in Mississippi Sound indicates that there are multiple clones in the sampled population—at least one female and one male since H. wrightii is dioecious (Ferguson et al., 1993). Because pollen is released at the or near the sediment surface (Ferguson et al., 1993) and pollen movement is predicted to be restricted within the canopy (Ackerman, 2002), these instances of successful pollination suggest that clones are located within close proximity of one another. The presence of developing fruits also confirms that, even if sexual reproduction is not common in this region, H. wrightii may occasionally produce sexual progeny. The genetic heterogeneity of populations with ongoing sexual recruitment may increase the resistance of the seagrass community to disturbance (Hughes and Stachowicz, 2004) and stress (Williams, 2001). The production of potentially dispersive progeny (i.e. seeds) also makes possible the colonization of new and distant areas and the natural re-colonization of extinct beds
249
(Duarte and Sand-Jensen, 1990; Hemminga and Duarte, 2000; Olesen et al., 2004; Rasheed, 2004). Such colonization potential is an important attribute for a species increasingly under threat. Acknowledgements We would like to thank the staff of the Dauphin Island Sea Lab for material support and Stan Bosarge in particular for help taking photographs. This research was supported by a grant from the U.S. Environmental Protection Agency’s Science to Achieve Results (STAR) program through the Alabama Center for Estuarine Studies. The work here has not been subjected to any EPA review and therefore does not necessarily reflect the views of the Agency, and no official endorsement should be inferred. References Ackerman, J.D., 2002. Diffusivity in a marine macrophyte canopy: implications for submarine pollination and dispersal. Am. J. Bot. 89, 1119–1127. Angel, R., 2002. Genetic diversity of Halodule wrightii using random amplified polymorphic DNA. Aquat. Bot. 74, 165–174. Balestri, E., 2004. Flowering of the seagrass Posidonia oceanica in a northwestern Mediterranean coastal area: temporal and spatial variations. Mar. Biol. 145, 61–68. Duarte, C.M., Sand-Jensen, K., 1990. Seagrass colonization: patch formation and patch growth in Cymodocea nodosa. Mar. Ecol. Prog. Ser. 65, 193–200. Duarte, C.M., Uri, J.S., Agawin, N.S.R., Fortes, M.D., Vermaat, J.E., Marba, N., 1997. Flowering frequency of Philippine seagrasses. Bot. Mar. 40, 497–500. Dunton, K.H., 1990. Production ecology of Ruppia maritima L. s.l. and Halodule wrightii Aschers, in two subtropical estuaries. J. Exp. Mar. Biol. Ecol. 143, 147–164. Durako, M.J., Moffler, M.D., 1987. Factors affecting the reproductive ecology of Thalassia testudinum (Hydrocharitaceae). Aquat. Bot. 27, 79–95. Eleuterius, L.N., 1987. Seagrass ecology along the coasts of Alabama, Louisiana, and Mississippi. Fla. Mar. Res. Publ. 42, 11–24. Ferguson, R.L., Pawlak, B.T., Wood, L.L., 1993. Flowering of the seagrass Halodule wrightii in North Carolina, USA. Aquat. Bot. 46, 91–98. Gobert, S., Lejeune, P., Lepoint, G., Bouquegneau, J.M., 2005. C, N, P concentrations and requirements of flowering Posidonia oceanica shoots. Hydrobiologia 533, 253–350. Handel, S.N., 1985. The intrusion of clonal growth patterns on plant breeding systems. Am. Nat. 125, 367–384. Hemminga, M.A., Duarte, C.M., 2000. Seagrass Ecology. Cambridge University Press, Cambridge. Hughes, A.R., Stachowicz, J.J., 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl. Acad. Sci. 101, 8998– 9002. Inglis, G.J., Lincoln Smith, M.P., 1998. Synchronous flowering of estuarine seagrass meadows. Aquat. Bot. 60, 37–48. Johnson, E.A., Williams, S.L., 1982. Sexual reproduction in seagrasses: reports for five Caribbean species with details for Halodule wrightii Ashers. and Syringodium filiforme Kutz. Carib. J. Sci. 18, 61–70. Kaldy, J.E., Dunton, K.H., 2000. Above- and below-ground production, biomass and reproductive ecology of Thalassia testudinum (turtle grass) in a subtropical coastal lagoon. Mar. Ecol. Prog. Ser. 193, 272–283. McMillan, C., 1976. Experimental studies on flowering and reproduction in seagrasses. Aquat. Bot. 2, 87–92. McMillan, C., 1982. Reproductive physiology of tropical seagrasses. Aquat. Bot. 14, 245–258.
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T.M. McGovern, K. Blankenhorn / Aquatic Botany 87 (2007) 247–250
Olesen, B., Marba`, N., Duarte, C.M., Savela, R.S., Fortes, M.D., 2004. Recolonization dynamics in a mixed seagrass meadow: The role of clonal versus sexual processes. Estuaries 27, 770–780. Pulich, W.M., 1985. Seasonal growth dynamics of Ruppia maritima L. s.l. and Halodule wrightii Aschers. in southern Texas and evaluation of sediment fertility status. Aquat. Bot. 23, 53–66. Rasheed, M.A., 2004. Recovery and succession in a multi-species tropical seagrass meadow following experimental disturbance: the role of sexual and asexual reproduction. J. Exp. Mar. Biol. Ecol. 310, 13–45. Reusch, T.B.H., 2003. Floral neighbourhoods in the sea: how floral density, opportunity for outcrossing and population fragmentation affect seed set in Zostera marina. J. Ecol. 91, 610–615.
Travis, S.E., Sheridan, P., 2006. Genetic structure of natural and restored shoalgrass Halodule wrightii populations in the NW Gulf of Mexico. Mar. Ecol. Prog. Ser. 322, 117–127. Vermaat, J.E., Rollon, R.N., Lacap, C.D.A., Billot, C., Alberto, F., Nacorda, H.M.E., Wiegman, F., Terrados, J., 2004. Meadow fragmentation and reproductive output of the SE Asian seagrass Enhalus acoroides. J. Sea Res. 52, 321–328. Walker, D.I., Campey, M.L., Kendrick, G.A., 2004. Nutrient dynamics in two seagrass species, Posidonia coriacea and Zostera tasmanica, on Success Banks, Western Australia. Est. Coast. Shelf Sci. 60, 251–260. Williams, S.L., 2001. Reduced genetic diversity in eelgrass transplantations affects both population growth and individual fitness. Ecol. Appl. 11, 1472– 1488.