Fragment production and recruitment ecology of the red alga Laurencia poiteaui in Florida Bay, USA
Highlights
► Laurencia poiteaui was the principal species in the fragment pool near Long Key. ► Fragmentation is an efficient life-history strategy for Laurencia poiteaui. ► Most fragments were small (< 6 cm), healthy, and proficient at attaching. ► Fragments with and without terminal apical tips had similar attachment success. ► Rapid attachment coupled with slow dispersal rates suggests local recruitment.
Introduction
Several species of Laurencia inhabit the patchy seagrass habitat of southeastern Florida Bay (Chiappone and Sullivan, 1994, Wick, 2002, Zieman et al., 1989). High abundance and the benthic drift lifestyle of Laurencia spp. benefit a diversity of marine organisms in these relatively calm waters by providing: 1) productive nursery habitat (Childress and Herrnkind, 1994, Davis and Dodrill, 1989, Forcucci et al., 1994, Fourqurean and Robblee, 1999, Herrnkind and Butler, 1994, Holmquist, 1994, Marx and Herrnkind, 1985a, Marx and Herrnkind, 1985b), 2) post-larval metamorphic cues and shelter to the economically important queen conch Strombus gigas and the Caribbean spiny lobster Panuliris argus (Davis and Stoner, 1994, Davis et al., 1990, Herrnkind and Butler, 1994), and 3) a primary mode of dispersal and food source for many fishes and invertebrates, especially brooders and organisms with short planktonic life-history stages (Holmquist, 1994, Stoner and Livingston, 1980).
The benthic drift lifestyle of one of the most ubiquitous species of Laurencia in Florida Bay, Laurencia poiteaui (Lamouroux) Howe, is not commonly seen on coral and sabellariid wormrock reefs in central and south Florida and is likely advantageous for this population. Smaller individuals, perhaps those able to drift easily with the current, tend to epiphytize other benthic organisms in Florida Bay (Frankovich and Fourquean, 1997, Humm, 1964, Wick, 2002). In 2001, L. poiteaui was documented to epiphytize most (70%) of the benthic macroalgae and sponges in Florida Bay near Long Key (Wick, 2002). One reason for the abundance of both drift and secondarily attached forms of this species in Florida Bay is its ability to reproduce via vegetative fragmentation (Cruz-Adames and Ballantine, 1996, Josselyn, 1975, Josselyn, 1977, Wick, 2002).
Vegetative fragmentation, the ability of algal fragments separated from the adult thallus to settle, secondarily attach, and grow as a clone, is an important reproductive strategy commonly used by marine macroalgae (Cecere et al., 2011, Kilar and McLachlan, 1986, Smith and Walters, 1999, Walters et al., 2002). Many species capable of fragmenting, or cloning, are particularly efficient at establishing new locations through rapid attachment rates and fragment longevity (Ceccherelli and Piazzi, 2001, Kilar and McLachlan, 1986). These include the well-known examples of algal invasions like the green alga Caulerpa taxifolia in the Mediterranean Sea, which was later introduced to California and Australia (Ceccherelli and Cinelli, 1999, Walters, 2009); Caulerpa brachypus, a Pacific native, which has increasingly been documented on several of the artificial and natural reefs in south Florida (Lapointe and Bedford, 2009); Hypnea musciformis, a red alga that was intentionally introduced to O'ahu from Florida for commercial purposes in 1974 (Doty, 1961, Russell 1992, Steneck and Carlton, 2001); and Acanthophora spicifera, a red alga found throughout the Hawaiian Islands thought to arrive as a passenger on a fouled ship hull from Guam in 1950 (Doty, 1961). In the Florida Keys, efficient cloners tend to persist throughout the year at relatively high abundances, such as Dictyota spp. along the reef tract and Laurencia spp. in Florida Bay (Beach et al., 2003, Herren et al., 2006, Walters and Beach, 2000, Wick, 2002, Zieman et al., 1989).
Although known to reproduce sexually in Quintana Roo, Mexico (Fujii et al., 1996), Josselyn, 1975, Josselyn, 1977 documented vegetative fragmentation to be the primary mode of dispersal of L. poiteaui in Card Sound, FL, northeast of Florida Bay. This species maintains continuous vegetative growth and fragmentation, but exceptionally warm water temperatures weaken the thallus and promote higher rates of fragmentation during the summer months (Biebl, 1962, Josselyn, 1977, Kilar and McLachlan, 1986, Thorhaug, 1971). The high summer fragmentation rates are followed by late summer and early fall rain events conveying land-based sources of nutrients to the phosphorus-limited waters of Florida Bay (Boyer et al., 1999, Fourqurean et al., 1993, Humm, 1964, Lapointe et al., 1992). Nutrient inputs were shown to play an important role in the growth, survival, and photosynthetic performance of drifting fragments by Vermeij et al. (2009). Lapointe (1989) also reported that L. poiteaui collected in the nearby Content Keys had high capacities for the phosphorus-extracting enzyme alkaline phosphatase and that its growth was stimulated with phosphorus enrichment. Following the flush of land-based nutrient associated with the wet season, the water temperatures in south Florida cool to the optimal temperature range (20–25 °C) for growth in this species (Thorhaug, 1971). Thus, if summer-generated fragment survivorship is high, then fragments have several months to re-attach and start vegetative growth during the fall when phosphorus inputs increase, water temperatures drop, and growth rates increase again.
Over time, the process of vegetative fragmentation can influence population structure and dynamics (Cecere et al., 2011, Coffroth and Lasker, 1998). Fragments, which are genetically identical to the parent thalli, may: 1) help reduce the chances of genotypic mortality (Coffroth and Lasker, 1998), 2) survive unpredictable environmental changes that are potentially lethal to the entire thalli, and 3) have a better likelihood of reaching new habitats and increasing local populations; potentially making fragmenting species more competitive than algal species that have not evolved this life-history strategy (Cecere et al., 2011). Although fragmentation has been documented as an important life-history trait in the genus Laurencia (Cecere et al., 2011, Cruz-Adames and Ballantine, 1996, Josselyn, 1975, Josselyn, 1977), little research has been conducted to understand the recruitment process of these fragments in the field. Consequently, the focus of this study was to better understand fragment: 1) accumulation rates, 2) variability, 3) dispersal distances, and 4) attachment rates.
Section snippets
Study location and study organism
Research was conducted at the Florida Institute of Oceanography's Keys Marine Laboratory (KML), located on Long Key, in June and July 2000 and 2001. Laboratory experiments were performed in continuously running outdoor seawater tables supplied by water drawn from Florida Bay immediately adjacent to KML. Because of the close proximity of the field study site to KML, the salinity and the temperature of the water in the experimental seawater tables and the field site were similar. Field
Fragment accumulation and variability
The algal fragment pool was comprised primarily of L. poiteaui in both July 2000 (63.1%) and July 2001 (51.7%; Table 1). The mean number of fragments collected/day/m2 (± S.E.) was statistically similar (ANOVA: F = 2.49, p = 0.13) in July 2000 (2.7 ± 3.3) and July 2001 (4.1 ± 0.9).
Most fragments of L. poiteaui were < 6 cm long (80.0% in 2000, 77.4% in 2001; Fig. 2). Although there was no significant difference (ANOVA: F = 0.05, p = 0.82) in the mean fragment length (± S.E.) in July 2000 (4.3 cm ± 0.3) and 2001
Fragment accumulation and variability
Water temperature and nutrients are strongly correlated with fragmentation and vegetative growth in L. poiteaui (Biebl, 1962, Josselyn, 1977, Lapointe, 1989, Thorhaug, 1971, Vermeij et al., 2009). This cyclical process starts with high fragmentation rates during the warm summer months (Josselyn, 1977), followed by exposure to land-based nutrients during the late summer/early fall wet season (Lapointe, 1989), and finally vegetative growth during the cool, dry months (Josselyn, 1977 and Thorhaug,
Conclusions
In conclusion, warm water temperatures, low water motion in Florida Bay, high rates of fragmentation, high fragment survival, and rapid attachment rates collectively suggest that vegetative fragmentation is an efficient life-history strategy for L. poiteaui. Most fragments of L. poiteaui were small (< 6 cm), healthy, and proficient at attaching to the benthos. In the field, rapid attachment success coupled with slow dispersal rates suggests local recruitment. L. poiteaui was the principal species
Acknowledgments
Funding for this research was provided by Florida Sea Grant, NOAA National Undersea Research Center, Florida Institute of Oceanography, University of Central Florida, and the University of Tampa. Dorothy Byron and Julie Liss dedicated countless hours of field and laboratory assistance. Richard Herren, Heidi Borgeas, Nicole Robinson, and the scientists and staff at the Florida Institute of Oceanography's Keys Marine Laboratory, especially Kevin McCarthy and Chris Humphrey, also provided
References (59)
- et al.
The impact of Dictyota spp. on Halimeda populations of Conch Reef, Florida Keys
J. Exp. Mar. Biol. Ecol.
(2003) - et al.
Trophic cues induce metamorphosis of queen conch larvae (Stombus gigas Linnaeus)
J. Exp. Mar. Biol. Ecol.
(1994) - et al.
Process influencing water column nutrients characteristics and phosphorus limitation of phytoplankton biomass in Florida Bay, FL, USA: inferences from spatial distributions
Estuar. Coast. Shelf Sci.
(1993) Benthic macroalgae as a dispersal mechanism for fauna: influence of a marine tumbleweed
J. Exp. Mar. Biol. Ecol.
(1994)Seasonal changes in the distribution and growth of Laurencia poitei (Rhodophyceae, Ceramiales) in a subtropical lagoon
Aquat. Bot.
(1977)- et al.
Ecological studies of the alga, Acanthophora spicifera (Vahl) Borg. (Ceramiales: Rhodophyta): vegetative fragmentation
J. Exp. Mar. Biol. Ecol.
(1986) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments
J. Exp. Mar. Biol. Ecol.
(2000)- et al.
Factors affecting the distribution of Himanthalia elongata (L.) S. F. Gray on the Northeast coast of England
Estuar. Coast. Mar. Sci.
(1973) - et al.
An experimental assessment of survival, re-attachment and fecundity of coral fragments
J. Exp. Mar. Biol. Ecol.
(1999) - et al.
Asexual propagation in the coral reef macroalga Halimeda (Chlorophyta, Bryopsidales): production, dispersal and attachment of small fragments
J. Exp. Mar. Biol. Ecol.
(2002)
Epibiotic traits of the invasive red seaweed Acanthophora spicifera in La Paz Bay, South Baja California (Eastern Pacific)
Mar. Ecol.
Temperaturresistenz tropischer Meeresalgen
Bot. Mar.
Fragments of Dictyota: Growth, Generation Forces and Entanglement/Attachment to Reef Organisms in the Florida Keys
Seasonal and long-term trends in the water quality of Florida Bay (1989–1997)
Estuaries
Cascading disturbances in Florida Bay, USA: cyanobacteria blooms, sponge mortality, and implications for juvenile spiny lobsters Panulirus argus
Mar. Ecol. Prog. Ser.
The role of vegetative fragmentation in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean
Mar. Ecol. Prog. Ser.
Dispersal of Caulerpa racemosa fragments in the Mediterranean: lack of detachment time effect on establishment
Bot. Mar.
How the unattached form of Acanthophora nayadiformis (Rhodophyta: Ceramiales) produces storage and perennating organs
J. Mar. Biol. Assoc. U. K.
Vegetative reproduction by multicellular propagules in Rhodophyta: an overview
Mar. Ecol.
Ecological structure and dynamics of nearshore hard-bottom communities in the Florida Keys
Bull. Mar. Sci.
The behavior of juvenile Caribbean spiny lobster in Florida Bay: seasonality, ontogeny and sociality
Bull. Mar. Sci.
Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance
Evolution
Asexual reproduction in Laurencia poiteaui (Rhodomelaceae, Rhodophyta)
Bot. Mar.
Recreational fishery and population dynamics of spiny lobsters, Panulirus argus, in Florida Bay, Everglades National Park, 1977–1980
Bull. Mar. Sci.
A comparison of two inducers, KCl and Laurencia extracts, and techniques for the commercial scale induction of metamorphosis in queen conch Strombus gigas Linnaeus, 1758 larvae
J. Shellfish. Res.
Effects of sediments on the development of Macrocystis pyrifera gametophytes
Mar. Biol.
Acanthophora, a possible invader of the marine flora of Hawaii
Pac. Sci.
Population dynamics of juvenile Caribbean spiny lobster, Panulirus argus, in Florida Bay, Florida
Bull. Mar. Sci.
Florida Bay: a history of recent ecological changes
Estuaries
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