Description
Agarophyton vermiculophyllum (formerly known as Gracilaria vermiculophylla) was originally described from Japan. The genera Gracilaria and Gracilariopsis are extraordinarily difficult morphologically, and molecular analyses are resulting in extensive revisions of their taxonomy and distribution (Gurgel and Frederiq 2004; Belorin et al. 2005; Rueness 2005). Gurgel and Frederiq (2004) identified a cylindrical red alga from Hog Island Bay, VA (initially identified as Gracilaria verrucosa, Thomsen 1998), as Gracilaria 'aff. tenuistipitata', using molecular methods. Rueness (2005) made an extensive molecular and morphological comparison of European invasive Gracilaria with Japanese species and identified the invasive plants as G. vermiculophylla. He also identified G. 'aff. tenuistipitata' from Virginia and California as probably also 'G. vermiculophylla', though reproductive structures were not available for morphological identification. DNA analyses of invasive Gracilariales from North Carolina have also identifed the species as A. vermiculophyllum (Freshwater et al. 2006). Further molecular studies (mitochondrial DNA) confirm that the dominant cylindrical from of Gracilaria-type seaweed in Hog Island Bay is A. vermiculophyllum, identical to specimens from Europe and Korea (Thomsen et al. 2005).
Taxonomy
| Kingdom | Phylum | Class | Order | Family | Genus |
|---|---|---|---|---|---|
| Protista | Rhodophyta | Rhodophyceae | Gigartinales | Gracilariaceae | Agarophyton |
Synonyms
Invasion History
Chesapeake Bay Status
| First Record | Population | Range | Introduction | Residency | Source Region | Native Region | Vectors |
|---|---|---|---|---|---|---|---|
| 1998 | Established | Expanding | Introduced | Regular Resident | Western Pacific | Western Pacific | Fisheries (Oysters-Accidental); Shipping (Ballast water; Fouling Community); |
History of Spread
Agarophyton vermiculophyllum is a red alga native to northwest Pacific, including the coasts of Japan, Korea, China, and Vietnam, (Guiry and Guiry 2005; Rueness 2005)). Algae of the family Gracilariales are widely cultured as a source of agar (Israel et al. 1999; Rueness 2005), and many references to their physiology and growth characteristics are available in "Biological Abstracts". The species of this family>are extraordinarily difficult morphologically, and molecular analyses are resulting in extensive revisions of their taxonomy and distribution (Gurgel and Frederiq 2004; Belorin et al. 2005; Rueness 2005; Freshwater et al. 2006, Saunders 2009, Sfriso et al. 2012, and Nettleton et al. 2013; Gurgel et al. 2018). Since 2000, A. vermiculophyllum has been identified from the Eastern Pacific, near Ensenada, Mexico (Bellorin et. al. 2004), Elkhorn Slough, California (Rueness 2005) and British Columbia (Saunders 2009), from the Northeast Atlantic, from Sweden to Spain (Rueness 2005), and from the Northwest Atlantic, from South Carolina to Virginia, Rhode Island, and New Hampshire (Gurgel and Frederiq 2004; Rueness 2005; Freshwater et al. 2006; Nettleton et al. 2013; Saunders 2009; Tyler et al. 2005). Some of the invasion sites in Europe and North Ameirca were near areas where Crassostrea gigas, the Pacific Oyster, was cultivated (Rueness 2005).
Agarophyton vermiculophyllum was probably introduced to the Atlantic Coast of North America some time before the year 2000. The earliest collection reported, so far, was from Hog Island Bay (identified as 'G. aff.tenuistipitata) , on the Atlantic Coast of Virginia in 1998 (Gurgel and Frederiq 2004; Thomsen and McGlathery 2006). In 2000, in Masonboro Sound NC, 'Gracilaria' sp. was reported fouling nets and covering intertidal mudflats. By 2002, it was causing problems in powerplants in the Cape Fear estuary, and was distributed over a wide salinity range (Thompson 2002, personal communication) and reports of the fouling of fishing gear were becoming widespread (North Carolina Sea Grant 2005; Freshwater et al. 2006) By 2004, it ranged from the south side of Cape Fear (Brunswick County) to Beaufort and Bogue Sound, Carteret County, NC (Freshwater et al. 2006). The vectors of introduction to the Northwest Atlantic are not clear. Few transplants of Pacific oysters (C. gigas) were made in this region. During World War II, extensive aquaculture of a Gracilaria-type alga was undertaken in the North Carolina sounds. The species was later found to be an undescribed native alga, Graciliaria hummi (Hommersand and Freshwater 2009),. More likely, this alga could have been introduced by ballast water or fouling. Recent genetic analysis supports Pacific Oyster introductions as the likely vector (Krueger-Hadfield et al. 2017).
Recent papers and molecular identifications have extended the range of A. vermiculophyllum to the north and south. Many early collections were overlooked, and identified as the native G. tikvahiae. Agarophyton vermiculophyllum was collected on the north and south sides of Cape Cod MA, as early as 200, and found in Great Bay NH in 2003 (Nettleton et al. 2013). To the south it was found to be abudant in estuaries in SC and GA (Byers et al. 2012).
In Hog Island Bay, just north of the mouth of the Chesapeake Bay, Agarophyton vermiculophyllum was collected in 1999 (Gurgel and Frederiq 2004). Large blooms of Gracilaria sp. had been observed in recent years (Tyler et al. 2005; Thomsen et al. 2005). This alga has also been collected in Chesapeake Bay proper, but the extent of its distribution and abundance is still being studied (James Norris, Department of Botany, USNMNH, personal communication). It is abundant in parts of the York River, near Gloucester Point (Falls 2008).This alga appears well-adapted for estuarine habitats, growing at 5-50 ppt, and growing best at 10-20 ppt at 20-25 C (Rueness 2005).
History References- AlgaeBase 2005; Belorin et al. 2005; Gurgel and Frederiq 2004; Hommersand and Freshwater 2004; Humm 1979; Israel et al. 1999; North Carolina Sea Grant 2005; Rueness 2005; Thompson 2002, personal communication; Thomsen et al. 2005; Tyler et al. 2005
Invasion Comments
None
Ecology
Environmental Tolerances
| For Survival | For Reproduction | |||
|---|---|---|---|---|
| Minimum | Maximum | Minimum | Maximum | |
| Temperature (ºC) | 5.0 | 34.0 | ||
| Salinity (‰) | 5.0 | 60.0 | 5.0 | |
| Oxygen | None | |||
| pH | ||||
| Salinity Range | meso-eu |
Age and Growth
| Male | Female | |
|---|---|---|
| Minimum Adult Size (mm) | 2000.0 | 2000.0 |
| Typical Adult Size (mm) | ||
| Maximum Adult Size (mm) | ||
| Maximum Longevity (yrs) | ||
| Typical Longevity (yrs |
Reproduction
| Start | Peak | End | |
|---|---|---|---|
| Reproductive Season | |||
| Typical Number of Young Per Reproductive Event |
|||
| Sexuality Mode(s) | |||
| Mode(s) of Asexual Reproduction |
|||
| Fertilization Type(s) | |||
| More than One Reproduction Event per Year |
|||
| Reproductive Startegy | |||
| Egg/Seed Form |
Impacts
Economic Impacts in Chesapeake Bay
Agarophyton vermiculophyllum is abundant in Hog Island Bay VA, where it contributes to large blooms of drift algae which can cover oyster and shellfish beds (Thomsen 1998). These drift algae are assumed to be unpleasant aesthetically, especially when washed up on shore, The extent of this algas's abundance and distribution in Chesapeake Bay proper is unknown. However, this alga was reported to foul the Brunswick Nuclear Powerplant along the Cape Fear River NC, and was also fouling fishing nets in NC coastal sounds (Thompson 2002, personal communication; Thomsen and Mclathery 2006; Freshwater et al. 2006). In 2009, 'hairballs' of algae, tentatively identified as this species (by Karen McGlathery), clogged crab nets in Tangier Sound, lower Chesapeake Bay (Bay Daily 2009). In lower Chesapeake Bay, dense growths interfere with crabbing and other fisheries (Vogelsang 2018).
Economic Impacts Outside of Chesapeake Bay
According to Thompson (2002, personal communication), Agarophyton vermiculophyllum was causing problems at the Brunswick Nuclear Powerplant near Wilmington NC: "It creates problems for us by severely clogging plant intake screening." This alga was also interfering with commericial fishing by clogging nets and turtle excluder devices in NC waters (North Carolina Sea Grant 2005; Freshwater et al. 2006).
Ecological Impacts on Chesapeake Native Species
Agarophyton vermiculophyllum is abundant in Hog Island Bay, the Chesapeake Bay region, and has been a component of sporadic blooms of drift algae. Ulva lactuca and A. vermiculophyllum together form 80% of the macroalgal biomass in Hog Island Bay (Thomsen 1998; Tyler et al. 2005). Dense drift algal accumulations, dominated by A. vermiculophyllum on reefs resulted in reduced animal abundance (Thomsen and McGlathery 2006). Agarophyton vermiculophyllum was incorporated into tubes of Diopatra cuprea, a tube-building polychaete. Reduced biodiversity was seen in mobile fauna in drift masses of A. vermiculophyllum (Thomsen et al. 2009). However, in Chesapeake Bay, patches of A. vermiculophyllum may offer refuges from predation for small Blue Crabs (Callinectes sapidus, partially compensating for the decline of seagrasses in the Bay. Reduced predation, compared with bare sediment, was seen both in mesocosm and field experiments (Falls 2008).
Agarophyton vermiculophyllum was reported to be highly invasive in the Cape Fear estuary, NC (Thompson 2002, personal communication; Freshwater et al. 2006), and is a potential competitor with native algae. This alga created extensive seaweed habitat in Charleston Harbor, Hilton Head, and Wassah Sound, by attaching to the tubes of Diopatra cuprea, providing habitat for invertebrate fauna, especially amphipods and snails (Byers et al. 2012). The large biomass of drift algae rapidly decayed, providing a potential food source for invertebrates and microbes in the mudflats (Byers et al. 2012). References- Freshwater et al. 2006; Thomsen 1998; Thomsen et al. 2005; Thomsen and McGlathery 2006; Tyler et al. 2005.
Ecological Impacts on Other Chesapeake Non-Native Species
Agarophyton vermiculophyllum is abundant in the Hog Island Bay VA, (and rpobably elsewhere in the Chesapeake Bay region) and has been a component of sporadic blooms of drift algae. Ulva lactuca and A. vermiculophyllum together form 80% of the macroalgal biomass in the Atlantic bays of Chesapeake Bay region (Thomsen 1998; Tyler et al. 2005). Agarophyton vermiculophyllum appears to compete for substrate with Codium fragile spp. fragile (Thomsen 1998; Tyler et al. 2005). Impacts of A. vermiculophyllum on habitat quality in the Chesapeake Bay region appears to be mixed. At lower densities, it can provide shelter for organisms in unvegeatated areas, and make up for the loss of seagrasses, but at higher densities, it may interfere with moevements and foraging of fishes and crabs (Falls 2008; Vogelsong 2018).
References
Bellorin, Alexis M.; Oliveira, Mariana C.; Oliveira, Eurico (2004) Gracilaria vermiculophylla: a western Pacific species of Gracilariaceae (Rhodophyta) first recorded from the eastern Pacific., Phycological Research 52: 69-79Bold, Harold C.; Wynne, Michael J. (1978) Introduction to the Algae: Structure and Reproduction, , Englewood Cliffs, NJ. Pp.
Byers, James E.; Gribben, Paul E.; Yeager, Caitlin; Sotka, Erik E. (2012) Impacts of an abundant introduced ecosystem engineer within mudflats of the southeastern US coast, Biological Invasions 14: 2587-2600
Falls, Justin A. (2008) The survival benefit of benthic macroalgae Gracilaria vermiculophylla as an alternative nursery habitat for juvenile blue crabs, None , Williamsburg. Pp. 1-69
Fredericq, Suzanne; Hommersand, Max. H . Freshwater, D. Wilson (1996) The molecular systematics of some agar- and carrageenan-containing marine red algae based on rbcL sequence analysis., Hydrobiologia 326/327: 125-135
Freshwater, D. Wilson; Greene, Julie K.; Hamner, Rebecca M. (2006) Seasonality of the invasive seaweed <>Gracilaria vermiculophylia along the southeastern coast, Journal of the North Carolina Academy of Science 122: 49-55
Freshwater, D. Wilson; Montgomery, Frank ; Greene, Julie K.; Hamner, Rebecca M. ; Williams, Melissa; Whitfield, Paula E. (2006) Distribution and identification of an invasive Gracilaria species that is hampering commercial fishing operations in southeastern North Carolina, USA., Biological Invasions 8: 631-637
2004-2023 AlgaeBase. National University of Ireland Galway--http://algaebase.org
Gurgel, Carlos Frederico D.; Fredericq, Suzanne (2004) Systematics of the Gracilariaceae (Gracilariales, Rhodophyta): a critical assessment based on rbcL sequence analyses., Journal of Phycology 40: 138-159
Gurgel, Carlos Frederico D.; Norris, James N.; Schmidt, William E.; Le, Hau Nhu; Fredericq, Suzanne (2018) Systematics of the Gracilariales (Rhodophyta) including new subfamilies, tribes, subgenera, and two new genera, Agarophyton gen. nov. and Crassa gen. nov., Phytotaxa 374: Published online
Hommersand, M. H.; Freshwater, D. W. (2004) 'A seaweed goes to war'- Taxonomic status of the agarophyte Gracilaria 'confervoides,/i>' harvested in North Carolina duirng WWII., Journal of Phycology 40: 8
Hommersand, M. H.; Freshwater, D. W. (2009) Gracilaria hummii sp. nov. (Gracilariales, Rhodophyta), a new name for the agarophyte ‘‘Fracilaria confervoides’’ harvested in North Carolina during World War I!, Journal of Phycology 45: 503-516
Israel, Alvar; Martinez-Goss, Milagrosa; Friedlander,Michael (None) Effect of salinity and pH on growth and agar yield of Gracilaria tenuistipitata var. liui in laboratory and outdoor cultivation, Journal-of Applied Phycology 11: 543-549
Nettleton, Jeremy C.; Mathieson, Arthur C.; Thornber, Carol; Neefus, Christopher D.; Yarish, Charles (2013) Introduction of Gracilaria vermiculophylla (Rhodophyta, Gracilariales) to New England, USA: Estimated arrival times and current distribution, Rhodora 115: 28-41
Raikar, S. V.; Iima, M.; Fujita, Y. (2001) Effects of temperature, salinity, and light intensity on the growth of Gracilaria sp. from Japan, Malaysia, and India., Indian Journal of Marine Sciences 30: 98-104.
Rueness, Jan (2005) Life history and molecular sequences of Gracilaria vermiculophylla (Gracilariales, Rhodophyta), a new introduction to European waters., Phycologia 44: 120-128
Saunders, Gary W. (2009) Routine DNA barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia, Molecular Ecology Resources 9: 140-150
Thomsen, M.S.; McGlathery, K. (2006) Effects of accumulations of sediments and drift algae on recruitment of sessile organisms associated with oyster reefs., Journal of Experimental Marine Biology and Ecology 328: 22-34
Thomsen, Mads S.; Gurgel, Carlos F.D.; Frederiq, Suzanne; McGlathery, Karen J. (2005) Gracilaria vermiculophylla (Rhodophyta, Gracilariales) in Hog Island Bay, Virginia: a cryptic alien and invasive macroalga and taxonomic correction., Journal of Phycology 42: 139-141
Tyler, Anna Christina; McGlathery, Karen J.; Macko, Stephen A. (2005) Uptake of urea and amino acids by the macroalgae Ulva lactuca (Chlorophyta) and Gracilaria vermiculophylla (Rhodophyta), Marine Ecology Progress Series 294: 161-172
Yokoya, Nair S.; Kakita, Hirotaka; Obika, Hideka; Kitamura, Kideo (1999) Effects of environmental factors and plant growth regulators on growth of the red alga Gracilaria vermiculophylla from Shikoku Island, Japan., Hydrobiologia 398-399: 339-347