Ulva ohnoi

Invasion History

First Non-native North American Tidal Record: 1999
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 1999

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General Invasion History:

Ulva ohnoi was described from Tosa Bay, Kochi prefecture, Shikoku Japan, on the Pacific Coast. It was also found in Hakata Bay in Fukuoka Prefecture, Kyushu, and in Okinawa (Hiraoka, et al. 2004). It has been found in Korea, India, Iran, Australia, and Hawaii (O'Kelly et al. 2010; Kirkendale et al. 2013; Pirian et al. 2015; Kazi et al. 2016; Guiry and Guiry 2022). It is more clearly introduced in the Gulf of California (2015, Chavez-Sanchez et al. 2019). In the Mediterranean, U. ohnoi was found in ballast water in Naples in 2003 (Flagella et al. 2007), and in Capo Pelora Lagoon, Italy, and the Gulf of Gabes, Tunisia in 2013–14 (Miladi et al. 2019), and in natural environments in Achziv, Israel in 2002 (Krupnik et al. 2018). Ulva ohnoi was collected on the Yucatan peninsula, Mexico, in 1999, and found at 18 locations on the Atlantic and Gulf coasts from 2012 to 2015.  This alga was found attached to rocky intertidal and mangroves, and also freely floating. Massive, smothering growths were noted in mangroves and seagrass beds in the Laguna Madre, Texas, and Biscayne Bay, Florida (Melton et al. 2016a). The low genetic diversity of the alga compared to global populations supports introduced status for this alga (Melton et al. 2016a). Ballast water, hull fouling, and Pacific Oyster (Crassostrea gigas) transplants are all possible vectors for introductions, varying in importance by region.

North American Invasion History:

Invasion History on the East Coast:

The earliest record of Ulva ohnoi on the Atlantic Coast of North America was in Cocoa, Florida, on the Indian River Lagoon. In 2013–2014, it was found on 5 locations on the Indian River Lagoon and Biscayne Bay.  An extensive overgrowth was found near Deering Estate, Miami Florida, in July 2013, with large sheets of floating algae floating draped over mangrove roots. Blooms of two other green algal species, Anadyomene  stellata, and Anadyomene sp. (possibly introduced) were producing blooms in Biscayne Bay, probably stimulated by inflows of nutrient-rich groundwater.  As in the case of Anadyomene  spp., Ulva ohnoi showed a high affinity for stable isotope 15N, suggesting that it was also stimulated by nutrient inputs in groundwater (Melton et al. 2016a).

Invasion History on the Gulf Coast:

The earliest record of Ulva ohnoi in the Gulf of Mexico is from an unspecified location in Yucatan in 1999, from an herbarium specimen. It should be noted that this species requires genetic identification, and so could be overlooked. However, it has produced dramatic blooms in well-studied areas (Melton et al. 2016a). Melton et al. sampled 14 Gulf Coast locations in Texas, Alabama, and Florida, from Aransas Pass to Florida Bay. Ulva ohnoi was found at all locations, mostly attached, or free-floating in the rocky intertidal (Melton et al. 2016a).  Gulf and Atlantic haplotypes of C. ohnoi showed lower diversity than a global sample (Japan, Hawaii, Australia, Naples), supporting non-native status.  Overgrowths of seagrasses were noticed, near Brazos Santiago Pass and South Padre Island, Texas (Melton et al. 2016a).
 

Invasion History in Hawaii:

Specimens of Ulva ohnoi were collected on Maui and Oahu Hawaii, before 2009 (O'Kelly et al. 2010). The date of introduction is unknown, and we considered its status in the Hawaiian Islands to be cryptogenic, given the taxonomic difficulty of the genus and the relatively recent description of the species.

Invasion History Elsewhere in the World:

Green algae of the genus Ulva are morphologically and taxonomically simple, but include many species that are ecologically opportunistic and rapidly respond to nutrients, light and disturbance. Until the development of molecular identification, invasions of Ulva spp. have been difficult to identify. Ulva ohnoi was described from Japan and we considered it to be native to the Northwest Pacific, and cryptogenic in the broad Indo-Pacific, including Australia, Hawaii, and Iran (O'Kelly et al. 2010; Kirkendale et al. 2013; Pirian et al. 2015; Kazi et al. 2016; Guiry and Guiry 2022). There are occurrences in the Gulf of California (Chavez-Sanchez et al. 2019), Mediterranean Sea (Flagella et al. 2007; Krupnik et al. 2018; Miladi et al. 2019), and Le Havre France (Verlaque and Breton 2018). In the Western Atlantic, it has been found on the Gulf and Atlantic coast from Yucatan, Mexico (1999), and from Texas to the Indian River Lagoon, Florida (2012–2015; Melton et al. 2016a).  It has also been found in the Caribbean Sea, on the coast of Venezuela (Melton et al. 2016b). 

 

 

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Description

Green algae of the genus Ulva, commonly called 'sea lettuce', form thalli consisting of simple leafy sheets or tubes, formed of two layers of cells, and attached or free-floating. The thalli of U. ohnoi are typically roughly round or oval but easily torn, 200–300 mm in diameter, and light green. The thalli are 30–55 µm thick in the distal region and 80–90 µm in the basal region. The alga reproduces asexually by fragmentation, and sexually by flagellated isogametes. Many of the distinctive features of Ulva spp. are microscopic and molecular methods are often required for identification (Bold and Wynne 1978; Hiraoka et al. 2004).

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Taxonomy

Ecology

General:

Available records for Ulva ohnoi suggest a preference for tropical to warm-temperate climates, and marine salinities (Melton et al. 2016a, 2016b; Guiry and Guiry 2022).  Ulva ohnoi survived 4-day exposure to 34° C, but died at 36° C, and the lower limit for growth is 0°C (Zanolla et al. 2019). Habitats include rocky intertidal areas, on sand, on shells, corals, and mangroves, as an attached or free-floating thallus (Hiraoka et al. 2004; Melton et al. 2016; Chavez-Sanchez et al. 2018). Ulva spp. are a common food for herbivorous invertebrates and fishes (Dupla et al. 2020). This alga has not been reported from brackish water.

Food:

Consumers:

Herbivorous fishes, invertebrates

Competitors:

Other Ulva spp.

Trophic Status:

Primary Producer

PrimProd

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Habitats

General Habitat	Grass Bed	None
General Habitat	Salt-brackish marsh	None
General Habitat	Unstructured Bottom	None
General Habitat	Oyster Reef	None
General Habitat	Marinas & Docks	None
General Habitat	Rocky	None
General Habitat	Mangroves	None
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Vertical Habitat	Epibenthic	None
Vertical Habitat	Planktonic	None
Vertical Habitat	Pelagic	None

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Life History

Ulva spp. reproduce asexually by fragmentation, and by quadriflagellate zoospores (meiospores).  Sexual reproduction occurs by isomorphic (same-sized) gametes, which fuse to form a thallus. The meiospores are negatively phototactic and settle on surfaces, and then divide to form filaments that grow into a leaf-like gametophytes, which began to release gametes at a size greater than 50 mm.  The thalli grow to about 300 mm wide to 200–300 mm long (Bold and Wynne 1978; Hiraoka et al. 2003).

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Tolerances and Life History Parameters

General Impacts

Ulva ohnoi is one of many species of Ulva that are associated with 'green tides', massive blooms of attached and floating sheets of 'sea lettuce' that interfere with swimming, boating, and fishing, and can decompose, leading to hypoxia and unpleasant odors (Hiroaka et al. 2004). In US Atlantic and Gulf waters, blooms were seen in Deering Estate, Biscayne Bay and in Florida Bay Florida, and near Brazos Santiago Pass, South Padre Island, Texas.  Ulva ohnoi in Biscayne Bay showed a high proportion of the stable isotope 15N, indicating uptake of nitrogen-rich groundwater, which contributes to algae blooms in the Bay (Melton et al. 2016a).

Blooms of Ulva spp. can smother seagrass beds and native seaweeds, degrading habitat for fishes and shellfish. The decay of Ulva blooms can contribute to die-offs off of marine fauna in estuaries (Hiraoka et al. 2004).

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Regional Impacts

CAR-I	Northern Yucatan, Gulf of Mexico, Florida Straits, to Middle Eastern Florida		Ecological Impact	Competition
Ulva ohnoi forms extensive green mats covering seagrass beds and negatively affecting them (Melton et al. 2016a)
CAR-I	Northern Yucatan, Gulf of Mexico, Florida Straits, to Middle Eastern Florida		Ecological Impact	Habitat Change
Ulva ohnoi forms extensive green mats covering seagrass beds and mangrove routes, and negatively affecting them (Melton et al. 2016a).
CAR-I	Northern Yucatan, Gulf of Mexico, Florida Straits, to Middle Eastern Florida		Economic Impact	Aesthetic
Massive floating blooms, 'green tides' of U. ohnoi were seen in southern Japan, and at Deering Estate, Biscayne Bay, Florda, and near near Brazos Santiago Pass, South Padre Island, Texas.  These 'green tides' can interfere with fishing, swimming, and boating, and be smelly and visually unpleasant (Hiraoaka et al. 2004; Melton et al. 2016a)

References

Krupnik, Nimrod; Paz, Guy; Douek, Jacob; Lewinsohn, Efraim; Israel, Alvaro; Carmel, Nava; ,Mineur, Federic; Maggs, Christine A. (2018) Native, invasive and cryptogenic Ulva species from the Israeli Mediterranean Sea: risk and potential, Mediterranean Marine Science 19(1): 132-146
DOI: http://dx.doi.org/10.12681/mms.2104

Bold, Harold C.; Wynne, Michael J. (1978) Introduction to the Algae: Structure and Reproduction, Prentice-Hall, Englewood Cliffs, NJ. Pp. <missing location>

Chávez-Sánchez, Tonatiuh; Piñón-Gimate, Alejandra; Melton, James T. III; López-Bautista, Juan Manuel; Casas-Valdez, Margarita (2019) First report, along with nomenclature adjustments, of Ulva ohnoi, U. tepida and U. torta (Ulvaceae, Ulvales, Chlorophyta) from northwestern Mexico, Botanica Marina 62(2): 113-123
https://doi.org/10.1515/bot-2018-0007

Flagella, Maria Monia; Verlaque, Marc; Soria, Alessio; Buia, Maria Cristina (2007) Macroalgal survival in ballast water tanks., Marine Pollution Bulletin 54: 1395-1401

Guiry, M. D.; Guiry, G. M. 2004-2023 AlgaeBase. https://www.algaebase.org/



Hiraoka, Masanori; Shimada,Satoshi; Uenosono, Masako; Michio Masuda (2004) A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan, Phycological Research 52: 17-29

Kazi, Mudassar Anisoddin; Kavale, Monica G.; V. Singh. Veerendra (2016) Morphological and molecular characterization of Ulva chaugulii sp. nov., U. lactuca and U. ohnoi (Ulvophyceae, Chlorophyta) from India, Phycologia 55(1): 45-54
DOI: 10.2216/15-11.1

Kirkendale, Lisa; Saunders, Gary W.; Winberg, Pia (2013) A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism, Journal of Phycology 49: 69-81

Melton, J. T.III; García-Soto, G.C.; López-Bautista, J. M. (2016b) A new record of the bloom-forming record of the bloom-forming green algal species Ulva ohnoi (Ulvalves, Chlorophyta) in the Caribbean Sea , Algas 51: 62-64

Melton, James T. III, Collado-Vides, Ligia; Lopez-Bautista, Juan M. (2016a) Molecular identification and nutrient analysis of the green tide species Ulva ohnoi M. Hiraoka & S. Shimada, 2004 (Ulvophyceae, Chlorophyta), a new report and likely nonnative species in the Gulf of Mexico and Atlantic Florida, USA, Aquatic Invasions 11(3): 225-237
http://dx.doi.org/10.3391/ai.2016.11.3.01

Miladi, Ramzi; ,Manghisi; Antonio; Armeli, Simona Minicante; Genovese. Giusspa;, Abdelkafi, Slim; Morabito, Marina (2022) A DNA Barcoding Survey of Ulva (Chlorophyta) in Tunisia and Italy Reveals the Presence of the Overlooked Alien U. ohnoi, Cryptogamie - Algologie 39(1): 85-107
doi/10.7872/crya/v39.iss1.2018.85

O’Kelly, Charles J.; Kurihara, Akira; Shipley, Tara C.; Sherwood, Alison R. (2010) Molecular assessment of Ulva spp. (Ulvophyceae, Chlorophyta) in the Hawaiian islands, Journal of Phycology 46: 728-735

Pirian, Kiana; Piri, Khosro; Sohrabipour, Jelveh; Jahromi, Saied Tamadoni; Blomster, Jaanika (2016) Molecular and morphological characterisation of Ulva chaugulii, U. paschima and U. ohnoi (Ulvophyceae) from the Persian Gulf, Iran, Botanica Marina 59(2-3): 47–158
DOI 10.1515/bot-2016-0009

Verlaque, Marc; Breton, Gérard (2019) Biological invasion: Long term monitoring of the macroalgal flora of a major European harbor complex, Marine Polution Bulletin 143: 228-241
https://doi.org/10.1016/j.marpolbul.2019.04.038

Zanolla, Marianela; Carmona, Raquel; Kawai, Hiroshi; Stengel, Dagmar B.; Altamirano, María (2019) Role of thermal photosynthetic plasticity in the dispersal and settlement of two global green tide formers: Ulva pertusa and U. ohnoi, Marine Biology 166(123): Published online
https://doi.org/10.1007/s00227-019-3578-1

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