Invasion History

First Non-native North American Tidal Record: 1927
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 1927

General Invasion History:

The red alga Bonnemaisonia hamifera is believed to be native to Japan (Dixon and Irvine 1977; Farnham 1980; Holmes 1897), although 'there is no direct evidence to support the assumption that Bonnemaisonia hamifera is in fact native to Japan' (McLachlan et al. 1969). However, all of the stages of the life cycle have only been found together in Japan. Elsewhere the gametophytes are less widely distributed than the tetrosporophytes (and males much rarer than females), and fertile gametophytes have not been found. The different life cycle phases appear to have propagated vegetatively in Europe and North America (Dixon and Irvine 1977; McLaughlin et al. 1969). Reports of the 'Trailliella' stage of this species on the Pacific coast of North America probably refer to the native Northeast Pacific form Bonnemaisonia nootkana (McLachlan et al. 1967).

Outside its native range, B. hamifera was first collected in Europe, in Falmouth, England, in 1893 (Holmes 1897), and subsequently spread around Europe, reaching the Mediterranean (Tunisia) by 1918 (Verlaque 1994). Its present eastern Atlantic range is from Morocco to Norway, Iceland, and the Azores (South and Tittley 1986). In the western Atlantic, it was first collected at Woods Hole, Massachusetts in 1927 (Lewis and Taylor 1928) and now ranges from Labrador to Virginia (Humm 1979; Mathieson and Dawes 2017). It has also been introduced to Argentina and New Zealand (Quartino 1990; Garbary et al. 2020).

North American Invasion History:

Invasion History on the East Coast:

In the western Atlantic, Bonnemaisonia hamifera was first collected at Woods Hole, Massachusetts in 1927 (Lewis and Taylor 1928) and now ranges from Labrador to Virginia (Humm 1979; South and Tittley 1986). 'Trailliella' tetrasporophytes, and gametophytes (as Asparagopsis hamifera) were first collected at Nobska Point, Woods Hole in 1927 (Lewis and Taylor 1928). Its abundance decreased sharply after a severe winter in 1933 (Taylor 1937). In 1940, it was collected in Long Island Sound (Taylor 1940), and it is now well-established in Narragansett Bay as well (Villalard-Bohnsack 1995). Bonnemaisonia hamifera was abundantly overgrowing Eelgrass (Zostera marina) in 2006 in Barengat Bay, New Jersey (Kennish et al. 2007). In Chesapeake Bay, the tetrasporophyte Trailliella form was collected at 6 stations in the vicinity of Tangier and Pocomoke Sounds in 1968, as the 'Trailliella' form growing as an epiphyte on eelgrass and seaweeds (Mathieson and Fuller 1969). It was also found growing on widgeongrass (Ruppia maritima) in the Guinea Marshes, Gloucester Point, York River, in 1974 (Humm 1979). The gametophyte has not been found in Chesapeake Bay (Humm 1979).  Bonnemaisonia hamifera was not reported from waters north of Cape Cod by Taylor (1937), but the tetrasporophyte phase ('Trailliella') was discovered in 1948 in the Northumberland Straits. This alga (probably the tetrasporophyte) has since been collected in southern Labrador (South and Tittley 1986). Currently, the gametophyte has been identified genetically from Narragansett to  the Bay of Fundy. while the 'Trailliella' form occurs further north (Saunders 2022). This alga has not been reported from North Carolina (Schneider and Searles 1997).
 

Invasion History Elsewhere in the World:

Outside its native range, Bonnemaisonia hamifera was first collected in Europe, in Falmouth, England, in 1893 (Holmes 1897), and subsequently spread around Europe, reaching the Mediterranean (Tunisia) by 1918 (Verlaque 1994), and the Black Sea (1986, Cinar et al. 2005). Currently, in the Eastern Atlantic it ranges south to Morocco (1935; Benhissoune et al. 2002) and north to Norway (1902; Hopkins 2002), and Iceland (1978; Thorarinsdottir et al. 2018). This alga reached the Azores by 2003 (Chainho et al 2015), and Argentina by 1989, (Quartino 1990).  Likely vectors for the spread of Bonnemaisonia hamifera are ballast waters, fouling community, and the transfer of shellfish, especially oysters.

 


Description

The red alga Bonnemaisonia hamifera has two very distinct life phases, a more conspicuous gametophyte, which is a feathery branched upright epiphytic form, and a small, filamentous tetrasporophyte, once considered a separate species named Trailliella intricata. The gametophyte is typically up to 100 mm (sometimes 200 mm), with a finely branched Christmas-tree shape, pink-to-deep-red in color. With magnification, the fronds can be seen to carry many deeply curved hooks, which help this alga to cling to other seaweeds. The gametophyte is sexually reproducing and occurs during the warmer seasons, while the tetrasporophyte form occurs year-round. The tetrasporphytes form dense tufts of irregularly branched filaments, dark red to rose-red, 10–25 mm in height (Taylor 1957; Humm 1979; Van Patten 2006; Mathieson and Dawes 2017).


Taxonomy

Taxonomic Tree

Kingdom:   Plantae
Phylum:   Rhodophycota
Class:   Rhodophyceae
Subclass:   Florideophycideae
Order:   Bonnemaisoniales
Family:   Bonnemaisoniaceae
Genus:   Bonnemaisonia
Species:   hamifera

Synonyms

Asparagopsis hamifera (None, None)
Bonnemaisonia intricata (None, None)
Trailliella intricata (None, None)

Potentially Misidentified Species

Asparagopsis armata
None

Asparagopsis taxifomis
None

Ecology

General:

Temperature- the maximum given is a field temperature in Chesapeake Bay at time of collection, July 1968 (Mathieson and Fuller 1969), which is the highest field temperature which we have seen reported for this species. Tetrasporophytes and gametophytes from Ireland survived and grew at 0–25 °C, but died at 30 °C. Maximum growth of tetrasporophytes was at 15–25 °C, but gametophytes grew optimally at 15 °C and showed abnormalities at 20–25 °C (Breeman et al. 1988). Sexual reproduction of this species is sharply limited by temperature. Gametophytes in culture became fertile at 5–20 °C, and carpogonia, the female reproductive organ in red algae, developed at 5–20 °C, but mainly at long day-lengths. Tetrasporangia, which produce gametophytes, require shorter day-lengths and temperatures above 11 °C. The 'reproductive window' in Virginia for tetrasporangia production occurs in September through October. Production of gametophytes occurs in spring-summer, at temperatures above 10 °C, in August through September in Nova Scotia CA, and July through August in Massachusetts. Production of males occurs at lower temperatures than that of females, so that males may be produced in winter (only one west Atlantic record, from Halifax), while females are not produced until summer. In southern Japan, however, the reproductive cycle is better synchronized, with higher winter temperatures permitting overlap among the sexes, and fertilization of carpogonia in spring, while summer temperatures rarely exceed the tolerance of gametophytes (Breeman et al. 1988).

Environmental tolerances: Salinity- The minimum given is a field record, Chesapeake Bay (Mathieson and Fuller 1969), the lowest which we have seen reported. Based on its occurrence elsewhere in the North Atlantic, B. hamifera ranges into euhaline waters, although it has not been reported from higher salinities in the Chesapeake region.

Trophic Status:

Primary Producer

PrimProd

Habitats

General HabitatRockyNone
General HabitatUnstructured BottomNone
General HabitatMarinas & DocksNone
Salinity RangeMesohaline5-18 PSU
Salinity RangePolyhaline18-30 PSU
Salinity RangeEuhaline30-40 PSU
Tidal RangeSubtidalNone
Tidal RangeLow IntertidalNone
Vertical HabitatEpibenthicNone

Life History

Reproduction: Sexuality Modes- Bonnemaisonia hamifera has distinct male and female gametophytes, but in much of the introduced range, either the gametophytes do not occur (in northern Europe (Dixon and Irvine 1977), Gulf of St. Lawrence (McLachlan et al. 1969), and possibly Chesapeake Bay (Humm 1979)) or only one sex is produced (Dixon and Irvine 1977; McLachlan et al. 1969). All of the life cycle stages have only been observed together in Japan; elsewhere, mature tetraspores and gametes are rarely found. The different life cycle stages appear to be largely uncoupled and dependent on vegetative reproduction (Dixon and Irvine 1977). Since the gametophytes and sexual reproduction has not been observed in our area, the data given here refer only to the tetrasporophyte stage. Reproductive season- Production of female gametophytes, where known from the west Atlantic, takes place in summer, in August through September in Halifax Nova Scotia CA, and July through August in Massachusetts. The one record of male gametophytes from the west Atlantic was in February in Nova Scotia. In Shimoda, Japan, sexual reproduction occurred in March through May (Breeman et al. 1988).

 Bonnemaisonia hamifera has a complex life cycle, with triphasic alternation of generations. Male gametes (spermatia, unflagellated) attach to female cells (carpogonia) on the adult plant  to produce a carposporophyte, a mass of fertile cells, or carpospores, considered the first life cycle phase. Carpospores are released and germinate into tetrasporophytes. Tetrasporophytes eventually mature to form tetrasporangia. Meiosis occurs in the tetrasporangia, resulting in four haploid nuclei, incorporated into tetraspores. Tetraspores germinate into haploid gametophytes which are much larger than the tetrasporophytes (Bold and Wynne 1978; Harder and Koch 1949).

The tetrasporophyte stage is morphologically distinct from the gametophyte and was once regarded as a separate species called Trailliella intricata, until the tetraspores of 'Trailliella' were found to germinate and grow into plants of B. hamifera (Harder and Koch 1949). In the full life cycle, mature male and female gametophytes of separate sexes release gametes, which fuse and are released and settle as the tetrasporophyte 'Trailliella' stage. Only the tetrasporophyte stage 'Trailliella', is known from Chesapeake Bay (Humm 1979). The gametophyte stage has not been reported south of Long Island (South and Tittley 1986; Taylor 1957). Sexual reproduction of this species, and the full life cycle, has been documented only in Japan (Dixon and Irvine 1977; Farnham 1980; McLachlan 1969).


Tolerances and Life History Parameters

Minimum Temperature (ºC)-1None
Maximum Temperature (ºC)29None
Minimum Salinity (‰)12Field, Chesapeke Bay, Mathieson and Fuller 1969
Maximum Salinity (‰)38

Typical Mediterranean salinity

Broad Temperature RangeNoneCold temperate-Warm temperate
Broad Salinity RangeNoneMesohaline-Euhaline

General Impacts

The red seaweed Bonnemaisonia hamifera has become a common and sometimes abundant epiphyte of seaweed community.  When abundant, it increases the structural complexity of communities by covering seaweeds with dense networks of filaments and fronds, but can also affect the host alga by depriving it of light (Minchin et al. 2013; Dijkstra et al. 2017). Bonnemaisonia hamifera  also produces compounds (e.g. (1,1,3,3-tetrabromo-2-heptanone), which discourages grazing by crustaceans and mollusks (Enge et al. 2012; Svensson et al. 2013).  The reduction in grazing may increase its role in habitat change, both in providing refuge, and in reducing growth of host algae and seagrasses (Svensson et al. 2013).


Regional Impacts

NA-ET2Bay of Fundy to Cape CodEcological ImpactCompetition
Displaces native algae ( Harris and Tyrell 2001)
B-IINoneEcological ImpactCompetition

In the Kattegat and Belt Sea, B. hamifera was classified as having some community impacts (Zaiko et al. 2011).

B-IIINoneEcological ImpactCompetition

In the Kattegat and Belt Sea, B. hamifera was classified as having a low level of community impacts (Zaiko et al. 2011).

NEA-IINoneEcological ImpactCompetition
Competition impacts were listed for the British Isles by Minchin et al. (2013).
B-INoneEcological ImpactFood/Prey
Bonnemaisonia hamifera produces a chemical compound (1,1,3,3-tetrabromo-2-heptanone), not present in competing algae, which discourages herbivory by native mollusks, isopods, and amphipods, in waters around Tjarno, Sweden, in the Skagerrak (Enge et al. 2012).
B-INoneEcological ImpactHabitat Change

Bonnemaisonia hamifera, because of its chemically-based resistance to herbivory, provides a refuge for herbivores (e.g., the isopod Idotea granulosa) (Enge et al. 2013).

B-INoneEcological ImpactCompetition

In experiments, Bonnemaisonia hamifera outcompeted native seaweeds, because of its chemical defenses against herbivory (Enge et al. 2013). One of its defensive compounds (1,1,3,3-tetrabromo-2-heptanone) inhibits the settlement of propagules of several native seaweeds and of microalgae, providing a competitive advantage through allelopathy (Svensson et al. 2013).

B-INoneEcological ImpactToxic

Bonnemaisonia hamifera produces a chemical compound (1,1,3,3-tetrabromo-2-heptanone), not present in competing algae, which discourages herbivory by native mollusks, isopods, and amphipods, in waters around Tjarno, Sweden, in the Skagerrak (Enge et al. 2012).

NA-ET2Bay of Fundy to Cape CodEcological ImpactHabitat Change
Around the Isles of Shoals, NH-ME, from the 1979 to 2015, there has been a trend of replacement of kelps and other larger brown seaweeds, by smaller, bushier red seaweeds (Bonnemaisonia hamifera, Dasysiphonia japonica, and Neosiphonia spp.) and Codium fragile, increasing the structural complexity of the environment, and the abundance and diversity of meso-sized invertebrates (Dijkstra et al. 2017).
N135_CDA_N135 (Piscataqua-Salmon Falls)Ecological ImpactHabitat Change
Around the Isles of Shoals, NH-ME, from the 1979 to 2015, there has been a trend of replacement of kelps and other larger brown seaweeds, by smaller, bushier red seaweeds (Bonnemaisonia hamifera, Dasysiphonia japonica, and Neosiphonia spp.) and Codium fragile, increasing the structural complexity of the environment, and the abundance and diversity of meso-sized invertebrates (Dijkstra et al. 2017).
NHNew HampshireEcological ImpactHabitat Change
Around the Isles of Shoals, NH-ME, from the 1979 to 2015, there has been a trend of replacement of kelps and other larger brown seaweeds, by smaller, bushier red seaweeds (Bonnemaisonia hamifera, Dasysiphonia japonica, and Neosiphonia spp.) and Codium fragile, increasing the structural complexity of the environment, and the abundance and diversity of meso-sized invertebrates (Dijkstra et al. 2017).
MEMaineEcological ImpactCompetition

Displaces native algae ( Harris and Tyrell 2001)

MEMaineEcological ImpactHabitat Change

Around the Isles of Shoals, NH-ME, from the 1979 to 2015, there has been a trend of replacement of kelps and other larger brown seaweeds, by smaller, bushier red seaweeds (Bonnemaisonia hamiferaDasysiphonia japonica, and Neosiphonia spp.) and Codium fragile, increasing the structural complexity of the environment, and the abundance and diversity of meso-sized invertebrates (Dijkstra et al. 2017).

NHNew HampshireEcological ImpactCompetition

Around the Isles of Shoals, NH-ME, from the 1979 to 2015, there has been a trend of replacement of kelps and other larger brown seaweeds, by smaller, bushier red seaweeds (Bonnemaisonia hamiferaDasysiphonia japonica, and Neosiphonia spp.) and Codium fragile, increasing the structural complexity of the environment, and the abundance and diversity of meso-sized invertebrates (Dijkstra et al. 201

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
NWP-3b None 0 Native Estab
NA-ET3 Cape Cod to Cape Hatteras 1927 Def Estab
NA-ET2 Bay of Fundy to Cape Cod 1957 Def Estab
NA-ET1 Gulf of St. Lawrence to Bay of Fundy 1957 Def Estab
NA-S3 None 1948 Def Estab
NEA-III None 1893 Def Estab
NEA-II None 1897 Def Estab
NEA-IV None 1905 Def Estab
WA-I None 1935 Def Estab
NEA-V None 1986 Def Estab
AR-IV None 1978 Def Estab
AR-V None 1919 Def Estab
B-I None 1902 Def Estab
B-II None 1902 Def Estab
B-III None 0 Def Estab
B-IV None 1939 Def Estab
NEA-VI None 1989 Def Estab
MED-III None 1910 Def Estab
MED-II None 1882 Def Estab
MED-I None 1982 Def Estab
NWP-4a None 0 Native Estab
M020 Narragansett Bay 1995 Def Estab
M010 Buzzards Bay 1927 Def Estab
M040 Long Island Sound 1972 Def Estab
M130 Chesapeake Bay 1967 Def Estab
N170 Massachusetts Bay 2003 Def Estab
N125 _CDA_N125 (Piscataqua-Salmon Falls) 1980 Def Estab
M070 Barnegat Bay 2004 Def Estab
M030 Gardiners Bay 1940 Def Estab
NWP-4b None 0 Native Estab
NWP-2 None 0 Native Estab
N100 Casco Bay 1995 Def Estab
N135 _CDA_N135 (Piscataqua-Salmon Falls) 1968 Def Estab
MED-IX None 1986 Def Estab
MED-V None 1997 Def Estab
N195 _CDA_N195 (Cape Cod) 1927 Def Estab
N160 Plum Island Sound 1968 Def Estab
N180 Cape Cod Bay 1971 Def Estab
N130 Great Bay 1985 Def Estab
N120 Wells Bay 2007 Def Estab
N010 Passamaquoddy Bay 1994 Def Estab
MED-VI None 2008 Def Estab
MED-VII None 1978 Def Estab
N120 Wells Bay 2013 Def Estab
SA-I None 1989 Def Estab
NA-S2 None 1968 Def Estab
NZ-IV None 2019 Def Estab
MED-VIII None 1984 Def Estab
MED-IX None 2017 Def Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude

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