H. musciformis was introduced to Hawaii in 1974. After a lag phase of approximately 3 years, the species became a dominant species on nearby reefs, and subsequently displaced the native Hypnea cervicornis as the predominant epiphyte...
H. musciformis was introduced to Hawaii in 1974. After a lag phase of approximately 3 years, the species became a dominant species on nearby reefs, and subsequently displaced the native Hypnea cervicornis as the predominant epiphyte on Acanthophora at some locations (Russell, 1992). The tendency for the species to detach from host plants, and to fragment, facilitates local dispersal by water movement and potentially regional dispersal through entanglement and translocation on boats, fishing gear etc. Elevated nutrient levels appear to facilitate high growth rates, which can result in a high biomass of drifting and beach cast weed (Smith et al., 2002).
The genus Hypnea was erected by JV Lamouroux with five species, including Fucus musciformis Wulfen. H. musciformis has been adopted as the lectotype of the genus Hypnea (Papenfuss, 1958; Farr et al., 1979; Masuda et al., 1997). The genus now includes approximately 50 species, but the status of some species described in the nineteenth century remains uncertain (Masuda et al., 1997). Taxonomic reviews of the genus and its species are chiefly part of floristic studies or in regional monographs (e.g. Tanaka, 1941; Mshigeni, 1978; Womersley, 1994) and revisions in other regions and critical reassessment of species reported to have wide geographical distributions are still needed.
Plants bushy, tangled, wiry, often in clumps or masses 10-20 (-50) cm high of loosely intertwined cylindrical axes; axes 0.5-1.0 (-2) mm in diameter below, tapering to apices; branching irregular and variable, in part from percurrent axes; axes and primary branches often terminating in broad, flattened, tendril-like hooks, often twisted around axes of other algae, hooks occasionally with small-spur-like branchlets on outer curve; branches with small spine-like branchlets 50-200 µm at base, also tapered, simple or bifurcate and more or less numerous on older or younger (basal or upper) parts of same plant; primary holdfast inconspicuous, disc-like, often difficult to recognize, and tangled by long tendrils or with algae. Medullary cells thick-walled, irregular, 100-200 µm diameter, surrounding small, often obscure central filament. Cortex 1-2 cells thick; cells rounded to irregular, 7-18 µm diameter, densely pigmented. Tetrasporangia zonate, terminal on corticating filaments within raised nemathecial sori encircling lateral branchlets; cystocarps globular, 0.3-1.0 mm diameter, clustered at apices or solitary on side branchlets. Colour yellowish-green to greenish, purplish, and brownish-red.
Widely distributed throughout the tropics and warm temperate seas in the eastern and western Atlantic, including the Mediterranean, around the Indian Ocean, and from northern Australia, Indonesia, Singapore, and the Philippines in the Indo-West Pacific.
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
In January 1974, H. musciformis, along with two morphs of Eucheuma isiforme, was introduced from southern Florida to the island of Oahu, Hawaii, and planted on reefs in Kaneohe Bay as part of an aquaculture project that was later abandoned (Russell and Balazs, 1994; Abbott, 1999; Smith et al., 2002). Within 3 years, the species had become abundant and, by 1982, the species had spread to most intertidal sites around this island; by December 1984 it had spread to Maui and was being washed up in windrows at Launuipoko Beach; in 1985 it appeared on the islands of Lanai and Molokai (Russell, 1992; Russell and Balazs, 1994). The species has yet to be reported from the islands of Hawaii or Kahoolawe (Abbott, 1999; University of Hawai’i at Manoa, 2001). In 1999, it was common on the islands of Oahu and Maui, but only appeared to bloom at discrete locations (Smith et al., 2002). During these surveys, H. musciformis was not common near the site of initial introduction in Kaneohe Bay and was found in fairly low abundance at only 1 of 15 sites sampled in the bay.
Inshore coastlines and reefs in the tropical and subtropical eastern, central and western Pacific are potentially susceptible to invasion by H. musciformis. Introduction to Hawaii from Florida was an intentional act, and any similar movement to new areas would constitute a significant invasion risk. After becoming established in Hawaii, H. musciformis began growing among Eucheuma and contaminated shipments of Eucheuma exported live to other countries in the Pacific (Russell and Balazs, 1994).
Boat and vessel traffic does not appear to be a high risk vector for medium to long distance translocation of this species as the species is not recorded as a fouling species. Boating has been attributed as a possible vector for inter-island dispersal in Hawaii (Russell and Balazs, 1994), but this may be from drifting plants becoming entangled in hull appendages, anchors etc.
In Hawaii on calm intertidal and shallow subtidal reef flats, tidepools and on rocky intertidal benches; frequently attached to species of Sargassum and Acanthophora spicifera, but also epiphytic on various other algae or directly attached to sandy flat rocks (Abbott, 1999; University of Hawai’i at Manoa, 2001).
The life history of H. musciformis is a triphasic alternation of generations, with isomorphic tetrasporophytes and dioecious gametophytes and a diploid carposporophyte developing on the female gametophyte.
Smith et al. (2002) did not observe sexual reproduction in plants examined during their 1999 survey in Hawaii. However, the species was found to propagate vegetatively in all size classes examined (0.5, 1.0, 2.0, 3.0, 4.0 cm long), with the greatest success observed in the smallest fragments.
H. musciformis plants attached by branch hooks to other plants can reach a biomass that results in the majority of the plant being detached from the host plant by wave action or other physical disturbance, leaving the “hooks” behind (Smith et al., 2002). These hooks can rapidly regrow into new plants. The detachment of plants from hosts also facilitates dispersion of the species as drift.
Physiology and Phenology
In Brazil, fertile tetrasporophytes occurred throughout the year, varying form 20-99% of the population (Schenkman, 1989). Highest frequencies were observed in months when the highest biomass was measured (e.g. June-August). In this study, cystocarpic plants were rare and found only four times during 23 months of regular observation. Tetrasporophytes were also found to predominate, with fertile gametophytes rare in India (Rao, 1977). More recent investigations in Rio de Janeiro State, Brazil, suggested that asexual reproduction predominated over sexual reproduction, with more vegetative than reproductive thalli under environmentally stressful conditions for growth such as high and low water temperatures and more hours of sunlight (Reis and Yoneshigue-Valentin, 2000). Cystocarpic plants were only collected from intertidal epilithic populations.
Phycocolloid content measured in H. musciformis in Brazil varied from 48-66% of the dry weight, with maximum yields in autumn and spring, compared with 16-48% dry weight measured elsewhere (Schenkman, 1989). From studies in Brazil, water movement, desiccation, low salinity, and extreme water and air temperatures were suggested to be the main abiotic factors that influenced the viscosity and yield of carrageenan (Reis et al., 2008). Adverse environmental factors were also proposed as causing plants to produce more viscous carrageenan as a protective defence.
H. musciformis grows as an epiphyte on Acanthophora spicifera and Laurencia scoparia in Brazil (Schenkman, 1989). In Hawaii, H. musciformis has occupied a similar niche, growing as an epiphyte on the alien Acanthophora spicifera and the native Laurencia nidifica, a species partly displaced by A. spicifera (Russell, 1992). The species is also often found as an epiphyte on Sargassum echinocarpum and Sargassum polyphyllum (University of Hawai’i at Manoa, 2001).
In Hawaii, when abundant, H. musciformis has also been commonly found to co-occur with Ulva fasciata, a weedy species from a genus known to require high nutrient flux for growth (Smith et al., 2002).
Growth rates of H. musciformis have been measured to increase as a function of irradiance (up to 40 µmol photons m-2 s-1), but above this there was light saturation and growth rates were unchanged (Yokoya et al., 2007). Highest growth rates were observed in temperatures of 20-25oC under long (14:10 h LD) and short (10:14 h LD) photoperiods.
In Brazil, H. musciformis biomass was found to be controlled by several factors, notably seawater temperature, diurnal lower spring tides on sunny days accompanied by calm seas soon followed by rough water, and grazing (Schenkman, 1989).
Guist et al. (1982) reported that growth rates were highest when cultures were supplemented with nitrogen and phosphorus.
After its introduction into Hawaii, H. musciformis, along with the previously introduced alien seaweed Acanthophora spicifera, became a prominent food source for green turtles (Chelonia mydas) (Russell and Balazs, 1994). Fish and crustaceans are also reported to graze on the species (Russell and Balazs, 1994) and, in Brazil, gammarid amphipods and sea-hares (Aplysia spp.) (Schenkman, 1989).
In experiments to determine the feeding preferences of herbivorous fish, of 20 seaweeds studied, H. musciformis was not one of the five species grazed (Ganesan et al., 2006b).
H. musciformis is prone to fragment, is readily dislodged from its host and can regenerate vegetatively. It can therefore be dispersed locally by water currents, wave action and tidal flows. Drifting fragments re-attach to other algae, especially Sargassum, which can detach during storms and float long distances ('rafting') carrying Hypnea along (Russell and Balazs, 1994; University of Hawai’i at Manoa, 2001).
Although there are no published reports of H. musciformis as a fouling species on boats or other vessels, the spread of Hypnea between islands in Hawaii does not conform with prevailing surface currents and boat traffic was implicated, particularly as first occurrences were within or near harbours (Russell and Balazz, 1994). Entanglement of drifting plants around boat hull appendages, such as propellers or rudders, anchoring or fishing gear could enable translocation without plants growing directly on the boat hulls.
H. musciformis was intentionally introduced from Florida to Kaneohe Bay, Oahu in the Hawaiian Islands in 1974 for marine agronomy experiments (Russell,1992; Smith et al, 2002).
H. musciformis has become a significant component in the diets of green turtles in Hawaii, sometimes representing close to 100% of the seaweed biomass found in their stomachs (Russell and Balazs, 1994).
In Hawaii, before 1950, a simple association of Laurencia spp. with Hypnea cervicornis as an epiphyte commonly occurred on inshore reefs (Russell, 1992). After its introduction after 1950, Acanthophora spicifera invaded this niche in competition with Laurencia, but enhanced the productivity of H. cervicornis and the reef as a whole. H. musciformis both epiphytises Acanthophora and competes with H. cervicornis, further increasing the productivity of reefs where they occur (Russell, 1992). The consequence of the higher growth is increased detachment of both host and epiphyte, leading to increased drift and windrows of seaweed on nearby beaches.
On Maui in the Hawaiian Islands, H. musciformis is often found in large, nearly unialgal mats cast ashore in windrows up to 0.5 m high, and the species can represent nearly 2/3 of the algal biomass (Abbott, 1999; University of Hawai’i at Manoa, 2001). This drift is considered a malodorous pest by both local inhabitants and tourists.
Hypnea species have been used for food and for the production of phycocolloids (Hoppe, 1969; Masuda et al., 1997). The phycocolloid carrageenan is a red algal galactan used as a texturing agent, with gelling and thickening properties for food and non-food applications, that is in increasing demand (Reis et al., 2008). The cell wall constituents of various Hypnea species, including H. musciformis, have been found to include kappa carrageenans (Santos and Doty, 1969). Gametophytes and tetrasporophytes of H. musciformis both produce the same type of carrageenan (McCandless, 1981). H. musciformis has been exploited as a commercial source of kappa carrageenan, in both Brazil and India (Faccini and Berchez, 2000; Ganesan et al., 2006a).
H. musciformis was introduced to Hawaii as a potential species for farming because of its production of kappa carrageenan, its rapid growth rate, its ability to colonise new areas, and its broad environmental tolerance (Russell and Balazs, 1994).
H. musciformis has become a significant food source for green turtles (Chelonia mydas) in the Hawaiian Islands (Russell and Balazs, 1994).
In Hawaii, H. musciformis is differentiated from other Hypnea species by the flattened, broad hooks at ends of branches that coil around axes of other algae (Abbott, 1999). Apices of other species, such as H. cervicornis and H. valentiae, may curve, but are narrow and not tendril-like.
The genus Hypnea is known as a taxonomically difficult genus (e.g. Abbott, 1997) due to its wide geographic distribution and the morphological similarity of many subgeneric taxa. The genus has yet to be the subject of a global critical review, either using classical morphological techniques or molecular sequencing. The name Hypnea musciformis has been applied widely, but numerous applications of the name are now considered incorrect. For example, in Japan, H. musciformis sensu Okamura (1909) is now considered to be H. japonica Tanaka, distinguished by its size and texture and the absence of numerous, short proliferations (Tanaka, 1941; Yamagishi and Masuda, 1997). In Taiwan, most branches of H. japonica have straight or curved tips, with the presence of tendrils not as common as in H. musciformis (Chiang, 1997).
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
As with Acanthophora spicifera, the other widespread and successful invasive macroalgal species introduced to Hawaii, the abundance, propensity to dislodge and fragment ,and the ability of H. musciformis to regenerate vegetatively from small fragments would render eradication all but impossible once the species is established.
No reports on efforts to control H. musciformis have been seen, but the chances of success are considered low due to the propensity of plants to fragment and regenerate from small fragments, unless isolated plants are detected before populations become established.
Any shipments of live seaweed, such as Eucheuma, should be checked for contamination by H. musciformis to avoid inadvertent transfer. Anchor chains, anchor lockers and fishing gear should be cleaned of entangled algae if moving out of areas of known Hypnea presence.
There are still taxonomic uncertainties within the genus Hypnea and more molecular studies are needed to assist in unravelling species and species relationships and geographical species distribution. At the species level, the conspecificity of Mediterranean, tropical Atlantic and Indian Ocean populations of H. musciformis seems worthy of further investigation.