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Pacific Mosquitofern (Azolla filiculoides) Ecological Risk Screening Summary

U.S. Fish and Wildlife Service, web version – 4/2/2017

Photo: Daniel J. Layton. Licensed under Creative Commons BY-SA 3.0. Available:

https://commons.wikimedia.org/wiki/File:Azolla_filiculoides_MUN.jpg.

1 Native Range and Status in the United States

Native Range From CABI (2014):

“According to Lumpkin and Plucknett (1980), A. filiculoides is native to the Rocky Mountain

states of the western USA and Canada, through Central America and to most of South America.”

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From EOL (2017):

“Azolla filiculoides was native in England and Europe in interglacial periods - fossils have been

found in Suffolk, Netherlands, Germany and Russia.”

Status in the United States From CABI (2014):

“According to Lumpkin and Plucknett (1980), A. filiculoides is native to the Rocky Mountain

states of the western USA and Canada, through Central America and to most of South America.”

From FAO (2015):

“Azolla filiculoides introduced to Hawaii (All the main islands) from South America”

Discrepancies exist as to the native or invasive status of this species throughout the United

States. See Section 5 Distribution Within the United States for more details.

Means of Introductions in the United States No clear statement of means of introduction into Hawaii was found. However, in other areas it

was introduced through ballast water, escape from ornamental gardens, and intentional release

(FAO 2015; CABI 2014).

Remarks From CABI (2014):

“Further spread is likely as A. filiculoides continues to be sold in nurseries as a fish pond plant.

In Africa and Europe, dispersal between countries will no doubt continue due to the movement

of waterfowl, which can spread plant fragments between bodies of water. A. filiculoides will

continue to invade countries where the presence of eutrophic waters, lack of natural enemies and

an unregulated nursery trade will contribute to its status as a weed.”

From EOL (2017):

“Azolla can be placed in its own family, Azollaceae, but is often included with Salvinia in the

family Salviniaceae. Salviniaceae and Marsileaceae (Marsilea, Pilularia and Regnellidium) form

a monophyletic group of water ferns, which are all heterosporous, ie. produce two kinds of

spores, large female megaspores and small male microspores. Many fossil species of Azolla are

known from the Upper Cretaceous. Today there are only 6 or 7 species in this genus. Azolla

species are difficult to identify because high magnification is required to see the distinguishing

characters clearly. In addition, the plants are often sterile and thus lack most of the features

essential for identification. This has led to many misidentifications, confused taxonomy and thus

uncertainty over species distributions.”

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“Azolla caroliniana and A. mexicana are very similar to A. filiculoides. Although A. filiculoides

is the common species in western Europe, both the others have been recorded, though some of

the identifications are questionable. All three species are native in the Americas. They differ

principally in:

- the number of cells in the hairs on the upper leaf lobes - A. filiculoides has single-celled hairs

whereas those of A. caroliniana and A. mexicana have at least 2 cells (light microscope required)

- the nature of the surface of the megaspore (female spore) – A. filiculoides has megaspores with

a warty surface, while those of A. caroliniana and A. mexicana are not warty (scanning electron

microscope needed)”

2 Biology and Ecology

Taxonomic Hierarchy and Taxonomic Standing From ITIS (2015):

“Kingdom Plantae

Subkingdom Viridiplantae

Infrakingdom Streptophyta

Superdivision Embryophyta

Division Tracheophyta

Subdivision Polypodiophytina

Class Polypodiopsida

Subclass Polypodiidae

Order Salviniales

Family Azollaceae

Genus Azolla

Species Azolla filiculoides Lam.”

“Taxonomic Status:

Current Standing: accepted”

Size, Weight, and Age Range From CABI (2014):

“A. filiculoides is a small aquatic heterosporous fern, rarely larger than 25 mm (O'Keeffe,

1986).”

From EOL (2017):

“Life Expectancy

Annual”

Environment No information on environmental requirements of Azolla filiculoides was found.

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Climate/Range From CABI (2014):

“Its native range is characterized by warm, tropical climates with humid summers and mild

winters.”

“Climatic requirements include suitably warm months for sporocarp development, adequate

radiation and light intensity for vegetative growth, and adequate amounts of rainfall to prevent its

aquatic habitat from drying up. This water fern of tropical origin is thought to have evolved a

cold-tolerant strain since its introduction into Britain (Janes, 1998b) and South Africa

(McConnachie, 2003). A. filiculoides may be able to survive temperatures as low as -10ºC before

death occurs.”

Distribution Outside the United States Native From CABI (2014):

“According to Lumpkin and Plucknett (1980), A. filiculoides is native to the Rocky Mountain

states of the western USA and Canada, through Central America and to most of South America.”

Introduced

From FAO (2015):

“Azolla filiculoides introduced to south Africa from South America.”

“Azolla filiculoides introduced to Cook Islands from South America”

“Azolla filiculoides introduced to Ireland from Not specificed”

“Azolla filiculoides introduced to Netherlands from Brazil.”

From CABI (2014):

“It has been introduced to Europe, North and sub-Saharan Africa, China, Japan, New Zealand,

Australia, the Caribbean and Hawaii.”

From EOL (2017):

“Distribution in Egypt:

Nile region (Delta).”

Means of Introduction Outside the United States From FAO (2015):

“Reasons of Introduction: 1) accidental, 1) ornamental”

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From CABI (2014):

“The species may have been accidentally transported in ballast tanks of ships, in water with fry,

or directly as an ornamental. Janes (1998a) noted the deliberate introduction of the plant as an

ornamental into Europe through mainland Britain at the end of the 19th century. Possibly as a

result of its various transport routes, A. filiculoides appeared independently in different places at

almost the same time. It then spread across nearly all of Europe.”

“A. filiculoides was introduced into Asia from East Germany in 1977 as an alternative to the cold

susceptible native strain of A. pinnata, used as a green manure in the rice industry (Lumpkin and

Plucknett, 1982). It was introduced to Africa in 1948 as an aquarium plant (Oosthuizen and

Walters, 1961; Jacot-Guillarmod, 1979).”

Short Description From CABI (2014):

“The Azolla macrophyte consists of a main rhizome, which branches into secondary rhizomes.

These all bear alternately arranged small leaves. Ventrally, unbranched adventitious roots hang

down into the water from nodes.”

From Hussner (2010):

“A. filiculoides is a heterosporous, up to 2.5 (10) cm large floating fern (Figs. 1-5 [in source

material]). Azolla plants are polygonal or triangular in shape (Lumpkin and Plucknett 1980). The

sporophytes consist of two-lobed leaves and rhizomes. The lower lobes of the leaves are usually

larger than the upper. Svenson (1944) described the lower lobes as so adapted for floating the

plant, that only the lower surface of these lower lobes comes in contact with water.”

“The plants are dark green to reddish and float on the water surface, either individually or in

mats, which can reach a thickness of up to 20 cm (McConnachie et al. 2004).”

Biology From CABI (2014):

“The genus is unique in that it grows in association with a heterocystous cyanobacterium (blue-

green alga), Anabaena azollae Strasburger (Nostocales: Nostocaceae), which is located in

cavities in the dorsal leaf-lobes (Ashton and Walmsley, 1984). This symbiotic association is the

only one known between a pteridophyte and a cyanobacterium (Ashton and Walmsley, 1984).

[…] Nutrients are absorbed directly from the water by the roots. In very shallow water, however,

the roots may touch the soil thus deriving nutrients from it (Wagner, 1997).”

“A. filiculoides is able to undergo rapid vegetative reproduction throughout the year by the

elongation and fragmentation of the small fronds, and under ideal conditions, the daily rate of

increase can exceed 15% with the doubling time being every 4-5 days (Lumpkin and Plucknett,

1982). Under favourable environmental conditions, A. filiculoides undergoes sexual

reproduction. Pairs of sporocarps are formed from a ventral lobe initial of a lateral branch. The

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sporocarps are of two types, male microsporocarps and female megasporocarps (Ashton, 1982;

Wagner, 1997). There is usually a pair of either microsporocarps or megasporocarps, but one of

each may be present (Moore, 1969). Microsporocarps are approximately 1.5 mm in diameter,

containing 8-130 microsporangia (Wagner, 1997). Within each microsporangium there are 64

microspores, which are, in turn, aggregated into 3-10 massulae (Moore, 1969). Megasporocarps

are approximately 0.5 mm in diameter, each producing a single megasporangium (Wagner,

1997). A single megaspore, which contains a small colony of Anabaena azollae is contained

within the megasporangium (Wagner, 1997). Upon reaching maturity, both micro- and

megasporocarps dehisce. Microsporangia release spongy masses of massulae into the water,

which attach to megasporocarps via barbed, protruding appendages (glochidia) (Lumpkin and

Plucknett, 1980). These entanglements usually sink to the bottom of a water body and, after a

period of dormancy, the micro- and megaspores will germinate to form prothalli (Wagner, 1997).

Ciliated, male gametes (antherozoids) develop in antheridia on the male thallus and female

gametes (oospheres) develop in archegonia on the female thallus. After fertilization of the

oospheres by the antherozoids, an embryo develops (Moore, 1969). Ashton (1982) found

megaspore germination to be affected by desiccation (desiccation for >40 days greatly reduced

germination); turbulence (severe turbulence lowered germination levels to a low 6%);

photoperiod; light intensity; and pH (no germination occurred at pH levels <4.5 or >9.5).”

“A. filiculoides in its native areas (South America and western North America) is a plant of slow

flowing streams and rivers, ponds and lakes (Reed, 1962; Lumpkin and Plucknett, 1980; Ashton,

1982).”

Human Uses From CABI (2014):

“Members of the genus Azolla are utilized throughout the world for a wide variety of purposes

besides its widespread uses as an ornamental in fish ponds and tanks (Lumpkin and Plucknett,

1980; 1982). A. filiculoides is used as a green manure in rice paddies, mainly in Asia, as an

inhibitor of weed growth in rice cultivation in China and Vietnam (Kröck and Alkämper, 1991),

and as an alternative high protein fodder for cattle, swine, poultry and fish, and possibly as an

alternative food source for humans, again, mainly in Asia. It has also been used as a nitrate-rich

compost which potentially increases soil organic nitrogen levels and cation exchange capacity. It

is used for purification of water, removal of heavy metals (Sanyahumbi et al., 1998) and removal

of nitrogen and phoshorous from wastewater (Forni et al., 2001). It has also been used variously

as an ingredient in soap production, a cure for sore throats and as a control for mosquitoes in

southern India as complete mats disrupt larval development (Rajendran and Reuben, 1991).”

Diseases No information on diseases of Azolla filiculoides was found.

Threat to Humans From Hussner (2010):

“There are no human health effects known.”

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From EOL (2017):

“[…] hazard to children and animals when cover is dense and gives the appearance of solid

ground”

From Chamier et al. (2012):

“Azolla filiculoides, which is known to be nitrogenfixing, has a symbiotic relationship with

cyanobacteria, which produce the neurotoxic non-protein amino acid β-methylaminol-alanine

(BMAA). Consumption of BMAA causes serious neurodegenerative disease such as

amyotrophic lateral sclerosis/parkinsonism-dementia complex (AL-SPDC) (Cox et al.,

2003). Biomagnification of BMAA tin the Guam ecosystem, has increased the incidence of

amyotrophic lateral sclerosis in humans 50- to 100-fold (Cox et al., 2003).”

3 Impacts of Introductions From FAO (2015):

“Type of Ecological effects: Adverse”

From CABI (2014):

“The economic impact of A. filiculoides in South Africa was examined by McConnachie et al.

(2003). Thick mats on reservoirs and slow-moving water bodies caused economic losses to

water-users. Among those water-uses most seriously affected were farming (71%), recreational

(24%), and municipal (5%). On average, A. filiculoides was found to cause on-site damages of

US$589 per hectare per year.”

“In eutrophic water systems, A. filiculoides grows rapidly, easily outcompeting indigenous

vegetation. Decaying root and leaf matter below a mat of A. filiculoides, and the lack of light

penetration, creates an anaerobic environment. Not only can very little survive under such

conditions, but the quality of drinking water is reduced, caused by bad odours, colour and

turbidity (Hill, 1997). Cases have been reported where both livestock and game farmers have lost

animals due to them refusing to drink from infested water bodies or drowning as a result of

mistaking the mat for solid ground.”

“A. filiculoides infestations may form thick mats (5-20 cm thick), on water bodies up to 10

hectares in size (McConnachie et al., 2003). Such infestations have been shown to severely

impact the biodiversity of aquatic ecosystems and have serious implications for all aspects of

water utilization (Gratwicke and Marshall, 2001).”

“One of the last remaining habitats of the endangered fish species, the eastern Cape rocky

(Sandelia bainsii Castelnau, 1861; Anabantidae) in South Africa, had become so overgrown with

the weed that had the biological control programme not been so successful, S. bainsii faced

extinction.”

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4 Global Distribution

Figure 1. Known global distribution of Azolla filiculoides. Map from GBIF Secretariat (2015).

Locations in open ocean, and not on islands, were considered erroneous and not included as

source locations in the climate match.

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5 Distribution Within the United States

Figure 2. Known distribution of Azolla filiculoides in the United States. Areas in green report A.

filiculoides as native, those in blue report A. filiculoides as invasive. Map from USDA, NRCS

(2015).

Figure 3. Known distribution of Azolla filiculoides in the United States and Canada. Brown

areas consider the species to be native, pink areas consider the species non-native. Map from

NatureServe (2015).

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Figure 4. Known distribution of Azolla filiculoides in the United States. The brown area

indicates the native range of A. filiculoides in the United States. Map from USGS (2017).

Figure 5. Known distribution of Azolla filiculoides in the United States. Map created with data

from BISON (2017).

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6 Climate Matching Summary of Climate Matching Analysis The climate match for Azolla filiculoides was low to medium in New England, the upper

Midwest and some areas of the Gulf States. It was very high everywhere else. The Climate 6

score (Sanders et al. 2014; 16 climate variables; Euclidean distance) for the contiguous U.S. was

0.677, high, and individually high in all states except Maine, Minnesota, North Dakota, South

Dakota, Vermont, Wisconsin, and Wyoming.

Figure 6. RAMP (Sanders et al. 2014) source map showing weather stations selected as source

locations (red) and non-source locations (grey) for Azolla filiculoides climate matching. Source

locations from GBIF Secretariat (2015), BISON (2017), and USGS (2017).

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Figure 7. Map from RAMP (Sanders et al. 2014) climate matches for Azolla filiculoides in the

contiguous United States based on source locations reported by GBIF Secretariat (2015), BISON

(2017), and USGS (2017). 0 = Lowest match, 10 = Highest match.

The High, Medium, and Low Climate match Categories are based on the following table:

Climate 6: Proportion of

(Sum of Climate Scores 6-10) / (Sum of total

Climate Scores)

Climate

Match

Category

0.000<X<0.005 Low

0.005<X<0.103 Medium

>0.103 High

7 Certainty of Assessment The certainty of assessment is high. There was an abundance of quality information available for

Azolla filiculoides. There are many records of introductions and the negative economic and

ecological impacts.

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8 Risk Assessment Summary of Risk to the Contiguous United States The history of invasiveness is high. Azolla filiculoides is native to the western areas of North,

Central, and South America. It has spread to every other continent except Antarctica and has had

negative impacts in some locations. Climate match is 0.467, high. The overall match did include

areas within the native range of A. filiculoides but eastern areas and around the Great Lakes basin

(areas outside the native range) also had high climate matches. Due to the high history of

invasiveness and the areas of high climate match outside of the native range in the United States,

the overall risk assessment is high.

Assessment Elements History of Invasiveness (Sec. 3): High

Climate Match (Sec. 6): High

Certainty of Assessment (Sec. 7): High

Remarks/Important additional information Azolla filiculoides is native to western

sections of the country.

Overall Risk Assessment Category: High

9 References Note: The following references were accessed for this ERSS. References cited within

quoted text but not accessed are included below in Section 10.

BISON. 2017. Biodiversity Information Serving Our Nation (BISON). United States Geological

Survey. Available: https://bison.usgs.gov. (February 2017).

CABI. 2014. Azolla filiculoides [original text by Martin Hill]. In Invasive Species Compendium.

CAB International, Wallingford, UK. Available: http://www.cabi.org/isc/datasheet/8119.

(March 2015).

Chamier, J., K. Schachtschneider, D. C. le Maitre, P. J. Ashton, and B. W. van Wilgen. 2012.

Impacts of invasive alien plants on water quality, with particular emphasis on South

Africa. Water SA 38(2):345–356.

Encyclopedia of Life (EOL). 2017. Azolla filiculoides Carolina mosquitofern. Available:

http://eol.org/pages/597510/details. (February 2017).

FAO (Fisheries and Agriculture Organization of the United Nations). 2015. Database on

introductions of aquatic species. FAO, Rome. Available:

http://www.fao.org/fishery/introsp/search/en. (March 2015).

GBIF Secretariat. 2015. GBIF backbone taxonomy: Azolla filiculoides Lam. Global Biodiversity

Information Facility, Copenhagen. Available: http://www.gbif.org/species/2650107.

(March 2015).

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Hussner, A. 2010. NOBANIS – invasive alien species fact sheet – Azolla filiculoides¬. Online

database of the European Network on Invasive Alien Species (NOBANIS). Available:

https://www.nobanis.org/. (March 2016).

ITIS (Integrated Taxonomic Information System). 2015. Azolla filiculoides Lam. Integrated

Taxonomic Information System, Reston, Virginia. Available:

http://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=1800

7. (March 2015).

NatureServe. 2015. NatureServe explorer: an online encyclopedia of life [web application].

Version 7.1. NatureServe, Arlington, Virginia. Available: http://explorer.natureserve.org.

(February 2017).

Sanders, S., C. Castiglione, and M. Hoff. 2014. Risk assessment mapping program: RAMP. U.S.

Fish and Wildlife Service.

USDA, NRCS. 2015. Azolla filiculoides. The PLANTS database. National Plant Data Team,

Greensboro, North Carolina. Available:

http://plants.usda.gov/core/profile?symbol=AZFI. (March 2015).

USGS (United States Geological Survey). 2017. Azolla filiculoides. USGS Nonindigenous

Aquatic Species Database, Gainesville, Florida.

https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=287. (February 2017).

10 References Quoted But Not Accessed Note: The following references are cited within quoted text within this ERSS, but were not

accessed for its preparation. They are included here to provide the reader with more

information.

Ashton, P. J. 1982. The autecolgy of Azolla filiculoides Lamarck with special reference to its

occurrence in the Hendrik Verword Dam catchment area. Doctoral dissertation. Rhodes

University, Grahamstown, South Africa.

Ashton, P. J., and R. D. Walmsley. 1984. The taxonomy and distribution of Azolla species in

southern Africa. Botanical Journal of the Linnean Society 89:239–247.

Cox, P. A., S. A. Banack, and S. J. Murch. 2003. Biomagnification of cyanobacterial neurotoxins

and neurodegenerative disease among the Chamorro people of Guam. Proceedings of the

National Academy of Science USA 100(23):13380–13383.

Forni, C., J. Chen, L. Tancioni, and M. Grilli Caiola. 2001. Evaluation of the fern Azolla for

growth, nitrogen and phosphorous removal from wastewater. Water Research

35(6):1592–1598.

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Gratwicke, B., and B. E. Marshall. 2001. The impact of Azolla filiculoides Lam. on animal

biodiversity in streams in Zimbabwe. African Journal of Ecology 38:1–4.

Hill, M. P. 1997. The potential for the biological control of the floating aquatic fern, Azolla

filiculoides Lamarck (red water fern / rooivaring) in South Africa. Report Number KV

100/97. Water Research Commission, Pretoria, South Africa.

Jacot-Guillarmod, A. 1979. Water weeds in southern Africa. Aquatic Botany 6:377–391.

Janes, R. 1998a. Growth and survival of Azolla filiculoides in Britain. Volume I. Vegetative

reproduction. New Phytologist 138(2):367–375.

Janes, R. 1998b. Growth and survival of Azolla filiculoides in Britain. Volume II. Sexual

reproduction. New Phytologist 138(2):377–384.

Kröck, T., and J. Alkämper. 1991. Azolla's contribution to weed control in rice cultivation. Plant

Research and Development 34:117–125.

Lumpkin, T. A., and D. L. Plucknett. 1980. Azolla: botany, physiology, and use as a green

manure. Economic Botany 34(2):111–153.

Lumpkin, T. A., and D. L. Plucknett. 1982. Azolla as a green manure: use and management in

crop production. Westview Press, Boulder, Colorado.

McConnachie, A. J. 2003. Post release evaluation of Stenopelmus rufinasus Gyllenhal

(Coleoptera: Curculionidae) - a natural enemy released against the red waterfern, Azolla

filiculoides Lamarck (Pteridophyta: Azollaceae) in South Africa. Doctoral dissertation.

University of the Witwatersrand, Johannesburg, South Africa.

McConnachie, A. J., M. P. de Wit, M. P. Hill, and M. J. Byrne. 2003. Economic evaluation of

the successful biological control of Azolla filiculoides in South Africa. Biological Control

28:25–32.

McConnachie, et al. 2004. [Source material did not give full citation for this reference.]

Moore, A. W. 1969. Azolla: biology and agronomic significance. Botanical Review 35:17–35.

O'Keeffe, J. H. 1986. Ecological research on South African rivers - a preliminary synthesis.

South African National Scientific Programmes Report 121:1–121.

Oosthuizen, G. J., and M. M. Walters. 1961. Control of water fern with diesoline. Farming in

South Africa 37:35–37.

Rajendran, R., and R. Reuben. 1991. Evaluation of the water fern Azolla microphylla for

mosquito population management in the rice-land agro-ecosystem of south India.

Medical and Veterinary Entomology 5(3):299–310.

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Reed, C. F. 1962. Distribution of Salvinia and Azolla in South America and Africa, in connection

with studies for control by insects. Phytologia 12(3):121–130.

Sanyahumbi, D., J. R. Duncan, M. Zhao, and R. van Hille. 1998. Removal of lead from solution

by the non-viable biomass of the water fern Azolla filiculoides. Biotechnology Letters

20(8):745–747.

Svenson, H.K. 1944. The new world species of Azolla. American Fern Journal 34(3):69–85

Wagner, G. M. 1997. Azolla: a review of its biology and utilization. The Botanical Review

63(1):1–25.