Arthurdendyus triangulatus (New Zealand flatworm)

Pictures

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Extended individual

The 'New Zealand flatworm', (Arthurdendyus triangulatus) extended and showing its speckled underside.

A.K. Murchie

Close-up

Close-up of a 'New Zealand flatworm', (Arthurdendyus triangulatus) extended and showing its speckled underside.

A.K. Murchie

Individual under plastic sheet

The 'New Zealand flatworm', (Arthurdendyus triangulatus), as typically found, under plastic sheeting.

A.K. Murchie

Individuals in a plastic jar

The 'New Zealand flatworm', (Arthurdendyus triangulatus), as collected within a plastic jar.

A.K. Murchie

Individuals in a plastic jar

Close-up of a 'New Zealand flatworm' (Arthurdendyus triangulatus), as collected within a plastic jar.

A.K. Murchie

Identity

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Preferred Scientific Name

Arthurdendyus triangulatus (Dendy, 1894) Jones and Gerard (1999)

Preferred Common Name

New Zealand flatworm

Other Scientific Names

Artioposthia triangulata (Dendy, 1894)
Geoplana triangulata Dendy, 1894

Local Common Names

Denmark: Newzealandsk fladorm
Faroe Islands: selendski flatmaðkurin
Germany: Neuseelandplattwurm
Iceland: Nýsjálenski flatorm
Norway: New Zealandsk flatorm
Sweden: Nyazeeländska plattmasken

Summary of Invasiveness

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A. triangulatus is a free-living terrestrial flatworm. Native to New Zealand, it was found outside its natural habitat in Belfast, Northern Ireland in 1963 (Ministry of Agriculture, Northern Ireland, 1963, 1964). The species is harmful because it is a predator of earthworms and a decline in earthworms could reduce soil fertility and earthworm-feeding wildlife. The flatworm is found in Ireland, Great Britain and the Faroe Islands. Although capable of active movement the flatworm has been spread mainly by the trade in containerised plants. Its tendency to shelter under debris on the soil surface and its sticky body, have facilitated inadvertent carriage on plant containers, agricultural equipment and soil. There have been several scientific reviews of the biology of A. triangulatus published (Blackshaw and Stewart, 1992; Cannon et al., 1999; Boag and Yeates, 2001). A. triangulatus is considered an indirect plant pest by the European and Mediterranean Plant Protection Organisation (EPPO) (IPPC-Secretariat, 2005).

Taxonomic Tree

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Domain: Eukaryota
Kingdom: Metazoa
Phylum: Platyhelminthes
Class: Turbellaria
Order: Tricladida
Family: Geoplanidae
Genus: Arthurdendyus
Species: Arthurdendyus triangulatus

Notes on Taxonomy and Nomenclature

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The classification of free-living flatworms is currently undergoing revision, in particular due to molecular phylogenetic studies. This classification follows Sluys et al. (2009).

Arthurdendyus triangulatus was originally described as Geoplana triangulata by Dendy (1894). Fyfe (1937) transferred it to the genus Artioposthia due to the presence of muscular gland organs (adenodactyli) in the genital atrium. Jones and Gerard (1999) subsequently erected the genus Arthurdendyus for planarians with elongate ovaries lateral to the male copulatory apparatus and a bell-shaped pharynx.

Description

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A. triangulatus is a large terrestrial flatworm measuring up to 10 mm wide and 200 mm in length when fully extended. However, the length is highly variable depending on the state of extension. The body is that of a flattened strap, narrowing towards the anterior. The colour is liver brown with a pale marginal fringe that extends from the underside. This fringe and the underside are beige and flecked with grey. The anterior head has a pink tinge with a row of minute black eye spots present on each side of the tip. The flatworm is covered in mucus and sticky to the touch. Non-specialist descriptions are given by Willis and Edwards (1977), Boag et al. (1994a) and Jones (2005). Egg capsules are shiny black and ovoid, typically measuring 4-8 mm in diameter.

Distribution

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A. triangulatus is widespread but relatively rare in its native range, which is restricted to the South Island in New Zealand. It has established itself in Ireland, Great Britain and the Faroe Islands but not so far in continental Europe. This is something of a puzzle as much of the horticultural plant trade to the British Isles and the Faroe Islands, the presumed method of transfer of these flatworms, passes through other countries, in particular the Netherlands. It was possibly introduced into Great Britain on plants collected by the Edinburgh Botanic Gardens since it was discovered there in 1965 (Boag et al., 1998b). Analyses of genetic variation in A. triangulatus using PCR-RFLP, suggests multiple introductions of A. triangulatus into the UK (Dynes et al., 2001). This contention is supported by the presence of several other non-indigenous flatworms in the UK and Ireland, e.g. Australoplana sanguinea, Kontikia andersoni and A. albidus. Therefore, the fact that this species has not established on continental Europe may be due to other factors such as climate. However, it would seem likely that at least some areas of continental Europe may be at risk from invasion by this species (Boag et al., 1995a).

Distribution Table

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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.

Last updated: 10 Jan 2020

Continent/Country/Region	Distribution	Origin	First Reported	Invasive	Reference	Notes
Europe
Faroe Islands	Present, Widespread	Introduced	1982	Invasive	Bloch (1992) Mather and Christensen (1992) Christensen and Mather (1998)	First record from the downpipes of the parliament building in Tórshavn
Iceland	Present, Only in captivity/cultivation	Introduced			Bloch (1992)	Reported from a glasshouse in Iceland. Either an isolated or unconfirmed report
Ireland	Present, Widespread	Introduced		Invasive	Anderson (1986) Hogan and Dunne (1996)	Summary of records in Ireland (both North and South)
United Kingdom	Present, Widespread	Introduced		Invasive	Boag et al. (1994) Willis and Edwards (1977) Jones and Boag (1996) Moore et al. (1998) Murchie et al. (2003)	Distribution in Scotland – mainly in the populated central belt from Glasgow to Edinburgh but also records from the islands
-Northern Ireland	Present, Widespread	Introduced	1963	Invasive	MINISTRY OF AGRICULTURE, NORTHERN IRELAND. (1963)	Northern Ireland -first record outside New Zealand
Oceania
New Zealand	Present, Widespread	Native			Dendy (1894) Johns et al. (1998)	Specimens collected from Christchurch, Rapaki and Ashburton on the South Island

History of Introduction and Spread

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A. triangulatus was first found outside of New Zealand in Belfast, Northern Ireland, in 1963. Exactly how this species came to be in Belfast is unknown but it is thought to have been carried inadvertently with ornamental plants such as daffodils, roses or rhododendrons (Willis and Edwards, 1977; Blackshaw and Stewart, 1992). A similar situation is likely to have happened in Scotland. The first record was from the Royal Botanic Gardens in Edinburgh, and many flatworm records have been associated with botanic gardens, garden centres and nurseries (Boag and Yeates, 2001). As an example, 22 live flatworms (though not A. triangulatus) were found within a Dicksonia antarctica (tree fern) from Australia (Parker et al., 2005). The spread of A. triangulatus to the relatively isolated Faroe Islands, was thought to have occurred via goods from Scotland, although direct transmission from New Zealand cannot be excluded (Mather and Christensen, 1992).

Introductions

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Introduced to	Introduced from	Year	Reason	Introduced by	Established in wild through		References	Notes
Introduced to	Introduced from	Year	Reason	Introduced by	Natural reproduction	Continuous restocking	References	Notes
Faroe Islands		1982			Yes		Bloch (1992); Mather and Christensen (1992)	May have been introduced accidentally from Scotland or New Zealand
Northern Ireland	New Zealand	1963	Horticulture (pathway cause)		Yes		Ministry and Northern (1964)	Accidental introduction (Blackshaw and Stewart, 1992). First confirmed record of this species outside of its native range in New Zealand
UK		1965	Horticulture (pathway cause)		Yes		Boag et al. (1994a); Boag et al. (1994b); Willis and Edwards (1977)	To Scotland and England, associated with botanic gardens and nurseries

Risk of Introduction

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A. triangulatus has been present in Ireland and Great Britain since the early 1960s. It has become almost ubiquitous within the populated areas of Northern Ireland (Moore et al., 1998) and has a cosmopolitan distribution in Scotland (Jones and Boag, 1996; Boag et al., 2006a). The colonisation of the Scottish and Faroe Islands demonstrates how this species can be easily spread from infected areas to relatively isolated regions. The risk of introduction of A. triangulatus is most severe in local regions of Ireland, Scotland, England and Wales. Unless steps are taken to limit local movement of this species, it is likely to continue to spread in Ireland and Great Britain.

A. triangulatus has not established on continental Europe, despite being present in Ireland and GB since the 1960s. Climate matching would suggest that A. triangulatus could establish in large areas of north-western continental Europe such as Denmark, Germany, the Netherlands and Belgium (Boag et al., 1995a; Boag and Yeates, 2001). The fact that A. triangulatus has not already been found on continental Europe is a puzzle and may suggest more stringent environmental conditions necessary for establishment. Outside of Europe, there are regions in the United States, Canada, Japan, Argentina and Australia, which are theoretically at risk from invasion by this species (Boag et al., 1995b). Perhaps of particular risk is Tasmania, which would be climatically similar to the South Island of New Zealand. A. vegrandis, another New Zealand species, has been found on the Australian subantarctic Macquarie Island (Greenslade et al., 2007).

Habitat

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Typically found under debris on the soil surface, mostly in gardens or on the margins of agricultural land. Increasingly found in pasture in Northern Ireland (Murchie et al., 2003) and in potato fields in the Faroe Islands (Christensen and Mather, 1998). A. triangulatus may be active on the soil surface at night.

Habitat List

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Category	Sub-Category	Habitat	Presence	Status
Terrestrial
Terrestrial	Managed	Cultivated / agricultural land	Principal habitat	Harmful (pest or invasive)
Terrestrial	Managed	Managed forests, plantations and orchards	Secondary/tolerated habitat	Harmful (pest or invasive)
Terrestrial	Managed	Managed grasslands (grazing systems)	Principal habitat	Harmful (pest or invasive)

Hosts/Species Affected

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A. triangulatus is a predator of earthworms and therefore an indirect plant pest. That is, the flatworm does not attack plants directly but by reducing earthworm numbers, soil fertility and hence plant productivity are also reduced. The concept of an indirect plant pest has been accepted by the European and Mediterranean Plant Protection Organisation (EPPO) (Schrader and Unger, 2003; IPPC-Secretariat, 2005; Murchie, 2008).

List of Symptoms/Signs

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Sign	Life Stages	Type
Roots / reduced root system
Whole plant / dwarfing

Biology and Ecology

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Reproductive Biology

As with other flatworms, A. triangulatus is a hermaphrodite. Mating has not been observed in this species but both male and female reproductive organs are fully functional (Fyfe, 1937; Baird et al., 2005b) suggesting that cross-fertilisation is the norm.

A. triangulatus produce shiny black ovoid egg capsules. These are extruded through the dorsal surface or the gonopore on the underside (Blackshaw and Stewart, 1992). In an experimental study, a maximum of nine egg capsules were produced during a 16 week period, equating to roughly one egg capsule every two weeks (Baird et al., 2005a). The size of egg capsules varies depending on the size and nutritional status of the adult. Baird et al. (2005a) gave the smallest egg capsule in their study as 2.5 mm x 2.4 mm (8 mg) with the largest as 8.0 mm x 5.6 mm (180 mg). Egg capsules are typically found in the same habitat as the adults. In the wild, in Northern Ireland, the main period of egg-laying is normally March to July, with a smaller peak in August to September. The time to hatch for egg capsules is dependent on temperature, taking 49 days at 10°C and 38 days at 14°C (Baird et al., 2000). Egg capsules contain between 1-14 juveniles, with an average of 6 (Blackshaw and Stewart, 1992; Christensen and Mather, 1997).

Unlike other flatworms, it is unlikely that A. triangulatus could reproduce by fragmentation as they are susceptible to any form of mechanical damage (Willis and Edwards, 1977).

Physiology and Phenology

Terrestrial flatworms possess few water-saving adaptations and therefore A. triangulatus is susceptible to desiccation (Blackshaw and Stewart, 1992). Flatworm presence at the soil surface shows a marked seasonality with a decline during the hottest months of July and August (AK Murchie, Agri-Food and Biosciences Institute, Northern Ireland, personal communication, 2009). It would seem that A. triangulatus migrate to the lower and cooler depths of the soil during these periods. Willis and Edwards (1977) record flatworms, presumably aestivating, from depths of 250-300 mm, tightly coiled within small chambers.

Nutrition

A. triangulatus feeds on lumbricid earthworms in the invaded areas. Little is known about its natural prey in New Zealand, although it is assumed to be megascolecid earthworms (Johns et al., 1998). The matter is complicated because much of New Zealand gardens and pasture have been colonised by European earthworm species (Stockdill, 1982). In laboratory tests, where A. triangulatus was presented with earthworm prey in Petri dishes, there was little evidence of direct preference for individual earthworm species (Stewart, 1993). Differential impacts on earthworm species observed in field sampling are likely due to earthworm niche characteristics, such as burrow width, which increase vulnerability to predation (Blackshaw and Stewart, 1992; Lillico et al., 1996). Anecic earthworms, which come to the soil surface, are particularly at risk (Jones et al., 2001). When no earthworms are available, A. triangulatus may occasionally feed on slugs (Gibson and Cosens, 2004).

Blackshaw (1991) found that A. triangulatus consumed 1.4 Eisenia fetida per week and converted 36% of the earthworm tissue into flatworm tissue while Yeates et al. (1998) reported a 53% food conversion efficiency. Lillico et al. (1996) gave a lower figure of 0.67 earthworms per week with a conversion rate of 10%. Baird et al. (2005a) worked on the basis of bodyweight and fed A. triangulatus at one-half of their bodyweight (c. 0.5 g) in E. fetida every two weeks, which gave a 12% reduction in weight over 100 days. The conversion of earthworm prey to egg capsule production was calculated as 13%.

Environmental Requirements

The main factors limiting A. triangulatus dispersal are soil temperature, soil moisture and the availability of prey (Boag et al., 1998a). Soil temperatures greater than 20°C are detrimental to A. triangulatus, with 100% mortality after 3 weeks (Blackshaw and Stewart, 1992). Similarly, consistent low temperatures of -2°C caused 100% mortality after 3 days, whereas at -1°C mortality had only reached c. 50% after 21 days (Scottish Executive Rural Affairs Department, 2000). There has been little quantitative work on the effects of soil moisture on A. triangulatus, although it is clearly important (Boag et al., 2005). Part of the reason for this, is that in the UK and Ireland, soil moisture and temperature are often correlated, with high temperatures corresponding to low soil moisture.

Climate

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Climate	Status	Description	Remark
Cs - Warm temperate climate with dry summer	Preferred	Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Rainfall Regime

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Summer
Winter

Notes on Natural Enemies

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Predatory ground beetles of the families Carabidae and Staphylinidae will prey on A. triangulatus (Blackshaw, 1996; Gibson et al., 1997) but it is unlikely that they will do so in sufficient numbers to limit flatworm spread. There are also consistent reports of birds and other generalist worm predators such as shrews feeding on flatworms (Cannon et al., 1999). However, it would seem that flatworms are not choice prey and are distasteful to most predators (Cannon et al., 1999). Arthur Dendy, who described A. triangulatus and in whose honour the genus is named, describes tasting two specimens of land planarian. He found it to be “an exceedingly unpleasant sensation” (Dendy, 1891). Ducks, geese and even ferrets are known to feed on them without ill effects (B Boag, The James Hutton Institute, UK, personal communication, 2013).

Little is known about the natural enemies of A. triangulatus in New Zealand, although they are presumed to be ground beetles and other flatworms. Planarivora insignis (Diptera: Keroplatidae) is a parasitoid of terrestrial flatworms in Tasmania (Hickman, 1965). It is possible that a similar species may exist in the native habitat of A. triangulatus.

Means of Movement and Dispersal

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Natural Dispersal (Non-Biotic)

In theory, A. triangulatus could be dispersed by floodwater washing along egg capsules or even adults but this is not considered a major mechanism for spread.

Vector Transmission (Biotic)

A. triangulatus may occasionally be carried sticking to domestic animals (Moore et al., 1998).

Accidental Introduction

A. triangulatus has predominantly been spread by movement of horticultural and garden plants (Cannon et al., 1999). Within infected regions, movement of garden plants, topsoil, manure and baled silage is the most probable means of transfer (Blackshaw and Stewart, 1992; Moore et al., 1998; Boag et al., 1999; Murchie et al., 2003).

Intentional Introduction

Intentional introduction of A. triangulatus is forbidden under national legislation (e.g. in the UK, The Wildlife and Countryside Act 1981, The Wildlife and Natural Environment Act (Scotland) 2011, and The Wildlife and Natural Environment Act (Northern Ireland) 2011).

There have been anecdotal stories about greenkeepers releasing flatworms in order to reduce earthworm casting on golf and bowling greens, but these are unsubstantiated.

Pathway Causes

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Cause	Notes	Long Distance	Local	References
Crop production	Possibly from Scotland to the Faroe Islands with potatoes, also via manure, silage & machinery	Yes	Yes	Boag et al., 1999; Mather and Christensen, 1992; Moore et al., 1998; Murchie et al., 2003
Horticulture	Movement of containerised plants	Yes	Yes	Blackshaw, 1992; Cannon et al., 1999; Dynes et al., 2001; Willis and Edwards, 1977
Landscape improvement	Movement of topsoil		Yes	Christensen and Mather, 1995
Nursery trade	Importation of containerised plants from New Zealand seems the most likely mechanism of invasion	Yes	Yes	Blackshaw and Stewart, 1992; Cannon et al., 1999; Dynes et al., 2001; Stewart and Blackshaw, 1993; Willis and Edwards, 1977
Ornamental purposes	Associated with botanic gardens	Yes		Boag et al., 1994a; Willis and Edwards, 1977

Pathway Vectors

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Vector	Notes	Long Distance	Local	References
Land vehicles	Could be moved on soil attached to farm equipment		Yes
Plants or parts of plants	Probably both adults and egg capsules could be introduced in this way	Yes	Yes	Blackshaw and Stewart, 1992; Cannon et al., 1999; Dynes et al., 2001; Willis and Edwards, 1977
Soil, sand and gravel	Local movement of topsoil and dung can facilitate flatworm spread		Yes	Murchie et al., 2003

Plant Trade

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Plant parts liable to carry the pest in trade/transport	Pest stages	Borne internally	Borne externally	Visibility of pest or symptoms
Bulbs/Tubers/Corms/Rhizomes	adults; eggs		Yes	Pest or symptoms usually visible to the naked eye
Growing medium accompanying plants	adults; eggs	Yes		Pest or symptoms usually visible to the naked eye
Roots	adults; eggs		Yes	Pest or symptoms usually visible to the naked eye

Plant parts not known to carry the pest in trade/transport
Leaves
Stems (above ground)/Shoots/Trunks/Branches

Impact Summary

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Category	Impact
Economic/livelihood	Negative
Environment (generally)	Negative

Economic Impact

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The economic impact of A. triangulatus is by reducing earthworm activity, which then limits plant growth. It is likely that the most serious impact will be in pasture. There are two reasons for this. First, A. triangulatus is commonest in relatively wet mild climates that are suited for grass production. Second, arable cultivation in itself is physically damaging to both earthworms and flatworms.

Results from a long-term field experiment into the effects of A. triangulatus on earthworms showed an overall reduction of 20% in earthworm biomass comparing high and low density flatworm plots (Murchie and Gordon, 2013).

Obtaining a good estimate of the economic value of earthworm activity in pastures is difficult due to the many factors involved and also because many yield experiments have been limited to pot studies. Perhaps ironically, some of the best field data comes from the introduction of European lumbricid earthworms to New Zealand and Australian pastures. Stockdill (1982) gave an increase in grass yield of between 9 and 29% in an area of a field in which one species of European earthworm (Aporrectodea caliginosa) had established for 10 years. In soil cores inoculated with Aporrectodealonga grass yield increased by up to 61%, although the results were highly variable across the ten Australian locations (Baker et al., 1999). In Ireland, reclaimed peat soils seeded with perennial ryegrass and white clover, treated with slurry and inoculated with earthworms showed an increase in herbage yield of 49% compared to similar plots without earthworms (Curry and Boyle, 1987).

Taking an estimate that earthworms contribute 20% towards grass yield and that A. triangulatus predation reduces earthworm biomass by 20%, the effect of A. triangulatus colonisation could be a 4% reduction in grass yield. Boag and Neilson (2006) calculated that the New Zealand flatworm could conservatively cost Scottish farmers c. £17M.

As highlighted by Alford (1998), one of the main economic effects of flatworm infestation could be limitations on trade. This applies to international trade and also to local trade in the sense that a garden centre, nursery or topsoil distributor may be held liable for distributing a harmful invasive species.

Environmental Impact

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Impact on Habitats

A flatworm-induced reduction in earthworm populations could change soil structure and hydrology (Haria, 1995; Haria et al., 1998) leading to poor soil drainage and encroachment of Juncus rushes in pasture (Alford, 1998). There is evidence of a build-up of dead organic matter on the soil surface at flatworm-infested sites (Blackshaw, 1995). Under apple trees, without herbicide treatments, A. triangulatus achieved densities of 9.3 m² and there was a build-up of thatch to a depth of 4 cm (Murchie and Mac an Tsaoir, 2006). Furthermore, it was speculated that this dense thatch provided an ideal microclimate for A. triangulatus.

Impact on Biodiversity

A. triangulatus is an invasive earthworm predator that directly reduces earthworm biodiversity. The extent to which A. triangulatus depletes earthworm populations varies across studies. Depletion of earthworms in relation to the presence of A. triangulatus was first noted by Blackshaw (1989), studying the effects of seaweed fertiliser on earthworms. The capability of A. triangulatus to reduce earthworm numbers was subsequently confirmed by field and laboratory studies (Blackshaw, 1990; Blackshaw, 1991; Blackshaw, 1995; Lillico et al., 1996; Blackshaw, 1997b; Blackshaw, 1997a). Perhaps the severest impact of A. triangulatus has been in the Faroe Islands, where the flatworm proved capable of locally eradicating earthworms within one year (Christensen and Mather, 1995), although this phenomenon may be restricted to horticultural or potato growing sites. In particular, the Faroese ‘reimavelta’ technique, which involves growing potatoes under inverted turf, restricted earthworm movement and provided ideal conditions for A. triangulatus predation (Mather and Christensen, 1992; Christensen and Mather, 1998). At other sites though, the impact of A. triangulatus has been less severe, with several reports of long-term coexistence (Boag et al., 1994b; Gibson et al., 1997) albeit with a reduced earthworm population (Cannon et al., 1999). Blackshaw (1995) considered that fluctuations in A. triangulatus and earthworms numbers from year to year, provided evidence of a predator-prey cycle.

It is increasingly clear that there is a hierarchy in earthworm vulnerability to A. triangulatus predation (Boag et al., 1994a; Lillico et al., 1996). Deep-living earthworms such as Octolasion cyaneum or endogeic species may be less susceptible to flatworm surface predation (Blackshaw, 1995; Boag et al., 1997), whereas anecic species that have semi-permanent burrows and feed on the surface may be most susceptible (Fraser and Boag, 1998). Multivariate analyses of earthworm species in two flatworm-infested fields and non-infested fields in Scotland, suggested that Aporrectodea caliginosa (endogeic), Aporrectodea longa (anecic) and L. terrestris (anecic) were most affected by A. triangulatus presence (Jones et al., 2001). In a replicated field experiment, there was a significant decrease in anecic earthworm biomass in plots with enhanced A. triangulatus populations, but no overall effect on epigeic or endogeic species (AK Murchie, Agri-Food and Biosciences Institute, Northern Ireland, personal communication, 2009). There is a threat therefore that A. triangulatus could deplete certain species, possibly to the point of local extinction, whilst maintaining themselves on less susceptible species. Furthermore, A. triangulatus are capable of surviving for over one year without feeding (Blackshaw, 1992; Baird et al., 2005b); therefore a residual population may remain in an area depleted of earthworm prey and prevent re-establishment of vulnerable species (Blackshaw and Stewart, 1992).

A decline in earthworms could have knock-on effects on earthworm-feeding wildlife (Alford, 1998). In the UK and Ireland, most vulnerable are badgers, hedgehogs, moles (not Ireland) and many familiar garden and farmland bird species (e.g. blackbirds, thrushes, rooks and lapwings). Earthworms are also an important food source for many invertebrates: e.g. carabid beeles (Symondson et al., 2000), testacellid snails and indigenous flatworm species. The only specific study on this topic was done on moles (Talpa europaea) in southwest Scotland. Boag (2000) found a significant negative relationship between the presence of A. triangulatus and that of moles.

Threatened Species

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Threatened Species	Conservation Status	Where Threatened	Mechanism	References	Notes
Lumbricus terrestris	No Details	Faroe Islands; UK	Predation	Blackshaw, 1990; Fraser and Boag, 1998; Jones et al., 2001; Lillico et al., 1996

Social Impact

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A. triangulatus is a garden pest spread by the movement of plants. Gardening is a popular hobby and many gardeners exchange plants through semi-formal networks such as gardening societies. Inadvertent spread of A. triangulatus has happened by this mechanism and therefore, where A. triangulatus is present, movement of containerised plants should be minimised.

Risk and Impact Factors

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Invasiveness

Proved invasive outside its native range
Has a broad native range
Highly mobile locally
Benefits from human association (i.e. it is a human commensal)
Long lived
Has high reproductive potential

Impact outcomes

Changed gene pool/ selective loss of genotypes
Damaged ecosystem services
Ecosystem change/ habitat alteration
Host damage
Modification of hydrology
Modification of nutrient regime
Negatively impacts agriculture
Negatively impacts livelihoods
Reduced native biodiversity
Threat to/ loss of native species
Negatively impacts trade/international relations

Impact mechanisms

Predation

Likelihood of entry/control

Highly likely to be transported internationally accidentally
Difficult to identify/detect as a commodity contaminant
Difficult/costly to control

Uses

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Economic Value

In theory, A. triangulatus could be a biological control for some earthworm species, e.g. invasive earthworms in North America. However, this would be dependent on limiting spread and given the adverse effects documented in the UK and Ireland, probably counter-productive.

Social Benefit

No obvious direct social benefit other than being a useful educational tool for invasive species: A. triangulatus, as a large and slimy earthworm predator, has caught the public imagination in the UK and Ireland.

The mucus of A. triangulatus is rich in proteins, which protect against predators, disease and the environment, as well as facilitating earthworm predation and consumption (McGee et al., 1998). It is possible that some of these proteins could have beneficial characteristics.

Environmental Services

A. triangulatus does not burrow but rather squeezes through gaps in the soil. It therefore does not confer the same aeration and drainage benefits as earthworm burrowing.

Diagnosis

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Diagnosis is by morphological features or species-specific DNA diagnostic primers. A. triangulatus is a distinctive species and microscope or molecular means for identification are rarely necessary. Jones (2005) provides user-friendly description of British terrestrial flatworms, including A. triangulatus.

Detection and Inspection

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A. triangulatus is mainly detected by visual inspection under plant pots, stones, wood, plastic sheeting and other debris on the soil surface (EPPO, 2001). The flatworm may also be detected by use of the expulsion techniques (e.g. formalin or mustard) used to assess earthworm populations (Gunn, 1992; Murchie et al., 2003). Shelter traps may be placed on the soil surface, these can be pieces of wood, tiles or plastic bags filled with soil. A sampling strategy to quantify the detection of the New Zealand flatworm was published by Boag et al. (2010).

Similarities to Other Species/Conditions

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A. triangulatus could be confused with other flatworm species but is considerably larger that the native Microplana flatworms in Ireland and GB. The ‘Australian flatworm’, Australoplana sanguinea is similar in body shape but is orange. Terrestrial leeches also have a cursory similarity but are segmented.

Prevention and Control

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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.

SPS Measures

A. triangulatus is considered an indirect plant pest by the European and Mediterranean Plant Protection Organisation (EPPO). The EPPO standard ‘Import requirements concerning A. triangulatus’ relate to the importation of containerised plants and specify: 1) plants should be grown on raised and slatted benches; 2) or come from an area free from A. triangulatus; 3) or a representative sample of the product should be examined and found free of A. triangulatus; 4) or the consignment should be subject to heat treatment.

As A. triangulatus is on quarantine lists in Denmark, Sweden, Norway and Iceland (Cannon et al., 1999; Boag and Yeates, 2001; Schrader and Unger, 2003), plant health inspectors can take appropriate action against this species.

Public Awareness

In the UK and Ireland, there has been considerable media interest in A. triangulatus, although this was sporadic and varied considerably from year to year (Moore et al., 1998). In Northern Ireland and Scotland, most horticultural producers, farmers and gardeners are aware of A. triangulatus and its potential impact on earthworms.

Eradication

There are no formal mechanisms for eradication of A. triangulatus, at least in the UK and Ireland. Part of the problem with A. triangulatus is that it was initially considered inconsequential and it was only after it was well established in Northern Ireland and Scotland that negative effects were apparent (Murchie, 2008).

Containment/Zoning

There are no established parameters for containment of an A. triangulatus invasion. Given the relatively low speed of natural movement of A. triangulatus, the zone would most likely be infected premises. The main factor in A. triangulatus spread is movement of plant or soil material.

Control

Cultural Control and Sanitary Measures

Hot-water treatment could be used to kill A. triangulatus in plant containers (Blackshaw, 1996). Immersion of A. triangulatus in water at 30°C for 20 minutes, killed adults within 24 h. A slightly higher temperature of 34°C and a lower exposure time of 5 minutes resulted in mortality within 1 h (Murchie and Moore, 1998).

Physical/Mechanical Control

A. triangulatus are prone to mechanical damage (Willis and Edwards, 1977), so cultivation of the soil is likely to be detrimental to this species, as it is to some earthworms (Ernst and Emmerling, 2009). Removal trapping of A. triangulatus using shelter traps on the soil surface was attempted by Blackshaw et al. (1996) who concluded that this method was too time-consuming for widespread control. It may, however, be of value where A. triangulatus re-invasion is limited.

Movement Control

A. triangulatus moves using cilia, peristaltic muscle contractions and mucus production (McGee et al., 1997; Gibson and Cosens, 1998). It is possible, although it has not been tested, that barriers repellent to slugs (e.g. copper, ureaformaldehyde, garlic (Schuder et al., 2003)) may also be effective against A. triangulatus.

Biological Control

Classical biological control using the flatworm-parasitic fly, Planarivora insignis, has been suggested (Blackshaw and Stewart, 1992; Blackshaw, 1996; Cannon et al., 1999). However, there has been little work on P. insignis aside from the paper by Hickman (1965), who described the species and its basic biology. During 1962, Hickman (1965) collected 118 Geoplana tasmaniana, of which 33 (28%) were parasitised by P. insignis. A. K. Murchie (Agri-Food and Biosciences Institute, Northern Ireland, personal communication, 2009) revisited the same site in Tasmania and collected 37 terrestrial flatworms of various species in August 2004, but found no evidence of parasitism. L. Winsor (James Cook University, Australia, personal communication, 2009) commented that parasitism of flatworms by P. insignis was relatively rare. The other problem is that it is not known whether P. insignis would parasitise A. triangulatus and to what extent. Clearly more research is required in this area and especially whether A. triangulatus has a similar parasitoid attacking it in New Zealand.

The slug parasitic nematode Phasmarhabditis hermaphrodita was tested against A. triangulatus but did not cause significant mortality (Rae et al., 2005).

Chemical Control

Chemical control of A. triangulatus is problematic because they are a cryptic, soil-dwelling species and therefore difficult to target. In addition, any pesticides applied to kill A. triangulatus may also affect their earthworm prey.

Individual A. triangulatus in Petri dishes were exposed to a selection of 14 then-approved grassland pesticides. At 1000 ppm a.i., flatworms survived over a three week period when earthworms died (Blackshaw, 1996). The only pesticide that killed A. triangulatus but had minimum effects on the test earthworm species, Eisenia fetida, was gamma hexachlorocyclohexane (lindane), since withdrawn in the UK. A similar result was obtained in cage bioassays with flatworms maintained in compost. Gamma-HCH, tebufenpyrad, imidacloprid, abamectin and pirimicarb (all insecticides or acaricides) did result in some mortality of A. triangulatus (KFA Walters, Central Science Laboratory, UK, personal communication, 2009) but this was generally low and these results need to be substantiated with greater replication.

Monitoring and Surveillance

Monitoring and surveillance of A. triangulatus is by visual inspection underneath stones, wood and shelter traps positioned on the soil surface. There is no nation-wide or formal mechanism for monitoring A. triangulatus.

Mitigation

Enhancing earthworm populations through provision of soil organic matter (e.g. farmyard manure) may mitigate against flatworm predation.

Ecosystem Restoration

It is possible to inoculate depleted sites with earthworms (van der Werff et al., 1998), although this would only be justified if A. triangulatus were removed and would be dependent on the scale of their impact on the earthworm population. Given time and removal of flatworm predation, it is expected that earthworms will naturally recolonise infested areas.

Gaps in Knowledge/Research Needs

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Impact

The economic impact of A. triangulatus is dependent on the contribution of earthworm species to soil fertility. To fully assess A. triangulatus impact, more information is required on the community ecology of earthworms. Although the value of earthworms to crop production is widely recognised (Edwards and Bohlen, 1996), the role of ecotypes and individual species needs to be clarified (Neilson et al., 2000). In essence, if A. triangulatus are reducing anecic earthworms, will this have a disproportionate impact on soil fertility or will other earthworm species compensate?

The importance of earthworms as a food source for mammals and birds requires investigation. This is particularly so if conservation measures are to be applied to these species. For example, farmland birds are being used by DEFRA as an indicator of environmental quality and indices show that farmland specialists have shown a decline since the 1970s (https://statistics.defra.gov.uk/esg/indicators/h6b_data.htm).

Control

More research is required on mechanisms to control A. triangulatus or prevent spread. From a practical viewpoint, hot-water phytosanitation provides a relatively cheap and easy means of disinfecting containerised plants. However, the precise temperatures required, the penetration of heat into compost or soil and the resilience of egg capsules to this treatment need to be determined.

References

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Distribution References

Anderson R, 1986. The land planarians of Ireland (Tricladida: Terricola) a summary of distribution records. Irish Naturalists' Journal. 141-146.

Bloch D, 1992. A note on the occurrence of land planarians in the Faroe Islands. Fródskaparrit. 63-68.

Boag B, Palmer L F, Neilson R, Chambers S J, 1994. Distribution and prevalence of the predatory planarian Artioposthia triangulata (Dendy) (Tricladida: Terricola) in Scotland. Annals of Applied Biology. 124 (1), 165-170. DOI:10.1111/j.1744-7348.1994.tb04124.x

Christensen O M, Mather J G, 1998. The 'New Zealand flatworm', Artioposthia triangulata, in Europe: the Faroese situation. Pedobiologia. 42 (5/6), 532-540.

Dendy A, 1894. Notes on New Zealand land planarians. Part 1. Transactions of the New Zealand Institute. 177-189.

Hogan R N, Dunne R, 1996. The distribution of the New Zealand flatworm Artioposthia triangulata (Dendy) in the Republic of Ireland. Irish Naturalists' Journal. 25 (6), 210-212.

Johns P M, Boag B, Yeates G W, 1998. Observations on the geographic distribution of flatworms (Turbellaria: Rhynchodemidae, Bipaliidae, Geoplanidae) in New Zealand. Pedobiologia. 469-476.

Jones H D, Boag B, 1996. The distribution of New Zealand and Australian terrestrial flatworms (Platyhelminthes: turbellaria: tricladida: terricola) in the British Isles-the Scottish survey and MEGALAB WORMS. Journal of Natural History. 30 (7), 955-975. DOI:10.1080/00222939600770511

Mather J G, Christensen O M, 1992. The exotic land planarian Artioposthia triangulata in the Faroe Islands: colonisation and habitats. Fródskaparrit. 49-60.

MINISTRY OF AGRICULTURE, NORTHERN IRELAND., 1963. Annual progress report on research and technical work 1963. 174 pp.

Moore J P, Dynes C, Murchie A K, 1998. Status and public perception of the 'New Zealand flatworm', Artioposthia triangulata (Dendy), in Northern Ireland. Pedobiologia. 42 (5/6), 563-571.

Murchie A K, Moore J P, Walters K F A, Blackshaw R P, 2003. Invasion of agricultural land by the earthworm predator, Arthurdendyus triangulatus (Dendy). Pedobiologia. 47 (5/6), 920-923.

Willis R J, Edwards A R, 1977. The occurrence of the land planarian Artioposthia triangulata (Dendy) in Northern Ireland. Irish Naturalists' Journal. 112-116.

Links to Websites

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Website	URL	Comment
GISD/IASPMR: Invasive Alien Species Pathway Management Resource and DAISIE European Invasive Alien Species Gateway	https://doi.org/10.5061/dryad.m93f6	Data source for updated system data added to species habitat list.
Habitas – Invasive Species in Northern Ireland	http://www.habitas.org.uk/invasive/index.html
Invasive Species Ireland	http://www.invasivespeciesireland.com
North European and Baltic Network on Invasive Alien Species (NOBANIS)	http://nobanis.org
The Food and Environment Research Agency, UK. Flatworm webpage	http://flatworm.csl.gov.uk/

Organizations

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Denmark: Aarhus University, Nordre Ringgade 1, 8000 Aarhus C, http://www.au.dl/en

UK: FERA (The Food and Environment Research Agency), Sand Hutton, York, Y0411LZ, http://www.fera.defra.gov.uk

UK: The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, http://www.hutton.ac.uk/

Northern Ireland: Agri-Food & Biosciences Institute (AFBI), Newforge Lane, Belfast, BT9 5PX, http://www.afbini.gov.uk

Scotland: Science and Advice for Scottish Agriculture (SASA), 1 Roddinglaw Road, Edinburgh, EH12 9FJ, http://www.sasa.gov.uk

New Zealand: University of Canterbury UC, Private Bag 4800, Christchurch 8140, http://www.canterbury.ac.nz

Contributors

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29/09/09 Original text by:

Archie Murchie, Agri-Food and Biosciences Institute, Applied Plant Science Division, Newforge Lane, Belfast, BT9 5PX. Northern Ireland, UK

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Arthurdendyus triangulatus (New Zealand flatworm)

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