Assessment of the global potential distribution of the predatory land planarian Artioposthia triangulata (Dendy) (Tricladida: Terricola) from ecoclimatic data

Abstract

Artioposthia triangulata was originally described from New Zealand in 1895 but was subsequently found to have spread to Northern Ireland in 1963 and Scotland and England in 1965. It is now widespread in both Ireland and Scotland, where it has been shown to reduce earthworm numbers to below detectable levels. Ecoclimatic data were used in the computer program CLIMEX to estimate the potential spread of A. triangulata to Europe and the rest of the world. Results indicated it could establish in agricultural land in most of north‐western Europe, and persist in domestic gardens throughout much of central Europe, east and west North America, Australia, southern South America, and South Africa. It is difficult to assess either the extent to which earthworm numbers and diversity would be decreased or how far the effect of their loss to soil structure, nutrient cycling, or wildlife would be detrimental in these areas.     

The effect of starvation on size and survival of the terrestrial planarian Artioposthia triangulata (Dendy) (Tricladida: Terricola)

Ten Artioposthia triangulata were kept without food at 5°C, 10°C, 15°C, 20°C and 23°C. Survival and weights were recorded weekly. All planarians died within one week at 23°C and within three weeks at 20°C. One individual survived for 60 wk at 5°C. A negative exponential equation was fitted to average survival times for planarians kept at 5°C, 10°C, 15°C and 20°C. Negative exponential models could also describe the pattern of degrowth by planarians deprived of food. The results are discussed in relation to possible survival of the planarian outdoors in Northern Ireland and the implications for earthworm populations.     

Genetic variation in populations of the terrestrial planarian Artioposthia triangulata (Dendy), and evidence for passive dispersal in Northern Ireland

Genetic variation in 12 populations of the terrestrial planarian Artioposthia triangulata from Northern Ireland and one in the Republic of Ireland were assessed using starch-gel electrophoresis. Seven enzymes - adenylate kinase, aspartate aminotransferase, enolase, malate dehydrogenase, phosphoglucose isomerase, phosphomannose isomerase and superoxide dismutase - provided consistent, resolved stains. Coefficients of genetic identity were similar for all comparisons suggesting that the populations did not belong to distinct taxa. There was no relationship between genetic distance and geographic distance for populations, thus confirming the role of passive dispersal in the spread of A. triangulata. Average percentage polymorphic loci and mean heterozygosities were higher in the east of the Province (41.4% and 0.240), than the west (37.5% and 0.185) suggesting that the planarian had spread westwards after an initial colonisation in the east.     

Distribution and prevalence of the predatory planarian Artioposthia triangulata (Dendy) (Trieladida: Terricola) in Scotland

The distribution of the New Zealand flatworm (Artioposthia triangulata) in Scotland was surveyed between July 1991 and February 1993. There were 348 records from domestic gardens, 56 from botanic gardens, garden centres and nurseries, with only 13 from farms. Although most of the records came from around the major cities the flatworm was found to have become established throughout the Scottish mainland and some of the Islands, e.g. Bute, Gigha, Orkney and Skye. The impact of the flatworm on earthworm populations in agricultural land in Scotland was, as yet, found to be minimal but the fact that seven adjacent farms near Dunoon were infected suggested it could be spread from farm to farm and that in the West of Scotland it could become widespread in agricultural land.     

The potential spread of terrestrial planarians Artioposthia triangulata and Australoplana sanguinea var. alba to continental Europe

A survey in Great Britain of the introduced terrestrial planarians Artioposthia triangulata and Australoplana sanguinea var. alba, which are obligate predators of earthworms, indicates that after 30 years Artioposthia triangulata is established throughout Scotland. However, apart from an initial record in 1965, Artioposthia triangulata was unrecorded from England until it was found again in 1992; currently there are 25 records.
There are fewer records of Australoplana sanguinea var. alba and these are mainly from the south and west of England. Ecoclimatic data from Edinburgh, where Artioposthia triangulata is common, and Plymouth, close to where Australopiana sanguinea var. alba has been recorded, were used by the computer programme CLIMEX to predict the potential spread of these planarians within Europe. Results suggest that Artioposthia triangulata could become established in north west Europe, including areas of Scandinavia, Germany and Poland, whereas Australoplana sanguinea var. alba would be confined to western Europe, including northern Spain. To slow their spread within Britain and prevent their establishment on continental Europe it is suggested that all nurseries and garden centres which sell containerised plants should initiate and maintain stringent hygiene regimes.     

Ultrastructural features of the epidermis of the planarian Artioposthia triangulata (Dendy)

The epidermis of the land planarian Arthioposthia triangulatawas examined by scanning and transmission electron microscopy. Thisinvestigation revealed that the flatworm was covered entirely withcilia and was especially densely populated on the ventral surface.In all regions the epidermis consisted of a one-layered columnarepithelium resting on a prominent basement membrane, but lacking aterminal web. Various secretions were found in the epidermistogether with epidermal rhabdoids. Below the basement membraneother secretory material was visible and this included thecytoplasmic lamellated granules and adenal rhabdites. The basementmembrane consisted of fibrils with a beaded appearance and thesewere arranged parallel to the epidermal layer but did not displaycross-banding. The secretory cells above and below the basementmembrane were compared and their products characterized on thebasis of shape, size and location. Their possible function isdiscussed.     

Density of the New Zealand flatworm, a predator of earthworms, in allotments in Edinburgh between 1993 and 1995

The density of the New Zealand flatworm, Artioposthia triangulata, found between 1993 and 1995 on the surface of the soil under various types of debris scattered in four allotments, was 1–2 m^?2. The type of debris did not markedly affect the density of the flatworm and the distribution of the flatworm within the allotment studied was significantly clustered. Fluctuation in numbers of specimens under different sets of compost‐filled plastic sacks varied in a similar manner to one another. The flatworm was most abundant in the upper 100 mm of soil and its egg capsules were most numerous between 100 and 200 mm below the surface. The flatworm was as abundant under the soil surface shelters as it was beneath shelters buried below the soil surface.     

Long-term effects of prey-availability, partnering and temperature on overall egg capsule output of 'New Zealand flatworms', Arthurdendyus triangulates

Arthurdendyus triangulatus is an invasive terrestrial flatworm that preys on earthworms. To assess A. triangulatus egg capsule production, flatworms were maintained in ventilated polypropylene tubs (7.5 L) kept in controlled environment (CE) chambers or outdoors in the ground. Controlled environment chambers were maintained at 8°C or 14°C, flatworms kept singly or paired within tubs and offered Eisenia fetida according to a weight equalling one‐eighth or one‐half of the mean flatworm weight, or left unfed. The tubs were a successful method for keeping flatworms, with some surviving for over one year. The greatest number of egg capsules produced by an individual A. triangulatus was nine over a 16 week period for a flatworm kept at 14°C and fed at the one‐half regime (0.56 egg capsules flatworm^‐1 week^‐1). Although the effects of treatments varied with CE chambers, there was some evidence from flatworms kept outdoors, that feeding affected egg capsule output, with those flatworms fed at the one‐half regime tending to produce more egg capsules (P= 0.057). Flatworms at the one‐eighth regime or that were unfed produced progressively lighter egg capsules and substantially declined in weight themselves. Nevertheless, even unfed flatworms continued to produce egg capsules for 18 weeks. The lightest egg capsule weighed 8 mg, whilst the heaviest was 180 mg. In the CE chambers at 14°C, there was evidence for two different reproductive/survival strategies. Some flatworms produced cumulatively more egg capsules the longer they survived, whereas others lived longer but produced fewer egg capsules. Flatworms kept without a partner still produced egg capsules up to 35 weeks later. Egg capsules contained a mean of 4.14 (CE chambers) or 4.62 (outdoors) juveniles, with a maximum of 11. Overall, juveniles were 45% of the weight of egg capsules, although larger egg capsules had more juveniles, which comprised a greater proportion of the egg capsule. The conversion of earthworm prey to egg capsule production was estimated at 13%.     

Mortality of the earthworm Eisenia fetida (Savigny) presented to the terrestrial planarian Ártioposthia triangulata (Dendy) (Tricladida: Terricola)

Ártioposthia triangulata is a terrestrial planarian that feeds on earthworms. Up to 76% of field collected A. triangulata fed on Eisenia fetida earthworms at 10°C in the laboratory. In one experiment, the feeding rate declined from 63% of earthworms attacked to 36% and 34% in the first, second and third feeding opportunities over a week. The average number of E. fetida eaten was 1.4 per planarian per week. The gain in weight of individual A. triangulata was significantly related to the amount of earthworm tissue lost during the feeding process. Over a one week period, the amount of earthworm tissue lost was related to the total amount presented to the planarians but not to their size. Frequency of attack was, however, related to planarian size. The results are discussed in relation to an hypothetical population of earthworms in pasture. It is concluded that the results support the contention that A. triangulata could seriously deplete earthworm populations.     

Studies of the behaviour of Artioposhia triangulata (Platyhelminthes; Tricladida), a predator of earthworms

A significant negative correlation between the numbers of earthworms and the flatworm was demonstrated in fromalin-sampled lawns. Their distributions, recorded by a transect from a shrub border where the flatworm is suspected to have been introduced, indicated that predation may lead to earthworm extinction. Two different vermarium designs demonstrated a gradation of earthworm vulmerability to the flatworm due to depth within the soil and burrow width rather than perference for specific earthworm species. A strong correlation between the level of earth worm predation and flatworm movement implied active hunting. A predation rate was found to be 0.67 of an earthworm per flatworm per week with a metabolic conversion rate of 10%.     

Studies on the local dispersal of the New Zealand flatworm, a predator of earthworms, in Edinburgh between 1993 and 1999

The flatworm Artioposthia triangulata was found, from studies using weighted down plastic sheeting, to move predominantly through the soil rather than over it and to use earthworm burrows. Under compost‐filled plastic sacks the flatworm was most active at night although its numbers were similar to those during the day. The transfer of specimens into an area covered with weighted plastic sheeting had no lasting effect on their numbers. The flatworm was regularly removed over 6 years from under paving stones, sheets of newspaper and cardboard placed on the ground in a garden. The rise and fall of the numbers of the flatworm under this debris suggest a predator‐prey periodicity between the flatworm and earthworms of 3 years.     

Surface movement rates of the New Zealand flatworm Artioposthia triangulata: potential for spread by active migration

Movement rates for the surface activity of the New Zealand flatworm Artioposthia triangulata (Dendy) (Tricladida: Terricola) were estimated under semi-field conditions in the Faroe Islands. The distance travelled during 10 consecutive 1-minute periods per individual was measured from mucus trails left behind as the flatworms moved over black plastic sheeting sprayed with fine droplets of water. Adult specimens were found to crawl at rates of up to 28 cm min^-1 (almost 17m h^-1), whereas juveniles crawled at rates of between 3 and 4cm min^-1 (approximately 2m h^-1). This study provides the first data concerning the potential for species spread by active migration.     

A revision of the cosmopolitan land planarian Bipalium kewense Moseley, 1878 (Turbellaria: Tricladida: Terricola)

Knowledge of the cosmopolitan land planarian Bipalium kewense is briefly reviewed. A neotype and paraneotypes are designated. External morphology and internal anatomy of the species are redescribed. Karyological studies on B. kewense reveal a diploid chromosome complement of 16; one subtelocentric, three submetacentric and four metacentric chromosome pairs. Taxonomy of B. kewense is revised and full synonomy provided. New synonomies include Placocephalus isabellinus Geba and Bipalium costaricensis Hyman. Species that phenetically resemble B. kewense are divided into three groups primarily on the basis of stripe pattern and cutaneous musculature. A differential diagnosis distinguishing B. kewense from taxa in these groups is provided. Present distribution of the species is mapped. New records are reported from Barbados, Colombia, Costa-Rica, El Salvador, Indonesia, Madagascar, Malaysia, Mauritius, Mexico, Puerto Rico, Tahiti, Taiwan and Zimbabwe. Worldwide B. kewense exhibits a disjunct distribution pattern. In Australia and in the United States a similar pattern of occurrence is evident. The species appears to be dispersed with rooted plants. The natural range of B. kewense extends from Vietnam to Kampuchea, possibly extending to Malaysia. Elsewhere it has been introduced by man. The bipaliid fauna of Vietnam, to which B. kewense belongs, appears to have closer phenetic affinities with the faunas of adjacent southern rather than northern regions.     

Selected characters of the copulatory organs in the land planarian family Bipaliidae and their taxonomic significance (Tricladida: Terricola)

Preliminary analysis was made of 76 species in the monotypic family Bipaliidae, for which the copulatory apparatus has been described. Four characters from the copulatory organs were selected: profile of the female organ (three character states), approachment of the ovovitelline ducts to the female organ (two states), shape of the penial papilla (two states), and shape of the male antrum wall (three states). Data were scored for five preliminary ingroup taxa, viz., the restricted genus Placocephalus, and four other a priori defined subgroups within the family, viz., the genus Bipalium sensu stricto and three other informal taxonomic groupings. An artificial outgroup taxon was constructed on the basis of character states generalized from the Geoplanidae subfamilies Caenoplaninae, Pelmatoplaninae and Rhynchodemidae subfamily Microplaninae. Analysis of the data matrix resulted in a single most parsimonious tree with the following topology: (outgroup (Placocephalus (Bipalium, group A (group B1, group B2)))). This revised version was published online in July 2006 with corrections to the Cover Date.     

The role of the atrial diverticulum in the copulatory apparatus of the terrestrial flatworm Platydemus manokwari de Beauchamp (Tricladida: Terricola)

Diverticula are present in the copulatory organs of many species of the Terricola. In some species these structures are copulatory bursae or resorptive vesicles. The function of diverticula present in the copulatory organs in species of Dolichoplana and Platydemus (Rhynchodemidae), in Australoplana (Geoplanidae) and in some other caenoplaninid genera has been an enigma. From histochemical and other investigations of the ventro-posterior copulatory diverticulum in Platydemus manokwari de Beauchamp, it is evident that this structure is neither a copulatory bursa, resorptive vesicle nor a uterus. It is an adhesive gland producing a viscid, collagen-like fibrous glycoprotein derived from two secretory elements present in the gland. The secretion is expelled during cocoon laying to adhere the cocoon onto the substratum. The diverticulum appears late in the development of the copulatory organs, and is present when the gonopore is patent; this has implications for the taxonomy of platydemid flatworms. This revised version was published online in July 2006 with corrections to the Cover Date.     

On the taxonomic status of a Dugesia species from Buenos Aires (Platyhelminthes: Turbellaria: Tricladida)

The taxonomic and distributional statuses of the freshwater planarians of South America are imperfectly understood, and a comprehensive review is sorely needed. The species known from the vicinity of Buenos Aires, Argentina, was first described by Böhmig (1902) under the name Planaria dubia Borelli, 1895. Subsequent authors (Kenk, 1930, 1974; Cazzaniga & Curino, 1987) have cast doubt on this assignation. Some have assigned it to Dugesia anceps Kenk; Hyman (1959) was inclined to regard the Buenos Aires planarian as a geographical variant of Dugesia sanchezi Hyman. A comparison of D. sanchezi from the mountainous region of central Chile with specimens from Buenos Aires confirms that the Argentinian material is a distinct species.The differences between the two species are subtle. The Argentinian specimens are distinctive in their possession of infranucleate epithelia of the atria, penis, and bursal canal, as well as in their penial structure. In both species, the epithelia of the atria and bursal canal are glandular. Those of D. sanchezi are nucleate and their secretions are cyanophilous. In the Argentinian specimens, these same epithelia are infranucleate; but while the secretion of the bursal canal is indeed cyanophilous, that of the atrium is erythrophilous. The presence, in these same specimens, of cyanophilous glands opening into the penial vesicles, and of erythrophilous glands whose secretions contribute to a viscous plug in the ejaculatory duct, suggests a difference in the physiology of copulation.It is apparent that the Argentinian specimens are distinct from D. sanchezi Hyman, and probably they represent a new species, one to be described in detail elsewhere. In any case, Hyman's (1959) suggestion that D. sanchezi occurs near Buenos Aires is mistaken; so also is Cazzaniga's & Curino's (1987) identification of specimens from Buenos Aires as D. anceps.     

Methods for taxonomic and distributional studies of terrestrial flatworms (Tricladida: Terricola)

Traditionally used methods for collecting and preserving terrestrial flatworms have proved deficient in various respects. Comparison of methods for preparing these animals for taxonomic study has shown that preservation of morphological characters can best be achieved using formaldehyde-calcium-cobalt fixative and subsequent storage in an aqueous solution of propylene phenoxetol plus propylene glycol and that the best-lasting histological preparations make use of light-fast, oxidation-resistant dyes and synthetic mounting media with an anti-oxidant.     

The diversity of earthworms in 200 Scottish fields and the possible effect of New Zealand land flatworms (Arthurdendyus triangulatus) on earthworm populations

Earthworm populations from 200 fields (132 pasture and 68 arable) in Scotland are compared. Earthworms populations from two pasture fields at a Scottish farm infested with the New Zealand terrestrial planarian, Arthurdendyus triangulates (a predator of earthworms), are compared with a subset of these 200 fields (none of which had planarians at the time of the survey). A variety of univariate and multivariate methods are used for comparison. Results from the 200 fields show that the number of individuals, number of species, richness and diversity decline eastwards and northwards across Scotland. There is an overall difference between pasture and arable fields at the same farm, with fewer anecic earthworms (Aporrectodea longa and Lumbricus terrestris), but more Aporrectodea rosea, in arable fields. Conversely, species richness and cumulative species diversity is greater in arable fields, and sample similarity is less. The planarian‐infested fields show differences from the subset of western Scottish pasture fields and from each other. Both have fewer Aporrectodea caliginosa (and endogeic total) and A. longa (and anecic total) than the western pasture fields. One field has fewer L. terrestris and fewer earthworms in total. Univariate factors show no significant differences between the infested fields and similar non‐infested fields, but multivariate analysis suggests differences. Waterlogging and recent growth of rushes in the infested fields are discussed in relation to the reduced population of earthworms and to rainfall.     

A new species of land planarian preying on termites in Kenya (Platyhelminthes: Turbellaria: Tricladida: Terricola)

A new species of land planarian is described from Kenya. Microplana rermirophaga sp. nov. preys on termites by capturing them at the openings to their nest. The pharynx is unusually far forwards for a land planarian and this is probably related to the active nature of the prey. There is an anterior depression caused by the termination of parenchymal longitudinal muscle bundles which might act as a sucker. All specimens are immature which leads to some difficulty in assigning the species to a genus.