ORIGINAL PAPER

Exotic Collembola on subantarctic islands: pathways,origins and biology

Penelope Greenslade • Peter Convey

Received: 8 March 2011 / Accepted: 3 August 2011 / Published online: 25 August 2011

� Springer Science+Business Media B.V. 2011

Abstract Three exotic species of Collembola are

here identified in collections made during surveys on

subantarctic South Georgia in the summers of

2005/2006 and 2009/2010. Previously, only two

exotic species of Collembola were known from the

island. Increased visitation by tourists, research and

maintenance personnel seems an obvious cause

despite strict quarantine controls imposed on all

visitors. The biology, habitat and distribution of the

new species records indicated that fresh vegetables,

imported in past years, were their likely means of

dispersal to the island. A risk analysis based on their

current distribution and ecology was conducted for

exotic collembolan species that could invade South

Georgia. Pathway analysis of the species with the

highest risk scores suggested additional quarantine

management protocols could include fumigation of

imported fresh food, and this is recommended to

minimise the risk of further invasions. A review of

exotic Collembola in the Antarctic and subantarctic is

provided and the biological traits of Collembola are

discussed in relation to their invasion potential.

Keywords South Georgia � New records �Quarantine management � Bourletiella hortensis �Sminthurinus elegans � Hypogastruridae � Springtails

Introduction

Ecosystems in the subantarctic and Antarctic are

particularly vulnerable to biological invasions as they

are thought to be unsaturated as to species compo-

sition, may have limited buffering abilities because of

the few species present naturally and, with climate

change, now possess habitats that are favourable to an

increasing number of exotic species (Frenot et al.

2005). If patterns seen elsewhere are also followed in

the Antarctic regions, it can be expected that new

invaders may outcompete native species, especially

as environmental conditions change under current

global and regional warming scenarios.

It is sometimes difficult to decide whether some

species are native or exotic. Lindroth (1957) first

applied criteria to determining the status of any

species, and these criteria have largely been followed

for southern regions by the senior author here

(Greenslade and Ireson 1986). In addition, terms

such as exotic, invasive, introduced, alien, natura-

lised, native, indigenous and endemic are not always

used consistently, especially as botanists, zoologists

and pathologists can use the same terms to define

P. Greenslade (&)

Environmental Management, School of Science

and Engineering, University of Ballarat, Ballarat,

VIC 3350, Australia

e-mail: Pgreenslade@staff.ballarat.edu.au

P. Convey

British Antarctic Survey, High Cross, Madingley Road,

Cambridge CB3 0ET, UK

123

Biol Invasions (2012) 14:405–417

DOI 10.1007/s10530-011-0086-8

quite different phenomena (Richardson et al. 2000).

For clarity, here we use the following terms as is

common usage for invertebrates:

Introduced – a species that has clearly been

brought to a new locality directly, or sometimes

indirectly, by human activities. Species such as those

first collected on obvious inoculation sites such as

rubbish dumps, in greenhouses or in hydroponics

installations fall into this category (Greenslade 2006;

Greenslade 2010).

Invasive – a species that has been introduced to a

new locality by any agency, even naturally, and has

colonised, reproduced and spread in the new locality

causing some disruption to the original ecosystem. A

likely Antarctic example amongst springtails is

Hypogastrura viatica (Tullberg) that colonises hab-

itats occupied by the native Cryptopygus antarcticus

Willem group in its absence (Convey et al. 1999).

This term can also include species that disperse

naturally, by wind or water for instance, as well as by

human agency.

Exotic – a species that is clearly native to another

region and not the locality under examination,

generally evidenced by its absence from earlier

collections at the same site. This term can include

species dispersed naturally by wind, water or anthro-

pogenic mechanisms.

Naturalised – an exotic or introduced species that

has successfully established populations in a new

locality. It may or may not include lineages that have

developed some genetic differences from the original

colonising population.

Native – a species that either originated in the

locality under examination, or has been present in the

locality for a considerable period of time, and may

even have developed genetic differences from other

populations of that species.

Endemic – a species that is only known from a

defined locality or region or is native to a specific

region and does not occur naturally elsewhere; note

that the term ‘endemic’ is itself independent of scale,

i.e. carries no implication of the size of locality or

region.

We consider that the term ‘alien’, commonly used

by botanists, is best avoided as it has alternative

meanings in a social context and is covered by one or

more of the terms above, although it has been used in

recent Antarctic literature. Similarly, the term

‘adventive’ can include species that are exotic,

introduced or invasive and therefore is not suffi-

ciently specific for our purposes.

The first record of an exotic species from a

subantarctic island was of Hypogastrura viatica from

Macquarie Island, collected in 1901 by H. Hamilton

(Carpenter 1909). Since then, numbers of records of

exotics from various subantarctic islands have been

accelerating as shown by the dates of first records

from Macquarie Island (Table 1). This is not thought

to result from an increase in collecting effort in the

region because, from the late nineteenth Century and

continuing well into the twentieth, there were

numerous scientific expeditions from Europe to the

southern polar regions and, in the mid twentieth

Century, several year-long surveys of the entomo-

logical fauna of some subantarctic islands (Watson

1967). The recent increase in the rate of exotic

records is therefore probably not likely to be simply

an artefact of increased collecting.

The first comprehensive review and description of

Collembola from subantarctic islands was that of

Deharveng (1981). He recorded a probable 14 exotic

species including five species of Hypogastruridae,

three Isotomidae, three Entomobryidae, one Neeli-

pleona and two Symphypleona in collections from the

South Indian Ocean islands of Marion (5 species),

Kerguelen (6), Crozet (3) and Heard Island (0).

Further exotic species records have not been reported

from any of these islands. Trave and Deharveng

(1981) noted that exotic species were more abundant

in degraded soils, and were only found near man-

made structures. The largest number (11 of the 24

reported species) of exotic Collembola has been

reported on Macquarie Island, which compares with

a native fauna of 24 species (Greenslade 2006;

Greenslade 2010). Five were found only in the now

demolished glasshouses, of which three have since

been found outside the glasshouses area, while the

other two have not and may be locally extinct. South

Georgia currently has only two records of exotics

(Convey et al. 1999).

Heard Island has been little visited so opportuni-

ties for exotic species to arrive and establish have

been minimal and, so far, no exotic Collembola have

been found there (Greenslade 1987; Chown et al.

406 P. Greenslade, P. Convey

123

2006). Greenslade (2002) developed a risk matrix for

species most likely to invade this island and included

recommendations for quarantine measures to limit

the risk of future invasions. The Hypogastruridae

were found to include the most invasive Collembola,

of which three (including H. viatica, the most

invasive) have colonised South Georgia.

The seven early publications on the Collembola of

South Georgia were reviewed by Wise (1970) but were

based on only three collections, and none recorded

exotics. Wise first reported H. viatica in collections

held in the Bernice P. Bishop Museum, collected

mainly by N. V. Jones and H. B. Clagg in 1961 and

1963/1964, respectively. Wise (1970) also docu-

mented a few specimens from the BAS (British

Antarctic Survey) collected by P. J. Tilbrook in early

1964. Convey et al. (1999) noted a second exotic

species, Hypogastrura purpurescens (Lubbock).

Recent collections from South Georgia made in the

austral summers of 2005/2006 and 2009/2010 uncov-

ered three new exotic species, which are documented in

more detail below.

Materials and methods

Some 440 samples were collected from a range of

terrestrial vegetation at ten locations around South

Georgia between 21 January and 7 February 2006

and extracted in Tullgren funnels. A further 400

samples (collected by pitfall, yellow water pan and

Malaise trapping, vacuum sampling, chemical gra-

dient funnel extraction using naphthalene of vacuum

samples and plant litter, and direct searching under

stones, litter, moss etc.) from 21 locations were

made in the 2008/9 austral summer, as part of the

South Atlantic Invasive Species Project (SAISP)

expedition (Key and Key 2009; see Convey et al.

2011 for a summary of both series of sampling

locations). Both these collections were aimed at

maximising the species diversity information

obtained from localities that had been subjected to

past human disturbance.

A subset of 300 of the ca. 840 invertebrate

extractions were examined by PG at the BAS in

September 2010, with the aim of documenting the

presence of both species known to be indigenous

on South Georgia, and of identifying any species

new to the island. Here, we present information on

the latter. Scrutiny of samples continued until no

new species were observed, when examination of

fresh tubes ceased. We are therefore confident that

the records documented here are a true reflection of

the ‘new’ species, but cannot preclude further

species being present in the remainder of the

material.

Table 1 Number of Collembola species considered to be exotic and introduced on Macquarie Island, and the year in which they

were first detected

Year

collected

or recorded

Species Author of first

record

Number of

new records

published

Cumulative

exotics

Comments

on intensity

of collecting

1901 Hypogastrura viatica (Tullberg) Carpenter 1909 1 1 Opportunistic

1937 Hypogastrura purpurescens (Lubbock) Womersley 1937 1 2 Opportunistic

1967 Lepidocyrtus violaceus (Geoffroy)

Desoria tigrina (Nicolet)

Watson 1967 2 4 Intensive focussed

year long survey

1972 Ceratophysella denticulata grp (Bagnall) Greenslade and

Wise 1986

1 5 Opportunistic

2006 Sminthurinus mime Womersley

Megalothorax sp.

Greenslade 2006 2 7 Intensive

2010 Mesaphorura macrochaeta Rusek

Proisotoma minuta (Tullberg)

Isotomurus palustris (Muller)

Protaphorura fimata (Gisin)

Greenslade 2010 4 11 Intensive,

restricted area

Synanthropic species not included

Exotic Collembola on subantarctic islands 407

123

Records of exotic species

ARTHROPLEONA: Hypogastruridae

Hypogastrura purpurescens (Lubbock)

This species was first recorded from South Georgia

by Convey et al. (1999), in collections made in 1982

at Hope Point, near the abandoned whaling station at

Grytviken. It was present in several collections

obtained in 2006 and 2009 from King Edward Point

and also near Grytviken. This indicates that it may

not have spread far from the first location from which

it was recorded, as all records are ca. 500 m of each

other. Like other Hypogastruridae, H. purpurescens

can almost certainly enter ecomorphosis, retreating

into the soil in adverse climatic conditions (Cassagnau

1986). Collection data are as follows.

Grytviken, 54�16046.400S, 36�30029.200W, pitfall

traps, 13/01/2009 with B. hortensis, Sample GVK-

3-v, RS & RJD Key: Grytviken, 54�16052.100S,

36�30027.900W, search sample, 13/01/2009, Sample

GVK-4-I, RS & RJD Key: Grytviken, 54�16052.100S,

36�30027.900W, Tullgren funnel extraction of sup-

ralitoral kelp, 13/01/2009, Sample GVK-4-ii, RS &

RJD Key: King Edward Point, 54�16059.400S,

36�29034.500W, suction sample, 14/01/2009, Sample

KEP-4-I, with F. tilbrooki, RS & RJD Key: King

Edward Point, Cross, Festuca sample, Jan/Feb 2006,

Sample KEP27, P. Convey: King Edward Point, Jan/

Feb 2006, Track edge, Lichen cf. Cladonia, Sample

KEP3, P Convey

Hypogastrura viatica (Tullberg)

The earliest South Georgian record of this species

was from the Grytviken whaling station, in moss

growing on a disused whaling station drier and at the

edge of water bodies, both collections being made in

early 1961 (Wise 1970). This species is now wide-

spread and abundant but sporadic in occurrence in

supralitoral communities on the north-east coast, with

new records extending as far west as Fortuna Bay. It

normally occurs as a monoculture and forms large

communities (Convey et al. 1999). This cosmopolitan

species has also been recorded from widely separated

locations along the Antarctic Peninsula as far south as

Leonie Island (Greenslade 1995). Hypogastrura

viatica is capable of dispersal on floating marine

debris (hydrochory) and can undergo its whole

development under water (Witteveen and Joose

1988). It occurs on all subantarctic islands except

for Heard Island, and has been shown to be

sufficiently homogenous in the COX1 gene, at least

in southern regions, for it to be considered a single

species (Greenslade et al. 2011). Collection data are

as follows.

Fortuna Bay, 54�09019.100S, 36�48057.400W, pitfall

traps, 6/01/2009, Sample FB-7-ii, RS & RJD Key:

Fortuna Bay, 54�09021.200S, 36� 49001.500W, pitfall

traps, 6/01/2009, Sample FB-8-v, RS & RJD Key:

Grytviken, beach, 54�16052.100S, 36�30027.900W,

naphthalene Tullgren extraction of kelp from

strandline, 13/01/2009, Sample GVK 4 II,. RS &

RJD Key: Hound Bay, coastal rocks, 54�23.49S02S,

36�15.160W, Polytrichum, 5.ii.2006, Sample

HOU35, P. Convey: King Edward Point, under

stones, 54�16056.900S, 36�29041.400W, strandline

search sample, 14/01/2009, Sample KEP1, RS &

RJD Key

Ceratophysella denticulata group (Bagnall)

new record

The four specimens available for study included two

juveniles and a single incipient male and female,

indicating that the species is breeding on the island.

These specimens are almost identical to literature

descriptions of this species (Fjellberg 1998; Thibaud

et al. 2004) but differ in several unexpected charac-

ters. The ocelli number varies from 4 ? 4 (female) to

6 ? 6 (male), when the normal number is 8, and the

dental setae varied from 5 ? 5 (female) to 7 ? 7

(male). The latter number is normal. Both the

variable morphology (Babenko et al. 1994) and some

molecular data indicate that a number of cryptic

species are likely to be included under this name

(Greenslade et al. 2011).

This species was only found in small numbers in

one collection, which suggests it is a recent arrival on

the island. The locality was at King Edward Point,

where the currently active administrative centre, jetty

and research station on the island are located, in a

small brownfield meadow behind the ‘Slop Chest’

building. The site is vegetated predominantly by non-

indigenous herbs on crushed slate, and is sheltered by

buildings, oil tanks and the adjacent topography.

408 P. Greenslade, P. Convey

123

Included on the site were a clean stream and various

small temporary and permanent pools of both clear

and organic rich water. Ceratophysella denticulata,

like other hypogastrurid species, can enter ecomor-

phosis, retreating into the soil in adverse climatic

conditions. The species has been recorded from

several other subantarctic islands. While currently

considered cosmopolitan, occurring on all continents

except for Antarctica, the precise identity and affin-

ities of these southern populations still require

molecular verification. Collection details of the single

record are:

King Edward Point, 54�17000.10S, 36�29018.900W,

suction sample, 14/01/2009, Sample KEP-3-I, RS &

RJD Key.

SYMPHYPLEONA: Bourletiellidae:

Bourletiella hortensis (Fitch) new record

The first, and only other record of this species,

commonly known as the garden springtail, from a

subantarctic island is from Kerguelen (Deharveng

1981), where a single specimen was collected by

J. Trave in December 1972, in the vicinity of the Algo

station at the base of Port-aux-Francais. The habitat

was dead Aceana, green algae and soil in a small and

recently dried depression. Further information on this

species’ distribution and continued occurrence on

Kerguelen is not available. An Antarctic record of

B. hortensis was made by Wise (1967) from McMurdo

Station on Ross Island, Victoria Land, where large

numbers of specimens were collected from garden soil

from New Zealand once brought indoors after being

left outside in subzero temperatures for 2 months.

Bourletiella hortensis is a cosmopolitan species

occurring on all continents and one of the few

Collembola that is regarded as a pest of economic

importance, often being found in association with

damaged seedlings. The animals form cavities in

plants during feeding which permit entry of patho-

genic fungi. It is polyphagous and is considered one

of the most damaging species in bare root nurseries,

building up to high numbers there and in fields in

North America, Europe and Australia (Ireson 1993).

It is also often found in synanthropic situations in

Europe (probably in connection with its preference

for almost bare habitats): on pavements, gravel roads,

sport fields, flat roofs covered with gravel, etc. From

here they can be driven by drought into houses, where

they may suddenly appear in vast numbers (Ellis

1974). The eggs of this species appear to be resistant

to extended periods of drought. In Europe it has been

noted that addition of water to soils subjected to a

4-month simulated drought resulted in synchronized

emergence of juveniles of both Sminthurinus elegans

and B. hortensis, both likely to have recently hatched

from eggs in the soil (Alvarez et al. 1999). From its

distribution in Europe, North America and Australia,

it might not be expected to be tolerant of conditions

experienced in polar regions, but its occurrence in the

past on Kerguelen (Deharveng 1981) and Ross Island

(Wise 1967) and more recently at the lip of a receding

glacier in the Arctic (Hagvar 2010) indicates that its

desiccation and temperature tolerant eggs can persist

and remain viable in severe conditions. Despite the

polyphagy of B. hortensis, and because of its current

distribution largely in temperate regions, its occur-

rence on South Georgia was unexpected. As Linden-

mayer et al. (2010) argue, ‘ecological surprises’ such

as this may become more common because of climate

change, resulting in new multiple and interacting

ecological stressors.

On South Georgia B. hortensis was only found in

three samples at two South Georgian localities, near

the old whaling station at Grytviken and at the nearby

King Edward Point, but it was very abundant at both

sites. It was not found in vegetation or soil funnel

extraction and was only collected by suction sam-

pling and in pitfall traps, techniques not previously

used on the island. The habitats from which these

samples were obtained included patchy, both sparse

and dense, ‘brownfield’ grassland with abundant non-

indigenous plants on crushed rock/shingle with some

bare gravel and moss/lichen cover. In one case

(GVK4) the sample was obtained from a herbicide

treated sparse brownfield on crushed shingle. All

three samples were therefore obtained from highly

disturbed locations. The gut contents of several

specimens examined were found to consist almost

entirely of largely digested grass pollen. Collection

data are as follows.

Grytviken, 54�16051.300S, 36�30036.100W, Malaise

Trap, suction sample, white malaise trays, ground

searching, yellow pan traps 12/01/2009, Sample

GVK—2(i)–(iv), RS & RJD Key: Grytviken,

54�16046.400S, 36�30029.200W, yellow pan traps,

13/01/2009, Sample GVK 3 (iv–v), RS & RJD Key

Exotic Collembola on subantarctic islands 409

123

(with H. purpurescens): King Edward Point,

54�16059.400S, 36�29034.500W, suction sample,

14/01/2009, Sample KEP4 (i), RS & RJD Key.

Katiannidae: Sminthurinus elegans (Fitch) new

record As S. elegans was only found in one

collection on the island, this again suggests that it

may be a recent arrival and has not yet become an

established invasive species.

Sminthurinus elegans is widespread in Europe and

North America and also occurs in Australia, but only

where exotic vegetation is present such as on

agricultural land and in pastures of introduced

grasses. It normally prefers woodland habitats in

Europe and is widespread but appears to be sporadic

in occurrence and is found mainly in low vegetation

in drier situations. In France it is said to be common

in vineyards and does not appear to be affected by

herbicides but is reduced by tillage. Unlike B. hort-

ensis, S. elegans does not feed on live plants and is

commonly found in leaf litter and under bark, feeding

on spores and fungal hyphae and other microorgan-

isms colonising dead organic matter (Anon 2006).

The single record details are:

King Edward Point, 54�16059.400S, 36�29034.500W,

suction sample, 14/01/2009, herbicide treated

sparse brownfield on crushed shingle, Sample

KEP4 I, RS & RJD Key.

Risk assessment

A risk assessment was designed for exotic Collem-

bola with the potential to establish on Heard Island,

which had no exotic Collembola and was a recently

designated World Heritage Area (Greenslade 2002).

In view of the seemingly increasing numbers of

exotics now being detected on South Georgia, it is

appropriate to develop an assessment for this island,

in the expectation that potential transport pathways

currently operating could be more effectively con-

trolled. The model provided by the Heard Island

protocol is followed here with some modification.

The main difference is that an additional criterion is

included, that of a pathway analysis, in recognition of

the far higher rates of visitation of vessels carrying

tourists, scientists, fisheries industry, military and

other government personnel, to South Georgia than to

Heard Island.

The species selected to be subjected to risk

analysis for South Georgia include all those which

have already invaded other subantarctic islands or are

known to be highly invasive in other regions so are

a priori the most likely to colonise South Georgia

(Table 2). Eighteen species are eligible for assess-

ment. Note that the number of exotic species on the

Kerguelen and Crozet island groups is not fully

known as no targeted surveys of Collembola have

been carried out at these locations for ca. 40 years.

The method involves applying six scored criteria

to the eighteen species with the known ability to

colonise subantarctic islands. The criteria are based

on the following traits: distribution, life history,

habitat, ecosystem synchronicity, dispersal ability,

climatic synchronicity and transportability. They can

be considered to represent (1) proximity potential, (2)

population potential, (3) establishment potential, (4)

persistence potential, (5) spread/entry potential, and

(6) potential pathway. The scores for each are

summed to give a total ‘Risk Potential’. Each

criterion is divided into four parts each consisting

of a question. A positive answer to any question gives

a score of 1 and a negative answer, 0. The scores are

summed, allowing species to be ranked in order of

probability of introduction to the island. A more

detailed description on the basis for selecting these

criteria is given in Greenslade (2002). The criteria are

as follows:

1. Distribution, preferred climate—maximum score

4.

a. proximity (1). Does it originate in the

Northern Hemisphere?

b. extent (1). Has it dispersed from its origin?

c. origin (1). Is the area it has so far invaded

large, i.e. a result of multiple invasions?

d. area invaded (1). How many other subant-

arctic islands has it invaded? (C3 = 1,

\3 = 0.5)

2. Life history—maximum score 5.

a. reproduction (1). Is it parthenogenetic?

b. population size (1). Does it have a rapid

intrinsic rate of increase, i.e. does it show

r-selected traits?

c. length of life cycle (1). Is the life cycle

short at the ambient temperatures to be

encountered?

410 P. Greenslade, P. Convey

123

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Exotic Collembola on subantarctic islands 411

123

Ta

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le

412 P. Greenslade, P. Convey

123

d. feeding type (1). Does it have generalist

feeding habits?

e. seasonality (1).Will it be able to survive

from season to season?

3. Habitat—maximum score 4.

a. landscape preference (1). Does the island in

some places have a landscape that the

species can tolerate?

b. microhabitat preference (1). Is the preferred

microhabitat present?

c. macrohabitat preference (1). Is the preferred

macrohabitat present?

d. predator vulnerability (1). Are low densities

of relevant predators present?

4. Ecological synchrony or tolerance—maximum

score 4.

a. climatic limitations, temperature (1). Are the

typical temperatures to be encountered

suitable?

b. climatic limitations, humidity (1). Are the

typical humidities to be encountered suitable?

c. tolerance of climatic variability (1). Is the

typical range of climatic variability to be

encountered tolerable?

d. tolerance of climatic extremes (1). Are the

extreme climatic limits to be encountered

tolerable?

5. Dispersal mechanisms—maximum score 4.

a. wind (1). Is the species dispersed by wind?

b. water (1). Is the species dispersed naturally

on water (fresh or saline)?

c. human intervention (1). Is the species dis-

persed in mechanised transport systems

(including associated with cargo, personnel

and logistic facilities)?

d. zoochory (1). Is the species dispersed natu-

rally in association with other organisms,

such as birds?

6. Pathways—maximum score 5.

a. has the species ever been or could it be found

in association with tourism (1) e.g. on

garments, boots, camera bags, etc.?

b. has the species ever been or could be found

in association with national operator staff (1)

e.g. on field equipment?

c. has the species ever been or could it be found

in association with soil on vehicles? (1)

d. has the species ever been or could it be

found in pot plants or in hydroponics instal-

lations? (1)

e. can the species be found on fresh vegetables,

both green and root crops? (1)

The common pathways for accidental introduc-

tions have already been identified in several publica-

tions (Pheloung 2003; Greenslade 2002). Background

information on the pathways specific to South

Georgia was required, and the information used is

given below. Clearly, this ranking system involves

caveats and pragmatism in use, not least as it has

been noted that some invasive species have been

recorded and disperse into new areas outside the

limits of the climatic range that they occupy in their

native region (Lindenmayer et al. 2010).

There are up to 70 cruise ships and 20 private

yachts carrying on average a total of ca. 7,000 visitors

each year and visiting 42 sites on the island. Tourists

are subjected to strict quarantine controls (clean

clothing and boots, no carrying of fresh food ashore,

quarantine controls between landings) before each

visit. There is also a government-run field station at

Husvik which is occupied for short-term periods by

small numbers of staff/scientists (\5). Official visi-

tors, staff and expeditioners are subject to the same

quarantine controls as are generally applied and no

soil or pot plants are permitted to enter station

buildings. Hydroponics facilities are not run on the

island but deliveries of fresh fruits and vegetables

from the Falkland Islands, some partly derived from

shipments from Chile to the Falkland Islands, arrive

monthly. The food is inspected for the presence of

soil and invertebrates but is not fumigated. All waste

other than grey water (which includes kitchen sink

water) is removed from the island, to landfill in the

Falklands

The resulting scores for the 18 species are given in

Table 3. The seven taxa of greatest risk (with highest

scores) are in descending order: Proisotoma minuta

(21), Mesaphorura spp. (20.5), Hypogastrura manub-

rialis (19.5), Megalothorax spp. (19), Ceratophysella

gibbosa (18), Lepidocyrtus violaceus and Parisotoma

notabilis (17.5). Three of these taxa are soil inhabitants

and the remaining four are commonly found associated

with horticulture including vegetable crops.

Exotic Collembola on subantarctic islands 413

123

Discussion

Given these new records, we consider here the factors

that may underlie the increasing number of exotics

being recorded on the island of South Georgia, and

how the risk of further exotic species colonisation

may be minimised. We examine firstly aspects of

their biology, including habitat, host availability and

specificity; secondly, lessons from other subantarctic

localities of invasives; thirdly, pathways; and,

fourthly, suggest possible quarantine gaps and mea-

sures to reduce risk of other species breaching border

protection.

First, is there anything distinctive about the traits

of invasive species in comparison with native or

endemic subantarctic species? Studies of the biology

of a few exotic Collembola species have been carried

out recently on Marion Island, where the habitat

preferences and interaction with other biota of four

exotic species were examined (Gabriel et al. 2001).

This study concluded that exotic species showed a

preference for sites that were moist, warmer and with

organically enriched soils, particularly those that had

been disturbed. Slabber et al. (2007) and Chown et al.

(2007) subsequently noted that climatic warming will

favour these particular exotic species as they tolerate

drought and warm conditions better than native

species, which contradicts to some extent the 2001

findings. However, this latter inference cannot be

applied to all exotic species. Moreover, life history

Table 3 Risk assessment for invasive exotic species of Collembola likely to establish on South Georgia

Taxon Criteria Total

score

Comments

1 2 3a 4 5 6

Ceratophysella gibbosa 2.5 2–3 4 3 3 3 18

Desoria tigrina 3.5 2 4 2 1 1 14

Entomobrya spp. 3.5 1 3 2 2 2 13.5

Folsomia candida 2 3/4 2 2 1 2 13.5 Warmed sites only

Hypogastrura manubrialis 2.5 4 4 3 3 3 19.5

Isotomurus maculatus 3.5 2 3 2 1 1 12.5 And some other species

in the genus

Lepidocyrtus violaceus 3.5 3 4 3 2 2 17.5

Megalothorax spp. 4 4 4 3 1 3 19

Mesaphorura macrochaeta 3.5 5 4 3 2 3 20.5 And some other species

in the genus

Orthonychiurus sp. nr folsomi 1/2 3 4 3 1 2/3 15

Parisotoma notabilis 3.5 4 3 3 2/3 2 17.5

Pogonognathellus flavcescens 2.5 1 4 3 1 1 12.5

Proisotoma minuta 4 4 4 3 2 4 21

Protaphorura fimata 2.5 1 3 2 1 3 12.5

Seira domestica 3.5 3 4 4 1 1 17 Only found in buildings

Sminthurides malmgreni 2.5 2 2 2 1 2 11.5

Sminthurinusquadrimaculatus

2 2 2 2 1 1 10 And some other species

in the genus

Stenacidia violaceus 3.5 2 2 3 1 3 14.5

Scores are higher than estimated for Heard Island because of the higher risks of introductions to South Georgia and inclusion of the

additional criterion (6). The scores are based on available information for each species; we accept that this is never complete, but that

reasonable approximations can be made based on analogous situations elsewherea Suitable habitat, both micro and macro, does not apply to the whole island. A positive score is given if it is known that a suitable

habitat exists somewhere on the island. In this case there are relative large areas of exotic weeds around the old Grytviken Station that

would be suitable for a range of exotic species

414 P. Greenslade, P. Convey

123

traits and the availability of host plants and other food

items were not considered in these studies, and nor

were biotic interactions examined in detail. Consid-

ering what is known of the biology of the species

listed in Table 2, they could nearly all be classified as

r-selected species, with high dispersal ability, short

life cycles, with large numbers of small eggs, a

preference for disturbed temporary habitats and with

a dormant stage which permits their survival in

adverse conditions (Greenslade 1983).

Second, some indication of possible future invaders

was given by Frenot et al. (2005), who listed 11

species of Collembola known from all subantarctic

islands, although this list does have some errors and

omissions (corrected and updated in Table 2) such as

the listing of Proisotoma minuta (Tullberg) as the

invalid name, Parisotoma minutea Tullberg. Alto-

gether Frenot et al. (2005) recorded five naturalised

species from Macquarie Island, and Greenslade

(2006) recorded a further five synanthropic species,

three of which are now naturalised (Greenslade 2010).

Greenslade 2010 recorded an additional naturalised

species on the island, Isotomurus palustris (Muller),

bringing the total recorded to a possible 11, of which

nine are certain naturalised species. Only three of

these are currently known to occur on South Georgia.

Using the available lists of exotics from other

subantarctic islands as an indication of which species

are most likely to be introduced to South Georgia in

future, a possible 17 epigaeic, hemiedaphic and

euedaphic taxa are candidates for potential colonisa-

tion (see Tables 2, 3). The only species unlikely to be

introduced based on this assessment is the tomocerid

of unknown origin on Marion Island (Table 2).

Third, as the localities of the three new records of

exotics reported here were all in, or close to, the

abandoned Grytviken whaling station and the cur-

rently active settlement at King Edward Point, human

activities are the likely pathway to the island for these

species. Between 1982 and 2000, the settlement at the

latter location was administered as a small military

encampment, with no effective quarantine controls

being imposed at this time (Pugh 1994). The known

biology of these three species, which in the Northern

Hemisphere occur in agricultural and horticultural

situations, is strongly consistent with their having

been introduced with imported foodstuffs, and this

appears to be the most plausible pathway. An

alternative but associated possibility is that unclean

imported machinery or vehicles could carry soil in

which C. denticulata could be present, as it is a

ground-living species (cf. Hughes et al. 2010).

Extensive patches of exotic weeds occur around this

area that are sporadically sprayed with herbicide.

Collembola as a rule are not controlled by herbicides

(Greenslade et al. 2010).

Fourth, are current quarantine protocols adequate

or does policy need to be revised especially, as regards

the importation of fresh vegetables? There are

currently no objective data to take this debate forward,

although a new South Georgian management plan is

in preparation. One problem is that Collembola, and

other microfauna, are, because of their small size and

cryptic habits, unlikely to be detected by visual

inspection alone. Moreover, any quarantine proce-

dures in place may be breached through ignorance,

such as was the case with the importation of unwashed

vehicles carrying large quantities of soil, invertebrates

and seeds from South Georgia to Rothera Station on

the Antarctic Peninsula via the Falkland Islands

(Hughes et al. 2010). It is significant that the three

newly recorded exotic Collembola were only found at

Gritviken and King Edward Point, the former a site

that was inhabited for many years prior to any

quarantine controls and the latter near the permanent

settlement. Furthermore, Gritviken is highly disturbed

and hosts a range of weed species over a large area,

offering potential habitat and other resources for

exotics. All cargo is now landed at King Edward Point

but, significantly, several of the exotic species are

found there also. These records of species only found

at these two locations indicate either local spread or

multiple introduction events at closely adjacent loca-

tions. It is clear that controls on the internal spread of

exotics need to be upgraded.

Although fresh vegetables are inspected before

dispatch to South Georgia, they are not fumigated

and, unavoidably, soil is sometimes present. It is

therefore important to note that the species assessed

as being of highest risk of invading South Georgia are

associated with soil habitats. Fresh produce imports

mostly originate in the Falkland Islands, although

some are also obtained from Chile (Punta Arenas),

either routed directly or via the Falkland Islands. It is

clearly therefore important to know the fauna asso-

ciated with horticulture on the Falkland Islands.

However, the collembolan fauna of these islands is

only partly known (Robinson 1984).

Exotic Collembola on subantarctic islands 415

123

All the new records reported here are of exotic

species that are frequently associated with horticultural

activities, as are several species ranked as of a high risk

of entering the island. These data indicate that fresh

vegetables are likely to be the major pathway by which

such incursions enter South Georgia, as was suggested

by Whinam et al. (2005) for subantarctic islands in

general. It is significant that no new records of exotic

Collembola have been made in the last 20 years on

either Heard Island or Marion Island, where no fresh

food is now allowed to be landed.

To date only one exotic species of Collembola

(H. viatica) has been recorded from the Antarctic

Continent or Antarctic Peninsula, although no sub-

sequent records from the location on Leonie Island

(Marguerite Bay) have confirmed its establishment.

Deception Island, in the South Shetland Islands, has

two species recorded, Folsomia candida, Protaphor-

ura fimata, in addition to H. viatica (Greenslade and

Wise 1984), although again no subsequent published

assessments of current status are available. Further

exotic species have recently been collected during two

separate studies on Deception Island during the

2009/2010 austral summer, including an unidentified

species of Onychiuridae (Potapov personal communi-

cation; P. Greenslade and P. Convey unpublished

data). Because of the increasing intensity of traffic by

sea in this region (Lynch et al. 2010), it is particularly

important that subantarctic islands should not act as

‘stepping stones’ for more exotics to be transported to

the Antarctic continent and Peninsula, with the clear

risks associated with this being graphically demon-

strated by Hughes et al. (2010).

Acknowledgments Thanks are due to the South Australian

Museum for partial travel funding, to the British Antarctic

Survey for hosting the senior author during part of this work

and to K. Fraser for information on South Georgian quarantine

controls. Roger Key kindly gave access to the collections of the

South Atlantic Invasive Species Project funded by the

European Commission through EDF-9. Two anonymous

reviewers and the Editor provided comments helpful in

revising the manuscript.

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