ORIGINAL PAPER

Pathways of alien invertebrate transfer to the Antarctic region

Melissa Houghton • Peter B. McQuillan •

Dana M. Bergstrom • Leslie Frost • John van den Hoff •

Justine Shaw

Received: 28 March 2014 / Revised: 19 August 2014 / Accepted: 12 October 2014

� Springer-Verlag Berlin Heidelberg 2014

Abstract Alien species pose an increasing threat to the

biodiversity of the Antarctic region. Several alien species

have established in Antarctic terrestrial communities, some

representing novel functional groups such as pollinators

and predators, with unknown impacts on ecosystem pro-

cesses. We quantified the unintentional introduction of

alien invertebrates to the Antarctic region over a 14-year

period (2000–2013). To do this, probable pathways (Aus-

tralian Antarctic cargo operations) and endpoints (research

stations) for invertebrate introductions were searched. In

addition, we undertook a stratified trapping programme

targeting invertebrates on supply vessels in transit to the

Antarctic region and also at cargo facilities in Australia

during the 2012–2013 austral summer field season. Our

results show that a diverse suite of invertebrate taxa were

being introduced to the Antarctic region, with 1,376 indi-

viduals from at least 98 families observed or trapped during

the sampling period. Many individuals were found alive.

Diptera, Coleoptera and Lepidoptera were the most

common taxa, comprising 74 % of the collection. At the

family level, Phoridae (small flies) and Noctuidae (moths)

were most commonly observed. Individuals from 38 dif-

ferent families were repeatedly introduced over the study

period, sometimes in high numbers. Food and large cargo

containers harboured the most individuals. These findings

can assist in improving biosecurity protocols for logistic

activities to Antarctica, thereby reducing the risk of inva-

sions to the Antarctic region.

Keywords Alien species � Invertebrates � Biosecurity �Quarantine � Propagule pressure � Sub-Antarctic

Introduction

Invasive alien species (also known as invasive non-native

species) are a major driver of global biodiversity loss

(Simberloff et al. 2013). They occur wherever humans

have facilitated their transfer (Richardson and Pysek 2006)

including isolated Antarctica (Hughes and Convey 2010;

Chown et al. 2012a). Annex II of the Protocol on Envi-

ronmental Protection to the Antarctic Treaty prohibits the

introduction of non-native species to Antarctica (Anon

1991) as do the management authorities of sub-Antarctic

islands (see de Villiers et al. 2006). Despite this, alien

species and their propagules continue to be introduced to

the Antarctic and sub-Antarctic islands.

Increased human activities in the region and the

changing global climate have reduced physical barriers to

the transfer and establishment of propagules to Antarctica,

and the rate and number of alien species established in the

region correlate with human visitation (Chown et al. 1998,

2012a). Human activity in Antarctica is largely concen-

trated in small ice-free areas which have high biodiversity.

This article is an invited contribution on Life in Antarctica:

Boundaries and Gradients in a Changing Environment as the main

theme of the XIth SCAR Biology Symposium. J.-M. Gili and R.

Zapata Guardiola (Guest Editors)

M. Houghton � D. M. Bergstrom � L. Frost � J. van den Hoff �J. Shaw

Australian Antarctic Division, Department of the Environment,

Kingston, Australia

M. Houghton � P. B. McQuillan

School of Geography and Environmental Studies, University of

Tasmania, Hobart, Australia

J. Shaw (&)

Environmental Decision Group, School of Biological Sciences,

The University of Queensland, Brisbane, Australia

e-mail: shaw.justine@gmail.com

123

Polar Biol

DOI 10.1007/s00300-014-1599-2

As such, these areas are environmentally sensitive (Convey

2011) and of high conservation values (Hughes and Con-

vey 2010; Chown et al. 2012b). Sub-Antarctic islands also

have high biodiversity and conservation values and are

vulnerable to invasions (Bergstrom and Chown 1999).

Here, we consider the sub-Antarctic and Antarctica as a

single unit, hereafter the ‘‘Antarctic region’’. This is con-

sistent with previous studies (Frenot et al. 2005; Lee and

Chown 2011) and appropriate in the context of this study

given the transit of shipping and shared logistic operations

between the continent and islands.

Invertebrates make up the majority of faunal diversity in

the species-poor terrestrial ecosystems of Antarctica

(Block 1984), including Acari, Collembola, Nematoda,

Rotifera, Tardigrada, Protista and Diptera (Hughes and

Convey 2010). There are 520 species of soil-dwelling

invertebrates in Antarctica, of which approximately 170 are

endemic (see Nielsen and Wall 2013). This is likely an

underestimate as much of ice-free Antarctica remains

poorly surveyed (Terauds et al. 2012). Sub-Antarctic

islands have higher invertebrate diversity. For example, on

Macquarie Island, 116 terrestrial insect species have been

identified, plus more than 119 species of Acarina (mites)

and 24 species of Collembola including three endemic

species (Greenslade 2006, 2010).

Given their relatively low species richness, narrow

habitat range, simple community structure and life history

attributes, these terrestrial invertebrate communities are

vulnerable to invasion (Bergstrom et al. 2006; Convey

et al. 2006). Currently, nine alien invertebrate species have

established in Antarctica, most in the maritime Antarctic.

They are as follows: a flightless midge (Eretmoptera

murphyi Schaeffer), a gnat (Trichocera maculi-pennis

Meigen), an earthworm (Christensenidrilus blocki Dozsa-

Farkas & Convey) and six collembola (Hypogastrura

viatica Tullberg, Mesaphorura macrochaeta Rusek, Deu-

teraphorura cebennaria Gisin, Protophorura fimata Gisin,

Proistoma minuta Axelson, and Folsomia candida Willem)

(Hughes and Worland 2010; Greenslade et al. 2012; Niel-

sen and Wall 2013; Volonterio et al. 2013). Trichocera

maculi-pennis Meigen is a synanthropic fly that success-

fully reproduces within the sewage system of a station on

King George Island, and this fly has recently been observed

flying outside the buildings (Volonterio et al. 2013).

Another synanthropic fly (Lycoriella sp.) has established in

the sewage system at Australia’s Casey station in East

Antarctica (Hughes et al. 2005) where it persists despite

concentrated eradication efforts. Lycoriella sp. has not

been observed in the outside environment. Compared to the

Antarctic, substantially more alien invertebrates have

established in the sub-Antarctic with 180 species known

across Southern Ocean islands (see Chown et al. 1998 and

Shaw et al. 2010 for detailed discussion on the drivers of

invasion on these islands). Most aliens in the sub-Antarctic

are in the orders Diptera, Hemiptera, Coleoptera and

Lepidoptera (Frenot et al. 2005; Shaw et al. 2010).

Alien species introductions to the Antarctic region have

the potential to impact on recipient ecosystems, including

the introduction of new functional groups (Lee et al. 2007;

Chown et al. 2008: Greenslade et al. 2008; Convey et al.

2010). Alien species can also compete with native species

(Slabber and Chown 2002), exacerbate changes to indige-

nous species such as increased body size (Ernsting et al.

1995), modify local food webs (Greenslade et al. 2007;

Laparie et al. 2010; Convey et al. 2011), act as vectors for

plant viruses (Lebouvier et al. 2011) and alter nutrient

turnover (Hanel and Chown 1998; Smith 2007).

Vectors and pathways

There are approximately 50 stations operating in Antarctica

(Chown et al. 2012a) and most large sub-Antarctic islands

have established research stations (de Villiers et al. 2006).

Most stations are resupplied annually with people, food,

cargo and building materials sourced from all over the

world by national programmes (Chwedorzewska 2009;

COMNAP 2009; Hughes et al. 2011). This cargo reaches

the Antarctic region principally via ships, which are known

vectors of alien species (Lee and Chown 2007). Air

transport is increasingly being used to move personnel and

equipment to Antarctica, enabling faster transport of alien

organisms and propagules, thereby increasing the likeli-

hood of their survival (Frenot et al. 2005). In addition to

approximately 7,000 personnel associated with national

polar programmes, as many as 33,000 tourists also visit the

Antarctic region annually (Chown et al. 2012a), travelling

there by ship.

While there have been a suite of studies quantifying the

transport and introduction of alien plant propagules to the

Antarctic region (e.g. Lee and Chown 2009a, b; Chown

et al. 2012a; Litynska-Zajac et al. 2012), fewer studies

have examined the introduction of alien invertebrates

(although see Whinam et al. 2005; Hughes et al. 2011;

Chwedorzewska et al. 2013; Tsujimoto and Imura 2012).

To date, many different vectors have been identified for

alien propagule transport to the Antarctic region, including:

clothing (e.g. Lee and Chown 2009a; Chown et al. 2012a),

food (e.g. Hughes et al. 2011; Chwedorzewska et al. 2013),

cargo items (e.g. Tsujimoto and Imura 2012), cargo

packaging (e.g. Whinam et al. 2005), vehicles and

machinery (Hughes et al. 2010a), building materials (e.g.

Lee and Chown 2009b; Osyzcka et al. 2012), horticultural

activities (Hulle et al. 2003) and ships hulls and ballast

water (Lewis et al. 2005; Lee and Chown 2007). Many of

the alien species discovered are invasive elsewhere (Whi-

nam et al. 2005; Chown et al. 2012a), and their propagules

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123

remained viable when they reached Antarctica (Hughes

et al. 2010b).

Propagules

The number of propagules introduced to an area, in relation

to their frequency of introduction, is referred to as ‘prop-

agule pressure’ (Williamson and Fitter 1996; Sagata and

Lester 2009). Repeated introductions of propagules

increase the likelihood of establishment and invasion suc-

cess (Rouget and Richardson 2003; Lockwood et al. 2009).

However, it is important to note that alien species can still

establish under low propagule pressure, sometimes from a

single gravid or parthenogenic individual (Gaston et al.

2003; Lee et al. 2007; Myburgh et al. 2007).

The Antarctic Non-native species manual (CEP 2011)

calls for the identification of high-risk invertebrate taxa to

the Antarctic. To date, there has not been substantiative

progress on this. There have been very few efforts to

quantify alien invertebrate propagule pressure and path-

ways to Antarctica involving multiple destinations and

across temporal scales. Here, we aim to do so by examining

alien invertebrates associated with logistics operations of a

national operator, the Australian Antarctic Division, over

14 years.

Materials and methods

We used two methods to identify and quantify alien

invertebrate transfer pathways throughout the Australian

Antarctic station resupply. Firstly, we examined archived

collections and recorded observations from four Australian

Antarctic research stations, cargo, cargo facilities (ware-

houses in Hobart, Australia) and two resupply modes

(shipping and air transport). Secondly, we implemented an

invertebrate-trapping regime at key locations along the

resupply pathway during the 2012–2013 shipping season.

Archived collection

Since 2000, the Australian Antarctic Division (AAD) has

encouraged Antarctic expeditioners and staff to collect and

record alien invertebrate found at the research stations,

cargo facilities, resupply ships and aircraft. For this pur-

pose, alien invertebrate collection kits and instructions

were dispatched to ships and stations. Expeditioners were

instructed on their use during pre-departure environmental

training. In 2004, an electronic database was created for

logging environmental incident reports, including obser-

vation of alien species incursions. Reports could be gen-

erated regardless of whether a physical specimen was

collected or not.

Specimens collected and returned to Australia along

with collection information were identified to the lowest

taxonomic level possible. Observational records not paired

with a specimen were omitted from taxonomic analysis

unless the specimen was identified upon collection as a

‘spider’, ‘fly’, ‘snail’ or ‘moth’. In such cases, it was

deemed that the distinct form and general familiarity of

these invertebrates provided sufficient identification to

categorise them as Araneae, Diptera, Gastropoda and

Lepidoptera, respectively, but no further taxonomic iden-

tity was assigned.

All collection notes and incident reports were reviewed

to identify an associated vector. Samples with unknown

vectors were excluded from analyses. Vector categories

were assigned as food, ship, aircraft and cargo type. Where

invertebrates were ‘‘hidden’’ in containers, ‘‘trapped’’ or

‘‘entangled’’ in cargo materials, the category was assigned

as ‘container and packaging materials’. Supply ships and

aircraft were considered vectors given they have the

potential to attract and accumulate invertebrates, with

invertebrates found in corridors, storage spaces, under ship

lights and on outside surfaces. These incursions are not

directly attributable to cargo operations. Observation

locations (Fig. 1) were defined as: ships and aircraft, the

four Australian Antarctic research stations—Macquarie

Island (54�S 158�E), Casey (66�S, 110� E), Davis (68�S,

77�E) and Mawson (67�S, 62�E)—and the Tasmanian

cargo handling facilities (42� S, 147�E).

We also included data based on targeted searches

undertaken during the 14-year time period (Whinam et al.

2005, AAD unpublished data). These searches were made

of cargo facilities, fresh produce, two CASA aircraft and an

A320 Airbus in conjunction with the International Polar

Year Aliens in Antarctica program (2007–2008).

Trapping

Two types of invertebrate traps were deployed on two

supply ships (totalling five voyages) and at cargo facilities

between October 2012 and March 2013. Durations varied

from 12, 14 (two voyages), 22 and 37 days. Battery-oper-

ated 8 W 12 V light traps (Australian Entomological

Supplies, Sydney, NSW) were complemented with sticky

colour pan traps constructed of yellow and white plastic

plates 18 cm in diameter, smeared with Tangle Trap �

brush-on, petroleum-based insect trap coating. The colours

chosen have been shown to attract a diverse range of

insects (Faustini et al. 1990; Kitching et al. 2001; Vrdoljak

and Samways 2012).

Three trap deployments were scheduled for each voy-

age: (1) upon leaving port, (2) while at sea and (3)

approaching the destination (land). Sea conditions varied

among voyages, which impacted on the frequency of the

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123

at-sea trap deployment, i.e. when conditions were extre-

mely rough (a common occurrence in the Southern Ocean),

traps could not always be set up. Light traps were auto-

matically activated by darkness and were illuminated for

up to 12 h at a time. Traps were placed in areas that were

dark at night, with access to the outdoors and in proximity

to food. At the cargo facilities, light and colour traps were

deployed for approximately three consecutive days while

the ship was in port loading cargo bound for research

stations. There were 39 trapping nights, totalling 418 h of

collection. Fifty-eight yellow and 58 white traps were

deployed for a total of 7440 h for each colour.

Trapping was also undertaken at cargo facilities during

2002–2004. In that study, blue, yellow and non-coloured

sticky traps were deployed for up to three weeks at a time.

Details of the number of traps and trapping frequency were

not available; therefore, we only included the taxa and

location information in our study.

Results

The study found 1,376 invertebrates representing 17 orders

and at least 98 families in the Australian Antarctic Divi-

sion’s resupply pathway. Diptera were the most diverse

order contributing 25 families, followed by Coleoptera

(20), Lepidoptera (13) and Araneae (10) (Table 1). The

most detected families were Noctuidae (49 incidents or

detection events), Phoridae (43), Sciaridae (33), Psychod-

idae (27), Chironomidae (24), Coccinellidae (18), My-

cetophilidae (14), Muscidae (13), Scarabaeidae (13),

Desidae (12), Formicidae (11), Pyralidae (11) and Ptinidae

Fig. 1 Major points along the

resupply pathway of the

Australian Antarctic program.

Resupply vessels depart from

Hobart, Australia, to the deliver

passengers and cargo to the four

research stations: Macquarie

Island, Casey, Davis and

Mawson

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123

(10) (Fig. 2). Generally, when targeted trapping occurred,

more specimens were detected compared with other years

(targeted trapping: 2002–2004 and 2012–2013). In addi-

tion, when focussed searching was undertaken (2000–2002,

2007–2008, 2012–2013), the number of detections was

generally higher (Fig. 3).

Taxonomic diversity and abundance differed between

survey methods (Fig. 2). Observed samples had greater

diversity and more individuals (83 families from 15 orders)

than trapped samples. The most abundant families

observed were noctuid moths (Noctuidae), ladybird beetles

(Coccinellidae), scarab beetles (Scarabaeidae), spiders

(Desidae) and ants (Formicidae).

Trapping in 2012–2013 yielded 95 individuals from 10

orders (32 families). Most individuals trapped were Diptera

(61 individuals from 17 families), followed by Lepidoptera

(22 individuals from five families). The most commonly

detected families were small flies such as phorid flies

(Phoridae), moth flies (Psychodidae), fungus gnats (Sciar-

idae) and midges (Chironomidae). Noctuid moths (Noc-

tuidae) were also abundant in traps.

Light traps captured a mean of 3.78 ± 5.49 (SE)

invertebrates per trapping night, and colour traps caught

0.14 ± 0.7 individuals per 24-h period. Light traps caught

86 individuals, and sticky colour traps caught nine (six

from yellow and three from white). Six invertebrate fam-

ilies were found only in light traps, including two spider

families (Theridiidae, Oecobiidae), one beetle family

(Cryptophilidae) and two moth families (Cosmopterygidae

and Geometridae). Springtails (Collembola) were found

exclusively in white sticky traps, whereas four families

Bdellidae (mites), Biphyllidae (beetles), Ceratopogonidae

(flies), Aphelinidae (midges) were only found in yellow

sticky traps. The existing data set on sticky traps from 2002

to 2004 had 29 individuals from 10 families on blue sticky

traps, while the yellow sticky traps caught 282 individuals

from 27 families and the non-colour traps caught 71 indi-

viduals from 18 families. There were taxonomic differ-

ences between the individuals trapped during 2002–2004

and those trapped in 2012–2013; for example, 13 families

detected in 2002–2004 were not detected in 2012–2013.

Most individuals (n = 722) were observed at cargo

facilities (i.e. the pre-departure point) followed by sub-

Antarctic Macquarie Island (222), ships and aircraft (204),

Casey (162), Mawson (26) and Davis (17). Twenty-one

individuals collected had no recorded location.

Flies (Diptera), beetles (Coleoptera), moths (Lepidoptera)

and spiders (Araneae) were detected at all locations (Fig. 4).

Moths (Lepidoptera) were most common on ships, while

flies (Diptera), beetles (Coleoptera) and spiders (Araneae)

were most common at cargo facilities. More introduced

Coleoptera, Araneae and Diptera were found on Macquarie

Island than at AAD continental research stations. Some

families were found only at the cargo facilities, spear-winged

flies (Lonchopteridae), acalyptratae flies (Lauxaniidae),

minute brown scavenger beetles (Latridiidae), leafhoppers

(Cicadellidae), jumping plant lice (Psyllidae) and rove bee-

tles (Staphylinidae). Others were only observed at research

stations, e.g. seed bugs (Lygaeidae), spider beetles (Ptinidae)

and huntsman spiders (Sparassidae).

Cargo categories could be assigned for 957 observed

individuals (Fig. 5) with ‘general and passenger cargo’

containing the most invertebrates (208 individuals). Cargo

containers and packaging transported 202 individuals and

food items transported 144 individuals. For invertebrates

found in food, more individuals were detected at research

stations (100 individuals) than at cargo facilities and on

ships (44 individuals), and more incursion events were

detected at stations compared with cargo facilities (59

compared with 21). Eighteen per cent of invertebrates

found in food on stations were alive, although this is likely

an underestimate as mortality status was not recorded for

most collections.

A high proportion of taxa were repeatedly detected.

Thirty-eight of 48 families were recorded more than three

times at research stations and on ships during this study.

Table 1 Abundance and diversity for all alien invertebrate collec-

tions made at Australian Antarctic cargo facilities, shipping and air

operations, and the four research stations at Macquarie Island, Casey,

Davis and Mawson, 2000–2013

Order Number of

individuals

Number of

families

Number of

individuals unable

to be identified

to family

Diptera 582 25 15

Coleoptera 255 20 8

Lepidoptera 184 13 73

Araneae 101 10 58

Hemiptera 52 9

Hymenoptera 51 8 16

Dermaptera 53 1 1

Acarina 42 2 1

Blattodea 7 1

Orthoptera 7 1

Neuroptera 6 1

Thysanoptera 6 1 4

Psocoptera 5 1 4

Gastropoda 5 1 4

Collembola 2 1

Julida 1 1

Annelida 1 1 1

Unknown 12a

a Twelve individuals in 11 incident reports were unable to be iden-

tified to an appropriate taxonomic level (Order), as no specimens were

provided

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123

The full data set used for this study is available at http://dx.

doi.org/10.4225/15/52EB19C68999D through the Austra-

lian Antarctic Data Centre (www.data.aad.gov.au).

Discussion

Our work clearly demonstrates that over the 14-year study

period (2000–2013), a diverse range of alien invertebrate

taxa were transported to the Antarctic region. Some of the

taxa we identified have not previously been documented

being transported to the Antarctic region. The most spec-

iose orders (Diptera, Lepidoptera, Coleoptera, Araneae and

Hemiptera) we observed and collected at research stations

are already well represented in the established alien faunas

of sub-Antarctic islands across the Southern Ocean (Frenot

et al. 2005; Shaw et al. 2010) and maritime Antarctica

(Block et al. 1984; Volonterio et al. 2013). A large number

of Hymenoptera individuals were collected during our

study (Table 1), yet alien Hymenoptera are not widely

established across the Antarctic region, occurring only on

sub-Antarctic Marion Island (Lee et al. 2007) and the

Falkland Islands (JNCC 2006). A comprehensive sampling

strategy (Whittle et al. 2013) was undertaken by utilising

two different trappingtechniques combined with observa-

tions made over 14 years. As a result, alien invertebrates

(both alive and dead) were detected at all stages of the

pathway (Fig. 4).

The suite of established alien invertebrates in the Ant-

arctic region is reasonably well documented (Frenot et al.

2005). Fifteen of the 36 alien invertebrate families recor-

ded for Macquarie Island (Greenslade 2006) were detected

again during this study. Of concern were the multiple

detections of the known synanthropes Australian spider

beetle (Ptinus tectus Boieldieu), seed bugs (Nysius sp.),

Indian meal moths (Plodia interpunctella H}ubner) and the

sporadic alien, Huntsman spider (Delena sp.) (Greenslade

2006) at Macquarie Island. While previously undetected

species undoubtedly pose a new risk to the region, these

continued introductions of previously detected taxa are of

particular concern. Increasing propagule pressure through

repeated introductions increases the risk of alien inverte-

brate establishment (Drury et al. 2007; Lockwood et al.

2009) and can enhance genetic variability to alleviate

founder effects (Chwedorzewska and Bednarek 2012). By

any benchmark, not least the Environmental Protocol to the

Antarctic Treaty, this situation requires immediate atten-

tion (Anon 1991). Intuitively, management strategies

0

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25

30

35

40

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Fig. 2 Frequency of detection of invertebrate families observed or

trapped on seven or more occasions. Samples came from cargo

facilities, resupply vessels (ships and aircraft) and research stations,

between 2000 and 2013. Grey columns are observed invertebrates,

and black ones are trapped invertebrates

Polar Biol

123

should aim to reduce species propagule pressure, (i.e.

introductions of high numbers or on numerous occasions).

However, species with low propagule pressure also need to

be considered as they can establish in the Antarctic region

(see Lee et al. 2007; Chown et al. 2008). For example, we

found only two Collembola individuals during this study,

yet alien Collembola are already widely established in the

Antarctic region (Terauds et al. 2011; Greenslade et al.

2012). Collembola are cryptic and small, and possibly trap-

specific; therefore, we may also have underestimated their

propagule pressure.

While some taxa were detected at multiple pathway

points, their abundance was often pathway dependent.

Flighted species were not ubiquitous across all vectors;

moths occurred in high numbers on ships, while flies

(Diptera) and beetles (Coleoptera) were most abundant at

the cargo facilities. It seems likely that some taxa found at

cargo facilities either do not become entrained or do not

survive conditions en route or at the destination. However,

some species were detected more at destinations (i.e.

research stations) than other pathway points. For example,

Black house spiders (Badumna insignis Koch) were found

only once in the cargo facilities but were observed twice on

the ship (en route) and on nine different occasions at

research stations (five times confirmed alive). Another

example is Australian spider beetles (P. tectus) that were

found nine times on Macquarie Island in large quantities

(up to 100 individuals), mostly in food and often alive, but

only once at the cargo facilities. Earwigs (Forficula au-

riculata Linnaeus and Labidura sp.) were found only at

Casey (51 individuals) and Davis (1 individual) stations.

Quarantine inspections and fumigation are undertaken at

the cargo facilities. The invertebrates detected at research

stations have clearly evaded those mitigation procedures,

possibly as they survived deep within cargo or fresh food.

One way of minimising this risk is to ban the transportation

of fresh food, as has occurred for sub-Antarctic Marion

Island (Cooper et al. 2003). Mitigating against inverte-

brates buried deep within cargo would possibly require

more effective targeted fumigation. Alternatively, inverte-

brate eggs may have been entrained at the source and then

hatched en route or upon arrival at the destination. How-

ever, in most cases, the sizes of the individuals observed

and the travel time elapsed between the ships departure and

its arrival at the destination suggest that they were

entrained and transported as live adults.

Many of the taxa detected were winged and therefore

have good dispersal abilities (e.g. Lee et al. 2014).

Organisms with wings do not need to be entrained inside

cargo to be introduced to the Antarctic region because they

0

10

20

30

40

50

60

70

80

90

100

Num

ber o

f det

ec�o

n ev

ents

Year

Fig. 3 Frequency of

invertebrate detections from

cargo facilities, resupply vessels

(ships and aircraft) and research

stations, between 2000 and

2013. Grey columns are

observed invertebrates, and

black ones are trapped

invertebrates

Polar Biol

123

are capable of unassisted wharf-to-ship and ship-to-shore

transfer. Lee et al. (2007) suggested that an invasive wasp

on sub-Antarctic Marion Island may have been self-dis-

persed ship-to-shore during an annual resupply voyage.

Live noctuid moths have previously been documented on

an Antarctic supply ship travelling into Antarctic waters

(Barnes and Convey 2005), remaining near a light source

throughout the journey. While our trapping study was

underway, 52 moths (mostly alive) were independently

detected on the deck of a tourist ship bound for Macquarie

Island. Flying insects are likely to be attracted to the ship’s

food stores, coloured surfaces, light sources or the ships’

micro-environment (Weinzierl et al. 2005; Quilici et al.

2012) while a ship is in port or soon after departure. The

number of invertebrates found on ships in this study further

highlights ships’ role in transporting live alien inverte-

brates to the Antarctic region, and as such the need for

improved management.

To date, few studies have focussed specifically on the

transferral of alien invertebrates into the Antarctic region—

most have focussed on plant propagules. Of the few studies

previously undertaken, Chwedorzewska et al. (2013)

examined cargo at the destination (i.e. Arctowski Station).

Whinam et al. (2005) and Tsujimoto and Imura (2012)

focused on departure points and Hughes et al. (2011)

inspected a single cargo category (i.e. food). There were

taxonomic similarities between the invertebrate taxa

detected in these studies and ours. However, in this study,

we have expanded on those findings by focusing on

invertebrates at multiple pathways and end points, thereby

quantifying the role of both vectors and pathways in the

introduction of invertebrate species into the Antarctic

region.

Conclusion and management implications

The Antarctic Non-native species manual (CEP 2011)

identifies the requirement for further research and devel-

opment, notably, to ‘reduce non-native species risks of the

Antarctic, including identifying regions/activities/vectors/

pathways of the highest risk of introduction of non-native

species’. We have filled some of these information gaps

and have quantified the high propagule pressure of a

diverse suite of alien invertebrates transported (sometimes

repeatedly and sometimes alive) to the Antarctic region.

We found a strong association between food and alien

invertebrates introduction. The finding of repeatedly

0

5

10

15

20

25

30

35

40

Num

ber

ofde

tec�

onev

ents

Loca�on

Diptera

Coleoptera

Lepidoptera

Araneae

Hymenoptera

Hemiptera

Acarina

Fig. 4 Most abundant

invertebrate orders observed at

each location: cargo facilities,

resupply vessels (ships and

aircraft) and research stations,

between 2000 and 2013

Polar Biol

123

introduced species (i.e. those with high propagule pres-

sure), especially in food, can assist managers in developing

taxa-specific mitigation measures such as specialised live

traps, fumigation techniques or strategies that target vul-

nerable life stages, to better manage introduction risk. Our

study has also shown that without improved ship-based

management (which may involve whole ship fumigation),

live invertebrates will, against recommendations of the

Antarctic Treaty System (Anon 1991), continue to be

transported to the region.

Undertaking targeted trapping enabled us to quantify the

invertebrate propagule pressure of the Australian Antarctic

program. Our data now provide a baseline to assess new,

more stringent mitigation measures currently being

implemented by the AAD. An improved cargo handling

and biosecurity facility for the Australian Antarctic pro-

gram became operational in late 2013. The new facility

incorporates recommendations of the Committee for

Environmental Protection (CEP 2011) and Council of

Manager of National Antarctic Programs (COMNAP 2010)

and has a specific set of biosecurity standard operating

procedures designed for improved surveillance and miti-

gation at the cargo facilities. However, even with these

biosecurity measures, we suggest that vigilance and sur-

veillance must be maintained at stations and on ships

(including those ships not managed by national operators)

that visit anywhere in the Antarctic region in order to

detect incursions. Finally, it is essential that rapid response

plans are developed to manage any new incursions as

delays in action can facilitate invasion of Antarctica and

the sub-Antarctic especially as tourism increases, climate

changes and air transport becomes more frequent.

Acknowledgments This study was supported logistically and

financially by the Australian Antarctic Division (as part of AAS

project 4024) and the National Environmental Research Program. We

thank all who assisted on this project: AAD staff and the Aurora

Australis crew assisted at the cargo facility and on the ship. Rachel

Alderman, Graham Cook, Justin Febey, John Kitchener, Mark Man-

gles, Aleks Terauds and Lauren Wise deployed insect traps on the

high seas. Kate Kiefer was instrumental in the establishment of the

Critter Kit sampling regime. Jennie Whinam documented the moth

occurrence on a tourist ship. Sandra Potter provided data from 2002 to

2004. Aleks Terauds provided helpful comments on the manuscript.

We are grateful to all expeditioners and Department of Primary

Industries, Water and the Environment, Tasmania, who have partic-

ipated in biosecurity surveillance over the last decade. This work was

part of the Aliens in Antarctica SCAR program. We thank the three

anonymous reviewers for providing comments that improved the

manuscript.

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Fig. 5 The number of observed

invertebrates and the cargo

types with which they were

associated, between 2000 and

2013

Polar Biol

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