Emerging associations on marine rocky shores - Wiley Online Library

Journal of Animal Ecology 2004 73, 294 – 308

Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae Blackwell Publishing, Ltd.

CYNTHIA D. TROWBRIDGE Hatfield Marine Science Center, Oregon State University, Newport, OR 97365, USA

Summary 1. Sacoglossan sea slugs (Gastropoda: Opisthobranchia) can change their highly specialized algal host associations in response to introduced hosts. 2. Adult sacoglossans (Placida dendritica) collected from the introduced green macroalga Codium fragile ssp. tomentosoides in west-coast Scottish sea lochs tended to associate with and consume introduced hosts over the native C. tomentosum in pairwise-choice feeding trials. 3. On west-coast Irish shores, where native congeneric hosts were more common, significantly more P. dendritica attacked C. tomentosum on the shore whereas Elysia viridis disproportionately attacked the exotics. In Lough Hyne, Co. Cork, Ireland, juvenile E. viridis attacked both C. fragile ssp. tomentosoides and the native, sympatric C. vermilara; in pairwise-choice feeding trials, sacoglossans preferred the host species from which they were collected. 4. In the Channel Islands, adult E. viridis were common on C. tomentosum on Guernsey shores. In pairwise-choice feeding trials adults exhibited no preference between native and introduced hosts, indicating that the stenophagous herbivores could change their associations. 5. On temperate Australian shores, the native sacoglossan Placida aoteana attacked the recently introduced C. fragile ssp. tomentosoides as well as native congeners and conspecifics. P. aoteana was common and its herbivory evident in Victoria and Tasmania. Slugs collected from native C. fragile exhibited no preference between algal subspecies in Victoria but a strong preference for the introduced subspecies in Tasmania. 6. Flexibility in host use enables stenophagous marine herbivores to respond within years to the presence of recently introduced hosts. The implicit peril of the host-specificity paradigm − that specialists could change their associations − does occur in stenophagous sacoglossans, and there is considerable intra- and interspecific variation in response. 7. Biological control of invasive green algae using sacoglossan herbivores is fraught with several risks, including taxonomic uncertainty of species’ boundaries, ecological flexibility of feeding, unexplored role of host susceptibility and insufficient evolutionary– developmental information to establish coevolutionary associations. Key-words: Codium fragile, host specificity, host switching, introduced species, sacoglossans. Journal of Animal Ecology (2004) 73, 294–308

Introduction Native oligophagous herbivores frequently modify their diet and / or host-plant use as introduced plants become available (Trowbridge 1995a, 1999; Marohasy 1996; Onstad & McManus 1996; Secord & Kareiva

© 2004 British Ecological Society

Correspondence: Cynthia D. Trowbridge, Hatfield Marine Science Center, Oregon State University, Newport, OR 97365, USA. Fax: 001 541 574 8413; E-mail: [email protected]

1996; Peters 1999; Trowbridge & Todd 1999b, 2001; Thibaut & Meinesz 2000; Secord 2003). Changes can be ecological responses to modified prey or host abundance; these responses may be comparatively labile and potentially reversible. Alternatively, behavioural variation based on genetic differences may have evolutionary consequences (e.g. population differentiation, race formation or sympatric speciation). These two types of responses produce not only different dynamics in how consumption is distributed within the community and

295 Emerging sea slug–algal associations

© 2004 British Ecological Society, Journal of Animal Ecology, 73, 294–308

different evolutionary outcomes, but also different risks associated with biological control efforts. Biological control of marine pests is in its infancy relative to terrestrial management efforts (review by Secord 2003). To date, there has been only a single maritime control effort initiated: herbivorous planthoppers (Insecta) introduced to control cordgrass. Yet, there have been proposals to introduce stenophagous, herbivorous sea slugs (Gastropoda) to control green algal pests, particularly the ‘killer alga’ Caulerpa taxifolia (e.g. Meinesz et al. 1996; Meinesz 1997a,b; Meinesz & Thibaut 1998; Thibaut et al. 1998, 2001; Coquillard et al. 2000; Thibaut & Meinesz 2000). There is considerable controversy regarding the ecological and evolutionary risks of such proposals. A crucial aspect of any biological control proposal is the rigorous assessment of host specificity. There are serious, but frequently overlooked, perils of the ‘hostspecificity paradigm’: particularly that the control agent could or would switch hosts (McEvoy 1996; Onstad & McManus 1996; Secord & Kareiva 1996; Louda et al. 1997; Follett & Duan 2000; Trowbridge & Todd 2001; Secord 2003). There are two ways to assess these risks: (1) rigorously controlled feeding preference experiments can be used to assess the capacity of individuals to alter host-use under different motivational conditions (e.g. no-choice situations or in the presence of conspecifics feeding on alternate hosts) (Trowbridge 1991a,b; Follett & Duan 2000; Thresher et al. 2000). (2) Assessment of changes in host use following inadvertent plant introductions can provide long-term ‘natural experiments’ of herbivore response on different temporal and spatial scales that are ecologically relevant. This latter approach, while uncontrolled, gives a temporally and spatially robust answer to whether the crucial assumption of the host specificity paradigm (i.e. no host-switching or host-range expansion) would be violated, thereby providing one assessment of the safety of a potential biocontrol agent. Because specialist herbivores are more frequent in terrestrial than marine environments, most considerations of flexibility in specialized associations are by terrestrial ecologists (e.g. McEvoy 1996; Onstad & McManus 1996; Follett & Duan 2000). Within the order Sacoglossa (= Ascoglossa), there have been at least two major species radiations; both have been associated with changes in algal hosts (Clark & Busacca 1978; Clark & DeFreese 1987; Jensen 1993a,b, 1994, 1997). Thus, there is strong systematic support for evolutionary changes in diets. However, in marked contrast to most specialized terrestrial insect–plant associations (Secord 2003), there is extensive taxonomic uncertainty and instability within the order Sacoglossa, not only at the species level but also at the genus and family level. Even the species boundaries of the best studied sacoglossans are controversial: are they species complexes or single species? This uncertainty is a strong reason to query unsubstantiated assertions of host-plant fidelity, specificity and coevolution in sacoglossans and to urge

caution applying the host-specificity paradigm to manage invasive macroalgal hosts. The objective of the present paper is to examine how putatively native, stenophagous sea slugs with potentially high larval dispersal have responded to (1) more than five decades of exposure to the availability of the introduced green macroalga Codium fragile (Sur.) Hariot on Scottish and Irish shores and (2) less than one decade of such exposure on Australian shores.

  Incursions of macroalgae from another biogeographical region offer the unusual opportunity to examine the response of highly specialized sacoglossans to introduced potential hosts. In the British Isles, there are two introduced subspecies of C. fragile (ssp. atlanticum (Cotton) Silva and ssp. tomentosoides (van Goor) Silva) as well as two native congeners (C. vermilara (Olivi) Delle Chiaje and C. tomentosum Stackhouse) that are morphologically similar (Silva 1955, 1957; Trowbridge 2001). Both introduced subspecies are presumed to have originated from north western Pacific shores, particularly Japan (Silva 1955, 1957). C. fragile ssp. atlanticum appeared on south western Irish shores c. 1808 and now occurs commonly on rocky intertidal shores of Ireland, Northern Ireland and Scotland; the highly invasive C. fragile ssp. tomentosoides arrived on and spread across north eastern Atlantic shores during this past century, with initial records for England in 1939, Ireland in 1941 and Scotland in 1953 (Silva 1955, 1957; Trowbridge 1998a, 2001; Trowbridge & Todd 1999a,b, 2001). C. fragile often coexists with the native C. tomentosum or C. vermilara on Irish and Channel Island shores (e.g. Parkes 1975; Burrows 1991; Trowbridge 2001) but not on Scottish shores, where the native algae are extremely scarce. The regions of coexistence prompt the intriguing question of how specialist herbivores select among their potential hosts. C. fragile ssp. tomentosoides appeared on New Zealand shores in 1973 and spread rapidly within the Hauraki Gulf of the North Island and then beyond (Dromgoole 1975, 1979; Trowbridge 1995a). Trowbridge (1995a, 1996) hypothesized that the alga would soon appear on south-eastern Australian shores due to the high volume of trans-Tasman shipping and the presence of the invasive alga at major New Zealand ports. The first report of the alga in Australia was 1995 for Corner Inlet and 1997 for Port Phillip Bay, Victoria; 1999 for Tasmania; and 2000 for Port Jackson and Bondi Beach, New South Wales (Trowbridge 1996, 1999; unpublished data; Campbell 1999; Lewis 1999; Talman et al. 1999). On temperate Australian shores, the introduced C. fragile ssp. tomentosoides, two native conspecifics (ssp. novae-zelandiae (J. Ag.) Silva and ssp. tasmanicum (J. Ag.) Silva), and many morphologically similar congeners coexist regionally (Silva & Womersley 1956).

296 C. D. Trowbridge

 


There is considerable intra- and interspecific variation in the extent of feeding specificity in sacoglossans. Several species of sacoglossan sea slugs exhibit extreme host specificity with limited capacity for individuals to change to algal host species that sympatric conspecifics consume; many individuals die in the presence of seemingly acceptable algal food (Jensen 1989; Trowbridge 1991a; Trowbridge & Todd 2001). Whether diet specificity is genetically or developmentally based is not yet known for sacoglossans, although both patterns have been reported for oligophagous insects. While the algal substratum upon which sacoglossans metamorphose is important, larval and post-larval development do not account for all the variation in slug feeding preferences (Krug & Zimmer 2000; Trowbridge & Todd 2001). Furthermore, while sacoglossans may be stenophagous or even monophagous at the local scale of individuals, at population and regional scales, sacoglossan feeding is considerably broader. Comparable patterns of host use have been demonstrated for insects (e.g. Fox & Morrow 1981). The sacoglossan Placida dendritica (Alder & Hancock 1843) is a well-studied ‘species’ in terms of population and feeding ecology. The ‘species’ is probably a complex of sibling species endemic to different regions; this issue is being investigated currently with molecular techniques (Trowbridge & Walsh, unpublished data). The British form of P. dendritica is the source of the type specimen (collected from Torbay, England: Alder & Hancock 1843) and occurs on shores throughout Ireland and Britain (Thompson 1976; Seaward 1990). On European Atlantic shores, P. dendritica feeds on C. adhaerens, C. tomentosum, C. vermilara, Bryopsis plumosa, B. hypnoides and the introduced C. fragile (Alder & Hancock 1843; Thompson 1976). P. dendritica grows to c. 11 mm in length (Thompson 1976), 20 mg in wet weight on Codium and 155 mg on Bryopsis in the British Isles (Trowbridge, unpublished data). On Australasian shores, the proposed synonymy of P. (= Hermaea) aoteana Powell with P. dendritica (Bleakney 1989) is disregarded based on genetic, ecological and reproductive grounds (Trowbridge & Walsh, unpublished manuscript). Powell (1937) described P. aoteana decades before the appearance of C. fragile ssp. tomentosoides in New Zealand (1973) and Australia (1995) (Dromgoole 1975, 1979; Trowbridge 1995a, 1996, 1999). Because 1973 was the first report of the exotic algal pest in the southern hemisphere, it is unlikely that the invader was present four decades earlier. Furthermore, genetic evidence does not indicate introduced genotypes (Trowbridge & Walsh, unpublished data). P. aoteana feeds on C. fragile, C. convolutum and Bryopsis vestita in Australasia (Willan & Morton 1984; Burn 1989; Trowbridge 1998b). The sacoglossan grows to 12 mm (25 mm exceptionally) in Australia (Burn 1989) and c. 15 mm in New Zealand (Trowbridge 1995b). Finally, the European sacoglossan, Elysia viridis (Montagu) has also been well studied and is native to

the British Isles (Jensen 1989; Trowbridge 1998a,b, 2000; Trowbridge & Todd 2001; references therein). E. viridis reaches 4–5 cm in length on C. fragile ssp. tomentosoides, much larger than the sympatric P. dendritica. E. viridis has an annual life cycle and Placida spp. have subannual ones. Most temperate-zone sacoglossans, including those in this study, have long-lived planktotrophic larvae; thus, local specialization is constrained, as larvae may disperse long distances before they are competent to select their benthic host and to metamorphose.

 The major aims of this study were: • to investigate the field populations of native slugs occurring on introduced and native congeneric algal hosts on the west and south coasts of the British Isles and the south-eastern coasts of Australia; and • to determine if the introduced hosts are more attractive than the original native hosts in pairwise-choice experiments in the laboratory. If slugs exhibited either no preferences between native and introduced hosts or significant preference for introduced hosts, then these stenophagous herbivores could change their host associations if introduced hosts were available. If slugs exhibited a significant preference for native hosts yet some slugs would feed on introduced hosts, then some slugs could switch if native hosts were not available. Both these issues are pertinent to the host-specificity paradigm: namely, whether or not populations of stenophagous grazers have the ecological capacity to change their associations in response to environmental changes in host availability or other factors. Terrestrial specialists frequently change and/or expand their hostplant associations (e.g. Louda et al. 1997). My ultimate objective is to demonstrate the inherent risks of taking management actions against marine pests, particularly as it applies to sacoglossans.

Materials and methods   British Isles From December 1996 to July 1997, C. fragile ssp. tomentosoides was searched monthly to bimonthly for sacoglossans in two fully marine lochs in Argyll, western Scotland (Fig. 1); for each Codium thallus found, branch tips were harvested for taxonomic identification. Loch Sween is a fjordic sea loch; the collection site was on the central east side of the loch (ordinance survey grid references NR 736819; N 55°58′ latitude, W 5°38′ longitude). Loch na Cille, Keillmore (NR 691803; 55°57′, 5°42′) is a small loch, north-west of Loch Sween (Fig. 1). Periodic searches were also made in 1997 and 1998 at Oban (NM 853304; 56°27′, 5°26′). C. fragile ssp. tomentosoides was attacked frequently by the sacoglossan E. viridis at all three locations (Trowbridge & Todd


Fig. 1. Location of European study sites in Loch Sween and Loch na Cille in Argyll, western Scotland; Co. Galway and Co. Clare in western Ireland; Lough Hyne, Co. Cork, Ireland; and Guernsey, Channel Islands. Sites were surveyed between 1996 and 2002 for Codium and associated sacoglossans.


1999b, 2001); the present account for Scotland focuses on P. dendritica. Specimens of P. dendritica were collected, placed into seawater and brought back to the laboratory. Search efficiency for the slugs was high despite the slugs’ small size; animals weighing < 0·5 mg are readily visible on Codium, particularly given their propensity to cause extensive grazing damage (Trowbridge 1993). To confirm that collections sampled slug populations adequately, algal thalli were harvested, brought back to the laboratory, placed in seawater in a cold-temperature room and examined subsequently for slugs. This assessment confirmed that the field collection of slugs was thorough. Each sea slug was blotted gently on paper towels, then weighed to the nearest 0·1 mg on an analytical balance for size–frequency analysis. The precision of this weighing protocol has been evaluated previously as c. 2% (Trowbridge 1991a). From 1996 to 2003, searches were made for populations of P. dendritica on the introduced C. fragile ssp. atlanticum in the following eight Scottish districts (in a clockwise direction around Scotland): Dumfries and Galloway, Argyll, Outer Hebrides, Orkney Islands, Shetland Islands, Grampian, Fife and East Lothian; the sites ranged from c. 55° to 60°N latitude (sampling details summarized in Table 1). For each thallus found,

branch tips were harvested for taxonomic identification. Samples, limited frequently by the scarcity of ssp. atlanticum, ranged between five and 201 thalli per location. Because of the scarcity of the native C. tomentosum in Scotland (Silva 1955; Trowbridge & Todd 1999b), the west coast of Ireland was visited in May 1999 and June 2000. This region is one of the few known areas of coexistence of native C. tomentosum and both introduced subspecies of C. fragile, both at the same site and often in the same tidepool (Burrows 1991; Trowbridge 2001). Four sites were visited: Spiddal (Co. Galway) and Black Head, Spanish Point, and Kilkee (Co. Clare) (Fig. 1); these sites ranged from c. 52° to 53°N latitude. At each site, the pools and emergent substrata were surveyed for Codium spp. and sacoglossans. For each thallus found, branch tips were harvested for taxonomic identification; the number of sacoglossan slugs on each thallus was also recorded. These occurrence data were evaluated in terms of slug preferences on coexisting algal hosts. In September 2001, Codium populations were surveyed in Lough Hyne (Ine) in Co. Cork, Ireland (Fig. 1) (W 093285; N 51°30′, W 9°18′). The lough is a known site of coexistence of the native C. vermilara and the introduced C. fragile ssp. tomentosoides (Maggs, Freamhainn


Table 1. Populations of Codium fragile ssp. atlanticum surveyed for Placida dendritica on Scottish rocky intertidal shores. Details about algal population structure, distribution and historical spread are summarized in Trowbridge & Todd (1999a) Scottish district and specific location Dumfries and Galloway Corsewall Point Argyll Clachan Seil Iona Outer Hebrides Cuinabunag, Benbecula Orkney Islands Brough of Birsay, Mainland Shetland Islands South Light, Fair Isle Grampian Kinnaird Head, Fraserburgh Roanheads, Peterhead Fife Doo Craigs, St Andrews

Castle Rocks, St Andrews

Fife Ness, East Neuk East Lothian Bayswell, Dunbar All locations

Ordinance survey grid references

Date

NW 979725

November 1996

19

0

NM 782189 NM 282242

September 1996 May 1997

20 20

0 0

NF 760523

June 2000

5

0

HY 238286

May 1996

30

0

HZ 019069

May 1998

20

5

NJ 999676 NK 138467

November 1996 November 1996

23 25

0 0

NO 508173

September 1996 January 1997 July 1997 April 2003 September 1996 July 1997 April 2003 September 1996

60 110 200 201 60 200 150 40

0

NO 515168

NO 638097 NT 675793

& Guiry 1983). Intertidal and subtidal thalli were collected individually and placed in plastic bags to retain associated slugs; subtidal thalli were bagged under water to prevent dislodgement of sacoglossans. Slugs were removed by hand and counted; slug body length was measured under a dissecting microscope with an ocular micrometer. Algal hosts were blotted on paper towels and then weighed to the nearest 0·01 g; species identifications were made based on utricle characters. Finally, in September 2002, Codium populations were surveyed on Guernsey rocky shores in the Channel Islands (St Peter Port: N 49°27′, W 2°32′). The Channel Islands have abundant populations of native Codium relative to that on the mainland of the British Isles. Pools and emergent substrata were searched across all tide levels at five sites: Lihou Causeway, Grange Rocques, Port Soif, Bordeaux and Moulin Huet (Fig. 1). Algal hosts were identified microscopically. Australia


In January and February 1999 and 2000, broad regional surveys were made for Codium spp. on south-eastern Australian shores (Fig. 2). The sites were concentrated around three regional centres: Port Phillip Bay and Western Port (VIC), Bass Strait and Tasman Sea (TAS) and Port Jackson (NSW); sites ranged from 33° to 43°S latitude and were all fully marine. Codium thalli were examined at as many sites in each region as was logis-

October 1996 1996 −2003

No. of algal thalli examined

59 1242

% of thalli with slugs

0

0 0 0·08

tically possible in order to evaluate the level of sacoglossan abundance and the intensity of slug attack. For each Codium thallus found, branch tips were harvested for taxonomic identification; the number of sacoglossan slugs was recorded (except at Bridport, TAS where the slugs were far too abundant to count in situ).

  Field patterns of slug occurrence could reflect intrinsic factors (such as slug selection of host plants) or extrinsic factors (such as predation). To establish that postmetamorphic sacoglossans have the capacity to distinguish between potential sympatric hosts, feeding experiments were conducted in the laboratory. In April 1997 a series of three short-term host preference experiments were conducted with slugs from Argyll, Scotland to test whether or not P. dendritica from introduced hosts retained the capacity to consume native host species. Ideally, reciprocal feeding preference experiments would have been conducted with slugs from introduced and native hosts to distinguish between feeding preferences per se and the effects of conditioning or recent feeding history; this approach was not possible, given the scarcity of the native C. tomentosum in Scotland. Raising slugs through their life cycle to obtain naive juveniles was attempted without success. Individual, preweighed P. dendritica collected from C. fragile ssp. tomentosoides were offered pairwise-choices


Fig. 2. Location of Australian study sites in Port Phillip Bay and Western Port, Victoria; Bass Strait and Tasman Sea, Tasmania; and Port Jackson and Bondi Beach, New South Wales. Sites were surveyed in 1999 and 2000 for Codium and associated sacoglossans.


of algal hosts. Branch tips (∼1 g wet weight) of each algal species or subspecies were placed in small dishes with ∼0·5 L of filtered seawater and one slug; replication ranged from 18 to 23 individual slugs per experiment. Branch tips were matched as closely as possible within each container (e.g. bifurcate vs. unbranched tips) to reduce the effect of slug preferences based on macrostructural differences. Because slugs did not feed on the severed end of the algae, the use of pieces should not have biased the results. Because P. dendritica does not retain functional chloroplasts (Clark et al. 1990) and does not exhibit a diurnal vs. nocturnal feeding periodicity (Trowbridge, unpublished data), the actual light conditions per se were not important. The algal choice of each slug was monitored periodically over a 2-day period; the slugs consumed the algae on which they occurred (see Trowbridge (1992) for explicit demonstration of host choice, consumption data and grazing damage). Categorical data at the last period sampled were analysed using χ2 tests. If slugs exhibited (1) no preferences between native and introduced hosts or (2) significant preference for introduced hosts, then it was considered that the stenophagous herbivores could and would change their host associations if intro-

duced hosts were available. If slugs exhibited a significant preference for native hosts yet some slugs would feed on introduced hosts, then some slugs could switch if native hosts were not available. In September 2001, juvenile E. viridis were collected from C. fragile ssp. tomentosoides and C. vermilara at Lough Hyne, Ireland (n = 30 slugs per host species). Branch tips of both algal species were placed into small dishes with ∼0·5 L of seawater and one slug (about 2–4 mm long). Slug selections were monitored over a 1·5-day period at ambient light and temperature conditions. The initial and final preferences of sacoglossans from the two algal sources were compared using G-tests; when the two groups of slugs responded similarly, the categorical data were pooled and the hypothesis of host preference was tested using a χ2 test. In September 2002, 24 E. viridis were collected from intertidal C. tomentosum at four sites on Guernsey. Native hosts were collected from mid- and low intertidal habitats; C. fragile ssp. tomentosoides was collected from upper mid-intertidal pools (only habitat occupied by the alga on Guernsey). Branch tips of each algal species were placed into small dishes with ∼0·5 L of seawater and one slug (mean 11 mm long). Slug selections were


monitored over a 1·5-day period at ambient light and temperature conditions. The initial and final preferences of sacoglossans from the two algal sources were compared, using Fisher’s exact tests. Finally, short-term feeding preference experiments were conducted in February 2000 in Victoria and Tasmania, Australia to test whether P. aoteana from native hosts would consume introduced conspecific hosts. Individual slugs collected from the native C. fragile ssp. tasmanicum were offered pairwise choices of algal subspecies. Branch tips (∼1 g wet weight) of each algal species or subspecies were placed into small dishes with ∼0·5 L of seawater and one slug. Half-day experiments were conducted on benches at room temperature; the algal choice of each slug was monitored periodically during each experiment. Replication was 20 slugs (Victoria) and 40 slugs (Tasmania) per experiment; the categorical data at the last time period were analysed using χ2 tests.

Results  


P. dendritica appeared on C. fragile ssp. tomentosoides in February 1997 at Loch na Cille and March 1997 at Loch Sween. This sacoglossan was never abundant in either loch (Fig. 3), but thalli surveyed at Oban had a higher frequency of attack and more intense attack than in the two sea lochs. The majority of P. dendritica on C. fragile ssp. tomentosoides were sexually mature adults, ranging from 2 to 22 mg in wet weight. The paucity of juvenile slugs (< 2 mg) both initially and overall implies that slug recruitment is low, juvenile mortality is high, or juvenile growth is high. Spawn masses appeared on the main axes and in branch dichotomies from May to July. In extensive searches in eight regions on Scottish shores, only one individual of P. dendritica was found on C. fragile ssp. atlanticum, namely at the Fair Isle, Shetland Islands in May 1998 (Table 1). This occurrence represents a frequency of 0·10% of the spring and summer thalli examined (n = 1006) and 0·08% of all 1242 algal thalli examined (irrespective of season). This slug scarcity was not due merely to low algal host abundance, because populations in St Andrew’s Bay were comprised of hundreds of thalli per pool. In pairwise-choice experiments, Scottish P. dendritica exhibited a slight, although non-significant, preference for C. fragile ssp. atlanticum over ssp. tomentosoides (Fig. 4a) (χ2 = 3·77, 1 d.f., P = 0·052). Slugs, however, preferred both introduced subspecies to the native C. tomentosum (Fig. 4b,c). Despite the small sample sizes (due to few slugs on the shore), these latter preferences were highly significant (χ2 = 8·07, 1 d.f., P = 0·005 for each experiment). Based on these experiments, slugs occurring on C. fragile ssp. tomentosoides preferred strongly both the familiar and the unfamiliar introduced hosts to the native hosts; the reciprocal experiment was not possible on Scottish shores.

Fig. 3. Placida dendritica on the introduced Codium fragile ssp. tomentosoides at three sites in Argyll, western Scotland: (a) percentages of introduced hosts with slugs and (b) mean number of slugs per attacked host. Data were collected between September 1996 and July 1997, plus February and April 1998. The number over each bar indicates the number of replicate algal hosts examined (a) and the number of hosts with slugs (b). Error bars denote + 1 SE.

In May 1999, P. dendritica and E. viridis were relatively common on Codium thalli on the west coast of Ireland (Fig. 5). Overall, there was highly significant variation in slug attack of different algal host species: P. dendritica was associated disproportionately with the native host (G-test, G = 8·9, 2 d.f., P < 0·012) and E. viridis was with the introduced hosts (G = 21·2, 2 d.f., P < 0·001). At Spiddal, 4% of the 25 C. fragile thalli in high intertidal tidepools were attacked by P. dendritica and 20% were attacked by E. viridis. E. viridis attacked both subspecies at the same frequency, despite the fact that ssp. atlanticum was four times more common than ssp. tomentosoides. At Black Head, 30% of the 50 Codium thalli were attacked by E. viridis. Although 82% of hosts were ssp. tomentosoides, there was no significant difference in frequency of attack between subspecies of C. fragile (G = 0·2, 1 d.f., P = 0·634). At Kilkee, P. dendritica was found on 3·2% of the thalli (n = 31). At Spanish Point, there was considerable spatial and temporal variation in slug attack. Codium thalli on emergent substrata, usually the native C. tomentosum, were attacked by P. dendritica: 8% of 25 thalli in the low red algal turf/kelp zone and 15·4% of the 13 thalli in the


Fig. 5. Frequency of occurrence of Placida dendritica and Elysia viridis on native and introduced Codium on west-coast Irish shores in May 1999. Numbers indicate the number of algal thalli examined. Algal abbreviations as in Fig. 4.

Fig. 6. Abundance of Elysia viridis on Codium fragile ssp. tomentosoides and C. vermilara (number of slugs per gram wet weight of algae) on the western shore of Lough Hyne, Co. Cork, Ireland. Data collected in September 2001. Intertidal refers to the lowest levels, fringe to the infralittoral fringe, shallow to 1 m and deep to 2 m.

Fig. 4. Feeding preferences of adult Placida dendritica from Scotland when offered pairwise choices of different Codium species and subspecies. Algal abbreviations: Ct = C. tomentosum, Cfa = C. fragile ssp. atlanticum, Cft = C. fragile ssp. tomentosoides. Replication ranged from 18 to 23 slugs per trial.


mussel zone. In contrast, pool-dwelling thalli were attacked more frequently by E. viridis: 64% of thalli (mainly C. fragile ssp. tomentosoides) in the wave-sheltered pools in the upper mussel to lower barnacle zone. In June 2000, the patterns of attack were different. No P. dendritica were found at all on 50 native hosts at Spanish Point, although 2% had egg masses of P. dendritica and 8% manifested slug grazing damage; also, P. dendritica attacked 3·3% of the 30 C. fragile ssp. tomentosoides examined. In contrast, at Blackhead slugs attacked one of the three C. tomentosum found and three of the 47 C. fragile surveyed; thus, although

the native host species was much less abundant, it was attacked disproportionately more frequently (33% vs. 6%) by P. dendritica. These observations indicate collectively that native sacoglossan slugs used native and introduced algal hosts, even when they coexisted. In September 2001, high densities of juvenile E. viridis were associated with Codium spp. in Lough Hyne, Co. Cork, Ireland. Intertidal thalli of C. fragile ssp. tomentosoides supported an average of 26·9 slugs per thallus (n = 10) and the native C. vermilara had an average of 100 slugs (n = 2); when densities were expressed on an algal wet weight basis, there was no significant difference in slug attack between algal species (Student’s t-test, t = 0·742, n = 4, P = 0·551). Slug density, however, was significantly lower in subtidal areas than in closely situated, intertidal ones (Fig. 6, Kruskal–Wallis, H = 11·2, P = 0·011). Sacoglossan body length did not differ between intertidal Codium spp. (Fig. 7a,b), suggesting that the introduced and native algal hosts were comparable in quality. In preference experiments, juvenile slugs selected algal hosts actively (Fig. 7c,d). The


Fig. 8. Frequency of occurrence of Elysia viridis on native Codium tomentosum on Guernsey rocky shores in September 2002. Numbers indicate the number of algal thalli examined.

Fig. 7. Body length and feeding preferences of juvenile Elysia viridis from the introduced Codium fragile ssp. tomentosoides (a,c) or native C. vermilara (b,d). Samples sizes (a,b) indicate the number of slugs measured. The pairwise choice experiment was conducted at Lough Hyne in September 2001; replication was 30 slugs from each algal source.


initial preferences of slugs did not vary with algal host source (G-test, P = 0·635): both disproportionately selected C. fragile (χ2 test, P = 0·016). Final preferences, however, did differ significantly with host source (G-test, P = 0·001): juvenile E. viridis from C. fragile ssp. tomentosoides strongly preferred that alga whereas conspecific slugs from C. vermilara preferred that one. E. viridis was common on Guernsey shores in September 2002. The slugs attacked 21·0% of the native C. tomentosum on mid and low intertidal shores (Fig. 8), but 0·0% of the C. fragile ssp. tomentosoides in upper mid-intertidal pools. The frequency of attack averaged 3·2 sacoglossans per attacked host (SE = 0·8, n = 24 thalli) across sites and microhabitats. The highest rate of attack was at the east-coast site Bordeaux on a low intertidal boulder field with a mean of 6·7 slugs per thallus (max. 17 adult slugs). Adult E. viridis (mean 11 mm long) from Guernsey exhibited no initial or final preferences between the

native host and the introduced congener (Fisher’s exact tests, P = 0·491 and P = 1·000, respectively). These results are noteworthy, as a lack of preference indicates that herbivores could and would use introduced hosts as they become available. Furthermore, the differential outcome of the Lough Hyne and Guernsey experiments demonstrates intraspecific variability in response. Whether the differential slug responses are due to spatiotemporal, ontogenetic or genetic variation is no known. The crucial point is the occurrence of intraspecific variation in the feeding behaviour of stenophagous herbivores.

 In the broad regional survey of south-eastern Australia (Fig. 2), most intertidal areas exhibited low frequencies of slug attack of C. fragile (Fig. 9). The major exception to this pattern was the high rates of slug attack of introduced C. fragile ssp. tomentosoides at Sisters in Port Phillip Bay, Victoria (Fig. 9a,b). The majority of thalli were attacked by large, sexually mature P. aoteana (> 5 mg) during two separate visits (January 1999 and February 2000). Furthermore, there was an average of eight slugs per attacked thallus (Fig. 10a), and c. 80% of the thalli exhibited visually obvious signs of slug grazing damage (Fig. 10b). Recent incursions of the introduced alga at Newhaven, San Remo and Flinders North at the mouth of Western Port Bay as well as Mornington on Bass Strait all had low rates of attack (Figs 9, 10). In 1999, the three Tasmanian sites near Hobart had moderate frequencies of slugs (10–25% of the thalli attacked) but only Tinderbox Marine Reserve had moderate slug densities (Figs 9 and 10a). In 2000, P. aoteana attacked algal hosts frequently on both sides of the Bass Strait: Flinders South, Bridport and Devonport. At Bridport, the slugs were so abundant on


Fig. 9. Frequency of occurrence of Placida aoteana on native and introduced Codium on south-eastern Australian shores in two consecutive summer surveys. The numbers over each bar indicate the number of thalli of Codium fragile examined at each site. Solid bars denote the introduced C. fragile ssp. tomentosoides; shaded bars denote native conspecifics. The low sample sizes at Cape Otway and Sisters were due to adverse conditions for sampling (high waves and stinging flies, respectively).


many thalli that precise slug counts were discontinued; of 50 thalli examined, 8% had a few P. aoteana (1–9 slugs per thallus), 24% had tens of slugs and 4% had hundreds. In pairwise-choice experiments, P. aoteana collected from native C. fragile ssp. tasmanicum in Victoria exhibited no significant preference between the native and introduced subspecies (χ2 = 0·8, 1 d.f., n = 20, P = 0·371, Fig. 11a). Tasmanian slugs from Bridport, however, preferred the introduced ssp. tomentosoides to native conspecifics (χ2 = 5·2, 1 d.f., n = 38, P = 0·023, Fig. 11b). In both cases, the native slugs were willing to feed on the introduced hosts. The variability in response is noteworthy: these two regions are separated by the Bass Strait which presumably would be readily traversed by planktotrophic sacoglossan larvae.

Fig. 10. Placida aoteana on Codium fragile at several sites on south-eastern Australian rocky shores in January 1999: (a) mean number of slugs per attacked host and (b) the frequency of detectable grazing damage. The number of each bar indicates the number of replicate algal hosts examined (a) and the number of hosts with slugs (b). Error bars denote + 1 SE.

Discussion    The introduced alga C. fragile ssp. tomentosoides is exploited by P. dendritica and E. viridis in the British Isles; the association formed since the alga’s appearance in Ireland in or before 1941 and Scotland in 1953 (Trowbridge & Todd 2001; Trowbridge, present study). In contrast, C. fragile ssp. atlanticum, introduced to Ireland and Scotland a century earlier, does not appear to be used commonly as a host by the slugs (Table 1), despite the fact that both sacoglossan species can eat the alga and E. viridis can metamorphose upon it (Trowbridge 1998a, 2000; Trowbridge & Todd 2001). These results suggest collectively that ssp. atlanticum would be an appropriate host if it were available to the slugs: the high intertidal location on Scottish shores may provide the alga a partial refuge from slug herbivory. The relative absence of this subspecies low on the shore may be due to herbivory (by slugs or generalist grazers); field transplant experiments are warranted to evaluate this hypothesis. Certainly, on Irish shores, E.


Fig. 11. Feeding preferences of adult Placida aoteana when offered pairwise choices of introduced Codium fragile ssp. tomentosoides and native C. fragile ssp. tasmanicum. Slugs were collected from native C. fragile at (a) Flinders South, Victoria and (b) Bridport, Tasmania. Introduced ssp. tomentosoides was collected from (a) Flinders North and (b) Oyster Bay (near Hobart); native conspecifics were collected from (a) Flinders South and (b) Kingston Beach. P-values were based on χ2 tests conducted on categorical data in the final time period.


viridis attacks mid-intertidal thalli of ssp. atlanticum (Fig. 5). These results suggest that P. dendritica can form viable populations on introduced algal hosts when native hosts are not available; those slugs prefer the introduced hosts in pairwise choice experiments. Whether this result is due to ingestive conditioning, genetic differences in slugs associated with larval host choice or other factors was not explored in this study. What is clear, however, is that slug populations can and do form on introduced congeneric hosts both (1) when natives are rare and generally not available (Scotland) and (2) when natives coexist with exotics (Ireland, Guernsey and some areas of south-eastern Australia). The differential response (both intra- and interspecific) of sacoglossans in feeding trials emphasizes that sacoglossans are ecologically (and probably genetically) diverse consumers, and their associations are flexible. These emerging associations are novel, not coevolved. Whether they are fully reversible is not certain; recent experimental work by Trowbridge & Todd (2001) indicates that the offspring of E. viridis that consume introduced

hosts have lost some capacity to consume native hosts. This would constrain host-switching. Two other studies (Jensen 1989; Trowbridge 1991a) reported that sacoglossans exhibited intraspecific variation in the capacity to change hosts; thus, there were ‘switchers’ and ‘nonswitchers’ in local populations. If host selection has any genetic basis, then ‘switchers’ could contribute to rapid evolutionary changes in associations. If host choice, however, is based on developmental and/or behavioural mechanisms, then sacoglossan host use would vary spatially and temporally with different algal host abundances. Little is known about how stenophagous marine herbivores have responded to introduced macroalgae in other regions. Clark & Franz (1969) suggested originally that the sacoglossan P. dendritica (as Hermaea dendritica) was an introduced herbivore to north western Atlantic shores, although Clark (personal communication) concluded subsequently that it was native to the region but had changed its diet from the native alga Bryopsis. Genetic evidence (Trowbridge & Walsh, unpublished data) supports Clark’s latter view. On north eastern Atlantic shores, E. viridis and P. dendritica have incorporated C. fragile into their host-plant ranges (Trowbridge & Todd 1999a,b, 2001; Trowbridge, this study). In the Netherlands, E. viridis also uses the introduced red alga Dasysiphonia sp. introduced from North Pacific shores (Van Bragt, personal communication). Changes in host-plant associations have occurred in two Codium-feeding sacoglossan species in Australasia: P. aoteana (as P. dendritica) and E. maoria (Trowbridge 1995a;b, 1996, 1999; unpublished data; Peters 1999). The two slug species fed on some, although not all, species of Codium available but readily incorporated the introduced C. fragile ssp. tomentosoides into their diets. As the invasive alga continues to spread within Australasia as well as to other geographical regions, additional sacoglossans that feed on Codium will presumably modify their dietary ranges accordingly. Only with a rigorous understanding of the extent to which changes in host-plant associations can and will occur will we gain a realistic understanding of the risks of biological control with sacoglossans. Reports of changing and expanding host range by biological control agents in terrestrial communities (e.g. Louda et al. 1997) indicates that that specialized associations can and do change on ecological time scales. Comparable changes have occurred in at least five species of sacoglossans which feed on Caulerpa. Two native Mediterranean sacoglossans, Oxynoe olivacea and Lobiger serradifalci, consume the invasive aquarium strain of C. taxifolia (Meinesz et al. 1996; Thibaut et al. 1998; ¸uljevic et al. 2001; Gianguzza et al. 2002). The Caribbean O. azuropunctata and E. subornata, both imported from Martinique to Nice, eat C. taxifolia (Meinesz et al. 1996; Thibaut et al. 2001). The newly reported E. cf. tomentosa in the Mediterranean and Australia now consumes the invasive C. taxifolia (www.seaslugforum.net). With the algal pest appearing recently on the shores of southern California and


south-eastern Australia, other native Caulerpa-feeding sacoglossans may soon shift their hosts. Comparable changes are happening in Florida where native sacoglossans are already feeding on the newly appeared Pacific C. brachypus (www.seaslugforum.net).

    :    Recent reviews of biological control (e.g. McEvoy 1996; Secord & Kareiva 1996; Louda et al. 1997; Follett & Duan 2000; Secord 2003) emphasize the risks of introduced control agents switching to use non-target species. For sacoglossans there are several areas of uncertainty concerning host-use, all of which bear on our ability to assess the risk of using these stenophagous herbivores as biocontrol agents against invasive algae. Unclear species’ identities For many sacoglossans, the species’ identities and boundaries are unclear (as discussed above for P. dendritica). One of the leading candidates for marine biological control of C. taxifolia, namely E. subornata, has been subject to taxonomic uncertainty. Although the species was described in 1901, E. subornata was synonymized with E. cauze recently and is highly variable in colour and morphology (Clark 1984); whether this synonymy will be supported by molecular evidence remains to be seen. The other candidate, O. azuropunctata, was described in only 1980 (Jensen 1980). Thus, understanding of both species is limited temporally and spatially in their native range. The paucity of information about the species is not an asset to any biological control programme. Incomplete knowledge of intraspecific variation in diet or host breadth


Interindividual variation in a species’ resource use is ‘a widespread but underappreciated phenomenon’ across a wide range of taxa (Bolnick et al. 2003). Although individual slugs may eat only one or two species, many sacoglossans appear more polyphagous when evaluated across different habitats and /or their geographical ranges (see Fox & Morrow 1981). Thus, whether results from host-specificity trials using progeny of Martinique slugs imported to France (Meinesz et al. 1996; Meinesz 1997a,b; Meinesz & Thibaut 1998; Thibaut et al. 1998, 2001; Thibaut & Meinesz 2000) are representative of the responses of the species as a whole is unclear. Also, sample sizes of 7–20 slugs per algal treatment (Thibaut et al. 2001) may not be sufficient to ascertain if intrapopulation variation occurs in E. subornata, a potential biocontrol agent. Finally, past research (Jensen 1981) on E. subornata (as E. cauze) and O. azuropunctata demonstrated that these sacoglossans have no significant preferences among Caulerpa spp. (if animal size was disregarded); thus, host changes would be expected.

Role of host susceptibility The role of algal physiology and stress in determining susceptibility vs. resistance to specialized sacoglossans is in its infancy (Trowbridge 1998b, 2002). Preference hierarchies can be reversed or modified depending on the condition and age of the algal hosts (Trowbridge, Hirano & Hirano, unpublished data). Plant–herbivore interactions are complex; marine risk assessment needs to incorporate and test explicitly such known vari-ation. McEvoy (1996), Secord & Kareiva (1996), Thresher et al. (2000) and references therein have made analogous comments for their respective study systems. Importance of intraspecific genetic variation Intraspecific genetic variation in sacoglossans is very high (Theisen & Jensen 1991) and population subdivisions (morphs, varieties, etc.) have long been recognized. Sacoglossans also exhibit considerable behavioural variation (Trowbridge 1991a,b; this study). Quantitative details about the relationship between genetic and behavioural variation are sorely needed before any intentional species introductions are made; this view has been emphasized by numerous terrestrial ecologists. Predictions made for specific inbred lineages (e.g. E. subornata), strains (e.g. of bacteria) or clones (e.g. viruses) may not be adequate to describe species-level responses. Risk assessment trials should incorporate intraspecific variation of host and control agent explicitly. Role of evolutionary change All biological control agents and hosts have the potential to evolve in response to varying conditions (Secord & Kareiva 1996; Simberloff & Stirling 1996). For sacoglossans with their known high genetic and behavioural variation, short generation times (annual to subannual) and generally high dispersal capabilities, host specificity − at the species level − has been overstated, particularly at large spatial and temporal scales. In conclusion, sacoglossan host-changes can readily occur on ecologically relevant spatial and temporal scales. Thus, the ‘peril of the host-specificity paradigm’ (sensu Secord & Kareiva 1996) − that specialists could change their associations − is exhibited by sacoglossans which are considered traditionally among the most oligophagous marine herbivores. The increased rate of accidental introductions of marine organisms and the frequent proliferation of marine pests warrants increased consideration of how native consumers will respond to introduced prey and the conditions under which marine biological control is a safe and predictive management strategy. As stated lucidly by Louda et al. (1997), ‘The eradication of a nonindigenous species after establishment is extremely difficult at best … , so the responsibility for demonstrating that a release [of a biological control agent] will have no unacceptable ecological consequences


must reside with the advocates of the introduction’ (p. 1090). Future scientific risk assessment of marine specialist herbivores should include comprehensive evaluations of (1) slug populations in native algal communities, (2) intra- and interpopulation variability in host use, (3) causal basis of host choice and (4) genetic variation (if any) associated with host-specific differences in preferences and diet breadth. Finally, risk assessments and management strategies should be scientifically rather than politically based.

Acknowledgements I thank C.D. Todd, S. Wieczorek and C. Bird for their generous advice and support during the Scottish portion of the project; C. Little, P. Stirling and A. Miles during the Lough Hyne trip; B. Farnham and L. White during the Guernsey trip; and C. Hewitt and M. Campbell during the Australian part of the project. Valuable assistance in the field and laboratory was provided by H.A. Ross, C. Little, P. Stirling and A. Miles. I thank the following friends and colleagues for their generous comments and constructive criticisms on earlier drafts: M.C. Miller, R. Taylor, D. Secord, J. Goddard and one anonymous referee; this paper was improved substantially by their advice and suggestions. I thank D. Raffaelli for his graciousness. This research was supported by the Hatfield Marine Science Center, Oregon State University; Gatty Marine Laboratory, University of St Andrews; Centre for Research on Introduced Marine Pests; a Leverhulme Trust Visiting Fellowship; and National Science Foundation grant INT-0211186.

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