Feeding ecology of the Antarctic herbivorous gastropod Laevilacunaria antarctica Martens

Journal of Experimental Marine Biology and Ecology, 236 (1999) 133–148

L

Feeding ecology of the Antarctic herbivorous gastropod Laevilacunaria antarctica Martens Katrin Iken* Alfred Wegener Institute for Polar and Marine Research, Postfach 120 161, Columbusstraße, D-27515 Bremerhaven, Germany Received 17 June 1998; received in revised form 14 October 1998; accepted 26 October 1998

Abstract The grazing activity of the Antarctic prosobranch gastropod Laevilacunaria antarctica on macroalgae was investigated in order to evaluate its position in the shallow water food web of Potter Cove, King George Island, Antarctica. From 12 abundant macroalgal species tested in feeding experiments, L. antarctica avoided only three species, the brown algae Ascoseira mirabilis, Phaeurus antarcticus, and Himantothallus grandifolius, significantly. The gastropod can be classified as a general feeder on macroalgae in the rocky intertidal and shallow waters of Potter Cove. Comparative grazing experiments showed that epiphytic diatoms contribute about 2 / 3 to the total diet of L. antarctica. Mean abundance and biomass of the snails in this area were 292.06135.3 (S.D.) ind m 22 and 1.54961.021 (S.D.) g AFDW m 22 , respectively. The total consumption of macroalgae by the population of L. antarctica in Potter Cove is estimated to be 118 kJ m 22 year 21 . This alone, however, is not sufficient to sustain the standing stock of gastropods in the investigation area. Grazing experiments showed that feeding on macroalgae which carry epiphytic diatoms is about three times higher than on macroalgae without epiphytes. It is therefore concluded that the population of L. antarctica in Potter Cove is maintained by consumption of both epiphytic diatoms and macroalgae. Feeding experiments showed that chemical compounds of macroalgae are not active in a chemical defense against grazing of L. antarctica. It is therefore discussed that structural characteristics of the algae can explain the low grazing rate of L. antarctica on some macroalgal species. Various models explaining macroalgal– herbivore relationships based on functional groups of algae are considered. The predictions on the feeding of L. antarctica derived from these functional form models in many cases correspond with the results derived from feeding experiments in this study. They are, however, inconsistent regarding grazing on or avoidance of some algal species and thereby obscure important information on special adaptations of organisms, e.g. L. antarctica, in macroalgal–herbivore interactions.  1999 Elsevier Science B.V. All rights reserved. Keywords: Antarctica; Feeding ecology; Herbivory; Laevilacunaria antarctica; Macroalgae

*E-mail: [email protected] 0022-0981 / 99 / $ – see front matter  1999 Elsevier Science B.V. All rights reserved. PII: S0022-0981( 98 )00199-3

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1. Introduction Interactions between macroalgae and herbivores are still poorly understood despite some extensive studies which are summarized in several reviews (Lubchenco and Gaines, 1981; Gaines and Lubchenco, 1982; Hawkins and Hartnoll, 1983; McQuaid, 1996). The attempt to deduce general patterns of algal–herbivore relationships normally leads to the conclusion that these relations are too complex to be generalized because they are affected directly or indirectly by many factors. These factors can be abiotic (height of shore, wave exposure, habitat structure) and biotic (community structure, algal growth and recruitment, herbivore density and feeding activity). Furthermore, most of these factors vary considerably in time (McQuaid, 1996). This makes general predictions on the outcome of algal–herbivore interactions difficult and detailed studies are necessary in most cases. There are, however, approaches which generalize macroalgal– herbivore interactions on the base of functional groups of algae (Littler and Littler, 1980; Steneck and Watling, 1982). The impact of herbivore grazing on macroalgal communities or the fitness of individual algae depends on the density of herbivores, their feeding activity as well as on algal defense mechanisms (Hawkins and Hartnoll, 1983; Hay, 1992). Among the taxonomic groups which represent herbivores (Hawkins and Hartnoll, 1983; Horn, 1989), littorinid gastropods are one of the major groups known from most temperate and tropical marine shallow water ecosystems (Norton et al., 1990; McQuaid, 1996). Littorinids are frequently known to function as a trophic link: nutrients assimilated by the algae are recycled by the gastropods and become available to higher trophic level species as faeces (for detritivores) or prey (for predators). In gastropods part of the energy intake is used for mucus secretion (Peck et al., 1993; Niu et al., 1998), which may serve as food for bacteria or other microorganisms. Few is known on the importance of macroalgal–herbivore relationships in Antarctic shallow water ecosystems (Iken, 1996; Iken et al., 1997). The littorinid gastropod L. antarctica is one of the most conspicuous species in the rocky intertidal of Antarctic shallow waters (Richardson, 1977; Picken, 1979). It is most abundant in the upper sublittoral down to 12 m depth and occurs mainly on the fronds of macroalgae or, less frequently, on bare rocks (Picken, 1979). Mean abundance and biomass show high seasonal and spatial variability (Picken, 1979). The importance of L. antarctica in predator–prey interactions and as a potential link between primary producers and higher level predators still remains unclear. L. antarctica and other species of the genus are known to be prey of demersal fish such as Notothenia coriiceps Richardson (Moreno and Zamorano, 1980; Iken, 1996), but very little information is available on the diet of this snail. Picken (1979) assumed it to feed on epiphytic diatoms only, but he did not investigate the feeding ecology of this species in detail. The present study evaluates the significance of macroalgae and epiphytic microalgae in the diet of L. antarctica and the trophic interactions between algae and snails to specify the trophic position of L. antarctica in the food web of the Antarctic rocky intertidal. This investigation aims at, (1) the significance of macroalgal species and the proportion of microalgae vs macroalgae of in the diet of L. antarctica; (2) estimation of

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the algal consumption by the gastropod; and (3) to decide whether macroalgae are protected against grazing by structural thallus features or by their chemical composition.

2. Investigation area, material and methods Sampling was carried out in Potter Cove, King George Island, South Shetland Islands (Fig. 1) from October 1993 to February 1994. The outer shores of Potter Cove consist of ¨ rocky bottom with dense macroalgal growth (Kloser et al., 1994). The south-eastern coast is characterized by a broad rocky intertidal platform which is partly protected against wave impact and grounding icebergs by protruding rocks. The adjacent open

Fig. 1. Geographical map of the study area. Sampling areas for qualitative (hatched area) and quantitative samples (striped area) are marked.

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sublittoral with weakly declining slopes extends from 2 to 10 m depth; the algal community is dominated by big phaeophytes (Desmarestia menziesii Agardh, D. anceps Montagne, Ascoseira mirabilis Skottsberg and Himantothallus grandifolius (Gepp et Gepp) Zinova) and rhodophytes (mainly Palmaria decipiens (Reinsch) Ricker, Iridaea cordata (Turner) Bory, Curdiea racovitzae Hariot in De Wildeman, Gigartina skottsber¨ gii Setchell et Gardner, Plocamium cartilagineum (Linnaeus) Dixon) (Kloser et al., 1996). Specimens of the gastropod Laevilacunaria antarctica attached to the fronds of macroalgae were collected by SCUBA diving in the upper sublittoral (2–5 m depth). Individuals of L. antarctica were distinguished into five size classes (SC): SC1 ( , 2.5 mm), SC2 (2.5–3.49 mm), SC3 (3.5–4.49 mm), SC4 (4.5–5.49 mm), SC5 ( $ 5.5 mm). Mean wet weight (WW), mean dry weight (DW; 608C, 24 h), and mean ash free dry weight (AFDW; 5008C, 5 h) were determined for the members of each size class. Additionally, the mean DW of single faecal pellets was determined for specimens of all size classes (608C, 6 h). Grazing, consumption, and algal defense were determined in feeding experiments:

2.1. Grazing experiments The collected snails were kept at least 1 week in aquaria for adaptation at ambient water temperatures of 18C (60.2) and in semidarkness. During this time they were fed with different macroalgal species. Prior to feeding experiments the animals remained without food for 24 h for gut clearance. For Laevilacunaria antarctica this proved to be a starving period in which most faecal pellets were produced, indicating the major part of gut clearance, without influencing, i.e. broadening, the selection of dietary algal species (Iken, pers. obs.). For grazing experiments the snails were placed into 0.5-l aquaria in following numbers per size class (SC / no.): 1 / 15, 2 / 10, 3 / 8, 4 / 5, 5 / 3. Three replicates of each of these size class experiments were installed to test each of the algal species. Twelve abundant macroalgal species were selected to test the feeding of Laevilacunaria antarctica (Table 2). From these algae, epiphytic diatoms were removed prior to the feeding experiments by incubating the thalli for 7 days in a medium of 500 ml saturated solution of GeO 2 per 1 l filtered seawater. For the experiments, equally sized pieces of diatom-free algae were added to two of the three aquarium replicates per size class, while the remaining replicate per size class stayed without food as a control. Snails and algae were removed from the aquaria after 24 h. Grazing had to be quantified indirectly, since a decrease in weight of algae by grazing could not be detected reliably because of concurrent weight increase owing to algal growth during the experimental period. Therefore, grazing was quantified by measuring the egestion of faecal pellets while feeding on the different algal species. Faecal pellets produced during the experiments were counted and their DW computed from the values given in Table 1. Faecal pellet production in experiments with algal supply was corrected by the pellets produced in the control experiments without algae. The amount of faecal material produced while grazing on different macroalgal species was tested for significant differences by ANOVA with subsequent post-hoc test of differences among means (Sokal and Rohlf, 1992).

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Table 1 Means of size, wet weight (WW), dry weight (DW), and ash free dry weight (AFDW) of five size classes (SC) of L. antarctica as well as the mean dry weight of single faecal pellets (fp) Size class interval (mm ind 21 )

21

Mean WW (mg ind ) Mean DW (mg ind 21 ) Mean AFDW (mg ind 21 ) Mean DW (mg fp 21 )

SC1 (,2.5)

SC2 (2.5–3.49)

SC3 (3.5–4.49)

SC4 (4.5–5.59)

SC5 ($5.5)

1.44 0.53 0.18 0.0007

12.63 3.80 1.83 0.0015

27.08 8.27 3.68 0.0036

49.36 15.41 8.03 0.0054

63.94 19.21 9.48 0.0089

Possible limitations of the approach to quantify consumption via faecal egestion should be kept in mind. Different gut retention time or different digestability of algal species by L. antarctica may influence the egestion rate. To evaluate the importance of macroalgae and diatoms, respectively, in the diet of L. antarctica, additional feeding experiments were conducted. Applying the same experimental conditions as described above, grazing of L. antarctica was tested on seven algal species which still carried epiphytic diatoms (Table 2). Mean faecal pellet production when feeding on algae with epiphytic diatoms was then compared with the faecal pellet production when feeding on algae where diatoms have been removed before the experiments.

2.2. Consumption Consumption (C) was calculated according to the energy balance equation C 5 E 1 A (Crisp, 1984). In feeding experiments with Laevilacunaria antarctica and Antarctic macroalgal species (see Section 2.1), E (egestion) was the produced faecal material. Table 2 Mean individual daily consumption of L. antarctica on macroalgae, derived from the egestion of faecal pellets E during feeding experiments (C5E / 0.6) Macroalgal species

C 2 (6S.D.)

C 1 (6S.D.)

C 1 /C 2

Monostroma hariotii Gain Palmaria decipiens (Reinsch) Ricker Gigartina skottsbergii Setchell et Gardner Plocamium cartilagineum (Linnaeus) Dixon Iridaea cordata (Turner) Bory Georgiella confluens (Reinsch) Kylin Curdiea racovitzae Hariot in De Wildeman Adenocystis utricularis (Bory) Skottsberg Himantothallus grandifolius (Gepp et Gepp) Zinova Desmarestia menziesii Agardh Ascoseira mirabilis Skottsberg Phaeurus antarcticus Skottsberg

0.11560.040 0.07360.067 0.28360.035 0.16860.101 0.18960.049 0.33660.090 0.09860.074 0.13060.049 0.00760.018*** 0.11960.069 0.00560.013*** 0.01960.022***

0.65560.147 0.02460.024 ND 0.69160.143 0.51860.091 ND ND 0.58160.205 0.02160.038 0.26660.095 ND ND

5.695 0.324 ND 4.114 2.745 ND ND 4.469 2.917 2.265 ND ND

Mean ratio C 1 /C 2

3.218

C 2 , consumption of algae without epiphytic diatoms. Significantly lower consumption is marked ( p50.001); C 1 , consumption of algae with epiphytic diatoms; ND, not determined.

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Assimilation (A) could not be determined directly, for no suitable method (e.g. radioactive labelling (Calow and Fletscher, 1972; Wightman, 1975; Weeks and Rainbow, 1990)) could be applied in field experiments in Antarctica. Therefore literature data for the assimilation efficiency (A /C) of herbivore gastropods were used, with a mean A /C 5 0.4 (mean value derived from: Hughes, 1971a,b; Paine, 1971; Wright and Hartnoll, 1981; Barkai and Griffiths, 1988; Davies et al., 1990). Then, consumption was computed as C 5 E / 0.6 [with C 5 E /(1 2 A /C)]. For estimation of population consumption, the abundance and biomass of Laevilacunaria antarctica and of macroalgal species were obtained by repeated monthly square samples (0.25 m 2 , N 5 4–13) taken by SCUBA diving. Snails were counted, their shell diameter measured, and the AFDW determined. Algae were identified to species level and DW (608C, 24h) was taken for the species separately. Daily consumption of the gastropod population (C.pop) was computed from the following parameters: (i) individual consumption in each size class and algal species (CSC,alga ), derived from regression equations presented in Table 3; (ii) number of individuals per size class in each square sample (NSC ); and (iii) proportion of each algal species on total algal biomass (DW) in each square sample (Palga ) Individual consumption per size class on all algal species i (i 5 1,..., N; N 5 12) per square sample was computed as:

O (C N

C.ind SC 5

SC,i

? Pi ) [mg ind 21 0.25 m 22 day 21 ]

i 51

Total consumption per size class and square sample was then calculated as: C.SC 5 C.ind SC ? NSC [mg SC 21 0.25 m 22 day 21 ] Table 3 Relation of consumption (mg; derived from faecal egestion E in feeding experiments with C5E / 0.6) and size (mm) of L. antarctica on different macroalgal species (x5gastropod shell size, y5consumption) Algal species

Regression equation

Monostroma hariotii Palmaria decipiens Gigartina skottsbergii Plocamium cartilagineum Iridaea cordata Georgiella confluens Curdiea racovitzae

y52.322x22.578 y51.06x27.841 y50.597x24.364 y50.742x25.639 y50.276x22.967 y51.478x21.521 y50.005x29.8?10 25 y50.126x20.51 y52.229x22.509 y51.054x21.849 0 (no consumption) 0 (no consumption) 0 (no consumption)

Adenocystis utricularis Desmarestia menziesii Himantothallus grandifolius Ascoseira mirabilis Phaeurus antarcticus

r 2 50.877 r 2 50.914 r 2 50.975 r 2 50.911 r 2 50.825 r 2 50.817 r 2 50.911 r 2 50.89 r 2 50.933 r 2 50.973

x5log (mm) x5(mm) x5(mm) x5(mm) x5(mm) x5log (mm) x5(mm) for x#4 mm x5(mm) for x.4 mm x5log (mm) x5log (mm)

y5log (mg) y5ln (mg) y5ln (mg) y5ln (mg) y5ln (mg) y5log (mg) y5(mg) y5(mg) y5log (mg) y5log (mg)

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Total consumption of all size classes j ( j51,..., M; M55) per square sample was computed as:

O C.SC M

C.square 5

j

[mg 0.25 m 22 day 21 ]

j 51

Mean total consumption per square meter of the population finally sums up from consumption of all square samples k (k51,..., Q; Q535)

SO Q

C.pop 5 4 ?

D

C.square k /Q [mg m 22 day 21 ]

k51

Annual consumption of the L. antarctica population was then estimated, proceeding from a biologically active period of 8 months per year of the gastropods (Picken, 1979).

2.3. Algal defense experiments Experiments for testing potential defense mechanisms of algae were conducted with five algal species, which were rarely, if ever, ingested by L. antarctica in grazing experiments. These were Ascoseira mirabilis, Phaeurus antarcticus Skottsberg, and Himantothallus grandifolius, all Phaeophyta, and Curdiea racovitzae and Palmaria decipiens, both Rhodophyta. Structural features of the algae were excluded by homogenizing the algae and solidifying them in agar, as originally described by Feeny (1970) for terrestrial plants. This method has been applied successfully by Geiselmann and McConnell (1981) and Steinberg (1988) for brown algae to test chemical defense activity of polyphenolics. While thereby the structure of algae is destroyed, the chemical composition of the algal tissue is conserved. For the present study, all test algae and one control alga (Monostroma hariotii Gain) were homogenized separately in seawater (ratio 1:2 w / w) with an Ultraturrax. Remaining thallus pieces were removed from these algal homogenates by sieving with 250-mm mesh size. For each ‘test agar’, 1.5 g agar were boiled in 40 ml filtered seawater and 10 ml test algal homogenate as well as 10 ml control algal homogenate were added to the agar while cooling down. A ‘control agar’ was prepared in the same way but adding control algal homogenate only (20 ml). Disks (3 cm Ø, 3 mm thickness) were cut from solid agars and used as food in algal defense experiments. The experiments were conducted with four specimens of L. antarctica of SC5 in 0.5-l aquaria. Before the experiments, the snails remained for 24 h without food for gut clearance. Each of the five algal species was tested by the following experimental design: eight replicate tests with test algal agars, three replicates with control algal agars, and three replicates remained without food as controls. After 24 h, faecal pellets produced when feeding on test agar disks were counted and compared with the amount of faecal pellets produced when feeding on the control agar and when staying without food. Feeding on different test agar disks was statistically tested by analysis of variance (ANOVA, a 50.05).

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3. Results Mean WW, DW and AFDW and the mean DW of individual faecal pellets per SC of L. antarctica are presented in Table 1.

3.1. Diet composition Laevilacunaria antarctica produced significantly less ( p50.001) faeces when feeding on Himantothallus grandifolius, Ascoseira mirabilis, and Phaeurus antarcticus compared to the remaining eight algal species. Faecal pellet production when grazing on Palmaria decipiens and Curdiea racovitzae was not significantly but considerably lower. Faeces production when feeding on the other algal species did not differ significantly (Table 2). The relation between consumption and individual size of Laevilacunaria antarctica is given as regression equations for the different algal species (Table 3). Mean consumption of algae without epiphytic diatoms (C 2 , derived from egestion of faecal pellets) compared to the consumption of the same algal species supporting epiphytic diatoms (C 1 ) varied considerably for the seven algal species tested (Table 2). On average, consumption was about three times higher when grazing on algae with epiphytic diatoms (mean C 1 /C 2 53.22).

3.2. Consumption Abundance and biomass of the gastropods in the rocky intertidal of Potter Cove amount to 2926135.3 (S.D.) ind m 22 and 1.54961.021 (S.D.) g AFDW m 22 , respectively (Table 4). Mean daily consumption of the population of L. antarctica amounts to 37.6 mg DW algae m 22 day 21 . Proceeding from a biologically active period of the gastropods of about 8 month per year (Picken, 1979), total consumption of L. antarctica in the rocky intertidal of Potter Cove can be estimated as 9.03 g DW algae m 22 year 21 .

3.3. Structural defense of macroalgae Agar disks were accepted as food by L. antarctica since faecal pellet production in Table 4 Monthly and total means of biomass (B), abundance (N), and consumption (C; computed from faecal egestion E with C5E / 0.6) of L. antarctica in Potter Cove derived from quantitative benthos sampling Month (replicates)

B (g AFDW m 22 )

N (N m 22 )

C (mg DW m 22 )

October 1993 (4) November 1993 (10) December 1993 (13) January 1994 (8)

1.30560.859 1.16860.859 1.63160.843 2.01461.441

256.06169.8 248.06136.6 290.26114.7 363.56144.9

43.96630.08 28.52626.49 40.21627.61 41.62629.31

Total mean

1.54961.021

292.06135.3

37.62627.33

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Fig. 2. Faecal pellet production of L. antarctica in feeding experiments with agar disks containing test algal extracts. Significant higher (* p,0.05) and lower faecal pellet egestion (*** p,0.001) are marked. T, test algal agar; C, control algal agar; B, blind (no agar).

experiments with agar disks as food was significantly higher ( p,0.001) than in those without food supply (Fig. 2). The gastropods grazed on all agar disks containing homogenates of algal species which were normally not ingested. The amount of faecal pellets produced when feeding on test and control agar disks, respectively, was not significantly different, except for Ascoseira mirabilis. For this brown alga, feeding on the test agar disk was significantly higher ( p,0.05) than on the control agar (Fig. 2).

4. Discussion In Antarctic shallow waters, grazing on macroalgae is poorly investigated. Mostly, herbivore feeding refers to grazing on microalgae only (e.g. Richardson and Whitaker, 1979). Few studies deal with the significance of macroalgae as food for invertebrates (Richardson, 1977; Brand, 1980) and none of them investigates the relative importance of different algal species in detail.

4.1. Diet composition Littorinid gastropods can generally be classified regarding their feeding type (McQuaid, 1996). Determination of the feeding type largely effects the conclusions one can draw on the ecological impact an organism has on the macroalgal community structure. Epiphytic grazers are generally supposed to have no direct effect on

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macroalgal communities but rather enhance algal fitness by reducing detrimental effects of epiphytes on the host algae like shading, drag forces, or frond breakage (D’Antonio, 1985). Macroalgal grazers may control algal biomass directly or indirectly due to subsequent tissue loss after damage by grazing (Johnson and Mann, 1986). The Antarctic shallow water prosobranch Laevilacunaria antarctica can be assumed to be either an epiphytic grazer or a macroalgal grazer. Therefore, in the present study the diet of L. antarctica was investigated to evaluate the importance of macroalgae and epiphytic microalgae, respectively. Lab experiments showed that this gastropod species is feeding on the macroalgae themselves and not only on the epiphytic diatoms, as assumed previously (Picken, 1979). L. antarctica is a general feeder on macroalgae as it grazes on most of the investigated algal species. Reasons for the low feeding rate of the snails on some algal species will be discussed below. Then, the grazing on macroalgae with and without epiphytic diatoms was compared. On average, feeding on algae with diatoms has been three times higher. The proportion of macroalgae and diatoms in the natural diet of L. antarctica can therefore be assumed to be 1 / 3 and 2 / 3, respectively. Obviously, L. antarctica has a mixed diet of macroalgae and of epiphytic diatoms and cannot be classified exclusively as an epiphytic or a macroalgal grazer.

4.2. Consumption Mean macroalgal consumption of the L. antarctica population in Potter Cove is computed to be 117.8 kJ m 22 year 21 (mean conversion factor for macroalgae is 13.05 kJ g DW 21 ; following Paine and Vadas, 1969). Is this food ingestion sufficient to maintain the standing stock of L. antarctica in Potter Cove? To evaluate the overall importance of macroalgae in the diet of L. antarctica, the consumption / biomass ratio (C /B) can be calculated. This ratio expresses the total consumption which is necessary to sustain the existing animal biomass. C /Bexpected for Laevilacunaria antarctica: C /Bex can be calculated from the known parameters growth efficiency (production / consumption; P/C) and productivity (production / biomass; P/B): C /Bex 5 (P/x) /(P/z) with P/C 5 x and P/B 5 z With a mean P/B of 1.5 year 21 for L. antarctica (Brey and Clarke, 1993) and a mean P/C for herbivores of about 0.1 (Pauly and Christensen, 1995), C /Bex can be computed as: C /Bex 5 (P/ 0.1) /(P/ 1.5) 5 15 year 21 The expected C /B ratio can be compared to the calculated ratio from actual consumption on macroalgae: C /Bcalculated for Laevilacunaria antarctica: C /Bcal for L. antarctica is derived from the known parameters of mean consumption (118 kJ m 22 year 21 ) and mean biomass (30 kJ m 22 , conversion factor is 18.85 kJ g AFDW 21 ; Brey and Clarke, 1993):

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C /Bcal 5 118 / 30 ¯ 4 year 21 The expected C /B ratio of L. antarctica is 3.75 times higher than the one calculated from the actual consumption on macroalgae. Hence, consumption on macroalgae alone is in fact too low to sustain the standing stock of L. antarctica. Feeding on macroalgae alone can accordingly explain only about 1 / 4 of the food supply needed to maintain the biomass of L. antarctica in Potter Cove. The remaining 3 / 4 of necessary food supply may be explained by feeding on epiphytic diatoms: in their natural environment the gastropods will encounter macroalgae which naturally carry epiphytic diatoms, and grazing in the field will hence be on macroalgae as well as on the epiphytes. As shown in feeding experiments in this study, epiphytic diatoms contribute with 2 / 3 to the diet of the snails, which is about the same order of magnitude as the 3 / 4 lacking in the C /B ratio. Consumption has to be trebled when grazing on epiphytes is taken into account. This will result in a C /B ratio of (3?118) / 30¯12 years 21 , which is well in the range of the expected 15 years 21 . This results show clearly that only the mixed diet of both the macroalgal tissue itself and the epiphytic microalgae enables L. antarctica to maintain its population in the rocky intertidal of Potter Cove. This supports the results shown above (Section 4.1), that L. antarctica can be classified as a mixed macroalgal-epiphyte grazer.

4.3. Structural defense of macroalgae Among the various factors mediating seaweed–herbivore interactions, most common in algal defense are chemical compounds or structural features of the algae (Paul and Hay, 1986; Hay and Fenical, 1988; Hay, 1992). A possible chemical defense of Antarctic macroalgae was checked in feeding experiments with algal agar disks, where the structural characteristics of those algae which are naturally avoided by L. antarctica were altered without changing their chemical composition. Feeding on all tested algal agar disks gave evidence that grazing of L. antarctica is not influenced significantly by chemical products of the algae. Compounds found in Antarctic algae such as polyphenolics (Iken, 1996) obviously do not serve as antifeedants against L. antarctica, although a repellent effect of such chemicals is frequently observed in tropical and temperate regions (Steinberg, 1986; Paul, 1987; Steinberg, 1988; Hay, 1992; Steinberg, 1992). However, the polyphenolics present in the Antarctic brown algae Himantothallus grandifolius, Ascoseira mirabilis and Phaeurus antarcticus (Iken, 1996) may well be active in algal chemical defense against other herbivores than L. antarctica. In the case of L. antarctica, structural attributes of the algae seem more likely to function as defense against the herbivore grazing. It is well known that structural characteristics of macroalgae such as thallus toughness and calcification play an important role in gastropod–algal relationships. Littler and Littler (1980) as well as Steneck and Watling (1982) developed a classification for algae based on algal morphology and anatomy and relate it, among others, to the susceptibility of algae to herbivore predators. Littler and Littler (1980) postulate in their ‘predation hypothesis’ that high thallus toughness combined with low photosynthetic rates and low calorific content should

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decrease the susceptibility of an algal species to herbivore predators. Such physiological parameters as light saturated net photosynthesis (Pmax , based on fresh weight) and C / N ratio were discussed by Weykam et al. (1996) for Antarctic macroalgae in relation to their growth form. I summarized their results for those algal species being of interest for the present study in Table 5, where predictions of grazed and not grazed algal species based on the model of Littler and Littler (1980) are compared with the results of the present study. The predictions of avoided macroalgal species are verified only by the brown algae Ascoseira mirabilis and Himantothallus grandifolius. These tough leathery algal species show high C / N ratios and comparatively low Pmax rates and are not grazed by L. antarctica. Other algal species which are rarely eaten by L. antarctica such as Phaeurus antarcticus, Curdiea racovitzae or Palmaria decipiens do not confirm the predictions made by the model of Littler and Littler (1980). These algal species exhibit very low C / N ratios and comparatively high Pmax rates, the latter especially the brown alga P. antarcticus. Reversely, some tough algal species showing high C / N ratios and low Pmax rates (e.g. Iridaea cordata, Gigartina skottsbergii) are grazed by L. antarctica which also is inconsistent with the hypothesis of Littler and Littler (1980). Steneck and Watling (1982) consider also the mode of grazing and structure of the feeding apparatus of herbivore gastropods in their classification of susceptibility of morphological algal groups. Different radula types should enable the respective gastropods to use optimally different algal groups of varying thallus toughness and growth forms. For gastropods with a taenioglossan radula like Laevilacunaria antarctica, the functional group approach of Steneck and Watling (1982) predicts feeding on microalgae and filamentous algae mainly. Because of the enlarged rachidian and lateral Table 5 C / N ratio and net photosynthesis rate Pmax (mmol O 2 g 21 FW h 21 ) of Antarctic macroalgae (Weykam et al., 1996), as well as their thallus form (classification of algal functional groups as defined by Steneck and Watling (1982)). Macroalgal species

Thallus structure

C/N

Pmax

L&L This study S&W This study

Monostroma hariotii Adenocystis utricularis Phaeurus antarcticus Plocamium cartilagineum Georgiella confluens Desmarestia menziesii Palmaria decipiens Gigartina skottsbergii Iridaea cordata Curdiea racovitzae Ascoseira mirabilis Himantothallus grandifolius

Foliose Saccate / foliose Filamentous / corticated Corticated Corticated Corticated Foliose / leathery Leathery Leathery Leathery Leathery Leathery

7.8 11.6 6.3 7.5 7.0 7.3 5.6 10.6 9.2 7.3 10.5 15.2

37.3 27.8 128.8 17.4 24.0 18.9 27.7 6.6 19.0 20.8 15.9 7.4

1 1 1 1 1 1 1 2 2 1 2 2

1 1 2 1 1 1 2 1 1 2 2 2

1 1 1 1 1 1 ? ? ? ? ? ?

1 1 2 1 1 1 2 1 1 2 2 2

The results of this study on the grazing of Laevilacunaria antarctica on macroalgal species are compared to the predictions made on grazed (1) and not grazed (2) algal species based on the models of Littler and Littler (1980) (L&L) and Steneck and Watling (1982) (S&W). (?) No clear predictions can be made by the model of Steneck and Watling (1982) on the grazing on leathery algal species.

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teeth, taenioglossan radulae are further characterized as universal tools which should enable the gastropods to graze on some corticated or even leathery algae (Steneck and Watling, 1982; Hawkins and Hartnoll, 1983). Comparison of the algal dietary range of L. antarctica with these predictions confirms that this gastropod species in fact is a general herbivore (Table 5). To the diet of L. antarctica comprise epiphytic microalgae which are scraped from the thallus surface, foliose species like Monostroma hariotii, corticated species such as Desmarestia menziesii, Georgiella confluens, or Plocamium cartilagineum, and even some leathery species like Iridaea cordata or Gigartina skottsbergii. The algal species which are rarely eaten by L. antarctica are the filamentous / corticated species Phaeurus antarcticus and some leathery species (Himantothallus grandifolius, Ascoseira mirabilis, Palmaria decipiens, Curdiea racovitzae). Referring to the hypothesis of Steneck and Watling (1982) the filamentous / corticated P. antarcticus should be easily grazed by L. antarctica. This inconsistency can be related to the dense cover of assimilation hairs in P. antarcticus which may impede a firm attachment of the snails to the thallus. As discussed by Watson and Norton (1985) for grazing Littorina species it is essential for gastropods to attach firmly to the substratum to compensate abrasion forces during radula use. The different feeding activity of L. antarctica on leathery algal species could possibly be explained by detailed investigations of their thallus structure and the interaction of the radula activity with the thallus surface. As described by Feeny (1970) algal thallus toughness can be measured relatively by the force needed to puncture the fronds. Furthermore, Watson and Norton (1985) determined abrasion resistance of algal thalli using an abrasive wheel simulating radula forces. Padilla (1985) improved the latter method by using the real radulae of limpets to measure abrasion forces and thallus resistance. Such measurements have to be subject of future studies on Antarctic macroalgae to give deeper insight in the feeding interaction between L. antarctica and algae. In general, models of algal functional groups and functional radula morphology can lead to useful predictions of algal–herbivore relationships. But as shown in this study, these relationships have to be checked carefully in detail and grazing of herbivores cannot be explained exclusively by functional form models considering thallus toughness and growth form. As already discussed by Padilla (1989), (1993) for tropical and temperate limpets, also the mode of feeding and the use of the radula have to be considered beside the morphology of the radula. To fully or at least better understand Antarctic algal–herbivore relationships also more detailed experimental investigations of algal defense mechanisms are needed. Trends in community ecology as suggested by Hay (1994), to increase ecological investigations only on the base of functional groups rather than on species level will obscure the unique adaptations in macroalgal–herbivore interactions. The latter, however, are necessary for our interpretation of the evolution and developmental stage of ecosystems. Summing up, Laevilacunaria antarctica can be evaluated as an important herbivore in Antarctic shallow waters. As a generalist on many macroalgal species and on epiphytic diatoms it is well adapted to use the different sources of primary production available. As a generalist it will also be able to flexibly compensate spatial and temporal variability

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of algal availability. It surely is an important link between primary production and higher trophic level predators in coastal Antarctic waters.

Acknowledgements This study was part of the joint German–Argentinean project RASCALS (Research on the Antarctic Shallow Coastal and Littoral Systems). The help of all scientific and logistic staff on the Antarctic base Jubany and Dallmann Laboratory is gratefully acknowledged. I want to thank especially Dr T. Brey and Professor Dr W. Arntz (Alfred Wegener Institute, Germany) for their continuous support and valuable comments on the manuscript. This is AWI Publication No. 1500.

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