Competitive interactions between two species of intertidal herbivorous gastropods from Victoria, Australia

f” E*cp.8%&X. B&t. Ecol., 1989, Vol. 125, pp. 1-12 Elsevier

JEM 01 I88

Competitive interactions between two species of intertidal herbivorous gastropods from Victoria, Australia G. P. Quinn and N. R. Ryan ~e~ar~en~

of Zoolo~,

University

of ~elb~ume, Parkviik, liictoria, Astrali&

(Received 29 April 1988; revision received 7 October 1988; accepted 14 October 19%) Abstract:

The competitive interactions between two species of intertidal herbivorous gastropods, Amnocochlea conscrictu (Lamarck) and Bembicium nanum (Lamarck), were examined experimentally at two times of the year on a rocky shore in Victoria, Australia. There was little mortality of either species during the experiment, except for A. constricta at the greatest experimental densities in summer/autumn. Competition for food does not appear to regulate the densities ofeither species, which contrasts markedly with the strong intraspecific and interspecific competitive interactions between herbivorous gastropods determined from similar but more extensive experiments on rocky shores in New South Wales. For each species, the effects of competition for food on body weights were greater in summer/autumn than in winter/spring, corresponding to seasonal changes in the abundance of macroalgae on the shore. For A. consticta, intraspecific competition had a stronger negative effect on body weight than interspecific competition with B. nanurn, whereas there was no such difference between intraspecific and interspeGi~c competition for 3. nanurn. The exclusion oftbe pulmonate limpet ~~~~~~~ ~je~e~e~~~ Quay et Gaimard in ~~nter/sp~~~ had a negative effect on body weights offA. cms#&fa but no effect on B. ~c17fum.These competitive interactions may be a result of the different feeding behaviours of the two species of snail.

Key words: Competition; Australia

Intertidal

gastropod;

Population regulation;

Seasonat variation;

Victoria,

INTRODUCTION

The importance of competitive interactions in regulating populations of marine invertebrates and structuring marine communities has received considerable recent attention (Branch, 1984). Much of the experimental work on competition for food has been done on intertidal herbivorous gastropods. Underwood (1976, 1978, 1984a), Geese 6% Underwood (1982) and Fletcher & Geese (198.5) have demonstrated that complex intraspecific and interspecific competitive interactions between herbivorous gastropods occur on rocky shores in New South Wales, Australia, and that the food available to intertidal grazers is generally limiting. Experiments from other parts of Australia on intraspeci~c competition (Parry, 1982; Quinn, 1988) and interspecific competition (Black, 1977, 1979) in hmpets have also ~dicated that food can be in short supply for intertidal grazers, at least seasonally. There are, however, few studies directly comparCorrespondence 3168, Australia.

address: G. P. Quinn, Department of Zoology, Mona& University, Clayton, Victoria

0022-098 1~89~~03.50Q 1989 Elsevier Science Publishers B.V. (Biomedical Division)

2

G.P.QUINI-4 AND N.R.RYAN

able in aim or methodology to those in New South Wales, although Ortega (1986) has described comparable experiments on limpets from Costa Rica. The need for such similar studies in different geographic regions has been emphasised by Underwood & Fairweather (19861, so that the generality of any conclusions can be assessed. In addition, there is little known about how competitive interactions on rocky shores might vary spatially or seasonally (see Underwood, 1984a; Quinn, 1988). This study examines intraspecific and interspecific competitive interactions between two species of mobile grazing gastropods, the trochid ~~~tr~~~~~~ c~~st~&t~ (Lamarck) and the littorinid ~e~~jc~~~ n~~~~ flamarck), in the mid- to upper Iittoral zone of an intertidd rocky shore in Victoria, Australia. Various aspects of the biology of each species have been described from New South Wafes [see Underwood (1979) and references therein], ~7700 km north of the present study, and B. n~nu~ has been included in an investigation of competitive interactions among grazing gastropods, also in New South Wales (Underwood, 1978). A. constricta was not included in that study because of its preference for rock pools (Underwood, 1978), a preference not shown by this species at the site of the present study. The effects of food availability on the growth of B. ~~~u~ (Unde~ood, 1984b) and the shell colour of A. con~t~cta (Underwood & Creese, 1976) have also been examined, The abundance of macroalgae in the mid- to upper littoral zone of the present study site shows strong seasonal variation (Parry, 1982; Quinn, 1988). The encrusting brown algae Ra$va spp. were absent during summer, becoming re-established in late autumn and reaching maximum abundance in spring. Foliose species were not common - the brown alga Scytos~~on ~~~~~t~~awas distributed patchily, and only occurred in spring, and the green algae U&a lu~t~c~ and ~~~e~~~~~~~~~~t~sti~a~~were only rarely observed. Parry (1982) and Quinn (1988) have also shown that the levels of intraspecific competition in, and the availability of food to, prosobr~ch and pulmonate limpets in the mid littoral zone vary seasonally and that starvation was a likely cause of mortality of two species during summer and autumn. Consequently, the experiments described here were done in winter/spring and in summer/autumn, corresponding to the maximum and minimum levels of food availability described by Parry (1982) and Quinn (1988).

MATERIALS AND METHCXXS

The study site was the sandstone inte~id~ shore at Girth Point, San Remo, Victoria, which has been described by Parry (1982) and Quinn (1988). The rock platform used for experiments extended from the edge of a sand belt at the top of the shore [ m 1.4 m above Chart Datum (CD.)] to an area of rock rubble (~0.3 m above CD.) which extended into the sublittoral. This region was numerically dominated by four species of grazing gastropods (Table I). ~ustru~~~~ieu constricts and Be~z~i~i~~ ~~~~~ occurred in the range 1.0-1.3 m above CD., although juvenile B. ~~~~~ occurred in large densities down to 0.5 m above C. D. The pulmonate limpet ~~~~~~a~

COMPETITION BETWEEN INTERTIDAL GASTROPODS

3

diemenen~is Quoy et Gaimard was common within the range of these two species of snails, but increased in abund~ce down the shore, reaching a m~~urn density of 3 1000 1 m - ’ at x 0.6 m (Quinn, 1988). The prosobranch limpet Celluna tramose~ca TABLE I

The mean densities (n .0.25 mm2 quadrat, f SD, n = 15; range in parentheses) of four species of grazing gastropods within the range 1.3 m (top of the platform) to 1.0 m above CD. (the lower limit of adults of A. consrricta and B. nanum). An experimental density of 10 per cage equals 5 25 0.25 m - ‘. Date May 1981 February 1982

S. diemenensis

A. constricta

B. nanum

C. tramosericct

38.2 + 6.5 (O-83) 41.4 f 7.5 (3-106)

9.7 + 3.6 (O-18) 5.5 + 1.4 (O-16)

41.5 + 10.4 (2-136) 34.5 + 10.9 (O-146)

1.0 * 0.4 (O-S) 1.6 * 0.6 (O-7)

Sowerby occurred in small densities over most of the area, although it was more abundant in sheltered regions of the shore (Parry, 1982). The only other common grazing gastropod, ZVeritaatramentosa Reeve, was restricted to crevices and rock rubble areas and was uncommon where the present experiments were done. A field experiment comparing the intraspecific and interspecific effects of increased density of A. constricta and B. nanum was done at two times of the year. Adult snails (A. constricta: 16-17 mm shell height; B. nanum: 11-12 mm shell height) were enclosed within cages constructed of galvanised steel mesh (120 mesh. m - ‘) with dimensions of 26 x 39 cm ( E 0.1 m’) and 3 cm high randomly positioned within the normal range of both species (1.0-1.3 m above C. D.). The experiment ran in winter/spring from 25 May 198 1 to 2 1 September 198 l(l19 days) and was repeated with new cage positions and animals in summer/autumn from 10 February 1982 to 13 May 1982 (94 days). Cages examining the effects of competition on A. cQ~t~cta contained the following combinations of species (A = A. cQ~~t~cta, B = B. nanum); lOA, 20A, 40A, 10A + lOB, 10A + 30B; those for B. Nahum contained: IOB, ZOB, 40B, IOB + IOA, IOB + 30A; each treatment was replicated twice. A density of 10 A. constricta per cage represents between 2 and 3 times natural density in May 198 1 and x 5 times in February 1982; a density of 10 B. nanum per cage represents between half natural and natural density at the start of both experimental periods (although z 60% of the population on the shore were juveniles, so 10 per cage is probably greater than natural density of adults). Larger cages were not practical and 10 snails per cage was chosen as a minimum experimental density to ensure enough individuals could be collected for dry weights at the end of the experiment. The cages did not restrict the crovement of smaller S. diemenensis (< 8 mm) and naturally occurring S. diemenen~is were not disturbed when the experiment was started. To examine the effects of S. d~emenensjs on the two species of snails, a stainless steel mesh fence (300 mesh. rn- ‘) was attached around the perimeter of four additional

4

G.P.QUINNAND

N.R.RYAN

cages, two with 10 A. constricta and two with 10 B. nanum, in the winter/spring

period.

All S. diemenensis were removed from these cages and the fence effectively excluded this species. Cages were examined at 2-wk intervals, the number of survivors were recorded and any missing animals were replaced with ones of the same species and similar sizes marked with paint. These replacement animals were not used in any analyses. At the end of each experiment, five original snails were collected from each cage. These snails were removed from their shells, and the soft tissues (less the operculum) were dried to a constant weight at 55 “C and weighed to the nearest 0.01 mg. Five uncaged A. constricta and B. nanum of the same shell heights as the experimental animals were collected at the same times and processed similarly. To examine the effects of the snails on the macroalgae, colour photographs were taken of each cage site at the beginning and the end of each experimental period. These were projected onto an image analyser (MOP 3, Carl Zeiss Inc.) and the percentage cover of each macroalgal species on each cage site was determined. The design and analyses of these experiments followed those originally used by Underwood (1978, 1984a). Dry tissue weights for each species were analysed with four factor (Density: between 20 and 40 per cage; Species: between cages with one species and those with both species; Period: between winter/spring and summer/autumn; Cage: between replicate cages within all treatments) ANOVAs with a nonorthogonal control group (10 per cage) (see Winer, 1971; Underwood, 1978). The effect of S. diemenensis on each species in winter/spring was analysed with two-factor (Presence/Absence of S. diemenensis, Cage) nested ANOVAs. Nested and interaction terms were pooled with the appropriate residual term if not significant (P > 0.25).

RESULTS

Very few individuals of either species Mortality exceeded 10% only in cages

died during either experimental period. with 40 Austrocochlea constricta during

summer/autumn (no. of snails dead, percentage mortality = 5, 12.5% and 7, 17.5% in each replicate cage). At a density of 10 per cage in winter/spring, there were no significant differences in body weights of Bembicium nanum between replicate cages nor between those in cages with or without Siphonaria diemenensis (Fig. 1A; ANOVA: Cages F2,16 = 1.87 NS, Presence/Absence of S. diemenensis F, .2 = 0.09 NS). Body weights of B. nanum in cages were significantly less in summer/autumn than in winter/spring in ah other treatments (Table II, Fig. lA), although uncaged animals, in contrast, were significantly heavier in summer/autumn (ts = 2.76, P < 0.05). This indicates that the effect on body weight of being caged at any density was greater in summer/autumn (i.e., when there was greater loss of tissue weight compared to uncaged controls). There were no significant differences between different densities nor between intraspecific or interspecific treatments

CQMPETITION BETWEEN INTERTIDAL GASTROPODS

5

(Table 11)and no interactions between any of the factors. There was si~~c~t variation between replicate cages within the treatments, a~thou~ for ease af presenta~on, data from replicate cages were pooled in Fig. 1. Low replication (n = 2 cages) precluded meaningful statistical analyses of macroalgal abundances, although some patterns were apparent. Only brown macroalgae were

A

::::: i::::

::::a i:::: 2::: .;zi; v::: . .. . :;ii’: piEi *:1:: .:::i :g :::: ::::

.::a .::.: ::I: :::: :::: :::: :::: :::: i::: :i:: :::i

~ IO6

UC 108 -5%

IOB

208

408

lOB+ fOA

lOB+ 30A

208

408

108t 10A

1OBt 30A

Fig. 1. (A) The mean dry tissue weights (_+SE, $8= 10 from two rep&ate cages or uncaged snaik) of Bembicium nanum. (B) The mean percentage cover ( f SE, n = 2 replicate cages) of the macroalgae Scytosiphon lomentariu (S), at the end of winter/spring only, and Rarfsiu spp. (R), at the end of winter/spring and summer/autumn, in experimental cages with Bembicium nanum. For both figures: unshaded represents the end of winter/spring period and shaded represents the end of summer/autumn period; UC, uncaged; B, Bembicium nanum; A, Austracachlea constricta; Sd, Siphonaria diemenensb.

6

G. P. QUINN

AND N. R. RYAN

found in cages with B. nanum (Fig. 1B). The foliose Scytosiphon lomentaria occurred

in

winter/spring, becoming abundant in the absence of S. diemenensis and in one of the cages with 20 B. nanum. The change in cover of encrusting Ralfsia spp. was generally TABLE II ANOVA

of dry tissue weights ofB. nanum measured at the end ofthe experiment (omitting limpet exclusion treatment). Data are transformed to natural logarithms to provide homogeneous variances (Cochran’s test, P > 0.05). Symbols: df, degrees of freedom; MS, mean square; F, Fratio; P, probability; NS, not significant (P > 0.05). Source

of variation

Between control density in each period Control densities vs. rest Density (excluding control) Between all densities (including control) Species Period Density x Species Density x Period Species x Period Density x Species x Period Cages w/i all treatments Residual Total

F

df

P

1

13.90

1.33

NS

1 1 2

1.12 5.20 3.16

0.11 0.49 0.30

NS

1 1 1 1 1 1 10 80 99

9.53 109.07 2.36 0.53 3.41 5.31 10.48 3.13

0.91 10.41 0.23 0.05 0.33 0.51 3.34

NS NS

NS

< 0.05 NS NS NS NS


greater in cages during the summer/autumn period (increasing from zero at the start) compared with winter/spring. At a density of 10 per cage in winter/spring, there were no significant differences in body weights of A. constricta between replicate cages or between those cages with or without S. diemenensis (Fig. 2A; ANOVA:

Cages F2,,6 = 2.21 NS, Presence/Absence

of

S. diemenensis F,,, = 17.67 NS). This test of the effect of S. diemenensis, however, has little power (1,2 df); inspection of Fig. 2A suggests that during winter/spring, body weights of A. constricta were reduced in the absence of S. diemenensis. As was the case for B. nanum, the body weights of A. constricta in cages were significantly smaller at the end of autumn than spring (Table III, Fig. 2A). There was no significant difference, however, in uncaged A. constricta between September and May (ts = 0.39, NS) indicating that, like B. nanum, the effect of caging on body weights of A. constricta was more severe in summer/autumn (Fig. 2A). There were significant differences between control densities (10 per cage) in each period and between control densities and the other treatments (Table III). The significant interaction between the factors Density and Species is because the body weight of A. constricta decreased with increasing intraspecific density but increased, particularly in winter/spring, when caged with increasing densities

of B. nanum (Fig. 2A).

COMPETITION BETWEEN INTERTIDAL

GASTROPODS

7

Very We S. ~~~~~~~~~~grew in any cages with A, ~~~*~~~c~a except where S, ~j~~~~~~~~ was excluded. The p&em of chaz~ge in ~bu~d~c~ of ~~~~# spp. in r&ion to the density of A. cu~~s~r~c~~ was similar to that in cages with B. nafaunt generally a greater increase during s~mer~autumn (increasing from zero) than during winter/sp~ng, with the exception of the treatment with IO A, c~~~~~~c~~ and 30 B. bandy (Fig. 23). Considerable amounts offoliase green algae (C.&a 1~~~~~~ and ~~~~~o~~$~h~ i~~~~~~~~~l~~ grew in cages with only A. c~~ls~~c~uin ~interls~ring~ irrespective of the

tic

1OA -Sd

10A

i !OA

4ClA

1DA

20A

45A

WA+ 15B

mA+ 358

Fig. 2. (A) The mean dry tissue weights <5 SE, n = IO from two repkate cages ar uncaged snails) d A~~srr~u&tea CCWZS~P&U. (B) The mean percentage cover f i SE, n = 2 replicate cages) of the macroalgae ~~yt~~~h~~ fomentutia (S), at the end of winter/spring only, and Rarfsia spp. (R), at the end of wi~ter~spr~n~ and summer/autumn, in experimental cages with Austrac&&a cons?ricta. (C) The mean pooled percentage cover (k SE, n = 2) of ~~rero~~r~~u inlestiturlir and Wvu lactica at the end of wi~ter/s~ring only, in experimentai cages with ~~~~c#c~le~ cuIEstTicta,Shading and other symbols as in Fig. 1.

8

G. P. QUINN AND N. R. RYAN

density of snails (Fig. 2C), but none in summer~autumn. These algae were rarely observed occurring naturally on the substratum at any time of the year, were not recorded in any cage which contained B. nanum, and were not influenced by the presence or absence of S. d~emenensis.

TABLE III

ANOVA of dry tissue weights of A. constricta determined at the end of the experiment (omitting limpet exclusion treatment). Variances were homogeneous. Symbols as in Table II. Source of variation

df

MS

F

P

x lo-*)

Between control density in each period Control densities vs. rest Density (excluding control) Between all densities (including control) Species Period Density x Species Density x Period Species x Period Density x Species x Period Cages w/i all treatments pooled with residual Total

1 1 I

2 1 1 1 1 1 1

90

1.02

71.17

< 0.001

0.32 0.09 0.20

22.08 6.31 14.19

< 0.001 < 0.05 < 0.001

0.62 1.68 0.12 0.06 0.01 0.04 0.01

43.25 116.76 8.07 4.39 0.08 2.65

< 0.001 io.001
99

DISCUSSION

In this study, the smaller body weights of uncaged Bembicium nanum at the end of the winter/spring period compared to summer/autumn were probably due to spawning of this species during late winter and early spring when egg masses were observed on the shore. No such differences in body weights were found for uncaged Austrocochle~ constricta which Underwood (1974) has shown to spawn throughout the year in New South Wales. The experimental densities represented a greater increase of natural density in summer/autumn than in winter/spring (Table I). Nevertheless, the experiments indicated that, compared to uncaged animals, increased density of either species resulted in a greater loss of tissue weight in summer~autumn than in ~nter/sp~ng. This implies that the relative av~lability of food to both species is reduced in summer and autumn. The abundances of fohose macroalgae (Ulna lactuca, Enteromo~~a i~test~nalis, Scytos~~on Iomenta~a) support this ~plication, only occurring in cages and on the shore in winter and spring. In addition, Parry (1982) and Quinn (1988) showed that the encrusting algae Ralfsia spp. disappeared from this shore in summer; in the present

COMPETITION BETWEEN ~~TERT~~AL GASTROPODS

9

study, there were no encrusting algae visible at the start of the summer~autum~ experimental period, whereas the average cover in cages at the start ofthe wint~~sp~ng period was 19%. The greater change in percent cover of Ra@%z spp. in summer~autumn comp~ed with winter~spring in most cages (Figs. l-2) is because autumn is the period when ~~~j~ re-establishes on the shore from zero abundance in February. A similar pattern of seasonal variation in intraspeci~c competition and av~lability of food has been reported by Parry (1982) for Ce&na tramuserica and Quinn (1988) for Siphonaria diemeaensis at Grifith Point. Underwood (1984a) has shown that two species of intertidal snails retained tissue weight at increased densities better in autumn~winter than other times in New South Wales. The seasonal variations in the intensity of competition and relative food a~~lability to A. c~~st~jct~and B. ~an~rn in this study suggest that food shortage, and subsequent starvation, is most likely to occur over summer and autumn, as is the case for C. trumoserica (Parry, 1982) and S. diemenensis (Quinn, 1988) at this site. Although the densities used in these experiments in summer/autumn represented at least twice the natural density of B. nanurn (probably greater for adults only) and up to 20 times the natural density of A. constricta, the loss of body weight due to competition for food was never great enough to cause significant mortality {except at the greatest experimental density of A. constricta). This suggests that mortality due to the effects of competition would only occur naturally if there were a considerable and sustained increase in the densities of populations of either species. Thus, in contrast to the situation determined from comparab‘le experiments in New South WaIes (Underwo~, 1978, 1984a; Creese & Underwood, 1982; Ffetcher & Creese, 1985) and elsewhere (Ortega, 1986}, the avaitabi~ty of food to these microalgal grazers is unlikely to limit density, although it may limit growth of A. constricta at high densities. Unfortunately, the growth of macroalgae, both encrusting and fohose, made measurements of the abundance of microalgal food, as used by Underwood (1984a), impossible, Other factors besides competition must clearly regulate adult densities of both species. One possibility is the recruitment of juveniles. The abundance of juvenile A. constricta was small on the rock platform during the study (unpubl. data) and this species may recruit continuously (Creese & Unde~ood, 1976). The population density of adult A. co~~~t~c~~ may be limited by this Iow, and probably variable, recruitment, as shown by Underwood (1975) for a population of A. con~t~cta on a moderately exposed shore in New South Wales. In contrast, the abundance of juvenile B. nanum was much greater than that of adult 3. natlum at all times of the year. The pap&ion density of adult B. nawm is probably not limited by juvenile recruitment although mortality rates of juvenile B. nanurn could be a major factor. There were no significant intraspeci~c nor interspecific competitive effects on B. ~a~u~~in either period, In contrast, the intraspeci~c effects of large densities were greater than the interspecific effects on A. ~u~~t~eta, p~icul~ly in winter~sp~ng. Similar results were reported by Underwood (1978) who found that the intraspecific effects on mortality and tissue weights of C. t~arn~~e~~~~ were considerably greater than

G. P. QUINN AND N. R. RYAN

10

the interspecific species,

effects due to B. nanum

however,

effects. Underwood

intraspecific (1984a),

or Nerita atramentosa.

effects were not obviously Fletcher

greater

For the latter two than

interspecific

& Creese (1985), and Ortega (1986) have also

demonstrated this type of asymmetrical competitive effect among intertidal gastropods. In soft sediments, Peterson (1982) found that the intraspecific effects on growth and reproduction in two infaunal bivalve species were greater than the interspecific effects and this was attributed to food limitation and partitioning among the two species. In this study, A. constricta were larger than B. nanum and were found to move 2-3 times further per day (unpubl. data). A. constricta has a wide, rhipidoglossan radula with rows of fine lateral and marginal teeth, which is probably suited to removing microalgae from the rock surface, as Underwood (1978) suggested for N. atramentosa (which has a similar radula). This suggests that A. constricta may require more food than B. nanum (due to its larger size) and may be restricted to feeding on, and moving further to obtain, surface microalgae. B. nanum has a narrow taenioglossan radula with few but welldeveloped lateral teeth. In contrast to A. constricta, B. nanum is probably a more robust feeder because it appeared to restrict the development of the green algae U. lactuca and E. intestinalis in winter/spring, and wherever patches of S. lomentaria occurred on the rock platform, B. nanum (and S. diemenensis) was often present actively feeding while A. constricta was rare. This agrees with the observations of Underwood (1980) who reported B. nanum grazing on, and reducing the cover of, a turf of Ulva in experiments in New South Wales. It is likely A. constricta may be assisted in its ability to obtain suitable microalgal food by other herbivores (e.g., B. nanum) which feed on, and reduce the development of, green and brown foliose macroalgae. Branch (198 1) and Hawkins & Hartnoll (1983) have described other cases where one species of grazer restricts macroalgal growth and thus facilitates the feeding by a second species. In particular, Ayling (198 1) showed that one species of limpet depended on urchins to clear surfaces suitable for microalgal grazing. The hypothesis that increased macroalgal growth (potentially kept in check by B. nanum) inhibits feeding by A. constricta is supported by the fact that the body weights of A. constricta were reduced when S. diemenensis was absent in winter/spring and S. lomentaria became abundant. It would also explain the significantly stronger effects of intraspecific compared with interspecific competition experienced by A. constricta (Fig. 2A). Underwood & Fairweather (1986) have emphasised the need for studies on rocky intertidal shores in different areas which are comparable in methodology and interpretation. The study described here provides such a comparison with the extensive experiments from New South Wales (Underwood, 1978, 1984a) and demonstrates that the importance and nature of competitive interactions between intertidal herbivores can vary considerably, both from season to season and from one place to another.

We would like to thank R. W. Day, P. G. F&weather, M. J. Littlejohn, G. D. Parry, and A. J. Underwood for advice and/or reading the manuscript and all those who helped with fieldwork. Comments from two referees improved the manuscript considerably. Support was provided by the Department of Zoology, University of Melbourne and the School of Biological Sciences, University of Sydney.

REFERENCES Ayling, A.M.,1981. The roie ofbiological disturbance in temperate subtidal encrusting communities. EcologJ), Vol. 62, pp. 830-847. Black, R., 1977. Population regulation in the intertidal limpet PuteliooidaaIt~c#stut~(Angas, i865). Oecologia [~erfjFl),Vol. 30, pp. 9-22. Black, R., 1979. Competition between intertidal limpets: an intrusive niche on a steep rocky gradient. J. An&r. Ecot., Vol. 48, pp. 401-411. Branch, G.M., 1981. The biology of limpets: physical factors, energy flow and ecological interactions. Oceunogr. Mar. Sol. Annu. Rev., Vol. 19, pp. 235-379. Branch, G.M., 1984. Competition between marine organisms: ecological and evolutionary implications. Oceanogr. Mar. Biol. Annu. Rev., Vol. 22, pp. 429-593. Creese, R. G. & A. J. Underwood, 1976. Observations an the biology of the trochid gastropod Austrocochlen c~)~~~r~cta (Lamarck) (Prosobran~hia~. 1. Factors affecting shell-banding. J. Exp. Mar. Biol. EC& Vol. 23, pp. 21 l-228. Creese, R. G. & A. J. Underwood, 1982. Analysis of inter- and intraspe~i~c competition amongst intertidal limpets with different methods of feeding. &c&g&r (Be&z), Vol. 53, pp. 337-346. Fletcher, W. J. & R-G. Creese, 1985. Competitive interactions between co-occurring herbivorous gastropods. Mar. Bioi., Vol. 86, pp. 183-191. Hawkins, S. J. & R. G. Hartnoll, 1983. Grazing of intertidal algae by marine invertebrates. Oceanogr. Mar. B&l. Annu. Rev,, Vol. 21, pp. 198-282. Ortega, S., 1986. Competitive interactions among tropical intertidal 1impets.J. Exp. .%iur.Biol. Ecol., Vol. 90, pp, 1l-2.5. Parry, G. D,, 1982. The evolution of life histories of four species of intertidal limpets. EC&.Monogr., Vol. 52, pp. 65-91. Peterson, C. H., 1982.The importance of predation and intra- and interspecific competition in the population biology of two infaund suspension-feeding bivalves, Promtka staminea and C.&one ~~date~~~.EcnL Monugr., Vof. 52, pp. 437-475. Quinn, G. P,, 1988,The ecology of the intertidal pulmonate limpet S~~~~~u~~diemenensti Quoy ef Gaimard. I. Population dynamics and av~lability of fbod. $. Exp. &fur. &I. Scot., Vol. 117, pp. 11.5-136. Underwood, A. J., 1974. The reproductive cycles and geographical distribution of some common Eastern Australian prosobranchs (Mollusca: Gastropoda). Ausr. J: Mar. Freshwater Res., Vol. 25, pp. 63-88. Ilnderwood, A.J., 1975. Intertidal zonation of prosobranch gastropods: analysis of densities of four coexisting species. J. Exp. Mar. Biol. Ecal., Vol. 19, pp. 197-216. Underwood, A. J., 1976. Food competition between age-classes in the intertidal neritacean Netita atramenYOS(X Reeve (Gastropoda : Prosobranchia). .I. Exp. Mar. Biol. Ecol., Vol. 23, pp, 145-154. Underwood, A. J., 1978. An evaluation of competition between three species of intertidal prosobranch gastrupods. Oecofogio (Berlin), Vol. 33, pp. 185-202. Underwood, A.J., 1979. The ecology of intertidal gastropods. Adv. Mar. Biol., Vol. 16, pp. I1 l-210. Underwoad, A.J., 1980. The effects of grazing by gastropods and physical factors on the upper limits of d~strjbution of intertidal macroalgae. Oec~~~a (Be&n), Vol. 16, pp. 201-213. Underwood, A. J., 1984a, Vertical and seasonal patterns in competition for microalgae between intertidal gastropods. ~ee~~a~~ (&r&r), VoL 81, pp. 21 l-222.

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AND N. R. RYAN

Underwood, A. J., 1984b. Microalgal food and the growth of the intertidal gastropods Nerita atrumento$a Reeve and Bembicium nanum (Lamarck) at four heights on a shore. J. Exp. Mar. Biol. Ecol., Vol. 79, pp. 277-29 1. Underwood, A. J. & R. G. Creese, 1976. Observations on the biology of the trochid gastropod Austrocochlea constricta (Lamarck) (Prosobranchia). II. The effects of available food on shell-banding pattern. J. Exp. Mar. Biol. Ecol., Vol. 23, pp. 229-240. Underwood, A.J. & P.G. Fairweather, 1986. Intertidal communities: do they have different ecologies or different ecologists? Proc. Ecol. Sot. Aust., Vol. 14, pp. 7-16. Winer, B.J., 1971. Statistical principles in experimental design. McGraw-Hill Kogakusha, Tokyo, second edition.