Competition conditional on recruitment and temporary escape from predators on a tropical rocky shore

J. Exp. Mar. Biol. Ecol., 1986, Vol. 95, pp. 155-166 Elsevier

155

JEM 619

COMPETITION

CONDITIONAL

ON RECRUITMENT

ESCAPE FROM PREDATORS

JOHN

P.

ON A TROPICAL

AND TEMPORARY ROCKY SHORE

SUTHERLAND

Duke University Marine Laboratory, Beaufort, NC 28516. U.S.A. and SONIA

ORTEGA

Department of Biology, University of South Carolina, Columbia, SC 29108, U.S.A. (Received

21 June 1985; revision

received

10 October

1985; accepted

30 October

1985)

Abstract: On a rocky headland on the Pacific Coast of Costa Rica we document a period of heavy recruitment of the barnacle, Chthamalusfusus Darwin, in an area infrequently visited by its major predator, the muricid gastropod, Acanthina brevidentata (Wood). For much of 1984, Chthamalusfissus occupied most available free space in the area, appearing to surround and imprison pulmonate limpets, Siphonaria gigas (Sowerby), on their home scars. Limpets lost weight when imprisoned, a situation which persisted until barnacles were removed by Acanthina brevidentata predation. Limpets had little effect on barnacles. Heavy barnacle recruitment in predator-free areas occupied by the limpet is unpredictable in space and time. As a result the negative effect of barnacles on limpets probably has little evolutionary consequence for the limpet. Key words: barnacles;

limpets;

gastropods;

recruitment;

competition;

predation

INTRODUCTION

Patterns of distribution and abundance of marine organisms on hard substratum result from the interplay between larval settlement, competition, predation (or herbivory) and physical disturbance (Connell, 1972,1975; Menge & Sutherland, 1976; Lubchenco & Gaines, 1981; Jackson, 1983; Sousa, 1984; Underwood & Denley, 1984). In addition to regulating structure, these processes determine the rate and direction of evolution. For example, the distribution and abundance of algae on coral reefs is controlled by herbivores (Hay, 1981, 1984a,b; Hay et al., 1983; Lewis, 1985, 1986; Lewis & Wainwright, 1985). Selection in algae is for competitive ability in areas where herbivores are scarce (Lewis, 1986) and for herbivore defense where herbivores are abundant (Hay, 1984b). However, neither competition nor predation are important if larval settlement is insufficient (Paine, 1974; Keough, 1984; Underwood & Denley, 1984) or if disturbances are too frequent (Sousa, 1984). Thus, understanding structure and evolution in these communities depends on knowing how biological and physical processes vary in space and time. Much recent work in the Bay of Panama suggests that predation is the most important 0022-0981/86/$03.50

0

1986 Elsevier

Science

Publishers

B.V. (Biomedical

Division)

156

JOHNP.SUTHERLANDANDSONIAORTEGA

biological process on tropical rocky shores in this region (Palmer, 1979; Bertness et al., 1981; Garrity & Levings, 1981, 1983; Menge & Lubchenco, 1981; Levings & Garrity, 1983, 1984; Lubchenco et al., 1984). Most sessile invertebrates are continuously removed from open surfaces by gastropod and fish predators. As a result there is much free space and competition is unimportant. Mobile invertebrates take refuge on home scars or in holes and crevices to escape fish predators at high tide. Is predation as intense and pervasive on all rocky shores in the eastern tropical Pacific as it is in the Bay of Panama? If not, which other biological processes, e.g., settlement and competition, are important and on what temporal and spatial scales do these processes vary? Here we provide a partial answer to these questions by documenting direct and indirect interactions between a barnacle, Chthamalusfissus Darwin, its major predator, the muricid gastropod, Acanthina brevidentata (Wood), and a pulmonate limpet, Siphonaria gigas (Sowerby). Barnacles settled heavily and temporarily escaped predation by gastropods. The resulting high barnacle densities impeded the grazing activities of the limpet, an interaction probably best described as competition for space. All processes appear to vary markedly in space and time.

STUDY SITE

The study site was the same as that used by Ortega (1985), a rocky headland called Punta Mala (= Punta Judas) on the central Pacific Coast of Costa Rica (9”3 1’N : 84” 32’W). The physical environment is similar to that described for Panama (Menge & Lubchenco, 198l), with a dry season extending from December to April and a wet season from May to November. The headland consists of horizontal, southwardly projecting, sandstone benches which in places are canted towards the east. Our observations were made in a 30 x 15 m area on one such gently sloping, east facing surface extending from mid-low to high intertidal zones ( + 1.0 m to + 2.6 m). In this case the high zone ends in a drop-off to deeper water which receives the full force of oceanic waves. The resultant spray keeps the high zone wet for greater periods of time than for other sites at similar tidal elevations. Animals abundant on open surfaces include the barnacles Tetraclita panamensis Pilsbry and Chthamalusfissus, the herbivorous gastropods Nerita funiculata (Menke), Fissurella virescens (Sowerby), Siphonaria gigas and Siphonaria maura (Sowerby), and the carnivorous gastropod, Acanthina brevidentata (Ortega, 1985). Crustose algae similar to those described by Lubchenco et al. (1984) and Levings & Garrity (1984) for Panama, are abundant throughout the site. Foliose algae are also present along the drop-off during the wet season.

RECRUITMENT,

COMPETlTION

METHODS

ABUNDANCE

OF LIMPETS

AND PREDATION

157

AND RESULTS

AND BARNACLES

Abundance of Chthamalus fissus was followed in several ways. Four permanent quadrats (6 x 9 cm) were marked with stainless steel screws at each of two sites 10 m apart at + 2.6 m near the drop-off. These quadrats were censused photographically with a Nikonos IV fitted with strobes and a 1: 3 extension ring and focal framer. The framer fitted in the slots of the screws, providing precise positioning of the camera from photograph to photograph (Wethey, 1984). Photographs were taken at l- to 3-month intervals from 31 March 1983 to 20 November 1984. Percent cover of C.fissus was estimated by projecting each negative onto a matrix of 100 evenly spaced points covering an area of 5 x 5 cm actual scale, and counting the number of points falling on live animals. Size was determined by tracing the opercular area of individual barnacles from negatives projected onto a computerized digitizing pad (Summagraphics Bit Pad One) (Wethey, 1984). Percent cover of live C. fissus and density of Siphonaria gigas were also estimated in contiguous quadrats (0.25 m’) along four permanent 15-m transects separated by 7 m running perpendicular to the shore. Each transect extended from = + 1.0 m to the drop-off and all were censused in November 1983 and in March, July and November 1984. In the permanent quadrats near the drop-off, percent cover of Chthamalusfissus was very low during most of 1983 (Fig. 1). From September through December 1983, these animals were quite small with opercular areas averaging < 0.5 mm* (Fig. 1). Massive recruitment occurred at both sites in November 1983, seen in Fig. 1 as a large increase in percent cover while mean opercular area remained small. Percent cover remained

1983

1984

Fig. 1. Size (mean opercular area + SD) and percent cover (mean f SD) of live Chthamalus jssus in permanent quadrats at two sites at + 2.6 m: size data from one quadrat at each site; percent cover data from four quadrats at each site; V, site 1; n , site 2.

158

JOHN

P. SUTHERLAND

AND

SONIA

ORTEGA

high through August 1984 with the barnacle population increasingly dominated by larger individuais. A large decrease in percent cover and mean size was seen by November (Fig. 1) as these sites were reached by Aca~lthina ~revi~entuta (see below). In the 15-m permanent transects, percent cover of Chthamalusfissus was low in November 1983, increased during March and July 1984 and decreased again in November 1984 (Table I). Abundance patterns seen in the permanent quadrats (Fig. 1) TABLE

I

Mean ( + SD) abundance of ~i~bonariu gigas (Sg) and C~zha~u[us fzssus (Cf) on Punta Mala, Costa Rica: data from four 15-m permanent transects from mid-low to high intertidal zones (+ 1.0-2.6 m).

sg (No:m-‘) November 1983 March 1984 July 1984 November 1984

46 38 49 65

+ 64.6 & 56.0 & 67.8 + 81.4

Cf percent cover 10 29 24 13

+ f * +

23.3 32.9 32.5 25.9

No. quadrats 119

120 117 118

were characteristic of the entire study area. Density of Siphonaria gigas remained constant until a period of recruitment between July and November 1984 (Table I). Variation in abundance of both species among quadrats in the transects was high (Table I, Fig. 2). In November 1983 there were many quadrats with high densities of

Fig. 2. Percent cover of ChGzamalusfssus and density of Siphonaria g&as in four permanent transects extending from + 1.0-2.6 m: A, November 1983; B, March 1984; C, July 1984; D, November 1984.

RECRUITMENT.

COMPETITION

159

AND PREDATION

S. gigus in the absence of Chthamalusfissus (Fig. 2A). In March and July 1984, however, quadrats with high densities of S. gigas generally had abundant populations of C. fissus (Fig. 2B,C). By November 1984 C.fissus had disappeared from many of the quadrats with high densities of limpets (Fig. 2D), and abundance patterns were similar to those in November 1983. INTERACTION

BETWEEN

BARNACLES

AND THEIR

PREDATOR

During 1984, additional permanent transects were established to follow the interaction between ChthamalusJissus and its major predator, Acanthina brevidentata. These transects were 1.2-2.0 m in length beginning within 1 m of, and running perpendicular to, crevices in which A. brevidentata were abundant. They were censused photographically with the Nikonos IV fitted with a close-up lens that included an area 16 x 25 cm. Photos were taken every 20 cm along each transect on 27 June, 9 July, 22 July and 8 August 1984. Percent cover of live Chthamalusfissus was estimated as

80-

- 800

I

-% - 200

%ZO-

LL

c

L

LL

80- IY %-

,800 - 600

20-

3 0

20 40 60 80 100 120 140 160 180 200

DISTANCE

(CM)

Fig. 3. Percent cover of Chthamalusfissus and density of Acanthina brevidentata in four (I-IV) permanent transects beginning within 1 m of, and running perpendicular to, crevices with abundant A. brevidentata: data from 4 dates, left to right in each group of bars: 27 June, 9 July, 22 July, and 8 August 1984; shaded portion of bars, dead Chthamalus f=sus; unshaded portion of bars, live C.j%sus; Acanthina brevidentata density (solid lines) plotted on date of maximum abundance in each transect; I, 9 July; II, III, IV, 27 June.

160

JOHN

P. SUTHERLAND

AND SONIA

ORTEGA

above from a 5 x 5 cm area taken from the center of each photo. The number of Acanthina brevidentata in each photo was also counted.

The effect of Acanthina brevidentata on Chthamalus jssus was also evaluated with cages that excluded Acanthina brevidentata. Cages were 10 x 10 x 5 cm constructed of 6 mm galvanized mesh and attached to the rock by stainless steel screws inserted into plastic wall anchors. Experiments were conducted within 1 m of two different crevices, each harboring many A. brevidentata. In both areas we placed two total exclusion cages and two three-sided cages which opened in the direction of the crevice to allow easy access by A. brevidentata. Large Chthamalus fissus (> 2-3 mm basal diameter) were collected on chips of rock and cemented into each cage with fast drying hydraulic cement. Censusing was done photographically using the 6 x 9 cm framer. The experiments were repeated twice, from 3-9 July and 29 July-8 August 1984, respectively. Percent survival of C.&us was estimated from maps of individual animals made from projected negatives. The disappearence of Chthamalus fissus during the course of 1984 was due to predation by Acanthina brevidentata. Near crevices, percent cover of Chthamalusfissus was always low, especially that of live animals (Fig. 3). On 27 June live barnacles were numerous at varying distances from the crevices, but most of these were dead by 8 August (Fig. 3). During June and July Acanthina brevidentata emerged from the crevices during late afternoon and early morning low tides and formed feeding fronts near the borders of populations of live barnacles. We show this in Fig. 3 by plotting the abundance of A. brevidentata in each quadrat on the date of its maximum abundance in each transect. No other barnacle predator, e.g. Thais melones (Duclos), was observed feeding on barnacles during this period. Density (& SD) of Acanthina brevidentata averaged over all transects from the four sample dates was 68.3 . m - 2 ( + 13 1.52).

I

t

I

I

AUGUST

JULY ‘984

Fig. 4. Percent survival of Chthamalus jssus on rock chips transplanted to within 1 m of crevices with abundant Acanthina brevidentata: V, data pooled from three-sided cages; n , data pooled from total exclusion cages; top, site 1; bottom, site 2; number of barnacles transplanted 3 July: V, site 1 = 171; n , site 1 = 253; ‘I, site 2 = 297; n , site 2 = 132; number of barnacles transplanted 29 July: V, site 1 = 239; n , site 1 = 184; V, site 2 = 200; n , site 2 = 123.

RECRUITMENT,

COMPETITION

AND PREDATION

161

Predation by A. brevidentata on large Chthamalus jssustransplanted near crevices was very intense; most barnacles disappeared within 6-10 days on rock chips exposed to snail predators (Fig. 4). In contrast, survival was high for transplanted barnacles inside cages, protected from predators. INTERACTION

BETWEEN BARNACLES

AND LIMPETS

At high densities, C. frssus completely surrounded Siphonaria gigas, often appearing to imprison the limpet on its home scar (Garrity & Levings, 1983). Although S. gigas suffers little mortality when maintained at artificially high densities, it does lose weight under these conditions (Ortega, 1985). Two different procedures were utilized to determine whether imprisoning by Chthamalusfissus would have a similar effect on the limpet. In the first, 65 imprisoned Siphonaria gigas which were at least 10 cm from the nearest limpet were individually numbered with DYMO plastic tape. We chose isolated limpets to minimize intraspecific effects (Ortega, 1985). After photographing each limpet with the 16 x 25 cm framer, a circular area 15 cm in diameter was cleared of barnacles around 32 limpets chosen at random. In the second procedure, 102 randomly chosen S. gigas were transplanted to circular areas cleared in dense populations of Chthamalusfissus. Half of the areas were 15 cm in diameter and half were only slightly larger than the shell of the transplanted limpet, such that it was imprisoned by barnacles. The experimental period for both groups was initiated after all transplanted limpets persisted for 2 days, and lasted from 16 June to 1 August 1984. At the end of the experiment all limpets in group 1 remaining on their original home scars were photographed again with the 16 x 25 cm framer. All limpets remaining on their scars (43 in group 1 and 49 in group 2) were collected, measured, their flesh dried to a constant weight at 80 “C and weighed. The possible effect of C.fissus on weight of Siphonaria gigas was evaluated with analysis of covariance (Sokal 8~ Rohlf, 1981) using size as the covariate. The effect of S. gigas on Chthamalus fzssus was evaluated in two ways. Eight imprisoned Siphonaria gigas were chosen from group 1 above, those for which the surrounding populations of Chthamalus fissus were not preyed upon by Acanthina brevidentata during the experimental period. Survival of Chthamalusfissus during the experimental period was estimated in two concentric circles surrounding each limpet, O-l cm and 2-3 cm, respectively, using maps of individual barnacles made from projected negatives. The dependency of percent survival on position was tested with a G-test for goodness of lit using the Williams correction (Sokal & Rohlf, 1981). Most C.fissus in the study area were large relative to the overall size range of this species (> 1.0 mm2 opercular area = > 2 mm basal diameter; J. P. Sutherland, unpubl. data). To determine the effect of Siphonaria gigas on smaller barnacles we exploited a chance occurrence of a single limpet in one of the permanent 6 x 9 cm quadrats mentioned above. We compared the survival and growth of a cohort which settled between 3 November and 8 December 1983, O-l cm from this limpet with that of the same

162

JOHN

P. SUTHERLAND

AND

SONIA

ORTEGA

cohort in the adjacent quadrat, > 5 cm from the nearest limpet. Data on individual barnacles were collected until 20 November 1984 from computerized maps made from negatives projected onto the digitizing pad (Wethey, 1984). S. gigas weighed more after 1.5 months when the surrounding Chthamalusfissus were removed, although the difference was significant only for nontransplanted animals (Table II). By 1 August the adjusted mean weight of nontransplanted Siphonaria gigas in clearings free of barnacles was 29% greater than those surrounded by barnacles (Table II). This is a conservative estimate of the effect of barnacles on limpets since many imprisoned limpets were freed by Acanthina brevidentata during the course of the experiment (e.g., Fig. 3). Weights of transplanted Siphonaria gigas did not diverge, possibly because they were transplanted to areas less favorable than those occupied by TABLE II Effect of ChrhamalusJssus (Cf)

on

adjusted mean weight of Siphonaria gigas (Sg) from 16 June to 1 August 1984 at Punta Mala, Costa Rica. Adjusted mean wt (g) 1 August”

SD Of adj. mean

N

Sg nontransplanted Cf removed Cf present

0.17” 0.12s

0.012 0.012

21 22

Sg transplanted Cf removed Cf present

0.14s 0.13b

0.011 0.012

26 23

a Analysis of covariance on all four groups significantly different (P z 0.05).

(Sokal

& Rohlf,

1981). Means

followed

by same letter not

TABLE III Percent

survival

of Chrhamalusjssus (Cf) from 16 June to 1 August 1984 in two concentric and 2-3 cm around individuals of Siphonaria gigas (Sg).

rings, O-l cm

Sg (cm)

Percent survival Cf O-1 cm

Percent survival Cf 2-3 cm

2.52 3.10 2.45 2.15 2.26 3.00 3.13 2.12

69 58 75 73 50 59 45 38

76 74 67 80 43 50 43 33

ns

Mean 2.29

16

71

ns

Length

a G-test of independence using Williams correction (Sokal & Rohlf, 1981) comparing percent dead, O-l cm and 2-3 cm from each limpet; ns, not significant; * significant,

Sig.”

* ns ns ns ns tlS ns

percent live versus P < 0.05.

RECRUITMENT,

COMPETITION

AND PREDATION

163

nontransplanted animals. Significant divergence in weights of transplanted limpets might have been seen in a longer experiment, but Acanthina brevidentata had removed the larger barnacles from much of the area by August (Fig. 3). Although there was a negative effect of ChthamaZusJissus on Siphonaria gigas, limpets had little effect on barnacles. From 16 June to 1 August 1984 percent survival of Chthamalusjksus was similar in concentric rings O-l cm and 2-3 cm from individuals of Siphonaria gigas (Table III). Mean size of S. gigas was similar to that of the entire population (Ortega, 1985) so the lack of a limpet effect on barnacles was not a result of our sample of limpets being biased towards smaller sizes. Barnacles surrounding these limpets were quite large during the experimental period (June-August 1984), belonging to the same cohorts illustrated in Fig. 1. However, even small barnacles survived and grew equally well O-1 cm from, and > 5 cm from a single limpet from December 1983 to November 1984 (Fig. 5). During this period the limpet did increase in area from 116 to 454 mm2, overgrowing barnacles in the process. Barnacles in this 3

,100

9

& i?

60

DJFMAMJJASOND

1984 Fig. 5. Size (mean opercular area + SD) and percent survival of Chthamalusjssus at + 2.6 m; V, O-l cm from one Siphonaria gigas (initial number of barnacles = 144); n , > 5 cm from S. gigas (initial number of barnacles = 488).

area physically occupied by the limpet were not included in Fig. 5, which only estimates possible bulldozing (Dayton, 1971) of barnacles by the limpet. DISCUSSION

The sequence of direct and indirect interactions described above was initiated by the massive recruitment of Chthamalus fissus during November and December 1983. Sufficient numbers survived and grew such that much of the study area was covered with dense populations of barnacles by March 1984. Foraging by Siphonaria gigas was

164

JOHN

P. SUTHERLAND

AND SONIA

ORTEGA

impeded by barnacles, an interaction probably best described as competition for space. Limpets lost weight until the barnacles were removed by Acanthina brevidentata foraging outward from crevices. There was little negative effect of limpets on barnacles (e.g. Levings & Garrity, 1984), except in areas (scars) physically occupied by limpets. These direct and indirect interactions have some features in common with the “indirect commensalism” described by Dethier & Duggins (1984). In their study, macroalgae outcompeted microalgae in the absence of herbivores. Limpets which specialized on microalgae depended on a chiton to remove macroalgae and allow diatom growth. Limpets thus benefited indirectly from the presence of the chiton even though chitons were potential food competitors, feeding on microalgae as well as macroalgae. In Costa Rica Siphonaria gigas was affected negatively by dense populations of Chthamalus jksus and benelitted indirectly from predation by Acanthina brevidentata on barnacles. However, the interactions described here were conditional on the heavy recruitment of Chthamalus Jissus in our study area during November and December 1983. This is not an annual event on all shores, even though observations in our study area subsequent to November 1984 (J. P. S., unpubl. data) indicate a repeat of this scenario during 1985. Percent cover of barnacles was low in the permanent quadrats during 1983 suggesting the absence of a similar period of high recruitment in 1982. Also, during 1984 the scenario was not repeated in other areas 1 km away where the distributions of C.J%SUS and Siphonaria gigas overlap (J. P. S., unpubl. data), because recruitment of Chthamalusfissus in these areas was much lower. Rather than consider the indirect effects described here “commensalism”, it is probably safer to categorize them presently as “epiphenomena” (Underwood et al., 1983) events occurring only occasionally with few evolutionary consequences. The densities achieved by C. fissus, Siphonaria gigas and other common organisms (Ortega, 1985), demonstrate that many species in our study area do escape their consumers for significant periods of time. In particular, fish predation is not as intense in Costa Rica (Ortega, 1986; J. P. S., unpubl. data) as in the Bay of Panama (Bertness et al., 1981; Garrity & Levings, 1981, 1983; Menge & Lubchenco, 1981; Lubchenco et al., 1984; Menge et al., 1985). In the present study, barnacle mortality as a function of time and distance from crevices suggests that nearly all was due to predation by Acanthina brevidentata. These gastropod predators are restricted in their activities in large degree due to severe heat and desiccation stress during daytime low tides (Garrity, 1984). As a result their effect on barnacles is spatially and temporally variable, a common feature of gastropod-barnacle interactions in intertidal communities (Dayton, 1971; Spight, 1974; Menge, 1976, 1978; Underwood et al., 1983). Variation in biological and physical processes is common in the Eastern Tropical Pacific. On a large spatial scale, the presence (Bay of Panama) or absence (central Costa Rica) of seasonal upwelling (Glynn et al., 1983) may have significant effects on fish populations and, indirectly, on the intensity of fish predation on the shore, On a large temporal scale we point out that the “El NiAo” of 1983 was the strongest of the century (Cane, 1983) and it was during this year that percent cover of Chthamalusfissus was

RECRUITMENT, COMPETITION AND PREDATION

165

low in our study area. Data in this paper make it clear that settlement, competition, and predation can also vary on smaller scales of space and time. Until we know more about this variation, it is too soon to generalize about the organization and evolution of these communities.

ACKNOWLEDGEMENTS

This work was supported by a Sigma-Xi Grant in Aid of Research (S.O.), an NSF Dissertation Grant (S.O.), a Jessie Smith Noyes Grant from OTS (S.O.), an NSF Research Grant OCE-83-08549 (J.P.S.), and a Fulbright Research Award (J.P.S.). The Universidad National de Costa Rica and CONICIT provided accommodation in Costa Rica during 1983. Our work was also made possible by the generous hospitality of D. and N. Izurieta, T. Crichton and T. Cm-ran, the latter Director of the T.H. Curran Marine Field Station, West Esterillos, Costa Rica. Help in the field was provided by H. Caffey, D. Perry, D. Sutherland and S. Sutherland.

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AND SONIA

ORTEGA

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