body-size variation exhibited by an intertidal limpet: influence

ELSEVIER Journal of Experimental Marine Biology and Ecology

189 (1995) 29-45

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Body-size variation exhibited by an intertidal limpet: Influence of wave exposure, tidal height and migratory

behavior

Alistair Hobday*

Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA

Received 24 April 1994; revision received 17 November 1994; accepted 16 December 1994

Abstract

Body size variation of the intertidal limpet Lottiu digitalis (Rathke) and the factors responsible for maintaining it were examined at three central California intertidal sites differing in wave exposure. Limpet body size increased with increasing tidal height. This increase in size with tidal height was correlated with exposure to wave splash and migratory behavior. In areas of high and intermediate wave splash, there was a significant positive correlation between increased limpet size and tidal height, while in sheltered conditions there was no significant gradient in body size. Transplant experiments suggested that the size gradient could be maintained by the upward migration of large limpets and downward migration of small limpets. In the area with little size gradient, there was no significant directional migration of transplanted limpets. Limpets initially exhibited a fixed migratory response when displaced both within an area and between areas differing in exposure. However, after an acclimation period of 5 days in a new exposure condition, the response of transplanted L. digitalis was indistinguishable from that of limpets native to that condition. The findings suggest that both fixed short-term and flexible long-term migratory behavior are in part responsible for the maintenance of body size gradients.

Keywords: Body size variation; Limpet; Lottiu digitalis; Migration; Rocky intertidal zone; Trans- plant experiment; Wave exposure

* Present address: Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0208, USA.

0022-0981/95/$9.50 0 1995 Elsevier Science B.V. All rights reserved SSDI 0022-0981(95)00009-7

30 A. Hobdq )lI J. Eq,. Mar. Bid. Ed 189 ilYY5) 29-45

1. Introduction

Within marine intertidal environments, variation in physical conditions often leads to pronounced interspecific zonation patterns. Such patterns of vertical zonation among rocky intertidal organisms have been documented extensively (Connell, 1961; Paine. 1969, 1974; Dayton, 1971; Vermeij, 1972; Chow, 1975; Bertness, 1977; Underwood, 1979; Doering & Phillips, 1983; Chen & Richardson, 1987; Cushman, 1989; see reviews by Underwood, 1979; Branch, 198 1). Traditionally the upper boundaries of upper intertidal species have been explained by physical factors (heating and desiccation) acting during tidal emersion, while biological factors (predation and competition) are thought to influence the lower distribution limits of intertidal species (Connell, 1961). More recently, several authors have discussed situations where biologically determined upper limits could occur (Underwood & Denley, 1984; Wootton, 1993).

The same physical conditions that influence interspecific zonation also give rise to intraspecific zonation patterns. One striking intraspecific pattern is size distributions. Vermeij (1972) reviewed the trends in shore level size gradients and concluded that there arc two general size patterns exhibited by rocky intertidal gastropods. For species inhabiting the upper intertidal, shell size tends to increase in an upshore direction, while for species inhabiting the lower intertidal, shell size tends to decrease with increasing tidal height. Vermeij considered both patterns to be a result of gradients in the inten- sity and nature of post-larval mortality, with physical extremes high in the intertidal operating most effectively against small gastropods. The generation of such patterns has been explained through differential rates of growth and survival at various tidal heights, while the maintenance of these patterns has been explained via active migration (Vermeij, 1972; Chow, 1975; Bertness, 1977; Doering & Phillips, 1983; Chen & Richardson, 1987; Cushman, 1989).

Within the Acmaeidae, limpet size gradients have been noted, but there have been no studies that have directly assessed body size variation with tidal height or exposure gradients. Although lacking data, some studies have suggested that a pattern of increasing body size with tidal height is usually found in upper intertidal limpets (Lewis, 1954; Frank, 1965; Haven, 197 1; Breen, 1972; Choat & Black, 1979). The upper limit of limpet distribution is thought to be restricted by the desiccating conditions, heat stress and osmotic stress (Lewis, 1954; Frank, 1965; Vermeij, 1972; Branch, 1981; Sanders et al., 1991; Marshall & McQuade, 1992; Edwards, 1969, with opisthobranch snails). According to this explanation for upper limits, small limpets with high surface- to-volume ratios are at a disadvantage compared to large limpets, so small limpets may be restricted to lower heights, leading to a size gradient with increasing tidal height. Frank (1965) and Haven (197 1) noted that the maximum height of the limpet zone depended on exposure to ocean spray, which supports desiccating conditions setting the upper limit.

Observed mortalities due to desiccation or temperature have been limited to high- shore species (Lewis, 1954; Frank, 1965). Wolcott (1973) found that only in high shore species did environmental conditions ever exceed the limpet’s tolerances. He hy- pothesized that this was because a high-shore species might have access to an unex- ploited food source, so it would benefit them to extend their range to the limits of their

A. Hobday /J. Exp. Mar. Biol. Ecol. 189 (1995) 29-45 31

tolerance to capitalize on this food. Thus, high-level limpets might move up and down the shore as seasonal conditions permit. Studies have shown that limpets do migrate seasonally, upshore during fall and downshore during spring (Frank, 1965; Haven, 1971; Breen, 1972). Frank (1965) further demonstrated that upward migrations were increased in response to higher densities. In addition, Miller (1968) showed short-term individual foraging migration in response to tidal cycles, although the limpets returned to the original height at the end of a feeding bout. Despite this understanding, few studies have demonstrated the conditions under which vertical body size gradients are found and maintained.

In this study, my overall objective was to evaluate the influence of tidal height and wave exposure on body size variation exhibited by the upper intertidal limpet Lottiu

digitalis (Rathke). I also investigated the behavioral patterns that could maintain body size patterns. The specific objectives were threefold. First, I measured the vertical ex- tent of the limpet zone at three different levels of wave exposure, then documented the body size pattern along a tidal gradient in these three areas of exposure. Following Vermeij (1972) I predicted that shell size would increase with tidal height, as L. digi-

talis is an upper intertidal species. Second, using transplant experiments, I evaluated the hypothesis that the migratory behavior of limpets was responsible for maintaining body size patterns. I predicted that, as with snails, the pattern would be maintained by migratory behavior, with downwardly displaced large limpets and upwardly displaced small limpets migrating toward the level from which they were removed, while control individuals would move smaller distances in random directions. Also, a series of between-site transplants were performed to determine if limpets from different exposure levels displayed fixed migratory behavior. Finally, to determine how long a particular migratory behavior was maintained, small limpets were transferred to new exposure areas, allowed to acclimate, then the new migratory response was measured. Based on preliminary experiments, I predicted that the magnitude of the migratory response would change to mimic the behavior of the limpets native to that area.

2. Organisms and study sites

Lottia digitalis ( = Collisella digitalis or Acmaea digitalis) (see Lindberg, 1986 for name conventions in Acmaeidae) is a common limpet in the upper intertidal region, ranging from the Aleutians to Baja California (Keen, 1971). Sexes are separate and external fertilization and spawning occurs at least through winter and spring (Fritchman, 1961). This limpet does not have a home scar. Lottia digitalis is the dominant limpet in Cali- fornia on upper intertidal vertical rock walls, extending above median high tide for as much as 2 to 3 m (Haven, 1971). This area, classified as Zone 1 by the scheme of Ricketts et al. (1985) is largely bare rock covered by a microalga film, with scattered Zone 2 barnacles and algae occurring in the lower portion. Foraging occurs during high tides, while during low tides L. digitalis remains immobile, attached to the rock surface with glue-like adhesion (Smith, 1992). Lottia digitalis is herbivorous and feeds on micro- scopic blue-green algae and diatoms, which are scraped from the rock surface using a toothed radula (Ricketts et al., 1985).

32 A. Hobday / J. Errp. Mar. Biol. Ecol. 189 11995) 29-45

The study was conducted at Pescadero Point, San Mateo County, California (37” 52’ 30.25” N, 122” 37’ 30.42” W) between 21 April and 16 May, 1993. This area is classified by Ricketts et al. (1985) as exposed outer coast. At this site the limpets inhabited a 5 m high granite peninsula extending 60 m at a right angle to the north-south coastline. The farthest, western end from the shore was exposed to the waves, while the southern side was more protected. Along the southern side of the peninsula was a boulder field, which was 20 m wide close to shore and narrowest at the ocean-facing end of the peninsula. This boulder field considerably reduced the amount and height of ocean spray hitting the shoreward portions of the cliff, and produced a gradient in wave exposure.

3. Methods

3. I. Shell-size variation

In order to evaluate differences in size distribution at different ocean spray exposure levels at Pescadero, I chose three areas, 20 m apart, and classified them as exposed (closest to the ocean), intermediate, and sheltered (closest to shore). To test the pre- diction that limpet body size increased with tidal height, three vertical transects were randomly chosen, covering the entire vertical range of L. digitalis within each area. These transects, 0.4 m wide, were divided vertically into 0.3-m intervals. I determined approximate tidal heights by measuring the height above mean lower low water (MLLW) for several days at low tide and averaged the result. This level was marked and referred to in all future measurements.

During low tides I removed all limpets greater than 5 mm in length from the rock surface in each transect in each area. Smaller individuals could not be removed with- out breaking the shell and it was difficult to identify such limpets to species. I measured the maximum length with vernier calipers and used least squares regression analysis to determine if a body size (length) increase was associated with tidal height in each transect, and a one-way ANOVA to determine if the mean size differed in each area.

3.2. Maintenance of shell-size patterns: within habitat transplants

In order to test the hypothesis that individual migration could maintain the pattern of increasing size with tidal height, I performed a series of transplant experiments between 24 April and 16 May, 1993 (Fig. 1). Because limpets at low tide usually attach with “glue-like adhesion” (Smith, 1992) I devised a removal procedure to minimize foot damage that prevents reattachment: limpets were sprayed with seawater and after a few minutes they were removed. This wetting may have induced them to relax their adhesion to the rock, and switch to the suction method associated with high tide and foraging (Smith, 1992). I left those limpets not removed on the first attempt, as limpets removed by the second and subsequent attempts were usually damaged (Wolcott, 1973; Hobday, pers. obs.). The transplanted limpets were held in place and sprayed with seawater for 10 min to assist reattachment. I marked all limpets with quick drying paint


. HIGH HIGH . HIGH

EXPOSED INTERMEDIATE SHELTERED

B’ 1 2 HIGH 2 1 HIGH

LOW

EXPOSED

0 LOW

INTERMEDIATE

Fig. 1. Lottia digitalis transplant experiments at Pescadero Point, CA (May 1993). Large dots indicate large limpets, small dots are small limpets. (A) Within habitat transplants are indicated by solid lines, between habitat transplants have dashed lines. (B) Long-term migratory response transplants. Initially, small limpets from low in the intermediate area are place high in the exposed area along with a control group from high in the exposed (Step 1). After 4 days, both groups are replaced high in the exposed area (Step 2). The migratory response was measured one day later.

pens. In all cases transplants were exposed to smooth rock surfaces, where the effect of substratum heterogeneity could be eliminated. Because the amount of splash and sunlight varied from day to day, comparisons of distances moved across different experimental days are not valid.

In the intermediate area, I collected 40 large (18-22 mm) and 50 small (7- 11 mm) limpets from between heights of + 3.5 to + 4.0 m (high) and + 2.0 to + 2.5 m (low) above MLLW, respectively. The large limpets were divided at random into two equal sets. One set (control) was replaced at + 4.0 m, the normal tidal height for this size class, and the other group (experimental) was placed low ( + 2.0 m). Similarly, limpets were divided into two groups which I placed at + 4.0 m (experimental group) and + 2.0 m (control group). On the following day, I recorded the vertical distance moved

by each limpet, ignoring lateral movements because they were small compared to the

34 A. Hobduy / .I. Exp. Mar. Biol. Ecol. 189 11995) 29-45

vertical, and have no bearing on the vertical size gradient (sensu Frank, 1965). I measured vertical migration after only 1 day to minimize the loss of limpets, and because preliminary observations showed that over a 5-day interval, more than half the vertical movement occurred during the first day.

Similarly, in the exposed and sheltered areas I vertically displaced groups of small (25 per treatment) and large limpets (10 per treatment) with appropriate controls (Fig. 1A). The hypotheses that small limpets migrate downwards and large limpets upwards using two-sample t-tests was evaluated.

3.3. Fixed migratory responses: between habitat transplants

Because it was predicted that limpets inhabiting areas with different spray-exposure levels would move different distances, and preliminary experiments supported this hypothesis, I also transplanted limpets between different exposure areas to determine if the magnitude of such migratory behavior was maintained, or changed in response to the new conditions (Fig. 1A).

Fifty small limpets were collected from low in the intermediate area (+ 2 m) and divided randomly into two equal groups. One was placed high in the intermediate area ( + 3.8 m, control group) and the other at high in the exposed area ( + 3.8 m, experimental group). Similarly, 25 small limpets from low in the exposed area were placed high in the exposed area ( + 3.8 m, control group) and 25 high in the intermediate area (+ 3.8 m, experimental group). One day later, I recorded the vertical distance each limpet had moved. No transplants involving small limpets were made to the sheltered area as this size class was not common there. The hypothesis that small limpets migrated the same distance regardless of the level of exposure to ocean spray was evaluated, i.e. which area they were transplanted to, using two-sample t-tests.

3.4. Longer term migratory response

In order to determine the effect of acclimation on limpet migratory behavior, I transplanted 50 small limpets from intermediate low (+ 2 m) to exposed high ( + 3.8 m, experimental group). A group of 25 small limpets were removed and replaced from exposed high to compare the initial migratory response (control group). After measuring the initial response of all limpets 1 day later, I allowed the transplanted limpets to remain in the exposed area for 4 days. Then all marked limpets within the exposed area were removed and replaced at their initial transplant height (+ 3.8 m in exposed area) (Fig. 1B). I also placed 25 previously unmanipulated limpets from high in the exposed area ( + 3.8 m) at the exposed high starting height, both to compare the response with the acclimated group and to control for multiple removal effects (Fig. 1B). One day later I again measured the vertical migration of each group and evaluated the hypothesis that the response of acclimated limpets was not different from controls using two-sample t-tests.

A. Hobday / J. Exp. Mar. Biol. Ecol. 189 (1995) 29-45 35

4. Results

4. I. Size patterns

At Pescadero Point, the maximum height of the limpet zone was + 4.7 m above MLLW in the exposed and intermediate areas, and + 2.6 m in the sheltered area. Limpet size increased significantly with tidal height in both the exposed area (ANOVA, Transect 1; F,,,= 15.388, pt0.006, Transect 2; F,,,= 12.544, p<O.O09 and

Transect 3; F,,, = 7.076, ~~0.038) (Fig. 2) and in the intermediate area (Transect 1; F,,, = 107.604, p-c 0.0001, Transect 2; F,,, = 40.140, p<O.OOOl and Transect 3; F,,, = 111.122 p-c 0.000 1) (Fig. 3). While there was a slight body-size increase with tidal height in the sheltered area, it was not significant in any transect (Transect 1; F,,, = 2.983,

0 1.7 z.0 2.3 2.6 z.9 3.2 3.5 3.8 4.1 4.4 4.7

TIDAL HEIGHT (m)

Fig. 2. Exposed area transects. Linear regressions of maximum limpet length vs tidal height for L. digitalis at Pescadero Point, CA. (A) Transect 1, y=5.4550+ 1.1877x, R*=0.155, piO.0001. (B) Transect 2, y= 6.5934 +0.96497x, R* = 0.109, p<O.OOOl. (C)Transect 3, y= 6.5448 +0.69883x, R*=0.041, p<O.O002.

A. Hobduy 1 J. E.xp. Mar. Biol. Ecol. 189 (1995) 29-45

24 C. TRANSECT 3

04 1.7 2.0 2.3 2.6 2.9 3.2 3.5 3.8 4.1 4.4 4.7 5.0

TIDAL HEIGHT (m)

Fig. 3. Intermediate area transects. Linear regressions ofmaximum limpet length vs tidal height for L. di@alis at Pescadero Point, CA. (A) Transect 1, ~‘=4.9471 + 1.6620x, R’=O.277, p<O.OOOl. (B.) Transect 2. y= - 0.69634 + 3.5457x,R’= 0.622,pcO.OOOl. (C)Transect 3, y= 1.2520 +3.0777x, R2= 0.526, p<O.OOOl.

p< 0.226, Transect 2; F,,, = 0.915, ~~0.440 and Transect 3; F,,,=0.179 p<O.69) (Fig. 4).

The mean limpet size differed significantly between the three sites when the means of the three transects in each area were compared (F2,6 = 8.769, p<O.O2). In the sheltered area the grand mean was 11.46 mm, while in the intermediate and exposed sites it was 9.96 and 9.22 mm, respectively. Only the sheltered area mean size was significantly different from the other areas (a-posteri Tukey comparison, ~~0.05 in both cases) (Fig. 5).

4.2. Maintenance of gradient patterns

In all limpets placed high, experimental and control, small and large, there was a downward migration for all treatments (Fig. 6). This is probably an effect of remov-


24 A. TRANSECT 1 :

20

16

12

8

4

0 0.5 0.8 1.1 1.4 1.7 2.0 2.3 2.6

TIDAL HEIGHT (m)

Fig. 4. Sheltered area transects. Linear regressions of maximum limpet length vs tidal height for L. digitalis at Pescadero Point, CA. (A) Transect 1, y= 9.9673 +2.0008x, RZ = 0.0.028, ~~0.1351. (B) Transect 2, I’= 9.7163 + 1.0202x, R2 = 0.008, ~~0.3505. (C)Transect 3, y= 9.9548 +0.44805x, R*=0.004, ~~0.4524.

ing a limpet from a well chosen roosting site on the rock. Following removal, limpets must move lower to reduce desiccation. In past experiments (Frank, 1965; Haven, 1971) control animals have not been removed from the rock when marked, and so the downward movement of displaced animals may have been overemphasized. The controls in the present study permitted the effect of vertical displacement to be separated from removal and replacement effects.

In the exposed area experiments small limpets transplanted to non-native heights did not move significantly up or down compared to control groups left at their native heights. (Fig. 6A).

In the intermediate area, large limpets transplanted low migrated significantly greater distances upward than did the control group (small limpets left low) (t3,, = 2.317, p < 0.05). Small limpets displaced upward moved significantly greater distances down-

A. H&day I J. Ewp. Mar. Biol. Ecol. 189 (IYYS) 29-45

LJ” 1 A. EXPOSED (n=1072)

250

? : B. INTERMEDIATE (~878)

E zoo-

z

250 C. SHELTERED (n=332)

0 -8 I

4.5 6.5 8.5 10.5 12.5 14.5 16.5 18.5 20.5 22.5

LIMPET LENGTH (mm)

Fig. 5. Shell length distributions for L. digitalis in the three areas, (A) exposed, (B) intermediate and (C) sheltered areas at Pescadero Point, CA. Transects have been pooled in each area.

wards compared to the control group (large limpets left high) (ts7 = 4.493, p< 0.001) (Fig. 6B).

In the sheltered area, large limpets transplanted downwards did not move significantly upwards compared to the control group. Large limpets displaced upwards did migrate downwards, but not significantly more than the control group (Fig. 6C).

4.3. Fixed migratory response

When small limpets were transplanted from low in the intermediate area to high in the exposed and intermediate areas, the distance moved downwards at the two exposure levels was not significantly different (Fig. 7). Limpets transplanted from low in the exposed area to high in the exposed and intermediate areas showed downward movements which were also not significantly different (Fig. 7). Overall, small limpets transplanted upward from low in the intermediate area to high levels at either exposure


:; A. EXPOSED (SMALL)

30

20 24

3 -5o ;;

FROM LOW FROM HIGH

F :: B.lNl’ERMEDlATE

g 30 -T-

9 LARGE LIMPETS SMALL LIMPETS k 40

30 20 10 0

-10 20 -30 -40

9 6 -50

FROM LOW FROM HIGH

Fig. 6. Mean upward and downward movements of marked L. digitalis over 1 day. The number of recaptured individuals is shown. Vertical bars represent 1 SE. Black bars indicate limpets placed high and hatched bars are limpets placed low. (A) Within exposed area. Small limpets are removed from high and low and placed high and low. (B) Within intermediate area. Large limpets removed from high are placed low and high. Small limpets from low are placed low and high. (C) Within sheltered area. Large limpets from high and low are placed high and low.

moved downwards significantly farther than small limpets upwardly transplanted from the exposed area (the = 3.766, p<O.OOOl).

4.4. Length offixed migratory behavior

Initially, small limpets from low in the intermediate area moved down an average of 32.6 cm when placed high in the exposed area. This was significantly different from the control group from high in the exposed area (t,,= 3.279, pt0.002). After the 4-day acclimation period, the vertical migration of the intermediate low group was not significantly different from either the old control group from exposed high habitats or a

40 A. Hobday ! J. Exp. Mm. Biol. Ecol. I89 11995) 29-45

FROM INTERMEDIATE H FROM EXPOSED

-60

TO INTERMEDIATE TO EXPOSED

Fig. 7. Mean downward movement of small, marked limpets transplanted between the intermediate and exposed areas. Limpets wcrc removed from low in each exposure area, and placed high in the exposed and intermediate areas in each case. The number of recaptured individuals is listed for each mean. Vertical bars rCpreSent 1 SE.

new group from the same location (Fig. 8). The two control groups from high in the exposed area did not differ in migratory behavior indicating that repeated removal did not lead to different migratory responses.

5. Discussion

5.1. Body-size patterns

In this study, it was demonstrated that the body size gradient observed in the limpet L. digitalis is correlated with exposure to wave splash and tidal height. Previous studies of size-variation in intertidal gastropods have not demonstrated the effects of

E O 9 g -10 E

8 5 -20

s

‘d

g -30 28 16

2

W INTERMEDIATE TO EXPOSED

-40 c PRE-ACCLIMATION POST-ACCLIMATION

Fig. 8. Pre-acclimation shows average downward movement of small marked limpets transferred from intermediate low heights to exposed high heights. The group of limpets moved from exposed high to exposed high are controls. Post-acclimation (4 days later) all initially transplanted limpets were again placed high in the exposed area, and mean downward movement after another day is shown. The number of recaptured individuals is listed for each mean. Vertical bars represent 1 SE.


habitat gradients, which I show have an important effect on the strength of observed patterns. At Pescadero Point there is a significant increase in L. digitalis body size with increasing tidal height in the intermediate area (Fig. 3), a lesser but still significant

increase in the exposed area (Fig. 2), and little or no body size increase in the sheltered area (Fig. 4). While this study involves only a single study site, it appears repre- sentative of much of the central California coast, and similar variation in body size gradients with changing exposure at other California sites have been observed (pers. obs., L. Basch, pers. comm.).

In contrast to the pattern found in this study, Wootton (1993) reported that the L. digitalis found higher were smaller than those occurring lower, but he considered only two sample areas, separated vertically by 1 m. The lower of these was in the barnacle zone of the rocky intertidal at Tatoosh Island, Washington, which was not comparable to the pattern found at higher levels in the intertidal zone in this study.

In the exposed area, where high levels of ocean spray may reduce the desiccation risk, small limpets occur throughout the vertical range of the species. Large limpets are less common, and never reach the sizes found in other areas. The intermediate area, with the most significant relationship between body size and tidal height, has many small limpets at low levels and fewer at high levels, whereas large limpets are found mainly at high levels. In the sheltered area, large limpets are found throughout the reduced vertical range and there was no significant correlation between body size and tidal height. The lack of small limpets in the sheltered area may be due to reduced recruit- ment and/or juvenile survivorship; this area may be populated only by laterally immi- grating large limpets. The pattern of an increase in average limpet length with decreasing exposure could also be the result of ontogenetic migration across the exposure gradient.

Sutherland (1970) found a body size increase with tidal height in Macclintockia

scabra, which settles throughout the limpet range. He attributed larger size at high levels to differential growth rates. Body size gradients may also be due to density-dependent growth rates, with faster growth occurring in the sparse densities of upper tidal heights (Vermeij, 1972; Creese, 1980). Breen (1972) in turn, found that vertically migrating limpets had faster growth. If density dependent growth occurs in L. digitalis, it could account for or reinforce the body size pattern produced by migratory behavior, as discussed below.

I documented an increase in total limpet numbers with greater wave exposure in my transects, attributable to both the larger vertical habitat range, and higher population densities (Fig. 5). High densities of small limpets can be also be attributed to settlement patterns or longer submersion times which could lower mortality due to desiccation (Sutherland, 1970; Haven, 1971). With more wave splash, settlement may occur at higher tidal levels, resulting in more small limpets at high levels, as observed in the exposed area.

5.2. Migratory behavior

Migration in the exposed area. There is more wave splash in the exposed area, resulting in less desiccation risk, which appears to allow survival of small limpets at all heights

42 A. Hobday / J. Exp. Mar. Biol. Ecol. 189 (1995) 29-45

within the range. Small limpets displaced high, or moving high at random, may face no pressure to move lower, as desiccation is not a threat in this area. Downwardly displaced small limpets also display no trend in migratory behavior (Fig. 6A). The tendency of limpets to move higher in the exposed area as they grow would result in the observed trend of increasing body size with tidal height. Fewer large limpets are found in the exposed area (Fig. 5A), which may be due to slower growth, emigration to less densely populated areas, size specific predation, selection against large limpets due to feeding disadvantages (Marshall & Keough, 1994) or other factors. Longer term studies are required to explain the smaller population size structure found in this area.

Migration in the intermediute urea. The maintenance of the body size pattern seen in the intermediate area (Fig. 3) can occur by the observed upward migration of large limpets and downward migration of small limpets (Fig. 6B). With intermediate spray exposure, large limpets can survive at higher levels than small limpets, which may migrate downward in order to escape desiccation and death. Frank (1965) noted that downwardly displaced L. digitalis individuals migrated upward in an exposed area, but made no mention of size, and did not demonstrate the converse pattern.

Migration in the sheltered area. Large limpets did not move higher when downwardly displaced (Fig. 6C) perhaps because desiccation is a threat at all heights in the sheltered area. The lower part of the sheltered area is similar in terms of spray exposure to high tidal levels in the other areas. Thus, large limpets fail to vertically migrate both at sheltered low heights and high regions of the intermediate area.

To explain both the increase in body size with tidal height and upward movement of large limpets, several hypotheses have been proposed. First, intraspecific lower height limits based on size could be explained by differential predation pressures. In support of this hypothesis, Wolcott (1973) Sorenson & Lindberg (1991) and Hahn & Denny (1989) have shown that oystercatcher predation has significant effects on limpet populations. Wootton (1993) found that on vertical walls like those in this study, L. digi-

talis was free from bird predation. 1 did not observe any cases of predation by birds, crabs or starfish at high or low tide during 12 h of observation during my study. Thus, L. digitalis is probably not subject to strong size-selective predation pressure in this area.

A second hypothesis to explain upward movement of large gastropods involves mating assortment. Edwards (1969) cites mating advantages as one reason that large snails move higher in the intertidal, away from smaller immature individuals. The neighbors are more likely to be sexually mature than if a random distribution occurred. Levitan et al. (1992) showed aggregation of mature subtidal echinoids enhanced external fertilization. With the increased intertidal flow regime, aggregation of mature limpets may be even more important.

An alternative explanation for large limpet upward migration comes from an observation by Stimson (1970) that small limpets, with smaller radulae, are more efficient grazers and can remove the algae closer to the rock. Thus, large limpets are not as effective as grazers, and would be outcompeted if they did not move to higher levels where small limpets cannot survive. Recently, Marshall & Keough (1994) found that

A. Hobduy / J. Exp. Mar. Biol. Ecol. 189 (1995) 29-45 43

small limpets, with smaller radulae, do have superior competitive ability in food gath- ering over larger conspecifics.

Little (1989) suggested that upward migration may allow optimal feeding by large limpets. Small limpets, restricted by desiccation to lower levels, may have to feed at non-optimal times in order to survive at high limpet densities. Large limpets, by migrating upwards can escape the high population densities found at lower levels, better avoid desiccation, avoid competition with superior foragers and still feed at optimum times during high tides.

Finally, the movement of large limpets to high levels could be a response to inter- ference and to space limitation caused by other Zone 1 species, especially the barnacles B&anus glundulu and Chthamalus dalli (Choat, 1977; Creese, 1982; Wootton, 1993). These barnacles are common at the low region of the limpet range, and would restrict the movement, feeding and attachment to the rock of large limpets.

5.3. Short-term and long-term migratory behavior

In the short term, limpets transplanted from one area to another responded as if they were subject to the physical conditions of their native area. To avoid desiccation in the intermediate area, a lower resting height may be required than in the exposed area. In the exposed area, where small limpets are found at higher levels, there is probably less pressure for downward migration.

After an acclimation period of only 4 days in the exposed area, the behavior of limpets transplanted from the intermediate area was indistinguishable from the residents (Fig. 8). The initial behavioral response can thus change to fit new local conditions. The short-term fixed response would prevent an inappropriate response to a short, uncom- mon event, such as a single dry day, while the plasticity would allow adjustment in response to real changes in the physical conditions such as seasonal effects and lunar spring/neap tidal cycles.

Thus, the limpets demonstrated short-fixed and long-flexible behavioral responses to changing exposure conditions, and this behavior is sufficient to explain the observed distribution.

Acknowledgements

This research was completed in partial fulfillment of the Undergraduate Honors Program in Biology at Stanford University. It is a pleasure to thank Dr. J. Hall Cushman for stimulating discussion and manuscript review. Drs. L. Basch, L. Levin, P. Franks, M. Ohman, R. Rowley, J. Roughgarden and two anonymous reviewers provided comments on drafts of the manuscript. Field and transportation assistance was provided by N. Young. Thanks to the brave K. Watson and A. Musch who risked life and limb in an earlier project attempt.

44 A. Hobday / J. Exp. Mar. Biol. Ecol. 189 (IWSJ 29-45

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