L
Journal of Experimental Marine Biology and Ecology, 240 (1999) 259–283
Physical and biological processes influencing zonation
patterns of a subtidal population of the marine snail,
Astraea (Lithopoma) undosa Wood 1828
*
Andrea C. Alfaro , Robert C. Carpenter
Department of Biology, California State University, Northridge, CA 91330, USA Received 20 April 1998; received in revised form 23 April 1999; accepted 1 May 1999
Abstract
The population density and size distribution of the marine gastropod, Astraea (Lithopoma) undosa Wood 1828, at Bird Rock, Santa Catalina Island, CA, reveal an inverse relationship between population density and mean individual size, over a depth gradient. This trend may be correlated with physical and biological differences between habitats for parameters such as water motion, competitive interactions, and predation.
The potential effect of hydrodynamic forces on the zonation patterns of Astraea undosa was tested in laboratory and field experiments. Based on theoretical predictions of the relationship between shear force and water velocity on different-sized snails, large snails are subjected to greater shear forces, as a result of water motion, than medium or small snails. Results of dislodgment experiments conducted in the laboratory indicated that for a given force per unit area, all snails dislodged at nearly the same frequency, with 50% of snails predicted to dislodge at about 4 m / s, and 100% of snails predicted to dislodge at about 8 m / s velocity. These results suggest that hydrodynamic forces may be an important factor in the shallowest subtidal zones.
A factorial-designed caging experiment was used to test the effects of snail population density on growth rates of snails of three different size classes. For small and medium size classes, results indicated an inverse relationship between population density and growth rates, which was especially pronounced for smaller snails. These data, in conjunction with long-term patterns of population density and size distribution in the field, suggest that intraspecific competition also plays a role in determining size-specific zonation patterns.
Tethering experiments, used to estimate predation rates in different algal-cover zones, suggest that there are no differences in survival rates among different snail size classes; however, survival rates differ among zones and may contribute further to the observed zonation patterns. Overall, data indicate that a combination of physical and biological processes controls the population
*Corresponding author. Present address: School of Environmental and Marine Sciences, The University of Auckland, Auckland, New Zealand. Tel.: 164-9-373-7599, ext. 7418; fax:164-9-373-7435.
E-mail address: [email protected] (A.C. Alfaro)
density and size-distribution of Astraea undosa over a depth gradient at Santa Catalina Island, California. 1999 Elsevier Science B.V. All rights reserved.
Keywords: Zonation; Subtidal; Gastropod; Hydrodynamics; Competition; Predation
1. Introduction
Patterns of distribution and abundance of marine organisms often exhibit distinct zonation. Factors that influence zonation patterns have been examined in a variety of intertidal gastropod populations (Frank, 1965; Chow, 1975; Underwood, 1975; Bertness, 1977; Chapman, 1995; Navarrete, 1996). Furthermore, generalizations from such studies have yielded descriptive and predictive models that characterize the relative importance of various factors affecting the zonation patterns of a species (MacArthur, 1960; Preston, 1962; Connell, 1972; Vermeij, 1972; Menge and Sutherland, 1976; Paine and Levin, 1981; Underwood and Denley, 1984; Navarrete and Menge, 1996). For example, Vermeij (1972) suggested that for upper-intertidal species, shell size increases in an upshore direction, whereas for lower-intertidal species, shell size decreases in an upshore direction. Differential growth rates and active migrations are two mechanisms proposed to explain size gradients within a population (Bertness, 1977). Extensive work in the intertidal suggests that physical factors strongly affect populations in the high intertidal, whereas biological factors are more important in the lower intertidal (Paine, 1969; Connell, 1972; Menge, 1992). However, few studies have investigated subtidal patterns of zonation (but see Witman, 1987). The majority of subtidal zonation studies have been conducted in the tropics, and specifically address coral reef zonation patterns (Wellin-gton, 1982; Graus and Macintyre, 1989). Theoretical models that incorporate the effects of physical and biological factors on zonation in subtidal systems remain to be developed.
Patterns of zonation may be determined by physical factors such as water motion and seasonality, and / or biological factors such as intra- and interspecific competition, predation, and recruitment. These factors also may influence the population density and size distribution of an organism throughout its range. Usually, no one factor alone can explain the population density and distribution patterns of a species (Connell, 1983; Quinn and Dunham, 1983; Underwood and Petraitis, 1993; Navarrete, 1996). In the population of Astraea (Lithopoma) undosa Wood 1828 at Bird Rock, Santa Catalina Island, population density and individual size are inversely related along a depth gradient. Large snails (|60 mm basal diameter) are found at low population densities in shallow and deep areas, and medium-sized snails (|40 mm basal diameter) are encountered in high population densities at intermediate depths. Similar zonation patterns of Astraea undosa in intermediate and deep areas have been observed by Myers (1986) at Bird Rock, Santa Catalina Island, and by Schwalm (1973) at Point Loma, San Diego, California.
effects of flow-induced hydrodynamic forces, intraspecific competition, and predation on the size-specific zonation patterns of Astraea undosa at Bird Rock, Santa Catalina Island, California.
2. Materials and methods
2.1. Organism and study site
Astraea undosa is one of the largest prosobranch gastropods found along the coast of
California (Glass and Foster, 1984), having a basal diameter between 5 and 150 mm (Johnson and Snook, 1967). A strictly herbivorous gastropod, Astraea undosa prefers fleshy algae such as Cystoseira, Halidrys, Sargassum, Zonaria, and Dictyota, but will also feed on less nutritious calcareous algae such as Corallina, Lithothrix, and Bossiella (Halliday, 1991). Very little is known about recruitment and settlement patterns of this snail species. Schwalm (1973) suggested that recruitment takes place in January– February, but recruitment differences among subtidal zones have not been observed. Furthermore, the ability of Astraea undosa to migrate, together with the presence of new recruits (,20 mm in basal diameter) throughout all zones at Catalina Island (Myers, 1986), indicate that any settlement patterns among different areas may not persist. Four potential predators have been identified at Catalina Island; the octopus Octopus
bimaculatus, the seastar Pisaster giganteus, the lobster Panulirus interruptus, and the
whelk Kelletia kelletii (Schmitt, 1982; Ambrose, 1986).
The study site is located on the north side of Bird Rock, about 1 km from the Wrigley Marine Science Center at Santa Catalina Island, California (338279N Lat.: 1188299W Long.) (Fig. 1). The slope of the substratum is gradual across an offshore distance of about 30 m and is composed of rocky outcrops, cobbles, and sand to about 18 m depth, where the slope abruptly increases, ending on a sandy bottom at a depth of about 21 m. Four zones within the gradual slope area (1 to 18 m depth) were identified according to differences in algal cover (Fig. 2).
The shallowest Eisenia zone ranges between 2 and 3 m in water depth and extends horizontally about 5 m from the shore. This zone usually is composed of a dense canopy of Eisenia arborea (southern sea palm) or Halidrys doica, with an understorey of
Gelidium spp., Pterocladia capillacea, and upright and crustose coralline algae (47%
fleshy algae, 33% calcareous algae, and 20% bare space; Carpenter, unpublished data). The Lithothrix zone is situated between 3 and 4 m in water depth and covers a horizontal distance of 4 m. This zone includes primarily upright corallines such as Lithothrix,
Corallina, and Bossiella, as well as algal turfs (almost 100% calcareous algae;
Fig. 1. Location of study site (arrow) near the Wrigley Marine Science Center (WMSC) on Santa Catalina Island, California.
kelp, Macrocystis pyrifera and an understorey consisting of Dictyota spp. and Zonaria
farlowii (60% fleshy algae, 39% calcareous algae, and 1% bare space; Carpenter,
unpublished data). The algal species composition at the study site comprises four distinct zones that persist year-round, although the algal abundance is higher during spring and summer months.
2.2. Population densities and sizes of Astraea undosa
The population density and size-distribution of Astraea undosa were monitored in monthly SCUBA surveys by placing two 30-m transect lines in each of the four zones.
2
Snails within 20 randomly placed 0.25 m quadrats along the transect lines were enumerated, and their greatest basal diameters were measured (to the nearest mm) with vernier calipers. For the Macrocystis zone, snail densities were usually so low that counts and measurements were made for all snails encountered along the transect. These surveys were conducted between October 1992 and August 1994 for a total of 14 months of data (weather conditions prevented data collection for some months). Snail recruitment was estimated by separating for statistical analysis all juvenile snails (,20 mm in basal diameter). Recruitment patterns were compared among all zones, except the
Fig. 2. (A) Mean population density (6S.E.) and mean size distribution (6S.E.) for four zones at Bird Rock, Catalina Island, CA. Diagrammatic representation of study site illustrating the dominant algal cover and location of different snail densities and sizes. (B) Population density (6S.E.) and maximum basal diameter (6S.E.) of snails at the study site for 14 months between October 1992 and August 1994.
2.3. Experiments on hydrodynamic forces
performed in the laboratory to estimate the forces required to dislodge snails of different sizes. Finally, field measurements of flow speeds at the study site, in addition to calculated theoretical flow speeds, were used to estimate the importance of hydro-dynamic forces in controlling zonation.
The relationship between shear force and water velocity was calculated using Morison’s equation (Denny, 1988). A representative natural range of velocities (0.01–
2
4.9 m / s) and accelerations (0–60 m / s ) were used for three different snail size classes (10–30, 31–50, and 51–70 mm basal diameter). In using this equation, the assumption was made that velocity and acceleration were acting in the same direction (Trussell, 1997). The areas projected perpendicular to the flow and volumes of 18 snails within the three size classes were estimated by image analysis of snail photographs and calculations for a cone, and the means for each of the three size classes were used in Eq. (1) (from Denny, 1988)
the projected area of snail (m ); Cd is the drag coefficient for a snail (unitless): small50.467; medium50.544; large50.544; Cm is the inertia coefficient for a snail
3
(unitless)51.72 (Denny, 1988); V is the volume of snail (m ) and a is the acceleration
2
(m / s ).
Drag forces of different-sized snail shells were estimated at different wind speeds in a wind tunnel (Hopkins Marine Laboratory), and drag coefficients were calculated. Five to eight shells were used for each of the three snail size classes. These estimates were then converted to drag forces in water. Specifically, drag coefficients were calculated from Eq. (2) and substituted into Eq. (1) (from Denny, 1988)
2
required number of snails to achieve true independence was prohibitive (|3000 snails). The random order of forces minimized the chances of a predictable effect of fatigue on dislodgment. The relationship between the probability of dislodgment and flow speed was generated by translating forces into the corresponding speeds from the shear force versus water velocity relationship (Eq. (1)).
Limited sampling of flow speeds at the study site were made with an InterOcean S4 electromagnetic current meter placed 0.5 m above the substratum. Measurements were made at least twice in each of the four zones over 2 days in April, 1994. For each sampling, the current meters were deployed for 20 min and were programmed to take one measurement per min. Theoretical water velocities for a set of wave heights (0.5–2 m) and periods (5–15 s) for the corresponding water depths (2, 3, 7, and 11 m) in each of the four zones were calculated using linear wave theory for shallow water (Eq. (3)) (from Denny, 1988)
acceleration (9.81 m / s ); d is the water depth (m); x is the distance in x-direction (m); w
21
is the wave frequency5(2p/T ) (s ); t5time (s).
These water velocity estimates provided evidence for the relative flow differences among zones.
2.4. Experiments on intraspecific competition
Enclosure experiments were conducted in seawater tanks at the Wrigley Marine Science Center to evaluate the effect of snail population density on growth rates of snails
2
in three size classes. Cages (0.32 m ) containing combinations of three snail densities (1, 3, and 6 individuals / cage) and three snail sizes (|20, |40, and |60 mm in basal
3
diameter) were arranged randomly inside two 7-m tanks with continuous seawater circulation. All snails used in these experiments were collected from the same area adjacent to the study site. In this factorial design (density and size as fixed factors), cages with three different densities per size class had four replicates for a total of 36 cages. Three additional cages were maintained as controls under the same conditions as the treatment cages, but without the addition of snails. The cages were constructed from plastic egg crate material with 10-mm mesh openings to allow a constant flow of water through the cages. Since the mean natural density of Astraea undosa at the Bird Rock
2
with vernier calipers approximately monthly for 6 months between January and August 1994. Basal diameter has been found to correlate directly to snail biomass, and is therefore a good index for snail growth (Schwalm, 1973). Because each snail was distinctly labeled, individual growth rates could be calculated as:
r5ln (L /L ) /tt o (4)
where Lo is the initial basal diameter, L is the basal diameter after each monthlyt
measurement, with t the days between sampling times (42, 13, 28, 22, 14, and 27 days, respectively, for the 6-month period) (Creese and Underwood, 1982). Only one snail died during the experiment and it was replaced immediately.
Rocks encrusted with typical algal species from the Sargassum zone were collected from the field and placed inside each of the cages. Algae were not replaced throughout the experiment. The amount of algal cover inside each cage was estimated before and after the experiment from photographs using a point-intercept method (Littler and Littler, 1985). Since cage covers were necessary to prevent snails from escaping, the amount of light reaching the bottom of the cages was reduced. The amount of light inside cages was recorded with a Li-Cor 1000 light meter with a 2p sensor. Fifty instantaneous light measurements were made inside the cages and compared to 30 instantaneous measurements made the same day at the study site at a depth of 7 m.
The same experimental cage set-up was attempted in the field at the study site, but was not taken to completion owing to a high level of snail escapes and mortality from octopuses which were able to intrude the cages. Nevertheless, growth rates of snails from unaffected field cages were compared to those from the lab cages.
2.5. Predation experiments
To estimate the effect of predation on the zonation pattern of Astraea undosa, survival rates of snails within the four zones (Eisenia, Lithothrix, Sargassum, and Macrocystis) were measured in the field using tethering experiments (Watanabe, 1984; Ambrose and Irlandi, 1992; Ruiz et al., 1993). While tethering may introduce artifacts to the experimental treatment, they provide a quantitative estimate of predation, particularly when the results are interpreted in light of predator behavior and ecological dynamics (Peterson and Black, 1994). In this study, the mechanism of tethering was designed to minimize the possibility of artifacts within the constraints of the natural environment. Extensive previous research on the predator dynamics at the study site (Engle, 1979; Schmitt, 1981, 1982; Ambrose, 1982, 1984, 1986) allowed for more accurate interpreta-tion of the patterns observed in this study.
retrieval. After 3 months, the nails were relocated and the number of live snails, empty shells, shell remains, and cut tethers was recorded. Non-parametric statistics (Friedman’s test) were used for comparisons of size-specific predation among zones.
Predator presence and abundances were noted qualitatively during the monthly surveys. The number of shell remains that were complete enough to constitute a single individual and clean enough to represent recent mortality also were recorded when found within the quadrats during the monthly population density surveys.
3. Results
3.1. Population densities and sizes
The population density of Astraea undosa varied greatly among the four zones within the study site. Low population densities were found at the shallowest and deepest depths (Eisenia and Macrocystis zones, respectively). Over the 14-month survey period, the
2
snail density in the Eisenia zone ranged from 0.25 to 3.08 individuals / 0.25 m , and had
2
a mean density (6S.E.) of 1.1160.25 individuals / 0.25 m (Fig. 2). Densities in the
2
Macrocystis zone ranged from 0.10 to 0.80 individuals / 0.25 m , with a mean density
2
(6S.E.) of 0.3360.40 individuals / 0.25 m . Although population densities were esti-mated only in 3 out of 14 months for the Macrocystis zone, qualitative observations during 4 additional months corroborated the low densities in this zone. Higher population densities were found at intermediate water depths (Lithothrix and
Sargas-2
sum). In the Lithothrix zone, densities ranged from 3.60 to 8.50 individuals / 0.25 m ,
2
with a mean density (6S.E.) of 6.1460.40 individuals / 0.25 m . The Sargassum zone
2
had densities that ranged from 2.15 to 5.25 individuals / 0.25 m , with a mean density
2
(6S.E.) of 3.1560.24 individuals / 0.25 m . Comparisons of the log-transformed data among the four zones (zone as a fixed factor) revealed a significant difference among the mean densities of the snails in these zones (ANOVA; F( 3,1502 )5208.37, P,0.001).
Over a period of 14 months, there was an inverse relationship between population density and mean snail size (Pearson correlation; r5 20.46; n54; P,0.05). Large snails were found in the Eisenia zone (19–80 mm size range, 41.3062.51 mm mean basal diameter) and Macrocystis zone (23–102 mm size range, 55.2662.84 mm mean basal diameter), and smaller snails were found in the Lithothrix zone (11–92 mm size range, 38.7260.49 mm mean basal diameter) and Sargassum zone (14–81 mm size range, 35.0260.57 mm mean basal diameter) (Fig. 2). A one-way ANOVA of mean snail sizes for the four zones was statistically significant (ANOVA; F( 3,3472 )5192.86,
Fig. 3. Total number of new recruits within three zones for 14 months between October 1992 and August 1994. New recruits were observed in the Macrocystis zone but were not recorded.
3.2. Experiments on hydrodynamic forces
When the relationship between shear force and water velocity is applied to the results of the dislodgment experiments, the prediction is that all snails of all sizes dislodge at about the same flow speed. Specifically, the relationship predicts that 50% of snails dislodge at about 4 m / s, and 100% at about 8 m / s (Fig. 4). Thus, while the mean forces (6S.E.) required to dislodge snails were 0.4060.06 N (small snails), 1.2460.16 N (medium snails), and 4.4060.54 N (large snails), these differences disappeared when the forces were translated into the equivalent flow speeds. The basis for this rationale is that the drag forces depend on shell area projected perpendicular to the flow, which are greater for larger snails.
The limited field measurements of flow speed indicated that higher flow speeds are found in shallow water, as expected. Maximum recorded flow speeds were 3.48 m / s for the Eisenia zone, 0.84 m / s for the Lithothrix zone, 0.36 m / s for the Sargassum zone, and 0.11 m / s for the Macrocystis zone (Table 1). Flow speeds among the Eisenia,
Lithothrix, Sargassum, and Macrocystis zones were significantly different when
Fig. 4. Predicted probability of dislodgment over a range of flow speeds for three size classes of Astraea
undosa.
Table 1
a Field measurements and theoretical calculations of hydrodynamic forces (A) Field measurements
Zone Highest mean Maximum flow
(6S.E.) (m / s) speed (m / s)
Eisenia 0.35 (0.01) 3.48
Lithothrix 0.18 (0.00) 0.84
Sargassum 0.10 (0.00) 0.36
Macrocystis 0.03 (0.00) 0.11
(B) Linear wave theory calculations
Water depth For: H50.5 m For: H52.0 m
T55 s T515 s
2 0.54 m / s 2.21 m / s
3 0.44 m / s 1.81 m / s
7 0.25 m / s 1.18 m / s
11 0.17 m / s 0.94 m / s
a
3.3. Experiments on intraspecific competition
The results of the caging experiments indicate that snail growth rates are higher at lower densities and that growth rates are higher for smaller size classes of snails (Fig. 5). For all densities, the small size class had the highest growth rates, with the highest mean
23
growth (6S.E.) of 4.4360.16 / day310 at the lowest density (one individual / cage)
Fig. 6. Mean growth rates (6S.E.) for three size classes at three densities. Means were obtained from data over a 6-month period.
(Fig. 6). For medium snails, the highest growth rates were also observed at the lowest
23
density, with mean growth (6S.E.) of 2.0660.27 / day310 , whereas large snails had equal growth rates at all densities (Fig. 6). Results of a repeated measures ANOVA (size and density as fixed factors, and month as random factor) yielded significant treatments and interactions, suggesting that snail growth rates differ among size classes, densities, and months (Table 2). In this case, growth rates decrease as density increases for small and medium snails, but growth of large snails is not affected by density (Fig. 6).
Light measurements indicated that the mean photon flux density (PFD) in the field
22 21
was 474694mmol photons m s , and inside the lab cages was 163.08676.93mmol
Table 2
Statistical comparisons (repeated measures ANOVA) of snail growth rates with size and density as fixed factors a
and month as random factor
Source df Mean square F-value P
Size 2 551.564 7.126 ,0.05
Density 2 45.157 11.470 ,0.05
Month 5 115.327 89.540 ,0.05
Size3density 4 15.723 4.034 ,0.05
Size3month 10 77.399 60.092 ,0.05
Density3month 10 3.937 3.057 ,0.05
Size3density3month 20 3.898 3.026 ,0.05
Error 666 1.288
a
22 21
photons m s . A three-way ANOVA (size, density, and time as fixed factors) suggests statistically significant changes (P,0.05) in cover of algae and bare rock within all cages between the start and end of the experiment (Table 3). A shift was observed from fleshy to calcareous algae and bare rock after the 6-month experiment (Fig. 7a). No statistical differences were observed in algal cover at the start or at the end of the experiment for all cover types (Table 3: ANOVA; P.0.05) except for percent fleshy algae in cages with different sizes of snails (Table 3: ANOVA; P,0.05). These results indicate that there were no differences in food preferences among snails of different sizes (fleshy algae are preferred over calcareous algae by all snails). The algal cover within control cages (containing no snails) showed a non-significant (one-way ANOVA; P.0.05) increase in calcareous algae and decrease in fleshy algae between the start and end of the experiment (Fig. 7b). These results indicate that changes in algal cover within treatment cages were due to grazing by snails and not caging artifacts.
In the field, 17 of 36 cages maintained their initial snail densities for at least the first
Table 3
Statistical comparisons (three-way ANOVA) of algal cover and bare rock inside snail cages. Size, density, and a
Size3density 4 11.389 0.120 0.975 ns
Size3time 2 210.889 2.225 0.118 ns
Density3time 2 369.847 3.902 0.026
Size3density3time 4 37.556 0.396 0.810 ns
Error 54 94.778
Fleshy algae
Size 2 117.764 4.131 0.021
Density 2 14.264 0.500 0.609 ns
Time 1 48 101.681 1687.504 0.000
Size3density 4 30.764 1.079 0.376 ns
Size3time 2 149.347 5.239 0.008
Density3time 2 10.931 0.383 0.683 ns
Size3density3time 4 39.347 1.380 0.253 ns
Error 54 28.505
Bare rock
Size 2 194.014 1.977 0.148 ns
Density 2 136.764 1.394 0.257 ns
Time 1 27 534.222 280.617 0.000
Size3density 4 37.306 0.380 0.822 ns
Size3time 2 683.764 26.969 0.002
Density3time 2 359.431 3.663 0.032
Size3density3time 4 22.972 0.234 0.918 ns
Error 54 98.120
a
Fig. 7. (A) Algal cover inside cages at start and end of competition experiments at three densities for three size classes of snails. (B) Algal cover inside control cages at start and end of competition experiments.
Fig. 8. Mean growth rates (6S.E.) of snails in field caging experiments for three size classes at three densities over a period of 1 month.
cages were unaffected to conduct statistical analyses, the growth rates of surviving snails were similar to the snails in lab cages (Fig. 8).
3.4. Predation experiments
The results of the predation experiments indicate that survival was highest in the
Lithothrix zone, followed by the Macrocystis, Sargassum, and Eisenia zones (Table 4).
Survival differed among zones (Friedman test; r50.89, 3 df, P50.046) but did not differ among size classes (Friedman test; r50.188, 2 df, P50.472). Of the 53% snails that did not survive the predation experiments, 17% were found as empty shells, 1% as broken shell remains, and 35% were completely absent (cut tethers often were found). In the Macrocystis zone, the whelk Kelletia kelletii was observed eating a tethered snail.
Table 4
Percent of missing snails, empty shells, broken shell remains, and snails that survived the predation experiment within four different zones at the study site
Zone Missing Empty Broken shell Survival
(%) shells (%) remains (%) (%)
Eisenia 72 15 0 13
Lithothrix 20 0 0 80
Sargassum 26 40 7 27
Macrocystis 20 13 0 67
Observations during monthly surveys suggest that the whelk and the sea star Pisaster
giganteus were found throughout the study site, but were more common in deeper areas
such as the Macrocystis and Sargassum zones (in accordance with Schmitt, 1982). The octopus Octopus bimaculatus commonly was found in dens surrounded by empty shells (mostly of Astraea undosa) in the Sargassum and Macrocystis zones (in accordance with Ambrose, 1986), and rarely in the Eisenia and Lithothrix zones. The lobster (mostly juveniles), Panulirus interruptus, was found in adjacent seagrass beds and among large boulders about 30 m away, but no lobsters were encountered within the study site.
The mean number (6S.E.) of shell remains found within quadrats in each zone during the monthly surveys were 1.6061.12 for the Eisenia zone, 5.7860.96 for the Lithothrix zones, 26.6363.02 for the Sargassum zone, and 30.2563.97 for the Macrocystis zone. One-way ANOVA tests (zone as factor) indicated significant differences between shell abundances (ANOVA; F( 3,59 )564.76, P50.001). Sizes of the empty shells were difficult to quantify since in some cases the shells were broken at the base. However, the mean sizes (6S.E.) of empty, intact shells were estimated as 48.0063.68, 42.0062.09, 43.4860.87, and 64.4661.26 for the Eisenia, Lithothrix, Sargassum, and Macrocystis zones, respectively. Statistical comparisons indicated significant differences among zones (ANOVA; F( 3,390 )570.34, P50.001), with shell sizes paralleling the patterns in live snail sizes across zones.
4. Discussion
Variation in both the physical and biological environment often leads to distinct zonation in the distribution and abundance of marine organisms. In general, physical factors, such as wave energy and desiccation, have been considered more important in shallower water, whereas biological factors, such as predation and competition, have been considered to be more important in deeper water (Quinn and Dunham, 1983; Menge, 1992). The significance of physical factors in intertidal communities has been studied extensively (Frank, 1965; Sutherland, 1970; Chow, 1975; Underwood, 1975; Bertness, 1977; Wahl, 1997). Examples of biological factors affecting zonation patterns in intertidal and subtidal areas also are well known (Paine, 1969; Lowery, 1974; Watanabe, 1984; Witman, 1987; Navarrete and Menge, 1996). The results of this study suggest that both physical and biological processes affect the distribution of a subtidal snail.
4.1. Effects of hydrodynamic forces
physically by water motion depends both on the ability of an organism to adhere to the substratum, and on the magnitude and / or frequency of wave-generated forces impacting the organism (Trussell et al., 1993). In this study, the ability of a snail to adhere to the substratum was estimated by recording the forces necessary to dislodge the organism. The forces required to dislodge snails may have been overestimated as snails can develop a stronger attachment to smoother surfaces (terra cotta tile used in this study) than to the more rugose natural substrate.
Predictions of the probability of dislodgment of snails at different flow speeds indicate that at flow speeds greater than 8 m / s, all snails would be dislodged, and that at flow speeds of 4 m / s half of the population would be dislodged. Since different-sized snails are not expected to be affected differentially by a given water speed, then tenacity appears to be size-independent for Astraea undosa. Certain behaviors may decrease the effects of hydrodynamic forces on snails, such as finding cover within crevices, aggregating, or taking refuge behind other organisms. Also, fatigue may increase the risk of dislodgment, as may occur within prolonged periods of high water motion. Those snails that were tested in the dislodgment experiments to determine the amount of time necessary for snails to firmly reattach to the substratum verified that less than 5 min between trials resulted in substantially higher dislodgment rates than those snails which were allowed 5 min or more to reattach. Once snails are dislodged and turned upside down (as can often be found in the field), they are not able to turn upright and reattach to the substratum for at least 10 min (A. Alfaro, personal observations). The conclusions made here are based on observations of snails under stationary conditions, which demonstrate higher tenacities than moving snails observed in the field (Denny et al., 1985), again suggesting that the predicted effects of hydrodynamics on Astraea undosa may be underestimated.
Both flow speed measurements (taken on relatively calm summer days), and linear wave theory calculations of flow speeds under normal conditions indicate that even in the shallowest zone, flow speeds are not as high as the speeds predicted to dislodge most snails. However, during stormy weather, large waves and flow speeds as high as 14–16 m / s have been recorded on wave-swept shores (Vogel, 1984, 1994; Denny, 1995). Although 14–16 m / s velocities may be uncommon at the Bird Rock site, occasional storm-generated swells and higher flow speeds during winter could be responsible for keeping the population density of Astraea undosa low in shallow water. In fact, a large number of live snails have been observed washed on shore after strong storms (J. Engle, A. Alfaro, personal observations). Although depth-dependent flow speeds measured with the S4 meter are descriptive of the free-stream flow (0.5 m above substratum), flow profiles made at 2 cm above the benthos at this site are within 80 to 100% of the flow at 0.5 m (Carpenter, unpublished data). These in situ measurements of flow speeds are not necessarily representative of daily flow conditions at the study site, but they do provide a relative comparison of flow conditions among different zones at Bird Rock. Because flow speed decreases with increasing depth, it is unlikely that hydrodynamic forces have much of an effect on the density of Astraea undosa at depths greater than 2–3 m.
4.2. Effects of intraspecific competition
intraspecific competition also may regulate the zonation patterns of Astraea undosa within the study site. Competition between snails was investigated by using growth rates of different size classes of snails at different densities (cf. Underwood, 1978, 1984; Marshall and Keough, 1994; Keough et al., 1997) in the lab, and the trend was corroborated in the field. Snail growth rates were estimated by changes in the basal diameter of the shells, which appears to be a good measurement of growth since these snails were found to follow isometric growth (Alfaro, 1994). Growth rates were higher for smaller snails than for medium snails, and higher for medium snails than for larger snails. Growth rates also were higher at lower snail densities for small and medium size snails, but almost no change in growth rates with density was observed in large snails. The low growth rates observed in large snails may be related to senescence, or a shift in energy allocation from growth to reproduction in older snails. Furthermore, the caging experiments showed that the size distribution pattern did not result in mortality of snails at any competitive level. The general inverse relationships between snail size and growth rates, and between population density and growth rates have been observed in many populations that exhibit intraspecific competition (Creese, 1980; Branch, 1984; Black and Johnson, 1994; Marshall and Keough, 1994; Keough et al., 1997). Since Astraea
undosa has not been found to exhibit territoriality and no interference behavior was
observed, it seems likely that Astraea undosa is affected by exploitative competition for food resources (Underwood, 1978).
Although mean photon flux density (PFD) inside the cages was reduced compared to the field, light reaching the algae inside the cages was within the range of saturation PFDs for species within the depths studied here (Lobban and Harrison, 1994). Furthermore, the algal composition was comparable across treatment cages at any given time throughout the experiment and was unaffected within control cages. While control cages maintained a selection of fleshy algae, snails consumed virtually all fleshy algae within treatment cages. The increase in estimated cover of calcareous algae by the end of the lab cage experiments could be because these species actually increased in abundance, or because these taxa were underestimated at the start of the experiment, when a fleshy algal canopy made it difficult to quantify species in the understorey. However, this underestimation should not affect the conclusions of these experiments.
By the end of the experiment, the resulting abundance of calcareous algae within the treatment cages exhibited a similarity to the algal cover within the Lithothrix zone, where snail population density is the highest at the study site. In fact, the nearly 100% calcareous algal composition of the Lithothrix zone may be the result of intense grazing by Astraea undosa. Halliday (1991) showed that snails maintained on a strictly calcareous diet had significantly lower growth rates than those fed fleshy algae, owing to the higher assimilation efficiency for fleshy algae versus calcareous algae for Astraea
undosa. These findings, combined with field size-specific patterns, suggest that
differential settlement patterns cannot be ruled out as a contributor to zonation patterns of Astraea undosa in this study. The recruitment peak in May 1993 remains un-explained, since the data do not show a peak in May 1994 nor was there a peak in January–February, as reported by Schwalm (1973) (Fig. 3). Furthermore, although competition between size classes was not investigated in this study, the effects of inter-class competition are expected to be greater than the within-class density effects observed in the caging experiment.
4.3. Effects of predation
Results from the predation experiments suggest highest survival rates for Astraea
undosa in the Lithothrix zone, and lowest survival rates in the Eisenia zone. Although
the distribution of empty shells agrees with predation patterns across zones, the lack of long-term replication from the tethering experiments imparts a low degree of confidence in these results. Because the tethering experiments could not differentiate among causes of disappearance of snails — i.e. hydrodynamic forces, natural mortality, successful escape, or predation — low survival rates cannot be attributed with certainty to high predation, but it is a likely cause. Assuming that the probability of a successful escape is negligible (all tethers with missing snails had been cut, presumably by a predator) and equal among all zones, missing snails may be attributed to hydrodynamic forces or predatory octopuses, which often carry snails back to their shelters (Ambrose, 1983). Unbroken empty shells may have resulted from natural mortality or predation by
Kelletia kelletii or Pisaster giganteus, both of which leave an unmarked empty shell
(Ambrose, 1986; Peterson and Black, 1993). At the Catalina Island study site, broken shell remains are known only to be caused by lobster predation.
The introduction of tethering artifacts probably are minimal since the tethers were inconspicuous, and the two predators which cause flight responses in Astraea undosa (Kelletia kelletii and Pisaster giganteus) (Schmitt, 1981) are present throughout the study site, thus making relative comparisons possible (Peterson and Black, 1994). Octopuses and lobsters are fast-moving predators that cause no flight response in
Astraea undosa (Schmitt, 1981) and these predators could easily forage on tethered and
untethered snails. Lobsters were found only within seagrass areas adjacent to the study site, where they feed on a nearby intertidal mussel bed (Engle, 1979; Schmitt, 1982; Ambrose, 1986; Robles, 1997). However, it is possible that lobsters may feed seasonally on Astraea undosa, within the shallowest Eisenia zone (Engle, 1979; Ambrose, 1986). If increased survival of Astraea undosa results from lower predator abundance in a given area, it is likely that the snail population density will be higher in areas with lower predation pressure. Schmitt (1985, 1987) found a negative association between the density of the snails Tegula eiseni and Tegula aureotincta and the abundance of their predators (same predators of Astraea undosa). In this study, the low survival rates of snails in the Sargassum zone are in accord with the high density of empty shells found in this zone and the observed high predator abundance in the Sargassum and
Macrocystis zones (Ambrose, 1982; Schmitt, 1982; Myers, 1986; Halliday, 1991; Alfaro,
slight preference for kelp forests (Macrocystis zone). However, octopuses are less likely to forage in the Eisenia and Lithothrix zones due to the high wave action and low availability of shelters.
High survival of snails in the deep Macrocystis zone does not agree with the high predator abundance in this zone; however, this snail population comprises mostly large snails, which may be able to escape predation by attaining a larger size (Palmer, 1983; McClanahan, 1990; Navarrete, 1996), and by avoiding nocturnal predation (e.g. climbing the kelp fronds; Halliday, 1991). Furthermore, Fawcett (1984) suggested that subtidal snails may migrate upshore from deeper areas to avoid predation. Indeed, Myers (1986) observed a migration trend of snails from deeper to shallower areas at the study site, which implies passive predator avoidance.
The shallower Lithothrix zone may serve as a refuge for Astraea undosa, as suggested by the reported low predation in shallow areas (Ambrose, 1982; Schmitt, 1982; Myers, 1986; Halliday, 1991; Alfaro, personal observations), low density of empty shells, and high snail density. The low survival rates of Astraea undosa in the shallowest Eisenia zone may be influenced by seasonal predation by lobsters, but more likely is compounded by the high-energy environment of this zone, a hypothesis supported by the low density of empty shells.
5. Conclusions
The observed zonation patterns of Astraea undosa at Bird Rock, Santa Catalina Island, are a product of interacting physical and biological factors that vary in their influences among zones. The deep-to-shallow migration of Astraea undosa documented by Myers (1986) at the Bird Rock study site implies that snails may be able to move to preferred zones. In this study, the physical disturbance by wave action in the shallowest
Eisenia zone may periodically reduce the snail density. The lower snail density may
decrease the level of intraspecific competition for food and allow higher growth rates. These ecological interactions lead to a low density of large snails in this zone. The pattern of high population density in the Lithothrix zone may indicate a refuge region for snails against the increased hydrodynamic or predation stresses of neighboring areas. Lab and field cage experiments also show that competitive interactions become more important at higher population densities. Thus, high population density within the
Lithothrix zone may be maintained by sufficient, but sub-optimal food resources
interacting physical and biological factors may vary somewhat seasonally, as reflected by slight fluctuations in population densities and size-distributions across zones.
Results from this study confirm that zonation patterns are present in subtidal environments, which are less well-understood ecologically than intertidal communities. The well-documented pattern that high-intertidal populations are affected greatly by physical factors, and that low-intertidal populations are influenced more by biological factors, also appears to hold true for subtidal Astraea undosa at the Bird Rock study site. However, for subtidal populations, the biological zones occupy more extensive regions of the seafloor, in a depth-gradient from zone to zone. This paper contributes to a better understanding of zonation patterns in subtidal populations, and concludes both that wave action may restrict the population in shallow areas and that predation may restrict the population in deeper areas. Because these physical and biological factors constrict the overall population range at its upper and lower depth limits, organisms may seek refuge in intermediate zones, with the cost of decreased growth rates due to high competition levels. Therefore, this study provides a platform from which to test hypotheses that subtidal zonation patterns are a result of physical and biological factors acting differentially throughout the range of a population.
Acknowledgements
We thank T. Schaeffer, C. Huntley, P. Pehl, L. Roberson, M. Calavetta, P. Slone, and the staff at the Wrigley Marine Science Center for their invaluable assistance in the field. Technical assistance was provided by W. Krohmer, B. O’Reilly, N. Hudson, and the Biology Office staff at the California State University, Northridge. Special thanks to M. Denny for guidance, support, and use of his lab at the Hopkins Marine Laboratory. M. Patterson, R. Ambrose, G. Trussell, S. Genovese, P. Edmunds, L. Allen, K. Campbell, and two anonymous reviewers provided helpful comments to earlier versions of this manuscript. This research was supported in part by the California State University, Northridge (C.S.U.N.), the Wrigley Marine Science Center, and grants to A. Alfaro by the James and Parnell Simpson Scholarship, Bennett-Bickford Biology Scholarship, C.S.U.N. Foundation Research Grant, C.S.U.N. Pre-Doctoral Fellowship, C.S.U.N. Student Equity Scholarship, Imperial Court of the San Fernando Valley, Sigma Xi Grant-in-aid of Research, California Pre-Doctoral Scholarship, and the Lerner-Gray Scholarship of the American Museum of Natural History.
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