Subtidal Tegula distributions Abstract Abundance and distribution data were collected on three species of turban snails (Tegula) in a temperate kelp forest, the Hopkins Marine Life Refuge. Similar data at identical sites in the same forest were collected by Watanabe (1984). Tegula abundances from the present study and Watanabe (1984) were compared. Overall Tegula density has increased significantly since the earlier study. A bathymetric zonation of Tegula that was documented in the earlier study was borne out in my study, Tegula brunnea occurs in shallow water (0-6m), T. pulligo occurs mostly in deep water (7-12m), and T. montereyi is the least abundant everywhere, but present everywhere. T. montereyi has been anecdotally observed to have increased in density in the past 15 years, and this trend appears in my data, but is not statistically significant. Subtidal Tegula distributions Introduction Three species of archaeogastropod trochid snails in the genus Tegula are abundant in subtidal kelp forests near Monterey: Tegula brunnea, T. pulligo, and T. montereyi (Abbott and Haderlie, 1980). They are closely related, but exhibit a bathymetric zonation: T. pulligo is most prevalent between 7- 12m, T. brunnea occurs from the low intertidal zone to about 6 meters subtidally, and T. montereyi is less abundant, and relatively evenly distributed between 2m and 12m subtidally (Lowry et al., 1974; Riedman et al., 1981) Tegula spp. are the most abundant grazer on the giant kelp Macrocystis pyrifera (Lowry et al., 1974), and are an important grazer on benthic algae (Schmitt, 1996). Pisaster giganteus and Pycnopodia helianthoides, two species of sea star, are the most common benthic predators on Tegula (Watanabe 1983). Enhydra lutris, the sea otter, also preys on Tegula, but does not take as many as the sea stars (Watanabe, 1984). Tegula abundances in the Hopkins Marine Life Refuge were recorded by Watanabe (1984). In this present study, I duplicated his study sites and methods, to try produce a dataset comparable to his, but at a later time. I will compare data from this study with data from the previous study to examine temporal changes in Tegula populations over the past 15 years. Subtidal Tegula distributions Materials and Methods All observations were made using SCUBA in the Hopkins Marine Life Refuge, off Cabrillo Point, California, USA (Fig. 1). Three study sites located in the Hopkins Marine Life Refuge were used in a study of Tegula conducted in 1978-1981 by Watanabe (1984), All observations in this present study were carried out at those study sites. All observations were made during daylight hours, in April and May of 1996. The study area consists of rocky (granitic) benches that gradually give way to pinnacles of rock in deeper water. This produces a substratum with both horizontal and vertical faces. Intermixed with the area of rocky substrate are patches of sand or shell fragment rubble. At the shallower site, there is a dense understory of Chondracanthus (=Gigartina) corymbifera and other genera of erect, small (less than .5 m frond length) algae. At the middle site, this algal turf is replaced by more encrusting algae and sessile invertebrates. At the deeper site, the biotic cover becomes a thin, low-relief crust in places. (For a more complete description of this area, see Riedman et al., 1981.) I gathered two different types of data, benthic and on Macrocystis pyrifera. To collect the benthic data, I used square 0.25m2 quadrats, Subtidal Tegula distributions placed in haphazard locations within each study site. I counted individuals of each of the three species of Tegula present in the quadrat. These numbers were multiplied by four to give densities (snails per meter?) of each of the three species, in each of the three depth zones. To collect the data on Macrocystis plants, I first haphazardly selected a plant within one study site. Then I counted all Tegula present on the plant. I began with the bottom 1.5m of kelp, including the holdfast, and counted each subsequent 1.5m section separately. I also counted the number of fronds on each kelp plant within each 1.5m depth interval. The number of individual snails of each species was then normalized to number of snails per frond (in each 1.5m section). To allow direct comparison with benthic data, these data were then multiplied by the average number of fronds per plant and average number of plants per meter?, to yield average number of snails on Macrocystis per meter? of substrate. I obtained the raw data from the previous study of the area by Watanabe (1984), and normalized it to number of snails per meter?, as outlined above. I then performed a fully factorial, four-way analysis of variance (ANOVA) on the numbers, to test for significant differences between: time (the present study and the prior one), the three different depths, habitat (benthic vs. Macrocystis), and snail species. All four factors were Subtidal Tegula distributions considered fixed factors. Results The three species of Tegula are distinctly segregated by depth. T. brunnea occurs more commonly in shallower depths, closer to shore (subtidally to 6m). T. pulligo is more common further from shore, deeper (7-12m). T. montereyi does not show a strong depth zonation, but is less abundant than the other two species at all study sites (Fig. 3, p«0.001). This is a change from the situation in the 1930's, when T. montereyi was the most abundant species (Rudolf Stohler, unpublished data) The overall Tegula density in the kelp forest at the three study sites has increased significantly since 1980 (Fig. 4, p=0.020). Tegula montereyi had been anecdotally observed to have increased in numbers between 1978 and 1996. Although this trend was shown by the data (the mean has doubled since 1978), it was not statistically significant (p=0.5, see Fig. 4). There were also some trends in the data I gathered on Macrocystis plants. T. montereyi were more abundant higher up on the plants than they were near the holdfast (Fig. 5). At some places, T. montereyi were even the most abundant species within a depth interval on a plant. These patterns of zonation within a Subtidal Tegula distributions plant are very transitory, since Tegula move so quickly along kelps. However, the data show some trends of usual heights of occurrence for Tegula of different species (Fig. 5). Discussion More research is needed to determine whether the increase in Tegula density is a long-term effect or simply a spike in the population, or a seasonal effect. Watanabe (1984) examined some possible causes for the observed habitat partitioning of the Tegula species. He found that the bathymetric zonation was maintained by an interaction of several factors. Larval settlement tends to set up the bathymetric zonation, with T. pulligo larvae settling deep and T. brunnea shallow. However, since the snails move very rapidly and live for several years, a mechanism is needed to maintain the distribution. Watanabe (1984) found in the same study that T. brunnea is more likely than T. pulligo to travel between Macrocystis plants on the substrate. T. pulligo travels between plants mostly through the canopy. Since there is a dense cover of erect benthic algae in shallower areas of the kelp forest, T. brunnea traveling between kelps in the shallow study site are more protected from benthic predation than they would be in deeper areas, where algal cover is less. So different behaviors Subtidal Tegula distributions leading to differential predation might maintain the bathymetric zonation that is set up by larval settlement. The change in overall Tegula abundance might be linked to a decrease in abundance of Pisaster giganteus, a sea star and important predator on all three species of Tegula. P. giganteus abundance is less now than it was when Watanabe's data was collected, but the difference is not statistically significant, (1.63 per 10 m2 in 1980, versus 1.15 per 10 m2 in 1996. Data from Watanabe, 1984, and Lu, 1996, unpublished data.) These data are only valid for the middle depth zone. Another factor that influences adult populations is larval settlement (eg. Lowry et al. 1974, Watanabe, 1984). If there has been an increase in settlement rate recently, that could explain the increase in Tegula populations with no reference to changing predation. The same is true of a decrease in post-settlement mortality; it could explain an increase in adult populations. did not examine larval settlement due to time constraints on my study. Another factor that I would have liked to examine but did not is the size structure of Tegula populations. Size structure of adult populations would give clues to past patterns of larval settlement (Lowry et al. 1974, Watanabe 1984). Modes (local maxima in the size frequency histogram) indicate past years of unusually successful recruitment (Lowry et al., 1974). If there Subtidal Tegula distributions were several very successful generations of snails in the recent past, this would show up as several modes in the adult size frequency distribution. Tegula in Southern California also exhibit bathymetric zonation (Schmitt, 1996), as do many other marine invertebrates (eg. Connell, 1961; Grosberg, 1982). This study should be re-done in several years, to determine whether the observed changes in Tegula abundance are trends or simply short-term anomalies. Conclusions Tegula exhibit a bathymetric zonation in this study area, similar to that found by Watanabe (1984). Overall Tegula abundance has increased significantly since Watanabe's 1984 study. Abundance of Tegula montereyi has also increased noticeably, but the change is not statistically significant. Subtidal Tegula distributions Works Cited Abbott, D.P. and Haderlie, E.C. (1980). Prosobranchia: Marine Snails. In Intertidal Invertebrates of California (R.H. Morris, D.P. Abbott, and E.C. Haderlie), pp. 230-307. Stanford, Calif: Stanford University Press. Connell, J.H. (1961). The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology. 42. 710-723. Grosberg, R.K. (1982). Intertidal zonation of barnacles: the influence of planktonic zonation of larvae on vertical distribution of adults. Ecology. 63. 894-899. Hunt, D.E. (1977). Population dynamics of Tegula and Calliostoma in Carmel Bay, with special reference to kelp harvesting. M.A. thesis, San Francisco State University, San Francisco, CA. Lowry, L., Mcelroy, A.J., and Pearse, J.S. (1974). The distribution of six species of gastropod molluscs in a California kelp forest. Biol. Bull. 147. 386-396. Riedman, M.L., Hines, A.H., and Pearse, J.S. (1981). Spatial segregation of four species of turban snails (Gastropoda: Tegula) in central California. The Veliger. 24 (2). 97-102. Schmitt, R.J. (1996). Exploitation competition in mobile grazers: tradeoffs in use of a limited resource. Ecology. 7 (2). 408- 425. Watanabe, J.M. (1983). Anti-predator defenses of three species of kelp forest gastropods: comparing adaptations of closely¬ related species. J. Expt. Marine Bio. and Ecology. 71. 257- 70. Watanabe, J.M. (1984). The influence of recruitment, competition, and benthic predation on spatial distributions of three species of kelp forest gastropods (Trochidae: Tegula). Ecology. 65 (3). 920-936. 10 Subtidal Tegula distributions Tegula abundances on Macrocystis, tabulated by height (meters) above the holdfast (N=5) T.brunnea Shallow Middle Deep mean std error mean std error mean std error 0-1.5 8.37 6.170 1.154 0.127 0.16 0.54 1.5-3 3.50 1.096 0.41 0.176 0.02 0.011 3-4.5 6.52 0.544 3.057 0.45 0.08 0.038 4.5-6 4.30 2.728 0.46 0.486 0.07 0.033 6-7.5 0.11 0.26 0.177 0.19 7.5-9 0.61 0.513 0.21 0.141 9-10.5 0.76 0.325 T.montere Shallow Middle Deep std error std error mean mean mean std error 0-1. 0.181 0.150 0.36 0.31 0.49 0.185 1.5-3 0.89 0.255 0.65 0.184 0.26 0.107 3-4.5 0.47 0.51 0.101 0.28 0.172 4.5-6 0.26 0.11 0.82 0.221 0.21 0.106 6-7.5 0.51 0.302 0.61 0.289 7.5-9 1.19 0.61 0.207 0.330 9-10.5 0.98 0.570 Deep T.pulligo Shallow Middle std error mean std error mean std error mean 0-1.5 1.141 1.750 2.02 1.29 0.473 2.76 1.5-3 0.53 0.231 1.00 0.360 0.91 0.275 3-4.5 0.599 0.30 1.78 0.132 0.62 0.282 4.5-6 0.342 0.00 0.000 0.52 0.191 1.10 6-7.5 1.07 0.94 0.012 0.435 7.5-9 0.000 0.45 0.25 0.335 9-10.5 0.024 0.05 11 Subtidal Tegula distributions Table 2: Number of stipes in each depth interval, tabulated by height (meters) above the holdfast (N=5) Stipes Shallow Middle Deep mean std error std error mean mean std error 0-1.5 19.60 9.373 10.198 25.80 35.00 9.324 1.5-3 18.40 5.784 27.40 6.615 7.926 23.40 14.80 4.954 3-4.5 5.943 19.20 20.40 5.490 4.5-6 4.000 12.00 18.40 6.831 17.80 4.748 6-7.5 4.324 15.40 6.743 14.00 7.5-9 7.60 2.638 14.20 6.717 9-10.5 13.00 2.828 12 Subtidal Tegula distributions Table 3: Data from Watanabe (1984) and my data, as used for ANOVA. All numbers represent individuals per square meter, normalized as outlined in the text, Means Mid Deep Shallow T.pulligo Kelp 1.05 9.81 4.90 T. montereyi 1.79 0.59 1.06 T.brunnea 4.60 3.24 0.34 Timel Shallow Mid Deep Benthic T.pulligo 2.67 9.07 2.05 T.montereyi 1.80 2.40 0.82 T.brunnea 22.86 0.27 0.41 Shallow Deer Mid T.pulligo Kelr 3.62 0." 4.40 T. montereyi Time2 1.19 2.52 2.20 T.brunnea 9.83 1.92 1.92 Shallow Mid Deep Benthic T.pulligo 8.84 4.19 12.00 T.montereyi 5.20 3.40 1.00 T.brunnea 14.00 2.60 0.20 Standard Deviations Shallow Mid Deer T.pulligo 4.34 Kelp 0.95 7.16 T. montereyi Timel 0.73 1.59 1.18 0.7 2.93 T.brunnea 3.21 Shallow Mid Deep Benthic T.pullige 4.84 3.65 23.23 T.montereyi 3.04 5.10 2.09 T.brunnea 43. 1.46 1.53 Shallow Mid Deer Time2 T.pulligo Kelr 0.47 2.68 2.98 T. montereyi 0.78 1.05 1.43 T.brunnea 1.55 7.78 1.08 Mid Deep Shallow Benthic T.pulligo 4.64 11.82 15.63 T.montereyi 9.63 4.55 1.78 T.brunnea 12.14 7.14 0.89 Table 3, continued Numbers of replicate observations Timel Kelp T.pulligo T.montereyi T.brunnea Benthic T.pulligo T.montereyi Time2 T.brunnea T.pulligo Kelp T.montereyi brunnea Benthic T.pulligo T.montereyi T.brunnea 14 Shallow Shallow Shallow Shallow 20 Subtidal Tegula distributions Mid Deep Mid Deep 30 39 30 Deep Mid Mid Deep 20 20 20 Table 4: Analysis of variance results on data from Watanabe (1984) and present study. ANALYS S OF VARIANC SOURCE SUM-OF-SQUARES F-RATIO DF MEAN-SQUARE TIMES 4.999 4.999 5.525 0.019 DEPTHS 18.185 9.092 10.048 O.000 HABITAT 2.667 2.947 0.087 2.667 SPECIESS 5.736 6.339 11.472 0.002 TIMESDEPT 0.876 0.438 0.484 0.616 TIMES*HABITAT: 1.659 1.659 1.835 0.176 TIMESSPECIES: 0.249 0.125 0.138 0.871 DEPTHS*HABITAT 4.069 8.138 4.49 0.012 DEPTHS*SPECIESS 15.57 56.367 14.092 0.000 HABITATS*SPECIES 0.065 0.033 0.036 0.964 TIMES*DEPTHS *HABITAT 2.241 0.291 1.120 1.238 TIMES*DEPTHS *SPECIESS 2.808 0.776 0.541 0.702 TIMES*HABITATS *SPECIESS 3.992 1.996 2.206 0.111 DEPTHS*HABITATS *SPECIESS 1.439 0.360 0.397 0.811 TIMES*DEPTHS HABITATSSPECIES 0.421 1.684 0.465 0.761 466.911 516 ERROR 0.905 Subtidal Tegula distributions Figure 1: Map of study sites in the Hopkins Marine Life Refuge, and a map of Central California showing their location, Figure 2: Tegula abundances separated by time, species, and habitat, graphed over depth zones. Figure 3: Relative Tegula abundances at the three study sites in 1996 Figure 4: Overall Tegula abundance changes between 1978 and 1996 Figure 5: Tegula abundance, as a function of height above holdfast on Macrocystis plants in 1996 15 San Francisco km Santa Cruz Moss Londing Pacific Grove Monterey Hopkins Marine Station 50m Pacific Grove, CA gpfpkel phe A study sites V Ss ode 1 28 20 3 r . 0 . SNAILS ON BOT TOM (No. m22) oooooo oooood88 o SNAILS ON KELP (m2 of Substr) kka- O — - 0 o OO — 1.2 Shallow Relative Tegula abundances by depth Mid Deep OT.pulligo ET.montereyi m T.brunnea 1 197 T. pulligo T. brunnea T. montereyi 1000 TE 10 Shallow relative frequencies —— —--------- 0.7 -——— —------------ 0.6 ------------------------ ----------------------- —---------------------- - - 0.2 —-- 0.14 0-1.5 1.5-3 3-4.5 4.5-6 Height above holdfast Middle relative frequencies —--------- - - - - - - — 0.4 +------— e --------- 0.2 +---- —------------------— — — — —------------—— 3-4.5 0-1.5 1.5-3 4.5-6 6-7.5 7.5-9 Hieght above holdfast Deep relative frequencies 0.9 08 —------- 0.7 +--------------------- - - - - —- 0.6 --- ---- 0.5 -- - - - - ---------------------,---------- 0.4 1----------------------------- 0.3 02 0.1 PP 4.5-6 0-1.5 1.5-3 6-7.5 3-4.5 7.5-9 9-10.5 Height above holdfast —2—T. puligo ----T. montereyi — A — T. brunnea —2—T. pulligo --T. montereyi — +- T. brunnea —2—T. puligo ----T. montereyi — +- T. brunnea