Marine Ecology, May 9 -16, 2008
Lecture 8 & 9: Biological interactions in the intertidal

I. Overview: Effects of biological interactions on zonation/distribution of intertidal organisms. A. Joe Connell (1972) proposed that physical factors (especially tolerance to desiccation) were most important in setting UPPER limits of species distributions, while biological interactions were more important in setting LOWER limits. 1. More recent studies show that upper limits can also be modified by biological factors, but still many cases where upper limits are related to physical factors. B. A variety of interspecific interactions and other biological processes have been studied to determine how they influence intertidal zonation, as well as distribution within a zone (for different microhabitats). This lecture focuses on those interactions and processes. II. Competition for space A. Example: Vertical distribution of the barnacles Chthamalus and Balanus/Semibalanus. Classic work of Joe Connell (1961) 1. Key observations a) Patterns of larval settlement: overlap in higher zones (see diagram) b) Patterns of adult distribution: Chthamalus higher than Semibalanus; no overlap at sites where both are found c) If Semibalanus is removed/excluded, the lower limit of Chthamalus is extended into the upper-mid-intertidal, but no further. • Why extended?: Semibalanus grows faster and "undercuts" Chthamalus. When removed, C. can grow • Why not go deeper?: Range not extended past the upper-mid-intertidal because of larval settlement patterns. d) If Chthamalus is removed/excluded, the lower limit of Semibalanus is not extended upward. e) Transplant Balanus/Semibalanus to higher zone: cannot survive. Why not? • Experimental shading: Balanus/Semibalanus does extend upward to replace Chthamalus. • Cooler climates (i.e. North of Cape Cod): Balanus/Semibalanus is found in high intertidal (and excludes Chthamalus) • Conclusion: Chthamalus is more tolerant to desiccation than Balanus. Upper limit of Balanus set by physical factors. 2. So, in this case, larval settlement and physical factors, as well as direct competition, lead to the distribution that exists. (Connell’s hypothesis holds for this example.) B. Example: Algal distribution 1. Removal experiments have shown that competition limits the lower extent of some algal species (work of Paul Dayton and others). Showed this by removal experiments similar to Joe Connell’s on barnacles. 2. Successional pattern seen: Small species initially settle and grow quickly on available open space (opportunistic), but eventually outcompeted by species which grow larger. a) What competitive advantage might these larger species have? Possibilities include: • Shading out smaller species • Utlizing nutrients more effectively • Growing over smaller species • Having grazing deterrents (see IV.C.) C. Example: owl limpet territoriality 1. Owl limpet, Lottia gigantea, maintains a territory and "chases" interlopers away. (This occurs on a very slow time scale...) D. Mussel bed succession in the mid-intertidal, “exposed” coast: one possible sequence of events 1. Opportunistic algae colonize bare rock 2. Barnacles displace the opportunistic algae (or can be the first settlers) 3. Mussels slowly overgrow and displace the barnacles (or can be the initial settlers), until a solid band of mussels exists. a) What features of the mussels enable them to win? (We discussed this on Wednesday, May 14, pretty carefully…) 4. But why does the mussel band end abruptly in the mid-intertidal? Think about this as we go through other factors. III. Predator-prey interactions also shape distribution patterns in the interidal A. Example 1: Nucella 1. The snails Nucella emarginata and Nucella lamellosa prey on barnacles, and may serve to establish a lower limit for the barnacle Balanus glandula. (Connell, 1970). The presence/absence of Pisaster will affect the influence of Nucella spp., since Pisaster feeds on Nucella. B. Example 2: Pisaster ochraceus Major studies by R. Paine (1966, 1972, 1985) on P. ochraceus in Washington. NOTE: This is a very important study. 1. Methods: Excluded the sea star Pisaster ochraceus from regions within and below where the mussel Mytilus californianus occurred. Used cages to keep Pisaster out. (Important control: non-excluding cages...) 2. Results, Part 1: a) Mussels settled and grew in the zone where they were previously excluded. The deeper mussels thrived and grew larger than those in the mid-intertidal. b) Mussels dominated more completely in the zone where they had been more patchy, suggesting that Pisaster also “thins” the mussels and promotes greater species diversity in those zones. 3. Results, Part 2: In 1985 follow-up of his experiments, Paine found that the lower limit of the mussel band persisted, despite removal of the cages 14-17 years before. Likely explanation: mussels reached a size refuge. a) Compare to New Zealand studies (similar results) and Chile results (returned to condition resembling the control when sea stars were added). • Why the differences among sites? Think! 4. “Natural” experiment on New England coast (Menge, 1976, Lubchenco and Menge, 1978) with a different star and mussel species. a) High wave action: Sea stars absent, mussels completely dominant b) Protected, decreased wave action Sea stars present, greater diversity. C. Pisaster and similar predatory stars are keystone species: Paine coined the term "keystone predator" based on Pisaster. 1. Two definitions of a “keystone predator.” a) Species compositon of the entire intertidal community is shaped by keystone predators such as Pisaster ochraceus. b) A keystone predator (such as Pisaster ochraceus) has a larger impact on the ecosystem than its numbers/proportions would suggest. 2. Pisaster is able to feed on species other than mussels, including many species the predatory snail Nucella spp. By feeding on Nucella, barnacles will persist to a greater extent. 3. Contrast keystone species concept with diffuse predation: total predation strong, but not due to a single species. 4. Important to realize that other conditions may affect the degree to which a keystone predator influences the community (i.e. role of larval transport/recruitment, disturbance, and temperature, which we will discuss shortly...) 5. Pisaster itself is limited by physical conditions (see Connell’s hypothesis). Can only feed in higher zones at high tide. Less time to feed in higher zones. D. Predation also influences distribution within a zone (think about microhabitats) 1. Peter Frank (1982) found 5 species of limpets at Cape Arago (southern Oregon) found primarily on vertical rock faces. He hypothesized that this was due to black oystercatcher predation. They can only reach and pry up limpets on horizontal faces, but those on vertical faces are out of reach. 2. Study by Tom Hahn in the Monterey bay: Collosella scabra on horizontal faces, Collosella digitalis on vertical faces. Tom watched oystercatchers feed, and also collected empty limpet shells to measure and identify to species. a) He confirmed that oystercatchers were eating C. digitalis, but not C. scabra. b) He always observed the oystercatchers taking limpets from horizontal, but not vertical, faces. 3. NOTE: Differences might also be caused by C. scabra’s ability to deal with desiccation more effectively a) How could you test this hypothesis (HINT: Look back at barnacle experiments dealing with desiccation… Also think about north vs. south-facing slopes.)

IV. Limitation by grazers A. Limitation of algae by grazers 1. Several studies show that grazers (including littorines, limpets, fly larvae and amphipods) can influence the upper limit of algal growth. a) So, not just physical factors, as previously suggested 2. Effects may be seasonal (grazing of diatom mats by littorines increased in summer, when littorines were more active.) 3. Case study: Katharina tunicata (a chiton): Does Katharina tunicata prevent prevent the growth of large kelp? a) Diether and Duggins (1988): removal of K. tunicata (a chiton) in intertidal area in Washington resulted in the development of kelp bed b) Simlar removal in Alaska did not have this effect. Why not? • Differences in K. tunicata density? • Perhaps physical conditions not suitable to kelp growth. • Other grazers have an inhibitory impact? • Anything else? Brainstorm! B. Maintenance of diversity by grazers 1. Comparisons of tide pools with and without grazing snails. a) Snails maintain greater algal diversity, by keeping fast-growing green algae from becoming dominant 2. What happens to the algal diversity/species composition when you add in crabs? 3. What happens to the algal diversity/species composition with bird predation on crabs?. C. Grazing deterrents 1. Morphological: calcium carbonate within tissues, or other “tough” tissue 2. Chemical defenses a) sulfuric acid, alkaloids, phenolic cpds, halogenated metabolites 3. Crustose forms in regions with high grazing pressure; erect forms of same algae in regions with lower grazing pressure. 4. Note: both r and K-selected algal species exist (as described earlier...) a) K-selected species reach size refuges D. Limitations of grazers by algae: 1. On the other hand, limpets may not be able to keep up with algal growth, and are subsequently excluded by algae, when algal species overgrow an area and make it impossible for limpets to hang onto the rock (Underwood and Jernakov, 1981, also in text). E. Physical conditions vs. grazing in affecting distribution of algae 1. Compare waveswept vs. sheltered locations V. Symbiotic relationships and species distribution A. Commensalism 1. Mussel beds: diverse assemblage of small invertebrates. Why? 2. Algae: The high intertidal alga Endocladia muricata found to support 93 species (mostly really tiny critters.) (Peter Glynn, 1965). 3. Unclear if there are benefits to the mussels or algal species involved. (Probably commensal, but hard to tell.) B. Mutualistic 1. Anthopleura spp. and protist symbionts (see Cnidaria lecture) a) Anthopleura spp. with symbiont will move toward lighted areas, while those without the symbiont do not. VI. Larval Types and Strategies A. What are larvae? 1. Larvae are a distinct stage, behaviorally and morphologically, from the adult form of an organism. a) They must undergo a profound change before becoming an adult. 2. Examples of adults and their larval stages B. Larval strategies 1. Description of key larval strategies a) Planktotrophic larvae • “plankton” = drifting; “trophic” = relating to food • Adults produce large numbers of eggs with little to no yolk. • Once hatched, they obtain their nutrition by feeding within the water column. • May spend a relatively long period of time within the plankton. b) Lecithotrophic larvae • “lecitho” = yolk; “trophic” = relating to food • Adults produce relatively low numbers of yolky eggs. • Once hatched, the larvae use the yolk as an energy source (non-feeding) • Spend relatively less time within the plankton. c) Non-pelagic or direct development • The larval stage occurs within the egg case. Neither eggs nor larvae are released into the plankton. The young hatch out as juveniles that basically resemble the adults. C. Benefits and costs of differing strategies 1. Planktotrophic larvae a) Benefits • Large numbers of produced for a given amount of energy • Offspring can disperse widely; effectively colonize new areas b) Costs • Unpredictable food resources • At the mercy of currents (Why a problem?) • Longer time in the plankton ( greater predation risk • In sum: A very high proportion of planktotrophic larvae die 2. Lecithotrophic larvae a) Benefits • Have their own energy supply for growth. • Less time to be “at the mercy of currents.” • Less time as plankton ( lower risk of predation b) Costs • Fewer eggs can be produced • Less time in the plankton means less dispersal • Still encounter some of the same risks as planktotrophic larvae. 3. Non-pelagic or direct development a) Benefits • Much lower mortality rate (Why?)(higher proportion survive • Begin their juvenile stage in a suitable habitat (Why more likely to do so than planktotrophic or lecithotrophic larvae?) b) Costs • Relatively few offspring can be produced • Little/no opportunity for dispersal. (Why a cost?) VII. Larval Ecology and Community Establishment A. Cues for settlement and their importance 1. Light a) Vertical position in the water column (Why important?) b) Sun vs. shade (Why important?) 2. Pressure (Why important?) 3. Currents (Why important?) 4. Salinity (Why important?) 5. Substrate type (Why important?) 6. Chemical cues a) From adults of the same species b) From from prey species c) From predators
VIII. Disturbance and succession A. Review: succession 1. First colonizers usually r-selected: lots of larvae or spores, fast-growing, but relatively poor competitors 2. Intermediate species next 3. K-selected can come to dominate a particular region in a “climax community” if there is no disturbance (Example: M. californianus and its associated fauna) B. Wave action as the major agent of disturbance 1. Waves cause drift logs to bash into the intertidal zone 2. Violent storms can also tear off organisms (climax community of mussels at risk) 3. Bare patches are created where mobile larvae can settle. But who settles? a) Available larvae/spores in water column highly variable in space/time • Why? (HINT: Think about specific abiotic and biotic factors that might impact them.) • Example (Gaines and Roughgarden, 1985) • Predation of juv. rockfish on barnacle larvae, can reduce stock to 1/50 of released larvae • Juv rockfish decline when kelp forest declines (warm years, El Nino for ex). • Bad year for kelp means a bad year for rockfish, and thus a good year for barnacle recruitment. • Ex: Connolly and Roughgarden (1998). Water movement: • Offshore movement of surface water, due to upwelling, can prevent larvae from settling onto the shore i) Larvae can only settle at times/locations with diminished wind from north (Why? How is this related to offshore water movement and upwelling?) • Stronger upwelling in CA; less intense larval settlement • Think about El Niño/La Niña (upwelling is reduced during El Niño...) 4. End result: Even within a single intertidal zone, a living “mosaic” comprised of patches of organisms at different stages occurs
Study questions
1. State, in your own words, Joe Connell’s general hypothesis for how upper vs. lower limits of species are set in the intertidal.

2. Be sure you have a good working knowledge of each example presented in class. In other words, you should know, at the level of lecture or text (whichever is greater) • Key concepts being introduced/explained by the example! • The name of the experimental organism, • The distribution pattern observed. • The type of experiments or observations made • The factor being tested (Predation? Desiccation? Importance of a symbiotic relationship? Etc...) • The interpretation of the key results • Limitations of the experiments/observations in explaining the distribution patterns seen or applying them to broader geographical areas.

3. What physical and/or biological factors appeared responsible for the lower limit of Chthamalus in the intertidal? What physical and/or biological factors appeared responsible for the upper limit of growth in Balanus? Describe the observational/experimental evidence upon which your answers are based.

4. What is a keystone predator? Why is Pisaster considered a keystone predator, while Nucella is not?

5. By what mechanism could a grazing snail actually cause increased algal diversity in a tide pool? Compare this to the mechanism by which Pisaster ochraceus maintains diversity in the mid-intertidal. What are the effects of crabs on these small tidepool ecosystems? What are the effects of gulls?

6. Describe Bob Paine’s initial experimental procedures and key results for Pisaster ochraceus removal experiments on the Washington coast.

7. When Bob Paine returned to his experimental sites 14-17 years after the Pisaster-exclusion cages were removed he found that the thick beds of mussels persisted in the low intertidal, even though Pisaster could now freely enter the area. In contrast, for a similar experiment in Chile, the initial conditions (clear boundary at bottom of the mid-intertidal) were re-established. Why the difference in the two studies? Would you expect the thick beds to persist indefinitely?

8. Be able to list the "general" types of both physical factors (i.e. “wave action” et al.,) and biological interactions (i.e. “competition for space” et. al.) which influence distribution of intertidal organisms. Then, give real examples of each (as provided in lecture) and explain them clearly.

9. One observation from the rocky intertidal of central California is that the limpet Collisella digitalis is found on vertical surfaces, while the limpet Collisella scabra is found on horizontal surfaces. • What are the two hypotheses provided for this observation? Are they mutually exclusive hypotheses? • What experimental evidence has been provided? • What additional evidence would be useful in determining which of these factors is key in determining the distribution?

10. Provide examples of how symbiotic relationships can impact distribution of intertidal organisms.

11. How might the distribution of algae limit the distribution of limpets and other snails?

12. What are larvae?

13. Describe the three key larval strategies, and then describe the major benefits and costs of each.

14. What basic trends have been observed in terms of latitude vs. particular strategies? Explain why these general trends exist from the perspective of the organisms’ survival. Are exceptions to these trends common? Provide at least one example.

15. What basic trends are thought to exist in terms of body size vs. particular strategies. Explain why this trend might exist from the perspective of the organisms’ survival.

16. If brooding (non-pelagic strategy) assures a higher percentage of survival of young, why don’t all marine animals, large and small, pursue this strategy?

17. List several cues that are used by larvae to find suitable habitats for settlement, and describe how each cue can be used by a larva.

18. Give an example of succession in an intertidal community, being sure to use the concepts of r-selected and K-selected species.

19. What is thought to be the major cause of disturbance in rocky intertidal communities? Describe a specific case of how such a disturbance could lead to a bare patch.

20. What is meant by a “mosaic” distribution of organisms?

21. Once a bare patch exists, what factors determine which particular organisms will colonize it?

22. Availability of particular larvae and spores are highly variable in both space and time. Explain why, using general concepts as well as specific examples to support your answer.

23. How might upwelling affect the availability of larvae ready to settle in the intertidal?

24. Describe the roles that larval settlement (i.e. colonization) vs. other factors play in determining why you see what you see where you see it in the intertidal.