Rocky Intertidal -- part II Connell and the experimental revolution review The development of experimental ecology I. Intertidal Zonation, part II 1. Follow ups on Connell 2. 3. Exceptions II. Horizontal Distribution 1. Variation in Relative Importance 2. Alternate Stable States

Impacts: 1) “Connell’s rule”: upper limits set by physical processes, lower limits set by species interactions 2) The dawn of appreciation and exploration of experimental field ecology

d) Specific hypotheses: The explosion of field experiments in the intertidal Shading areas above upper limit of Semibalanus will… 1) allow Semibalanus to extend higher 1. David Wethey (1984, Biological Bulletin) 2) cause decrease in Chthamalus because of increase in Semibalanus a) System - same as Connell’s (Semibalanus and Chthamalus) but in New England on east coast of US e) Experimental Design: - “control” treatment (unmanipulated) to compare with manipulations b) Pattern - same as Connell’s (Semibalanus and Chthamalus) - manipulations designed to test for artifacts of main manipulation but focus on explaining upper limits of Semibalanus Treatment Predators Shade Roof c) General hypotheses: i) Solar exposure sets upper limit of Semibalanus 1) Unmanipulated control + – – 3) 2-sided cage with opaque plastic roof + + + ii) with Semibalanus sets lower limit of Chthamalus 4) 2-sided cage with screen “roof” + – – 5) 2-sided cage with clear plastic roof + – + 6) Full cage with opaque plastic roof – + + 7) Full cage with screen “roof” – – – Chthamalus 8) Full cage with clear plastic roof – – + tidal height Semibalanus Many treatment comparisons test effects of shading, others predation, and others “cage artifacts”. Which comparisons test which effects?

Wethey (1984) 2. Importance of predation in determining zonation f) Results: Semi Robert Paine 1966, 1974 i) no cage or roof material effects Chth (i.e., no artifacts) a) System / Pattern: ii) no effects of predators (above predator zone) i) Rocky intertidal in Pacific Northwest (Olympic Peninsula, Washington) iii) Semibalanus survived above survivorship normal adult distribution in shade No Shade Shade ii) Mytilus californianus (1,3,4,6,7) (2 & 5) iv) Chthamalus died at higher rate in • dominant in mid-intertidal shade because of increased - why not higher? (assumed desiccation) of Semibalanus - why not lower? g) Conclusions: • lower limit remarkably stable i) Upper limit of Semibalanus set by “solar exposure”  ii) Lower limit of Chthamalus set by competition with Semibalanus • can migrate, and they settle below adult distribution - so settlement may not be very important

1 Paine 1966, 1974 Rocky Intertidal Zonation

a) System / Pattern (cont’d): mussels iii) Pisaster ochraceus • main predator on mussels gooseneck • occurs mainly in lower intertidal - upper limit may be set by desiccation?

anemones, tunicates, b) General hypothesis: sponges • lower limit of Mytilus set by predation by Pisaster

c) Specific hypothesis: coraline • in areas where Pisaster is removed, Mytilus distribution will expand lower into the intertidal Pisaster

Paine 1966, 1974 Paine 1966, 1974

d) Test: f) Conclusions: i) removed Pisaster from lower intertidal at two sites i) predation sets lower limit of mussels ii) replicate “control” area at each site with no removals ii) supports general paradigm that biotic interactions set lower limits of distribution in intertidal  problem with experimental design: no replication of removal and control at each site -- Can you distinguish treatment vs. area effects?

e) Results: i) over several years, Mytilus distribution extended into lower ii) where Mytilus extended into lower intertidal zone, declined… another story

Paine 1966, 1974 Paine 1966, 1974

g) Postscript: g) Postscript: ii) Two important implications: i) After experiment ended, Paine quit removing Pisaster, but cont’d to sample sites: a) Experimental design: site-site variability can mask experimental high results  replication at the scale of sites is needed

b) Patterns: Distributions can be the result of temporary environmental Lower limit conditions (in this case the reduction of Pisaster) of Tatoosh site Mytilus - mussels do settle to lower intertidal, and if they can survive long Mukkaw site enough, they can grow and escape predation by their greater low size removals time - another example: Southern California species that recruit to and a) at one site, lower limit moved back up as Pisaster reinvaded remain in central California during episodic El Niños b) at other site, it did not!

2 The experimental revolution, cont. c) General hypotheses: 1. grazing determines upper limit of foliose algae 3. Exceptions to the paradigm (of upper and lower limits) 2. physical factors determine upper limit of algae a) Upper limits determined by physical factors? 3. both grazing and physical factors… Underwood 1980, Oecologia 4. other factors - e.g., spores don’t settle above upper limit of algae

a) System: Grazing gastropods and foliose macroalgae in d) Specific hypotheses: intertidal of Australia 1. areas cleared and kept free of grazers in mid-intertidal will b) Pattern: Grazers occurs in zone above the alga they eat become colonized by foliose algae 2. areas shaded will become colonized by foliose algae 3. only areas both cleared of grazers and shaded will become colonized by algae

grazers mid foliose algae lower

e) Test: f) Results: 1.full cage (with roof) provides shade and excludes grazers • algae never occurred in open plots • algae colonized the grazer exclusions (“fences”), but not the roof-only or the open plots 2.roof only provides shade only • in fenced areas: – algal cover reached 100% but never lived long 3.cage with no roof (“fence”) only excludes grazers enough to reproduce – high cover due to continuous recolonization by new spores 4.open is control • algae only grew and survived to reproduce in the shaded full cages (with roof) grazers algal cover algal reproduction

roof full grazers grazers only cage shade no yes no yes open fence shade interaction no yes no no

Underwood 1980 3. Exceptions to the paradigm (of upper and lower limits)

f) Conclusions: Lower limits determined by biological factors? • upper limit of distribution set by biotic factor: grazing! • upper limit of reproduction set by interaction between grazers and a) intertidal organisms are adapted to marine and terrestrial physical stress b) most studies find that lower limit set by biotic interactions, but… c) exceptions: - Littorina () limited to very high intertidal and will die if submerged too long - two macroalgae, Silvetia and Fucus, die if submerged too long d) few studies have tested this!!!!

grazers mid foliose algae lower

Silvetia compressa

3 II. Horizontal patterns of distribution and abundance Fucus vesiculosus Mytilus edulis Nucella lapillus 1. Variation in relative importance of ecological processes - Menge 1976, Ecology a) Background: we have focused on vertical zonation, but what about horizontal gradients? d) General hypotheses: i) Competition and predation are important in determining b) System: barnacles, mussels, algae, predatory snail in these patterns, but New England rocky intertidal ii) Importance of competition and predation differ in exposed c) Patterns: along a gradient from exposed to protected and protected sites sites… e) Specific hypotheses (experimental design): CHARACTERISTIC EXPOSED SHORE PROTECTED SHORE Complicated design using cages and cage controls to assess effects of: Dominated by Mussels Fucoid algae Free Space Rare (<10%) Common (40-90%) i) competition: barnacles, mussels, and algae Predators/Grazers Uncommon (16-80/m2) Common (108-450/m2) ii) predation / grazing Cover Low Low iii) exposure: importance and how it varied along gradient iv) all areas initially cleared

f) Results: Exposed Shores f) Results: Protected Shores

Cage Cage Cage Cage Open Cage (-Fucus, (-Fucus, Control (-Predators, Control Open Cage (-Predators, (no manipulation) (-Fucus) (-Fucus, -predators) -predators, -predators, -grazers) (no manipulation) (-Fucus) (-Fucus, -predators) -grazers) -mussels) -mussels) Algae (Fucus) Barnacles Mussels

Mussels Mussels Barnacles Barnacles Barnacles Mussels Barnacles Barnacles Barnacles Mussels Mussels Barnacles

Mussels Mussels Fucus Algae (Fucus) Abundance Abundance Fucus Time Time Time Time Time Time Time Time Time Time At protected sites - effects of predators At exposed sites - same pattern for cages with Fucus and predator removals and a) abundance is kept low by predators, allowing Fucus removals (open areas) barnacles to colonize and persist in low numbers outside a) barnacles colonize then are out-competed by mussels (no additional effect of of cages predators: see open areas) b) without predators, barnacles are out-competed in cages b) If mussels are removed then barnacles persist by mussels

- pattern is similar to that in protected shores c) barnacles persist in high numbers only if you remove mussels, predators, & algae d) if you remove only predators (including grazers) algae and barnacles colonize but get out-competed by mussels

g) Conclusions: h) More generally: Physical Predation Competition Processes Different processes are important at exposed and protected sites: General paradigm of High organization in Importance to a) at exposed sites -- predation/grazing unimportant - competition is the primary rocky intertidal community organizing force in the system organization 1. predators are generally uncommon (Connell 1975, Menge and Sutherland 1976, Menge 1976, 2. mussels are competitively dominant (over algae and barnacles) Low Lubchenco and Menge 1978, Underwood and Denley 1984) Benign Severe b) at protected sites -- predation important Environmental harshness 1. with predation, barnacles dominate if Fucus is removed 2. without predation mussels out-compete barnacles and algae • in habitats with relatively benign physical environments - predation structures communities 3. predation keeps competition from occurring with mussels (mussel abundance is kept low) • with increasing environmental harshness - predation efficiency is decreased and competition becomes a major process structuring communities

c) Importance of predation varies with exposure; at exposed sites • with even greater environmental harshness - importance of competition decreases predators are uncommon, their feeding ability is reduced because they and physical processes become most important have to spend more time hanging on and not feeding • local escapes from predation (in benign environments) or physical stress (in harsh environments) cause patchiness in the community

4 2) Alternative stable states - Lubchenco 1978, Am. Naturalist a) Question: Why might sites exhibit different stable a) Background: Why might sites exhibit different stable communities in the absence of environmental differences? communities in the absence of environmental differences? b) System: grazing snail and algae in New England rocky b) System: grazing snail and algae in New England rocky intertidal intertidal c ) Patterns: spatial variation in community structure: c1) Patterns: spatial variation in community structure: 1

Chondrus crispus Littorina Enteromorpha Chondrus/Fucus Diversity Tidepools common rare common low Tidepools intermediate intermediate intermediate high Tidepools rare common rare low Enteromorpha Rock common rare common low Rock intermediate rare common intermediate Littorina littorea Rock rare uncommon common high Fucus vesiculosus

c ) Patterns: spatial variation in species diversity varies as 2 d) Hypotheses: a function of grazer density and habitat type: i) Littorina prefers to eat Enteromorpha ii) Enteromorpha out-competes other algae in tidepools (if no Littorina) Tidepools Rock (emergent) iii) Littorina can suppress competitive abilities of Enteromorpha in High High tidepools

iv) Enteromorpha is competitively inferior on emergent rock surfaces

Diversity

Diversity e) Study Design: Why might sites exhibit different stable Low Low Low High Low Higher communities in the absence of environmental differences? Littorina density Littorina density i) assessed food preferences of Littorina ii) manipulated density of Littorina in pools

f) Results: Lubchenco 1978 Results Summary i) Enteromorpha are favored food of Littorina (in pools and on rock) 1. in tidepools, intermediate densities of Littorina increase algal diversity ii) patterns from pools… (by eating the dominant competitor) Control Littorina addition Littorina removal 2. on emergent rock surfaces, Littorina reduces algal diversity (by eating (Littorina common) (rare before) (common before) the subordinate competitor) High Chondrus High High Enteromorpha Enteromorpha Tidepools Rock (emergent) Chondrus High High Enteromorpha

Low Low Low Chondrus

Percent Cover Cover Percent Time Time Time Pools

Diversity

1) Enteromorpha can out-compete Chondrus, but… Diversity 2) high densities of Littorina can suppress effects of Enteromorpha 3) intermediate densities of Littorina allow coexistence of most species Low Low 4) Littorines are a but maximum effect on diversity occurs at intermediate Low High Low Higher densities Rock Littorina density Littorina density 1) Enteromorpha competitively inferior - but still favored prey 2) Fucus (mid) and Chondrus (low) are superior competitors 3) Littorina’s effect is to graze already uncommon species (Enteromorpha and other ephemerals) 4) Grazing on uncommon species speeds up competitive exclusion and acts to reduce species diversity

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