Connell and the Experimental Revolution

Rocky Intertidal Ecology Connell and the experimental revolution The development of experimental ecology I. Intertidal Zonation 1.
Follow ups on Connell 2.
Predation 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 The explosion of field experiments in the intertidal 1. David Wethey (1984, Biological Bulletin) a) System - same as Connell’s (Semibalanus and Chthamalus) but in New England on east coast of US b) Pattern - same as Connell’s (Semibalanus and Chthamalus) but focus on explaining upper limits of Semibalanus i) Solar exposure sets upper limit of Semibalanus ii) Competition with Semibalanus sets lower limit of Chthamalus lus ma us tha h C lan iba m Se f) Results: ii)
no effects of predators (above predator zone) iii) Semibalanus survived above normal adult distribution in shade iv) Chthamalus died at higher rate in shade because of increased abundance of Semibalanus Semi Chth survivorship no cage or roof material effects (i.e., no artifacts) 1)
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Unmanipulated control 2-sided cage with opaque plastic roof 2-sided cage with screen “roof” 2-sided cage with clear plastic roof Full cage with opaque plastic roof Full cage with screen “roof” Full cage with clear plastic roof Predators + + + + – – – Shade Roof – + – – + – – – + – + + – + Many treatment comparisons test effects of shading, others predation, and others “cage artifacts”. Which comparisons test which effects? Wethey (1984) i)
e) Experimental Design: - “control” treatment (unmanipulated) to compare with manipulations - manipulations designed to test for artifacts of main manipulation Treatment c) General hypotheses: tidal height d) Specific hypotheses: Shading areas above upper limit of Semibalanus will… 1) allow Semibalanus to extend higher 2) cause decrease in Chthamalus because of increase in Semibalanus 2. Importance of predation in determining zonation Robert Paine 1966, 1974 a) System / Pattern: i) Rocky intertidal in Pacific Northwest (Olympic Peninsula, Washington) No Shade Shade (1,3,4,6,7) (2 & 5) g) Conclusions: i) Upper limit of Semibalanus set by “solar exposure” ii) Lower limit of Chthamalus set by competition with Semibalanus ii) Mytilus californianus •
dominant in mid-intertidal - why not higher? (assumed desiccation) - why not lower? •
lower limit remarkably stable •
mussels can migrate, and they settle below adult distribution - so settlement may not be very important 1 Paine 1966, 1974 Rocky Intertidal Zonation mussels a) System / Pattern (cont’d): iii) Pisaster ochraceus gooseneck barnacles •
main predator on mussels •
occurs mainly in lower intertidal - upper limit may be set by desiccation? anemones, tunicates, sponges b) General hypothesis: •
lower limit of Mytilus set by predation by Pisaster c) Specific hypothesis: •
in areas where Pisaster is removed, Mytilus distribution will expand lower into the intertidal coraline algae 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 intertidal zone ii) where Mytilus extended into lower intertidal zone, species diversity 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: high Lower limit of Mytilus Tatoosh site Mukkaw site low a) Experimental design: site-site variability can mask experimental results  replication at the scale of sites is needed b) Patterns: Distributions can be the result of temporary environmental conditions (in this case the reduction of Pisaster) - mussels do settle to lower intertidal, and if they can survive long enough, they can grow and escape predation by their greater size removals time a) at one site, lower limit moved back up as Pisaster reinvaded b) at other site, it did not! - another example: Southern California species that recruit to and remain in central California during episodic El Niños 2 The experimental revolution, cont. c) General hypotheses: 3. Exceptions to the paradigm (of upper and lower limits) a) Upper limits determined by physical factors? Underwood 1980, Oecologia 1.
grazing determines upper limit of foliose algae 2.
physical factors determine upper limit of algae 3.
both grazing and physical factors… 4.
other factors - e.g., spores don’t settle above upper limit of algae a) System: Grazing gastropods and foliose macroalgae in intertidal of Australia b) Pattern: Grazers occurs in zone above the alga they eat d) Specific hypotheses: 1.
areas cleared and kept free of grazers in mid-intertidal will 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 mid lower zers lgae gra a ose foli f) Results: e) Test: 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 enough to reproduce 3.
cage with no roof (“fence”) only excludes grazers –
high cover due to continuous recolonization by new spores 4.
open is control grazers •
algae only grew and survived to reproduce in the shaded full cages (with roof) algal cover roof only full cage open fence shade Underwood 1980 f) Conclusions: algal reproduction grazers grazers no yes no yes no yes no no interaction shade 3. Exceptions to the paradigm (of upper and lower limits) 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 physical stress a) intertidal organisms are adapted to marine and terrestrial habitats b) most studies find that lower limit set by biotic interactions, but… c) exceptions: - Littorina (snail) 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!!!! mid lower zers lgae gra a ose foli Silvetia compressa 3 II. Horizontal patterns of distribution and abundance Fucus vesiculosus Semibalanus balanoides 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)
b) System: barnacles, mussels, algae, predatory snail in New England rocky intertidal Competition and predation are important in determining these patterns, but ii)
Importance of competition and predation differ in exposed and protected sites c) Patterns: along a gradient from exposed to protected sites… e) Specific hypotheses (experimental design): CHARACTERISTIC EXPOSED SHORE PROTECTED SHORE Dominated by Mussels Fucoid algae Free Space Rare (<10%) Common (40-90%) i)
Predators/Grazers Uncommon (16-80/m2) Common (108-450/m2) ii)
predation / grazing Barnacle Cover Low Low iii)
exposure: importance and how it varied along gradient Complicated design using cages and cage controls to assess effects of: competition: barnacles, mussels, and algae iv)
all areas initially cleared f) Results: Exposed Shores Mussels Open (-Fucus) Barnacles Mussels Cage (-Fucus, -predators) Cage (-Predators, -grazers) Barnacles Barnacles Algae (Fucus) Time Fucus Time Time Cage (-Fucus, -predators, -mussels) Cage (-Fucus, -predators) Cage (-Predators, -grazers) Mussels Barnacles Mussels Barnacles Mussels Time Time Open (-Fucus) Algae (Fucus) Mussels Barnacles Mussels Control (no manipulation) Abundance Abundance Control (no manipulation) f) Results: Protected Shores Cage (-Fucus, -predators, -mussels) Barnacles Barnacles Mussels Fucus Time Time Time Time Time At protected sites - effects of predators At exposed sites - same pattern for cages with Fucus and predator removals and Fucus removals (open areas) a) barnacles colonize then are out-competed by mussels (no additional effect of predators: see open areas) b) If mussels are removed then barnacles persist - pattern is similar to that in protected shores a)
mussel abundance is kept low by predators, allowing barnacles to colonize and persist in low numbers outside of cages b)
without predators, barnacles are out-competed in cages by mussels 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: Different processes are important at exposed and protected sites: a) at exposed sites -- predation/grazing unimportant - competition is the primary organizing force in the system 1.
predators are generally uncommon 2.
mussels are competitively dominant (over algae and barnacles) b) at protected sites -- predation important h) More generally: General paradigm of community organization in rocky intertidal (Connell 1975, Menge and Sutherland 1976, Menge 1976, Lubchenco and Menge 1978, Underwood and Denley 1984) Predation High Competition Physical Processes Importance to community organization Low Benign Severe Environmental harshness 1.
with predation, barnacles dominate if Fucus is removed 2.
without predation mussels out-compete barnacles and algae 3.
predation keeps competition from occurring with mussels (mussel abundance is kept low) c) Importance of predation varies with exposure; at exposed sites predators are uncommon, their feeding ability is reduced because they have to spend more time hanging on and not feeding •
in habitats with relatively benign physical environments - predation structures communities •
with increasing environmental harshness - predation efficiency is decreased and competition becomes a major process structuring communities •
with even greater environmental harshness - importance of competition decreases and physical processes become most important •
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) Background: Why might sites exhibit different stable communities in the absence of environmental differences? a) Question: Why might sites exhibit different stable communities in the absence of environmental differences? b) System: grazing snail and algae in New England rocky intertidal b) System: grazing snail and algae in New England rocky intertidal c1) Patterns: spatial variation in community structure: c1) Patterns: spatial variation in community structure: Chondrus crispus Habitat Tidepools Tidepools Tidepools Rock Rock Rock Enteromorpha Littorina littorea Littorina common intermediate rare common intermediate rare Enteromorpha rare intermediate common rare rare uncommon Chondrus/Fucus common intermediate rare common common common Diversity low high low low intermediate high Fucus vesiculosus c2) Patterns: spatial variation in species diversity varies as a function of grazer density and habitat type: d) Hypotheses: i) Littorina prefers to eat Enteromorpha Tidepools ii) Enteromorpha out-competes other algae in tidepools (if no Littorina) Rock (emergent) High iii) Littorina can suppress competitive abilities of Enteromorpha in tidepools iv) Enteromorpha is competitively inferior on emergent rock surfaces Diversity Diversity High Low Low Low High Low Littorina density Higher Littorina density e) Study Design: Why might sites exhibit different stable communities in the absence of environmental differences? i) assessed food preferences of Littorina ii) manipulated density of Littorina in pools f) Results: Lubchenco 1978 i) Enteromorpha are favored food of Littorina (in pools and on rock) ii) patterns from pools… Chondrus High Littorina removal (common before) High Chondrus Low Chondrus Low Time Tidepools Rock (emergent) High Enteromorpha Time the subordinate competitor) Enteromorpha Enteromorpha Low (by eating the dominant competitor) 2.
on emergent rock surfaces, Littorina reduces algal diversity (by eating Time Pools 1) Enteromorpha can out-compete Chondrus, but… 2) high densities of Littorina can suppress effects of Enteromorpha 3) intermediate densities of Littorina allow coexistence of most species 4) Littorines are a keystone species but maximum effect on diversity occurs at intermediate densities Rock 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 High Diversity High Littorina addition (rare before) 1.
in tidepools, intermediate densities of Littorina increase algal diversity Diversity Percent Cover Control (Littorina common) Results Summary Low Low Low High Littorina density Low Higher Littorina density 5