Multiple-species interactions

Left: Image from Wikimedia Commons of one of the earliest known depictions of a food web, by Victor Summerhayes & Charles Elton (1923) for Bear Island, NorwayRight: Provenance of “A simplified food web for Northwest Atlantic” unknown

Trophic (energy & nutrition) relationships among organisms

LinksFlow of material (including

energy-rich molecules)

NodesTaxonomic or functional categories

Paine, R. T. (1966) – Food webs are the “ecologically flexible scaffolding

around which communities are assembled and structured”

Food Webs

Provenance of image unknown

Pyramid could represent numbers,

biomass, energy consumed per year,

etc.

Elton’s hypothesis: Predators must be larger than prey to subdue them

Image from http://mrskingsbioweb.com/ecology.html

Elton (1927) observed that predators tend to be larger & less numerous than their prey – “pyramid of numbers” (a.k.a. “Eltonian pyramid”)

Food Webs

Food Webs

Inverted pyramids of biomass can occur (e.g., whales, krill, phytoplankton in southern oceans), but only when productivity and turnover of producers is extremely high

Lindeman (1942) introduced the “energy-efficiency hypothesis” – the fraction of energy entering one trophic level that passes to the next higher level is low (~ 5 - 15%)

The first and second laws of thermodynamics predict inefficiency:

1st Law = Conservation of Energy

2nd Law = Energy transformations result in an increase in entropy, i.e., only a fraction of the energy captured by one trophic level is available to do work in the next

“Green” or livingfood web

“Brown” or detrital food web

1 Producers

1 Consumers

2 Consumers

1 Consumers

2 Consumers

Trophic levelswithin a simple

food chain;donor levels

supply energy or nutrients to

recipient levels

Levin, S. A. (1992) – “Is a taxonomic subdivision most appropriate… would a functional one serve better? Should subdivision… consider different demographic classes, be partitioned according to genotype, etc.?”

Food Webs

Web jargon:

Connectance (c): Number of links (L) or connections between species (S) or nodes – expressed as a proportion of maximum connectance:

c = L / [S(S-1)/2]Maximum connectance = S(S-1)/2

Linkage density (L/S): Average number of trophic links per species

Compartmentation: Degree of isolation of subwebs – the number of species that interact with any given pair of species versus those that interact with only one member of the pair

Food Webs

Same-chainomnivory

Web jargon:

Omnivory: Feeding on more than one trophic level

Different-chainomnivory

Food Webs

4

3

2

1

4

3

2

1

3’

2’

1’

A B

A B

C

Web jargon:

Cycles & loops: Species have reciprocal feeding relationships

Cycle E.g., wasps that prey

on spiders that in turn catch wasps in their webs

Loop E.g., “rock-paper-scissors” interactions among plankton (see Huisman refs.)

Food Webs

1

2

3

4 1 2 3 4

1 - - 0 0

2 + 0 - 0

3 0 + 0 -

4 0 0 + 0

0 = no connection / no interaction+ = positive effect; prey supplying energy to predator- = negative effect; predation

Values corresponded to interaction strengths

May (1973) and Pimm & Lawton (1977, 1978) used multispecies Lotka-Volterra models to examine various configurations for stability

Modeling food webs:

Which food web configurations promote stable equilibria?

Food Webs

Food Webs

Simulations generally examine the influence of small changes in predator & prey populations away from equilibria

Two criteria for assessing stability:

Do populations return to equilibrium sizes?

How long does the system take to return to equilibrium?

The way in which the matrices are constructed (e.g., lengths of food chains, connectedness, etc.) determines stability

Do real-world food webs yield repeated patterns? If so, do the patterns have ecological significance?

Food Webs

Are ratios of species at different trophic levels constant across communities?

This may simply reflect greater lumping into functional groups for prey than predators

Cohen (1978) reviewed published community webs – relatively high consistency of predators to prey (4:3)

How long are food chains?

As expected, relatively short; rarely more than 5 trophic levels (Pimm & Lawton 1977; Pimm 1982)

Invertebrate ectotherms vs. vertebrate ectotherms vs. vertebrate endotherms at trophic level 2

Energy-conversion efficiency:

invert. ectotherms > vert. ecototherms > vert. endotherms (invert. ectotherms are about an order of magnitude more efficient than vert. endotherms)

Percent of chains supporting consumer(s): 23% > 9% > 6%

invert. ectotherms > vert. ecototherms > vert. endotherms

Food Webs

How long are food chains?

Yodzis (1984) – meta-analysis of 34 published food webs (Briand 1983) to examine the influence of energy efficiency on food-chain length

Natural tree-holes contain 4-level trophic chains: litter -- mosquito larvae -- larvae of predatory midge -- tadpoles

Litter at 100% natural level (938 g/m2/yr), 10% natural level, 1% natural level

Well-replicated study tracked for 48 wk

If efficiency of energy transfer primarily determines food chain length, then manipulating productivity should influence food chain length

Plastic buckets in an Australian forest to resemble water-filled tree-holes with different amounts of litter to generate a productivity gradient

Food Webs

How long are food chains?

Jenkins et al. (1992) – direct test of the energy-efficiency hypothesis

Food Webs

Figure from Jenkins et al. (1992)

How long are food chains?

Jenkins et al. (1992) – direct test of the energy-efficiency hypothesis

Decreased productivity resulted in decreased number of coexisting species & decreased number of trophic levels & links

Polis (1991) – a skeptic of food web theory – characterized desert food webs in great detail

Two-species cycles and three-species loops occur, and are especially common in communities characterized by size-dependent predation

Role reversals between predators and prey are not uncommon

Omnivory is quite common

Food Webs

Modeling suggested that cycles, loops, and omnivory would destabilize food webs

Do cycles and loops occur in nature?Is omnivory common?

Unlike the randomly defined interaction strengths of the earliest modeling approaches, interaction strengths are not normally distributed; they are heavily skewed toward weak interactions

“…weak interactions may be the glue that binds natural communities together” (McCann, Hastings & Huxel 1998)

This shows that evaluating interaction strength (of combined direct & indirect effects) and not merely trophic links is essential to understanding population dynamics and stability within food webs

Interaction Webs

The distribution of interaction strengths is very important for determining modeling outcomes

How are interaction strengths distributed in nature?

Dissecting exploitation competition reveals its indirect nature

H

-

P

Solid arrows indicate direct effects, dotted arrows indicate indirect effects

-+ +

- H

Direct & Indirect Effects

Redrawn from Menge (1995)

Dissecting the ant-acacia mutualism reveals its indirect components

ant

-

P

Solid arrows indicate direct effects, dotted arrow indicates indirect effect

-+ +

-

Direct & Indirect Effects

As consumers, ants have direct negative effects on acacias (eating Beltian bodies, etc.), but indirect positive effects mediated through herbivores

H

+

P

Apparent Competition

H

Tri-trophic Interactionor Trophic Cascade

-

P

Solid arrows indicate direct effects, dotted arrows indicate indirect effects

-++

-

H

P

C

- +

- +

++

Direct & Indirect Effects

Redrawn from Menge (1995) & Morin (1999)

P

H

-

P

Solid arrows indicate direct effects, dotted arrows indicate indirect effects

++

-

KeystonePredation

HabitatFacilitation

H

P

-+ - (e.g., inhibits

feeding)

+H

Direct & Indirect Effects

Redrawn from Menge (1995) – found 83 distinct types of indirect interactions in 23 communities

IndirectMutualism

P

-

P

+

-

H + H

+ -

Direct & Indirect Effects

Figure modified from Wootton (1993)

Interaction chain indirect effect – results from “linked direct interactions”(e.g., bird predators enhance barnacle abundance b/c they consume limpets that dislodge & sometimes consume barnacles); relatively predictable from the direct interactions

bird

bird

limpet

limpet

barnacle

barnacle

Interaction modification indirect effect – “a third species changes how a pair of species interacts;” the third species changes the per capita effect of one species on another (e.g., when barnacles are present, limpets are harder for birds to find); difficult to predict a priori

Direct & Indirect Effects

Werner & Peacor (2003)

Density-mediated indirect interactions– “indirect effects… propagated by changes in densities of intervening species” e.g., “keystone predator effects, trophic cascades, and exploitative competition… [as] traditionally conceived”

Approx. the same as interaction chain indirect effect

Trait-mediated indirect interactions– “If a species reacts to the presence of a second species by altering its phenotype [phenotypic plasticity], the trait changes in the reacting species can alter the per capita effect of the reacting species on other species…”

Approx. the same as interaction modification indirect effect

Experiment: Continually transplanted bivalves to maintain high densities of bivalves in sites with high densities of gastropods

Prediction (if apparent competition operates): Predator density will increase, gastropod density will decrease

Direct & Indirect Effects

Apparent competition (an example from Schmitt 1987)

Prey species: Sessile bivalve filter feeders occur mostly in crevices

Gastropods occur on rock surfaces and graze algae

(Limited opportunities for direct competition, since neither diet nor space requirements overlap greatly)

Common predators: Lobsters, octopi, whelks

P

Apparent competition

C

-

P

-++

-

Control sites

Sites with added bivalves

Direct & Indirect Effects

Figure modified from Schmitt (1987)

Apparent competition (an example from Schmitt 1987)

Found increased predator density and decreased gastropod density when bivalves were added relative to control sites

Direct & Indirect Effects

Menge (1995) reviewed 23 experimental studies of rocky intertidal habitats that were sufficiently well replicated and long enough in duration for indirect effects to become evident

Considered only “ecologically significant” effects (that caused at least a 10% change in the abundance of one or more species)

How important are indirect effects?

Found that 83 types of indirect effects accounted for 40% of the observed changes in community structure caused by manipulations (e.g., predator or prey removal)

Most of the indirect effects were cases of keystone predation (35%) and apparent competition (25%)

Exploitative competition constituted only 3% of indirect effects!

Bottom-Up vs. Top-Down

Are abundances or distributions of organisms controlled by resources (bottom-up processes) or by predation & disease (top-down processes)?

Bottom-up view: Organisms at each trophic level are food limited

Top-down view: Top level is food limited, lower levels are alternately predator vs. food limited (originated with Hairston, Smith & Slobodkin 1960 – HSS)

Trophic cascade

H

P

C

- +

- +

++

Are Trophic Cascades “All Wet”?

Polis (1991), Strong (1992) & etc. argued that the idea of discrete trophic levels, which trophic cascades are predicated on, is invalid b/c of the prevalence of omnivory

Strong (1992) posed the question above, in part b/c omnivory appeared more prevalent in terrestrial communities (making trophic cascades more likely in aquatic communities)

Photo of Gary Polis from http://science.marshall.edu/fet/euscorpius/images/polis.JPG

A likely example of a terrestrial trophiccascade (McLaren & Peterson 1994)

500 km2 Isle Royale National Parkin Lake Superior

Primary producer: Balsam fir

Herbivore: Moose (59% of winter diet is Balsam fir)

Carnivore: Wolf (colonized island in 1959)

A Terrestrial Trophic Cascade

Photo of Isle Royale from Wikipedia

Figure from McLaren & Peterson (1994)

McLaren & Peterson (1994):

“The shaded areas highlight intervals of forage suppression

that… are closely tied to periods of elevated moose density, which in

turn follow periods of low wolf density (note the lags…)… these intervals have no correspondence

to AET [climatic fluctuations]”

A Terrestrial Trophic Cascade

A change in behavior of a top predator cascades through a community (Post et al. 1999)

On Isle Royale, fluctuations in North Atlantic Oscillation (NAO) result in changes in winter snow accumulation

Annual aerial surveys show close correlation between wolf pack size and the status of the NAO

Photo of winter wolf pack (in Yellowstone National Park) from Wikipedia

A Terrestrial Trophic Cascade

Figure from Post (1999)

Post (1999):

“a, Increase in the mean size of wolf packs in snowy (negative

NAO) winters…”

“b, Increase in the winter kill rate of wolf packs with pack size… kill rate per individual wolf also

increased during snowy winters”

“c, Decline in moose density one year after increase in size of winter

wolf packs”

“d, Increased growth of fir trees one year after decline in moose density” [notice reversed x-axis]

A Terrestrial Trophic Cascade

Changes in wolf behavior have ecosystem-level effects on Isle Royale because moose dramatically influence net primary production, litter

production & edaphic nutrient dynamics (Post et al. 1999)

Photo of moose from Wikipedia

A Terrestrial Trophic Cascade

Bottom-Up vs. Top-Down

Hunter and Price (1992) – we should always start with a bottom-up template: “the removal of higher trophic levels leaves lower levels present (if perhaps greatly modified), whereas the removal of primary producers leaves no system at all”

Echoed in John McPhee’s (1998) Annals of the Former World, pg. 84: “Break the food chain and creatures die out above the link”

Fretwell (1977) & Oksanen et al. (1981) – OFAN – proposed a reconciliation: productivity determines the number of trophic levels that can be supported in a community; plant productivity therefore ultimately dictates when top-down forces could cascade back down

In general the top-down vs. bottom-up question applies to NPP, but in principal could be asked of a variety of variables at a variety of

trophic levels.

Foundation Species

Photo from Wikipedia; definitions from Ellison et al. (2005)

Figure from Whitham et al. (2008)

“Foundation Genotypes”

Keystone predator – a predator whose activities maintain species diversity at lower trophic levels by disallowing competitive exclusion (Paine 1966)

Keystone resource – first applied to plant species that sustain frugivores through periods of food scarcity in tropical forests, e.g., figs (Terborgh 1986)

Keystone Species

Photos from Wikipedia

Pisaster eating mussel

Barbet eating fig

An ecosystem engineer has a large impact beyond simply assimilating and dissimilating material

The definition is especially useful when applied to organisms that modify the environment through means other than trophic activities

Ecosystem Engineers

Photo of Clive Jones from Cary Institute of Ecosystem Studies

Ecosytem engineer – an organism that creates, modifies, or maintains habitat (or microhabitat) by causing physical state changes in biotic or abiotic materials that, directly or indirectly, modulate the availability of resources to other species (Jones et al. 1994)

Ecosystem Engineers

Photo of beaver dam on Tierra del Fuego from Wikipedia

Allogenic ecosystem engineer – organism that changes the environment by transforming living or nonliving materials from one physical state to another, via mechanical or other means (Jones et al. 1994)

E.g., Beaver

Ecosystem Engineers

Autogenic ecosystem engineer – organism that changes the environment via its own physical structures, i.e., living & dead tissues (Jones et al. 1994)

E.g., Long-leaf pines

K. Harms’ photo of Pinus palustris at Camp Whispering Pines, Tangipahoa Parish, LA

Assembly Rules

Photo of Jared Diamond from Wikipedia

Diamond (1975) coined the term for broad patterns of bird species distributions in the Bismark Archipelago & Solomon Islands

Wilson & Whittaker (1995; pg. 801): “generalised restrictions on species presence or absence that are based on the presence or absence of one or several other species, or types of species (not simply the response of individual species to the environment)…”

Connor & Simberloff (1979) kicked off a long and continuing debate about assembly rules and testing for them

E. Weiher (quoted in Stokstad’s piece in Science, 2009, v. 326, pg. 34):“I think what we’re going to find out is that assembly rules are vague, gentle constraints”

Priority Effects

Petraitis et al. (2009) provide an experimental example of priority effects and multiple stable states in the Gulf of Maine

Ice scour can create open patches; experiments mimicked these disturbances (rockweed stands cleared in 1996 and followed through 2005)

In sheltered bays, rockweed stands or mussel beds established, depending on which arrived first, and were not invaded by the other species

Figure from Petraitis et al. (2009)

As required by Peterson (1984) to establishmultiple stable states, “the very same site could come to be occupied by different, self-replicating communities”

Community Assembly / Coalescence

From: J. N. Thompson et al. 2001. Frontiers of Ecology. BioScience 51:15-24.

“We use the term community coalescence to refer to the development of complex ecological communities from a regional species pool. This coalescence depends on interactions among species availability,

physical environment, evolutionary history, and temporal sequence of assembly.”