Consequences of genetic and species diversity for the functioning and resilience of marine systems Jay Stachowicz, University of California Davis
Marine ecologists have long studied the effects of ecosystem processes on the maintenance of species diversity Nutrient availability Productivity Substrate heterogeneity Species diversity Consumer pressure Disturbance/ stability But have been slower to assess reciprocal links whereby (species) diversity alters ecosystem processes
What are the consequences of biodiversity change for marine systems? Human Society Impacts Marine biodiversity Genetic Species Ecosystem Linkage? Marine ecosystem functions Carbon and nutrient cycling Primary and secondary productivity Food and habitat provision Transformation of waste products Linkage? Marine ecosystem services Climate control Water quality control Seafood production Tourism and recreation Benefits
The lost functions of biodiversity must be replaced somehow When a species vanishes, the world loses not only that species, but the wide range of highly specialized physical and biochemical functions that species served. These ecological losses necessitate the creation of new, synthetic products capable of serving the same function. So, for example, when we lose a strain of microbe that filters the water we drink, we compensate by developing the amazing Brita water filter, with its patented filtration technology. When we lose a plant in the jungles of Indonesia whose berry bears an extremely rare nutrient, we develop in its place fruity, fun-to-eat Flintstones chewable vitamin supplements." Attributed to David Quammen The Onion, November 1998
What do we mean by Biodiversity?? Phenotypic diversity Order and higher Functional Group or Trophic Level Family Genus Species Which kinds of diversity matter? Which kinds of diversity are changing, and how? Genetic variation between populations Genetic variation within populations Phenotypic plasticity
Outline: How does diversity change at various levels really matter? (a biased, but illustrative selection of studies) 1. Terrestrial analogs: sessile species diversity effects on ecosystem production and invasion resistance 2. What happens when communities are dominated by a single species? does genetic diversity matter? 3. Real diversity loss often involves higher order consumers. How does changing food web structure affect function?
Potential mechanisms underlying diversity effects on biomass accumulation Resource utilization efficiency Low diversity = Low productivity, high resource availability Resource state Resource utilization efficiency Resource state High diversity = High productivity low resource availability complementarity Resource utilization efficiency Resource state High sp. richness = High productivity because of a sampling effect
Why might diversity enhance the capacity of a system to tolerate disturbance without shifting to an alternate state)? 1. Species redundancy: Diversity provides insurance against stochastic loss of species (diversity as a spare tire) 2. Species complementarity (based on niche partitioning): a. Species differ in their tolerances to environmental stresses and thus respond differently to perturbations b. Species differ in their effects on ecosystem processes such that increasing diversity fundamentally changes ecosystem states
Drought resistance (db/bdt/ yr -1 ) Effects of species richness on ecosystem processes in grasslands Hector et al. 1999 Tilman and Downing 1994 Plant species richness before drought
An algal mosaic on midhigh intertidal benches in California
Pelvitiopsis limitata Endocladia muricata Cladophora columbiana Mastocarpus papillatus *These 4 species comprise >85% of total algal cover
Cladophora (6 treatments x 12 reps = 72 plots) Endocladia Mastocarpus Pelvetiopsis 1.5 m
Quarterly (July 2004 - present): -weeding to remove non-target species in monocultures; -removal of an equivalent biomass of all species from polycultures to control for disturbance -percent cover of all algae and sessile inverts -abundance of sessile and mobile invertebrate in four 25 x 25 cm subquadrats
-This result is contrary to some mesocosm studies of marine algae (which lack environmental heterogeneity). In an even moderately heterogeneous environment no one algal species can perfectly compensate for the loss of others. Resource utilization efficiency Mesocosm: no heterogeneity Field: high heterogeneity Resource spectrum
Diversity and invasion resistance in suspension feeding invertebrate communities
Survival, recruitment and percent cover of invaders decline with increasing native community diversity Botrylloides Ascidiella.9.8 R 2 =.792 R 2 =.628 survival of invaders.7.6.5.4.3.2.1 0 0 1 2 3 4 0 1 2 3 4 # of native species Stachowicz et al. 1999 Science, 2002 Ecology
. The mechanism lies in differences in the natural history of each species (temporal niches) native species abundance 1 - Species system total unoccupied space Percent cover 2 - Species system 3 - Species system More diverse communities are buffered against the loss (or decline) of individual species Time Time
More diverse communities have less space available, and are more consistent in their use of space over time Unoccupied space (% ) 80 60 40 20 1 species 2 species 3 species 4 species 0 20 30 40 50 60 70 Duration of experiment (days) More diverse communities experience smaller fluctuations in limiting resources.
Exotic Species Richness 2.5 2 1.5 1.5 Experimental results agree with field patterns Field Survey from Poquonnock River, CT Quadrat scale (.25 x.25m) R 2 = 0.42 3.5 3 2.5 2 1.5 1.5 Site scale (50 x 50m) R 2 =.592 0 0 2 4 6 8 10 12 14 0 4 6 8 10 12 14 16 18 20 Native Species Richness Stachowicz et al. 2002 Ecology
Sessile marine species often show similar effects of diversity as found in terrestrial studies, with diversity enhancing function -intertidal algal communities due to microniche preferences of species that preclude compensation -sessile invertebrate communities due to temporal niche partitioning In both cases, a long term, field-based approach or one in which realistic heterogeneity is incorporated are required for diversity effects to emerge Tilman 2001, Science
So diversity can matter, but do these principles apply to the types of diversity changes that are actually occuring, or the types of natural gradients in diversity that exist? 1.Consequences of higher trophic level diversity loss 2.Genetic diversity of dominant or keystone species Functional Group or Trophic Level Family Genus Species Genetic variation between populations Genetic variation within populations Phenotypic plasticity
Predators are important, but what about predator diversity? Southern California Kelp Forest Graham 2004 Ecosystems
Otters present Otters absent
trophic cascades result from local otter extinction in AK but not in So Cal Humans Otters (1) Pred. fishes Lobster Otters (1) Urchins (1) Crustaceans (2) Urchins (3) Herb. Fishes (4) Kelp (3) ALASKA Kelp (8) California Does predator diversity affect the strength of top-down control?
Field Survey Data from Channel Islands Kelp Forest Monitoring (1986-2004) 8 7 6 p=0.008 r 2 =0.407 5 4 3 2 1 Byrnes et al. 2006 Ecology Letters 0 0.5 0.7 0.9 1.1 1.3 1.5 Predator Diversity (Shannon-We
Patterns consistent with the idea that diversity strengthens cascades 90 80 70 60 p=0.0506 r 2 =0.246 50 40 QuickTime and a TIFF (Uncompressed) decompressor are needed to see this picture. 30 20 10 0 0.5 0.7 0.9 1.1 1.3 1.5 Predator Diversity (Shannon-We 8 7 6 p=0.0232 r 2 =0.316 5 4 QuickTime and a TIFF (Uncompressed) decompressor are needed to see this picture. 3 2 1 0 0 10 20 30 40 50 60 70 80 90 Herbivore Abundance (# per sq. m
Experimental manipulation of the Bodega Harbor kelp bed food web Cancer productus Cancer magister Pycnopodia helianthoides Pugettia producta Tegula brunnea T. funebralis Strongylocentrotus purpuratus S. franciscanus
Experiment: Hold predator biomass constant but vary species richness No predators 1 Species X 3 or X 3 or 3 Species X 3 n=6 n=6 per species n=8
Predator diversity maintains kelp biomass Change in Kelp Mass (g) 50 0-50 -100 p=0.0004 Predator Diversity r 2 =0.39 3 0 1 2 3-150 -200 Byrnes et al. in press, Ecology Letters
Predator diversity does not affect herbivore death rate
Does Predator Diversity Alter Herbivore Behavior? X 3 or X 3 or X 3 n=6 n=6 per species n=8
Predator diversity reduces herbivore feeding rates Change in Kelp Mass (g) -15-20 -25-30 -35-40 p=0.024 r 2 =0.36 0 1 2 3 Predator Diversity -45-50
Individual predator species have no effect on total herbivory 20 10 Change in Kelp Biomass (g) 0-10 -20-30 -40-50 No Predators C. magister Pycnopodia C. productus Polyculture No Herbivores
Behavioral complementarity Change in Kelp Mass (g) 15 10 5 0-5 -10-15 -20 Pugettia c bc c ab bc a -25-30 -35 No Predators C. magister Pycnopodia C. productus Polyculture No herbivores Change in Kelp Mass (g) 8 4 0-4 -8-12 S. purpuratus c c ab c b a -16 No Predators C. magister Pycnopodia C. productus Polyculture No herbivores
These effects are not found in all systems Decrease Herbivory, Increase producer biomass 1) facilitation among predators 2) complementarity (different predators affect different prey) 3) reduction of intraspecific competition Predator A Herbivores Predator B Increase Herbivory Decrease Plant biomass 1) intraguild predation (Finke and Denno, 2003, 2006: Spartina insects) 2) predator emigration 3) change in predator behavior Plants 4) omnivory (Bruno and O Connnor 2005 subtidal algal community)
3 lessons about diversity from kelp forest studies Diversity can buffer kelp forests both through redundancy and complementarity The guild of invertebrates is redundant to sea otters but both crabs and seastars are needed to compensate for the loss of otters because of their complementary effect on herbivores.
Effects of diversity at a given level depend on diversity at other levels Predator diversity only important when there is a diversity of herbivores Predatory Crabs would be Unimportant if kelp crabs were absent
Effects of diversity at a given level depend on diversity at other levels QuickTime and a TIFF (Uncompressed) decompressor are needed to see this picture. Increasing herbivore diversity could decrease the strength of trophic cascades) by increasing the likelihood of their being at least one herbivore that is unaffected by available predators.
Predator diversity and foundation species abundance are interconnected QuickTime and a TIFF (Uncompressed) decompressor are needed to see this picture. 8 7 6 5 4 3 2 1 0 0.5 0.7 0.9 1.1 1.3 1.5 Predator Diversity (Shannon-We
Many communities are dominated by single, important species QuickTime and a TIFF (Uncompressed) decompressor are needed to see this picture.
Why eelgrass? High primary and secondary production Also: Nutrient cycling Sediment stabilization Buffers eutrophication Photos by S. Williams and F. Short
Diversity need not be just at the species level. Create plots that vary in genotypic richness (1-8 / m 2 ) Functional diversity can occur at any level of biological organization: species may be redundant or species may have multiple complementary phenotypes Eelgrass, Zostera marina Use microsatellite DNA to identify distinct clones
Small-scale genotypic diversity 20 18 16 14 Observations 12 10 8 6 4 2 0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Number of genotypes / m 2 Mean = 4.1; Median = 3.0
Shoot density over time 400 350 300 250 200 150 100 50 0 7/13/02 7/27/02 8/10/02 8/24/02 9/7/02 9/21/02 10/5/02 10/19/02 11/2/02 11/16/02 11/30/02 12/14/02 12/28/02 1/11/03 1/25/03 2/8/03 2/22/03 3/8/03 3/22/03 4/5/03 4/19/03 5/3/03 5/17/03 5/31/03 6/28/03 6/14/03 7/12/03 Number of shoots / m 2 2002 Date 2003 1 genotype 2 genotype 4 genotype 8 genotype Significant No strong loss effects of of shoots diversity during on shoot December density, epiphyte (Month 5) or invertebrate abundance, or porewater ammonium.
What we didn t t know at the start of the experiment:
Shoot loss: Grazing by geese BEFORE (December 2002) AFTER (January 2003)
Genotypically more diverse plots are more resistant and recover faster from perturbation % Shoots Remaining in postgrazing 75 65 55 45 35 R 2 =.635 P=0.04 1 2 4 8 # of unique genotypes Weeks to Recovery 23 21 19 17 15 1 2 4 8 # of unique genotypes Hughes and Stachowicz 2004, PNAS
Other possibilities: differential grazing tolerance among genotypes or shoot-shoot interactions? Clonemates (i.e., monoculture) Non-clonemates (i.e., polyculture) Compare: shoot:root ratio, # of shoots, etc.
Non-clonemates tend to allocate more biomass to roots -increased survival when aboveground biomass is removed? -decreased likelihood of uprooting by browsing geese? Shoot:root ratio (g) 6.00 5.75 5.50 5.25 5.00 4.75 4.50 4.25 4.00 3.75 3.50 3.25 Clonemates p = 0.09 (currently re-doing with greater replication) Non-clonemates Who cares? If true, it suggest that it may not matter which combinations of genotypes are included, just diversity itself is important.
After disturbance, more diverse plots were more similar to the pre-disturbance condition. Disturbance Shoot density Epiphyte biomass Genetic diversity Tested link, not significant Tested link, significant Invertebrate abundance Porewater [NH 4+ ] Sexual reproduction Diversity may commonly buffer communities against environmental perturbations (invasions or disturbance), having an overall stabilizing effect on ecosystem functions.
Stock diversity buffers against salmon fishery collapse because of locally adapted populationsthat differ in response to environmental change Hilborn et al. 2003, PNAS
Nature 2000
Prochlorococcus
Summary: What do we know about the consequences of variation in marine diversity for ecosystems? Sessile species diversity often show similar effects as found in terrestrial systems-- mechanisms generally applicable Genetic diversity within key species reduces community susceptibility to disturbance, providing biological insurance Predator diversity may help maintain control of herbivores and reduce overgrazing of kelp by altering herbivore behavior Diversity may commonly buffer communities against perturbation, having an overall stabilizing effect on ecosystem functioning.
Future direction # 1: Diversity manipulations that reflect realistic changes currently being experienced by food webs -Simultaneous investigation of change at many trophic levels -Not just diversity loss (quantitative) but diversity CHANGE, qualitative and quantitative -65.1% -24.6% +50.0% -3.3%
Future Direction #2: How do the feedbacks between diversity and ecosystem level processes play out? Nutrient availability Productivity Substrate heterogeneity Species diversity Consumer pressure Disturbance/ stability
Humans directly affect both ecosystem processes and diversity Productivity (Tilman et al 2001 Science) Diversity Intermediate Dist. Hypothesis Hughes and Stachowicz (2004) Diversity Disturbance disturbance # of genotypes
Future Direction #3: Adopting correlative approaches to complement experiments [Even Tilman manipulated only 32 species of plants] Worm et al, unpublished
My lab: Randall Hughes, Jarrett Byrnes, Kristin Hultgren Suzanne Olyarnik, Carol Thornber Matt Bracken Marie Nydam Cameron Coates Kris Aquilino Kyle Edwards Ambre Chaudoin Kirsten Sellheim Jonathan Schram QuickTime and a TIFF (Uncompressed) decompressor are needed to see this picture. Other Collaborators: Bob Whitlatch, Rick Osman, Emmett Duffy Mike Graham John Bruno Funding: NSF Biological Oceanography, CT Sea Grant, National Sea Grant, NCEAS
Letters: Relation Between Diversity and Stability, in the Real World References and Notes: 1. R.M. May, Stability and Complexity in Model Ecosystems (Princeton Univ. Press, Princeton, NJ, 1973). Science 27 October 2000: Vol. 290. no. 5492, pp. 714-715 In 1973, there was a widely cited belief that more complex or diverse ecosystems--more species, richer webs of interrelationship--were thereby better able to resist disturbance. I showed that there was no such arbitrarily general rule. Quite the contrary: randomly constructed complex ecosystems are more likely to lose species after disturbance than are simple ones. But, I emphasized, "the balance of evidence would seem to suggest that, in the real world, increased complexity is usually associated with greater stability. There is no paradox here...the real world is no general system. Nature represents a small and special part of parameter space [shaped ultimately by evolutionary forces acting on individuals]" (1, p. 75). Sir Robert M. May Zoology Department, Oxford University, Oxford OX1 3PS, UK.
Distinguishing between complementarity and sampling (dominant species effects) productivity 1. Species complementarity 2. Sampling effect (presence of a key species) Species richness