How metabolic nichesshape marine life

Craig R. McClain Department of Biology, Triangle Center for Evolutionary Medicine, Duke University

@DrCraigMc craigmcclain.com

Veined Octopus (Amphioctopus marginatus) eating a crab

Life requires energy

carbon

C6 12.011

Species Physiological and EcologicalResponses and Adaptations

DIVERSITY

12

1900 2000

“We observe declines in eight out of ten ocean regions… this decline will need to be considered in future studies of marine ecosystems, geochemical cycling, ocean circulation and fisheries.”

Nature. 2010 Jul 29;466(7306):591-6.Global phytoplankton decline over the past century.Boyce DG, Lewis MR, Worm B.

Productivity of the oceans may be changing

1Patterns of diversity on the ocean floor Links to food availability

324 m (1063 ft)

36.5m (120 ft)

4500m, 2.8 miles, 14 Eiffel Towers

3%

The deep ocean are energy-deprived systems

McClain, C.R., J.Nekola, L.Kuhnz, and J. Barry (2011) Local-scale faunal turnover on the deep Pacific floor. Marine Ecology Progress Series, 442:193-200

YourNana’s QuiltPatterns of invertebrate diversity

Grandmother’s Quilt: Turnover At Small Spatial Scales 1a

Monterey

Santa Cruz

Deadwood3200m

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Distance: Rho= 0.05, p=0.076

Distance: Rho= 0.04, p=0.081

1 2.52

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2 2.68 6 3.22

7 2.29

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2D Stress: 0.10

2D Stress: 0.11

1 2.52

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Distance: Rho= 0.05, p=0.094% Carbon: Rho= 0.42, p=0.021

Distance: Rho= 0.06, p=0.078% Carbon: Rho= 0.31, p=0.036

MDS: a matrix of item–item similarities, then assigns a location to each item in N-dimensional space. Distance in plot correlates with differences in community composition

Cluster of cores

% Carbon in Sediment

Correlation and p-value for how well distance predicts relationship

Correlation and p-value for how well % Carbon predicts relationship

Station M. 4200m Pacific Abyssal PlainVideo from K. Smith and H. Ruhl

Pining for answers:Tests of energetic theory with experimental deep-sea wood falls

McClain, C.R. and J. Barry (2014) Beta-Diversity on Deep-Sea Wood Falls Reflects Gradients in Energy Availability. Biology Letters 10:20140129

McClain, C.R. et al. (2016) Multiple processes generate productivity-diversity relationships in experimental wood-fall. Ecology in press

1b

A very “poplar” question “fir” ecology: What are the processes that underly

diversity-productivity relationships?

Div

ersi

ty

Productivity

Invertebrates on wood falls are endemic and reliant on the wood as their only food source

Xylophaga

Invertebrates on wood falls are endemic and reliant on the wood as their only food source

Set 1

Set 2

November 2006-October 2011 (5 years)

November 2006-October 2013 (7 years)

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Dillwynella (Ganesa) panamesis

Protanais sp. nov.

H2: Relaxed pressure for optimal body size

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H5: Species-energy relationship within size classes

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2No Food No Cry:

Adaptations and Energetics of

marine invertebrates

What suites of traits make species low vs. high

energy adapted?

Species have an Energetic (Metabolic) Niche

Community ecology is comparative physiology

Energetics and metabolism structure communities

energy budget and energy adaptation views

energy resources are viewed as resource allocation that can be

translated into work and mass, e.g. the metabolic theory of ecology

Animals as machines

2aEnergy Budget: the energetics of life on the seafloor from individuals to ecosystems

McClain et al. (2012)The energetics of life on the deep seafloor. Proceedings of the National Academy of Science, U.S.A. 109:15366-15371

“Metabolism provides a basis for using first principles of physics, chemistry, and biology…Metabolic theory predicts how metabolic rate, by setting the rates of resource uptake from the environment and resource allocation to survival, growth, and reproduction, controls ecological processes at all levels of organization from individuals to the biosphere.”

B=b0*Mb*e-E/kTB = basal metabolic rate b0 = intercept (changes among clades & ecologies) M = mass b = scaling coefficient (2/3 or 3/4) E = activation energy (~0.65 eV) k = Boltzmann’s constant T = Temperature (˚K)

Brody 1945

Is the scaling of metabolism with body size stable over evolutionary time?

All Skeletonized only Anthozoa Articulata

Asteroidea Bivalvia Cephalopoda Cirripedia

Crinoidea Decapoda Demospongiae Echinoidea

Gastropoda Gymnolaemata Holothuroidea Inarticulata

Ophiuroidea Ostracoda Polychaeta Polyplacophora

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ahem…deep sea?

Body size and temperature through its control of individual metabolic rates sets the rates and sums of resource uptake from the environment

There are high and low metabolic demand deep-sea species

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Abundance Increases Lead to Diversity Increases on Wood falls

<aside>

Architeuthis dux Giant Squid

12m (39.37 feet) in length

</aside>

The caloric restriction hypothesis in the wild: energy budget or adaptation?2b

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• The Energetic Basis of Aging: An Evolutionary Perspective Working Group (August 2015)

• Test caloric restriction hypothesis in wild populations • Brings together 15 specialists on a variety of taxa, habitats, methods,

and disciplines • Link together

• global climate and productivity data • longevity data • phylogenetic relationships • comparative and spatial analyses

• Identify new model organisms, reveal underlying genetic mechanism

Maximum Age of Marine Invertebrates vs. Ocean Primary Production

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Alcyonaria

Amphipoda

Canalipalpata

Decapoda

Diptera

Euechinoidea

Heterodonta

Isopoda

Mysida

Neotaenioglossa

Oligochaeta

Ophiuroidea

Opisthobranchia

Prosobranchia

Protobranchia

Pteriomorphia

Scolecida

2c50 Shades of Food:Energy and reproductive adaptations

in marine gastropods

Planktotrophic: feed in the plankton during their larval stage and are considered to have longer dispersal potential

Lecithotrophic: larvae derive nourishment from yolk and are non-feeding and are considered to have longer dispersal potential

Direct: young develop directly into the adult form without a larval phase and typically have limited dispersal potential Low

Food

planktonic larvae cheap minimize larval/adult competition

dispersal phases allow for bet hedging

direct development expensive retention of larvae favored

High Food

% P

lank

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c La

rvae

McClain, C.R. et al. Proceedings of the Royal Society, B 2014

sqrt (Median Carbon Flux)

Probability o

f O

ccurrence

Mixed

Direct

Lecithotrophic

Planktotrophic

50 150 2500.0

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Planktotrophic: feed in the plankton during their larval stage and are considered to have longer dispersal potential

Lecithotrophic: larvae derive nourishment from yolk and are non-feeding and are considered to have longer dispersal potential

Direct: young develop directly into the adult form without a larval phase and typically have limited dispersal potential

McClain, C.R. et al. Proceedings of the Royal Society, B 2014

Low Food High

Food

% H

erm

aphr

odite

s

density low mate availability low

density high mate availability high

Abundance

Hyselodoris bennetti

McClain, C.R. et al. Proceedings of the Royal Society, B 2014

50 150 250

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Probability o

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ccurrence

Hermaphroditic

Non-Hermaphroditic

=

Basal metabolic rates of nudibranchs are the highest among gastropods.

Metabolically expensive to be a simultaneous hermaphrodite

McClain, C.R. et al. Proceedings of the Royal Society, B 2014

carbon

C6 12.011

Energy Budget(Response)

EnergyAdaptation

DIVERSITY

Future Research Directions

carbon

C6 12.011

Species Physiological and EcologicalResponses and Adaptations

DIVERSITY

Theoretically and conceptually link? Empirically document and test?

Theoretically and conceptually link? Empirically document and test?

1. Deep-Sea Biodiversity and Food Limitation • The role of food patchiness in driving deep-sea biodiversity • Experimental tests of productivity/diversity relationships • How energetic niches drive local scale diversity patterns

2.Metabolic controls of oceanic and global diversity gradients • How the strength of these relationships relates to the metabolic demand of the clade • How do metabolic controls impact phylogenetic, functional, and species diversity

patterns 3. Adaptations and tradeoffs in marine invertebrates in response to carbon variability

• The suite of physiological traits that makes species adapted to particular levels productivity

• Carbon availability and trophic adaptations 4. The evolution of metabolism

• Whether the relationship mass-scaling of metabolic rate has evolved through time? • What is the rate of the evolution? • Is the relationship constrained? • Whether there have been discrete transitions between alternate evolutionary optima?

Future Research Directions

Acknowledgements

• Collaborators: Jim Barry, Jeff Nekola, James Brown, Michael Rex, Andrew Allen, Derek Tittensor, Jon Payne, Josh Auld,

• Technicians: Linda Kuhnz, Patrick Whaling, Kurt Buck, Chris Lovera

• Undergraduates: Candace Leong, Mickie Ream, Taylor Gullet, Justine Jackson Ricketts, Ryan Filler

• Graduate Students: Meghan Balk

• Complete Sizing Ocean Giants Team

• Crews of the R/V Pt Lobos, R/V Western Flyer, ROV Tiburon, and ROV Ventana

National Evolutionary Synthesis Center

Monterey Bay Aquarium Research Institute