A talk examining how the energy requirements for life in the ocean impact evolution, ecology, and ultimately biodiversity. I examine this through the lense of both energy allocation and energy adaptation theory.

1. How metabolic niches
shape marine life
Craig R. McClain
Department of Biology, Triangle Center for Evolutionary Medicine, Duke University
@DrCraigMc
craigmcclain.com

2. Veined Octopus (Amphioctopus marginatus) eating a crab
Liferequires energy

3. carbon
C6 12.011
Species Physiological and Ecological
Responses and Adaptations
DIVERSITY
12

4. 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.
Productivityof the oceans may be changing

5. 1
Patternsof
diversity
on the ocean floor
Links to food availability

6. 324 m (1063 ft)
36.5m (120 ft)

7. 4500m, 2.8 miles, 14 Eiffel Towers

9. 3%
The deep ocean are energy-deprived systems

10. 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
Your
Nana’s Quilt
Patterns of
invertebrate
diversity
Grandmother’s Quilt:
Turnover At Small Spatial Scales
1a

11. Monterey
Santa Cruz
Deadwood
3200m

14. 1 2 3 4 5 6 7 8
350 m

15. : 0.25
4 2.75
2D Stress: 0.11
1 2.52
3 2.94
2 2.68
6 3.22
7 2.29
8 2.34
5 1.57
4 2.75
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

17. Station M. 4200m Pacific Abyssal Plain
Video from K. Smith and H. Ruhl

18. 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

19. A very “poplar” question “fir” ecology:
What are the processes that underly
diversity-productivity relationships?
Diversity
Productivity

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

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

26. Set 1
Set 2
November 2006-October 2011 (5 years)
November 2006-October 2013 (7 years)

28. −1.0 −0.5 0.0 0.5
−1.0−0.50.00.5
NMDS1
NMDS2
1
2
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0.3
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0.8
Species Composition Changes
Dillwynella (Ganesa) panamesis
Protanais sp. nov.

29. H2: Relaxed pressure for optimal body size
no.ofspecies
H3: Shifts in optimal body size
no.ofspecies
H5: Species-energy relationship within size classes
o.ofspecies
H1: Increased packing into optimal body size
no.ofspecies
H4: Mulitmodal distributions with increased rare resources
no.ofspecies
log10 body size classes
kurtosisvarianceaveragesize
wood-fall size (energy availability)
no.ofmodes
1
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7 1
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−2.1
−1.8
−1.5
−1.2
−0.9
0.0 0.5 1.0
MeanLog10BodySize
C
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0.0 0.5 1.0
StandardDeviationofBodySize
D
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−1
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0.0 0.5 1.0
Log10 Woodfall Weight
SkewnessofBodySizes
E
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−2.0
−1.5
−1.0
−0.5
0.0
0.5
0.0 0.5 1.0
Log10 Woodfall Weight
KurtosisofBodySizes
F

30. 2
No Food No Cry:
Adaptations and
Energetics of
marine invertebrates

31. 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

32. Animalsas machines

33. 2a
Energy 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

34. “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.”

35. B=b0*Mb*e-E/kT
B = 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

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

37. All Skeletonized only Anthozoa Articulata
Asteroidea Bivalvia Cephalopoda Cirripedia
Crinoidea Decapoda Demospongiae Echinoidea
Gastropoda Gymnolaemata Holothuroidea Inarticulata
Ophiuroidea Ostracoda Polychaeta Polyplacophora
−3
−1
1
3
5
−3
−1
1
3
5
−3
−1
1
3
5
−3
−1
1
3
5
−3
−1
1
3
5
−6 −4 −2 0 2 −6 −4 −2 0 2 −6 −4 −2 0 2 −6 −4 −2 0 2
Log10 Body mass (g AFDM)
Log10Respiration(Jind−1
d−1
)
0
10
20
30
Temp

38. ahem…
deep sea?

39. 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

41. 1
2
3
4
5
6
7
8
9
10
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32
35
5
10
15
20
1.5 2.0 2.5 3.0
Log10 Abundance
Richess
Set
a
a
1
2
Abundance Increases Lead to Diversity Increases on Wood falls

42. <aside>

43. Architeuthis dux
Giant Squid
12m (39.37 feet) in length

48. </aside>

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

51. -0.3
-0.2
-0.1
0
0.1
0.2
MassandTemperatureCorrectedLifespan
5 5.5 6 6.5
Log Depth (m)

52. • 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

53. Maximum Age of Marine Invertebrates vs. Ocean Primary Production
−1
0
1
2
3
6 7
log(primprod)
log(A_max)
Alcyonaria
Amphipoda
Canalipalpata
Decapoda
Diptera
Euechinoidea
Heterodonta
Isopoda
Mysida
Neotaenioglos
Oligochaeta
Ophiuroidea
Opisthobranc
Prosobranchia
Protobranchia
Pteriomorphia
Scolecida

54. 2c50 Shades of Food:
Energy and reproductive adaptations
in marine gastropods

55. 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
%PlanktonicLarvae
McClain, C.R. et al. Proceedings of the Royal Society, B 2014

56. sqrt (Median Carbon Flux)
ProbabilityofOccurrence
Mixed
Direct
Lecithotrophic
Planktotrophic
50 150 2500.00.51.0
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

57. Low
Food
High
Food
%Hermaphrodites
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

58. 50 150 250
0.00.51.0
sqrt (Median Carbon Flux)
ProbabilityofOccurrence
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

59. carbon
C6 12.011
Energy Budget
(Response)
Energy
Adaptation
DIVERSITY

60. Future Research Directions
carbon
C6 12.011
Species Physiological and Ecological
Responses and Adaptations
DIVERSITY
Theoretically and conceptually link?
Empirically document and test?
Theoretically and conceptually link?
Empirically document and test?

61. 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

62. 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