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INTRODUCTION |
Professional societies in biology
tend to segregate themselves taxonomically. In 1992, the National
Science Foundation of the U.S. formed a proposal review panel for
"Functional Biology" (now named "Ecological and Evolutionary
Physiology") that entertained proposals without regard to biological
kingdom. From their experiences on this panel, many panel members and
managers have become advocates for cross-kingdom activities. In
particular, Martin Feder and James Coleman, who served as presidents
for the Society for Integrative and Comparative Biology (formerly known
as the American Society of Zoologists) and the Physiological Ecology
Section of the Ecological Society of America, respectively, sponsored
symposia at their national meetings in 2001. Here, we report on two
symposia, "Plant-Animal Physiology" and "Living Together: The
Dynamics of Symbiotic Interactions," held at the Society for
Integrative and Comparative Biology Meetings in Chicago (January 5-7,
2001) with support from the National Science Foundation and the U.S.
Department of Agriculture Competitive Grants Program, respectively. The
proceedings of these symposia will be published in American
Zoologist later this year.
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PLANT-ANIMAL PHYSIOLOGICAL ECOLOGY, COMPARATIVE
PHYSIOLOGY/BIOCHEMISTRY, AND EVOLUTIONARY PHYSIOLOGY |
Martin E. Feder (University of Chicago) began the symposium with
an inquiry into the forces responsible for the divergence between the
studies of plants and animals. Until 50 years ago, plant and animal
physiological or evolutionary ecologists commonly worked together.
Some, like Per Scholander, conducted research in both kingdoms, but
even those who did not cross over communicated with their counterparts.
For example, G. Ledyard Stebbins and Theodosius Dobzhansky were fully
aware of each other's work.
From about 1950, funding opportunities from biomedical and agricultural
sources began to separate the kingdoms. Through the 1970s, plant
physiological ecologists concentrated on photosynthesis, a process
without animal equivalent. Animal physiological ecologists, in turn,
focused on the role of behavior, a factor assumed to be less important
in plants (but see below). Plant physiological ecologists have migrated
more recently toward large-scale phenomena such as global climate
change, whereas animal physiological ecologists have studied phenomena
amenable to molecular approaches.
Plant and animal disciplines benefit from the sharing of common
resources; for example, facilities that analyze stable isotope ratios
or sequence DNA serve both plant and animal studies. Perhaps the most
compelling reason for enhancing interactions is that the perspective of
another discipline promotes better science. Proof of this abounds in
the subsequent presentations that fell into four categories: (a) global
change biology, (b) sensing and signaling, (c) dormancy, and (d) escape
versus tolerance.
Global Change Biology
James R. Ehleringer (University of Utah, Salt Lake City) described
how atmospheric CO2 levels have declined by
two-thirds over the last 65 million years. This
"CO2 starvation" has selected for plants with
compensatory mechanisms such as C4 carbon
fixation, particularly in warmer climates. The
13C values of fossil teeth provide a record of
whether animals were feeding on C3
(13C 
12.4 
) or
C4 plants (13C +1.8
). Teeth older than 8 million years ago have a
13C signature that indicates a diet of
C3 plants only. A dramatic shift in the
terrestrial flora and fauna occurred from 6 to 8 million years ago, and
the teeth signatures support that C4 plants and
the herbivores equipped to chew them became prevalent in warmer climates. Future increases in atmospheric CO2
levels may result in resurgence of C3 plants and
their herbivores in certain areas of the world.
Warren P. Porter (University of Wisconsin, Madison) applied a
sophisticated energy balance model to large animals, ranging from elk
in Yellowstone National Park, chuckwallas in the deserts of the
southwestern U.S. and Mexico, to an ectotherm predator (rattlesnake)
and endotherm prey (ground squirrel and wood rat) in Southern
California. In each case, radiation exchange between animals and their
surrounding vegetation proved to be a critical factor. For example, elk
in Yellowstone sleep under the forest canopy during the winter because
radiant temperatures of the open sky are 15°C to 20°C colder; when
the recent Yellowstone fires removed the tree needles, the elk were
exposed to stressful temperature conditions. The model also predicts
that rattlesnake density will increase with clear cutting of trees as a
result of the altered thermal environment. As a consequence, the role
of vegetation extends beyond that of a food source.
Sensing and Signaling
Jack C. Schultz (Pennsylvania State University, State College)
discussed shared signals between plants and animals, a presentation that provided valuable material for any plant biologist who must engage
an auditorium filled with premedicine and preveterinary students. He
documented several signals through which both plants and animals
perceive biotic stimuli and how they have led to
similar response mechanisms. Examples include
prostaglandin-/octadecanoid-mediated responses to wounding,
steroid-based signaling systems, and pathogen recognition mechanisms.
That many pharmaceuticals have their origins in natural plant compounds
is not due to happenstance: Similar pathogens are responsible for
disease in plants and animals, and antibacterial or antifungal agents
from plants are often broad spectrum. Herbivores and plants, in that
they use common modes for information gathering, may act like
adversaries in a spy novel, breaking codes and substituting messages
for their own benefit. Understanding the bases of these interactions
and fully exploiting them for human benefit will require an expansion
of integrative plant and animal studies.
Peter L. Lutz (Florida Atlantic University, Boca Raton) continued on
this theme in a presentation in which he detailed how larger animals
sense oxygen deprivation. Small deviations are sensed through central
and peripheral chemoreceptors that trigger responses such as heavy
breathing, and chronic deprivation is sensed through cellular oxygen
signals that induce gene expression. An immediate emergency or crisis
is sensed through changes in energy metabolite concentrations that
invoke metabolic shutdown. As a model system, brains from a freshwater
turtle
an organism that can survive at least 48 h of anoxiashow
multiple physiological mechanisms for coping with such conditions.
Rowan F. Sage (University of Toronto) described how terrestrial
organisms sense, signal, and respond to carbon dioxide. He discussed
the wide variations in atmospheric CO2 levels
over geologic time, variations that influenced the evolution of
organisms. In plants, CO2 directly influences
carbon fixation, stomatal aperture, mitochondrial respiration, and gene
expression. With the exception of carbon fixation where
CO2 is a substrate, the signal perception of
CO2 in plants and the mechanisms for an
integrative response remain the subject of active inquiry. Relatively
little attention has been given to CO2 perception
in other kingdoms. Certain mushroom species use
CO2 as a cue to position their fruiting bodies
above the boundary layer at the soil surface, thus insuring better
spore dispersal. In most animals, CO2 inhibits
respiration, but only at levels two orders of magnitude above the
current levels. Insects, particularly blood parasites such as
mosquitoes, have special olfactory sensilla with specific
CO2 receptors that initiate membrane potential
shifts when exposed to even small (<10 µmol
mol
1) changes in CO2.
Will rising atmospheric CO2 levels impede this sensing mechanism?
Dormancy
Nelson G. Hairston, Jr. (Cornell University, Ithaca, NY) described
how planktonic animals bury diapausing embryos in the sediments of
ponds, lakes, and near-shore marine environments; these can hatch even
after years and sometimes centuries. Such an accumulation of eggs, like
the seed banks of many plants, may maintain diversity in a fluctuating
environment by introducing at various times species or genotypes laid
in the distant past. In crustaceans, as well as in plants, prolonged
embryo dormancy, a long-lived adult stage, and far-ranging dispersal
appear to be alternative strategies. Within a single lake, egg banks
may serve as a record of the rates and trajectories of past ecological
and evolutionary changes in species composition as well as provide,
from the more disturbed areas, propagules dispersed through time.
Escape versus Tolerance
Raymond B. Huey (University of Washington, Seattle) noted that all
organisms must deal with stress. They may: (a) evade it through
behavior or dormancy, (b) develop resistance to it through greater
plasticity or reduced sensitivity, or (c) activate repair mechanisms. A
common assumption is that animals, because of their greater mobility,
have more behavioral options than plants; for example, an animal may
move around in a heterogeneous environment to avoid predation or to
maximize the time it spends at optimal temperatures. In more
homogeneous environment, however, movement can be a waste of energy.
Plants in heterogeneous environments may also move to more favorable
conditions either at certain life stages such as pollen and seeds,
through growth above ground and below ground, or by relatively rapid
leaf movements including various heliotropisms, drooping, and wilting.
Nonetheless, plants as slower moving organisms should show greater
phenotypic plasticity than animals, but suitable measures for
comparison are often lacking. Enhanced cooperation among plant and
animal biologists should permit a more thorough examination of such issues.
John H. Crowe (University of California, Davis) posed the question:
"Is there a single biochemical adaptation to anhydrobiosis (the state
where an organism survives the loss of nearly all its water)?" As one
might suspect, the answer is a qualified yes. Diverse organisms, which
tolerate anhydrobiosis, accumulate disaccharides in their cells and
tissues during drying. Animals such as brine shrimp or nematodes and
fungi such as yeast accumulate trehalose, whereas seed and pollen
grains of higher plants accumulate Suc. Some resurrection plants, such
as Myrothamnus flabellifolia, accumulate a combination of
Suc and trehalose. These disaccharides serve to stabilize membranes and
labile proteins in a dry state. Membranes, in the absence of these
compounds, experience a phase change during rehydration after drying
that causes a profound loss in membrane selectivity. Interactions
between the disaccharides and membrane lipids prevent such phase
changes. Diminished seed or pollen viability over time is correlated
with the accumulation of free fatty acids. Arbutin, a glycosylated
hydroquinone found in extremely high concentrations (20% of the dry
weight) in certain resurrection plants, may prevent the formation of
free fatty acids in certain membranes. This area of research holds
great promise for improving the preservation of human blood platelets
and mammalian cells.
N. Michele Holbrook examined the dynamics of "dead wood." To
distribute water through a highly branched system, plants employ a
structural solution without moving parts. Yet treating plant vascular
systems as static plumbing is incorrect. The hydrostatic conditions
within the xylem vary widely diurnally, ranging from small pressures to
tensions that are much larger than one can generate without great
difficulty in a laboratory. Such extremes can lead to cavitation, the
breaking of the continuous water column in the xylem by air bubbles.
Plants refill cavitated vessels by hydraulically isolating the damaged
tissue, pumping ions from the surrounding cells, and fostering water
entry through bordered pits. Even the hydraulic conductance of intact
xylem vessels is highly dynamic. Hydrogels, analogous to the materials
in diapers, are located in the border pit membranes. These swell and
shrink in response to ion concentrations, changing the porosity of the border pit. Thus, "dead wood," perhaps a useful term under certain circumstances, does not accurately describe botanical situations.
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LIVING TOGETHER |
The widespread occurrence of symbiotic associations underscores
the importance of interdisciplinary training and scientific interactions that traverse traditional taxonomic boundaries. Although such integration has long been the hallmark of symbiosis research, the
diversity of symbiotic associations and the potential for separation
between basic and applied efforts indicates the need for broad
communication within the symbiosis community. In addition, the
ecological and evolutionary importance of symbiotic associations demonstrates the need for a more general appreciation of new findings in this field. A 2-d symposium organized by March Beth Saffo (Arizona State University West, Phoenix) provided a significant step in this
direction. "Living Together: The Dynamics of Symbiotic
Interactions" brought together a diverse group of basic and applied
scientists whose research focuses on the mechanics, ecology, and
evolutionary dynamics of both mutualistic and antagonistic symbioses.
The talks were wide ranging, extending from a discussion of the
transmission dynamics and evolution of computer viruses to a
consideration of the contribution of lichen symbiosis to the
diversification of fungi. Several presentations focused on symbiotic
associations involving plants, including Rhizobium legumes,
ectomycorrhizal fungi, and ectomycorrhizal epiparasites, as well as
fungal endophytes. Here, due to space constraints, we go against the
overall theme of these two symposia and consider a taxonomically
delimited subset of the presentations (only two of the 18 talks)one
involving legume interactions with root symbionts and one focusing on
fungal endophytes.
Symbionts
Mycorrhizae are ancient associations that perhaps played a key
role in the colonization of the land by plants. In contrast, symbiotic
associations between legumes and nitrogen-fixing bacteria (Rhizobiaceae) evolved more recently. The existence of several common
elements between these two symbioses has led to the hypothesis that the
Rhizobium-legume symbiosis evolved from an
arbuscular-mycorrhizal association. Ann M. Hirsch (University of
California, Los Angeles) discussed the evidence for functional
interactions between the two symbioses and presented data on the
response of four classes of non-nodulating
(Nod) Melilotus alba mutants to
their mycorrhizal symbiont (Glomus intraradices). Several of
the Nod mutants also failed to form mycorrhizal
associations (i.e. they were Myc), suggesting
that multiple steps in the symbiotic process are conserved. Hirsch
noted that all the white sweet clover Myc
mutants are incapable of forming infected nodules. This suggests that,
at least, some of the initial steps in Rhizobium infection are upstream of those leading to mycorrhizal association. The overlap
between the two symbioses and the interactions between Nod and Myc phenotypes
indicates some sort of shared heritage. Further studies are needed to
understand the functional and genetic overlap between the two symbioses.
Endophytes
In contrast to root symbionts, fungal endophytes are typically
asymptomatic inhabitants of aboveground plant tissues. Because endophytes produce alkaloids that may act as feeding deterrents, they
have been described as a form of acquired defense against herbivores.
However, the nature of their relation with their plant hosts is more
complex than this hypothesis initially suggests, with the association
ranging from mutualistic to antagonistic and showing significant
variation across both spatial and temporal (both ecological and
evolutionary) scales. Stanley Faeth (Arizona State University, Tempe)
described endophytes as common symbionts but unusual mutualists. He
noted that most studies of endophytes have been conducted with
introduced, agronomic grasses and that little is known of endophytes in
natural populations. His data on the effects of Neotyphodium
infection of native fescue (Festuca arizonica) demonstrate a
significant interaction between plant genotype and the degree to which
endophytes enhanced growth. However, the benefits of harboring
endophytes were not observed in well-watered and fertilized plants. A
graphical model exploring the cost-benefit tradeoffs of endophyte
infection in relation to soil nitrogen levels illustrated how
endophyte-host interactions may change in varying environments and
argue for a more synthetic appreciation of this extremely common and
highly diverse symbiotic association.
The absolute dependence of life on symbiotic associations demonstrates
the dangers of taxonomic isolation. Mutualistic as well as antagonistic
interactions increase life's amplitude and provide fresh grist for the
evolutionary mill. Thus, we ignore our sister disciplines at our own
peril. By bringing together scientists specializing in plants and
animals and in symbiotic associations based on diverse taxa, these two
symposia provide a good lesson in what there is to be gained through
the lateral exchange of thoughts, approaches, and ideas.
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INTRODUCTION
PLANT-ANIMAL PHYSIOLOGICAL...