Download The “Invisible Hand” of Floral Chemistry

PERSPECTIVES
PLANT SCIENCE
The “Invisible Hand” of
Floral Chemistry
Volatile compounds help flowering plants
balance attracting pollinators and maximizing
overall reproductive success.
lowering plants that compete successfully for pollinator services often advertise their commodities—nectar, pollen,
and other nutritious rewards—with dazzling
color displays and alluring perfumes. Pollinator abundance and preference may limit a
plant’s reproductive success, especially if its
reproductive window is brief (1). Such circumstances predict a “buyer’s market” for
pollinators, which should engender fierce
competition among neighboring plant species
for attracting pollinators through quality
rewards and truthful, enticing advertisements.
Flowers that abuse the good will of their consumers with meager or distasteful rewards
should fare poorly in such an arena. Enter
Nicotiana attenuata, a tobacco from North
America’s Mojave Desert that laces its floral
nectar with nicotine (see the figure). Why
would a plant adopt such a strategy when its
hawkmoth and hummingbird pollinators are
demonstrably repelled by the taste and odor of
nicotine (2)? On page 1200 of this issue,
Kessler et al. address this conundrum (3) by
combining gene silencing, paternity analysis,
and field experiments. Surprisingly, the combination of nicotine and benzyl acetone (the
most attractive scent component) best serves
the reproductive interests of the tobacco
plant. Those with this floral blend sire more
seeds on other plants and produce larger seed
capsules themselves.
One novel aspect of this study is its selective manipulation of specific scent and nectar
components. The amount of scent and nectar
can be augmented (4, 5), but their experimental deletion is more difficult. Kessler et al.
silenced genes associated with nicotine and
benzyl acetone biosynthesis in N. attenuata
and then presented pollinators with arrays of
such plants whose flowers emitted different
nicotine-benzyl acetone combinations. The
presence of nicotine decreased the time hummingbirds and hawkmoths spent drinking
from individual flowers but increased the
number of flowers visited, presumably to satisfy the caloric demands of hovering flight.
Conversely, birds and moths visited fewer
flowers for longer periods when nectar lacked
CREDIT: D. KESSLER
F
Department of Neurobiology and Behavior, Cornell University,
Ithaca, NY 14853, USA. E-mail: [email protected]
of a competitor. In N. attenuata, nicotine functions as a floral filter (8) for
antagonistic visitors (caterpillars and
nectar-robbers) but manipulates pollinators by altering their movement patterns (and pollen export) through a
population. For this to work, nicotine
must be somewhat tolerable—if
deterrent—to hummingbirds, or the
local nectar market must be poor. In
either case, nicotine would function
more as an economic hurdle (9) than
as a filter, which suggests that pollinators supplement additional reproductive options at the tobacco’s disposal. Such a scenario is amenable to
a game theory approach. Indeed, N.
attenuata flowers are self-compatible,
capable of maturing seed capsules
without pollinators.
In this light, testing a pollinator’s
Better pollination through chemistry. The desert tobacco tolerance for nicotine-spiked nectar
N. attenuata lures hummingbirds (Archilochus alexandri) with appears less risky. Yet, how might outsweet nectar flavors but sends them away with nicotine. This crossing—when a flower is fertilized
strategy allows them to both attract pollinators and effectively by pollen from a different plant—benmove their pollen between plants.
efit a plant that can pollinate itself,
such as N. attenuata? Perhaps the
nicotine, which suggests that the pollinators’ answer lies in the plant’s life history. It is a
interests are best served by extended visits to a fire-adapted desert annual that can spend
few nectar-rich flowers (6). Responses to decades as a dormant seed, awaiting a smoke
plants lacking benzyl acetone were more signal that will trigger germination. This lifeambiguous. The taste and/or scent of this com- style is notoriously unpredictable, and betpound are preferred by hummingbirds and hedging strategies are commonly invoked
hawkmoths (2), and plants lacking both nico- (10) in studies of germination success. Even a
tine and benzyl acetone were ignored by hawk- low percentage of outcrossing might improve
moths, possibly because of reduced odor (7). seedling survivorship, especially if seeds gerFlowers with nicotine absolutely deterred minate under variable climatic conditions.
florivory by caterpillars and nectar-robbing by
This study adds to a growing list of ruses by
carpenter bees, both of which could directly which plants manipulate pollinator movement
reduce reproductive fitness. These results, to optimize gene flow. Nearly a third of all
combined with seed and seed capsule produc- orchids have no floral nectar (11). When sugar
tion data, suggest that chemically mediated solutions are added to such flowers, pollinators
“pull” and “push” strategies optimize repro- remain longer at individual plants, resulting in
ductive fitness in N. attenuata by attracting increased inbreeding or pollen wastage (12).
pollinators, preventing them from loitering, Similarly, the reduction of nectar by extrinsic
and deterring floral enemies.
factors (such as mites) may benefit plants by
The study of Kessler et al. highlights a par- altering pollinator movement or floral contact
adox in floral behavior: Flowers must compete (13). Another floral scheme is to turn up the
vigorously for pollinators without being so heat. Dramatic increases in temperature and
attractive that they never leave. A plant must odor concentration compel cycad pollinators to
encourage a pollinator to visit other flowers of leave male cones (where they feed on pollen)
its own species without forsaking it for flowers for female cones on different plants, thereby
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Robert A. Raguso
1163
PERSPECTIVES
effecting cross-pollination (14).
The results of Kessler et al. present a cautionary tale: The subtle interactions between
N. attenuata and its floral visitors could not
have been revealed through mainstream pollination studies, in which nonvisual floral traits
and nonsugar nectar components are often
ignored (15). Through the “invisible hand” of
floral volatiles, the self-interests of tobacco
plants and their pollinators are mediated with
an apparent net outcome of mutual benefit.
References
1. T. M. Knight et al., Annu. Rev. Ecol. Evol. Syst. 36, 467
(2005).
2. D. Kessler, I. T. Baldwin, Plant J. 49, 840 (2007).
3. D. Kessler, K. Gase, I. T. Baldwin, Science 321, 1200
(2008).
4. T.-L. Ashman et al., Ecology 86, 2099 (2005).
5. L. S. Adler, R. E. Irwin, Ecology 86, 2968 (2005).
6. J. A. Riffell et al., Proc. Natl. Acad. Sci. U.S.A. 105, 3404
(2008).
7. R. A. Raguso, M. A. Willis, Anim. Behav. 69, 407 (2005).
8. S. D. Johnson, A. L. Hargreaves, M. Brown, Ecology 87,
2709 (2006).
9. R. H. Frank, The Economic Naturalist (Basic Books, New
York, 2007).
10. M. J. Clauss, D. L. Venable, Am. Nat. 155, 168 (2000).
11. S. Cozzolino, A. Widmer, Trends Ecol. Evol. 20, 487 (2005).
12. S. D. Johnson et al., Proc. R. Soc. London Ser. B 271, 803
(2004).
13. C. Lara, J. F. Ornelas, Oikos 96, 470 (2002).
14. I. Terry, G. H. Walter, C. Moore, R. Roemer, C. Hull,
Science 318, 70 (2007).
15. R. A. Raguso, Entomol. Exp. Appl. 128, 196 (2008).
10.1126/science.1163570
How is a dead massive star still able to
energize extremely relativistic particles?
Life After Death
Annalisa Celotti
I
International School for Advanced Studies (SISSA), via
Beirut 2-4, 34014 Trieste, Italy. E-mail: [email protected]
1164
tic particles and electromagnetic fields. Highly
energetic particles moving in such a field will
emit radiation. The x-ray image (see the figure) reveals morphological features over a
scale of about 5 light-years, comprising a narrow collimated “jet” and a doughnut-shaped
“torus,” as well as ripples, wisps, and arcs.
Even 40 years after the discovery of the
Crab pulsar and more than 20 years after the
basis of the currently accepted interpretation
was formulated (7, 8), key questions remain:
How is the rotation power converted into the
electromagnetic and the kinetic power of the
wind? How are particles accelerated to emit
high-energy radiation?
Understanding how the Crab system
works will elucidate the late stages of stellar
evolution, the physics of magnetized relativistic plasma, the conditions of matter at nuclear
densities, and the mechanisms by which
extremely relativistic particles are efficiently
accelerated in the universe. Indeed, observations of radiation from the Crab at extremely
high energies (9), up to ~100 TeV (1 TeV =
1012 eV), requires electrons (and positrons) to
have been energized to 100 million times the
energy associated with their own mass.
The spectrum of the Crab, from radio to
gamma-ray frequencies, is well known.
Its brightness in x-rays promoted it to the role
of a flux (and time) calibrator
for x-ray detectors. The high
degree and direction of polarization at high energies reported by Dean et al. provide
valuable information on the
site of acceleration of the particles and on the structure of the
magnetic field associated with
the pulsar. Such information
cannot be provided by the spectrum alone.
Electromagnetic waves oscillate in a plane perpendicular to
their direction of travel. They
are linearly polarized if the
electric and magnetic field
vectors oscillate along the
same direction in such a plane.
For that to occur, the emitting
system has to be characterized
by some order, or degree of
symmetry. For synchrotron radiation, an elevated level of
The Crab nebula. A composite of optical data (red) from the polarization thus indicates that
Hubble Space Telescope and x-ray imaging (blue) from the the magnetic field (and possibly the radiating particles) is
Chandra X-ray Observatory.
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VOL 321
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CREDIT: X-RAY: NASA/CXC/ASU/J. HESTER ET AL.; OPTICAL: NASA/HST/ASU/J. HESTER ET AL. (2002).
n 1054 C.E., Chinese and Arab (1–3)
astronomers recorded the observation of a
bright explosion in the sky. Now known to
have been a supernova explosion, the remnant—the Crab nebula—still emits particles
energized to extremely relativistic energies
and radiates light at x-ray and gamma-ray
wavelengths. On page 1183 of this issue,
Dean et al. (4) report the discovery that the
high-energy radiation (hard x-rays) from the
Crab is polarized, yielding insights into the
processes and mechanisms involved in making a dead star so active.
When a massive star exhausts its fuel for
nuclear fusion, it collapses under its own gravity into a neutron star or black hole, releasing
energy that heats and expels the outer star layers. The material expands at a speed as high as
1% that of light, sweeping through the interstellar medium and giving rise to a supernova
remnant. The Crab nebula is such a remnant,
resulting from the explosion of a star thought
to have been 10 times as massive as the Sun. It
is located in our galaxy, in the constellation
Taurus, about 6500 light-years from Earth,
and is about 10 light-years in size.
Inside the Crab, a relatively young neutron
star (5, 6) of 1.4 to 2 solar masses is active as a
pulsar. The neutron star rotates at about 30
times per second. As it slows down, at a rate of
38 ns per day, its rotational energy is converted
in part to radiation collimated along the axis
determined by the pulsar magnetic field.
Because this magnetic axis is misaligned with
the rotation axis, like the beam from a lighthouse, such emission is observed from Earth
as pulses of light from radio- to gamma-ray
wavelengths. But most of the neutron star spin
energy goes into powering a wind of relativis-
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ASTRONOMY