Chemical signaling processes in the marine environment

20 Pages·2000·8.4 MB·English

by  R K Zimmer

Reference: Biol. Bull !* lApnl 20001
Chemical Signaling Processes in the
Marine Environment
KICH\KD K /IMMFK1 AND CHI.KYI ANN HITMAN2
1Department ofBiology, i'liiversity <>t'California. Los An^ele^. California V0095-1606; ami 'Applied
Ocean Phvsics and l.n^in, <nm; Department, Mail Stop 12. \\'ooJ\ Hole Oceanographic Institution,
U(><A Hole. Massachusetts 025
\bstract. Understanding the mechanisms by which envi- Introduction
ronmental chemical signals, chemical defenses, and other "Keller 'l'liint;\ fur Heller Lniim IIn,nigh Clu'mistry"-
chemical agents mediate various life-history processes can Former DuPont corporate slogan
lead to important insights about the forces driving the ecol-
ogy and evolution of marine svstems. For chemical signals The foundation ofbiological sciences is evolution, which
released into the environment, establishing the principles stresses phylogenetic relationships. Therefore, questions re-
that mediate chemical production and transport iscritical for lating to speciation. hiogeography. and biodiversity are par-
interpreting biological responses to these stimuli within ticularly compelling. Improved understanding of how
appropriate natural, historical contexts. Recent technologi- chemical signals and otherchemical agents interact with the
cal advancements pn>\ ide outstanding opportunities tornew environment can lead to important insights about the natural
discoveries, thus allowing quantification ol interactions be- selective forces driving ecology and evolution. If. for ex-
tween hydrodynamie. chemical, and biological factors at ample. organisms release waterborne compounds into the
nicuamlleyromuesdisapatteidalparnodcetsesmesporianlvoslcvailnegs.oPragsatnwisomrsk oanndchtehemi-r cetrhnaevtmiiironcosan.lmeanpntrd,odfiulncuvtxeiesostniogfaanthdiioontasrcalmnisuvpseotrtm.foolTceuhcseulosentsrtuhmcetuusrptersi,hnceciopilndeecsnetnoi--f
environment have emphasi/ed habitat colonization by lar-
fied. and the rates ofadvection and diffusion (molecularand
vae and trophic relationships. Future research priorities turbulent must be measured to establish chemical distribu-
should include these topics as well as courtship and mating, iions overI time and in space. Knowledge of these factors
fertili/ation. competition, symbiosis, and microbial chemi- makes it possible to analv/e the constraints imposed by
cal ecology. There are now vast new opportunities for natural phvsicochemical phenomena on biological re-
determining how organisms respond tochemical signals and sponses al individual, population, and community levels
employ chemical defenses under environmentally realistic
(Fig. I I.
n>minions. Integrating these findings within a larger eco-
il and evolutionalv liamewoik should lead to im- Cheinienl mediation ofecological interactions
proved understanding of natural phvsicochemical phenom-
ena that innsiiam hmloL'kal responses at the individual, Chemistry indeed mediates a vaiietv ofcritical ecological
population. ;ind community levels of oigam/ation. interactions. Considerable information is now available on
the many types of biological responses to environmental
chemical stimuli. Sensory perception of chemical signals.
for example, strongly influences predation (Zimmer-Faust,
1989; Leonard el al.. 1999). courtship and mating (Gleeson
Received ipled 1 < Ivn-mhcr I'MCI el a/.. I9S4: Hardege el al.. 1996). aggregation and school
CoTmhmiusnipcaapteiron nn,: p.ixium.Mw|h>incxhmmw.niisK-.Ll-M< li,mrm'si.aml formation (Hamner el al.. 19X3; Katchford and F.ggleston,
Diego. California. was imileil In ihe Western I99X). and habitat selection (Morse. I9'l. I'awhk. 1992).
St>cic(y ofNaturalists ;r Lin| Additionally, prey organisms (both animals and plants) ot-
IdX
CHEMICAL SIGNALING PROCESSES 169
CHEMICALSIGNALING ecules by gas chromatography and mass spectrometry is
Concentration ^f?"""""***. Structure often straightforward. By comparison, much less is under-
stood about chemically mediated interactions in aquatic
habitats. Aqueous solubility (imparted mainly by electronic
charge or hydrophilicity), rather than gaseous volatility,
may constrain the types of substances principally acting as
waterborne chemical agents. Even insoluble compoundscan
provide effective chemical signals when suspended and
transported by fluid flow in the watercolumn. The identities
ofcues mediating habitat selection (including settlement by
and metamorphosis of larvae), predator avoidance, mating,
and social interactions in aquaticenvironmentshave thus far
proven elusive except in a few isolated cases (e.g., Howe
and Sheikh. 1975; Sleeper et al., 1980; Hardege et al..
1996).
Feeding attraction and deterrence: examples of
chemically mediated ecologicalprocesses
Nevertheless, an impressive body ofknowledge has now
accumulated concerning feeding stimulants and attractants
BEHAVIORAL
released from animal flesh. These compounds are believed
(orphysiological)
RESPONSE to be primarily amino acids, although there also may be
effects of quaternary ammonium bases, nucleotides and
nucleosides. and organic acids (Carr, 1988; Carr et al.,
1996). The sensory basis for animal perception of amino
porFt,igaunrde 1p.ercDepitaigornamofofwattheerfbaocrtonrescthhaetmidceatlermsiignnealtshebpyroaducmtaicorno,sctroapnisc- acids, including complex mixtures, has been studied exten-
organism. sively for 70 years, especially in crustaceans and fishes
(Luther. 1930; Case. 1964; Ellingsen and Doving, 1986;
Valentincic et al.. 1994: Derby et al., 1996). With a single
ten produce chemical defenses that render their tissues exception, however, the hypotheses that amino acids and
unpalatable to primary or secondary consumers (Bakus el other small metabolites are attractants and stimulants have
cil.. 1986: Paul, 1992; Hay, 1996). Although chemicals are not been tested under field conditions simulating the natural
widely recognized as having critical importance ecologi- fluxes of these materials from intact live or injured prey or
cally, largely unexplored are the mechanisms by which such from carrion. The exception was a series of field experi-
stimuli contribute to processes that structure communities. ments in which mud snails (Ilyanassa obsoleta) were sig-
Marine natural products chemistry and chemical ecology nificantly attracted to injured prey and carrion, but not to
are in their infancy and have emphasized studies ofsecond- intact prey (Zimmer et al.. 1999). Synthetic mixtures of
ary metabolites acting as toxins and antifeedants. Still, amino acids, simulating fluids leaking from injured prey,
outstanding examples are emerging in which either chemi- were also highly attractive. When field trials were per-
cal signals or secondary metabolites are known to regulate formed to assess the relative effects of amino acid compo-
the behavioral or physiological responses of individuals at sition, concentration, mean volume flow rate (of chemical
lower trophic levels (Simenstad et al., 1978; Hay. 1992; input), and flux (concentration X flow rate), only flux was
Steinberg et al., 1995). These regulatory effects are then directly correlated with the number of mud snails attracted.
transferred to consumers at higher trophic levels with pro- The foraging behavior of mud snails is thus more tightly
found impacts on the distributions and abundances of or- coupled to the release and physical transport of chemical
ganisms. stimuli than to the molecular properties of specific amino
The physical and chemical properties of habitats can acids.
determine the nature and success ofecological interactions. Feeding deterrents, including terpenes, acetogenins, alka-
In terrestrial environments, for example, compounds with loids, halogenated hydrocarbons, and polyphenols, arecom-
high vapor pressures (low molecular weights, hydrophobic) monly found in marine microbes, plants, and sedentary
facilitate chemical transport in air. Because the requirement animals (Hay and Fenical, 1988; Paul, 1992; Pawlik, 1993).
for gaseous volatility imposes strong constraints on molec- These substances are mostly hydrophobic and sequestered
ular designs, the isolation and identification of signal mol- within tissues rather than released into the environment.
170 R. K. ZIMMtR AND C. A. BUTMAN
Because, in many cases, their identities are known or can gus)can be trained in the laboratory todiscriminate between
he determined following bioassay-guided separation feed- different mixtures ofidentical compounds (including ainino
ing deterrents have served as valuable probes for investi- acids, organic acids, amine bases, and nucleotidesi When
gating the ecological impacts ofchemically mediated inter- presented at the same concentration and (lux. each mixture
actions <?..(.. Vervoort ei ai, 1998: Nagle et ai. 1998). is recognized as having its own unique composition that
Direct tests at environmentally realistic doses have been characterizes the tissues of either crab, oyster, shrimp, or
performed in Held habitats. Some deterrent compounds in- fish (Derby et ai. 1989: Fine-Levy et ai. 1989).
hibit feeding (McClintock and Janssen. 1990; Pennings et
ai. 1994). kill or suppress the growth ofcompetitors (Jack- Role ofhydrodynamics
son. 1977; Thacker et ai. 1998) and microbial pathogens
(King. 1986: Gil-Turner et ai. 1989). and diminish sub- Turbulent odor plumes operate at macroscopic scales and
strate colonization by plant and animal propagules (Woodin are common features of the marine environment (Fig. 2).
et ai. 1993: Lindquist and Hay. 1996). Main members of They form olfactory seascapes through which animals must
marine communities benefit from feeding deterrents. Bi- navigate in order to locate resources and avoid potential
valve molluscs feeding on toxic dinoflagellates accumulate hazards (Nevitt et ai. 1995). Turbulent odor plumes can be
poisons in certain body tissues. If sea otters, fishes, and described by stable, mean concentration proliles averaged
birds forage on the toxin-laden portions of these bivalves. over relatively long time scales that animals may use for
they may become sick or die. Otters are also known, how- orientation, i.e., via chemotaxis (movement in response to a
ever, to feed selectively on the least-toxic tissues and are gradient in chemical concentration) (Ingram and Hessler,
chemically deterred from eating the toxins. Moreover, otters 1983; Sainte-Marie and Margrave. 1987). However, an or-
appear to have been historically absent from areas where ganism's neural or behavioral response time in an odor-
dinoflagellate blooms were common (Kvitek et ai. 1991). mediated search is much faster than the time necessarv to
Nonetheless, poisons produced by blooms of both generate mean concentration profiles (Gome/ et ai. 1994:
dinotlagellates and cyanobacteria potentially alter the struc- Zimmer-Faust et ai. 1995: Gomez and Atema. 1996). Field
ture and production ofcommunities through theireffects on measurements made at shorter, biologicallv relevant time
predators (Paerl, 1988; Noga vt ai. 11W6: Nagle and Paul. scales indicate that turbulent plumes are not characterized
1998). by well-defined gradients, but contain discrete odor fila-
ments (eddies) separated by clean water (Zimmer-Faust el
The Importance of Clu'inical Siynuliiij; Processes ai. 1988; Atema et ai. 1991: Finelli et ai. 1999). Under
in Marine Kcology these conditions, organisms larger than a few millimeters
are unlikely to use chemotaxis in navigating towards a
Organism recognition ofchemical stimuli
distant odor source because their sensory systems sample
There is ample evidence that chemical composition, con- faster than the averaging time scale to perceive a stable
centration, flux, and hydrodynamic transport all have pro- gradient (Fig. 3).
found effects on chemically mediated ecological interac- Still, large animals like blue crabs (Callinectes sapiihix)
tions. Forexample, small peptides with arginine or lysine at employ their chemical senses while searching for valuable
theircarboxy termini induce ovigerous mud crabs (Rhithro- resources (Pearson and Olla, 1977). Crab success in locating
panopeus harrisii) to release and disperse brooded embryos live intact clams (Mercenaria mercenaria) was highly de-
and induce oyster (Crassostrea virginica) larvae to settle pendent on the hydrodynamic transport of metabolite at-
nearconspecific adults (Forward etat.. 1987: Browne et ai. tractants by both advection (bulk flow) and turbulent mix-
1998). Moreover, in contrast to the more typical sigmoid- ing. In fact, perception of chemical stimuli caused crabs to
shaped dose/response curve, chemical induction in these move upstream, but How provided the signpost directing
marine organismsoccurs only within a very narrow range in crab navigation. Predatory success was highest at a free-
concentration, spanning less than one order of magnitude. stream flow speed of I cm/s (smooth-turbulenl bottom
=
Animals can distinguish the quality of chemical stimuli boundary layer, * 0.1 cm/s). but rapidly decayed in the
by recori!i/iii<_' ciihei novel compounds or unique blends of absence of How (because there was no polarization for
common sut lances in mixtures (C'arr. 1988). Based on the chemical stimulus to direct locomotion) ami at How speeds
qualitative chemical properties of tood. animals expiess 4 cm/s (transitional to rough-turbulent bottom boundary
markedly dittei Iceding preferences in natural habitats. layer, it^ S 0.3 cm/s: Weissburg and Zimmer-Faust, 1993,
For instance. <>\ :i drills i/ 'mxalpinxcinerea) differentiate ll)94) (Fig. 4). These results indicate that mechanisms gov-
between barnacl i.i^sel. ami ovsk-r prey. The stimuli that erning the transport of chemical signals can have profound
evoke foraging b !K are low molecular weight influences not onlv on sensory and behavioral mechanisms.
peptides, presun \cl structures (Rittschot'el ai. hut also on pivdalion winch, in turn, can mediate comniu
1984). In contrast. < spin) lobsters (l',uii//irii\ <//- nity structure Blue crab chemosensory systems appear
CHEMICAL SIGNALING PROCESSES 171
Figure 2. Odor plume produced by the release ofmetabolites from the excurrent siphon ofa hard clam,
Mercenaria mercenaria. Flow was visualized by releasing fiuorescein dye through the excurrent siphon and
photographed using slit illumination. The metabolites act as chemical signals triggering search responses by
=
predators,butthe likelihoodofpredatory successdependsonthephysicaldynamicsofwaterflow. Scalebar
2 cm.
geared primarily to extracting information from hydrody- streets create coherent chemical trails "information high-
namically smooth flows. Thus, estuarine habitats with either ways" that can be used by animals searching for mates,
no or high flows conceivably could provide prey with ref- food, andotherresources. In the watercolumn, forexample,
uges from crab predation. copepods may locate mates by navigating along streets
Chemicals are transported from regions of high to containing pheromone vortices shed downstreamofconspe-
low concentration via molecular and turbulent diffusion. cifics (Weissburg, 2000; Yen, 2000). Likewise, odor vorti-
Whereas these processes operate at small (molecular) and ces generated from decaying animal matter may guide ly-
large (turbulence) scales, at intermediate spatial scales, un- sianassid amphipods and other scavengers to ephemeral
diluted chemical patches can be transported in organized prey in relatively slow-flow regions, such as protected bays
fluid tracks. In such flows, rotating parcels of fluid vorti- and estuaries, the deep-sea, and polar regions (Busdosh et
ces are shed periodically in the lee ofa flow disturbance, al, 1982; Kaufmann, 1992; Tamburri and Barry, 1999).
such as the organism emitting the signal (Doall et ai. 1998; Provided below are examples of how chemical signals
Weissburg etai, 1998; Yen. 2000). This alternating pattern dictate trophic and defense relationships for a wide variety
of vortex shedding creates "streets" of odor packets of a of marine organisms. The examples are grouped as a func-
characteristic size and frequency (Fig. 5). Vortex streets tion of spatial dimension to emphasize that chemical sig-
develop in the lee of relatively large objects (e.g., 1 cm in naling phenomena are now known to operate at scales from
diameter) in relatively slow flows (e.g.. 0.1-1 cm/s) or of less than millimeters to greater than kilometers. That is, the
small objects (e.g., 100 ju,m in diameter) in fast flows (e.g., sea contains a vast array of chemical information dis-
10-100 cm/s). Chemical signals transported in vortex solved, in suspension, attached to substrates and associated
172 R K X.IMMKR AND C. A. BITMAN
Distance from
Midline (cm) 60
CHEMICAL SIGNALING PROCESSES 173
20 30 40
Time
(s)
Figure4. Usingcomputer-assistedvideomotion analysis,tracestotherightarepathswalkedhybluecrabs
astheysearchedforclamsina 10-m-longracewayflumeatflowspeedsot'O. 1,and4cm/s(toptobottom).Each
'O' marks the location where a search began, and each 'X' indicates the ultimate site ofclam capture. Graphs
to the left are histograms ofwalking speed versus time plotted foreach path displayed to the right. The most
efficient paths were those walked by crabs in 1 cm/s flow. In each case, intermittent walking and stopping
characterized a search. The "stop interval" was defined as the time when crabs reset their attack angle (i.e..
turned) before moving on.
called chemotaxis even though cells do not navigate strictly increases the exposure between cells and nutrient patches
with respect to a chemical concentration gradient. In the (Bowen etal.. 1993). When these nutrients are taken up and
turbulent mixed layer of the ocean, positive chemotaxis used in metabolism, prolonged exposure leads to higher
Figure 5. Artist's interpretation ofa von Karman vortex street in the wake ofa circularcylinder, from a
photographby PeterBradshaw(VanDyke, 1982). Reynoldsnumber(Re)ofabout300(whereRe = LU/r;L =
characteristic length scale, U = characteristic velocity scale and v = kinematic viscosity ofthe fluid) is at the
upper limit for stability ofthe vortex street, as indicated by the breaking up ofthe vortices at the downstream
edgeofthedrawing. AtlowerReapairofvorticesformsintheleeofthecylinderbutis notshed intotheflow,
and at higherRe the vortices break up completely into a disorganized turbulent wake.
174 R K. Z1MMF.R AND C. A. BL'TMAN
Concentration Fields Around Spherical Cells
Puie diffusion Svnmuuus,01 Inotationalshe>=u
Pf = Pe= 1 Pf= 1
-10 0-
-50-
T o.O-
5.0-
10.0 T l^
-101.0 -5I0 0.I0 50 100 -100 -510 0I0 5I0 10I0 -100 -50 00 50 10.0
20-
2.0
Concentration
Figure 6. Concentration distributions ofa hypothetical chemical signal molecule uniformly released from
the surfaces ofmicroscopic point sources (purple circles) in three different How regimes: stagnant water (pure
diffusion, no advective transport); uniform flow (i.e., cell swimming or sinking in stagnant water; the cell is
MIII\ing from right toleft soflowisfrom left toright);and laminarshear Mow luniaxial eMensional flow), where
the third dimension can be visuali/.ed by rotation about the v-axis. The Peclet number (Pel is a measure of
ad\ecti\e li.uisp.ni icl.une to molecular diffusion (where Pe = LU/D,,,; L = characteristic length scale, U =
iharacleristic velocity scale, and Dnl = coefficient of molecular diffusion). The upper panel illustrates the
concentration field at distances up to 10 cell radii from the center of the cell. The lower panel is a "blow-up"
ofthe concentration field near the cell surface, up to a distance oftwo radii from the centerofthe cell. In the
absenceoffluidmotionadiffusiveboundarylayerextendstoaboutninecellradiifromthecellsurface. Uniform
and shear flows distort the boundary layer and steepen the concentration gradient in certain regions. Because
transport viadiffusion is dominant in the thinnest regions ol the boundary layer, cells m uniform 01 shear flow
will experience enhanced rates ofchemical signal release umipaicd to nonmolile cells in stagnant water. This
illustration was provided as a courtesy by L. Karp-Boss. and methods used in calculating concentration
distributions appealed in Karp-Boss et at. (1996).
rates of cell division and population growth. Because mi of translocated materials from the algae is controlled by
crnhial communities are critical to global biogeochemical chemical communication with the coral host. Specifically,
cycling, mechanisms pertaining to chemotaxis and nutrient the chemical signal that induces carbon release is a mixture
uptake have considerable significance. offree amino acids unique to the tissues ofcorals and other
W.
Chemical signals are known to regulate the trophic rela- cnidarian species (Gates ct al.. I1 1MW).
tiMii hips dt corals. All species ofreef-building corals have
mutualistic symbioses with unicellular algae, called /no Use ofchemical .w.i;;i<//.s nt large .v<v//<'\
xanthcllac. which live within the coral cells and arc abun-
dant in tissues exposed to sunlight (Muscatine. 1490). Al- In the open ocean, chemical signaling helps structure
though reef corals arc uniquely versatile in their ability to both annual and plant communities. Dinoflagellates and
procure nutrients .md energy, they principally depend on the other phyloplankton cells, for instance, create dense blooms
translocation ol carbon Iroin their algal symbinnts to meet al convergent /ones where high nutrient levels occur in
their energy demands (Falkowski el al., 1984). The release surface waters. These cells have extremely high concentra-
CHEMICAL SIGNALING PROCESSES 175
tions of dimethylsulfoniopropionate (DMSP) that equalize comparable influence and the intensity of herbivory on
osmotic pressure between the cytoplasm and external ocean kelps is significantly higher than in the North Pacific. From
environment, thus maintaining a constant cell volume experimental results it appears that chronically high rates of
(Vairavamurthy etai, 1985: Dacey etai. 1987; Matrai and herbivory in Australasia have selected for high concentra-
Keller. 1994). When phytoplankton cells burst open during tions ofkelp chemical defenses and increased tolerances of
DMSP
zooplankton grazing, is released into the seawater these substances by herbivores (Estes and Steinberg, 1988;
and is enzymatically degraded to dimethylsulfide (DMS) Steinberg et ai, 1995). Top-level consumers may thus
and acrylic acid (Dacey and Wakeham. 1986) (Fig. 7). The strongly influence the ecology and evolution ofkelp-herbi-
acrylic acid in seawater may act as a chemical deterrent vore interactions, mediated through the production of plant
against protozoan grazers (Wolfe eta!., 1997; Wolfe, 2000). chemical defenses.
DMSP
In contrast, serves as a chemoattractant to biodeg-
radatory bacteria (Zimmer-Faust et ai, 1996), and atmo- Current State of the Field
DMS
spheric guides seabirds over kilometers to rich zoo-
Identification ofecologically relevant molecules
plankton feeding grounds (Nevittetai, 1995; Nevitt, 2000).
Chemistry is important in the evolution of marine com- Significant progress in identifying ecologically relevant
munities. Species distributions and animal abundances in molecules is being made formarine systems, particularly on
kelp forests, for example, are strongly influenced by inver- secondary metabolites acting as chemical defenses. The
tebrate grazing on bottom-attached algae (e.g., Dean et al., structures of more than 2000 secondary metabolites have
1984; Harrold and Reed. 1985). In the North Pacific Ocean, been fully characterized (Hay. 1996, pers. comm.). Most of
seaotterpredation on invertebrates substantially reducesthe these substances can be extracted from animals, plants, and
intensity ofherbivory onkelps (Estes and Palmisano, 1974). microbes by organic solvents (such as methanol or dichlo-
In contrast, temperate Australasia has no known predator of romethane). The compounds are separated by reversed-
phase or hydrophobic-interaction HPLC and gas chroma-
tography before structures are identified by means of mass
spectrometry, NMR, and other spectroscopic methods. Be-
_t cause secondary metabolites are available in partially or
fully purified forms, they provide outstanding tools for
quantitative studies. They are now being used to investigate
the synthesis, inducibility, and seasonal and geographical
variability in chemical defenses (Paul and van Alstyne,
ff
DMS 1992; Steinberg, 1995; Cronin and Hay, 1996; McClintock,
Acryli H 1997; Targett and Arnold, 1998). Also under study are
* mechanisms of detoxification and patterns of associations
(mutualism, commensalism, and parasitism), including co-
Enzymatic
Phytoplanktonnddeeffeennssee JTborfeaDkMdSoPwn evolution, between chemically defended and nondefended
agaihnesrtbpirvoortroeszoan jp^^^ species (Gil-Turner et ai, 1989; Vrolijk and Targett, 1992;
Targett et ai, 1995; Stachowicz and Hay, 1996). These
results will undoubtedly expand understanding ofthe direct
consequences of chemically mediated interactions to pro-
Bacteriaattractant
Phytoplankton vide more predictive insights about population regulation
contain
DMSP and community structure.
DMSP Purifications of ecologically relevant molecules other
released
than secondary metabolites are often more challenging, and
thus advances are occurring more slowly. Considerable
eatenby
zooplankton effort has been expended in identifying environmental sig-
nal molecules that induce marine larvae to settle and meta-
morphose (Morse. 1990; Pawlik, 1992; Rodriquez et ai,
1993). This research has met limited success because many
ofthese morphogens are (1 ) unstable, (2) tightly complexed
(adsorbed or bound) with other molecules, or (3) present in
only trace amounts. Neurotransmitters, such as gamma-
Figure7. Diagram ofthe marine community that uses dimethylsulfo- aminobutyric acid (GABA) and dihydroxyphenylalanine
niopropionate (DMSP) and its breakdown products, dimethylsulh'de
(DMS) and acrylic acid, as chemical signals, at convergence zones in the (DOPA), have been suggested to mimic the function of
open ocean. natural signal molecules (Morse et ai, 1979; Morse, 1985;
176 R. K. Z1MMF.R AM) C. A. HITMAN
Bonur ct til.. 1990; Boettcher and Target!, 1998). hut the have been required on almost a case-by-case basis. Natural
peripheral or central neural site (or sites) ofaction by these waterborne cues in trace amounts below chemical analytical
mimetics is still unclear. Progress to date on at least partial detection limits often have strong biological effects. Purifi-
purification of metamorphic inducers is encouraging (Had- cations can thus require significant efforts in concentrating
field and Pennington. 1990; Morse and Morse. 1991; Zim- (and desalting) these substances while avoiding contami-
mer-Faust and Tamburri. 1994; Krug and Man/i. 1999), and nant introductions.
will he particularly compelling when such research is cou- One strategy used by organisms for producing chemical
pled with physiological studies able to isolate the chemo- signals is to synthesize a novel substrate for each cue-
receptors. Recently, however, promising advances have needed, as with anthopleurine. an alarm pheromone in the
been made towards isolating these chcmoreceptor proteins sea anemone (Howe and Sheikh. 1975). Another effective
from the cilia ofabalone larvae <\V ,cka and Morse. 1991; method is to employ a polymeric system with different
Baxter and Morse. 1992). repeating units. Peptides. a well-known class of polymer,
Remarkably few attempts ha\e been made to characteri/e are logical signal molecules within organisms and aquatic
the structures of pheromones oilier than sperm attractants. environments for several reasons. First, because of the
Courtship and mating pheromones can be difficult to iden- charged nature of the terminal primary amine and carbox-
tify because breeding seasons are short and materials hard to vlic acid groups at neutral pH. peptides are water-soluble
obtain. Specific courtship behavioral acts are often trouble- and not volatile. Second, the machinery (enzymes), tem-
some to discriminate from other activities, thus making plates (DNA. through mRNA). and structural units (amino
bioassay of active material impossible in some cases. Still, acids) for producing peptides are already in every living
outstanding progress has been made towards elucidating the organism (Lehningerctul.. 1993). Third, using the 20coded
structures of mating pheromones in brown algae (Maier and amino acids available in eukaryotic systems, a vast variety
Muller. 19S6: Boland. 1945). polychaete worms (Zeeck ct of information can be presented in a short amino acid
<//.. 1994: Hardege el til.. 1996). and fishes (I)ulka ct til.. sequence: with as few as five ammo acids, there are 205 :
1987: Sorensen. 1992). \\'hereas terpenes and other hydro- 3.2 million possible unmodified peplides. Fmallv. intracel-
carbons appear to be the principal pheromones in worms lular and extracellular proteases can degrade peptides to
and brown algae, steroid hormones and their metabolites their constituent amino acids, thus terminating signal initi-
produced by ovulating female fish are potent attractants to ation (but not necessarily propagation: Hughes. 1978; De-
mature males in some species. cho etal., 1998).
Gamete recognition factors embedded in cell membranes In fact, peptides are emerging as important chemical cues
have been identified for a varietv of marine organisms. in marine environments (Rittschol. I99()|. Recent work with
These substances plav a critical role in establishing barriers sand dollar, abalone. and oyster larval settlement (Burke.
to cross-fertili/ation between individuals, thus leading to 1984: Morse and Morse. 1984: Zimmer-Faust and Tarn-
genetic isolation and speciation in the sea (Knowlton. 1993: burn. 1994) indicate that the inducing agents are small
Palumbi. 1994). In sea urchins, for example, glycoproteins peptides from conspecifics or plants associated with juve-
located in the egg vitelline envelope are recognized by the nile habitats (Table 1 1. Nitrogen fixation and heterocyst
sperm acrosome protein, bindin. Bindin has lectin-like prop- formation in cvaiiobacteria is inhibited by peptides (Yoon
erties enabling it to bind egg glvcoprotcins il oh/ and Lan- and Golden. 1998). whereas abdominal pumping (for larval
narz, 1994: Hofmann and (ilabe. 1994). In abalone sperm. release and dispersal) in mud crab is stimulated by small
lysin a rapidly evolving protein recogni/es species spe- peptide cues (Forward ct n/.. 1987). Remarkably, these
cific glycoproteins of the egg vitelline envelope (Lee and peptide signals in ovsteis. mud crabs, and cyanobacteria are
Vacquier. I992(. Similarly, in rotifers, surface glycopro- all structurallv related to the carboxy-terminal sequence of
teins on the female body surface bind to unique receptor mammalian C5a anaphylatoxin. a potent white blood cell
proteinson the male coronaand confer species speciliciiv in chemoattractant. The receptors responsible for transmitting
mating (Snell ct til.. 1995). Thus, fertili/ation in marine peptide signals in marine organisms have yet to be isolated
organisms is often controlled by chemical communication and characterized. Nevertheless, quantitative structure-ac-
operating at the surface membranes of sperm and eggs. tivity relationships (QSARs) have been modeled to relate
l'i"'eins. peptides. organic nitrogen bases, carbohydrates, the physicochemical properties of signal molecules to their
fatty and humic acids, and other types ofchemicals are all biological functions (Browne ct til.. 1998). Similarities be-
putatiu igents mediating ecological processes in the ocean iwecn the anaphylatoxins and the oyster/mud crab/cya-
(Gurin and ('arr. 1974: Pawlik and Faulkner. I'S(,; nobacleria peptides suggest that there may be homology
Rittschof. I 190; forward ct til.. 1997; Krug and Man/i. among their respective receptors. Sequence analysis ol the
1999). Such wide diversity in the structures has. perhaps. receptor protein for C5a indicates that it belongs to the
slowed progress inwards isolating and identifying specific rhodopsin superlamilv (Houlav ct ul.. 1991; Gerard and
chemical markers because different unahlical approaches Gerard. ll)')li. Members of the rhodopsin receptor family
CHEMICAL SIGNALING PROCESSES 111
Tahlt 1
E-\am/'les ofnaturalpeptide signal molecules ortheirsvntheticanalogs
Environment