A Comparison of Terrestrial and Marine Chemical Ecology
Chuck Lang
Colorado State University
Fort Collins, Colorado 80523
Chemical Ecology EN570
Spring 1994
Abstract: Both marine and terrestrial plants produce a diversity of
secondary metabolites that deter feeding by herbivores; differences
occur primarily by virtue of the available elements in the sea. While
similarities do exist, it is apparent that marine organisms have
developed secondary metabolic pathways that are distinct from
terrestrial systems. Evidence available from marine communities
suggests that terrestrial models of plant-herbivore interactions and the
types of chemical defenses that have evolved (qualitative vs
quantitative) cannot be applied to the marine environment.
Introduction
The importance of secondary plant compounds in reducing herbivory
in terrestrial communities is well studied and generally viewed as being
one of the most effective defensive mechanisms. In contrast to the well-
studied interactions between terrestrial plant metabolites and
herbivores, the potential importance of seaweed secondary compounds on
marine herbivores are largely un-investigated. Only within the last
decade have researchers began to realize the biological potential of
marine secondary metabolism. As in terrestrial ecosystems, marine plant
communities must escape, deter or tolerate herbivory in order to
persist. A comparison of chemical defense in marine versus terrestrial
communities raises the following questions: 1) How does marine
secondary metabolism compare to that of terrestrial communities? 2)
Can present terrestrial plant-herbivore theories be applied to the
marine environment?
I Contrasts in Marine - Terrestrial Secondary Metabolism
Elemental Composition Both marine and terrestrial plants produce a
diversity of secondary metabolites that deter feeding by herbivores;
differences occur primarily by virtue of the composition of available
elements in the sea (Hay and Fenical 1988). The halide - rich marine
environment has facilitated the incorporation of bromine, chlorine and
iodine into organic structures. These elements are not only
incorporated into diverse structure types, but also appear to play an
essential role in terpene biosynthesis. The occurrence of halogens in
terrestrial secondary metabolism is a rare process observed only in a
few microorganisms (Fenical 1982).
Although sulfur concentration is high in seawater, primarily as
sulfate (2700 mg/liter), the reduced organic form of the element is rare
in marine secondary metabolism (Fenical 1982). A few novel examples do
exist, however, including the isolation of nereistoxin (1), a disulfide
from the marine worm Lumbriconereis heteropoda (Okaichi and Hashimoto
1967). Nereistoxin isolation provided the framework for the
structurally related insecticide Padan (2), commonly used in Japan (Fig.
1). One example illustrating similar biosynthetic pathways in marine
and terrestrial systems is the polysulfide, lenthionine (3), isolated
from the red seaweed Chondria californica (Wratten and Faulkner 1976).
Lenthionine had previously been associated as a antibacterial component
of the mushroom, Lentinus edodes.
Terpene Biosynthesis
Perhaps the most significant modification in marine secondary
metabolism can be found in terpene biosynthesis. Terpenes are common in
both marine plants and animals and their formation via the condensation
of isopentenyl pyrophosphate units is similar to terrestrial metabolism.
The emphasis in the marine environment is found largely in the
production of higher weight terpenes, particularly the diterpenes. On
land, however, the occurrence of monoterpenes is a prominent feature of
many common plants (Fenical 1982).
A modification of considerably more interest is found in the
incorporation of halogens, particularly bromine, in the primary
production of terpenes via cyclization reactions. On the basis of
structural features the production of cyclized terpenoids in terrestrial
systems involves modifications of the monoterpene precursor geraniol,
followed by a hydrogen ion-induced cyclization to produce the
carbocyclic ring (Fig. 2). In marine plants this process is replaced by
a bromine - induced cyclization, perhaps involving an electron -
deficient bromonium ion (Fenical 1975). This terpenoid process
utilizing bromine is common in marine organisms and approximately 400
haloterpenoids have been isolated (Hay and Fenical 1988).
Marine Alkaloids Basic, nitrogen-containing compounds (alkaloids) are
common components of terrestrial plants but rare and perhaps even
completely absent in the marine environment (Hay and Fenical 1992). Two
reported references of 'true' marine alkaloids were both isolated from
marine sponges (Fig. 3). Flustramine A (4), isolated from the marine
sponge flustra foliacea, is a brominated alkaloid (Carle and
Christophersen 1979). The second example is an isoquinoline alkaloid,
renierone (5), isolated from the sponge Reniera (McIntyre and Faulkner
1979).
Marine Acetogenins
Acetogenins are linear, non-branched compounds normally produced from
the condensation of C2 acetate units via the precursor, acetyl-coenzyme
A . This primary metabolic pathway is responsible for the production of
plant lipids and fatty acids. In both marine and terrestrial organisms
modifications of this pathway yield secondary metabolites of unique
biological significance. Within the acetate pathway several marine
species produce molecules that are unprecedented in terrestrial systems.
Perhaps the most noteworthy example of unique acetogenins
synthesis is that of the red seaweed Asparagopsis taxiformis. This
plant, reported to be highly odorous, produces large amounts of
halomethane type derivatives 6 - 10 (Fig. 4) (McConnell and Fenical
1977). Halogenated methanes are considered to be potent biocides adding
to the unpredictability of their natural synthesis. Asparagopis also
produces small amounts of chloroform (9) and carbon tetrachloride (10),
considered to be totally manmade and possible carcinogens (Lovelock et
al. 1973).
Two more examples of marine acetogenins are brevetoxin B (BTX-B)
and palytoxin, both being the subject of considerable investigation over
the past two decades due to their significant economic impact to costal
areas. Outbreaks of the toxic marine dinoflagellate Gymnodinium breve
("Red-tide") may result in massive fish and bird mortalities as well as
considerable discomfort to humans from consuming toxic oysters and
clams. Lin (1981) was the first to characterize the G. breve toxins, BTX
- B, (Fig. 5) as being a C 50 polyether. Polyethers are considered to
be ion chelators, possibly accounting for the potent biological activity
of the G. breve toxins.
Palytoxin, or "Limu-make-o-Hana" by its Hawaiian name, is a highly
toxic marine compound isolated from the zoanthid coral Palythoa (Fig.
6). The early Hawaiians recognized the potent toxicity of this organism
and applied it to the tips of their spears as a poison. Palythoa
species are abundant in most tropical waters with many species reported
to be at least "moderately toxic" (Fenical 1982). The palytoxin
isolated from P. toxica is thought to be one of the most poisonous
nonproteinaceous substances known (Moore 1971 and Scheuer).
Moore (1971) and his associates in Hawaii were the first to
successfully elucidate the structure of this highly complex compound.
Palytoxin is comprised of a linear arrangement of 115 carbon atoms with
8 methyl groups and the somewhat uncommon two cyclic ketal
constellations which are part of 11 ether linkages. Even by todays
current standards and technological advancements, the successful
characterization of this complex compound should be considered a major
achievement.
While similarities do exist it is apparent that marine organisms
have developed secondary metabolic pathways that are distinct from
terrestrial systems. However, the original question of how secondary
metabolism compares in these two communities may be somewhat unresolved
primarily due to the nature of the distinct taxa that occurs within
these two environments.
II Can terrestrial plant-herbivore theories be applied to the
marine environment?
Co-Evolution
Secondary plant metabolites have been shown to play a major role in
susceptibility of terrestrial plants to herbivory (Rosenthal and Janzen
1979, Coley et al. 1985). Even though the defensive nature of these
plant secondary metabolites has been clearly demonstrated, it is not
unusual to find specialist herbivores that have evolved a tolerance to
these compounds (Rosenthal and Janzen 1979, Crawley 1983). The majority
of these specialist feeders tend to be relatively immobile larvae of
small invertebrates (Ehrlich and Raven 1965, Freeland and Janzen 1974).
In contrast to the well-studied patterns seen in terrestrial
systems, marine communities are dominated by a diverse assemblage of
generalists grazers such as fishes (Hay 1991), urchins (Lawrence 1975)
and gastropods (Duffy and Hay 1990) that feed from many plant types and
families. It has been estimated that about 90% of herbivorous insect
species feed on three or fewer plant families (Bernays 1989) while
marine herbivores are considerably more opportunistic, often feeding on
more than 20 plant families and even supplementing their diets with
animal material (Hay and Fenical 1988). Thus, the potential for closely
linked co-evolution between pairs of interacting species in the marine
environment would be less likely than that which might occur in
terrestrial communities.
The potential for co-evolution in the marine environment may be
further discounted by considering two fundamental differences between
terrestrial and marine communities. First, most insects have generation
times that are usually much shorter than those of the plants on which
they feed. Theoretically this should allow insects to adapt to plant
defenses faster than plants can respond to acquired insect feeding
preferences. In marine communities, this may not be the case. Fishes
and sea urchins, the primary herbivores within the marine environment,
have generation times that are similar or even greater than the seaweed
on which they graze (Hay and Fenical 1988).
The second fundamental difference between these two herbivore
communities is in the manner of host selection by juveniles. In many
specialized insects, adults are highly mobile and selectively search
large areas so as to carefully oviposit their offspring on appropriate
hosts. In contrast to this, herbivorous fishes and sea urchins have
larval stages that are liberated into a large ocean with only a slight
ability to choose a particular micro-habitat. Additionally, larvae
approaching costal area are subjected to intense predation and therefore
may be constrained or discouraged from approaching multiple times to
select for a rare host plant (Hay and Fenical 1988). These factors
should select for generalists feeders that can utilize a wide variety of
host plants and minimize the potential for reciprocal coevolution.
It should be mentioned, however, that some small marine organisms
(mesograzers) are specialized to certain host plants (Hay et al. 1987).
These herbivores also tend to be exceptions to the patterns in
generation times and means of dispersal as outlined above. Mesograzers
such as amphipods brood their young or undergo direct development and
therefore avoid random dispersal stages. These differences between
mesograzers and larger marine herbivores could explain, in part, why
some mesograzers have adapted to seaweed chemical defenses that
effectively deter generalists feeders (Hay and Fenical 1992). It
appears, however, that these mesograzers have only a marginal impact on
plant fitness so the potential for true co-evolution between mesograzers
and their prey is probably limited (Carpenter 1986; Lewis 1986; Hay and
Fenical 1992).
Plant apparency and resource availability models
One of the most influential models to provide a conceptual framework for
plant-herbivore interactions has been the plant apparency model (Feeney
1976; Rhoades and Cates 1976). This model contrasted two different
plant types, long lived and short lived, and attempted to explain
fundamental differences in their defensive strategies. Long lived or
slow growing plants, that commonly dominated climax communities were
'bound to be found' and termed apparent plants. These apparent type
plants would have to invest heavily in defenses that were generalized
and effective against a broad range of herbivores. Tannins were
proposed to fill this role by acting as digestibility reducers with
little possibility of counter adaption on the part of herbivores. Since
tannins were thought to function in a dose dependent manner they were
termed as a quantitative defensive mechanism.
In contract, fast growing, short lived plants that were
unpredictable in space and time were termed unapparent plants since
plants with these characteristics would be more likely to escape
detection by herbivores. Because this plant type allocated most of
their resources to rapid growth, reproduction and dispersal, unapparent
plants should be defended by relatively inexpensive toxins that would be
effective in low concentrations by generalists herbivores. However,
specialist herbivores should evolve the ability to circumvent these
toxins by a variety of detoxification mechanisms. Because the toxicity
of these compounds was thought to be effective at low concentrations
they were termed qualitative defenses. According to this model,
apparent plants were thought to differ from unapparent plants in three
primary ways (Fox 1981):
1. the overall amount of resources invested by the plant
for defense;
2. the types and modes of action of compounds used for
defense, for example digestibility reducers versus
toxins; and
3. the underlying potential for co-evolution of plants and
their corresponding herbivores.
A somewhat more recent model (Coley et al. 1985) explains the above
observed patterns as attributable to a plant's available resources
rather than its apparency. The resource availability model retains many
of the same distinctions regarding differences in costs and effects of
qualitative versus quantitative defenses. Both of these models were
developed based on terrestrial-herbivore interactions but the ecological
and evolutionary generalities upon which the models were formed suggests
that they should apply equally well to plant-herbivore interactions
within the marine environment as well.
Application of the plant apparency theory to the marine
environment would predict that apparent seaweeds, such as kelps, should
have high levels of phlorotannins as compared to the less apparent
Fucales but the available data indicates the opposite pattern (Estes and
Steinberg 1988, Steinberg 1985). The resource availability model would
predict that seaweeds in nutrient rich habitats (shallow temperate
seaweed beds) would have lower phlorotannin levels as compared to
seaweeds with less nutrients available (shallow coral reefs); this
again, is not the case. Phlorotannins are common and relatively
abundant in temperate brown algae but nearly absent altogether from
similar tropical species (Steinberg 1989).
Additionally, apparent seaweeds on shallow tropical reefs are
attacked by a wide variety of generalists predators (Hay and Fenical
1992). Even though herbivory can be extreme in these areas (losses of
60-100% of primary production), seaweeds produce little, if any,
phlorotannins but rather seem to rely on qualitative defensive compounds
such as terpenes (Steinberg 1989). Both the plant-apparency model and
the resource availability model would predict the opposite; these plants
should be defended by phlorotannins rather than qualitative defenses.
Both of the above models make the major assumption that high
concentrations of quantitative type defenses (tannins) are more costly
than low concentrations of more toxic qualitative defenses (terpenes or
alkaloids). While it is apparent that more energy is stored in
quantitative type defenses it is not clear, however, that energy can be
correlated with costs. Toxins could actually be more expensive than
tannins in some cases due to the fact that once tannins are produced
they appear to have minimal maintenance costs (Fox 1981). Additionally,
seaweeds are often nutrient poor and carbon rich, and they may leach
large amounts of carbon when resources are limited and the excess carbon
cannot be used for growth (Hay and Fenical 1992). It is therefore
possible that phlorotannins may serve at times as simply a means to
store excess carbon and may constitute no cost at all to the plant.
From the above examples it is apparent that previous
generalizations about the effectiveness and mode of action of
qualitative versus quantitative chemical defenses cannot be applied to
the marine environment. Just as a single compound can have a
considerable variation on its effects on the feeding of different
herbivores, very similar compounds can differ markedly in their effects
on the same or similar herbivores. Although terrestrial ecologists have
often undertaken investigations of plant chemical defenses by simply
lumping compounds into classes and assuming that these classes of
compounds have similar biological activities, this is apparently not a
useful approach for the marine ecosystem.
While similarities do exist between marine and terrestrial
organisms, it is apparent that the secondary metabolic processes that
have evolved in the marine environment are distinct from their
terrestrial counterparts. Marine and terrestrial plants comprise
different taxonomic groups making comparisons somewhat difficult and
forcing crude generalizations. However, focusing on the similarities
and differences in these two communities may provide clues to factors
affecting the evolution of plant-herbivore interactions in general.
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