Download The ecology and evolution of seaweed

Coral Reefs (1997) 16, Suppl.: S67—S76
The ecology and evolution of seaweed-herbivore
interactions on coral reefs
M. E. Hay
University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, NC 28557, USA
Phone: 919—726—6841 ext. 138 FAX: 919—726—2426 E-mail: [email protected]
Accepted: 18 November 1996
Abstract. Because seaweeds grow rapidly and are easy to
manipulate, they have provided a wealth of information
on how consumers affect coral reef community organization. Herbivory is the dominant force affecting the distribution and abundance of reef seaweeds, with seaweed
morphology, structure, chemistry, and competitive ability
often being a function of herbivory by fishes and larger
invertebrates. Seaweeds that deter these herbivores become the favored living sites and foods of smaller, less
mobile mesograzers that derive protection from consumers by associating with defended hosts. Host specialization reduces mesograzer susceptibility to predation
through crypsis, sequestration of chemical defenses, and
reduction of encounters with consumers. Mesograzers can
serve as either pests or mutualists, depending on their
feeding behavior and how it affects the host. Some mesograzers protect hosts from competitors while others attack
hosts, causing induction of chemical defenses. More limited studies of corals and sponges parallel findings for
seaweeds.
Introduction
Seaweeds are rarely studied by coral reef ecologists. Of the
nearly 400 papers that have been published in Coral Reefs
since the journal’s inception, 46% focus on corals, 22% on
other invertebrates, 9% on fishes, 7% on seaweeds, and
16% deal with other topics such as physical processes,
biogeochemical cycling, and methodology. Most of the
papers dealing with seaweeds were published in a special
issue devoted to Halimeda, leaving only about 3% of the
regular publications devoted to seaweeds. The minimal
focus on seaweeds appears appropriate if one looks at
their abundance on many reefs. However, this view misses
the point that, if they are not removed by herbivores, they
are the competitively dominant organisms on coral reefs
and are capable of destroying reefs as we know them
(Hughes 1994). Although studying macrophytes on reefs
often borders on the study of what is not there, the small
size and robustness of reef seaweeds make experimental
transplantation remarkably easy, and the high productivity of reef seaweeds allows growth rate responses to be
measured in days rather than months or years (Hay 1981a,
1985; Hay et al. 1983; Lewis 1986; Carpenter 1988). Seaweeds are, therefore, exceptional tools for studying the
basic processes affecting population and community organization on coral reefs. Below, I provide an overview of
general ecological and evolutionary insights that have
been provided by the study of reef seaweeds. Because
recent investigations of sponges (Dunlap and Pawlik
1996) and corals (Littler et al. 1989) both found patterns
and processes mirroring those known for seaweeds, seaweed investigations may provide a template for understanding the ecology and evolution of coral reefs in
general.
Herbivory on coral reefs
Although seaweed distribution and abundance are determined by the interactive effects of herbivory, competition,
and physical disturbances or stresses (Littler and Littler
1984; Steneck and Dethier 1994), repeated experiments on
coral reefs have documented the overwhelming importance of herbivory in most situations (Randall 1965; Hay
1985, 1991a; Lewis 1986; Carpenter 1986; Lessios 1988;
Morrison 1988; Hughes 1994; Hixon and Brostoff 1996).
Herbivores commonly remove almost all seaweed biomass on shallow fore reefs, leaving primarily encrusting
corallines, which are resistant to herbivore removal, and
small rapidly growing filamentous algae that tolerate herbivory by rapidly replacing lost tissues (Steneck 1988;
Duffy and Hay 1990).
On topographically complex portions of coral reefs,
herbivorous fishes bite the bottom at rates of 20 000 to
156 000 bites/m2/day, and either fishes alone or, in some
locations, sea urchins alone can remove nearly 100% of
algal production (Hatcher and Larkum 1983; Carpenter
1986, 1988; Klumpp and Poulunin 1989). Rates of herbivory on coral reefs exceed rates measured in any other
habitats, either terrestrial or marine (Carpenter 1986).
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These high rates are generated by the high density and
diversity of reef herbivores, the high metabolic rates of
some species (e.g., fishes) and high densities of others (e.g.,
sea urchins), and by the need for herbivores to consume
large masses of low protein algae in order to acquire
adequate nitrogen for growth and reproduction (Mattson
1980; Horn 1989). As an example, in their quest for adequate protein, herbivorous fishes on the Great Barrier
Reef have been estimated to consume 10 times as much
carbon as is needed to meet their energetic needs (Hatcher
1981). The high productivity of reefs combined with the
tight coupling between production and consumption result in plant-herbivore interactions being one of the dominant forces affecting community structure as a whole.
The studies cited provide a wealth of experimental
demonstrations of the strong effects that herbivores have
on seaweeds and the strong effects that seaweeds can have
on other reef organisms (Hughes 1994). Grazing scars left
in fossilized coralline algae demonstrate a long evolutionary history of herbivory on coral reefs (Steneck 1983). To
persist on reefs, seaweeds must escape, tolerate, or deter
herbivory (Lubchenco and Gaines 1981). In this work
I concentrate on determining (1) which types of herbivores
have the greatest impact on reef seaweeds, (2) seaweed
traits that deter these herbivores, and (3) the indirect
effects of these defensive traits on non-target organisms
and on reef communities in general.
Herbivores and their effects on reef seaweeds
Reefs may be populated by diverse groups of herbivores
including fishes, sea urchins, turtles, manatees, dugongs,
crabs, amphipods, polychaetes, and other invertebrates.
The diversity of herbivore life histories, sizes, mouth parts,
and digestive physiologies makes it difficult, if not impossible, for reef seaweeds to escape or deter all herbivores.
However, if seaweeds are to persist on reefs, they have to
decrease herbivory to levels that allow production to
exceed removal. Many experimental studies have
documented the large and direct effects of fishes and sea
urchins on coral reef seaweeds (see reviews by Birkeland
1989; Hay 1991a). As an example, when Lewis (1986)
excluded fishes from shallow reef areas in Belize for 10
weeks, abundance of palatable macroalgae increased dramatically, overgrowing and killing corals and several less
palatable seaweeds. When fishes were allowed to re-enter
this area, virtually all of this increased algal mass was
consumed within 48 hours. Equally dramatic results occur
when sea urchins are excluded from reefs where they are
abundant (Carpenter 1986; Morrison 1988; Lessios 1988).
In many instances, palatable seaweeds persist in tropical
communities only because they grow in mangroves, seagrass beds, reef flats, or topographically simple areas that
serve as spatial refuges from reef herbivores (Hay 1981a,
1984b, 1985, 1991a), apparently because herbivores are at
greater risk of predation in these habitats.
Several studies suggest that overharvesting of fishes on
coral reefs may allow sea urchin populations to expand
because of fewer predatory and competing fishes (Hay
1984a; Hay and Taylor 1985; Carpenter 1986, 1990;
McClanahan and Shafir 1990). When Carpenter (1986)
evaluated grazing by fishes versus sea urchins on a reef in
St. Croix, he found that the groups had different effects on
algal standing stock, but that either fishes or sea urchins
alone could remove virtually all algal production. This
suggests that removal of sea urchins alone or fishes alone
might not significantly decrease herbivory on seaweeds in
this habitat; however, recent events have shown that removal of both groups allows seaweeds to escape control
by herbivores, sometimes killing entire reef systems.
Hughes (1994) provides impressive documentation of how
overfishing of reefs in Jamaica did not appear to have
dramatic effects on the reefs until the sea urchin Diadema
antillarum, which occurred there in very high densities,
experienced a mass mortality due to disease (Lessios
1988). Once neither herbivore group was common on
Jamaican reefs, seaweed cover increased from 4% to 92%
and coral cover declined from 52% to 3% on the 9 reefs
Hughes studied along 300 km of coastline. The increased
cover of seaweeds prevented coral recruitment, killed
many adult corals, and effectively destroyed Jamaican
reefs.
Although other herbivores, such as crabs (Coen 1988;
Stachowicz and Hay 1996), chitons (Littler et al. 1995), or
limpets (Steneck 1997) can have important effects on
a limited spatial scale, fishes and larger invertebrates like
sea urchins appear to be responsible for most herbivory
on coral reefs (Carpenter 1986; Klumpp and Pulfrich
1989; Hay and Steinberg 1992). That these groups exert
stronger effects on tropical coral reefs than on temperate
rocky reefs is also indicated by the recent findings that
both temperate and tropical sea urchins prefer temperate
over tropical seaweeds and that most of those preferences
can be explained by the greater deterrency of chemical
extracts from the tropical seaweeds (Bolser and Hay 1996).
Thus, greater herbivory on tropical reefs appears to have
resulted in more potent chemical defenses among tropical,
as opposed to temperate, seaweeds.
All of these considerations suggest that selection for
traits that deter reef herbivores will be greater in tropical
than in temperate areas and will be generated by a diverse
assemblage of generalist fishes and invertebrates that differ in mobilities, habitat requirements, feeding modes, and
digestive physiologies. In the face of this type of diffuse
herbivore pressure (Fox 1981), selection should favor seaweeds with traits that are broadly active against numerous
types of herbivores. Because single groups of herbivores
such as fishes alone or sea urchins alone are capable of
consuming all algal production in some habitats (Carpenter 1986), the evolution of species-specific or even groupspecific herbivore deterrents may be of limited value unless they are coupled with additional defenses that deter
other herbivores. This may be why seaweeds on herbivore-rich coral reefs so commonly employ combinations
of structural, morphological, and chemical defenses and,
in some cases, coordinate these defenses with patterns of
temporal and microhabitat escape (Hay 1984b; Paul and
Hay 1986; Lewis et al. 1987; Paul and Van Alstyne 1988a;
Hay and Fenical 1988; Hay 1996). Some secondary
metabolites that have been demonstrated to be broadly
deterrent against a wide variety of reef herbivores can
also function to deter fouling or possibly microbial pathogens (Schmitt et al. 1995). These multiple roles for single
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metabolites further limit the importance of individual
herbivore species in selecting for particular plant traits.
Seaweed defenses against herbivores
Tropical seaweeds possess morphological, structural, mineral ("CaCO ), and chemical traits that deter reef herbi3
vores (Hay and Fenical 1988, 1996; Duffy and Hay 1990;
Hay and Steinberg 1992; Paul 1992; Hay 1996). Many
seaweeds combine several of these defensive traits and, in
some instances, these act additively or synergistically to
reduce losses to herbivores (Hay et al. 1994; Schupp
and Paul 1994; Meyer and Paul 1995; Hay 1996; Pennings
et al. 1996).
Morphological and structural deterrents
Seaweeds vary tremendously in their size, shape, toughness, degree of calcification, and thus susceptibility to
being bitten or damaged by herbivores. Herbivore mouth
parts, biting force, and digestive physiology also vary
considerably, affecting how seaweeds may interact with
different herbivores. Littler, Steneck, and their co-workers
have developed general models of how seaweed productivity and susceptibility to being eaten change as a function of seaweed morphology (Littler and Littler 1980;
Steneck and Watling 1982; Littler et al. 1983a,b; Steneck
1983; Steneck and Dethier 1994). They predict that microalgae are most susceptible to herbivores and that resistance to herbivores increases in the following order:
filamentous algae, sheet-like algae, coarsely branched algae, leathery or rubbery algae, jointed calcareous algae,
and crustose corallines (see Fig. 1 in Steneck and Watling
1982 or Table 1 in Littler et al. 1983a). This hierarchy is
based in part on the decreasing food value that should
occur as seaweeds devote more of their mass to indigestible structural materials that make them tougher and
more difficult to bite. Feeding patterns of molluscs
(Steneck and Watling 1982) and sea urchins (Littler et al.
1983a, b) are somewhat supportive of this hypothesis. Assays with reef fishes have been more variable (Hay 1991a).
Littler et al. (1983b) found patterns supporting the model.
However, using a larger data set from multiple reefs, Hay
(1984b) found that only the extreme ends of the morphological spectrum differed significantly in their susceptibility to herbivores. The model had limited predictive
value in the central portion of the morphology-susceptibility spectrum (also see Lewis 1985). Both Hay (1984b)
and Paul and Hay (1986) also found that many of the
tougher or calcified seaweeds produced unusual secondary metabolites that could act as chemical defenses, thus
potentially confounding the effects of chemical and morphological traits.
A few studies have addressed directly the effects of algal
morphology on susceptibility to herbivores. Steneck and
Adey (1976) demonstrated that the encrusting coralline
¸ithophyllum congestum grew as a smooth crust on subtidal reef slopes where feeding by fishes was intense but
produced upright branches when it grew on the edges of
reef flats where herbivory by fishes was reduced. Production of upright branches allowed enhanced growth and
reproduction but also increased susceptibility to parrotfishes, which precluded the upright morphology from the
reef slope. Hay (1981b) found that clonal seaweeds like
Halimeda, Dictyota, and ¸aurencia could occur as loose
aggregations that grew rapidly but had increased susceptibility to herbivorous fishes and sea urchins, or they could
occur as densely packed colonies of uprights that had
lowered susceptibility to herbivores but also lower rates of
growth due to increased self-shading and diffusion gradients. On reef areas most affected by herbivores, these
species occurred as tightly packed colonies. On reef areas
minimally affected by herbivores, they occurred as loosely
arranged uprights that could grow more rapidly.
One of the more dramatic examples of morphological
shifts in response to herbivory was investigated by Lewis
et al. (1987). They documented a striking morphological
dichotomy for the brown seaweed Padina jamaicensis and
demonstrated that the different forms were a direct result
of spatial patterns in grazing by herbivorous fishes. In
heavily grazed areas, Padina grew as an uncalcified turf of
small, irregularly branched and prostrate axes that were
tightly attached to the substratum by rhizoids produced
on ventral portions of the thallus. Branches on this form of
the alga terminated in a single apical meristem. On areas
of the reef where herbivory was slight, Padina grew as
a calcified, upright, and foliose blade with the entire margin of the blade being composed of meristematic cells (see
Fig. 1 in Lewis et al. 1987). These two forms are so
dissimilar that taxonomists initially placed the two forms
in different genera (the turf form being designated as
Dictyerpa, »aughniella, or Dilophus). When herbivorous
fishes were excluded from heavily grazed portions of the
reef, the uncalcified turf form started growing as the calcified upright form within 96 h. After a few weeks of herbivore exclusion, the upright form began overgrowing and
killing reef corals. A series of transplant and caging experiments demonstrated that the upright form of Padina grew
rapidly, reproduced, and was a superior competitor; however, it was highly susceptible to removal by herbivorous
fishes. In contrast, the turf form could persist in areas of
high herbivore impact, but it did not outcompete other
reef species and was never observed to reproduce. These
examples indicate that morphological plasticity helps seaweeds persist in areas that are heavily grazed but that the
morphologies that resist herbivory entail a significant cost
in terms of growth and reproduction.
Calcification as a deterrent
Calcification of seaweeds has generally been viewed as
deterring herbivory by making seaweeds harder and more
difficult to bite or by diminishing their nutritional value
due to the addition of indigestible structuring materials
(Littler and Littler 1980; Steneck 1983, 1986; Hay 1984b;
Duffy and Hay 1990; Targett and Targett 1990; Duffy and
Paul 1992; Pennings and Paul 1992; Pitlik and Paul 1997).
These assumptions are consistent with the fact that
CaCO -containing seaweeds are often relatively low
3
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preference foods for reef herbivores (Littler et al. 1983a,b;
Hay 1984b; Paul and Hay 1986; Steneck 1988). However,
although the increased hardness of the thallus undoubtedly prevents some herbivores from feeding on heavily calcified seaweeds (Steneck and Watling 1982), many reef
herbivores (e.g., parrotfishes, sea urchins) can easily bite
into calcified seaweeds, and several recent investigations
indicate that the CaCO in seaweed thalli may actually
3
serve as a chemical, as well as a structural, deterrent (Hay
et al. 1994; Schupp and Paul 1994, Meyer and Paul 1995;
Pennings et al. 1996).
Pennings and Paul (1992) developed methods for
adding CaCO to artificial foods to test its effects on
3
herbivore feeding preferences. This method mimics the
presence of CaCO in an algal food but does not increase
3
hardness. This methodology was modified by Hay et al.
(1994) so that algal-based foods could be created that
differed only in the presence of CaCO , not in food value
3
or toughness. Assays with gastropods, fishes, sea urchins,
and amphipods indicated that CaCO could significantly
3
affect the feeding of some species of these herbivores, even
when the CaCO was added in a way that had no effect on
3
the nutritional value or toughness of the food (Pennings
and Paul 1992; Hay et al. 1994; Schupp and Paul 1994).
The study by Schupp and Paul (1994) gave the clearest
indication of what mechanisms might be operating to
produce this effect. Adding CaCO to foods significantly
3
decreased the feeding rates of fishes with acidic digestive
tracts, but stimulated, or did not affect, feeding by fishes
with neutral or more basic guts (also see Hay et al. 1994;
Meyer and Paul 1995; Pennings et al. 1996). These patterns suggest that CaCO may deter feeding for some
3
species because of the neutralizing effect that it would
have in a low pH gut and possibly because of the large
amount of CO that would be released. These findings do
2
not diminish the potential importance of CaCO in defend3
ing seaweeds by increasing their hardness (Pitlik and Paul
1997), but they do indicate that CaCO can also deter
3
herbivory in other ways, possibly by functioning as a chemical defense. Schupp and Paul (1994) suggested using the
term mineral defense to distinguish this chemical effect
from that of CaCO serving as a hardening agent or from
3
the chemical effects of bioactive secondary metabolites.
Recent work also has demonstrated that the CaCO
3
contained in seaweeds need not lower their nutritional
value as foods and that, in fact, the heavily calcified
corallines may provide as much, or more, metabolizable
plant mass per bite than most other macrophytes on the
reef (ME Hay and QE Kappel in preparation). Most reef
herbivores consume and process food on a volumetric
basis (i.e., how much nutrition does a seaweed yield per
bite, per mouthful or per gut full?). Viewing seaweed cross
sections in a basic phycology text shows that many seaweeds are largely water rather than nutritious plant cytoplasm (e.g., the internal volume of many fleshy seaweeds
largely comprises of water-filled medulary cells that
have minimal nutritional content). In the calcified seaweeds, CaCO can simply replace water and thus need
3
not dilute the nutritional value of the plant per bite.
Additionally, many calcified red seaweeds are composed
of densely packed cells that are filled with organelles
and storage products rather than water. We recently
measured the ash-free-dry mass (AFDM) per volume of 40
species of seaweeds and found that heavily calcified seaweeds
like Halimeda, Penicillus, Amphiroa, and Neogoniolithon
could contain 0.6 to 5.6 times as much AFDM per volume
as fleshy seaweeds like ¸aurencia, Acanthophora, Gracilaria,
or Dictyota. Most investigators might have assumed that
the fleshy species would have been more nutritious because
of the absence of calcification. For the 40 species investigated, there was no significant difference in AFDM/volume between calcified and noncalcified seaweeds. Thus,
incorporation of CaCO into algal thalli may not lower
3
the alga’s nutritional value to an herbivore, and ‘‘structural’’ traits like calcification can also be acting as chemical defenses. Given that both defensive metabolites and
the digestive processes of consumers are sensitive to changes in gut pH, there is considerable potential for CaCO
3
to change gut pH in ways that alter digestive efficiency
and affect the activities of algal secondary metabolites
(Hay et al. 1994).
Secondary metabolites as deterrents
Investigations of how secondary metabolites produce
among-species differences in susceptibility to consumers
have provided insights into factors (a) driving ecological
specialization (Hay 1992), (b) affecting population and
community organization (Hay 1984b, 1991a; Morrison
1988; Hay and Fenical 1996), (c) determining herbivore
feeding patterns and digestive efficiencies (Horn 1989; Hay
1991a; Pennings and Paul 1992; Targett et al. 1995; Lindquist and Hay 1995; Paul 1997), and (d) producing parallels and contrasts between marine and terrestrial
communities (Hay 1991b; Hay and Steinberg 1992). An
increased understanding of seaweed chemical defenses
thus provides insights into a wide range of ecological and
evolutionary topics.
Because herbivory in tropical marine systems is so
intense and because these systems are often more experimentally tractable and less disturbed than terrestrial systems, it has been possible to identify the most ecologically
important herbivores that should be used in laboratory
bioassays or to test compounds in the field to determine
their effectiveness against the diverse assemblage of herbivores that occur there (reviewed by Hay and Steinberg
1992). Thus, marine investigators can apply pure metabolites at natural concentrations to otherwise palatable
organisms or can imbed the metabolites in experimental
foods placed on natural reefs and determine in a very
short period of time whether or not the compounds decrease herbivory under natural field conditions (Hay et al.
1987b; Hay 1991a; Hay and Steinberg 1992; Paul 1992).
This ability to assay secondary metabolites under field
conditions on remote reefs where the densities and diversities of herbivores have been minimally affected by humans
is relatively unique to marine systems. In this respect,
marine investigators have some advantage over terrestrial
ecologists. Field bioassays of plant chemical defenses
have rarely been conducted in terrestrial communities.
Additionally, the tremendous changes in abundance of
terrestrial herbivores resulting from the Pleistocene extinctions, agricultural practices, deforestation, and other
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anthropogenic alterations to terrestrial communities
make it difficult to determine which types of herbivores
would have been most likely to have affected the evolution
of defenses in present-day plants. It is possible that the
tremendous focus on chemical-mediation of plant-insect
interactions in terrestrial systems is actually the study of
how compounds that evolved in response to 50 million
years of feeding by megaherbivores serendipitously affect
herbivorous insects now that the larger herbivores are
absent (Crawley 1989; Hay and Steinberg 1992). Coral
reefs provide a less disturbed evolutionary setting in
which to place chemically mediated plant-herbivore interactions.
In the last decade, a large number of investigations have
demonstrated that many seaweed secondary metabolites
strongly deter feeding by reef herbivores under both field
and laboratory conditions (for reviews, see Paul and Fenical 1987; Hay and Fenical 1988, 1992, 1996; Van Alstyne
and Paul 1988; Duffy and Hay 1990; Hay 1991a, 1996;
Hay and Steinberg 1992; Paul 1992). Most of the common
macrophytes on coral reefs (i.e., Halimeda, Penicillus,
ºdotea, Caulerpa, Chlorodesmis, ¸aurencia, Ochtoides,
Dictyota, Stypopodium, etc.) produce lipid-soluble chemical defenses that deter feeding by reef herbivores. Thus,
a large number of diverse seaweed secondary metabolites
deter herbivores; however, there can be considerable
variability in the effects of a given compound on different
herbivores or of related compounds on a single species of
herbivore (see Hay and Steinberg 1992; Schupp and Paul
1994). Reviews on the particulars of seaweed chemical
defenses have become a growth industry. Rather than
repeat this information I will focus on the general ecological patterns emerging from studies of seaweed chemical
defenses.
Chemical structure and ecological function
The biological effects of different chemical defenses are
often generalized on the basis of structural class alone. As
an example, tannins have been called nontoxic digestibility reducers whereas alkaloids and other small organic
molecules have been called toxins (Feeny 1976). Presumably because similar types of compounds function in similar ways, investigators often measured ‘‘total’’ plant
defenses (e.g., total phenolics) without establishing which
specific compounds were present and often without demonstrating that any particular compound, or even the
crude chemical extract, had any deterrent effect on herbivores (see Hay and Steinberg 1992; Hay 1996 for a discussion of problems associated with this approach). These
types of generalizations are invalid because effects of seaweed secondary metabolites are unique to specific metabolites and herbivores (Hay and Fenical 1988; Hay and
Steinberg 1992; Hay 1996; Paul 1997). Although many
seaweed secondary metabolites are broad-spectrum feeding deterrents, several have no known effects against herbivores, and few, if any, deter all herbivores.
Because minute changes in chemical structure may
drastically modify the deterrent properties of compounds,
generalizations about compound functions are misleading. As an example, brown algae in the order Dictyotales
produce a family of structurally similar diterpenes called
dictyols. Pachydictyol-A, dictyol-E, and dictyol-B are
three examples. Pachydictyol-A differs from the others by
the replacement of an OH by hydrogen; dictyol-E and
dictyol-B differ only in the position of the additional OH.
Although these compounds are very similar structurally,
dictyol-E either stimulates or does not affect feeding by
Caribbean and Pacific reef fishes, whereas the other compounds are significant deterrents (Hay and Steinberg
1992). Similar patterns are also apparent in tests against
other types of herbivores. Variation in the effects of particular compounds on different herbivores and of structurally similar compounds on particular herbivores
appears to be the rule rather than the exception (Hay
1991b; Paul 1992; Hay and Steinberg 1992; Paul 1997).
However, compounds produced by many reef seaweeds
significantly suppress feeding when they are tested in the
field against the diverse groups of herbivores on coral reefs
(Hay et al. 1987b; Hay 1991a; Paul 1992). These compounds clearly increase survivorship for the seaweeds.
Integrated pest management
Although seaweed secondary metabolites have strong demonstrable effects on herbivore feeding preferences, they
do not act in isolation from other plant traits or from the
environmental context in which seaweed-herbivore interactions occur (Cronin and Hay 1996b; Hay 1996). The role
of seaweed chemical defenses will not be adequately
understood until we appreciate the full range of defenses
that seaweeds use and how these defenses are integrated
and altered under different circumstances.
Few investigators have simultaneously manipulated
multiple defenses or varied defensive traits along with prey
nutritional quality to assess how multiple defenses may
work in concert to affect algal susceptibility to consumers.
When Duffy and Paul (1992) evaluated how marine secondary metabolites affected feeding by reef fishes using
foods that differed in their ratios of protein to carbohydrate, they found that some compounds were effective at
defending low protein foods but ineffective at defending
higher protein foods. Hay et al. (1994) noted a similar
pattern when they varied algal concentrations in agarbased foods being consumed by a sea urchin. Paul and
coworkers have also documented numerous instances in
which seaweeds with both chemical and CaCO defenses
3
deterred a broad spectrum of reef fishes. Parrotfishes
generally were deterred by the chemical but not the
CaCO , defenses, while surgeonfishes were deterred by the
3
CaCO but not the chemicals (Schupp and Paul 1994;
3
Meyer and Paul 1995; Pennings et al. 1996; Paul 1997).
The combination of traits provides protection against
a broader range of herbivores than would be provided by
either trait in isolation.
The defensive value of secondary metabolites in seaweeds of variable nutritional quality should change as
a function of how compounds affect herbivores. If a compound strongly suppresses survivorship or reproduction,
then consumers should avoid the compound regardless
of the nutritional value of the seaweed producing it.
However, if a compound lowers growth rate or digestive
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efficiency rather than survivorship or fecundity, then an
herbivore might choose a defended but high quality alga
over an undefended but lower quality alga because the
herbivore’s net income from the defended but nutritionally rich alga could be higher. These possibilities have
rarely been assessed, but the demonstrations that deterrent secondary metabolites have variable effects when
applied to foods of differing nutritional quality (Duffy and
Paul 1992; Hay at al. 1994) suggest that this interaction
should be evaluated more closely.
Chemically defended seaweeds commonly produce
multiple secondary metabolites that could interact to produce synergistic or additive effects. Investigations are
needed on the interactive effects of multiple metabolites;
however, the very limited studies done to date have rarely
found synergistic interactions among secondary metabolites. As an example, when Lumbang and Paul (1996)
tested multiple brominated sesquiterpenes produced by
the green alga Neomeris annulata against two reef fishes
and a sea urchin, they found that each compound was
significantly deterrent at or below its natural concentration and that all of the compounds together were not
more deterrent than each alone. More studies like this will
be needed before the potential effects of interacting metabolites can be evaluated.
Several studies have indicated that chemical and mineral defenses (i.e., CaCO ) commonly co-occur in marine
3
plants and can function either additively or synergistically
to reduce susceptibility to consumers (Hay et al. 1994;
Schupp and Paul 1994; Meyer and Paul 1995). As an
example, the green alga Halimeda goreauii contains both
an unusual secondary metabolite and a heavily calcified
thallus. When sea urchins and a nutritionally valuable
food were used to test the effects of the metabolite alone or
of CaCO alone, neither trait had any deterrent effect;
3
when these traits were combined, they interacted synergistically to strongly suppress feeding (Hay et al. 1994). This
interaction changed when the experiment was repeated
using a food of lower quality, indicating that food value,
CaCO , and secondary metabolites were interacting to
3
affect sea urchin food choice.
Several species of Halimeda also appear to substitute
mineral for chemical defenses as plant segments mature
and change their nutritional value and thus attractiveness
to herbivores. Halimeda produces its new segments at
night while herbivorous fishes are inactive. The new segments are uncalcified and more nutritious than older
segments, but they are also defended by higher concentrations of more potent feeding deterrents (Hay et al. 1988a;
Paul and Van Alstyne 1988a). As the new segments calcify
during the first day following their production, they become more heavily invested with CaCO , less nutritious,
3
and the concentration of chemical defenses decrease.
These examples demonstrate that seaweed defenses will
not be adequately understood unless they are viewed as
suites of interacting characteristics.
Induction of chemical defenses
The production of chemical defenses is hypothesized to be
costly because defenses utilize resources that could have
been allocated to growth or reproduction (Herms and
Mattson 1992). Constitutive defenses require expenditure
of resources even when herbivores are absent and the
benefits of protection are not realized. In contrast, inducible defenses allow costs to be delayed until herbivores
have been detected. Induced resistance may therefore minimize costs by keeping defenses low until they are needed
(Harvell 1990; Baldwin 1994).
For some seaweeds, the pattern of variation in secondary metabolites suggests that herbivore-induced increases
of chemical defenses may be responsible for some intraspecific variation in concentrations of secondary metabolites. For example, seaweeds from areas of coral reefs
where herbivory is intense often produce more potent and
higher concentrations of chemical defenses than plants
from habitats where herbivory is less intense (Paul and
Fenical 1986; Paul and Van Alstyne 1988a). However, in
the green seaweeds Halimeda, ºdotea, and Caulerpa that
show this pattern, clipping experiments failed to induce
increased terpenoid chemical defenses (Paul and Van Alstyne 1992). Clipping or sea urchin grazing of temperate
seaweeds also failed to induce higher levels of phlorotannins in the kelps Ecklonia and Alaria or in the rockweed
Sargassum (Pfister 1992; Steinberg 1994, 1995). Thus, the
higher levels of constitutive chemical defenses from sites
with many herbivores could have been generated by preferential grazing that removed the more susceptible individuals, founder effects, local selection, or among-habitat
differences in other variables.
Additionally, for some of the siphonous green seaweeds
studied by Paul and Van Alstyne (1992), weakly deterrent
metabolites stored in the alga were immediately converted
to more strongly deterrent metabolites if the alga was
damaged by crushing or cutting it. To distinguish this
rapid enzymatic conversion of available metabolites from
the classic notion of induction, Paul and Van Alstyne
termed this process, ‘‘activation.’’
There are two documented examples of herbivores inducing chemical defenses in seaweeds (Van Alstyne 1988;
Cronin and Hay 1996c). In contrast, there are many examples of inducible chemical defenses in the terrestrial literature (Baldwin 1994 and references therein). This
discrepancy between marine and terrestrial systems could
be due to the construction of vascular terrestrial plants
versus non-vascular seaweeds (e.g., the induction stimulus
from localized damage may not be efficiently translocated
in seaweeds, see Cronin and Hay 1996a); but lack of
research on seaweeds relative to terrestrial plants may
also explain the disparity.
Furthermore, most terrestrial investigations of induction have focused on insect grazing, while most marine
investigations have focused on larger herbivores such as
fishes and sea urchins rather than on mesograzers such as
amphipods that may be more ecologically similar to insects (Hay et al. 1987a; Hay and Steinberg 1992). Mesograzers have been considered to be less important than
larger herbivores because of the perception that they remove little seaweed biomass relative to the larger herbivores (see the debate among Bell 1991; Duffy and Hay
1991b; Brawley 1992).
Ignoring mesograzers as potential inducers of seaweed chemical defenses is inappropriate. The two clear
S73
examples of induction in seaweeds (Van Alstyne 1988;
Cronin and Hay 1996c) both involve mesograzers (a snail
and an amphipod), each of which could graze for long
periods on a plant without killing it and could thus be
affected by a defense that took days, or weeks, to induce.
In contrast, fishes and sea urchins are large relative to
many seaweeds and are often capable of rapidly killing
a plant that they find palatable. Thus, to avoid being
killed by these larger more mobile herbivores, plants may
need to be constantly defended rather than inducing defenses following attack. For many chemically defended
seaweeds and invertebrates, low concentrations of chemical defenses are generally effective deterrents against
fishes and sea urchins but are less effective or may even
stimulate feeding by mesograzers (Hay et al. 1987a, 1988b,
1989, 1990a,b; Hay 1991b, 1992, 1996; Van Alstyne and
Paul 1992; Duffy and Hay 1991a, 1994).
I suggest that it is the smaller, less mobile mesograzers
that will cue induction of chemical defenses in seaweeds.
These types of herbivores feed over temporal and spatial
scales that would allow induced responses to be beneficial
to seaweeds, and it is the mesograzers that often are not
deterred by chemical defenses until the metabolites are
induced to higher levels (Cronin and Hay 1996c; Hay
1996). It is therefore possible that induction in seaweeds
has appeared uncommon, because it rarely occurs in response to clipping or grazing by larger herbivores but
occurs more often in response to mesograzer feeding.
There are too few studies of chemical induction to
adequately evaluate the relative importance of large mobile versus small sedentary herbivores in inducing seaweed chemical defenses. However, the results of Cronin
and Hay (1996c) illustrate that mesograzer feeding can
cause induction. These authors noted spatial and temporal patterns of amphipod abundance, algal defensive
chemistry, and algal palatability that suggested that the
brown seaweed Dictyota menstrualis was inducing terpenoid chemical defenses in response to amphipod feeding. When Dictyota plants were split and grown in the
field for 2—3 weeks with one half of each plant periodically
subjected to amphipod grazing and the other half not
grazed, plant halves attacked by amphipods produced
higher levels of defensive compounds and became less
susceptible to amphipod grazing. This lowered susceptibility to amphipods resulted from induction of defensive
compounds in attacked plants rather than from alterations in plant nutritional content or from previous grazers selectively removing the least defended tissues and thus
leaving more chemically rich tissues. The among-site differences in palatability and concentrations of chemical
defenses occurred in years when amphipods were abundant but not in years when they were rare. Thus, both
spatial and temporal variance in palatability may have
been generated by induced defenses following attack by
amphipods. Preliminary experiments suggest that induction in response to mesograzer feeding also occurs in other
seaweeds (discussed in Hay 1996).
These examples indicate that seaweed chemical defenses
can be allocated in complex ways that may vary with time,
other defenses, nutritional state of the alga, and history of
previous attack. Marine chemical ecologists have recently
focused more attention on trying to understand seaweed
defenses within these broader, more ecologically realistic,
and more holistic contexts. These efforts are well founded
and need to continue.
Cascading effects of seaweed chemical defenses
The tremendous feeding activity of reef herbivores makes
seaweed chemical defenses especially important on tropical coral reefs (Bolser and Hay 1996). In areas where
generalist consumers feed intensively, small mesograzers
like amphipods and polychaetes that use plants as both
food and habitat could be consumed incidentally if they
lived on plants that were preferred by fishes. Therefore, it
has been hypothesized that selection should favor sedentary mesograzers that can live on and eat seaweeds that
are chemically defended from fishes because these seaweeds can provide mesograzers with safe sites from both
direct and incidental consumption (Hay et al. 1987a,
1988b; Hay 1992).
Initial tests of this hypothesis in the temperate Atlantic
found that the tube-building amphipod Amphithoe longimana and the tube-building polychaete Platynereis
dumerilii both minimized contact with fishes by selectively
living on and consuming the brown alga Dictyota menstrualis, which produced diterpene alcohols that deterred
fish feeding but that had little effect on feeding by the
amphipod or polychaete (Hay et al. 1987a, 1988b; Duffy
and Hay 1991a, 1994). In seasons when fishes were common, amphipod species that could not tolerate algal
chemical defenses became locally extinct while the amphipod Amphithoe longimana remained abundant because
it used a defended alga as a safe site from fish predation
(Duffy and Hay 1991a, 1994).
The hypothesis that small sedentary consumers could
minimize predation by associating with, or specializing
on, toxic hosts was tested more broadly using amphipods,
crabs, and molluscs that live on chemically defended seaweeds in the Caribbean or tropical Pacific (Hay et al.
1989, 1990a,b). In all of these cases, mesoconsumers were
undeterred, or sometimes stimulated, by host compounds
that deterred fish feeding. Additionally, mesograzers escaped or deterred predation through their association
with these chemically rich hosts (Hay 1992). As one
example (Hay et al. 1990a), the Caribbean amphipod
Pseudamphithoides incurvaria lives in a mobile, bivalved
domicile that it constructs from the chemically defended
seaweed Dictyota bartayresii. The diterpene alcohol that
causes fishes to reject the alga as food is the compound
that cues domicile building by the amphipod. Amphipods
in domiciles built from this alga are rejected as food by
predatory fishes but are rapidly eaten if they are removed
from their domiciles or if they are in domiciles that they
have been forced to build from a seaweed that is not
chemically defended. Although the amphipod cannot
physiologically sequester its host’s chemical defenses, it
achieves sequestration behaviorally by building its domicile from this defended alga.
Herbivorous ascoglossans that feed selectively on
chemically rich seaweeds, sequester the seaweed toxins,
and use these in their own defense provide welldocumented examples of physiological sequestration of
S74
host chemical defenses by mesoherbivores (Paul and Van
Alstyne 1988b; Hay et al. 1989, 1990b; Hay 1992). These
animals generally feed on noxious seaweeds in the order
Caulerpales (e.g., Caulerpa, Halimeda, Avrainvillea,
Chlorodesmis) and concentrate the algae’s chemical defenses until they comprise as much as 3—8% of the gastropod’s dry mass (Paul and Van Alstyne 1988b; Hay et al.
1990b). Concentrations of these compounds in the seaweeds rarely exceed about 1% of plant dry mass. Sequestered compounds serve to defend both the adult animal
and its egg masses, which are placed on the surface of its
host plant. A taxonomically diverse assemblage of specialized mesograzers escape or deter their consumers by living
on, feeding from, and, in some cases, morphologically
mimicking or sequestering defensive compounds from
their toxic hosts (see Hay 1992; Hay and Steinberg 1992;
Paul 1992; Hay 1996). These compounds are known to be
deployed in defense of ascoglossan egg masses (Paul and
Van Alstyne 1988b). They might also be passed on to
larvae, as occurs for other groups of chemically defended
invertebrates (Lindquist and Hay 1996).
In most instances, mesograzers showing strong preferences for particular plant species appear to be functioning
simply as herbivores. However, a few of the mesograzers
on encrusting corallines play a mutualistic role, sometimes
despite their direct feeding on the host. Littler et al. (1995)
demonstrated that about 50% of the diet of the herbivorous chiton Choneplax lata consisted of its preferred host
coralline, Porolithon pachydermum. However, if this herbivore was removed from its host, the host became fouled by
other algae, and these algae attracted parrotfishes that fed
on both the palatable epiphytes and the coralline host
(termed ‘‘shared doom’’ by Wahl and Hay 1995). The deep
bites of the parrotfish caused more damage to the coralline host than had been done by the chiton. Thus, removal
of the herbivorous chiton increased, rather than decreased, grazing on the coralline. Stachowicz and Hay
(1996) found a somewhat similar mutualistic association
between an herbivorous crab and the branched coralline
Neogoniolithon. When the crab was removed from this
structurally complex coralline, the crab was quickly eaten
by fishes. Without the grazing activity of the crab, the
coralline was rapidly overgrown by other seaweeds.
As with mesograzers, palatable seaweeds that are usually driven to local extinction by herbivores can sometimes persist in herbivore-rich communities if they grow
on or beneath their herbivore resistant competitors (Hay
1986; Littler et al. 1986; Wahl and Hay 1995). As an
example, numerous species of palatable seaweeds are significantly more common near the base of the chemically
defended seaweed Stypopodium zonale than several centimeters away; if the deterrent plant is removed, these
more palatable species are rapidly eaten (Littler et al.
1986). When plastic mimics of Stypopodium are placed in
the field, they also provide a partial refuge for palatable
species, but they are less effective than the real plants,
suggesting that associational refuges are generated in part
by the physical presence of a non-food plant, but that the
plant’s chemical repugnance makes the associational refuge more effective. These associational refuges can significantly increase the numbers of species co-existing in
a community, and under some circumstances, a seaweed
can be completely dependent on its major competitor to
keep it from being driven to local extinction by consumers
(Hay 1986; Hay and Fenical 1996). In addition juvenile
stages of many reef invertebrates and some fishes escape
predators by using well defended seaweeds as protective
nursery habitats (reviewed by Hay 1997).
Conclusions
Although seaweeds are not commonly studied by coral
reef ecologists, they are exceptionally productive experimental tools. Manipulations using seaweeds have provided a wealth of information on processes affecting
population and community structure on coral reefs. Studies on corals and sponges parallel those for seaweeds,
suggesting that seaweed studies may provide a template
for understanding processes affecting a broad variety of
reef organisms. Herbivorous fishes and sea urchins have
a profound effect on the distribution, abundance, and
species richness of coral reef seaweeds, which are the
potential competitive dominants on tropical reefs. When
overfishing or natural disturbances remove too many of
these herbivores, seaweeds can overgrow and kill other
species, prevent recruitment of invertebrate larvae, and
destroy coral reefs as we know them. To cope with the
intense feeding of herbivores, reef seaweeds have developed complex suites of chemical, mineral, morphological, structural, and nutritional traits that diminish
susceptibility to fishes and sea urchins. By their mere
presence, seaweeds that deter these large herbivores create
microsites of lowered consumer activity. Defended seaweeds thus become safe sites for small, less mobile mesograzers, for juveniles of several species of reef invertebrates
and fishes, and for more palatable seaweeds that may be
dependent upon their unpalatable competitors to prevent
their local extinction due to herbivory. Seaweed defenses
thus produce substantial cascading effects that alter reef
community organization and species richness.
Acknowledgements. This manuscript benefited from NSF grant
OCE 95—29784 and from comments by P Hay, V Paul, and
R Steneck.
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