UNIHI-SEAGRANT-BC-83-01
Proceedings of the Seventh International Coral Reef Symposium, Guam, 1992, Vol. 2
Deterrent Effects of Seaweed Extracts and Secondary
Metabolites on Feeding by the Rabbitfish Siganus spinus
VALERIE
J. PAUL,KAREND. MEYER,STEPHEN
G.NELSONAND HERLINGR. SANGER
University of Giam Marine Laboratory, Mangilao, Guam, 96923, USA
Abstract. Seventeen extracts and nine isolated secondary metabolites from tropical seaweeds were
coated on the palatable green alga Enteromorpha
clathrata at natural concentrations, paired with untreated control Enteromorpha, and offered to the
rabbitfish Siganus spinus in outdoor tanks on
Guam. Six algal extracts and one seagrass extract
affected feeding responses, but none of the isolated
metabolites deterred feeding by S. spinus. Previous
tests with the congener S. argenteus also indicated
that few seaweed extracts and secondary metabolites deterred feeding. Results for the rabbitfish contrast with those for other herbivorous fishes including acanthurids and scarids that are deterred
from feeding by numerous algal extracts and isolated secondary metabolites. These comparisons
suggest that seaweed chemical defenses differ in
their effectiveness toward different species of her;
bivorous fishes. The feeding behavior of some
fishes, particularly siganids, may not be strongly
affected by seaweed secondary chemistry.
Introduction
It is now well documented that many secondary
metabolites produced by tropical seaweeds function
as chemical defenses toward herbivorous fishes in
coral reef habitats (reviewed in Hay and Fenical
1988, Hay 1991, Paul 1992). Because herbivores
differ physiologically (e.g. types of digestive tracts,
gut pH) and in methods of foraging, the effectiveness of any particular plant defense could decrease
as the diversity of herbivore types increases within
a community (Lubchenco and Gaines 1981, Gaines
1985, Hay 1991).
Several studies have focused on how marine herbivores differ in their responses to specific algal secondary metabolites (Hay et al. 1987, Paul'et al.
1987, Hay et al. 1988a, 1988b, Paul et al. 1988, Hay
1991). For example, Hay et al. (1988b) hypothesize
that small, relatively sedentary herbivores that live
on plants should be more resistant to chemical defenses than large, relatively mobile herbivores that
move among many plants (reviewed by Hay 1992).
Paul et al. (1988, 1990) have shown that even different species of large, mobile, herbivorous fishes
with similar feeding methods respond differently to
seaweed secondary metabolites.
In this study, we continue our efforts to understand the dietary preferences of tropical herbivorous fishes by comparing the responses of individual herbivore species to seaweed extracts and
secondary metabolites. We are particularly interested in contrasting how different herbivore species
respond to seaweed secondary chemistry. Here we
present new data from feeding assays with seaweed
extracts and isolated metabolites tested against the
rabbitfish Siganus spinus and compare the results
with those of similar assays with other herbivorous
fishes. Rabbitfish are important herbivores on
Guam reefs particularly during episodic recruitment events that occur in April and May (Kami
and Ikehara 1976). In some years, S. spinus and S.
argenteus recruit in such large numbers that they
consume virtually all of the seaweeds and seagrasses
on the reef flats around Guam (Tsuda and Bryan
1973, pers. obs.). We asked the following questions:
(1) Do extracts and isolated metabolites from seaweeds that produce secondary metabolites deter
feeding by Siganus spinus? (2) How do deterrent
effects of seaweed secondary metabolites toward S.
spinus compare with deterrent effects toward other
rabbitfish and other herbivorous fishes?
Paul et al.
Methods
Source Material
Seaweeds and fish used in this study were collected
from various reef habitats around Guam, including
reef slopes, reef flats, and seagrass beds. Information concerning the seaweeds of Guam, including
taxonomic descriptions and authorities, is presented by Tsuda & Wray (1977). We selected common species of seaweeds that were abundant
enough to use in the preference trials and also to
provide sufficient material for chemical extractions.
Many of these seaweeds contain secondary metabolites and have been examined in other studies of
seaweed-herbivore interactions. Seaweeds .were
maintained outdoors in large, flowing seawater
tanks and were extracted within 24 hours of collection. Damaged or discolored plants were not
used. Individual Siganus spinus (15-20 cm TL)
were collected by dip net or cast net and maintained
on a diet of food pellets (Kruse's Perfection Brand
catfish pellets) and the seaweed Enteromorpha
clathrata in outdoor flow-through tanks for periods
ranging from several days to weeks prior to the.
study.
Chemical Analyses
Seaweeds were 'blotted dry, wiped clean of epiphytes, and extracted by homogenizing them in a
blender with a 1:1 mixture of dichloromethane and
methanol. The extracts were filtered, and the solvents were evaporated under reduced pressure with
a rotary evaporator to yield a viscous oil.
Thin layer chromatographic analysis (TLC)
(Noms & Eenical 1985) and proton nuclear magnetic resonance (NMR) spectroscopy were used to
detect the presence or absence of secondary metabolites in the algae (Paul & Hay 1986). TLC plates
were developed in two solvent systems, 1:9 ethyl
acetate:hexane and 1: 1 ethyl acetate:hexane, to
screen for secondary metabolites of different polarities. The plates were viewed under an ultraviolet
lamp to observe activity indicative of unusual metabolites. The plates were then sprayed with 50%
sulfuric acid and heated so that unusual color reactions, indicating the presence of secondary metabolites, could be observed. Because TLC tells little about the chemical structures of compounds in
the extracts unless the compounds can be related
to known standards, we also examined, the extracts
by proton NMR. Known compounds can be readily
detected and identified by NMR spectroscopy.
Individual secondary metabolites were isolated
by silica gel column chromatography followed by
high performance liquid chromatography (HPLC)
(Paul & Fenical 1985, 1986).
Feeding Assays
Methods similar to those used in this studv have
been used in evaluating the feeding deterrence of
crude extracts and isolated metabolites toward
other herbivorous fishes (Wylie and Paul 1988, Paul
et al. 1988, 1990). Small pieces of a palatable alga
Enteromorpha clathrata were pressed and blotted
dry on paper towels and then coated with a solution
of either the extract or the isolated metabolite dissolved in diethvl ether. The final concentrations on
treated Enteromorpha were 4-5% of the estimated
dry mass (1% wet mass) in trials with extracts and
approximately lYo of the estimated dry mass (0.25%
wet mass) in trials with pure metabolites. Dry mass
of the wet Enteromorpha was estimated by a previously calculated wet mass:dry mass ratio of approximately 4.5: 1. These concentrations approximate natural concentrations of most of the extracts
of the seaweeds. As determined during extraction,
organic extracts of the uncalcified algae ranged from
5-8% of the dry mass of the plants, and extracts of
the calcified algae were 3-6% of the dry mass of the
plants. Control pieces of Enteromorpha were coated
with diethyl ether.
Both the organic extracts and the pure metabolites are lipophilic and adhere to'the surfaces of
the Enteromorpha after the ether evaporates.
McConnell et al. (1982), Hay et al. (1987), and Paul
(1987) used similar methods and found that the
compounds remained on the coated algae for at
least 4-8 hours. Hay and Fenical (1988) reported
that 93% of the diterpene pachdictyol-A remained
on the coated plants after 24 hr in seawater. Given
the excellent retention of these compounds and extracts that have been quantitatively evaluated, the
similar solubility characteristics of the different extracts and isolated metabolites, and the short duration of our assays (1 5-30 min), we assumed that
loss of the compounds to seawater was negligible.
Individuals of Siganus spinus were placed into
separate compartments in flow-through tanks and
tested as groups of 2-4 fish. At least 8 replicate
groups of fish were used for each extract or pure
metabolite tested. For testing the crude extracts,
pieces of Enteromorpha that weighed approximately 2.5-g were used for both control and treated
pieces, while smaller, approximately 2.0-g pieces
were used for testing most of the isolated secondary
metabolites. However, for the four pure com-
Deterrent Effects of Seaweed Extracts and Secondary Metabolites on Feeding by the Rabbiffish
869
Table 1. Results of Siganus spinus assays with algal crude extracts coated on the preferred seaweed Enteromorpha clathrata
at 1% wet mass unless otherwise noted. Data presented as amount of Enteromorpha (g) consumed. N = number of replicate
pairs. Significant feeding deterrents were determined by using a paired t-test. *: Significant feeding deterrent (2-tailed).
Taxonomic
Group
Asparagopsis taxijormis
Falkenbergia (tetrasporophyte) stage
Avrainvillea obscura
Bryopsis pennata
Caulerpa racemosa
Chlorodesmisfastigiata
C. jhstigiata (1.5%)
Dictyota bartayresii
Enhalus acoroides
Halimeda discoidea
Halimeda macroloba
Halophila minor
Halymenia durvillaei
Liagora farinosa
Microcoleus lyngbyaceus
Portieria (=Desmia) hornemanni
Tydemania expeditionis
Valoniafastigiata
Control
Eaten
+ S.E.
"
Treated
Eaten
S.E.
N
p-Value
Red
Green
Green
Green
Green
Green
Brown
'
Seagrass
Green
Green
Seagrass
Red
Red
Blue-green
Red
Green
Green '
pounds: aplysistatin, palisadin A, udoteal, and caulerpenyne, 0.5-g pieces of Enteromorpha were used
because insufficient amounts of the compounds
were available to use 2.0-g pieces.
One piece of treated and one piece of control
Enteromorpha were inserted in opposite ends of a
strand of polypropylene line and offered to the
groups of rabbitfish for about 15-30 minutes. Lines
were suspended 0.1 m above the bottom from PVC
racks so that fish could access the algae from all
directions. We observed the.fish during the assays
and removed the lines before all of either the control or treated algae had been consumed. The rabbitfish always attacked both treated and control algae initially; and thus, they did not appear to detect
any extract in the water around the algae. Enteromorpha pieces were weighed before and after the
feeding trials. The pieces were carefully pressed and
blotted dry with paper towels and weighed to
determine the amount of control and treated algae
consumed. A paired t-test was used to compare
amounts of treated and control Enteromorpha
consumed.
Because many of the same fish were used for
testing the different algal extracts, we were concerned that the results of any particular trial might
be influenced by previous trials. We randomized
the order in which the extracts were tested by using
a random numbers table and ran approximately
half of the replicates (usually 8 groups of fish) for
each extract on one date and the remaining repli-
cates on a later date after new fish were captured.
Most of the pure compounds were tested only on
one date, since the limited amount of material isolated limited the number of replicates we could run
(usually 8-1 1 replicates). Only one assay was conducted per day, and fish were fed an abundance of
algae and pellet food between trials. Fish that did
not feed normally were removed from the tanks and
replaced with healthy fish that fed readily.
Results
Seven of the extracts significantly deterred feeding
by the rabbitfish Siganus spinus (Table 1). These
were extracts of the red algae Portieria (=Desmia,
Silva et al. 1987) hornemanni, Asparagopsis taxiformis, and Liagora farinosa, which all contain
known secondary metabolites; the green algae Chlorodesmis fmtigiata that contains diterpenes and Valonia fastigiata that does not have known compounds; the cyanobacterium Microcoleus
lyngbyacats that contains malyngamides; and the
seagrass Halophila minor, which may have phenolic acids (Table 2). Most of the 17 extracts we
tested are known to contain secondary metabolites;
however, only some of the secondary metabolites
appeared to have any effect on feeding by the rabbitfish. The ineffectiveness of seaweed natural products as feeding deterrents was confirmed by the results of feeding assays with the purified algal
secondary metabolites (Table 3). None of the 9 pure
870
Paul et al.
Table 2. Results of chemical analyses for algaefseagrasses that were used in this study. -: No toughnessfcalcification;C =
calcified; T = tough; YES = crude extract was a significant feeding deterrent (p < 0.05); NO = crude extract was not a
significant feeding deterrent (p > 0.05). ? = secondary metabolites are present by TLC of crude extract, but structures are
unknown.
Species
Tough/
Calcified
Green Algae
Avrainvillea obscura
Bryopsis pennata
Caulerpa racemosa
Chlorodesmis fastigiata
Halimeda discoidea
Halimeda macroloba
Tydemania expeditionis
Valonia fastigiata
Red Algae
Asparagopsis taxiformis
Falkenbergia stage
Halymenia durvillaei
Liagora farinosa
Portieria hornemanni
Secondary Metabolites
avrainvilleol
bryopsin
caulerpenyne caulerpin
chlorodesmin,
related aldehyde
halimedatrial halimedatetraacetate
halimedatrial halimedatetraacetate
Tydemania alcohol
?
No
No
No
Yes
No
No
No
Yes
haloforms, halogenated
ketones and acetones
?
acetylene-containing fatty acid
ochtodene, and other halogenated monoterpenes
Yes
No
No
Yes
Yes
pachydictyol A, and other dictyol diterpenes
No
malyngamide A,B, and minor related compounds
Yes
?
No
Yes
+
Brown Algae
Dictoyota bartayresii
Cyanophyte
Microcoleus lyngbyaceus
Seagrass
Enhalus acoroides
Halophila minor
Deterrent
phenolic acids, ?
Table 3. Results of Siganus spinus assays with algal pure metabolites coated at 0.25% wet mass on the preferred seaweed
Enteromorpha clathrata. Data presented as amount of E. clathrata (g) consumed + standard error of the mean and analyzed
with paired t-tests. N = number of replicate.pairs. Two-tailed p-values are reported. None of the pure metabolites were
significant feeding deterrents.
Control Eaten
+ S.E.
Treated Eaten
+ S.E.
Aplysistatin
Bryopsin
Caulerpenyne
Caulerpin
Chlorodesmin
Flexilin
Pachydictyol A
Palisadin A
Udoteal
compounds significantly deterred feeding by
S. spinus.
Discussion
Siganus spinus is apparently not as strongly affected
by the secondary metabolites of tropical seaweeds as
some other herbivorous fishes (Tables 4 and 5). Only
seven of seventeen seaweed extracts reduced feeding
by S. spinus, even though all of the extracts we tested
either contain known secondary metabolites or have
been shown to deter other herbivorous fishes in similar assays (Table 4). None of the pure compounds
deterred S. spinus, although many of these same
compounds did reduce feeding by other herbivorous
fishes in similar studies (Table 5).
Several of the extracts that did deter feeding by
Siganus spinus have also affected feeding by other
herbivorous fishes. Extracts of the red alga Portieria
hornemanni contain ochtodene and other halogenated monoterpenes (Burreson et al. 1975b, 1975c,
Paul et al. 1987). Thalli coated with extracts of this
-
Deterrent Effects of Seaweed Exbacts and Secondary Metabolites on Feeding by the Rabbitfish
.
Table 4. Comparison of results of feeding assays between independent studies of herbivorous fishes in the laboratory. Assays
used algal organic extracts. YES = Significant feeding deterrent (p < 0.05). NO = Not a significant feeding deterrent (p >
0.05). - = Not tested. Significant differences in deterrence among fish species were observed (X2 = 11.86, = 0.018). Data
compiled from: = Paul et al. work in progress; = Wylie and Paul 1988; ' = Paul et al. 1990; = this paper.
Zebrasoma
jlavescens2
Scarus .
sordidus'
Asparagopsis taxiformis
Avrainvillea obscura
Bryopsis pennata
Caulerpa racemosa
.
Chlorodesmis fastigiata
Dictyota bartayresii
Enhalus ascoroides
Halimeda discoidea
Halimeda macroloba
Halophila minor
Halymenia durvillaei
Liagora farinosa
Microcoleus lyngbyaceus
Portieria (=Desmia) tiornemanni
Tydemania expeditionis
Valonia fastigiata
-
.
+
Z:
871
No .
'Yes
Yes
. No
No
No
Yes
Yes
.Yes
No
.'
Yes
No
Yes
Yes
Yes
. Yes
*
<
No
No
Yes
No
Yes
Yes
Siganus
argenteus
Adults3
Siganus
argenteus
Juveniles3
No
No
No
No
No
No
Yes
Yes
No
No
Yes
No
Yes
Yes
Yes
No
No
No
No
No
No
No
No
No
No
No
No
.
-
Yes
-
-7'
Yes
Yes
Yes
Yes
.
-
t
'
-
Yes
Yes
No
No
.
Siganus
spinup
Yes
No
No
No
Yes
No
No
No
No
Yes
No
Yes
Yes
Yes
No
Yes
Table 5. Comparison of results of feeding assays between independent studies of different species of herbivorous fishes in the
laboratory. Assays used purified secondary metabolites. YES=Significant feeding deterrent (p < 0.05). NO = Not a significant
feeding deterrent (p > 0.05). - = Not tested. Data compiled from Paul et al. work in progress1;Paul et al. 1988'; Wylie and
Paul 1988'; Paul et al. 1990'; Paul et al. this paperJ.
i:
i
i s
:
~plysistatin
Avrainvilleol
Bryopsin
Caulerpin
Caulerpenyne
Chlorodesmin
Elatol
'
Rexilin
,
Ochtodene
Pachydictyol A
Palisadin A
Udoteal
Scarus
sordidus'
N02'
-
NO'
-
Yes
No
No'
-
'
No
-
,
Yes
Yes
No '
No
No
Zebrasoma
jlavescens
I
NO'
Yes3
No2
Yes2
Yes3
Yeszk3
No2
Yes2
alga were avoided by all herbivorous fishes we have
tested them against including rabbitfish, surgeonfish, and parrotfish (Table 4). The pure metabolite
ochtodene has also been shown to be an effective
defense against a variety of herbivorous fishes (Table 5). Unfortunately, this metabolite was not available to test against S. spinus. Another extract that
has been consistently deterrent against herbivorous
fishes, including S. spinus, is the extract of the filamentous cyanobacterium Microcoleus lygbyaceus
(Table 4). This extract and its major nitrogenous
metabolites, the malyngamides (Cardellina et .al.
-
Siganus
argenteus
Adults4
No
No
No
No
No
Yes
No'
Yes
Yes
No
No
No
Siganus
argenteus
Juveniles4
Siganus
- spinus5
.
No
No
-
No
Yes
No
1979), also ,reduced feeding by herbivorous fishes
in field assays on Guam (Paul and Pennings 1991).
Other extracts that reduced feeding by Siganus
spinus have deterred some but not all other herbivorous fishes, including the extracts of Liagora
farinosa, Valoniafas~igiala,and Chlorodesmisfastigiata (Table 4). Liagora farinosa produces acetylene-containing acetogenins (Paul and Fenical
1980). The chemistry of Valonia is ,not known.
Chlorodemis produces chlorodesmin and related
acyclic diterpenoids (Wells and Barrow 1979, Paul
and Fenical 1985). Isolated chlorodesmin did not
Paul et al.
affect feeding by S. spinus; however, it is possible
that other metabolites in the extract, higher concentrations of chlorodesmin, or combinations of
metabolites found in the whole extract are necessary to deter feeding. Our results with crude extracts
(Table 4) are consistent with the observation by
Tsuda and Bryan (1973) that, on Guam, Chlorodesmis is rejected by S. spinus but is readily consumed by S. argenteus. Hay et al. (1988a) also found
that S. doliatus on the Great Bamer Reef readily
consumed algae coated with chlorodesmin.
The extract of the red alga Asparagopsis taxiformis was rejected by S. spinus but did not affect
other herbivorous fishes in our assays. A. taxiformis
produces halomethanes and halogenated ketones
and acetones (Burreson et al. 1975a, McConnell
and Fenical 1977, Woolard et al. 1979). Many of
the metabolites of A. taxiformis such as the halomethanes are quite volatile and are easily lost during the extraction process (McConnell and Fenical
1977), therefore we are probably only testing a subset of the secondary chemistry of A. taxiformis in
our assays. Extracts of the Falkenbergia stage (tetrasporophyte) ofA. taxiformis did not significantly
deter feeding, but these results may be a function
of the smaller sample size for the Falkenbergia assay
since similar amounts of control and treated Enteromorpha were eaten for the Asparagopsis and
Falkenbergia assays (Table 1).
Extracts of several algal species, including Dictyota bartayresii, Halimeda spp., and Tydemania
expeditionrs, which produce high concentrations of
secondary metabolites were readily eaten by the
rabbitfish, and neither their extracts nor their isolated metabolites significantly deterred feeding (Tables 1 and 2). We did not observe the fish displaying
any symptoms of illness or any reluctance to feed
after consuming these chemically-rich extracts. Extracts of Caulerpa racemosa and the pure major
metabolites caulerpin and caulerpenyne did not deter S. spinus and have not been deterrent toward
any herbivorous fishes examined (Tables 4 and 5).
Meyer and Paul (1 992) tested Caulerpa extracts and
isolated metabolites in field assays and also found
that even high concentrations of these compounds
did not reduce feeding by herbivorous fishes on
Guam.
None of the pure compounds we tested deterred
feeding by S. spinus, although we cannot rule out
that either higher concentrations of metabolites or
naturally occumng mixtures of these metabolites
might be deterrent. However, all other herbivorous
fishes we have used in similar assays have been
deterred by at least a few pure seaweed secondary
metabolites (Table 5).
Paul et al. (1990) concluded that there was no
clear relationship between secondary metabolite
production by seaweeds and susceptibility to herbivory by Siganus argenteus. Several algae that produced high concentrations of secondary metabolites
were readily eaten by S. argenteus (Tables 2 and 4).
S. spinus seems to be similarly resistant to the
chemical defenses of some tropical seaweeds, indicating that this may be a characteristic of the family. Few species of seaweed were rejected by S. spinus in laboratory assays, suggesting that these fish
eat a broad variety of macroalgae (Tsuda and,Bj a n
1973, Bryan 1975). Hay et al. (1988a) also suggested
that siganids may be unusually resistant to seaweed
chemical defenses because Siganus doliatus was not
deterred by some metabolites that deterred other
herbivorous fishes. Information on how siganids
could physiologically overcome plant defenses is
lacking (Horn 1989). There has been relatively little
work on the digestive physiology of herbivorous
reef fishes, but the role of the intestinal microflora
has recently been receiving increased attention
(Choat 199 1). Terrestrial mammalian herbivores
have physiological and biochemical mechanisms to
detoxify secondary metabolites (Lindroth 1988),
and if the capacity of these cletoxification systems
is exceeded mammals become ill and die. Changes
in gastrointestinal physiology, detoxification by gut
microflora, and detoxification by tissue enzymes
are some mechanisms by which terrestrial vertebrates deal with plant secondary metabolites (Lindroth 1988).
'I
Morphological defenses of seaweeds such as calcification and toughness do appear to be associated
with low susceptibility to grazing by siganids. Individual S. argenteus, particularly juveniles, do not
readily consume seaweeds that are calcified or
tough (Paul et al. 1990). Many seaweeds such as
Halimeda spp. and Tydemania expeditionis would
likely not be consumed by S. spinus because they
are highly calcified, even though their extracts did
not deter this herbivore. The differential effectiveness of particular seaweed chemicals or morphological defenses .against specific herbivores may in
part account for the diversity of seaweed secondary
metabolites (Faulkner 1984, 1986), the variability
of their production (Paul and Fenical 1986, Meyer
and Paul 1992), and the frequent combination of
calcification and chemical defenses in tropicalalgae
(Hay 1984, Paul and Hay 1986, Paul and Fenical
1986).
These studies suggest that siganids may not be
as strongly affected by seaweed natural products in
comparison to other species of herbivorous fishes.
However, such comparisons between species
Deterrent Effects of Seaweed Extracts and Secondary Metabolites on Feeding by the Rabbitfish
should be made with caution; Paul et al. (1990)
showed significant trial effects and trial-extract interactions even in studies with a single herbivore.
Differing metabolic levels and hunger levels of the
fish between trials could account for differences between single-herbivore tests. Also, seaweed secondary metabolite composition can vary seasonally and
between collection sites (Meyer and Paul 1992). Simultaneous multi-species comparisons will have to
be made to clearly document any differences in herbivore response to seaweed defenses.
Acknowledgements. This research was supported by the University of Hawaii Sea Grant College Program under Institutional Grant No. NA85AA-D-SG072 from NOAA Office of
Sea Grant, Department of Commerce. Kevin Foster, Irene
Imanil, and Karl Kuetzing assisted with the feeding assays.
Critical reading by Steve Pennings and two anonymous reviewers improved earlier drafts of this manuscript. This is
contribution #322 of the University of Guam Marine Laboratory.
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