ArticlePDF Available

Coral reef benthic cyanobacteria as food and refuge: Diversity, chemistry and complex interactions

Authors:

Abstract and Figures

Benthic filamentous cyanobacteria are common in coral reefs, but their ecological roles are poorly known. We combined surveys of cyanobacteria-associated fauna with feeding preference experiments to evaluate the functions of benthic cyanobacteria as food and shelter for marine consumers. Cyanobacterial mats from Guam and Palau yielded 43 invertebrate species. The small sea hare Stylocheilus striatus was abundant on cyanobacterial mats, and only fed on cyanobacteria in multiple-choice experiments. In contrast, feeding experiments with urchins and fishes showed that these macrograzers preferred algae as food and did not consume either of two cyanobacteria offered. Extracts from the cyanobacterium Lyngbya majuscula stimulated feeding by sea hares but deterred feeding by urchins. Thus, some small coral reef grazers use cyanobacteria that are chemically-defended from macrograzers as food and refuge. Cyanobacteria could indirectly influence local biodiversity by affecting the distribution of cyanobacteria-dwelling organisms.
Content may be subject to copyright.
Proceedings 9th International Coral Reef Symposium, Bali, Indonesia 23-27 October 2000,Vol. 1.
Coral reef benthic cyanobacteria as food and refuge: Diversity, chemistry
and complex interactions
E. Cruz-Rivera1 and V.J. Paul1,2
1 University of Guam Marine Laboratory, UOG Station, Mangilao, GU 96923, USA
2 vpaul@uog9.uog.edu
ABSTRACT
Benthic filamentous cyanobacteria are common in coral reefs, but their ecological roles are poorly known. We
combined surveys of cyanobacteria-associated fauna with feeding preference experiments to evaluate the functions of
benthic cyanobacteria as food and shelter for marine consumers. Cyanobacterial mats from Guam and Palau yielded
43 invertebrate species. The small sea hare Stylocheilus striatus was abundant on cyanobacterial mats, and only fed
on cyanobacteria in multiple-choice experiments. In contrast, feeding experiments with urchins and fishes showed
that these macrograzers preferred algae as food and did not consume either of two cyanobacteria offered. Extracts
from the cyanobacterium Lyngbya majuscula stimulated feeding by sea hares but deterred feeding by urchins. Thus,
some small coral reef grazers use cyanobacteria that are chemically-defended from macrograzers as food and refuge.
Cyanobacteria could indirectly influence local biodiversity by affecting the distribution of cyanobacteria-dwelling
organisms.
Keywords Algal-herbivore interactions, Chemical
defenses, Cyanobacteria, Lyngbya, Mesograzers, Sea
hares
Introduction
Studies of algal-herbivore interactions have offered
important information on the roles of eukaryotic
macroalgae as food and shelter for marine consumers.
Complex interactions develop around chemically-
defended seaweeds that deter larger consumers such as
fish and urchins (macrograzers) while providing safe
habitats for small herbivorous crustaceans, polychaetes,
and gastropods (mesograzers) adapted to the chemical
defenses of the algae (Hay 1992, Hay and Steinberg 1992,
Paul et al. 2001).
Large benthic filamentous cyanobacteria are common
and often abundant in some coral reefs (Thacker and Paul
in press). Because of their biomass and productivity,
benthic cyanobacteria have the potential to be important
food sources for coral reef grazers and to be shelters for
small animals, thus playing important roles in marine
communities in a fashion similar to that of eukaryotic
algae. Like many eukaryotic algae, some marine
cyanobacteria have deterrent chemicals that defend them
from macroherbivores (Pennings et al. 1997, Nagle and
Paul 1998, 1999) but, some smaller consumers appear
adapted to feed on these cyanobacteria (Paul and
Pennings 1991, Pennings and Paul 1993, Nagle et al.
1998). However, the relative use of cyanobacteria by
diverse marine consumers is poorly known.
In this study, we assess the role of benthic
cyanobacteria as food and shelter for marine consumers.
We combine observations on the distribution of
cyanobacterial epifauna with experiments on feeding
behavior of diverse marine grazers to draw parallels
between the ecologies of eukaryotic algae and
cyanobacteria in coral reefs. In particular, we ask 1) Do
small benthic organisms find shelter within coral reef
benthic cyanobacteria?, 2) Are these cyanobacteria treated
differently as food by macro- and mesoconsumers?, and
3) Do cyanobacterial metabolites play a role in these
interactions?
Materials and Methods
Field surveys and collections were conducted at Piti
Reef in Guam (130 30’N, 1440 45’ E) during July 1999
and at three different sites (Lighthouse Channel, Oolong
Channel, and Short Drop Off) at the Republic of Palau (70
30’ N, 1340 30’ E) during April of 1999 and 2000.
Surveys of cyanobacteria-associated fauna were
conducted using snorkel or SCUBA by collecting ten
individual mats of each cyanobacterium. Mats were
sealed inside plastic bags underwater, brought to the
laboratory, and inspected under a dissection microscope at
low magnification. Animals were counted, sorted into
species, and densities recorded as number of individuals
per gram wet mass of cyanobacteria. To eliminate excess
water, cyanobacterial mats were either spun in a salad
centrifuge or pressed gently on absorbent paper,
depending on the structure and cohesiveness of the mats.
Our surveys included only organisms that could
potentially be mesograzers (Paul et al. 2001) and
therefore, did not include smaller consumers such as
copepods, ostracods, small nematodes, or foraminiferans,
that were sometimes abundant.
Cyanobacteria were identified to genus under a
compound microscope following the taxonomic system of
Desikachary (1959). Faunal surveys were conducted on
four cyanobacterial species (Lyngbya majuscula, L.
bouillonii, Symploca sp., and Oscillatoria sp.) The
Symploca from Piti forms prostrate golden yellow mats on
sand and coral rubble, with densely packed upright
filaments only a few cm high. The Oscillatoria forms
thin dark brown mats on sand and rubble that spread as
thin slimy films over the substrate.
The three cyanobacteria surveyed in Palau included an
unidentified bright red Lyngbya sp. and two unidentified
Symploca spp. The Lyngbya forms upright feathery
colonies about 10 cm tall on rocks and dead coral.
Symploca sp. 1 was found mostly on the underside of
corals (although it also occurs in the open) forming small
discreet reddish orange colonies about 3-5 cm high,
resembling the shape of Schizothrix mexicana. Symploca
sp. 2 forms prostrate, sometimes extensive, mats with
filaments around 5 cm high. The mats are delicate, with a
cotton-like appearance and light pink shades (towards the
tops of the mats) over a white background. Lyngbya sp.
and Symploca sp. 2 were collected in both April of 1999
and 2000 from the same sites. Data from faunal surveys
were seldom distributed normally and variances were
rarely homogeneous, thus, most analyses were performed
either by Kruskal-Wallis or Mann-Whitney U tests (Palau
2000 surveys), but ANOVA was utilized when
appropriate.
Multiple choice feeding assays were conducted with
the most abundant organism found on cyanobacterial mats
in Guam and Palau, the small sea hare (Opisthobranchia)
Stylocheilus striatus (previously Stylocheilus longicauda
– see Rudman 1999). In Guam, two small (20-30 mm)
sea hares were placed in round dishes (16 cm diameter, 6
cm height) filled with sea water and offered a
simultaneous choice among five eukaryotic macroalgae
(the green algae Enteromorpha clathrata and Caulerpa
racemosa, the brown algae Padina tenuis and Sargassum
polycystum, and the red alga Acantophora spicifera) and
two common cyanobacteria (Lyngbya majuscula and L.
bouillonii). Similarly sized pieces of each alga were spun
in a salad centrifuge to remove excess water and weighed
at the start of the assays. Algal pieces differed in weight
(ca.150-2000 mg) because of differences in algal
densities, but because the pieces were of similar size the
animals had similar likelihood of encountering each alga.
Ten replicate experimental containers received sea hares
and algae while another seven had algae without sea hares
and served as controls for changes in algal mass unrelated
to consumption. After allowing animals to feed for 1.5
days, algae were weighed again (after removing excess
water) and the amount consumed was calculated and
corrected for autogenic changes in algal mass (Peterson
and Renaud 1989). Algae that were not consumed and
grew appear as negative values in the results. Organisms
for these and other feeding assays (see below) were
collected from sites at Piti Reef, Pago Bay, and Tumon
Bay in Guam. Data from these multiple-choice feeding
assays were analyzed using Friedman’s tests (see
Stachowicz and Hay 1999).
Feeding assays with the common urchin Echinometra
mathaei followed a similar laboratory protocol to that for
Stylocheilus, but used larger algal pieces (1.5-5.0 g).
Single urchins were placed in round flow-through tanks
(25 cm diameter, 25 cm height) and allowed to feed for
two days. Feeding assays with fishes were conducted in
the field using algal pieces suspended on plastic ropes.
Each replicate rope had one piece of each alga or
cyanobacterium (3-11 g) threaded at the base into the rope
and arranged haphazardly within replicates. Ropes were
taken to the field and attached by one end to dead corals
or rocks. Small floats kept the ropes upright while
attached to the bottom. Two separate assays were
conducted at Western Shoals (N=12) and Cocos Lagoon
(N=11) in Guam. Ropes were left for 1-3 hr in the field.
Because these assays ran for such a short period and
because fish consumption was so high, controls for
autogenic changes in mass were not used. However, we
scored these assays conservatively by classifying algae
only as eaten (> 50% mass lost) or not eaten (<50% mass
lost), and analyzed the data using contingency table
analyses. Ropes in which none of the 7 algal species was
consumed by 50% or more did not offer information on
fish feeding preferences and were not used in the
analyses.
Consumers could avoid cyanobacteria due to the
presence of defensive secondary metabolites. We tested
this by comparing the palatability of crude extracts from
the common cyanobacterium Lyngbya majuscula offered
to sea hares and urchins. We hypothesized that extracts
would not deter the sea hares but would deter the urchins.
Freeze-dried L. majuscula was extracted in 1:1 ethyl
acetate/methanol. The crude extract was diluted in ethyl
ether and coated at natural concentration (per dry mass)
onto freeze-dried powdered Enteromorpha, using a rotary
evaporator to eliminate the organic solvent. Enough ether
was used to completely cover the freeze-dried algae in the
flask. This provided our treatment food. Control food
was prepared by treating Enteromorpha with ether alone.
The foods were then used to prepare agar-based artificial
diets following methods in Hay et al. (1998). Our
standard recipe contained 2g of freeze-dried algae, 0.36g
of agar, and 18 ml of distilled water. Pair-wise choice
assays were performed by simultaneously offering grazers
food strips containing freeze-dried Enteromorpha either
with or without L. majuscula extracts. Three small sea
hares, or one urchin, were placed in replicate containers
(n=15 and 12, respectively) similar to those described
previously. Replicates in which no food was consumed
were not used in the analyses because they provided no
information on consumer feeding preference. Sea hares
and urchins were allowed to feed on these artificial diets
for 2 and 3 days, respectively. Data from these assays
were analyzed with two-tailed t- tests.
Results
A diverse fauna of 43 animal species was associated
with the benthic cyanobacteria (Figs. 1-3). Gastropods,
crustaceans, and polychaetes dominated in numbers and
probably in species diversity as well. The total number of
species is probably an underestimate because the taxo-
nomy of such groups as cephalaspidean snails and
polychaetes is poorly understood. Overall, the most
abundant cyanobacteria-associated animals were the small
sea hare Stylocheilus striatus, the cephalaspidean snails
Diniatys dentifera and Ventomnestia villica, and a small
unidentified rissoellid snail (Jeffreysilla sp.). All these
animals were observed in more than one cyanobacterial
species from Guam and/or Palau (e.g., Stylocheilus, Figs.
1-3). Other gastropods observed included the snails
Cerithium zebrum (=Bittium zebrum) and C. punctatum
(=C. alveolus), and the cephalaspideans Haminoea ovalis,
H. nigropunctatus and an undescribed Diniatys sp. The
crustacean fauna was dominated by amphipods (Ampithoe
sp.) and tanaids (Leptochelia cf. dubia). Portunid crabs
(Thalamita corrugata and Thalamita integra) were also
common in mats of Lyngbya majuscula from Guam,
suggesting that predators could also find refuge among
cyanobacteria.
Small tube-building alpheid shrimp (Alpheus sp.) were
only collected in Palau, where they occurred on both
Lyngbya and Symploca (Figs. 2-3). However, we also
observed the congeneric Alpheus frontalis, a large tube-
building shrimp common on L. bouillonii in Guam and
Palau, but it was not included in our surveys because the
shrimp avoided collection (and thus, positive
identification). Other taxa found among cyanobacterial
mats included large nematodes, nemerteans, oligochaetes,
cumaceans, nudibranchs, caprellid amphipods, non-
alpheid shrimps, hermit crabs, majid crabs, galatheid
crabs, isopods, and pycnogonids.
Fig. 1 Mean (+1SE) abundance of animals associated
with four benthic cyanobacteria from Guam in July 1999
(N=10). Analyses are by one-way ANOVA or Kruskal-
Wallis followed by Tukey’s HSD post hoc tests or Tukey-
type non-parametric comparisons. Same letter above two
bars indicates statistically equivalent means.
There were noticeable interspecific differences among
cyanobacteria in the numbers and diversity of their
associated faunas. Lyngbya majuscula from Guam had a
more diverse epifauna than the other three cyanobacteria
sampled in Guam (Fig. 1). This species had significantly
more Stylocheilus striatus (p<0.001, Kruskal-Wallis) and
amphipods (p=0.018, Kruskal-Wallis) than at least two of
the other cyanobacteria sampled, a significantly higher
number of cephalaspideans (p=0.003, Kruskal-Wallis)
and tanaids (p=0.035, Kruskal-Wallis) than at least one of
the other cyanobacteria surveyed and showed a strong,
though not significant, trend (p=0.083, Kruskal-Wallis)
towards higher density of snails than all other
cyanobacteria (Fig. 1). In contrast, the congeneric
Lyngbya bouillonii had the lowest numbers and
diversity of epifauna of all the cyanobacteria sampled
(Fig. 1). Interspecific differences in the abundances of sea
hares, tanaids, polychaetes, cephalaspideans, and alpheid
shrimps were also found for the cyanobacteria surveyed in
Palau in both years (Figs. 2-3).
Fig. 2 Mean (+1SE) abundance of eight animal groups
associated with three benthic cyanobacteria from Palau in
April 1999 (N=10). Analyses and symbols as in Fig. 1
Sea hares, urchins, and fishes showed different
patterns of feeding preferences for eukaryotic macroalgae
versus cyanobacteria (Fig 4). Stylocheilus strongly
preferred Lyngbya majuscula and to a lesser extent L.
bouillonii, but the urchin Echinometra mathaei showed
significant feeding preferences for some macroalgae
when offered a choice among algae and cyanobacteria
(p<0.001, Friedman’s test, Fig. 4). Grazing was highest
on the red alga Acantophora, followed by Padina,
Sargassum, and Enteromorpha.
Fig. 3 Mean (+1SE) abundance of five animal groups
associated with two benthic cyanobacteria from Palau in
April 2000 (N=10). Analyses are from t-tests or Mann-
Whitney U tests.
Despite large differences in mean consumption, variance
was high and consumption of these four algae was
statistically equivalent after post hoc tests. Consumption
of the green alga Caulerpa racemosa was very low and
statistically equivalent to that of cyanobacteria did not
graze on any of the other algae offered (p<0.001,
Friedman’s test). The large variance in Caulerpa mass
loss during the Stylocheilus assays was caused by some of
the algae becoming reproductive and not by sea hares
consuming this seaweed.
The urchin Echinometra mathaei showed significant
feeding preferences for some macroalgae when offered a
choice among algae and cyanobacteria (p<0.001,
Friedman’s test, Fig. 4). Grazing was highest on the red
alga Acantophora, followed by Padina, Sargassum, and
Enteromorpha. Despite large differences in mean
consumption, variance was high and consumption of these
four algae was statistically equivalent after post hoc tests.
Consumption of the green alga Caulerpa racemosa was
very low and statistically equivalent to that of
cyanobacteria.
Natural assemblages of fishes from two different reefs
showed different patterns of feeding among the
macroalgae. At Cocos Lagoon the brown alga Padina
tenuis was the species most consistently consumed, but all
eukaryotic algae tested were significantly eaten compared
to cyanobacteria (p<0.001, Chi-square). In contrast, only
Enteromorpha and Caulerpa were significantly consumed
at Western Shoals (p<0.001, Chi-square test).
Fig. 4 Feeding choices of the sea hare Stylocheilus
striatus, the urchin Echinometra mathaei, and fishes from
two reefs offered five eukaryotic algae and two
cyanobacteria (Lyngbya majuscula and L. bouillonii). For
fishes, data are the number of replicates in which >50% of
that alga was eaten. Analyses are by Chi-square or
Friedman’s tests. Letters above bars indicate significant
groupings
Fig. 5 Feeding by sea hares (Stylocheilus) and urchins
(Echinometra) on artificial diets containing (treatment) or
lacking (control) extracts from the cyanobacterium
Lyngbya majuscula. Both diets were offered simul-
taneously. Analyses are by t-tests.
A more diverse fish community occurred at Cocos
Lagoon than at Western Shoals during these experiments
and most grazing at this latter site was done by the
“blacktongue unicornfish” Naso hexacanthus (E. Cruz-
Rivera, personal observation). Despite differences in
feeding patterns, none of the two cyanobacteria tested
were eaten by fishes at either site.
Cyanobacterial chemical deterrence explained some of
the feeding choices observed. Crude extracts of the
cyanobacterium Lyngbya majuscula, the preferred food of
the sea hare (Fig. 4), strongly stimulated feeding by this
mesograzer (Fig. 5). In contrast, the urchin Echinometra
mathaei was strongly deterred (p<0.001, t-test) by
Lyngbya extracts. Thus, our data showed opposite results
for the meso- and macrograzer feeding on live algae (Fig.
4) and cyanobacterial extracts (Fig. 5).
Discussion
The role of eukaryotic macroalgae as food and refuge
for small herbivores (mesograzers) has been studied
extensively in both tropical and temperate marine
systems. Chemically-defended macroalgae can indirectly
enhance the survival of mesograzers by providing
“enemy-free space” and a variety of animals selectively
associate with, and feed on, defended algae, are cryptic on
defended algal hosts, and behaviorally or physiologically
sequester chemicals from the algae and use those
chemicals as acquired defenses against predators (Hay
1992, Hay and Steinberg 1992, Paul et al. 2001).
We show that some large benthic cyanobacteria in
coral reefs host a diverse animal fauna (Figs. 1-3) and that
some of these animals selectively consume cyanobacteria
that are low preference items for larger grazers (Fig. 4).
We also demonstrate that chemical feeding deterrents
against macrograzers occur in at least some cyanobacteria
but that the same chemicals do not deter feeding by a
specialist mesograzer (Fig. 5). Thus, some defended
benthic cyanobacteria serve as food and shelter for small
grazers and, in this context, they parallel chemically-
defended eukaryotic macroalgae in coral reefs. The
diversity of epifauna on cyanobacterial mats and the
dependence of some of these animals on cyanobacteria as
food suggest that cyanobacteria can potentially enhance
local biodiversity patterns in some coral reefs.
These “positive” roles of marine cyanobacteria have
been largely ignored because cyanobacteria have seldom
been treated as normal components of coral reef
communities. This is likely because benthic cyano-
bacteria are mostly noted when they form blooms that
adversely affect marine communities (Nagle and Paul
1998), or when associated with diseases in humans (e.g.,
“swimmer’s itch,” Moore 1984) or corals (Rutzler and
Santavy 1983, Feingold 1988). Researcher have also
suggested that benthic cyanobacteria may be used as
indicators of environmental degradation in both
freshwater (Perona et al. 1998) and marine benthic
habitats (La Pointe 1999). While the view of cyano-
bacteria as abnormal nuisances rather than normal
components of benthic environments prevails in marine
community studies, cyanobacteria are typical members of
the benthic community in many reefs around Micronesia
and often occur in densities similar to those of other
components of the coral reef biota (Thacker and Paul in
press).
Epifaunal diversity varied significantly among the
cyanobacterial species surveyed; the highest number of
species was associated with Lyngbya majuscula while the
lowest numbers were on L. bouillonii. The low diversity
on the latter could be related to the strong association
between the large alpheid shrimp Alpheus frontalis and L.
bouillonii. In Guam, the shrimp is found solely on L.
bouillonii where it builds a tube from the cyanobacterium.
Like all snapping shrimp, A. frontalis uses its large claw
in aggressive encounters towards other animals. This
explanation for the low diversity of epifauna on L.
bouillonii is consistent with our experimental results that
Stylocheilus readily consumed L. bouillonii (Fig. 4), even
though it was never found on this cyanobacterium in the
field (Fig. 1).
Lyngbya majuscula extracts stimulated feeding by
Stylocheilus striatus (Fig. 5) which is consistent with
previous demonstrations that feeding in this sea hare is
often not deterred and can be stimulated by secondary
metabolites from L. majuscula (Nagle et al. 1998).
However, the types and yields of secondary metabolites
can vary dramatically between populations of L.
majuscula and the same metabolite can be a feeding
stimulant or deterrent to Stylocheilus depending on its
concentration (Nagle et al. 1998, Paul et al. 2001). Thus,
cyanobacterial grazers might encounter foods that are
either stimulatory or deterrent depending on
cyanobacterial secondary metabolites, even when faced
with the same species of cyanobacterium.
Lyngbya majuscula was not readily consumed by
urchins or fishes (Fig. 4). For the urchin Echinometra
mathaei, we demonstrated that L. majuscula extracts were
strongly deterrent (Fig. 5). Other benthic cyanobacteria
are also chemically defended against macrograzers
(Pennings et al. 1997, Nagle and Paul 1998, 1999, Paul et
al. 2001). For example, Nagle and Paul (1999) tested
extracts of 10 cyanobacterial collections from Guam
against an herbivorous parrotfish and found strong
deterrence in all of the extracts.
Plant and algal chemical diversity have shaped the
evolution of plant-herbivore interactions and associations
in both terrestrial and marine systems (Rosenthal and
Berenbaum 1992, Hay and Fenical 1996, Paul et al.
2001), but until recently the chemical interactions
between benthic cyanobacteria and marine consumers
have not been considered (Paul et al. 2001). Benthic
cyanobacteria show strong parallels with eukaryotic
macroalgae on their roles as food and shelter for coral reef
consumers. Because these cyanobacteria are persistent
and often abundant components of coral reefs, they
should be integrated into the study of benthic community
processes, rather than treated as rarities or ecological
“noise” in benthic community patterns.
Acknowledgements We thank J. Biggs, R. Chang, and
S. Shjestad for assistance with collections and field
experiments. We are also grateful to the staff at the Coral
Reef Research Foundation in Palau. Funds for this
research were provided by an NIH Postdoctoral
Supplement (to E. Cruz-Rivera) to NIH grant CA 53001
(to J. Horwitz, P.I.). This is contribution # 458 of the
University of Guam Marine Laboratory.
References
Desikachary TV (1959) Cyanophyta. Indian Council of
Agricultural Research, New Delhi
Feingold JS (1988) Ecological studies of a cyanobacterial
infection of the sea plume Pseudopterogorgia acerosa
(Coelenterata: Octocorallia). Proc 6th Int Coral Reef
Symp 3: 157-62.
Hay ME (1992) The role of seaweed chemical defenses in
the evolution of feeding specialization and in the
mediation of complex interactions. In: Paul VJ (ed)
Ecological roles of marine natural products.
Comstock Publishing Assoc, Cornell University Press,
Ithaca: 93-118.
Hay ME, Fenical W (1996) Chemical ecology and marine
biodiversity: insights and products from the sea.
Oceanography 9:10-20.
Hay ME, Stachowicz JJ, Cruz-Rivera E, Bullard S, Deal
MS, Lindquist N (1998) Bioassays with marine and
freshwater macroorganisms. In: Haynes KF, Millar
JR (eds) Methods in chemical ecology, volume 2,
bioassays. Chapman and Hall, New York: 39-141.
Hay ME, Steinberg PD (1992) The chemical ecology of
plant-herbivore interactions in marine versus terres-
trial communities. In: Rosenthal GA, Berenbaum MR
(eds) Herbivores: their interactions with secondary
plant metabolites, volume II, ecological and
evolutionary processes. Academic Press, San Diego:
372-408.
Lapointe BE (1999) Simultaneous top-down and bottom-
up forces control macroalgal blooms on coral reefs
(Reply to the comment by Hughes et al.). Limnol
Oceanogr 44:1586-1592.
Moore RE (1984) Public health and toxins from marine
blue-green algae. In: Ragelis EP (ed) Seafood toxins.
American Chemical Society Symposium Series 262,
Washington: 369-376.
Nagle DG, Camacho FB, Paul VJ (1998) Dietary pre-
ferences of the opisthobranch mollusc Stylocheilus
longicauda for secondary metabolites produced by the
tropical cyanobacterium Lyngbya majuscula. Mar Biol
132:267-273.
Nagle DG, Paul VJ (1998) Chemical defense of a marine
cyanobacterial bloom. J Exp Mar Biol Ecol 225:29-
38.
Nagle DG, Paul VJ (1999) Production of secondary
metabolites by filamentous tropical marine cyano-
bacteria: ecological functions of the compounds. J
Phycol 35:1412-1421.
Paul VJ, Cruz-Rivera E, Thacker RW (2001) Chemical
mediation of macroalgal-herbivore interactions: eco-
logical and evolutionary perspectives. In: McClintock
J, Baker W (eds) Marine Chemical Ecology, CRC
Press, Boca Raton.
Paul VJ, Pennings SC (1991) Diet-derived chemical
defenses in the sea hare Stylocheilus longicauda
(Quoy et Gaimard 1824). J Exp Mar Biol Ecol
151:227-243.
Pennings SC, Pablo SR, Paul VJ (1997) Chemical
defenses of the tropical benthic marine cyano-
bacterium Hormothamnion enteromorphoides: diverse
consumers and synergisms. Limnol Oceanogr 42:911-
917.
Pennings SC, Paul VJ (1993) Sequestration of dietary
secondary metabolites by three species of sea hares:
location, specificity, and dynamics. Mar Biol 117:535-
546.
Perona E, Bonilla I, Mateo P (1998) Epilithic cyano-
bacterial communities and water quality: an
alternative tool for monitoring eutrophication in the
Alberche River (Spain). J Applied Phycol 10: 183-
191.
Peterson CH, Renaud PE (1989) Analysis of feeding
preference experiments. Oecologia 80:82-86.
Rosenthal GA, Berenbaum MR (eds) (1992) Herbivores:
their interactions with secondary plant metabolites,
volume II, ecological and evolutionary processes.
Academic Press, Inc., San Diego.
Rudman WB (1999) Stylocheilus longicauda and
Stylocheilus citrina nomenclatural discussion. Sea
Slug Forum, http://seaslugforum.net/stylnome.htm
Rutzler K, Santavy DL (1983) The black band disease of
Atlantic reef corals, I. Description of the cyanophyte
pathogen. PSZNI Mar Ecol 4:301-319.
Stachowicz JJ, Hay ME (1999) Mutualism and coral
persistence: the role of herbivore resistance to algal
chemical defense. Ecology 80:2085-2101.
Thacker RW, Paul VJ (in press) Are benthic cyano-
bacteria indicators of nutrient enrichment? Relation-
ships between cyanobacterial abundance and environ-
mental factor on the reef flats of Guam. Bull Mar Sci.
... 20 be attracted to the secondary metabolites produced by the cyanobacterium [10]. However, some secondary metabolites may be more or less accepted by these herbivores or more or less tolerated depending on concentrations. ...
... Secondary metabolites play an important role in the interactions between different organisms within the trophic chain [10,16]. Some compounds are toxic and have been selected by cyanobacteria as an effective defense strategy against herbivorous predators. ...
... Although a few studies have been done on the impact of secondary cyanobacterial metabolites on predation [10,12,13,144], very little research has involved laxaphycins and their derivatives. Among these studies, many have shown that the sea hare Stylocheilus striatus was not repelled by certain secondary cyanobacterial metabolites. ...
Thesis
Due to climate change, the lagoon of Moorea in French Polynesia is impacted by cyanobacteria blooms asphyxiating corals, causing reef degradation and decreasing food resources. Lyngbya majuscula and Anabaena torulosa are two filamentous benthic cyanobacteria that proliferate on sand and corals. They produce many secondary metabolites that can be toxic. Anabaena torulosa produces cyclic lipopeptides such as laxaphycins A and B, composed of 11 and 12 amino acids, respectively. This cyanobacterium has been able to develop chemical strategies of protection against grazers, which can be repelled by the toxic molecules produced such as laxaphycin B. In turn, herbivores must circumvent these defenses and in some cases even take advantage of them to protect themselves from their own predators. This is the case of Stylocheilus striatus, a sea hare that feeds on Lyngbya majuscula and Anabaena torulosa, and appears to be less susceptible to predation on Anabaena torulosa. Stylocheilus striatus consumes the latter without being affected by laxaphycin B toxicity. To overcome this toxicity, the sea hare has developed an adaptive mechanism that allows the biotransformation of laxaphycin B into non-toxic acyclic laxaphycin B. While non-toxic laxaphycin A is bioaccumulated in its digestive gland, laxaphycin B undergoes two successive cleavages at the C-terminal position of two hydroxyleucines. In order to study the enzymatic mechanism involved in this biotransformation, we have synthesized various analogues of laxaphycin B. First, we optimized their chemical synthesis, allowing us to confirm the structure of trichormamide C, a natural peptide analogous to laxaphycin B. In a second step, the synthesized analogues could be submitted to the studied enzyme and showed the reproducibility of the cleavage on different sequences. First characteristics of the enzyme could be identified, such as its cleavage specificities. Finally, our efforts focused on the design of a minimal peptide sequence for the recognition of the enzyme, in order to consider different strategies to isolate it.
... While invertebrate mesograzers, such as Opisthobranch molluscs (‗sea slugs', especially Stylocheilus spp.), are known specialist consumers of benthic cyanobacterial mats [47][48][49], they likely have little direct impact on reef-scale cyanobacterial mat abundance and distribution because of their typically low abundance [19]. Some mat forming cyanobacterial species, largely belonging to the genera Lyngbya, Moorena, or Dapis [50][51][52], are prolific producers of toxic secondary metabolites [53,54], and are shown to be unpalatable to most large-bodied reef herbivores in multiple feeding preference assays [44,[54][55][56][57][58][59][60]. However, recent evidence contradicts the generality of cyanobacterial avoidance, suggesting instead that cyanobacteria are a preferred nutritional target for many mobile reef grazers [61,62]. ...
Article
Full-text available
Climate change threatens to alter the processes of ecological interactions in addition to the composition and function of communities. Traditional ecological paradigms typically do not account for strong differences in the impacts of environmental stressors by trophic level, focusing instead on differential effects on competitors or functional types. Massive cyanobacterial blooms now represent a common phenomenon across most freshwater and marine communities. Here, we present a perspective considering marine cyanobacterial mats as an extreme but accessible system in which traditional ecological trophic paradigms may be tested, and make recommendations for future research on this topic.
... However, some toxic mat-forming species are known www.nature.com/scientificreports www.nature.com/scientificreports/ to deter grazing 22,[36][37][38][39][40][41][42] , and consequently, benthic cyanobacterial mats are currently viewed as largely unpalatable to large-bodied herbivores. While Clements et al. (2016) presents recent evidence that B. muricatum individuals consume benthic cyanobacterial mats on Pacific reefs 29 , no large-bodied consumers have been documented consuming cyanobacterial mats on Caribbean coral reefs where cyanobacterial mat abundance is rapidly increasing 10 . ...
Article
Full-text available
Herbivory is an important process in the general structuring of coral reef benthic communities. However, evidence of its ability to control coral reef benthic cyanobacterial mats, which have recently proliferated on reefs worldwide, remains ambivalent. Here, we report that the French Angelfish (Pomacanthus paru), Striped Parrotfish (Scarus iseri), Rock Beauty (Holacanthus tricolor), Ocean Surgeonfish (Acanthurus bahianus), Blue Parrotfish (Scarus coeruleus), and Atlantic Blue Tang (Acanthurus coeruleus) consume benthic cyanobacterial mats on coral reefs in Bonaire, Netherlands. We documented the foraging patterns of P. paru and S. iseri, and found that benthic cyanobacterial mats comprised 36.7% ± 5.8% and 15.0% ± 1.53% (mean ± standard error) of the total bites taken by P. paru and S. iseri respectively. This magnitude of consumption suggests that grazing by reef fishes may represent a potentially important, but previously undocumented, top-down control on benthic cyanobacterial mats on Caribbean reefs.
... The island fauna have been the subject of biodiversity research focused on marine and coral reef ecosystems (e.g. Cruz-Rivera and Paul 2000; Bentis et al. 2000; Burdick et al. 2008). Terrestrial studies have focused on the diversity of endemic vertebrate and plant species, but the introduction of numerous exotic species, land conversion and natural resources exploitation have negatively impacted these (Weston Jr 1912; Stone 1971; Whistler 1995; Denslow et al. 2009; Pregill and Steadman 2009). ...
Article
Full-text available
Ceraceosorales is a monotypic order in Ustilaginomycotina. Its namesake, Ceraceosorus bombacis, was described as a phytopathogen of Bombax ceiba in India. In this study, we describe Ceraceosorus guamensis sp. nov., collected on the South Pacific island of Guam, which appears to represent the second isolation of any member of this order in over 40 years. Ceraceosorus species are monokaryotic and filamentous in culture, producing conidia on potato dextrose agar. However, both species behave yeast-like when cultured on corn meal agar. The internal transcribed spacer (ITS) region (spanning the ITS1–5.8S–ITS2) in both species of Ceraceosorus is highly heterogeneous containing multiple disparate copies that can vary intragenomically by up to 3.5 %. Moreover, this region could not be amplified using the fungal ITS primers most frequently used for culture-independent methods of assessing fungal biodiversity. This fact, combined with the extremely slow growth rates on commonly employed media, may indicate that members of this lineage are potentially underdetected by current sampling methods.
... Thus, once established, those mats can act as net nitrogen sources, supplying additional nitrogen to the system and perpetuating a nutrient pollution problem (Hoffmann 1999). Cyanobacterial mats are also known to support a community of associated organisms, from other bacteria to invertebrate grazers (Cruz-Rivera and Paul 2002). ...
Article
Full-text available
Molecular analysis of cyanobacterial mat communities indicated that cyanobacteria, ammonia-oxidizing Archaea (AOA), and ammonia-oxidizing bacteria (AOB) coexist in those systems, competing for ammonium; this situation would imply competitive exclusion. We attempted to model how ammonia utilization niche partitioning occurs, and how ammonium levels can influence the interaction between those groups in a one-dimensional diffusionlimited system using Michaelis-Menten kinetics to describe ammonium consumption by each of those three groups. In our model, AOAs were able to dominate ammonium uptake by the community under most circumstances, except for unrealistically high (millimolar) levels of ammonium, where AOBs gained advantage. Cyanobacteria were unable to effectively compete for ammonium with either AOBs or AOAs throughout the mat at all ammonium concentrations and cell counts, suggesting that the presence of AOAs or AOBs forces cyanobacteria into nitrogen fixation mode. Such interaction can make cyanobacterial mats a net nitrogen source, as well as provide a carbon-independent energy transfer pathway from primary producers to the rest of the ecosystem.
... An increasing abundance of cyanobacterial mats in coral reefs has been documented and largely attributed to anthropogenic disturbances of watersheds, particularly eutrophication (Kuffner and Paul 2001;Paul et al. 2005;Sharp et al. 2009). Large-scale shifts from coral-dominated to cyanobacteria-dominated communities can result in a severe loss of biodiversity (e.g., Paul et al. 2005), although an enhancement of biodiversity may occur under nonbloom conditions due to the recruitment of specialized and transient cyanobacteria-associated epifauna, many of which are invertebrates that directly consume the mats (Cruz-Rivera and Paul 2002Paul , 2006. Increases in cyanobacterial mat abundance have been also linked to skin conditions from contact with, and respiratory problems from inhalation of, cyanobacterial secondary metabolites during blooms (Sharp et al. 2009;Osborne et al. 2001). ...
Article
Coral-reef filamentous cyanobacterial mats are complex communities of microbes. We used DGGE and eubacterial and archaeal 16S rRNA and amoA ammonium monooxygenase subunit A primer sets to explore the presence of genes mediating nitrogen conversion within cyanobacterial mats from Hawaii. DGGE band analysis revealed the presence of halophiles such as Halococcus salifodinae and of Nitrosopumilus-like organisms. Twenty seven out of 31 clone sequences exhibited a 95 % or greater 16S rRNA gene identity with known archaeal ammonia oxidizers such as Nitrosopumilus maritimus. The presence of Archaea within those mats, as well as the co-occurrence of both ammonia-oxidizing Archaea and ammonia-oxidizing Bacteria suggests importance of the former in the cyanobacterial mat community, and suggests greater than anticipated diversity of nitrogen conversion processes and organisms in those systems.
Article
Full-text available
Cyanobacteria have multifaceted ecological roles on coral reefs. Moorena bouillonii, a chemically rich filamentous cyanobacterium, has been characterized as a pathogenic organism with an unusual ability to overgrow gorgonian corals, but little has been done to study its general growth habits or its unique association with the snapping shrimp Alpheus frontalis. Quantitative benthic surveys, and field and photographic observations were utilized to develop a better understanding of the ecology of these species, while growth experiments and nutrient analysis were performed to examine how this cyanobacterium may be benefiting from its shrimp symbiont. Colonies of M. bouillonii and A. frontalis displayed considerable habitat specificity in terms of occupied substrate. Although found to vary in abundance and density across survey sites and transects, M. bouillonii was consistently found to be thriving with A. frontalis within interstitial spaces on the reef. Removal of A. frontalis from cyanobacterial colonies in a laboratory experiment altered M. bouillonii pigmentation, whereas cyanobacteria-shrimp colonies in the field exhibited elevated nutrient levels compared to the surrounding seawater.
Article
Full-text available
Benthic cyanobacteria have commonly been a small but integral component of coral reef ecosystems, fulfilling the critical function of introducing bioavailable nitrogen to an inherently oligotrophic environment. Though surveys may have previously neglected benthic cyanobacteria, or grouped them with more conspicuous benthic groups, emerging evidence strongly indicates that they are becoming increasingly prevalent on reefs worldwide. Some species can form mats comprised by a diverse microbial consortium which allows them to exist across a wide range of environmental conditions. This review evaluates the putative driving factors of increasing benthic cyanobacterial mats, including climate change, declining coastal water quality, iron input, and overexploitation of key consumer and ecosystem engineer species. Ongoing global environmental change can increase growth rates and toxin production of physiologically plastic benthic cyanobacterial mats, placing them at a considerable competitive advantage against reef-building corals. Once established, strong ecological feedbacks [e.g., inhibition of coral recruitment, release of dissolved organic carbon (DOC)] reinforce reef degradation. The review also highlights previously overlooked implications of mat proliferation, which can extend beyond reef health and affect human health and welfare. Though identifying (opportunistic) consumers of mats remains a priority, their perceived low palatability implies that herbivore management alone may be insufficient to control their proliferation and must be accompanied by local measures to improve water quality and watershed management.
Article
Full-text available
While benthic, filamentous cyanobacteria can be common on coral reefs, the factors influencing their distribution are poorly understood. Cyanobacterial blooms, like macroalgal blooms, may result from a combination of coastal eutrophication and reduced herbivory. Because benthic cyanobacteria are unpalatable to generalist herbivores, there may be little top-down control of cyanobacterial abundance. Since bottom-up factors may exert more influence on cyanobacterial populations, we hypothesized that high cyanobacterial abundance may be an indicator of high nutrient availability. In addition, cyanobacteria may compete with macroalgae for light and nutrients. Thus, we also hypothesized that cyanobacterial abundance may be negatively associated with macroalgal abundance. Since many strains of cyanobacteria wash ashore during periods of high wave action, we hypothesized that cyanobacterial abundance is negatively associated with wave height. We monitored cyanobacterial abundance, macroalgal abundance, nitrogen availability, phosphorus availability, salinity, and water temperature at nine reef flat locations around Guam. Average wave height for eastern and western shores, rainfall, minutes of sunshine, and wind speed were also monitored. Stepwise regression was used to determine which variable or combination of variables best explained variation in cyanobacterial abundance. Although nutrient availability was not significantly associated with cyanobacterial abundance, a positive association with macroalgal abundance explained 11.5% of the observed variation in total cyanobacterial abundance. At one site, negative relationships with macroalgal abundance and wave height explained 79.4% of the observed variation in the abundance of the cyanobacterium Oscillatoria margaritifera. Variation in cyanobacterial abundance can be best explained by examining individual strains of cyanobacteria, rather than by treating all cyanobacteria as a single ecological unit. Physical disturbance can be a more important influence on cyanobacterial abundance and distribution than either nutrient availability or interactions with macroalgae.
Article
Cyanobacterial blooms are becoming more common in many reef habitats. The broadly acting feeding deterrent compound ypaoamide, produced by a mixed cyanobacterial assemblage, has been linked to bloom formation and mass fish die-offs (Siganus argenteus and Siganus spinus) in Guam. Specific metabolites produced by Lyngbya majuscula Gomont act as both feeding attractants to the specialist herbivore Stylocheilus longicauda, and as effective feeding deterrents to generalist fishes. Two-dimensional TLC (2D-TLC) analysis of cyanobacterial crude extracts was used to select chemically distinct populations (chemotypes) of bloom-forming filamentous cyanobacteria for chemical and ecological evaluation. Crude extracts produced by different species, chemotypes, and chemically distinct Micronesian marine cyanobacterial assemblages deter feeding activity of generalist reef herbivores. The ecological function of cyanobacterial secondary metabolites, especially as related to diversity of compound production and the relationship of metabolite production to bloom formation is discussed.
Simultaneous top-down and bottom-up forces control macroalgal blooms on coral reefs (Reply to the comment by Hughes et al.)
  • Lapointe
Lapointe BE (1999) Simultaneous top-down and bottom-up forces control macroalgal blooms on coral reefs (Reply to the comment by Hughes et al.). Limnol Oceanogr 44:1586-1592