Turbinaria 2

Turbinaria ornata and its associated community composition in Moorea, French
Polynesia
Laura Anderson, Megan Moriarty, Brennan Wenck
Abstract:
Turbinaria ornata is a very abundant species of brown algae that is common in
Moorea, French Polynesia. It is controversial whether Turbinaria is an invasive or
simply opportunistic species. Whatever its role in the ecosystem, Turbinaria is indicative
of a disturbed coral reef. It is crucial to understand the affect of Turbinaria on coral reef
environments and the unique community that Turbinaria may support. Our study took
place at West Opunohu, Moorea from November 9th through November 29th, 2006. We
found that floating Turbinaria mats are used by a specific species of fish recruits
(Pygoplites diacanthus). Turbinaria mats may be a means of transport for fish recruits to
cross the crest and enter the lagoon. Our results also suggest that juvenile fishes eat the
epiphytes/epifauna found on detrital Turbinaria. When Turbinaria is removed from a
coral bommie, a slight change in species composition occurs, however, more work needs
to be done on this subject. The conservation of coral reefs is important and includes
understanding how species compositions are adjusting to a changing ecosystem.
Introduction:
Turbinaria ornata is a brown fucoid alga that proliferates along disturbed coral
reef crests and coral bommies in French Polynesia. This alga grows densely in two
morphological forms: on the reef crest the alga is short and stubby due to constant
disturbance from crashing waves, while away from the crest the alga grows taller,
increasing its ability to absorb sunlight (Payri et al., 2000). These tall patches of algae are
found more densely at the reef crest and dwindle further from the crest towards shore.
Turbinaria can be found sparsely distributed on the outside of the crest, which is likely
due to depth and turbulence. (Kingsford and Choat, 1985).
It is controversial whether Turbinaria is invasive or not, due to its r-selected
population dynamics; Turbinaria reproduces often and successfully with large numbers
of progeny. Given these characteristics, Turbinaria is an opportunistic species that is
able to readily invade susceptible environments such as damaged coral reefs (Schaffelke
et al., 2006).
Disturbances tend to break Turbinaria free from its holdfast. This loose
Turbinaria collects and forms floating mats that are subject to movement by currents and
wind advection. These mats often travel within lagoons, due to the ebb and flow of tides
and currents. At times, these mats float into the open ocean and occasionally make their
way back over the crest and into the lagoon. The integrity of these mats is aided by the
presence of teeth on the leaves of the algae, which act like natural Velcro and hold the
pieces together (Payri et al., 2000).
The commonness of Turbinaria in the lagoon system of Moorea suggests that the
coral reef could be compromised. Often, the more algae present, the less space, light and
resources are available to corals; this changes the ecosystem and associated food web
(Schaffelke et al., 2006). The microbes found in algae often advance the destruction of
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coral reefs because they are fatal to corals (Smith et al., 2006). However, algae (and
especially the structure provided by algae) have been shown to be beneficial to reef
residents by providing food for herbivores, habitat for small fish (Dempster and
Kingsford, 2004), and possibly even shelter for recruits crossing the crest. The degree to
which this holds true for Turbinaria however, is unknown.
In many temperate systems, drift macroalgae often collects and forms rafts that
can be used as alternative habitats for pelagic species. Fish and invertebrates from the
open ocean can find protection and resources in these microhabitats. These floating
environments have been studied extensively in temperate regions (Dwyer, 2002;
Dempster and Kingsford, 2004), however tropical drift systems have not.
Studies have shown that Turbinaria is sometimes eaten by tropical herbivores
(Steinberg, 1986). Specifically, a study by Lewis found that Sparisoma (parrotfishes)
and Acanthurus (surgeonfishes) are the primary consumers of fleshy tropical algae
(1985). Juveniles of these families have commonly been found among algae
communities (McClanahan et al., 2000) however, it is unknown whether they consume
Turbinaria or not.
The removal of fleshy algae (such as Turbinaria) from Caribbean coral reefs has
been shown to increase the abundance of some herbivorous and invertebrate-eating
fishes. This could be due to an increase in the accessibility of substrate, and thus the
availability of benthic prey. When macroalgae is removed, early successional turf algae
usually replaces it. The amount, net production, and palatability of turf algae also
increase with the removal of fleshy algae (McClanahan et al., 2000).
In this study we investigated three general questions to assess the relationship
between Turbinaria and its surrounding community.
Question 1: Are fish recruits transported across the reef crest in Turbinaria mats?
Question 2: Do fishes use Turbinaria or the epiphytes and epifauna on Turbinaria as
food?
Question 3: How does the presence of Turbinaria affect residential species
assemblages?
To address these questions we developed the following specific hypotheses:
Hypothesis 1: More recruits will be found on an artificial Turbinaria mat
placed outside the crest than on a mat placed on the inside of the crest.
Hypothesis 2: When fishes are presented with cleaned detrital Turbinaria as
well as uncleaned detrital Turbinaria, they will be seen nibbling on the
uncleaned Turbinaria more often because of the associated epifauna and
epiphyte assemblage.
Hypothesis 3: When Turbinaria is removed from a coral bommie, the
resulting species assemblage will be different from the original assemblage.
This study aims to assess the interactions between Turbinaria and its surrounding
community. Understanding this algal system may increase our overall knowledge
of coral reef environments.
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Materials and Methods:
Spatial and Temporal Conditions:
This study took place in Moorea, French Polynesia at a site in Opunohu Bay
known as West Opunohu. This area contains a large proportion of damaged or dead
Porites coral and coral rubble. We worked mostly inside the lagoon at depths between 2
and 6 feet. Periodically, we worked outside the reef crest at the surface where depths
reached 20 to 30 feet. Surge and wind conditions outside the crest were generally
stronger than inside the lagoon. Our study was done using skin diving techniques. The
study took place from November 9th to November 29th; this time period included two
quarter moons and a new moon.
Species Description:
Turbinaria ornata is an erect brown fucoid alga having a firm, terete stalk that grows
up to 15 cm tall. The branchlets extend to give the alga about 5 cm of lateral depth. The
leaves terminate in a crown of teeth; this unique morphology increases surface area while
simultaneously deterring herbivory (Payri et al., 2000).
Artificial Turbinaria mats as transportation for fish recruits across the crest
Natural Turbinaria mats are typically abundant in Moorea, however at the time of
this study none were present at our study site. Therefore we removed attached
Turbinaria in order to construct two artificial Turbinaria mats. We made these by tying
individual stalks of Turbinaria onto a 1½ m by 1½ m grid of plastic fencing material
(Image 1). The mats included five plastic bottles as floatation devices and a wooden pole
for maintaining structure. We also made two control mats from the same fencing
material that had strips of black plastic tied to the grid (Image 2). One treatment mat and
one control mat were placed outside the crest while the other two were placed inside the
lagoon. All were anchored using rope and a cinderblock.
We placed our first treatment Turbinaria mat outside the crest on November 12th.
It remained outside until November 19th, at which point it was stolen. To replace the
stolen mat, we constructed another treatment mat and deployed it on November 22nd.
This mat, however, was anchored too deep and sank below the surface. The outside
control mat was deployed on November 15th and remained outside until November 19th,
when it too was stolen (apparently Turb mats are a hot commodity). On November 22nd
we replaced this control mat and continued to observe the replacement until November
29th. We were unable to access our outside mats every day on account of inclement
weather and ocean conditions. We placed our inside treatment mat and control mat
inside the lagoon on November 15th and continued observing it until November 29th.
Since there was no treatment mat on the outside to contrast with our outside control mat,
we ended all of our comparison studies on November 18th.
The quarter moons occurred on November 12th and November 28th. The new moon
occurred on November 20th; specific phases of the moon correlate with recruitment of
particular fish species (Robertson, 1992). Each day we observed these mats and
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occasionally used hand held nets to collect a few specimens for identification. To
analyze this data we used a Pearson Chi Squared test.
Image 1
Treatment Turbinaria mat
Image 2
Control mat
Turbinaria or its epifauna/epiphytes as food:
We selected a large patch of detrital Turbinaria (approximately 15 m2) where
Turbinaria had accumulated and settled on the sand between several large coral
bommies. We observed this patch on twelve different days for ten minutes each time and
noted the species, number, and behavior of all fishes that interacted with the detrital
Turbinaria. We made these observations in order to monitor fish species composition
and the relationship between fishes and detrital Turbinaria over time.
We collected and cleaned (by freshwater dipping and scrubbing) stalks of
Turbinaria taken from the detrital patch. This Turbinaria was then attached to a
cinderblock using netting (Image 3) and placed in a separate detrital patch. We observed
this patch every other day for three days and recorded fish preference for
cleaned/uncleaned Turbinaria as food. Each day of observation we did a quick visual
inspection to determine when epifauna/epiphytes began to appear; we ended this portion
of the study once this occurred. This should have taken place everyday on account of
how fast the Turbinaria once again became dirty. Because of this we repeated the
process once more with observations taking place everyday for another three days. We
analyzed the resulting data using Primer software (version 6) that produced a MDS graph,
an ANOSIM test, and a SIMPER analysis.
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Image 3
Cleaned Turbinaria attached to cinderblock for food study.
Turbinaria removal and its effect on species assemblage
Three large coral bommies were selected in different areas (one close to the crest
and two further away). On the first day of sampling we observed species number and
behavior of all fishes associated with the attached Turbinaria for ten minutes at each site.
We then removed all the Turbinaria covering these bommies. In the following days we
performed the same observations on these removal patches in order to determine whether
species composition changed over time. This was again determined using Primer
software that produced an MDS graph and an ANOSIM test.
Results
Artificial Turbinaria mats as transportation for fish recruits across the crest
Over the 7 days that we had both our control and treatment Turbinaria mats
outside the crest, a total of 5 recruits came to the treatment mat and 3 came to the control
mat (Figure 1). All the observed recruits were Pygoplites diacanthus (Regal Angelfish).
Inside the lagoon, no recruits came to either the control or the treatment mat. In order to
determine if there was a significant difference between the treatment and control rafts on
the outside, a Pearson Chi Squared test was performed. The resulting Pearson Chi
Squared Value was 1.061, df = 1: p = 0.303. This indicated that there was not a
significant difference; therefore, the material composition of the mat was insignificant.
During the time period between November 15th and November 29th, no recruits were
observed on either of the inside mats. Between November 22nd and November 29th, no
recruits were observed on the outside control mat.
The mat on the inside never collected any recruits while the mat on the outside
did (Figure 2). A Pearson Chi Squared test was also performed on this data to determine
whether there was a significant difference between the treatment mats on the inside and
on the outside. The Pearson Chi Squared Value was 5.6, df = 1: p = 0.018. The
difference was significant.
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Figure 1: The number of fish recruits observed outside the crest on the treatment and control Turbinaria
rafts over seven consecutive days. The last quarter moon occurred on November 12th and the new moon
was on November 20th.
Figure 2: The number of fish recruits observed on the treatment Turbinaria rafts both inside and outside
the lagoon over a period of 10 days. The last quarter moon occurred on November 12th and the new moon
was on November 20th.
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Turbinaria or its epifauna/epiphytes as food:
Using Primer software (version 6), we created a MDS (non-metric
multidimensional scaling) graph where a short distance between points corresponds to a
high similarity between sites and vice versa (Figure 3). We sampled cleaned and
uncleaned (dirty) Turbinaria at the same area through time. The species composition was
highly variable in cleaned sites, especially as the cleaned Turbinaria became dirty over
time. The species composition remained constant at the dirty site. Figure 3 shows that
there is a difference between cleaned and uncleaned sites. We transformed the data by
taking the fourth root to make rare species of fishes more important to our study. We also
ran an ANOSIM (Analysis of Similarities) test, which measures how different
communities are from each other. We found a significant difference between cleaned and
uncleaned Turbinaria (Global R= 0.17, p= 0.039). We also performed a SIMPER
(Similarity of Percentages) analysis, which took into account species richness and
abundance to determine which species were most consistent and may have driven the
pattern we observed. The most consistent and abundant fishes were Sacrus sordidus
(Bullethead Parrotfish juvenile), Ctenochaetus striatus (Stripped Bristletooth
Surgeonfish), Stetathojulis bandanensis (Redshoulder Wrasse juvenile), and Halichoeres
hortulanus (Checkerboard Wrasse). These four species represent 54.98% of the
community composition and could be responsible for the difference between cleaned and
dirty Turbinaria sites.
Figure 3: Non-metric multidimensional scaling graph showing the difference between cleaned Turbinaria
and dirty Turbinaria communities. Each point represents a day of sampling the cleaned and dirty
Turbinaria sites (which were at the same location).
MDS Graph of Cleaned and Dirty Turbinaria
Transform: Fourth root
Resemblance: S17 Bray Curtis similarity
2D Stress: 0.01
Site
Clean
Dirty
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Turbinaria removal and its effect on species assemblage
Using Primer software, we created a MDS graph (Figure 4) and transformed the
data by taking the square root. We also ran an ANOSIM test and did not find a significant
difference between pre and post removal Turbinaria sites. However, when comparing
the three sites to each other, we found a significant difference between the sites (Global
R=0.518, p=0.01).
Figure 4: Non-metric multidimensional scaling graph showing the difference between three different coral
bommies before and after Turbinaria removal (1=before removal, arrow = trend of species composition
change). Site 1 and Site 3 are parallel and further from the crest while Site 2 is relatively close to the crest.
MDS Graph of 3 Sites Before and After Turbinaria Removal
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Discussion
Artificial Turbinaria mats as transportation for fish recruits across the crest
When wave action is sufficient enough to move water over the crest, any floating
objects nearby are also carried over. Based on this, we assumed that if our artificial
Turbinaria mat was not anchored, it would cross the crest, thereby transporting any
associated recruits into the lagoon. We anchored our mat because if it crossed over the
crest and we were unable to reach it immediately, any recruits might have settled before
being observed. To account for this, we placed a control and treatment mat on the inside
of the lagoon. This determined that if recruits had been found on the lagoon mats, they
were possibly using Turbinaria as settlement substrate and not as a means of
transportation across the crest. Since recruits were found only on the outside mats and
not on the inside mats, this supports our hypothesis that recruits are using the mats as a
means of transportation.
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We made control mats to determine if fish recruits were using a Turbinaria mat
because it was made of Turbinaria or simply because it was a floating object in the open
ocean. The fact that we found recruits on both the control and treatment rafts indicated
that fish recruits in a pelagic environment make use of shelter provided by floating
structures, regardless of composition. In a similar study done by Dempster and
Kingsford (2004) fishes were also found associating with control mats and algae clumps
because these both provided three-dimensional structure.
It is especially interesting that the only species of recruits found on our mats were
Pygoplites diacanthus (Regal Angelfish). This could show that Turbinaria (or simply a
floating object outside the crest) is used by a very specific cohort. This species of recruit
has never been observed using any other recruit collection method such as light traps,
RADCULTS, or coral manipulation. P. diacanthus adults are typically found on fringing
reefs, such as Coconut Grove, Moorea (Bernardi, personal communication). A possible
explanation for finding P. diacanthus recruits on the outside of the crest is that these
recruits use floating Turbinaria as transportation from a pelagic environment to the
fringing reef of a lagoon. This could indicate that an association with floating objects is
an important part of fishes’ early life stages (Dempster and Kingsford, 2004).
If time and resource constraints had not been an issue during this study, we would
have made more and larger control and treatment mats for outside and inside the crest.
Turbinaria or its epifauna/epiphytes as food:
Our feeding experiment intended to determine whether fish in a patch of detrital
Turbinaria were consuming Turbinaria itself or the epiphytes/epifauna associated with it.
Since the fishes did not nibble on the cleaned Turbinaria until it got dirty, but did nibble
on the uncleaned Turbinaria, this suggests that fish were in fact not eating Turbinaria,
but more likely eating the epiphytes/epifauna that had been removed from the Turbinaria.
This result was significant as a cumulative effect and not a day-to-day effect.
Detrital patches may provide food, habitat, shelter, and renewable resources for fish
species. In our study we consistently found more juveniles associated with detrital
Turbinaria. This could be for a few reasons: niche partitioning and jaw morphology
(Lewis, 1985). It is possible that adult fish may outcompete juveniles for food and space
on coral heads. Therefore, juveniles may utilize detrital Turbinaria sites as an appropriate
niche. Also, since juveniles’ jaws are not full-grown, they may be unable to eat the
actual Turbinaria and instead nibble on the associated epiphytes and epifauna. This is
opposed to adults that have been shown to eat Turbinaria itself; parrotfishes have
powerful jaws and fused dental plates for nibbling through hard materials such as coral.
This morphology allows them to eat algae that have physical defense mechanisms such as
Turbinaria, which is tough and spiny (Lewis, 1985).
It would have been ideal to examine the gut contents of the fish we were observing
to be more certain of their diet, as done in a study by Eagle and Jones (2004). However,
given the partially disintegrated nature of detrital Turbinaria and the very small size of
the juveniles associated with this form of Turbinaria, examining gut contents would have
been difficult. In future studies, stable isotope analysis would help address this question
more definitively. Also, we should have included cinderblocks covered with dirty
Turbinaria to control for the effect of the block on fish behavior.
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Turbinaria removal and its effect on species assemblage
We originally expected to observe a change in fish species composition between pre
and post Turbinaria removal sites however, due to the limited pre removal data, we were
unable to sufficiently answer this question. However, figure 4 visually shows that when
Turbinaria is removed, the species composition does not conform to the pre-removal data
point. Instead our data demonstrated a pattern between the three sites in relation to their
distance from the crest. The difference in species composition may not be due to
Turbinaria presence but instead to distance from the crest. Sites 1 and 3 are further from
the crest (and parallel to each other). When they were cleared of Turbinaria, the species
composition became more like that of site 2 (before Turbinaria removal), which is closer
to the crest. A possible explanation for this is that with cleared Turbinaria, the coral
bommie may be exposed to more current, thereby more closely resembling conditions
near the crest.
Possible confounding factors in this part of our study were that the removal of
Turbinaria made it easier to see and count the resident fish and our sampling technique
likely improved with time. We should have made more observations of the three coral
bommies before removing Turbinaria, instead of only one day of observations for each
site. In future studies, we recommend observing one or more nearby control bommies
with intact Turbinaria for comparison with the coral bommies stripped of Turbinaria.
Tubinaria is useful to its surrounding community in all its forms: attached, floating,
and detrital. This study has shown that Turbinaria is an integral part of Moorea’s coral
reef ecosystem. Our Turbinaria mats may be used by fish recruits as shelter and
transportation. The epiphytes and epifauna on detrital Turbinaria have been shown to be
important food sources for specific juvenile fishes and may even serve as protection.
Attached Turbinaria may also provide protection for fishes from abiotic factors such as
strong currents. Turbinaria removal may increase exposure, in turn affecting species
assemblages.
Our study has several implications for conservation. It is crucial to understand algal
systems and their role in changing ecosystems, for instance the function of Turbinaria in
damaged coral reefs. Turbinaria may support a unique community composed of species
that fill various niches. Before any possible Turbinaria removal programs are enacted,
this associated community should be taken into account. However, a removal program
could be unfeasible due to the reproductive success and wide distribution of Turbinaria.
In a study done by Andrefouet et al. (2004), the biomass of Turbinaria and its
distribution were documented before a removal event took place for cosmetic industries.
Although this study made sure there was enough Turbinaria to harvest, it should have
assessed the environmental impact as well. Any resulting change, whether deleterious,
advantageous, or neutral, should be studied and documented before enacting large-scale
removal plans.
The history of Turbinaria in and around French Polynesia is not well known. It is
controversial whether Turbinaria is invasive or simply an opportunistic species. Because
of this, it is questionable whether Turbinaria removal could return coral reefs to a
previous state; this state itself is unknown. The history of Turbinaria is relatively
unimportant. What is important is that Turbinaria is a well-established and incorporated
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component of coral reefs. Turbinaria itself may not be the main cause of coral reef
mortality in Moorea. Instead it is possible that anthropogenic damage, such as global
warming and pollution, along with natural damage, such as cyclones, could simply have
allowed Turbinaria to flourish as an opportunistic species. The conservation of coral
reefs is crucial and includes understanding how the community is adapting in response to
a changing ecosystem.
Acknowledgements:
Big Hammer, Ribbon Dancer, and EWW Brennan would like to thank everyone
who was coerced into hours of building Turb mats surrounded by biting bugs, rank
smells, and oppressive humidity. We would also like to thank the entire Bio162 class and
the CRIOBE Staff for being one big supa cool fam. We deeply appreciate everyone who
made this amazing trip possible (Mom, Dad, Julio, Pete R. and Giacomo). Thanks also
to Kendra, Tish, and Kristin for being such supportive TAs and talented boat drivers.
Lyrics and her backup singers would especially like to thank Pete Dal Ferro for being
their eternal spoken word muse. The Turbo Turbinator Trio would like to acknowledge
that much Turbinaria was perTurbed during this study. Heehee
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Works Cited
Andrefouet, S, M. Zubia, C. Payri. 2004. Mapping and biomass estimation of the
invasive brown algae Turbinaria ornata and Sargassum mangarevense on heterogeneous
Tahitian coral reefs using 4-meter resolution IKONOS satellite data. Coral Reefs. 23
(1): 26-38
Dempster, T. and Kingsford, M.J. 2004. Drifting objects as habitat for pelagic juvenile
fish off New South Whales, Australia. Marine and Freshwater Research. 55: 675-687
Dwyer, T.R. 2002. Temporal patterns in drift algal community structure. Friday Harbor
Laboratories.
Eagle, J.V. and Jones, G.P. 2004. Mimicry in coral reef fishes: ecological and
behavioural responses of a mimic to its model. The Zoological Society of London. 264:
33-43.
Kingsford M.J. and Choat, J.H. 1985. The fauna associated with drift algae captured
with a plankton-mesh purse seine net. Limnology and Oceanography. 30: 618-630.
Lewis, S.M. 1985. Herbivory on coral reefs: algal susceptibility to herbivorous fishes.
Oecologia. 65: 370-375.
McClanahan, T.R., K. Bergman, M. Huitric, M. McField, T. Elfwing, M. Nystrom, I.
Nordemar. 2000. Response of fishes to algae reduction on Glovers Reef, Belize. Marine
Ecology Progress Series. 206: 273-282.
Payri, C., A.R. N’Yeurt, J. Orenpuller. 2000. Brown algae (fucophyceae). in Algae of
French Polynesia. Au Vent des Iles. Singapore. pp.148-149.
Robertson, D.R. 1992. Patterns of lunar settlement and early recruitment in Carribbean
reef fishes at Panama. Marine Biology. 114: 527-537.
Schaffelke, B., J.E. Smith, C.L. Hewitt. 2006. Introduced macroalgae – a growing
concern. Journal of Applied Phycology.
Smith, J.E., M. Shaw, R.A. Edwards, D. Obura, O. Pantos, E. Sala, S.A. Sandin, S.
Smriga, M. Hatay, F.L. Rohwer. 2006. Indirect effects of algae on coral: algaemediated, microbe-induced coral mortality. Ecology Letters. 9: 835-845.
Steinberg P.D. 1986. Chemical Defenses and the susceptibility of tropical marine brown
algae to herbivores. Oecologia. 69: 628-630.
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