Swarming and Hibernation Project Proposal Annika Binet Ecology
Distribution of the parasitic snail, Cyphoma gibbosum, and its effects on the health of its soft coral hosts in Utila, Honduras
1. Distribution of the parasitic snail, Cyphoma gibbosum, and its effects on the health of its soft
coral hosts in Utila, Honduras
by
Muriel Magnaye
A report submitted to the Department of Environment and Geography,
University of Manitoba,
in partial fulfillment of the requirements for course
ENVR 4500 (Honours Thesis Project)
April, 2015
2. i
Abstract
Cyphoma gibbosum is a generalized predator of octocorals in Caribbean reefs. Its
contribution to the rapidly declining health of coral reefs, particularly disease and algal
overgrowth, is examined here. Benthic surveys were conducted at five sites surrounding Utila,
Honduras and one site was monitored regularly over 42 days to examine host preference and the
health state of the hosts. Adult C. gibbosum were found most frequently on Eunicea flexuosa,
Gorgonia ventalina, and Antillogorgia americana; juvenile C. gibbosum were found consistently
on A. americana. C. gibbosum does not select its host in proportion to the host abundance on the
reef. Adult snails were more abundant in shallow reefs (5m) than deep reefs (15m). Contrary to
previous research, C. gibbosum was not found to prefer diseased over healthy hosts. No
significant relationships were identified between snail occupation and disease and overgrowth.
Other environmental factors or anthropogenic effects may be the cause and should be considered
when investigating the declining health of coral reefs.
3. ii
Acknowledgements
First and foremost, I would like to thank my research supervisor Vanessa Lovenburg.
Without her assistance and support from the beginning and through every step of the way, this
project would not have been possible. She raised many important discussion points which I had
not considered beforehand, and I hope I’ve addressed them here. Thank you very much for your
patience and understanding through this past year and a half. I could not have asked for a better
supervisor, both in the field and afterwards.
I would also like to express my gratitude to Rick Baydack, Norman Kenkel, and David
Walker. Rick Baydack was my co-ordinator and mentor throughout the past three years and has
always pointed me in the right direction; I would not have come across the opportunity to work
on this project without your guidance. Norman Kenkel and David Walker assisted me with the
statistical analyses and offered important feedback and suggestions.
In June 2014, I went to Utila, Honduras through Operation Wallacea in order to collect
the data for this project. My time there provided me with important experience and the field
season would not have been successful without my fellow dissertation students and research
assistants. Finally, thank you Dan Exton for your guidance and consultation, both in the field and
off.
4. iii
Table of Contents
Abstract............................................................................................................................................ i
Acknowledgements......................................................................................................................... ii
Table of Contents ...........................................................................................................................iii
List of Tables.................................................................................................................................. iv
List of Figures................................................................................................................................. v
Introduction..................................................................................................................................... 1
Methods........................................................................................................................................... 6
Study Site.................................................................................................................................... 6
Benthic Surveys .......................................................................................................................... 8
Monitoring: ................................................................................................................................. 8
Statistical Analysis.....................................................................................................................11
Results........................................................................................................................................... 15
Species distribution and preference .......................................................................................... 15
Host health ................................................................................................................................ 25
Discussion..................................................................................................................................... 28
Bibliography ................................................................................................................................. 33
5. iv
List of Tables
Table 1: Octocoral densities and Ivlev's electivity index values (E) (Ivlev 1961) for adult and
juvenile Cyphoma gibbosum at 5m and 15m. Absence of electivity values indicate the absence of
host species at the respective depth. ............................................................................................. 16
Table 2: Distribution of Cyphoma gibbosum across shallow and deep reefs .............................. 20
Table 3: Residence time of Cyphoma gibbosum on hosts in Coral View Reef............................ 24
6. v
List of Figures
Figure 1: Study Sites around Utila, Honduras ............................................................................... 7
Figure 2: Male Cyphoma gibbosum............................................................................................. 10
Figure 3: Female Cyphoma gibbosum genital pore (gp) within the tissue of the foot ................ 10
Figure 4 C. gibbosum host distribution around the 5 sites: Coral View, Little Bight, Stingray
Point, Spotted Bay, and The Maze. ............................................................................................... 19
Figure 5: Host preference of C. gibbosum at 5m around the five sites: Coral View, Little Bight,
Stingray Point, Spotted Bay, and The Maze ................................................................................. 21
Figure 6: Host preference of C. gibbosum at 15m around the five sites: Coral View, Little Bight,
Stingray Point, Spotted Bay, and The Maze ................................................................................. 21
Figure 7: Cyphoma gibbosum host occupancy and movement around Coral View Reef............ 23
Figure 8: Frequency of adult and juvenile Cyphoma gibbosum by health class of hosts (0 –
healthy; 1 – light predation; 2 - heavy predation; 3 – light disease; 4 – heavy disease) around
Utila............................................................................................................................................... 26
Figure 9: Relation between Snail Occupation (SnO), a size corrected measure of frequency, and
Host Health, with regard to Predation, Disease, and Algal Overgrowth ...................................... 27
7. 1
Introduction
Coral reefs are being lost worldwide at dramatic rates and their loss is most critically
observed in the Caribbean. The primary cause of reduced coral cover is attributed to disease
outbreaks (Aronson et al. 2003), and a phase shift from coral dominated to marcroalgae
dominated reefs (Wahle 1985). The past few decades have shown increased prevalence of
disease in Caribbean reefs and greatly reduced coral populations (Muller and Woesik 2012;
Harvell et al. 1999). The most widespread disease in the Caribbean, Aspergillosis, transported
via large Aeolian dust fluxes from Africa (Shinn et al. 2000), is hypothesized to secondarily
spread via the soft coral predatory snail, Cyphoma gibbosum (Rypien and Baker 2009). Coral
reefs are valued at just under 800 billion USD worldwide, for their contributions to fisheries,
coastal protection, tourism and recreation, and overall biodiversity value (Cesar et al. 2003). It is
important to understand the causes of degradation in order to implement informed and effective
management plans.
Octocorals are a group of cnidarians often called soft corals because they do not produce
a consolidated calcium carbonate skeleton; these are the dominant coral in the Caribbean reefs
(Bruno et al. 2011). Most octocorals are not considered reef-building (Jeng et al. 2011) because
they typically do not leave behind a calcium carbonate skeleton after death like scleractinian
(hard) corals. However, it has been suggested that Sinularia species in the Red Sea are also
capable of contributing material to create reef structures by the cementing of skeletal elements
called sclerites (Schuhmacher 1997; Jeng et al. 2011). Sclerites are spiny skeletal structures,
often used for identification (Bayer 1961; Aharonovich and Benayahu 2011). Soft corals provide
a three-dimensional structure to the reefs that fish and invertebrates utilize for habitat and
protection against predators (Sanchez et al. 2003). Like hard corals, they also rely on an
8. 2
endosymbiotic relationship with zooxanthellae as an energy source in addition to nutrients from
planktonic organisms in the water column taken in through filter feeding (Patterson 1984;
McFadden 1986).
Coral disease is one of the main factors leading to the rapid decline of corals (Goreau et
al. 1998; Hernandez et al. 2009). At least nine coral diseases affecting Caribbean reefs have been
identified (Goreau et al. 1998). Bacterial and fungal growth is accelerated with higher
temperatures (Lesser et al. 2007); this, in conjunction with impaired host immunity with warmer
temperature, increases the susceptibility of corals to disease (Bruno et al. 2007).
Disease in corals is characterized by lesions or distinct bands of tissue loss and may be
caused by bacteria, viruses, or fungi (Harvell et al. 2007). It can alter or reduce the reproductive
success of a coral population, impacting the ecosystem dynamics, which can lead to an overall
change in the species composition and structure (Harborne et al. 2011). Aspergillosis is a disease
transmitted by the fungal pathogen, Aspergillus sydowii, and was first isolated in diseased sea
fans in 1996 (Smith et al. 1996); in Caribbean reefs, it has been observed in Gorgonia ventalina
and G. flabellum (Nagelkerken et al. 1997; Ward et al. 2006). The pathogenicity of A. sydowii in
sea fans is highly dependent on the genetic composition and health of the host (Alker et al.
2001), as aspergilli are known to be opportunistic and affect immune-compromised hosts (Kim et
al. 2000).
Symptoms of infected individuals include dark purple lesions, irregular patterns of tissue
and nodules. Lesions caused by Aspergillosis are areas of tissue necrosis and holes on the surface
of sea fans which are distinctly dissimilar to those formed from hurricane and storm damage and
predation (Nagelkerken et al. 1997) because the edges are often purple (Mullen et al. 2006). The
purple pigmentation of the sea fan blade is due to an increase in the proportion of sclerites
9. 3
containing purple carotenoids. Smith et al. (1998) suggest that the recruitment of pigmented
sclerites serves as a defense mechanism to prevent the spread of disease in the colony. This
“purpling” has been associated with the production of a melanin layer which is thought to act as
a barrier against pathogens (Ellner et al. 2007). This results in thickened areas of tissue and the
protein gorgonin, called nodules (Bruno et al. 2011). The area of the sea fan blade exhibiting
these symptoms can be implemented as a measure of relative disease severity.
Octocorals have various secondary antifungal secretions that act as a defense against
fungal pathogens and predation (Kim et al. 2000); however, this is compromised at higher
temperatures or increased host stress (Ross et al. 1996). This is a growing concern with trends of
warmer sea temperatures because most microbial pathogens have a higher temperature tolerance
range than their hosts, favouring the success of the pathogen in current conditions (Alker et al.
2001). Octocorals also release chemicals that deter fish predation (Van Alstyne and Paul 1992);
these chemicals however, do not entirely negate predation by Cyphoma gibbosum.
The flamingo tongue snail, C. gibbosum, is a marine snail which acts as the primary
consumer of octocorals in the Caribbean reefs, as it feeds on them exclusively (Gerhart 1986;
Lasker et al. 1988). Octocorals serve as a food source, protection, and provide a site for mating
and laying eggs (Lasker et al. 1988; Nowlis 1993). The many chemical defenses octocorals
produce appear to be largely ineffective against predation from C. gibbosum (Harvell and
Fennical 1989), who will actually sequester these toxic allelochemicals and use them as defense
against its own predators, such as hogfish (Gerhart 1986). The mantle of flamingo tongue snails
is brightly coloured when they reach adulthood, which serves an aposematic function, or warning
signal (Rosenberg 1989). Cyphoma gibbosum has been observed in clumped distributions when
found on prey (Gerhart 1986; Lasker and Coffroth 1988); Hazlett and Bach (1982) conclude that
10. 4
this distribution was not attributed to the size of colonies or the distance between the nearest
neighbouring host colony. It is hypothesized that snails aggregate to decrease risk of predation
(Gerhart 1986) and to find mates (Nowlis 1993).
Octocorals that are subject to predation exhibit little physical damage (Harvell and
Suchanek 1987) and the colonies suffer only partial mortality (Chiappone et al. 2003). However,
an extreme case at Mona Island, Puerto Rico resulted in mass mortalities of gorgonian corals due
to an outbreak of C. gibbosum (Schärer and Nemeth 2010). An average density of 34.4 snails per
colony and a maximum density of 190 snails per colony were reported, resulting in over 90%
total loss of shallow-water octocorals in the area. Such cases are rare and extreme but highlight
the detrimental effects of a prey/host imbalance in an ecosystem.
Cyphoma gibbosum occupation and foraging may have other secondary effects that
attribute to soft coral degradation. Cyphoma gibbosum predation exposes the skeleton and allows
macroalgae to colonize, which inhibits regeneration of octocoral polyps (Harvell and Suchanek
1987). A fragmented host may result in reduced fecundity of the coral polyps (Burkepile and
Hay 2007).
The flamingo tongue snail has been found to prefer diseased over healthy tissue to inhabit
(Nagelkerken et al. 1997) and has thus been suggested to act as a vector of disease (Slattery
1999; Rypien and Baker 2009). Aspergillus can be spread by grafting infected tissue onto
healthy tissue and by inoculating healthy colonies with cultures of Aspergillosis (Smith et al.
1996). Rypien and Baker (2009) suggest that C. gibbosum attributes to the spread by ingesting
the diseased tissue and as it migrates to healthy colonies, viable fungal spores are passed through
its digestive system and left in its waste. Furthermore, damaged tissue makes gorgonians more
susceptible to pathogens. Predation by this snail may go as deep as the coral’s skeleton, allowing
11. 5
algae to settle and grow over the exposed area.
We will test the following hypotheses:
1. Cyphoma gibbosum show a preference for diseased hosts
2. Life stages and behaviour predict host preference
This study aims to determine the host preference of C. gibbosum and the health of its
octocoral host. We will also examine the relation between predation and the overall health of the
host coral. The health parameters addressed in this study are the two primary causes of reduced
coral cover: disease and algal overgrowth (Wahle 1985; Aronson et al. 2003).
12. 6
Methods
Study Site
This study took place on Utila, the second largest Bay Island of Honduras. It is
approximately 29 kilometers from the Honduras mainland and is surrounded by the Caribbean
Sea. The island is 13 kilometers long and four kilometers wide with a population of
approximately 7000 people, most of which live around the Eastern Harbour (Saunders et al.
2009). The Bay Islands are the eastern-most extent of the Mesoamerican Barrier Reef Complex,
which is the second largest reef in the world, after the Great Barrier Reef in Australia. The
average water temperature during the field season was 28°C.
Three sites were surveyed from the south side of the island: Little Bight, Coral View, and
Stingray Point; and two from the north side: The Maze and Spotted Bay (Figure 1).
14. 8
Benthic Surveys
Benthic surveys of Cyphoma gibbosum were carried out on SCUBA at five sites around
the island of Utila, Honduras during June-August 2014. Data of octocoral abundance and
richness at the same sites were collected in 2013 and used in this study as a measure of host
availability. Divers placed a total of 30 50×1m belt transects at two depths at each site: 5m at the
crest and 15m at the slope and each depth had three replicates. The presence of C. gibbosum
within the belt was recorded, as well as the species of coral on which it was found, the height of
the coral, and the size of the snail. The health of the coral was scored on a relative scale of 0 – 4:
0 = no visible symptoms of disease or predation
1 = low levels of predation
2 = high levels of predation
3 = low levels of disease and predation
4 = high levels of disease and predation
The life stage of C. gibbosum was determined based on shell length; those equal to or
greater than 2cm were considered adult, and those less were considered juvenile.
Monitoring:
In the beginning of the field season, coral colonies at Coral View Reef within an area of
50x50m over a depth of 2m-12m, which had at least one C. gibbosum present were tagged to
examine the progression of predation, disease, and algal overgrowth. A total of 34 snails were
tagged and followed through the season; 23 snails were considered in the analyses due to lack of
confidence in tracking some individuals. A rank system was used to quantify the health of the
hosts. Predation (P), disease (D), and overgrowth (OG) were examined separately with the
15. 9
following rank system:
0 = no visible symptoms
1 = low levels of P, D, or OG
2 = Intermediate levels of P, D, or OG
3 = High levels of P, D, or OG
These colonies were revisited at least four times a week over 42 days for changes in
health. The snails and their colonies were photographed for record. The individual snails were
also tagged to track their movement within and between colonies, and determine residence time.
Divers collected snails in individually labelled Whirlpak bags and transported them to the field
station’s wet lab for tagging and sex determination.
The sex of the snails was determined by submerging them in a solution of 5% methanol
in saltwater for approximately 3-5 minutes, until the foot of the snail appeared relaxed, according
to methods described by Nowlis (1993). If the foot was still retracted after 10 minutes in the
solution, the snail was removed, placed under running saltwater, and submerged in saltwater for
10 minutes before returning to the methanol solution for a second attempt.
Once the foot of the snail was relaxed, the right side of the foot was gently stroked, as if
to pull the foot away from the mantle and shell. If male, a penis was found (Figure 2); if female,
a genital pore (Figure 3), which appeared to be a small pore or tube within the tissue of the foot.
After the sex was determined, the snails were run under saltwater to rinse the solution off, and
then submerged in saltwater. The snails were then returned to the colonies on which they were
found within three hours after collection.
16. 10
Figure 2: Male Cyphoma gibbosum
Figure 3: Female Cyphoma gibbosum genital pore (gp) within the tissue of the foot
17. 11
Three methods of tagging were employed, with varying success. In all cases the snails were
placed in a petri dish of seawater, with their shell partially submerged, and the mantle was
separated on the back of the shell in order to tag the area.
1. Nail polish: Once the top of the shell was dried, small roman numerals were painted on
with nail polish, and a red dot was painted on if female, blue if male. The mantle was
held apart as the nail polish dried. This was unsuccessful because the nail polish wore off
in the water almost immediately in several cases.
2. Nail File: A nail file was used to make unique markings on the shell, making sure to hold
the mantle apart so as not to damage the snail tissue. This was the method of tagging used
by Lasker et al (1988), however, we decided the amount of distress this caused the snails
made this an unacceptable tactic.
3. Waterproof paper and glue: Once the shell was dry, a small piece of numbered waterproof
paper, affixed with waterproof glue was placed on the shell, keeping the mantle down
until the glue dried. This method proved the most effective, remaining attached for 2 – 5
weeks.
Statistical Analysis
All statistical tests were performed using R (R Development Core Team 2014) using the
packages Rcmdr (Fox 2005), stats (R Development Core Team 2014), Hmisc (Harrell et al.
2014), and vegan (Oksanen 2013); graphs were made using Micrsoft Excel.
Species distribution and preference
A diversity index was calculated for the octocoral composition at 5m and at 15m using
18. 12
the Simpson-Gini Index value (Eq. 1) to get a measure of host availability for the sites using
extensive octocoral species data collected in 2013 (Lovenburg, unpublished). This measure is
less sensitive to rare species than the Shannon Index (Hill, 1973), which is important given the
number of rare species found around Utila. The inverse of the Simpson index is used.
Eq. 1
D =
1
∑ 𝑝𝑖
2𝑠
𝑖=1
Ivlev’s (1961) Electivity Index was used to examine prey selection (Eq 2). This value
ranges from -1 to +1; a value of -1 indicates that C. gibbosum does not utilize the host at all, 0
indicates that C. gibbosum utilizes the host in proportion to its abundance, and a value of +1
indicates C. gibbosum prefers a host and does not utilize any others. Spearman rank correlation
tests coefficients were used to assess the relationship between octocoral availability and
occupancy (Chiappone et al. 2003)
Eq. 2
𝐸 =
(ri − pi)
(ri + pi)
ri = proportion of host species occupied
pi= proportion of host species available
The distribution of C. gibbosum across shallow (5m) and deep (15m) reefs surrounding
Utila was examined using a proportion test, with the null hypothesis that they are distributed
evenly across different depths.
Goodness of fit was tested for the data collected from the five sites using chi-square
analyses to determine if C. gibbosum is distributed evenly among different host species. The
distribution of adult and juvenile snails on octocoral hosts was evaluated against the expected
distribution based on the null model that snail frequency is independent of host type/identity.
19. 13
The distribution of C. gibbosum around Coral View Reef was analyzed based on patterns
outlined by Lasker et al. (1988):
i. Occupancy: the number of times C. gibbosum was observed on a host species throughout
the monitoring period.
ii. Movement: when a snail changed host species or a previously unrecorded snail appeared
on a host within the monitoring area.
iii. Residence time: the number of days an individual spent on a single host.
Occupancy and Movement was analyzed using chi-square analyses, with the null
hypothesis that the distribution of C. gibbosum is random. Residence time was analyzed using
ANOVA to examine the difference in variance of residence time between different host species.
Host health
Chi-square analysis was done to examine distribution of C. gibbosum based on the health
state of its hosts. The observed frequency of snails was compared to the expected distribution by
health class (0 – healthy; 1 – light predation; 2 – heavy predation; 3 – light disease; 4 – heavy
disease), assuming the null model that C. gibbosum distribution is independent of health of the
host.
Snail Occupation, a size-corrected measure of frequency (separate from previously
mentioned Occupancy), was calculated for each colony at the end of the monitoring period
(Eq.3). Pictures taken at the end of the monitoring period were analyzed using ImageJ to
estimate the cover of predation, disease, and overgrowth on the hosts. Snail Occupation values
were log-transformed to correct for skewed distribution resulting from a small sample size.
Incidence time for sea fans (Gorgonia ventalina), Eunicea spp., and A. americana was calculated
20. 14
and analyzed using ANOVA to examine the relationship between occupancy and host health,
with the null hypothesis that mean snail occupancy is equal for low, medium, and high levels of
predation, disease, and overgrowth.
Eq. 3
SnO =
Obs
ap,d,or o
frequency/cm2
SnO = Snail Occupation
Obs = number of observations of C. gibbosum
ap, d, or o = relative area cover of predation, disease, or overgrowth, respectively, at the end of the
monitoring period (cm2)
21. 15
Results
Species distribution and preference
Octocoral host densities for Utila, Honduras are given in Table 1. Shallow reefs
(D=10.06) were much more diverse than deep reefs (D=4.64). This indicates that shallow reefs
were more even octocoral distribution. Antillogorgia elisabethae abundance increases with
depth, making up approximately 19% of the reef at five meters and 44% of deep reefs.
Conversely Gorgonia ventalina density decreases dramatically at deeper reefs, making up 20%
of the reef at five meters and only 4% at fifteen meters. Briarium asbestinium and Eunicea
flexuosa decrease moderately in density with depth.
Adult Cyphoma gibbosum show a high preference for Pseudoplexaura porosa at 5m
(e=0.0.931) and 15m (e=0.937); Antillogorgia americana at 5m (e=.711) and 15m (e=0.875); and
E. flexuosa at 5m (e=0.513) and 15m (e=0.674), given their respective host densities. Juvenile
snails show a high preference for for A. americana that almost completely excludes all other
hosts (e=0.929, e=0.935 respectively) (Table 1). Spearman rank correlation coefficient tests
resulted in a significant correlation between adult C. gibbosum density and octocoral density (r =
0.46; p<0.01). There was no significant correlation between juvenile C. gibbosum densities and
host densities (r = 0.19; p>0.05).
22. 16
Table 1: Octocoral densities and Ivlev's electivity index values (E) (Ivlev 1961) for adult and
juvenile Cyphoma gibbosum at 5m and 15m. Absence of electivity values indicate the absence of
host species at the respective depth.
24. 18
Chi-square tests indicated that there was significance in the frequency that snails were
found across the five sites. Adult C. gibbosum was found most frequently on Eunicea spp.
(28%), Antillogorgia spp. (22%), and Gorgonia ventalina (21%); juvenile snails were found
primarily on Antillogorgia spp. (86%) (χ2
= 74.76; df = 8; p «0.001) (Figure 4).
Proportion tests indicated that more adult snails occurred in shallow reefs (71%)
compared to deep reefs (χ2
= 12.96; df = 1; p «0.001). Juvenile snail distribution reflected adult
distribution; 65% of juveniles occurred in shallow reefs (χ2
= 4.98; df = 1; p< 0.05) (Table 2).
The proportion of juveniles and adults does not change with depth; there are approximately 60%
adults and 40% juveniles in the reefs, regardless of depth (Error! Not a valid bookmark self-
reference.).
The host preference of C. gibbosum at 5m reflects the overall preference given in Figure
4. Juvenile snails were found primarily on Antillogorgia spp. (95%); adult snails occurred largely
on Gorgonia ventalina (28%), Antillogorgia spp. (22%), and Eunicea spp. (17%) (χ2
= 49.64; df
= 7; p«0.001) (Figure 5). Host preference of C. gibbosum at 15m however, differs from its
preference at 5m. Juvenile snails were found predominantly on Antillogorgia spp. (68%) at 15m;
however, a larger proportion was found on Muricea/Muriceopsis spp (32%) than at 5m. Adult
snails were frequently found on Antillogorgia spp. (48%) and Eunicea spp. (41%), though none
were found on G. ventalina (Figure 6) at this depth. Cyphoma gibbosum was found on a wider
variety of hosts at 5m than at 15m, reflecting the diversity of host availability.
25. 19
Figure 4 C. gibbosum host distribution around the 5 sites: Coral View, Little Bight, Stingray Point,
Spotted Bay, and The Maze.
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
ProportionofC.gibbosum
Host
Juvenile
Adult
26. 20
Table 2: Distribution of Cyphoma gibbosum across shallow and deep reefs
Depth 5m 15m
Proportion of Juvenile snails (n=65) 0.65 0.35
Proportion of Adult snails (n=79) 0.71 0.29
Life Stage Juvenile Adult
Proportion at 5m (n=98) 0.40 0.60
Proportion at 15m (n=46) 0.41 0.59
27. 21
Figure 5: Host preference of C. gibbosum at 5m around the five sites: Coral View, Little Bight, Stingray
Point, Spotted Bay, and The Maze
Figure 6: Host preference of C. gibbosum at 15m around the five sites: Coral View, Little Bight, Stingray
Point, Spotted Bay, and The Maze
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
ProportionofC.gibbosum
Host
Juvenile
Adult
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
ProportionofC.gibbosum
Host
Juvenile
Adult
28. 22
Distribution around Coral View Reef
The distribution of C. gibbosum based on Occupancy and Movement throughout the
monitoring period in Coral View Reef is given in Figure 7. This distribution differs significantly
from a random expectation. Snails showed preference in occupancy for Eunicea flexuosa (36%),
and Gorgonia ventalina (33%) (χ2
= 130.87, df = 6, p«0.001). Similar patterns are observed in
the movement data: G. ventalina (38%) and E. flexuosa (28%) were preferred based on snail
migration patterns (χ2
= 147.03, df = 6, p«0.001). The average residence time of C. gibbosum
was longest on Plexaurella spp. (20 days) and on Antillogorgia spp. (19.5 days), and shortest on
algae or rock (1 day). However, an ANOVA test failed to reject the null hypothesis that residence
time is independent of host species (F = 1.45, df = 6, p > 0.20) (
30. 24
Figure 7: Cyphoma gibbosum host occupancy and movement around Coral View Reef
0
0.05
0.1
0.15
0.2
0.25
0.3
0.35
0.4
0.45
Proportionofobservations
Host
Occupancy
Movement
31. 25
Table 3: Residence time of Cyphoma gibbosum on hosts in Coral View Reef
Host Average residence time (days)
Plexaurella spp. 20.00
Antillogorgia spp. 19.50
Eunicea flexuosa 14.29
Muricea/Muriceopsis 9.20
Gorgonia ventalina 7.56
Other Eunicea spp. 5.00
Algae/rock 1.00
32. 26
Host health
A significant difference in the distribution of snails around Utila was observed between
different levels of health of the hosts (χ2
= 32.13, df = 4, p «0.001). Approximately 70% of adult
snails recorded were found on hosts that showed signs of past predation, while only 18% were
found on hosts that showed any symptoms of disease. Over 50% of all juvenile snails were
found on healthy hosts that showed no signs of disease or predation; only one of the juvenile
snails was found on a host that showed any sign of disease (
Figure 8).
ANOVA tests failed to reject the null hypothesis that mean snail occupancy is
independent of level of disease (F = 0.39; df = 3; p>0.75) and overgrowth (F = 0.92; df = 3;
p>0.45). However, a test of variance on levels of predation rejected the null (F = 6.10; df = 3;
p<0.05); greater occupancy results in higher levels of predation. Increased occupation is
associated with higher levels of predation, but not disease or overgrowth (Figure 9).
0
0.1
0.2
0.3
0.4
0.5
0.6
0 1 2 3 4
ProportionofC.gibbosum
Health Class
Juvenile
Adult
33. 27
Figure 8: Frequency of adult and juvenile Cyphoma gibbosum by health class of hosts (0 – healthy; 1 –
light predation; 2 - heavy predation; 3 – light disease; 4 – heavy disease) around Utila
0
0.1
0.2
0.3
0.4
0.5
0.6
0 1 2 3 4
ProportionofC.gibbosum
Health Class
Juvenile
Adult
34. 28
Figure 9: Relation between Snail Occupation (SnO), a size corrected measure of frequency, and Host
Health, with regard to Predation, Disease, and Algal Overgrowth
0
0.04
0.08
0.12
0.16
0.2
0 1 2 3
SnO(freq/cm2) Predation
0
0.04
0.08
0.12
0.16
0.2
0 1 2 3
SnO(freq/cm2)
Overgrowth
0
0.04
0.08
0.12
0.16
0.2
0 1 2 3
SnO(freq/cm2)
Health State
Disease
35. 29
Discussion
Data collected from monitoring Coral View Reef show no significance in the relationship
between Cyphoma gibbosum occupation and host health, with respect to disease or overgrowth.
This trend is also reflected in the benthic surveys, which show that neither adult nor juvenile
snails prefer diseased octocoral hosts. This differs from previous conclusions that C. gibbosum
prefers diseased hosts (Nagelkerken et al. 1997) and that flamingo tongue snails act as a vector
of Aspergillosis in Caribbean reefs (Rypien and Baker 2009).
Wahle (1985) reported that heavy predation that exposes the octocoral axis leads to
marcoalgal overgrowth, though this is not the case in Utila. Since no significant correlation was
identified between snail occupation and algal overgrowth, the data cannot support or refute
Wahle’s conclusion (1985). Some cases of algal blooms were found on hosts, which had only
light predation or none at all. Perhaps the monitoring period was not long enough to observe
overgrowth, or the predation observed was not severe enough to lead to overgrowth.
Data shows that C.gibbosum does not select its host based on its abundance in the reef.
The factors that largely influence preference and distribution of the flamingo tongue snail are
host species and characteristics, predator life stage, previous snail occupancy, and reef depth.
Lasker et al. (1988) suggests that snails may move from colony to colony in a random
pattern, but certain traits of a colony determine occupation. Sclerite size and concentrations may
affect host selection (Lasker and Coffroth 1987); Harvell and Suchanek (1987) reported a
negative correlation between C. gibbosum foraging time and spicule size, which suggests that
sclerites provide corals with defense against predators. Eunicea flexuosa has a high percent
composition and one of the largest sclerite sizes of all Caribbean octocorals (Grajales et al.
2007). Despite this, E. flexuosa is one of the preferred hosts of adult C. gibbosum. Van Alstyne
36. 30
and Paul (1992) concluded that sclerites act as a deterrent to predators, however, the high
occupation and sampling/grazing behaviour of C. gibbosum on E. flexuosa in the current study
suggests that while sclerites may reduce grazing, they do not eliminate predation entirely.
The composition of secondary chemical compounds may also affect the viability of a host
to a migrating snail. Octocorals are well known to be rich in allelochemicals that deter predation
(Epifanio et al. 2007; Harvell and Fenical 1989; Van Alstyne and Paul 1992). Cyphoma
gibbosum has evolved biochemical resistance mechanisms, such as glutathione S-transferase
(GST), a family of enzymes whose primary function is the detoxification of chemical defenses
released by their hosts (Whalen et al. 2010). Secondary compounds from gorgonians widely
vary, which may explain the vast range of hosts that snails occupy. Gorgonians, such as Plexaura
homomalla, have high concentrations of deterrent cyclopentenon prostaglandid, which act as
strong GST inhibitors to deter predation (Whalen et al. 2010). Epifiano et al. (2007) suggest that
the chemical defenses released by Antillogorgia americana originate from the symbiotic
zooxanthellae. Kim et al. (2000) demonstrated Gorgonia ventalina and G. flabellum possess
antifungal compounds. Antifungal assays revealed that both antifungal and antimicrobial
properties were found in crude extracts from sea fans, which suggests a generalized antimicrobial
reaction, irrespective of the colonizing microorganism.
Defense mechanisms such as sclerite composition and secondary chemical defenses were
not examined in this study, therefore could not be included in the analyses. The preference of C.
gibbosum for G. ventalina, Eunicea spp., and A. americana suggests there may be more benefit
to be gained from these hosts, or conversely, the defenses of these hosts are the least effective.
Harvell and Fennical (1989) reported a negative correlation between sclerite dry weight and
crude extract dry weight of Pseudopterogorgia rigida (Antillogorgia rigida), which suggests an
37. 31
evolutionary trade-off between the two defense mechanisms. A species will likely concentrate on
one defense method over the other, depending on the stresses placed on it.
Prior occupation of conspecifics may also affect the distribution and occupation of C.
gibbosum. Chemical defenses may be induced by previous foraging (Harvell and Suchanek,
1987), which could make a preferred host species less inhabitable by future snails. Findings from
the current study differ from this observation; most adult snails were found on hosts that had
received previous predation. However, predation levels were generally low, which suggests that
gorgonians can tolerate a certain level of predation and increased chemical defenses are released
beyond a certain threshold. Data from the monitoring period shows that movement between
colonies is not random, like Lasker et al. (1988) suggested, instead choosing hosts in a pattern
that almost mirrors occupancy (Figure 7). These data bolster the hypothesis that snails follow the
mucous trails of other conspecifics (Gerhart 1986), which supports the evolutionary theory of
gregarious behaviour in the aposematically coloured C. gibbosum.
It is unclear whether juvenile snails also follow mucous trails of conspecifics. Juveniles
were consistently found on Antillogorgia americana that showed no signs of previous predation,
though this does not necessarily mean no previous occupation occurred. Many studies have
examined adult Cyphoma gibbosum host preference (Lasker and Coffroth 1988; Lasker et al.
1988; Chiappone et al. 2003), though none have shown juvenile preference, therefore this study
provides important baseline information going forward. Although A. americana was one of the
preferred hosts for adult flamingo tongue snails, there was often little to no sign of predation;
perhaps C. gibbosum utilizes hosts for different purposes. Lasker et al. (1988) reported that
Pseudopterogorgia americana (A. americana) received the least predation of the available hosts,
and was mainly used for egg deposition, taking advantage of the large size and structural
38. 32
complexity for safety from predators. Although the larvae of marine gastropods are typically
pelagic veliger larvae (Jablonski & Lutz 1983), the chemical signal of C. gibbosum egg
deposition might be a cue that future larvae use to settle on the colony.
Reef depth largely influences Cyphoma gibbosum distribution, although it is not well
studied or understood. Adult distribution varied significantly between 5m and 15m reefs. Goulet
and Coffroth (2003) concluded that the symbiotic relationship between octocoral and
zooxanthellae remains stable over different depths however, morphological changes in the host
were observed. Depth and wave exposure are the main factors related to the variation in
octocoral composition and densities (Sanchez et al. 1998). The difference observed in C.
gibbosum preference at 5m and 15m may be due to the difference in reef composition. No snails
were found on Gorgonia ventalina at 15m, though there was a much lower abundance of sea fans
in the deeper reefs. The reduced variety of host occupation at 15m reflects the reduced diversity
of the reef.
Although more extensive monitoring and longer intervals are necessary to fully assess the
distribution and host-predator dynamics of Cyphoma gibbosum and its hosts, data suggests that
there is no relationship between snail predation and algal overgrowth or Aspergillosis, and
flamingo tongue snails do not prefer diseased over healthy gorgonians which contradicts
previous studies on the relationship between C. gibbosum and octocoral disease (Nagelkerken
1997). Kim et al. (2000) concluded that predation by C. gibbosum reduces the health of its host,
which allows pathogens such as Aspergillus to establish, however this is not observed in the data.
This may be because the measure of Snail Occupation (SnO) doesn’t differentiate between
different snail behaviours; it assumes that the snails are always feeding, but they may be
sampling, mating, or laying eggs. If C. gibbosum predation doesn’t influence disease or
39. 33
overgrowth, other environmental factors or anthropogenic effects may be the cause and should
be considered. The factors identified to influence preference include: host species, life stage, and
reef depth. Future research should examine previous C. gibbosum occupation and host defenses
such as: sclerite size, shape, and concentration; and chemical defenses.
40. 34
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