Download Competition and locomotion in a free-living

J. Exp. Mar. Biol. Ecol., 1988, Vol. 123, pp. 189-200
189
Elsevier
JEM 01163
Competition and locomotion in a free-living fungiid coral
Nanette E. Chadwick
Department of Zoology. University of Calfoomia at Berkeley, Berkeley, California, U.S.A.
(Received 8 March 1988; revision received 9 August 1988; accepted 16 August 1988)
Some fimgiid corals asexually produce unconnected polyps that lie loose on the substratum
between coral colonies. These free-living corals cannot build large three-dimensional structures and thus
risk overgrowth during competition for space or light with colonial neighbors on coral reefs. This study
examined the ecological importance and mechanisms of interspecific competitive damage and movement
by the free-living fungiid coral Fungia scufaria (Lamarck). Over 40% of a population of F. scutaria on
Hawaiian patch reefs was observed to contact other species of corals and macroalgae. F. scutaria caused
unilateral damage to colonial corals in 294% of natural contacts. In contrast, macroalgae overgrew and
smothered F. scutaria in all observed cases. During experimental field contacts, small polyps of F. scutaria
moved away from resident coral colonies, while larger individuals remained in contact and induced tissue
damage to residents. F. scutaria move over short distances by nocturnal expansion of tissues that push
against adjacent surfaces. Laboratory and field experiments suggest that long-distance movement may be
via passive transport by water motion. The mechanism of interspecific damage is unique among corals thus
far studied; nocturnally expanded polyps deposit a thick layer of mucus 5-15 mm wide onto neighboring
corals. The tissue of corals beneath this mucus layer becomes necrotic and sloughs off within 4 days. The
abundant mucus secreted by F. scuraria contains numerous nematocysts, unlike that of all other Hawaiian
corals examined to date. The ability of some free-living corals to actively damage or move away from
encroaching corals may be important to their survival on reefs dominated by colonial species.
Abstract:
Key words:
Competition; Free-living coral; Fungia scufaria; Life-history strategy; Locomotion; Mucus
secretion
INTRODUCTION
Free-living corals of the family Fungiidae are common on coral reefs throughout
much of the tropical Indo-Pacific
(Wells, 1966). Some members of this family, the
mushroom corals, exhibit an unusual life history in that they begin life attached to the
substratum,
break off and then reproduce asexually to form unconnected
free-living
polyps (Wells, 1966). Individuals may reach 30 cm or more in length (Bosch, 1967), but
are small in relation to colonial corals, many of which through asexual growth form
branching or massive colonies several meters wide (Connell, 1973). Members of these
colonial species can successfully monopolize much of the limited substratum
space
available to benthic reef organisms
(Connell,
1973; Glynn,
1973; Porter, 1974;
Benayahu & Loya, 1981). Given the lack of connection between individual polyps and
Correspondence
Israel.
address: N. E. Chadwick, Interuniversity Institute of Eilat, P.O. Box 469, Eilat 88103
0022-0981/88/$03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)
190
N. E. CHADWICK
the relatively small size of the mushroom corals, how do they prevent themselves from
being overgrown by large colonial corals on tropical reefs?
Members of the genus Fungiu, a type of mushroom coral, appear to interact with the
environment and with other organisms in ways that allow them to coexist with colonial
species. First, they appear to survive storm-generated abrasion better than do cooccurring colonial corals (Jokiel & Cowdin, 1976). Second, members of the more mobile
Fungia species also actively locomote (Abe, 1939), and thus could avoid overgrowth by
moving away from other corals and into unoccupied areas of the reef (Maragos, 1974).
Third, some corallivorous sea stars reject Fungia spp. and prey selectively upon some
species of colonial corals (Ormond et al., 1976; Glynn & Krupp, 1986). In addition,
many fungiid polyps form aggregations (Abe, 1939; Wells, 1966) that, through their
feeding or other activities, may retard settlement and encroachment by benthic organisms (Jackson, 1977). Storms or other disturbances that create high turbulence can
disperse aggregations of unattached corals, however, and Fungia often exist as single
polyps surrounded by colonial corals. Members of some fungiid species thus may
contact massive or branching corals for long periods, and risk being partially or
completely overgrown between disturbance events. An important feature that may
counteract this process is the ability of some fungiids to actively damage the growing
edges of adjacent coral colonies (Hildemann et al., 1975a,b, 1977).
Investigation of the interspecific damage reaction of fungiids has thus far been limited
to laboratory experiments and anecdotal field observations (Hildemann et al., 1975a,b,
1977; Sheppard, 1979). Little is known about competitive interactions in natural populations of Fungiu, or of the behavioral mechanisms involved. It is important to examine
this type of interaction quantitatively in the field, where ecological processes such as
predation (Cox, 1986) and interference by epifauna (Bak et al., 1982) can affect the
intensity and outcome of competition occurring naturally between corals.
In the present study I assessed the frequency and outcome of natural contacts
between polyps of the fungiid Fungia scuturiu (Lamarck) and other species of corals and
macroalgae on Hawaiian reefs. I then conducted field experiments to determine the
effects of introduced contacts on rates of interspecific damage and movement by
F. scuturia. Finally, in the laboratory I observed the behavioral mechanisms of competition and locomotion employed by members of this species.
MATERIALSAND METHODS
STUDY SITE
This study was conducted during the summer of 1983 at the Hawaii Institute of
Marine Biology in Kaneohe Bay, Oahu, Hawaii. Field investigations were carried out
on patch reefs in the bay (see Holthus, 1986, for map and description of reefs in Kaneohe
Bay).
CORAL COMPETITION AND LOCOMOTION
FIELD
191
OBSERVATIONS
The proportion
of individuals
of F. scuturia that naturally
contacted
other species of
sedentary organisms was estimated by snorkeling over each of eight patch reefs in
Kaneohe Bay during daylight hours, and noting whether each observed polyp contacted
other scleractinian corals or macroalgae (species given in Table I). Polyps of F. scutariu
were scored as contacting other organisms if their contracted tissues were within 10 mm
of the live tissue of the latter. Individuals of this coral expand their tissues nocturnally
to z 10 mm above the skeletal surface (pers. obs.), and thus periodically should contact
all sessile organisms within this distance. Polyps that were isolated on sand flats or
occurred in the midst of conspecific aggregations were scored as not in interspecific
contact.
The outcome of natural contacts between F. scutaria and other sedentary organisms
was determined by observation at the above eight sites. The outcome of each interaction
was categorized as: damage to neither individual, damage only to F. scutaria, damage
only to the other species, or damage to both. Localized coral injuries were clearly visible
as a zone of necrotic tissue or exposed skeleton along the region of interspecific contact
(after Wellington,
1980).
FIELD
EXPERIMENTS
In order to examine the effects of introduced contact between F. scutariu and colonial
corals, an experiment was performed along the eastern edge of a patch reef adjacent to
the Hawaii Institute of Marine Biology (see Jokiel et al., 1983, for description and map
of this reef). The margin of this patch reef contained a large population of F. scuturiu
interspersed
among several species of colonial corals. To experimentally
introduce
F. scutaria into contact with resident coral colonies at this reef, I first collected nine
F. scutaria in each of three size classes from reefs throughout the bay. In the laboratory,
the length of each coral was measured as the distance across the longest part of the
oblong oral disk. The three size classes were (range of lengths): small (49-62 mm),
medium (83-120 mm), and large (142-180 mm). Sizes in the three groups were significantly different (nonparametric
multiple comparisons
test, P < 0.01). Each specimen
was marked by engraving a numeral into the calcareous skeleton through live tissue on
its aboral surface with an electric engraver. This label caused no apparent long-term
damage to the corals, and was visible for the duration of the experiment.
Each labelled F. scuturia was then transported to the field and placed adjacent to a
haphazardly-chosen
undamaged colony of one of the two most common corals, Montiporu verrucosa (Lamarck) or Porites compressa Dana (within 1 mm but tissues not
touching), at l-2 m depth along the reef edge. Each colonial coral was marked by tying
a section of numbered plastic line around one branch. I also marked nine coral colonies
that were intermingled among the treatment colonies but did not contact F. scutaria, as
controls for damage to corals not associated with interspecific contact. Once a week
for 4 wk, I assessed the condition of each coral colony and its introduced polyp of
F. scutariu, and measured the distance separating the specimens.
192
N. E. CHADWICK
LABORATORY EXPERIMENTS
To observe the behavioral
I collected
specimens
mechanisms
of locomotion
from patch reefs throughout
and competition
Kaneohe
in F. scutaria,
Bay. Eight corals were
collected in each of two size classes, measured as above (range of lengths): small
(43-58 mm) and large (108-168 mm). The sizes of corals in the two groups were
significantly different (Mann-Whitney
U test, P < 0.01). Corals were maintained
in
large, shaded outdoor aquaria supplied with running seawater at ambient sea temperature (25 “C). The substratum
in these tanks was smooth plastic. Each polyp of
F. scutaria was placed within 1 mm of a live fragment of the colonial coral Montipora
verrucosa, also collected from Kaneohe Bay. Each pair of corals was observed once
every 2 h for 24 h, then intermittently
for several days, and the distance between the
individuals of each pair was recorded each week for 3 wk.
The copious mucus secreted by Fungia scutaria was collected to examine its nematocyst content. A small pipette was used to gently suction mucus from the surface of a
polyp while it remained submerged in seawater, care being taken not to touch the surface
of the coral. This mucus sample was observed at 400 x under a phase-contrast
microscope and the types (according to Mariscal, 1974) of nematocysts
noted.
RESULTS
FREQUENCY OF NATURAL INTERSPECIFIC CONTACTS
Of 819 individual F. scutaria that were observed, 307 or 34.93%
other scleractinian corals (species given in Table I). An additional
contacted macroalgae (species, Table I). The remaining 59.17%
aggregated conspecific polyps, or occurred singly on sand flats or
with other organisms.
were in contact with
52 corals, or 5.92 %,
were surrounded by
rubble, out of contact
OUTCOME OF NATURAL CONTACTS
Of the F. scutaria polyps that naturally contacted corals, over 94% (289/307) unilaterally damaged members of other species of scleractinian
corals (Table I). The
proportion of F. scutaria that damaged other corals was independent of the type of coral
contacted (R x C test of independence
using G test, P > 0.10). Polyps of other coral
species often appeared expanded and healthy except in the immediate vicinity of the
fungiids. The tips of coral branches adjacent to F. scutaria usually bore encrusting algae
or a layer of mucus. Small fragments of colonial corals which had fallen into the midst
of aggregations of F. scutaria were completely dead if < 2 cm in length.
In contrast, macroalgae showed no deleterious effects of contact with F. scutaria; they
appeared instead to overgrow and damage the corals they encountered
(Table I).
F. scutaria occurring in the midst of conspecific aggregations appeared undamaged,
although no quantitative data were collected on these interactions.
CORAL COMPETITION
AND LOCOMOTION
193
TABLE I
Occurrence of tissue damage in natural contacts between the coral Fungia scutaria and other benthic
macro(~rganisms on patch reefs in Kaneohe Bay, Oahu, Hawaii. Each observation represents a different
individual of lo. scututia.
Number of observed contacts
with damage to:
Type of organism
contacting
Total
contacts
Fungia scutarin
Fungia
wdaria
only
Sderactinian
Other
species
only
Both
Neither
corals
Porites compressa Dana
~ont~~ru verrucosa (Lamar&)
Pocillopora damicornb (L.)
189
7s
39
4
178
68
39
4
Other coral species
4
289
3
11
(green bubble alga)
Crustose coralline algae
10
42
0
0
0
0
0
10
0
42
All algae
52
0
0
0
52
All corals
307
Macroalgae
Ddyosphaeria
cavernosa
OUTCOME OF INTRODUCED
CONTACTS IN THE FIELD
The distances moved by corals in experimental field contacts differed significantly
among the three size classes of F.scutaria (Kruskal-Wallis test, P < 0.01) (Fig. 1A).
During the 4 wk of observation, small individuals of F.scutaria moved significantly
farther away from resident colonial corals than did the medium and large polyps
(nonp~~etri~
multiple comparisons test, P < 0.05).
One very small coral (49 mm
polyp width), which became caught under the overhanging edge of an adjacent colonial
coral, apparently was unable to move and remained there for the duration of the
experiment.
The proportion of colonial corals damaged depended on the size class of F.~c~tar~~
they contacted (R x C test of independence, P-c0.01).
Most medium and large
F.scutaria remained within tissue contact of resident colonial corals, and by the end of
4 wk had caused damage to a significantly greater proportion of residents than did the
small polyps (test of homogeneity of replicates, P -c0.01) (Fig. 1B). Localized damage
to colonial corals occurred within 4 days of initiation of contact, and persisted
throughout the experiment. The transplanted polyps of F.scutaria did not show any
tissue damage. The control coral colonies that did not contact F.scutaria exhibited
signi~cantly less damage (O/9 colonies damaged) than did the treatment colonies (15/27
damaged) (G test of independence, P < 0.01).
N. E. CHADWICK
194
A
small
medium
Size class
large
of Funqia
Fig. 1. Variation in (A) distance moved away from resident corals, and (B) damage inflicted on resident
corals, with size of Fungiu scutariu after 4 wk in the field. n = nine polyps in each size class.
LABORATORY
OBSERVATIONS
ON LOCOMOTION
When placed adjacent to fragments of the colonial coral Montipora verrucosa in the
laboratory, most polyps of Fungia scutaria moved very little. After 3 wk, small corals
had moved only 7.12 k 11.04 mm (mean 2 SD), and large corals had moved
3.12 k 2.42 mm (not significantly different, Mann-Whitney
U test, P > 0.10). One
small coral (52 mm length) moved 34 mm, and was the only polyp to move > 10 mm
during the course of the experiment. These results contrast sharply with the large
distances moved by small corals in the field (Fig. 1A).
Polyps of F. scutaria appeared to locomote in the laboratory via nocturnal expansion
of their soft tissues to 5-15 mm above their calcareous skeletons. The expanded tissues
pushed the polyps away from adjacent coral skeletons and other surfaces. Using this
mechanism, most polyps moved an average of only a few mm each week (see above),
and remained in intermittent
tissue contact with adjacent corals during nightly expansions.
CORAL COMPETITION AND LOCOMOTION
195
LABORATORYOBSERVATIONSON AGGRESSION
Specimens of both Montipora verrucosu and Fungia scutaria appeared to maintain their
health in aquaria during the 3-wk observation period. Portions of the colonial coral
Montipora verrucosa that occurred within contact of the expanded tissues of Fungia
scutaria were covered by these tissues for lo-12 h each night. Upon contraction of
F. scutariu in the morning, a layer of mucus was observed on the adjacent corals. During
the 1st day following contact, polyps under this layer were still intact. Within 2 days,
coral tissue underneath the mucus began to decay, and microorganisms invaded the
mucus. By 4 days, the mucus had sloughed off and exposed bare coral skeleton (Fig. 2;
see also photographs in Hildemann et al., 1975a,b, 1977). After 2-3 week, a layer of
entrusting algae often colonized this area and remained on the coral for the duration
of the experiment. Corals were capable of complete regeneration of tissues within 3 wk
after separation from F. scutaria.
The copious mucus secreted by F. scutariu contained many nematocysts. The types
observed were microbasic p-mastigophores, holot~chous isorhizas, and spirocysts.
Nematocysts were only a minor component of the mucus by volume.
DISCUSSION
FREQUENCYAND OUTCOMEOF NATURALCONTACTS
This study demonstrates that a substantial proportion (>40%) of specimens of
F. scuturia in Kaneohe Bay are in soft-tissue contact with other species of sedentary
macroorg~isms. Contact with colonial corals was over three times as frequent as
contact with algae.
The high proportion of F. scutaria that caused unilateral damage in natural contacts
with other species of corals (> 90 %, Table I) is consistent with anecdotal field observations and laboratory studies on other members of this genus. Sheppard (1979) reported
that Fungia spp. were dominant over all six species of colonial corals that they contacted
on reefs in the Chagos Archipelago, Indian Ocean. Hildemann et al. (1975a,b) observed
that F. fungites at Enewetak Atoll, Pacific Ocean, caused unilateral damage to at least
five species of colonial corals in both field and laboratory contacts. In Hilo, Hawaii,
Hildemann et ai. (1977) also found that F. scutaria damaged six of the most common
Hawaiian corals during laboratory pairings. The quantitative observations reported here
show a strong, one-way effect of field interactions (Table I). This lack of observed
reversals supports the suggestion that this competitive outcome is rarely reversed by
other ecological factors such as fish predation (Cox, 1986) or growth of epifauna (Bak
et al., 1982).
The dominance of algae over F. scuturia is similar to their effect on other Hawaiian
corals (Banner & Bailey, 1970). Macroalgae are known also to damage corals in other
tropical reef systems (Glynn, 1973; Potts, 1977).
196
N.E. CHADWICK
Fig. 2. The free-living coral Fungia scurariu (right) and the colonial coral Montiporu verrucosa after 7 wk in
the laboratory.
(A) At 5 mm inter-skeletal
distance. Note that F. scutariu has deposited a small patch of
mucus (arrow) on the colonial coral during nocturnal
expansions,
but that the latter’s tissue remains
uninjured. (B) Less than 1 mm inter-skeletal distance. Note the 5-10 mm wide margin on h4, ~err~cos~ that
has been injured by the expansion of tissues and deposition of mucus by F. SC~ZU~~.Note also the strand
ofmucus retained between the two corals. Nylon restraining bands visible in the photographs
were not used
on corals during quantitative
behavioral observation.
Ruler lines = 1 mm.
CORAL
OUTCOME
OF INTRODUCED
The experiment
COMPETITION
197
AND LOCOMOTION
CONTACTS
performed
in this study demonstrates
that F. scutaria can actively
damage colonial corals in the field. The results suggest that corals of this species benefit
from alternate competitive strategies at different life-history stages. Small specimens
( < 70 mm polyp length), unless restrained, tended to avoid competition by moving away
from adjacent coral colonies. In contrast, larger specimens (> 90 mm polyp length)
moved little during the course of a month, and instead damaged the growing edges of
neighboring corals. The effect of this size-related variation is to disperse small F. scutaria
to other, possibly less-crowded
areas of the reef, while the more sedentary large
individuals,
which may be too heavy to move much, defend space for growth by
damaging encroaching neighbors.
This study measured the movement rates of only transplanted
individuals placed in
contact with colonial corals. Specimens of F. scutaria that have not been transplanted,
or do not contact coral colonies, may exhibit different rates of movement in the field.
MECHANISM
OF MOVEMENT
The mechanisms
of movement employed by these unattached
corals appear to be
two-fold. F. scutaria actively locomote over short distances (< 10 mm) by expanding
their tissues and pushing against adjacent hard surfaces. Long-distance
movement
(10 mm to several m) may be primarily passive, via water motion. This interpretation
is suggested by the observation that small corals, which weigh little ( z 40 g wet weight),
move large distances in the field (Figure 1A) where turbulence is high. In laboratory
aquaria where water motion is relatively low, small corals do not move significantly
farther than do the larger, heavier corals (Z 300 g wet weight) (see Results). However,
small corals may also move less in the laboratory because they are unable to gain
traction on the smooth substratum, or due to other factors that differ between laboratory
and field. For example,
michelinii) are transported
in natural
habitats,
by symbiotic
some unattached
sipunculid
corals (Heteropsammia
worms (Goreau
& Yonge, 1968). In
the present study, mobile invertebrates
were not observed to associate with Fungia
scutaria. Even on sandy substratum in the laboratory, members of this species move little
in comparison
with other, more “acrobatic”
species of free-living corals (Hubbard,
1972; Hubbard & Pocock, 1972). Current evidence is consistent with the hypothesis
that movement of F. scutaria over distances greater than a few millimeters occurs mainly
through water motion. Further evidence is needed to directly test this hypothesis.
MECHANISM
OF INTERSPECIFIC
DAMAGE
Behavioral observations
on the mode of competitive damage by F. scuturiu support
the suggestion that mucus secretion may be involved. The observed polyps did not apply
special structures such as the sweeper tentacles (Den Hartog, 1977; Wellington, 1980)
or mesenterial
filaments (Lang, 1973; Chadwick,
1987) used by some corals and
198
N. E. CHADWICK
corallimorpharians
during competition.
a thick layer of mucus onto adjacent
Individuals
Instead,
they simply expanded
and deposited
corals.
of F. scutaria are known to secrete large quantities
of mucus, even when
not in contact with other species (Coles & Strathmann,
1973; Glynn & Krupp, 1986).
Mucus secretion is thought to serve several functions in corals, including rejection of
sediment (Hubbard & Pocock, 1972), food capture (Lewis & Price, 1976) and supply
of organic nutrients to symbiotic crabs that protect the corals from predators (Knudsen,
1967; Glynn, 1976). My observations support the idea that F. scutaria also uses mucus
to competitively damage encroaching species of colonial corals. The secretion of many
nematocysts into the mucus may be related to this function. F. scutaria is the only coral
for which competitive use of mucus has been documented,
and it is also the only
Hawaiian coral species known to secrete large quantities of nematocysts in its mucus,
out of six common Hawaiian species examined by Coles & Strathmann
(1973).
Hildemann et al. (1977) proposed a mechanism of interspecific damage in F. scutaria
involving non-dialyzable,
xeno-cytotoxic
molecules present in secreted mucus. Their
evidence, however, is consistent with an alternate hypothesis in which the cytotoxic
agents are nematocysts. Either mechanism can be used to explain why algae are resistant
to damage by F. scutaria; the algae observed in this study have thick cell walls of
cellulose or calcium carbonate that may be impermeable to penetration by nematocysts
or cytotoxic molecules. The exposed soft tissue of corals, in contrast, appears to be more
susceptible to damage from competing cnidarians.
The mucus secreted by F. scutaria may serve as a matrix that carries nematocysts
which then remain in contact with the target coral for several days. This would explain
why damage to adjacent corals is not observed immediately, but occurs only after
several days under the mucus layer. It is also possible that after several days of being
covered by mucus, the marginal tissues of colonial corals suffocate (are oxygen starved),
or are more susceptible to attack by bacteria. It is not clear whether F. scutaria directly
injures corals or creates a situation in which injuries are likely to occur. In contrast,
anthozoans
that attack their neighbors
by applying
specialized
structures
(acrorhagi,
sweeper tentacles) laden with nematocysts appear to cause direct, immediately damage
to victims (Bigger, 1982; Hidaka & Miyazaki, 1984). Further experiments to isolate and
test different fractions of the mucus of F. scutaria would more precisely determine what
component of the mucus in this species indirectly or directly causes interspecific injury.
Polyps of F. scutaria do not appear to cause competitive damage to conspecitics
(Hildemann et al., 1977; pers. obs.). However, in some corals the effects of intraspecific
competition
are quite subtle (Rinkevich & Loya, 1983) and would not have been
detected in this study. The lack of obvious injury during intraspecific contact in freeliving corals, even when they are piled several layers deep (Goreau & Yonge, 1968; pers.
obs.), may contribute to their survival in shifting aggregations. F. scutaria is the only
species of Fungia to occur in Hawaii. However, it would be interesting to observe the
outcome of intra-generic contacts in regions where several species of the genus co-occur.
The copious mucus secreted by these unattached corals surrounds them with a protec-
CORAL COMPETITION AND LOCOMOTION
199
tive sheath that may, in addition to the other functions mentioned above, offer protection from conspecific or congeneric polyps in aggregations.
ACKNOWLEDGEMENTS
I thank the students and staff of the 1983 Summer Program in Marine Biology at the
Hawaii Institute of Marine Biology for their support, especially E. Cox, P. Glynn, R.
Grigg, M. Holloran, P. Holthus, P. Jokiel, D. Krupp, and B. Richmond. I also thank
C. Bigger, C. Hand, J. Lang, D. Potts, B. Rinkevich, and W. Sousa for comments that
improved the manuscript. Financial support was generously provided by the Edwin C.
Pauley Foundation of the University of California, the University of Hawaii
Foundation, and a Sea Grant Program entitled “Summer Program in Marine Science”,
project no. F238-F-582-B-3 15, under grant no. NA&lAA-D-00070.
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