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Winter Quiescence, Growth Rate, and the Release from
Competition in the Temperate Scleractinian Coral Astrangia
poculata (Ellis & Solander 1786)
Sean Grace*
Abstract - I examined winter quiescence (dormancy), growth rate, and competition in the
scleractinian coral Astrangia poculata (Northern Star-coral) at an intertidal and a subtidal
site in Rhode Island. I observed the onset, duration, and cessation of quiescence from November
2013 to May 2014 and noted when coral tentacles no longer exhibited tactile responses,
which I used as a proxy for quiescence. Results demonstrated that intertidal corals entered
quiescence in December 2013, when air/water temperatures ranged from 0.71 °C to 5.7 °C,
whereas subtidal populations entered quiescence in January when water temperatures ranged
from 3.4 °C to 4.3 °C. Corals exited quiescence at similar temperatures (6.0–8.5 °C), again
doing so earlier in the intertidal than subtidal populations (April and May 2014, respectively).
Corals at both sites grew (added polyps) over the course of the study, but during quiescence,
growth ceased in subtidal corals, and intertidal corals lost peripheral polyps. Competitive
interactions between Northern Star-coral and the tunicate Didemnum vexillum (Carpet Tunicate)
decreased during quiescence with a corresponding increase in “halo” width around each
coral. I observed no change in halo-width between coral and the sponge Cliona celata (Red
Boring Sponge). All corals examined exhibited winter quiescence, grew during the course of
the study, and were released from competition with Carpet Sea-squirt Tunicate; no change in
competition with Red Boring Sponge was observed.
Introduction
The winters in New England create environmental conditions that induce a quiescent
state in many organisms. This quiescence may serve as a way to avoid the
costs associated with winter’s unfavorable conditions (Cáceres 1997). Quiescence
occurs when the basic physiological processes in marine invertebrates are halted
due to decreasing or increasing temperatures (Betti et al. 2012, Caceres 1997, Coma
and Ribes 2003, López-Legentil et al. 2013, Teixidó et al. 2015). The costs and benefits
of quiescence to the biology and ecology of organisms remain understudied.
During quiescence, organisms can cease growing, be outcompeted for space, and
overgrown, or depredated upon, and they may be exposed to severe environmental
conditions (freezing, dessication) that may ultimately affect their survival, distribution,
and abundance (Caceres 1997, Comeau et al. 2012, Dimond et al. 2012).
Southern New England intertidal and subtidal communities are comprised of
many invertebrate species (Dimond et al. 2012, Grace 2004, Harlin and Rines
1993). One conspicuous organism in these habitats is the temperate scleractinian
*Department of Biology, Southern Connecticut State University, New Haven, CT 06515;
graces2@southernct.edu.
Manuscript Editor: Jay Dimond
Winter Ecology: Insights from Biology and History
2017 Northeastern Naturalist 24(Special Issue 7):B119–B134
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coral Astrangia poculata Ellis & Solander (Northern Star-coral), which is typically
found in the shallow subtidal from Cape Cod south through the northernmost
reef tracts of Florida and throughout the Gulf of Mexico (Cummings 1983, Dimond
and Carrington 2007, Dimond et al. 2012, Grace 2004, Peters et al. 1988).
This coral is abundantly distributed on hard-bottom substrate in subtidal (depths
of 0–30 m) areas of southern New England where it competes for space with other
invertebrate species and macroalgae (Grace 2004). The morphology of Northern
Star Coral ranges from encrusting to finger-like, with more finger-like colonies
found on vertical substrates (Grace 2004); small populations of this coral can be
found in the intertidal.
Intertidal populations of scleractinian corals are rare worldwide. Those coral
species that do exist in the intertidal are typically limited in distribution to the tropics
(Anthony and Kerswell 2007, Brown et. al. 2002). Although some temperate and
subtropical intertidal-coral species exist (Hellberg 1994, Scott 1984), the presence
of intertidal corals in such northerly lattitudes as southern New England is intriguing.
The presence of intertidal Northern Star-coral raises questions as to how corals
can withstand the abiotic (wave-exposure, salinity changes, temperature extremes,
desiccation, UV stress, and mid-day irradiances) and biotic factors (competition
and predation) known to affect other intertidal taxa like barnacles, mussels, snails,
and several divisions of the macroalgae in temperate regions (Carrington 2002,
Helmuth 1998, Menge and Branch 2001).
Northern Star-coral is also one of several species of Cnidaria (Betti et al. 2012,
Caceres 1997) that experience quiescence during the winter months when temperatures
decrease (Grace 1996, Dimond and Carrington 2007). The onset of quiescence
appears to begin when coral tentacles become unresponsive to touch, at which time
the body and tentacles retract into the calcium carbonate theca and the oral plate
puffs out, resulting in a characteristic ring inside the polyp. With polyp retraction,
active feeding may cease during quiescence and coral growth can be negative.
Jacques et al. (1983) found negligible calcification rates in colonies acclimated
at 6.5 °C in comparison to those acclimated at higher temperatures. Moreover,
Dimond and Carrington (2007) found that corals exhibited a decline in live-polyp
number due to tissue loss during the winter and early spring, and they hypothesized
that during this time of inactivity corals were more likely to be over-grown by other
species. The biological and ecological significance of quiescence in intertidal and
subtidal colonies of Northern Star-coral is unknown. Quiescence may allow intertidal
corals to over-winter and survive adverse environmental conditions.
Didemnum vellixum Kott (Carpet Tunicate) is a non-native invasive species
introduced in Narragansett Bay in the 1980s (Bullard et al. 2007), and it competes
with Northern Star-coral by growing to the edges of the coral. This growth creates
a “halo effect” around the coral ccolony. Growth of the tunicate is then inhibited
by an unknown mechanism that might involve the production of allelochemicals
(Hoeksema and Voogd 2012), nematocysts present in coral’s tentacles that come in
contact with the tunicate, or, as has been demonstrated in other temperate anthozoans,
presence of sweeper tentacles (Sebens and Miles 1988). Although the effects
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of some tunicates on tropical reefs have been detrimental (e.g., Diplosoma simile
(Sluiter) smothers both coral and coralline algae; Littler and Littler 1995), little
research has been done on temperate reefs to examine coral–tunicate interactions
or how these interactions may change community structure over time.
Cliona celata Grant (Red Boring Sponge) is often observed in direct competition
with Northern Star-coral. This competition often presents itself subtidally as
a coral colony surrounded by sponge tissue. Given the limestone bio-eroding nature
of this sponge’s ecology (Brusca and Brusca 1990, Duckworth and Peterson
2013, Wisshak et al. 2012), it often erodes under the coral, possibly decreasing
the coral’s attachment strength, thus affecting community structure. It is possible
that both Carpet Tunicate and Red Boring Sponge may overgrow colonies during
coral quiescence.
The goal of my study was to determine in both intertidal and subtidal populations
of Northern Star-coral, the onset, duration, and cessation of quiescence;
examine growth rate; and describe interactions between this coral and 2 competing
invertebrates—Carpet Tunicate and Red Boring Sponge—during quiescence.
Methods
Field-site description
I studied 2 locations with known coral populations within lower Narragansett
Bay and Rhode Island Sound (Fig. 1). The intertidal site, Bass Rock (41°48'21"N,
71°58'21"W), adjacent to Rhode Island Sound in Narragansett, RI, is a moderately
wave-exposed rocky shore (Carrington 2002). It is a typical New England intertidal
habitat with large granite boulders with seasonal populations of sessile barnacles,
mussels, tunicates, sponges, and macroalgae, as well as mobile snails and crabs.
The subtidal site, at Fort Wetherill State Park (41°28'40"N, 7121'24"W) in Jamestown,
RI, has several coves with subtidal bedrock walls extending from 5 m to 40
m in depth (Grace 2004). Consistent with observations from other subtidal studies,
the shallow horizontal substrates in this area are dominated by macroalgae (Grace
2004, Harlin and Rines 1993), and vertical substrates are covered with epifaunal
invertebrates such as corals, hydroids, tunicates, sponges, and several mobile fauna
(Dimond and Carrington 2007, Grace 2004, Velimirov and Griffiths 1979, Witman
and Grange 1998, Witman and Sebens 1988).
Quiescence and growth
I established one 50-m transect line at the Bass Rock intertidal site, 0.1 m
above mean lower low water (MLLW) and tagged the first 30 corals encountered. I
scraped areas of substrate near the corals with a wire brush and attached aluminum
tree-tags to the substrate using Z-spar epoxy splash-zone compound (Pettit-A788,
available in marine hardware stores). Using SCUBA, I established one 50-m transect
line at at the Fort Wetherill subtidal site at a depth of 14 m depth and tagged 30
corals as described above. Only aposymbiotic corals (those lacking dinoflagellate
symbionts and which appear white) were used in the study because they were most
common at both sites.
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Figure 1. Map of the 2 Rhode Island
sites: Bass Rock (BR) intertidal in
Narragansett, RI, and Fort Wetherill
(FW) subtidal in Jamestown, RI.
Top map:. Rhode Island (author unknown)
Bottom map: Available online
at http://www.worldatlas.com/webimage/
countrys/namerica/usstates/outline/
ri.gif. Accessed 8 July 2016, reproduced
with permission from World
Atlas).
To determine the initiation and cessation of quiescence, beginning in November
2013, I touched each tagged colony monthly with a blunt probe to examine polyp
behavior. The initiation of quiescence was indicated by a lack of tentacle retraction
(non-responsive to touch), observation of a retracted polyp body with full or partial
retraction of the tentacles into the calcium carbonate theca, and a puffed or inflated
oral plate. Cessation of quiescence was determined when touch resulted in a tentacle
contraction.
I measured the growth of tagged colonies at 3-month intervals for 1 year beginning
in September 2013. As in Dimond and Carrington (2007), I counted the
numbers of polyps per monitoring date (September 2013, December 2013, March
2014, June 2014, and September 2014). Growth rate for each colony was analyzed
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by 2-way repeated measures ANOVA with site (Bass Rock and Fort Wetherill) and
date (September 2013, December 2103, March 2014, June 2014, and September
2014) as fixed factors; the repeating factor was polyp number per coral. I conducted
post hoc comparisons with Holm-Sidak tests. To correct for unequal variances, α
was adjusted to 0.025 (Keppel and Wickens 2004). All statistical tests were completed
in Systat 13.0 (SPSS, Inc., Chicago, IL).
Competition
Coral–tunicate and coral–sponge assemblages were defined as situations in
which either invertebrate was present around a coral (encroaching it), with the
interaction forming a characteristic halo-effect. In these cases, the Northern Starcoral
was surrounded by a halo of either Carpet Tunicate or Red Boring Sponge. At
each site, I noted the frequency of corals alone, coral–tunicate, and coral–sponge
assemblages during transect and swath surveys. At the Bass Rock intertidal site,
I established one 50-m transect line 0.1 m above MLLW and counted all corals
(growing separately), coral–tunicate, and coral–sponge assemblages within a 0.25-
m–wide swath centered on the transect line. I used SCUBA to set up transects at
the subtidal site. Due to greater coral abundance, I established three 30-m transect
lines at a depth of 14 m and counted all corals (growing separately) and coral–
other invertebrate assemblages by swimming along each transect within a 0.25-
m–wide transect-centered swath. I employed a chi-square test for independence to
determine if the observed proportion of coral–tunicate associations, coral–sponge
associations, or corals found alone were independent of site.
To examine the changes in competition, defined as change in halo-width (cm), I
tagged coral–tunicate assemblages (n = 20 intertidall, n = 20 subtidal) and coral–
sponge assemblages (n = 5 intertidal, n = 20 subtidal) along the transects described
above. I included only aposymbiotic corals because they were most common at the
site. At both sites, I used calipers to make monthly measurements of halo-width for
1 year beginning in September 2013. I analyzed the change in halo-width for each
coral–tunicate and coral–sponge assemblage by conducting 2-way repeated measures
ANOVA with site (Bass Rock and Fort Wetherill) and date as fixed factors and
halo-width per coral–competitor assemblage as the repeating factor. I conducted
post hoc comparisons with Holm-Sidak tests and adjusted α to 0.025 to correct for
unequal variances (Keppel and Wickens 2004).
In situ temperature was measured and recorded throughout the monitoring
period by data loggers (Stowaway Hobo-Temp TidBit, Onset Computer, Bourne,
MA) attached to the substrate adjacent to transects in both intertidal and subtidal
habitats. I set the loggers to measure temperature every 8 min once deployed. After
6 months, the recorders were collected, downloaded, relaunched, and placed back
in situ; thus, I obtained 1 year of continuous temperature data from the intertidal
and subtidal habitats. I calculated average temperature per monitoring day from the
continuous recordings.
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Results
Quiescence and growth
All corals experienced quiescence, but the initiation and cessation of quiescence
was dependent on habitat and temperature (Fig. 2). I first observed quiescence in
the intertidal population in December 2013 and it lasted through April 2014. In the
subtidal population, I first observed quiescence in January 2014 and it ended May
2014. Temperature recordings from both sites suggested a lag between temperature
and the initiation of quiescence in subtidal populations (Fig. 2). The data suggest
that intertidal corals enter quiescence when air/water temperatures range from 0.71
°C to 5.7 °C and exit quiescence when temperatures range from 6.0 °C to 8.9 °C,
whereas subtidal populations enter quiescence when water temperatures range from
3.4 °C to 4.3 °C and exit when the water temperatures range from 6.1 °C to 8.5 °C.
All corals grew during the course of the 1-year study (Fig. 3); however, growth
slowed for subtidal colonies, and was negative for intertidal corals, which exhibited
a loss in polyp number during the December to March timeframe only. Results of the
2-way repeated measures ANOVA demonstrate that coral growth was significantly
Figure 2. Average temperature (°C ± SD) on monitoring dates taken from continuous temperature
measurements per site. Temperature profile for Bass Rock (open circles) and Fort
Wetherill (closed circles). Solid and dashed lines indicate the period of quiescence in intertidal
corals (solid) and subtidal corals (dashed).
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dependent on date (F4,116 = 557.52, P < 0.001; Table 1A), but not on site or on site
x date interactions. Holm-Sidak post hoc tests demonstrated that coral-growth rate
was different between the 2 sites in June 2014 (Table 1B).
Competition
Coral–tunicate and coral–sponge interactions occurred at both intertidal and
subtidal sites, albeit coral–sponge interactions happened less frequently in the
intertidal (Fig. 4). At Bass Rock, 55.3% (67) out of 121 of corals examined were
in an interaction with Carpet Tunicates, 4.1% (5) with Red Boring Sponges, and
40.5% (49) had no interactions. At Fort Wetherill, out of a total of 2761 corals
examined, 41.8% (1154) were with Carpet Tunicates, 23.1% (639) were with Red
Boring Sponges, and 35.4% (978) had no interactions at the time examined. Results
of the chi-square analysis (Table 2) show that the proportion of assemblages was
significantly different between sites (df = 2, χ2 =24.51, P < 0.05). Coral–sponge
assemblages were more likely to be found in subtidal than intertidal habitats and
coral–tunicate assemblages were common in both (Fig. 4).
Figure 3. Mean (± SE) number of polyps per colony (n = 30) for intertidal Bass Rock (open
circles) and subtidal Fort Wetherill (closed circles). Growth was significantly dependent on
date (F 4,116 = 557.52, P < 0.001; Table 1A) but not site or site by date interactions. All corals
added polyps from the beginning to the end of the study, but growth slowed for subtidal
colonies and was negative for intertidal corals exhibiting a loss in polyp number during the
December–March timeframe only.
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Table 1. (A) 2-way repeated measures ANOVA. Coral (n = 30) growth-rate comparisons at 2 sites (BR
= intertidal, FW = subtidal) on 5 dates (13 September, 13 December, 14 March, 14 June, 14 September).
(B) Post hoc Holm-Sidak tests demonstrating between-site comparisons by date (significance
level = 0.025). df = degrees of freedom, SS = sum of squares, and MS = mean square.
(A)
Source of variation df SS MS F P
Subject 29 1.776 0.0612 1.116 0.385
Site 1 0.199 0.1990 3.691 0.065
Site x coral 29 1.587 0.0547
Date 4 18.311 4.5780 557.597 less than 0.001
Date x coral 116 0.953 0.0082
Site x date 4 0.071 0.0176 2.184 0.076
Residual 109 0.880 0.0081
Total 292 24.623 0.0843
(B)
Comparison Difference of means t P P < 0.025
September 2013 0.0071 0.198 0.844 No
December 2013 0.0260 0.752 0.455 No
March 2014 0.0642 1.860 0.067 No
June 2014 0.0922 2.611 0.011 Yes
September 2014 0.0768 2.035 0.046 No
Figure 4. The percent of interactions noted in both subtidal (black bars) and intertidal habitats
(gray bars). The percent occurrence of coral–tunicate interactions was higher in both
intertidal and subtidal habitats than coral–sponge interactions, but the percent of coral–
sponge interactions was higher in the subtidal than intertidal (df = 2, χ2 = 24.51, P < 0.05).
Corals without interactions were common in both habitats.
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Halo-width increased with decreasing temperature at both sites for the coral–tunicate
assemblages but the difference was more pronounced in the intertidal than
subtidal habitat (Fig. 5). The halo-width in the intertidal habitat increased from
an average of 0.23 (± 0.09) cm in warmer conditions (September–November) to
0.82 (± 0.14) cm in colder conditions (December-April). Subtidal coral–tunicate
assemblages had an average halo-width of 0.44 (± 0.07) cm in warmer months
(September–December) and 0.61 (± 0.09) cm in colder months (January–May).
Results of the 2-way repeated measures ANOVA indicated a significant site-by-date
interaction (F11,209 = 50.405, P < 0.001; Table 3A). The results of Holm-Sidak post
hoc tests demonstrate that halo-width was similar between sites in October through
December 2013, but then differed significantly between the sites from January
through September 2014 (Table 3B). No change in halo-width for coral–sponge
assemblages was found throughout the study.
Discussion
Quiescence and growth
All corals entered quiescence in both habitats, though at different times based on
temperature (Fig. 2). The first observation of a non-response to touch was noted for
intertidal corals on 18 December 2013, when daily intertidal temperatures ranged
from 0.71 °C to 5.7 °C. It is likely the intertidal corals entered quiescence prior
to that date because intertidal temperatures dropped from a November average of
10.9 (±2.2) °C to 4.7 (± 1.4) °C in December. Subtidal corals exhibited no response
to touch on 12 January 2014 when subtidal temperatures ranged from 3.4 °C to
Table 2. Results of chi-square analysis, (df = 2, χ2 = 24.51, P < 0.05). The frequency of coral–tunicate,
coral–sponge assemblages, and corals alone were different.
Subjects Intertidal Subtidal
Coral alone
Counts 49 978
Expected counts 43.11 983.88
Row % 4.77 95.23
Column % 40.49 35.42
Total % 1.7 33.93
Coral–tunicate
Counts 67 1154
Expected counts 51.26 1169.7
Row % 5.48 94.52
Column % 55.37 41.79
Total % 2.32 40.04
Coral–sponge
Counts 5 629
Expected counts 26.62 607.38
Row % 0.78 99.22
Column % 4.13 22.78
Total % 0.17 21.83
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4.3 °C. The exact dates of initiating and exiting quiescence is unknown because
sampling occurred only monthly. Colder temperatures were documented earlier at
the intertidal than at the subtidal site, and this temperature difference corresponded
with an earlier onset of quiescence at the intertidal site. Likewise, intertidal
colonies experienced warmer temperatures sooner than subtidal colonies and thus
exited quiescence earlier (April versus May). It is noteworthy that individual polyps
sometimes exhibited activity before the whole colony, suggesting incomplete
cessation of quiescence. This intra-colony difference in response occurred in April
2014 at the subtidal site, 1 month before complete cessation of quiescence.
Besides becoming non-responsive to touch, Northern Star-coral demonstrates
quiescence by pulling in its tentacles, puffing out its oral plate, and remaining inactive
until water temperatures rise. Other temperate anthozoans exhibit quiescence
similarly. Betti et al. (2012) observed that the temperate Mediterranean octocoral
Cornularia cornucopiae (Pallas) (a soft coral) developed a characteristic perisacral
envelope covering the stolon and the calyx of each polyp formed. This covering
isolated the dormant living tissue from the exterior. They also found that during
Figure 5. Coral–tunicate (n = 20) halo-width changes over the monitoring period in both
the intertidal habitat Bass Rock (A) and subtidal habitat Fort Wetherill (B). Halo-widths
(cm) represented by closed black circles (mean ± 1 SD) and average water temperature
(°C) on monitoring dates (taken from continuous temperature recordings) represented by
open circles (mean ± 1 SD). There was a significant site by date interaction (Table 3A) with
increases in size for both habitats but it was significantly greater in the intertidal than the
subtidal during January through September 2014 (Table 3B).
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winter, the polyps degenerate and the dormant stolons remain in their envelopes.
One interesting observation made on all subtidal colonies in the current study was
the release of mesenterial filaments through the coral mouth; the reason for this behavior
is unknown. Although quiescence in Northern Star-coral involves a similar
pulling in of tissue and the formation of a protective sac as described by Betti et al.
(2012) for C. cornucopiae, the release of mesenterial filaments observed in Northern
Star-coral at the end of quiescence has not been documented for other corals.
Quiescence is not only a cold-temperature phenomenon. A number of recent
studies have demonstrated quiescence at warmer temperatures in Mediterranean
corals (Caroselli et al. 2015, Coma and Ribes 2003, Teixidó et al. 2015). Coma and
Ribes (2003) suggested that low food-availability (energetic constraint) underlies
the summer-dormancy phenomenon observed in benthic suspension feeders. Also,
Caroselli et al. (2015) found that Balanophyllia europaea (Risso) (Pig-tooth Coral)
becomes dormant in the summer months due to lower nutrient levels and zooplankton
densities typically found in stratified summer waters in the Mediterranean.
Northern Star-corals and other temperate anthozoans, including Alcyonium siderium
Verrill (a soft coral) and Metridium senile (L.) (Plumose Anemone) (Sebens and
Table 3. (A) 2-way repeated-measures ANOVA. Coral–assemblage halo-width comparisons (n = 20)
at 2 sites (BR = intertidal, FW = subtidal) and at monthly intervals (October 2013–September 2014).
(B) Post hoc Holm-Sidak test demonstrating between-site comparisons per date (significance level =
0.025). Subject equals individual coral–tunicate assemblage. df = degrees of freedom, SS = sum of
squares, and MS = mean square.
(A)
Source of variation df SS MS F P
Subject 19 185.515 9.764
Site 1 268.329 268.329 34.629 less than 0.001
Site x subject 19 147.223 7.749
Date 11 279.853 25.441 64.206 less than 0.001
Date x subject 209 82.814 0.396
Site x date 11 172.131 15.648 50.405 less than 0.001
Residual 209 64.884 0.310
Total 479 1200.749 2.507
(B)
Comparison Difference of Means t P P < 0.025
October 2013 0.322 1.057 0.297 No
November 2013 0.455 1.492 0.144 No
December 2013 0.145 0.477 0.636 No
January 2014 1.353 4.437 less than 0.001 Yes
February 2014 1.831 6.004 less than 0.001 Yes
March 2014 2.554 8.372 less than 0.001 Yes
April 2014 2.848 9.338 less than 0.001 Yes
May 2014 2.586 8.480 less than 0.001 Yes
June 2014 2.798 9.174 less than 0.001 Yes
July 2014 2.407 7.891 less than 0.001 Yes
August 2014 1.738 5.697 less than 0.001 Yes
September 2014 0.752 2.465 0.018 Yes
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Koehl 1984), rely heavily on substrate-associated Corophium spp. (amphipods) as
prey (Grace 1996). These amphipods experience dormancy in winter months (Wilson
and Parker 1996). Hence, because prey is scarce when temperatures decrease,
it is likely that temperature is not the only environmental cue to initiate quiescence
in these temperate corals.
All corals sampled grew in both intertidal and subtidal habitats. Even intertidal
corals, which are subject to emersion, wind exposure, freezing temperatures, and ice,
survived throughout the period of this observational study and added polyps. Results
on intertidal coral-growth rate coincide with those reported in Dimond and Carrington
(2007), where growth increased through December and decreased thereafter
till March with a recovery of growth in the warmer months (Fig. 3). In the present
study, the decrease in growth was evident in intertidal but not subtidal colonies from
December to March. Most intertidal corals in this study exhibited partial mortality
along the colony’s peripheral thinnest polyps, which may be due to freezing winter
temperatures. Similarly, Betti et al. (2012) found that during winter, the temperate
Mediterranean octocoral Cornularia cornucopiae shrank, but commenced growth
again in summer months. Unlike the intertidal colonies, the subtidal colonies in the
present study did not lose nor add polyps during quiescence.
The loss of peripheral polyps in intertidal coral may be due to other factors.
Wave exposure, UV stress, or high irradiance and resultant desiccation (during low
tide) could have affected peripheral polyps (Miller 1995, Miller and Hay 1996); I
did not assess these factors in the current study. Although Dimond et al. (2012) suggested
the possibility of overgrowth in dormant corals, I did not observe overgrowth,
overtopping, or depredation by other invertebrates (tunicates, barnacles, mussels or
sponges) during this year-long study. The macroalga Chondrus crispus Stackhouse
(Irish-moss) settled directly on the skeleton (between polyps) of several intertidal
encrusting colonies, but upon the cessation of quiescence the algae did not interfere
with polyp behavior or activity, and all polyps responded when touched.
Competition
Coral–tunicate assemblages were more common than coral–sponge assemblages
at both sites (Fig. 4), and coral–sponge assemblages were more common
at the subtidal than intertidal site. The percent change in halo-width—a measure of
the competitive interaction between corals and tunicates—increased with decreasing
water temperature significantly more in the intertidal than subtidal (Fig. 5).
Valentine et al. (2007) studied the effects of emersion on tunicates and found that
these organisms undergo fission in the intertidal when exposed to colder temperatures,
and are open to predation by Littorina littorea (L.) (Common Periwinkle).
During this study, I noted the presence of L. littorea near coral–tunicate assemblages,
but saw no direct predation.
The temporal consistency of these coral–tunicate and coral–sponge assemblages
suggests that this competition is continuous, but the ultimate outcomes of the interactions
are unknown. This particular coral–tunicate interaction is relatively recent
because Carpet SquirtTunicate is non-native, whereas Northern Star-coral and Red
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Boring Sponge are native to Narragansett Bay. Thus, this study documents the first
occurance of a coral–tunicate competition in local waters. The coral–tunicate competitive
stand-off (halo effect) lasts only as long as there are warm temperatures.
Some tunicates do “hibernate” (go dormant) or die off when temperatures decrease
(Burighel et al. 1976, Valentine et al. 2007), though the opposite is also true, in
that some become dormant in the summer (López-Legentil 2013). Both corals and
tunicates experience quiescence; thus, it appears that both are released from this
competition yearly. During the winter release, the organisms are open to predation,
settlement, and overgrowth by other organisms. However, I observed no overgrowth
of either corals, tunicates, or sponges during this study.
The competitive release noted in the coral–tunicate assemblage was not obvious
in the coral–sponge assemblage. The coral–sponge competition did not appear to
change at all during the study because there was no change in halo-width. Although
clionaid sponges are known to bio-erode corals on tropical reefs (Glynn and Manzello
2015), the rate of sponge bioerosion taking place under Northern Star-coral is
difficult to determine and was not measured. Decreasing temperature is known to
decrease the rate of sponge bioerosion (Duckworth and Peterson 2013, Fang et al.
2013); however, I did not assess this parameter in the current study. I observed that
Red Boring Sponge affects corals by eroding under the coral skeleton, dislodging
the colony yet holding the coral in place within a sponge matrix. By doing so, the
sponge decreases coral structural integrity, opening it up to dislodgement forces via
water flow in the subtidal, or both water flow and wave exposure in the intertidal.
Reduced attachment strength caused by sponges has been documented in the tropics
(Bell et al. 2013) but remains little studied on temperate reefs. The growth and
bioerosion rates of sponges increase in warmer waters; thus, it is likely that with
global climate change, more temperate and tropical corals will become unattached
(Bell et al. 2013, Wisshak et al. 2012), which may lead to a possible alternative
stable state in the tropics (Norström et al. 2009) and an increase in sponge abundance
on temperate reefs.
In conclusion, all corals entered and exited winter quiescence, though intertidal
corals did both earlier than subtidal corals. All corals grew from September to December,
but intertidal corals lost polyps from December to March, whereas subtidal
corals maintained their polyp numbers during this time. After quiescence, both
intertidal and subtidal colonies resumed growth. Halo-width, used as a measure of
competition, increased in coral–tunicate assemblages under colder temperatures,
suggesting a competitive release. In contrast, I observed little change in halo-width
in coral–sponge interactions. I did not observe overgrowth in either the intertidal
or subtidal habitat.
Acknowledgments
I thank J. Dimond for editing and providing comments on the manuscript. S. Smedley,
T. Wickman, and 3 anonymous reviewers provided valuable insight which made the manuscript
stronger. I am grateful for the taxonomic consultations of J. Reinhardt and L. Stefaniak.
G. DiPreta, S. Koerner, and T. Massari provided diving and logistical support. The
Northeastern Naturalist
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2017
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Vol. 24, Special Issue 7
work was completed with the aid of a research grant from the Connecticut State University
and partly supported by the Werth Center for Coastal and Marine Studies at SCSU.
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