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First published online April 18, 2006
Journal of Experimental Biology 209, 1690-1695 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02168
Energy integration between the solitary polyps of the clonal coral Lobophyllia corymbosa
1 Department of Zoology, Tel Aviv University, Tel Aviv, Israel
2 Department of Zoology and The Martin Ryan Marine Science Institute,
National University of Ireland, Galway, Ireland
* Author for correspondence (e-mail: yosiloya{at}post.tau.ac.il)
Accepted 16 February 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: Lobophyllia, integration, injury, allorecognition, 14C-labeling
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Hughes et al.,
1992). Traditionally, two morphologically based growth forms are
distinguished in clonal organisms: solitary and colonial. Solitary clonal
organisms are morphologically discrete and physiologically independent. They
are not interconnected by tissue. A colony, by contrast, is a physiologically
united clone in which the individual modules (polyps/zooids) maintain
prolonged tissue continuity, enabling them to exchange metabolites and cells
through common tissues.
The within-colony degree of integration in hermatypic corals, the main
tropical reef constructors, has long been the focus of scientific interest.
Connell reported that large colonies have a better capacity to heal injuries
than smaller ones of the same species
(Connell, 1973). Loya found
that skeletal regeneration restores the symmetry of the original colony shape
(Loya, 1976). Wallace noted
that in some coral species fertile polyps are distributed unevenly within the
colony (Wallace, 1985). Kojis
and Quinn (Kojis and Quinn,
1985) and Szmant-Froelich
(Szmant-Froelich, 1985) showed
that the number of polyps in a colony, rather than colony age, is the primary
threshold determining reproductive stage in many colonial corals. Shelton
documented that polyp retraction is coordinated within colonies in some corals
(Shelton, 1982). Oren and
coworkers found that regeneration of injury in Porites colonies
activates an extended magnitude of energy integration throughout the colony
and that the extent of this integration is regulated by the colony, in
accordance with lesion characteristics
(Oren et al., 2001).
Carbon transfer between sources and sinks within colonies has been
documented (Pearse and Muscatine,
1971; Rinkevich and Loya,
1983a; Rinkevich and Loya,
1983b). Taylor hypothesized that soluble organic compounds and
Ca2+ are translocated among polyps, probably towards regions of
maximal demand (Taylor, 1977).
This early idea has since been experimentally confirmed by Oren and coworkers,
who demonstrated an oriented intra-colonial transport of
14C-labeled photosynthetic products towards regeneration areas in
the hermatypic corals Favia favus, Platygyra lamellina and
Porites sp. (Oren et al.,
1997; Oren et al.,
1998), and by Fine and coworkers in the encrusting stony coral
Oculina patagonica from the Mediterranean
(Fine et al., 2002).
Another aspect of colony integration is that of histocompatibility: in
colonial coral species, separated clonemates fuse when recontacted even after
being isolated for years. Allogeneic (interclonal) grafts, by contrast, always
fail to fuse (Hildemann et al.,
1977).
The above studies provide evidence that colonial corals show a certain
degree of recognition and cooperation among the individual polyps that may
outweigh the `interest' of a single polyp. The situation in solitary corals is
less clear. Integration among solitary clonal cnidarians has been studied in
the sea anemone Anthopleura elegantissima, which often remains
associated as dense aggregations. Within-clone polymorphism and division of
labor have been demonstrated in this species
(Ayre and Grosberg, 1996).
Histocompatibility or other forms of clonal recognition are well documented in
solitary clonal cnidarians (e.g. Jokiel and
Bigger, 1994). However, translocation of energetic products
between clonemates in solitary forms has not, as yet, been studied.
Lobophyllia corymbosa Forskål is a common inhabitant of shallow-water coral reefs in the northern Red Sea. This clonal coral starts its post-metamorphic life as a colony (Fig. 1a). Later, the tissues connecting individual polyps die, transforming the colony into a clone of solitary polyps (Fig. 1b,c). Clonemates, previously belonging to a single colony, usually remain associated, occupying the numerous extremities of one skeleton (corallum). Although separated, occasional, temporal tissue contact between the individual polyps may occur during the night, when polyp body columns expand (i.e. broaden). These contacts do not result in tissue fusion (Fig. 1d).
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Allorecognition assays
Fifty-two polyps from 14 clones whose polyps have already undergone tissue
separation were removed from their original corallum. Fourteen intact polyp
pairs were prepared: seven isografts and seven allografts. They were pair-wise
fastened by insulated copper threads, bringing them into direct and permanent
tissue-to-tissue contact. We then longitudinally sectioned 24 polyps, ensuring
that each section contained a portion of the original mouth. Pair-wise grafts
were then prepared from sections of the same polyp (autografts)
(N=4), clonemates (isografts) (N=6) and non-clonemates
(allografts) (N=14). Graft terminology was adopted from Jokiel and
Bigger's work on the solitary mushroom coral Fungia
(Jokiel and Bigger, 1994). The
results of all grafting experiments were evaluated after 6 weeks and
documented in terms of tissue fusion, skeleton fusion, no response, cytotoxic
rejection and tissue overgrowth. Two isografts and two autografts were fixed
in 4% formalin in seawater (24 h) for histological examination. Following
fixation, samples were rinsed in tapwater, decalcified in formic acid/sodium
citrate solution, dehydrated in ethanol series, embedded in paraffin,
sectioned and stained with hematoxylin and eosin using standard protocols.
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14C-labeling of the polyps was conducted in 4-liter aquaria placed in a radioactive hood. The aquaria were illuminated for a period of 20 h (400–700 nm) to enable active photosynthesis and high 14C incorporation (final concentration of the radioactive carbon in the aquaria was 0.2 µCi ml–1). Following this labeling procedure, the polyps were transferred to another similar sized aquarium in which they were washed with seawater for a period of four hours.
Recent studies have shown that oriented transport of photosynthetic
products within colonial corals is initiated following tissue injuries
(Oren et al., 1997;
Oren et al., 1998;
Fine et al., 2002), already
detectable 48 h post-injury. Therefore, after attaching each hot polyp to its
appropriate corallum, we injured one of its adjacent polyps. These small
tissue lesions (projected area of approximately 2 cm2) were
inflicted by air-pick (i.e. an air tube connected to the SCUBA regulator
enabling a strong accurate air jet, which locally removes the tissue, causing
only minor damage to the skeleton beneath). A schematic representation of the
experimental setup is given in Fig.
2. In addition to the above treatments, three polyps from three
different clones were similarly labeled with 14C. These polyps were
kept in the lab for an additional period of 48 h and thereafter used to
determine 14C activity in their released mucus.
Forty-eight hours after reattachment of the hot polyp to the experimental clones, we sampled four fragments (tissue + skeleton) from each clone using a round stainless-steel corer, enabling collection of similar sized fragments (1 cm2 each, presuming similar tissue thickness in all polyps). One fragment was taken from the hot polyp, one from the injured polyp adjacent to the hot polyp, one from an intact polyp also adjacent to the hot polyp, and one from an intact remote polyp (for sampling locations, see Fig. 2). The fragments were placed individually in plastic vials and brought to the lab. The seawater was drained from each vial and 8 ml of 30% hydrogen peroxide was added in order to digest the tissues. After complete digestion (24 h), the remaining skeletons were removed and two replicates of 0.5 ml from each vial were sampled. Five milliliters of Biodegradable Counting Scintillation cocktail (BCS; Amersham, Bucks, UK) were added to each sample. Activity of 14C in the tissues (c.p.m. cm–2) was determined by a liquid scintillation counter (Tri-Carb 1500; Packard, Bowners Grove, IL, USA). Examination of 14C activity in the mucus was performed by attaching a filter paper to the lateral side of the labeled polyps for a period of 30 s. The filter papers were added to 5 ml of Biodegradable Counting Scintillation cocktail and their 14C activity (c.p.m. cm–2) was determined by a liquid scintillation counter.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The results from the grafting experiments involving sectioned polyps showed different patterns, as follows: all auto- and isografts had fused completely by tissue and skeleton within the 6-week study period. Histological sections of fused partners confirmed the continuity of their tissues across the original contact area. By contrast, none of the allografts had fused. Instead, they either remained in a non-responsive state, healing the wounds caused by the sectioning, or cytotoxically rejected their allogeneic confreres using an unknown effector mechanism.
Energy integration
Forty-eight hours after reattaching the 14C-labeled polyps to
their original clone, the hot polyps showed high 14C activity
(>2000 c.p.m. cm–2;
Table 1). Tissues taken from
the injured adjacent polyps demonstrated significantly higher 14C
activity compared with tissues taken from intact control clones (1-way ANOVA,
P<0.01). By contrast, tissues taken from adjacent, healthy polyps
(Fig. 2) exhibited
14C activity similar to the control tissues (1-way ANOVA,
P>0.05).
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When hot polyps were wrapped with a plastic collar before being reattached to their original clones (i.e. treatment 3; Fig. 1) they demonstrated no significant translocation to any of their adjacent polyps (i.e. both healthy and injured) (Table 1).
When hot polyps were introduced into allogeneic Lobophyllia colonies, the 14C activity of the tissues sampled from injured adjacent, healthy adjacent and healthy remote polyps indicated insignificant shifts of photosynthetic products towards them (1-way ANOVA, Scheffe F-test, P>0.05). That is, their tissues exhibited 14C activity similar to tissues taken from intact control clones. High 14C activity was recorded in the mucus of the labeled polyps 48 h afterlabeling.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Allorecognition assays showed that Lobophyllia does not differ
from other clonal invertebrates in this regard: genetically identical animals
repeatedly recognize their clonemates as `self', while allogeneic individuals
are treated as foreign and rejected. The results of the transplantation
experiments resemble those of experiments done with the solitary clonal coral
Fungia (Jokiel and Bigger,
1994). Contact between intact polyps usually resulted in no
visible response (independent of the genetic identity of the counterparts),
while cut polyps fused only with (cut) clonemates, rejecting allografts. These
results also indicate that the separation of polyps during ontogeny is
genetically programmed rather than environmentally induced, since intact
polyps `insisted' on maintaining their solitary state rather than fusing with
clonemates and re-forming a colony. Contact between cut polyps may be
interpreted as regeneration, in which only clonemates' tissues are accepted as
`tissue donors'.
The results of the radioactive experiments showed a significant and
oriented translocation of photosynthetic products from the labeled polyps
towards the adjacent injured polyps in Lobophyllia clones. These
results resemble previous studies done on `genuine' colonial corals with
developed coenosarc, such as the massive stony corals Favia favus,
Platygyra lamellina (Oren et al.,
1997) and Porites sp.
(Oren et al., 1998) and the
encrusting stony coral Oculina patagonica
(Fine et al., 2002).
Lobophyllia forms a colony only in early ontogeny and directly
following budding, whereas the adult coral constituted a cluster of separated
polyps without interconnecting tissue (I.B., personal observation).
Nonetheless, Lobophyllia clonemates displayed here a typical
`colonial' behavior in regard to energetic collaboration.
One of the questions arising from our results is that of the mechanism of
transfer of photosynthetic materials among these separated polyps.
Translocation of organic compounds between polyps could result from diffusion
down a concentration gradient (Murdoch,
1978; Fang et al.,
1989) or from active (i.e. oriented) transport
(Rinkevich and Loya, 1983a;
Fang et al., 1989;
Oren et al., 1997). In the
present study, active, oriented transport was evident, as significantly less
labeled material was transferred to healthy clonemates and to injured
allogeneic polyps, compared with translocation to injured clonemates. How are
the metabolites transferred in an oriented way without an existing tissue
bridge? We suggest two possibilities, which may apply to Lobophyllia.
(1) The material is transferred in the form of mucus. As can be seen from the
results, part of the photosynthetic production was channeled toward mucus
production, and coral mucus has recently been shown to have a significant role
in the carbon household in coral reefs
(Wild et al., 2004). Mucus may
be moved across the coral's surface by ciliary beat, which, in turn, could be
oriented. (2) The material is transferred in living, migrating cells when
polyp body columns touch at night (Fig.
1). A combination of the two modes, i.e. transfer of
cell-containing mucus, is also possible. Mucus alone would constitute rather a
`poor aid' due to its low nutritional value. Cells offer a more complete
resource for regeneration. Migratory cells may be transferred through mucus
when body columns contact at night. Indeed, preventing physical contact by
means of the plastic collar eliminated the transfer of radioactivity and fits
both modes of transfer.
Interestingly, in the coral Stylophora pistillata, Rinkevich and
Loya documented oriented translocation of photosynthetic metabolites among
allogeneic, incompatible colonies, also without a tissue bridge between source
and sink tissues (Rinkevich and Loya,
1983a). These authors interpreted their results as competition,
with the direction of transport being from the inferior colony towards the
dominant one. Although transport of energy via cells is possible also
in this case, there is a basic difference in our study as follows. Movement of
cells among clonemates enables incorporation of living cells in the
recipient's soma. This would not be possible among distinct genotypes since
allogeneic cells would have likely been rejected by the recipient's
allorecognition system. Hence, among allogeneic partners, donor cells could
only be used as `food' following phagocytosis by the recipient's cells. Olano
and Bigger have reported that phagocytic activity increases following wounding
in the gorgonial coral Swiftia exserta
(Olano and Bigger, 2000).
Allogeneic interaction may be interpreted as `stress', similar to wounding,
which could stimulate phagocytosis of allogeneic cells.
Previous workers have attempted to make connections between the colony
structure, pattern of vegetative reproduction and degree of integration
existing in a colony. Branching structures, polymorphic polyps, perforations
in walls and well-developed coenosarc are among the morphological characters
that indicate integration in coral colonies
(Ryland and Warner, 1986;
Soong and Lang, 1992). In the
present study, a high degree of integration was found in Lobophyllia
clones, as revealed by the translocation of photosynthetic products towards
injured clonemates only, despite no tissue bridge existing between the polyps
and the lack of any other morphological indication for integration.
Why should a coral colony select to transform into a clone of solitary
polyps? `True' colonial growth form may offer better physical conditions for
transfer of metabolites and cells (we could only demonstrate translocation to
adjacent polyps, in contrast to long-distance transfer in colonial species). A
continuous tissue may also facilitate communication between clonemates. A
solitary life strategy, by contrast, may offer a better protection against
pathogens, which cannot (or can less easily) infect clonemate polyps living
without tissue bridges. Furthermore, the formation of a clone of disconnected
polyps also facilitates the dispersal of the genotype in space. This has also
been shown in fungiid mushroom corals, where the detachment of polyps from the
colony occurs earlier in ontogeny. Lobophyllia corymbosa seems to
combine the two strategies: in early post-metamorphic stages, a high degree of
integration is necessary to increase survival chances (see also
Shenk and Buss, 1991). In line
with this, Lobophyllia indeed forms colonies at this stage. Later on,
survival of polyps (and of the whole clone) is less dependent on common
tissues and the coral takes advantage of its solitary growth form as a better
protection against pathogens and more efficient dispersal. As demonstrated
here, however, intra-clonal aid is still possible among morphologically
isolated clonemates.
Taken together, our results show that integration among clonal marine invertebrates does not necessarily depend on structure but can also be maintained between separated clonemates. Examining the structure of coral reef communities from this point of view may provide a new perspective regarding energy shifts within this highly complex ecosystem.
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Acknowledgments |
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References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Ayre, D. J. and Grosberg, R. K. (1996). Effects of social organization on inter-clonal dominance relationships in the sea anemone Anthopleura elegantissima. Anim. Behav. 51,1233 -1245.[CrossRef]
Connell, J. H. (1973). Population ecology of reef-building corals. In Biology and Geology of Coral Reefs, vol. 2 (ed. O. A. Jones and R. Endean), pp. 205-245. New York: Academic Press.
Fang, L. S., Chen, Y. W. J. and Chen, C. S. (1989). Why does the white tip of stony coral grow so fast without zooxanthellae? Mar. Biol. 103,359 -363.[CrossRef]
Fine, M., Oren, U. and Loya, Y. (2002). Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 234,119 -125.[CrossRef]
Hildemann, W. H., Raison, R. L., Cheung, G., Hull, C. J., Akada, L. and Okamoto, J. (1977). Immunological specificity and memory in a scleractinian coral. Nature 270,219 -222.[CrossRef][Medline]
Hughes, R. N. (1989). A Functional Biology of Clonal Animals. New York: Chapman and Hall.
Hughes, R. N., Ayre, D. and Connell, J. H. (1992). Evolutionary ecology of corals. Trends Ecol. Evol. 7,292 -295.[CrossRef]
Jokiel, P. L. and Bigger, C. H. (1994). Aspects of histocompatibility and regeneration in the solitary reef coral Fungia scutaria. Biol. Bull. 186,72 -80.[Abstract]
Kojis, B. L. and Quinn, N. J. (1985). Puberty in Goniastrea favulus: age or size limited? Proc. 5th Int. Coral Reef Symp. 4,289 -293.
Loya, Y. (1976). Skeletal regeneration in a Red Sea scleractinian coral population. Nature 261,490 -491.[CrossRef][Medline]
Murdoch, G. R. (1978). Digestion assimilation, and transport of food in the gastrovascular cavity of a gorgonian octocoral (Cnidarian: Anthozoa). Bull. Mar. Sci. 28,354 -362.
Olano, C. T. and Bigger, C. H. (2000). Phagocytic activities of the gorgonian coral Swiftia exserta. J. Invertebr. Pathol. 76,176 -184.[CrossRef][Medline]
Oren, U., Rinkevich, B. and Loya, Y. (1997). Oriented intra-colonial transport of 14C labeled materials during regeneration in scleractinian corals. Mar. Ecol. Prog. Ser. 161,117 -121.
Oren, U., Brickner, I. and Loya, Y. (1998).
Prudent sessile feeding by the corallivore snail Coralliophila
violacea on coral energy sinks. Proc. R. Soc. Lond. B Biol.
Sci. 265,2043
-2050.
Oren, U., Benayahu, Y., Lubinevsky, H. and Loya, Y. (2001). Extent of coral colony integration during regeneration. Ecology 82,802 -813.[CrossRef]
Pearse, V. B. and Muscatine, L. (1971). Role of
symbiotic algae (zooxanthellae) in coral calcification. Biol.
Bull. 141,350
-363.
Rinkevich, B. and Loya, Y. (1983a). Oriented translocation of energy in grafted reef corals. Coral Reefs 1,243 -247.
Rinkevich, B. and Loya, Y. (1983b). Short term fate of photosynthetic products in a hermatypic coral. J. Exp. Mar. Biol. Ecol. 73,175 -184.[CrossRef]
Ryland, J. S. and Warner, G. F. (1986). Growth and form in modular animals: ideas on the size and arrangement of zooids. Philos. Trans. R. Soc. B Biol. Sci. 313, 53-76.
Shelton, G. A. B. (1982). Anthozoa. In Electrical Conduction and Behavior in `Simple' Invertebrates (ed. G. A. B. Shelton), pp.141 -154. Oxford: Clarendon Press.
Shenk, M. A. and Buss, L. W. (1991). Ontogenetic changes in fusibility in the colonial hydroid Hydractinia symbiolongicarpus. J. Exp. Zool. 257, 80-86.[CrossRef]
Soong, K. and Lang, J. C. (1992). Reproductive integration in reef corals. Biol. Bull. 183,418 -431.[Abstract]
Szmant-Froelich, A. (1985). The effect of colony size on the reproductive ability of the Caribbean coral Montastrea annularis (Ellis and Solander). Proc. 5th Int. Coral Reef Symp. 1,295 -300.
Taylor, D. L. (1977). Intra-colonial transport of organic compounds and calcium in some Atlantic reef corals. Proc. 3rd Int. Coral Reef Symp. 1, 431-436.
Wallace, C. C. (1985). Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar. Biol. 88,217 -233.[CrossRef]
Wild, C., Huettel, M., Klueter, A., Kremb, S. G., Rasheed, M. Y. M. and Jørgensen, B. B. (2004). Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428,66 -70.[CrossRef][Medline]
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