MARINE ECOLOGY PROGRESS SERIES Published November 14 Mar Ecol Prog Ser

NOTE

Do reproduction and regeneration in damaged corals compete for energy allocation?

B. Rinkevich

National Institute of Oceanography, Tel-Shikmona. PO Box 8030, Haifa 31080, Israel

ABSTRACT Several field studles have revealed that dam- different stages of the 's life (Kozlowski & aged corals have lower fecundity during regeneration as com- Wiegert 1986). Although growth, maintenance and pared to intact colonies. Thls finding was ~nterpretedas repair are supposed to be dependent on a common suggesting that there is a trade-off in the allocation of energy between reproductive activities versus growth and regenera- resource pool, the interaction between these functions tion in corals, where sexual reproduction is easily disrupted. remains relatively obscure (e.g. Wahle 1983). The However, 3 independent lines of evidence critically challenge accepted paradigm is that reproduction as well as the paradigm of energy allocation trade-off and suggest that growth and regeneration in corals are 'energy-costly' (1) sexual reproduction in cnidarians may not always be subject to energy constraints and may possess a hierarchial processes (reviewed in Rinkevich & Loya 1989, Harri- function, (2) shallow-water scleractinians may not be prone to son & Wallace 1990). Thus, there should be a trade-off energy constraints, and (3) regeneration is a regulated in resource allocation between them, and injuries may process expressed through programmed events and not lead to temporary or permanent shifts in energy alloca- directly related to the energy trade-off principle Growth, tlon. It is widely agreed that sexual reproduction in tissue repair and the production of the germ cell require 1 major resource, the stem cells It is suggested that any corals is a highly sensitive life history characteristic extensive use of these reserve cells may reduce their numbers which is easily disrupted during regeneration (Rinke- and significantly affect one or more biological functions. Sev- vich & Loya 1989). The decrease in reproductive activ- eral studies indirectly confirm this idea. Trade-offs for stem ities, according to this idea, results from a limited cells between tissue repair and sexual reproduction should be considered as a relevant factor shaping reproduct~veactivi- amount of energy resources and the allocation of ties during regeneration in reef corals. energy among various biological functions. Several field studies support this idea. Kojis & Quinn KEYWORDS: Corals Regeneration Reproduction . Stem (1985) found lower fecundity in damaged cells Trade-offs between traits fuvulus colonies, compared to intact controls, and sug- gested that this resulted from reallocation of limited energy resources to repair damaged tissue. Rinkevich The paradigm. The ability to regenerate damaged & Loya (1989) found that fecundity in regenerating tissue is a well-documented phenomenon for a variety colonies of Stylophora pistillata was an order of magni- of marine invertebrates including cnidarians that tude lower than in undamaged control colonies up to inhabit coral reefs. The capacity of coral colonies to 19 mo after breakage. Van Veghel & Bak (1994) stud- recover lesions or repair damaged parts has attracted ied regeneration versus reproduction in the Caribbean ecologists who have studied the consequences of coral Montastrea annularis and found that the number regeneration on survival, growth rates, energy alloca- of eggs in polyps adjacent to the regenerating lesions tion and fitness (Meesters et al. 1992, 1994, Meesters & was significantly reduced. Relevant to the above stud- Bak 1993, Van Veghel & Bak 1994, Ward 1995, Kra- ies is the argument that, among organisms frequently marsky-Winter & Loya 1996 and literature therein). damaged as a result of physical circumstances, natural Available energy is often limited and must be selection should favor repairhegenerative processes divided between several biological functions, such as above other requirements (Karlson 1988). repair, maintenance, reproduction and somatic growth. The accepted paradigm of energy trade-off is based One important facet of this general idea is the concept on controlled field studies. However, this does not nec- of optimizing energy allocation to reproduction during essarily mean that the interpretation is inevitably cor-

O lnter-Research 1996 Resale of full article not permitted 298 Mar Ecol Prog Ser

rect. No study has yet identified how energy resources viding most of their energy requirements, including are channelled between the 'competing' b~ological maintenance, tissue and skeletal growth, reproduction functions nor how energy trade-offs are activated. and also reserves (Muscatine & Porter 1977, Muscatine The enigma. Three unrelated lines of argument et al. 1981, 1984, Rinkevich 1989). Consequently, obtained from cnidarians critically challenge the above corals may maintain high quantities of lipids in their paradigm that reproduction and regeneration in dam- tissues, either as structural or as storage materials, for a aged corals compete for the same limited amount of variety of purposes (Patton et al. 1977, Stimson 1987). energy budget. Much interest has been devoted to the energy inter- (1) Sexual reproduction in corals may not be subject actions between zooxanthellae and the coral host. In to energy constraints. Although much evidence in the shallow water branching coral colonies, Muscatine et literature points to energy trade-off between sexual al. (1984) found that the carbon translocated to the host reproduction and various biological functions, other was > 140 % of its daily energy requirements. By using studies show that reproduction may also be expressed a different scientific approach, Davies (1984, 1991) and independently of energy constraints. This has been Edmunds & Davies (1986) calculated for 5 reef corals recorded in corals, in a variety of other cnidarians (Tar- that on a cloudless day the energy input of the translo- dent 1985) and . For example, while growth cated carbon is in excess of that required. Intake of rates of many coral slowed down after the zooplankton or particulate organic matter may onset of sexuality (references cited in Chornesky & increase the total die1 carbon input. The surplus Peters 1987), growth rates of female Porites astreoides energy may be stored for future needs, which include colonies increased concurrently with the onset of sex- reproductive activities (Rinkevich 1989, Harrison & ual reproduction (Chornesky & Peters 1987). Polyps of Wallace 1990) and repair. These results indicate the Monastrea annulans in mid-colony locations, includ- potential error of applying a general theory of energy ing both fast-growing tips of knobs and slower-grow- trade-offs (Kozlowski & Wiegart 1986, Roff 1992) to ing flat areas, displayed similar reproductive activity field observations on reproduction and regeneration in (Szmant 1991). Studies done on barnacles and fishes hermatypic corals. No study has, as yet, clearly docu- (reviewed in Roff 1992) further indicate that although mented that shallow water scleractinians are always sexual reproduction is a 'costly' biological function, it is prone to energy constraints, not even during regenera- sometimes independent of growth or body weight. In tion. This conclusion does not hold for shallow water the same way, very small, sexually mature colonies of corals under chronic stress conditions (i.e. Szmant & the ascidian Botrylloides sp., the remnants of larger Gassman 1990, Allison et al. 1996). colonies that had died, show no change in reproduc- (3) Regeneration is a regulated process, not related tive effort (Rinkevich et al. 1993). to energy trade-off.If regeneration is not an energy- Energy allocation to various biological functions in limited phenomenon, but is a 'preset' independent corals may be hierarchical (Harrison & Wallace 1990) process, one may expect to detect events which are and programmed, where sexual reproduction may correlated only to the repair operation. Moreover, if take precedence over other functions, such as growth regeneration does not deplete the coral's energy and maintenance, or vice versa. Studies on corals have resources below some threshold, we may find cases shown the effects of regeneration on reproductive where coral colonies are able to meet other demands activities (Kojis & Quinn 1985, Rinkevich & Loya 1989, during the regeneration process, such as growth and Van Veghel & Bak 1994), the effect of sexual reproduc- reproduction. Twelve such representative studies were tion on growth rates (Kojis & Quinn 1981, 1985, Harri- employed on 1 medusa, 2 sea anemones, 2 gorgonians son & Wallace 1990, Ward 1995), the effect of intraspe- and 7 scleractinian corals (Table 1).In 3 studies, it was cific competition on growth rates and reproduction shown that energy constraint had no significant role in (Rinkevich & Loya 1985), and regeneration versus regeneration, and in 1 case such correlation was pro- growth rate or pattern formation interrelationships posed. In 2 studies (Wahle 1983, Ward 1995; Table 1) (Kobayashi 1984, Meesters et al. 1994, Kramarsky- reproductive efforts were clearly not correlated with Winter & Loya 1996). These studies may support the energy trade-off for regeneration. In 6 studies, regen- energy trade-off idea, but may also be intepreted as eration was proposed to be associated with or con- showing a preset hierarchy of biological functions. trolled by cellu1a.r elements (Young 1974, Lang da Sil- (2) Shallow water scleractinians may not be prone to veira & Van't Hof 1977, Patterson & Landolt 1979, energy constraints. In reef building corals, sources for Wahle 1983, Lesh-Laurie et al. 1991, Kramarsky-Win- energy inputs are primarily photosynthates translo- ter & Loya 1996; Table 1).In 2 studies (Bak & Steward- cated by zooxanthellae and food particles captured by Van Es 1980, Bak 1983; Table l) the recovery of dam- tentacles and cilia. The zooxanthellae translocate a aged tissue slowed down with time, a result which may variety of 0rgani.c compounds to the host corals, pro- indicate the depletion of resources other than energy Rinkevich: Energy allocation in damaged corals 299

Table 1 Representative list of studies on regeneration in the Scyphozoa and . Analysis of the results indicates that tissue repair is a complex and highly regulated process, not necessarily related to energy constraints. + means regeneration is controlled by cellular elements; na: no data available

Organism Relevant results on tissue regenerat~on Evldence or proposed role Source studied in regeneration for: Cellular Energy elements resources

A urel~a Isolated tentacles regenerated, complete No limitation Lesh-Laurie et al. (1991) aurjta polyps Calliactis Influx of arnoebocytes into the wound Young (1974) parasitica Anthopleura Wound repair starts with rapid influx of cells + n a Patterson & Landolt elegantissima derived from arnoebocytes in the rnesoglea (1979) Plexa ura Regeneration rate was independent of Proposed No limitation Wahle (1983) homomalla either colony size or reproductive phase Plexaura Repeated injuries caused a decrease in na Lang da Silveira & flexuosa regeneration Van't Hof (1977) Pocillopora Fragmented corals had no significant No limitation Ward (1995) damicornis change in growth rate or lipids but had increased reproductive effort Porites No influence on lesion regeneration, whether No limitation Meesters et al. (1992) asteroides it was positioned at the top or at the colony side, where 70% less light was recorded Mon tastrea Regeneration is influenced by tissue bor- Proposed Meesters et al. (1994) annularis dering the damaged area (lesion perimeter, and literature cited not lesion size or colony size) therein A cropora Recovery of damaged tissue slows down - Bak (1983) palmata with time Agaricia agarici- Recovery of damaged tissue slows down Bak & Steward-Van Es tes and Porites with time. This is a 'physiological char- (1980) astreoides acterist~c'of the corals Fungia scutaria Mesenterial filaments which do no contain Proposed No limitation Krupp et al. (1993). and other all tissue elements fail to regenerate Kramarsky-Winter & fungiid corals Loya (1996)

or which may be a physiological characteristic of the such as regeneration, pattern formation, reproduction repair process in corals (Bak & Steward-Van Es 1980). and growth, are characterized by 'preset' regulated There are other studies which indicate that regener- processes that are not influenced directly through ation in corals is a complex and highly regulated changes in other biological functions. process. In Acropora palmata, regeneration along a The proposed theorem. Cumulatively, the studies branch from tip to base at the first 25 cm was associ- discussed above do not meet with the assumptions of ated with tissue senesence (Meesters & Bak 1995). In the paradigm that regeneration and sexual reproduc- Goniastrea favulus, fragmented old colonies were tion in corals are related through energy trade-off. more fecund than young colonies of the same colony Several studies showed a reduction in reproductive size (Kojis & Quinn 1985). Growth rates of Porites activities during regeneration (Kojis & Quinn 1985, astreoides female colonies increased over the size Szmant-Froelich 1985, Rinkevich & Loya 1989, Van range associated with the onset of reproduction, Veghel & Bak 1994, Ward 1995) and documented vari- instead of decreasing (Chornesky & Peters 1987). In ations in reproduction related to localized regions of fungiid corals (Kramarsky-Winter & Loya 1996 and lit- growth (Rinkevich & Loya 1979, 1989, Oliver 1984, erature therein) coral fragments retaining part of the Heyward & Collins 1985, Wallace 1985, Kojis 1986, parental mouth regenerated around the original mouth Harrison & Wallace 1990). However, the studies dis- and did not develop buds, as opposed to fragments iso- cussed here (Kojis & Quinn 1985, Chornesky & Peters lated from the animals' periphery. These findings fur- 1987, Meesters & Bak 1995, and references in Table 1) ther indicate that basic biological functions in corals, may also suggest that, if there is any deprivation of a 300 Mar Ecol Prog Ser

resource, reproduction and regeneration processes in with deflned interstitial cells (reviewed in Young normal, unstressed corals may be competing for some- 1974), cases of regenera.tion in hydroz0an.s will not be thing other than energy. discussed here. Growth, tissue repair and production of the germ At least 2 studles, on Calliactis parasitica (Young cells require 1 major resource, the stem cells. The out- 1974) and Anthopleura elegantissima (Patterson & put of new and different types of cells, in the right Landolt 1979), have recorded that wound repairs start numbers and at the right time, is central to the mainte- with rapid influx of cells derived from amoebcytes in nance of the adult animal. One of the central Issues in the mesoglea. However, no mitotic increase has been this field is the determination of the factors that regu- observed in the mesoglea or in the endoderm after late the activity of the stem cells. Commitment of prog- wounding (Young 1974). This points to the route of dif- enitor cells to different types of somatic cells or to ferentiation of amoebocytes to ectodermal and endo- either soma or germ cells may also be influenced by dermal cells, and to a pool (probably small) of reserved environmental factors (Wolpert 1988). In regenerating cells in the mesoglea that are available for immediate planarian worms, male germ cells take part in response. Thus we may re-analyze the results of Lang blastema formation and are then capable of redifferen- da Silveira & Van't Hof (1977), who found that tiating into somatic cells. The more mature male germ repeated injuries caused a decrease in regeneration in cells degenerate (literature cited in Gremigni et al. Plexaura homomalla, as the depletion of this pool of 1982). In the round worm Caenorhabditis elegans, a cells, and the results of Meesters et al. (1994), who single cell located at the distal tip of each end of the found that regeneration in Montastrea annularis was gonad may prevent formation of sex cells. When it is influenced by the tissue bordering the damaged area, destroyed, all nearby nuclei carry out meiosis and form and not by lesion size or colony size, as the conse- gametes, irrespective of energy allocation (Austin & quence of an available 'front line' for stem cell wan- Kimble 1987). In Hydra spp., germ and somatic cells dering. In a similar way, the results of Bak (1983) and are produced from the same stem cells (Tardent 19851, Bak & Steward-Van Es (1980), who recorded a slow- and environment rather than lineage plays the major down with time in the recovery of damaged tissue in role in determining the fate of stem cell progeny. Spa- Acropora palrnata, may be due to a depletion of tial variation in the distribution of various differenti- reserve cells. The results of Meesters & Bak (1995), ated cell types is the consequence of local stem cell who recorded that regeneration along a branch of commitment (reviewed in Hall & Watt 1989, Bode A. palmata decreased significantly from tip to base, 1996). may be due to the accumulation of stem cells in the fast The importance of stem cells in coral regeneration growing tip. The importance of cellular components in has already been discussed more than once. Lang da regeneration processes over shortage of energy Silveira & Van't Hof (1977) claimed that repeated resources was also demonstrated. In Aurelia aurita cycles of injuries and regenerations in Plexaura flex- polyps, isolated tentacles are capable of regenerating ousa can inhibit future regeneration by depleting a whole new polyps by cell profileration and reorganiza- critical population of self-renewal stem cells. This idea tion (Lesh-Laurie et al. 1991). In the solitary corals Fun- was also discussed favorably by Wahle (1983), who gia spp., fragments containing all cell types success- examined the influence of regeneratlon on 3 Jamaican fully regenerate, as opposed to fragments containing gorgonians and found that regenerat~onwas ~ndepen- only endodermal cells (Krupp et al. 1993, Kramarsky- dent of either colony slze or reproductive phase. Winter & Loya 1996). Szmant-Froelich (1985) proposed that gametogenesis In reef corals, therefore, there must be a reserve of and budding processes in corals may interact through cells able to migra.te to wounds, to fast growing parts competition for 'interstitial cells', as was demonstrated and to areas where germ cells are developed. These in Hydra spp. [reviewed in Bode 1996). In at least 6 cells are also available to other basic biological func- studies (Table l), evidence for cellular elements In tions, such as rep1acemen.t of senescent cells and para- cnidarian regeneration was discussed. sitic elimination. However, no high mitotic rate of these While some studies have suggested that all cnidarian cells has ever been recorded (Young 1974, Lang da Sil- germ cells develop from interstitial cells (reviewed in veira & Van't Hof 1977, Pa.tterson & Landolt 1979). Any Campbell 1974, Tardent 1985), many other studies extensive use of those reserve cells (in repeated indicate that true interstitial cells are missing in the injuries, fast growth, during regeneration, sexual Scyphozoa and Anthozoa. Amoebocytes, mainly in the reproduction wi.th tissue repair, etc.) may reduce their mesoglea, serve as the stem cells (reviewed in Robson numbers and significantly affect one or more of the 1957, Chapman 1974, Young 1974, Larkman 1981, other biological functions. A similar situation, termed Fadlallah 1983) Since Scyphozoa and Anthozoa lack 'exhaustion', was proposed for results in the mam- the extensive regenerative powers of the Hydrozoa malian system showing immune unresponsiveness to Rinkevich: Energy allocation in damaged corals

antigens that should elicit strong responses (Mosko- Gremigni V, Nigro M, Pucc~nelli1 (1982) Ev~denceof male phidis et al. 1993, Rocha et al. 1995).Partial deletion of germ cell redifferentiation into female germ cells in pla- reactive i.mmune cells temporarily reduces the ani- narian regeneration. J Embryo1 Exp Morph01 70:29-36 Hall PA, Watt FM (1989)Stem cells: the generation and main- mal's responsiveness to xenogeneic challenges. tenance of cellular diversity. cvDevelopment 106:619-633 The idea that under conditions of regeneration there Harrison PL. Wallace CC (1990) Reproduction, dispersal and is a conflicting demand for increasing the number of recruitment of scleractinian corals. In: Dubinsky Z (ed) depleted stem cells versus increasing the rate of differ- Coral Reefs. Elsevier, Amsterdam, p 133-207 Heyward AJ, Collins JD (1985) Growth and sexual reproduc- entiation from stem cells IS not new (Lajtha 1979) and tion in the scleractinian coral Montipora digitata (Dana) the process of competition for precursor cells in Hydra Aust J Mar Freshwat Res 36:441-446 spp. regeneration has recently been proposed (Miiller Karlson RH (1988) Size dependent growth in the zoanthid 1995). Evidence in the literature has already pointed species: a contrast in clonal strategies. Ecology 69. out that, as a result of such competition between stem 1219-1232 Kobayashi A (1984) Regeneration and regrowth of frag- and differentiated cells, the production of differenti- mented colonies of the hermatypic corals Acropora for- ated descendants becomes limited (Lajtha 1979). It is, mosa and Acropora masuta. Galaxea 3:13-23 therefore, proposed here that a trade-off for stem cells Kojis BL (1986) Sexual reproduction in Acropora (Isopora) between tissue repair and sexual reproduction should species (Coelenterata- ) I. A. cuneata and A. palifera on Heron Island reef, Great Barrier Reef. Mar Biol be considered when we study changes in reproductive 91:291-309 activities during regeneration in reef corals. Kojis BL, Quinn NJ (1981) Aspects of sexual reproduction and larval development in the shallow water hermatypic coral, Acknoruledgements. This study is part of the research done in Gonjastrea australensls (Edwards and Haime, 1857). Bull the Minerva Center for Marine Invertebrate Immunology and Mar Sci 31558-573 Developmental Biology and was also supported by EC grant Kojis BL, Quinn NJ (1985) Puberty in Goniastrea favulus: age (INCO) no. ERB3514 PL950184. I thank U. Frank, N. Hall, T or size limited? Proc 5th Int Coral Reefs Congr 4:289-293 Hughes and H. M Szmant for critically reading this paper. Koz1owsk.i J. Wiegert RG (1986) Optimal allocation of energy to growth and reproduction. Theor Popul Biol 29:16-37 Kramarsky-Winter E. Loya Y (1996) Regeneration versus bud- LITERATURE CITED ding in fungiid corals: a trade-off. Mar Ecol Prog Ser 134: 179-185 Alllson N,Tudhope AW, Fallick AE (1996)Factors influencing Krupp DA, Jokiel PL, Chartand TS (1993)Asexual reproduc- the stable carbon and oxygen isotopic composition of tion by the solitary scleractinian coral Fungia scutaria on Porites lutea coral skeletons from Phuket, south Thailand. dead parent coralla in Kaneohe Bay, Oahu, Hawaiian Coral Reefs 1543-57 Islands. Proc 7th Int Symp Coral Reefs 1:527-534 Austin J, Kimble J (1987) glp-l is required in the germ line for Lajtha LG (1979) Stem cell concepts. Differentiation 14:23-34 regulation of the decision between mitosls and n~eiosisin Lang da Silveira F, Van't Hof T (1977) Regeneration in the C. elegans. Cell 51589-599 gorgonian Plexaura flexuosa (, Octocorallia). Bak RPM (1983) Neoplasia, regeneration and growth in reef Bijdr Dierk 47:99-108 building coral Acropora palmata. Mar Biol77:221-227 Larkman AU (1981) An ultrastructural investigation of the Bak RPM, Steward-Van Es Y (1980) Regeneration of super- early stages of oocyte differentiation in Actinia fragacea ficial damage in the scleractinian corals, Agaracla agar- (Cnidana: Anthozoa). Int J Invert Reprod 4:147-167 ~,E purpurea and Porltes astreoides. Bull Mar Sci 30: Lesh-Laurie GE, Hujer A, Suchy P (1991) regeneration 883-887 from isolated tentacles of Aurelia scyphistomae: a role for Bode HR (1996) The interstitial cell llneage of hydra: a stem gating mechanisms and cell division. Hydrobiologia cell system that arose early in evolution. J Cell Sci 109: 216/217:91-97 1155-1164 Meesters EH, Bak RPM (1993)Effect of coral bleaching on tis- Campbell RD (1974) Cnideria. In: Giese AC. Pearse JS (eds) sue regenerating potential and colony survival. Mar Ecol Reproduction of marine invertebrates 1 Academic Press, Prog Ser 96189-198 New York, p 133-199 Meesters EH, Bak RPM (1995) Age-related deterioration of a Chapman DM (1974) Cniderian histology In: Muscatine L, physiological function in the branching coral Acropora Lenhoff HM (eds) Coelenterate biology, reviews and new palmata. Mar Ecol Prog Ser 121:203-209 perspectives. Academic Press, New York, p 2-92 Meesters EH, Bos A, Gast GJ (1992) Effects of sedimentation Chornesky EA. Peters EC (1987) Sexual reproduction and and lesion position in coral tissue regeneration. Proc 7th colony growth in the scleractinian coral Porites astreoides. Int Coral Reef Symp 2:671-678 B101 Bull 172 161-177 Meesters EH, Noordeloos M, Bak RPM (1994) Damage and Davies PS (1984) The role of zooxanthellae in the nutritional regeneratlon. Links to growth in the reef building coral energy requirements of Pocillopora eydouxi. 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This note was submitted to the edilor Manuscnpt first received- May 17, 1996 Revised version accepfed. September 12, 1996