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Nutrient and energy allocation during arm regeneration in Echinaster paucispinus (Clark) (Echinodermata; Asteroidea)
Journal of Experimental Marine Biology and Ecology
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
180 (1994) 49-58
Nutrient and energy allocation during arm regeneration in Echinaster paucispinus (Clark) (Echinodermata; Asteroidea) Michael T. Lares”, John M. Lawrence
Received 14 September 1993; revision received 28 January 1994; accepted 25 February 1994
Abstract
individuals of Echinctsrerpaufispinu.r (Clark) were either intact or had two arms amputated, and fed a sub-maintenance ration of food. After 7 months, the new arm was 17”, the radius of the intact arm. This rate of regeneration is much lower than that of other species of asteroids fed similar food levels. The greater amount of protein in the body wall of Echirrasterpaucispinits may be responsible. Gonadal growth occurred in both intact and regenerating individuals with an overall decrease in size of the pyloric caeca. Allocation to reproduction takes precedence over the deposition and retention of nutrient stores. Regenerating individuals gained energy (kJ), while intact individuals lost energy. This difference may result from a combination of higher food levels/individual and more efficient food utilization and decreased maintenance requirements (especially of body wall). This leads to more energy available for growth. Asteroids in general, show similar responses in allocation to the disturbance of arm loss and the stress of sub-optin~ai food. The stress-tolerant species, E~hi~~sfer pauci,spinus, has a slow rate of arm regeneration. Keywords:
Asteroidea;
Echinodermata;
Regeneration
1. Introduction
The capacity to regenerate lost body parts is considered characteristic of echinoderms (Hyman, 19.55; Swan, 1966; Emson & Wiikie, 1980). The loss of a body component constitutes disturbance (Grime, 1977; Sousa, 1984; Pickett et al., 1989), and may represent a significant cost to the individual. In asteroids, the loss of an arm can result in decreased locomotion and foraging efficiency (Lawrence, 1991b). Since the arms contain the pyloric caeca and gonads, nutrient storage and reproductive output * ~~rr~spondin~ author. 0022-0981!94/$7.00 0 1994 Elsevier Science B.V. All rights reserved SSDl OO’Z-09X1(94)00038-F
50
M. T. Lares. J.M.
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Ed.
180 (1994) 49-58
are decreased (Lawrence et al., 1986; Lawrence, 1991b). The energy required to replace body structures is a further cost of arm loss. A decrease in production constitutes stress (Grime, 1977) and can occur when food is limited (Lawrence, 1991a). With limited food, there may be trade-offs between regeneration and other energy uses, such as reproduction (Ebert, 1982). Allocation of energy to regeneration in the asteroid Luidia clathrata depends on food level. With a low level of food available, allocation is to the pyloric caeca and gonads of intact arms only (Lawrence et al., 1986); with a high level of food availability, allocation is to both the intact and regenerating arms (Lawrence & Ellwood, 1991). The pattern of allocation of energy to regeneration may be expected to vary among species of asteroids of different body forms and life-history characteristics. Luidia clathrata is a member of the order Paxillosida (Clark & Downey, 1992) is a voracious infaunal predator (Lawrence & Dehn, 1979; McClintock, 1984) and has an arm structure that lends itself easily to breakage (Clark & Downey, 1992). The body form of Luidia provides support and flexibility at the expense of armor (Blake, 1989). A species with this body form would be expected to have a high incidence of arm loss (Lawrence, 1991b). Up to 86p,,, of individuals of Luidia cfathrata in a population have arm loss (Lawrence & Dehn 1979). Luidia clathrata has been suggested to have a life-history strategy (C-R-S) associated with a relatively high capacity to obtain food and potential for arm loss (Lawrence, 1990). In contrast, Echinaster paucispinus is a member of the order Spinulosida (Clark & Downey, 1992) is an epifaunal browser (Ferguson, 1969), and has a robust body structure (Clark & Downey 1992). This body form gives flexibility with sturdiness, and restricts predatory abilities (Blake, 1989). Few Echinaster spp. show arm loss (Lawrence, unpubl.). Echinaster paucispinus has been suggested to have a life-history strategy (stress-tolerant) associated with a relatively low capacity to obtain food and potential for arm loss (Lawrence, 1990). Species with different life-history strategies may show different responses to the stress of low food availability and to the disturbance from arm loss. The objective of this study was to examine the response of Echinasterpaucispinus (Clark) to arm loss and low food availability.
2. Materials and methods Echinasterpaucispinus were collected from hard bottom substratum (N 10 m depth) off Egmont Key (27” 35’ N; 82” 46’ W), Florida on 22 September 1990, transferred to laboratory aquaria at 30%, S and 20 “C, and allowed to adjust to these conditions for 1 wk. Individuals were weighed and the radius (R; center of disc to the ray tip) measured. They were divided into two groups (n = 9/group). Two non-adjacent arms were removed from the individuals in one group. The proximate composition of amputated arms was assumed to be representative of both groups and were analyzed to characterize the two groups at time zero. The amputated individuals and a group of intact individuals were equally divided between two laboratory aquaria to decrease the possibility of an aquarium effect, and fed a sub-maintenance ration of 2-3 clams (Donax variabilis) per individual every 2 days. Seastars were placed directly on the clams to
M. T. Lares. J.M. Lawrence I J. hp.
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180 (19941 49-58
51
increase the probability that equivalent amounts were eaten. As the regenerating individuals had two fewer arms, they received more food per unit weight than the intact ~ndividua~s. After 7 months, all seastars were weighed, measured, and the arms dissected into components (body wall, pyloric caeca, gonads). The stomach was not included as it is relatively small. Regenerating and intact arms of amputated individuals were dissected and analyzed independently. The indices of the arm components (body wall, pyloric caeca and gonads) were calculated as percentages of the dry weight (Giese & Pearse, 1974). Arm components were dried over sulfuric acid in a vacuum desiccator, weighed, ground in a Wiley Mill and analyzed for proximate composition (total organic material, soluble and insoluble protein, total lipid, total carbohydrate) (Lawrence, 1973). Tissues were pooled when sufficient tissue was not available for individual analysis (viscera of regenerating arms, testes of intact and regenerating individuals). The non-extractable Table 1 Radius (mm) and dry weights (g) of arm components for all arms Group: Date: Arm:
Radius
Intact individuals 29 Sept. 1990 Intact 67k la (9)
Dry weight Single arm Body wall
1.23 + 0.08a (9)
Pyloric Caeca Ovaries
0.17 +_0.02a (9) 0
of Echinasterpatrcispi~2usin single arms and calculated
Intact individuals 2 May 1991 Intact 59+ lb (9)
I.11 i0.09a (9)
0
6.16 5 0.39a (9)
Pyloric Caeca Ovaries
0.86 + 0.36a
(9)
0.28 $: 0.02b (9)
0.08 k O.Olb
0.01 i. O.Olc
(9) 0.04 2 0.02a
(9) 0.01 _+O.Olb
0.009 & 0.013
5.57 + 0.46a (9)
(4) 0.004~0.0013 (5)
0.003 $. O.OOia (5)
(9)
0.5 1 f 0.06b
0.26 & O.Qlc
(9) 0.18 f 0.04a
(9) 0.14 i: 0.04a
0
0.05 + 0.03b (3)
(4)
3.97 + 0.26b
(9) 0
(6) Testes
1.14 & 0.080
10 + 0.1 (9)
(9) 0.04 * O.Ola
(3) All arms Body wall
59 ?: lb (9)
Regenerating
0.10 +O.Olb
(6) Testes
Regenerating individuals 2 May 1991 intact
(4) 0.02 -+ O.Olb (5)
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. 4. 1 SE and (n) are given. Values in a row with the same letter are not significantly different (p> 0.05).
52
M. T. Lares. J.M. Luwrence
/J. E.up. Mar. Bid. Ed.
180 (19941 49-58
material of body wall, pyloric caeca and ovaries is considered insoluble protein (Lawrence & Kafri, 1979). The energetic composition of body wall, pyloric caeca and ovaries was calculated by multiplying by the calorific equivalents of Brody (1945). As the DNA in the testes was not measured, the energetic composition of the testes was not calculated. Treatments were compared using a one way ANOVA, in conjunction with Baye’s Exact Test multiple comparison procedure (Steele & Torrie 1988). Percent composition data were transformed using an arcsine square root transformation before statistical analysis. Untransformed data are presented in the results. In all cases, significance was determined at the 5”, level.
3. Results The wounds of amputated arms closed by muscular action and were healed completely z 3 wk after amputation. All individuals showed negative growth over the experimental period, as the radius and the dry weights of the body wall and pyloric caeca of both intact and regenerating individuals decreased (Table 1). The decrease in the radius and pyloric caeca was significant, but not significantly different between the intact and regenerating individuals. Small amounts of gonads developed in both intact and regenerating individuals. The body wall indices of intact arms of both intact and regenerating individuals did not change significantly. The regenerating arms had a slightly but significantly higher body wall index than intact arms of initial or intact individuals, but not of intact arms of regenerating individuals (Table 2). The pyloric caeca index of intact arms of intact and regenerating individuals decreased significantly, and were significantly higher than
Table 2 Indices (“<>dry weight) of arm components Group: Date: Arm: Body wall
Pyloric Cacca Ovaries
Testes
Intact individuals 29 Sept 1990 Intact
of Echinasrer pauckpirtus in a single arm Intact individuals 2 May 1991 Intact
Regenerating individuals 2 May 1991 Intact
88 2 3a
9Oi3a
92 _t 3ab
(91
(91
(91
12_t3a (91 0
0
8 5 2b
6+ lb
(91 3k la
(91 3 + 2a
(61
&t-
1 f la (31
Regenerating
0.3 2 0.2a (51
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. 4, 1 SE and (n) are given. Values in a row with the same letter arc not significantly different (p>O.O5).
M. T. Lures. J.M.
Lawrence
; J.
E.xp. MIX.
Biol. EA.
53
180 119941 49-58
the pyloric caeca index of regenerating arms. The indices of the ovaries and testes did not differ significantly. Some major changes in the proximate constituents are apparent (Table 3). Most important is the decrease in the concentration of lipid in the pyloric caeca. The decrease was statistically significant in intact arms of regenerating individuals, but not in intact individuals. The concentration was low in the pyloric caeca of regenerating arms, but there was insufficient material for statistical analysis. The other notable difference is the similar and significantly higher concentration of ash and lower concentration of nonextracted organic material (probably protein) in the body wall of intact arms of both intact and regenerating individuals than those of regenerating arms. The kJ/g dry weight of the body wall, pyloric caeca and ovaries of the arms were not significantly different between initial. intact and regenerating individuals (Table 4). The Table 3 The proximate
composition
(“, dry weight) of body components
of Echirmter
puucispimo
Ash
Carbohydrate
Lipid
Soluble protein
Nonextracted material
,,
Intact arm Body wall Pyloric caeca
57.1 f 1.7a 8.7 i 0.9a
0.7 +O.la 1.7 f O.?a
2.6 &0.2a 17.7 + 0.9a
24.1 f_ 1.6a 53.2 & 1.8a
15.6 f 2.4, 18.8 5 2.2a
9 9
It~tcr<,tir~diiriduuk 7 Ma\ Intact arm Bad\ wall Pyloric caeca Ovaries Testes
56.0 f I .4a 9.5 f 0.3a 5.6 +_0.3a 8.05
0.6 f O.la 4.0 f 0.4a 0.7 + 0. la 0.9
3.1 f 0.3a 15.9 f 0.4, 48.5 + 1.8a 8.2
28.7 k l.3b 50.2 2 0.8a 40.9 2 l.Oa 41.5
11.6 & 2.5a 20.5 + 0.8a 4.3 +O.la 41.4
9
60.9 + 1.8a 9.8 f 0.4a 5.2_+0.la 17.3
0.5 &0.03a 4.0 *0.3a 0.8_+O.la I.5
2.5 k 0.2a 13.2 & l.4b 45.9 _+6.0a 10.9
24.0 f l.8a 49.1 f 1.7a 41.7 _+3.2a 47.8
12.2 + 2.4a 23.9I2.la 6.5 k 3.2a 2.6
9 9 4
50.0 + 3.7b 10.10 3.89 12.99
0.5*0.la 3.1 0.8 2.8
2.7 &0.2a 14.0 44.2 14.5
22.6 -+ 1.7a 44.2 44.3 54.3
24.4 + 2.8b 28.6 6.8 15.5
lntucr it~di~idmrls ZY Sept.
9
5
Re,qenercrritr,q individuh 2 Ma,
Intact arm Body wall Pyloric acaeca Ovaries Tcstcs Re,qerrerutitl,q urm
Body ~a11 Pyloric caeca Ovaries Testes
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. The non-extracted organic material is considered to be protein in the body wall. ovaries, and pyloric caeca and to be protein and DNA in the testes. 4 and I SE are given. Values for each body component in a column with the same letter arc not significantly different (p>O.O5).
54
M. T. Luves. J.M. Luwretlce /J. Eup. Mur. Biol. Ecol. 180 (19941 49-54
Table 4 The energetic composition (kJ;arm, Ethimrteu pul~~.i.~~iFI~4~~
kJ/individual,
and kJ!g dry weight) of the arm components
of female
kJ/arm
kJ/individual
kJ/g dry wt
II
29 Sept. Intact arm Body wall Pyloric cacca 13
128 + 523 46*6a 174
638 + ‘la 209 + 3na 847
11 + 0.43 24 * 0.2a 36
9 9
Irrt~~c’tBidi~~i&ml.~ 7 blay Intact arm Bodv wall Pyktric caeca Ovaries E
121*11a 24 f 3b 13+2a 158
603 + 52a 12Oi 14b 61*12a 184
Ii + 0.3a 24*0.ia 30 t osa 65
9 9 5
Regetlercr fing individuth 2 Ma) intact arm Body wail Pyloric caeca Ovaries z
108 + 6a 1822b 13+5a 139
324k 19b 39 i 14a 419
10 + 0.4a 23 + 0.3a 3OA la 63
9 9 3
68 * lc 22 30 120
12+ la 23 30 65
9
Itrtucr indivithtuls
Regenemtirlg urm Body wall Pyloric cacca Ovaries z
34+3b 11 15 60
56&hC
2 1
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. Z and 1 SE are given. Values for each body component in a column with the same letter are not significantly different t,p> 0.05).
negative growth of the body wall and pyloric caeca resulted in a decrease in the kJ/ arm and kJ/individual (Table 4). Intact females lost 63 kJ (796 of the original) over the seven-month experiment, while regenerating females, which were fed more, gained a small amount, 17 kJ (3:; of the original).
4. Discussion Hyman (1955), Anderson (1965) and Swan (1966) stated without documentation that regeneration in asteroids is a slow process. Lawrence (1991b) concluded that this is true under low food conditions. In Eckinaste~paucispiizus wound healing and appearance of the new arm rudiment took z 3 and 4 wk, respectively. After 7 months, the new arm was z 17’!,; the size (R) of the intact arm. Asteriusfivbesi regenerates an arm bud in
M. T. Lares. J.M. Luwrence / J. Exp. Mar. Bid. Ed.
180 (I 9941 49-58
55
1 wk (Donachy et al., 1990). In Luidia clathrata on low levels of food, the arm rudiment appears in z 1 wk and grows to 1496 the length of an intact arm in one month (Adams, 1991). In contrast, the regenerating arms of Luidia clathrata fed abundant food grows to 703; the length of an intact arm in 5 months (Lawrence & Ellwood, 1991). Therefore, the rate of regeneration of the new arm varies with taxa, and food level. Because of their low capacity for production, species with a stress-tolerant life history strategy should have well developed protection from disturbance (Grime, 1977). If these defenses are well developed, little arm loss would be expected, as observed in Echinaster paucispims (Lawrence unpubl.). Blake (1989) noted the body form of the echinasteroid group provides sturdiness and protection from arm loss. Therefore, arms that are strong structurally are not lost easily or replaced rapidly (as in Echinaster paucispinus), and arms that are weak structurally are lost easily, and replaced quickly (as in Luidiu clathrata). Stress-tolerators have less relative rates of growth (Grime, 1977). As regeneration involves production, a stress tolerant species should replace and grow a lost arm slowly. Regenerating Echinasterpaucispinus in this study produced z 2.4 kJ/month, while regenerating Luidia clathrata produced 3.4 kJ/month (Adams 1991). Because of differences in feeding and size of individuals in these two studies, it is difficult to make conclusions on this difference in production. Gonads developed to the same extent in intact and regenerating individuals of Echinasterpaucispinus with a decrease in the size of the pyloric caeca. This suggests that gonadal production is taking precedence over deposition of nutrient reserves. Gonadal production occurs at the expense of somatic production on low food level in Luidia clathrata (Lawrence, 1973; Dehn, 1980, 1982; George et al., 1991) and Sclerasterias wollis (Xu & Barker, 1990). In contrast, starved Pisaster gigalzteus allocates material to the pyloric caeca over the gonads (Harrold & Pearse, 1980); Asterias rubens, under starvaticn or from impoverished areas gives priority to the body wall over both the pyloric caeca and the gonads (Jangoux & van Impe, 1977; Nichols & Barker, 1984). These variations in allocation appear directly related to food level. When little or no food is available, somatic development in the body wall or pyloric caeca takes precedence over gonadal development. With maintenance or sub-maintenance levels of food, gonad development occurs at the expense of somatic tissues; with abundant food, simultaneous allocation to somatic and reproductive tissues occurs. In general, the proximate composition of the body components of Echinaster paucispirzus is similar to that of other asteroids (Lawrence & Guille, 1982; Lawrence, 1987; McClintock et al., 1990a,b), and Echinaster type I at the same time of year (Scheibling & Lawrence, 1982). However, the concentration of soluble protein in the body wall of Echinasterpaucispinus is twice that of Luidia clathrata (McClintock et al., 1990b: Adams 1991). Echinaster paucispinus may grow arms slower than Luidia clathrata as more protein needs to be deposited in the body wall. There was a higher concentration of insoluble protein and lower concentration of ash in the body wall of regenerating arms of Echinasterpaucispinus. This suggests Emson’s proposal that growth of echinoderm body wall requires little energy may be incorrect (Emson, 1984). His hypothesis would have been supported if the same amount of protein were present in intact and regenerating arms. The basis for the production of energy and growth of the new arm may be similar
56
M. T. Lures. J.M. Lawrence j J. Esp. Mur. Biol. Erol. 180 (1994) 49-58
to that suggested by Adams (1991). Regenerating individuals in this and Adams’ study received more food/weight basis than intact individuals (1.5 and 1.2 f&d more, respectively). They may also have been more ef&ient in its use. This emphasizes the importance offeeding a weight-based (rather than an individual-based) ration in studies on regeneration. Additionally, regenerating individuals have less maintenance costs as the amounts of body wall and pyloric caeca are less, and should be able to allocate a larger proportion of their food resources towards new growth (Adams, 199 1). Consequently, the energy for regeneration may COEXas a resuft ofincreased food levets and/or reduced maintenance needs in regenerating individuals. The evidence here, and studies on Luidia ctathrata, strongly suggest that nutrient level determines the allocatiou of material to regeneration in asteroids. Some regeneration occurs even under starvation conditions (Lawrence et al., 19X6), indicating that the process is important. On sub-maintenance levels of food, regeneration is slow and alfocation is primarily to existing arms (Lawrence et al., 1986; this study). Rapid rates of regeneration, with simultaneous aflocation of energy to intact and regenerating arms occur with abundant food (Lawrence & Ellwood, 1991). The main difference between species of asteroid with different life history strategies to the disturbance of arm loss appears to be in the time required for regenerating the new arm.
We thank A. Ellwood. J. Hintz, and J. Adams for help in collecting; T. Hopkins for identifying Echinaster paucispinus; and C. Pomory, B. Robbins, and T. Hopkins for constructive comments.
References Adams, J.M .) 199 1. The eflect of urm loss ONrespiration,excretion und biomass production in Luidik clathrutu /Ech&odermata: Asteroidea). MSc. Thesis. University of South Florida, Tampa, FL, 49 pp. Anderson, J.M., 1%5. Studies on visceraf regeneration in seastars II. Regeneration of prloric caeca in Asteriidac, with notes on the source off& in regenerating organs. B&t. Bu#.. Vol. 128, pp. I-13. Blake. D.B., 1989. Asteroidea: Functional marphoiogy, classification and phylogeny. ~e~i~~~~~e~~~~ Sfttdies. Vol. 3. pp. 179-223. Brody. S., 1945. Bioenergetics urrdgrowth. Hafner Publishing, New York, 1023 pp. Clark, A.M. 6i M.E. Downey, lY92. Starfishes qfthe Atlantic. Chapman and Hall, London, 794 pp. Dehn, P.F., 1980. The annual reproductivecycle of two populations of Luidiu clurhrura(Asteroidea) I. Organ indices and wcurrence of larvae. In. EchinlderN~s:pre~e~~~ ffir~~~~.~f, edited by M. Jangoux. AA. Balkema. Rotterdam, The Netherlands. pp. 361-367. Dehn. P.F.. 1982. The effect of food and temperature on reproduction in tuidia ckzf~rutn(AsteroideaI. In, Echinoderms: Proceedings of the InternatiotnalCorfirertce. Tampa Eul; edited by J.M. Lawrence, A.A. Balkema, Rotterdam, The Netherlands, pp. 457-463. Donachy. J.E.. N. Watabe & R.M. Showman. 1990. Alkaline phosphatase and carbonic anhydrasc activity associated with arm regeneration in the seast;~r Asterks forbesi. Mur. Biol., Vol. 11?5,pp. 47 I-476. Ebert. T.A., 1983. Longevity, lift history and reiative body wall size in sea urchins. Ecol. Monop., Voi. 52, pp. 353-394. Emson. R.H., 1984. Bone idle- A recipe for success‘? In, ~cbj~~oder~rfffo.edited by Keegan. B.F. & B.D.S. O’Connor, A.A. Balkema. Rotterdam, The Netherlands, pp. 25-30.
M. T. Lure.~, J.M. Luwrerrse i J. E.xp. Mar. Bioi. Ecol. I&7 il%‘4i 49-58 Emson. R.H. & I.C. Wilkie, 1980. Fission and autotomy
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Jangoux. M. & E. van Impe 1977. The annual pyloric cycle ofAsreriti.v r&errs L. (Echinodermata: Asteroidea). J. Exp. A4ar. Biui. Em/.. Vol. 30, pp. 165-184. Lawrence, J.M., 1973. Level, content. and caloric equivalents of the lipid, carbohydrate. and protein in the body components of Luidiu rlurhrutu (Echinoderm&: Asteroidea: Platyastcrida) in Tampa Bay. .I. !?\-I,. h4rrr. Bbd. Ed.. Vol. II, pp, 263-273. Laarencc. J.M., 1987. Echinodermata. In. Anir,~a/er2erRetics.I’oo[.2. edited by Pandian. T.J. & F.J. Vernberg. Academic Press. New York, pp. 229-321. Lawrence. J.M., 1990. The effect of stress and disturbance on echinoderms. Zool. Sci., Vol. 7, pp. 17-X Lawrence, J.M., 199la. Analysis of characteristics of echinoderms associated with stress and disturbance. In. Ejf~~~~~~~ t?~‘E~hilltirlentlura, edited by T. Yanagisawa. I. Yasumasu, C. Oguro, N. Suzuki&T. Motokaw~, A.A. Balkema, Rotterdam, The Netherlands, pp. 1 l-26. Lawrence, J.M.. 199 lb. Arm loss and regeneration in Asteroidca (Echinodermata). In, Echimdem reseurch IYYl, cditcd by Scalera-Liaci, L. & C. Canicatti, A.A. Balkema. Rotterdam, The Netherlands. pp. 3952. Lawrence. J.M. & P.F. Dehn, 1979. Biological characteristics of Luidia cluthmra (Echinodermata: .Asteroidea) from Tampa Bay and the shallow waters of the Gulf of Mexico. Fk. Sci.. Vol. 42. pp. 9Lawrence. J.M. & A. Eilwood. 1991. Simultaneous allocation of resources to arm regeneration and to somatic and gonadal production in ~~;~j~ ~i~~hrur~~ (Say) (E~hinodermata: Asteroidea). In, ~il~~~~~ c$Echirwdwn~t~iru, edited by 1. Yanagisawa, I. Yasumasu. C. Oguro. N. Suzuki & T. Motokawa. AA. Balkema, Rottcrdam. The Netherlands, pp. 543-548. Laurence, J.M. & ,4. Guille. 1982. Organic composition of tropical, polar and temperate water echinoderms. Contp, Bi&ern. Physiol., Vol. 72B. pp. 283-287. Lawrence. J.M. & J. Kafri. 1979. Numbers. biomass. and caloric content of the echinoderm fauna of the rocky shores of Barbados. Mur. Biol.. Vol. 52. pp. 87-91. Lawrence. J.M.. T.S. Klinger. J.B. McClintock, S.A. Watts, C.-P. Chen, A. Marsh 8 L. Smith, 1986. Allocation of nutrient resources to body components by regenerating Luidiu clnrhrutu (Say) (Echinodermats: Asteroidea). J. E-t-12.Mm. Birrl. Eu~., Vol. 102. pp. 47-53. McClintock. J. B. 1984. Arr ~~p~j~~lj~~~i(~~~ stu& on r/z~~~edit~~ be/z~~i~~r of Luidia sktrhrafa (Sayi (EehCri,du~rnclritt Awmideu). Ph.D. Dissertation, University of South Florida, Tampa. FL, 175 pp. McClintock. J.B.. J.L. Cameron & C.M. Young, 1990a. Biochemical and energetic composition of bathyal cohinoids and an asteroid, holothuroid and crinoid from the Bahamas. Mm. f&l., Vol. 105. pp. 175183. McClintock. J.B., T. Hopkins, S.A. Watts & K. Marion, 1990b. The biochemical and energetic composition of somatic body components of echinoderms from the northern Gulf of Mexico. Conrp. Bkwhem. Ph.txiol., Vol. 95‘4. pp. 529-532. Nichols. D. & h4.F. Barker. 1984. A comparative study of reproductive and nutritional periodi~ities in two p~~pulations of Aster&s rubem (Echinodern~ata: Asteroidea) from the English Channel. f. Mar. &o!. .dr.wc. L’.K., Vol. 63, pp. 471-484.
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M. T. Lures. J. M. Lawrence / J. E-up. Mar. Biol. Ecol. 180 (1994) 49-58
Pickett, S.T.A., J. Kolasa, J.J. Armesto & S.L. Collins, 1989. The ecological concept of disturbance and its expression at various hierarchical levels. Oikm, Vol. 54, pp. 129- 136. Scheibling, R.E. 81 J.M. Lawrence, 1982. Differences in reproductive strategies of morphs of the genus Echina.~rer (Echinodcrmata: Asteroidea) from the eastern Gulf of Mexico. Mar. Biol., Vol. 70. pp. Sl62. Sousa. W.P.. 1984. The role of disturbance in natural communities. Ann. Rev. Ec~col. Syrt., Vol. 15. pp. 353391. Steel, R.G. 81 J.H. Torrie, 1988. Principles atzdprocedures of.mri.~ics. McGraw-Hill, New York, 633 pp. Swan, E.F., 1966. Growth, autotomy and regeneration. In, PhZ.sio~~~~~~~cchinodertata, edited by Boolootian, R.A., John Wiley and Sons, New York, pp. 397-434. Xu. R.A. & M.F. Barker, 1990. Laboratory experiments on the effects of diet on the gonad and pyloric caeca indices and biochemical composition of tissues of the New Zealand starfish .Sc/ercrsrericr.s ntollis (Hutton) (Echinodermata: Asteroidea). J. E.Y~. Mar. Biol. Ecol., Vol. 136, pp. 23-45.
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
180 (1994) 49-58
Nutrient and energy allocation during arm regeneration in Echinaster paucispinus (Clark) (Echinodermata; Asteroidea) Michael T. Lares”, John M. Lawrence
Received 14 September 1993; revision received 28 January 1994; accepted 25 February 1994
Abstract
individuals of Echinctsrerpaufispinu.r (Clark) were either intact or had two arms amputated, and fed a sub-maintenance ration of food. After 7 months, the new arm was 17”, the radius of the intact arm. This rate of regeneration is much lower than that of other species of asteroids fed similar food levels. The greater amount of protein in the body wall of Echirrasterpaucispinits may be responsible. Gonadal growth occurred in both intact and regenerating individuals with an overall decrease in size of the pyloric caeca. Allocation to reproduction takes precedence over the deposition and retention of nutrient stores. Regenerating individuals gained energy (kJ), while intact individuals lost energy. This difference may result from a combination of higher food levels/individual and more efficient food utilization and decreased maintenance requirements (especially of body wall). This leads to more energy available for growth. Asteroids in general, show similar responses in allocation to the disturbance of arm loss and the stress of sub-optin~ai food. The stress-tolerant species, E~hi~~sfer pauci,spinus, has a slow rate of arm regeneration. Keywords:
Asteroidea;
Echinodermata;
Regeneration
1. Introduction
The capacity to regenerate lost body parts is considered characteristic of echinoderms (Hyman, 19.55; Swan, 1966; Emson & Wiikie, 1980). The loss of a body component constitutes disturbance (Grime, 1977; Sousa, 1984; Pickett et al., 1989), and may represent a significant cost to the individual. In asteroids, the loss of an arm can result in decreased locomotion and foraging efficiency (Lawrence, 1991b). Since the arms contain the pyloric caeca and gonads, nutrient storage and reproductive output * ~~rr~spondin~ author. 0022-0981!94/$7.00 0 1994 Elsevier Science B.V. All rights reserved SSDl OO’Z-09X1(94)00038-F
50
M. T. Lares. J.M.
Lawrence
I J.
Exp. Mar. Bid.
Ed.
180 (1994) 49-58
are decreased (Lawrence et al., 1986; Lawrence, 1991b). The energy required to replace body structures is a further cost of arm loss. A decrease in production constitutes stress (Grime, 1977) and can occur when food is limited (Lawrence, 1991a). With limited food, there may be trade-offs between regeneration and other energy uses, such as reproduction (Ebert, 1982). Allocation of energy to regeneration in the asteroid Luidia clathrata depends on food level. With a low level of food available, allocation is to the pyloric caeca and gonads of intact arms only (Lawrence et al., 1986); with a high level of food availability, allocation is to both the intact and regenerating arms (Lawrence & Ellwood, 1991). The pattern of allocation of energy to regeneration may be expected to vary among species of asteroids of different body forms and life-history characteristics. Luidia clathrata is a member of the order Paxillosida (Clark & Downey, 1992) is a voracious infaunal predator (Lawrence & Dehn, 1979; McClintock, 1984) and has an arm structure that lends itself easily to breakage (Clark & Downey, 1992). The body form of Luidia provides support and flexibility at the expense of armor (Blake, 1989). A species with this body form would be expected to have a high incidence of arm loss (Lawrence, 1991b). Up to 86p,,, of individuals of Luidia cfathrata in a population have arm loss (Lawrence & Dehn 1979). Luidia clathrata has been suggested to have a life-history strategy (C-R-S) associated with a relatively high capacity to obtain food and potential for arm loss (Lawrence, 1990). In contrast, Echinaster paucispinus is a member of the order Spinulosida (Clark & Downey, 1992) is an epifaunal browser (Ferguson, 1969), and has a robust body structure (Clark & Downey 1992). This body form gives flexibility with sturdiness, and restricts predatory abilities (Blake, 1989). Few Echinaster spp. show arm loss (Lawrence, unpubl.). Echinaster paucispinus has been suggested to have a life-history strategy (stress-tolerant) associated with a relatively low capacity to obtain food and potential for arm loss (Lawrence, 1990). Species with different life-history strategies may show different responses to the stress of low food availability and to the disturbance from arm loss. The objective of this study was to examine the response of Echinasterpaucispinus (Clark) to arm loss and low food availability.
2. Materials and methods Echinasterpaucispinus were collected from hard bottom substratum (N 10 m depth) off Egmont Key (27” 35’ N; 82” 46’ W), Florida on 22 September 1990, transferred to laboratory aquaria at 30%, S and 20 “C, and allowed to adjust to these conditions for 1 wk. Individuals were weighed and the radius (R; center of disc to the ray tip) measured. They were divided into two groups (n = 9/group). Two non-adjacent arms were removed from the individuals in one group. The proximate composition of amputated arms was assumed to be representative of both groups and were analyzed to characterize the two groups at time zero. The amputated individuals and a group of intact individuals were equally divided between two laboratory aquaria to decrease the possibility of an aquarium effect, and fed a sub-maintenance ration of 2-3 clams (Donax variabilis) per individual every 2 days. Seastars were placed directly on the clams to
M. T. Lares. J.M. Lawrence I J. hp.
Mur. Bid. Ed.
180 (19941 49-58
51
increase the probability that equivalent amounts were eaten. As the regenerating individuals had two fewer arms, they received more food per unit weight than the intact ~ndividua~s. After 7 months, all seastars were weighed, measured, and the arms dissected into components (body wall, pyloric caeca, gonads). The stomach was not included as it is relatively small. Regenerating and intact arms of amputated individuals were dissected and analyzed independently. The indices of the arm components (body wall, pyloric caeca and gonads) were calculated as percentages of the dry weight (Giese & Pearse, 1974). Arm components were dried over sulfuric acid in a vacuum desiccator, weighed, ground in a Wiley Mill and analyzed for proximate composition (total organic material, soluble and insoluble protein, total lipid, total carbohydrate) (Lawrence, 1973). Tissues were pooled when sufficient tissue was not available for individual analysis (viscera of regenerating arms, testes of intact and regenerating individuals). The non-extractable Table 1 Radius (mm) and dry weights (g) of arm components for all arms Group: Date: Arm:
Radius
Intact individuals 29 Sept. 1990 Intact 67k la (9)
Dry weight Single arm Body wall
1.23 + 0.08a (9)
Pyloric Caeca Ovaries
0.17 +_0.02a (9) 0
of Echinasterpatrcispi~2usin single arms and calculated
Intact individuals 2 May 1991 Intact 59+ lb (9)
I.11 i0.09a (9)
0
6.16 5 0.39a (9)
Pyloric Caeca Ovaries
0.86 + 0.36a
(9)
0.28 $: 0.02b (9)
0.08 k O.Olb
0.01 i. O.Olc
(9) 0.04 2 0.02a
(9) 0.01 _+O.Olb
0.009 & 0.013
5.57 + 0.46a (9)
(4) 0.004~0.0013 (5)
0.003 $. O.OOia (5)
(9)
0.5 1 f 0.06b
0.26 & O.Qlc
(9) 0.18 f 0.04a
(9) 0.14 i: 0.04a
0
0.05 + 0.03b (3)
(4)
3.97 + 0.26b
(9) 0
(6) Testes
1.14 & 0.080
10 + 0.1 (9)
(9) 0.04 * O.Ola
(3) All arms Body wall
59 ?: lb (9)
Regenerating
0.10 +O.Olb
(6) Testes
Regenerating individuals 2 May 1991 intact
(4) 0.02 -+ O.Olb (5)
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. 4. 1 SE and (n) are given. Values in a row with the same letter are not significantly different (p> 0.05).
52
M. T. Lares. J.M. Luwrence
/J. E.up. Mar. Bid. Ed.
180 (19941 49-58
material of body wall, pyloric caeca and ovaries is considered insoluble protein (Lawrence & Kafri, 1979). The energetic composition of body wall, pyloric caeca and ovaries was calculated by multiplying by the calorific equivalents of Brody (1945). As the DNA in the testes was not measured, the energetic composition of the testes was not calculated. Treatments were compared using a one way ANOVA, in conjunction with Baye’s Exact Test multiple comparison procedure (Steele & Torrie 1988). Percent composition data were transformed using an arcsine square root transformation before statistical analysis. Untransformed data are presented in the results. In all cases, significance was determined at the 5”, level.
3. Results The wounds of amputated arms closed by muscular action and were healed completely z 3 wk after amputation. All individuals showed negative growth over the experimental period, as the radius and the dry weights of the body wall and pyloric caeca of both intact and regenerating individuals decreased (Table 1). The decrease in the radius and pyloric caeca was significant, but not significantly different between the intact and regenerating individuals. Small amounts of gonads developed in both intact and regenerating individuals. The body wall indices of intact arms of both intact and regenerating individuals did not change significantly. The regenerating arms had a slightly but significantly higher body wall index than intact arms of initial or intact individuals, but not of intact arms of regenerating individuals (Table 2). The pyloric caeca index of intact arms of intact and regenerating individuals decreased significantly, and were significantly higher than
Table 2 Indices (“<>dry weight) of arm components Group: Date: Arm: Body wall
Pyloric Cacca Ovaries
Testes
Intact individuals 29 Sept 1990 Intact
of Echinasrer pauckpirtus in a single arm Intact individuals 2 May 1991 Intact
Regenerating individuals 2 May 1991 Intact
88 2 3a
9Oi3a
92 _t 3ab
(91
(91
(91
12_t3a (91 0
0
8 5 2b
6+ lb
(91 3k la
(91 3 + 2a
(61
&t-
1 f la (31
Regenerating
0.3 2 0.2a (51
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. 4, 1 SE and (n) are given. Values in a row with the same letter arc not significantly different (p>O.O5).
M. T. Lures. J.M.
Lawrence
; J.
E.xp. MIX.
Biol. EA.
53
180 119941 49-58
the pyloric caeca index of regenerating arms. The indices of the ovaries and testes did not differ significantly. Some major changes in the proximate constituents are apparent (Table 3). Most important is the decrease in the concentration of lipid in the pyloric caeca. The decrease was statistically significant in intact arms of regenerating individuals, but not in intact individuals. The concentration was low in the pyloric caeca of regenerating arms, but there was insufficient material for statistical analysis. The other notable difference is the similar and significantly higher concentration of ash and lower concentration of nonextracted organic material (probably protein) in the body wall of intact arms of both intact and regenerating individuals than those of regenerating arms. The kJ/g dry weight of the body wall, pyloric caeca and ovaries of the arms were not significantly different between initial. intact and regenerating individuals (Table 4). The Table 3 The proximate
composition
(“, dry weight) of body components
of Echirmter
puucispimo
Ash
Carbohydrate
Lipid
Soluble protein
Nonextracted material
,,
Intact arm Body wall Pyloric caeca
57.1 f 1.7a 8.7 i 0.9a
0.7 +O.la 1.7 f O.?a
2.6 &0.2a 17.7 + 0.9a
24.1 f_ 1.6a 53.2 & 1.8a
15.6 f 2.4, 18.8 5 2.2a
9 9
It~tcr<,tir~diiriduuk 7 Ma\ Intact arm Bad\ wall Pyloric caeca Ovaries Testes
56.0 f I .4a 9.5 f 0.3a 5.6 +_0.3a 8.05
0.6 f O.la 4.0 f 0.4a 0.7 + 0. la 0.9
3.1 f 0.3a 15.9 f 0.4, 48.5 + 1.8a 8.2
28.7 k l.3b 50.2 2 0.8a 40.9 2 l.Oa 41.5
11.6 & 2.5a 20.5 + 0.8a 4.3 +O.la 41.4
9
60.9 + 1.8a 9.8 f 0.4a 5.2_+0.la 17.3
0.5 &0.03a 4.0 *0.3a 0.8_+O.la I.5
2.5 k 0.2a 13.2 & l.4b 45.9 _+6.0a 10.9
24.0 f l.8a 49.1 f 1.7a 41.7 _+3.2a 47.8
12.2 + 2.4a 23.9I2.la 6.5 k 3.2a 2.6
9 9 4
50.0 + 3.7b 10.10 3.89 12.99
0.5*0.la 3.1 0.8 2.8
2.7 &0.2a 14.0 44.2 14.5
22.6 -+ 1.7a 44.2 44.3 54.3
24.4 + 2.8b 28.6 6.8 15.5
lntucr it~di~idmrls ZY Sept.
9
5
Re,qenercrritr,q individuh 2 Ma,
Intact arm Body wall Pyloric acaeca Ovaries Tcstcs Re,qerrerutitl,q urm
Body ~a11 Pyloric caeca Ovaries Testes
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. The non-extracted organic material is considered to be protein in the body wall. ovaries, and pyloric caeca and to be protein and DNA in the testes. 4 and I SE are given. Values for each body component in a column with the same letter arc not significantly different (p>O.O5).
54
M. T. Luves. J.M. Luwretlce /J. Eup. Mur. Biol. Ecol. 180 (19941 49-54
Table 4 The energetic composition (kJ;arm, Ethimrteu pul~~.i.~~iFI~4~~
kJ/individual,
and kJ!g dry weight) of the arm components
of female
kJ/arm
kJ/individual
kJ/g dry wt
II
29 Sept. Intact arm Body wall Pyloric cacca 13
128 + 523 46*6a 174
638 + ‘la 209 + 3na 847
11 + 0.43 24 * 0.2a 36
9 9
Irrt~~c’tBidi~~i&ml.~ 7 blay Intact arm Bodv wall Pyktric caeca Ovaries E
121*11a 24 f 3b 13+2a 158
603 + 52a 12Oi 14b 61*12a 184
Ii + 0.3a 24*0.ia 30 t osa 65
9 9 5
Regetlercr fing individuth 2 Ma) intact arm Body wail Pyloric caeca Ovaries z
108 + 6a 1822b 13+5a 139
324k 19b 39 i 14a 419
10 + 0.4a 23 + 0.3a 3OA la 63
9 9 3
68 * lc 22 30 120
12+ la 23 30 65
9
Itrtucr indivithtuls
Regenemtirlg urm Body wall Pyloric cacca Ovaries z
34+3b 11 15 60
56&hC
2 1
Intact individuals were dissected on 29 September 1990 and 2 May 1991. Regenerating individuals from which two arms had been amputated on 29 September were dissected on 2 May. Z and 1 SE are given. Values for each body component in a column with the same letter are not significantly different t,p> 0.05).
negative growth of the body wall and pyloric caeca resulted in a decrease in the kJ/ arm and kJ/individual (Table 4). Intact females lost 63 kJ (796 of the original) over the seven-month experiment, while regenerating females, which were fed more, gained a small amount, 17 kJ (3:; of the original).
4. Discussion Hyman (1955), Anderson (1965) and Swan (1966) stated without documentation that regeneration in asteroids is a slow process. Lawrence (1991b) concluded that this is true under low food conditions. In Eckinaste~paucispiizus wound healing and appearance of the new arm rudiment took z 3 and 4 wk, respectively. After 7 months, the new arm was z 17’!,; the size (R) of the intact arm. Asteriusfivbesi regenerates an arm bud in
M. T. Lares. J.M. Luwrence / J. Exp. Mar. Bid. Ed.
180 (I 9941 49-58
55
1 wk (Donachy et al., 1990). In Luidia clathrata on low levels of food, the arm rudiment appears in z 1 wk and grows to 1496 the length of an intact arm in one month (Adams, 1991). In contrast, the regenerating arms of Luidia clathrata fed abundant food grows to 703; the length of an intact arm in 5 months (Lawrence & Ellwood, 1991). Therefore, the rate of regeneration of the new arm varies with taxa, and food level. Because of their low capacity for production, species with a stress-tolerant life history strategy should have well developed protection from disturbance (Grime, 1977). If these defenses are well developed, little arm loss would be expected, as observed in Echinaster paucispims (Lawrence unpubl.). Blake (1989) noted the body form of the echinasteroid group provides sturdiness and protection from arm loss. Therefore, arms that are strong structurally are not lost easily or replaced rapidly (as in Echinaster paucispinus), and arms that are weak structurally are lost easily, and replaced quickly (as in Luidiu clathrata). Stress-tolerators have less relative rates of growth (Grime, 1977). As regeneration involves production, a stress tolerant species should replace and grow a lost arm slowly. Regenerating Echinasterpaucispinus in this study produced z 2.4 kJ/month, while regenerating Luidia clathrata produced 3.4 kJ/month (Adams 1991). Because of differences in feeding and size of individuals in these two studies, it is difficult to make conclusions on this difference in production. Gonads developed to the same extent in intact and regenerating individuals of Echinasterpaucispinus with a decrease in the size of the pyloric caeca. This suggests that gonadal production is taking precedence over deposition of nutrient reserves. Gonadal production occurs at the expense of somatic production on low food level in Luidia clathrata (Lawrence, 1973; Dehn, 1980, 1982; George et al., 1991) and Sclerasterias wollis (Xu & Barker, 1990). In contrast, starved Pisaster gigalzteus allocates material to the pyloric caeca over the gonads (Harrold & Pearse, 1980); Asterias rubens, under starvaticn or from impoverished areas gives priority to the body wall over both the pyloric caeca and the gonads (Jangoux & van Impe, 1977; Nichols & Barker, 1984). These variations in allocation appear directly related to food level. When little or no food is available, somatic development in the body wall or pyloric caeca takes precedence over gonadal development. With maintenance or sub-maintenance levels of food, gonad development occurs at the expense of somatic tissues; with abundant food, simultaneous allocation to somatic and reproductive tissues occurs. In general, the proximate composition of the body components of Echinaster paucispirzus is similar to that of other asteroids (Lawrence & Guille, 1982; Lawrence, 1987; McClintock et al., 1990a,b), and Echinaster type I at the same time of year (Scheibling & Lawrence, 1982). However, the concentration of soluble protein in the body wall of Echinasterpaucispinus is twice that of Luidia clathrata (McClintock et al., 1990b: Adams 1991). Echinaster paucispinus may grow arms slower than Luidia clathrata as more protein needs to be deposited in the body wall. There was a higher concentration of insoluble protein and lower concentration of ash in the body wall of regenerating arms of Echinasterpaucispinus. This suggests Emson’s proposal that growth of echinoderm body wall requires little energy may be incorrect (Emson, 1984). His hypothesis would have been supported if the same amount of protein were present in intact and regenerating arms. The basis for the production of energy and growth of the new arm may be similar
56
M. T. Lures. J.M. Lawrence j J. Esp. Mur. Biol. Erol. 180 (1994) 49-58
to that suggested by Adams (1991). Regenerating individuals in this and Adams’ study received more food/weight basis than intact individuals (1.5 and 1.2 f&d more, respectively). They may also have been more ef&ient in its use. This emphasizes the importance offeeding a weight-based (rather than an individual-based) ration in studies on regeneration. Additionally, regenerating individuals have less maintenance costs as the amounts of body wall and pyloric caeca are less, and should be able to allocate a larger proportion of their food resources towards new growth (Adams, 199 1). Consequently, the energy for regeneration may COEXas a resuft ofincreased food levets and/or reduced maintenance needs in regenerating individuals. The evidence here, and studies on Luidia ctathrata, strongly suggest that nutrient level determines the allocatiou of material to regeneration in asteroids. Some regeneration occurs even under starvation conditions (Lawrence et al., 19X6), indicating that the process is important. On sub-maintenance levels of food, regeneration is slow and alfocation is primarily to existing arms (Lawrence et al., 1986; this study). Rapid rates of regeneration, with simultaneous aflocation of energy to intact and regenerating arms occur with abundant food (Lawrence & Ellwood, 1991). The main difference between species of asteroid with different life history strategies to the disturbance of arm loss appears to be in the time required for regenerating the new arm.
We thank A. Ellwood. J. Hintz, and J. Adams for help in collecting; T. Hopkins for identifying Echinaster paucispinus; and C. Pomory, B. Robbins, and T. Hopkins for constructive comments.
References Adams, J.M .) 199 1. The eflect of urm loss ONrespiration,excretion und biomass production in Luidik clathrutu /Ech&odermata: Asteroidea). MSc. Thesis. University of South Florida, Tampa, FL, 49 pp. Anderson, J.M., 1%5. Studies on visceraf regeneration in seastars II. Regeneration of prloric caeca in Asteriidac, with notes on the source off& in regenerating organs. B&t. Bu#.. Vol. 128, pp. I-13. Blake. D.B., 1989. Asteroidea: Functional marphoiogy, classification and phylogeny. ~e~i~~~~~e~~~~ Sfttdies. Vol. 3. pp. 179-223. Brody. S., 1945. Bioenergetics urrdgrowth. Hafner Publishing, New York, 1023 pp. Clark, A.M. 6i M.E. Downey, lY92. Starfishes qfthe Atlantic. Chapman and Hall, London, 794 pp. Dehn, P.F., 1980. The annual reproductivecycle of two populations of Luidiu clurhrura(Asteroidea) I. Organ indices and wcurrence of larvae. In. EchinlderN~s:pre~e~~~ ffir~~~~.~f, edited by M. Jangoux. AA. Balkema. Rotterdam, The Netherlands. pp. 361-367. Dehn. P.F.. 1982. The effect of food and temperature on reproduction in tuidia ckzf~rutn(AsteroideaI. In, Echinoderms: Proceedings of the InternatiotnalCorfirertce. Tampa Eul; edited by J.M. Lawrence, A.A. Balkema, Rotterdam, The Netherlands, pp. 457-463. Donachy. J.E.. N. Watabe & R.M. Showman. 1990. Alkaline phosphatase and carbonic anhydrasc activity associated with arm regeneration in the seast;~r Asterks forbesi. Mur. Biol., Vol. 11?5,pp. 47 I-476. Ebert. T.A., 1983. Longevity, lift history and reiative body wall size in sea urchins. Ecol. Monop., Voi. 52, pp. 353-394. Emson. R.H., 1984. Bone idle- A recipe for success‘? In, ~cbj~~oder~rfffo.edited by Keegan. B.F. & B.D.S. O’Connor, A.A. Balkema. Rotterdam, The Netherlands, pp. 25-30.
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