nutrient and energy allocation during arm regeneration in echinaster paucispinus (clark)...

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY

Journal of Experimental Marine Biology and Ecology

180 (1994) 49-58

AND ECOLOGY

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 charac- terize 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 pos- sibility 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 in- cluded 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 of Echinasterpatrcispi~2us in single arms and calculated

for all arms

Group: Intact Intact Regenerating Regenerating

individuals individuals individuals

Date: 29 Sept. 1990 2 May 1991 2 May 1991 Arm: Intact Intact intact

Radius 67k la 59+ lb 59 ?: lb 10 + 0.1

(9) (9) (9) (9)

Dry weight

Single arm

Body wall 1.23 + 0.08a I.11 i0.09a 1.14 & 0.080 0.28 $: 0.02b

(9) (9) (9) (9)

Pyloric 0.17 +_ 0.02a 0.10 +O.Olb 0.08 k O.Olb 0.01 i. O.Olc

Caeca (9) (9) (9) (9) Ovaries 0 0.04 * O.Ola 0.04 2 0.02a 0.01 _+O.Olb

(6) (4) (4)

Testes 0 0.009 & 0.013 0.004~0.0013 0.003 $. O.OOia

(3) (5) (5)

All arms

Body wall 6.16 5 0.39a 5.57 + 0.46a 3.97 + 0.26b

(9) (9) (9)

Pyloric 0.86 + 0.36a 0.5 1 f 0.06b 0.26 & O.Qlc Caeca (9) (9) (9) Ovaries 0 0.18 f 0.04a 0.14 i: 0.04a

(6) (4)

Testes 0 0.05 + 0.03b 0.02 -+ O.Olb

(3) (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 composi-

tion 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 com- pletely z 3 wk after amputation. All individuals showed negative growth over the ex-

perimental 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 of Echinasrer pauckpirtus in a single arm

Group:

Date: Arm:

Intact

individuals

29 Sept 1990

Intact

Intact

individuals

2 May 1991

Intact

Regenerating

individuals

2 May 1991

Intact

Regenerating

Body wall

Pyloric

Cacca

Ovaries

88 2 3a

(91

12_t3a

(91 0

9Oi3a

(91

8 5 2b

(91 3k la

(61

Testes 0 1 la f

(31

92 _t 3ab

(91

6+ lb

(91 3 + 2a

&t-

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. 180 119941 49-58 53

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 non-

extracted 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

Non-

extracted

material

,,

lntucr it~di~idmrls

ZY Sept.

Intact arm

Body wall

Pyloric caeca

It~tcr<,t ir~diiriduuk

7 Ma\

Intact arm

Bad\ wall

Pyloric caeca

Ovaries

Testes

Re,qenercrritr,q individuh

2 Ma,

Intact arm

Body wall

Pyloric acaeca

Ovaries

Tcstcs

Re,qerrerutitl,q urm

Body ~a11

Pyloric caeca

Ovaries

Testes

57.1 f 1.7a

8.7 i 0.9a

56.0 f I .4a

9.5 f 0.3a

5.6 +_ 0.3a

8.05

60.9 + 1.8a

9.8 f 0.4a

5.2_+0.la

17.3

50.0 + 3.7b

10.10

3.89

12.99

0.7 +O.la

1.7 f O.?a

0.6 f O.la

4.0 f 0.4a

0.7 + 0. la

0.9

0.5 &0.03a

4.0 *0.3a

0.8_+O.la

I.5

0.5*0.la

3.1

0.8

2.8

2.6 &0.2a 24.1 f_ 1.6a 15.6 f 2.4,

17.7 + 0.9a 53.2 & 1.8a 18.8 5 2.2a

3.1 f 0.3a 28.7 k l.3b 11.6 & 2.5a

15.9 f 0.4, 50.2 2 0.8a 20.5 + 0.8a

48.5 + 1.8a 40.9 2 l.Oa 4.3 +O.la

8.2 41.5 41.4

2.5 k 0.2a 24.0 f l.8a 12.2 + 2.4a

13.2 & l.4b 49.1 f 1.7a 23.9I2.la

45.9 _+ 6.0a 41.7 _+ 3.2a 6.5 k 3.2a 10.9 47.8 2.6

2.7 &0.2a

14.0

44.2

14.5

22.6 + 1.7a 24.4 2.8b - +

44.2 28.6

44.3 6.8

54.3 15.5

9

9

9 9

5

9

9

4


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, kJ/individual, and kJ!g dry weight) of the arm components of female

Ethimrteu pul~~.i.~~iFI~4~~

kJ/arm kJ/individual kJ/g dry wt II

Itrtucr indivithtuls 29 Sept.

Intact arm

Body wall

Pyloric cacca

13

Irrt~~c’t Bidi~~i&ml.~ 7 blay

Intact arm

Bodv wall

Pyktric caeca

Ovaries

E

Regetlercr fing individuth 2 Ma)

intact arm

Body wail

Pyloric caeca

Ovaries

z

Regenemtirlg urm Body wall

Pyloric cacca

Ovaries

z

128 + 523

46*6a

174

121*11a 24 f 3b

13+2a

158

108 + 6a

1822b

13+5a

139

34+3b 68 * lc

11 22

15 30

60 120

638 + ‘la

209 + 3na

847

603 + 52a

12Oi 14b

61*12a

184

324k 19b

56&hC

39 i 14a

419

11 + 0.43

24 * 0.2a 36

Ii + 0.3a

24*0.ia

30 t osa

65

10 + 0.4a

23 + 0.3a

3OA la

63

12+ la

23

30

65

9 9

9

9

5

9

9

3

9

2

1


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 rudi-

ment 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 pau-

cispirzus 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 of feeding 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). Conse- quently, the energy for regeneration may COEX as a resuft of increased 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.

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