Arm regeneration in two populations of Acrocnida brachiata (Montagu) (Echinodermata: Ophiuroidea) in Douarnenez Bay, (Brittany: France): An ecological significance

Journal

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

of Experimental Marine Biology and Ecology 184 (1994) 123-139

Arm regeneration in two populations of Acrocnida brachiata (Montagu) (E c h ino d ermata: Ophiuroidea) in Douarnenez Bay, (Brittany: France): An ecological significance Allain Bourgoin *, Monique

Guillou

URA CNRS DI513. OcPanographie Biologique, UniversitPde Bretagne Occidentale. Facultk des Science.c, 6, avenue Le Gorgeu, B.P. 809. 2928.i Brest Cedex. France Received

21 March

1994; revision received 4 July 1994; accepted

26 July 1994

Abstract The incidence of arm regeneration in the brittlestar Acrocnidu bruchiutu is assessed for an intertidal and a subtidal population in the Bay of Douarnenez, France. The growth rate of regenerating arm parts in the field and under laboratory conditions and the annual regenerating biomass production complete the study. The frequency of arm regeneration is extensive and comprises nearly 70% of the total arm population in both sampling sites. The position of the breakage points mostly occur in mid-arm level in the tidal flat area and mainly in the distal third part of the arms in the subtidal site. The biomass composed of regenerating tissue is significantly different in both zones accounting for 11.1“/, ( & 9.5 06) of the total individual biomass in the intertidal area and 6.4% (+ 8.4%) subtidally. Actively feeding arms appear to be the least damaged. To maximize fitness, the intertidal individuals of Acrocnida bruchiuta seem to allocate energy to arm regeneration at the expense of somatic growth. Highest arm growth per individual was recorded in the field and comprises 1.2 mm.day -’ for individuals with two amputated arms. Subtidally, the annual production invested in regenerating tissue is 33 g dry wt.rn-’ (19 g AFDW.m

-‘).

Keyword.~:Acroclzidu

bruchiutu;

Amphiurid;

Biomass;

Ecological

significance;

Regeneration

1. Introduction The capacity of echinoderms to self-mutilate under stress conditions and regenerate their lost parts is a well known phenomenon (Emson & Wilkie, 1980). In ophiuroids, * Corresponding author. Present address: Universite de Moncton, Box 2000, Shippagan, New-Brunswick EOB 2P0, Canada

Centre universitaire

0022-0981/94/$7.00 0 1994 Elsevier Science B.V. All rights reserved SSDI 0022-0981(94)001 15-4

de Shippagan,

P.O.

124

A. Bourgoin, M. Guiilou I J. Exp. Mm. Biol. Ecol. 184 (1994) 123-139

the rate of regeneration after discarding arms has been studied on individuals of several species under various experimental conditions (Zeleny, 1903; Morgulis, 1909; Milligan, 1915; Salzwedel, 1974; Donachy & Watabe, 1986; Sides, 1987; Sullivan, 1988). Recently, the process of energy allocation during to disc and arm regeneration has been examined in the amphiurid Microphiopholis grucillima (Stimpson) (Clements et al., 1988; Dobson et al., 1991; Fielman et al., 1991). At a population level, the natural occurrence of regeneration in amphiurid species has been evaluated (Buchanan, 1964; Singletary, 1980; Bowmer & Keegan, 1983; Duineveld & Van Noort, 1986; Alva & Jangoux, 1990; Munday, 1993). Regenerating lost tissue parts contribute significantly to the total biomass represented by the species in its natural habitat. However, how these sublethal arm injuries, and in some cases the visceral mass, effects the population structure is not well known. In the present investigation, the significance of regeneration in two distinct habitats, an intertidal and a subtidal population of Acrocnidu brachiatu (Montagu), a boreomediterranean burrowing amphiurid, was assessed to measure the ecological significance of sublethal arm damage on the species. The growth rates of amputated arm parts were also monitored on a number of specimens under laboratory and in field conditions, in order to evaluate the turnover of this renewable biomass in the annual production. 2. Materials and methods The populations of Acrocnida brachiata used in this study were gathered from an intertidal and a subtidal area (20 m depth) of fine sand sediment (- 2% fines) situated in the northern part of the Bay of Douarnenez (48” 10’ N, 4” 25’ W) in Brittany (France). A detailed description of the study area and sampling stations are found in Bourgoin et al. (1991). For each sampling site and during the sampling period from March to July 1985, 14 to 40 individuals were gathered on a monthly basis, in order to study in situ regeneration. In the intertidal zone, the brittlestars were individually hand collected at low tide. In the subtidal zone, each specimen was extracted by a suction sampler using SCUBA. In all cases, the individuals were placed in separate glass jars filled with ambient seawater. This allowed collection of the parts autotomized during transportation and fixation. In the laboratory, the samples were first immersed in tap water to prevent the arms from curling, and after death, transferred for fixation to 70% ethanol. Each specimen was then analysed in terms of frequency of regeneration and biomass using a similar method to that employed by Bowmer & Keegan (1983) for AmphiuraJiliformis (O.F. Mtiller). 2.1. Frequency of arm injury Each individual was examined under a binocular microscope at 6.4x magnification. After measuring the disc diameter, the total length of each arm as well as the length of their intact and regenerated parts were recorded from the disc periphery by placing the brittlestar in a Petri dish, overlying l-mm scaled graph paper. As in other ophiuroids, the recently regenerated parts are distinguished by their lighter colouration and

125

A. Bourgoin, M. Guillou / J. Exp. Mur. Bid. Ecol. 184 (1994) 123-139

usually by an abrupt change in thickness at the breakage point along the arm (Singletary, 1980; Bowmer & Keegan, 1983; Sides, 1987; Alva & Jangoux, 1990; Aronson, 1992a; Munday, 1993). Even in those specimens in which regeneration has progressed to the point where size of the regenerated part has become identical to the intact stub, distinctly lighter colours persist for some time. If there was a doubt, the breakage point was considered undamaged. Since older regenerated parts are eventually unrecognizable either by size or colour, the results of the total incidence of arm damage may be slightly underestimated. Owing to the high number of possible combinations of regenerating points along the arms, the samples of Acrocnida brachiata were treated as a population of arms rather than as belonging to individuals. Broken arms lacking any evidence of a new arm rudiment were not counted as regenerating for breakage could have occurred during collection. Following the standard system used in echinoderms, the position of each arm is identified relative to the madreporite (Ct.¬, 1948). In this manner, it was possible to verify the eventual vulnerability in the frequency of the incidence of damage of one or more specific arms using a model of equiprobability. 2.2. Position of the breakage points For each sampling station, the relationship collected individuals and their disc diameters

between the longest intact arms of the have been assessed (Fig. 1). These two

Y =19,6 X - 33,i n = 84

TIDAL

r = 0,922

’

INTERTIDAL

fj3$;;;;;X 0

a.

/

- 5,6

r = 0,895

I

, 5

Fig. 1. Relationship between the disc diameter subtidal and the intertidal sites.

I

I

10 DISC DIAMETER

I

,I 15

(mm)

and the length of the longest intact arms of individuals

in the

126

A. Bourgoin, M. Guillou /J. Exp. Mar, Biol. Ecol. 184 (1994) 123-139

linear relationships served as a basis to define a theoretical length (Lt) expected to be attained by an intact arm of an individual. In turn, the position of the breakage points were defined by an index named “Position index” (Lc/Lt), which is expressed by the distance contained between the disc periphery and the point of rupture along the arm (Lc) and the theoretical length. The value of this relative index is 0 when the point of rupture is at the disc periphery, and 1 if the arm is intact or has reached the theoretical growth length.

Each specimen was dissected into three seperate parts: the regenerated portions of the arms, their intact parts and finally the disc deprived of its appendages, Each part was placed in separate containers and dried to a constant weight at 60 “C and weighed on an analytical balance. The dry weight of each portion was then expressed as a percentage of the total dry weight of the individu~. In June and July 1985, each component from both sampling zones was also burnt at 480 *C for 2-4 h (Byers et al., 1978) and the ash-free dry weights (AFDW) were determined as the weight losses of the dried remains after combustion.

To estimate the rates of arm regeneration, 20 individuals of a similar disc diameter collected from the intertidal zone were transported to the laboratory in separate glass jars filled with ambient seawater. The individuals were then transferred, in equal numbers, into four separate 2-l beakers half filled with sieved (l-mm mesh) native sediment. The beakers were in turn submerged in a plastic container @led with constantly aerated seawater. Once a week, the container was cleaned, the water renewed and, the animals were fed with a broth of mussels @4+&s edulis L.) and a small quantity of phytoplankton (Salzwedel, 1974; Ockelmann & Muus, 1478). During the experiment, temperature and salinity were maintained at 12.4 “C (+ 1.2 “C) and 34.3%, ( ? 0.9x,). After one month of acclimation, individuals had the shortest arms amputated at 2 to 3 cm from the disc with tke following frequency: 1 arm from 10 individuals, 2 arms from 5 individuals and 3 arms from the remaining 5 individuals. The regenerating parts of each specimen were measured after 7, 30, 45 and 65 days. These measurements were done in a similar fashion as described above except that the individuals were kept immersed in a small quantity of seawater. In the field, a delimited surface of 4 rn2? situated just below the mean low water neap tide level, was initially sieved (l-mm mesh) to gather all Rcrocnida specimens within this defined zone. As a marking criteria, each collected amphiurid had two adjacent arms amputated a few centimeters from the disc. In this way, 405 individuals were identified before being reburied in the central part of the cleared area. After 30 days, the square meter at the centre of the delimited zone was sampled. Thirty days latter, the zone was again sampled by extending the surface area to 3 m2. Each time, all the individuals sampled were brought to the laboratory for analysis The regenerating arms of the ophiuroids initially amputated and recaptured were measured to determine the regeneration progress.

A. Bourgoin, M. Guillou 1 J. Exp. Mar. Biol. Ecol. 184 (1994) 123-139

127

On July 2, 1985, in the intertidal zone, a sample of 45 individuals were analysed within the substratum. The appearance of the arms whether out streched or curled up within the burrow were registered. Afterwards, each respective arm of an individual was closely inspected to classify its regenerating state: early regeneration; intact arm or old wound: arm of unknown structure. 2.5. Production attributed to regeneration The annual production of Acrocnida brachiata attributed to regeneration was evaluated from the results gathered on the rate and incidence of regeneration (this study) and from the size distribution and population density obtained during a two year monitoring study of the species (Bourgoin, 1987). Calculations are inspired by Sullivan (1988).

3. Results Altogether between both sampling sites, a total of 223 specimens were studied corresponding to 1115 arms with a total of 872 identified breakage points. A test of the equiprobability of the vulnerability of the respective arms to breakage shows an equivalent risk between arms (intertidal zone: x2 = 6.98; df = 4; ~~0.05; Subtidal zone: x2 = 3.79; df= 4; p
A. Bourgoin. hf. Guillou /J. Exp. Mar. Biol. Ecol. 184 (1994) 123-139

128

Table I Acrocnida brachiata: Frequency (“/,) of occurrence and site. (A) subtidal zone; (B) intertidal zone (A) Subtidal

19 March 1985

No. of individuals per sample Total no. of regeneration points Total percentage of arms with regenerations 1 regeneration/arm 2 regenerations/arm 3 regenerations/arm Percentage of intact arms Percentage of missing arms of unknown structure Mean number of regenerating arms/animals (B) Intertidal

No. of individuals per sample Total no. regeneration points Total percentage of arms with regenerations 1 regeneration/arm 2 regenerations/arm 3 regenerations/arm Percentage of intact arms Percentage of missing arms of unknown structure Mean number of regenerating arms/animal

Table 2 Frequency

(Y,) of the regeneration

Arms within the burrow Arms extending out of the burrow

15 53 53.4 38.7 14.7

and position of arm regenerations

10 April 1985

4 June 1985

35 111

26 102

for each sampling date

I2 July 1985

Totals (means +

14 73

90 339

SD)

67.1 56.9 10.8 _

85.7 67.1 18.6 _

(70.4 k 14. I) (58.9 _t 7.5) (11.3+7.0)

10.7

57.8 52.6 4.6 0.6 34.9

30.0

14.3

(26.4 k 10.8)

(35.9)

7.3

2.3

2.7

2.9

3.4

9 March 1985

6 April 1985

2 June 1985

3 July 1095

Totals

40 139

35 156

24 103

34 135

133 533

61.5 54.0 7.0 0.5 35.5

73.2 58.9 13.7 0.6 22.3

3.0

4.5

3.1

3.1

state in 45 individuals

sampled

4.x (3.3 * 0.7)

4.3

76.7 47.5 9.2 _ 23.3

3.8

in the intertidal

(means

65.3 53.5 10.6 I.2 29.4

(69.2 (58.5 (10.1 (0.8 (27.6

f SD)

+ 7.0) k 6.5) i2.8) f 0.9) k 6.1)

5.3

(4.3 f 1.2)

3.3

(3.5 + 0.4)

zone

Early regeneration state

Intact arm or old wound

Arms of unknown structure

69.6 28.6

18.3 65.7

12.1 5.7

3.2. Position of the breakage points The length of the longest intact arm of an individual varies in accordance with the disc diameter and the sampling zone (Fig. 1). The frequency distributions of the “Position Index” for each series of sampling dates and zones show that there are breakage points at all levels along the arms (Fig. 2). By regrouping this information into three respective portions: the proximal (O-0.33) median (0.34-0.66) and distal

A. Bourgoin. M. Guillou / J. Exp. Mar. Bid. Ed.

129

184 (1994) 123-139

A SUBTIDAL 30-

INTERTIDAL

25-

25 - 2020-

15-

19 March 1985

,

:t

,

,

,

,

,

,

,

0

9March1985

SUBTIDAL

25

I.IIl-“TIT\11

10 April 1985

c -/- 0 I/W

6 April 1985 A INTERTIDAL

A2525-

2o-

20-

15-

15-

lo-

A 2525-

20-

20-

151

0

INTERTIDAL

/

,

0,l

0,2

,

,

,

,

0,3 0,4 0,5 0,6

I

,

0,7 0,8

0,9

, *

3JW19*5

1

POSITION Fig. 2. Frequency

histogram

distributions

of the position

index for the respective

INDEX sampling

dates and sites.

130

A. Bourg~~n, M. Gi~~i~ou/J. Exp. Mar.

Biol. Ecol. 184 (1994)

123-139

(0.67-1.00) parts of an arm, it is observed that in the subtidal zone, 647; of the breakage points appeared in the distal parts of the arms. In contrast, in the tidal flat area, breakage occurs more often in the central part of the arm, accounting for almost 50% of the rupture points. Finally, at both sites, the arms amputated in the proximal position are few.

80 -

A

SUBTIDAL ( March- April- June- July)

60 s 4 ill

40-

2 ::

20-

I 0

50

100

REGENERATED WEIGHT/TOTAL WEIGHT x

60 -

40

I1

B

INTERTIDAL

( March-

100

April- June- July)

1

20

0

50

100

REGENERATED WEIGHT /TOTAL WEIGHT Y Fig. 3. Frequency distribution (y;) of the regenerated biomass per individual of sampled individuafs per site. A: subtidal zone; B: inte~idal zone.

estimated

loo from the total number

A. Bourgoin. M. Guiliou 1 J. Exp. Mar. Biol. Ecol. 184 (1994) 123-139

131

3.3. Biomass The regenerated biomass (dry regenerated weight/total dry weight of the organism) fluctuate greatly. There are no linear correlations between the weight of regenerated parts and the total weight of an animal, or with the weight of the disc, whether by date or sampling site (r2 < 0.5). Kolmogorov-Smirnoff tests (Sokal & Rohlf, 1981) applied to the frequency distribution of the regenerated biomass reveal no significant differences between samples of the same zone (Bourgoin, 1987). Thus, for comparison between zones, all the values

Table 3 Acrocnida hrachiatu: mean biomass of the disc, intact and regenerated the total individual body dry weight for each sampling date and site

arms represented

as a percentage

10 April 1985

4 June 1985

12 July 1985

15 9.3 f 1.4

35 10.4 + 1.0

26 10.4i

1.0

14 9.5 + 1.5

25.1 + 5.4

23.7 i 3.2

27.6 f 3.5

23.1 i 3.2

70.7 f 5.2

67.7 2 2.3

65.5 + 7.6

66.9 + 8.0

56.9 i 1.4

57.9 * 1.2

6.9 5 8.3

9.9 + 8.4

56.3 + 2.7

60.3 k 5.6

6 April 1985

2 June 1985

3 July 1985

(A) Subtidal

19 March

No. of individuals per sample Mean disc diameter (mm) f SD Mean percentage of the disc dry weight + SD Mean percentage of disc AFDW + SD Mean percentage of intact arms * SD Mean percentage of intact arms AFDW k SD Mean percentage of regenerated arms _+SD Mean percentage of regenerated arms AFDW f SD

1985

72.9 + 9.4

65.7 _+8.2

3.4 2 8.4

9.2 f 7.0

(B) Intertidal

9 March

No. of individuals per sample Mean disc diameter (mm) f SD Mean percentage of the disc dry weight f SD Mean percentage of disc

40 8.9 f 0.6

35 9.7 _+0.7

24 10.2 * 0.4

34 8.7 + 1.1

25.5 2 1.9

32.0 k 2.9

32.3 + 2.5

25.1 i_ 3.2

74.9 f 3.5

68.4 f 2.6

58.1 i 8.7

63.3 & 12.4

56.6 + 0.8

56.9 + 1.0

9.7k8.1

11.62 11.5

AFDW i_ SD Mean percentage

of

1985

of intact

arms _t SD Mean percentage of intact arms AFDW + SD Mean percentage of regenerated arms f Mean percentage of regenerated arms AFDW k SD

SD

63.5 it 11.3

11.05 10.4

56.8 + 7.9

11.2~7.1

56.1 + 1.9

The mean percentage of the ash-free dry weight (AFDW) in each component June and July from the samples of both sites. (A) subtidal zone; (B) intertidal

analysed zone.

58.5 +_3.4 are represented

in

A. Bourgoin, M. Guillou /J. Exp. Mar. Biol. Ecol. 184 (1994) 123-139

132

for each date are grouped for each sampling site (Fig. 3A,B). It appears that 93% of subtidal and 86% of the intertidal individuals studied had less than 20% of their total dry weight invested in regeneration. Only a few individuals had up to 50% of their total dry weight composed of regenerating tissue. The proportion of the mean dry weight of each analysed portion (disc, intact and regenerating arms) show within a site, little fluctuation from one sample to the next (Table 3). Considering all the specimens collected in the intertidal zone, 11.1% ( + 9.5 %) of the total effective biomass is composed of regenerating tissue. In the subtidal zone, this mean value is 6.4% ( k 8.4%). A significant difference in the regenerating tissue per individual is observed between zones (t-test; d = 3.75; n, = 133; n2 = 90; p> 0.01). The organic matter (AFDW) composing the intact and regenerating arms are much the same and account for -57% of the total dry weight of the arm parts. These values fluctuate between 68 and 75% for the disc (Table 3). 3.4. Rates of regeneration The ophiuroids kept under laboratory conditions and excised of 1, 2 or 3 arms, presented no external perceptible regenerating rudiments after the seventh day of

Parms)

In the laboratory

0

7

30

45

60

65

DAYS Fig. 4. Time series results of the mean regenerated length of an arm for the individuals kept under laboratory conditions and with one, two, and three amputated arms; and for individuals with two amputated arms observed in the field. Error bars represent standard deviations of the mean. Points are offset slightly for graphical clarity.

A. Bourgoin, M. Guillou /J. Exp. Mar. Biol. Ecol. 184 (1994) 123-139

133

amputation (Fig. 4). The three series of measurements registered 30, 4.5 and 65 days after ablation show linear growth, the slope representing the rates of arm regeneration. Individuals with 1 arm amputated show the weakest arm growth rate. Individuals with either 2 or 3 amputated arms evole in a similar manner. In the field, where the individuals all had 2 arms amputated, the growth rate of the regenerating arm is higher than the observed rates found in laboratory specimens. Finally, in all cases and considering growth is linear, by extrapolation, it appears that a damaged arm would start to form a rudiment 20 days after amputation. In the laboratory, 65 days after amputation, the mean rate of renewed arm tissue for Acrocnida brachiata amputated were 0.33, 0.83 and 1.21 mm.day-‘.ind-’ respectively of 1, 2 and 3 arms. Under natural conditions, 60 days after ablation, the mean regenerated rate of arm growth per individual with 2 amputated arms was 1.20mm.day-‘.ind-‘, a 30% higher rate when compared to the specimens with 2 arms amputated and kept under laboratory conditions. The biomass of the regenerating parts was not directly assessed. It was evaluated by taking into account previous measurements obtained from the dry weight of regenerating arm parts from the subtidal individuals. Regenerating parts of an arm with a length measuring less than 100 mm give a mean dry weight of 0.11 x lo-’ g.mm-‘.arm-’ (n = 13; t 0.05) (pers. obs.). Thus, the biomass of regenerating arm parts in the field specimens would be -0.13 x 10m3 g.day-‘.ind-’ (0.11 x 10m3 x 1.20). Sixty days after amputation, a specimen in the field would most likely have mobilized 7.8 x lo-’ g dry weight to regrow its two missing arms. Although these figures are limited, they nevertheless serve as a comparison point and are useful in evaluating annual production. 3.5. Production attributed to regeneration Annual production attributed to regeneration in the present paper is evaluated for the subtidal population only. The mean cohort weights are first evaluated from the allometric relationship between the disc diameter and the disc dry weight estimated from 68 individuals taken subtidally (Bourgoin, 1987). The power curve is: W = 0.129 x 1O-3 D2.99

(r2 = 0.993)

where W, is the individual disc dry weight (g) and D, is the disc diameter (mm). The mean disc diameter values of the respective cohorts taken into account in the above equation are obtained from the disc size frequency histograms of each sample monitored during a 2-yr study of the population (Bourgoin, 1987, Annexe 3A; Bourgoin et al., 1991). As for the respective number of individuals composing each cohort, they are evaluated from the overall density of 426 ind.m-* obtained during the same study period. From these results, the standing biomass for a surface area of 1 m*, is evaluated by summing the biomass of the respective cohorts (mean weight x density). In this manner, the biomass of the total disc dry weight in the subtidal population varies between 40 g+mP2 (27 July 1985) and 54 g.m-2 (4 June 1985). Since the mean dry weight of the disc and the regenerating arms account for 25 and 6.4 %, respectively,

134

A. Bourgoin. M. Guiilou 1 J. Exp. Mar. Biol. Ed.

184 (1994) 123-139

of the total mean individual biomass (Table 3) then regenerating arm biomass will be 10.2 and 13.8 g dry wt.me2. As mentioned above, the regeneration rate in the field is w 0.13 x 10 -’ g dry wt.day-‘.ind-’ for individuals with 2 arms amputated. Although these values are obtained from intertidal experiments, for the purpose of the present study the same regenerating rate will be applied subtidally. Furthermore, the latter population is composed of individuals with an average of 3.3 regenerating arms at any given moment (Table 1). Assuming that the regenerating rate augments linearly with the number of missing arms, it would then be expected that 0.21 x 10m3 g dry wt*day -‘ind -’ is regenerating in the natural environment. Considering the overall density (426 ind.m m2), then nearly 90 x 10 -3 g dry wt.m -’ (0.21 x 10 -3 x 426) of regenerating arms would be produced daily. Finally, knowing that at a given time, the standing regenerating biomass accounts for 10.2 to 13.8 g dry wt.m-2 and the regenerating rate is 90 x lo-’ g dry wt.rnm2. day-‘, then the turnover period for renewal of regenerating biomass (6.4% of the total biomass) would be 113 to 153 days or 2.4 to 3.2 times yearly. Thus, the annual production would globally represent 33 g dry wt.m -’ of regenerating matter and by using a 10:6 ratio (Table 3) 19 g AFDW.m-‘.

4. Discussion Sublethal arm injury in Acrocnidu brachiuta is extensive. The overall percentage of total regenerating arms is nearly 70% in both populations studied and at the individual level, almost all (> 96 %) specimens presented at least one regenerating arm. These values are in accordance with other estimates in natural populations of various ophiuroid species, which often show more than 50% of the total number of arms are undergoing regeneration at any given time (Buchanan, 1964; Emson & Wilkie, 1980; Singletary, 1980; Bowmer & Keegan, 1983; Duineveld & Van Noort, 1986; Sides, 1987; Sullivan, 1988; Aronson, 1989, 1992a; Alva & Jangoux, 1990; Munday, 1993). From the frequency of regenerating arms, it appears that the two populations of Acrocnidu bruchiatu studied suffer from arm damage pressure to a similar degree even though the physical contraints of the environment are presumably harsher in the intertidal zone when compared to the subtidal site situated at 20 m depth. In crinoid populations, Mladenov (1983) and Meyer (1985) eliminate the physical stress such as wave action, as a main cause of arm and pinnule injuries. In ophiuroids, although Woodley et al. (1981) noted, off the Caribbean coast, an increase in damage after Hurricane Allen in 1980, Aronson (1991a,b, 1992a) observes, in the back reefs of the same tropical waters, that other hurricanes (Gilbert and Hugo) have had little effect on the frequency of arm injury in brittlestar populations. Predation is the more likely cause of arm loss in ophiuroids (Buchanan, 1964; Emson & Wilkie, 1980; Bowmer & Keegan, 1983; Duineveld & Van Noort, 1986; Aronson, 1987, 1989, 1991b, 1992a,b; Munday, 1993). The importance of predation intensity in causing observed patterns of sublethal arm injury are such that even in fossil assemblages, frequency of tissue damage to crinoids and ophiuroids are used as a predation

A. Bourgoin, M. Guillou 1 J. Exp. Mar. Bid. Ed.

184 (1994) 123-139

135

index to census predation intensity (Meyer, 1985; Schneider, 1988, Aronson, 1991b). Since both analysed populations of Acrocnida brachiata suffer in a similar manner from frequency of arm damage, it would be expected that predation intensity would also be similar. Aronson (1989) in studying predation on tethered ophiuroids in the British Isles states that attacks were almost 4 times more frequent in the rocky reef habitats in comparison to the brittlestar beds and that predators differed at each site. In contrast, Acrocnida brachiata does not show any difference between habitats in the percentage of individuals regenerating one or more arms (predation index of Aronson), whether considering the brittlestar bed comprised by the subtidal population or the intertidal population situated adjacent to a rocky reef. Acrocnida brachiata, is an infaunal species, while Aronson worked on epifaunal ophiuroids; this difference in the life habits of the respective species might explain the observed differences in the results. In this regard, Schneider (1988) has shown a relationship between the frequency of regenerated arms in comatulid crinoids and the variety of lifestyles of the respective species. In ophiuroids, Alva & Jangoux (1990) state that Amphipholis (Axiognathus) squamata Delle Chiaje is protected from predation by its cryptic lifestyle. Aronson (1992b), furthermore, underlines that if predation intensity passes a certain threshold, the brittlestar beds cannot persist. In infaunal amphiurids, even with a high percentage of arm damage, there appears to be relative stability in population structure (Bowmer & Keegan, 1983; O’Connor et al., 1983; Duineveld et al., 1987; Munday, 1993). In contrast to epifaunal ophiuroids, the infaunal lifestyle of certain Amphiuridae such as Acrocnida brachiata may permit the species to support high predation pressure. Acrocnida brachiata, like other amphiurids (Woodley, 1975; Ockelmann & Muus, 1978; Singletary, 1980; Bowmer, 1982), usually does not extend its five arms simultaneously into the water column. At least one or two arms remain curled up in the sediment for burrow construction, maintenance, respiration and even to help anchor the individual in the substratum (Woodley, 1975; Clements, 1985). Being protected from the external environment, the arms within the burrow must be less vulnerable than those extended in the water column. Yet, as in other amphiurids (Bowmer & Keegan, 1983; Munday, 1993), each respective arm of an individual of Acrocnida brachiatu presents the same vulnerability to injury. Observations have shown (Table 2), that the arms of Acrocnida brachiata within the sediment are mostly in an early state of regeneration while the arms actively feeding are those that are either intact or showing an older wound. There seems to be a “rotation” among the arms of each individual: the exposed arms suffering injury, become as a result, less or even non-functional for feeding purposes. The injured arm is retracted to the protection of the burrow. It is substituted by an arm in a more functional or less damaged state. The advantages of this process would be three-fold: (1) it would assure that the individuals are at all times optimizing their feeding activity; (2) it would permit the damaged arms, to regenerate under more protected conditions, and consequently; (3) it would permit this infaunal species to better resist to predation pressure. The need of amphiurids to possess a minimum number of functional arms has been underlined by Fielman et al. (1991) for the amphiurid, Microphiopholis gracillima. In Acrocnida bruchiata, arm rotation probably assure this minimal vital threshold.

The process of arm rotation could also partly explain the noted preponder~ce of a single regeneration point per arm observed in amphiurids (Bowmer & Keegan, 1983; Munday, 1993; Table 1 of this study) and the significance of the high values of the total number of regenerated arms per individuals observed in different studies (Buchanan, 1964; Bowmer & Keegan, 1983; Munday, 1993; this study). The position of the breakage points mostly occur at mid-arm level in the intertidal population and mainly in the distal third part in the individuals gathered subtidally. Moreover, the mean percentage of regenerating tissue is significantly higher in the tidal flat area. In other words, not only do the individuals in the latter zone have relatively less intact arms but more energy seems to be directed to arm replacement. In terms of bioenergetics, a balance is required between demand {metabolism, gonad development, growth) and food availability. A minimum amount of acquired nutrients is necessary for maintenance. Above this first threshold, gonad growth, then somatic growth can occur according to food supply gradient (Lawrence, 1987). In Acrocnida brachiuta, the intertidal population attains the second threshold described above since the individuals survive and reproduce annually (Bourgoin & Guillou, 1990) but their maximum disc diameter reaches a smaller size (Bourgoin et al., 1991) and the total length of their arms are shorter (Fig. 1) when compared to the individuals found subtidally. In the intertidal area, where feeding is reduced to periods of emersion and where food supply is lower (Bourgoin et al., 1991), maximal fitness of the individuals would be reached at the expense of somatic growth. In fact, trade-offs are necessary extracting a physiological cost whose burden may affect growth, reproductive potential and general viability of the individuals (Lawrence, 1987; Dobson et al., 1991; Fielman et al., 1991). Since arms are the feeding organs for these suspension-feeders, energy allocation to maintain the arms in a functional state probably maximizes the feeding capability of the individuals and thus increases fitness. In the case of the intertidal population, the individuals suffer more arm loss than those sampled subtidally where food supply is higher. To maintain fitness, the intertidal animals most likely need to mobilize more energy for arm regeneration, thus the observation of a significantly higher registered regenerated biomass as compared to the individuals found subtidally. In contrast, in the subtidal population, the individuals can feed at all times, their food supply is more abundant (Bourgoin et al., 1991), and they show less arm damage. In this case, the external factors causing stress and disturbance to the population (Lawrence, 1991), would be weaker, and energy transfer for arm regeneration for maximal fitness would be less imperative. Consequently, more reserves can be channelled into gtobal somatic growth. As observed by Fielman et al. (1991) for the amphiurid ~~c~~~h~o~~#~i~ gmcillima, to maintain a “minimal functional configuration” (MFC), trade-offs are made in such a way as to ensure that the essential organs needed for maintenance arc kept in a functional state. Given the incidence and rate of regeneration, the population structure and overall density, the annual production of regenerating arm parts represents approximately 33 g dry wt.mw2 (19 g AFDW*m -*). Using a different approach, O’Connor et al. (1986) obtain values of 105 g dry wt.m-2.yr-’ for an A~zphiu~a~f~ormis population in Galway Bay (Ireland). In their analysis, O’Connor et al. (op. cit.) have evaluated the potential production of the species, i.e. considering all the arms would have entirely regenerated

A. Bourgoin, M. Guillou 1 J. Exp. Mar. Bid. Ed.

184 (1994) 123-139

137

without being damaged. Since these potential values cannot be attained in the natural environment because of stress and disturbance to the individuals of a population (Lawrence, 1991), in contrast, in the present study the annual production has been estimated from the standing biomass rather than from the potential biomass (position index). In other words, the arm deficiency (Sides, 1987) has not been considered. Other factors can explain the marked differences observed in the annual production between species. Estimated regeneration rates are different for each species. For Amphiuru jihformis, this value is 0.15 g dry wt.ind-‘.yr-’ and in Acrocnida brachiata it is 0.08 g dry wt.ind-‘.yr-‘, or almost 50% less. Finally, marked differences in annual production are also affected by the density of the studied species. In amphiurids sampled off the Florida coast, Singletary (1980) obtains an annual production of missing arm regeneration varying from 0.23 to 0.91 g.mm2. These results contrast with those mentioned above, but in the latter case the densities varied between 34 and 56 ind.mm2 which is much lower than the values of 700 and 426 ind.m-’ recorded for Amphiuru ,filifrmis and Acrocnida brachiatu. Since, predation appears to be the main cause of arm cropping in ophiuroids (op. cit.), then in some amphiurid populations, the biomass regenerated annually may constitute an important element in the food web. Stomach content analysis of demersal fish in Douarnenez Bay show that Acrocnida arms composes up to 18% (wet weight) of the diet of the dab, Limanda limanda (Linnaeus) (Quiniou, 1978). Other demersal fishes analysed seem only to prey sporadically on this amphiurid. In the southern North Sea, Duineveld & Van Noort (1986) observed that Amphiurufiliformis arms accounted for w 60% of the wet weight of the stomach content of the dab population and from the biomass of these flatfishes and their feeding rate, it was evaluated that the dabs in the study area consume 6% of the arm population (1330 ind.me2). In comparing the stomach content results of both studies, dabs in Douarnenez Bay seem to prey much less on Acrocnida brachiata arms than they do on AmphiuraJiliformis arms in the North Sea. To better understand community ecology and the food web cycle, much more information would be needed on the diversity and abundance of available food to the predator, predator density and predation pressure.

Acknowledgements

This paper represents a portion of the these 3” cycle submitted by A. Bourgoin to the Laboratoire d’oceanographie biologique, Universite de Bretagne Occidentale, Brest. A. Bourgoin gratefully acknowledges Professeur M. Glemarec for his hospitality and for access to facilities. The authors also thank Mr. R. Marc and Ch. Tartu for technical assistance and constant support in the field and to Miss J. L’Hostis for typing. The work of A. Bourgoin at the Universite de Bretagne Occidentale was funded by a French government grant (1981-1986) and a scholarship by CIES (1991).

138

A. Bourgoin, M. Guillou 1 J. Exp. Mar. Biol. Ecol. 184 (1994) 123-139

References Alva, V. & M. Jangoux, 1990. Frequence et causes presumees de la regeneration brachiale chez Amphipholis squamata (Echinodermata: Ophiuroidea). In, Echinoderm research, edited by C. DeRidder, P. Dubois, M.C. Lahaye & M. Jangoux, A.A. Balkema, Rotterdam, The Netherlands, pp. 147-153. Aronson, R.B., 1987. Predation on fossil and recent opiuroids. Paleobiology, Vol. 13, pp. 187-192. Aronson, R.B., 1989. Brittlestar beds; low-predation anachronisms in the British Isles. Ecologv, Vol. 70, pp. 856-865. Aronson, R.B., 1991a. Hurricane effects on Caribbean echinoderm faunas: Preliminary results. In, Biolog,v qf echinodermata: Proceedings of the Seventh International Echinoderm Conference, edited by T. Yanagisawa, 1. Yasumasu, C. Oguro, N. Suzuki & T. Motokawa, A.A. Balkema, Rotterdam, The Netherlands, p. 143. Aronson, R.B., 1991b. Predation, physical disturbance, and sublethal arm damage in ophiuroids: a JurassicRecent comparison. Mar. Ecol. Prog. Ser., Vol. 74, pp. 91-97. Aronson, R.B., 1992a. The effects of geography and hurricane disturbance on a tropical predator-prey interaction. J. Exp. Mar. Biol. Ecol., Vol. 162, pp. 15-33. Aronson, R.B., 1992b. Biology of a scale-independent predator-prey interaction. Mar. Ecol. Prog. Ser., Vol. 89, pp. 1-13. Bourgoin, A., 1987. Ecologic et dtmographie d’rlcrocnida brachiata (Montagu) (Echinodermata: Ophiuroidea) en baie de Douarnenez (Bretagne). These 38me cycle, Universitt de Bretagne Occidentale. Brest, France, 146 pp. Bourgoin A. & M. Guillou, 1990. Variations in the reproductive cycle ofAcrocnida brachiata (Echinodermata: Ophiuroidea) according to environment in the bay of Douarnenez (Brittany). J. Mar. Biol. Assoc. U.K., Vol. 70, pp. 57-66. Bourgoin A, M. Guillou & M. Glemarec, 1991. Environmental instability and demographic variability in Acrocnida brachiata (Echinodermata: Ophiuroidea) in Douarnenez bay (Brittany: France). P.S.Z.N.I.: Mar. Ecol., Vol. 12, pp. 89- 104. Bowmer, T., 1982. Aspects of the biology and ecology of Amphiura~lij+mis (O.F. Mtiller) (Echinodermata: Ophiuroidea). Ph.D dissertation, National University of Ireland, Galway, Ireland, 99 pp. Bowmer, T. & B.F. Keegan, 1983. Field survey of the occurrence and significance of regeneration in Amphiura filiformis (Echinodermata: Ophiuroidea) from Galway bay, western coast of Ireland. Mar. Biol.. Vol. 74, pp. 65-71. Buchanan, J.B., 1964. A comparative study of some features of Amphiura~lfirmis and Amphiura chiajei (Ophiuroidea) considered in relation to their distribution. J. Mar. Biol. Assoc. U.K., Vol. 44. pp. 565576. Byers, S.E., E.L. Mills & P.L. Stewart, 1978. A comparison of methods of determining organic carbon in marine sediments, with suggestions for a standard method. Hydrobiologia, Vol. 58, pp. 43-47. Clemcnts, L.A.J., 1985. Post-autotomy feeding behavior of Micropholis gracillima (Stimpson): implications for regeneration. In, Echinodermata: Proceedings of the Fifth International Echinoderm Conference, edited by B.F. Keegan & B.D. O’Connor, A.A. Balkema, Rotterdam, The Netherlands, pp. 609-616. Clements, L.A.J., K.T. Fielman & S.E. Stancyk, 1988. Regeneration by an amphiurid brittlestar exposed to different concentrations of dissolved organic matter. J. Exp. Mar. Biol. Ecol., Vol. 122, pp. 47-61. C¬, L., 1948. Anatomie, tthologie et systematique des Cchinodermes. In, Traiti de zoologie. Vol. II., edited by P.P. Grass&, Masson, Paris, pp. 3-362. Dobson, W.E., S.E. Stancky, L.A. Clements & R.M. Showman, 1991. Nutrient translocation during early disc regeneration in the brittlestar Microphiopholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). Biol. Bull. (Woods Hole, Mass), Vol. 180, pp. 167-184. Donachy J.E. & N. Watabe, 1986. Effects of salinity and calcium concentration on arm regeneration by Ophiotrix angulata (Echinodermata: Ophiuroidea). Mar. Biol., Vol. 91, pp. 253-257. Duineveld, G.C.A. & G.J. Van Noort, 1986. Observations on the population dynamics ofAmphiuru,filfirmi.~ (Ophiura: Echinodermata) in the southern North Sea and its exploitation by the dab Limanda limandu. Neth. J. Sea Rex, Vol. 20, pp. 85-94. Duineveld, G.C.A., A. Kttnitzer & R.P. Heyman, 1987. Amphiurafilformis (Ophiuroidea: Echinodermata)

A. Bourgoin,

in the North

Sea. Distribution,

M. Guillou 1 J. Exp.

present

123-139

139

and size composition.

Neth. J. Seu Res.,

Mar. Biol. Ecol. 184 (1994)

and former abundance

Vol. 21, pp. 317-329. Emson, R.H. & I.C. Wilkie, 1980. Fission and autotomy

in echinoderms.

Oreanogr.

Mar. Biol. Annu. Rev.,

Vol. 18, pp. 155-250. Fielman, K.T., S.E. Stancyk, W.E. Dobson & L.A.J. Clements, 1991. Effects of disc and arm loss on regeneration by Microphiopholis gracillimo (Echinodermata: Ophiuroidea) in nutrient-free seawater. Mur. Biol., Vol. I1 1, pp. 121-127. Lawrence, J.M., 1987. A functional biology qf echinoderms. John Hopkins University Press, Baltmore, Maryland, 340 pp. Lawrence, J.M., 1991. Analysis of characteristics of echinoderms associated with stress and disturbance. In. Biology of Echinodermata: Proceedings of the Seventh International Echinoderm Conference, edited by T. Yanagisawa, I. Yasumasu, C. Oguro, N. Suzuki & T. Motokawa, A.A. Balkema, Rotterdam. The Netherlands, pp. 1 l-26. Meyer, D.L., 1985. Evolutionary implications of predation on Recent comatulid crinoids from the Great Barrier Reef. Puleobiology, Vol. 11, pp. 154-164. Milligan, M., 1915. Rate of regeneration in a brittlestar. Zoologist, Vol. 19, p. 119. Mladenov, P.V., 1983. Rate of arm regeneration and potential causes of arm loss in the feather star Fk)rometra serratissima (Echinodermata: crinoidea). Can. J. Zool., Vol. 61, pp. 2873-2879. Morgulis, S., 1909. Regeneration in the brittlestar Ophiocomapumila, with reference to the influences of the nervous system. Proc. Am. Acad. Arts Sci., Vol. 44, pp. 655-659. Munday, B.W., 1993. Field survey of the occurrence and significance of regeneration in Amphiura chiqjei (Echinodermata: Ophiuroidca) from Killary Harbour, west coast of Ireland. Mar. Biol.. Vol. 115, pp. 661-668. O’Connor, B., T. Bowmer & A. Grehan, 1983. Long-term assessment of the population dynamics of Amphiuraflijkmis (Echinodermata: Ophiuroidea) in Galway bay (west coast of Ireland). Mar. Biol., Vol. 75, pp. 279-286. Ockclmann, K.W. & K. Muus, 1978. The biology, ecology and behaviour of the bivalve My.vella hidenduta (Montagu). Ophelia, Vol. 17, pp. l-93. Quiniou. L., 1978. Les poissons demersaux de la baie de Douarnenez. Alimentation et tcologie. These 3tme cycle. Universite de Bretagne Occidentale, Brest, France, 222 p. Salzwedel, H., 1974. Arm-regeneration bei Amphiura @firmis (Ophiuroidea). Veroff: Inst. Meerrforsch. Bremerh., Vol. 14, pp. 161-167. Schneider, J.A.. 1988. Frequency of arm regeneration of comatulid crinoids in relation to life habits. In, Echinoderm biology: Proceedings of the Sixth International Echinoderm Conference, edited by R.D. Burke, P.V. Mladenov, P. Lambert & R.L. Parsley, A.A. Balkema, Rotterdam, The Netherlands, pp. 531-538. Sides, E.M., 1987. An experimental study ofthe use of arm regeneration in estimating rates of sublethal injury on brittle-stars. J. Exp. Mar. Biol. Ecol., Vol. 106, pp. I-16. Singletary, R.L.. 1980. The biology and ecology of Amphioplus coniortodes, Ophionephthys limicola and Microphiopholis gracillima (Ophiuroidea: Amphiuridae). Caribb. J. Sci., Vol. 16, pp. 39-55. Sokal, R.R. & F.J. Rohlf, 1981. Biometry. W.H. Freeman & Co, San Francisco, second edition, 859 pp. Sullivan, K.M., 1988. Physiological ecology and energetics of regeneration in reef rubble brittlestars. In, Echinoderm Biology: Proceedings of the Sixth International Echinoderm Conference, edited by R.D. Burke, P.V. Mladenov, P. Lambert & R.L. Parsley, A.A. Balkema, Rotterdam, The Netherlands, pp. 523-529. Woodlcy, J.D.. 1975. The behaviour of some amphiurid brittle-stars. J. Exp. Mar. Biol. Ecol., Vol. 18. pp. 29-46. Woodley, J.D., E.A. Chornesky, P.A. Clifford, J.B.C. Jackson, L.S. Kaufman, N. Knowlton, J.C. Lang, M.P. Pearson, J.W. Porter, M.C. Rooney, K.W. Rylaarsdam, V.J. Tunnicliffe, C.M. Wahle, J.L. Wulff, A.S.G. Curtis, M.D. Dallmeyer, B.P. Jupp, M.A.R. Koehl, J. Neigel & E.M. Sides, 198 1. Hurricane Allen’s impact on Jamaican coral reefs. Science, Vol. 214, pp. 749-755. Zeleny, C., 1903. A study of the rate of regeneration of the arms in the brittlestar, Ophioglypha hcertosu. Biol. Bull. (Woods Hole, Mass.), Vol. 6, pp. 12- 17.