Marine Biology 111, 431-435 (1991)

@ Springer-Verlag 1991

Skeletal changes in the test and jaws of the sea urchin Diadema antillarum
in response to food limitation
D. R. Levitan *

Bamfield Marine Station, Bamfield, British Columbia VOR lBO, Canada, and Department of Zoology, University of Alberta, Edmonton,
Alberta T6G 2E9, Canada

Date of final manuscript acceptance: August 16,1991. Communicated by J.M. Lawrence, Tampa

Abstract. When food-limited, Diadema antillarum in- limited conditions appears to be a general phenomenon.
creases the relative size of Aristotle's lantern compared to The present study elucidates the morphometric changes
the size of the test. This is accomplished primarily by in the skeleton and provides evidence of these changes
decreasing the size of the test: the demipyramid grows at under experimental manipulations of population density
a reduced rate as the test shrinks. These results suggest and resource availability.
that an altered relationship between demipyramid and
test size can provide evidence for food-limitation in field
populations. The sizes of the lantern and test of museum
Materials and methods
and fossil specimens can be investigated for the presence
of food limitation and biotic interactions in recent and Two experiments were conducted to determine how population den-
past times. sity and food availability affect the growth of Diadema antillarum
(for details, see Levitan 1989). The first was an 8-mo field experi-
ment in which individuals from two size classes (25.0 to 30.0 and
35.0 to 40.0 mm test diameter) were placed in subtidal cages
Introduction (0.25 m2 in area) at two densities (12 and 24(m2). Each treatment
group had eight replicate cages (total of 144 individuals). The sec-
ond was a 6-mo laboratory experiment in which individuals from
Food limitation in echinoids results in an increase in the one size class (40.0 to 45.0 mm) were given one of four levels of food
relative size of Aristotle's lantern compared to the size of (4, 2, 1, and 0 9 wet weight of the green alga U/va /actuca, every 4 d).
the test (Ebert 1980, Black et al. 1982, 1984, Edwards and The laboratory experiment had two levels of crowding (one and
Ebert 1991). Ebert proposed the "plastic resource alloca- three individuals per container), with both levels receiving the same
tion" hypothesis when he noted this relationship in two per capita food level. Each treatment group had eight replicates
(total of 128 individuals). Crowding did not affect growth (Levitan
species (Strongylocentrotus purpuratus and Diadema seto- 1989), and for the present study these data were pooled by food
sum). He suggested that food-limited echinoids increased level. In both these experiments, test diameter and the length of the
the size of the jaw apparatus (measured by the length of demipyramid were measured for each individual. Test diameter was
the demipyramid) which increased their capacity to measured by picking up the echinoid with tongs, turning it oral side
graze. Black et al. (1982) noted a similar relationship up, and placing the tips of needle-nose vernier calipers between the
spines from one interambulacral region across the mouth to the
between demipyramid and test size dependent on popula-
opposite ambulacral region. Each individual was measured on three
tion density in the echinoid Echinometra mathaei; as pop- different diameters to 0.1 mm and the mean diameter was used as
ulation density increased so did the relative size of the the datum (the mean standard error of the three measurements was
jaws. Black et al. (1984) suggested that a relatively larger 0.18 mm). Each individual was measured at the start of the experi-
Aristotle's lantern was associated with increased grazing ment and every 2 wk thereafter for a total of 32 wk in the field
ability. However, since these studies did not provided experiment and 23 wk in the laboratory experiment. In the labora-
information on initial sizes (Ebert 1980, Black et al. 1984) tory experiment, each echinoid was individually identified, and only
those echinoids that survived to Week 22 were included in the
or did not follow single individuals over time (Edwards analysis (those echinoids which died in the last week were kept and
and Ebert 1991), it is unknown whether this relationship their skeletal measurements recorded). In the field experiment, indi-
is a result of an increase in demipyramid size and/or a viduals could not be identified within a cage, and thus differential
decrease in the size of the test. The altered relationship mortality might have influenced measurements of changes in size.
between the size of the test and demipyramid under food- However, in this latter experiment, mortality rate was not signifi-
cantly different between treatments, and in three out of four treat-
ments the final sizes were outside the initial size range (Levitan
* Present address: Department of Zoology, University of califor- 1989). In analyses where initial sizes were needed, only data from
nia at Davis, Davis, California 95616-8755, USA the laboratorY experiment were used.
432 D. R. Levitan: Skeletal plasticity in sea urchins
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2.1lf-
2.5 3 3.5 4 4.5 3.3 3.4 3.5 3.6 3.7 3.8 3.9
In Test Diameter (mm) In Test Diameter (mm)
Fig. I. Diadema antillarum. Demipyramid length vs test diameter Fig. 2. Diadema antillarum. Demipyramid length vs test diameter in
for field-collected sea urchins. (Regression equation at end of "Ma- experimental treatment. 0: Final seaurchin sizesin field experiment
terials and methods") (B: initially large sea urchins; S: initially small sea urchins; (L: low
density; H: high density); 0: laboratory experiment (numbers indi-
cate grams wet wt Ulva lactuca fed every 4 d) and regression of
field-collected sea urchins. Data points show means I standard er-
The length of the demipyramid was measured, with vernier
rors; only half error bars plotted for field experiment and only lower
calipers to 0.05 mm, from oral tip to the epiphysis junction at the
half of 95% confidence interval (dotted line) plotted for regression
aboral end (as in Ebert 1980) at the termination of the experiment.
of field-collected seaurchins for clarity. Arrows indicate size change
A mean of five demipyramids per individual was used as the datum
from initial conditions
(the mean standard error of the five measurements was 0.03 mm).
The demipyramids and tests of field-collected individuals were
measured for comparative purposes. These field-collected individu-
als were in a food-abundant environment and grew rapidly (Levitan Table I. Diadema antillarum. Analysis of variance of demipyramid
1988a). length as a function of population density and initial size in field
Initial demipyramid length in the laboratory experiment was experiment. Data are mean values for each cage (3 of 32 cages
estimated from the initial test diameter and the regression of missing due to mortality). SS: sum of squares; MS: mean square
demipyramid length and test diameter calculated from the field data
[In demipyramid length (mm) = 1.101 x In test diameter (mm) - Source of ss MS F
dl
1.547, R2=0.92, N=92, Fig.1]. variation

16.626 44.549 ***

Density 16.616

Results Size 3.336 3.336 8.944**

Interaction 1 0.056 0.056 O.152NS
Error 25 9.324 0.373
In the field experiment, Diadema antillarum changed test Total 28 28.858
diameter in a density-dependent manner, by growth or
shrinkage (Levitan 1989). A two-way ANOVA examining *** P<O.OOl,** P<O.Ol, NSP>O.OS
differences in test diameter as a function of population
density and initial size class indicated a highly significant
effect of density, but not of size (Levitan 1989). A similar high density and the initially large individuals at low and
ANOVA examining differences in demipyramid length high density, respectively; data are weighted means:
indicated that both population density and initial size Fig. 2). The positive deviation of demipyramid length in
were significant factors (Table 1). treatments with positive test growth is expected, since the
The laboratory echinoids changed test diameter (also growth rate of field-collected echinoids was higher than
by growth or shrinkage) as a function of food availability that of experimental echinoids [30 to 35 mm/yr (Levitan
(Levitan 1989, and present Table 2). An ANOVA examin- 1988a) and 12 mm/yr (Levitan 1989), respectively].
ing differences in demipyramid length indicated a signifi- An inverse relationship between food level and rela-
cant effect of food level (Table 3). tive demipyramid size was apparent in the laboratory
Fig. 2 shows the relationship between demipyramid study, which revealed demipyramid length deviations of
length and test diameter for the individuals in the field 0.06,0.94,0.95,1.14 mm for the 4,2,1, and 0 food group,
experiment, the laboratory experiment, and the field col- respectively (data are weighted means: Fig. 2). An
lection. The food-limited individuals in the field experi- ANOVA testing the deviation in demipyramid length in-
ment increased demipyramid size relative to test size. The dicated highly significant differences among the four
increases in relative demipyramid size, measured as the treatments (Table 4). The laboratory individuals fed the
deviation of the demipyramid length from the length pre- maximum ration had a demipyramid : test ratio similar to
dicted by the field sample (for its test size), suggest an that of the field-collected individuals (the deviation of the
inverse relationship between growth rate and relative demipyramid length is within the 95% confidence inter-
demipyramid length. Changes in test diameter were 7.3, vals of the field regression line: Fig. 2).
3.1, -1.7, and -6.7 mm for deviations of predicted To examine whether the changes in the demipyramid
demipyramid lengths of 0.85, 0.94, 1.31, and 1.61 mm, and test were due to an increase in demipyramid length or
respectively (for the initially small individuals at low and a decrease in test diameter (or to some combination of the
DoRo Levitan: Skeletal plasticity in sea urchins 433

Table 2. Diadema antillarumo Growth as a function of food avail- Table 2 (continued)

ability (grams wet wt Ulva lactuca every 4 d) in laboratory experi-
ment. Table shows initial (inotest), final (f.test) and change (dotest) Food Size (mm): (#)
in test size and initial (inodemi), final (f.demi) and change (dodemi) (g)
in demipyramid length, and container number ( # ). Initial demipyra- in.test f.test d.test in.demi f.demi d.demi
mid length predicted from initial test size and the test-demipyramid
regression equation (Fig. 1 and "Materials and methods") 4 46.5 43.7 -2.8 14.59 13.20 -1.31 (33)
4 44.9 47.2 2.3 14.04 14.11 0.07 (47)
Food Size (mm): (#) 4 46.3 48.7 2.4 14.52 14.55 0.03 (48)
(g) 4 42.1 44.5 2.4 13.08 14.23 1.15 (48)
in.test f.test d.test in.demi f.demi d.demi 4 40.9 43.5 2.6 12.67 13.12 0.45 (53)
4 40.2 42.0 1.8 12.43 13.14 0.71 (53)
o 40.5 36.7 -3.8 12.53 12,29 -0.24 (7) 4 44.5 47.3 2.8 13.90 14.55 0.65 (53)
o 39.0 36.5 -2.5 12.02 13.67 1.65 (13) 4 42.5 45.7 3.2 13.21 14.38 1.17 (54)
o 42.4 37.5 -4.9 13.18 13.05 -0.13 (25) 4 47.8 48.9 1.1 15.04 14.93 -0.11 (59)
o 44.0 40.3 -3.7 13.73 14.34 0.61 (39) 4 43.4 42.1 -1.3 13.52 13.59 0.07 (60)
o 42.3 38.3 -4.0 13.14 13.02 -0.12 (39)
o 39.3 36.0 -3.3 12.12 11.05 -1.07 (43)
o 44.8 41.8 -3.0 14.00 13.14 -0.86 (45)
o 40.6 37.7 -2.9 12.56 13.35 0.79 (46)
0 47.0 42.9 -4.1 14.76 13.39 -1.37 (57)
1 43.9 42.1 -1.8 13.69 13.65 -0.04 (5) Table 3. Diadema antillarum. Analysis of variance of changes in
1 45.7 42.1 -3.6 14.31 14.06 -0.25 (6) demipyramid length as function of food level in laboratory experi-
1 45.0 43.2 -1.8 14.07 14.22 0.15 (11) ment. Data are mean size for each container in the laboratory (11
1 40.3 42.5 2.2 12.46 15.19 2.73 (12) of 64 containers missing due to mortality)
1 40.5 37.3 -3.2 12.53 12.12 -0.41 (17)
1 43.6 39.9 -3.7 13.59 14.92 1.33 (17) sv dl ss MS F
1 45.7 40.6 -5.1 14.31 13.61 -0.70 (18)
1 40.0 38.4 -1.6 12.36 13.07 0.71 (31)
1 40.5 38.1 -2.4 12.53 13.09 0.56 Food level 3 13.980
6.067 **
(32) 4.660

1 39.2 39.3 0.1 12.09 12.35 0.26 (37) Error 49 37.636 0.768

1 43.1 37.1 -6.0 13.42 12.21 -1.21 (38) Total 52 51.616

1 42.6 38.6 -4.0 12.25 12.12 -1.13 (44)
1 44.2 41.7 -2.5 13.80 12:82 -0.98 (49)
** P<O.Ol
1 42.2 39.9 -2.3 13.11 13.18 0.07 (50)
1 43.6 40.8 -2.8 13.59 12.54 -1.05 (63)
47.2 43.7 -3.5 14.83 15.62 0.79 (64)
1 42.6 40.2 -2.4 13.25 13.32 0.07 (64)
2 43.8 43.6 -0.2 13.66 15.13 1.47 (3) Table 4. Diadema antillarum. Comparison of laboratory popula-
2 40.4 41.8 1.4 12.50 13.26 0.76 (4) tion with naturally-occurring population. Analysis of variance ex-
2 42.2 40.6 -1.6 13.11 14.25 1.14 (9) amining differences in deviation of demipyramid length from length
2 44.0 42.9 -1.1 13.73 13.51 -0.22 (10) predicted by the field-collected urchins (regression from Fig. 1) as a
2 42.5 41.5 -1.0 13.21 14.21 1.00 (10) function of food level. Data are mean values from each container
2 46.2 42.8 -3.4 14.48 14.93 0.45 (23)
2 46.1 44.4 -1.7 14.45 16.29 1.84 (24)
2 43.3 42.2 -1.1 13.49 13.73 0.24 (29)
2 41.4 42.3 0.9 12.84 13.82 0.98 (30)
2 42.4 41.9 -0.5 13.18 13.56 0.38 (35)
2 45.9 43.1 -2.8 14.38 16.15 1.77 (36)
2 44.0 41.6 -2.4 13.73 13.24 -0.49 (41)
2 45.4 41.5 -3.9 14.21 13.18 -1.03 (42)
** P<O.Ot
2 42.5 41.7 -0.8 13.21 13.29 0.08 (55)
2 41.3 40.7 -0.6 12.80 13.33 0.53 (55)
2 39.6 40.9 1.3 12.22 14.75 2.53 (56)
2 45.1 44.3 -0.8 14.11 13.54 -0.57 (61)
2 42.1 44.9 2.8 13.08 13.87 0.79 (62) two ), the change in demipyramid length was plotted
4 42.2 42.6 0.4 13.11 13.07 -0.04 (1) against the change in test dia,meter (Fig. 3). Only the lab-
4 44.8 50.0 5.2 14.00 14.16 0.16 (1) oratory results are plotted, since the exact initial sizes of
4 43.9 45.3 1.4 13.69 15.04 1.35 (2) the individuals from the field experiment were unknown
4 39.5 42.1 2.6 12.19 12.57 0.38 (16)
4 47.6 47.8 0.2 14.97 14.53 -0.44 (due to mortality of some individuals). When food was
(16)
4 44.8 45.7 0.9 14.00 16.55 2.55 (16) limiting, proportionally more growth occurred in the
4 47.8 47.1 -0.7 15.04 15.86 0.82 (21) demipyramid than in the test. On an absolute scale, how.
4 39.2 36.8 -2.4 12.09 12.27 0.18 (21) ever, demipyramid growth diminished with decreasing
4 45.2 46.2 1.0 14.14 15.08 0.94 (22) food availability. When food was moderately limiting,
4 45.6 47.2 1.6 14.28 14.72 0.44 (27) the test decreased in size while some growth occurred in
4 44.9 48.3 3.4 14.04 14.10 0.06 (28)
4 43.8 44.6 0.8 13.66 13.89 0.23 the demipyramid. When food was severely limiting, the
(28)
4 41.4 40.3 12.84 13.57 0.73 (28)
test decreased in size and the demipyramid stopped grow-
4 46.6 47.6 .0 14.62 15.86 1.24 (33) ing or perhaps decreased slightly in size.
434 D. R. Levitan: Skeletal plasticity in sea urchins

shrank around them (as suggested by the present study).

E 2
.5
Since the jaws of the starved echinoids became relatively
~ larger, but showed no indication of growth, negative test
0,
~
"
.J
"0
.e
0.5
0
* growth seems to be the most parsimonious explanation.
Ebert also noted clear tetracycline lines in the coronal
~
>-
.~
E
"
o -0.5
S
0

t-+ plates of some fed individuals, and faint lines in the

starved individuals. The presence of faint tetracycline
lines in the starved echinoids, suggesting some calcite
" addition in these individuals, presents an unresolved
"'
~ -1 problem and underscores our ignorance of the mecha-
..
~
0 nisms of calcite deposition and resorption in echinoids.
1.5
-4 -3 -2 -1 O 2 Pearse and Pearse (1975) found no evidence ofresorp-
Change in Test Diameter (mm) tion in two tetracycline studies of starved and fed
Fig. 3. Diadema antillarum. Change in demipyramid length vs Strongylocentrotus purpuratus. However, in their 3-mo-
change in test diameter for laboratory experiment. Data points show long study, the eight individuals in the starvation treat-
means:!: standard errors; numbers indicate grams wet wt Ulva lac- ment had a slight weight gain (6%). This was attributed
tuca fed every 4 d. Line shows predicted ratio of In test diameter and to nutrients from ingested wood and other debris found
In demipyramid length from slope of the tield-collected sea urchins in the gut. In their 2-yr experiment, two individuals fed
discontinuously (over four, 3- to 4-wk starvation periods)
lost weight in only one starvation period. Perhaps the
Discussion periods of -stress were not long enough to cause resorp-
tion of skeletal elements.
These results on Diadema antillarum are consistent with Lewis et al. (1990) found no evidence of resorption of
those reported by Ebert (1980), Black et al. (1982, 1984) 45calcium from the test of starved Strongylocentrotus pur-
and Edwards and Ebert (1991) in that the relative size of puratus and its transfer and deposition in the still growing
the demipyramid increased when echinoids were food- teeth. They suggested that resorption may take longer
limited. High plasticity in Aristotle's lantern has been than the 4-wk starvation period of their study.
noted in several species of sea urchins (Ebert 1988). The Markel (1979, 1981) found differences in the patterns
present study documents that, for D. antillarum, this rela- of calcification and resorption in cidaroid and non-
tionship primarily is due to a decrease in the size of the cidaroid echinoids. Pearse and Pearse ( 1975) and Lewis et
test. When food is limiting, more growth occurs in the al. (1990) found no evidence of skeletal reworking in
demipyramids compared to the test, but demipyramid Strongylocentrotus purpuratus. The differences in the
growth diminishes on an absolute scale (also noted by rates or patterns of calcite deposition and resorption be-
Edwards and Ebert 1991). This suggests that proportion- tween Diadema and Strongylocentrotus species may be
ately more energy is being allocated to jaw growth as the taxonomic and perhaps related to the faster growth and
total amount of available energy diminishes. The thinner test of Diadema spp. [see Ebert (1982) for com-
changed demipyramid : test ratio induced by shifting en- parative growth data]. Investigations of taxonomic dif-
ergy allocation is greatly enhanced by the shrinking test. ferences in skeletal plasticity should compensate for dif-
The decrease in the size of the test of echinoids when ferences in growth rate by an appropriate scaling of the
food is limited has been known for some time (Ebert experimental time frame.
1967, Cocanour 1969, Dix 1972, Moss and Lawrence The ecological significance of plasticity in body com-
1972, Levitan 1988 b, 1989). In addition, a small amount ponents is that individuals can maximize reproductive
of calcite resorption takes place in the plates of the test output under rapidly changing conditions of food
during normal growth (Loven 1892, Deutler 1926, Gor- availability and population density. This is accomplished
don 1926, Mortensen 1927, Cutress 1965, Regis 1979, by an increase in the relative size of Aristotle's lantern,
MarkeI1981). Markel's study, using tetracycline growth thus increasing energy intake (Ebert 1980, Black et al.
lines and SEM, suggest clear zones of resorption in the 1984), and a decrease in the size of the body, thus decreas-
interambulacral plates of both Eucidaris tribuloides and ing the energetic costs of maintenance (Ebert 1968,
Diadema antillarum during growth. Calcite is resorbed in Sebens 1982, Levitan 1988 b, 1989).
both echinoid spines (Markel and Roser 1983) and parts The ratio between the demipyramid and test can be
of Aristotle's lantern (MarkeI1979). used to ascertain the nutritional status of echinoids. Once
Feeding and starvation studies of urchins injected with the relationship between test and jaw size is established in
tetracycline give equivocal evidence of skeletal reworking a population of well-fed individuals, the degree of devia-
and perhaps of calcite resorption. In Ebert's (1980) study, tion from this ratio can be used as an index of food
a clear tetracycline growth line was found in the jaws of limitation for that species. This can be done at one sam-
Diadema setosum that were fed, but not in those that were pling period, and may be preferable to monitoring long-
starved. The starved echinoids had relatively larger jaws term growth experiments which necessitate repeated
compared to the fed individuals. The lack of tetracycline measures of tagged individuals. This technique could be
lines on the jaws of starved echinoids suggest that these important for studies investigating intra- and inter-
individuals either reworked calcite (as suggested by specific competition. It may also be important for studies
Ebert) and/or that the jaws did not grow and the test investigating whether small size is due to age or food
D. R. Levitan: Skeletal plasticity in sea urchi!

availability. Individuals which are size-stunted, due to Ebert, T. A. (1988). Allometry, design and constraint of body com-
food limitation, would have larger jaws compared to ponents and shape in sea urchins. J. nat. Hist. 22: 1407-1425
Edwards, P. B., Ebert, T. A. (1991). Plastic response to limited food
young well-fed individuals.
availability and spine damage in the sea urchin Strongylocentro-
The paleobiological implications of this phenomenon tus purpuratus (Stimpson). J. exp. mar. BioI. Ecol. 145: 205-220
include a record of biotic interactions in an echinoid's Estes, J. A., Palmisano, J. F. (1974). Sea otters: their role in structur-
skeleton. Many biotic interactions influence per capita ing nearshore communities. Science, N.Y. 185: 1058-1060
food availability. These interactions include intra- or in- Gordon, I. (1926). The development of the calcareous test of Echi-
terspecific competition for food, changes in predation nus miliaris. Phil. Trans. R. Soc. (Ser. B) 214: 259-312
Hay, M. E. (1984). Patterns offish and urchin grazing on Caribbean
pressure affecting that competition, and factors influenc-
coral reefs: are previous results typical? Ecology 65: 446-454
ing the productivity of the algal resource. Present-day Lessios, H. A., Robertson, D. R., Cubit, J. D. (1984). Spread of
examples are known of temporal and spatial shifts in the Diadema mass mortalities through the Caribbean. Science, N .y:
abundance of competing species (Hay 1984), predators 226: 335-337
(Estes and Palmisano 1974) and conspecifics (Pearse and Levitan, D. R. (1988a). Algal-urchin biomass responses following
Hines 1979, Miller and Colodey 1983, Lessios et al. 1984, the mass mortality of Diadema antillarum Philippi at Saint John,
U.S. Virgin Islands. J. exp. mar. BioI. Ecol. 119: 167-178
Scheibling 1984, Scheibling and Stephenson 1984, Levi-
Levitan, D. R. (1988 b). Density-dependent size regulation and neg-
tan 1988 a). Analysis of relative demipyramid size of mu- ative growth in the sea urchin Diadema antillarum Philippi. Oe-
seum collections and fossil specimens of extant species in cologia 76: 627-629
combination with present-day experiments can provide Levitan, D. R. (1989). Density-dependent size regulation in Diade-
evidence of changes in food availability and community ma antillarum: effects on fecundity and survivorship. Ecology
structure in times past (Levitan in preparation). 70: 1414-1424
Levitan, D. R. (1991). Detecting biotic interactions in times past:
influence ,of human fishing pressure on algal-urchin interactions
(in preparation)
Acknowledgements. I wish to thank S. Genovese and C. Levitan for Lewis, C. A., Ebert, T. A., Boren, M. E. (1990). Allocation of
assistance in the field. R. Aronson, R. Karlson, J. Lawrence, R. 45calcium to body components of starved and fed purple sea
Martin, R. Mooi, D. Pawson and M. Sewell made helpful com- urchins (Strongylocentrotus purpuratus) Mar. BioI. 105: 213-
ments on this manuscript. The U .S. National Park Service, Virgin 222
Islands Ecological Research Station, University of the Virgin Is- Loven, S. (1892). Echinologica. K. svenska VetenskAkad. Handl.
lands, School For Field Studies, University of Delaware, and Bam- 18: 1-73
field Marine Station provided support and facilities. Miirkel, M. (1979). Structure and growth of the cidaroid socket-
joint lantern of Aristotle compared to the hinge-joint lanterns of
non-cidaroid regular echinoids (Echinodermata, Echinoidea).
Zoomorphologie 94: 1-32
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D. dissertation. University of Maine, Orono and protein levels with age and seasonin the sand dollar Mellita
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