BULLETIN
OF MARINE SCIENCE.
RELATIVE
30(2): 467-474. 1980
CORAL REEF PAPER
GROWTH OF SEA URCHIN JAWS: AN EXAMPLE OF
PLASTIC RESOURCE ALLOCATION
T. A. Ebert
ABSTRACT
The tropical sea urchin Diadema setosum was grown in Zanzibar from 1976 to 1977 in the
field and in a large indoor tank. After I year, animals in the indoor tank had jaws (halfpyramids of Aristotle's lantern) that were relatively larger than the jaws of urchins in the
field. The most obvious difference between the field and the tank was that there was less
food in the tank. The hypothesis that available food led to an adaptive response in growth
was partially tested by examining samples of the urchin Strongylocentrotus purpuratus from
areas of Sunset Bay, Oregon, with documented food differences. The samples of S. purpuratus supported the hypothesis that low food availability leads to increased size of the
food gathering apparatus in sea urchins.
A change or shift in resource allocation among body parts or phys-iological
functions in different environments is called an organism's plastic response; such
a response may be adaptive (Bradshaw, 1965; Hickman, 1977; Gilbert, 1966,
1968). Like plants, many marine invertebrates, because of limited abilities to
change habitats, must grow in accordance with opportunities provided by the
environment, so adaptive morphological plasticity would be expected (Bradshaw,
1965).
There is a growing body of evidence that echinoids frequently are food limited
(Lawrence, 1975) so adaptive plasticity is likely to occur in allocation to structures
associated with food gathering. The purpose of this paper is to present information
on what can be interpreted as an adaptive allocation in two sea urchin species in
response to availability of food.
METHODS
The allocation hypothesis for urchins emerged as an attempt to explain a curious anomaly in data
from a growth study of Diadema setosum in Zanzibar. As part of the growth study, 383 D. setosum
were collected at Yange Sand Bank off the port of Zanzibar (16 June 1976) and individuals tagged
with 4 mg of tetracycline in 0.2 ml of sea water (Kobayishi and Taki, 1969). Then 358 urchins were
placed at the sea water intake of the East African Marine Fisheries Research Organization laboratory
and 25 were placed in a large sea-turtle tank inside the EAMFRO lab. In addition, 74 animals were
collected at the sea water intake, tagged and returned.
The sea water intake is a pile of concrete rubble at a depth of about 2 m surrounded by silty sand
and was selected as a suitable location for studying growth because it supported a population of D.
setosum, which appeared to be confined to the rubble. Macroalgae were present on the rubble and
turtle grass (probably Thalassia sp.) grew on the surrounding sand.
The turtle tank is constructed of concrete and is about 2.5 m deep and 5 m across. It is inside the
EAMFRO laboratory and receives no direct sunlight and very little natural light. No macroalgae were
apparent in the tank.
Urchins were permitted to grow for I year and were then collected for study. They were dried in
sunlight in the open, then shipped to San Diego.
Half-pyramids of Aristotle's lantern-jaw
elements-were
used to measure growth; tetracycline
fluoresces under ultraviolet light and growth in length could be measured without need to grind parts
(Ebert, 1977). Five pyramids, each consisting of two demi- or half-pyramids, constitute the major
skeletal elements of the lantern. The pyramids are the support structures of the teeth which project
from the oral ends of the pyramids, run through the inside of the pyramids and curl into the dental
sac on the aboral side of the lantern. The ever-growing teeth develop at their aboral ends and move
through the pyramids to the mouth (Hyman, 1955). Length of the half·pyramids was measured with
467
468
BULLETIN
OF MARINE SCIENCE. VOL. 30, NO.2,
1980
vernier calipers from Ihe oral tip to the flat shoulder al the aboral end: the articulating surface between
the half-pyramid and its epiphysis. This articulation is at the aboral end of the ridges on the jaw where
interpyramidal or comminator muscles attach.
RESULTS
AND DISCUSSION
There were two surprising results: (1) no animal in the turtle tank showed a
clear tetracycline mark in its jaws; and (2) urchins in the turtle tank had relatively
larger jaws than animals at the sea water intake.
Of the 86 Diadema setosum collected from the sea water intake at the EAMFRO laboratory in Zanzibar, 57 or 66% had clear tetracycline marks and 29 were
apparently without a mark or showed confusing patterns of fluorescence. Of the
]4 D. setosum recovered from the turtle tank, none showed a clear mark in the
jaws although faint lines were evident in coronal plates of 11 individuals indicating
that a small amount of growth had taken place. Because animals in the tank and
in the field were tagged at the same time, 66% of the animals from the turtle tank
(9 individuals) would be expected to have tagged jaws. The difference between
recovery of individuals with tagged jaws from the sea water intake and from the
turtle tank is highly significant when tested for independence of mark and location
2
(X calc = 15.96; X2"~0.01 = 6.64).
The lack of tetracycline lines in the jaws of urchins in the turtle tank is a
fascinating problem. Jaws of over one half of the animals were growing when
they were injected with tetracycline as indicated by 66% with a clear mark in the
jaws at the sea water intake. It is also clear that 11 (78%) of the animals in the
turtle tank were growing at the time of tagging because tetracycline was taken-up
by the coronal plates. Two possible explanations for lack of tetracycline lines in
the jaws of urchins in the turtle tank are: (1) animals placed in the turtle tank had
growing coronal plates and non-growing jaws but animals placed at the sea water
intake had both coronal plates and jaws which were depositing calcium carbonate
when tagged; or (2) growth of jaws and coronal plates were similar for animals
placed in both areas but something happened to the tetracycline incorporated into
the skeleton of animals in the turtle tank. A reasonable hypothesis is that the
jaws and to a lesser extent the coronal plates of animals in the turtle tank were
reworked; calcite was resorbed and redeposited.
Tetracycline has a very short life once mixed with sea water and probably lacks
ability to tag the growing skeleton after a day or two under tropical conditions
(Barnes, 1971); however, once tetracycline is incorporated into the skeleton it is
protected from oxidation. Skeletal parts are cleaned with the oxidant sodium
hypochlorite (5% solution) to remove tissue without damaging the tetracycline
lines in the skeleton.
All animals had been collected from the same location at Yange Sand Bank and
so the urchins placed at the water intake and in the turtle tank should have been
growing about the same for their first day or two, and so initially would have
incorporated the same amount of tetracycline.
There is evidence for skeletal reworking in urchins and this explanation seems
more reasonable then suggesting that there were initial differences in growth
between the urchins placed at the two locations. Negative growth has been shown
in Strongylocentrotus purpuratus (Ebert, 1967), resorption has been described in
Echinus and Eucidaris (Gordon, 1926; Cutress, 1965), and extensive reworking
of the skeleton has been argued (Nichols and Currey, 1968) on more theoretical
grounds concerning the repair of hairline fractures in the calcite crystal. Pearse
and Pearse (1975), however, found no evidence of reworking in starved S. purpuratus.
EBERT: GROWTH OF SEA URCHIN JAWS
469
Figure 1. Half-pyramids-jaw
elements-of Aristotle's lantern from two individuals of the sea urchin
Diadema setoslIm in Zanzibar. Jaws are 1.5 em and 1.8 em long and came from animals of similar
diameter (4.6 cm). Jaw on the left is from an animal from the sea water intake. while the jaw on the
right is from an urchin held in the turtle tank at EAMFRO. Arrows indicate points used in measuring
length: from the oral tip (bottom arrow) to the epiphysis junction (top arrow). Ridges are sites of
muscle attachment.
The relative difference in size of jaws of animals from the turtle tank and sea
water intake is shown in Figures I and 2. Figure 1 shows half-pyramids
from
animals of similar test diameter (4.6 cm) but from the two environments.
Thejaw
from the animal in the turtle tank is 1.8 cm long compared with 1.5 cm for the
animal at the sea water intake.
In Figure 2, two clusters of points are evident with animals from the turtle tank
showing relatively much larger half-pyramids
than animals from the sea water
intake. The sums of squares for the analysis of covariance of loge transformed
data are given in Table 1. The slopes cannot be separated at the 5% level (F1,95 =
0.395; Feril "=0.05 = 3.94) but the adjusted means, and hence the V-intercepts,
are different (FI•95 = 68.14). Using the common slope, the two regression equations are, with L = half-pyramid length and 0 = test diameter:
water intake:
In L
=
0.9156 In 0 - 1.0597
(1)
turtle tank:
]n L
=
0.9156 ]n 0 - 0.8577
(2)
470
BULLETIN
OF MARINE SCIENCE, VOL. 30. NO.2.
1980
2.2
•
2.0
IntakeN=84
.& Turtle Tank N= 14
1.8
-
1.6
-
1.4
E
2
.c
Cl
C
Q)
--.J
~
1.2
-,ro
1.0
0.8
0.6
0.4
1
2
4
3
5
6
7
8
Test Diameter (em)
Figure 2. Jaw (half-pyramid) length vs. test diameter; Diadema setoslim. Zanzibar, 1977; upper line
is for animals in the turtle tank; lower line for urchins at the sea water intake.
For descriptive purposes, because both measurements are subject to error, a
functional regression (Ricker, 1973) is more appropriate. The common functional
slope is equa1 to the predictive common slope (0'.9156, Table 1) divided by the
common correlation coefficient obtained from the common sums of squares in
Table 1 which is equal to 0.899. The functional slope v is equal to 1.02 which is,
for practical purposes, equal to 1.00. The functional relationships are:
water intake: L
turtle tank:
L
=
=
0.3080D
0.3733D
or
or
D
D
=
=
3.246L
2.679L
(3)
(4)
The obvious differences between what now can be called two treatments are:
water movement, light, food (very little in the turtle tank), and, of course, density
of turtles. Low food availability was evident in the animals shipped to me. The
guts of the urchins from the turtle tank were packed with chips of paint, and so
food difference was the most attractive possible reason for the observed differ-
EBERT: GROWTH OF SEA URCHIN JAWS
471
J
t-
*
tt-
0\
I'<)
t-
OCNON
\0
t-
NN
00 -
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t-Ol'<)
\Ot-O
00 00 00
\0 00
00 N
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0\0
0"":
Cs
-
..:.
<1oi*
0-
"u".~
I:
0""
uo""
oon
Non
00
00
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00
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o
00
,
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til
'"'"
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>
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t- -
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t- on
O\-'<t
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ooN'<t
ONon
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'<t
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on on 0
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00
-N
onNon
-1'<)0
00
000
I
00 00
'<tl'<)
0\I'<)
z
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Non
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.~
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00 -
z
on
00
000
0\ on on
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00
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-
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-
N
472
BULLETIN OF MARINE SCIENCE.
VOL. 30. NO.2.
1980
1.4
1.2
e-
1.0
.g
-
or. 0.8
OJ
c:;
Q)
...J
0.6
...,co==
0.4
•
Boulder Field N=21
o
Eel Grass Area N=23
•. Poslelsia Zone N=30
0.2
3
4
5
6
7
8
9
Test Diameter (em)
Figure 3. Jaw length vs. test diameter; Strongylocentrotus purpuratlls. Sunset Bay, Oregon, 1964;
upper line for animals in the Postelsia Zone and Eel Grass Area (low food); lower line for urchins
with more food (Boulder Field).
ences in jaw size. The response could be interpreted as adaptive and furthermore
the hypothesis that jaw size was related to food abundance is testable.
If differences in food availability cause changes in allocation to Aristotle's
lantern, with greater relative allocation under low food conditions, then field
collections of urchins living under documented different food regimes would show
the same allocation difference as those of Diadema setosum in Zanzibar.
A collection of Strongylocentrotus purpuratus had been made in Sunset Bay,
Oregon, in August 1964. Animals came from three regions that differed in the
amounts of available food which was shown in the field by measuring the amount
eaten per day after feeding urchins small pieces of tattooed algae and killing the
animals after 24 h and weighing the amount of food in the gut between the mouth
and the tattooed algae; by the differences in probability of accepting a small piece
of tattooed algae; by differences in amounts of drift algae held by urchins in
different areas; and by measuring the amounts of less desirable food in the guts
(calcareous algae) (Ebert, 1968). The three areas have been designated, in order
of increasing availability of food: the Postelsia Zone (30 individuals collected),
Eel Grass Area (N = 23), and Boulder Field (N = 21). Food differences also
were indirectly evident by showing that animals in the Boulder Field grew faster
and larger than animals in the other two areas. There also were differences in
gonad development: urchins in the Postelsia Zone had the smallest gonads (Ebert,
1968).
Urchins collected in the three areas of Sunset Bay previously had been used
to analyze spine repair and regeneration (Ebert, 1968). Half-pyramids of the Sunset Bay urchins were measured and plotted vs. test diameter (Fig. 3). Regressions
473
EBERT: GROWTH OF SEA URCHIN JAWS
of the loge transformed data for the animals in the three areas (Table 2) have
similar slopes (F2.70= 1.66; Ferita=o.05= 3.13). The adjusted means, however,
are significantly different (F2•70 = 73.73). Using Snedecor and Cochran's (1956)
modification of Tukey's test for significant differences among adjusted means,
animals from the Postelsia Zone and Eel Grass Area cannot be distinguished at
a = 0.05 but both areas have animals which are distinct from animals in the
Boulder Field with respect to the relationship between jaw length and test diameter. The urchins from the Poste/sia Zone and Eel Grass Area have a Yintercept significantly higher than the urchins in the Boulder Field. With a common slope and two distinct populations (I) EG and PZ and (2) BF, the regression
equations are:
combined PZ and EG:
BF:
In L
In L
=
=
0.8580 In D - 1.3052
0.8580 In D - 1.4816
(5)
(6)
The functional regressions using a common slope are:
combined PZ and EG:
BF:
L
L
= 0.2685Do.8658 or D = 4.5667L1.I550
=
0.2245Do.8658 or
D
=
5.6197L1.I550
(7)
(8)
The results are consistent with the prediction based on Diadema setosum from
Zanzibar and strengthen the tentative conclusions concerning cause and effect:
that food availability leads to differences in allocation to the jaw apparatus.
Under different conditions of available food, urchins of the two species appear
to respond by adaptive allocation of resources. When food is scarce, relatively
more of the urchin's available resources are devoted to the food gathering apparatus. The advantage of the larger half-pyramids probably is the increased
strength in scraping: muscles connecting pyramids together are those associated
with pulling the teeth together. Whether the relative increase in size of the halfpyramids is a direct result of low food level or due to more intense rasping cannot
be deduced from the current study.
Negative growth of the test in Strongylocentrotus purpuratus was associated
with low food (Ebert, 1967, 1968) and reworking of the half-pyramids in Diadema
setosllm appears to be associated with food availability. The adaptive significance
of the relationship between food availability and reworking of the skeleton is not
clear unless it is energetically less expensive to remodel than to build with new
materials. Clearly data are needed to show how CaC03 becomes functionally
available to urchins and how it is related to the energetics of microarchitectural
construction.
The ability to rework skeletal elements suggests that plastic resource allocation
to the jaws in urchins may not be a permanent expenditure but subject to remodeling if food changes for a given animal. The ability to grow and shrink parts
would be highly adaptive in environments with fluctuating food supplies which
include food limitation. A jaw/test ratio may prove to be a useful way of describing
food conditions in field populations of urchins. The prediction concerning shrinking jaws could be easily tested using fast growing urchins such as Diadema sp.
ACKNOWLEDGMENTS
Space and support at the East African Marine Fisheries
Research
Organization
laboratory
was
made available to me through the kindness of the government
of Tanzania and the laboratory director
Mr. G. E. B. Kitaka. Mr. R. Nzioka of EAMFRO helped in the field in 1976 and collected and shipped
urchins to me in 1977. This work was supported
by grant DES75-I0442
from the National Science
Foundation
and by the State of California
which granted me a sabbatical
leave. The manuscript
benefitted from the critical comments
of P. Frank, C. Hickman and J. Hickman and two anonymous
reviewers.
474
BULLETINOF MARINESCIENCE,VOL.30, NO.2, 1980
LITERATURE
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---.
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DATE ACCEPTED: February 23, 1979.
ADDRESS: Department of Biology, San Diego State University, San Diego, CA 92182.