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Annual reversible plasticity of feeding
structures: cyclical changes of jaw
allometry in a sea urchin
rspb.royalsocietypublishing.org
Thomas A. Ebert1, José Carlos Hernández2,† and Sabrina Clemente2,†
1
2
Research
Cite this article: Ebert TA, Hernández JC,
Clemente S. 2014 Annual reversible plasticity
of feeding structures: cyclical changes of jaw
allometry in a sea urchin. Proc. R. Soc. B 281:
20132284.
http://dx.doi.org/10.1098/rspb.2013.2284
Received: 2 September 2013
Accepted: 10 January 2014
Subject Areas:
ecology, evolution
Keywords:
morphology, Strongylocentrotus purpuratus,
Aristotle’s lantern, fitness, reaction norm,
Oregon
Author for correspondence:
Thomas A. Ebert
e-mail: [email protected]
†
Present address: Departamento de Biologı́a
Animal (Ciencias Marinas), Universidad de La
Laguna, La Laguna, Tenerife, Islas Canarias.
Department of Zoology, Oregon State University, Corvallis, OR 97331, USA
Department of Biology, Villanova University, Villanova, PA 19085, USA
A wide variety of organisms show morphologically plastic responses to
environmental stressors but in general these changes are not reversible.
Though less common, reversible morphological structures are shown by a
range of species in response to changes in predators, competitors or food. Theoretical analysis indicates that reversible plasticity increases fitness if organisms
are long-lived relative to the frequency of changes in the stressor and morphological changes are rapid. Many sea urchin species show differences in the sizes
of jaws (demi-pyramids) of the feeding apparatus, Aristotle’s lantern, relative to
overall body size, and these differences have been correlated with available
food. The question addressed here is whether reversible changes of relative
jaw size occur in the field as available food changes with season. Monthly
samples of the North American Pacific coast sea urchin Strongylocentrotus
purpuratus were collected from Gregory Point on the Oregon (USA) coast and
showed an annual cycle of relative jaw size together with a linear trend from
2007 to 2009. Strongylocentrotus purpuratus is a long-lived species and under
field conditions individuals experience multiple episodes of changes in food
resources both seasonally and from year to year. Their rapid and reversible
jaw plasticity fits well with theoretical expectations.
1. Introduction
Developmental variation of organisms in response to environmental stresses is
well known and there are numerous examples of morphological, physiological,
behavioural and life-history changes [1–6]. Plastic responses are a part of the
norms of reaction of a species and can be continuous or discontinuous and
reversible or irreversible [7]. Most morphological responses are not reversible
and can occur in both short- and long-lived species, such as rotifers [8] and
trees [9]. Less common is reversible plasticity of morphological structures.
Reversible plasticity shows increased fitness if stresses occur many times over
the lifespan of individuals. This relationship has been modelled in the context of
the mode and breadth of tolerance functions [10] and a plastic response to stress
may shift the mode or the variance (breadth) of a tolerance function. There are lags
in the plastic response to changing stress both from the non-stressed condition to
the stressed and back again as stress is relieved, and the changes may show a hysteresis curve rather than just following a reverse path. Ideally, the response times
in both directions should be short to provide maximum fitness.
Examples of reversible morphology include both structures associated with
food and feeding as well as defence from predators. The development of a carnivore morph from an omnivore morph in spadefoot toad tadpoles can be shifted
back towards a more omnivore morphology by changing diet [11]. Tree frog tadpoles show reversible morphological changes in response to changes in presence
of dragon fly nymphs [12]. Some snakes show a rapid increase in intestinal mass
following a meal [13] and this is followed by reduction as the meal is digested.
Morphological changes have been documented in perch (fish) following shifts
in habitat complexity and food type [14]. Galápagos marine iguanas resorb
bone and shrink during low food conditions associated with El Niño but recover
bone and increase in size when food availability improves [15]. In birds, gizzard
size in Japanese quail has shown reversible changes to dietary fibre with a
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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(a) Study species and site
The purple sea urchin S. purpuratus has a reported geographical
range from Isla Cedros, Baja California (288 N) [41] to at least
Torch Bay, Alaska (58.338 N) [42] and is a common and abundant
member of both intertidal and subtidal environments. Monthly collections of 20 S. purpuratus were made in the intertidal at Gregory
Point, Oregon (438200 2400 N; 1248220 3000 W) from January 2007 to
July 2009 as part of a study of gonad development related to latitude and ocean conditions [40]. Gregory Point is 0.7 km
northwest of Sunset Bay where S. purpuratus has been studied for
many years [43,44]. Measurements used for gonad analysis were
test diameter and height, total wet weight, and gonad weight. Following dissection, body walls and lanterns were saved and
bleached with sodium hypochlorite, soaked in tap water to
remove residual bleach and dried. Specimens were saved and subsequently jaws (demi-pyramids) of Aristotle’s lantern were
measured with digital callipers. Four of the saved samples were
missing lantern parts and so reduced the analysis to 615 individuals. Jaw measurements were from the oral tip of the jaw to the
distal shelf that articulates with the epiphysis as used in previous
studies [44]. All data have been archived and are available [45].
(b) Methods of analysis
The approach to analysis was to look for an annual cyclical
pattern of jaw length, J, relative to test diameter, D, or total
J ¼ aDb
ð2:1Þ
or
ln J ¼ lna þ b lnD.
ð2:2Þ
Analysis of the annual cyclic change in jaw size started with a
modification of a general model used to describe biocycles [46]:
2p
yi ¼ A þ M cos
ð2:3Þ
ti þ f þ e i :
t
Two additional parameters were then added to permit b to vary
seasonally. Also, year-to-year variation in jaw allometry could
occur. To model these additional complications, equation (2.3)
was modified [40]:
2p
ln J ¼ A þ M cos
ti þ f þ b lnD
t
2p
þ C cos
ð2:4Þ
ti þ f lnD þ B1 ti þ ei :
t
where lnD ¼ ln-transformed test diameter, D; A ¼ the mean of
lna, which in equation (2.4) was seasonally adjusted by
M cosðð2p/tÞ þ fÞ; M ¼ the amplitude of half the total predicted
change of lna; t ¼ duration of one cycle, which was fixed at 1.0
year; ti ¼ time in years when samples were collected starting
with 0 at 1 January 2007; f ¼ lag from reference time of the
crest of the cycle; b ¼ mean of the allometric exponent adjusted
seasonally by C cosðð2p/tÞti þ fÞ; C ¼ the amplitude of one
half predicted change in b, and so similar to M; B1 ¼ coefficient
of linear change with time, ti; and e i ¼ error.
The inclusion of a coefficient of linear change with time, B1, is
appropriate in this study but probably would have to be changed
for other datasets. For example, a second-order term has been
included in analysis [40], but with datasets spanning many
years direct inclusion of environmental data probably would
be preferable to adding additional higher order terms.
Parameter estimates were made by nonlinear regression [47]
using all data, including outliers. Analyses were done with and
without the linear term, B1, and with and without an annual
cycle of allometric change. Comparison of these four models
was made using Akaike’s Information Criterion [48] with small
sample adjustment, AICc:
AIC ¼ nlnðs2 Þ þ 2K:
ð2:5Þ
The number of parameters, K, includes SSE so, for example,
in equation (2.4) with both cyclic and linear change with time,
K ¼ 7. AIC differences, Di, were computed and used to calculate
Akaike weight, wi, which is the weight of evidence of model i
being the best model of the group of models considered.
Measuring diameter and height of living sea urchins is not easy
because spines and associated tubercles can interfere with positioning calliper jaws. Sea urchins are not circular around the
ambitus but rather slightly pentagonal and so a measurement of
maximum diameter requires positioning callipers running from
the centre of an ambulacral area to the centre of the opposite interambulacral. There are also problems with positioning calliper jaws
perpendicular to the sea urchin test. All of these problems can lead
to errors or biases in measurement [49]. It is reasonable, however,
to assume that unlike linear measurements, weight measurements
with a digital balance are mostly free of problems of investigator
technique although inconsistency in removing excess water can
lead to errors. Comparison of linear and weight measurements
over time can address the problem of consistency. There is also a
problem that monthly collections might have been made at slightly
different microhabitats and so any trends may not indicate the performance of a single site. We approach this problem by asking
2
Proc. R. Soc. B 281: 20132284
2. Material and methods
wet weight, T. The starting point for analysis was the basic
allometric equation
rspb.royalsocietypublishing.org
hysteresis curve of gizzard length [16] and the bills of marsh
sparrows change in size on an annual cycle associated with
growth of the keratinized rhamphotheca [17]. The sea urchin
Strongylocentrotus purpuratus has shown changes in demipyramid ( jaw) size in response to changes in available food,
and jaws become relatively larger at a low feeding rate; the
pattern can be reversed if food is increased [18,19].
Differences in the relative size of jaws (demi-pyramids) of
Aristotle’s lantern or the entire lantern have been reported for
a large number of sea urchin species in field studies, including
S. purpuratus [20], Mesocentrotus (Strongylocentrotus) franciscanus
[21,22], Strongylocentrotus droebachiensis [23,24], Echinometra
mathaei [25,26], Diadema setosum and Diadema antillarum
[25,27], Sterechinus neumayeri [28], Evechinus chloroticus [29],
Arbacia punctulata [30], Centrostephanus rodgersii [31] and
Heliocidaris erythrogramma [32]. Changes in jaw and diameter
allometry also have been induced under laboratory conditions
of food manipulations in S. purpuratus [18,33,34], S. droebachiensis
[24,35], M. franciscanus [36,37], D. antillarum [27], Paracentrotus
lividus [38] and Lytechinus variegatus [39].
Under laboratory conditions, the change in relative lantern or jaw size can be rapid as reported for S. purpuratus
[33], where well-fed sea urchins developed relatively smaller
jaws than the original field sample within a month. The time
and shape of the reverse course, however, have not been
studied in detail [18,19].
Where food is scarce, jaws tend to be large relative to test
diameter. Consequently, the relationship between jaw length
and test diameter should reflect food conditions in the field
and be correlated with growth rates as shown for M. franciscanus
[22]. Available food changes seasonally along the Pacific coast of
North America [40], and given rapid responses of jaw allometry
observed in the laboratory, seasonal changes in relative jaw
length would be expected under field conditions. This is the
hypothesis we explore for S. purpuratus.
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diameter (cm)
8
6
4
1.70
jaw length (cm)
1.50
1.30
1.10
0.90
0.70
0.50
total wet weight (g)
300
200
100
0
J M M J S N
2007
2008
year
2009
Figure 1. Monthly samples of S. purpuratus at Gregory Point, OR, USA, showing
the distributions of diameter and wet weight measured on live sea urchins, and
length of jaws (demi-pyramids) measured on bleached specimens.
whether sizes in collections changed and whether there was a
change in height versus diameter.
3. Results
Monthly samples collected at Gregory Point always contained
a range of sizes (figure 1). Diameter measurements for the 620
dissections had a range of 2.53–9.17 cm with a mean of 6.15
(1.35 s.d.) cm. Total wet weight ranged from 8.26 to 297.7 g
with a mean of 119.62 (62.66 s.d.) g. Jaw (demi-pyramid)
measurements ranged from 0.53 to 1.64 cm with a mean of
1.12 (0.22 s.d.) cm (N ¼ 615).
Analysis of lnJ as a function of lnD and time (table 1)
showed that the model with the most support, largest wi
(99.6%), was the one with both a seasonal cycle and a
linear trend from 2007 to 2009. Analysis with a trend from
4. Discussion
The suggested significance of relative jaw size related to food
is that larger jaws increase the ability to graze and this has
been shown for E. mathaei [26] at Rottnest Island, Western
Australia. Sea urchins with larger jaws grazed larger areas
on rock surfaces. The direct demonstration of increased grazing ability with increased jaw size has not been done for other
sea urchin species but the many studies presented in the introduction confirm that there is a relationship between relative
jaw size and available food. Our interpretation of results for
S. purpuratus at Gregory Point is that relative growth of the
jaws and test changes during a year in response to changes
in available food, with relatively larger jaws arising in response
to decreases in food. The linear trend downward from 2007 to
2009 means that jaws became relatively smaller in addition to
the cyclical pattern within a year, suggesting that food availability improved during this time, which is consistent with
the maximum annual gonad sizes that were observed from
2007 to 2008 at Gregory Point [40]. Gonads in November
2008 were larger than in November 2007 and the relative size
of the jaws was smaller, indicating better food conditions, in
2008 compared with 2007.
Proc. R. Soc. B 281: 20132284
2
3
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2007 to 2009 but no annual cycle had little support as the
best model (wi ¼ 0.37%), which also was the case for an
annual cycle but no trend (wi ¼ 0.002%).
The ANCOVA with lnJ as the dependent variable, lnD as
a covariate and monthly sample date, ti, as a fixed factor
(table 2) provides an estimate of lnJ for each sample adjusted
to an overall mean lnD of 1.78879 (mean D ¼ 5.928 cm). The
interaction term of lnD sample date, ti, was not significant
( p ¼ 0.33). A plot of adjusted means of lnJ together with the
fitted line using the parameters in table 1 both transformed
back to J (elnJ ¼ J ) shows both the seasonal and linear
trends (figure 2). Jaws were relatively large early in a year
and then declined in relative size during the summer with
a minimum in October or November. The linear decline
could indicate improving food conditions each year from
2007 to 2009. There are, however, other possibilities including
problems with measurement or with sampling sea urchins
from different microsites during the study.
Wet weights of sea urchins in samples (figure 1) did not
change during the study (F1,618 ¼ 1.747, p ¼ 0.19) but shape
might have changed if sea urchins were collected from slightly
different microsites. No shape change, however, was detected
with the logarithm of height, lnH, as a function of the logarithm
of diameter, lnD, and time (table 3). Both the analysis of total
weight and analysis of shape indicate that microsite changes
during the study were not major contributors to the observed
change in jaw : diameter allometry.
Analysis of ln jaw length, lnJ, as a function of ln total wet
weight, lnT, and time (table 4a) showed a significant linear
trend with a negative slope indicating decreasing relative
jaw size during the period of study. An ANCOVA with lnJ
as the dependent variable, lnT, as a covariate and sample
time, ti, as a fixed factor provided a pattern of monthly lnJ
adjusted to a common wet weight, lnT (4.58381). This pattern
does not differ in any major way from the pattern shown by
lnJ as a function of lnD (figure 3). There is a cyclical pattern to
jaw size relative to diameter or total wet weight together with
a general downward trend from January 2007 to July 2009.
10
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parameter
estimate
s.e.
– 95%
195%
cycle and
trend
A
M
– 1.3212
0.0580
0.0163
0.0233
21.3532
0.0122
21.2891
0.1037
f
b
C
B1
A
b
B1
A
M
f
b
C
A
b
21.4254
0.8220
0.2365
0.0090
21.8898
0.8043
20.9610
0.8397
trend but
no cycle
cycle but
no trend
no cycle or
trend
20.0260
0.0129
20.0513
20.0007
20.0144
21.3112
0.0029
0.0161
20.0202
21.3428
20.0086
21.2795
0.8178
20.0152
0.0089
0.0030
0.8003
20.0210
0.8352
20.0094
21.3310
0.0600
0.0165
0.0234
21.3633
0.0140
21.2987
0.1060
21.3197
0.2256
21.7627
20.8767
0.8172
20.0266
0.0091
0.0129
0.7993
20.0520
0.8350
20.0012
21.3215
0.8126
0.0163
0.0090
21.3535
0.7949
21.2894
0.8303
parameter
no.
SSE
AICc
wi %
7
1.7783
23581.10
99.632
4
1.8291
23569.88
0.366
6
1.8484
23559.35
0.002
3
1.9084
23545.79
0.000
Table 2. Strongylocentrotus purpuratus at Gregory Point, OR, USA; ANCOVA of ln jaw length, lnJ, as a function of ln diameter, lnD, with sample time, ti, as a
fixed factor; N ¼ 615; r 2 ¼ 0.94.
source
SS
lnD
sample, ti
24.8431
0.1965
1.7120
error
d.f.
MS
F-ratio
p
1
30
24.8431
0.0066
8460.2572
2.2305
, 0.0001
0.0002
583
0.0029
Table 3. Strongylocentrotus purpuratus at Gregory Point, OR, USA; the
natural logarithm of test height, lnH, as a function of the logarithm
of diameter, lnD, and time in years; 20 individuals dissected each month;
N ¼ 620, r 2 ¼ 0.93.
1.20
jaw length (cm)
1.18
1.16
1.14
effect
coefficient
s.e.
t
p
1.12
constant
21.0626
0.0242
243.9000
,0.001
1.10
ln diameter
time (year)
1.2396
20.0046
0.0133
0.0044
92.9184
21.0339
,0.001
0.302
1.08
J M M J S N
2007
2008
2009
year
Figure 2. Change in ln jaw length adjusted to a mean ln test diameter of
1.78879 (5.982 cm) of S. purpuratus at Gregory Point, OR, USA, by ANCOVA;
sample date was as fixed factor; ln values back transformed for plotting;
fitted line based on parameters in table 1.
Strongylocentrotus purpuratus has shown variation in
relative jaw size at a very local scale in Sunset Bay, Oregon,
[20] where samples collected approximately 50 m apart were
different. The sea urchins with the smallest relative jaw sizes
also had the largest test diameters, the largest gonads and
the fastest growth rates [43]. Differences in growth related to
relative jaw size also have been reported for Mesocentrotus
(Strongylocentrotus) francsicanus [22], S. droebachiensis [24],
E. chloroticus [30], H. erythrogramma [33], Anthocidaris crassispina
[50] and C. rodgersii [32].
The food environment changes around S. purpuratus at
Gregory Point on an annual basis [40]. Under laboratory conditions, allometric changes in response to food availability
Proc. R. Soc. B 281: 20132284
model
4
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Table 1. Analysis of monthly jaw length, J, and test diameter, D, measurements of S. purpuratus collected at Gregory Point, OR, USA, from January 2007 to
July 2009; data were first transformed using natural logarithms; lnJ ¼ A þ M cosðð2p/tÞti þ fÞ þ b lnD þ C cosðð2p/tÞti þ fÞ lnD þ B1 ti þ ei ;
definition of parameters given in text.
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Table 4. Strongylocentrotus purpuratus at Gregory Point, OR, USA; N ¼ 615.
5
effect
coefficient
constant
lnT
21.1451
0.2823
s.e.
0.0134
0.0029
t
p
285.5000
98.6934
,0.0001
,0.0001
sample, ti
20.0131
0.0028
24.7352
,0.0001
2
(b) ln jaw length, lnJ, as a function of ln total wet weight, lnT, and sample (time), ti, as a fixed factor; r ¼ 0.94; interaction term, lnT ti, p ¼ 0.74
source
lnT
SS
d.f.
F-ratio
p
25.06936
1
25.0694
9837.7712
,0.0001
0.17304
1.48565
30
583
0.0058
0.0026
2.2634
0.0002
sample, ti
error
1.20
1.18
jaw length (cm)
MS
1.16
1.14
1.12
1.10
1.08
J M M J S N
2007
2008
year
2009
Figure 3. Comparison of ln jaw length adjusted to a mean ln test diameter
of 1.78879 (5.982 cm) (open circles as in figure 1) and ln total wet weight
adjusted to a mean total wet weight of 4.58381 (97.886 g) (filled circles)
showing similar patterns of a cycle and a downward trend; ln values back
transformed for plotting. (Online version in colour.)
have a short response time and are obvious after only a few
weeks [33]. Food changes in the field are more complex
because, on any particular day, an individual sea urchin in
a tide pool may or may not have a piece of algae to eat and
may just rasp the substrate for small, attached algal filaments.
Given the patterns of change in relative jaw size seen in both
the laboratory and in the field, tracking of food availability is
very good and morphological response is rapid.
There is an interesting problem posed by the reversible
plasticity presented here; specifically, is the plasticity actually
adaptive in the sense of having a positive effect on survival?
Annual survival rates for S. purpuratus in the field have been
estimated to be as high as 0.9 [44], which means that 5% of a
population could be 30 years old or older. Strongylocentrotus
purpuratus has remarkable survival ability when faced with
starvation. Under laboratory conditions, sea urchins were fed
at different frequencies [18,19]: ad libitum, once per week,
once every two weeks, once every four weeks and once every
eight weeks. Mortality began to increase in the once-in-eightweeks treatment after 30 weeks. During this time, the sea urchins had been fed just three times all that could be eaten in 24 h
after which all uneaten food was removed. The last survivor
was dead at 52 weeks. The treatment of being fed once every
four weeks showed a rapid decline in survivorship at 45
weeks but some individuals were still alive when the experiment was terminated at 64 weeks. These severe levels of
food shortage probably never occur in the field. The point is
that food reduction unless very severe does not cause increased
mortality under laboratory conditions. Additional physical
and biological stresses in the field, however, may make starved
individuals more vulnerable than in the laboratory and hence
small increases in food intake would improve survival rates.
Resorption as well as deposition occurs in the endoskeleton. Possibly the earliest demonstration of this was in spines
of sea urchins in the order Cidaroida [51]. Cellular processes
associated with resorption have been described in a variety of
sea urchin ossicles [52 –55] but not in plates of the test or jaws
(demi-pyramids) of Aristotle’s lantern.
There are reports of shrinkage of the body wall in echinoids
[27,43] but such body changes may best be explained as problems of measurement [49] or tightening of sutures between
test plates [56,57] without resorption of skeletal elements,
although the very large changes shown for D. antillarum in
both field and laboratory experiments [58] indicated resorption
of test plates. No statistically significant decrease in test diameter, however, was found in S. purpuratus fed only one day
every eight weeks in the laboratory [18,19]. There always is
some food in the field and so it is unlikely sea urchins would
shrink while those starved in the laboratory did not. In general,
changes in jaw allometry are probably best thought of as due to
changes in resource allocation to body parts rather than resorption and rebuilding and so would be energetically very
inexpensive. In this regard, jaw allometry differs from the
changes in gut structures of snakes or birds [13,16] or bones
in iguanas [15], which require energy first to breakdown
and then rebuild. Diadema antillarum, however, may be an
exception [58] and deserves additional study.
Allometric adjustments of jaws of sea urchins indicate
changes in available food. Adjustments are reversible and
rapid and so fit well with the model presented by Gabriel
[10], but additional work is needed that focuses on how the
reversible changes explicitly contribute to fitness. If, as
suggested, reversible plasticity is very inexpensive in terms
of both energy and materials, small changes in survival of
large individuals of long-lived species can be very important,
as shown for the long-lived sea urchin M. franciscanus [59].
Proc. R. Soc. B 281: 20132284
and so not included in analysis
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(a) ln jaw as a function of ln wet weight and sample time, ti; time ¼ 0 at 1 January 2007; r2 ¼ 0.94; interaction term p ¼ 0.09 and analysis redone
without interaction
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changes in stress associated with available food will involve
cell-signalling systems. The changes of relative jaw size we
have shown for S. purpuratus may provide a model system
for exploring the details of regulatory networks involved in
reversible plasticity.
Acknowledgements. Monthly collections and dissections were done by
Bruce Miller, Oregon Department of Fish and Wildlife, Charleston,
Oregon. Miller also froze body walls and lanterns and sent them to
Villanova University for further processing. Collection was done
under a permit from the Oregon Department of Fish and Wildlife.
Funding statement. Portions of this work were supported by the Ocean
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