1
Growth and age structure of sea urchins (Heliocidaris
erythrogramma) in complex barrens and native macroalgal
beds in eastern Tasmania
Hugh G. Pederson and Craig R. Johnson
Pederson, H. G., and Johnson, C. R. 2008. Growth and age structure of sea urchins (Heliocidaris erythrogramma) in complex barrens and native
macroalgal beds in eastern Tasmania. – ICES Journal of Marine Science, 65: 1– 11.
The formation of small-scale barrens of sea urchins on the east coast of Tasmania allows for direct comparison of the growth rates and
age structures of sea urchin populations in barrens and habitats dominated by native macroalgae. However, such barrens are atypical
of any previously described in temperate regions worldwide mainly because of the establishment and seasonal colonization by the
introduced macroalga Undaria pinnatifida. Growth models were fitted to sea urchin (Heliocidaris erythrogramma) data, based on
tag-recapture information from two distinct community types, a native macroalgal bed and a sea urchin barren colonized by U. pinnatifida. Despite the distinct contrast in habitats, size-at-age relationships and age frequency distributions were not significantly different between the two populations. However, the relationship between jaw length and test diameters was significantly different between
populations, sea urchins in barrens possessing larger jaws relative to conspecifics of similar test diameter in native macroalgal habitats.
It is proposed that the growth of sea urchins on barrens is not adversely affected by the loss of native macroalgae in the presence of
U. pinnatifida. However, sea urchins display a level of resource limitation in barrens because of differences in the relationships of sea
urchin morphometrics.
Keywords: age structure, barrens habitat, growth, Heliocidaris erythrogramma, size structure, Undaria pinnatifida.
Received 15 December 2006; accepted 19 October 2007; advance access publication 20 November 2007.
H. G. Pederson and C. R. Johnson: School of Zoology, Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, GPO Box 252-05,
Hobart, Tasmania 7001, Australia. Correspondence to H. G. Pederson: Present address: Marine Research Laboratories, Tasmanian Aquaculture
and Fisheries Institute, University of Tasmania, Private Bay 49, Hobart, Tasmania 7001, Australia; tel: þ61 3 62277276; fax: þ61 3 62278035;
e-mail: [email protected]
Introduction
Sea urchins are conspicuous herbivores of temperate marine ecosystems worldwide (Lawrence, 1975) and can alter the structure of
subtidal communities through overgrazing (North and Pearse,
1970; Wharton and Mann, 1981; Choat and Schiel, 1982;
Fletcher, 1987; Shears and Babcock, 2002; Wright et al., 2005).
Sea urchin overgrazing is associated with the transition of
macroalgal-dominated reef habitats to barrens, and such a
change results in a 100-fold decrease in primary production
(Chapman, 1981). Unlike other sessile benthic invertebrates, sea
urchins can persist at high population density when resources
are limited owing to their plastic allocation of resources
(Johnson and Mann, 1982).
The growth of many sea urchin species (Ebert, 1982; Gage,
1991, 1992; Sanderson et al., 1996; Minor and Scheibling, 1997;
Ebert et al., 1999; Lamare and Mladenov, 2000) and the influence
of resource availability on sea urchin growth and morphometrics
has been well documented (Ebert, 1980b; Black et al., 1982;
Edwards and Ebert, 1991; McShane and Anderson, 1997).
However, despite this wealth of information, few studies have
examined how sea urchin growth rates vary between particular
habitat types (Rowley, 1990; McShane and Anderson, 1997;
# 2007
Russell, 2000), more specifically between established macroalgal
beds and adjacent barrens habitats devoid of erect macroalgae.
The application of tag-recapture methods to study the growth
of sea urchins is relatively common, most studies utilizing chemical tagging techniques (Kobayashi and Taki, 1969; Pearse and
Pearse, 1975; Ebert, 1977; Rowley, 1990; Gage, 1992; Kenner,
1992; McShane and Anderson, 1997; Lamare and Mladenov,
2000). Tetracycline labelling of sea urchin skeletons has proven
to be an effective method to follow growth of individuals, in
some instances over several years (Gage, 1992; Lamare and
Mladenov, 2000). However, variability in recovery rates (10 –
50%) can require a substantial tagging effort to gain sufficient
data to construct precise size-at-age relationships. Despite the
time required between tagging and recapture (annual increments),
and the number of individuals to be tagged, the method can
produce accurate and precise results from relatively few recaptured
animals. Growth functions such as the generalized Richards function (Richards, 1959) have been fitted to tag-recapture data to
produce size-at-age relationships. Constructing size-at-age
relationships and ageing individuals using techniques that rely
on counting natural growth lines in the jaws and test plates of
sea urchins have also been examined (Sumich and McCauley,
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2
1973; Walker, 1981; Sime, 1982; Gage and Tyler, 1985; Turon et al.,
1995; Sellem et al., 2000). Although natural line counts are rapid
and require fewer animals than tag-recapture methods, the technique is seldom accurate without validating the rate at which
growth lines are deposited (reviewed by Russell and Meredith,
2000).
The temperate sea urchin Heliocidaris erythrogramma is
endemic to southeastern Australia, with a distribution from
southern Western Australia to the central coast of New South
Wales and around Tasmania (Endean, 1957; Dix, 1977a). It is a
conspicuous herbivore in the shallow subtidal zone in New
South Wales (Underwood et al., 1991), and is found in moderate
abundance in sheltered subtidal rocky reef habitats between 10 and
40 m deep in eastern Tasmania (Dix, 1977b; Edgar, 2000), where it
is the dominant invertebrate herbivore (Sanderson et al., 1996). Its
individual growth and its population size structure have been previously examined in different parts of its distribution (Ebert, 1982;
Sanderson et al., 1996).
Within Mercury Passage on Tasmania’s east coast, H. erythrogramma has formed patchy barrens devoid of native macroalgae
in subtidal reef habitats over spatial scales of 101 –103 m.
However, the barrens are atypical, because the average density of
sea urchins is relatively low (7 m22; Johnson et al., 2004) compared with those in other temperate regions (.50 m22; North
and Pearse, 1970; Estes and Palmisano, 1974; Wharton and
Mann, 1981; Gagnon et al., 2004), and they are seasonally colonized by the introduced macroalgae Undaria pinnatifida
(Valentine and Johnson, 2003; Johnson et al., 2004). This
pattern provides a unique opportunity to compare sea urchin
growth and population age structures in atypical barrens, with a
seasonal influx of U. pinnatifida, and adjacent habitats supporting
native macroalgae with lower densities of sea urchins.
Here, we construct size-at-age relationships for H. erythrogramma using tag-recapture data over a 2-year period, and use
the information to examine differences in sea urchin growth in
distinct habitat types. We examine sea urchin morphometrics
from populations in contrasting habitats for evidence of resourcelimited growth and construct age frequency distributions using
size-at-age relationships to examine differences in age structures
between sea urchin populations.
Methods
Populations of H. erythrogramma were chemically tagged during
January and February 1999 at two sites in Mercury Passage on
Tasmania’s east coast (Figure 1). The sites were located on rocky
reefs and chosen on the basis of their similar topography and
their exposure to prevailing weather and currents, but they were
distinguished from each other by the abundance of macroalgae.
The site at Lords Bluff was located on the most extensive sea
urchin “barren” within Mercury Passage, one subject to seasonal
growth of the introduced macroalgae U. pinnatifida (Valentine
and Johnson, 2003) where the average sea urchin density was ca.
7 m22. Sea urchins were in lesser abundance at Four Mile Point
(ca. 3 m22), where the reef supported a dense cover of native
canopy-forming macroalgae, unaffected by sea urchin overgrazing,
and characteristic of rocky reefs in southeast Tasmania (Edgar,
1984). Although sites were not replicated within each habitat
type, they were considered to be representative of the extremes
in community structure found in Mercury Passage.
Approximately 400 sea urchins were tagged at each of the two
sites by divers removing all sea urchins from an experimental plot
H. G. Pederson and C. R. Johnson
Figure 1. Location of sea urchin populations sampled within
Mercury Passage on the east coast of Tasmania. Sea urchins were
tagged using tetracycline in a native macroalgal bed at Four Mile
Point (FMP), and on urchin barrens at Lords Bluff (LB). Size
frequency distributions were determined for non-tagged sea urchin
populations on urchin barrens and in adjacent macroalgal beds at LB
(LB-NT) and Stapleton Point (SP-NT).
located on the 5-m contour. The experimental plot measured
10 m 6 m at Lords Bluff and 10 m 12 m at Four Mile
Point. Although the experimental plots yielded a range of sea
urchin sizes, small animals in their first year of life occupied
cryptic habitat and were rarely sampled.
Test dimensions of each sea urchin were measured to the
nearest millimetre using knife-edge vernier callipers before injecting them with a solution of tetracycline hydrochloride (Kobayashi
and Taki, 1969) at a concentration of 10 g l21 in seawater, using a
small-gauge hypodermic needle (adapted from Ebert, 1977). To
ensure that all sea urchins received a standard dose of the tetracycline solution (0.006 ml g wet weight21), test diameter (D)
measurements were used to estimate wet body weight (W ) from
a pre-determined function (W ¼ 3.49D – 154.14; n ¼ 40, r 2 ¼
0.93). Tagged sea urchins were returned to experimental plots
soon after receiving injections. Mortality from handling was
assessed 72 h post-tagging by searching experimental plots for
fresh mortalities, and was estimated to be ,5% of tagged animals.
Experimental plots were sampled three times between February
1999 and February 2001 (12, 14, and 24 months post-tagging).
Approximately one-quarter of the number of sea urchins originally
tagged were recaptured after 12 and 14 months of growth
(Table 1), with approximately half the original number of tagged
sea urchins left in the plots to complete 24 months of growth posttagging. The recaptured sea urchins were selected to represent the
Growth and age structure of sea urchins in eastern Tasmania
3
Table 1. Recovery of tagged sea urchins across the three sampling
periods (12, 14, and 24 months post-tagging) from two sites within
Mercury Passage.
Relative
Number of
Number of Number of
sea urchins sea urchins positive tag recovery
rate (%)
returns
collected
tagged
Four
Mile
Point
...............................................................................................................................
0
355
–
–
–
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
12
–
83
71
86
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
14
–
72
65
90
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
24
–
230
57
24
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
Overall
–
–
–
54
recovery
Month
Lords
Bluff
...............................................................................................................................
0
431
–
–
–
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
12
–
115
71
62
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
14
–
98
65
66
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
24
–
288
92
32
. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .
Overall
–
–
–
53
recovery
Positive tag returns were animals with clear tetracycline bands present on
the surface of their jaws (Figure 2).
Figure 2. Heliocidaris erythrogramma jaw under ultraviolet
illumination with the tetracycline tag (1), epiphysis junction (2),
external edge (3), and oral tip (4) identified. Growth increments (DJ)
were measured to the nearest 0.05 mm from the point where the
tetracycline tag met the external edge to the epiphysis junction of
jaws using a dissecting microscope with an optical micrometer under
20 magnification. Jaw length at the time of sampling (JtþDt) was
measured to the nearest 0.05 mm using knife-edge vernier callipers,
and jaw length at the time of tagging (Jt) was calculated by
subtracting the growth increment from JtþDt.
range of sizes present, and were frozen before dissection in the laboratory. On the final sampling in early February 2001, all remaining sea urchins were removed from the plots and from within a
1-m band around the plots.
The test diameter of each sea urchin was measured before dissection. On dissection, half of the test and the entire Aristotle’s
lantern were placed into a solution of 5% sodium hypochlorite.
The calcified material remaining after 24 h was rinsed thoroughly
with fresh water before being air-dried for 48 h. Demipyramids
(hereafter referred to as jaws) and test plates from the prepared
samples were exposed to ultraviolet light and examined for the
presence of the tetracycline tag (Figure 2).
A small sample of sea urchins (n ¼ 30) was collected from areas
adjacent to each of the experimental sites during February 2000
and prepared for ultraviolet examination. These samples were controls for the presence of background auto-fluorescence in jaws and
test plates. Of the 90 control sea urchins collected, none showed
any sign of fluorescence in either test plates or jaws. We interpret
the absence of background fluorescence to indicate that the marks
detected in experimental animals are a result of the tagging process
and not environmental contamination.
The growth increment (DJ) was measured on one-half of a jaw
from each animal displaying a visible tag from the point where the
fluorescent band met the external edge to the epiphysis junction
(Figure 2). Measurements were taken using an ocular micrometer
under 20 magnification on a stereo dissecting microscope with
an accuracy of 0.05 mm. Jaw length at the time of sampling
(JtþDt) was measured from the oral tip to the epiphysis junction
to the nearest 0.05 mm using knife-edge vernier callipers, and
jaw length at the time of tagging (Jt) was calculated by subtracting
the growth increment from the length of the jaw at the time of
sampling (JtþDt 2DJ). Growth measurements were taken from
the jaws because the tetracycline marks there were more often
clearly visible and easier to read than on test plates, and a large
proportion of animals displayed readable tags on jaws but had
no corresponding marks on test fragments. Growth at the oral
tip of jaws was not observed in our samples except in some
smaller sea urchins where a fluorescent mark was visible but
growth could not be measured accurately.
Growth parameters of tagged populations were estimated by
fitting the generalized Richards function (Ebert, 1999) to data
obtained from the individuals recovered 12, 14, and 24 months
after tagging. The use of the Richards function for the construction
of growth models was based on the shape of the plot of jaw length
at the time of sampling (JtþDt) and dependent on jaw length at the
time of tagging (Jt; Walford, 1946; Ebert, 2001). The linear nature
of the relationship between JtþDt as a function of Jt suggests that
the generalized Richards function is appropriate to describe
growth in H. erythrogramma (Figure 3). The Richards function
can be written as Jt ¼ J1 (12be2kt)2n’, where Jt is jaw length at
time t, J1 the asymptotic jaw length (when t!1), k the growth
rate constant, b is (J1 –J0)/J1, where J0 is the jaw length at recruitment to the population, and n’ describes a shape parameter. When
fitting this function to data collected from several different time
þ(J 21/n’
–
intervals, it can be rewritten as JtþDt ¼ [J21/n’
t
1
2kDt 2n’
21/n’)
Jt
(1–e
)] , where JtþDt is the jaw length after a period
of time (Dt) has passed (Ebert, 1999). Optimum fits were determined by minimizing weighted squared differences between the
observed growth increments (DJ) and the expected growth increments (weighted using JtþDt/J̄tþDt, where J̄tþDt is the mean jaw
length at the time of sampling). Weighting the observed growth
increments was required to stabilize variance, and to meet the
assumption of homogeneity of variance in calculating the
F-statistic, when comparing growth trajectories using an analysis
of residual sums of squares (Haddon, 2001).
When fitting growth models to tag-recapture data, where most
data involve large animals, estimating size at recruitment to the
population (i.e. J0) is important to anchor the size-at-age relationship. In the absence of this estimate, fitted growth models are likely
to return inaccurate estimates of size-at-age for juveniles. Because
recently settled juveniles are cryptic and hidden deep within
4
H. G. Pederson and C. R. Johnson
Figure 3. Jaw length at the time of sampling (JtþDt) as a function of jaw length at time of tagging (Jt) for sea urchins collected 12, 14, and 24
months after tetracycline tagging. Solid lines represent linear relationships between JtþDt and Jt for Four Mile Point (12 months, JtþDt ¼
0.89Jt þ 1.74, r 2 ¼ 0.99, n ¼ 71; 14 months, JtþDt ¼ 0.83Jt þ 2.73, r 2 ¼ 0.97, n ¼ 65; 24 months, JtþDt ¼ 0.86Jt þ 2.22, r 2 ¼ 0.98, n ¼ 57) and
Lords Bluff (12 months, JtþDt ¼ 0.89Jt þ 1.92, r 2 ¼ 0.98, n ¼ 71; 14 months, JtþDt ¼ 0.83Jt þ 2.79, r 2 ¼ 0.98, n ¼ 65; 24 months, JtþDt ¼
0.87Jt þ 2.16, r 2 ¼ 0.98, n ¼ 92). Dashed lines represent zero growth between the time of tagging and the time at sampling.
crevices, our samples did not include these animals. Instead, we
estimated jaw size at settlement (J0) from sea urchins (n ¼ 24)
recruited to artificial collectors deployed in November 2000 and
sampled each month until May 2001 to ensure detection of
recent settlement (this period covered the adult spawning period;
Sanderson et al., 1996). The collectors were 15 cm15 cm sections
of artificial turf secured to concrete blocks of similar dimension
placed at Lords Bluff. Artificial turf has been used successfully for
this purpose (Lambert and Harris, 2000). Juvenile sea urchins
were located on the collectors 6 months after initial deployment.
The test diameter of individuals was measured to the nearest
0.05 mm using an ocular micrometer before dissection. Sea
urchins were identified as H. erythrogramma using the pore structure of the interior surface of test plates (Baker, 1982). Following
dissection, jaw length was measured using an ocular micrometer
to the nearest 0.05 mm, with the jaw length at the time of recruitment to the population (J0) estimated to be 0.47 mm (+s.e. 0.046)
with corresponding test diameters of 1.26 mm (+s.e. 0.10).
By fitting the Richards function to growth increment data
obtained from sea urchins at each of the tagging sites, estimates
of size at a given age post-recruitment can be calculated from
the size-at-age relationships. The age of sea urchins was calculated
from the jaw length at the time of sampling using the relationship
for size-at-age. Age frequency distributions for the tagged populations were constructed from all individuals collected at each
site, using jaw length to determine the age.
Growth morphometrics in the two tagged populations were
also compared by examining the relationships between jaw
length and test diameter at the time of sampling. Differences in
the relationship between jaw length and test diameter between
the populations were examined with analysis of covariance
(ANCOVA), using habitat type as the covariate.
Sea urchin barrens within Mercury Passage appear as patches at
scales of 101 –103 m and often situated alongside undisturbed
native macroalgal beds. The close proximity of sea urchin
barrens to undisturbed stands of native macroalgae on reefs with
similar rock type, topographic relief, and exposure to prevailing
weather allows for direct comparison of sea urchin populations
in habitats with contrasting food resources. We collected size frequency information from non-tagged populations of H. erythrogramma in barrens and adjacent macroalgal beds at two
locations, Lords Bluff and Stapleton Point, within Mercury
Passage (Figure 1).
In the absence of tag-recapture information for each separate
non-tagged population, we converted size frequency distributions
(test diameter) to age frequency distributions using the size-at-age
relationships constructed from tagged populations described
earlier. We used the size-at-age function derived for tagged sea
urchins in the native macroalgal bed at Four Mile Point to construct age frequency distributions for the non-tagged populations
in similar native macroalgal beds at Lords Bluff and Stapleton
Point. Similarly, the size-at-age function derived for the tagged
population on barrens habitat at Lords Bluff was used to construct
age frequency distributions for the non-tagged populations in
barrens habitat at each of the two locations. Using the size-at-age
functions from tagged populations to construct age frequency distributions of non-tagged populations assumes similar growth rates
of sea urchins across the sites within each habitat category.
5
Growth and age structure of sea urchins in eastern Tasmania
To estimate age structures of non-tagged sea urchin
populations, i.e. for populations where only test diameter
measurements could be taken during non-destructive sampling,
jaw length size-at-age relationships derived from the tagged sea
urchin populations were converted to test diameter size-at-age
relationships using the allometric relationship J ¼ aD b, where J
is jaw length and D the test diameter of sea urchins at the time
of sampling, and the constants a and b were determined using a
geometric mean functional regression (Ricker, 1973).
To ensure that we could apply the size-at-age relationships
derived from tagged sea urchins to determine the age of nontagged individuals, we made a direct comparison of the relationship between the jaw length and test diameters in a sample of
tagged and non-tagged individuals. We used jaw length and test
diameter measurements of animals taken at each site (Four Mile
Point and Lords Bluff) to test for background (auto-) fluorescence
in sea urchin skeletons (n ¼ 30 at each site), and measurements
taken from tagged individuals used in the model that were collected 1 year after tagging (n ¼ 71 at each site, Table 1). Using
ANCOVA, we determined that there was no significant interaction
between tagging and the relationship between jaw length and test
diameter (p ¼ 0.31 and p ¼ 0.46 at Four Mile Point and Lords
Bluff, respectively) and that the intercepts were not significantly
different (p ¼ 0.41 and p ¼ 0.61 at Four Mile Point and Lords
Bluff, respectively). We therefore assume that using size-at-age
relationships derived from tagged sea urchins to determine the
age of non-tagged sea urchins in the same habitat type is valid.
Age frequency distributions of adjacent sea urchin populations
were compared using a randomization procedure with the
Kolmogorov–Smirnov test statistic (D). Age frequency data were
pooled and individuals reallocated randomly to each population,
then the test statistic (D) was recalculated. The procedure was
repeated 1000 times, and the test of significant difference
between the two populations made by comparing the value of
the observed test statistic to the distribution of D-values obtained
by the randomization procedure. Significant differences were
identified when fewer than 25 of the randomized D-values
exceeded the value of D from the original populations (see
Haddon, 2001, for overview).
Results
Fitting the Richards function to growth data from sea urchins collected up to 2 years after tagging indicated that individuals in the
native macroalgal bed at Four Mile Point had faster rates of growth
(k ¼ 0.099) and reached a larger asymptotic size than animals in
the population on the barrens at Lords Bluff (J1 ¼ 16.49, D1 ¼
100.96; Table 2, Figure 4). Growth of sea urchins on barrens
habitat at Lords Bluff was slower (k ¼ 0.093), and animals there
reached a smaller asymptotic size (J1 ¼ 16.23, D1 ¼ 94.35). The
Richards function did not fit data obtained from Lords Bluff as
well as data collected from Four Mile Point, the model having
greater sums of square error (Table 2). However, when the fitted
growth curves were compared, using analysis of residual sums of
squares, the difference was not significant (F2640 ¼ 228.92, p .
0.05).
ANCOVA indicated that relationships between test diameter
and jaw length differed between sea urchins tagged at Four Mile
Point with those tagged at Lords Bluff (p , 0.0001). The relationship between jaw length and test diameter of small sea urchins was
also different between populations, small animals in the native
macroalgal bed at Four Mile Point having larger jaws than conspecifics of similar test diameter in the barrens at Lords Bluff
(Figure 5). However, the relationship was reversed when animals
reached 49 mm test diameter, sea urchins at Lords Bluff possessing larger jaws than conspecifics of similar test diameter at Four
Mile Point.
The sea urchin population in the native macroalgal bed at Four
Mile Point consisted of larger animals than that at Lords Bluff,
with ca. 70% of the population .80 mm test diameter
(Figure 6). In contrast, sea urchins .80 mm test diameter constituted just 17% of the population on the barrens at Lords Bluff. The
modal size of sea urchins at Four Mile Point was 82 mm, noticeably larger than sea urchins at Lords Bluff (72 mm).
Comparison of sea urchin age frequencies revealed significant
differences among the populations (p , 0.0001). Almost 20% of
individuals in the population at Four Mile Point were older than
20 years, whereas at Lords Bluff just 7% of the population was
older than that.
Although the size-at-age relationships for the populations at
Four Mile Point and Lords Bluff were not significantly different,
the predicted ages of individuals of similar size in each population
were noticeably different. For example, a sea urchin with a test
diameter of 60 mm had an estimated age of 7 years at Four Mile
Point and 9 years at Lords Bluff. The predicted range of test
sizes within each estimated age class was consistently larger from
the population in the barrens at Lords Bluff than in the population
at Four Mile Point.
Comparisons of non-tagged sea urchin populations in barrens
and native macroalgal beds yielded notable differences in size frequency distributions at two separate locations (p , 0.001 for
Stapleton Point and Lords Bluff). Also, at both locations, there
were fewer sea urchins ,70 mm in the algal beds than in the adjacent barrens habitat population (Figure 7). In contrast, there was
no difference in the age frequency distributions between barrens
habitat and native macroalgal beds at either Stapleton Point or
Lords Bluff (p ¼ 0.125 and p ¼ 0.142, respectively).
Discussion
Whereas the growth dynamics of sea urchin species have been
described using a range of growth functions, the generalized
Richards function has been the one most commonly used
(Ebert, 1980a, b, 1982; Gage and Tyler, 1985; Russell, 1987;
Table 2. Estimates of the Richards growth function parameters for sea urchin populations at two sites within Mercury Passage, where k is
the growth rate, J1 the asymptotic jaw length (mm), D1 the asymptotic test diameter (mm), n’ the shape parameter, SSE the weighted
error sums of squares, and n the number of sea urchins in each sample.
Site
k
J1
D1
n’
SSE
n
Four
Mile
Point
0.099
(0.070
–0.127)
16.49
(16.99
–16.16)
100.96
(99.38
–103.37)
21.10
(21.17
–1.04)
8.4497
193
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . .
Lords Bluff
0.093 (0.075 –0.103)
16.23 (16.75 –15.97)
94.35 (93.07 –96.88)
21.04 (21.13 –0.96)
10.7251
228
Values of k, J1, and n’ result in the least SSE, and 95% confidence intervals are estimated from 1000 bootstrap samples (in parentheses).
6
H. G. Pederson and C. R. Johnson
Figure 4. Size-at-age relationships developed using the Richards function fitted to data combined from three sampling periods (12, 14, and 24
months post-tagging) for Four Mile Point (solid line) and Lords Bluff (dashed line). Series on the left represent jaw length-at-age, and series on
the right represent size-at-age relationships based on test diameter estimated from the allometric relationship between jaw length and test
diameter of tagged sea urchins at each site.
Ebert and Russell, 1992; Kenner, 1992; Lamare and Mladenov,
2000). This reflects the versatility of the function, which allows
for the inclusion of known size-at-age data and in particular the
size at recruitment (Ebert, 1999, 2001), and the inclusion of data
from multiple sampling periods (Ebert, 1999). The linear nature
of the relationship we observed between JtþDt and Jt suggests
that the generalized Richards function was the most appropriate
to model the growth of H. erythrogramma in the habitats we
sampled (Ebert, 2001).
Parameter estimates of the Richards function describing growth
in H. erythrogramma determined here are different from those of
Ebert (1982) for New South Wales and Western Australia. Our
Figure 5. Jaw length (JtþDt) as a function of test diameter (D) at the time of sampling from tagged sea urchins at Four Mile Point (FMP, open
squares, J ¼ 0.131D þ 3.365, r 2 ¼ 0.63, solid line) and Lords Bluff (LB, open triangles, J ¼ 0.169D þ 1.481, r 2 ¼ 0.79, dashed line). ANCOVA
indicated significant differences in slope (p , 0.0001). The dashed vertical line indicates the point at which the two relationships are
equivalent (49 mm).
Growth and age structure of sea urchins in eastern Tasmania
7
Figure 6. Size and age frequency distributions derived from growth functions fitted to tag-recapture data, of tagged sea urchins in a
population in a native macroalgal bed (Four Mile Point, n ¼ 385) and a population in a barrens (Lords Bluff, n ¼ 501). Sea urchin sizes are test
diameters.
estimates of asymptotic size were greater, but the growth rate (k)
was slower, than with those of Ebert (1982). The differences in
growth estimates between the two studies would, however, be
expected given the broad geographic range and differences in habitats between the sites here and those of Ebert (1982). We expect
that H. erythrogramma will display a wide range of growth rates
and achieve different asymptotic sizes given its large geographic
range (Endean, 1957; Dix, 1977a) and the variety of habitats it
occupies, from deep intertidal to subtidal reefs and seagrass beds
(Underwood et al., 1991; Growns and Ritz, 1994; reviewed by
Keesing, 2001).
In a similar study, Sanderson et al. (1996) constructed a growth
function of H. erythrogramma using the generalized Richards
function (where n’ ¼ 21, i.e. von Bertalanffy model), from sea
urchins tagged on a barrens habitat several kilometres from our
site at Lords Bluff. Their estimates of growth rate (k ¼ 0.20) and
asymptotic test diameter (85.0 mm) are markedly different from
those estimated here (k ¼ 0.093 and D1 ¼ 94.35 mm) on a
similar barrens habitat. This suggests that sea urchin growth
might be variable across relatively small spatial and/or short
temporal scales, perhaps exceeding the variation between different
habitats in other sea urchin species (Russell, 2000). Alternatively,
the differences may be due in part to the size ranges used to fit
the growth models, or that Sanderson et al. (1996) estimated
growth parameters from plots of jaw length at the time of sampling
(JtþDt) as a function of jaw length at tagging (Jt, see Ebert, 1980a),
which do not take into account estimates of size at recruitment
(J0), the shape of the growth function (n’), or minimize prediction
error by optimizing parameter estimates.
Barrens habitats are typically characterized by a complete
absence of erect macroalgae (Breen and Mann, 1976; Estes et al.,
1978; Fletcher, 1987), significant reduction in reef primary productivity (Chapman, 1981), and persistent sea urchin populations
relying on limited supplies of drift, micro- and coralline algae
(Johnson and Mann, 1982). The similarity of the growth trajectories of sea urchins in habitats supporting a canopy of native
macroalgae with those from barrens with a seasonal influx of the
introduced macroalgae U. pinnatifida suggests that there are sufficient food resources for sea urchins to maintain normal somatic
growth in these atypical barrens. Although the collective area of
8
H. G. Pederson and C. R. Johnson
Figure 7. Size and estimated age frequency distributions of non-tagged sea urchin populations in barrens and adjacent native macroalgal beds
at Stapleton Point (n ¼ 209 and n ¼ 218, respectively) and Lords Bluff (n ¼ 213 and n ¼ 79, respectively). Sea urchin sizes are test diameters.
barrens within Mercury Passage is relatively large (105 –106 m2),
the area of individual barrens is relatively small (101 –103 m2), so
the amount of native drift algae within individual barrens may
be relatively high. The preference of H. erythrogramma for drift
over attached native macroalgae has been documented in other
parts of its range (Vanderklift and Kendrick, 2005), but a preference for native drift algae over U. pinnatifida by this sea urchin
has not been demonstrated. Experimental evidence and in situ
9
Growth and age structure of sea urchins in eastern Tasmania
observations suggest that H. erythrogramma grazes on a combination of U. pinnatifida and native drift algae when present
within these atypical barrens (Valentine and Johnson, 2005).
Although the fitted growth functions for sea urchins on barrens
and in the macroalgal bed suggest that the two populations had
similar growth trajectories, individuals in the barrens on average
had significantly larger jaws relative to their test diameter
(Figure 3). This suggests that the population in the barrens is
resource-limited. Similar observations have been made for
Evechinus chloroticus, resource-limited animals having significantly larger jaws than conspecifics of similar test size in
resource-rich habitats (McShane and Anderson, 1997).
Significant differences in the relationships between jaw length
and test diameter in response to limited food resources have
been demonstrated for other temperate sea urchins (Ebert,
1980b; Black et al., 1982, 1984; Levitan, 1991). Increased relative
jaw size is thought to increase grazing potential, which is likely
to be of adaptive significance in resource-limited environments
(Black et al., 1984). Notably, differences in relative jaw length
among sea urchins in the native macroalgal bed and barrens populations were not consistent across sea urchin size. Small sea urchins
in the native macroalgal beds had relatively larger jaws than conspecifics of equivalent size in the barrens, but this pattern was
reversed for individuals .49 mm in diameter. At our sites,
animals ,50 mm in diameter were rarely observed and remained
cryptic. Therefore, the apparent shift in resource allocation to jaw
development between the two populations may reflect an ontogenetic shift in diet. Juveniles emerging from crypsis in the
barrens habitat may experience food limitation relative to newly
emergent conspecifics in native macroalgal beds, leading to allocation of resources to the development of jaws to increase their
grazing ability. These results suggest that overall jaw growth in
H. erythrogramma is less sensitive to resource limitation than
other internal allocation of resources, such as test growth.
Similarly, changes in test thickness have been found to be more
sensitive in terms of response to resource availability than test
diameter (Ebert, 1982).
Hypotheses accounting for barrens formation have been long
argued and essentially fall into two broad categories, those based
on changes in sea urchin population density, and those based on
invoking changes in sea urchin behaviour. Occasional prodigious
recruitment events, across large spatial scales (105 –106 m), have
been suggested as a possible mechanism to increase sea urchin
population density rapidly to a level to facilitate barrens formation
(Hart and Scheibling, 1988).
Our comparison of non-tagged sea urchin populations at two
separate locations in Mercury Passage suggests that the establishment of barrens is not the result of a single prodigious broad-scale
recruitment event, for several reasons. First, the age structure of
populations between barrens and adjacent native macroalgal
beds was not distinctly different. Second, the age structure of sea
urchin populations in barrens did not contain prominent
cohorts that were absent in populations in adjacent macroalgal
beds. Finally, barrens in Mercury Passage occur over much
smaller spatial scales (101 –103 m) than the hypothesized scale
over which prodigious recruitment has been suggested as possible.
Although we can conclude that broad-scale prodigious recruitment events are unlikely to be the cause of barrens in Mercury
Passage, we cannot rule out the influence of small-scale differences
in sea urchin recruitment. Perhaps a combination of small-scale
recruitment coupled with sea urchin grazing can initiate the
formation of patchy barrens. We propose that a more detailed
examination of the small-scale variability in sea urchin recruitment be made.
Acknowledgements
This research would not have been possible without the assistance
of the staff and students of the School of Zoology and the Marine
Research Laboratories at the University of Tasmania. We particularly acknowledge the contributions made by J. Valentine,
R. Magierowski, M. Lawler, E. Forbes, and S. Campbell during
the collection and tagging of sea urchins in the field.
Correspondence with T. A. Ebert and M. Haddon during construction of growth models was invaluable and greatly appreciated.
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doi:10.1093/icesjms/fsm168