Growth, morphometrics and size structure of the Diadematidae sea urchin Centrostephanus rodgersii in northern New Zealand

Abstract

The sea urchin Centrostephanus rodgersii has increased its range in Eastern Australia resulting in important ecological changes. C. rodgersii may also have expanded its distribution range to northern New Zealand in the last five to six decades, although little is known about this process and of the biology of the species in New Zealand. We investigated morphometrics as well as growth using two techniques (growth line count in genital plates and tag–recapture using the fluorescent marker tetracycline). These methods allowed modelling of size at age of C. rodgersii in New Zealand, which we compared with populations recently established in Tasmania. The modelled growth rate was only slightly higher in the New Zealand population, and no differences in morphometrics were observed. The New Zealand population structure suggests that annual recruitment occurs regularly, with the population including a range of ages (3 to 10+ years).

Full text

Growth, morphometrics and size structure of the
Diadematidae sea urchin Centrostephanus rodgersii
in northern New Zealand
Danilo Pecorino
A
,
B
,Miles D. Lamare
A
and Mike F. Barker
A
A
Department of Marine Science, University of Otago, Dunedin, New Zealand.
B
Corresponding author. Email: danilo.pecorino@gmail.com
Abstract. The sea urchin Centrostephanus rodgersii has increased its range in Eastern Australia resulting in important
ecological changes. C. rodgersii may also have expanded its distribution range to northern New Zealand in the last five to
six decades, although little is known about this process and of the biology of the species in New Zealand. We investigated
morphometrics as well as growth using two techniques (growth line count in genital plates and tag–recapture using the
fluorescent marker tetracycline). These methods allowed modelling of size at age of C. rodgersii in New Zealand, which
we compared with populations recently established in Tasmania. The modelled growth rate was only slightly higher in the
New Zealand population, and no differences in morphometrics were observed. The New Zealand population structure
suggests that annual recruitment occurs regularly, with the population including a range of ages (3 to 10þyears).
Additional keywords: climate change, competition, growth lines, range expansion, tag–recapture.
Received 7 February 2012, accepted 30 April 2012, published online 2 July 2012
Introduction
Centrostephanus rodgersii (Agassiz, 1863) is a large Diade-
matidae sea urchin that occurs intertidally and subtidally (0 to
30 m depth) along the eastern coast of mainland Australia,
Tasmania, Norfolk and Lord Howe Islands, and northern New
Zealand (Andrew 1993; Andrew 1994; Andrew and Byrne
2007). It is associated with hard corals in the north of its dis-
tribution and kelp communities in the south, where it is capable
of forming and maintaining extensive patches of barrens habitat
(Andrew and Underwood 1989, 1993; Andrew 1991, 1993; Hill
et al. 2003; Andrew and Byrne 2007; Connell and Irving 2008;
Ling et al. 2009a).
In the last 5–6 decades, C. rodgersii has expanded its range
from south-eastern mainland Australia to Tasmania, where it
was first recorded in 1978 (Johnson et al. 2005). In the subse-
quent years the southern range expansion continued, and by
2005 the species had reached the south-western tip of Tasmania
(Ling et al. 2008). There is anecdotal evidence that suggests
C. rodgersii increased in range into New Zealand at about the
same time. It was noted to be present in New Zealand at the Poor
Knights Islands in 1967 (Barker pers. obs.) and later on nearby
off-shore islands immediately south, namely the Mokohinau and
Great Barrier Islands (Choat and Schiel 1982).
The southward range expansion of C. rodgersii has been
attributed to a strengthening of the Eastern Australian Current
(EAC) and its increased southerly extension (Ridgway 2007;
Ling et al. 2009b). This has, in turn, increased winter sea surface
temperatures above 128C, a temperature that allows larvae of
C. rodgersii to develop (Ling et al. 2008). For this reason, the
establishment of a population around the Tasmanian coastline
is closely linked to increases in winter sea surface temperatures
above the 128C winter threshold (Ling et al. 2009b). The
potential for changes in population size and ranges of
C. rodgersii in New Zealand as a result of changes in the EAC
and increases in sea surface temperatures is unknown.
To gain a better understanding of the processes that may
affect C. rodgersii populations in New Zealand, information on
the biology of this species, including growth, morphometrics
and population structure is required. In the present paper we
examine growth in a New Zealand population and compare
estimates of size-at-age of C. rodgersii with those in Tasmania.
C. rodgersii is a moderately fast growing sea urchin, reaching
50 mm test diameter (TD) at an age of 4–5 years, and approach-
ing a maximum size of ,114 mm after ,25 to 35 years, after
which, growth slows considerably (Ling et al. 2009b). The
species shows a degree of spatial variation in growth between
environments, with higher growth rates in macroalgal bound-
aries compared with barren grounds (Ling and Johnson 2009).
Rates of growth of the New Zealand population are unknown,
although they may differ from the Tasmanian population, given
the plasticity of growth rates that are known in sea urchin species
based on differences in temperature and food availability (Ebert
et al. 1999).
Quantifying growth in sea urchins requires changes in size at
age to be established and that an appropriate model of growth is
utilised. Growth in sea urchins has been examined using several
methods including annual growth ring counts (Gage 1992; Brey
et al. 1995), tag–recapture (Ebert and Russell 1992; Lamare and
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Mladenov 2000; Kirby et al. 2006; Ling et al. 2009b), laboratory
rearing (Lamare and Mladenov 2000), and cohort analysis
(Swan 1958; Ebert 1968; Raymond and Scheibling 1987).
Similarly, a range of growth models have been applied to sea
urchins including those that assume asymptotic growth such
as the Brody–Bertalanffy (von Bertalanffy 1938; Brody 1945)
and Richards functions (Richards 1959) to more complex
models that allow for continued growth through the life of
the animal, such as the Tanaka function (Tanaka 1982).
The advantages of the different approaches and details of the
methods have already been widely discussed (Dix 1970; Pearse
and Pearse 1975; Nelson and Vance 1979; Olson and Newton
1979; Ebert 1988; Gage 1992; Ebert and Russell 1993; Bureau
1996; Robinson and MacIntyre 1997; Ebert et al. 1999; Lamare
and Mladenov 2000; Russell and Meredith 2000; Duggan and
Miller 2001; Rogers-Bennett et al. 2003; Kirby et al. 2006;
Pederson and Johnson 2008; Ellers and Johnson 2009; Ling and
Johnson 2009; Ling et al. 2009b).
We use both tag–recapture and growth line counts to estimate
growth in C. rodgersii in a population in northern New Zealand,
and apply three growth models to our data. At the same time we
examine morphometrics and size at age distributions in the
same population. These data allow for the first estimates of
growth of the species in New Zealand, and increase our
understanding of its population biology at this location. Given
the significant changes in the Tasmanian coastal ecosystems that
have been attributed to the expansion of C. rodgersii, the
implications of our findings for the species in terms of its
establishment in New Zealand and future ecological interactions
are discussed.
Materials and methods
Study site and collection
Populations of C. rodgersii were examined at two sites located
in the Mokohinau Islands, a cluster of small islands situated
north-east of the northern part of the North Island, New Zealand
(Fig. 1). Site 1 is at North-East Bay of Fanal Island (35856.1460S,
175808.9220E), and site 2 is on the eastern side of Burgess Island
(35854.1170S, 17587.1430E). The habitat at both sites is char-
acterised by large rock boulders (1 to 2 m) and dense macroalgal
coverage, dominated by the canopy forming brown seaweed
Ecklonia radiata. The sea urchin C. rodgersii is patchily dis-
tributed and occurs sympatrically with the more numerous New
Zealand endemic echinoid Evechinus chloroticus (Echinome-
tridae). Sea urchins were chemically tagged in situ by SCUBA
divers on 24 January 2010 and were sampled one year later, on
31 January 2011 for the tag–recapture study (see ‘Tetracycline
tagging and recapture’ for details). Between January 2010 and
November 2010, sea urchins were sampled on 7 occasions to
provide age estimates obtained from growth lines (see ‘Growth
lines’ paragraph for details). Samples were collected from a
depth of 5 to 15 m, with between 10 and 20 sea urchins collected
on each sampling date. The sea urchins that were collected
included both tagged and untagged individuals because tags
were not visible externally.
Morphometrics
The TD of each individual collected between January 2010 and
November 2010 (n¼84) was measured (to the nearest 0.1 mm)
with digital callipers, then they were drained of water and
coelomic fluid, weighed (0.01 g precision) and dissected. Major
body components (Aristotle’s lantern and test) were weighed
and the genital plates and Aristotle’s lantern were bleached in
10% NaClO overnight to remove organic matter. Following this,
the lantern was disassembled and the average length of each
demi-pyramid (referred to hereafter as ‘jaws’) measured from
the oral tip to the epiphysis. Jaw length was plotted against TD to
check for its size relatively to the diameter. An average lantern
index (LI) for the population, defined as the ratio between jaw
length and test diameter and expressed as a percentage, was then
calculated as the average of the LI of each individual.
Growth estimates
Growth lines
Age lines were counted on the same individuals used for
morphometric measurements. Bleached genital plates were
dried at 608C for 1 day and subsequently placed into a muffle
furnace at 5008C for 15 min to make growth lines more visible.
At that point, each genital plate had the external surface gently
sanded with fine sandpaper (P240 grade), rinsed in 96% ethanol
and air-dried, before being submerged in xylene. To estimate
age, the number of lines was counted under a dissecting
microscope, with one translucent and one opaque growth line
assumed to represent a 1-year time period.
Marginal increment analysis was used to validate annual
growth lines deposition in the genital plates (Schuhbauer et al.
2010). For this, one randomly selected genital plate from each
aged individual was examined under a dissecting microscope,
and whether the outermost growth region was translucent or
opaque was noted. Periodicity of opaque and translucent line
deposition was determined from the proportion of individuals
that exhibited a translucent line at the margin of the genital
plates on each sampling time. Periodicity of deposition of
growth lines was also validated by using the genital plates of
tagged individuals recollected one year after tagging (n¼24
individuals that exhibited a fluorescent mark on the genital
35⬚54⬘S
35⬚57⬘S
175⬚09⬘E
1 km
Mokohinau Islands
North New
Zealand
Burgess Island
Fanal Island
175⬚05⬘E
Fig. 1. Location of the Mokohinau Islands in New Zealand. The position of
Centrostephanus rodgersii sampling and tagging sites at Fanal Island and
Burgess Island is indicated by the circles.
BMarine and Freshwater Research D. Pecorino et al.

plates, see ‘Tetracycline tagging and recapture’ for the marking
and reading method) by counting the number of lines visible
after the tag and assuming that no more than two growth lines,
one opaque and one translucent, can be deposited each year,
assuming line deposition follows an annual pattern.
Tetracycline tagging and recapture
On 24 January 2010, 80 C. rodgersii were chemically tagged
with an injection of 2–4 mL of a 1% tetracycline solution
through the peristomial membrane into the coelomic cavity.
SCUBA divers performed the task using a syringe that
automatically refills, with the gauge set to deliver 2 mL. One
or two injections were administered to each animal according
to its estimated size (approximately 2 mL of tetracycline if
TD ,70 mm, and approximately 4 mL of tetracycline if TD .
70 mm). On 31 January 2011, the tagging site was revisited and
91 sea urchins were collected, returned to the mainland and their
TD measured. Each urchin was dissected and Aristotle’s lantern
and test weighed. The lanterns were cleaned in 10% NaClO
overnight and the jaws separated and inspected for fluorescent
tags under a dissecting microscope equipped with an external
UV light source. Tetracycline that has been incorporated into the
skeleton is fluorescent under UV light. The location of the
fluorescent tag in the jaw represents the length of the jaw at the
time of tagging J
t
. If a tag was found, the total length of the jaw
J
tþ1
and increment DJat the aboral end (i.e. the length of
the portion of jaw that was deposited at the aboral end during the
1-year time interval before tagging and recapture) were mea-
sured and the length of the jaw at the time of tagging J
t
was
obtained (Fig. 2). No measurable growth was present at the oral
end of the jaws. Twenty-four tagged specimens (and jaws) were
recovered.
The relationship between jaw length (J) and test diameter
(TD) was assessed using the following equation:
TD ¼61:821 ln J101:61;
with jaw length converted to TD at the time of tagging (TD
t
) and
at the time of recapture one year later (TD
tþ1
).
Growth model
Three growth equations were used to model growth of
C. rodgersii. The equations used for size (TD
t
) at age (t) were:
Brody–Bertalanffy (von Bertalanffy 1938; Brody 1945)
TDt¼TD1ð1bektÞð1Þ
Richards (Richards 1959)
TDt¼TD1ð1bektÞnð2Þ
and Jolicoeur (Jolicoeur 1985)
TDt¼TD1ð1btkÞ1ð3Þ
where TD
t
is size at time t,TD
N
is the asymptotic size, bis the
scaling parameter to adjust for size t6¼ 0 at time 0, Kis the
growth constant and nis the shape parameter for the Richards
model.
The three growth models were applied to both tetracycline
tagged animals and animals aged from growth lines. To apply
the models to growth-line aged animals, the size versus age
(i.e. the number of growth lines) for each individual was plotted
and the parameters of each growth curve estimated by perform-
ing a non-linear regression using the Newton method.
To estimate growth rates from the tetracycline tagged
animals, the relationship between test diameter at time of
tagging (TD
t
) and test diameter at time of recapture, one year
after marking (TD
tþ1
), was plotted using a Walford plot
(Walford 1946) and either a linear or non-linear regression of
the difference equation for each model used to estimate para-
meters for each growth equation (Ebert and Russell 1992;
Lamare and Mladenov 2000). The difference equations for each
growth model are as follows:
Brody–Bertalanffy
TDtþ1¼cþmTDtð4Þ
Richards
TDtþ1¼cþmTD1
n
t

n
ð5Þ
and Jolicoeur
TDtþ1¼TD1
1bTDtTD1
bTDt

1
kþDt

kð6Þ
Details on parameter fitting can be found in Ebert and Russell
(1992) and Lamare and Mladenov (2000).
Instantaneous growth rates
After fitting curves to the data, the derivative of each growth
equation with respect to time, together with the fitted
parameters, were used to plot the instantaneous growth rate
Tetracycline tag
(a)(b)
10 mm 2.5 mm
ΔJ
Jt
Jt⫹⌬t
Fig. 2. From left to right (a) a demi-pyramid with measurements for growth
modelling indicated and (b) a genital plate of a 5 year old individual with
growth lines visible. Tetracycline tags appear much brighter to the naked eye
than we could obtain by photography.
Growth of Centrostephanus rodgersii in New Zealand Marine and Freshwater Research C

(IGR, mm year
1
) and the age of maximum growth and maxi-
mum growth rate (MGR, mm year
1
) for each curve.
Model comparisons
Growth model fits obtained from growth lines and tag–recapture
data were assessed considering residuals standard sum of
squares error (SSE), distribution of residuals and second order
Akaike Information Criterion (AICc) paired with the D
i
statistic
to compensate for differences in the number of parameters in
each model (Akaike 1974; Burnham and Anderson 1998).
Sea surface temperatures
Changes in sea surface temperature (SST) at the Mokohinau
Islands over the study period were obtained from the SST probe
of the satellite Terra MODIS (http://oceancolor.gsfc.nasa.gov/,
data can be accessed through the ‘Level 3 browser’ by selecting
the appropriate time frame). The SST for the Mokohinau Islands
at each time were calculated from the average SST for a 9 pixels
reticulum (16 km
2
each) centred on the coordinates of the
sampling site.
Statistical analyses
All statistical analyses and non-linear modelling were per-
formed using JMP7 (SAS Institute Inc., Cary, NC).
Results
Morphometrics
A significant relationship existed between demi-pyramid length
and test diameter (R
2
¼0.882, d.f. ¼90, P,0.001, Fig. 3a) and
between test wet weight and test diameter (R
2
¼0.898, d.f. ¼90,
P,0.001, Fig. 3b). Using jaw length and test diameter for
each individual, we calculated a mean s.e. lantern index for
C. rodgersii of LI% ¼26.2 2.2 mm, with the lantern index
found to be independent of test diameter (Fig. 3c).
Marginal increment analysis
An example of a genital plate with alternating opaque and
translucent annular lines can be seen in Fig. 2b. A plot of the
proportion of genital plates with a translucent margin in each
sampling month (Fig. 4a) indicated a peak in the occurrence of
individuals with a translucent margin in September (91.7%). By
November no individuals had translucent marginal bands. The
maximum proportion of individuals with translucent margins
corresponded with the minimum sea surface temperature
(14.8 0.18C, mean s.d.) during the year (Fig. 4b).
Growth parameters estimates from growth lines
The estimated parameters of the three growth models obtained
from fits to the annular lines are summarised in Table 1.
Maximum test diameter estimates were similar among the three
models, ranging from 119.1 mm for the Richards model to
126.4 mm for the Jolicoeur function (Table 1a). The rate of
change in growth was slightly higher for the Jolicoeur curve
(k¼1.698) and similar for the Brody–Bertalanffy and the
Richards curve (k¼0.235 and k¼0.305 respectively, Table 1).
In terms of model goodness-of-fit, all three models have a
similar residual SSE when fitted to the annular data (Table 1),
the lowest being the Jolicoeur curve (SSE ¼6162.6). The D
i
also
indicated that the Jolicoeur model had the highest support
(D
i
¼0), followed by the Brody–Bertalanffy function (D
i
¼1),
and Richards function (D
i
¼3), which were also well supported.
Using the Jolicoeur model, instantaneous growth in C. rodgersii
0
0
0
0
21
22
23
24
25
26
27
28
29
30
31
100
200
300
15
20
25
J (mm)Test wet weight (g)Lantern index (%)
30
35
(a)
(b)
(c)
50 60 70 80 90 100 110
y ⫽ 0.245x ⫹ 1.391
y ⫽ 4.488x ⫺ 214.279
y ⫽ ⫺0.018x ⫹ 27.862
120 130
0 50 60 70 80 90 100 110 120 130
05060708090100
TD (mm)
110 120 130
Fig. 3. Relationship between (a) jaw length (J) and test diameter (TD),
and (b) test wet weight and test diameter and (c) Lantern index (%) and
test diameter for Centrostephanus rodgersii from the Mokohinau Islands,
n¼84.
DMarine and Freshwater Research D. Pecorino et al.

was found to reach a maximum rate of 23.8 mm year
1
at an age
of 1.4 years, with growth decreasing to ,10 mm year
1
by age 5
(Fig. 5). Animals reach a size of ,85 mm TD by age 5 (Fig. 6a),
and approach an asymptotic size of 126 mm TD between 15 and
20 years (Fig. 6a).
Growth parameters estimates from tag–recaptures
The estimated parameters of the three growth models obtained
from tag–recapture data are summarised in Table 1. Maximum
growth rate ranged from 14.3 mm year
1
for the Richards
function to 20.3 mm year
1
for the Brody–Bertalanffy model.
Age of maximum growth rate ranged from 2.8 years in the
Jolicoeur model to 2.5 years in the Richards model and at
settlement (age 0) for the Brody–Bertalanffy model, with the
rate of change in growth rate greatest for the Jolicoeur model
(k¼2.322) and least for the Brody–Bertalanffy model
(k¼0.189) (Table 1). Maximum test diameter was estimated at
TD
N
¼108.0 mm for Brody–Bertalanffy, TD
N
¼106.6 mm for
Richards and TD
N
¼106.2 mm for Jolicoeur (Table 1).
In terms of model goodness-of-fit, the residual SSE for
curves fitted to the tagged individuals was lowest for the
Jolicoeur model (SEE ¼10.574) and highest for the Richards
model (SEE ¼30.387) (Table 1). The AICc gave similar
results, with the lowest D
i
found in the Jolicoeur model (D
i
¼0)
and the highest value in the Richards model (D
i
¼25). All the
models, aside from Jolicoeur, receive essentially no support
from the data when comparing AIC (i.e. D
i
.10; Burnham and
Anderson 1998). Using the Jolicoeur model of growth of the
tagged sea urchins, instantaneous growth in C. rodgersii
was found to reach a maximum rate of 17.7 mm year
1
at an
age of 2.8 years (Table 1, Fig. 5), with growth decreasing
to ,13 mm year
1
by age 5 (Fig. 5). Animals reach a size of
,63 mm TD by age 5, and approach an asymptotic size
of 106 mm TD between 10 and 15 years (Fig. 6b).
For the Jolicoeur model, the residuals move from negative to
positive with increasing size, indicating that growth continues
even after the asymptotic size has been reached. This was also
apparent for the Brody–Bertalanffy and Richards models,
suggesting that growth is continuous in the largest animals.
Discussion
During the past 50 years, the sea urchin C. rodgersii has greatly
expanded its southern distributional range along the south-
eastern Australian and Tasmanian coastlines. This has been
attributed to an increase in the southward and eastward flow of
the East Australian Current and a corresponding increase in sea
surface temperatures along the SE Australian and Tasmanian
coasts (Ridgway 2007; Ling et al. 2009b) that has enhanced
C. rodgersii larval survival and recruitment (Ling et al. 2008).
Anecdotal evidence suggests that the changes in the East
Australian Current may also have allowed for the establishment
of this species in northern New Zealand. Determining if its
occurrence in New Zealand is recent is difficult because very
little is known on the biology of the species in New Zealand,
including aspects of its population biology such as growth,
morphometrics and recruitment. So as to gather information on
the population biology of the species in a new environment,
growth in a New Zealand population of Centrostephanus
rodgersii from the Mokohinau Islands was studied.
Growth was estimated using two methods, the first by
estimating the age of individuals by counting annular lines in
the genital plate and assuming that they are related to differences
in the deposition of the stereom over an annual cycle (Pearse and
Pearse 1975). Aging by this method has been applied to several
echinoderm species (Pearse and Pearse 1975; Gage and Tyler
1985; Nichols et al. 1985; Brey et al. 1985; Gebauer and Moreno
1995; Robinson and MacIntyre 1997; Schuhbauer et al. 2010).
The validity of such a method, however, requires knowing at
what periodicity the growth lines are added because it has been
shown that patterns of calcium deposition rates are not always
correlated with seasonality, but merely to periods of different
abundance of food regardless of season (Ebert 1988). Indeed, in
the case of sea urchins, growth lines have been shown to be
unreliable for some species (Ebert 1988; Russell and Meredith
2000) and therefore validation is essential.
We validated our aging data by marginal increment analysis
(Schuhbauer et al. 2010) to quantify the proportion of indivi-
duals in each sample of genital plates with opaque lines at their
margin. Most of the marginal transluscent bands occurred in
September samples (91.3%), which decreased to 0% in Novem-
ber. This indicates that the deposition of the translucent band is
rapid, probably lasting only 1–2 months, and is followed by the
slow deposition of the opaque band that occurs over the
remainder of the year. This is consistent with a pattern of one
J
0
14
16
18
SST (⬚C) Proportion
20
22
0
0.25
0.50
0.75
1.00
(a)
(b)
FMAM
Month
JJASON
Fig. 4. (a) Proportion of translucent margins at the edges of the genital
plates and (b) mean sea surface temperature at the Mokohinau Islands during
2010.
Growth of Centrostephanus rodgersii in New Zealand Marine and Freshwater Research E

translucent and one opaque line deposited annually in
C. rodgersii, and with growth occurring during or after mini-
mum temperatures, which has also been demonstrated for the
sea urchin Loxechinus albus (Schuhbauer et al. 2010).
We also validated the annual nature of growth lines by
examining the number of opaque and translucent lines in genital
plates deposited in the year following tetracycline tagging. In all
urchins examined, we observed that no more than one pair of
lines (an opaque and a translucent one) was deposited beyond
the fluorescent tag, although in two very large individuals (113.1
and 111.1 mm) there were no lines apparent. This clear
deposition pattern was most evident in the skeletal elements of
smaller specimens in which growth is faster compared with
larger individuals. It also implies that age estimates conducted
using this method are more reliable for young individuals in
which lines are clear and well spaced, than for older individuals,
in which the lines corresponding to the latest deposition of
calcium carbonate tend to overlap. In this case, the age of older
animals will be underestimated.
The second method of estimating growth was through tag–
recapture of tetracycline marked individuals, which, together
with the use of other fluorescent tags, has become widely used to
measure growth in sea urchins (Ebert 1988; Gage 1992; Ebert
and Russell 1993; Bureau 1996; Ebert et al. 1999; Lamare and
Mladenov 2000; Rogers-Bennett et al. 2003; Kirby et al. 2006;
Pederson and Johnson 2008; Ellers and Johnson 2009; Ling and
Johnson 2009; Ling et al. 2009b). The advantage of tagging
individuals is that growth is measured directly without making
assumptions on the growth pattern of the population as a whole
(as done using modal progressions for example).
For both methods of estimating growth, selecting the
appropriate growth model to describe size at age is equally
important. Our conclusion, on the basis of the analysis of the
residuals of the models and the values of D
i
, is that the Jolicoeur
function fitted using growth line data may provide the best
current model of growth for C. rodgersii in New Zealand. The
Jolicoeur model assumes an asymptotic size, which may under-
estimate growth in older individuals, but has been applied to
Table 1. Estimates of Centrostephanus rodgersii growth parameters for the Brody]Bertalanffy, Richards and Jolicoeur
curve by both growth lines and tag]recapture methods
Brody–Bertalanffy Richards Jolicoeur
Growth lines
TD
N
(mm) 122.9 TD
N
(mm) 119.1 TD
N
(mm) 126.4
TD
0
(mm) 1.4 TD
0
(mm) 0 TD
0
(mm) 0
k0.235 k0.305 k1.698
b1.011 b1.012 b7.431
n1.415
Age of MGR 0 Age of MGR 1.1 Age of MGR 1.4
MGR (mm year
1
) 29.1 MGR (mm year
1
) 21.8 MGR (mm year
1
) 23.8
SSE 6212.062 SSE 6210.701 SSE 6162.653
AICc 368 AICc 370 AICc 367
D
i
1D
i
3D
i
0
Tag–recapture
m0.827 m0.757
c18.69 c2.029
TD
N
(mm) 108.0 TD
N
(mm) 106.6 TD
N
(mm) 106.2
TD
0
(mm) 0.5 TD
0
(mm) 0.5 TD
0
(mm) 0
k0.189 k0.278 k2.322
b0.996 b0.921 b28.134
n2.199
Age of MGR 0 Age of MGR 2.5 Age of MGR 2.8
MGR (mm year
1
) 20.3 MGR (mm year
1
) 14.3 MGR (mm year
1
) 17.7
SSE 22.122 SSE 30.387 SSE 10.574
AICc 3 AICc 13 AICc 12
D
i
15 D
i
25 D
i
0
0
0
5
10
15
IGR (mm year
⫺1
)
20
Tag–recapture
Growth lines
25
5
A
g
e (years)
10 15
Fig. 5. Estimated change in instantaneous growth rate (IGR) with age for
Centrostephanus rodgersii for growth line counts and tag–recapture
methods.
FMarine and Freshwater Research D. Pecorino et al.

several temperate sea urchin species (Ebert and Russell 1993;
Lamare and Mladenov 2000; Lau et al. 2011). Using this model,
growth of C. rodgersii in northern New Zealand shows an initial
lag phase over the first year of growth, with a maximum
instantaneous growth of 23.8 mm year
1
at 1.4 years, when
the animals have reached a size of 26.7 mm. Growth rate
decreases beyond this size with an asymptotic size approached
at ,10–15 years. The initial lag in growth likely reflects dietary
constraints to growth on smaller cryptic individuals when they
may not have access to macroalgae in their first year. Initial lags
in growth followed by accelerated growth have been described
for juvenile sea urchins and have been attribute to dietary shifts
and movement from cryptic to open habitats (Raymond and
Scheibling 1987; Rowley 1990; Lamare and Mladenov 2000).
The subsequent decrease in growth after ,3 years is likely
related to the onset of gametogenesis, which causes nutrients to
be shifted from somatic to gonadic growth. Indeed, gonad
production is only evident in New Zealand C. rodgersii
individuals at a size of 40–50 mm TD (3–4 year old) (Pecorino
et al. in press), which coincides with the size and age of
decreasing somatic growth rates.
Modelled growth of C. rodgersii in this New Zealand
population was faster than that estimated for Tasmanian popula-
tions. Comparing growth of C. rodgersii in this New Zealand
population with the Tasmania population (Fig. 7) suggests that,
for individuals older than 1 year, the species has a higher growth
rate in New Zealand. Even when the same inverse logistic model
used by Ling et al. (2009b) is applied to both New Zealand and
Tasmanian populations, a higher growth rate in New Zealand
was observed (Table 2). Estimated growth to 1 year was
equivalent in both populations (Table 2). The divergence in
growth rates after 1 year would be at an age when fast growth
and a shift in diet to macroalgae probably occur, so it is possible
that the faster growth in New Zealand is related to higher food
availability in this environment. A larger jaw size (i.e. lantern
index) is often used as a proxy for poorer nutritional status in sea
urchins (Ebert 1980; Black et al. 1982, 1984; Levitan 1991;
Hagen 2008; Lau et al. 2009) and we might, therefore, expect to
see differences between the two populations if food is limiting
growth. A comparison of lantern indices between the New
Zealand populations with those recorded by Ling et al.
(2009b) for the macroalgal habitat in Tasmania shows only a
small difference, with the latter populations having smaller
jaws, relative to test diameter (i.e. jaw height of ,22 mm in
New Zealand and ,20 mm in Tasmania at a test diameter of
80 mm). There was no difference between the populations in
other morphometric measurements such as the wet weight of the
test, therefore nutritional differences between the two popula-
tions are only partially supported.
Growth rate may be related to differences in ambient water
temperatures. Indeed, the faster growth rate of New Zealand
populations coincides with a 38C warmer winter sea surface
temperature (158C versus 128C) and a ,48C warmer summer
temperature (218C versus 16–188C), which would be consistent
with a positive effect of temperature on growth rate. Ebert et al.
(1999) suggest that temperature does not influence growth rates
within a species across a range of latitudes, whereas there are
several laboratory studies that have shown a direct relationship
between growth rate and optimal temperatures when other
variables such as food are kept constant (Spirlet et al. 2000;
Pearce et al. 2005; Watts et al. 2011). Similarly, a field study by
Duineveld and Jenness (1984) on the echinoid Echinocardium
0
0
20
40
60
TD (mm)
80
100
120
12345
A
g
e (
y
ears)
67891011
0
0
20
40
60
80
100
120
(a)
(b)
1234567891011
Fig. 6. Growth curves of Centrostephanus rodgersii using data from
(a) growth lines counts (n¼84) and (b) tag–recapture jaw growth estimates
(n¼24).
0
0
20
40
60
TD (mm)
80
100
120
510
New Zealand – Jolicoeur (growth lines)
New Zealand – Jolicoeur (tag–recapture)
Tasmania – Inverse logistic (tag–recapture)
New Zealand – Inverse logistic (tag–recapture)
15 20
A
g
e (years)
25 30 35
Fig. 7. Comparison of size-at-age plotted using the parameters obtained
from the tag–recapture and growth lines in New Zealand Centrostephanus
rodgersii, and from a tag–recapture study of Centrostephanus rodgersii in
Tasmania (Ling et al. 2009b).
Growth of Centrostephanus rodgersii in New Zealand Marine and Freshwater Research G

cordatum suggested higher growth rates for individuals at higher
temperatures. Given that C. rodgersii is a warmer water species,
and the Tasmanian populations are at the colder end of the
species range, it is possible that these newly established
populations are living in suboptimal temperatures in terms of
growth.
Unlike Tasmanian populations that have colonised regions
lacking large heterospecific sea urchin populations, C. rodgersii
in New Zealand lives sympatrically with the dominant native
echinoid E. chloroticus, whose strong grazing activity has been
shown through removal experiments (Villouta et al. 2001). The
degree to which the two species interact in terms of competition
is unknown, although, given the abundance of E. chloroticus
(densities of up to 40 individuals per m
2
in northern New
Zealand; Choat and Schiel 1982) and the ability of this species
to form barrens, it could potentially limit C. rodgersii in New
Zealand. Indeed, the slightly larger lantern indices observed in
the New Zealand populations of C. rodgersii may reflect some
food limitation exerted by a strong competitor. A similar case of
interspecific competition has already been reported for Para-
centrotus lividus and Arbacia lixula in the Mediterranean
(Privitera et al. 2008), with such competition resulting in food
limitation and a shift in the trophic niche of P. lividus (from
generalist to grazer of non-encrusting macrophytes) when
A. lixula is present at high population densities.
An important component of the interaction between
E. chloroticus and C. rodgersii in New Zealand will be differ-
ences in the growth between the two species, which could, in
turn, affect their survival rates through size-specific predation
and their ability to dominate resources. Growth of E. chloroticus
has been well described (McShane and Anderson 1997; Lamare
and Mladenov 2000) and when compared with C. rodgersii,
exhibits a lower maximum growth rate (15.1–16.8 mm year
1
for E. chloroticus and 23.8 mm year
1
for C. rodgersii) attained
at an older age (4.0–4.8 years and 1.4 years respectively). This
difference in size and growth rate may influence the suscepti-
bility of the two species to predation by, for instance, the rock
lobster Jasus edwardsii. Andrew and MacDiarmid (1991)
showed that this species can predate all sizes of E. chloroticus,
but that preference is given to smaller sea urchins (,50 mm).
The same species of rock lobster also predates C. rodgersii,
although they tend to target larger individuals. Ling et al.
(2009b) found that only very large rock lobsters (carapace
length .140 mm) are able to predate C. rodgersii in the field,
and smaller sea urchins (,60 mm TD) are not targeted due to
their cryptic nature.
Crucial to the understanding of future population dynamics
of C. rodgersii is information on recruitment processes in New
Zealand populations. Our data on size distributions (Fig. 8a,b)
show a poly-modal distribution of sizes of C. rodgersii at the
Mokohinau Islands characteristic of a population with ongoing
Table 2. Average estimates of size at age for Centrostephanus rodgersii in New Zealand and Tasmania using similar techniques
*¼present study; y¼Ling et al. 2009b;y¼method by Ling et al. 2009bapplied to the data of this study
Method Average test diameter (mm)
Age (years) 1 2 3 4 5 6
Growth lines (New Zealand) 15.00 38.45 58.82 74.15 85.28 93.38
Jolicoeur *
Tag–recapture (New Zealand)
Jolicoeur * 3.65 16.03 33.25 49.98 63.60 73.83
Inverse logistic y15.15 25.67 36.15 46.54 56.71 66.35
Tag–recapture (Tasmania)
Inverse logistic y15.58 26.16 36.60 46.72 56.26 64.79
3
55 65 75 85 95 105 115 125
0
5
10
15
Frequency
20
25
30
0
5
10
15
20
(a)
(b)
4567
A
g
e (
y
ears)
TD (mm)
89ⱖ10
Fig. 8. (a) Size-frequency and (b) age-frequency distributions for Cen-
trostephanus rodgersii collected from the Mokohinau Islands between
January 2010 and December 2011 (n¼155).
HMarine and Freshwater Research D. Pecorino et al.

recruitment and supply of settling larvae. Ling et al. (2008)
showed that the larvae of C. rodgersii have a thermal threshold
of 128C, below which advanced two-arm plutei will not develop.
The continuous recruitment events at the Mokohinau Islands,
therefore, suggest that larval development is not prevented or
hindered at sea temperatures presently experienced in the area,
which are 158C, and above the thermal threshold for their larvae.
Whether the long-lived larvae (4 months; Huggett et al. 2005)
are originating from local populations or are being transported
from Australia is unknown. It is clear that the populations in
New Zealand are undergoing a characteristic annual reproduc-
tive cycle and are producing viable gametes (Pecorino et al.
in press) meaning that local recruitment is possible. Equally,
genetic evidence indicates that the Australian and New Zealand
populations are not genetically separate (Banks et al. 2007) so
ongoing trans-Tasman transport of larvae can also not be
discounted.
C. rodgersii may be a new arrival to New Zealand, and its
ability to compete with and displace the existing species is of
interest. Quantifying growth rates of this species in New
Zealand is an important element of understanding how it will
interact with close competitors such as E. chloroticus, and its
wider affect on its habitat. Further research is needed to under-
stand the population biology of the species in New Zealand,
especially in relation to reproduction and recruitment under
New Zealand oceanic conditions.
Acknowledgements
The authors thank the staff of Portobello Marine Laboratory (Otago, New
Zealand) and of Leigh Marine Laboratory (Northland, New Zealand), Jake
Lamare for helping with the dissections of the sea urchins and collection of
biometric data, and Miles Hayward for his hospitality during field work.
They also wish to acknowledge the University of Otago for the Postgraduate
Scholarship to Danilo Pecorino, and the staff of Goat Island Dive Centre in
Leigh (Northland, New Zealand) for helping with collection of the sea
urchins. Thanks also to Dr. Bob Scheibling for assisting with tagging.
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