Journal of Experimental Marine Biology and Ecology 321 (2005) 135 – 144

www.elsevier.com/locate/jembe

The relationship between egg size and the duration of the

facultative feeding period in marine invertebrate larvae
Benjamin G. Minera,b,T, Lari A. McEdwarda, Larry R. McEdwarda,F
a
Department of Zoology, University of Florida, Gainesville, FL 32611-8525, United States
b
Bodega Marine Laboratory, University of California, Davis, P.O. Box 247, Bodega Bay, CA 94923-0247, United States
Received 1 November 2004; received in revised form 25 November 2004; accepted 22 January 2005

Abstract

Feeding larvae of marine invertebrates fuel development from both endogenous egg energy and exogenous energy obtained
from the planktonic environment. Although both sources of energy likely influence certain larval stages, only the effects of
exogenous food have been well studied. Despite the lack of research on the effects of egg size on larval stages, investigators
have hypothesized that egg size influences the duration of the facultative feeding stage—the stage in which larvae can feed but
do not have to because development is still being fueled by egg energy. To test this hypothesis, we investigated six species of
sand dollars with different sized eggs and quantified the duration of the larval facultative feeding period of each species by
comparing when fed and starved larvae diverged in size. Regardless of whether phylogeny was taken into account, the duration
of the facultative feeding period was positively correlated with egg size. We further determined that our conclusions were not
sensitive to either our estimation of the duration of the facultative feeding period, or the branch lengths of the phylogeny we
used. This relationship is likely a result of larger eggs being provisioned with more energy, and may affect how well larvae can
cope with natural variability in food concentrations. Furthermore, our results support an assumption of a theoretical model
developed to understand the evolution of different life-history strategies in marine invertebrate larvae, which suggests that this
relationship has important evolutionary consequences.
D 2005 Elsevier B.V. All rights reserved.

Keywords: Echinoid; Egg size; Feeding; Larvae; Life history; Marine invertebrates; Model; Sand dollar

1. Introduction

Many benthic marine invertebrates possess a

larval stage early in development, and these larvae
T Corresponding author. Bodega Marine Laboratory, University of are morphologically and ecologically diverse within
California, Davis, P.O. Box 247, Bodega Bay, CA 94923-0247,
United States. Tel.: +1 707 875 2038; fax: +1 707 875 2009.
and among phyla (Nielsen, 1995; Young et al.,
E-mail address: bgminer@ucdavis.edu (B.G. Miner). 2002). Despite this diversity, there is an obvious
F
Deceased. dichotomy among species with planktonic larvae.
0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2005.01.008
136 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144
Species typically produce either small eggs that
develop into larvae that must feed (planktotrophy),
or large eggs that develop into nonfeeding larvae
(lecithotrophy; Thorson, 1946, 1950). Both types are
found in almost every animal phylum, and phyloge-
netic analyses suggest an evolutionary transition
between the two types has occurred many times
(Wray, 1996; Duda and Palumbi, 1997; Cunningham,
1999; Rouse, 2000; McEdward and Miner, 2001). A
factor that appears to play an important role in this
evolutionary transition is the amount of energy
provisioned in an egg. Larvae must have the ability
to feed if they develop from a small energy-poor
egg. In contrast, nonfeeding larvae can only evolve
when larvae develop from a relatively large energy-
rich egg that provides a larva with all the energy
necessary to complete larval development.
The importance of egg size on the evolution and
ecology of these two strikingly different strategies
prompts the question whether egg size plays an
important ecological or evolutionary role within
either planktotrophic or lecithotrophic strategies.
Herrera et al. (1996), and McEdward and Janies
(1997) have suggested that among planktotrophs,
egg size might influence the duration of a certain
larval stage. There are three general stages during the
development of feeding larvae—the pre-feeding
stage, the facultative feeding stage, and the obligate
feeding stage. The pre-feeding stage begins at
fertilization and ends when larvae are first able to
acquire particulate food. The facultative feeding
stage follows the pre-feeding stage, and ends when
egg reserves are exhausted. Thus, during the
facultative feeding stage larvae can feed but do not
have to (i.e. larvae cannot starve during this stage).
The obligate feeding stage follows the facultative
feeding stage and ends at metamorphosis. During the
obligate feeding stage, larvae must acquire exoge-
nous food or starve.
Of these three stages, Herrera et al. (1996), and
McEdward and Janies (1997) argued that the
duration of the facultative feeding stage is likely
most influenced by egg size. The onset of feeding
does not appear to correlate with egg size (Herrera,
1998), and thus the duration of the pre-feeding stage
is likely independent or weakly dependent on egg
size. The duration of the obligate feeding stage is
also likely independent of egg size. Although the
beginning of the obligate feeding stage is probably
influenced by egg size, the end of this stage is
influenced by the amount of exogenous food
acquired, and therefore food probably has the
greatest effect on the duration of this stage.
However, the duration of the facultative feeding
stage might be strongly correlated with egg size,
given that the onset of this stage appears to be
independent of egg size, yet the end of this stage is
dependent on the amount of maternal reserves
available during this stage.
It is also possible that egg size doesn’t affect the
duration of the facultative feeding period, but some
other aspect of larval development. For example,
larvae that develop from larger eggs might be
greater in size, and because energy was spent on
building a larger larva, egg size has little or no
effect on the duration of the facultative feeding
period.
Whether or not egg size affects the duration of the
facultative feeding stage has biological consequen-
ces. McEdward (1997) developed a model, modified
from Vance (1973), which incorporated the facul-
tative feeding stage. By incorporating this stage he
found that an intermediate egg size was optimal
within planktotrophs—a pattern observed in nature,
and different from predictions of previous models
(Vance, 1973; Christiansen and Fenchel, 1979;
Roughgarden, 1989). An important assumption made
by McEdward (1997) was that the duration of the
facultative feeding period is related to egg size. If
this assumption is not correct, then the predictions of
the model are qualitatively different and inconsistent
with nature.
To determine whether the duration of the
facultative feeding stage is correlated with egg
size, we quantified the duration of the facultative
feeding period in three pairs of closely related
species of sand dollars that differed in egg size.
For each species, we measured larvae reared with
and without food to determine when starved larvae
stopped growing—indicating the exhaustion of
maternally derived egg reserves and the end of
the facultative feeding period. We then calculated
the proportion of larval development spent facul-
tatively feeding for each species and tested whether
it correlated with egg size (with and without
considering phylogeny).
 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144
2. Methods
2.1. Adult collection and larval rearing
Adult sand dollars were collected from shallow
marine habitats around Florida USA during the
spring and summer of 1999 and 2000. Clypeaster
rosaceus, Encope aberrans, and Leodia sexiesper-
forata were collected near Long Key, and subsequent
experiments on these species were conducted at the
Long Key Marine Laboratory. Clypeaster subdepres-
sus and Mellita tenuis were collected near Seahorse
Key. Individuals were brought to the University of
Florida, and held in re-circulating tanks for no more
than a month before adults were spawned and an
experiment started.
We used a standard protocol (Strathmann, 1987)
to collect gametes from each species. Eggs were
fertilized and zygotes were reared in 2-L glass
beakers with 0.45 Am Millipore-filtered seawater
(FSW) until blastulae hatched. Five-hundred blastu-
lae and 1.6 L of FSW were then placed in each of
the six 2-L glass beakers. Natural seawater collected
from the Atlantic Ocean, near the Whitney Marine
Laboratory, was used for all experiments. Three of
the six beakers were randomly assigned to a fed
treatment and the other 3 beakers to a starved
treatment. Larvae in the fed treatment were given 6
cells AL
1 of the unicellular alga Dunaliella tertio-
lecta. To clean a beaker, we removed 90% of the
water by siphoning water through NytexR mesh (45
Am). This mesh size allowed us to remove the food
yet retain the larvae in a beaker. We poured the
remaining water and larvae into a clean 2-L beaker
and refilled it to 1.6 L with FSW. All beakers were
cleaned every 2 days. Immediately after each water
change, we added food to the beakers of the fed
treatment.
For larval food, we reared the alga D. tertiolecta in
f/2 algal medium. Just before each larval feeding, we
measured the density of an algal culture in log-phase
growth with a hemocytometer, and calculated the
amount of algal culture needed. We removed the algal
growth medium by centrifuging the algal culture,
decanting the supernatant, and re-suspending the
algae in a known amount of FSW. The approximate
number of algal cells was then added to the
appropriate larval beakers.
137
2.2. Larval morphometrics
Larvae were sampled 24 h after fertilization with
the exception of C. rosaceus, which was sampled 36
h after fertilization. We then measured larvae every
12 h with the exception of L. sexiesperforata, which
was sampled every 6 h. L. sexiesperforata develops
much faster than the other species investigated. For
all species, both treatments were sampled as follows.
Several larvae were haphazardly pulled from each
beaker of a treatment, pooled, and preserved in 1%
formalin. Within 10 h, ten larvae from each treat-
ment were haphazardly chosen and their skeletons
measured. The lengths of the following skeletal rods
were measured: postoral arms, posterodorsal arms,
anterolateral arms, preoral arms, body rods, ventral
transverse rods, dorsal transverse rods, and dorsal
arch tail (Fig. 1). With the exception of the dorsal
arch tail, we present the average of the left and right
sides of the larva. Because we investigated species
with relatively large eggs, the larvae were very yolky
and opaque. To make the tissue transparent for
measuring the skeleton, we used the following
procedure. We put larvae through 3 ethanol (EtOH)
washes (70, 90, and 100% EtOH). After larvae were
dehydrated, they were placed in clove oil. The
density of clove oil is similar to lipid, and makes
larvae transparent. This process does not affect the
length of the larval skeleton. For accuracy, we
99 33
11
10
66
11
55
22
88
77
44
Fig. 1. Larval skeletal measurements: (1–2) postoral arm rod, (6–7)
posterodorsal arm rod, (9–10) preoral arm rod, (2–3) anterolateral
arm rod, (2–4) body rod, (2–5) ventral transverse rod, (7–8) dorsal
transverse rod, and (10–11) dorsal arch tail.
138 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144
measured larvae in 3 dimensions with a light
microscope (20) equipped with differential inter-
ference contrast (McEdward, 1985).
2.3. Estimating the duration of the facultative period
The length of the facultative feeding period was
measured as the time from fertilization to diver-
gence between the fed and starved treatments. This
estimate is based on the argument that development
rate should decrease in starved larvae when they
run out of egg energy. However, the allometric
growth of larval characters was unknown, so we
compared the larval skeleton size between starved
and fed larvae to determine when starved larvae
stopped growing. Additionally, our estimate of the
facultative period includes the pre-feeding period
because we were not able to observe when larvae
of each species began to feed—clove oil also makes
algal cells transparent. Instead, we used fertilization
as the beginning of the facultative period, even
though this overestimates the duration of the
facultative period. We decided to use this estimate
for several reasons. In species with plutei, the onset
of feeding occurs when larvae develop a second
pair of arms (i.e. 4-arm stage), and the rate of
development at which larvae reach this stage has
been shown not to correlate with egg size, but with
development time (Herrera, 1998). Thus, by analyz-
ing the proportion of development spent faculta-
tively feeding (see below), our overestimate of the
facultative period only affects the intercept of the
regression (which is not tested with Independent
Contrasts analysis), and not the significance or
slope of our analyses.
We determined when fed and starved larvae
diverged in size as follows. For each species, we
performed a Principal Component analysis (PCA) on
the log-transformed data, and used the principal
component scores from the first principal component
axis (PC1) to test for differences in larval skeleton
size between the fed and starved treatments. The
PC1 scores provide an estimate of overall larval size,
and incorporate information from all the skeletal rods
providing us with a better estimate of size as
compared to any one skeletal rod measurement. In
addition, any single skeletal rod only provides
information on size for a proportion of larval life
(because different rods start and stop growing at
different points during larval development); and
since we expect species to diverge at different larval
stages, we feel PC1 scores provide a consistent way
to detect divergence in all species. A T-test was
performed to determine whether the two treatments
differed in PC1 scores (i.e. size) at each sample date
for each species. For a species, divergence was
assessed only if the two following conditions were
met: (1) there was a significant difference between
the two treatments, and (2) all subsequent sampling
dates were also significant. Condition 2 decreases the
risk of falsely rejecting the null hypothesis of no
difference between treatments. Divergence time for
each species was assumed to occur sometime
between the first sampling date that met both
conditions (upper estimate), and the preceding date
(lower estimate). We used these estimates of
divergence time to estimate the length of the
facultative feeding period (h). To complement these
estimates, we also estimated the length of the
facultative feeding period with a percent difference
between treatments (as opposed to a statistical
estimate of divergence, which is influenced by the
variance in a treatment). With the percent different
approach, divergence was considered to have
occurred when larvae from the fed treatment were
25% larger than larvae from the starved treatment.
To do this we back-calculated the factor scores from
PC1 to the original units. Because the results from
both approaches (the statistical and percent diver-
gence) were very similar, we have just presented the
statistical divergence because it was the more
conservative of the two.
For each species, the proportion of larval develop-
ment spent facultatively feeding–abbreviated as
PDFF–was then calculated in order to facilitate
comparisons among species. Because larvae of each
species develop at different rates, we divided the end
of the facultative period (h) by the total length of
larval development (h) for each species. The total
length of larval development for a species was taken
from our experiments or the literature.
2.4. Statistical analyses
Without considering phylogeny, we first tested
whether egg volume and the PDFF were correlated.
 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144
v1
v7 M. tenuis
v2
v10 L. sexiesperforata
v3
v8 E. aberrans
v4
E. michelini
v5
v9 C. subdepressus
v6
C. rosaceus
Fig. 2. Phylogenetic relationship among the six species investigated
(based on Mooi, 1987, 1990).
Egg volume was calculated with the following
equation.
p
volume ¼ d diameter3
6 randomly chose values between the upper and lower
We calculated the midpoint between the lower and
upper estimate of the PDFF for each species, and
performed a linear regression analysis (PDFF vs. egg
volume). Although we were unable to get embryos
from Encope michelini, Eckert (1995) provided the
needed data to calculate the PDFF, and we included
this species in our analysis.
To take phylogeny into account, we estimated the
relationship between PDFF and egg volume with an
Independent Contrasts analysis (Felsenstein, 1985).
The phylogenetic tree we used was taken from Mooi
(1987, 1990) (Fig. 2). We could not find information
on the branch lengths, so we initially made the
assumption that all branch lengths were equal and
assigned each branch a value of 1. The contrasts were
calculated on the raw data because the relationship
between egg volume and PDFF appears linear, an
important assumption of independent contrasts anal-
ysis (Quader et al., 2004), and there is no biological
expectation that this relationship is not linear. We
analyzed the contrasts with a linear regression through
the origin to determine whether there was a significant
positive relationship between the contrasts for egg
volume and PDFF, which indicates a positive relation-
ship between the original variables.
Because there is a large amount of uncertainty
associated with each branch length, we tested whether
trees with different branch lengths produced different
results. We randomly generated 10,000 trees with
branches of different lengths (but the same topology),
and performed an independent contrast analysis on
139
each tree. For a given tree, we randomly assigned each
branch a length N0 and V1, while constraining
branches that diverged from a common ancestor to
be equal. We then compared the slope and p-value
estimated when all branch lengths were equal to 1
with the distribution of slopes and p-values estimated
when branch lengths differed. We further examined
which branches had a relatively large effect on the
significance or slope of the relationship by plotting the
length of each branch against the p-value or slope.
In addition to the uncertainty surrounding branch
lengths, our estimates of the PDFF also have a
relatively large amount of uncertainty, and might be
any value between the upper and lower estimate.
Thus, we also investigated whether our results were
sensitive to the PDFF estimate. To do this, we
estimate from a uniform distribution for each species,
and performed an independent contrasts analysis with
an equally branched tree (our results suggest that our
conclusions are not sensitive to the assumption of
equal branch lengths). We repeated this 10,000 times
to generate distributions of p-values and slopes, and
compared these distributions with the results gener-
ated when we assumed the PDFF ended midway
between the lower and upper estimates.
3. Results
The first principle component (PC1) captured over
half the variance in data for all species except L.
sexiesperforata (Table 1). In addition the factor
loadings were mostly large and positive indicating
that PC1 represents the general size of the larval
skeleton (Table 2). The small or negative loadings on
PC1 for the body rod and the ventral transverse rod
are because these rods either stop growing early in
development or are re-absorbed during development.
Table 1
Percent variance explained by PC1, PC2, and PC3-8
Species PC1 PC2 PC3-8
Mellita tenuis 52 19 29
Leodia sexiesperforata 41 18 41
Encope aberrans 58 15 27
Clypeaster subdepressus 61 15 24
Clypeaster rosaceus 65 13 22
140 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144
Table 2
Factor loadings for PC1
Skeletal rod Mellita tenuis Leodia sexiesperforata
Postoral arm rod 0.864 0.452
Body rod
0.116
0.586
Ventral transverse rod
0.207
0.720
Anterolateral arm rod 0.940 0.703
Dorsal arch tail 0.777 0.699
Dorsal arch 0.940 0.785
Posterodorsal arm rod 0.930 0.881
Dorsal transverse rod 0.911 0.821
The fed and the starved treatments diverged in all
species except C. rosaceus (Fig. 3). The lack of
divergence in C. rosaceus was expected because
previous work on C. rosaceus demonstrated that the
length of larval development is not affected by food
(Emlet, 1986). The end of the facultative feeding
period ranged from 2 days to 7 days, which translated
into a range of the PDFF between 0.14 (C. sub-
depressus) and 1.0 (C. rosaceus; Table 3). In other
words, 14% to 100% of larval development is spent
facultatively feeding.
Egg volume and the PDFF were positively
correlated, regardless of whether or not phylogeny
was accounted for. The analysis of the original
variables, which did not consider phylogeny, indicated
that the intercept was not significantly different from
zero, whereas the slope was significantly greater than
zero (intercept=0.045, p=0.41; slope=92.06, pb0.001;
r-squared=0.96). The analysis on the contrasts, which
considered phylogeny, also indicated that the slope
was significantly greater than zero (slope=97.55,
p=0.002; r-squared=0.97; Fig. 4).
When we randomly generated values of the PDFF
between the upper and lower estimates, we always
found a significant positive relationship between the
PDFF and egg size (alpha=0.05; Fig. 5). Our
estimation of the slope from the independent contrasts
analysis (which was 97.55) matched well with the
generated distribution of independent contrasts slopes
(normally distributed with a mean of 97.57 and a
variance of 1.3; Fig. 6A). However, our estimation of
the slope using the original variables (which was
92.06) fell outside and was less than the generated
distribution of slopes calculated from the original
variables (normally distributed with a mean of 99.3
and a variance of 1.2; Fig. 6B).
Encope aberrans Clypeaster subdepressus Clypeaster rosaceus
0.753 0.532 0.877

0.410 0.117 0.107
0.049
0.787 0.537
0.902 0.701 0.975
0.862 0.661 0.757
0.949 0.790 0.948
0.935 0.845 0.954
0.734 0.325 0.892
For the situation where we randomly generated
trees with different branch lengths, we found that
96.8% of the trees resulted in a significant positive
relationship between the PDFF and egg size
(alpha=0.05; Fig. 7A). The distribution of slopes
indicated a wide range of possible slopes from 79.1 to
146.6 (Fig. 7B). However, there was an obvious peak
at 106. The bClypeasterQ branch (v9; Fig. 2) was the
only branch that had an obvious affect on the
significance of the results. The more recently the
two Clypeaster species diverged, the smaller the p-
value (Figure not shown).
4. Discussion
There was a positive correlation between the
proportion of larval development spent facultatively
feeding (PDFF) and egg volume, regardless of
whether or not we considered phylogeny. In addition,
this result was robust to the uncertainty in our
estimation of the PDFF, and the uncertainty in the
length of phylogenetic branches.
Our results support the assumption made by
McEdward (1997) that the length of the facultative
feeding period is correlated with egg size. The
McEdward (1997) model indicated that including a
facultative period in development resulted in a shift in
the optimal egg size predicted by fecundity–time
models (i.e. optimum at the boundary between
planktotrophy and lecithotrophy, s=1) to a smaller
optimal egg size (sb1). McEdward (1997) suggested
that this might explain why an intermediate egg size
for planktotrophs is most common in nature.
Although we demonstrate that one assumption of
the McEdward (1997) model is supported, other
 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144 141

* *
2 2
C. subdepressus C. rosaceus
1 * * 1

0 0
*
-1 -1
Fed
-2 Starved -2

-3 -3
24 36 48 60 72 84 96 108 24 48 72 96 120

2
* * 2
M. tenuis
* L. sexiesperforata *
Factor score for PC1

1 1

0 0

-1 -1

-2 -2

-3 -3
24 36 48 60 72 84 30 36 42 48 54 60

2
E. aberrans *
1 * * * *
0

-1

-2

-3
24 36 48 60 72 84 96 108

Time (hrs)
Fig. 3. Graph of divergence times. For each of the five species, factor scores of the first principle component axis (PC1) vs. time for fed and
starved larvae. Asterisks indicate when treatments differed, and arrows indicate our estimate of the end of the facultative feeding period. Error
bars representFone standard error.

assumptions still require empirical testing, or have
been shown to be violated. McEdward (1997)
assumed that all the basic underlying relationships
were linear. Although, our data suggest the relation-
ship between the PDFF and egg size is linear, the
relationship was estimated with only 5 data points
and does not provide strong evidence for the shape
of the relationship. It would therefore be interesting
to see how changes in the shape of the relationship
between the PDFF and egg size affect the predictions
of McEdward’s (1997) model. If they do, then
further empirical data will be needed to parameterize
the model. Furthermore, Levitan (2000) demonstra-
ted that a non-linear relationship between develop-
142 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144

Table 3 There are several possible proximate explanations

Egg size data, and the estimates of the facultative feeding period for for the correlation between the PDFF and egg size.
the six species used in our analyses
One hypothesis is that an increase in the amount of
Species Egg Time to End of PDFF
egg energy fuels a longer PDFF. Egg energy and egg
diameter metamorphosis fac (h)
(Am) (d) size are positively correlated among species in
echinoderms (Jaeckle, 1995; McEdward and Morgan,
Mellita tenuis 125 10 48–60 0.2–0.25
Leodia 200 5 54–60 0.45–0.5 2001), and thus larger eggs have more energy. Both
sexiesperforata the increase in egg energy and the increase in the
Encope 175 14 72–120 0.214–0.357 PDFF with egg size suggest that there is a causal link
michelini a between egg energy and the PDFF. A second
Encope aberrans 190 7b 48–60 0.286–0.357
hypothesis is that individuals with a longer PDFF
Clypeaster 165 18c 60–72 0.139–0.167
subdepressus produce smaller larvae. Energy is saved by producing
Clypeaster 270 7c 168c 1.0 a smaller larva, and the energy saved fuels a longer
rosaceus PDFF. A third hypothesis is that individuals with a
Values for the last two columns indicate the lower and upper longer PDFF produce smaller juveniles. By producing
estimates. Egg diameters were calculated from 2 females (n=25) for a smaller juvenile, larvae would require less energy to
each female. metamorphose and the duration of the obligate
a
Data from Eckert, 1995.
b
Data from Herrera, 1998.
feeding period would be reduced. The reduction in
c
Data from Emlet, 1986. the obligate feeding period would result in an increase
in the PDFF. However, qualitatively there is no
indication that the PDFF is correlated with larval or
ment time and egg size can also affect the optimal
egg size, and thus provides an alternative explanation
for why an intermediate egg size is most common 800 A
among planktotrophs. Given that both models,
McEdward (1997) and Levitan (2000), provide 600
important but different mechanistic explanations for
why intermediate egg sizes are favored among 400
planktotrophs, future models should include both
200
facultative feeding (not incorporated in the Levitan
Frequency

model) and the observed non-linearity in the relation-

0
ship between development time and egg size (not
incorporated in the McEdward model). B
1500

0.6
Contrasts for proportion of

1000
facultative period

0.4
500

0.2
0
0.002 0.004 0.006 0.008 0.01
0
P-value

-0.2 Fig. 5. Sensitivity of significance to our estimate of the PDFF. A

-0.003 -0.001 0.001 0.003 0.005 frequency distribution of p-values calculated from (A) an inde-
Contrasts for egg volume (ml) pendent contrasts analysis, or (B) a regression analysis of the raw
data for 10,000 generated data sets. For each data set, values of the
Fig. 4. Independent contrasts analysis. Contrasts for the PDFF vs. PDFF were randomly generated between the upper and lower PDFF
contrasts for egg size. estimates.
 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144 143

juvenile size (Levitan, 2000), making the last two 30

hypotheses unlikely. A
25
There are important ecological and evolutionary
consequences for larvae with different durations of 20
facultative feeding. Larvae can acquire needed food 15
during either the facultative feeding period or the
10
obligate feeding period. Changes in the PDFF there-

Frequency (hundreds)
fore affect the amount of food that is required to 5
metamorphose, but not the time in which larvae can 0
capture food. This means that changes in the PDFF 0.025 0.05 0.075 0.1 0.125
P-value
affect the rate at which larvae need to acquire food.
This may be important for plutei because food is 12
temporally and spatially variable and plutei vertically B
migrate dielly (Pennington and Emlet, 1986). As a 10
result plutei almost certainly experience variable food 8
concentrations within a larva’s life. Species with
6
longer facultative feeding periods might therefore be
able to survive when food is more variable. 4
The facultative feeding period might also have 2
important consequences for postlarval stages. Clearly,
0
80 100 120 140
800 A Slope

Fig. 7. Sensitivity to phylogenetic branch length. A frequency

600 distribution of the (A) slope and (B) p-value for 10,000 randomly
generated phylogenies with different branch lengths.
400

in the case of feeding larvae where the facultative

200
feeding period represents nearly the entire time from
Frequency

the pre-feeding stage to metamorphosis, feeding does

0 not have a large effect on development time, but
might affect juvenile performance (Emlet and Hoegh-
800 B Guldberg, 1997; Moran and Emlet, 2001; Phillips,
2002). Larvae with a longer PDFF will use less
600 exogenous energy to complete larval development and
have more energy to spend as a juvenile. Incorporat-
400 ing possible postlarval advantages associated with the
PDFF into recent fecundity–time models might
200 provide insights into the advantages of large lecitho-
trophic eggs.
0
94 96 98 100 102
Slope
Acknowledgements
Fig. 6. Sensitivity of the slope to our estimate of the PDFF. A
frequency distribution of the slope calculated from (A) an We would like to thank J. Cowart, A. Heyland, C.
independent contrasts analysis, or (B) a regression analysis of the
raw data for 10,000 generated data sets. For each data set, values of
Miles, A. Reitzel, T. Edward, and B. Walling for help
the PDFF were randomly generated between the upper and lower with data collection, and M. Miner, A. Mace, J.
PDFF estimates. Shinen, and S. Morgan for comments on the manu-
144 B.G. Miner et al. / J. Exp. Mar. Biol. Ecol. 321 (2005) 135–144
script. The manuscript was further improved by D.
Levitan’s review and suggestions. This work was
supported by a NSF grant to L. McEdward (OCE
9819593), and a NSF grant to S. Morgan and B.
Miner (OCE 0325028). Contribution number 2228,
Bodega Marine Laboratory, University of California,
Davis. [SS]
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