American Society of Naturalists

University of Chicago Press

Settlement of Planktonic Larvae: A Theory of Habitat Selection in Varying Environments

Author(s): Roger W. Doyle
Source: The American Naturalist, Vol. 109, No. 966 (Mar. - Apr., 1975), pp. 113-126
Published by: University of Chicago Press for American Society of Naturalists
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 THE
AMERICAN NATURALIST
Vol. 109, No. 966 The American Naturalist March-April 1975

SETTLEMENT OF PLANKTONIC LARVAE: A THEORY OF

HABITAT SELECTION IN VARYING ENVIRONMENTS

ROGER W. DOYLE

Department of Biology, Dalhousie University,Halifax, N.S., Canada

Sessile marine invertebratesalmost always have a free-swimminglarval stage

in their life histories,during which they may migrate hundreds of kilometers
fromtheir place of origin (Scheltema 1971). Planktonic existence is terminated
by attachment and metamorphosis following an episode of "exploratory"
behavior when the surfaces of several potential substrates may be visited.
Differentsubstrates within the dispersal range of the larva present an environ-
mental heterogeneity which is more generally known as habitat diversity.
Marine larvae faced with this heterogeneity usually clearly display classic
habitat selection. Marine larvae can be remarkably restrictivein their choice
of substrates.
I will here attempt to explain a number of features of the behavior of larvae
during the period when they are physiologicallycapable of settlingon a suitable
substrate. Some of these characteristic features of larval behavior have been
well studied experimentally, such as the decrease in substrate specificity-
choosiness-with time. Other aspects have not been studied previously but new
evidence is provided here, particularlywith regard to interpopulationvariation.
Genetic aspects have not yet been studied experimentally,but some predictions
can be made concerningpatterns of dominance and additive genetic variation.
The paper includes a theoretical model of the way in which natural selection
acts on habitat preference.The model is intended to be fairlygeneral but also
realistic enough to aid in the interpretationof laboratory and field studies of
an exemplar marine animal, Spirorbis borealis. Some preliminaryobservations
on the settling behavior of Spirorbis will be presented here to illustrate the
model. In later papers the ecological genetics of habitat selection in Spirorbis
will be examined in more detail.
The development of the larvae of sessile marine animals can be divided into
two stages with quite differentmorphological, physiological, and behavioral
characteristics(Scheltema 1967). The developmentalstage, which may be absent
in nonfeeding larvae, or which may extend for months in some planktivorous

Amer.Natur. 1975. Vol. 109, pp. 113-126.

? 1975 by The Universityof Chicago.All rightsreserved.

113

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114 THE AMERICAN NATURALIST

species, is a period of growth and differentiation.The delay stage is a period

during which the larva is capable of settlingand metamorphosingon a suitable
substrate. As its name suggests,the duration of the delay stage is variable and,
under otherwise constant physiological and environmental conditions, depends
on the availability of suitable substrates.
Scheltema's definition of the onset of delay phase involves both develop-
mental criteria (cessation of growth and differentiation)and behavioral criteria
(ability to settle on a suitable substrate). For the purposes of the present paper
the delay phase begins when a larva is able to metamorphose on at least one
of a set of potential substrates, if the substrate is encountered. It follows from
this purelybehavioral definitionthat the start ofdelay phase is partlydependent
on the range of substrates considered to be available, which may be very wide
in natural situations or very narrowin a controlledexperiment.A corresponding
operational definition suitable for use in an experiment can be expressed as
follows. Out of a number of larvae exposed to an array of substrates, the
number in delay phase during a particular period is N, the number which
settled during that period: N = NA + NB... + N,, where Ni is the number
settled on thejth substrate. Let Pi be the probabilitythat a larva will encounter
the jth substrate, and let y be the probability of settlementon the jth substrate
if it is encountered. We will call the coefficienty the attractivenessof the jth
substrate. It follows that Nj = yPjN, and
_N1
-P~Nj (1)
PiN
In other words, the attractiveness of a substrate in a completely defined set of
substrates is simply the proportionof larvae which settle on it, weighted by the
probability of the larva's encountering the substrate. The weighting factor P1
falls between the two limiting values of unity (fine-grainedmixture) and the
relative abundance ofthejth substrate (coarse-grainedmixture). In experiments
we can put the substrates close together and allow enough time so that each
larva encounters a substrate many times. If the time interval is sufficiently
long
the probability that all the potential substrates have been encountered at least
once is close to unity, and the relative attractiveness is equal to the relative
numbers of settled larvae in the experiment.

SETTLEMENT AS A MARKOV CHAIN

Consider the case of an animal which, as a larva, lives in a homogeneous

mixture of substrates A and B (a fine-grained mixture in Levins's 1968
terminology).A larva swims until it encounters eitherof two types of substrates
with probability a, b. The unit of time in this model is the interval between
encounterswith substrates,so a + b = 1. The larva then eithermetamorphoses
on the substrate with probability a, ,6 or abandons it and resumes swimming.
If the substrate is abandoned the larva has a certain probability, 1 - s, of
dying before encounteringa substrate again. If metamorphosis occurs then the
larva either dies or survives to reproduction with a probability A, B which

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 THEORY OF PLANKTONIC LARVAL SETTLEMENT 115

3, lanktonic survival

encountering B

r >
~~reproductionRI

e
Ttling on A settling on ,/

8 entering plankton
S
FIG. 1.-Flowchart depictingthe settlementbehavior of a larva in the presence
of two potential substrates, A and B. The vertices of the graph represent be-
havioral and physiological states numbered to correspondto the columns in the
Markov chain Q, eq. (2). The directed connecting lines representthe transition
probabilities. A larva is assumed to remain in this chain until it enters either of
the two absorbing states, reproduction(vertex 1) or death (vertex 2).

representsthe characteristic suitabilityof the substratein that environment.

(Note that the lettersA, B are used bothto label the substratesand to denote
theirsuitability.The contextwill make clear whichusage is intended.)With
each individualin each generationthe processis repeateduntilthe individual
is eitherreproducingor dead. For simplicitythe relativesuitabilityof each
substrateis presumedto lie solelyin its effecton the survivalof the animal
aftermetamorphosis, althougheffectson otheraspects of the lifetable (e.g.,
fecundity)could easily be accommodated.This descriptionof the lifehistory
of a sessile marineanimal is presentedas a directedgraph in figure1. The
variousstates (death,reproduction, etc.) are representedby the verticesof the
graph,whiletheprobabilities ofgoingfromone stateto anotherare represented
by symbolsbesidethe connectinglines.
The phenotypic(behavioral) variables are the substrate attractiveness
coefficientsccand fi,whichrepresentthe probabilitiesthat metamorphosis will
take place when a larva encountersa substrateof a given type. Note that a

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116 THE AMERICAN NATURALIST

ofthelarva,notthesubstrateitself.By definition,
and ,6are properties themost
fit phenotypesin any environmentare those in which the values of c, ,6
maximizethe probabilityof survivalto reproductivematurity.The directed
graphcan be arrangedin the formof a matrix,Q, of transitionprobabilities
betweenthe variousstates:

1 0 0 0 0 0 0 0
0 1 0 0 0 0 0 0
o 0 0 a b 0 0 0
_ o 0 0 0 oc 0 1-ce

A 1-A 0 0 0 0 0 0
B 1-B 0 0 0 0 0 0
o 1-s s 0 0 0 0 0

The matrixQ is a Markovchainin whichthe firsttwo columns,reproduction

and death, respectively,representtransitionsto absorbingstates. Once in
eitherofthesestatesthe animalcannotleave again in the same generation.As
time passes aftera larva entersthe planktonthe probabilitythat it will be
foundin one oftheabsorbingstatesapproachesunity.The limitingprobabilities
of each absorbingstate may be obtainedby determining the limitapproached
by Qkas the arbitraryexponentk approachesinfinity. Sincetheelementsofthe
last six columnstend to 0 as k -+ ?o, and sincethe sum of the elementsin
each rowequals 1 at all values of k, onlythe firstcolumnof Qu is shownhere:

1
0
r(I -sin)
ocA+ sr(I - oc)(( - smn)
fiB + sr(I - fl)(1 -sm)-
A
B
sr(I - smn)

These expressionshave been simplifiedsomewhatby introducingtwo new

variablesin,r, wheremn= [a(1 - c) + b(I - fi)]and r = [ccaA+ flbB].
The elementsof this vectorrepresentthe finalprobabilitythat an animal
startingin each ofthe eightpossiblestateswillsurviveto reproduction.
The probabilityof survivalto reproduction definesthe absolutefitnessof an
individualifage at reproductionand fecundityare nottakenintoconsideration.
To definea unique fitnessa transientstate mustbe chosenas a startingpoint.
The thirdelement,survivalin the planktonuntila substrateis encountered,
seems the most appropriateto the definitionof delay phase adopted in this
paper.The fitnessof a larva forwhichthe probabilityof settlingon substrates
A and B is a and fi,respectively,
is givenby:

W,, = [ocaA+ flbB]{1 - s[a(1 - c) + b(I - f3)]}'. (3)

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 THEORY OF PLANKTONIC LARVAL SETTLEMENT 117

In any environmentcontaininga fine-grained mixtureof substrates(or

habitats)A and B, selectionwillact in the directionwhichtendsto maximize
the value of (3). We take the firstpartialderivativeand obtain
aW A(1 -s) -sb/(B-A) (4)
80 [s(ac + bfi)-s + 1]2
The signof (4) dependsonlyon the signof the numeratorand is independent
ofo0.Consequently,in a fine-grained
mixtureofhabitats(3) represents
a straight
line with a maximum at either o = 0 or cc= 1, when oais plotted as the x-
variate and W as the y-variate. In biological systems (if not always in math-
ematical ones) the maximal value of fitnessis also the optimal value.
This is a rather surprisingresult: The model predicts that fitnessis highest
for a larva which either settles immediately on a substrate or never settles on
it at all. There are no fine-grainedmixtures in which an intermediate settling
probabilityis advantageous forany substrate. Yet it is oftenobserved that even
when a highly suitable substrate is available, larvae undergo an exploratory
phase before settling. And some larvae, such as the tube worm Spirorbis, will
eventually settle on such unsuitable substrates as the surface film (Knight-
Jones 1953). This kind of behavior will be explained later when we consider the
problem faced by larvae in a coarse-grainedenvironment.

COARSE-GRAINED HETEROGENEITY IN THE ENVIRONMENT

Mixtures of habitats can be classifiedaccording to the value of the numerator

of (4). Rearranging this expression and setting it equal to 0, we obtain the
critical line
aA a8/3(B -A) (5)
bB B(1-8)
For any given phenotype /3,the optimum value of a will be 1 for mixtures of
substrates to the left of the line (fig. 2) and 0 for mixtures lying to the right
of the line. Mixtures of substrates (or habitats) will have the same optimum
phenotype if they are located on the same side of the critical line even if the
properties of the mixtures in respect to abundances and suitabilities of their
components differ.In a coarse-grained,heterogeneous environment, however,
the spatial distributionof optimal phenotypes should be discontinuous along an
environmentalgradient or dine in the region where the critical line is crossed.
Now, consider the case of a larva which is released into an environment
consisting of two mixtures of habitats falling on opposite sides of the critical
line. (It is importantto avoid confusionhere. Within a mixturethe distribution
of substrates is always fine grained. But the distribution of mixtures in the
environment may be coarse grained if mixtures fall on opposite sides of the
critical line. Unfortunately,this increases the number of arbitraryparameters
required to describe the situation. It is a consequence of tryingto deal with a
real organism.) Let 1 be the probability of encounteringmixture L (to the left
of the line); let (1 - 1) be the probability of encountering mixture M to the
right of the line. Environmental heterogeneitywill clearly reduce the fitnesses

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118 THE AMERICAN NATURALIST

aA
bB

(I-S)
FIG. 2.-A graph on whichall possiblehomogeneousmixturesof substratesA and
B can be plotted. On the ordinate,a, b representthe probabilitiesof encountering
the substrates and A, B representthe probabilitiesof survival to reproductionon
the substrates (see fig. 1). On the abscissa, (1 - s) is a measure of the death rate
in the plankton. To the left of the "critical line" the optimal settlingprobability
on A is 0, while to the rightof the line it is 1. An environmentmay contain several
homogeneous mixturesof substrates which can be plotted on this graph. If they
all fall on one side of the criticalline the environmentas a whole is "finegrained."
If they fall on opposite sides the environmentis "coarse grained."

of both possible phenotypes, because animals will occasionally find themselves

on the wrong side of the critical line. Let x represent the reduction of fitness
of phenotype oa = 1 in mixture L, and let y represent the reduction in fitness
of phenotype c = 0 in mixture M. Suppose the phenotype is fixed at c = 1,
then the reduction in fitnessin the heterogeneous environmentis the reduction
in fitnessin mixture L multiplied by the probability that the larva is in this
mixture, or
lx =l(WL, = O - WL, =o). (6)
Similarly,if a = 0, the total reduction in fitnessis
(1 - l)y = (1 - 1)(WMa=1 WMa=?) (7)

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 THEORY OF PLANKTONIC LARVAL SETTLEMENT 119

The terms lx and (1 -1)y can be called "L-error," representingthe cost of

having phenotype a = 1 in mixture L, anid "M-error," respectively.
Which phenotype (either 0 or 1) is the most fitin the heterogeneous environ-
ment as a whole will depend on the relative magnitudes of lx and (1 - 1)y.

INCREASE OF SUBSTRATE ATTRACTIVENESS WITH TIME IN

A HETEROGENEOUS ENVIRONMENT

In many species of marine larvae the substrate-attractivenessphenotype is

not constant throughout the delay phase. It is well known that as the delay
phase progresses without metamorphosis taking place, larvae usually become
less demanding in their choice of substrate. Spirorbis borealis,forexample, may
eventually metamorphose on the surface filmor without attaching to anything
at all. Although this phenomenon could presumably be studied as a non-
stationary Markov chain, notoriously difficultmathematically, a cost/benefit
approach is adopted in this paper.
It can easily be demonstrated that a phenotype in which the value of a
alternates randomlybetween the two values of 0 and 1 is never more fit than
one or the other of the two fixed values and is almost always less fit. Suppose,
however, that the phenotype of the individual larvae changes nonrandomly
during the delay phase in such a way as to produce a correlation between the
actual and the optimal values of a in the local mixture of habitats. This implies
that while in the delay phase the larva is able to obtain informationabout its
surroundings and adjust its phenotype accordingly. There are a number of
mechanisms by which a larva might obtain information about the local
optimum phenotype. One might be to measure either the frequency of en-
counters with substrates or the time which has elapsed since the last encounter.
If this interval is long the probability of death between encounters is high,
making the value of 1 - s relatively large and increasing the probability that
the true location of the larva is somewhere to the right of the critical line in
figure2. The phenotype of the larva is initially 0 while it is obtaining informa-
tion; later on it can be either0 or 1 depending on the nature of the information
gathered. Let t represent the duration of an initial information-gatheringor
"exploratory" period during the delay phase of larval development.
As in the case of the fixed phenotypes, we will analyze the consequences of
this type of behavior in terms of L-error and il3-error.
The reduction of fitnesswhen the true larval position is mixture L is i(t) . xl,
where i(t) is a decreasing function of the duration of the exploratory phase.
Similarly, the reduction in fitnessin mixture M, mostly due to the increased
probability of death in the plankton, is r(t) . y(l - 1), where r(t) is an increasing
function of t. The minimum reduction in fitnessof a fixed phenotype is either
xl or y(l - 1) in the heterogenous environmentconsidered is a whole.
For an initial "information-gathering" period to be advantageous, the
followinginequality must hold:

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120 THE AMERICAN NATURALIST

FIXED PHENOTYPE(Ca=o)

a FIXED PHENOTYPE (Ci =I_

In

t ~ ~ ~ ~ ~~O

LOG t
FIG. 3.-An example showingthe improvementwhich resultswhen a larva has
a variable phenotype a, delaying settlement in a coarse grained environment.
Abscissa: logarithm of the duration of the "exploratory phase," i.e., time spent
in the plankton while the larva improves the correlationbetween its phenotype
and the optimal value in its presentlocation with respectto the criticalline in fig.2.
Ordinate: reduction in fitnesscompared to that of a hypothetical animal which
always has the appropriate value (either a = 0 or a = 1, depending on its
location). The variable phenotype has a settlementprobability of 0 while in the
exploratoryphase, changingto 1 later on. The optimal duration of the exploratory
phase is marked by the inflectionpoint in the variable phenotype curve.

A necessaryconditionforthisinequalityto be trueforsome positivevalue

inequalityalso be true:
of t is that the following

lim
a[i(t)Xl] >
.
lim ali(t) Y
. - (9)
(9)
at t-0 at
Expressedin words,thisstatesthatiftherateofimprovement in fitnessduring
the exploratory phase is greaterthanthe loss offitnessdue to M-error(mainly
death in the plankton)thena temporaryexploratory phase is advantageous.
In figure3 the advantageofan initialexploratory phase is illustratedwitha
numericalexample.We must rememberthat everyreal phenotypeis less fit
than a hypotheticalphenotypein whichthe correlation betweenthe value of o

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 THEORY OF PLANKTONIC LARVAL SETTLEMENT 121

and the optimal value is perfect-an animal which has complete information
about which side of the critical line it is on. The coarse-grained heterogeneity
of the environmentdoes not affectthe fitnessof such an animal because it has
phenotype oc = 0 in mixture L and phenotype o = 1 in mixture M. Real
animals will be less fit than this, the reduction in fitness of each phenotype
(compared with the optimal phenotype with perfect correlation) being plotted
in figure3 against the logarithm of the duration of the exploratory phase. The
lower the fitness,the fartherup the ordinate a phenotype will plot in figure3.
Consider an environmentin which (1 -- 1)y > xl, that is, an environmentin
which M-error exceeds L-error. The fitnessof the fixed phenotype a = 0 is less
than that of fixed phenotype oc = 1. However, the fitnessof a variable pheno-
type which starts off with a = 0 and after a period of time, t, changes to
oc = 1 may be greaterthan either fixed phenotype, depending on the numerical
value of the sum of the two functions i(t) xl and r(t) y(l - 1). In figure3 i(t)
is defined as (20t + 1) 1 and r(t) as t(t + 1) -1, with a logarithmic abscissa
being used to compress the scale. The variable phenotype is closer to the
theoretical optimum than either of the two fixed phenotypes. The environment
is composed of mixtures of substrates lying on opposite sides of the critical
line, and during the exploratory phase the animal improves the correlation
between its phenotype and the optimal phenotype for the mixture in which it
happens to find itself. This results fromthe rate of improvement in fitness,in
the early stages of planktonic substrate searching,being greater than the death
rate in the plankton. A phenotype which becomes less demanding about its
substrate requirementswith the passage of time has the greatest fitnessin this
example. This kind of behavior is very widely observed in marine plankton.

GENETICS OF SUBSTRATE ATTRACTION

In a fine-grainedmixture of habitats or in an environment consisting of

several such mixtures on the same side of the critical line, the optimal fixed
phenotype has been shown to be either o = 0 or oc = 1. On the phenotypic
level this parallels the demonstration by Kimura (1954) that in randomly
varying environments there is near fixation of the allele having the highest
average fitness.
Preliminary work with genetically related Spirorbis larvae does not lead us
to suspect the segregation of major genes for substrate attractiveness. The act
of settling on a particular substrate probably represents a threshold value of
an underlyingpolygenic trait. The phenotypic value of this trait would depend
not only on the genetic constitution of the larva but on its developmental and
physiological history and the time it has been in the delay phase. Natural
selection for o and f8in particular environments determines the incidence of
phenotypes on each side of the threshold value.
Since substrate attractiveness has an optimal value of exactly 1 or exactly 0,
this trait is a major component of fitness, sensu Robertson (1955). Major
components of fitnessare traits, such as fecundity,which have an optimal value
considerably above the observed mean of the population. It is generally

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 122 THE AMERICAN NATURALIST

believed that such traits are maintained at suboptimal values in natural

populations because of negative correlations between major components of
fitness,such as that between the fecundity of a female bird and her ability to
provide food for each offspring.Traits such as this typically show relatively
little additive genetic variance within populations but may show considerable
genotypic variance. Because of directional dominance, major components of
fitness frequently exhibit heterosis and inbreeding depression under appro-
priate breeding schemes. The relative amounts of additive genetic variance
(heritability)and dominance deviation can readily be assessed in Spirorbis,the
latter being particularly easy because wild-caught animals can be made to
self-fertilize.

Spirorbis Borealis oN AscophyllumAND Fucus

Experimental and field observations on the serpulid tube worm Spirorbis
borealis (Daudin) are offeredas an aid to understanding the Markov chain
model. A much more complete study of the ecological genetics of habitat
selection in this animal will be published later.
Spirorbis borealisis a polychaete worm common in the intertidal and shallow
subtidal waters of Nova Scotia. As an adult the animal lives in a calcareous
shell permanently attached to Ascophyllum and several species of Fucus.
Larvae are released fully developed from the parental tube and spend from
4 to 24 h as free-swimming trochophoresbefore settling. Spawning and release
of larvae take place at approximately 2-week intervals throughoutthe summer,
with 10-80 larvae being liberated at each spawning.
To properly illustrate the application of the model to a natural situation we
need to compare mixtures of algal substrates falling on opposite sides of the
criticalline in figure2. This requires us to identifysubstrates which are, relative
to other substrates, less abundant and/or less suitable in some places than in
others. Ascophyllumnodosum lives higher in the intertidal zone and in more
sheltered locations than any of the Fucus species colonized by Spirorbis. In
certain partially isolated tide pools Ascophyllumis essentially the only brown
alga present, and larval Spirorbis settle on it in profusion. Here, Ascophyllum
is an abundant and apparently suitable substrate. Because of the low abundance
of other possible substrates the ratio aA/bB is high (letting A represent
Ascophyllum),and such tide pools are located to the right of the critical line.
Conditions may be entirelydifferentonly a few meters away in more exposed
locations where Ascophyllum plants can also be found, this time in close
association with Fucus species. The Fucus is usually heavily encrusted with
Spirorbis, while Ascophyllum,immediately adjacent and at the same tide level,
bears few or none. Spirorbis appears not to be able to cement itself to the
surface of Ascophyllumfronds nearly as strongly as to any of the species of
Fucus. The exposed locations are turbulent enough so that an appreciable
number of Spirorbis fall offthe substrate after settlement. Because of its poor
adhesion the probability of survival of a larva that metamorphoses on
Ascophyllum in a turbulent location is lower than if it metamorphosed on
Fucus, and probably also lower than it would be on Ascophyllumin a tide pool.

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 THEORY OF PLANKTONIC LARVAL SETTLEMENT 123

A.SC. (C)
.20 eASC. (W)
\ASC.(V)

Io F5 .' 2UCUS (C)

DIAMETER
IN MILLIMETER

LU
Cif~~~~~~~~~
~ ~
0 1o52 . .4 . .

.05 .S

.2 .4 .6 .8 1.0 1.2 1.4

DIAMETER
IN MILLIMETERS
FIG. 4.-Distribution of size classes of Spirorbis borealisattached to Fucus and
Ascophyllumin locations C (exposed coast), W (open tide pool) and V (protected
tide pool). The Ascophyllumcurves are displaced to the left,reflectingthe reduced
postmetamorphosissurvival on this substrate compared with that on Fucus.

One can easily feel the differencein adhesion by scraping adult Spirorbis off
the substrates with a fingernail.If this phenomenon is important in nature it
should be possible to detect increased mortalityof settled Spirorbis by analyzing
the shape of survivorship curves. Although owing to the variation in the size
of successive spatfalls true survivorship curves are somewhat difficult to
obtain, the relative unsuitability of Ascophyllum in exposed locations does
influence the distribution of sizes of metamorphosed individuals (fig. 4). The
firstspatfall each year, in early June, is somewhat heavier than subsequent
ones. The distributionof sizes of Spirorbis collected on Fucus fromall locations
is strongly skewed to the left because of the continued survival of these first

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124 THE AMERICAN NATURALIST

TABLE 1
ASSOCIATION IN THE "Spirorbis TOLERANCE ZONE"
Spirorbis-Ascophyllum

Colonized
Spirorbis Observations Ascophyllum Ascophyllum
Populations (N) Occurrences Occurrences

V ............................ 31 31 (100) 31 (100)

W............................ 44 25 (57) 20 (45)
X ............................ 93 55 (59) 40 (43)
C .... ................. 142 64 (45) 18 (13)
Z ........................... 17 9 (53) 1 (6)

NOTE.-Percentages shown in parentheses.

arrivals. In the most sheltered locations the Ascophyllumcurves resembled the

Fucus curves. In more exposed and turbulent locations, however, the peaks of
the Ascophyllumcurves are displaced toward the younger age classes and the
curves are more symmetrical or even skewed to the right, just as one would
predict on the basis of increased postmetamorphosismortality.If A represents
Ascophyllumand B representsFucus, it follows that exposed locations have a
relatively low aA/bB ratio because substrate A is both less abundant and less
suitable than in the tide pools.
Field observations made on five locations near Halifax stronglysupport the
idea that settlement of Spirorbis is related to the abundance and suitability of
Ascophyllumas a substrate. The two genera of alga, Fucus and Ascophyllum,
are occupied to some extent in all the locations except V (table 1), which is an
almost isolated tide pool. Three Fucus species, evenescens, edentatus and
vesiculosis, are lumped together as Fucus in the table. The five locations can
be brieflydescribed as follows: V is a protected tide pool, W is a more open
tide pool with greater tidal exchange, X is a small fjord, C and Z are shallow
indentations on an exposed coast.
The data in the table were obtained by surveying the abundances of
Ascophyllum,Fucus, and Spirorbis and the nature of their association with each
other, at each of the five sites. The surveys were conducted just after low tide
by laying down a 1.5-m tape parallel to, and just touching, the land-water
interfaceand recording the occurrence of Spirorbis and either or both types of
algae in the immediate vicinity of the tape. This process was repeated at
approximately 3-m intervals around the perimeterof the site. The presence of
a substrate was recorded as an "occurrence" whatever the actual size of the
plant. Since no occurrence was recorded if Spirorbis was not present, the data
in table 1 refersolely to the Spirorbis tolerance zone defined by the presence
of Spirorbis itself.
The occurrence of Ascophyllumdecreased from 100% in the most protected
tide pool to about 50%0 in the most exposed sites. The decline in utilization of
Ascophyllumas a substrate was more dramatic: from 100% to less than 10%.
As has been mentioned previously, population V is located above the critical
line in figure2, while populations C and Z are presumed to be below the line.

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 THEORY OF PLANKTONIC LARVAL SETTLEMENT 125

The sudden drop in the occurrence of Ascophyllum colonized by Spirorbis

between populations X and C may representthe change in optimal phenotype
fromcc = 1 to oc = 0. This drop cannot be ascribed merely to the direct effect
of postmetamorphosis mortality, since newly settled animals do not fall off
Ascophylluminstantaneously even in population Z. The smaller size classes, at
least, would have been observed if significantsettling had taken place at each
spawning.
Finally, in an experiment aimed at testingdirectlythe relative attractiveness
of substrates to these populations, larvae from C and V were reared in the
laboratory in plastic petri plates containing carefullymatched 4-cm lengths of
Ascophyllum.Settlementon the Ascophyllur,and on the petridish was recorded.
Plastic bearing a bacterial film is an attractive substrate for Spirorbis. The
assumption that larvae were exposed to both substrates is probably valid in
this experiment. The differencein behavior was quite obvious, with the ratio
of settlement on Ascophyllumto that on the plastic being twice as high in
larvae fromthe tide pool as in larvae fromthe exposed location (24% vs. 12%,
2= 34.8 with 1 df). Interpopulation differencesin substrate preference are
probably widespread in S. borealis. A very similar situation has been described
by Knight-Jones et al. (1971) in the eastern Atlantic, where S. borealis is
commonly found on F. vesiculosis and F. serratus.In an abandoned, flooded
quarry in Pembrokshire, F. serratus is very scarce and S. borealis is found
almost entirely on vesiculosis. In other locations along the Welsh coast the
opposite situation prevails, with F. serratuscarryingmost of the Spirorbis. In a
series of replicated experiments larvae from the two locations showed very
strong preferentialsettlement on the substrate from which their parents had
been collected. The possibility of a nongenetic "conditioning" of the larvae
during embryogenesis was discounted by these authors, because in locations
where both substrates were abundantly colonized no particular loyalty to the
parental substrate was observed.

SUMMARY

A theory of habitat selection is developed which, although fairlygeneral in

form, is intended to apply with some realism to the settlement behavior of
planktonic larvae of marine organisms. It is assumed that differentsubstrates
represent differenthabitats and that the environmentcan be heterogenous on
two scales of distance: (1) a "fine grained" heterogeneityin which larvae are
exposed to a homogeneous mixture of substrate types during the settlement
period, and (2) a "course grained" heterogeneityin whichthe compositionofthe
mixture varies from place to place. The objective is to predict whether settle-
ment will occur on both substrates in the fine grained mixtures or only on one
-in other words, whether larvae will exhibit habitat preference.
Settlement behavior is treated as an absorbing Markov chain in which the
transition probabilities are the probability on encountering a substrate, the
probability of metamorphosing on it, the probability of adult survival and
the probability of death in the plankton.

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126 THE AMERICAN NATURALIST

Observations on the serpulid tube-worm Spirorbis borealis are introduced to

illustrate the model. The relative attractiveness of species of fucoid algae as
substrates for Spirorbis larvae is shown to differ between populations of
Spirorbis. Both the field occurrence of Spirorbis on these substrates and its
relative settlement on them in experimental tests are correlated with the
availability and suitability of the substrates.

ACKNOWLEDGMENT

This research was supported by an operating grant from the National

Research Council of Canada.

LITERATURE CITED

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random fluctuationsof selection intensities. Genetics 29:280-295.
Knight-Jones, E. W. 1953. Decreased discrimination during settling after prolonged
planktonic life in larvae of Spirorbis borealis (Serpulidae). J. Marine Biol. Ass.
U.K. 32:337-345.
Knight-Jones,E. W., J. H. Bailey, and M. J. Isaac. 1971. Choice of algae by larvae of
Spirorbis spirorbis. Pages 89-104 in D. J. Crisp, ed. Fourth European marine
biology symposium.Cambridge UniversityPress, Cambridge.
Levins, R. 1968. Evolution in changing environments. Princeton University Press,
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Robertson, A. 1955. Selection in animals: synthesis.Cold Spring Harbor Sympos. Quant.
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