Download Behavioural variability in marine larvae

Australian .founial of Ecoloi^y (1990) 15, 427-437
Behavioural variability in marine larvae
PETER T, RAIMONDI
MICHAEL J, KEOUGH
Department of Zoolot^y. i'nivcrsitr of Melbourne. Parkvil/e. ]'le. 3052. Australia
Abstract
Despite inereasing reeognition of the iniportanee of larval .settlement, reeeni models have
coneentrated on small and large seale hydrodynamie efleels as determinants ol larval settlement. Implieit in most of these diseiissions is the
assumption thai variability in larval behaviour
either does not exist, or is unimportant.
H 'epresent evidenee ihat this is an inaeeuraie
deseription oj larval behaviour at the time of
settlement. There e.xists eonsiderable variation
in behaviour at a nundwr ol seales. even under
controlled laboratory eonditions. For almost all
species examined, responses to attraeiive and
discrete stimuli were non-uniform. The eaiises
of variability in larval behaviour both within
and between populations are largely une.xptored. We suggest that variable behaviour, in
response to discrete stimuli, may be a seleetable
trait. If .so. the manifestation of sueh variability
in individuals within a population is simply the
expression of an adaptive traii. By this reasoning, differenees in larval behaviour between
populations are evidenee for varying seleetive
pressures. We eonelude with an examination of
possible eonsequenees to a population, arising
from variable larval behaviour.
Introduction
In recent years, there has been renewed recognition that variation in recruitment and/or
settlement may be important in determining
species' distributions and abundances (e.g.
Keough 1984a: Underwood & Denley 1984;
Caffey 1985: Raimondi 1988a), This has led to
a resurgence, after the initial pulse of investigations in the 1950s and 1960s (see reviews by
Meadows & Campbell 1972; Crisp 1974;
Scheltcma 1974), ofempirical studies into lactors affecting propagule settlement and metamorphosis (see Morse & Morse 1984; Gaines &
Roughgardcn 1987; Raimondi 1988a; Young
& Gotelli 1988. for examples) and the incorporation of settlement into models of population and community structure (Underwood
& Denley 1984; Connell 1985; Roughgarden
etal. 1985; Menge& Sutherland 1987). In the
earlier studies, the behaviour ot settling larvae
was emphasized, and a large body ofliterature
was produced documenting that behaviour,
usually under laboratory conditions. In contrast. CLirrent work, particularly current models, has concentrated on small and large scale
h\drodynamic effects as determinants of lar\ al
settlement (Shanks 1983; Roughgarden ei al.
1987; Denny 1988), Implieitly assumed in
these models, though nowhere stated in the
empirical literature, is that variability of larval
behaviour either does not exist or is unimportant. Larval behaviour, when acknowledged by
modellers, is considered to be constant. This is
manifestly untrue. As an example, the lar\aeof
many species are considered to be gregarious
settlers (Jackson 1985), If all of the larvae of
such species settle gregariously there would be
no behavioural variability. However, if most of
the larvae settle near rather than far from conspecific individuals, there is variability, Ifthe
latter is true, what of those non-gregarious
individuals in a gregarious species? Are they
simply noise that is filtered out by selection, or
do they survive and reproduce successfully?
E\en when lar\al settlement behaviour has
been doeumented under field or laboratory
conditions, any variation that might have been
present in the original study vanishes when the
work is later summarized. For example, larvae
that showed some preference for lighted areas
are summarized as being positively phototactic
(see Ryland I960. 1976; Buss 1979 for examples), implying constant beha\ iour.
We suspect that uniform responses to stimuli are rare within and between populations of
larvae. In the first section of this paper we pre-
42H
P I. Raiinoiidi and .\/. ./.
sent evidence for variability in larval behaviours. To demonstrate this, we have concentrated on the responses of larvae to discrete
stimuli and, as a result, most of the data are
from laboratory experiments. It may seem a
trivial task to look for variability in the responses of larvae to stimuli, because even the
most casual observer realizes that the answer is
that there is some. However, it is not obvious
why there should be such variability, particularly in the settlement response of larvae to
discrete stimuli. Settlement is an extremely critical stage for many marine species, especially
for those that are sessile as adults, because relocation following settlement is impossible. It
follows that larvae should have developed
means to discriminate between good and bad
settlement sites and it appears that many
species respond to very specific biochemical
and physical 'cues', using them as guides to
settlement (see reviews by Meadows & Campbell 1972; Dewolf 1973; Scheltema 1974).
There is mounting evidenee that at least some
of these cues are specific chemicals that induce
larval metamorphosis by acting as a 'key' in an
enzymatie pathway (Morse & Morse 1984).
The usual adaptive explanation for these responses is that response to cues increases
average fitness (Raimondi 1988a). Variability
in larval behaviour therefore seems paradoxical.
The settlement response of a larva to a discrete stimulus can be divided into two elasses.
First, its behaviour may be unaffected by the
stimulus. In this case, variability in settlement
is not interesting, beeause it isexpected undera
random settlement model. Second, a larva may
settle preferentially in response to a stimulus.
Here, non-uniform behaviour is interesting,
and can result from two causes: (i) responses to
variable, uncontrolled external stimuli, or (ii)
intrinsic variability in larval behaviour. Unfortunately, there is no way to decouple completely these two sources of variation within
populations. Even under laboratory conditions, external stimuli (e.g. vibration, different
temperatures of settlement arenas) may be
confounding factors in examinations of intrinsic variation of larval behaviours. In this paper
we advocate, without accepting, the 'intrinsic
variability' interpretation.
Evidence for variability in larval behaviour
in response to discrete stimuli
H 'ithin populations
While there have been many investigations
into the behaviour of settling larvae (see
Meadows & Campbell 1972; Scheltema 1974
for reviews), there have been few detailed
investigations of intra-population variability
in larval settlement behaviour (see Doyle 1974,
for an exception). However, there are data
from studies that addressed other questions.
We were specifically interested in whether any
stimuli elicited a response in all the members
of a population in examples from a variety of
species.
The data from the experiments described
below are presented in Fig. 1.
Aseidians Young and Braithwaite (1980)
examined the settlement behaviours for the
larvae of Chelyosoma prodiietum. They looked
at whether individuals preferred to settle in
light or dark and whether they settled on the
top or bottoms of surfaces and found that the
larvae showed no preference for the lighted or
dark (shaded) regions of petri dishes and
settled more tVequently. but never exclusively,
on the top of surfaces. Young (1982) reported
similar results from a number of other subtidal
aseidians,
S\ ane (1987) examined the same settlement
beha\ iourof the larvae oiAseidia mentula. He
found more, but not all, settled in the dark and
on the bottom surfaces than in the light or on
the tops of surfaces (means of 88% and 75%
settled in the dark and lower surfaces respectively).
Barnaeles Crisp and Meadows (1962) investigated the effeet of barnacle extract on the
settlement of conspecific individuals of the
species Balanus batanoides. Settlers had a
strong preference for natural and manmade
(Tufnol) surfaees that had been treated with
barnacle extract. However, nearly 10% of all
settlement was on untreated control surfaces,
Bryozoans Keough and King (unpubl.
data) examined the settlement response of
Bugida neritina to light and dark (shaded) sur-
liehayiounil vuiudulitv in niannc Uirvac 429
100|-
80 -
—
—
60
20
—
—
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FIG. 1. Variation in larval settlement behaviour. The histogram bars show ihe percentage of larvae responding to a particular
stimulus. Sources and stimuli were as follows: Ascuiui mciilnin. light/dark and top/bottom; S \ a n c (14K7); iiuiynsonni
pinduclitm. light/dark and top/bottom; ^ oung & Braithwaite (1481)); Baiuiius iuiiantiiiic.s. extract from Lonspocihc shell; Crisp &
Meadows (1962); Piicsiitia sihioxtic. extracts troni coralline algae; ^ool cl at. (1986); HatioUs ^//l•^<<•»^. GABA; Morse cl ai.
(1980); StrongyioccnliotiLs purptiralus. hare rock, coralline- and turr-covered rock; Rowley (1989); .Spinui'i^ i-imcaiis. conspecific individuals; Knight-Jones (1953); Hiii^itia ncrilina. light/dark; M. J. Keough; Pitrat^nialopttnui cuiitor/iica. cxtracl trom
tubes ot conspecilic worms; "i ool cl ai. 1986.
faces. In contrast to most other studies of lar\ al
settlement behaviour only one larva was used
per trial (there were 100 trials per experiment).
In this way the confounding effects of gregarious or density dependent settlement were
avoided. A series of experiments was performed using the same protocol over the reproductive season of Bugula. Although the larvae
generally settled on the dark surfaees. the response was never uniform.
Eehinoids Rowley (1989) examined the
settlement behaviour of Strongyloeentrotus
purpuratus larvae in response to a \ariety of
substrate types. He placed larvae into experimental eontainers that held one test substratum. After 24 h. he seored whether the larvae
had metamorphosed. The experimental surfaees were bare rocks, or rocks covered with
algal film, eoralline algae or algal turf. The percentage of individuals that underwent metamorphosis was lowest on bare roek and greatest
on algal turf, but in no ease was it 100'><i.
Gastropods In one of the few cases of a uniform response to a settlement cue. all of the
lar\ae of Phestilla sihogae. in two separate
trials, metamorphosed in response to the extract of coralline algae (Yool et al. 1986).
In sterile glass eontainers. competent Ualiotis rufeseens larvae did not metamorphose
(Morse ei al. 1980), but in the presence of the
neurotransmitter GABA, 95-97'yii metamorphosed in repeated trials.
Folvehaeies In repeated trials. 8O'Vli of the
larvae of the sabellarid. Phragmatoponia ealiforniea. metamorphosed in response to an extract of tube cement from conspeeific worms
(Yool ei al. 1986).
Knight-Jones (1953) compared settlement of
larval Spirorbis borealis of \arious ages onto
small pieces of Fueus serratus with or without
previously settled individuals. He was testing
the hypothesis that gregarious settlement
ehanged as a function of swimming time (time
since liberation of the larvae prior to settlement). The swimming time of the larvae
ranged from 0 to 24 h after release. For presentation, we classified larvae < 3 h old as
'Young', and all older larvae as 'Old', beeause
430
/ ' Raimondi
and
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this latter group were homogeneous. Old larvae showed no preference for either of the two
surfaees whereas new ones settled preferentially but not uniformh' on surfaces with resident eonspecific individuals.
Between populations
Comparisons of larval behaviour between populations are not eomplieated by the inseparable effects of intrinsic variability and external
uncontrolled stimuli. This is because, with
proper experimental techniques, uncontrolled
external stimuli will be similar for both populations.
It is usually assumed that there is little variation in larval behaviour, and single studies,
from single sites, are \iewed as representative
for that species' presence (e.g. Ryland 1974, for
Bugula neriiina. but see Doyle 1974 for an
exception). This assumption seems weak,
given documented geographic differences
between populations of adults and the restrieted dispersal of many sessile animals and
plants. The latter phenomenon should limit
genetic exchange between populations and
allow adaptation to local settlement cues.
Despite this possibility we can find few studies
of larval variation between populations.
One species that has been studied in many
locations is Btiguta neritina. The results of several of such studies are presented in Fig. 2,
which shows larval settlement behaviour in the
light or shade. Error bars are absent from cases
where a description of the behaviour, but no
data, was given. There is eonsiderable variability between populations and the preference for
stimuli changes between locations. In four of
the populations. St Leonards. Williamstown.
Japan and Beaufort, at 19° larvae settled preferentially in the dark, while in the others they
generally settled in the light.
The tendency for individual B. neritina to
settle in aggregations, and the duration of the
larval swimtning period, were studied by
Keough and King (unpubl. obs.; Keough
1984b. 1989) in four widely separated populations. Two were in the USA (California and
Florida) and two were in Australia (Vietoria
and South Australia). In these aggregation experiments, the spatial pattern of groups of larvae was documented. Unrelated individuals
settled randomly in all populations, although
the Victorian population showed a tendency to
settle in aggregates (Table 1), Related individuals exhibited different settlement behaviours. Groups of related larvae from California
settled in aggregations, while those in Florida
FIG. 2. Variation in the response ol settling Biii;uia iicrinna lar\ac to light. The histogram bars sbow tbe n u m b e r of larvae
settling in the ligbt. Error bars represent variation between experiments, with eaeh experiment including 100 individual lar\ae.
( — ) random settlement. Data from Florida and Australia were eollected by M. J. Keough. Other sources were; Japan;
Mawatari (1951); Beaufort, Nortb Carolina; Lynch (1947); Menai Bridge, Wales; Ryland (1960). (B) North .America;
(•) Europe; (•) Australia.
fieliavioiiral varuihilitv in marine lanuc
behaved like unrelated individuals and settled
randomly. In the second set of experiments,
time to settlement was recorded by following
individual larvae in petri dishes (Table 1). The
duration of the planktonic period, in the
absence of stimuli, was least for the Florida
population, followed by those from South
Australia, Victoria and California.
The preferred orientation at settlement also
varies between populations of B. neriiina.
Individuals from Williamstown in Victoria
settled preferentially on vertieal surfaces,
while those in Point Turton. South .'\ustralia
showed no orientation preference (Keough.
unpubl. obs,; Table I). In a related study, the
orientation of newly reeruited B. neritina at
Beaufort. North Carolina was compared for
populations separated in time (Table 1).
McDougall (1943) found that individuals preferred to settle on the bottom of substrata (0 or
45°), When Maturo (1957) did similar experiments, his results were similar to McDougall's
in one experiment, but different in a later
experiment.
An extretne form of larval variability,
though one that is not always related to settlement, is poecilogony, here considered only as
multiple larval types within a single species.
This phenomenon has been reported for a
number of species (Thorson 1950; Jablonski &
Lutz 1983). but in a recent review. Hoagland
and Robertson (1988) concluded that nearly all
examples needed further substantiation. At
least two examples, however, are adequately
supported.
Eyster (1979) demonstrated that within a
population of the opisthobranch Tenellia pallida. some individuals produced pelagic larvae
and others produeed non-pelagic larvae. This
polymorphism is an extreme case of variability
in larval behaviour. Pelagic larvae can disperse
and settle in newly available habitats, while
non-pelagic larvae stay in the 'predictable' parental habitat.
Levin (1984) showed that populations of the
polychaete Streblospio benedieti could often be
distinguished solely by their larval type; some
populations had planktotrophic while others
had lecithotrophic larvae. Of the 11 populations she sampled, four had lecithotrophic.
six had planktotrophic and one had both types
of larvae. The results of breeding experiments
indicated that larval type had a genetic com-
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ponent. Females could produce only one larval
type with this pattern being maintained
through four generations in the laboratory.
These diflerences in larval type were not evidence for separate species, because individuals
of one larval type could breed with those of the
other, produeing larvae with intermediate
eharacteristies.
Finally. Raimondi and Morse (unpubl. data)
were able to distinguish between eoastal populations and an isolated founder population of
the barnacle Balanus amphitrite. based solely
on heritable larval morphological characters.
In contrast to the larvae, the observed divergence between adults was not underlain by genetic differences.
Mechanisms producing larval variability
Variation in larval settlement behaviour may
be derived from genetic variation among larvae, ontogenetic changes in behaviour, parental environmental effects, modification of
responses by other environmental cues (i.e.
plasticity or genotype-environment interaction), or the overriding of behavioural responses by physical processes, such as waves.
At present we do not clearly understand the
relative contributions of genetie and environrnental faetors to larval behaviour.
In 1975, Doyle lamented the lack of sophisticated breeding experiments with marine invertebrates and his statement still applies to
larval behaviour. The most efficient way to
distinguish between genetic and environmental effects is through controlled crosses, but
such experiments are rare. The next best
option is a comparison of offspring from a
number of parents, in an uncontrolled full- or
half-sib design (Falconer 1981). For brooding
species, there is a ready supply of at least halfsibs. but for broadcast-spawning species, laboratory erosses are the only way to control the
genetic relatedness of larvae.
Within populations
We can reject ontogenetic changes and physical disruption as causes of much of the variation in larval behaviour that we have discussed. Some larvae do alter their behaviour
with age but most workers have used larvae of
known or constant ages, or deliberately exam-
ined the relationship of variation in behaviour
with age (Knight-Jones 1953; Ryland 1960), so
larval age can be excluded as a cause of at least
this variation. Ontogenetic changes may, however, contribute to variable field settlement.
Similarly, laboratory experiments are done
under benign physical conditions, under which
larvae are capable of swimming actively, so
physical disruption can be ruled out.
In most of the cases we have examined,
behavioural variation occurs within, rather
than between family groups, arguing against
genetically-based polymorphisms.
In Bugula neritina. at least three larval attributes show little variation between sibling
groups. At Santa Catalina Island, the degree of
gregariousness at settlement did not vary between groups of larvae from different parents
(Keough 1984b), nor was there familial variation in larval swimming times (Keough
1989). In a Victorian population, light responses of larvae varied within sibling groups
in a single experiment, with no significant variation between parent colonies or experiments
(Keough, unpubl. data).
Levin (1 984) reported that larval swimming
times in the polyehaete Sireblospio benedieti
varied considerably among progeny of a single
parent or cross. Her data included larvae from
worms that had been reared in the laboratory,
suggesting that there is little genetic variation
in swimming times within populations. In
another polvchaete, Boeeardia proboseidea.
Petch (1989) has reported that individual
worms produced two kinds of larvae within a
single egg capsule.
In Spirorbis
borealis,
Doyle (1974) com-
pared photo-behaviour of larvae between populations, experiments and families (groups of
full- or half-sibs), and found significant variation between populations, but not between
families within populations. Under the
assumption that larvae from a single parent
were half-sibs. he calculated an upper limit to
the heritability of 0,36. with the actual value
probably lower. When he cotnpared developmentally synchronized larvae to unsynchronized larvae within one population, he found no
significant effect on families and suggested
some maternal environmental effects on
photo-behaviour.
The remaining hypotheses are non-genetic
parental effects and plasticity, but we could
Bi'/iuvloiii'dl varuihilily in nuiniw larvae
find few data to test either hypothesis. For larval swimming time, maternal ertects, such as
egg or embryo size, may be important. Variation in larval development rate in urchins
may depend on egg size (Sinervo & McEdward
1988), but it is not clear whether a similar
phenomenon explains the considerable variation in swimming time in Bii^'iilu and Strchlospio. There are no measurements of variation
in larval size in B. iieridna. and, although
Levin (1984) noted that larvae varied in size,
there is no indication whether this variation
was related to swimming time.
It is not clear how other beha\ iour. such as
responses to light, eonspecitic individuals etc.,
might be inOuenced maternally, but absence of
a mechanism is not evidence against this hypothesis. We do note that the least variable experiments are those involving specific chemical
cues (Morse & Morse 1984; \'ool ci al. 1986),
rather than more general cues, such as light.
This evidence is consistent with a plasticity
hypothesis, but would not be predicted from
maternal environmental effeets. We stress the
need for clear tests of these hypotheses.
In contrast to these results, the types of larvae produced are less plastic. The two reproductive phenotypes of laboratory-reared
Tenellia pallida produced larvae of the maternal type (Eyster 1979), even when crossed
with the other type, suggesting that the type of
larvae produced is maternally-controlled.
In another bryozoan Parasmiltina niliila.
two sympatric 'morphotypes' differed in adult
colony morphology when reared in the laboratory from larvae, and the offspring of these
colonies also dift'ered morphologieally (Maturo 1973; Humphries 1975). The morphology
of the larvae also differed, although genetic and
maternal environmental effects could not be
differentiated.
Whatever the mechanisms, variable behaviour exists in the larvae of most species; even
under controlled laboratory conditions, most
parents produce offspring that exhibit a range
of behaviours in responses to clear, simple
stimuli.
Between populations
Most studies are consistent with the hypothesis
of a heritable component to variation between
populations. Ontogenetic explanations can be
433
rejected but few studies can distinguish
between genetic and maternal environmental
effects. Two exceptions arc Slichlospio hcnccllcti and Balanii.s aniphilritc, discussed earlier,
in which laboratory rearing through at least
two generations allowed the elimination of
maternal environmental eflects as causes of
variation.
Experiments in which larvae from different
parent populations were tested under the same
conditions provide strong evidence for either a
genetic or maternal environmental effect. In
the case of Biti^iila neiitiiia. major difterenees
are seen under nearly identical laboratory conditions, for a wide range of larval attributes.
The same conclusions can be drawn from
Doyle's Spirorhi.s experiments, but for neither
species can the effects be separated unambiguousfy.
For three of the four species that we have
discussed here, larval periods are short, so
there is considerable potential for adaptation
of populations to loeal selection regimes. In
future studies, there is a great need for a better
interface between genetics and ecology.
Consequences arising from variability in
the behaviour of larvae
Thus far, we have presented evidence for
\ariabifity in the behaviour of settling larvae
and have discussed some of its possible causes.
Neither would be of much interest toecologists
if larval behaviour had no effect on the distribution or abundance of conspecific individuals or other species (population or eommunity eff'ects). There have been few studies on
the effect of larval behaviour in a speeiesonthe
eeology of other speeies (it is a subject that
needs attention), so we will restriet our discussion to the population consequenees of variability in larval behaviour.
Variability of larval behaviour can be classified according to whether it is adaptive or
not. Non-adaptive variability may indicate
that the behaviour is not under independent
genetic control. The eff"ect of this on population size may depend on the level of settlement. When overall settlement is high, the
numbers of adults are unlikely to be affected by
variation in settlement, as there are many more
potential settlers than there are places for them
in the environment (Connefl 1 985). Thus, non-
434
F. I'. Rainuuuli and M. ./. Kcinigh
adaptive variability in species with typieally
high settlement, probably does not affect adult
abundance. In eontrast, population size is
likely to be affected when overall settlement is
intermediate or low, because variability at
settlement, whatever its cause, will be maintained through subsequent ontogenetic stages.
In most cases, the distribution of a species will
not be affected by non-adaptive variability.
Is variability in larval behaviour adaptive'^
Simple optimization notions suggest that selection should fa\our larvae that respond to cues
that are associated with the most favourable
habitats. These ideas have been criticized
heavily (see, for example. Rose et al. 1987),
and there are a number of reasons why larval
responses might remain variable. First, traits
do not evolve in isolation, and the fixation of a
trait in a population may be retarded by negative genetic correlations with other traits.
Second, variability might be maintained by
fluctuating selection pressures, such that a cue
is sometimes positive and sometimes negative.
This eould result from either spatial or temporal variation in the environment.
A third mechanism might be frequencydependent selection, whieh we illustrate using
the photo-response of sessile benthic animals.
Negative phototaxis may be a means by which
microhabitats free of algae or low in sedimentation are located. As long as such behaviour is
rare, it is adaptive, but as its frequeney increases, so does the likelihood of inter- or
intra-specific competition for space. At some
point, the scfective differential between the
two microhabitats may reverse.
These alternative explanations can only be
distinguished by careful field studies documenting the strength and variability of natural
selection. The first hypothesis predicts that
settlement behaviour is retarded from reaching
an optimum, i.e. that larvae make mistakes,
while the other two mechanisms imply that
larval variation may be adaptive and that
behavioural variation it.self is a heritable trait.
There are few data to distinguish between these
competing explanations, but we provide three
examples that suggest that variation may be
adaptive.
In Florida Bugula neritina typically settle on
sea grass leaves, where about 40% and 60% of
TABLE 2. Consequences of settlement variation in
ncnliiui
Basal end of Distal end of
leaf (elose to
leaf (up in
sediment)
water eolumn)
Settling at that position
(%)
Growth rate
Maximum size
Age at first reproduetion
Mortality in growing
season
Mortality between growing
seasons
40
low
similar
> 3 5 days'
50
high
similar
14 days
high
low
low "M
100%
'Mortality of basal colonies was so high that, within
experiments, no eolony ever reprodueed. and all colonies
died within 35 days.
The table compares life history attrjbutes of 5. ncniina
colonies that settled on distal li basal ends of seagrass leaves.
Data are drawn from Keough (1986) and Keough and
Chernolf (1987).
the settlement is on the basal and distal ends,
respectively (Keough 1986). This pattern is
maintained irrespective of the density of previously settled residents, suggesting that the
variability may be intrinsic. Successive cohorts
settle over the course of a growing season,
which ends when the water temperature gets to
approximately 27°C, or when a cold snap occurs (Keough & Chernoff" 1987). For most life
history parameters, individuals settling at the
distal end appear to be favoured. Individual
growth rate, maximum size, age at first reproduction and survivorship over the course of a
growing season are higher at the distal end than
at the basal end of sea grass leaves (Table 2).
However, only those individuals that are on
the basal ends of leaves survive between seasons. If the duration of the growing season were
predictable an adaptation may have evolved
whereby parents produced larvae that chose
distal ends of leaves until near the end of the
season. Near the end of the season, only larvae
choosing basal ends would be produced.
However, the duration of the growing season is
not predictable and individuals with that adaptation would be selected against. Hence, successful parents are those producing offspring
that vary in their settlement behaviour.
Cluhamalus anisopoma is an intertidal barnacle that lives in the northern Gulf of California (Brusca 1980). Within its intertidal distribution it oecurs in dense patches with dis-
lichavKmicit vtniatulilv in nninnc larvae
TABLE 3. Comparison of lil'i; history chLiraitcrs of
Chlhainalus iiiiisopoiiia individuals that settled inside and
outside the main distribution of the speeies
Inside
distribution
(gregarious
settlers)
Settled in zone-- (')ii)
Growth rate
Maximum size (basal
diameter)
Age at first reproduetion
Mortality-''^
Outside
distribution
(independent
settlers)
>'-)5"/ii
< 5'Ki
highi
7 mm'
4 : - 5 6 daysi f
low
10 mmi
2 5 - 3 5 daysi
high
ip. T. R a i m o n d i . unpubl. obs. -Raimondi (1988a).
•'Raimondi (1988b). •'Raimondi (1990). -^Raimondi (in
review). ''Lively (1986). 'Brusea (1980).
tinct edges. Adjacent to these patches, at the
same tidal heights, are areas without barnacles
that could be successfully colonized (individuals settling there would sur\i\e to reproduce) if larvae settled upon them (Raimondi
unpubl. data). In the field, approximately 95%
of settling larvae attach next to previously
settled conspecific barnacles (Table 3), which
acts to maintain current barnacle patches. The
remaining 5%, here called independent settlers, settle in uncolonized areas and have a
highergrowth rate, a larger maximum size, and
an earlier age of first reproduction compared to
gregarious settlers. The ad\ antages in independent settlement derive from the low density of
conspecific animals; simply, there is no
crowding. The disadvantages however are
severe; many independent settlers die because
they settle in areas that are not survi vable. That
is, they settle in areas that are outside their
survivable distribution, as well as in uncolonized areas within their survivable distribution.
We suggest that the advantages of variable
offspring: individuals capable of both independent settlement and much more commonly,
gregarious settlement, are greater than the
costs incurred through the loss of offspring settling in areas where they cannot survive. An
additional advantage of independent settlement, though one that is hard to imagine selection for, is that without it the species would
soon become extinct. Patches of barnacles are
not permanent. Many types of physical disturbance could wipe out a patch. With only
gregarious settlers, a patch that was destroyed
would never be re-established and new patches
435
would never appear. Thus the population
would decrease monotonically over time as the
number of patches declined.
For our third example we will reconsider the
phototactic behaviour of ascidian and bryozoan larvae. As discussed earlier, in no instance was the settlement response to lighted or
dark surfaces uniform (Table 2). In one
species, Bui;uhi ncrilina. the preference appeared to change over the course of a season.
Bujiula and both species of ascidians have
Iccithotrophic larvae, which in laboratory experiments usually settle soon after release.
Also, most asctdian larvae followed tn the held
settled within 20 minutes after release (Olson
I'^85; Young 1986; Davis 1987). However,
many did not, leaving open the possibility that
they might disperse over long distances. If both
short and long range dispersal occurred there
would effectively be a dispersal polymorphism
(Keough 1988). Variability in phototactic behaviour could promote variability in the distance dispersed by larvae. Those that were
negatively phototactic would be likely to settle
quickly near parents, while those that were
positively phototactic would rise to the surface
where the\ could be transported considerable
distances by surface currents. Here variability
as a trait might be adapti\e because the parental costs associated with either limited (sibling
competition, parent sibling competition) or
long range dispersal (low probability of offspring survival) need not be paid in full.
It is abundantly clear that larval behaviour is
variable and that such variability may aHect
populations. However, the mechanisms underlying variability in larval behaviour remain
largely unexplored. Only when these are uncovered will we be able to determine if variability in the behaviour of larvae is a heritable
and potentially adaptive trait.
Acknowledgements
We are grateful to Alan Butler, Mark Carr, Joe
Connell, Andrew Constable, Sally Holbrook,
Russ Schmidt, Tony Underwood and Craig
Young for helpful discussions, and especially
to Alan Butler, Alice King, Craig Young and an
anonymous reviewer who commented on the
manuscript. Financial support was provided
bv the Australian Research Council, NSF grant
436
P. I Rainidiuli anil M. ./.
OCF 84-00404 to M.J.K., and a University of
Melbourne Research Fellowship to P.T.R.
References
Brusca R. C. (1980) Cmnmiiit liilcrlidal Inrcrlchralc aj ihc
Gulf of Ccilijornici. 2nd edition. University of
Arizona Press. Tueson.
Buss L. W. (1979) Habitat seleetion, directional growth, and
spatial refuges: why colonial animals have more hiding places. In: Bialdfiv ciiiil SysU'nuilic^ i>l Colonial
Organisms (eds G. Larwood & B. R. Rosen), pp.
459-97. Aeademie Press, London.
Caftey H. M. (1985) Spatial and temporal \ariation in
settlement and recruitment ot an intertidal barnacle.
£(•()/. MoiwRr. 55, 313-32.
Connell J. H. (1985) The consequenees of \ariation in initial
settlement vs. post-settlement mortality in roeky
intertidal communities. ,/. Kxp- Mar Bioi licol 93.
I 1-46.
Crisp D. J. (1974) Factors influencing the settlement of
marine invertebrate larvae. In: Chcniorcccplion in
Marine Inverlehrales (eds P. T. Grant and A. M.
Mackie). pp. 177-265. Aeademie Press. London.
Crisp D. J. & Meadows P. S. (1962) The chemical basis of
gregariousness in eirripedes. Froc R. Soc. Loiui
Biot. Sei. 156. 500-20.
Davis A. R. (1987) Variation in reeruitment of the subtidal
eolonial ascidian Poiloiiavella cylindrica (Quoy &
Gaimard): the role of substratum choice and early
survival. ./ /;.v/) Mar Bioi Ecol. 106. 57-71.
Denny M. (1988) Biolot;y and llw Mechanics ot lite Waveswept Environment. Princeton University Press.
Princeton.
DeWolf P. (1973) Eeologieal observations on the mechanisms of dispersal of barnaele larvae during planktonic life and settling. Nethertands J. Sea Res. 6.
1-129.
Doyle R. W. (1974) Choosing between darkness and light:
the ecological geneties of photic behaviour in the
planktonic larva of Spirorbis boreatis. Mar. Biot. 25.
311-7.
Doyle R. W. (1975) Settlement of planktonie larvae: a theory
of habitat selection in varying en\ ironments. .4mer
Nal 109. I 13-26.
Eyster L. S. (1979) Reproduction and de\elopmental variability in the opisthobraneh Tenettia pallida. Mar.
Biol. 51. 133-40.
Falconer D. S. (1981) lnlrodiieliou to Quanniative Genelics.
2nd edition. Longman. Essex.
GainesS. D. & Roughgarden J. (1987) Fish in ofl'shore kelp
forests affect recruitment to intertidal barnacle
populations. Science 235. 479-81.
Hoagland K. E. & Robertson R. (1988) An assessment of
poecilogony in marine invertebrates: laet or fantasy?
Biol. Bull 174. 109-25.
Humphries F. M. (1975) A new approach to resolving the
question of speciation in smittinid bryozoans
(Bryozoa Cheilostomata). Doeumenis des Laboratoires Geologic de la Faeutle des Scienee.s tie Lvon,
HorsSeriei. 19-35.
Jablonski D. R. & Lutz R. (1983) Larval biology of benthie
marine invertebrates: paleobiologieal implications.
Biol Rev. 58. 21-89.
Jaekson J. B. C. (1985) distribution and ecology of clonal
and aclonal benthic invertebrates. In: Popiitalion
Bidliii^vandlivttliilion olClonalOri^anisins (eds J. B.
Q\ Jackson. L. W. Buss & R. E. Cook), pp. 297-356.
Yale University Press, New Haven.
Keough M. J. (1984a) Dynamics of the epifauna of the
bisalve Finna bicotor: interactions among recruitment, predation and competition. A"(vi/(<i,'r65. 67788.
Keough M. .1. (m84b) Kin-recognition and the spatial distribution of lar\ae of the bryozoan Biifiula nerilina
(L.) l.volulion 38. 142-7.
Keough M. J. (1986) The distribution of a bryozoan on
seagrass blades: settlement, growth and mortality.
/;'(V)/()i,'r 67, 846-57.
Keough M. J. (1988) Benthic populations: is recruitment
liniitingorjust fashionable'.'/'roc. 6ltilnl. Coral Reel
Syitip. 141-X.
Keough M. J. (I 989) Dispersal of the bryozoan Bugiita ncriiiiiii and cfiects of adults on newly metamorphosed
iu\eniles. .\fcir. t'eol. Frog. Ser. 57. 163-71.
Keough M. J. & Chernoff J.( 1987) Dispersal and population
variation in the brvozoan Biigida neriilna. Ecolog\'
68, 199-210.
Knight-JonesE. W. (1953) Decreased diserimination during
setting after prolonged planktonic life in larvae of
Spirortv\ borealis (Serpulidae)../ Mar. Biol. .-In. IK
32, 337-45.
Le\in L. .\. (I9S4) Multiple patterns of de\elopment in
Slret^tospio txnediili Webster (Spionidae) from
three eoasts of North .America. Biot. Butt. 166.494508.
Lively C. M. (I 9S6) Competition, comparative life histories
and the maintenance of shell dimorphism in a
barnaele. Eeotogy 67, 858-64.
Lynch W. F. (1947) The behaviour and metamorphosis of
the larvae ofBuguta nerilina (Linmeus)\ experimental modification of the length of the free-swimming
period and the responses of the larvae to light and
gravity. Biot But! 92, 1 15-50.
Maturo F. J. S. (1957) Seasonal distribution and settling
rates of estuarine Bryozoa. Eeologv 40, 116-27.
Maturo F. .1. S. (1973) Offspring variation from known
maternal stoeks of Fara\nuliina nilida (Verrill). In:
l.ivnig and Eowit Bryozoa (ed. G. P. Larwood). pp.
577-84. Academic Press, London.
Maw atari S. (1951) Natural history of a common fouling
bryozoan Bugiita neriima (Linnaeus). Mi\c. Rep.
Rev !n\l \al. Resources Tokyo 20. 47-54.
McDougall K. D. (1943) Sessile marine invertebrates at
Beaufort. North Carolina. Ecot \lonogr. 13, 32174.
Meadows P. S. & Campbell .1. I. (1 972) Habitat selection by
aquatic invertebrates. .Aitv. Mar. Biot. 10. 271382.
Menge B. \. & Sutherland ,1. P. (1987) Community regulation: variation in disturbance, eompetition and
predation in relation to environmental stress and
reeruitment. .Anier. \al. 130. 730-57.
Morse A. N. C. & Morse D. F. (1984) Recruitment and
metamorphosis of Haliolis larvae induced by moleeules uniquely available at the surfaces of crustose
red algae. ./. E.\p. Mar. Biot. Ecol. 75, 191-215.
Morse D. F.. Hooker N. & Duncan H. (1980) GABA induees
metamorphosis in Hatiolis. V. Stereochemical
specificity. Brain Res Bull. 5, 381-7.
Olson R. R. (I 985) The consequences of short-distance lar-
liehavioural variahility in inarinc taivac 437
val dispersal in a sessile marine invertebrate. lUotogy 66, 30-9.
Petch D. A, (1989) I arialion in Itw Spionid Folychaele Boecardia proboscidea. PhD dissertation. University of
Melbourne,
Raimondi P, T, (1988a) Settlement cues and determination
ofthe vertieal limit of an intertidal barnacle, i'.cotogv
69, 400-7,
Raimondi P. T. (1988b) Rock type aflects settlement,
recruitment, and zonation ofthe barnacle Ctiltianiatus iinisoponia Pilsbury. ./. /. vy .Mar Biot. Ecot
123, 253-67.
Raimondi P. T. (1990a) Patterns, meehanisms and
consequences of variability in settlement and recruitment of an intertidal barnacle. Ecot .\l(}nogr.
60, 283-309.
Raimondi P. T. (1990b) The settlement behaviour of
Cluhamalus anisopoma largely determines its adult
distribution (in press).
Rose M. R,. Service P. M, & Hutehmson F. W. (1987) Three
approaehes to trade-ofts in life-history evolution. In:
Genetic Constraints on .Adaptive Evolution (ed. V.
Loeschcke), pp, 91-105. Springer-Vcrlag, Berlin.
Roughgarden J., Gaines S. & Pacala S. (1987) Supply side
ecology: the role of physical transport processes. In:
Organization oj Coiyvnunilies: Fast and Freseni
(eds P. Giller & J. Gee), pp. 491-518. Blaekwell
Seientifie Publieations, London.
Roughgarden J., Iwasa J. & Baxter C. (1985) Demographic
theory for an open marine population with spacelimited reeruitment. Ecology 66, 54-67.
Rowley R. J. (1989) Settlement and recruitment of sea
urehins {Sirotigylocentrolus spp.) in a kelp bed and
urehin barren ground: are populations regulated by
settlement or post-settlement proeesses'' .Mar Biol
100, 485-94.
Ryland J. S. (I960) Experiments on the inlluence of light on
the behaviour of polyzoan larvae. ./. A.V/J Biol 37.
783-800.
Ryland J. S. (19741 Behaviour, settlement and metamorphosis of bryozoan larvae: a review. Ttiatassia .liigostavica 10. 239-62.
Ryland J. S. (1976) Physiology and ecology of marine
bryozoans. .-idv. Mar. Biot. 14, 286-443.
Scheltema R. S. (1974) Biological interactions determining
larval settlement of marine invertebrates. Ihalassia
.lugostaviea 10. 263-96.
Shanks A. L. (1983) Surface slicks associated with tidally
foreed internal waves may transport pelagic larvae
of benthie invertebrates and fishes shoreward. Mar.
Ecot Frog. Scr 1,3. 31 1-5.
Sinervo B. & McEdward L. R. (1988) Developmental
consequences of an evolutionary change in egg size:
an experimental test. Evotution 42, 885-99.
Svane 1.(1987) On larval behaviour and post-metamorphic
mortality ot.4scidia inenluta O F. Muller. Optietia
27, 87-100.
Thorson G. (1950) Reproductive and larval ecology of
marine bottom invertebrates. Biot. Rev. 25, 1-45.
Underwood A. J. & Denley F. J. (1984) Paradigms, explanations, and generalizations in models for the strueture of intertidal communities on rocky shores. In:
Ecotogicat Cotnmunilies: Coiieeptual Issues and the
Evidenec (eds D. R. Strong. D. S. SimberloH. L. G.
Abele & A. B. Thistle) pp. 151-80. Princeton University Press. Princeton.
Vool A. J.. Grau S. M.. Hadfield M. G., Jensen R. A., Markcll D. A. & Morse D. F. (1986) Fxcess Potassium
induces larval metamorphosis in four marine invertebrate species. Biot. Butt 170, 255-66.
Young C. M. (1982) Larvat behavior, predation and earty
posl-scllling morlality as determinants olspatial disIribulion in sublidat sotilary aseidians of the San
./uan Istaihh. Wastiinglon PhD Thesis, University
of Alberta, Fdmonton, Canada.
Young C M. (1986) Direct observations of field swimming
behavior in larvae of the eolonial ascidian Eeleinascidia turtvnala. Butt. Mar. Sci. 39, 279-89.
^'oung C. M. & Braithwaite L. F. (1980) Larval behavior
and post-settling morphology in the ascidian.
Ctietyosomaprodueliim Stimpson. J. E.\p. .Mar Biot
Ecot 42. 157-69.
Young C. M. & Gotelli N. J. (1988) Larval predation in
barnacles: efteets on patch colonization in a shallow
subtidal community. Ecotogy 69. 624-34.
(Final manuscript accepted April 1990)