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First published online August 31, 2007
Journal of Experimental Biology 210, 3228-3235 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.004192
Larval desperation and histamine: how simple responses can lead to complex changes in larval behaviour
1 Centre for Marine Biofouling and Bioinnovation/School of Biological, Earth
and Environmental Sciences, The University of New South Wales, New South
Wales, 2052, Australia
2 School of Integrative Biology/Centre for Marine Studies, University of
Queensland, Queensland, 4072, Australia
* Author for correspondence (e-mail: r.swanson{at}unsw.edu.au)
Accepted 23 June 2007
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Summary |
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Key words: desperate larva hypothesis, settlement behaviour, metamorphosis, histamine, Holopneustes purpurascens
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Mullineaux and Butman, 1991;
Raimondi and Morse, 2000). In
the absence of obligatory settlement cues, larval species from a range of
phyla are able to postpone metamorphosis until such cues are encountered
(Pechenik, 1990). This ability
of some larvae to delay metamorphosis, despite being developmentally ready for
the transition (or `competent'), is believed to increase the chance of
settling into habitats that can support survival to adulthood
(Morgan, 1995;
Pechenik, 1990;
Thorson, 1950). Extending the
planktonic phase, however, comes with an increased risk of larval mortality
and can lead to detrimental carry-over effects for juvenile/adult performance
(Maldonado and Young, 1999;
Marshall et al., 2003;
Pechenik et al., 1998;
Wendt, 1998).
Lecithotrophic (non-feeding) larvae have limited energetic reserves to
support their development during the planktonic phase and through
metamorphosis, and so have a limited time to locate a favourable habitat to
resume the benthic phase. Knight-Jones
(Knight-Jones, 1953) and
Wilson (Wilson, 1953) first
noted that larvae become less discriminating with regard to habitat selection
as they age. Thus, some species are presumed to accept a broader range of
microhabitats as they age because they are approaching their energetic minimum
and are therefore `desperate' to settle and metamorphose anywhere. This view
has subsequently been described as the `desperate larva hypothesis' – or
DLH (Toonen and Pawlik, 1994)
– and, since then, the DLH has been used to explain the decreased
substratum specificity observed in a range of older non-feeding larvae
(Gribben et al., 2006;
Marshall and Keough, 2003;
Miron et al., 2000). More
recently, the DLH has been modified to incorporate the effects of larval
feeding and the consequences of habitat specialisation. Botello and Krug
(Botello and Krug, 2006) have
shown that for the opisthobranch Alderia sp., which feeds exclusively
on the alga Vaucheria longicaulis
(Krug and Manzi, 1999;
Krug and Zimmer, 2000), older
larvae do not metamorphose indiscriminately. Rather, older, starved larvae of
Alderia sp. became more sensitive to settlement cues from the host
alga, but older, fed larvae did not
(Botello and Krug, 2006). They
suggest that the DLH should not apply to host-dependant species because
metamorphosis in the absence of such hosts/prey would likely be fatal
(Botello and Krug, 2006), and a
theoretical consideration of the problem supports this suggestion
(Elkin and Marshall, 2007).
Despite the increased interest in the DLH and its apparent applicability to
a wide range of species (reviewed in Elkin
and Marshall, 2007), we have little idea as to the mechanism of
decreased selectivity with respect to settlement cues (i.e. `desperation').
Desperate larvae are rarely indiscriminate; for example, larvae of the
opisthobranch Haminaea callidegenita react to a greater variety of
cues as they age; young larvae metamorphose in response to a single inducer
but older larvae metamorphose in response to Zostera marina and a
green alga but not biofilmed sediment
(Gibson, 1995). How do
relatively simple larvae increase the range of cues that they react to whilst
continuing to reject other cues? To examine this question, we used the
lecithotrophic larvae of the Australian sea urchin Holopneustes
purpurascens. H. purpurascens is a relatively specialised herbivore that
lives on and consumes kelp, Ecklonia radiata, during the adult
benthic phase (Steinberg,
1995; Williamson et al.,
2004). As a newly settled juvenile, it is found predominantly on
the red alga Delisea pulchra and coralline turfing algae Amphiroa
anceps and Corallina officinalis
(Swanson et al., 2006). The
observed distribution of new recruits in the field matched settlement choices
in the laboratory, where larvae metamorphosed in response to D.
pulchra and coralline algae but not E. radiata
(Swanson et al., 2006).
H. purpurascens larvae metamorphose specifically in response to
dissolved histamine, a naturally occurring settlement cue produced in high
quantities by the red foliose alga D. pulchra
(Swanson et al., 2006;
Swanson et al., 2004). The
settlement cue(s) from coralline algae are unknown but seem to be produced by
the surface-associated microbial community (biofilm) and may be bacterial
histamine (Swanson et al.,
2006). H. purpurascens appears to be a typical species to
which the DLH applies: red algae (D. pulchra, A. anceps, C.
officinalis) are common hosts of new recruits of H. purpurascens
(Swanson et al., 2006), and
these algae induced 20–100% metamorphosis of newly competent (6-day-old)
larval H. purpurascens
(Williamson et al., 2004).
Brown algae (Sargassum vestitum, E. radiata) induce minimal
metamorphosis of newly competent larvae; however, as they age, their response
to brown algae increases (Williamson et
al., 2004). S. vestitum and E. radiata contain
histamine but at much lower levels than the preferred host of new recruits,
D. pulchra (Swanson et al.,
2006). Thus, older H. purpurascens larvae may expand the
range of host algae by metamorphosing in response to lower concentrations of
histamine. Alternatively, they may be responding to different cues present in
brown algae as they age and use entirely different response pathways. We
sought to distinguish among these hypotheses.
We tested the hypothesis that older H. purpurascens respond to a
greater range of host algae by reducing the threshold concentration of
histamine required for metamorphosis using settlement bioassays. Three batches
of larvae were tested against a range of concentrations of dissolved
histamine, at competence and each week thereafter for 2–3 weeks, to see
if older larvae (1) became more sensitive (responsive) to low concentrations
of histamine and (2) showed decreased specificity for histamine as a
settlement cue. Recent findings suggest that older larvae may require less
exposure to settlement cues than younger larvae to induce metamorphosis
(Jackson et al., 2005).
Therefore, we also tested the hypothesis that older H. purpurascens
required less exposure to histamine than newly competent larvae to induce
metamorphosis by exposing larvae at 7, 14 and 21 days old (same batch) to 10
µmol l–1 histamine for different time periods.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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2000)
were kept for settlement assays over ensuing weeks. Each batch of larvae was
of mixed parentage, with parents also differing between batches.
Settlement assays
All assays were done in the CTR in 36-mm sterile Petri dishes with 4 ml SSW
under static conditions. Replicates were randomly assigned among treatments.
Treatment and control dishes were prepared by first adding aliquots of
concentrated stock solutions of histamine in SSW followed by the addition of
SSW to bring histamine concentration to the desired test concentration. Larvae
were added once all Petri dishes were prepared. Larval H.
purpurascens reach competence (developmentally ready for metamorphosis,
recognised by the presence of five well-developed tube-feet) at around 6 days
old (6 days post fertilisation).
Dose–response of larvae of different ages
The dose–response of H. purpurascens larvae was investigated
to see if older larvae become more sensitive to lower concentrations of
histamine as an inducer of metamorphosis. Assays were done with three batches
of larvae (A, B and C) at 7 days old (i.e. newly competent larvae), 14 days
old (1 week post initial-competence), 21 days old (2 weeks post
initial-competence) and 28 days old (3 weeks post initial-competence;
batch A only). Histamine was tested at 1 µmol l–1, 100
nmol l–1 and 10 nmol l–1 in each assay as an
inducer of metamorphosis. Histamine was tested at 10 µmol
l–1 as a positive control because this concentration induced
maximal metamorphosis of larvae in previous studies
(Swanson et al., 2004;
Swanson et al., 2006). SSW was
tested in all assays as a measure of spontaneous metamorphosis. Twenty-five
larvae from batches A and B were used per treatment (five dishes with five
larvae), and 100 larvae from batch C were used per treatment (10 dishes with
10 larvae). Percent metamorphosis was scored at 1, 24, 48 and 72 h.
A repeated-measures ANOVA was used to examine the effects of larval age on
the sensitivity of larvae to lower concentrations of histamine as an inducer
of metamorphosis (SYSTAT® 10.0 for Windows). Only histamine concentrations
of 1 µmol l–1, 100 nmol l–1 and 10 nmol
l–1 were included in the analysis because 10 µmol
l–1 histamine induced maximal metamorphosis and SSW induced
minimal metamorphosis, regardless of larval age. Histamine was treated as a
categorical factor rather than a co-variate because of the small range of
values but the outcome of the analysis was the same in either case (D.J.M.,
unpublished analysis). Finally, values were pooled across all three
experimental runs (i.e. batches A, B and C) with 7-day-old, 14-day-old and
21-day-old larvae for the analysis. We also applied the alternative approach
of analysing each run separately, but the results were not qualitatively
different and we therefore opted for the most parsimonious approach of pooling
batches. Note that we first tested for interactions between run and the
factors of interest but, as these were non-significant and of no biological
interest, they were omitted from the final model following Quinn and Keough
(Quinn and Keough, 2002). Data
from batch A were analysed separately to include the response of 28-day-old
larvae. For both analyses, Greenhouse-Geisser adjusted P-values were
used as 
<0.75 (Quinn and Keough,
2002). The use of Greenhouse-Geisser P-values represents
a conservative approach that takes into account the fact that the assumption
of `sphericity' for the repeated-measures ANOVA was not met in our analyses
[Quinn and Keough (Quinn and Keough,
2002), p. 337].
Effect of duration of exposure to histamine on inducing metamorphosis
H. purpurascens larvae were exposed to 10 µmol
l–1 histamine for varying time periods at 7 days old, 14 days
old and 21 days old to determine the duration of exposure that was required to
induce settlement, a reversible process, and metamorphosis, an irreversible
process, in larvae of different ages. Histamine was tested at 10 µmol
l–1 in these experiments as this concentration induced
maximal settlement/metamorphosis of larvae in previous studies
(Swanson et al., 2004;
Swanson et al., 2006). Herein,
settlement is defined as the attachment of larvae to a surface via
tube-feet, and metamorphosis is defined as the morphological transformation to
the juvenile form. It was noted that attachment of H. purpurascens
larvae immediately triggered the retraction of the larval body and the partial
extrusion of juvenile spines and podia from the vestibule. However, these
initial morphological changes in settled larvae were potentially reversible if
they were removed from histamine exposure and placed in SSW. That is, a
proportion of settled larvae reverted back to swimming larvae when placed in
SSW depending on the duration of histamine exposure.
Seven-day-old larvae were exposed to 10 µmol l–1 histamine for 15 min, 20 min, 30 min, 45 min, 1 h, 2 h, 3 h, 4 h and 5 h, and percent settlement was scored before transferring individuals to SSW. Percent metamorphosis of individuals was scored (in SSW) 24 h after commencing the experiment. Larvae were continuously exposed to 10 µmol l–1 histamine or SSW for 24 h in control treatments. A further set of procedural control dishes was included, transferring larvae from 10 µmol l–1 histamine dishes to another set of 10 µmol l–1 histamine dishes at each exposure time, to determine if the transfer process alone affected the metamorphosis of larvae. The assay was repeated with 14-day-old and 21-day-old larvae; however, not all exposure times could be tested due to limited numbers of larvae. Larvae that were 14 days old were exposed to 10 µmol l–1 histamine for 1 h, 2 h, 3 h, 4 h and 5 h, while 21-day-old larvae were exposed to histamine for 30 min, 45 min, 1 h and 2 h (shorter times were selected as the majority of older larvae were metamorphosing after 1 h exposure). Fifty larvae were used for each treatment (five dishes with 10 larvae). From these data, a `reversion score' was calculated, which is the difference between the proportion of larvae that were metamorphosed at 24 h (in SSW) and the proportion of larvae deemed to have settled during exposure to 10 µmol l–1 histamine, before transferring to SSW. Thus, a positive score indicates that all larvae that had settled during exposure to histamine metamorphosed after transfer to SSW and that additional larvae also metamorphosed in the 24 h period. Conversely, a negative score indicates that a proportion of larvae that had settled during histamine exposure did not metamorphose after transfer to SSW but reverted back to swimming larvae. A two-factor (age = fixed factor, exposure time = fixed factor) analysis of variance (ANOVA) was used to examine the effects of larval age and exposure time on the induction of metamorphosis in H. purpurascens. The `reversion scores' of newly competent larvae (7 days old) and older larvae (21 days old) in the 30 min, 45 min, 1 h and 2 h exposure treatments were compared; only these treatments were analysed as not all exposure times were tested with larvae of different ages.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Larval age strongly affected the minimum concentration of histamine that induced metamorphosis in H. purpurascens, with older larvae responding to lower concentrations of histamine than newly competent larvae (Table 1, Fig. 1). Older larvae metamorphosed in greater numbers than newly competent larvae in response to low concentrations of histamine (Table 1, Fig. 1). Because batch A had more time periods (7-day-old, 14-day-old, 21-day-old and 28-day-old) than the other batches, we also analysed this batch separately to include the response of 28-day-old larvae (Table 2). Older larvae from batch A also metamorphosed at lower concentrations than newly competent larvae (Fig. 1); however, in the analysis, this interaction was obscured by a significant time x age x concentration interaction (Table 2).
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Effect of duration of exposure to histamine on inducing metamorphosis
Larval age strongly affected the induction of metamorphosis of H.
purpurascens larvae, with older larvae requiring less exposure to 10
µmol l–1 histamine than younger larvae to induce
metamorphosis (Table 3). Over
60% of newly competent larvae (7 days old) had settled after 20 min exposure
to 10 µmol l–1 histamine
(Fig. 2A). However, most
settled larvae reverted back to swimming larvae once removed to SSW when
exposed to histamine for 1 h or less, as indicated by the negative reversion
scores (approximately –0.6) (Fig.
3A). Following 2 h exposure to 10 µmol l–1
histamine, approximately half of the settled larvae metamorphosed into
juveniles after transfer to SSW. Newly competent larvae required 3 h
continuous exposure to 10 µmol l–1 histamine to induce
metamorphosis of >90% of settled larvae after transfer to SSW
(Fig. 2A,
Fig. 3A). Conversely, most
14-day-old larvae that had settled during 1 h (or longer) exposure to 10
µmol l–1 histamine metamorphosed after transfer to SSW,
generating reversion scores close to zero
(Fig. 2B,
Fig. 3B). Although fewer
21-day-old larvae overall had settled after 30–45 min exposure to 10
µmol l–1 histamine, most settled larvae metamorphosed
after transfer to SSW (Fig. 2C,
Fig. 3C). Larvae of all ages
that were continuously exposed to 10 µmol l–1 histamine
were metamorphosed after 24 h. None of the 7-day-old or 14-day-old larvae had
metamorphosed in control SSW after 24 h; however, approximately 10% of
21-day-old larvae had metamorphosed in control SSW after 24 h. All larvae in
the procedural control treatment (transferred from 10 µmol
l–1 histamine to 10 µmol l–1 histamine)
were metamorphosed.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
H. purpurascens joins a growing list of species that show shifts in
the response of larvae as they age (reviewed in
Elkin and Marshall, 2007).
Given that H. purpurascens recruits are found on a number of
different algae (Swanson et al.,
2006), it seems reasonable to assume that this species, whilst
having settlement preferences, is not a strict specialist at settlement. Thus,
whilst larvae that settle and metamorphose on preferred host algae may have
higher fitness, larvae that settle and metamorphose on other algae (i.e. brown
algae) in the habitat may still survive. The shift to a broader range of host
algae to facilitate metamorphosis of aging non-feeding larvae is predicted by
a theoretical model (Elkin and Marshall,
2007). As larvae accumulate direct (planktonic mortality) and
indirect (reduced energetic stores) costs in the plankton, the benefits of
metamorphosing in a sub-optimal habitat increase
(Elkin and Marshall, 2007).
Despite older H. purpurascens larvae reacting to lower and lower
concentrations of histamine, only a very small proportion (<5%) of very old
larvae (28-day-old) metamorphosed spontaneously in the absence of any algal
cues. Thus, older larvae do not metamorphose indiscriminately but become more
sensitive to the settlement cue. Given that histamine is found at lower
concentrations in other algae in the habitat, this increased sensitivity is
likely to result in older larvae accepting a broader range of host algae. Our
results appear therefore to be a novel example of expanding settlement
preferences by becoming more responsive to a single settlement cue, which can
occur here because of quantitative differences in the concentration of
histamine among algae in the field
(Swanson et al., 2006). By
using histamine concentration as a proxy for a general habitat cue, complex
changes in the settlement behaviour of older larvae can result from a simple
change in their response to a single cue.
A number of studies have found that older polychaete, gastropod and abalone
larvae metamorphose faster than younger larvae
(Barlow, 1990;
Botello and Krug, 2006;
Knight-Jones, 1953;
Pechenik and Cerulli, 1991).
Similarly, older larvae of Haliotis asinina metamorphosed after
shorter exposure periods to inductive algae than did younger larvae
(Jackson et al., 2005). H.
purpurascens larvae settled rapidly when exposed to 10 µmol
l–1 histamine regardless of age (R.L.S., personal
observation). Some morphological changes were evident in settled larvae such
as the retraction of the larval body and the partial extrusion of juvenile
spines and podia from the vestibule (R.L.S., personal observation). These
initial changes in morphology were reversible in a proportion of younger
larvae when exposed to histamine for less than 3 h, which suggests that
components of the morphogenetic pathway were not activated sufficiently to
trigger metamorphosis. Over 90% of 7-day-old larvae had settled after 45 min
exposure to 10 µmol l–1 histamine; however, most of these
reverted back to swimming larvae when placed in SSW. Newly competent larvae
required 3 h of continuous exposure to 10 µmol l–1
histamine to induce metamorphosis of all settled larvae. On the other hand,
21-day-old larvae required less than 1 h of exposure to 10 µmol
l–1 histamine to trigger metamorphosis of all settled larvae.
Thus, older larvae are induced to metamorphose soon after exposure to the
settlement cue whereas younger larvae appear to be more flexible at the time
of settlement. Newly competent H. purpurascens larvae that settle on
an alga have the potential to reject the site for a limited period after
attachment if the settlement cue is no longer perceived [for an alternative
process in ascidian larvae, see Jacobs et al.
(Jacobs et al., 2006)].
The increased sensitivity of H. purpurascens larvae to histamine
occurred gradually with age, suggesting that there is a progressive decrease
in the stimulus-threshold required to induce an aging larva to metamorphose,
as noted for other invertebrate larvae
(Coon et al., 1990;
Crisp, 1974;
Gibson, 1995;
Knight-Jones, 1953;
Pechenik, 1980;
Rittschof et al., 1984). The
mechanisms in older larvae that lead to increased sensitivity to histamine and
a reduction in exposure time required for metamorphosis are unclear but are
likely to have the same basis. Jackson et al. refer to `competence factors'
reaching a critical level in order for larvae to attain competency
(Jackson et al., 2005). These
factors may include chemoreceptors
(Trapido-Rosenthal and Morse,
1986), components of internal signalling pathways
(Clare et al., 1995;
Knight et al., 2000) or
transcription factors (Jackson et al.,
2005). These competence factors may continue to accumulate in
older larvae, meaning they are `primed' to respond to settlement cues, both to
lower concentrations and more quickly than younger larvae
(Jackson et al., 2005). For
example, changes in endogenous levels of neurotransmitters may affect
sensitivity to cues.
Catecholamines, such as dopamine and its precursor L-DOPA, appear to
modulate competency and control metamorphosis in the gastropods Crepidula
fornicata (Pechenik et al.,
2002; Pires et al.,
2000b) and Phestilla sibogae
(Pires et al., 2000a).
Increasing the endogenous dopamine concentrations of competent P.
sibogae larvae made them more sensitive to the settlement cue present in
coral extract [Porites compressa
(Pires et al., 2000a)]. In the
gastropod Ilyanassa obsoleta, metamorphosis only occurs following the
removal of endogenous levels of nitric oxide (NO), a specific inhibitor of
metamorphosis (Leise et al.,
2001). Bath application of serotonin induced metamorphosis of
I. obsoleta but not in the presence of two NO donors, and
metamorphosis of I. obsoleta was induced, in the absence of serotonin
or any other inducer, when endogenous NO production was inhibited
(Leise et al., 2001). Other
studies suggest that internal energy reserves also affect the sensitivity to
settlement cues. Botello and Krug found that unfed larvae were more sensitive
to settlement cues than fed larvae (Botello
and Krug, 2006), and Marshall and Keough found that larger larvae
(with more nutritional reserves) can delay settlement in the absence of cues
for longer than smaller larvae (Marshall
and Keough, 2003). Ultimately, each of these factors may also
contribute to the increased sensitivity of older H. purpurascens
larvae to histamine. However, it seems that the expansion of settlement
preferences in older H. purpurascens larvae
(Williamson et al., 2004) is
based on simple changes in their response to a single settlement cue.
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Acknowledgments |
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