Effects of sex and mass
We find limited support for the hypothesis that among-individual
behavioural differences are explained by sex and/or size (mass).
Refitted univariate models provide no statistical support for
differences in behavioural means between assigned sexes (Table 3), nor
did we detect any significant sex:size interactions. However, we did
detect significant main effects of size (mass) on OFT Track
Length and OFT Area Covered . Both coefficients are positive
meaning heavier individuals on average cover longer distances and a
larger area in OFT trials. Estimates of VI and R from
these refitted univariate models were very similar to those estimated
unconditional on the extra fixed effects (Figure 2), providing further
confirmation that neither sex nor size affects considerable
among-individual behavioural variation in single traits. This same
result also holds for the multivariate phenotype in that the correlation
structure in IDsex:mass is very similar to that
in ID (Figure 3). Moreover, the first vector ofIDsex:mass captures 65% (95% CI
47.96%-73.26%) of multivariate variance and has trait loadings almost
identical to those of idmax (Figure
4). Finally, plotting individual behavioural scores onidmax confirms the absence of clustering by sex
(Figure 5). While a net positive association between mean weight andidmax can be seen, it is also clear that size
accounts for only a small fraction of the variation present. We present
the full table of fixed effects estimates in Table S4 and the fullIDsex:mass . variance-covariance
matrix from which the correlations are derived in Table S5.
DISCUSSION
Our repeated measure design provided strong statistical support for
consistent among-individual differences in behaviour across the Open
field (OFT) and Food and shelter (FST) assays. As expected, multivariate
analyses also yielded evidence of strong individual-level correlations
among the specific traits assayed. However, in asking whether the
structure of multivariate behavioural variation was consistent witha priori expectations of an underlying axis of shy-bold
personality variation, our results provided a somewhat mixed picture.
Specifically, we did find a dominant leading eigen vector of IDthat explains most (61%) of individual level variation in, and
covariation-among, traits. However, several of the behaviours measured
load antagonistically on this axis, a pattern that does not match oura priori predictions for a simple shy-bold axis. Further analyses
provided little statistical support for major contributions of size- or
sex-effects to the personality variation described (though some size
effects were found). Below we discuss each of these main results in the
context of the existing literature and highlight some important caveats
to our conclusions.
Behavioural repeatabilities were statistically significant in seven of
the eight behavioural traits tested. This confirms the presence of
personality variation in red cherry shrimp and shows it is readily
detected using simple testing paradigms adapted from fish models.
Although personality has yet to be widely tested in decapods, our
results align with the conclusions of ) who demonstrated
among-individual variation in startle response duration (a proxy of
boldness) in male hermit crabs. Repeatability in traits associated with
shy-bold and/or exploratory personality variation has also been
demonstrated in the European crayfish (Astacus astacus ; , and the
rock pool shrimp (Palaemon elegans ; . In these latter examples,
boldness was also negatively correlated with resource holding potential,
suggesting a trade-off whereby bolder individuals may be better at
finding resources but less able to defend them in competition (. We do
not yet know if similar relationships hold in N. heteropoda but
investigating the functional significance of personality in relation to
competition and other ecological processes ) in this species would be
useful. More generally, testing for associations of behavioural profiles
with individual life histories would permit scrutiny of whether
personality variation is maintained through adaptive processes (e.g.,
resource allocation trade-offs ), and/or arises through differences in
resource acquisition coupled to state-dependent behaviour .
While estimates clearly varied among traits, some repeatabilities were
notably high in comparison to the wider animal personality literature.
For example, estimates of R=0.63 and R=0.56 for OFT Track Lengthand Area Covered are high compared to a median behavioural
repeatability of 0.37 reported by . This may, at least in part, reflect
the use of a short inter-observation interval; R is known to decline as
the time between observations increases (e.g., ). However, high
repeatabilities also have some implications worth noting. First, R sets
an upper limit for heritability (and so potential rate of selection
response) and facilitates more accurate selection
. Selection on behaviour has been suggested as a way to improve growth
and other production traits in commercial shrimp cultivation and in this
context, high repeatability of the selection target would be
advantageous. In a study of Pacific white shrimp (Litopenaeus
vannamei ), found that individuals interacting more with feed had a
lower latency of approach and consumed food more rapidly. In our FST
assay, latency to enter the zone containing food in the FST was actually
not repeatable (and so not heritable). However, if simple behavioural
biomarkers of improved feeding could be identified, then selecting on
these could be valuable in an industry where food waste is a major
source of economic inefficiency .
Although the implications are perhaps less clear at present, personality
variation has been widely linked to the likelihood of establishment
and/or invasive spreading of species following accidental introduction
For instance in the American signal crayfish (Pacifastacus
leniusculu s), found repeatable differences in shy-bold type behaviour
that predicted individual motivation to disperse by passing through
weirs (though not successful at doing so). Invasion processes could
therefore be considered a ‘selective filter’ whereby only individuals
with appropriate combinations of personality and other traits can invade
a novel environment successfully Working on the same species of
crayfish, , found invasive populations were bolder and more aggressive
on average than populations within their native range. However, this was
only true where invasive populations were allopatric to native crayfish,
and the extent to which differences were present prior to invasions, as
opposed to emerging after as adaptations to a new environment is unclear
. Moreover, whether population level repeatability to shy-bold type
behaviours (as opposed to individual or population mean) influences
invasive potential is unresolved. Low repeatability implies high
plasticity- at least relative to ‘fixed’ individual differences- and
there is a long-standing hypothesis that plasticity plays an important
role in adaptation to novel environments following dispersal . A recent
study found differences in behavioural repeatability between native and
invasive species of nudibranchs that is consistent with this idea , but
more empirical studies are needed to see if low behavioural
repeatabilities reliably predict risk of invasive spread.
Although we found strong support for personality in red cherry shrimp,
multivariate analyses show the structure of behavioural variation
differs somewhat from our initial predictions. Our eigen decomposition
of the ID matrix is consistent with the presence of a latent
personality axis that describes the majority of among-individual
(co)variation in the measured behavioural traits . This was expected:
all traits analysed were chosen precisely because they are putatively
measures of the same underlying shy-bold personality axis. Thus, the
important result here is not the presence of correlation structure inID , but the overall ‘shape’ of that structure. Specifically,
because traits were scaled such that higher numbers denoted putatively
bolder phenotypes, we had also predicted that covariances inID , would be uniformly positive, and all traits would load on
the main eigenvector with concordant signs. Some, but not all,
relationships were as expected. For example, individuals that travelled
further than average in the OFT, also have higher track length in the
FST, cover more area (OFT), and freeze less (both assays). These
behavioural characteristics meet a priori expectations for the
bolder end of the shy-bold continuum indicating that exploratory
individuals are associated with the propensity to take greater risks .
However, the same individuals also tend to swim closer to the tank walls
in the OFT (i.e., be more thigmotaxic) and take longer to visit the food
zone in the FST, which are characteristics typically associated with shy
personality types. Neither of these traits load significantly onidmax (based on 95% CI not overlapping zero)
and among-individual variance for FST -(Food Latency) was not
statistically supported in the univariate model. However, FST Time
in Open loads significantly on idmax with a
negative sign and is also moderately repeatable. This actually means
individuals considered bolder and/or more exploratory in the OFT spend
longer durations than average in the shelter during FST, a result that
is counterintuitive. Very speculatively, it is possible that the shelter
provided may have been perceived as a risky environment (rather than a
safe one as intended). This could arise if, for instance, our shelter
mimicked the type of structure used by drift-feeding and opportunistic
foraging predatory fish . With this considered, it would be interesting
to investigate whether a refuge with greater structural complexity
and/or smaller open spaces may be preferred (as demonstrated in mud
crabs Scylla serrata ; .
We find limited evidence for sex and size effects on behaviour and
conclude that these aspects of state do not make a major contribution to
personality (co)variation in our population. The absence of sex effects
is perhaps somewhat surprising given the extensive evidence of
behavioural sexual dimorphism in decapods. For example, male rock pool
prawns (Palaemon elegans ) are bolder and more active than females
, while aggression is sexually dimorphic in white shrimp (Penaeus
vannamei ; , rock shrimp (Rhynchocinetes typus ;) and American
lobsters (Homarus americanus ;). In these species, males tend to
be more aggressive and able to monopolise food for longer durations
relative to females. In finding an absence of sexual dimorphism here we
acknowledge that uncertainty in sexing the shrimp reduces statistical
power. Of the 53 shrimp tested, we ultimately classified 22 as being of
unknown sex. These were, on average, smaller individuals than those
assigned to male or female categories and likely to be younger (and
potentially sexually immature). We therefore cannot exclude the
possibility that our study partially conflates sex, age and maturation
status in ways that mask any dimorphism. Nevertheless, we also note that
several other decapod studies have reported an absence of sex effects on
shy-bold type traits. For example, found no difference in mean boldness
or activity between male and female Chinese mitten crabs Eriocheir
sinensis, while sex did not predict startle response duration in hermit
crabs Pagurus bernhardus .
We did find some evidence for size-dependent behaviour. Statistical
support was limited to two traits in the OFT, with larger (heavier)
individuals traveling slightly further and covering more area on
average. These trait-specific effects drive a trend towards larger
individuals having higher behaviour scores onidmax . This could potentially be explained by
links between behavioural type and life-history strategy as proposed
under heuristic frameworks such as the ‘Pace of Life Syndrome’ . For
instance, high metabolic rate may be associated with bolder behaviour,
increased resource acquisition, and faster growth leading to increased
size , albeit at the likely cost of higher mortality risk (e.g. from
predation; Wolf et al., 2007). At present we lack individual level data
on life histories to test these hypothesised relationships. We also lack
sufficient ecological data to explore (arguably) simpler explanations
for size-dependence. For instance, argued size-dependent behaviour of
mud crabs (Panopeus herbstii ) was linked to size-dependent
predation risk. Small crabs used refuges more than large crabs and also
increased use in the presence of predators. Other mechanisms proposed
for generating size-behaviour relationships in decapods are related to
mating traits. For instance, male-male competition can drive
size-dependent mating tactics with larger males engaging more in mate
guarding and contest behaviour while smaller rivals adopt exploratory
mate searching tactics . Although we cannot yet rule out similar
processes in cherry shrimp, it is notable we found no sex by size
interactions on the behaviours assayed here (i.e., both larger males and
females have higher Track Length and Area Covered in the
OFT).
In conclusion, this is the first study to our knowledge that describes
patterns of among-individual variation in putative measures of shy-bold
variation in the cherry shrimp, N. heteropoda. Using simple
assays widely applied to small fish models, our results are consistent
with the verbal model of a single major personality axis underlying
among-individual differences observed. However, the structure of this
axis does not fully match a priori expectations of shy-bold. This
could be because our initial assumptions of what constitutes ‘riskier’
behaviour in this species are incorrect. We also found no evidence for
sexual dimorphism in behaviour and only limited support for
size-behaviour relationships. Our description of personality variation
in red cherry shrimp adds to the growing picture of this phenomenon in
invertebrates generally and decapod crustaceans specifically . We
therefore hope this study will set the foundations for future
investigations of mechanism and functional significance in this emerging
model system, as well as providing baseline data for more applied
research across ecotoxicology, aquaculture, and invasion biology.