Download does variable coloration in juvenile marine crabs reduce

Notes
Ecology, 82(10), 2001, pp. 2961–2967
q 2001 by the Ecological Society of America
DOES VARIABLE COLORATION IN JUVENILE MARINE CRABS REDUCE
RISK OF VISUAL PREDATION?
ALVARO T. PALMA1
AND
ROBERT S. STENECK
University of Maine, Darling Marine Center, Walpole, Maine 04573 USA
Abstract. We discovered that newly settled marine rock crabs, Cancer irroratus, exhibit
a variety of non-adult colors early in life. This color polymorphism predominates in populations of minute juvenile crabs living in polychromatic habitats where it apparently renders
them inconspicuous to visual predators such as fish. Experiments revealed lower frequencies
of non-adult color morphs in monochromatic three-dimensional habitats with predators and
polychromatic habitats from which predators were excluded. These patterns result from
selective predation on visually contrasting color morphs. Adult crabs are monochromatic,
conspicuous, and not associated with shelters. Both polymorphic newly settled and monochromatic large individuals occur in environments dominated by small predatory fish where
larger adult crabs are at low risk of predation. Behavioral and visual crypsis may only be
important early in life when post-settlement mortality is high, and survival at that stage
determines recruitment and ultimately population densities. The well-known examples of
camouflage among insects usually apply to adults who, unlike these marine counterparts,
are small relative to their predators and thus remain vulnerable throughout their lives. Many
other large marine crustaceans are cryptic only early in life, suggesting that this early
developmental color polymorphism might be an important difference between marine and
terrestrial arthropods.
Key words: camouflage; Cancer irroratus; color polymorphism; color variants; crypsis; Gulf of
Maine; predation; post-settlement; rock crabs; settlement; subtidal.
INTRODUCTION
The ecological and evolutionary success of many
organisms depends on their ability to hide from predators. Myriad species of insects evolved remarkable
ways to blend into their surroundings. For example, the
peppered moth (Biston betularia) adapted chromatically to the pollution-blackened trees of England due
to selective predation by birds on contrasting light
moths (Kettlewell 1955, Majerus 1998). While such
antipredator camouflage is well known among adult
insects and small marine crustaceans (e.g., Hay et al.
1989, Hacker and Steneck 1990, Duffy and Hay 1994,
Stachowicz and Hay 1999), similar patterns in large
marine arthropods are rare.
In marine systems, crustaceans are the most diverse
group of arthropods. Among crustaceans, decapods
such as crabs, lobsters, and shrimps comprise an ecologically and economically important component of
Manuscript received 24 July 2000; revised 8 February 2001;
accepted 2 March 2001.
1 Present address: Facultad de Ciencias, Universidad Católica de la Ssma. Concepción, Paicavi 3000, Casilla 297,
Concepción, Chile. E-mail: [email protected].
many marine systems. Decapods are highly valued food
for humans and other predators because of their high
food value (caloric content). Prey size relative to predator size is critical to the susceptibility of prey. Since
marine decapods are particularly vulnerable to predators at the time of and just after settlement, mechanisms
that mediate predation then may be critically important
to the demography and possibly the evolution of the
species. Many studies have demonstrated strong habitat
dependency among decapods that are small as adults,
or are vulnerable to predators at the time of settlement.
Examples include refuge dwelling decapods such as
crayfish in freshwater (Stein and Magnuson 1976), stomatopods in the marine realm (Steger 1987), settling
American lobsters (Wahle and Steneck 1992), stone
crabs (Beck 1995), the tropical reef crabs Caphyra rotundifrons (Hay et al. 1989), mangrove crabs (Wilson
1989), and Mithrax crabs (Stachowicz and Hay 1996).
Less well known than these examples of physical crypsis (the use of structural refuges) are the examples of
visual crypsis or camouflage.
In this study we document a previously unreported
strategy of visual crypsis discovered among newly set-
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NOTES
Ecology, Vol. 82, No. 10
FIG. 1. (Right photo) Newly settled rock crabs (Cancer irroratus) on natural polychromatic shell hash substratum. (Left)
Highlight of the same seven individuals.
tled rock crabs (Cancer irroratus) of the western North
Atlantic. We found a color polymorphic pattern (i.e.,
different colored individuals within a population) that
may be important in reducing early post-settlement
mortality for this species. We suspect that this strategy
is more widespread than is currently recognized. Polymorphic juvenile rock crabs possess this trait only early
in their benthic life. We speculate that this brief (weeks
to months) developmental crypsis could be due to the
relatively brief period of vulnerability of this species
to predators. Unlike many insects, marine decapods can
attain large size (e.g., over 20 kg for Homarus americanus; Wolff 1978) that renders them relatively immune to predators (e.g., Wahle 1992, Steneck 1997).
Although the expression of color camouflage and mimicry is common and has been described for many small
marine invertebrates (Atkinson and Warwick 1983,
Hughes and Jones 1985, Mercurio et al. 1985, Cook
1986, Espoz et al. 1995) and other crustaceans in particular (Hogarth 1978, Buss and Iverson 1981, Bulnheim and Fava 1982, Main 1987, Hacker and Madin
1991, Guarino et al. 1993), few studies have considered
developmental crypsis confined to juveniles undergoing a crucial ecological transition (but see Wicksten
1979, 1983, Pennings 1990, Stachowicz and Hay
1999).
Cancer irroratus is a common large benthic brachyuran decapod in shallow environments of the western
North Atlantic (Williams 1984). Post-larvae of this species settle indiscriminately into several types of substrata (sandy and rocky bottoms) at similar densities
(Palma et al. 1999). High mortality rates at this stage
result in the highest survivorship occurring in shelterproviding cobblestone habitats (Palma et al. 1998).
Within this system, we discovered and quantified color
polymorphism among newly settled crabs (i.e., individuals colored differently from adults) in both natural
polychromatic and artificial monochromatic habitats
(Fig. 1). We employed a standardized color classification scheme in which crabs colored differently than
the drab brown adults were identified as white, yellow,
tan, and dark brown. The color of individual crabs only
changed between molts, which progressively decline
in frequency after settlement (A. Palma, personal observation). The proportion of polymorphic individuals
decreased with the size of individuals. If color variations among newly settled individuals confer protection
through visual crypsis, we hypothesized that its frequency of occurrence would be greatest in polychromatic natural substrata. We tested this against settlement within manufactured monochromatic gray PVC
settlement collectors that mimic the interstitial spatial
geometry of cobblestone nursery habitats, but not their
color. Adjacent controls were comprised of two natural
substrata, shell hash and cobblestone.
MATERIALS
AND
METHODS
Because chromatic patterns vary with size we conducted all comparisons synchronously among recently
settled cohorts. We operationally defined newly settled
crabs as those with ,10-mm carapace width. Quantitative surveys of new settlers were made in eight sites
along the central coast of Maine. Specific locations are
given in Palma et al. (1999). At each site, two different
natural substrata (cobblestone and coarse shell hash)
were surveyed using scuba at depths of 10 m below
MLW. Divers haphazardly tossed 0.5-m2 quadrats and
all organisms and material present in each area was
October 2001
NOTES
2963
FIG. 2. Frequency of the different color variants for individuals of Cancer irroratus collected in natural substrata (cobblestones and
sand) in different size classes. Numbers above
each graph represent the number of individuals
quantified in each class.
sampled using suction to a depth of about 20 cm (methods of Wahle and Steneck 1991, Palma et al. 1998).
Newly settled individuals were collected during the
settlement season (August–September) between 1994
and 1997. Throughout the study, parametric comparisons of abundance or proportion of individuals with
color variants were analyzed, and transformations applied to ensure normality and homogeneity of variance.
Experimental treatments were placed at randomly defined locations. Data of proportions or percentages,
throughout this study, were subject to arcsin(square
root) angular transformations (Zar 1999). Further details on study area, experimental design, and general
methods are published elsewhere (Palma et al. 1998).
Both abundance and the proportion of color variants
among newly settled crabs were simultaneously quantified in natural substrata and in manufactured collectors that provided a monochromatic background while
maintaining the structural complexity. Collectors were
placed in several of the study sites throughout the settlement period. Collectors were 0.24-m2 square structures made of rows of 3-cm diameter gray PVC pipes
spaced 1 cm apart and stacked three rows deep in tiers
of alternating row direction. The stack was placed inside a wire basket lined with 1-mm mesh nylon screen
(Palma et al. 1998).
The effect of visual predators on the proportion of
color variants among newly settled individuals was
tested in the field. The predator-exclusion experiment
was a two-way, fixed-factor design with substratum
(cobblestones and sand) and 0.5-m2 cage treatment (total predator exclusion, open control, and roofed cage
control) as factors, and proportion of color variants as
response variable. There were five replicate plots for
each of the six treatment combinations for a total of
30 plots. The experiment was surveyed twice; thus we
performed a repeated-measures ANOVA. The final data
matrix was not perfectly square because some data had
to be excluded due to cage breakage.
The effect of predators on the proportion of polychromatic newly settled individuals inside PVC collectors was also tested. Using the PVC collectors, a
predator-exclusion experiment was implemented during the settlement period of 1998, between August and
September. Ten collectors were covered with the same
plastic 4-mm mesh screen and 10 were left uncovered.
Collectors were randomly interspersed at the west side
of Damariscove Island, in the same location in Maine
where the previous exclusion experiment on natural
substrate took place. By the end of September all collectors (with and without screen) were retrieved and
all decapods quantified in the laboratory using a 2-mm
mesh size sieve.
RESULTS
Newly settled crabs display a variety of colors that
correspond with the variety found in their settlement
habitat (Fig. 1). Over 70% of the newly settled crabs
were non-adult colors (Fig. 2). Whereas .70% of individuals one year and older (.15 mm in carapace
width) were adult brown in color (Fig. 2). The combined proportion of individuals with non-adult brown
color was significantly greater in the smallest size class
compared to any of the larger size classes (F5,99 5
8.542, P , 0.0001).
To eliminate the potential confounding influence of
body size with color change in our experiments (e.g.,
Fig. 2), we quantified color differentiation of only similar-sized newly settled individuals. The population
density of new settlers of ;10 individuals/m2 was similar in all three substrata (cobblestone, shell hash, and
PVC collectors; F41,2 5 0.141, P 5 0.869). However,
the proportion of polymorphic color variants was significantly higher in the two natural polychromatic habitats compared to the artificial monochromatic substrata
(F26,2 5 11.98, P , 0.001; Fig. 3). Although reduced
color polymorphism occurs ontogenetically, the short
2964
NOTES
Ecology, Vol. 82, No. 10
factor repeated-measures ANOVA comparing the joint
effect of substratum and cage treatment. Pairwise comparisons for the different treatment and substrata combinations were performed using Tukey’s test (Fig. 4A,
Table 1). A subsequent experiment using screen-covered and uncovered collectors tested the potential effect
of predators on color polymorphism inside monochromatic PVC collectors. This time, polymorphism was
significantly lower inside the monochromatic, predatorrich (uncovered) collectors (0.48 6 0.26 vs. 0.77 6
0.11; F1,16 5 7.87, P 5 0.013, Fig. 4B).
DISCUSSION
FIG. 3. Proportion of newly settled (#10 mm carapace
width) individuals with non-adult color variants on natural
(polychromatic cobblestones and sand) and artificial (monochromatic gray PVC collectors) substrata (61 SE). All treatments had the same post-settlement duration. Interrupted horizontal line below the figure denotes significant difference.
duration deployment (,2 mo) of PVC collectors minimizes ontogenetic effects in this treatment.
Since fish predators control the abundance of newly
settled rock crabs (Palma et al. 1998), we used predatorexclusion cages at 10-m (MLW) depths where settlement rates were high (Palma et al. 1998). Cages were
covered with plastic 4-mm mesh screen, so that only
new settlers could enter. A significantly lower proportion of newly settled crabs with non-adult color were
found inside the predator-exclusion cages irrespective
of substrate, with no significant interactions in a two-
Newly settled Cancer irroratus crabs display a spectrum of non-adult colors (Figs. 1, 2) that disappear as
they grow. This transient polymorphic condition may
be a bet-hedging strategy in a chromatically diverse
and unpredictable world in which visual predators
prowl. Since this species settles indiscriminately but
suffers high rates of post-settlement mortality (Palma
et al. 1998), the color pattern of the nursery habitats,
if visual predators are present, can control the color
morphs that survive. For example, a much lower percentage of color polymorphs survive in monochromatic
habitats with predators than in those habitats where
they are predator-free (Fig. 4B), presumably due to the
higher predation rates on the several color morphs that
contrast strongly against the monochromatic substrate.
Conversely, a much higher percentage of color polymorphs survive in polychromatic, natural habitats with
predators than in those habitats when they are predator
free (Fig. 4A). Here local predation rates resulted in
FIG. 4. (A) Proportion of newly settled (#10 mm carapace width) crabs with non-adult color variants in predator-exclusion,
open control, and roofed-cage control polychromatic (natural substrate) cages (61 SE) for the two times the experiment was
surveyed. Treatments had the same post-settlement duration. Given the lack of significance (Table 1) between polychromatic
cobblestone and sand plots, these results were pooled. (B) Proportion of newly settled crabs with non-adult color variants
in the monochromatic PVC-collector exclusion experiment under predator-exclusion and open conditions (61 SE). Interrupted
horizontal lines at the top of each histogram indicate significant differences.
NOTES
October 2001
2965
TABLE 1. Results of the two-factor repeated-measures ANOVA for the exclusion of predators
(Treatment) and sand or cobblestone plots (Substrate). The response variable is the proportion
of individuals with non-adult color variants.
df
MS
F
P
Between subjects
Substrate
Treatment
Substrate 3 Treatment
Error
1
2
2
16
0.008
0.502
0.262
0.121
0.062
4.159
2.169
0.806
0.035
0.147
Within subjects
Trial
Trial 3 Treatment
Trial 3 Substrate
Trial 3 Treatment 3 Substrate
Error
1
2
1
2
16
0.001
0.041
0.002
0.503
0.203
0.003
0.203
0.008
2.477
0.959
0.818
0.931
0.116
Source
colors that match their polychromatic habitat (Fig. 1).
This newly discovered survival strategy of developmental crypsis in this species may contribute to its
remarkable abundance in the Gulf of Maine (Palma et
al. 1999). The mechanism by which this species undergoes changes in color morphs throughout its ontogeny is not known. However, multicolored post-settlers
kept in the laboratory turned to an adult brown color
after several molts over a period of several months.
Marine ecology has undergone a paradigm shift in
recent decades. Processes such as competition and predation among adults were once assumed to be the primary drivers of local demography and community
structure (Paine 1969, Dayton 1975, Lubchenco 1978).
More recently, however, ‘‘supply side’’ ecology (e.g.,
Underwood and Fairweather 1989) emphasizes processes affecting early settlement and post-settlement
phases (Gaines and Roughgarden 1985, Doherty and
Fowler 1994). If strong interactions early in life diminish ontogenetically, due to increased body size,
then the specific mediating characteristics may be important only during early benthic stages. Our study suggests that developmental crypsis confers an advantage
to newly settled rock crabs in environments with small
visual predators.
Predator–prey size scaling may be different in marine and terrestrial systems. Whereas large crabs may
pass through a brief period of predator vulnerability,
most insects are small and remain vulnerable throughout their life. The phenomenon of color polymorphic
new settlers and monochromatic large crabs occurs in
environments dominated by small predatory fish (Hacunda 1981, Malpass 1992, Wahle and Steneck 1992,
Steneck 1997), where larger crabs are less threatened.
Undoubtedly large predatory fish were much more
abundant in historic and prehistoric times in coastal
areas of the Western North Atlantic (Witman and Sebens 1992, Steneck 1997). Thus it is possible that until
recently (i.e., the past century) large fish predators
could have had a stronger impact on larger rock crabs
than they do today. Nevertheless, small crabs have
probably always been most vulnerable to the widest
range of fish predators in the Gulf of Maine. It is unknown if the developmental crypsis we describe may
have persisted later into a crab’s ontogeny when larger
predators were more common. We do not know why
color polymorphism is lost as crabs mature. It is possible that it is a ‘‘costly’’ condition to maintain. However the advantages of light color morphs (e.g., white
and yellow) that mimic shell chips (Fig. 1) are lost at
large sizes since most rocks of adult crab size are drab
over the range of this species (A. Palma, personal observation).
Crypsis is found among other decapods that are bite
sized. Small crabs remain cryptic through all developmental stages. For example, the chip crab, Heterocrypta granulata, is camouflaged to resemble shellhash. It ‘‘. . . so closely resembles the bits of shell and
rock fragments among which it hides that it is difficult
to know how common it might be (Gosner 1978).’’ Other small decapods such as small adult shrimp mimic
the brown alga Sargassum in the Sargasso Sea (Hacker
and Madin 1991). However, among relatively large
decapods such as lobsters, crypsis is only known early
in life. The transparent phyllosoma phase may protect
spiny lobster post-larvae by minimizing contrast with
the pelagic realm in which they develop (Herrnkind
and Butler 1986). Several species of newly settled
spiny lobsters are cryptically colored to blend in with
the algal habitats in which they settle. Examples include Panulirus argus (Marx and Herrnkind 1985), P.
japonicus (Yoshimura and Yamakawa 1988), and P.
cygnus (Pearce and Phillips 1994). The American lobster (and other clawed lobsters) are not visually cryptic
but are physically cryptic living their first several benthic years within small, shelter-providing spaces where
they are relatively safe from predators (Wahle and Steneck 1992). Much smaller decapods such as freshwater
NOTES
2966
crayfish (Stein and Magnuson 1976) and marine stomatopods remain hidden within their shelters during
their entire life (Steger 1987).
Despite their staggering diversity, insects are small.
Arguably, their small body size results from phyletic
constraints on respiration, which is limited by trachea
and an open circulatory system. More importantly,
most insects are small relative to their predators and
thus, as a group, they do not typically outgrow their
vulnerability the way large marine decapod crustaceans
can. This may be a fundamental ecological distinction
between arthropods of the terrestrial realm and some
marine groups. Because body-size-related niche shifts
are so great among some large decapods (e.g., Wahle
1992), the rock crab–insect analog may only apply to
insect-sized baby crabs.
ACKNOWLEDGMENTS
We are thankful for the valuable help in the field and laboratory provided by several interns between 1994 and 1998.
We thank the University of Maine’s Darling Marine Center
for its facilities and help from its support staff. The ideas
within this manuscript were greatly improved by the helpful
comments of M. Bertness, M. Fogarty, R. Wahle, L. Mayer,
L. Watling, S. Zimsen, P. Marquet, M. Fernandez, and F.
Labra. This research was also supported by NOAA/NURC at
University of Connecticut at Avery Point and University of
Maine/University of New Hampshire Sea Grant Program to
R.S.S. A.T.P. also acknowledges the support of a postdoctoral
grant (Fondecyt No. 3990032) while working on this manuscript. This is contribution No. 365 to the Darling Marine
Center.
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