Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34

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Journal of Experimental Marine Biology and Ecology

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e

Cryptic coloration as a predator avoidance strategy in seagrass arrow

shrimp colormorphs
Benjamin L. Cournoyer 1, Jonathan H. Cohen ⁎
Department of Marine Science, Eckerd College, 4200 54th Avenue South, St. Petersburg, FL 33711, USA

a r t i c l e i n f o a b s t r a c t

Article history: The arrow shrimp, Tozeuma carolinense, is a highly abundant small crustacean inhabiting seagrass beds along
Received 2 September 2010 the US southeastern and Gulf coast. These shrimp inhabit the tops of seagrass blades, feeding on epiphytic
Received in revised form 17 March 2011 algae. Despite T. carolinense abundance, it is largely underrepresented in the diets of predatory fish,
Accepted 18 March 2011
presumably due to its cryptic morphology and behavior. Here, we quantify the degree of crypsis of green and
brown colormorphs of T. carolinense to the visual systems of two potential predators, dichromatic Cynoscion
Keywords:
Chromatic contrast
nebulosus and trichromatic Sciaenops ocellatus, using a visual chromatic contrast model. Contrast of shrimp
Crypsis colormorphs viewed against seagrass backgrounds was similar between predators but varied greatly for both
Tozeuma carolinense colormorphs among the backgrounds. For both dichromatic and trichromatic predators, green morphs
Visual ecology produced significantly less contrast than brown morphs on live seagrass, while brown morphs produced
significantly less contrast than green morphs on dead seagrass. Each colormorph had at least one
complimentary seagrass species against which it would be difficult for fish predators to discriminate.
Model predictions were largely borne out in a survey of a natural population of T. carolinense in Tampa Bay, FL
(USA), where shrimp were found only in monospecific patches of live Syringodium filiforme, and green morphs
significantly outnumbered brown morphs. Although these shrimp do not rely solely on cryptic coloration for
predator evasion, the ability of T. carolinense to match its background does minimize visual contrast and likely
contributes to their lack of representation in the diets of predatory fish.
© 2011 Elsevier B.V. All rights reserved.

1. Introduction invertebrates, the caridean shrimp Gnathophylloides mineri both

Seagrass beds and other structurally complex habitats in shallow-
water marine environments provide both productive areas for feeding
and a refuge from predation for a range of invertebrate and juvenile
fish species (Heck et al., 2003). Seagrass habitats may confer
protection for prey species through a reduction in predation rate
with increasing habitat complexity, but recent studies have ques-
tioned this long-held hypothesis (Canion and Heck 2009). Further-
more, prey organisms residing in seagrass beds are vulnerable to both
transient and resident predators which commonly differ in predatory
tactics and whose efficiency for prey detection and capture are
differentially affected by habitat structure (e.g. Horinouchi et al.,
2009). Consequently, prey species in seagrass beds posses a variety of
predator avoidance strategies, including morphological and behav-
ioral crypsis, to protect themselves from a suite of predators.
Cryptic organisms, irrespective of habitat, typically rely on a
complimentary assortment of adaptations to avoid detection and
subsequent capture (Endler, 2006). Among shallow-water marine
⁎ Corresponding author: Tel.: + 1 727 864 7827; fax: + 1 727 864 7964.
E-mail address: cohenjh@eckerd.edu (J.H. Cohen).
1
Present address: Department of Marine Science, University of Connecticut, 1080
Shennecossett Road Groton, CT 06340, USA.
matches the coloration of its echinoid host, Tripneustes ventricosus,
and holds its claws perpendicular to the host mimicking spines
(Patton et al., 1985; Macia and Robinson, 2009). The majid crab,
Microphrys bicornutus, achieves crypsis by covering its carapace in
local flora and fauna (Getty and Hazlett, 1978; Wicksten, 1993).
Decorating behavior in other majid crabs combines the use of
chemically defended algal species as well as algal food resources to
be consumed at a later time (e.g. Cruz-Rivera 2001). In rafts of pelagic
Sargassum, two species of shrimp (Latreutes fucorum and Hippolyte
coerulescene) morphologically mimic different structural components
of the alga and segregate behaviorally, clinging to the mimicked
structures (Hacker and Madin, 1991).
Complimentary cryptic strategies are similarly employed by the
caridean shrimp Tozeuma carolinense Kingsley (1878), an epibenthic
crustacean ranging from Massachusetts to Brazil (Williams, 1984). It
associates closely with seagrass along the US southeastern and Gulf
coasts, including three of the most common seagrass species:
Syringodium filiforme, Thalassia testudinum, and Halodule wrightii
(Mutchler et al., 2004; Hays, 2005). T. carolinense feeds on epiphytic
algae covering seagrass or other structures (Mutchler et al., 2004).
Under normal conditions this species controls epiphyte growth on
seagrass blades, allowing beds to grow unhindered (Hays, 2005). At
higher nutrient concentrations, seagrass has been shown to produce

0022-0981/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2011.03.011
28 B.L. Cournoyer, J.H. Cohen / Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34
greater biomass in the presence of T. carolinense grazing, yet in the
absence of grazing epiphytes outcompete seagrass for light, stunting
growth (Hays, 2005). Accordingly, populations of T. carolinense are
integral to the health of seagrass beds as they buffer deleterious
effects of epiphytic algal growth.
Predator–prey interactions often regulate prey populations in
seagrass communities (Leber, 1985). Small shrimp represent a large
portion of the diet of many highly visual fish predators in coastal
seagrass beds (Hetter, 1989; Scharf, 2000), and these potential prey,
including T. carolinense, employ several strategies to remain visually
inconspicuous in this habitat (Main, 1987). Morphologically, the
nearly transparent body of T. carolinense is narrow and elongated with
a single band of green or brown color running along its anterior–
posterior body axis. Color is controlled partially by a series of
chromatophores which run the length of the body flanking the gut
(Ewald, 1969). As the majority of the shrimp body tissue is clear, gut
contents also contribute to the overall coloration. Along the US
southeastern and Gulf coasts, green and brown colormorphs are
dominant, but shades of red and purple are common further south
with ingestion of different food items such as alcyonarian corals
(Williams, 1984). Behaviorally, shrimp cling to seagrass blades or
swim in a head down vertical position allowing the single band of
color to seamlessly blend in with the surrounding seagrass (Main,
1987). As evidence of its possible cryptic success, T. carolinense is
underrepresented in fish diets based on its overall biomass in seagrass
communities (Main, 1985).
Main (1987) thoroughly described the role of behavior in
T. carolinense predator evasion within seagrass habitats. It exhibits
nine general behaviors, including three adapted specifically for predator
evasion: clinging, moving around the blade, and the Caridoid escape
response. In laboratory observations, the presence of a fish predator
(Lagodon rhomboides) significantly increased the occurrence of these
three behaviors (Main, 1987). The most novel of these was movement
around the blade. When a predator gets within 15 cm, T. carolinense
swings itself around a grass blade, using the blade as a physical shield
between it and the predator. As the eyes of T. carolinense are located on
stalks, it can position them on either side of a thin blade and watch the
predator as it moves by. Main (1987) also conducted a predation
experiment in order to test the effect of cryptic coloration, but was
unable to definitively conclude that cryptic coloration plays a significant
role in the predator evasion strategy of T. carolinense, although the
possibility was not dismissed.
In considering visual crypsis of shrimp colormorphs, it is important
to note that the visual systems of fish preying upon shrimp are not
identical, leading to complications for visually cryptic prey species
needing to avoid multiple predator species. Key parameters affecting
the ability of a specific predator to visually detect a given prey item
include: (1) the environmental illuminant; (2) the spectral reflec-
tance of the visual target; (3) the behavior of the observer; and (4) the
physiological capabilities of the observer's visual system (Troscianko
et al., 2009). While the first two parameters might not change
between two fish predators, the latter two parameters might differ.
Observer behavior and visual physiology determine the quality and
quantity of light reflected from a visual target that ultimately activate
the observer's visual system, making the behavior and visual
physiology of predators important parameters for understanding
the utility of cryptic coloration in a given habitat (Marshall et al.,
2003).
Understanding the apparently heavy visual component of
T. carolinense predator avoidance behavior and morphology is
important for understanding its population dynamics and role in
seagrass habitats. Therefore, in the present study a visual contrast
model (Vorobyev and Osorio, 1998; Vorobyev et al., 2001) was used to
investigate whether green or brown colormorphs of T. carolinense are
more advantageous for crypsis when viewed by fish predators under
natural illumination conditions against three common seagrass
species as backgrounds: S. filiforme, T. testudinum, and H. wrightii.
The potential predators viewing T. carolinense in the model represent
fish species with different visual systems; Cynoscion nebulosus vision
is dichromatic with two visual pigments, while vision in Sciaenops
ocellatus is trichromatic with three visual pigments (Horodysky et al.,
2008). It was expected that T. carolinense colormorphs would vary in
their degree of crypsis when viewed against different seagrass
backgrounds by these two fish species. Furthermore, if crypsis aids
in T. carolinense predator avoidance, these differences were expected
to effectively predict colormorph distribution in seagrass habitats,
assessed by sampling T. carolinense abundance in monospecific
patches of seagrass in Tampa Bay, Florida (USA).
2. Materials and methods
A chromatic discrimination model was used to calculate the
distance in receptor space between a visual target (T. carolinense) and
a background (live and dead seagrass, S. filiforme, T. testudinum, and
H. wrightii) as seen by a predator (C. nebulosus or S. ocellatus). In the
model, greater distance in receptor space between the visual target
and background yields greater visual contrast for the observer (i.e. the
predatory fish) (Vorobyev and Brandt, 1997). This model operates
under the assumptions that visual performance is limited by receptor
noise, color is coded by opponent mechanisms, and mechanisms are
insensitive to changes in light intensity. These assumptions have all
been made previously for visual contrast models in marine fish (e.g.
Letteiri et al., 2009).
2.1. Model parameters
Model parameters include: (1) the environmental light spectrum,
(2) spectral reflectance of shrimp as visual targets, and (3) the
receptor spectral sensitivities of fish as observers (Vorobyev and
Osorio, 1998; Vorobyev et al., 2001; Kelber et al., 2003). To quantify
the spectrum of environmental light available to illuminate shrimp in
seagrass habitats, irradiance was measured in an S. filiforme seagrass
bed in Boca Ciega Bay (FL, USA; 27° 42′ N, 82° 41′ W). Irradiance
spectra at 1 m depth were collected using a USB2000 fiber-optic
spectrometer fitted with a 600 μm UV/VIS optical fiber with CC-3
cosine corrector positioned orthogonal to the water surface, and
stored with SpectraSuite software (Ocean Optics, Dunedin, FL, USA).
Irradiance spectra under full sun were measured on January 14, 2010
and May 18, 2010 at 09:00, 12:00, and 15:00, which corresponded to
ebb, low, and flood tides on both days. These spectra (400–750 nm)
were averaged, yielding a single spectrum to capture temporal and
tidal differences in environmental light under sunny conditions at this
location. Dawn and dusk spectra were measured at 06:00 and 20:00
on May 17 and 18, 2010. These twilight spectra were averaged and
modeled separately, as light during this time of day is increasingly
attenuated at wavelengths from 540 to 640 nm, and this is a period of
heightened feeding activity in nearshore fish (e.g. Hobson et al.,
1981).
For spectral reflectance measurements, T. carolinense and seagrass
were collected during January 2010 from Boca Ciega Bay (FL, USA)
near the light measurement site described above. Specimens were
kept in aerated, ambient seawater and all reflectance measurements
were made within 48h of specimen collection; no change in the extent
or quality of coloration in either shrimp or seagrass was qualitatively
observed over that time. Diffuse spectral reflectance (400–750 nm)
was measured using a USB2000 fiber-optic spectrometer fitted with a
600 μm UV/VIS optical fiber mounted on the phototube of a
compound microscope. Magnification was 400×, and illumination
was provided at ~ 45° by a Dolan Jenner FiberLite DC-950 voltage-
regulated illuminator with a bifurcated light guide. A strip of white
Teflon tape mounted on a glass slide yielded a reflectance value of
100% at all wavelengths and served as a diffuse white standard.
 B.L. Cournoyer, J.H. Cohen / Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34 29

Colormorph spectral reflectance was measured along the strip of A

pigment between the third and fourth abdominal segments. Mea-
surements were taken when the animal occupied at least 75% of the
ocular field of view, ensuring that the pigmented region encompassed
the entire field of view of the optical fiber. Similar spectral reflectance
measurements were made for live and dead seagrass (S. filiforme,
T. testudinum, and H. wrightii). Live samples appeared green and
healthy, whereas dead blades were light to dark brown in color. All
seagrass were securely anchored into the sediment at the time of
collection. All spectral reflectance data were collected at 0.3 nm
resolution, smoothed by subsampling at 1 nm, and then by moving
averages at 3 nm prior to averaging replicate reflectance spectra for
use in model calculations (n = 7 colormorph spectra, n = 10 seagrass
spectra).
Two predatory fish, C. nebulosus and S. ocellatus, were selected as
model predators for determining the effectiveness of T. carolinense
cryptic coloration. These species were chosen because they commonly
B
inhabit seagrass communities and prey upon shrimp and other small
crustaceans during portions of their life history (Hetter, 1989; Rooker
et al., 1998; Scharf, 2000). Additionally, photoreceptor spectral class
data are required for the model, and Horodysky et al. (2008)
determined the visual spectral sensitivity of both species using
electroretinography, reporting C. nebulosus to be a dichromat with
λmax values at 450 and 542 nm, while S. ocellatus is a trichromat with
λmax values at 444, 489, and 564 nm. For the receptor sensitivity
parameter in the model, a template for A1-based visual pigment
absorbance (Govardovskii et al., 2000) was used to generate a
sensitivity spectrum based on predicted λmax values and associated
weighting proportions from Horodysky et al. (2008) (Fig. 1A and B).

2.2. Model calculations

C
The quantum catch of each receptor type (qi) was calculated over
the wavelength range 400–750 nm independently for shrimp color-
morphs serving as visual targets and seagrass species serving as visual
backgrounds. Quantum catch was calculated as the integrated product
of the receptor spectral sensitivity (Ri), spectral reflectance of the
target (S), and the environmental light spectrum (I) (Eq. (1)). Color
constancy under varying illumination conditions is incorporated as a
scaling factor into quantum catch calculations using a receptor-
specific von Kries adaptation coefficient (ki) (Eq. (2)), that has been
used previously in chromatic discrimination models for a variety of
animals, including marine fish (Kelber et al., 2003; Marshall and
Vorobyev, 2003; Letteiri et al., 2009).

qi = ki ∫Ri ðλÞSðλÞIðλÞdλ
ki = 1 = ∫Ri ðλÞIðλÞdλ
The contrast between a given shrimp colormorph and its seagrass
background was calculated for each fish receptor type (Δƒi) as the
natural logarithm of the quotient of these quantum catches (Eq. (3)).
Δƒi = ln½qi ðshrimpÞ = qi ðseagrassÞ
The discrimination value (ΔS) was calculated as the contrast
between receptor types (Eqs. (4) and (5)). An assumption of the
model is that detection thresholds are set by receptor noise in
accordance with Weber's Law, which is accounted for by calculating
the noise value (wi) for each receptor class (Vorobyev and Osorio,
1998). The proportion of receptors and Weber fractions of each
receptor class are unknown for both species of predatory fish
considered in the present study, therefore the noise values were
estimated using approximate Weber fractions (vi) of each receptor
class and approximate receptor proportions (e.g. Matz et al., 2006;
ð1Þ Fig. 1. Predatory fish receptor sensitivity and environmental light in seagrass habitats.
(A) Receptor sensitivities for dichromatic C. nebulosus used in model calculations.
Alpha-band of A1-based visual pigment absorbance spectra were calculated after
ð2Þ Govardovskii et al. (2000) using predicted visual pigment λmax (450 and 542 nm) and
weighting factors (1.00 and 0.69) determined electrophysiologically by Horodysky
et al. (2008). (B) Receptor sensitivities for trichromatic S. ocellatus used in model
calculations, as described for (A), using predicted visual pigment λmax (444, 489 and
564 nm) and weighting factors (0.76, 1.00 and 0.69). (C) Normalized quantal flux
measured at 1 m depth in a seagrass bed (Syringodium filiforme) in Boca Ciega Bay (FL,
USA). Average day (solid line) represents the average of spectra (n = 6) measured at
09:00, 12:00, and 15:00 on 14 Jan 2010 and 18 May 2010. Dawn/dusk (dotted line)
ð3Þ
represents the average of spectra (n = 4) measured at 06:00 and 20:00 on 17 May 2010
and 18 May 2010.
Letteiri et al., 2009). It was assumed that the Weber fraction of the
long wavelength receptor in both C. nebulosus and S. ocellatus is
approximately 0.05, and the individual proportion of short (S),
medium (M), and long (L) receptors within the retina are 1:2 (S:L)
for dichromatic C. nebulosus, and 1:2:2 (S:M:L) for trichromatic
S. ocellatus (e.g. Letteiri et al., 2009). If these approximations are
incorrect, the discrimination values would be affected. However, the
relationships among the comparisons would not be altered, and the
30 B.L. Cournoyer, J.H. Cohen / Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34

relative relationships between colormorphs and backgrounds rather A

than exact discrimination values are the most reliable and most
interesting ecologically (Matz et al., 2006). Discrimination value
equations (Eqs. (4) and (5)) differ based on the number of receptor
types present in the predatory fish.
Dichromatic C. nebulosus:
h i
2 2 2 2
ΔS = ðΔƒS −ΔƒL Þ = wS + wL ð4Þ

Trichromatic S. ocellatus:
h i
2 2 2 2 2 2 2
ΔS = wS ðΔƒL −ΔƒM Þ + wM ðΔƒL −ΔƒS Þ + wL ðΔƒS −ΔƒM Þ ð5Þ
h i
2 2 2
= ðwS wM Þ + ðwS wL Þ + ðwM wL Þ B

The discrimination values estimate contrast of a shrimp color-

morph as viewed by a predatory fish against a seagrass background
under environmental light. The unit for this measure of contrast is
‘jnd’ (just noticeable difference). Although 1 jnd is the threshold for
detection, Siddiqi et al. (2004) estimated that any signal below
≈ 4 jnd is likely difficult to see. Model results were compared
statistically using two-way ANOVAs for each predatory fish, with
shrimp colormorph and seagrass background type as the main effects.

2.3. Field study

A survey of T. carolinense colormorph abundance in live seagrass C

was performed in Tampa Bay, FL (USA) during May and June 2010.
Sample sites were seagrass beds in three locations (Boca Ciega Bay, Ft.
DeSoto, and Fergie Shoal) in lower Tampa Bay, with each site
containing large, monospecific patches of live seagrass (S. filiforme,
T. testudinum, and H. wrightii). Ten replicate 1 m2 areas were sampled
within each grass type using a dip net swept through the seagrass. All
grass blades present in the sample were manually inspected for
shrimp by running the blade between the thumb and index fingers.
The number of each colormorph (green and brown) was quantified in
each sample, and averaged across sites for all samples collected within
each monospecific seagrass habitat (n = 30 samples per seagrass
species).
3. Results
3.1. Model parameters
The average daytime downwelling light spectrum in an S. filiforme
bed had a broad peak at green/yellow wavelengths (550–582 nm;
Fig. 1C). The twilight (dawn/dusk) spectrum differed from the daytime
spectrum, with less light below 460 nm and above 680 nm. A
pronounced increase in light was observed at blue/green wavelengths
between 460 and 545 nm, and loss of light at green/yellow wavelengths
between 550 and 630 nm (Fig. 1C). Both average daytime and twilight
spectra were used in initial model calculations, and resulting contrast
values were nearly identical. Accordingly, only model results using the
average daytime environmental light spectrum are provided below.
Reflectance values of live seagrass were similar among the three
species measured. All spectra were relatively constant between 400 and
500 nm, rising to peaks centered between 552 and 556 nm, and
gradually reaching a minimum ~680 nm before sharply rising at longer
wavelengths (Fig. 2A). Maximum reflectance at the peaks relative to a
100% reflectance standard ranged from 10% in T. testudinum to 17% in
H. wrightii, with reflectance values reaching ~30% by 700–710 nm
(Fig. 2A). Spectral reflectance of dead seagrass was also similar among
species, and differed from live seagrass blades. Spectra again were
relatively constant between 400 and 500 nm, rising less sharply with
wavelength to a broad peak ~650 nm before falling to a minimum
Fig. 2. Spectral reflectance of seagrass and shrimp. All spectral reflectance measure-
ments are shown as percentage reflectance relative to a Teflon tape standard that
reflected at 100% across all wavelengths. (A) Live seagrass. Mean spectral reflectance of
ten replicate samples was used in model calculations: Halodule wrightii (solid line),
Thalassia testudinum (dotted line), and Syringodium filiforme (dashed line). (B) Dead
seagrass. Mean spectral reflectance of ten replicate samples plotted as described for (A).
(C) Tozeuma carolinense colormorphs. Mean spectral reflectance of seven replicate
shrimp for each colormorph: green (solid line) and brown (dotted line). Reflectance
spectra of individual shrimp were used in model calculations.
~670 nm then rising at longer wavelengths (Fig. 2B). Reflectance ranged
between 7% in dead S. filiforme and 11% in dead H. wrightii, reaching
~30% between 730 and 750 nm (Fig. 2B).
T. carolinense green and brown colormorph reflectance spectra
were similar to live and dead seagrass, respectively (Fig. 2C). Green
morphs have a maximum reflectance of ~ 14% at a peak centered
between 530 and 545 nm, decreasing to ~ 9% at 650 nm, and
increasing at longer wavelengths to 17.5% at 750 nm. Spectral
reflectance of brown morphs was lower overall, gradually increasing
to ~ 5.5% between 580 and 590 nm, with an increase N675 nm
reaching 11% by 750 nm (Fig. 2C).
3.2. Model output
The chromatic discrimination model used the spectral reflectance of
shrimp visual targets on seagrass backgrounds under environmental
light spectra within seagrass habitats as viewed by weighted
 B.L. Cournoyer, J.H. Cohen / Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34 31

photoreceptor spectral sensitivity of fish predators in order to calculate
chromatic discrimination values in units of contrast (jnd). The model
produced a wide range of discrimination values for each colormorph
(Fig. 3). Both the lowest and highest values were observed for the
dichromat (C. nebulosus) for which green T. carolinense morphs ranged
from 0.99 ± 0.24 jnd (mean ± SE) on live H. wrightii, to 6.40 ± 0.23 jnd
on live T. testudinum. Similarly, brown morphs ranged from 1.27 ±
0.34 jnd on dead T. testudinum, to 9.05 ± 0.60 jnd on live T. testudinum
as seen by the dichromat. Overall, discrimination values for both
C. nebulosus and the trichromatic predator S. ocellatus were similar, with
significant differences observed for each fish viewing T. carolinense
colormorphs within the seagrass types (p b 0.001, two-way ANOVAs)
(Fig. 3). For both predators, green morphs produced significantly lower
contrast than brown morphs on live seagrass backgrounds (p b 0.001,
Tukey Test) (Fig. 3). However, on dead seagrass backgrounds brown
morphs produced significantly lower contrast than green morphs on
H. wrightii (p b 0.001, Tukey Test) for both the dichromatic and
trichromatic fish, whereas no difference in contrast was found between
green and brown morphs on dead T. testudinum for either predator
(p = 0.103, p = 0.898, Tukey Test) (Fig. 3). Brown morphs did have
lower contrast on dead S. filiforme for dichromatic C. nebulosus, but not
for trichromatic S. ocellatus (p b 0.01, p = 0.066, Tukey Test) (Fig. 3).
When comparing contrast values within each colormorph for
dichromatic C. nebulosus, green morphs produced contrast values at or
below 4 jnd on all seagrass backgrounds except live T. testudinum and
dead H. wrightii (Fig. 3A). For green morphs viewed by the dichromat,
contrast was lowest when viewed against live H. wrightii, live
S. filiforme, and dead T. testudinum (Table 1). In this scenario, contrast
did not differ between live and dead S. filiforme, but increased
significantly from live to dead H. wrightii, and decreased significantly
from live to dead T. testudinum; no difference was observed between
live and dead S. filiforme (Table 1). For brown morphs viewed by the
dichromat, contrast values were below 4 jnd on all backgrounds
except live T. testudinum and S. filiforme (Fig. 3A). Contrast was equally
low on dead specimens of each seagrass species, and was significantly
higher in live versus dead seagrass for each species (Table 1).
For contrast values within each colormorph viewed by the
trichromatic S. ocellatus, the general patterns described above for the
dichromat apply. However, contrast decreased to below 4 jnd for green
morphs on dead H. wrightii (Fig. 3B). Similarly, contrast for green
morphs on dead S. filiforme when viewed by the trichromat was reduced
relative to the dichromat such that the lowest contrast values for green
morphs viewed by the trichromat were against live H. wrightii , live
S. filiforme, dead T. testudinum, and dead S. filiforme (Table 2). Contrast

Fig. 3. Chromatic contrast of shrimp on seagrass backgrounds as viewed by predatory fish. (A) Discrimination values for a dichromatic fish, Cynoscion nebulous. Discrimination values
are shown as contrast in ‘just noticeable difference’ units (jnd) for green (open bars) and brown (gray bars) T. carolinense morphs viewed against live and dead seagrass backgrounds
(Halodule wrightii, Thalassia testudinum, and Syringodium filiforme). (B) Discrimination values for a trichromatic fish, Sciaenops ocellatus. Data are plotted as described for (A).
Asterisks indicate p-values (Tukey Test following two-way ANOVA for each fish) for comparisons between T. carolinense green and brown morphs within each seagrass background:
n.s. = p N 0.05, ** = p ≤ 0.01, *** = p ≤ 0.001.
32 B.L. Cournoyer, J.H. Cohen / Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34

Table 1
Tukey multiple comparisons for dichromatic fish (C. nebulosus) model discrimination values. P-values are provided for comparisons between live and dead seagrass types
(Syringodium, Thalassia and Halodule) within each T. carolinense color morph (green and brown). Asterisks denote significant differences: * = p b 0.05, ** = p ≤ 0.01 and
*** = p ≤ 0.001; exact p-values are provided if p-value N0.05; dash (―) indicates p-value for comparison is elsewhere in the matrix.

Live seagrass Dead seagrass

Syringodium Thalassia Halodule Syringodium Thalassia Halodule

Green morphs
Live seagrass Syringodium ― ― ― ― ― ―
Thalassia *** ― ― ― ― ―
Halodule 0.151 *** ― ― ― ―
Dead seagrass Syringodium 0.775 *** ** ― ― ―
Thalassia 1.000 *** 0.273 0.586 ― ―
Halodule * *** *** 0.339 ** ―
Brown morphs
Live seagrass Syringodium ― ― ― ― ― ―
Thalassia *** ― ― ― ― ―
Halodule 0.151 *** ― ― ― ―
Dead seagrass Syringodium *** *** ** ― ― ―
Thalassia *** *** *** 1.000 ― ―
Halodule *** *** * 0.994 0.969 ―

values of brown morphs as viewed by the trichromat were similar to the
dichromat (Fig. 3, Table 2).
3.3. Field study
The three locations sampled were monospecific beds composed
mostly of live seagrass. T. carolinense were found only in S. filiforme; no
shrimp were found in H. wrightii or T. testudinum. In S. filiforme, green
morphs significantly outnumbered brown morphs, with 31 ± 5 green
morph shrimp m−2 and 3 ± 1 brown morph shrimp m−2 (p b 0.001,
Mann–Whitney Rank Sum Test).
4. Discussion
Fish predation on cryptic shrimp species in seagrass habitats has
been shown to be a function of prey accessibility, not preference, with
vision playing a substantial role in prey detection (Main, 1985,
Luczkovich, 1988). Behavioral adaptations in T. carolinense to enhance
crypsis and avoid visual detection have been well documented and
contribute to its under-representation in the diets of predatory fish
species (Main, 1985, 1987). However, the effectiveness of cryptic
coloration as an antipredation strategy in T. carolinense is less clearly
established. In the present study we hypothesized that brown and
green colormorphs of T. carolinense differ in their degree of crypsis on
varying natural seagrass backgrounds as viewed by two potential
predatory fish. Results from the receptor noise limited contrast model
indicate that shrimp colormorphs do differ in cryptic ability against
fish visual detection, with green morphs being significantly more
cryptic on live seagrass backgrounds, while brown morphs are more
cryptic on dead backgrounds.
The light data collected within an S. filiforme bed used as the model
illuminant was spectrally similar to coastal light measurements made
by Marshall et al. (2003). Seasonal spectral differences were minimal,
while daytime and dawn/dusk spectra differed with a loss of yellow
wavelengths at twilight consistent with the Chappuis Effect (e.g.
Forward, 1988). This change in spectral composition had little effect
on contrast for either predator viewing T. carolinense against seagrass.
This could be due to differences in spectral reflectance between
shrimp colormorphs being greatest at wavelengths b550 nm, while
those wavelengths most altered at twilight were longer (540–
640 nm). Any differences in seagrass spectral reflectance at yellow
wavelengths were also not sufficient to affect model contrast.
Accordingly, visual crypsis of T. carolinense colormorphs appears
robust to diel spectral changes, which would aid in protecting shrimp
from fish feeding both at twilight and midday, as has been observed in
juvenile sciaenids (Waggy et al., 2007).
If visual crypsis is the sole mechanism used by T. carolinense for
habitat selection, and the visual systems of C. nebulosus and S. ocellatus
are representative of its suite of visual predators (but see discussion
below), then green morphs should be found on both H. wrightii and
S. filiforme, as they had the lowest contrast among live seagrass types.
Consistent with this expectation, shrimp were absent from T. testudinum

Table 2
Tukey multiple comparisons for trichromatic fish (S. ocellatus) model discrimination values. P-values are provided for comparisons between live and dead seagrass types
(Syringodium, Thalassia and Halodule) within each T. carolinense color morph (green and brown). Asterisks denote significant differences: * = p b 0.05, ** = p ≤ 0.01 and
*** = p ≤ 0.001; exact p-values are provided if p-value N0.05; dash (―) indicates p-value for comparison is elsewhere in the matrix.

Live seagrass Dead seagrass

Syringodium Thalassia Halodule Syringodium Thalassia Halodule

Green morphs
Live seagrass Syringodium ― ― ― ― ― ―
Thalassia *** ― ― ― ― ―
Halodule 0.497 *** ― ― ― ―
Dead seagrass Syringodium 0.999 *** 0.282 ― ― ―
Thalassia 0.929 *** 0.966 0.767 ― ―
Halodule 0.140 *** *** 0.289 * ―
Brown morphs
Live seagrass Syringodium ― ― ― ― ― ―
Thalassia *** ― ― ― ― ―
Halodule 0.246 *** ― ― ― ―
Dead seagrass Syringodium *** *** ** ― ― ―
Thalassia *** *** * 0.999 ― ―
Halodule *** *** * 0.999 1.000 ―
 B.L. Cournoyer, J.H. Cohen / Journal of Experimental Marine Biology and Ecology 402 (2011) 27–34
patches; contrast values for both green and brown morph shrimp on
T. testudinum were the highest calculated in the study and well in excess
of the 4 jnd criterion value found in previous studies to be an upper limit
for discrimination (e.g. Siddiqi et al., 2004). Additionally, T. testudinum
blades are the widest of the seagrass species studied, which may be
harder for small invertebrates to grasp and perform antipredatory
behaviors, such as the ‘hide behind the blade’ technique of T. carolinense
(Lewis, 1984; Main, 1987). This result is also supported by Ewald (1969)
who noted that T. carolinense was rare in monospecific beds of
T. testudinum.
Interestingly, all T. carolinense at the three field sites in Tampa Bay
were found in S. filiforme, with none in H. wrightii. Structural
differences between the two grasses could influence T. carolinense
distribution. S. filiforme grows taller and has more robust blades than
H. wrightii, making it more structurally complex and therefore a more
protective habitat (Lewis, 1984; Orth and Heck, 1984; Heck et al.,
2003). However, visual crypsis may also play a role in T. carolinense
favoring S. filiforme habitat. The majority of grass blades in each
seagrass bed were living, and green colormorphs highly outnumbered
brown in field collections, which fits with the lower contrast values
for green colormorphs on live seagrass. Of the seagrass species tested,
only in S. filiforme were contrast values of green morphs similar
between live and dead grasses. This seagrass species is therefore the
most predictable habitat for green morphs, with crypsis against live
blades coupled with some degree of visual protection in areas of the
seagrass bed containing dead blades.
Some brown morphs were also present in S. filiforme, and with
model contrast values in excess of 4 jnd should be visually
conspicuous to fish predators. As T. carolinense displays both
behavioral and morphological cryptic strategies, each must signifi-
cantly reduce predation if they are to be maintained by the species
(e.g. Hultgren and Stachowicz, 2007). Although a green morph
behaving on a live blade or brown morph behaving on a dead blade
would almost certainly minimize the threat of detection, its behavior
alone is likely cryptic enough for a small proportion of brown morphs to
survive on live backgrounds. It is also possible that brown morphs were
on the few dead blades in each sampling area upon collection, which
would not be evident from the sampling technique. In organisms with
multiple cryptic adaptations, as is the case with T. carolinense, no one
adaptation is solely responsible for predator evasion. Rather, the
adaptations complement each other to maximize cryptic success (e.g.
Endler, 2006; Schaefer and Stobbe, 2006; Stevens et al., 2006). The
comprehensive cryptic strategy of T. carolinense becomes more robust
when its coloration and behavior are taken into account.
A chromatic visual system transduces visual signals based on
opponent mechanisms, or the relative differences between receptor
signals (Vorobyev and Brandt, 1997). By this logic dichromatic systems
should produce higher contrast as the relative differences between
receptor signals are greater between two receptors than among three,
given the same sensitivity range. This is supported by Morgan et al.
(1992) who showed that in humans, dichromatism is better suited for
breaking textural and color camouflage than trichromatism. We
expected a similar trend in predatory fish, yet contrast differences
between dichromatic (C. nebulosus) and trichromatic (S. ocellatus)
predators were very small over all habitats and backgrounds. While
these predatory fish differ in terms of visual spectral sensitivity, they are
functionally very similar in their lunging predation strategy. Ambush
predators such as Syngnathids (pipefish and sea horses) that prey upon
T. carolinense (e.g. Main, 1985) are more efficient predators in complex
seagrass habitats than are lunging fish like the sciaenids used in the
present study (e.g. Flynn and Ritz, 1999). Visual spectral sensitivity data
are not available for Syngnathid species sympatric to T. carolinense.
Visual pigments have been identified in several Australian Syngnathid
species, and suggest these fish possess long wavelength shifted visual
pigments with better color discrimination at green and yellow
wavelengths than either C. nebulosus or S. ocellatus (Mosk et al., 2007).
33
Future physiological, modeling, and behavioral work on Syngnathid/
shrimp visual interactions is warranted.
Although Main (1987) did not find an effect of shrimp coloration
in response to fish predation in laboratory experiments, we have
shown that a colormorph has a distinct cryptic advantage if its color
corresponds to that of the seagrass blade to which it is clinging, and
abundance of T. carolinense colormorphs in a natural population
corresponds fairly well to predicted distributions based on visual
contrast. However, distribution based on cryptic coloration alone is not
always observed. As cryptic adaptations are costly and must increase
survival if they are to be maintained (Hultgren and Stachowicz, 2007),
behavioral tactics alone likely produce enough protection for a small
portion of the population to survive in less than ideal conditions. While
cryptic coloration is not the only predator evasion strategy used by
T. carolinense, both model and field evidence indicate colormorphs have
the highest degree of crypsis on complementary colored backgrounds
and that cryptic coloration alone can be an effective solution for seagrass
invertebrates when avoiding predation by fish.
Acknowledgements
We thank K. Barr, E. Brucks, and B. Tate for aiding in field collections,
and L. Letteiri for helpful discussions. [SS]
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