Crypsis in the Pelagic Environment

Author(s): Margaret J. McFall-Ngai

Source: American Zoologist , 1990, Vol. 30, No. 1 (1990), pp. 175-188
Published by: Oxford University Press

Stable URL: https://www.jstor.org/stable/3883433

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Amer. Zool., 30:175-188 (1990)

Crypsis in the Pelagic Environment1

MargaretJ. McFall-Ngai
Department of Biological Sciences, University of Southern California,
Los Angeles, California 90089-0371

Synopsis. Pelagic aquatic environments differ from terrestrial environments in being

three-dimensional and relatively homogeneous, rather than two-dimensional and heter-
ogeneous. The present paper examines the causes and consequences of these differences
in the context of their influence on the interactions of animals with environmental light.
Particular emphasis is placed on light as a determinant of effective modes of crypsis in
the two different habitats. The terrestrial world has selected for the expression of crypticity
in the form of superficial color patterns. The heterogeneity of this habitat has resulted
in evolutionary divergence of these superficial color patterns, often in very closely-related
animals. In contrast, in the homogeneous pelagic aquatic habitats, evolutionary convergence
on three main forms of crypsis is evident: (1) transparency; (2) reflection of most, if not
all visible wavelengths; and, (3) ventral bioluminescence as counterillumination; thus, to
be cryptic most animals in these habitats use one or a combination of these modalities to
variously transmit, reflect or mimic environmental light. In the present paper, special
attention is given to transparency as the most prevalent, yet least understood, of these
mechanisms that are used in predator-prey interactions.

Introduction these animals, such a phenomenon can be

An examination of books and research considered a kind of "photomorphogene-
publications on animal coloration and sis," a term thus far only applied to plants.
crypsis reveals the absence of any serious In contrast, the whole body morphology
treatment of the vast aquatic pelagicofenvi? most terrestrial animals results primarily
ronment and the selection pressures from that selection pressures imposed by grav-
such an environment has imposed on ani? ity (Little, 1983; Hildebrand et al, 1985;
mals in terms of cryptic body form (Poul- Radinsky, 1987), and crypticity is usually
ton, 1890; Pycraft, 1925; Elton, 1939; only Cott,"skin deep." To develop these ideas
1957; Wickler, 1968; Edmunds, 1974; within the specific context of this sympo?
Owen, 1980). This omission is a reflection sium, I would like to: (1) contrast the eco-
of the limited extent to which we recog- logically relevant properties of light in the
nize, much less understand, the mecha? aquatic and terrestrial environments, and
nisms by which animals have becomethe role of these properties in the selection
cryptic within the three-dimensional, ho- of the different kinds of crypsis observed
mogeneous nearshore and oceanic envi? in the two environments; (2) discuss exam?
ronments. It should be clear, then, that an ples of convergent evolution in the three
important question to be addressed is this: most prevalent light dependent cryptic
How is crypsis achieved in the pelagic envi? mechanisms in the pelagic zone: biolu-
ronment and what are the antipredation minescence, reflectivity, and transparency;
strategies available to animals in this iso- and, 3) consider in depth the phenomenon
tropic (Hutchinson, 1961) environment? of transparency, the least understood yet
The present paper examines the concept probably the most significant of cryptic
that selection for crypticity in aquatic light mechanisms in aquatic habitats.
fields is a prime determinant of the whole
body morphology, and often the anatomy, The Quality of Light in the
of animals in the pelagic zones. Among Terrestrial and Aquatic Worlds
To understand trends in the relationship
between light and modes of animal crypsis
1 From the Symposium on Concepts of Adaptation in
in the pelagic portions of the ocean or the
Aquatic Animals: Deviations from the Terrestrial Paradigm
presented at the Annual Meeting of the American terrestrial world, we must first compare and
Society of Zoologists, 27-30 December 1988, at San contrast the nature of the quality of light
Francisco, California. that animals experience in the two envi-
175

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176 Margaret J. McFall-Ngai

location,
Table 1. Factors affecting light quality in that includeen?
different the light's inten?
vironments.
sity, color, angular distribution and polar-
ization. The features of the environment
that modulate these properties can be
divided into abiotic and biotic influences
(Table 1).
(1) Medium effects.?As sunlight passes
through the earth's atmosphere, it is atten-
uated through scattering by air molecules,
dust, water molecules, and through
absorbtion by dust, water vapor, ozone,
carbon dioxide and oxygen. Thus, the earth
is subject to two light sources, direct solar
radiation and diffuse hemispherical sky
* Stability of all factors as a function of time and
space.
light produced by scattering (McCartney,
1976). However, over the relatively short
distances of the terrestrial biosphere, the
magnitude of these processes is negligible,
ronments. Special attention is given to those
features that appear to directly influenceand the light quality is little changed. In
expression of differential cryptic patterns.contrast, water itself significantly influ?
ences the quality of environmental light
The depth of the habitats over very short distances (Jerlov, 1976;
A considerable difference exists in the Kirk, 1983; Wheeler and Neushul, 1981).
distance over which light travels through In pure water, light intensity decreases log-
the terrestrial and aquatic realms. Inarithmically
the with increasing distance from
the source and the spectrum is narrowed
terrestrial world, the biosphere is vertically
compressed upon the surface to a thin by absorbance of short, ultraviolet and long
veneer rarely more than 50 m deep. Only visible wavelengths ofthe spectrum, result?
birds and insects operate within the fluid ing in a predominance of blue light at
that is air, and generally only transiently.depth.
Under these circumstances, a major theme Light attenuation in the sea occurs over
of selection has been concerned with inter? considerable distances, creating a photoc-
actions ofthe organisms with the substrate, line divided into the euphotic, dysphotic
rather than with the fluid environment, and a aphotic zones, which are defined on
condition analogous to only the benthic the basis of light quantity (Marshall, 1980).
portions of the aquatic world. In contrast, The euphotic zone extends to a depth of
the aquatic environment in some places about 200 m in the clearest of oceanic
extends as deep as 11,000 m (Sverdrup et waters and is defined as that area where
al, 1942). A set of niches is created, that
there is sufficient light for net photosyn?
have no true analogue in the terrestrial thetic production. In the dysphotic zone
world, in which the organisms interact which extends from about 200 m down to
throughout their entire life history withinabout 1,000 m, some light is still present
the fluid environment, often miles away but it is insufficient for effective photosyn?
from the substrate. thesis. Here the quality of surface-derived
light is essentially predictable because its
Abiotic and biotic influences on intensity, spectral composition and angular
light quality distribution change in a regular way both
As it passes through the biosphere, light
diurnally and with the phases of the moon
will be variously transmitted, absorbed, (Jerlov, 1968). The aphotic zone, which
reflected or scattered (Campbell, 1981; encompasses the majority of the earth's
Kirk, 1983). The interplay of these pro? biosphere, extends from about 1,000 to
over 11,000 m, with an average depth of
cesses results in a set of ecologically rele?
vant properties characteristic of a given 4,000 m over the abyssal plains. In the

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 Crypsis in the Pelagic Environment 177

aphotic zone, surface-derived irradiation

restrial and nearshore aquatic worlds, pho?
has been completely attenuated, and exert
tosynthetic eucaryotes thethe most sig?
only ambient light is bioluminescent nificant potential in
and actual
ori? biotic effects
gin. on light quality. In tropical rain forests, the
(2) Dissolved substances and suspended par- light is attenuated by plant life often by
ticles in nearshore pelagic environments.? over 99% as it travels from the top of the
While the water itself may be the only or canopy to the forest floor (Chazdon and
most important determinant of light qual? Fetcher, 1984). While some ofthe green
ity in open ocean environments, nearshore light is reflected or transmitted (Loomis,
pelagic environments are influenced by a 1965; Smith, 1986), chlorophylls and
number of abiotic and biotic factors. One carotenoids of plants absorb much of the
ofthe most important abiotic factors isvisible the spectrum, except in the far red
presence of soluble and suspended, organic wavelengths (between 700 and 800 nm)
and inorganic, light-absorbing material (Smith,
in 1986).
In nearshore aquatic environments,
the medium (Jerlov, 1968, 1976). In the
terrestrial world, particles suspended in air are two distinct forms of plant life
there
(dust storms, volcanic ash, smog, etc.) that
are affect light processes in different ways:
both ephemeral in time and limited(1)inbenthic macroalgae (kelp) and sea-
space. This low density medium cannot
grasses, which are most often associated
support particulate material for protracted
with the substrate; and (2) phytoplankton
periods. In contrast, in nearshore pelagic(suspended unicellular algae). The presence
environments, the suspended particles, of kelp in the environment can reduce light
because of the viscosity and density of incidence
the on the benthos by 90% or more
aquatic medium, can persist for extended (Neushul, 1971; Reed and Foster, 1984),
periods of time. However, their geograph- but the effects of the water itself on the
ical extent may be quite variable and epi-spectral quality of the light often override
sodic, depending upon such factors as the the absorbance, transmission and reflec-
amount of terrestrial runoff, local wave tion by kelp fronds themselves. In contrast,
energy and the distance from shore. Thus, phytoplankton blooms are diffuse and can
the influence of these abiotic factors on reach densities at which they may affect not
light quality is also quite variable. only light intensity but also the color ofthe
(3) Bacterial blooms.?The biotic influ? light in much the same way as bacteria and
ences that are known to affect light quality suspended inorganic particulates can (Kie-
in nearshore areas include the presence of fer and Austin, 1974;Kirk, 1983; Atlas and
bacteria, photosynthetic eucaryotes (phy? Bannister, 1980).
toplankton, macroalgae, and seagrasses), Although the spatial distribution of pho?
and animals. Because bacteria require an tosynthetic organisms may affect light
aqueous medium in which to grow, bac? quality in both terrestrial and aquatic near?
terial blooms do not occur in air. However, shore environments, there is a major dif?
in freshwater and marine lakes (Truper and ference in the time scale over which plant
Genovese, 1968; Matsuyama and Shi- biomass persists in the two environments.
rouzu, 1978; Hamner et al, 1982), as well In much of the terrestrial world, the car?
as the surface film of the open ocean bon in plant material is stably fixed for
(Lapota et al, 1988), visibly dense popu? periods of tens to hundreds of years. Even
lations of bacteria can occur where nutrient
in the temperate zones, which experience
and physical conditions are favorable for seasonal fluctuations in the amount of
growth. These bacterial blooms can be sta? foliage, the patterns of carbon fixation ar
ble or stochastic, and in some cases have some ofthe most predictable of all pattern
been shown to affect the light transmit- in the biological world. In contrast, while
tance and spectral quality markedly (Ham? a kelp forest community also may persist
ner et al, 1982). for many years, the time scale of majo
(4) Photosynthetic eucaryotes: Consideration phytoplankton blooms often is on the orde
of time and space scales.?In both the ter- of days. Plankton blooms are an important

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178 Margaret J. McFall-Ngai

although unpredictable variable,

influencedepending
on on their abundance
the
andpelagic
light regime of nearshore distribution within any given area.
waters.
Nevertheless,
Under proper environmental where major terrestrial
conditions,
phytoplankton blooms can plants occur they are
typically stable and predictable
cover
in both time
hundreds of square kilometers toand
a space.
depth With the exception
of the Antarctic, both
of 10 m, appearing and disappearing benthic and pelagic
within
a period of a few days tonearshore
weeks areas experience
(Brink et a very wide
al, 1981; Kirk, 1983). variety of unpredictable influences on light
A notable exception to the
quality. transient and
often unpredictable plankton blooms ofthe
temperate zones are the The Influence of Lightsea?
predictable, Quality on
the Expression of Crypsis
sonal blooms of algae in the Antarctic sea
ice during austral spring (Lewis To understand how light quality w
and Weeks,
1970; Sullivan and Palmisano, 1981; Pal- influence crypticity, we must consider t
misano and Sullivan, 1983), a time when use of cryptic patterns within the conte
pack ice can cover 10% of the world's of predator-prey interactions. In Feder a
oceans (Ainley et al, 1986). Algae grow to Lauder's book Predator-Prey Relationshi
high density in the layers of ice that inter? (1986), Endler divides the successful pr
face with the water column. The sea ice dation event into five stages: 1) detectio
and its associated community form aby kind
the predator's sensory system; 2) ide
of firmament over the fluid environment tification ofthe cue as a potential prey item
3) approach; 4) subjugation; and, 5) con
affecting the intensity and spectral quality
of the light below (SooHoo et al, 1987;
sumption. In each one of these stages
Palmisano et al, 1987). Light is attenuated
variety of defense mechanisms have evolv
to such a degree at these times, with under-
in prey organisms to avert a successful p
ice irradiances usually less than 1 % of dation
the event. For visually orienting pred
ators, the characteristics of environment
surface (Sullivan et al, 1983), that certain
nonvertically migratory mesopelagic light regime will influence most signifi
cantly the detection, identification an
species occur in ice-covered surface waters
(Ainley et al, 1986). The seasonal patterns
approach stages. Crypsis is one of the be
of these areas are quite stable and pre? documented prey mechanisms for avo
dictable, and thus reminiscent of the ter?
ing detection by predators using visual cu
restrial temperate deciduous forests. This strategy works by reducing the sign
to-noise ratio of the prey's image in t
(5) The secondary effects of zooplankton graz-
ing.?Recently it has been demonstrated predator's visual field (Endler, 1986
by Huntley and co-workers (1987) that Within this context, Endler distinguishe
grazing zooplankton within the water col? two kinds of crypsis: 1) masquerade,
umn also can have an indirect but signifi?
which the animal resembles an object th
is not normally eaten; and 2) eucryps
cant effect on the light quality in the water
by influencing the density of phytoplank?where the animal resembles a random sam?
ton. Comparable effects exhibited by non-ple of the background in which it resides.
aquatic animals are rare and transitory
events (e.g., locust swarms). Crypsis in terrestrial and benthic
aquatic habitats
In summary, the terrestrial and open
ocean pelagic environments have in com?
As biologists we are well aware of the
mon that their light quality is affected variety
pri? of studies of animal crypsis that have
marily by a single component; however,been in reported from terrestrial and near?
the terrestrial world that component is benthic aquatic environments (Poul-
shore
plant abundance, while in the pelagic ocean
ton, 1890; Pycraft, 1925; Elton, 1939; Cott,
1957; Wickler, 1968; Edmunds, 1974;
it is the medium itself. Thus, the light qual?
ity in the open ocean is most influenced Owen,
by 1980; Endler, 1978, 1981, 1984;
a constant, intrinsic condition, while in Wicksten,
the 1983; Greene, 1989). Examples
terrestrial world, the influence of plantsof is
both masquerade and eucrypsis can be

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 Crypsis in the Pelagic Environment 179

found in both of these two habitats. Ani? ment, the three-dimensional, homoge?
mals in benthic nearshore habitats express neous pelagic world appears to have
similar strategies to those of terrestrial selected
ani? for the convergent evolution
mals; however, these benthic animals expe? among disparate phyla (from cnidarians to
rience a wide array of abiotic and biotic chordates and crustaceans) of three fun?
influences on light quality (Wicksten, 1983).
damental strategies of eucrypsis: transpar?
Thus, these compounding factors have
ency, reflectivity and luminescence. To
been integrated into the resulting selection
reduce the signal-to-noise ratio, the organ-
of cryptic body coloration. For example,ism's body form resembles a random sam?
because red light is filtered out with depth
ple of a homogeneous habitat by variously
in the water column, a red crustacean that
transmitting, reflecting, or mimicking the
would be conspicuous against its back? quality ofthe ambient photic environment
ground in air is a camouflaged shade of All three mechanisms are used by
itself.
gray in its natural environment. While
animals in the pelagic aquatic environ?
there is this difference in the variety ments
of (Marshall, 1971), resulting in mor-
phologies and behavior that rarely
influences, cryptic color patterns reflect the if
interaction of the animals with a solid sur? ever made the water-to-land transition.
face both on the land and in the nearshore Although the offshore and nearshore
benthos, and are divergent and variable pelagic environments differ in their pre-
because of the heterogeneity of the sub?dictability and stability, these strategies
stratum. Under these circumstances, diver?
often are possible in both environments
because they are a response to the photic
gence of color pattern among closely-related
species is not uncommon, and reflects dif? environment itself and not to the interac?
ferential attempts to either appear as some- of the animal with the substratum.
tion
thing inedible or match a random sample(2) Biogeographic trends in pelagic cryptic-
of their heterogeneous habitat. ity.?Patterns in the use of these three
modes of crypsis in any given animal are
Crypsis in the pelagic zone
related to 1) the biogeography ofthe species
Hamner and co-workers (1975) and Zaret and, 2) characteristics ofthe biology ofthe
(1975), studying marine and freshwater animal, such as size and life history strat?
systems, respectively, analyzed antipreda- egy. In clear oceanic waters, where the light
tory strategies in pelagic habitats. In both
quality is relatively predictable and stable,
environments, four types of antipredation certain biogeographic trends in the occur?
mechanisms were recognized: 1) time and rence of bioluminescence, reflectivity and
space (e.g., vertical migration); 2) body-size;
transparency are apparent (Fig. 1).
3) visibility; and, 4) behavior (e.g., school?a. The oceanic euphotic zone. Diurnally
ing). Of these categories, visibility is that
in the euphotic zone, transparency is the
strategy with which detection and, hence, dominant mechanism and all phyla have
crypsis is of greatest significance. transparent representatives. Reflectivity is
also a conspicuous mode in the euphotic
(1) Evolutionary and morphological conse?
quences.?There are two important and zone and is best exemplified by schooling
fishes. Often these fishes will be counter-
distinctive characteristics of cryptic adap?
tations in the isotropic, pelagic environ? shaded, with the dorsum dark and the ven-
ment. Firstly, convergent evolution of sim?trum light, to camouflage from above and
ilar cryptic mechanisms by phylogeneticallybelow. Because ambient light levels are so
different organisms is common, and sec- high in this portion of the ocean, the use
ondly, morphological adaptation often of bioluminescence is precluded during the
involves the entire anatomy, rather than day as a form of camouflage.
simply the adoption of superficial color? b. The oceanic dysphotic zone. The
ation patterns. As opposed to divergence
dysphotic zone is characterized by the
into a vast number of superficial cryptic
prevalence of bioluminescence as a cryptic
coloration patterns as in the two-dimen-
mechanism (Herring, 1978). Examples of
sional, heterogeneous terrestrial environ-
this kind of adaptation are particularly

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 180 Margaret J. McFall-Ngai

ency, reflectivity and luminescence, wh

use or mimic light in the environment,
not adaptive in this habitat.
Into this seemingly simple set of tre
100 is woven a number of other factors, suc
as diurnal photic cycle and life hist
X
h-
strategy of the individual. At night,
CL
UJ
photic quality ofthe upper waters is alte
Q
such that there is no longer a euphotic z
Under these circumstances, the use of b
1OO0 luminescence can be effective right up
the surface of the open ocean, and m
animals vertically migrate into these ar
at night (Vinogradov, 1968; Robiso
1972), effectively counterilluminati
against moonlight and starlight. Furth
Fig. 1. Relative importance of the major crypticity whether or not these traits are found within
modes characteristic of the pelagic zones of the open
a certain individual is a function of a num?
ocean. Capital letters signify dominance of a mode;
ber of organismal factors including life his?
lower case letters signify that such a mode is of lesser
importance. tory strategy. For instance, some fish species
have transparent larval stages that, upon
prevalent among midwater fishes, cepha- metamorphosis, become reflective, coun-
lopods and crustacea, all of which oftentershading members ofthe euphotic zone;
express their light as serial, ventral pho-
other species migrate down to the meso-
tophores. In these areas of the ocean,
pelagic zone to become bioluminescent
counterilluminating fishes (Greenwood,
ambient light quality is attenuated enough
1975). Another strategy, common among
and stable enough to have selected for the
larval fishes and small crustaceans, is to have
expression of ventral luminescence, which
is thought to be used to mimic downwelling
most parts of the body transparent, and to
light to camouflage the silhouette inmake
a reflective those portions where
behavior called counterillumination transparency cannot be maintained (e.g.,
(Clarke, 1963; McAllister, 1967). theCoun?enteric tract). Further, many lumines?
terillumination is considered analogous
cent to
systems are composed of photogenic
countershading. A number of studies tissue, on
either autogenic or bacterial, that is
the animals in this environment have complemented
shown by reflectors and transpar?
that their luminescence systems produce
ent lenses (Herring, 1978). These highly
complex luminescence systems often
light similar in color, angular distribution
involve
and intensity to that of light in the meso-large portions of the anatomy and
pelagic zone (Denton et al, 1972; morphology
Young, of the animal.
1977; Latz and Case, 1982). The anatomy
d. Nearshore pelagic environments.
While
of the predator visual systems in the trends in the use of transparency,
meso-
pelagic zone suggests that acuityreflectivity
is low and bioluminescence such as
those described above may occur in the
(Munk, 1966); thus, the serial photophores
open
might be perceived as one continuous ocean, in nearshore pelagic environ?
dif?
fuse glow against dim downwelling ments
envi?similar patterns are not so clearly
ronmental light. discernable. Transparency and reflectivity
c. The oceanic aphotic zone. In arethe
the primary modes of crypsis in these
waters,is
aphotic zone, where solar illumination while bioluminescence is compar-
absent, animals are most often black or red
atively rare. Where it does occur, camou-
(Marshall, 1971), colors that would mostluminescence in nearshore animals
flaging
effectively absorb point sources of(primarily
biolu- fishes and cephalopods) is often
minescent light produced by potential
characterized by an internal, bacterial light
organ. One striking example of this can be
predators. The cryptic modes of transpar-

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 Crypsis in the Pelagic Environment 181

found in leiognathid fishes, a predator/prey

response to group of interactions? 3)
approximately 25 species What do we know aboutper-
of nearshore the biochemical
ciforms. These fishes inhabit the shallow,
and developmental mechanisms by which
transparency
low visibility waters along coastlines is both
of theachieved and main?
tained? Biolumines?
Indo-West Pacific province.
cence produced by a single internal, bac?
terial light organ is used Transparency
in a wide as anvariety
aquatic-specific
characteristic
of behavioral displays, one of which is
counterillumination (McFall-Ngai
Probably the two most andimportant differ?
ences between
Dunlap, 1983). In these fishes much theofthe
aquatic and terrestrial
anatomy is recruited intoworlds
thethat counterillu?
would influence the expression
mination camouflaging mechanism.
of transparency are Light
1) refractive indices of
produced by the symbiotic air and bacteria
water, and 2) theinamount
a of inci-
circumesophageal light organ is reflected
dent ultraviolet light penetrating these two
off a silvery-surfaced gas bladder
different media.(McFall-
Because animals are largely
Ngai, 1983a) into nearly water,transparent
the refractive indices of their tissues
hypaxial musculature and could through pre-that of water
theoretically approach
itself (1.34 in
cisely oriented guanine platelets at 20?C;
theMaurice,
skin 1957), and,
(McFall-Ngai, 1983&). The thus,
systems work
be very different frominthat of air (1.00
concert to produce a ventral luminescent
at 20?C) (Jerlov, 1976). As light travels from
glow that camouflages thethefish from
surrounding below.
water into the aquatic ani?
The resultant ventral glow canthe
mal's tissue, be con?
incident angle would be
trolled at each level of the light
little organ
changed sys?
and, if there are no scatter?
tem, producing a variableing or absorbing
mottled elements, the animal
effect.
Such a display in these waters of transparent.
would appear variableThe significant
optical quality might bedifference in the refractive
considered anal- index of air and
ogous to the phenomenon the terrestrial animal's tissues creates an
of disruptive
coloration (Morin, 1983).
easily perceived outline, and is probably
the single most important factor that pre-
Transparency as a Cryptic cludes the achievement and use of trans?
Mechanism in Pelagic
parency in the morphology of most non-
Environments
aquatic animals.
Whereas differences in medium refrac?
Reviews on the subject of cryptic mech?
anisms rarely include coverage of pelagic
tive index produce an optical constraint,
animals, and when they do, they concen-
the damaging effects of ultraviolet light on
trate on bioluminescence and reflectivity.
biological systems (Ichihashi and Ramsay,
1976; is
Transparency as a cryptic mechanism Rothman and Setlow, 1979; Kantor
almost totally neglected, even though et al.,
it is1980) create a biochemical limita-
probably the dominant form of crypsis in the expression of transparency by
tion on
the aquatic environment and biosphere. terrestrial organisms. The general absence
For this reason, I believe it deserves of
special
transparency among nonaquatic animals
attention within the context of thismay sym?be considered indirect evidence of a
posium. limitation overcome in only a few excep-
There are three biologically relevant tional cases. A search of the literature
questions that I will review and explore: 1) reveals few examples in which the majority
What factors render cryptic transparency of the body of a terrestrial animal is trans?
speeific to the pelagic, aquatic environ? parent or nearly transparent, with some
ment; or stated from another viewpoint, indication that the transparency is used in
why is transparency not used extensively crypsis. In one instance, some species of
in the terrestrial environment as a cam?
the small glass frogs of the family Centro-
lenidae, which occur in the rainforests of
ouflaging mechanism? 2) What is the evi?
Central and South America, are often
dence that transparency is used by pelagic
organisms as a form of camouflagenearly in transparent (McDiarmid, 1975), but

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182 Margaret J. McFall-Ngai

only from a ventral view.species (such as certain

Dorsally, theseatherinid species)
frogs are pigmented (Schwalm with larvaeetthat are 1977).
al, at the water's surface
It is believed that the dorsal during pigmentation
times of high incident ultraviolet
and ventral transparency radiation work have in concert
distinct dorsal pigmentation
to provide effective camouflage and, under
in the experimental
frog's conditions, resist
environment. ultraviolet light damage (Moser, 1982).
The second example of terrestrial use ofThere have also been a number of stud?
transparency comes from a study of trop? ies of the effects of UV on freshwater and
ical rainforest butterflies. Papageorgis marine invertebrates. In freshwater cope-
(1975) found that assemblages of butter? pods, the presence of carotenoids has been
implicated as photoprotection against high
flies stratify by wing color in the Peruvian
rainforests. The various color patterns
energy solar irradiation (Hairston, 1976,
1978, 1979). Further, Jokiel (1980) showed
appear to be used by the butterflies to effect
crypsis during flight under the differing
that certain epifaunal species on coral reefs
occur only in shaded areas and are killed
light regimes from the top of the canopy
either when moved to sunlit areas on the
to the forest floor. This is also the only
example that appears in the literaturereefof or are experimentally exposed to UV-
terrestrial crypsis in three-dimensionalrich light fields. Species that occur in highly
space. The butterfly assemblage closest to
lit areas of the reef have protective pig?
mentation.
the forest floor is almost entirely transpar?
ent, camouflaging them within the large
patches of filtered light characteristic ofTransparency in predator-prey interactions
that portion of the rainforest. As with theNo organism is completely transparent,
glass frog, the butterflies are in an area and
of the degree of transparency among
greatly attenuated ambient sunlight. Fur- pelagic species varies over a wide range
thermore, while transparency in insect (Hamner, 1974; Chapman, 1976a, b; Greze,
wings is not uncommon, the analysis ofthe 1964a, b). In addition, the extent to which
color patterns of these butterflies appearsan increase in transparency translates into
to be the only really good study of insectsa significant advantage in predator-prey
interactions is difficult to ascertain. How?
where transparency statistically correlated
with predator avoidance. ever, as Hamner (1974) points out, any-
Although some ultraviolet light does thing that reduces the contrast and bright-
penetrate into water (Jerlov, 1976; Baker ness of the animal would make it more
and Smith, 1982), a good deal of it is fil?difficult to see and would, in the context
tered out within a few meters of the sur? of predator-prey interactions, be an adva
face, so that organisms living some distance
tage.
below the surface do not experience the
(1) Morphological and behavioral evi?
deleterious effects of high-energy irradia-
dence.?There are only a few examples in
tion. However, other evidence that the the literature that transparency is an
presence of ultraviolet light precludesimportant mode of crypsis in predator-prey
transparency comes from the studies of interactions. In analyses of aggressive mim-
marine fish larvae and invertebrates that icry in siphonophores, Purcell (1980)
occur in surface waters where UV irradia- describes two species that appear to use
tion can be substantial. Hunter etal. (1981)
transparency to enhance predatory suc?
showed that entirely transparent larvae, cess. The siphonophores Agalma okeni and
such as those ofthe anchovy, Engraulis mor-
Athorybia rosacea are highly transparent,
dax, do not survive well when experimen?
except for nematocyst batteries that mimic
tally exposed to ultraviolet light. These
the appearance of a copepod and a larval
findings are correlated with the fact that
fish, respectively. It is hypothesized that
the larval development of these fishes theiscopepod-mimics attract potential prey
restricted to months ofthe year when inci-
to the otherwise invisible siphonophores
dent solar irradiation is sub-maximal. Fish (Purcell, 1980; Mackie et al, 1987).

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 Crypsis in the Pelagic Environment 183

Observations of another siphonophore,

(2) Ecological correlates.?Direct evidence
the Mediterranean species Hippopodius
that hip-
prey visibility is important in preda?
tion in pelagic
popodus (Mackie and Mackie, 1967;environments
Bassot has been
etal, 1978), revealed reversible-blanching
obtained from studies of crustacean species
behavior. Upon stimulation, the
in freshwater lakesanimal
(Zaret, 1975; Kerfoot,
changes from almost completely 1980; Lazzaro,transpar?
1987). For many years,
ent to a milky white in 1-2 either see.
body size
If (Brooks and Dodson, 1965;
the ani?
mal is then left undisturbed, Brooks, transparency
1968) or behavior (Jacobs, 1965)
is restored in 15-30 min. The behavior is of the prey had been the focus of studies
effected by the control of the movement on cues used by fish predators. However,
of granules contained in the mesoglea. more recent analyses show that, at least in
When Hippopodius is transparent, these some species, the most important factor is
granules are punctate, and upon stimula? the overall visibility of the prey (Zaret,
tion, the granules disperse through1972; the Mellors, 1975; Zaret and Kerfoot,
mesoglear matrix, rendering the siphono? 1975; Confer et al, 1978). Zaret (1972)
phore visible. Although these studies compared
con- rates of predation on two daph-
centrated on the mechanism of the revers- nia morphs that are of the same size, but
ible blanching, Mackie hypothesized that which differ in visibility due to the absolute
transparency confers an advantage on the size of the eyespot. In laboratory experi?
siphonophore by making it invisible ments, to he offered these two morphs in dif?
fering mixtures to a known fish predator
potential prey, while the blanching creates
a large visible object that will be avoided
and found that the predator preferentially
by fishes and other animals that could selected the large-eyed morph in higher
potentially damage this delicate animal. proportion than would be predicted by
Morphological correlates for the use of their proportion in the mixture. Further,
transparency in predator-prey interactions
he changed the visibility of the small-eyed
can also be found among larval fishes.type A by feeding them India ink to create a
"super-eye" spot, which was now larger
wide variety of fishes are transparent dur?
than the eye of the naturally large-eyed
ing their pelagic larval and juvenile stages
(Breder, 1962; Meyer-Rochow, 1974; Las- type. Under these conditions, the preda?
ker, 1982). Upon metamorphosis onto the tors preferentially selected organisms with
two-dimensional environment of the reef, the artificially-produced super eye. These
the fish lose their transparency and assume
findings were supported by Zaret in a field
study in collaboration with Kerfoot (Zaret
coloration that renders them cryptic against
the substratum. One striking example and of Kerfoot, 1975), which showed that
this phenomenon occurs in the postlarval when predators are absent, average eye size
or "acronurus" stage of the acanthurid is always significantly larger. Further, Mel?
surgeonfishes (Randall, 1961; Thresher, lors (1975) investigated predation on daph-
1984). During this stage, which immedi? nia bearing ephippia, pigmented envelopes
on the dorsum containing resting eggs.
ately precedes settlement on the reef, indi?
viduals averaging roughly 20 to 25 mm areThese structures, produced in the Spring
virtually transparent except for their sil-
and Fall, go through a tanning process prior
very gut tract. Upon settlement, they to release from the maternal daphnia. Mel?
transform to a fully pigmented adult fishlors found that the more visible ephippial
within as little as 24 hr. While the bio? daphnia had higher predation rates than
chemical and structural mechanisms
non-ephippial individuals of the same
underlying this process are not species.
under? Because the ingested eggs survive
stood, the resulting phenomenon suggests
passage through the gut of the predators,
that transparency is a developmentally pro-
Mellors concluded that this system aids in
dispersal. Further, Confer et al. (1978)
grammed cryptic adaptation used specifi?
cally during the larval and postlarval stages
showed that daphnia with high concentra?
of these fishes.
tions of hemoglobin were more likely prey

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 184 MargaretJ. McFall-Ngai

which
Table 2. Ways by which animals it occurs
achieve may lend some
transparency. insight
(Table 2). These conditions have proven
Reduced chromophore content
High water content
to be a complex interrelationship of body
Low tissue complexity size, water content, tissue complexity, and
At least one dimension small the arrangement of the anatomical com?
Regular arrangement of components ponents ofthe system. High water content
is characteristic of the tissues of many
transparent cnidarians and ctenophores,
which can attain very large sizes. Much of
than transparent daphnia. These studies the body mass of a medusa is represented
by the mesoglea, a primarily acellular,
all show that, in at least some systems, zoo?
plankton predation is positively associated watery tissue. In measurements of trans?
with their relative degree of transparency. parency in these animals, Chapman (1976a,
b) found that the mesoglea transmits nearly
How is transparency achieved and all of the incident light and the very thin
maintainedf
layer of ectodermal cells that overlies the
Quanta within the spectral range of vis- mesoglea is where some light loss occurs.
ible light can only be efficiently absorbed However, more complex animals, with
by a few specialized biological molecules, more tissue types and without mesoglea,
such as carotenoids and chlorophylls. These cannot attain large size and transparency
molecules have extended pi-electron sys?simply by depending on the wateriness of
tems that promote electronic excitation their tissues. John Tyler Bonner's new
within the energy range of visible light book, The Evolution of Complexity by Means
(Needham, 1974). Most cell constituents, of Natural Selection (1988), includes esti?
such as nucleic acids, proteins, carbohy- mates ofthe number of cell types in organ?
drates and lipids, cannot themselves absorb isms from one, in unicellular animals, to
quanta in the visible wavelengths. Thus, about 55 in the squid and 120 in verte?
one way to reduce visibility is to limit the brates. It seems logical that the more com?
number of absorbing molecules or pig? plex the animal, the more different types
ments. However, transparency of a system of tissues must be adapted for specific func?
can also be compromised by the scattering tions, and the more difficult it would be to
of light. When the constituents of cells are achieve overall body transparency. One way
organized into more complex structures, to get around this problem is to be small
such as membranes and organelles, and in at least one dimension. The leptoceph-
these cells become organized into tissues, alus larvae of eels may have body lengths
scattering becomes significant. If a struc- and depths of up to several hundred mil-
turally complex or large animal is to attain limeters and achieve transparency by being
transparency, it must conquer this prob? leaf-like (i.e., small in width) (Meyer-
lem. The problem is further exacerbated Rochow, 1974). A great majority of the
because cell constituents and their orga?transparent species ofthe higher phyla are
nization are subject to perturbation by small in overall body size.
environmental stresses such as tempera? In addition to these mechanisms, trans?
ture and pressure. Therefore, the orga? parency can be achieved through the reg?
nization of such structures to achieve trans? ular arrangement of cellular components.
parency is also likely to be perturbed by The most notable cases of transparency
such stresses, and the adaptation to differ? occur in the dioptric apparati of the eye
ent environments must be not only bio? (the lens and cornea), which are thought
chemical (Hochachka and Somero, 1984), to achieve transparency in this manner (Cox
but also morphological. et al., 1970; Delaye and Tardieu, 1983).
Our understanding of how transparency Chapman (1976a, b) has suggested that cer?
is achieved and maintained is poor. How? tain transparent animals, such as chaeto-
ever, an analysis of those conditions under gnaths, may also have some precision in

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 Crypsis in the Pelagic Environment 185

the arrangement of tissue components to

promote transparency. TERRESTRIAL PELAGIC AQUATIC

Transparent animals, like all organisms,

must tolerate environmental and physio?
PHYSICAL CHARACTERISTICS
logical stress. The degree to which such
OF THE PHOTIC ENVIRONMENT

stresses may compromise transparency

2-D, 3-D,
heterogenous
itself is an area that has not homogenous
been explored.
However, a large body of literature does
long-term, transient,
predictable stochastic
exist indicating that animals in stressful
habitats have metabolic machinery that
BIOLOGICAL is
CONSEQUENCES
FOR CRYPTIC PATTERNS
adapted to work optimally under the set of
primarily primarily
environmental conditions that they expe?
divergent convergent
rience (Hochachka and Somero, 1984). As
transparency. bioluminescence.

ambient conditions move away from this and reflectivity

superficial whole body

preferred temperature/pressure range, only and superficial
biological molecules, particularly proteins, 'PHOTOMORPHOGENESIS'
will cease to function properly and, even-
Fig. 2. Summary of the physical differences in th
tually, denature and precipitate. Whereas
light quality in the terrestrial and aquatic realms, and
no data are available on how such processes
the biological consequences of these differences in th
would influence transparency
selection of of pelagic
crypticity.
animals, some data do exist on the influ?
ence of temperature on transparency in one
tissue: the vertebrate eye lens. In a recent, with the casual observations of many
yet unpublished study, we analyzed the marine biologists that transparent organ?
resistance of lenses and their constituent isms often become opaque just before
proteins to temperature stress (McFall-Ngai
death, strongly suggests that the transpar?
et al, in preparation). The study included
ency is maintained by active physiological
ingroups and outgroups within all the ver?
means.

tebrate classes, including organisms with

preferred body temperatures that ranged
from 2? to 39?C. Our results showed a CONCLUSIONS

strong positive correlation between both

Although crypsis has been a widely stud?
ied phenomenon in terrestrial and benthic
the retention of transparency ofthe whole
aquatic habitats, its involvement in pred?
lens and the solubility of its constituent
ator-prey interactions in the pelagic envi?
proteins, and the preferred body temper?
ature of the animal. Though much ronment
more is poorly understood. Intrinsic dif?
complex, the transparent bodies of pelagicferences exist between the expressions of
animals may be similarly adapted to acrypticcer? body form, because of the nature
tain range of environmental conditions. of the light environment experienced by
The loss of transparency as a result animals
of in these various habitats (Fig. 2).
physiological stress has been well docu- The light environment ofthe pelagic zones
mented in cataractogenesis of the verte? has selected for the convergent evolution
brate eye lens (Bloemendal, 1981). Whereasof transparency, reflection of all wave?
pelagic animals have been little studied lengths,
in and bioluminescence as crypticity
this regard, Hamner (1984) reports thestrategies
loss in a wide variety of pelagic phyla.
Of these modes, transparency is probably
of transparency in krill, Euphausia superba,
the most prevalent, yet least understood.
as a result of parasitism. Within all dense
schools of krill, he observed significant As a mode of crypsis, transparency differs
numbers of white individuals, which from most others by involving most, if not
showed clear signs of physiological stressall, of the anatomy and morphology of the
in swimming behavior and survivorship animal. Thus, to understand this mode of
upon capture. Such information, coupled crypsis, new approaches will be required to

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 186 Margaret J. McFall-Ngai

understand how it is achieved and main? mesopelagic organisms. Nature (London) 265:
1244-1246.
tained, developmentally as well as under a
Confer, J. L., G. L. Howick, M. H. Corzette, S.
variety of environmental stresses. Kramer, S. Fitzgibbon, and R. Landesberg. 1978
Visual predation by planktivores. Oikos 31:27
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Cox, J. L., R.
Ruby for critical reviews ofthe manuscript.
ham. 1970. The transparency ofthe mammalian
cornea. J. Physiol. 210:601-616.
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