Download Crypsis in the Pelagic Environment1 An examination of books and

AMER. ZOOL., 30:175-188 (1990)
Crypsis in the Pelagic Environment1
MARGARET J. 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 heterogeneous. 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.
these animals, such a phenomenon can be
considered
a kind of "photomorphogeneAn examination of books and research
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 pelagic envi- of most terrestrial animals results primarily
ronment and the selection pressures that from selection pressures imposed by gravsuch 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; Cott, only "skin deep." To develop these ideas
1957; Wickler, 1968; Edmunds, 1974; within the specific context of this sympoOwen, 1980). This omission is a reflection sium, I would like to: (1) contrast the ecoof 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 become the 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 examronments. 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: bioluronment and what are the antipredation minescence, reflectivity, and transparency;
strategies available to animals in this iso- and, 3) consider in depth the phenomenon
of transparency, the least understood yet
tropic (Hutchinson, 1961) environment?
probably the most significant of cryptic
The present paper examines the concept mechanisms in aquatic habitats.
that selection for crypticity in aquatic light
fields is a prime determinant of the whole
THE QUALITY OF LIGHT IN THE
body morphology, and often the anatomy,
TERRESTRIAL AND AQUATIC WORLDS
of animals in the pelagic zones. Among
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
Aauatic Animals: Deviationsfrom 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 enviINTRODUCTION
175
176
TABLE 1.
MARGARET J. MCFALL-NGAI
Factors affecting light quality in different en-
vironments.
Terrestrial
Abiotic
Medium
—
Dissolved materials
—
Suspended particles —
Biotic
Bacteria
—
Plants
+
Animals
—
Relative stability*
high
Benthic
aquatic
+
+
+
Nearshore Oceanic
pelagic pelagic
+
+
+
+
—
—
+
+
—
+
+
+
+
—
low to low to high
high
high
* Stability of all factors as a function of time and
space.
ronments. Special attention is given to those
features that appear to directly influence
expression of differential cryptic patterns.
The depth of the habitats
A considerable difference exists in the
distance over which light travels through
the terrestrial and aquatic realms. In the
terrestrial world, the biosphere is vertically
compressed upon the surface to a thin
veneer rarely more than 50 m deep. Only
birds and insects operate within the fluid
that is air, and generally only transiently.
Under these circumstances, a major theme
of selection has been concerned with interactions of the organisms with the substrate,
rather than with the fluid environment, a
condition analogous to only the benthic
portions of the aquatic world. In contrast,
the aquatic environment in some places
extends as deep as 11,000 m (Sverdrup et
al., 1942). A set of niches is created, that
have no true analogue in the terrestrial
world, in which the organisms interact
throughout their entire life history within
the fluid environment, often miles away
from the substrate.
Abiotic and biotic influences on
light quality
As it passes through the biosphere, light
will be variously transmitted, absorbed,
reflected or scattered (Campbell, 1981;
Kirk, 1983). The interplay of these processes results in a set of ecologically relevant properties characteristic of a given
location, that include the light's intensity, color, angular distribution and polarization. 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 attenuated 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
light produced by scattering (McCartney,
1976). However, over the relatively short
distances of the terrestrial biosphere, the
magnitude of these processes is negligible,
and the light quality is little changed. In
contrast, water itself significantly influences the quality of environmental light
over very short distances (Jerlov, 1976;
Kirk, 1983; Wheeler and Neushul, 1981).
In pure water, light intensity decreases logarithmically with increasing distance from
the source and the spectrum is narrowed
by absorbance of short, ultraviolet and long
visible wavelengths of the spectrum, resulting in a predominance of blue light at
depth.
Light attenuation in the sea occurs over
considerable distances, creating a photocline divided into the euphotic, dysphotic
and aphotic zones, which are denned on
the basis of light quantity (Marshall, 1980).
The euphotic zone extends to a depth of
about 200 m in the clearest of oceanic
waters and is defined as that area where
there is sufficient light for net photosynthetic production. In the dysphotic zone,
which extends from about 200 m down to
about 1,000 m, some light is still present
but it is insufficient for effective photosynthesis. Here the quality of surface-derived
light is essentially predictable because its
intensity, spectral composition and angular
distribution change in a regular way both
diurnally and with the phases of the moon
(Jerlov, 1968). The aphotic zone, which
encompasses the majority of the earth's
biosphere, extends from about 1,000 to
over 11,000 m, with an average depth of
4,000 m over the abyssal plains. In the
CRYPSIS IN THE PELAGIC ENVIRONMENT
177
aphotic zone, surface-derived irradiation restrial and nearshore aquatic worlds, phohas been completely attenuated, and the tosynthetic eucaryotes exert the most sigonly ambient light is bioluminescent in ori- nificant potential and actual 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 of the 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
of the most important abiotic factors is the visible spectrum, except in the far red
presence of soluble and suspended, organic wavelengths (between 700 and 800 nm)
and inorganic, light-absorbing material in (Smith, 1986).
the medium (Jerlov, 1968, 1976). In the
In nearshore aquatic environments,
terrestrial world, particles suspended in air there are two distinct forms of plant life
(dust storms, volcanic ash, smog, etc.) are that affect light processes in different ways:
both ephemeral in time and limited in (1) benthic macroalgae (kelp) and seaspace. 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 the incidence 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 reflecamount 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 of the
(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 (Kiein 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 phoand animals. Because bacteria require an tosynthetic organisms may affect light
aqueous medium in which to grow, bac- quality in both terrestrial and aquatic nearterial blooms do not occur in air. However, shore environments, there is a major difin 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 caras 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 are
ble or stochastic, and in some cases have some of the most predictable of all patterns
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 major
phytoplankton blooms often is on the order
(4) Photosynthetic eucaryotes: Consideration
of time and space scales.—In both the ter- of days. Plankton blooms are an important,
178
MARGARET J. MCFALL-NGAI
although unpredictable influence on the
light regime of nearshore pelagic waters.
Under proper environmental conditions,
phytoplankton blooms can typically cover
hundreds of square kilometers to a depth
of 10 m, appearing and disappearing within
a period of a few days to weeks (Brink et
al, 1981; Kirk, 1983).
A notable exception to the transient and
often unpredictable plankton blooms of the
temperate zones are the predictable, seasonal blooms of algae in the Antarctic sea
ice during austral spring (Lewis and Weeks,
1970; Sullivan and Palmisano, 1981; Palmisano and Sullivan, 1983), a time when
pack ice can cover 10% of the world's
oceans (Ainley et al., 1986). Algae grow to
high density in the layers of ice that interface with the water column. The sea ice
and its associated community form a kind
of firmament over the fluid environment
affecting the intensity and spectral quality
of the light below (SooHoo et al., 1987;
Palmisano et al., 1987). Light is attenuated
to such a degree at these times, with underice irradiances usually less than 1% of the
surface (Sullivan et al., 1983), that certain
nonvertically migratory mesopelagic
species occur in ice-covered surface waters
(Ainley et al., 1986). The seasonal patterns
of these areas are quite stable and predictable, and thus reminiscent of the terrestrial temperate deciduous forests.
variable, depending on their abundance
and distribution within any given area.
Nevertheless, where major terrestrial
plants occur they are stable and predictable
in both time and space. With the exception
of the Antarctic, both benthic and pelagic
nearshore areas experience a very wide
variety of unpredictable influences on light
quality.
THE INFLUENCE OF LIGHT QUALITY ON
THE EXPRESSION OF CRYPSIS
To understand how light quality will
influence crypticity, we must consider the
use of cryptic patterns within the context
of predator-prey interactions. In Feder and
Lauder's book Predator-Prey Relationships
(1986), Endler divides the successful predation event into five stages: 1) detection
by the predator's sensory system; 2) identification of the cue as a potential prey item;
3) approach; 4) subjugation; and, 5) consumption. In each one of these stages, a
variety of defense mechanisms have evolved
in prey organisms to avert a successful predation event. For visually orienting predators, the characteristics of environmental
light regime will influence most significantly the detection, identification and
approach stages. Crypsis is one of the best
documented prey mechanisms for avoiding detection by predators using visual cues.
This strategy works by reducing the signal(5) The secondary effects of zooplankton graz- to-noise ratio of the prey's image in the
ing.—Recently it has been demonstrated predator's visual field (Endler, 1986).
by Huntley and co-workers (1987) that Within this context, Endler distinguishes
grazing zooplankton within the water col- two kinds of crypsis: 1) masquerade, in
umn also can have an indirect but signifi- which the animal resembles an object that
cant effect on the light quality in the water is not normally eaten; and 2) eucrypsis,
by influencing the density of phytoplank- where the animal resembles a random samton. Comparable effects exhibited by non- ple of the background in which it resides.
aquatic animals are rare and transitory
Crypsis in terrestrial and benthic
events (e.g., locust swarms).
aquatic
habitats
In summary, the terrestrial and open
ocean pelagic environments have in comAs biologists we are well aware of the
mon that their light quality is affected pri- variety of studies of animal crypsis that have
marily by a single component; however, in been reported from terrestrial and nearthe terrestrial world that component is shore benthic aquatic environments (Poulplant abundance, while in the pelagic ocean ton, 1890; Pycraft, 1925; Elton, 1939; Cott,
it is the medium itself. Thus, the light qual- 1957; Wickler, 1968; Edmunds, 1974;
ity in the open ocean is most influenced by Owen, 1980; Endler, 1978, 1981, 1984;
a constant, intrinsic condition, while in the Wicksten, 1983; Greene, 1989). Examples
terrestrial world, the influence of plants is of both masquerade and eucrypsis can be
CRYPSIS IN THE PELAGIC ENVIRONMENT
found in both of these two habitats. Animals in benthic nearshore habitats express
similar strategies to those of terrestrial animals; however, these benthic animals experience a wide array of abiotic and biotic
influences on light quality (Wicksten, 1983).
Thus, these compounding factors have
been integrated into the resulting selection
of cryptic body coloration. For example,
because red light is filtered out with depth
in the water column, a red crustacean that
would be conspicuous against its background in air is a camouflaged shade of
gray in its natural environment. While
there is this difference in the variety of
influences, cryptic color patterns reflect the
interaction of the animals with a solid surface both on the land and in the nearshore
benthos, and are divergent and variable
because of the heterogeneity of the substratum. Under these circumstances, divergence of color pattern among closely-related
species is not uncommon, and reflects differential attempts to either appear as something inedible or match a random sample
of their heterogeneous habitat.
179
ment, the three-dimensional, homogeneous pelagic world appears to have
selected for the convergent evolution
among disparate phyla (from cnidarians to
chordates and crustaceans) of three fundamental strategies of eucrypsis: transparency, reflectivity and luminescence. To
reduce the signal-to-noise ratio, the organism's body form resembles a random sample of a homogeneous habitat by variously
transmitting, reflecting, or mimicking the
quality of the ambient photic environment
itself. All three mechanisms are used by
animals in the pelagic aquatic environments (Marshall, 1971), resulting in morphologies and behavior that rarely if
ever made the water-to-land transition.
Although the offshore and nearshore
pelagic environments differ in their predictability and stability, these strategies
often are possible in both environments
because they are a response to the photic
environment itself and not to the interaction of the animal with the substratum.
(2) Biogeographic trends in pelagic cryptic-
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 of the species
Hamner and co-workers (1975) and Zaret and, 2) characteristics of the biology of the
(1975), studying marine and freshwater animal, such as size and life history stratsystems, 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 occurmechanisms 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., schoola. 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
(1) Evolutionary and morphological conse- also a conspicuous mode in the euphotic
quences.—There are two important and zone and is best exemplified by schooling
distinctive characteristics of cryptic adap- fishes. Often these fishes will be countertations in the isotropic, pelagic environ- shaded, with the dorsum dark and the venment. Firstly, convergent evolution of sim- trum light, to camouflage from above and
ilar cryptic mechanisms by phylogenetically below. 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 colorb. 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
180
MARGARET J. MCFALL-NGAI
ency, reflectivity and luminescence, which
use or mimic light in the environment, are
TRANSPARENCY
not adaptive in this habitat.
REFLECTIVITY
EUPHOTtC
btolumlnescence
Into this seemingly simple set of trends
is woven a number of other factors, such
100
as diurnal photic cycle and life history
strategy of the individual. At night, the
transparency
reflectivity
DYSPHOTIC
photic
quality of the upper waters is altered,
BIOL.UUNESCENCE
such that there is no longer a euphotic zone.
Under these circumstances, the use of bioluminescence can be effective right up to
woo
the surface of the open ocean, and many
transparency
animals vertically migrate into these areas
A PHOTIC
reflectivity
btolumlnescence
at night (Vinogradov, 1968; Robison,
1972), effectively counterilluminating
against moonlight and starlight. Further,
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 numocean. Capital letters signify dominance of a mode;
lower case letters signify that such a mode is of lesser ber of organismal factors including life history strategy. For instance, some fish species
importance.
have transparent larval stages that, upon
prevalent among midwater fishes, cepha- metamorphosis, become reflective, counlopods and Crustacea, all of which often tershading members of the euphotic zone;
express their light as serial, ventral pho- other species migrate down to the mesotophores. In these areas of the ocean, pelagic zone to become bioluminescent
ambient light quality is attenuated enough counterilluminating fishes (Greenwood,
and stable enough to have selected for the 1975). Another strategy, common among
expression of ventral luminescence, which larval fishes and small crustaceans, is to have
is thought to be used to mimic downwelling most parts of the body transparent, and to
light to camouflage the silhouette in a make reflective those portions where
behavior called counterillumination transparency cannot be maintained (e.g.,
(Clarke, 1963; McAllister, 1967). Coun- the enteric tract). Further, many luminesterillumination is considered analogous to cent systems are composed of photogenic
countershading. A number of studies on tissue, either autogenic or bacterial, that is
the animals in this environment have shown complemented by reflectors and transparthat their luminescence systems produce ent lenses (Herring, 1978). These highly
light similar in color, angular distribution complex luminescence systems often
and intensity to that of light in the meso- involve large portions of the anatomy and
pelagic zone (Denton et al., 1972; Young, morphology of the animal.
1977; Latz and Case, 1982). The anatomy
d. Nearshore pelagic environments.
of the predator visual systems in the meso- While trends in the use of transparency,
pelagic zone suggests that acuity is low reflectivity and bioluminescence such as
(Munk, 1966); thus, the serial photophores those described above may occur in the
might be perceived as one continuous dif- open ocean, in nearshore pelagic environfuse glow against dim downwelling envi- ments similar patterns are not so clearly
ronmental light.
discernable. Transparency and reflectivity
c. The oceanic aphotic zone. In the are the primary modes of crypsis in these
aphotic zone, where solar illumination is waters, while bioluminescence is comparabsent, animals are most often black or red atively rare. Where it does occur, camou(Marshall, 1971), colors that would most flaging luminescence in nearshore animals
effectively absorb point sources of biolu- (primarily fishes and cephalopods) is often
minescent light produced by potential characterized by an internal, bacterial light
predators. The cryptic modes of transpar- organ. One striking example of this can be
CRYPSIS IN THE PELAGIC ENVIRONMENT
found in leiognathid fishes, a group of
approximately 25 species of nearshore perciforms. These fishes inhabit the shallow,
low visibility waters along coastlines of the
Indo-West Pacific province. Bioluminescence produced by a single internal, bacterial light organ is used in a wide variety
of behavioral displays, one of which is
counterillumination (McFall-Ngai and
Dunlap, 1983). In these fishes much of the
anatomy is recruited into the counterillumination camouflaging mechanism. Light
produced by the symbiotic bacteria in a
circumesophageal light organ is reflected
off a silvery-surfaced gas bladder (McFallNgai, 1983a) into nearly transparent
hypaxial musculature and through precisely oriented guanine platelets in the skin
(McFall-Ngai, 19836). The systems work in
concert to produce a ventral luminescent
glow that camouflages the fish from below.
The resultant ventral glow can be controlled at each level of the light organ system, producing a variable mottled effect.
Such a display in these waters of variable
optical quality might be considered analogous to the phenomenon of disruptive
coloration (Morin, 1983).
TRANSPARENCY AS A CRYPTIC
MECHANISM IN PELAGIC
ENVIRONMENTS
Reviews on the subject of cryptic mechanisms rarely include coverage of pelagic
animals, and when they do, they concentrate on bioluminescence and reflectivity.
Transparency as a cryptic mechanism is
almost totally neglected, even though it is
probably the dominant form of crypsis in
the aquatic environment and biosphere.
For this reason, I believe it deserves special
attention within the context of this symposium.
There are three biologically relevant
questions that I will review and explore: 1)
What factors render cryptic transparency
specific to the pelagic, aquatic environment; or stated from another viewpoint,
why is transparency not used extensively
in the terrestrial environment as a camouflaging mechanism? 2) What is the evidence that transparency is used by pelagic
organisms as a form of camouflage in
181
response to predator/prey interactions? 3)
What do we know about the biochemical
and developmental mechanisms by which
transparency is both achieved and maintained?
Transparency as an aquatic-specific
characteristic
Probably the two most important differences between the aquatic and terrestrial
worlds that would influence the expression
of transparency are 1) refractive indices of
air and water, and 2) the amount of incident ultraviolet light penetrating these two
different media. Because animals are largely
water, the refractive indices of their tissues
could theoretically approach that of water
itself (1.34 at 20°C; Maurice, 1957), and,
thus, be very different from that of air (1.00
at 20°C) (Jerlov, 1976). As light travels from
the surrounding water into the aquatic animal's tissue, the incident angle would be
little changed and, if there are no scattering or absorbing elements, the animal
would appear transparent. The significant
difference in the refractive index of air and
the terrestrial animal's tissues creates an
easily perceived outline, and is probably
the single most important factor that precludes the achievement and use of transparency in the morphology of most nonaquatic animals.
Whereas differences in medium refractive index produce an optical constraint,
the damaging effects of ultraviolet light on
biological systems (Ichihashi and Ramsay,
1976; Rothman and Setlow, 1979; Kantor
et al., 1980) create a biochemical limitation on the expression of transparency by
terrestrial organisms. The general absence
of transparency among nonaquatic animals
may be considered indirect evidence of a
limitation overcome in only a few exceptional cases. A search of the literature
reveals few examples in which the majority
of the body of a terrestrial animal is transparent or nearly transparent, with some
indication that the transparency is used in
crypsis. In one instance, some species of
the small glass frogs of the family Centrolenidae, which occur in the rainforests of
Central and South America, are often
nearly transparent (McDiarmid, 1975), but
182
MARGARET J. MCFALL-NGAI
only from a ventral view. Dorsally, these
frogs are pigmented (Schwalm et al., 1977).
It is believed that the dorsal pigmentation
and ventral transparency work in concert
to provide effective camouflage in the frog's
environment.
The second example of terrestrial use of
transparency comes from a study of tropical rainforest butterflies. Papageorgis
(1975) found that assemblages of butterflies stratify by wing color in the Peruvian
rainforests. The various color patterns
appear to be used by the butterflies to effect
crypsis during flight under the differing
light regimes from the top of the canopy
to the forest floor. This is also the only
example that appears in the literature of
terrestrial crypsis in three-dimensional
space. The butterfly assemblage closest to
the forest floor is almost entirely transparent, camouflaging them within the large
patches of filtered light characteristic of
that portion of the rainforest. As with the
glass frog, the butterflies are in an area of
greatly attenuated ambient sunlight. Furthermore, while transparency in insect
wings is not uncommon, the analysis of the
color patterns of these butterflies appears
to be the only really good study of insects
where transparency statistically correlated
with predator avoidance.
Although some ultraviolet light does
penetrate into water (Jerlov, 1976; Baker
and Smith, 1982), a good deal of it is filtered out within a few meters of the surface, so that organisms living some distance
below the surface do not experience the
deleterious effects of high-energy irradiation. However, other evidence that the
presence of ultraviolet light precludes
transparency comes from the studies of
marine fish larvae and invertebrates that
occur in surface waters where UV irradiation can be substantial. H u n t e r s al. (1981)
showed that entirely transparent larvae,
such as those of the anchovy, Engraulis mordax, do not survive well when experimentally exposed to ultraviolet light. These
findings are correlated with the fact that
the larval development of these fishes is
restricted to months of the year when incident solar irradiation is sub-maximal. Fish
species (such as certain atherinid species)
with larvae that are at the water's surface
during times of high incident ultraviolet
radiation have distinct dorsal pigmentation
and, under experimental conditions, resist
ultraviolet light damage (Moser, 1982).
There have also been a number of studies of the effects of UV on freshwater and
marine invertebrates. In freshwater copepods, the presence of carotenoids has been
implicated as photoprotection against high
energy solar irradiation (Hairston, 1976,
1978, 1979). Further, Jokiel (1980) showed
that certain epifaunal species on coral reefs
occur only in shaded areas and are killed
either when moved to sunlit areas on the
reef or are experimentally exposed to UVrich light fields. Species that occur in highly
lit areas of the reef have protective pigmentation.
Transparency in predator-prey interactions
No organism is completely transparent,
and the degree of transparency among
pelagic species varies over a wide range
(Hamner, 1974; Chapman, 1976a, b; Greze,
1964a, b). In addition, the extent to which
an increase in transparency translates into
a significant advantage in predator-prey
interactions is difficult to ascertain. However, as Hamner (1974) points out, anything that reduces the contrast and brightness of the animal would make it more
difficult to see and would, in the context
of predator-prey interactions, be an advantage.
(1) Morphological and behavioral evidence.—There are only a few examples in
the literature that transparency is an
important mode of crypsis in predator-prey
interactions. In analyses of aggressive mimicry in siphonophores, Purcell (1980)
describes two species that appear to use
transparency to enhance predatory success. The siphonophores Agalma okeni and
Athorybia rosacea are highly transparent,
except for nematocyst batteries that mimic
the appearance of a copepod and a larval
fish, respectively. It is hypothesized that
the copepod-mimics attract potential prey
to the otherwise invisible siphonophores
(Purcell, 1980; Mackie et al., 1987).
CRYPSIS IN THE PELAGIC ENVIRONMENT
Observations of another siphonophore,
the Mediterranean species Hippopodius hippopodus (Mackie and Mackie, 1967; Bassot
et al., 1978), revealed reversible-blanching
behavior. Upon stimulation, the animal
changes from almost completely transparent to a milky white in 1-2 sec. If the animal is then left undisturbed, transparency
is restored in 15-30 min. The behavior is
effected by the control of the movement
of granules contained in the mesoglea.
When Hippopodius is transparent, these
granules are punctate, and upon stimulation, the granules disperse through the
mesoglear matrix, rendering the siphonophore visible. Although these studies concentrated on the mechanism of the reversible blanching, Mackie hypothesized that
transparency confers an advantage on the
siphonophore by making it invisible to
potential prey, while the blanching creates
a large visible object that will be avoided
by fishes and other animals that could
potentially damage this delicate animal.
Morphological correlates for the use of
transparency in predator-prey interactions
can also be found among larval fishes. A
wide variety of fishes are transparent during their pelagic larval and juvenile stages
(Breder, 1962; Meyer-Rochow, 1974; Lasker, 1982). Upon metamorphosis onto the
two-dimensional environment of the reef,
the fish lose their transparency and assume
coloration that renders them cryptic against
the substratum. One striking example of
this phenomenon occurs in the postlarval
or "acronurus" stage of the acanthurid
surgeonfishes (Randall, 1961; Thresher,
1984). During this stage, which immediately precedes settlement on the reef, individuals averaging roughly 20 to 25 mm are
virtually transparent except for their silvery gut tract. Upon settlement, they
transform to a fully pigmented adult fish
within as little as 24 hr. While the biochemical and structural mechanisms
underlying this process are not understood, the resulting phenomenon suggests
that transparency is a developmentally programmed cryptic adaptation used specifically during the larval and postlarval stages
of these fishes.
183
(2) Ecological correlates.—Direct evidence
that prey visibility is important in predation in pelagic environments has been
obtained from studies of crustacean species
in freshwater lakes (Zaret, 1975; Kerfoot,
1980; Lazzaro, 1987). For many years,
either body size (Brooks and Dodson, 1965;
Brooks, 1968) or behavior (Jacobs, 1965)
of the prey had been the focus of studies
on cues used by fish predators. However,
more recent analyses show that, at least in
some species, the most important factor is
the overall visibility of the prey (Zaret,
1972; Mellors, 1975; Zaret and Kerfoot,
1975; Confer et al, 1978). Zaret (1972)
compared rates of predation on two daphnia morphs that are of the same size, but
which differ in visibility due to the absolute
size of the eyespot. In laboratory experiments, he offered these two morphs in differing mixtures to a known fish predator
and found that the predator preferentially
selected the large-eyed morph in higher
proportion than would be predicted by
their proportion in the mixture. Further,
he changed the visibility of the small-eyed
type by feeding them India ink to create a
"super-eye" spot, which was now larger
than the eye of the naturally large-eyed
type. Under these conditions, the predators preferentially selected organisms with
the artificially-produced super eye. These
findings were supported by Zaret in a field
study in collaboration with Kerfoot (Zaret
and Kerfoot, 1975), which showed that
when predators are absent, average eye size
is always significantly larger. Further, Mellors (1975) investigated predation on daphnia bearing ephippia, pigmented envelopes
on the dorsum containing resting eggs.
These structures, produced in the Spring
and Fall, go through a tanning process prior
to release from the maternal daphnia. Mellors found that the more visible ephippial
daphnia had higher predation rates than
non-ephippial individuals of the same
species. Because the ingested eggs survive
passage through the gut of the predators,
Mellors concluded that this system aids in
dispersal. Further, Confer et al. (1978)
showed that daphnia with high concentrations of hemoglobin were more likely prey
184
MARGARET J. MCFALL-NGAI
TABLE 2. Ways by which animals achieve transparency.
Reduced chromophore content
High water content
Low tissue complexity
At least one dimension small
Regular arrangement of components
than transparent daphnia. These studies
all show that, in at least some systems, zooplankton predation is positively associated
with their relative degree of transparency.
How is transparency achieved and
maintained?
which it occurs may lend some insight
(Table 2). These conditions have proven
to be a complex interrelationship of body
size, water content, tissue complexity, and
the arrangement of the anatomical components of the system. High water content
is characteristic of the tissues of many
transparent cnidarians and ctenophores,
which can attain very large sizes. Much of
the body mass of a medusa is represented
by the mesoglea, a primarily acellular,
watery tissue. In measurements of transparency in these animals, Chapman (1976a,
b) found that the mesoglea transmits nearly
all of the incident light and the very thin
layer of ectodermal cells that overlies the
mesoglea is where some light loss occurs.
However, more complex animals, with
more tissue types and without mesoglea,
cannot attain large size and transparency
simply by depending on the wateriness of
their tissues. John Tyler Bonner's new
Quanta within the spectral range of visible light can only be efficiently absorbed
by a few specialized biological molecules,
such as carotenoids and chlorophylls. These
molecules have extended pi-electron systems that promote electronic excitation
within the energy range of visible light book, The Evolution of Complexity by Means
(Needham, 1974). Most cell constituents, of Natural Selection (1988), includes estisuch as nucleic acids, proteins, carbohy- mates of the number of cell types in organdrates 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 verteone way to reduce visibility is to limit the brates. It seems logical that the more comnumber 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 funccan 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 leptocephthese 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 milturally 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) (Meyerlem. The problem is further exacerbated Rochow, 1974). A great majority of the
because cell constituents and their orga- transparent species of the higher phyla are
nization are subject to perturbation by small in overall body size.
environmental stresses such as temperaIn addition to these mechanisms, transture and pressure. Therefore, the orga- parency can be achieved through the regnization 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 ai, 1970; Delaye and Tardieu, 1983).
Our understanding of how transparency Chapman (1976a, b) has suggested that ceris achieved and maintained is poor. How- tain transparent animals, such as chaetoever, an analysis of those conditions under gnaths, may also have some precision in
185
CRYPSIS IN THE PELAGIC ENVIRONMENT
the arrangement of tissue components to
promote transparency.
Transparent animals, like all organisms,
must tolerate environmental and physiological stress. The degree to which such
stresses may compromise transparency
itself is an area that has not been explored.
However, a large body of literature does
exist indicating that animals in stressful
habitats have metabolic machinery that is
adapted to work optimally under the set of
environmental conditions that they experience (Hochachka and Somero, 1984). As
ambient conditions move away from this
preferred temperature/pressure range,
biological molecules, particularly proteins,
will cease to function properly and, eventually, denature and precipitate. Whereas
no data are available on how such processes
would influence transparency of pelagic
animals, some data do exist on the influence of temperature on transparency in one
tissue: the vertebrate eye lens. In a recent,
yet unpublished study, we analyzed the
resistance of lenses and their constituent
proteins to temperature stress (McFall-Ngai
et al., in preparation). The study included
ingroups and outgroups within all the vertebrate classes, including organisms with
preferred body temperatures that ranged
from 2° to 39°C. Our results showed a
strong positive correlation between both
the retention of transparency of the whole
lens and the solubility of its constituent
proteins, and the preferred body temperature of the animal. Though much more
complex, the transparent bodies of pelagic
animals may be similarly adapted to a certain range of environmental conditions.
TERRESTRIAL
PELAGIC AQUATIC
PHYSICAL CHARACTERISTICS
OF THE PHOTIC ENVIRONMENT
2-D,
heterogenous
3-D.
homogenous
long-term,
predictable
transient,
stochastic
BIOLOGICAL CONSEQUENCES
FOR CRYPTIC PATTERNS
primarily
divergent
primarily
convergent
transparency, blolumlnascance.
and r«fl«ctMty
superficial
only
whole body
and superficial
'PHOTOMORPHOGENESIS'
FIG. 2. Summary of the physical differences in the
light quality in the terrestrial and aquatic realms, and
the biological consequences of these differences in the
selection of crypticity.
with the casual observations of many
marine biologists that transparent organisms often become opaque just before
death, strongly suggests that the transparency is maintained by active physiological
means.
CONCLUSIONS
Although crypsis has been a widely studied phenomenon in terrestrial and benthic
aquatic habitats, its involvement in predator-prey interactions in the pelagic environment is poorly understood. Intrinsic differences exist between the expressions of
cryptic body form, because of the nature
of the light environment experienced by
The loss of transparency as a result of animals in these various habitats (Fig. 2).
physiological stress has been well docu- The light environment of the pelagic zones
mented in cataractogenesis of the verte- has selected for the convergent evolution
brate eye lens (Bloemendal, 1981). Whereas of transparency, reflection of all wavepelagic animals have been little studied in lengths, and bioluminescence as crypticity
this regard, Hamner (1984) reports the loss strategies in a wide variety of pelagic phyla.
of transparency in krill, Euphausia superba, Of these modes, transparency is probably
as a result of parasitism. Within all dense the most prevalent, yet least understood.
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 stress all, 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
186
MARGARET J. MCFALL-NGAI
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Confer, J. L., G. L. Howick, M. H. Corzette, S. L.
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Kramer, S. Fitzgibbon, and R. Landesberg. 1978.
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