AMER. ZOOL., 26:389-401 (1986)
Light in the Sea—Correlations with Behaviors of
Fishes and Invertebrates1
WILLIAM N. MCFARLAND
Section of Ecology and Systematics, Division of Biological Sciences,
Cornell University, Ithaca, New York 14853
SYNOPSIS. Light is characterized by three basic properties: intensity, the frequency of
electromagnetic vibration, and polarization. Beneath the surface of the sea each of these
properties of light is modified in ways that could affect the behaviors and the underlying
physiological and biochemical mechanisms that control the behavior of organisms. How
light changes under water in several time domains, such as seasonal, daily, and even shorter
periods of time, is described. The correlation between diel shifts in the activity of fishes
and marine invertebrates and the daily changes in light under water is described. It is
concluded that exactly how light influences these daily shifts in animal activity, and whether
or not circadian rhythms also influence the shifts, is, for most species, not known.
INTRODUCTION
Photoperiodic-induced shifts in the
behaviors of organisms and the mechanistic processes that underly these behavior
shifts are, by definition, dependent on
changes in light. Such obvious photic processes as photosynthesis and vision require
adequate light intensities to function. In
addition, a multitude of other processes,
such as diel and seasonal shifts in the endocrine balance of marine animals, changes
in their reproductive state, and in their
overt behaviors {e.g., migration) are ultimately influenced by the properties of light,
although less obviously so than are photosynthesis and vision. How light affects
these processes and, particularly, what specific properties of light are critical in producing behavioral changes is not always
evident. It is the purpose of this review,
therefore, to examine how light can vary
in the sea and to correlate daily changes in
light with shifts in the diel behavior of
marine fishes and invertebrates.
Literature on submarine light in the sea
is extensive. Two recent treatises consider
in highly quantitative terms the physical
nature of underwater light (Jerlov, 1976;
Preisendorfer, 1976). More general references useful to the marine biologist
include Jerlov (1951, 1963, 1968), Smith
and Baker (1978, 1981), Smith and Tyler
(1967), Tyler (1978), Tyler and Smith
(1967, 1970), and a recent book by Kirk
(1983). The difficulties of measuring light
beneath the water surface are too often
unappreciated by the biologist. For accuracy a photographic light meter in an
underwater housing will just not do, and
even so-called modern quantum meters
have their shortcomings. Before embarking on projects involving measurements of
underwater light the unwary biologist
should seek expert advice. In the absence
of such counsel several papers introduce
the general principles of measuring light
(units, etc.) and point out the difficult optical problems (Jerlov, 1965; Smith, 1969;
Arnold, 1975; and Kirk, 1983).
Natural light has three basic properties:
intensity, frequency, and the presence or
absence of polarization. Both daily and seasonal astronomical and both local and general meteorological conditions dramatically affect the properties of light. In
aquatic systems the density of water molecules as compared to air molecules rapidly
increases the attenuation of light.
VARIATION OF LIGHT IN THE SEA
Variation in intensity
The presence of sea salts in pure water
appears to have little effect on either the
absorption or scattering of light (Clarke
and James, 1939; Lenoble, 1956; Armstrong and Boalch, 1961; Sullivan, 1963).
1
From the Symposium on Photoperiodism in the Thus, the extensive studies on Crater Lake,
Marine Environment presented at the Annual Meeting
of the American Society of Zoologists, 27-30 Decem- Oregon, have provided a carefully controlled set of data for very clear water
ber 1984, at Denver, Colorado.
389
390
WILLIAM N. MCFARLAND
and its yearly procession around the sun,
however, are basically different from those
produced by clouds and waves because over
WaveTranslength
mitunce
Attenuation
Scatteri ns
time (hours) they are sustained in direction
(m "')
(nm)
C?-m-')
(m")
and
are highly predictable. Organisms that
5.03 x 10"
400
95.8
43 X iorespond to photoperiod might thus be
450
19 X 10"
98.1
3.05 x 10"
expected to key onto changes that are pro500
36 X io96.5
1.97 x iolonged over several orders of magnitude
550
69 X 10"
93.3
1.33 x io600
83.3
0.93 x 10"
186 X 10"
of light intensity, and this is mostly asso650
75.0
0.67 x io288 X 10"
ciated with twilight during dawn and dusk.
X
700
10"
500
0.49 x io60.7
The length of twilight varies as a func750
9.0
0.38 x io-»
2,400 X io800
tion of latitude and season (Fig. 2). Dra2,050 X 10" 1
18.0
0.29 x 10-'
matic changes, however, in the duration of
* Modified from Table XI in Jerlov (1968).
twilight generally occur over the seasons
only at latitudes in excess of 30° (Fig. 3).
against which light penetration into var- Rates of change of light during twilight
ious types of oceanic waters can be com- will thus tend always to be high at low latitudes and to be lower and more variable
pared (Tyler and Smith, 1970).
at
higher latitudes. How organisms respond
Scattering of light by water molecules is
most significant at the blue end of the spec- to this is poorly denned, but interesting
trum and, generally, is unimportant at behavioral effects do occur. For example,
longer wavelengths (Table 1). Paniculate in very high latitudes fishes that normally
matter and dissolved substances, especially feed during the night reverse their feeding
organic materials (Kalle, 1938, 1966; Sha- habits during periods of lengthened twipiro, 1957), produce variable effects all of light and daylength (Eriksson, 1978; Mulwhich lead to an increased attenuation of ler, 1978).
transmitted light. Because these effects
In general, daylength follows the seaproduce spectral shifts in transmitted light, sons. At low latitudes it hardly varies
discussion is deferred to the next section throughout the year, but at higher lation light frequency.
tudes can achieve durations of 24 hours.
In any given body of water, at least near The effects of these changes in daylength
the surface, light intensity varies during and the duration of twilight on light
each day over a dynamic range of approx- beneath the surface of the sea have as yet
imately 8 to 9 decades of magnitude. The to be explored in detail (see section on twimost rapid change in intensity is associated light spectrum).
with the twilight periods following sunset
Associated with the seasonal and latituand preceding sunrise (Fig. 1). Differences dinal changes in the duration of twilight
in the rates of change of light intensity are changes in the length of the hours of
throughout the day are considerable. Near daylight and darkness (Fig. 2). It is clearly
high noon, in tropical seas, light intensity documented in many terrestrial organisms
changes slowly at about 0.1% per minute. and also many aquatic species that circaDuring twilight, light intensity can change dian rhythms are entrained, largely by dayby approximately 50% per minute. As dark length and/or the length of the dark period
clouds suddenly obscure the sun, light (Harker, 1958, 1964; Cold Spring Harbor
intensity can decline by as much as 75% Symposium on Quantitative Biology, 1960;
over a few seconds. Even more pronounced Cloudsley-Thompson, 1961; Aschoff,
are the changes in light intensity produced 1965; Bunning, 1967; Blaxter, 1970; Segal,
by the passing of surface waves, which can 1970; Pittendrigh, 1975). Organisms liveffect changes well in excess of 200% per ing in more tropical latitudes over the
second (Schenck, 1957; McFarland and course of a year are subjected to less severe
Loew, 1983). Diel changes in light intensity changes in the daily photoperiod and in
produced by the daily turning of the earth the length of twilight than organisms that
T A B L E 1.
Relation oftranmiltance, attenuation and scat-
tering in pure water.*
391
LIGHT AND ANIMAL BEHAVIORS
INVERTEBRATES
X
c
£
X
- 5
CO
111
-
4
-
3 o
o
LU
o
X
LU
_l
Q.
-
-
o
2
1 O
N
DC
O
X
0.0001
1200
1800
2400
TIME OF DAY
0600
(hours)
0
1200
FIG. 1. Correlations between light intensity, the rate of change of light intensity, and the transitional diel
behaviors of coral reef fishes and invertebrates. Open circles are horizontal luminance for a clear sunny day;
closed circles are luminance for a heavily overcast day; open triangles are luminance during moonlight. The
rate of change in light intensities at sunset (SS) and sunrise (SR) are represented by the solid lined curves and
scaled on the right ordinate. The stippled columns (QP) represent the beginning and end of the transitional
quiet periods (see text and Hobson, 1972). The small open rectangles represent the times of the evening
evacuation of the water column by diurnal fishes (SS), and their emergence from the reef and entrance into
the water column near dawn (SR); the small closed rectangles represent the times of the evening emergence
of the nocturnal fish from the reef and entrance into the water column after dusk (SS), and their evacuation
of the water column and return to the reef near dawn (SR). The symbols labelled "invertebrates" represent
the changing activities of sessile forms such as anemones and corals. The horizontal line represents the range
from the beginning to the end of their transitional behaviors; the enlarged blackened rectangle represents
the times when the activities were 50% completed. All data were collected during January of 1981 by W. N.
McFarland.
inhabit temperate to boreal latitudes. The
general consequences on photoperiodic
responses of this major difference in the
way light is presented to organisms have
yet to be thoroughly studied. Careful studies, for example, even on the spectral quality of light beneath the sea during twilight,
let alone in the air at the surface, have yet
to be carried out across latitudes from the
equator to arctic or antarctic (see next section on frequency). It is suggested, therefore, that investigators who examine photoperiodic phenomena in marine organisms
(usually at a single latitude) keep in mind
that not only the length of the photoperiod
varies as a function of season, but also that
the duration of twilight changes and, especially, that the rate of change of light inten-
392
WILLIAM N. MCFARLAND
x
o
o
X
0
J F M A M J
5
40
VIL
.IGHT (mi
/I
80
60 \
\
\—y
• • — -
i
-
-
A S O N D
i1 \\;1/
100
c
J
\i
/
,—
i
i
'
20
,6 5
40
1
I
I
o
J
F M A M J J A S O N D
MONTH
OF
YEAR
FIG. 2. Duration of daylight and of civil twilight as
a function of latitude and time of year. Latitudes above
65° have not been graphed because of the effects of
constant or nearly constant daylight when the sun
approaches, and passes through the solstices. The
dashed line for twilight at 65° latitude indicates these
complications. Civil twilight represents that time
period when the upper limb of the sun is between the
horizon and 6° below the horizon. See Nielsen (1961,
1963) for further information on twilight.
sity during twilight is not a constant. This
can be particularly critical if light-induced
thresholds of photoperiodic responses fall
within the twilight periods, which in fishes
is often the case (McFarland et ai, 1979).
Frequency: The special quality of
light beneath the sea
Numerous investigators have established that as light penetrates very clear
water the higher but intermediate frequencies (shorter wavelengths) representing blue light, ca. 400-500 nm, are transmitted more readily than the lower
frequencies (longer wavelengths) (see Jerlov, 1951; Tyler and Smith, 1970; Kirk,
0
30
LATITUDE
FIG. 3. Relationship between the shortest and longest duration of twilight during the year at various
latitudes. Calculated as the percentage of change. Note
the exponential increase with the largest shifts occurring only at latitudes above 30°.
1983). Therefore clear oceanic water
transmits blue light most readily and
strongly attenuates red light (above ca. 575
nm) and near UV-light (below ca. 400 nm).
As a result, in clear seas at depths of only
25 m the world appears homogeneously
blue to a diver and also to the color film
in an underwater camera when exposed at
these depths (Lythgoe, 1979).
Generalizations based on human vision
and the color balance of photographic film
are misleading, however, because both near
UV-light (ca. 300-400 nm) and yellowgreenish to orange light (ca. 550-600 nm)
can in clear seas penetrate to considerable
depths (Smith and Baker, 1981; Table 2).
If one assumes, for example, that a fish or
invertebrate possessed a UV-visual pigment system with a peak absorption (Xmax)
at 310 nm and a sensitivity threshold equivalent to that for human photopic vision (ca.
10-' W/cm 2 , Clarke and Denton, 1962)
then, during midday, a sufficient number
of UV-photons at 310 nm would penetrate
to depths of 50 m to produce excitation.
A UV-visual system centered at 350 nm
instead of at 310 nm would make retinal
excitation possible to depths slightly in
excess of 100 m. Even in less clear continental seas these visual systems theoretically could function to depths of 10 m at
393
LIGHT AND ANIMAL BEHAVIORS
TABLE 2.
Percentage of surface irradiance present for different wavelengths of light that penetrates to the specified
depths. *
Clear sea (ocean type 1)
X (nm)
% T-m-'
Depth (m)
0
1
5
10
30
50
100
500
97.2
310
86
350
94
400
97.2
100
86
47
22
1.1
0.05
—
100
94
73
54
16
4.5
0.21
Percent light at each depth
100
100
100
97
97
98
91
87
87
75
83
75
56
43
43
24
38
24
5.8
5.8
14.7
450
98.1
550
94.2
600
85
100
94
73
54
16
4.5
0.25
100
85
44
20
1
0.03
—
550
86.5
600
75
100
86.5
48
23
1.3
0.07
—
100
75
24
6
0.02
Continental sea (ocean type III)
X (nm)
% T-m-'
Depth (m)
0
1
5
10
30
50
100
310
50
350
71
400
84
100
50
3.1
0.1
—
100
71
18
3.3
0.003
—
—
Percent light at each depth
100
100
100
54
89
88.5
54
56
42
18
30
31
0.5
3
2.6
0.3
0.02
0.22
—
—
—
450
88.5
500
89
—
* A clear sea is ocean type I; a continental sea is ocean type III. Percentage transmittance values are from
Jerlov (1968); see also Figure 4.
310 nm and to 30 m at 350 nm (Table 2).
Of course the enhanced scattering of near
UV-light by water molecules and other
small particles at these short wavelengths
presumably would make an image-forming
visual system less useful than one spectrally
located at longer wavelengths in the blue
and green regions of the spectrum. But,
the point is that a considerable number of
short wavelength photons (<400 nm) and
long wavelength photons (>500 nm) do
penetrate effectively into the surface layers
of most seas, and could excite photochemical systems in organisms if thresholds do
not require extreme intensities of light {e.g.,
at the surface).
The presence of dissolved substances
(Kalle, 1966), and of particulate inclusions,
e.g., phyto- and zooplankton, have the effect
of decreasing the overall transmittance of
light, and particularly in the blue shortwavelength region of the spectrum. This
has been clearly demonstrated in the now
classic studies ofJerlov (1951,1968) as portrayed in his figure that spectrally classifies
different seas (Fig. 4). As dissolved and par-
ticulate matter increase in sea water, there
is a distinctive shift in the transmitted light
from the blue-green region of the spectrum to the green-orange region of the
spectrum, which must be further enhanced
as light penetrates to greater depths. This
tendency for the available light to become
more monochromatic in the blue region of
the spectrum in clear seas, and more monochromatic in the green to orange region
of the spectrum in coastal seas and lakes,
has been beautifully displayed in the colored figure portrayed in the review article
on vision in fishes by Levine and McNichol
(1982). In modified form, the figure is
reproduced here in black and white (Fig.
5). Again, it is evident that in near surface
depths both short- and long-wavelength
photons are relatively abundant, even
though the dominant hue is blue to our
eyes.
The actual spectral radiance, therefore,
that impinges on an aquatic organism, will
depend on (1) the direction of the radiance
field (=direction of regard), (2) the spectral
attenuation characteristics of the water
394
WILLIAM N. MCFARLAND
15 -
30 -400
500
WAVELENGTH (nm)
600
<
700
FIG. 4. Transmittance as a function of wavelength
for various types of ocean water as classified by Jerlov
(1968, 1976). Type I is the clearest open ocean, Type
III a coastal sea, such as offshore from Puget Sound.
Types 1 through 9 include increasing concentrations
of phytoplankton and other particulates and dissolved
organics. They would be typified by coastal lagoons
and inshore areas with heavy plankton blooms (see
McFarland and Munz, 19756,; Hobson et ai, 1981,
for specific examples).
type, and (3) the depth. The presence of a
solar beam and the solar angle will influence the spectral radiance, especially its
intensity. Variation in the spectral radiance in a clear tropical sea as a function of
direction of view (line of sight) indicates
how the spectrum rapidly narrows when
viewed more than 20° to 30° off the axis of
the solar beams (Fig. 6). Near the surface
in sea water that contains increasing
amounts of inclusions and because of light
scattering, the narrowing of the spectrum
is far less obvious than in clear water.
In a real sense one can conclude that the
nature of light that impinges on an organism underwater will be a specific function
of (1) depth, (2) water type, and (3) the
direction of the radiance field from the
organism. In general, the closer to the surface the broader will be the overall spectrum. And the greater the presence of dissolved organic constituents and particulate
matter in the water, the less intense will be
the transmitted light at any given depth
and relatively fewer the short wavelength
photons.
Comparisons of a typical daytime midday spectrum in air with spectra for twilight, moonlight, and starlight reveal distinct differences (Fig. 7). Beneath the water
surface the spectral distribution of light
CO
o 45
E
a 60 w
a
75
0
25
400
500
600
WAVELENGTH (nm)
700
FIG. 5. The extinction of daylight as a function of
wavelength for a very clear sea and a coastal sea or
lake. The spectral distribution of daylight (typical) is
shown in Figure 7. The upper graph represents the
transmittance characteristics of a Type I sea (curve I
in Fig. 4). The lower graph is approximated by a
coastal sea of Types 5—7 (Fig. 4), or a lake containing
phytoplankton blooms (see McFarland and Munz,
19756). Note that with increasing depth the light
becomes homochromatically "bluer" in the open sea,
and "greener" in the coastal sea.
associated with particular times of the day
can be modulated in a variety of ways
dependent on the particular spectral attenuation coefficients of the type of water. In
clear oceanic waters during twilight the
near surface underwater spectrum (upper
10 m) tends to be less broad than either a
daytime spectrum or a nighttime spectrum
(Fig. 7). In seawater types that contain more
dissolved organics and particulates, and
therefore tend to be greenish in color, the
twilight spectrum is narrowed, but retains
395
LIGHT AND ANIMAL BEHAVIORS
V
10
A*
CM
o
°° -
30°
5 -
- 1000
1—
X
0
i
i
400
1
1
1
1
500 600
700
0°
(0
u
<D
(0
E
s
-*- 90°
c
90°
- 5
CM
E
u
1
180<
z 4 0 0 500 6 0 0 700
CO
1
400 500
600
700
o
IO
I
\
180°
5 "/
1
1
400 500 600 700
WAVELENGTH (nm)
FIG. 6. Spectral radiance distribution of light for different lines of sight in a tropical coral reef lagoon. The
sun's axis beneath the water was at approximately 25°. The noise in the curves at 0°, 20°, and to a lesser
extent 90° (toward the sun) result from wave induced flicker. The solid line in the 20° curve results from a
smoothing routine applied to the data. The vertical line in each graph represents the central wavelength that
partitions the area under the curve into equal numbers of photons (XP50 of Munz and McFarland, 1977). Note
that the horizontal (90°) and nadir spectra (180°) are very similar, and that the broad spectrum associated
with the sun's axis narrows rapidly off axis (usually within less than 30°). Curves were obtained on a clear
sunny day in Enewetak lagoon at a depth of 3 m below the sea surface; total depth was 23 m, with a clear
sand bottom (albedo 23%).
its greenness, although its peak transmission may shift slightly toward longer wavelengths (McFarland and Munz, 19756).
Whether these spectral shifts have pronounced effects on the photoperiodic
responses of organisms is a moot point, but
there is evidence to suggest that they have
a pronounced effect on the vision and
behavior of marine and freshwater fishes,
and, presumably, also invertebrates (Hobson, 1972; Munz and McFarland, 1973,
1977; McFarland and Munz 1975a, b; Hobson etal., 1981).
Interestingly, the aerial spectra of both
moonlight and starlight are richer in long
wavelength photons (redder) than a typical
daytime spectrum (Fig. 7). Beneath the
water surface, however, the spectral differences from daylight are less dramatic
than during twilight because of the rapid
attenuation of longer wavelengths (Fig. 7).
Polarization in the sea
The presence of polarized light fields
beneath the water surface as viewed
through Snell's window (the bright cone of
light that subtends an angle of ca. 96° that
can be observed overhead by a diver, and
which results from the refraction of light
at the air-water interface; see Lythgoe,
1979, for details), as in air, is partly dependent on the presence of a non-overcast sky
WILLIAM N. MCFARLAND
396
100
50
z
o
H
o
X
Q.
o
z
700
100
i-
LLJ
EC
400
500
600
WAVELENGTH (nm)
700
FIG. 7. Comparisons at different times of the day
between the spectral distribution of light impinging
on the sea's surface and the downwelling irradiance
recorded 3 m beneath the surface. All curves are
normalized for easy comparison of the spectra. The
midday (D), twilight (T), and moonlight (M) curves
were all obtained at Enewetak Atoll in the Marshall
Islands. The starlight curve (S) in air was obtained in
Oregon, and the underwater curve was calculated on
the basis of the attenuation of light to 3 m that occurred at Enewetak. The high peaks in the starlight
curve represent atmospheric emission bands in the
zenith sky resulting from the daily solar activation of
oxygen and other atmospheric constituents. Note the
bimodal shape of the twilight spectrum in air. Details
are described more fully in Munz and McFarland
(1977).
(some blue sky visible). Most of the underwater polarization arises from the scattering of light by water molecules and particles (see Waterman, 1981, for an extended
discussion). A recent useful description of
polarization in the atmosphere (Brines and
Gould, 1982) supplements a series of papers
that carefully describe light polarization
patterns under the sea (Waterman, 1954,
1955, 1961; Waterman and Westell, 1956;
Ivanoff and Waterman, 1958a, b; Lundgren, 1971). Natural polarization in air and
beneath the sea can be described by the
percentage of light polarized along a given
line of sight (=radiance field), and by the
orientation of the e-vector (the electric
vector of light when light propagation is
considered as an electromagnetic wave; the
e-vector is orthogonal to the magnetic vector of light). Under water, as in air, when
the sun is at zenith maximum polarization
occurs around the horizontal field of view,
and the e-vector orientation is horizontal
at all azimuth bearings. When the sun angle
is low (e.g., at sunset) maximum percent
polarization is found directly downward
and at other angles normal to the sun's
bearing (Waterman, 1954). Under sunset
conditions the e-vector tilt is not symmetrical but maximally tilted (ca. 45°) at all
bearings 90° from the sun's axis. In addition, as the sun's altitude diminishes both
the percentage of polarization and the
e-vector tilt increase (underwater polarization maxima are 60% polarization, and
an e-vector tilt of 45°). Decreased water
clarity and increasing turbidity, as well as
increased amounts of overcast skies, result
in a diminishment of the percentage of
polarization and the angle of e-vector tilt.
Although retinal mechanisms are known
to exist for the detection of polarization in
many marine invertebrates (e.g., Crustacea,
Waterman, 1966; octopus, Moody and Parriss, 1961), hard data that demonstrate its
presence in fish have been shaky (Waterman and Forward, 1970, 1972; Waterman,
1975). Orthogonal orientation of the cone
outer segment discs in the retina of
anchovies, however, could serve as a basic
mechanism for polarization detection
(Fineran and Nicol, 1978). By using operant heart conditioning procedures, Kawamura et al. (1981) claim to have demonstrated polarized light detection in
freshwater cichlids, rainbow trout, and
marine yellowtail, but not in freshwater
carp nor sea bream. The behavioral use of
polarized light detection by animals mainly
centers on orientation and navigation (as
in bees, von Frisch, 1949, 1967; and
pigeons, Kreithen and Keeton, 1974; Delius
LIGHT AND ANIMAL BEHAVIORS
et al., 1976). Whether polarized light
detection is useful in photoperiodic
responses is a moot question. Its detection,
however, could be important as a timing
signal since an increase in the degree of
polarization and e-vector asymmetry occurs
at both dusk and at dawn. But dramatic
changes in light intensity and the spectral
distribution of light also occur at dusk and
dawn.
397
defined by the time of active feeding (Hobson, 1979). Some species are active day and
night and others feed most only during the
"twilight" crepuscular hours. The best
studied examples amongst marine organisms are the highly diverse coral reef fishes,
which can be classified into a variety of
distinct feeding guilds (Hobson, 1975;
Hobson and Chess, 1978) and show highly
species-specific behavior with respect to
changing activity patterns and the time of
Real time temporal fluctuations in
day (Collette and Taylor, 1972; Hobson,
submarine light
1972; Domm and Domm, 1973). Shortly
after
sunset and just before dawn an
As described in the preceding sections,
both the seasonal and daily movement of unusual behavioral event occurs. For a
the earth relative to the sun effect dramatic short period of time (usually less than 20
changes in the characteristic properties of min) both the diurnal and nocturnal fishes
light. In aquatic ecosystems and near the that feed high over the reef vanish from
surface, light usually flickers. Local waves the water column to the bottom. This soand ripples on a disturbed sea surface act called transitional "quiet period" presumas dynamic lenses that rapidly modify their ably functions to remove the fishes from
optical focus on a locus beneath the sur- an increased threat by predators. The
face. If the sun is shining the effect is dra- heightened threat is believed to result from
matic, for any reflective surface beneath an enhanced visual edge that the predators
the waves, be it a fish or the bottom, flick- obtain as a result of the attainment of interers in response to the focusing and defo- mediate light levels during which neither
the daytime photopic visual system (cones)
cusing of the sun's rays (Schenck, 1957).
Flickering light produced by waves has nor the nocturnal scotopic visual system
two inherent properties, (1) a change in (rods) of fishes functions at peak efficiency,
light intensity (2) presented usually at a i.e., mesopic vision (Munz and McFarland,
complex rate of change that is measured 1973). For diurnal fishes it has been shown
in seconds or less rather than in minutes that this departure from the water column
or more (McFarland and Loew, 1983). In at evening twilight correlates quite well with
general, the frequency range produced by the onset of light to dark adaptation proflicker is from 1 Hz to 100 Hz in the upper cesses in the retina (Munz and McFarland,
meter of a clear sea (average ca. 15 Hz), 1977). The emergence of the nocturnal
and falls off rapidly with depth (average 4 fishes from the reef interstices and their
Hz at 4 to 5 m; McFarland and Loew, 1983). entrance into the water column begins with
Can flickering light affect the photoperi- the completion of dark adaptation of the
odic responses of marine organisms? There retina (see Levinson and Burnside, 1981,
are no data on this question. However, for a review of the mechanisms underlying
flicker produced by waves can enhance light and dark adaptation in fishes). A
visual contrast of objects for fishes reverse sequence of these behaviors occurs
(McFarland and Loew, 1983) and does at dawn. These specific behaviors are preimprove photosynthetic output in marine cise and can be shown to occur at specific
phytoplankton (Walsh and Legendre, light intensities during twilight (Hobson,
1972; Munz and McFarland, 1973;
1983).
McFarland et al., 1979). Similar transitional behaviors occur in temperate marine
DIEL ACTIVITY CHANGES IN FISHES AND
fishes (Hobson et al., 1981) and in freshINVERTEBRATES AND THEIR CORRELATION
water fish communities (Helfman, 1979,
WITH THE DAILY LIGHT CYCLE
1981), although the precision of the behavMost animals can be classified as diurnal iors may be less tightly coupled to exact
or nocturnal, behavioral categories usually
398
WILLIAM N. MCFARLAND
light levels in the temperate fishes. An
important question with respect to photoperiodic control of diel activities underlies these various studies on fishes: How
much of the precision in their migratory
behavior results from endogenous daily
rhythms? Or can the precision in their
behaviors be accounted for by the direct
influence of light on the visual system? At
present there are no clear answers. Circadian rhythms do exist in tropical reef
fishes, but studies are limited to only a few
species (Livingston, 1971). Results from
studies on the retinomotor movements, or
light-dark adaptation mechanisms in fishes,
are ambiguous. In some species retinomotor movements are apparently not influenced by endogenous rhythms, whereas in
others they are (Levinson and Burnside,
1981). It seems clear, nevertheless, that
where circadian involvement is present that
complete light or dark adaptation of the
retina requires the presence of a light-dark
cycle. One can tentatively conclude, therefore, that the changing suite of behaviors
that characterize a reef fish as diurnal or
nocturnal requires the intervention of natural light cycles. And that requirement
quite probably protects a fish from deviant
behaviors resulting from a free-running
endogenous rhythm that might place it in
jeopardy in the presence of an alert predator (e.g., a diurnal fish remaining in the
water column too long, or a nocturnal fish
entering the water column too soon).
Because the duration of twilight only
changes dramatically at high latitudes (Fig.
2), we might expect twilight intensities (or
rates of change) to have a more direct influence on light and dark adaptation processes in temperate fishes than in tropical
fishes, and circadian rhythms to be more
dominant in tropical fishes than in temperate fishes. Although the evidence is
scant, this may actually be so (Levinson and
Burnside, 1981).
The precise switches from diurnal to
nocturnal behavior in coral reef fishes not
only reduce the threat from predation, but
also serve to temporally and spatially separate potential competitors. What happens, therefore, amongst the highly diverse
groups of marine invertebrates that also
inhabit coral reefs? This question has been
only partly answered in an investigation of
30 taxa of invertebrates in 5 phyla that
inhabit the same coral reef (Suchanek and
McFarland, unpublished manuscript).
Individual species in 3 of the 5 phyla showed
precise diel behavior changes usually coupled to the rapid changes in light intensity
during sunrise and sunset. At dusk, 6 taxa
of arthropods (all zooplankton), several
cnidarians (3 species of corals, 2 anemones,
and 2 zoanthids), and the sea urchin, Diadema antillarum, showed precise transitions
from little activity during daylight to
increased activity at night and the reverse
at dawn. Certain sessile annelids, a shelled
mollusc, and some cnidarians (octocorals),
in contrast, showed no discernible patterns
of diel behavior changes. Where activity
changes did occur they tended to be
strongly correlated with the most rapid
changes in light intensity, and were usually
50% completed at the time of the peak
rates of change in intensity. In contrast to
the rather rapid shifts in behavior seen in
the tropical coral reef fishes, the shifting
activity patterns in the invertebrates generally began earlier and ended later in the
evening at dusk, and similarly so at dawn
(Fig. 1). In short, the activity changes were
slower. The sea urchin Diadema and the
emergence of the reef zooplankton, which
are all highly motile like fishes, were exceptions. The reef zooplankton, for example,
emerged over a short period of time which
coincides closely with the emergence of the
nocturnal planktivorous fishes.
The longer total response times in the
remaining invertebrates perhaps implies
the presence of a controlling circadian
rhythm. In general, however, the first indication of a behavioral change occurred in
all instances only after the change of light
intensity achieved a value of at least 30%
per minute, a rate likely detectable by the
photic systems of many marine invertebrates. As in fishes, the actual demonstration of circadian rhythms in tropical marine
invertebrates is equivocal. For example, in
stony corals a demonstrable rhythm may
be present in some species and not in others (Sweeney, 1976). I am left to conclude
that the precise changes in diel behavior
LIGHT AND ANIMAL BEHAVIORS
patterns that occur in tropical marine fishes
and in invertebrates are triggered, if not
controlled, by changes in natural light that
are prolonged in a given direction, e.g., at
dusk or dawn. What is not clear is whether
the trigger in each species is the result of
the achievement of some absolute light
threshold, or a directional and prolonged
duration of rate of light intensity change,
or the achievement of a specific rate of
light intensity change, or some interactive
combination of all of these factors (see
Segal, 1970, for review). And, in some
instances, might the behavior shifts even
involve changes in hue or the degree of
polarization beneath the sea's surface as
well as changes in light intensity and photoperiod duration? Solid answers will
require carefully controlled experiments
on representative animals at the cellular,
organismal, and environmental levels.
399
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