Download Behavior of Plankton and Patch Formation in Pelagic Ecosystems

BULLETIN OF MARINE SCIENCE, 43(3): 752-757, 1988
BEHAVIOR OF PLANKTON AND PATCH FORMATION IN
PELAGIC ECOSYSTEMS
William M. Hamner
ABSTRACT
One of the most pervasive characteristics of pelagic ecosystems is the perpetual threedimensional motion exhibited not only by the water but also by all organisms within the
water column. This constant motion contrasts sharply with the general absence of motion in
terrestrial ecosystems, where most of the biomass is in the form of large, multicellular, and
immobile plants within and about which animals live and hide, I review previous discussions
that contrast pelagic and terrestrial ecosystems and to those thoughts I add the argument that
in the pelagic realm the pervasive movement of all the organisms, the absence of physical
barriers to vertical and horizontal migrations, and the absence of cover create fundamental
differences between the ways that events transpire on land and in the water column. Ramifications of the behavior and mobility of plankton are then discussed with regard to patch
formation in pelagic ecosystems.
The Greek word from which "plankton" is derived usually is interpreted in
English to mean "wandering." The Greek term really is more explicit, however,
and has "a distinctly passive sense meaning 'that which is made to wander and
drift', i.e., drifting beyond its own control-unable to stop ifit wanted to" (Hardy,
1965). How does one reconcile behavioral passivity and random, uncontrolled
distributions with the concern ofthis session, the quite opposite subjects of swimming behavior and patchiness of plankton? Since the word "plankton" is lovely
and since it will be with us forever, we must simply ignore the etymology of the
word and use it to designate the extremely broad assemblage of mostly smaller
organisms, from bacteria to larval fish, that occur in pelagic waters, almost all
being capable of either active swimming or passive transport via changes in
buoyancy. Perhaps the most pervasive characteristic of pelagic marine and limnetic ecosystems is the perpetual three-dimensional motion exhibited not only by
the medium but also by the bacteria, protozoans, plants, and animals. The constant
motion that is characteristic of pelagic organisms contrasts sharply with the general
absence of movement in terrestrial ecosystems, where most of the biomass is in
the form of large, multicellular, and deeply rooted immobile plants, within and
about which animals hide (Elton, 1939; 1966).
Other fundamental contrasts between pelagic and substrate-oriented ecosystems
have been considered by previous authors. Parsons (1976) noted the importance
of the buoyancy of water and consequent differences in gravity in the sea as
opposed to land that result in low requirements for structural support at sea, a
general absence of refractory structural materials (as opposed to a storehouse of
cellulose on land), a protein based economy at sea (carbohydrate based on land),
and rapid growth of populations at sea up to a size large enough to avoid predators.
Isaacs (1977) and later Dayton (1984) emphasized another basic difference
between pelagic and terrestrial ecosystems in that the size of food particles is a
primary determinant of food web structure in the open sea. Isaacs (1977) stated,
"In the pelagic realm a sort of food web composed of the progeny of many species
seems to constitute a major pathway of material to the larger forms. This pathway
is dominated by growing larvae and juveniles, which suffer immense mortality
... Such a system is in sharp contrast with other food webs where large plants
752
HAMNER: SWIMMING BEHAVIOR AND PATCHINESS
753
provide the initial input, large herbivores are supported, the populations are
dominated by adults, and mortality is low."
Steele (1985) suggested other major differences between terrestrial and marine
ecological systems that result from another attribute of water, its high specific
heat ... the damping of short-term thermal variability, dominance of the oceans
by poikilotherms even at higher trophic levels, the ability of these poikilotherms
to release reproductive products directly into the sea, and a decoupling of larval
and adult phases with their different feeding and mortality patterns.
Smetacek and Pollehne (1986) argued forcefully that there is a "
fundamental
difference in the relationship between auto- and heterotrophs of
terrestrial
and pelagic systems ... [based on asymmetries in the] ... temporal and spatial
patterns of nutrient cycling ... On land, the material [and ultimately limiting]
resource is water ... passed up the food pyramid but ... not recycled ... because
of evaporation." In aquatic systems water is never limiting, and other so-called
limiting nutrients (N, P, etc.) are only limiting some of the time. Dayton (1984)
argued that in plankton communities nutrients are the potentially limiting resource, but that they are "not directly relevant to the planktonic heterotrophs."
Many biologists apparently continue to attempt to reconcile terrestrial and
pelagic conceptual frameworks (Smetacek and Pollehne, 1986, cite various authors). I would, however, concur with Parsons, Isaacs, Dayton, Steele, and Smetacek and Pollehne that the differences between the two systems are profound. I
argue here, in addition to the differences noted above, that the pervasive movement of all of the organisms in the sea, the absence of physical barriers to vertical
or horizontal migration, and the absence of cover in the pelagic realm (Elton,
1939; 1966; Hamner et a1., 1975; Hamner, 1985), result in a fundamental difference between the ways events transpire on land and in the water column and
between the ways we, as scientists, perceive those events.
Perhaps part of the proof lies in the ecological literature on patchiness. For
example, in The Ecology of Natural Disturbance and Patch Dynamics (Pickett
and White, 1985) only one reference out of some 1,700 cites "Spatial Pattern in
Plankton Communities" (Steele, 1978), a book about patchiness of plankton. This
lack of citation in Pickett and White does not happen because terrestrial biologists
are ignorant of marine science since articles by benthic and intertidal ecologists
(Connell and Keough, 1985; Sousa, 1985) are included therein, but rather because
patchiness in all substrate-oriented ecosystems, whether terrestrial, intertidal, or
benthic, is fundamentally different from patchiness in the pelagic realms of lakes
or the sea.
In substrate-dependent systems patchiness usually means the absence of organisms whereas in pelagic systems patchiness means the presence of organisms.
In both cases the patch is recognized against background density differences. In
substrate-dependent systems the densities in the surround are higher than in the
patch, whereas in pelagic systems the densities of the species surrounding the
patch are lower. In Pickett and White (1985) discussions revolve around the ways
physical-chemical events (e.g., tree falls or fire) create open space by elimination
ofthe previous inhabitants. Oceanographers (Steele, 1978), however, use the term
patchiness in an opposite sense, worrying about how physical-chemical events
such as fronts or thermoclines aggregate organisms.
These differences in connotation are not semantic trivialities, but reflect very
real differences in the structure of these two kinds of ecosystems. For example,
in the relatively static world of the substrate-oriented terrestrial ecologist, seedlings
transform over ecological time into forests and the forest becomes the entity
against which long term events are evaluated and within which animals hide. In
754
BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988
the pelagic realm of the open sea, by contrast, tiny, often extremely motile autotrophs do photosynthetic duty and they do it quickly and divide before they
are eaten or adversely advected. They provide no spatial reference either for their
consumers or for oceanographic observers, and at sea there is no photosynthetic
fabric comparable to a forest against which to evaluate events. In the forest
populations respond slowly to disturbances via succession over ecological and
evolutionary time, but in the water column patches transform rapidly. At sea,
unless within the protection of a motile, polarized school, it is dangerous to be
in patches because consumers usually find their food and mortality is high. At
sea, patchiness is synonymous with ephemerality.
The disparate natures of patches in pelagic and substrate-oriented systems are
further emphasized by an appraisal of their respective fates. At sea small-scale
patches disperse, usually quite rapidly, although meso-scale eddies (Wiebe et aI.,
1976)or very large intrusions (Paffenhofer et aI., 1984)do show modest population
changes over time. In the forest even small-scale patches undergo gradual succession until they once again exhibit the characteristics of the " ... surrounding,
unaffected or less affected matrix" (White and Pickett, 1985).
The volumes edited by Steele (1978) and Pickett and White (1985) are both
based on precisely the same premise, that patchiness results from some category
of physical, chemical, or biological disturbance. For example, in "The Ecology of
Natural Disturbance and Patch Dynamics," White and Pickett (1985: p. 11, table
2) list 21 categories of disturbances, mostly physical, while Haury et al. in Spatial
Pattern in Plankton Communities (1978: p. 302, table 2) list 14 important categories of physical disturbances. Why then does the 1985 book not cite the earlier
one if both are concerned with the same questions? Because, although the effects
are described by the same word (patches), the causes are different. On land the
most important cause of patchiness is fire. In open water the most important
cause of patchiness is the thermocline. The lack of congruence between the two
lists of causal events generating patchiness in these two different environments is
startling. Almost nothing of significance that generates patchiness in substrateoriented ecosystems is important in the pelagic realm. Does this real lack of
congruence then provide us, as oceanographers and limnologists, with a valid
excuse to ignore almost everything written by terrestrial ecologists on patchiness?
Probably not, because a quite massive body of terrestrial literature is relevant to
pelagic ecosystems, but it is a literature more concerned with behavior of animals
than with their ecology.
Patchiness in pelagic waters certainly is affected by all the physical and chemical
ecological processes noted throughout Steele (1978), but in open water patchiness
also can result from purely behavioral phenomena. Indeed, pelagic patchiness is
often synonymous with behavioral aggregation. Animals, of course, aggregate for
a wide variety of reasons. Brown's (1975) categorization of animals into groups
of various kinds serves to illustrate the rich variety of patterns that we can expect
to encounter in lakes and at sea. Animals may be associated with each other in
kin groups as clones, families, or extended families that fail to disperse and thereby
create aggregations based on genetic propinquity (e.g., phytoplankton blooms) .
.Mating groups are common both on land and in pelagic waters, in pairs when
mating (a patch of two), in harems, leks (see Morin, 1986, for ostracode leks),
and spawning groups (e.g., medusae: Russell, 1970; Hamner et aI., in prep.).
Colonial groups are common among seabirds and seals, and survival groups, such
as schools of fish, squid, krill, and marine mammals dominate the water column.
Brown (1975) adds, almost as an afterthought, the category of coincidental groups.
Here he includes groups formed by physical factors acting on migrating or moving
HAMNER: SWIMMING BEHAVIOR AND PATCHINESS
755
animals (thereby including everything mentioned both in Steele and in Pickett
and White) and groups formed by attraction to a common resource, such as food
or water (e.g., bears at a garbage dump).
Most of the contributions on patchiness and swimming behavior in this symposium fall into Brown's category of coincidental groups. There are reports on
swimming behavior and the resultant patchiness from attraction to food (e.g.,
chemoreception in protists), a report on formation of groups by common reaction
of copepods to salinity differences near a river plume, and on aggregation of
copepods and whales on an oceanic front. Almost any behavior exhibited by an
animal (or bacterium or plant) can exlain the patchiness observed in coincidental
groups. The slightest alteration in behavior can cause coincidental patchiness
(Fraenkel and Gunn, 1961). For example, a simple decrease in swimming speed
can increase density. When automobiles on the open road approach a small town
they slow down and traffic becomes locally congested (Fraenkel and Gunn, 1961).
Density of copepods on the thermocline should increase similarly if the copepods
pause even briefly on passing through (Harder, 1968). Equally, a simple increase
in turning rate can generate patchiness. Most of our present knowledge about
plankton behavior and patchiness is at about this level of complexity, but more
sophisticated behaviors are required when animals get more social, such as occurs
within schools of euphausiids, in which the animals synchronize their changes in
speed, direction, and nearest neighbor distances (Hamner et aI., 1983; Hamner,
1984).
In order to understand the nature of patchiness we must observe the behavior
of individual animals (Hamner, 1985), a point we did not emphasize in an earlier
discussion of patchiness and sampling (Omori and Hamner, 1982). Indeed, observation of particular individuals is the absolute essence of behavioral research,
whether in the laboratory or the field, but such observations are almost entirely
lacking for pelagic animals (Hamner, 1985; Hamner et aI., 1987). For example,
although thousands of publications have examined what may be the dominant
behavioral pattern on earth, that of vertical diurnal migration, not one of those
investigations has been concerned with what one individual animal actually does
during the course ofa 24-hour day. Since most vertical migrations can be accomplished quickly, even in an hour or two, sometimes one wonders what the zooplankton do with the rest of their time.
In the past, answers to questions about the behavior of individual plankters at
sea were obscured because our questions were addressed at the population level
and almost exclusively in statistical terms. Statistics, however, relate only to the
behavior of the population as a whole. Although one can compute the parameters
of a population from the sum of the individual parts, one can never infer the
behavior of the individual from a population statistic. Evolution operates by
selection on individuals that vary within a population, not upon averages. A
concern with averages and with a statistical "deceptive semblance of accuracy"
(Haeckel, 1890) has dominated biological oceanography for the past 100 years
and probably is why most biological oceanographers have an agricultural mentality
(Hamner, 1985; Smetacek and Pollehne, 1986). I have noted elsewhere (Hamner,
1988) that most of the interesting biological events that occur in the water column
happen within or about aggregations of organisms, and we should be spending
more time looking at patch dynamics and less time, on average, worrying about
averages.
The focus in oceanography on statistical sampling programs has resulted in
such neglect of the behavior of individual animals at sea that to date only one
paper (Hamner et aI., 1987) has specifically considered the in situ ethology of a
756
BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988
planktonic species. The essence of an animal (as opposed to that of an attached
plant) is that it is mobile and that it exhibits individual behaviors that can be
either independent of or synchronized with the behavior exhibited by other individuals in the population. Hopefully this symposium will stimulate interest in
the behavior of plankton, behavior that is often exhibited in order to avoid
predators or to exploit patches of food or the tides and the ocean currents. However
much we learn about plankton behavior, one fact will only become more obvious;
plankton probably never are aimlessly adrift. They can control their movements
and they can stop whenever and how often they wish, for almost any reason at
all. When they do elect to stop they often form dense aggregations, and this
invariably creates patchiness in the water column.
LITERATURE
CITED
Brown, J. L. 1975. The evolution of behavior. Norton, New York. 761 pp.
Connell, J. H. and M. J. Keough. 1985. Disturbance and patch dynamics of subtidal marine animals
on hard substrata. Pages 125-151 in S. T. A. Pickett and P. S. White, eds. The ecology of natural
disturbance and patch dynamics. Academic Press, New York.
Dayton, P. K. 1984. Processes structuring some marine communities:
are they general? Pages 181197 in D. R. Strong, Jr., D. Simberloff, L. G. Abele and A. B. Thistle, eds. Ecological communities.
Princeton Univ. Press, Princeton.
Elton, C. 1939. On the nature of cover. J. Wildlife Management
3: 332-338.
--.
1966. The pattern of animal communities.
Wiley, New York. 432 pp.
Fraenkel, G. S. and D. L. Gunn.
1961. The orientation
of animals. Kineses, taxes and compass
reactions. Dover, New York. 376 pp.
Haeckel, E. 1890. Planktonic studies: a comparative investigation of the importance and constitution
of the pelagic fauna and flora. Jena. Z. 25 (Engl. transl. 1892, Rep U.S. Commnr. Fish Fish.,
1889-91, pp. 565-641).
Hamner, W. M. 1984. Aspects of schooling in Euphausia superba. J. Crust. BioI. (Spec. No. I):
67-74.
--.
1985. The importance of ethology for investigations of marine zooplankton. Bull. Mar. Sci.
37: 414-424.
--.
1988. The 'lost year' of the sea turtle. TREE 3: 116-118.
--,
P. P. Hamner, S. W. Strand and R. W. Gilmer.
1983. Behavior of Antarctic krill, Euphausia
superba: chemoreception,
feeding, schooling, and molting. Science 220: 433-435.
---,
L. P. Madin, A. L. Alldredge, R. W. Gilmer and P. P. Hamner.
1975. Underwater observations of gelatinous zooplankton:
sampling problems, feeding biology, and behavior. Limnol.
Oceanogr. 20: 907-917.
---,
S. W. Strand, G. I. Matsumoto and P. P. Hamner.
1987. Ethological observations on foraging
behavior of the ctenophore Leucothea pulchra in the open sea. Limnol. Oceanogr. 32: 645-652.
Harder, W. 1968. Reactions of plankton organisms to water stratification. Limnol. Oceanogr. 13:
156-168.
Hardy, A. 1965. The open sea: its natural history. Part I: the world of plankton. Houghton Mifflin,
Boston. 335 pp.
Haury, L. R., J. A. McGowan and P. H. Wiebe.
1978. Patterns and processes in the time-space
scales of plankton distributions.
Pages 277-327 in J. H. Steele, ed. Spatial pattern in plankton
communities.
Plenum Press, New York.
Isaacs, J. D. 1977. The life of the open sea. Nature 267: 778-780.
Morin, J. G. 1986. "Firefleas" of the sea: luminescent signaling in marine ostracode crustaceans.
Fla. Entomol. 69: 105-121.
Omori, M. and W. M. Hamner.
1982. Patchy distribution
of zooplankton:
behavior, population
assessment and sampling problems. Mar. BioI. 72: 193-200.
Paffenhofer, G.-A., B. T. Wester and W. D. Nicholas.
1984. Zooplankton abundance in relation to
state and type of intrusions onto the southeastern
United States shelf during summer. J. Mar.
Res. 42: 995-1017.
Parsons, T. R. 1976. The structure oflife in the sea. Pages 81-97 in D. H. Cushing and J. J. Walsh,
eds. The ecology of the seas. Blackwell Scientific Publications, Oxford.
Pickett, S. T. A. and P. S. White.
1985. The ecology of natural disturbance and pateh dynamics.
Academic Press, New York. 472 pp.
Russell, F. S. 1970. The medusae of the British Isles. II. Pelagic Scyphozoa with a supplement to
the first volume on hydromedusae.
Cambridge Univ. Press, Cambridge. 284 pp.
HAMNER: SWIMMING BEHAVIOR AND PATCHINESS
757
Smetacek, V. and F. Pollehne. 1986. Nutrient cycling in pelagic systems: a reappraisal of the conceptual framework. Ophelia 26: 401-428.
Sousa, W. P. 1985. Disturbance and patch dynamics on rocky intertidal shores. Pages 101-123 in
S. T. A. Pickett and P. S. White, eds. The ecology of natural disturbance and patch dynamics.
Academic Press, New York.
Steele, J. H., ed. 1978. Spatial pattern in plankton communities. Plenum Press, New York. 470 pp.
--.
1985. A comparison of terrestrial and marine ecological systems. Nature 313: 355-358.
White, P. S. and S. T. A. Pickett. 1985. Natural disturbance and patch dynamics: an introduction.
Pages 3-13 in S. T. A. Pickett and P. S. White, eds. The ecology of natural disturbance and patch
dynamics. Academic Press, New York.
Wiebe, P. H., E. M. Hulburt, E. J. Carpenter, A. E. Jahn, G. P. Knapp III, S. H. Boyd, P. B. Ortner
and J. L. Cox. 1976. Gulf Stream cold core rings: large-scale interaction sites for open ocean
plankton communities. Deep-Sea Res. 23: 695-710.
DATE ACCEPTED:
ADDRESS:
May 17, 1988.
Department oj Biology, University oj California, Los Angeles, California 90024-1606.
ApPENDIX:
DISCUSSION AFfER
HAMNER
J. Atema: I would disagree with your statement that one difference between ter-
restrial and pelagic aquatic environments is that there's nowhere to hide in
the ocean. Whether something is a hiding place depends upon the sensory
capabilities of whatever it's hiding from, and shouldn't be assessed from the
viewpoint of those of us that rely primarily on vision. We need to define the
details of the sensory environment that each animal perceives.
C. Boyd: One problem with doing good behavioral work on zooplankton may be
that none of us have any formal training in that field. Instead of immediately
collecting more data, maybe we all would benefit from going back and taking
some ethology courses.
W. Hamner: I agree with that, but probably we could benefit just from reading
some of the classic ethology texts like Tinbergen's rather than taking courses.
Most oceanography departments today have a dismal record in this areabiologists trained in them graduate knowing nothing about evolution and
behavior.
C. Keifoot: But half of the behavior we observe may be irrelevant to population
processes. We need to know whether variations in behavior result in differences in births or deaths, or whether behavior is a "carry-over" of historical
events that are no longer relevant. How much do behavioral studies really
contribute to our understanding of community processes?
W. Hamner: Andy Heron's study on Thalia is the only one to define cohorts.
Very few other studies have been able to follow discrete populations, which
is a major difference between the disciplines oflimnology and oceanography.
Because oceanographers can seldom delimit the populations that they study,
many of us have turned to investigations of behavior phenomena that can
be studied with individuals.
J. Atema: Any good scientists, whether they work on communities, populations,
individual behavior or physiology, should "bracket" their own research by
considering the implications of their findings for the levels above and below.
P. Verity: I agree. If each of you think about the papers which you feel are the
best examples of research in your field, they invariably have the following
characteristics in common: (I) a thorough knowledge of the physiology of
the test species, and (2) an equivalent awareness of factors influencing the
activities of organisms one trophic level removed. I would urge all of us to
resist the temptation to measure processes as flows in and out of a black box.
Start with the "bug" and work up from there.