Download The Study of Vertical Zonation on Rocky Intertidal Shores—A

INTEG.
AND
COMP. BIOL., 42:776–779 (2002)
The Study of Vertical Zonation on Rocky Intertidal Shores—A Historical Perspective1,2
KEITH R. BENSON3
Science and Technology Studies, National Science Foundation, Arlington, Virginia 22230
SYNOPSIS. Intertidal zonation, observed from earliest studies of the marine littoral zone, was first studied
in the U.S. by ecologists with a botanical orientation. Using the physiological methods favored by Cowles,
Clements, and Shelford, these early studies sought causal and deterministic explanations. By the 1930s, the
limitations of these studies became apparent and ecologists returned to more descriptive approaches. With
the creation of year round research laboratories on the west coast, ecologists soon shed the botanical orientation and began to adopt more stochastic and non-deterministic approaches to intertidal ecology, approaches that still characterize the research tradition.
Although a complete historical review of intertidal
ecology would be far beyond the scope of this review,
what follows are a few salient reflections on the field
primarily within its American context. In doing so,
these comments center on many of the more influential
features selected from the numerous historical events
crucial to the formation of intertidal ecology. Thus, the
paper will emphasize the early twentieth-century influence of physiology and experimentation on the formation of American ecology, the formation of marine
ecology within curricula at marine stations in the U.S.,
the re-emergence of natural history within the context
of intertidal ecology in the 1930s, and the crucial role
that permanent and year around marine institutions
played in the development of intertidal ecology.
The now well-known zonation patterns observed
within intertidal communities worldwide was first noted along the shorelines in Europe and the United
States in the late nineteenth century. In fact, one of
the earliest works in American marine biology was
conducted by A. E. Verrill between 1870 and 1873,
surveying the groupings of invertebrate animals in
Vineyard Sound, the area adjacent to the present-day
MBL in Woods Hole (Verrill, 1872). Several other descriptive studies appeared by the beginning of the
twentieth century, all noting the characteristic zonation
patterns along the littoral fringes of the coastline but
without any discussion of the causes for the patterns
(Summer, 1908). At this time, as many historians have
stressed, biology was mainly a descriptive and historical science. Indeed, studies along the marine zone followed Anton Dohrn’s admonition in the 1870s to use
marine organisms to evaluate the accuracy of Charles
Darwin’s new theory of evolution. Following Dohrn’s
tradition at the Stazione Zoologica in Naples, this
meant the careful description of the adaptive strategies
employed over historical time by organisms to live
where they were located.
A number of historians of science have recently argued that physiological methods invaded the natural
history oriented biological sciences in the United
States at the end of the nineteenth century and the
beginning of the twentieth century (Allen, 1975; Rainger et al., 1988). In part, the invasion was facilitated
by many younger biologists who had become dissatisfied with the descriptive orientation of natural history, descriptions that usually ignored the cause and
effect relationships common in the physical sciences.
After all, physiologists did not pursue historical explanations in their investigations of animal function; instead they sought the proximate causes behind adaptive strategies employed by organisms. But perhaps
just as important, many younger naturalists wanted to
place their scientific interests on a more exact footing,
one that mirrored the precision of the physical sciences
and one that allowed them to test their observations
rigorously. Physiology’s orientation offering causal
factors provided the naturalists with the new methodological approach they desired.
Such causal explanations depended upon either
careful measurements of the underlying physical conditions surrounding the fauna and flora or careful laboratory experimentation to determine the factors behind the distribution of plants and animals. Both aspects were incorporated by Frederic Clements in his
Research Methods in Ecology (1905) and in Charles
Adams’s 1913 work Guide to the Study of Animal
Ecology (Clements, 1905; Adams, 1913). Clements
and Adams stressed the need to understand the physical features of a landscape, features that causally determined the nature of the biotic communities. In fact,
Clements went so far as to suggest in Plant Succession
(1916) that it was the physical factors of the environment that deterministically controlled plant communities (Clements, 1916). Furthermore, these communities developed in an step-wise and predictable or-
1 From the Symposium Physiological Ecology of Rocky Intertidal
Organisms: From Molecules to Ecosystems presented at the Annual
Meeting of the Society for Comparative and Integrative Biology, 2–
7 January 2002, at Anaheim, California.
2 This review is dedicated to the memory of Larry McEdward. He
was one of my first students at the University of Washington, he
was instrumental in suggesting to me the need to study the history
of intertidal ecology, and he was a wonderful human being. In addition, he was a superb developmental biologist, working on marine
larval development often at Friday Harbor Laboratories. Larry died
unexpectedly this past summer . . . and while his presence in many
of our lives will be missed, he left an indelible memory among his
legions of friends and colleagues.
3 E-mail: [email protected]
776
HISTORY
OF INTERTIDAL
ganic fashion through a series of successional communities to an optimum state, the climax community,
all under the control of physical features.
The most influential biologist for marine investigations who was profoundly affected by the tradition
from Clements and Adams was the University of Chicago biologist Henry Chandler Cowles. Basing his
work upon his earlier investigations of sand dune communities, primarily botanical, adjacent to Lake Michigan (Cowles, 1899), he carried the program to Washington’s San Juan Islands, where he implemented the
country’s first course in ‘‘marine ecology’’ at the new
marine station for the University of Washington.
Cowles’s intent was to develop a ‘‘physiographic ecology’’ along the west coast that mirrored his sand dune
work, emphasizing the botanical approaches typical of
ecology in the early twentieth century. But importantly, Cowles was not a slavish advocate of Clements’s
successional ideas. Having been deeply impressed in
his early geology training by T. C. Chamberlain’s arguments for multiple working hypotheses in science
(Chamberlain, 1897), Cowles was constantly on the
lookout for experimental approaches to challenge existing ideas in ecology.
This same pragmatic attitude was imparted to his
most famous student, Victor Shelford, who followed
his mentor to Friday Harbor and then taught the marine ecology course every other summer from 1912
until 1928 (Benson, 1992). Shelford extended
Cowles’s work, now referring to ‘‘physiological animal geography’’ as he attempted to determine the
physical features that could explain the distribution of
sessile invertebrate forms in the intertidal communities, much like ecologists had done earlier on the sessile botanical forms. Taking animals into the laboratory at Friday Harbor, Shelford experimentally
searched for causal explanations for zonation. Importantly, and clearly associating his work with the new
directions in biology, he stated that this new method
enabled ecologists to free themselves from historical
explanations by examining intertidal communities for
proximate causes, not the ultimate causes associated
with the former descriptive studies. However, by 1928
the experimental approach, modeled on plant ecology,
failed. Shelford was not able to uncover the physiological mechanisms to explain zonation patters and he
concluded that the ‘‘time was not right’’ for the laboratory-based investigations. Instead, he called for a return to descriptive studies in the natural history tradition, including a return to extensive surveys of community structure along the Pacific coastline (Benson,
1992).
At this same time, Shelford knew there was a complementary approach to American marine ecology, an
approach pioneered by the Danish biologist C. G. J.
Petersen. Petersen had been investigating the collapse
of the North Sea fishery by examining the community
structure of the benthic zone in the early twentieth century. Working with a specialized bottom dredge, he
was able to demonstrate how specific areas of the
ECOLOGY
777
ocean’s floor had characteristic community structure
depending on the physical characteristics of the region
(Petersen, 1913). Thus, it did not matter if one examined the marine zone intertidally or benthically, familiar patterns for community structure predominated.
Additional work by A. C. Stephens in 1933 along the
Scottish coastline extended these patterns geographically, illustrating the quantitative ordering of intertidal
communities over their intertidal range (Stephens,
1933). Thus, natural history re-emerged within marine
ecology to add to the understanding of the growing
universality of marine community structure, with increasing evidence based on faunistic characteristics not
patterned from floristic studies.
By the 1930s, the infrequent botanical references
almost completely disappeared, the term physiological
animal geography was dropped, and marine ecology
emerged as part of the American ecological tradition,
especially at marine laboratories along the west coast.
In addition, descriptive studies of marine communities
predominated, now pointing to the interrelationships of
the organisms making up the structure of those communities. Of course, by this same time Clements’s successional program had generated much controversy,
especially in terms of succession’s almost complete reliance upon physical factors as causal agents and in
terms of the deterministic nature of the successional
stages. Among those who attacked Clements, Charles
Elton emphasized the importance of an organism’s
niche (Elton, 1927) and A. G. Tansley offered a new
ontological basis for ecology with his notion of the
ecosystem (Tansley, 1935). In other words, both Elton
and Tansley appreciated the need to consider biotic
factors in ecology, overtly turning away from the abiotic factors preferred by the more physiologically-oriented plant ecologists.
The new biotic focus of marine ecology gave the
natural history approach renewed support. By this
time, the Chicago school of ecology, now directed by
Warder C. Allee, also began to emphasize studies of
community structure, only now adopting a sociological
spin (Mitman, 1992). But this was no accident, for
Allee attracted to his program a sociologist, Thomas
Park, who brought to ecology his own bias for studying the role of community structure. The influence of
Park was noticeable and immediate, especially in Allee’s early animal aggregation work, published in 1927
and 1931 (Allee, 1927, Allee, 1931). Missing was the
traditional emphasis on physical factors, now replaced
by the interactions of the organisms making up the
community. Then Thorsten Gislen published his influential work in what he called ‘‘marine sociology,’’ noting the plant-animal communities characteristic of marine community structure (Gislen, 1930, 1931). Gislen
first characterized the nature of the physical environment he was investigating, then provided the ‘‘associations’’ that inhabited that specific environment.
John Colman extended and elaborated upon Gislen’s
approach, noting that the physical features created tolerance levels that would limit the distribution of ani-
778
KEITH R. BENSON
mal associations, but that sociological factors regulated
the recruitment patterns within the tolerable environments (Colman, 1936). Thus, a new population orientation emerged within marine ecology by the end of
the 1930s.
At this same time, the first longitudinal natural history studies of marine environments were conducted
by George MacGinitie. MacGinitie had been hired by
the geneticist T. H. Morgan to found Caltech’s marine
laboratory, the Kerckhoff Marine Laboratory in Corona del Mar. As a fulltime marine ecologist with no
teaching responsibilities at a land-bound university,
unusual at the time, MacGinitie turned his attention to
study over time the Elkhorn Slough near Monterey
Bay during the 1930s, eventually publishing ‘‘Ecological aspects of a California marine estuary’’ in 1935
(MacGinitie, 1935). In this work, he illustrated the
need for marine ecology to be based on long-term
studies, not merely summer time examinations of an
intertidal community. MacGinitie later wrote that intertidal ecology must be based on the ‘‘study of the
social life of animals and their relationship to their
environment,’’ adding to this the critical element of
the individual life histories of the organisms under investigation. Critiquing directly the early and influential
work of Shelford, he emphasized that laboratory approaches alone would not work. In their place, the marine ecologist must accept the variable and dynamic
nature of marine communities, which required continuous natural history observations within a field setting.
Borrowing a statement from his colleague W. E. Allen
from Scripps, he claimed: ‘‘. . . the way to learn about
anything is to go to it directly, get as much contact
with it as possible, and study it as much as possible
in the conditions of its natural existence’’ (MacGinitie,
1935).
Willis G. Hewatt, a Stanford graduate student working at Hopkins Marine Station, adopted MacGinitie’s
recommendation for long-term study of intertidal communities but incorporated field experiments to investigate the dynamic nature of marine communities. In
a classic paper in 1937, ‘‘Ecological studies on selected marine intertidal communities of Monterey Bay,
California,’’ Hewatt studied denuded rocks to determine how animals are recruited to marine environments and how animal dynamics change as the community develops in time (Hewatt, 1937). His conclusions included the then surprising hypothesis that the
ranges of intertidal animals are more related to biological phenomena than physical phenomena, especially
those phenomena of interspecific relationships for food
and shelter. Extending Hewatt’s work to zonation in
the southern hemisphere, T. A. Stephenson noted similar observations. In a review article, he concluded that
physical factors were most important to determine the
upper and lower limits of intertidal communities, but
biological factors predominated in life between the
tidemarks (Stephenson, 1949).
There was one additional and critical factor behind
the impressive new insights into intertidal communi-
ties made by biologists in the 1930s and 1940s. With
few exceptions, the work was done by west coast investigators who had access to marine laboratories that
were open all year. In California, the Hopkins Marine
Station, the Kerckhoff laboratory, and Scripps Institution were year around facilities with full time staffs
of researchers by 1930. Of course, by this time Scripps
had made a move away from pure marine biology to
more oceanographic work, but W. K. Fisher at Hopkins and George MacGinitie at Caltech’s laboratory
either conducted year around research or encouraged
others to do the same. This type of longterm attention
was the essential factor, first, to frame a new approach
to study the dynamics of intertidal communities and,
second, to enable researchers to obtain information
from prolonged observations and experimentation. To
the north, Friday Harbor first started work in intertidal
ecology in 1906, but the laboratory was open for researchers like Shelford only during the summer
months. Then in 1930, the laboratory also received
funding from the Rockefeller Foundation to pursuer an
oceanographic focus and further studies in marine
ecology were not renewed until the early 1950s.
Armed with information from these longtitudinal
studies, by the mid twentieth century intertidal ecology
emerged completely free from its traditional roots in
botanical ecology, emphasizing physical causes. This
change enabled marine ecology to take full advantage
of a new perspective, pointing to the dynamic nature
of intertidal communities. Combining the population
biology approach from the Chicago school of Allee,
modeling from ecosystem ecology popularized by the
Hutchinson and Odum schools, and the growing preference for testing hypotheses through carefully constructed experiments, studies of intertidal zonation
soon made impressive and substantial contributions to
twentieth-century ideas of animal ecology. Even more
important, however, was the growing appreciation and
acceptance in the 1960s and later that ecological research might not be as predictive and exact as research
in the physical sciences. Indeed, one of the cherished
assumptions of ecology, dating from Stephen Forbes’s
work on lakes at the end of the nineteenth century that
the natural world existed in some kind of finely balanced equilibrium state, a state that could be known
(Forbes, 1887), soon gave way to the notion of the
thoroughly dynamic and stochastic nature of the natural world. Demonstrated most convincingly in recent
studies by Robert Paine, J. H. Connell, and Paul Dayton, marine ecologists now consider intertidal zonation
patterns to reflect a snapshot of marine communities
in time, not the deterministic result of physical features
(Paine, 1966; Connell, 1961; Dayton, 1971).
Admittedly, this historical treatment of intertidal zonation has been very sketchy. Neverthless, it is important to understand how early notions of marine
communities were initially influenced by investigators
closely tied to the botanical biases of physiological
ecology, especially in the work of Clements, Cowles,
and Shelford. A new direction was promised with the
HISTORY
OF INTERTIDAL
self-conscious formation of marine ecology within the
context of the new marine laboratories, which soon
called for more comprehensive natural history investigations of marine communities. These studies, especially along the U.S. west coast in the 1930s revealed
the inadequacy of both the botanical approach and laboratory-based experiments. By the Second World War,
several marine ecologists suggested that physical factors, so popular with earlier studies, were important
only as limiting factors for the marine fauna and flora.
The intriguing zonation patterns that attracted the attention of biologists in the first place, were the product
of biotic factors. Of course, the limiting condition up
to this time was that year-around marine stations
equipped to facilitate the longitudinal investigations
necessary to ask these questions and to evaluate the
results of the investigations did not exist. But by the
fifth decade of the twentieth century, this condition
had been remedied, funding for the work was provided
from federal sources (ONR and NSF) in the century’s
sixth decade, and marine ecology entered into its modern phase.
In conclusion and from the perspective of an historian, the current suggestion for greater collaboration
between physiologists and ecologists implicit in the
context of this symposium represents an indication of
the maturity of marine ecology. After all, faced with
the new challenges of the twenty-first century, it requires a certain amount of confidence for investigators
within a specific and well-defined field to call for more
integration from other fields such as physiology, genetics, and molecular biology. Certainly such an invitation is a harbinger for a robust and productive future in intertidal ecology.
REFERENCES
Adams, C. C. 1913. Guide to the study of animal ecology. Macmillan, New York.
Allee, W. C. 1927. Animal aggregation. Quarterly Review of Biology 2:367–398.
Allee, W. C. 1931. Animal aggregations: A study in general sociology. University of Chicago Press, Chicago.
Allen, G. 1975. Life science in the twentieth century. John Wiley,
New York.
Benson, K. R. 1992. Victor Shelford and a failed method for ecology. History and Philosophy of the Life Sciences 14:34–56.
Chamberlain, T. C. 1897. The method of multiple working hypotheses. Journal of Geology 5:837–848.
Clements, F. E. 1905. Research methods in ecology. University Publishing Company, Lincoln.
Clements, F. E. 1916. Plant succession: An analysis of the development of vegetation. Carnegie Institution of Washington,
Washington, D.C.
Colman, J. 1933. The nature of the intertidal zonation of plants and
animals. J. Mar. Biol. Assoc. 18:435–476.
ECOLOGY
779
Connell, J. H. 1961. The influence of intro-specific competition and
other factors on the distribution of the barnacle Chthamalus
stellatus. Ecology 42:710–723.
Cowles, H. C. 1899. The ecological relations of the vegetation of
the sand dunes of Lake Michigan. Botanical Gazette 27:95–117;
167–202;281–308;361–391.
Dayton, P. 1971. Competition, disturbance, and community organization: The provision of subsequent utilization of space in a
rocky intertidal community. Ecol. Mono. 41:351–389.
Elton, C. 1927. Animal ecology. Metheun, London.
Forbes, S. A. 1887. The lake as microcosm. Bulletin of the Science
Association of Peoria, Illinois. 1887:77–87.
Gislen, T. 1930. Epibiosis of the Gullman fjord. II. Kristinebergs
Zoological Station 4:1–380.
Gislen, T. 1931. A survey of the marine associations of the Misaki
district. J. Fac. Sci., Imperial Univ. of Tokyo 2:389–444.
Hewatt, W. G. 1937. Ecological studies on selected marine intertidal
communities of Monterey Bay, California. Am. Midl. Nat. 18:
161–206.
MacGinitie, G. E. 1935. Ecological aspects of a California marine
estuary. Am. Midl. Nat. 16:629–765.
MacGinitie, G. E. 1939. Littoral marine communities. American
Midland Naturalist 21:28–55.
McIntosh, Robert P. 1985. The background of ecology: Concept and
theory. Cambridge University Press, New York.
Mitman, G. 1992. The state of nature: Ecology, community and
American social thought, 1900–1950. University of Chicago
Press, Chicago.
Odum, E. P. 1953. Fundamentals of ecology. Saunders, Philadelphia.
Paine, R. T. 1966. Food web complexity of species diversity. Am.
Nat. 100:65–75.
Petersen, C. G. J. 1913. Valuation of the sea. II. The animal communities of the sea bottom and their importance for marine zoogeography. Reports of the Danish Biological Station 21:1–44.
Rainger, R., K. R. Benson, and J. Maienschein. 1988. The American
development of biology. University of Pennsylvania Press, Philadelphia.
Shelford, V. E. 1916. Physiological differences between marine animals from different depths. Publications of the Puget Sound
Biological Station 1:157–174.
Shelford, V. E. 1925–28. Animal communities of the San Juan Channel and adjacent areas. Publications of the Puget Sound Biological Station 5:37–73.
Shelford, V. E. 1929. Geographical extent and succession in Pacific
North Ameircan intertidal barnacles (Balanus) communities. Puget Sound Biological Station 7:217–223.
Shelford, V. E. 1935. Some marine biotic communities of the Pacific
coast of North America. Ecological Monographs 5:251–354.
Stephens, A. C. 1933. Studies on the Scottish marine fauna: The
natural faunistic divisions of the North Sea illustrated by quantitative distribution of the mollusks. Transactions of the Royal
Society of Edinburgh 57:391.
Stephenson, T. A. and A. Stephenson. 1949. The universal feature
of zonation between tidemarks on rocky coasts. J. Ecol. 37:289–
305.
Sumner, F. B. 1908. An intensve study of fauna and flora on a restricted area of sea bottom. Bulletin of the U.S. Bureau of Fisheries 28:1125–1263.
Tansley, A. G. 1935. The use and abuse of vegatational concepts
and terms. Ecology 16:284–307.
Verrill, A. E. 1871–72. Report on the invertebrate animals of Vineyard Sound and adjacent waters. Report of the U. S. Fish Commission 296–778.