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The Study of Vertical Zonation on Rocky Intertidal Shores—A HistoricalPerspectiveAuthor(s): Keith R. BensonSource: Integrative and Comparative Biology, 42(4):776-779. 2002.Published By: The Society for Integrative and Comparative BiologyDOI: http://dx.doi.org/10.1093/icb/42.4.776URL: http://www.bioone.org/doi/full/10.1093/icb/42.4.776
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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 studiedin 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, thelimitations of these studies became apparent and ecologists returned to more descriptive approaches. Withthe creation of year round research laboratories on the west coast, ecologists soon shed the botanical ori-entation and began to adopt more stochastic and non-deterministic approaches to intertidal ecology, ap-proaches that still characterize the research tradition.
Although a complete historical review of intertidalecology would be far beyond the scope of this review,what follows are a few salient reflections on the fieldprimarily within its American context. In doing so,these comments center on many of the more influentialfeatures selected from the numerous historical eventscrucial to the formation of intertidal ecology. Thus, thepaper will emphasize the early twentieth-century influ-ence of physiology and experimentation on the for-mation of American ecology, the formation of marineecology within curricula at marine stations in the U.S.,the re-emergence of natural history within the contextof intertidal ecology in the 1930s, and the crucial rolethat permanent and year around marine institutionsplayed in the development of intertidal ecology.
The now well-known zonation patterns observedwithin intertidal communities worldwide was first not-ed along the shorelines in Europe and the UnitedStates in the late nineteenth century. In fact, one ofthe earliest works in American marine biology wasconducted by A. E. Verrill between 1870 and 1873,surveying the groupings of invertebrate animals inVineyard Sound, the area adjacent to the present-dayMBL in Woods Hole (Verrill, 1872). Several other de-scriptive studies appeared by the beginning of thetwentieth century, all noting the characteristic zonationpatterns along the littoral fringes of the coastline butwithout any discussion of the causes for the patterns(Summer, 1908). At this time, as many historians havestressed, biology was mainly a descriptive and histor-ical science. Indeed, studies along the marine zone fol-lowed Anton Dohrn’s admonition in the 1870s to use
1 From the Symposium Physiological Ecology of Rocky IntertidalOrganisms: From Molecules to Ecosystems presented at the AnnualMeeting 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. Hewas one of my first students at the University of Washington, hewas instrumental in suggesting to me the need to study the historyof intertidal ecology, and he was a wonderful human being. In ad-dition, he was a superb developmental biologist, working on marinelarval development often at Friday Harbor Laboratories. Larry diedunexpectedly this past summer . . . and while his presence in manyof our lives will be missed, he left an indelible memory among hislegions of friends and colleagues.
3 E-mail: [email protected]
marine organisms to evaluate the accuracy of CharlesDarwin’s new theory of evolution. Following Dohrn’stradition at the Stazione Zoologica in Naples, thismeant the careful description of the adaptive strategiesemployed over historical time by organisms to livewhere they were located.
A number of historians of science have recently ar-gued that physiological methods invaded the naturalhistory oriented biological sciences in the UnitedStates at the end of the nineteenth century and thebeginning of the twentieth century (Allen, 1975; Rain-ger et al., 1988). In part, the invasion was facilitatedby many younger biologists who had become dissat-isfied with the descriptive orientation of natural his-tory, descriptions that usually ignored the cause andeffect relationships common in the physical sciences.After all, physiologists did not pursue historical expla-nations in their investigations of animal function; in-stead they sought the proximate causes behind adap-tive strategies employed by organisms. But perhapsjust as important, many younger naturalists wanted toplace their scientific interests on a more exact footing,one that mirrored the precision of the physical sciencesand one that allowed them to test their observationsrigorously. Physiology’s orientation offering causalfactors provided the naturalists with the new method-ological approach they desired.
Such causal explanations depended upon eithercareful measurements of the underlying physical con-ditions surrounding the fauna and flora or careful lab-oratory experimentation to determine the factors be-hind the distribution of plants and animals. Both as-pects were incorporated by Frederic Clements in hisResearch Methods in Ecology (1905) and in CharlesAdams’s 1913 work Guide to the Study of AnimalEcology (Clements, 1905; Adams, 1913). Clementsand Adams stressed the need to understand the phys-ical features of a landscape, features that causally de-termined 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 environ-ment that deterministically controlled plant commu-nities (Clements, 1916). Furthermore, these commu-nities developed in an step-wise and predictable or-
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ganic fashion through a series of successional com-munities to an optimum state, the climax community,all under the control of physical features.
The most influential biologist for marine investiga-tions who was profoundly affected by the traditionfrom Clements and Adams was the University of Chi-cago biologist Henry Chandler Cowles. Basing hiswork upon his earlier investigations of sand dune com-munities, primarily botanical, adjacent to Lake Mich-igan (Cowles, 1899), he carried the program to Wash-ington’s San Juan Islands, where he implemented thecountry’s first course in ‘‘marine ecology’’ at the newmarine station for the University of Washington.Cowles’s intent was to develop a ‘‘physiographic ecol-ogy’’ along the west coast that mirrored his sand dunework, emphasizing the botanical approaches typical ofecology in the early twentieth century. But important-ly, Cowles was not a slavish advocate of Clements’ssuccessional ideas. Having been deeply impressed inhis early geology training by T. C. Chamberlain’s ar-guments for multiple working hypotheses in science(Chamberlain, 1897), Cowles was constantly on thelookout for experimental approaches to challenge ex-isting ideas in ecology.
This same pragmatic attitude was imparted to hismost famous student, Victor Shelford, who followedhis mentor to Friday Harbor and then taught the ma-rine ecology course every other summer from 1912until 1928 (Benson, 1992). Shelford extendedCowles’s work, now referring to ‘‘physiological ani-mal geography’’ as he attempted to determine thephysical features that could explain the distribution ofsessile invertebrate forms in the intertidal communi-ties, much like ecologists had done earlier on the ses-sile botanical forms. Taking animals into the labora-tory at Friday Harbor, Shelford experimentallysearched for causal explanations for zonation. Impor-tantly, and clearly associating his work with the newdirections in biology, he stated that this new methodenabled ecologists to free themselves from historicalexplanations by examining intertidal communities forproximate causes, not the ultimate causes associatedwith the former descriptive studies. However, by 1928the experimental approach, modeled on plant ecology,failed. Shelford was not able to uncover the physio-logical mechanisms to explain zonation patters and heconcluded that the ‘‘time was not right’’ for the labo-ratory-based investigations. Instead, he called for a re-turn to descriptive studies in the natural history tradi-tion, including a return to extensive surveys of com-munity structure along the Pacific coastline (Benson,1992).
At this same time, Shelford knew there was a com-plementary approach to American marine ecology, anapproach pioneered by the Danish biologist C. G. J.Petersen. Petersen had been investigating the collapseof the North Sea fishery by examining the communitystructure of the benthic zone in the early twentieth cen-tury. Working with a specialized bottom dredge, hewas able to demonstrate how specific areas of the
ocean’s floor had characteristic community structuredepending on the physical characteristics of the region(Petersen, 1913). Thus, it did not matter if one ex-amined the marine zone intertidally or benthically, fa-miliar patterns for community structure predominated.Additional work by A. C. Stephens in 1933 along theScottish coastline extended these patterns geographi-cally, illustrating the quantitative ordering of intertidalcommunities over their intertidal range (Stephens,1933). Thus, natural history re-emerged within marineecology to add to the understanding of the growinguniversality of marine community structure, with in-creasing evidence based on faunistic characteristics notpatterned from floristic studies.
By the 1930s, the infrequent botanical referencesalmost completely disappeared, the term physiologicalanimal geography was dropped, and marine ecologyemerged as part of the American ecological tradition,especially at marine laboratories along the west coast.In addition, descriptive studies of marine communitiespredominated, now pointing to the interrelationships ofthe organisms making up the structure of those com-munities. Of course, by this same time Clements’s suc-cessional program had generated much controversy,especially in terms of succession’s almost complete re-liance upon physical factors as causal agents and interms of the deterministic nature of the successionalstages. Among those who attacked Clements, CharlesElton emphasized the importance of an organism’sniche (Elton, 1927) and A. G. Tansley offered a newontological basis for ecology with his notion of theecosystem (Tansley, 1935). In other words, both Eltonand Tansley appreciated the need to consider bioticfactors in ecology, overtly turning away from the abi-otic factors preferred by the more physiologically-ori-ented plant ecologists.
The new biotic focus of marine ecology gave thenatural history approach renewed support. By thistime, the Chicago school of ecology, now directed byWarder C. Allee, also began to emphasize studies ofcommunity structure, only now adopting a sociologicalspin (Mitman, 1992). But this was no accident, forAllee attracted to his program a sociologist, ThomasPark, who brought to ecology his own bias for study-ing the role of community structure. The influence ofPark was noticeable and immediate, especially in Al-lee’s early animal aggregation work, published in 1927and 1931 (Allee, 1927, Allee, 1931). Missing was thetraditional emphasis on physical factors, now replacedby the interactions of the organisms making up thecommunity. Then Thorsten Gislen published his influ-ential work in what he called ‘‘marine sociology,’’ not-ing the plant-animal communities characteristic of ma-rine community structure (Gislen, 1930, 1931). Gislenfirst characterized the nature of the physical environ-ment he was investigating, then provided the ‘‘asso-ciations’’ that inhabited that specific environment.John Colman extended and elaborated upon Gislen’sapproach, noting that the physical features created tol-erance levels that would limit the distribution of ani-
778 KEITH R. BENSON
mal associations, but that sociological factors regulatedthe recruitment patterns within the tolerable environ-ments (Colman, 1936). Thus, a new population ori-entation emerged within marine ecology by the end ofthe 1930s.
At this same time, the first longitudinal natural his-tory studies of marine environments were conductedby George MacGinitie. MacGinitie had been hired bythe geneticist T. H. Morgan to found Caltech’s marinelaboratory, the Kerckhoff Marine Laboratory in Co-rona del Mar. As a fulltime marine ecologist with noteaching responsibilities at a land-bound university,unusual at the time, MacGinitie turned his attention tostudy over time the Elkhorn Slough near MontereyBay during the 1930s, eventually publishing ‘‘Ecolog-ical aspects of a California marine estuary’’ in 1935(MacGinitie, 1935). In this work, he illustrated theneed for marine ecology to be based on long-termstudies, not merely summer time examinations of anintertidal community. MacGinitie later wrote that in-tertidal ecology must be based on the ‘‘study of thesocial life of animals and their relationship to theirenvironment,’’ adding to this the critical element ofthe individual life histories of the organisms under in-vestigation. Critiquing directly the early and influentialwork of Shelford, he emphasized that laboratory ap-proaches alone would not work. In their place, the ma-rine ecologist must accept the variable and dynamicnature of marine communities, which required contin-uous natural history observations within a field setting.Borrowing a statement from his colleague W. E. Allenfrom Scripps, he claimed: ‘‘. . . the way to learn aboutanything is to go to it directly, get as much contactwith it as possible, and study it as much as possiblein the conditions of its natural existence’’ (MacGinitie,1935).
Willis G. Hewatt, a Stanford graduate student work-ing at Hopkins Marine Station, adopted MacGinitie’srecommendation for long-term study of intertidal com-munities but incorporated field experiments to inves-tigate the dynamic nature of marine communities. Ina classic paper in 1937, ‘‘Ecological studies on se-lected marine intertidal communities of Monterey Bay,California,’’ Hewatt studied denuded rocks to deter-mine how animals are recruited to marine environ-ments and how animal dynamics change as the com-munity develops in time (Hewatt, 1937). His conclu-sions included the then surprising hypothesis that theranges of intertidal animals are more related to biolog-ical phenomena than physical phenomena, especiallythose phenomena of interspecific relationships for foodand shelter. Extending Hewatt’s work to zonation inthe southern hemisphere, T. A. Stephenson noted sim-ilar observations. In a review article, he concluded thatphysical factors were most important to determine theupper and lower limits of intertidal communities, butbiological factors predominated in life between thetidemarks (Stephenson, 1949).
There was one additional and critical factor behindthe impressive new insights into intertidal communi-
ties made by biologists in the 1930s and 1940s. Withfew exceptions, the work was done by west coast in-vestigators who had access to marine laboratories thatwere open all year. In California, the Hopkins MarineStation, the Kerckhoff laboratory, and Scripps Insti-tution were year around facilities with full time staffsof researchers by 1930. Of course, by this time Scrippshad made a move away from pure marine biology tomore oceanographic work, but W. K. Fisher at Hop-kins and George MacGinitie at Caltech’s laboratoryeither conducted year around research or encouragedothers to do the same. This type of longterm attentionwas the essential factor, first, to frame a new approachto study the dynamics of intertidal communities and,second, to enable researchers to obtain informationfrom prolonged observations and experimentation. Tothe north, Friday Harbor first started work in intertidalecology in 1906, but the laboratory was open for re-searchers like Shelford only during the summermonths. Then in 1930, the laboratory also receivedfunding from the Rockefeller Foundation to pursuer anoceanographic focus and further studies in marineecology were not renewed until the early 1950s.
Armed with information from these longtitudinalstudies, by the mid twentieth century intertidal ecologyemerged completely free from its traditional roots inbotanical ecology, emphasizing physical causes. Thischange enabled marine ecology to take full advantageof a new perspective, pointing to the dynamic natureof intertidal communities. Combining the populationbiology approach from the Chicago school of Allee,modeling from ecosystem ecology popularized by theHutchinson and Odum schools, and the growing pref-erence for testing hypotheses through carefully con-structed experiments, studies of intertidal zonationsoon made impressive and substantial contributions totwentieth-century ideas of animal ecology. Even moreimportant, however, was the growing appreciation andacceptance in the 1960s and later that ecological re-search might not be as predictive and exact as researchin the physical sciences. Indeed, one of the cherishedassumptions of ecology, dating from Stephen Forbes’swork on lakes at the end of the nineteenth century thatthe natural world existed in some kind of finely bal-anced equilibrium state, a state that could be known(Forbes, 1887), soon gave way to the notion of thethoroughly dynamic and stochastic nature of the nat-ural world. Demonstrated most convincingly in recentstudies by Robert Paine, J. H. Connell, and Paul Day-ton, marine ecologists now consider intertidal zonationpatterns to reflect a snapshot of marine communitiesin time, not the deterministic result of physical features(Paine, 1966; Connell, 1961; Dayton, 1971).
Admittedly, this historical treatment of intertidal zo-nation has been very sketchy. Neverthless, it is im-portant to understand how early notions of marinecommunities were initially influenced by investigatorsclosely tied to the botanical biases of physiologicalecology, especially in the work of Clements, Cowles,and Shelford. A new direction was promised with the
779HISTORY OF INTERTIDAL ECOLOGY
self-conscious formation of marine ecology within thecontext of the new marine laboratories, which sooncalled for more comprehensive natural history inves-tigations of marine communities. These studies, espe-cially along the U.S. west coast in the 1930s revealedthe inadequacy of both the botanical approach and lab-oratory-based experiments. By the Second World War,several marine ecologists suggested that physical fac-tors, so popular with earlier studies, were importantonly as limiting factors for the marine fauna and flora.The intriguing zonation patterns that attracted the at-tention of biologists in the first place, were the productof biotic factors. Of course, the limiting condition upto this time was that year-around marine stationsequipped to facilitate the longitudinal investigationsnecessary to ask these questions and to evaluate theresults of the investigations did not exist. But by thefifth decade of the twentieth century, this conditionhad been remedied, funding for the work was providedfrom federal sources (ONR and NSF) in the century’ssixth decade, and marine ecology entered into its mod-ern phase.
In conclusion and from the perspective of an his-torian, the current suggestion for greater collaborationbetween physiologists and ecologists implicit in thecontext of this symposium represents an indication ofthe maturity of marine ecology. After all, faced withthe new challenges of the twenty-first century, it re-quires a certain amount of confidence for investigatorswithin a specific and well-defined field to call for moreintegration from other fields such as physiology, ge-netics, and molecular biology. Certainly such an in-vitation is a harbinger for a robust and productive fu-ture in intertidal ecology.
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