S PECIES T RAITS AND E NVIRONMENTAL C ONSTRAINTS : Entomological Research and the History of Ecological Theory

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October 25, 2000 11:4 Annual Reviews AR119-10

Annu. Rev. Entomol. 2001. 46:291–316Copyright c© 2001 by Annual Reviews. All rights reserved

SPECIES TRAITS AND ENVIRONMENTAL

CONSTRAINTS: Entomological Researchand the History of Ecological Theory

Bernhard Statzner,1 Alan G. Hildrew,2

and Vincent H. Resh31Centre National de la Recherche Scientifique Ecologie des Hydrosystemes Fluviaux,Universite Lyon 1, 69622 Villeurbanne Cedex, France;e-mail: [email protected] of Biological Sciences, Queen Mary and Westfield College, University of London,London E1 4NS, United Kingdom; e-mail: [email protected] of Environmental Science, Policy and Management, University of California,Berkeley, California 94720; e-mail: [email protected]

Key Words demography, habitat templet concept, niche, nonequilibrium andequilibrium conditions, succession

■ Abstract The role that entomology has played in the historical (1800s–1970s)development of ecological theories that match species traits with environmental con-straints is reviewed along three lineages originating from the ideas of a minister(Malthus TR. 1798.An Essay on the Principle of Population.London: Johnson) and achemist (Liebig J. 1840.Die Organische Chemie in ihrer Anwendung auf Agriculturund Physiologie.Braunschweig: Vieweg). Major developments in lineage 1 focus onhabitat as a filter for species traits, succession, nonequilibrium and equilibrium condi-tions, and generalizations about the correlation of traits to environmental constraints.In lineage 2, we trace the evolution of the niche concept and focus on ecophysiolog-ical traits, biotic interactions, and environmental conditions. Finally, we describe theconceptual route from early demographic studies of human and animal populations tother-K concept in lineage 3. In the 1970s, the entomologist Southwood merged thesethree lineages into the “habitat templet concept” (Southwood TRE. 1977.J. Anim.Ecol.46:337–65), which has stimulated much subsequent research in entomology andgeneral ecology. We conclude that insects have been a far more important resource forthe development of ecological theory than previously acknowledged.

CONTENTS

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292A MINISTER AND A CHEMIST AS PROPHETS OF CURRENT

ECOLOGICAL THEORY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293

0066-4170/01/0101-0291$14.00 291

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292 STATZNER ¥ HILDREW ¥ RESH

BIOLOGICAL TRAITS AND ENVIRONMENTAL CONSTRAINTS(LINEAGE 1) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295Habitat as a Filter for Biological Traits. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 296Succession, Nonequilibrium and Equilibrium Conditions. . . . . . . . . . . . . . . . . . . 299Problems and Agreements Relating to Biological Traits and

Environmental Constraints at the End of the 1920s. . . . . . . . . . . . . . . . . . . . . . 300Generalizations about the Correlation of Traits to Environmental Conditions. . . . . 301

THE NICHE (LINEAGE 2) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303Development of Different Views of the Niche Until the 1920s. . . . . . . . . . . . . . . 303Development of Hesse’s and Pearse’s View of the Niche. . . . . . . . . . . . . . . . . . . 305Development of Elton’s View of the Niche. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306The Hutchinsonian Niche. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

DEMOGRAPHY (LINEAGE 3) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 308MERGING THE THREE LINEAGES INTO THE HABITAT TEMPLET CONCEPT 310THE CONTRIBUTIONS OF ENTOMOLOGY TO ECOLOGICAL THEORY. . . . 311

INTRODUCTION

The number and diversity of insects, and the number of scientists currently study-ing them, underline the extraordinary contributions of entomology to many bio-logical disciplines. Clearly, ecology has benefited from the vast store of data oninsects and on the suitability of insects for experimentation. Entomology hasalso benefited in turn from advances in ecology. A century ago, Forbes wrote“...ecology is to the economic entomologist what physiology is to the physician.”(63, p. 296), and this statement is undisputed in the current era of integrated pestmanagement.

This article1 examines the roots of current ecological theories that match speciestraits with environmental constraints as well as the role that entomological researchhas played in the historical development of these theories. Examination of speciestraits and environmental constraints constitutes a substantial portion of theoreticalpopulation and community ecology, including unifying concepts such as the niche(e.g. 46) and succession (e.g. 69) or explanatory concepts such as the intermediatedisturbance hypothesis (e.g. 14). Species traits include biological features thatconfer fitness either alone or in combination, with the latter often involving trade-offs (68). Traits include ecophysiological features such as responses to temperature,humidity, oxygen, flow, etc (110), or aspects of the life history and morphologysuch as the number of reproductive cycles, food, body size, shape, etc that we refer

1Because we often used sources that are difficult to access and are written in Germanor French, we present information in two formats. The printed text includes ma-jor developments and examples that illustrate the conceptual evolution of the topicstreated here. In the supplemental materials section of the Annual Reviews Web site(http://www.AnnualReviews.org), we provide information for those interested in furtherdetails or material for teaching; we use the notation#1– #10to refer to material providedon the Web site.

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ENTOMOLOGY AND HISTORY OF ECOLOGY 293

to as “biological traits”(96). A major thread in ecological research uses life historytraits to develop ecological theory (54, 97).

The practice and history of entomology covers millennia, reflecting attemptsto counter the damage caused by insects and to exploit the benefits they offer(90). Insect ecology has no well-defined beginning. Centuries-old entomologicalobservations and generalizations can be seen in modern ecological principles. Thewritings of the eighteenth and nineteenth centuries deal with what we now callpopulations, communities, ecosystems, and the modern concepts of food chainsand energy flow are recognizable (4).

It is now generally acknowledged, however, that botanists initially made themost significant contributions to ecology (e.g. 19, 51, 63). For example, by 1900,botanists had a complete view of the principle of the ecophysiological niche ofplants (e.g. 22). They also knew that soil patchiness affects plant diversity, andthat disturbances create nonequilibrium conditions and subsequent successionthat can affect species traits and competitive interactions among plants (113;see#1 in the supplemental materials section of http://www.AnnualReviews.orgfor more details about the views of early plant ecologists). In contrast, ento-mology textbooks of that period (37, 49) were almost exclusively of a technical(i.e. taxonomic, morphological, and applied) nature and contained little of theconceptual flavor of the botany texts. However, Forbes noted in 1909 that eco-nomic entomologists are “...the leading ecologists in America today.” (29, p. 29),although he recommended that they should also use the methods of “active youngecologists” who were “...unfettered by any responsibility for an economic result.”

In this review of ecological theories about species traits and environmentalconstraints, we emphasize historical aspects covered insufficiently elsewhere. Westart with two nonbiologists, Malthus (a minister) and Liebig (a chemist), whoseideas arguably anticipated this group of theories. We then describe three lineagesof research in animal ecology that lead to an understanding of species traits andenvironmental constraints as defined in the habitat templet concept of the ento-mologist Southwood (92). Southwood’s synthesis combined elements of biologicaltraits, environmental constraints, succession, nonequilibrium and equilibrium con-ditions (our lineage 1), with the niche concept (our lineage 2), and demography(our lineage 3). We first review historical developments in these three lineages upto the publication of the habitat templet concept in 1977 and then merge theselineages into that synthesis. Finally, we describe the impact of Southwood’s ideaon subsequent ecological and entomological research.

A MINISTER AND A CHEMIST AS PROPHETSOF CURRENT ECOLOGICAL THEORY

Major progress in science is typically ascribed to the individual contributors whoseaccomplishments brought about these advances. In this review, we could have cho-sen to start with Aristotle, who related changes in aquatic communities to environ-mental constraints caused by inputs of organic pollution (103); with Fabricius, who

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related morphological structures of insects to their function and the environment(107); or with Darwin, who found the variety of biological traits in insects ex-tremely useful for discussing natural selection (78).

This historical overview begins, however, with Malthus and Liebig, despite thefact that neither of them was an entomologist or even what would traditionally bedescribed as a biologist. Malthus (1766–1834) was a minister who later worked as ahistorian and political economist (47). Ecologists associate Malthus primarily withthe study of the population growth rate (sometimes called “Malthusianr”) and itsrestraints (51). Liebig (1803–1873) was a chemist who had enormous impact on thedevelopment of his discipline (more than 40 Nobel Prize winners in chemistry arescientific heirs of Liebig) as well as on the transfer of knowledge from chemistryto other disciplines (41). Ecologists associate Liebig primarily with his “law of theminimum” (84). As we will show, both Malthus and Liebig, in addition to theirother contributions, provided ideas of importance to ecology and entomology thatgo far beyond the concepts usually associated with them.

In his Essay on the Principle of Population, published in 1798, Malthus (60)integrated several elements to explain the control, size, and oscillations of all typesof populations (including plants and animals), although his focus was clearly onhumans. He related environmental constraints (which he presented as what we nowcall the carrying capacity,K ) to biological behavior (e.g. traits such as delayedreproduction or mobility of humans) and included density-dependent regulationor disturbance (e.g. accidents of nature) as causes of nonequilibrium conditionsover the short (K unchanged) or the long (K changed) term, respectively. (In#2in the supplemental materials section of http://www.AnnualReviews.org, we havesummarized the ideas of Malthus about the growth of human populations.)

Although Malthus (60) concluded that the production of more food cannot bethe solution to human population problems, increasing the food supply for hu-mans was an important issue in the nineteenth century, which brings us to Liebig’scontributions. Liebig clearly saw limits to food production and emphasized theneed to recycle critical components such as plant nutrients (41). He synthesizedthe progress made in chemistry in the early 1800s to respond to society’s need formore food. In 1840, he publishedDie Organische Chemie in ihrer Anwendung aufAgricultur und Physiologie(Organic Chemistry in its Application to Agricultureand Physiology) (57), which focused on plants but derived some of its central ar-guments from the physiology of humans and animals. Liebig’s book showed howenvironmental conditions affect physiological processes and integrated several el-ements into a concept that explained the principles of growth for all types of plants.Liebig described the spatial variability in the many environmental factors that mayact as ecophysiological constraints for a species if any factor is at minimum (nowknown as Liebig’s “law of the minimum”) or, for some factors, is at maximum(i.e. he described a multidimensional niche). He addressed species-specific re-sponses in growth, survival, and biological traits to these ecophysiological con-straints. He also included biotic interactions among plants based on the effects ofplants on the soil, which was later used as one process to explain plant succession,

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or based on competition for nutrients, now referred to as competitive exclusion.(In #3 in the supplemental materials section of http://www.AnnualReviews.org,we have summarized the ideas of Liebig about the growth of plants.)

Liebig’s law of the minimum typifies the problem of ascribing progress in ascientific field to a particular individual. For example, animal ecologists associatethe minimum law with the name of Liebig (e.g. 84), perhaps because the zoolo-gist Shelford (86) saw his own tolerance law as an extension of Liebig’s law ofthe minimum. However, historical overviews in agricultural chemistry repeatedlyshow that Liebig’s ideas about the law of the minimum (and other subjects) hadbeen previously expressed by others (e.g. De Saussure, Sprengel) (56). (See#4in the supplemental materials section of http://www.AnnualReviews.org for moredetails about the problems in tracking the historical roots of ecological theory.)

Many of the ideas of Malthus and Liebig have been overlooked in historicalreviews of ecology and entomology, although it is evident that they foreshadowedlater developments in ecological theory. It is generally accepted that Darwin wasmuch more influenced by Malthus than by Liebig (51, 105) and, consequently,that Malthus had a major impact on subsequent developments in ecology throughDarwin’s writings. However, as we will see in our lineage 3 on demography, someof the basic ideas of Malthus that were particularly relevant to ecology were soonforgotten.

BIOLOGICAL TRAITS AND ENVIRONMENTALCONSTRAINTS (LINEAGE 1)

It is evident that there has been interest in the relationship between biological traitsand environmental constraints since the earliest days of ecology as a scientificdiscipline. For example, in 1880, Semper (85) stated that monophagous animalsare more vulnerable to temporal habitat variations than polyphagous ones and thatsmaller habitats usually contain smaller, more mobile animals than larger ones.His insect examples included the resistance of eggs to drying, food impact on thecolor of butterflies, and the temperature-induced switch from parthenogenetic tosexual reproduction in aphids.

Since Semper, ecologists have continuously focused on animal size and shapeand on the implications of these characteristics for other traits and their relation-ships to environmental constraints. Peter’s (74) synthesis of much of this worktakes an animal’s energy budget as a starting point to discuss the relationship ofbody size to the rates of ingestion and respiration, to predator-prey dynamics, orto life history. The contribution of entomology to the development of a theoryof size relations has varied. Before the 1970s, entomology contributed little tothe development of views on relationships between the body size and metabolismof animals (as is apparent from three reviews spanning the 1930s to the 1970s)(10, 52, 115). In contrast, throughout the twentieth century, insects were promi-nent in the search for relationships between size or shape and other biological

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traits and the relationships of these traits to environmental constraints (e.g. 50, 66,73, 81, 99).

Ecologists’ perceptions of the significance of a biological trait, such as bodysize or shape, changed over time as ecological research progressed. The rela-tionship between the size or shape of stream insects and the flow of water is anexcellent example to illustrate this point. Research on this relationship began withfield observations and speculations about flow forces (98), continued with simplephysical measurements (12), and then incorporated concepts from hydrodynamics(112) and aerodynamics (43). Later, more sophisticated flow measurements (2) ortotally new technologies (95) made their contribution. Biological interpretationsnecessarily changed over the nine decades of research since Steinmann’s work in1907 (98), from the view that dorsoventrally flattened or streamlined shapes andsmall size are best suited to swift flows to the realization that, for a given flow,no body shape exists that simultaneously reduces all flow constraints, becausewe now understand the importance of a variety of flow factors (e.g. lift or drag).[See#5 in the supplemental materials section of http://www.AnnualReviews.orgfor changing perceptions on the relationship between size or shape in stream in-sects and their physical environment and see Koehl (53) for a recent review ofother morphology-flow relationships]. The historical change in views about sizeand shape in stream insects corresponds to a general pattern revealed in the litera-ture about biological traits: The general significance of a trait was noted early, butthe details of its significance took much longer to be clarified.

Habitat as a Filter for Biological Traits

An early example of thought on the relationship between the biological traits ofarthropods and habitat conditions is contained in the classic paper in 1887 ofthe renowned entomologist Forbes (28) entitled, “The Lake as a Microcosm.”Forbes noted an effect of the size of bodies of glacial water on the biological traitsof the cladoceranDaphnia. He observed that species from large lakes have lessfood available than those from small lakes, so the former are smaller, have lowerfecundity, and have more slender bodies, which enables rapid locomotion and awider range of movements.

In 1900, Levander (55) published his long-term observations on the flora andfauna, including insects, of numerous small ponds that are more or less disturbedby drought or by complete freezing. He found that resistant life stages are requiredto survive severe conditions. He also noted that temporary ponds have smallerspecies than permanent ones. Reanalyzing these data, Hesse [in 1924 (42)] addedthat species in temporary ponds are not only smaller but also are shorter-lived, withgreater fecundity, and potentially more generations per year than species in perma-nent ponds. In describing terrestrial systems in 1913, Shelford (86) emphasized thatsimilar climates in different parts of the world have different taxonomic groups ofplants yet have vegetation that is similar in growth, form, and appearance. They alsohave animals with similar biological and ecophysiological traits (although Shelfordacknowledged that the evidence is less strong for animals than for plants), because

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animal species with similar traits select similar habitats. Shelford also noted, how-ever, that similar habitats may have animal species with very different biologicaltraits because there are different solutions to live under a given environmentalconstraint. Shelford called this latter case “ecological equivalence,” which in prin-ciple corresponds to what is currently known as trade-offs among traits. Beyondthese fundamental aspects, Shelford, like many entomologists and ecologists of histime, was interested in the applied aspect of these fundamental concepts. (See#6in the supplemental materials section of http://www.AnnualReviews.org for threeexamples of the potential application of fundamental insect research provided byShelford.)

Thienemann (100, 101), referring to work he and Hesse published indepen-dently, viewed habitat as a filter for biological and ecophysiological traits when hepublished descriptions of his first and second biocoenotic principles in 1918 and1920 (paraphrased for insects in 111). Drawing on his previous research on insects,Thienemann documented this concept of a habitat filter by comparing invertebratesthat occur in a series of habitats: quiet bays in lakes filled with aquatic macrophytes,lakeshores exposed to waves, swiftly flowing streams, or along gradients of salin-ity and organic pollution. He concluded that the number of species increases withhabitat diversity (i.e. with a greater diversity of filters) and that the traits of speciesin a community become more similar if the habitat becomes extreme.

Desert ecologists were also concerned with environmental extremes and therelated biological traits in insects. Buxton (9), in 1923, emphasized the enormousannual variations in desert insects caused by drought, torrential rain, unusual frost,or whirlwinds. For terrestrial insects, the traits prevalent in this environment includethe tolerance of larvae to lack of food and water, dormant stages, and burrowingto escape high temperature. Many desert insects are wingless, unlike their closerelatives elsewhere, and many desert beetles are flightless because their wing casesare fused. Buxton related this flightlessness to the desert wind because flightlessinsects also occur on mountaintops or small islands, which are windy but other-wise very different from deserts. He noted that switches from one food plant toanother are common in desert butterflies, which enables exploitation of succes-sively occurring and disappearing plants. Similarly, species of desert Hymenopteraare very polyphagous. Buxton observed trait patterns in aquatic insects similar tothose found by Levander (55) in temporary ponds in Nordic regions.

According to the 1924 work by the zoogeographer Hesse (42) [as well as toThienemann (100, 101)], the environment also acts as a filter for biological traits,and increasing environmental harshness produces increasingly similar traits in an-imal communities. Thus, although Hesse focused on zoogeography rather than onthe ecological scales of Thienemann, both arrived at the same conclusion. Hessegave many examples of the relationship between biological traits and the envi-ronment of insects. For example, insects and related arthropods that live in mosspatches on rocks or trees have similar biological traits whether they are found in thetropics or toward the poles: They are small and mostly feed on detritus, can avoidwashout from the moss during rain, and survive dry periods in resistant stages.Similarly, Hesse noted that insects, other invertebrates, and vertebrates living in

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mountain streams of different continents have a similar body shape, possess suctiondevices, or use stones as ballasts (as in caddisflies), which helps them withstandthe forces of flow.

Focusing on how ecological fundamentals explain zoogeography, Hesse (42)considered many ecological patterns that were related to the size of islands andtheir isolation from continents (e.g. the number of species in animals increaseswith island size and proximity to a continent). For biological traits, he noted thatsmaller islands (or ponds and other insular habitats) have smaller species thanlarger ones [repeating the earlier view of Semper (85)] because larger species needmore space. He repeatedly pointed out which biological traits of insects facilitatedispersal to islands (or similar habitats). For example, he attributed the dominanceby curculionid species of the beetle fauna on islands, compared with continents,to their life stages inside wooden logs, which facilitate their transport to islands.Hesse was also aware that insects with a high dispersal potential (e.g. sphingidbutterflies) can maintain small populations in unsuitable environments beyond thereal limits of their tolerance through regular immigration of specimens that em-igrated from suitable environments elsewhere; nowadays, such environments arecalled sink and source habitats.

In 1926, Pearse (73) also referred to the relationship between environmentalconstraints and biological traits. For example, he stated that terrestrial insect speciesnumbers decrease rapidly along a northward latitudinal gradient; forest insectspecies decline first, then phytophagous species, with scavengers and predatorsextending the farthest north. Pearse was well aware that trade-offs exist amongbiological traits. He noted that there is no general correlation between size, activity,complexity of structure or constitution, and longevity (using cicindelid beetlesas one example). However, Pearse still tried to generalize about related trendsin biological traits. He noted that long-lived animals generally produce feweroffspring and reproduce less frequently than shorter-lived ones. Similarly, thenumber of offspring produced is inversely proportional to the amount of parentalcare given to the eggs and young (although he clearly stated that there are manyexceptions to this pattern). As an example, he compared the degree of parental careamong insects (flies and beetles) in cow manure.

Compared to his contemporaries, Elton (26), in 1927, was less concerned withenvironmental constraints and biological traits other than feeding habits. Withhis niche definition emphasizing trophic relations among animals (see lineage 2),Elton related food size to the size of the feeder or feeding apparatus; these haveto match within certain limits. For example, a tsetse fly can suck the blood ofmany mammals and birds that have small blood corpuscles, but it is unable to suckthe blood of the lungfish, which has corpuscles too large to pass through the fly’sproboscis. Therefore, Elton concluded that along herbivore-carnivore food chains,animal size increases; however, size decreases along host-parasite-hyperparasitefood chains. In discussing plant-herbivore relations, Elton did not cite any insectexample and simply wrote “It is hardly necessary to quote examples from amongstinsects, since they are so numerous” (26, p. 47).

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Succession, Nonequilibrium and Equilibrium Conditions

As in the previous section, Forbes’ 1887 classic work (28) is the starting point ofthis discussion. Earlier work by Forbes on the control of insects by birds and onbiotic interactions in lake communities actually anticipated the ideas expressed inthat classic work (63). Forbes’ article is widely regarded as a pioneer work thatcombines the effects of competition and predation to achieve an equilibrium incommunities (e.g. 19, 25, 63). What is often forgotten in descriptions of his 1887article, however, is that Forbes referred to equilibrium conditions in communitiesonly in certain parts of it. In fact, to emphasize the functioning of stable lakes ofglacial origin and their equilibrium communities, Forbes described the contrastingfunctioning of fluvial oxbow lakes that are regularly impacted by river floods. Inthese fluvial lakes and in the river related to them, the occurrence of species andtheir abundance are extremely variable, depending chiefly on the frequency, ex-tent, and duration of spring and summer floods. After a flood disturbance, speciesin oxbow lakes have extraordinary rates of population growth, and biotic controls(through predation) affect, successively, the abundance of protozoa, insect larvaeand entomostraca, rapidly breeding fish, and, finally, slowly breeding game fish.How far this biotic succession develops depends on the duration and timing ofthe disappearance of the floodwater, and Forbes considered drying to be anothertype of sequential disturbance. Therefore, before an equilibrium is established, theebbing of the floodwaters changes the biotic interactions in oxbow lakes. A betterappreciation of the dichotomy of equilibrium in glacial lakes and nonequilibriumin oxbow lakes, as described by Forbes, would have avoided much of the mis-understandings in the long-lasting subsequent debate about biotic versus abioticregulation of populations or communities.

An early example (1896) of the relationship between biological traits of insectsand succession considered their feeding habits and the decomposition of humanbodies. To estimate the time since death of a human body in a forensic analysis,Megnin (64) described the food types that a decomposing human corpse offers fordifferent insect feeding groups. These groups occur successively and always inthe same order if the cadaver is not buried (i.e. one “habitat type”). The durationof each successional phase depends on the season, temperature, and volume ofthe cadaver (i.e. on variation of the habitat type). If the cadaver is buried (i.e. asecond habitat type), there are far fewer species per insect feeding group but theindividuals of the species occur in higher numbers.

In 1909, using a study that related animals (mainly birds but including manyinsects) to plant communities, Adams (1) introduced botanical views (see Introduc-tion) of succession into animal ecology. However, apart from remarks about mobil-ity, his 26 principles of animal succession were less explicit in terms of the biolog-ical traits that dominate in early or late succession than were the botanists’ ideas.Four years later, Shelford (86) identified a potential problem in the cosuccessionof plant and insect (and other animal) communities that is related to the differencein lag time in the response of trees and animals to changing physical conditions.

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Thienemann (100, 101), using insects and other invertebrates as examples, notedin 1918 and 1920 that as habitats become more and more extreme, the number ofspecies decreases, whereas the abundance per species increases. His explanationwas that communities are in equilibrium and that, for a given amount of food, fewerspecies can have a greater abundance per species. However, as it was typical foranimal ecologists of his time, Thienemann immediately added that this equilibriumis fragile and is affected by short-term cyclic (e.g. seasonal) changes, by unidirec-tional, long-term (e.g. aging of lakes) changes and/or by natural and human-madedisturbances. Hesse (42), in 1924, considered communities generally to be in afragile equilibrium, easily disturbed by short-term changes in external conditions.As an example, he cited the mass development of caterpillars feeding on oak andthe consequences this has for (a) other insects feeding on oak (which decrease innumbers because of food shortage); (b) the vegetation of the forest floor (wheregrowth increases because of fertilization from the caterpillar excrement); (c) deer(which emigrate because they feed on herbs that become covered with the moltedcaterpillar skins, which have poisonous hairs); and (d ) birds (cuckoos immigratebecause they feed on the caterpillars). However, Hesse concluded that high repro-duction and competition soon result in reestablishment of predisturbance levels ofabundance and equilibrium.

In contrast to previous views, Elton clearly stated in 1927 that “...succession(at any rate in animals) does not take place with the beautiful simplicity whichwe could desire, and it is better to realize the fact once and for all rather than totry and reduce the whole phenomenon to a set of rules which are always brokenin practice!” (26, p. 27). Elton included a chapter on variations in the number ofanimals in his book, noting that animal numbers usually fluctuate considerably,primarily because of the unstable nature of the environment. However, he alsoacknowledged that there is an “optimum” population density at any one place andtime. In addition, he stated that if smaller and larger species (e.g. the small and thelarge white cabbage butterfly) use the same food, the smaller species would be themore abundant per unit resource.

Problems and Agreements Relating to Biological Traitsand Environmental Constraints at the End of the 1920s

The material we have reviewed in our discussion of lineage 1 clearly indicates threemajor problems that remained at the end of the 1920s. First, ecologists were awarethat trade-offs in biological traits enable animals with different trait combinationsto live in the same habitat. Because of the large number of animal species, it was notas easy to generalize about patterns in the biological traits of animals as it was forplants. Second, the question of equilibrium versus nonequilibrium conditions in an-imal communities was controversial. Third, regarding succession, some ecologistssaw order in the changing sequences of animal communities, whereas others wereoverwhelmed by the enormous variations in these communities. The clear exam-ples that supported each of these contrasting views [e.g. the orderly succession of

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insects on human cadavers (64) compared to the stochastic variations in desert in-sects (9)] caused much debate. In principle, this debate had already been resolvedby the dichotomy described by Forbes (28) in 1887 (i.e. disturbed oxbow lakeswith infrequent biological regulation compared with the stable glacial lakes withintense biological interactions).

Despite the three problems described above, there was some consensus at thistime about the relationship between biological traits and environmental constraints.Habitat was clearly seen as a filter for biological traits, and greater spatial habitatvariability (i.e. greater filter diversity) was seen as the reason for greater diversityof traits in animal communities. It was also agreed that more disturbed habitatshave more animal species with resistant stages, smaller body size, greater repro-ductive potential, and less food specialization than do less disturbed habitats. Inaddition, similar environmental constraints were viewed as the cause of similarspecies traits in animals from different continents. That is, the trait composition ofcommunities was seen as being independent of their taxonomic composition on aglobal scale.

These problems and agreements about biological traits and environmental con-straints persisted for the next two decades. Then, in the 1950s, generalizationsabout the correlation of traits to environmental conditions began to emerge.

Generalizations about the Correlation of Traitsto Environmental Conditions

Articles by Dobzhansky in 1950 (20) and Cole in 1954 (13) anticipated laterattempts (e.g. see 58, 75) to match biological traits with environmental con-straints. Dobzhansky (20), who derived many of his arguments from research onDrosophila, suggested that natural selection in the physically more benign tropicsresults in adaptations that are different from those that occur in harsher temperateclimates. In the temperate climates, evolution should favor opportunism rather thanspecialization, and this opportunism should be correlated with increased fertilityand rapid development and reproduction. The major impact of Cole’s (13) work washis argument that population phenomena may be related to changes in the physicalenvironment or competition with other species, so that natural selection will shapelife history patterns and “population efficiency” accordingly. However, Cole clearlystated that the range of conceivable combinations of life history traits, such as totalfecundity, maximum longevity, and the schedules of reproduction and mortality,is essentially infinite. This latter statement subsequently has often been ignored.

Beginning in the early 1960s, entomologists and ecologists continued to gener-alize about biological traits and the environment. For example, in a detailed reviewof arthropod dispersal, Southwood (91) concluded in 1962 that the migratory po-tential of a species (and, theoretically, its reproduction rate) is negatively correlatedwith its habitat persistence. Furthermore, within a species, the tendency to migratemay increase toward the edge of its range, where the availability of habitats thatcan be colonized will fluctuate from year to year. In 1963, Margalef (62) reasoned

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that biological traits in mature systems would be expected to differ from those indisturbed, physically fluctuating, or less mature systems. To less mature systems,Margalef assigned smaller body size, less specialization (e.g. in food), shorterlongevity and life cycles, more offspring and a higher reproductive rate, greaterpopulation fluctuations, greater dispersal potential, higher energy flow per unit ofbiomass, less parental care, and a greater phenotypic and life cycle plasticity. Hediscussed these patterns in the context of selection, evolution, and applied aspects(e.g. that pests have traits suited to disturbed systems whereas related nonpestshave traits suited to mature systems).

Although MacArthur & Wilson (58) developed their concept ofr-K selection(see lineage 3) in 1967 using islands as examples, they emphasized that all naturalhabitats are more or less insular in nature. For them, small island size implies areduced habitat variety (i.e. spatial variability) and favorsr-selection. To live insmall areas requires traits that favor the ability to colonize. MacArthur & Wilsondemonstrated mathematically that the probability of successful colonization in-creases more with a shorter development time and a longer reproductive periodthan with increasing fecundity. Despite this generalization, however, MacArthur& Wilson were aware that the success of different species or species groups(e.g. birds, ants, beetles, and other insect orders) in colonization can be relatedto very different biological traits. A subsequent test of trait patterns and otheraspects of the MacArthur & Wilson model was based on the experimental re-moval of the fauna of small mangrove islands, followed by surveys to documenttheir recolonization by terrestrial arthropods. In 1969, Simberloff & Wilson (87)noted that aerial transport is an important means of dispersal to these islands.Early immigrants include strong fliers (e.g. moths and wasps) but also weak fliers,including flightless arthropods (e.g. psocopterans, chrysopids, and spiders); theweak fliers are wind transported and are often much smaller and able to increasetheir population sizes more rapidly than the strong fliers.

MacArthur & Wilson’sr-K concept (58) had an immediate impact on the eco-logical thought at the time. For example, EP Odum (69) used the concept in anarticle on ecological succession in 1969. To early successional stages, he assignedr-selection, broad niches, small body size, and short, simple life cycles; he ex-pectedK-selection, narrow niches, large size, and long, complex life cycles in latesuccessional stages. In 1970, Pianka (75) argued that no organism is completelyr- or K-selected but must reach some compromise between these two extremeson anr-K continuum. However, he included a table with some correlates of theextremes ofr- andK-selection in his article. Pianka’s table, for example, correlatedr-selection with variable and/or unpredictable climate, rapid development, earlyreproduction, small body size, and short life cycles. In contrast,K-selection wascorrelated with fairly constant and/or predictable climates and the opposite trendsin these biological traits. Pianka’s table was later reproduced in many introductoryecological texts and became a source of misuse of ther-K concept (8).

Also in 1970, Hynes (48) remarked that the physical environment in swiftlyflowing streams is perhaps so harsh that these systems serve as a refuge for many

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primitive yet highly adapted insect groups. He argued that more highly evolvedforms have been unable to displace primitive ones from niches in these severehabitats.

Greenslade (35) expanded Hynes’ ideas in 1972 in a study of staphylinid bee-tles. He described relationships among beetle size, morphology, dispersal potential,and habitat disturbance in the context of ther-K dichotomy, but he noted a furthertype of selection, which he termed “beyondK ” (which is now termedA-selection).He related this new type of selection to species that are evolutionary relicts liv-ing in consistently and predictably unfavorable habitats that select for a typicalstaphylinid morphology and against migratory activity.

Finally, in 1975, FE Smith (88) emphasized that adaptations generally involvetrade-offs among both competitive and noncompetitive features, which producemany exceptions in correlates among species traits. However, to simplify, he relatedsimple trends in such traits (e.g. size, generation time, and growth rate) to patternsof habitat disturbance.

Thus, between 1950 and 1975, ecologists largely agreed that the biological traitsof insects and other organisms are related to the spatial and/or temporal variabilityof their habitats. However, they disagreed about the extent of possible trade-offsamong these biological traits. Either they expected that many traits would becorrelated along habitat gradients or they expected that different species or speciesgroups would show different trends in their biological traits along such gradients;some ecologists, however, vacillated between the two positions.

THE NICHE (LINEAGE 2)

Development of Different Views of the Niche Until the 1920s

In 1880, Semper (85) published what is clearly a description of the principle of anecophysiological niche for animals. He included the effects of multiple factors andthe existence of a changing ecological response between a minimum and a maxi-mum of these factors, as well as interactions among them. However, he did not usethe term “niche,” and his emphasis was on abiotic factors rather than on biotic ones.

Almost 30 years later, Forbes (28) summarized the advances of the knowledgeon ecological factors made in economic entomology. Forbes emphasized problemsarising from the fact that pest insects are affected by many varying and interactingfactors. Only 1 year later, in 1910, the term “niche” was used in an ecological sensefor the first time in a work on coccinellid beetles by Johnson (see 30). Johnsonstated that “One expects the different species in a region to occupy different nichesin the environment.” (30, p. 490) and that the erratic temporal and spatial changesin the abundance of coccinellids cannot simply be attributed to food supply. In1913, Shelford (86) then formalized the concept of the niche (again without usingthe term) in his tolerance law, which he saw as an expansion of Liebig’s law ofthe minimum. Shelford argued that “...habitat is the mold into which the organism

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fits” (86, p. 35). Experiments on the effect of slope, soil type, and moisture on theegg-laying of cicindelid beetles were used as evidence for the tolerance law andits applicability to habitat selection and use. Shelford’s tolerance law repeats theprinciples already described by Semper (85), but Shelford provided more evidencefor the complex, interacting effects of environmental factors on animals as well asevidence that these factors themselves may depend on each other.

The ornithologist Grinnell used the term “niche” in his publications from1913 onward (16). In 1917, he described the niche in terms of the spatial habitatelements used by an animal because the animal’s biological traits match these spa-tial elements (36). The spatial emphasis of Grinnell’s view of the niche was latersimplified by others to represent the type of spatial structure (e.g. microhabitats)used by different animal species (see 47). This simplification led to less consider-ation of biological traits involved, and therefore we do not pursue Grinnell’s ideaof the niche further.

Possibly unaware of developments in these ecological concepts (his paper con-tains no references), Ball (5), in 1910, compared climatological data for differentplaces by plotting their monthly temperatures against monthly relative humiditylevels. He concluded that plots combining temperature and humidity (and poten-tially other factors) would be useful for physicians in recommending a suitablehealth resort to a patient. In 1916, the entomologist Pierce (76), possibly unawareof Ball’s work, used experimental data to plot limits of the developmental speed,dormancy, and death of a weevil species in a diagram using mean temperature andrelative humidity as axes. Pierce’s diagram showed that the limits of a given weevilresponse form ellipses near optimum conditions and become circles with increaseddistance from the optimum. It also showed that the axes of the ellipses are not par-allel to the temperature and the humidity axes. With this contribution, entomologyprovided an early and convincing example of the complexity of interactions amongthe ecophysiological traits that define the niche of a species.

The article by Pierce (76) stimulated a wealth of subsequent research in ap-plied entomology. In 1924, Cook [referring to Ball and other climatologists (15)]introduced the term “climograph” for curves that relate the life cycle of insectsto temperature and humidity. Cook used temperature and precipitation at sites ofpest outbreaks to determine the optimal moisture curves for a cutworm species. Hethen used the climographs of optimal and less optimal conditions of this cutwormto determine the probable extent of the pest’s economic distribution and the areasmost liable to infestation.

Hesse (42), in 1924, and Pearse (73), in 1926, provided in-depth treatmentsof environmental factors, ecophysiological traits, and biotic factors. They statedwhat are still modern views about the principles of the niche (e.g. a minimum,optimum, and maximum for the factors as well as interactions among factors). Incontrast, Elton (26), in 1927, thought it more important to understand processesand interactions in the environment than to know about the physiology of animals.He justified this view, unusual for the time, by asserting that simple tropismsguide most animals toward their preferred habitat. As an example, he citedPieris

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butterflies that select leaves of certain crucifers for oviposition, in response to themustard oils contained in the plant leaves. Elton defined and used the term “niche”to describe an animal’s “...place in the biotic environment, its relations to food andenemies” (26, p. 64). For instance, every type of forest in England has some speciesof aphid that are preyed upon by some species of ladybird beetle. Many of the latterfeed exclusively on aphids and die when they have consumed all of their prey.

Thus, by 1927, there were three distinct niche concepts: (a) that of Johnson(see 30), which was not in use but had elements that later were more completelydeveloped by Hesse (42) and Pearse (73) (who did not use the term “niche”); (b) thatof Grinnell (36), not reviewed further by us (see above); and (c) that of Elton (26).

Development of Hesse’s and Pearse’s View of the Niche

In 1930, Bodenheimer (7) synthesized progress on the relationship between cli-mate and pest outbreaks. He presented mathematical models of the temperaturedependence of insect development and stressed that interactions of temperatureand humidity control insect survival. His three main points were that (a) abioticfactors cause a greater percentage of mortality in pest insects than does parasitism;(b) recent evidence (reviewed by him) showed that climatic factors affect insectabundance far more than biotic regulation or the equilibrium of nature; and (c) as aresult of the findings summarized in the first two points, biological control shouldbe difficult or impossible in harsh climates but easier in nonseasonal ones, suchas that of Hawaii (in which he acknowledged many examples of effective insectcontrol by parasites). Recall that Bodenheimer worked in what is now Israel andwitnessed the immediate effect of the desert climate on pest insects (40). Thus, hisemphasis was similar to that of Buxton (who also worked in deserts; see lineage 1)and, later, to that of entomologists familiar with harsh climatic conditions (e.g. 3).However, Bodenheimer saw clearly the relative importance of abiotic and bioticfactors in the niche of insects in either fluctuating or stable environments.

Despite this more balanced view, Bodenheimer was considered the founder ofa school focusing on the importance of abiotic factors for insect populations. Forexample, HS Smith (89), a protagonist of biotic regulation, somewhat unfairly (i.e.omitting Bodenheimer’s point that biotic control can occur in stable climates) at-tacked him in 1935 as being one of a very few investigators who considered bioticfactors as being of little importance. Smith argued that density-independent mortal-ity (e.g. mortality caused by climate) operating alone could never determine the av-erage density of an insect population, which requires density-dependent regulation.Nevertheless, Smith did consider meteorological variation as the cause of oscilla-tions around an average density that is determined by density-dependent regulation.

Ecologists working on the population cycles of mammals and birds tried toassociate them with the 11-year cycle of sunspot abundance. By the 1930s, meteo-rologists had evidence that sunspot cycles cause periodic variation in temperatureand precipitation, and entomologists started to investigate their importance. Forexample, Eidmann (23), in 1931, analyzed pest outbreaks in conifer forests over a

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period of 125 years, implicating the climatic change caused by sunspot cycles. Itis interesting that Eidmann (24) subsequently changed his view and then relatedpest cycles to density-dependent regulation. (See#7 in the supplemental materi-als section of http://www.AnnualReviews.org for another long-term insect studyabout sunspot cycles.)

Conflicting views accumulated about the relative importance of temperature orhumidity for terrestrial insects. In 1932, experiments by Mellanby (65) with larvaland adult insects of economic importance showed that when the combined effectof temperature and humidity results in death it depends not only on the exposuretime but also on the insect traits (i.e. body size and the ability to conserve water inthe body).

In 1933, Elton (27) suggested the use of climographs to forecast the spreadof pest insects. This view and other evidence stimulated further experimentalresearch on terrestrial insects of economic importance. Over the next 30 years,the mortality, development time, activity, preferences, or fertility of these insectswere studied in combination with temperature and humidity (among other factors)(38, 45, 59, 82, 83). In general, these studies found the same complicated interac-tions described originally by Pierce (76).

Freshwater entomologists and ecologists were obviously less concerned withhumidity, but they did focus their attention on other physical factors such as tem-perature, oxygen, and water movement (velocity in streams and mixing in lakes).For example, the relationship between oxygen concentration and the chironomidcommunity played a major role in the development of a functional lake typol-ogy in the 1920s (see 103). In 1924, Dodds & Hisaw (21) related the gill size ofmayflies to oxygen and velocity in their microhabitats. Dodds & Hisaw suggestedthat flowing water facilitates respiration because it counteracts oxygen depletion inthe immediate vicinity of the insect’s body. Two years later, Ruttner (80) and laterothers expanded this view by focusing on the physiological consequences of theinteractions between oxygen content, temperature, and velocity and demonstrated,as for terrestrial insects, complicated responses to gradients of combined factors.

However, this clear evidence for interactions among factors has been ignoredrepeatedly by ecologists. For example, in 1942, Thienemann (102) redescribedLiebig’s minimum law (not citing Liebig) in his law of the “effects of environmentalfactors” (our translation), and Hutchinson (46) also ignored such interactions inhis niche definition (see below).

Development of Elton’s View of the Niche

Because Elton (26) focused on the trophic interactions among species, he shouldperhaps have welcomed attempts by Lotka and others to model biotic interactions.However, he viewed these attempts equivocally. (See#8 in the supplemental ma-terials section of http://www.AnnualReviews.org for the evolution of Elton’s viewabout mathematics in ecology.)

As we point out in our discussion of lineage 3, the application of the logis-tic equation to more than one species was to some extent initiated by Pearl and

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advanced by Lotka, Volterra, and later by others. Because this development iswell reviewed elsewhere (e.g. 47, 51), we mention here only some of the majorcontributions involving insects.

The research of Lotka and Volterra stimulated immediate discussion and criti-cism. For example, in 1935, the economic entomologist Nicholson and the physi-cist Bailey (67) emphasized deficiencies in the work of Lotka, Volterra, and othersand focused on a mathematical examination of the patterns produced by compe-tition among animals that search for resources in various circumstances. Theirtheoretical analyses of host-parasite interactions considered many processes thatcould potentially occur in insects, although Nicholson & Bailey acknowledgedthat they had confined their attention to comparatively simple situations and thattheir conclusions might not be widely applicable in nature.

Gause (31), in 1933, emphasized the need for experimental tests of such math-ematical theories. He showed that the Lotka-Volterra equations are too simple todescribe real host-parasite interactions. Therefore, he modified the equations andchecked their outcome using experimental data on insects. Three years later, Gausereviewed studies about regulation and organization in communities and stated thatthe limitation of the number of species “...is apparently connected with the limitednumber of the ‘ecological niches’ which can be utilized by different species withoutexpelling one another...” (32, p. 321). Gause therefore concluded that the speciesnumber saturating a habitat is greater in more diverse environments. However,he also noted that such saturation is not obtained in communities of short-livedorganisms that perceive seasonal variation as disturbance.

Gause’s work stimulated many experimental studies on the niche, and what isnow termed competitive exclusion, in the 1930s and 1940s [reviewed in 1947 byCrombie (17)]. Stored-products insects,Drosophila, and insect parasitoids werefrequently used as study organisms. Crombie showed that (a) different insectspecies having different niches (defined in terms of needs and habits) survivetogether in the same uniform medium (e.g. flour), whereas in insect species havingthe same niche, one always exterminates the other; (b) different insect specieshaving the same niche can only coexist in spatially more heterogeneous media(e.g. crushed wheat compared to the more uniform flour); and (c) different insectspecies become more competitive if the experimental temperature approaches thatof their natural habitat.

The Hutchinsonian Niche

Hutchinson (46) was certainly aware of the complicated ecological response pat-terns to combinations of factors when he wrote his “niche” classic, published in1957. As an aid to understanding, however, he simplified his explanation of themultidimensional niche. He considered physical and biotic factors to be indepen-dent in their action and the probability of survival to be equal within the minimumand maximum of each factor. Because of this simplification, his niche formalizationresembled the ideas expressed by Liebig (57) in 1840. Hutchinson used this simpli-fication to describe the conditions under which competitive exclusion (also an idea

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of Liebig) between species occurs or does not occur because he wanted to resolvethe discussion between proponents and opponents of the competitive organizationof communities.

Hutchinson (46) discussed the Volterra-Gause principle of competitive exclu-sion in the context of the habitat and the niche of species. He proposed the conceptthat spatial (Liebig’s view) and temporal (Malthus’ view for disturbed humanpopulations) habitat variability reduces the probability of competitive exclusionamong species because the nonintersection of niches increases with increasinghabitat variability. He also emphasized that habitat variability has to be expressedat the scale of the organisms being considered because short-lived insects andlong-lived birds perceive the same seasonal climate differently.

The simplifications in Hutchinson’s explanation of a multidimensional nichewere soon either criticized (see 19) or simply ignored. For example, Schwerdtfeger(84), who worked on forest pest insects, argued, without citing Hutchinson, thatLiebig’s law of the minimum (which is similar to Hutchinson’s view) is unrealisticbecause it neglects well-known evidence for interactions among factors. Similarly,Watt (114), a modeler of pest populations, did not refer to Hutchinson’s nichearticle but emphasized that the knowledge about interactions among factors isoften inadequate to build useful models for pest insects.

Reviewing niche formalizations up to the 1970s, Vandermeer (108) stated thatearly naturalists laid the foundations of niche theory, which developed throughGrinnell and Elton to “...perhaps the only specific principle or law of natureever to be proposed in ecology, Gause’s axiom.” (108, p. 110). He argued thatHutchinson’s multidimensional niche “...led to a revolution in niche theory.” (108,p. 109). Because Hutchinson’s view was close to that of Liebig, perhaps we shouldassign this revolutionary role to Liebig. Vandermeer also acknowledged “...that theinsights of the early naturalists are now being quantified and that this quantificationis what niche theory is all about.” (108, p. 108). Liebig, of course, was more thana naturalist.

DEMOGRAPHY (LINEAGE 3)

This third lineage leading to the habitat templet concept begins with early demo-graphic studies of human and animal populations and ends with ther-K concept. Itis reviewed only briefly because several historical overviews of ideas in this areaare already available (e.g. 8, 33, 47, 51).

Mathematical formulations of human demography following Malthus were firstaimed at the “laws” of mortality and ways in which these laws could be used tocalculate annuities at different ages and the probability of survival for insurancepurposes [e.g. in 1825 by Gompertz (34)]. In 1838, the mathematician Verhulst(109), freely referring to Malthus (60), published his first note on a law of humanpopulation growth, which is now known in its form

dN/dt = r N [(K − N)/K ].

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Verhulst’s formalization neglected the oscillations expected from Malthus’ rea-soning, and, consequently, Verhulst’s work corresponded only in parts to that ofMalthus. Verhulst’s development of the logistic equation probably made little im-pression on his contemporaries because it was cited only once before 1920 (47).Despite its lack of immediate impact, the growth rater (i.e. the unrestricted rate ofincrease), the carrying capacityK, and, especially, the equilibrium captured in theequation affected ecological theory for more than a century after the equation’spublication.

Applied entomologists were among the first to realize the potential value ofquantitative population ecology. In 1897, Marchal (61) gave a verbal descriptionof the logistic equation but did not cite Verhulst. He then stated that an insectpest and its parasite would not stay in equilibrium but would oscillate because oftime lags in the population responses of the two species. Twenty-five years later,Marchal presented a note by Thompson to the Academie des Sciences; this notecouched Marchal’s earlier question mathematically (104). McIntosh (63) reportedthat the medical entomologist Ross (in 1911) developed mathematical equationsshowing the relationship between the incidence of human malaria and the densityof anopheline mosquitoes, that Lotka later noted the similarity of Ross’ malariacurve to the logistic curve, and that Howard & Fisk (in 1911) presented the firststatement of the concept of density dependence and pest control.

The 1920s marked the expansion of theoretical population ecology, and Pearlplayed a key role in this expansion (see 47) when he reinvented the Verhulst equa-tion during a study on human population growth in the United States (with Reed in1920). One year later, Pearl acknowledged Verhulst’s priority (47). In establishingexperimental support for logistic population growth, Pearl himself (e.g. 71, 72) andothers (e.g. 39) studied population parameters ofDrosophilareared in microcosms.Insects in stored products were also frequently used in experiments on parame-ters of the logistic equation (e.g. 6, 11, 44, 70). Beside stimulating research onsingle species, Pearl also encouraged progress in the formalization of interactionsbetween two or more species (see lineage 2) by inviting Lotka in 1921 to work inhis laboratory, while Alpatov, a teacher of Gause, spent nearly 2 years there (63).

The development of ther-K concept, which relates selection for demographicfeatures that favor the establishment and early growth of populations (r) or theefficient use of resources (K), was one result of the continuing debate over theVerhulst equation and the many modifications suggested (47). Some of the cor-nerstones in this development were (a) increasing evidence for differences in thecompetitiveness ofDrosophilamutants [reviewed periodically up until 1947 byCrombie (17)]; (b) the formalization in 1954 by Cole (13) of different life his-tory features (e.g. total fecundity, maximum longevity, and reproductive age) inthe context of population patterns and selection; and (c) a consideration of theeffects of life history parameters on the immigration and extinction rate of popula-tions, which led to generalizations about evolutionary strategies by MacArthur &Wilson (58) in 1967.

However, the deterministic model ofr-K selection was not easily applicable toreal populations. In 1977, Stearns (97) reviewed life history data for all types of

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organisms, including insects, in the context of the evolution of life history traits. Heconcluded that no general and reliable theory of life history evolution was supportedby the data and that it would be difficult even to collect appropriate data to test sucha theory adequately. Nevertheless, Verhulst’s (109) equation, inspired by Malthus(60), has had an enormous impact on developments in population ecology.

MERGING THE THREE LINEAGES INTO THE HABITATTEMPLET CONCEPT

By the 1970s, the three lineages could be joined together into a theory that linksthe ecological characteristics of organisms to variation in environmental factors.Such a framework has been a primary objective since the beginning of ecology asa scientific discipline (79). By expanding on earlier ideas by himself and others(e.g. 94), the entomologist Southwood (92), in 1977, proposed a solution to thisfundamental quest. He used the premise that habitat provides the templet on whichevolution shapes characteristic life history strategies, and this premise serves asthe basis of the habitat templet concept. Southwood’s idea is simple but elegant:the habitat is the templet for ecological responses, and habitat conditions selectcombinations of species traits that enhance fitness. A major objective of this con-cept was to provide for ecologists an equivalent of the inorganic chemists’ periodictable. As Southwood stated, before this discovery by the chemists “Each fact hadto be discovered for itself and each must be remembered in isolation.” (92, p. 337).Therefore, he attempted to stimulate a similar approach for ecology that createsorder and enables predictability in a field in which diversity is overwhelming.

To organize ecological responses in such an ecological “periodic table,”Southwood (92) combined many elements that we described in our three lin-eages. For example, he related the niche and selection for ecological strategies(r, K, andA) to species traits (focusing on size, dispersal, and dormancy) or topopulation oscillations (focusing on density dependence versus independence).These elements were then related to a reproductive matrix that discriminates space(here or elsewhere) and time (now or later). He considered ecological responsesranging from those of individuals to those of all types of ecosystems, although hisemphasis was on the species level and terrestrial systems (often using terrestrialinsects as examples).

Southwood (92) clearly saw that an ideal habitat templet should have severalquantitative characters that must be scaled according to an organism’s temporal(e.g. length of a generation) and spatial (e.g. foraging and migratory ranges) dimen-sions. Because such a periodic table cannot be visualized in multiple dimensions,Southwood simplified it by using two basic dimensions: the spatial and temporalvariability of habitats. For him, spatial variability indicated the durational stabilityof habitats (i.e. the ratio of duration of habitat suitability to the length of the gener-ation time, so that the spatial axis integrated temporal aspects), whereas temporalvariability indicated resource availability and constancy. To these habitat charac-teristics, Southwood related gradients in the life history strategy of species, life

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forms (i.e. species traits being correlates of the strategies), community processes(e.g. succession), and community character (e.g. breadth of the fundamental andrealized niches). However, Southwood, in 1977 (92) and later in 1988 (93), ac-knowledged that certain problems (e.g. interaction of processes along the templetaxes and trade-offs among traits) must be overcome before the habitat templetconcept can serve as a periodic table for ecology. (See#9 in the supplementalmaterials section of http://www.AnnualReviews.org for details on problems withthe habitat templet concept acknowledged by Southwood.)

What influences has Southwood’s habitat templet concept had on ecologicalresearch since its appearance? Southwood’s (92) article has been cited almost600 times since 1977 in journals covered by theISI Citation Index(which cov-ers only a small fraction of journals published worldwide). Originally developedprimarily from and applied to terrestrial habitats and insects, the concept has nowbeen broadly applied to various groups of organisms and habitats. For example,by analyzing the titles that mention specific organisms, it is apparent that insectecologists continue to use the habitat templet concept. However, what is indicativeof a broader use is that 39% of the citations are in articles on organisms otherthan insects and related arthropods (e.g. spiders and mites); these include plants,mammals, fish, and even viruses. The broader application of the habitat templetconcept is also confirmed by noting that about 20% of its citations are in generalstudies not specific to particular organisms. The expansion of the habitat templetconcept from terrestrial into other habitat types over time can be seen by examin-ing the distribution of the habitats studied in papers citing Southwood’s (92) 1977article. In citations from 1978–1980, 84% of these studies were conducted in ter-restrial systems, 11% in freshwater environments, and 4% in marine environments.From 1997–1999, the number of citations in marine habitat studies remained low,whereas those in freshwater and terrestrial studies were almost equal (45% and49%, respectively). In contrast, references to a habitat templet approach devel-oped for rivers (106) were almost exclusively in articles on freshwater systems(again, 37% of the citations were in nonentomological studies). That this concept,developed by an entomologist, has been widely cited and applied to groups otherthan insects, that references to it have expanded from mainly terrestrial to bothterrestrial and freshwater system studies, that many of the citations are in generalstudies not specific to particular organisms, and that it has even been proposed asoffering a “changing worldview of ecology” (54) are testimony that Southwood’sconcept has contributed widely to modern ecological research.

THE CONTRIBUTIONS OF ENTOMOLOGYTO ECOLOGICAL THEORY

Entomologists, throughout most of the history of their discipline, have arguablynot been even slightly concerned with contributing to or developing ecologicaltheory (e.g. 90). Rather, they have been interested either in solving pest prob-lems (29) or in describing and classifying the multitude of insect species (18).

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However, it has become apparent to us that research on insects has been a ma-jor resource in the development of ecological theory that links species traits andenvironmental constraints. In fact, the contributions of entomology have been farmore numerous than has been acknowledged in historical treatments prepared bynonentomologists (19, 63). Research on insects was the predominant source ofinformation as theories developed from the work of our “prophets” (Malthus andLiebig) and other great contributors [e.g. Darwin (see 78)], when the ideas of theearly botanists were tested for their relevance to animal ecology, and in the recentbroad applications of the habitat templet concept. This conclusion is also sup-ported by other lines of evidence. [See#10 in the supplemental materials sectionof http://www.AnnualReviews.org for the contribution of entomology to 40 classicpapers in ecology, reprinted in (77).]

What thoughts do we take away from the preparation of this review? First,the farsightedness and foresight of our ecological predecessors are astonishing,whether one starts from the early naturalists, from Malthus and Liebig, or fromentomologists and ecologists up to the 1920s. However, the lack of appreciationthey currently receive is surprising. We admit, on reflection, that we behaved asdid many others in this respect because we have been involved in habitat templetresearch (e.g. 79, 96, 106) but only fully understood its historical roots when work-ing on this review. We regret that this tendency to lose connections with the pastwill continue as the editorial policies of journals increasingly dictate that only se-lected examples of recent citations be used. Furthermore, the technology availablein academic libraries enabled us to retrieve vast amounts of recent information, buteconomic considerations made us unable to exploit archives of our history. This isunfortunate because our historical antecedents in entomology still have much tooffer in terms of the development of ecological theory.

ACKNOWLEDGMENTS

GK Judel loaned us the only copy of the first edition of Liebig’s book (57) fromthe collection of the Liebig Museum in Giessen and informed us of early develop-ments in agricultural chemistry. G Bretschko, S Dolédec, B Hugueny, and P Jolycommented on earlier drafts of the manuscript. N Kobzina assisted in the citationresearch. Their assistance is gratefully acknowledged.

Visit the Annual Reviews home page at www.AnnualReviews.org

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Annual Review of Entomology Volume 46, 2001

CONTENTS

BIOGEOGRAPHY AND COMMUNITY STRUCTURE OF NORTH AMERICAN SEED-HARVESTER ANTS, Robert A. Johnson 1

MATING BEHAVIOR AND CHEMICAL COMMUNICATION IN THE ORDER HYMENOPTERA, M. Ayasse, R. J. Paxton, J. Tengö 31

INSECT BIODEMOGRAPHY, James R. Carey 79

PREDICTING ST. LOUIS ENCEPHALITIS VIRUS EPIDEMICS: Lessons from Recent, and Not So Recent, Outbreaks, Jonathan F. Day 111

EVOLUTION OF EXCLUSIVE PATERNAL CARE IN ARTHOPODS, Douglas W. Tallamy 139MATING STRATEGIES AND SPERMIOGENESIS IN IXODID TICKS, Anthony E. Kiszewski, Franz-Rainer Matuschka, Andrew Spielman 167

GENETIC AND PHYSICAL MAPPING IN MOSQUITOES: Molecular Approaches, David W. Severson, Susan E. Brown, Dennis L. Knudson 183

INSECT ACID-BASE PHYSIOLOGY, Jon F. Harrison 221EVOLUTION AND BEHAVIORAL ECOLOGY OF HETERONOMOUS APHELINID PARASITOIDS, Martha S. Hunter, James B. Woolley 251

SPECIES TRAITS AND ENVIRONMENTAL CONSTRAINTS: Entomological Research and the History of Ecological Theory, Bernhard Statzner, Alan G. Hildrew, Vincent H. Resh 291

Genetic Transformation Systems in Insects, Peter W. Atkinson, Alexandra C. Pinkerton, David A. O'Brochta 317

TESTS OF REPRODUCTIVE-SKEW MODELS IN SOCIAL INSECTS, H. Kern Reeve, Laurent Keller 347

BIOLOGY AND MANAGEMENT OF GRAPE PHYLLOXERA, Jeffrey Granett, M. Andrew Walker, Laszlo Kocsis, Amir D. Omer 387

MODELS OF DIVISION OF LABOR IN SOCIAL INSECTS, Samuel N. Beshers, Jennifer H. Fewell 413

POPULATION GENOMICS: Genome-Wide Sampling of Insect Populations, William C. Black IV, Charles F. Baer, Michael F. Antolin, Nancy M. DuTeau 441

THE EVOLUTION OF COLOR VISION IN INSECTS, Adriana D. Briscoe, Lars Chittka 471

METHODS FOR MARKING INSECTS: Current Techniques and Future Prospects, James R. Hagler, Charles G. Jackson 511

RESISTANCE OF DROSOPHILA TO TOXINS, Thomas G. Wilson 545

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CHEMICAL ECOLOGY AND SOCIAL PARASITISM IN ANTS, A. Lenoir, P. D'Ettorre, C. Errard, A. Hefetz 573

COLONY DISPERSAL AND THE EVOLUTION OF QUEEN MORPHOLOGY IN SOCIAL HYMENOPTERA, Christian Peeters, Fuminori Ito 601

JOINING AND AVOIDANCE BEHAVIOR IN NONSOCIAL INSECTS, Ronald J. Prokopy, Bernard D. Roitberg 631

BIOLOGICAL CONTROL OF LOCUSTS AND GRASSHOPPERS, C. J. Lomer, R. P. Bateman, D. L. Johnson, J. Langewald, M. Thomas 667

NEURAL LIMITATIONS IN PHYTOPHAGOUS INSECTS: Implications for Diet Breadth and Evolution of Host Affiliation, E. A. Bernays 703

FOOD WEBS IN PHYTOTELMATA: ""Bottom-Up"" and ""Top-Down"" Explanations for Community Structure, R. L. Kitching 729

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Documents

S PECIES T RAITS AND E NVIRONMENTAL C ONSTRAINTS : Entomological Research and the History of Ecological Theory