BIO-ECOLOGY ^"'^ BY FREDERIC E. CLEMENTS Carnegie Inditution of T]\ixliington AND VICTOR E. SHELFORD The Uiiivemity of Illinois NEW YORK: JOHN WILEY & SONS, Inc. LONDON: CHAPMAN & HALL, Limited 1939 Copyright, 1939, by Frederic E. Clements and Victor E. Shelford All Rights Reserved This book or any part thereof must not he reproduced in any form without the written permission of the publisher. Printed in the U. S. A. Published by John Wiley & Sons, Inc. By arrangement with The University of Chicago Press PREFACE From the beginnings of life, organisms have lived together in some kind of grouping. Since the differentiation of plants and animals, communities in which both occurred and interacted have undoubtedly characterized the arrangement of living things on the face of the earth. We know now that there are no habitats in which both l)lant and animal organisms are able to live, in which both do not occur and influence each other. In contrast, the development of the science of ecology has been hindered in its organization and distorted in its growth by the separate development of plant ecology on the one hand and animal ecology on the other. The authors were brought together in this task of attempting to correlate the fields of plant and animal ecology by the common belief that it would tend to advance the science of ecology in general. It was this common interest rather than agreement in all matters which led to the initiation of this book as a joint project several years ago. In part, it grew out of the fact that the junior author's experience in dealing with the marine communities of the Puget Sound region had led to the discovery of community phenomena paralleling those found on land and fitting the system of classification in use by the senior author. The phenomena under discussion naturally bring up the question of the community processes, concepts, and nomenclature. A zoologist may be unfamiliar with various ecological terms in use among plant ecologists, and the reverse is also usually true. Here the writers have not introduced all the terms which they are inclined to use in their individual papers, designed for a more limited group of readers, but have attempted to substitute less technical terms. Those terms ap- plicable to communities are given to aggregations of organisms suffi- ciently well known to enable the reader to build up a fairly clear conception of the whole, so that the terms may be applied to the proper grouping. For example, the term biome has been applied only to those communities in which studies have established something of the processes of development and the character of the final stage or vi PREFACE climax. Adjective nomenclatures so extensively developed in fields of limnology and oceanography are deplored by the writers as admit- ting of an almost unlimited degree of vagueness without commitment to status for either the community or its habitat. On the other hand, the letter nomenclatures used by European students of the sea prove to be very difficult because many of the generic names which have 'been abbreviated are not known to the reader. The general plan of the book is in the main that of the senior author. It was already on hand when collaboration began and has been modified only through rearrangement of chapters and the omis- sion of treatments of several large biotic communities such as decidu- ous forest, coniferous forest, and desert. Their omission results from lack of detailed knowledge of the animal relations, and hence it has become desirable to restrict such discussion to the grassland biotic community. In preparing the book, the authors have not sepa- rated their work by making a sharp division into the fields of botany and zoology. The plant ecologist has had experience in the field of animal ecology, and vice versa, so that separation along these lines was not easy. For example, the organization of most of the material in Chapters 1 and 2 w'as made by the senior author, who also undertook to prepare the tables dealing with the food of birds and the material on bird migration, on all matters relative to sunspots, and the general index. The junior author is almost entirely responsible for the chapters on communities of water; he played a large part in the organization of the grassland chaptef and the chapters on climax and sere, and in the preparation of the illustrations. He did the greater part of the work on the bibliography and prepared the author index in connection with it. After the book was considered prac- tically complete, the authors had the good fortune to have the manu- script read and criticized by their sympathetic colleague, Professor John Phillips of South Africa, who made many valuable suggestions and caused them to delay publication in order to give the manuscript an additional period of study. In the scientific nomenclature for American plants and for both European plants and animals, the authors' names are omitted. Au- thors' names for all American animals are included at least once, usually at the point of most important discussion of the species, except in a few cases where all the names come from a single source cited in the paragraph or section where they occur. Santa Barbara, California Champaign, Illinois November 1038 November 1938 CONTENTS CHAPTER 1. Nature and Relations of Bio-ecology PAGE 1 20 68 103 145 200 229 2. Community Functions 3. Reaction : The Influence of Community on Habitat 4. CoACTioN : The Interrelations of Organisms 5. Aggregation, Competition, and Cycles .... 6. Migration 7. Clim.\x and Sere 8. The North American Grassland: STiPA-ANTiLOCAPa\ Biotic Forma- tion (Biome) 251 9. Aqu.atic Climax Communities 294 10. Marine Biotic Communities 313 Appendix 353 Bibliogr.\phy 359 Index 395 52557 BIO-ECOLOGY CHAPTER 1 NATURE AND RELATIONS OF BIO-ECOLOGY Significance of the Name. The term bio-ecology has been proposed primarily for the sake of emphasis, but partly also for greater clarity and definiteness (Clements, 1922). Although the field is here re- garded as coextensive with ecology, the meaning and content of that term still vary too widely in use to permit employing the two as exact synonyms at present. This conclusion gains force from the fact that the term ecology is itself not infrequently replaced by biology, sociol- ogy, geography, or geobotany, and that its synthetic nature is too often obscured by such subdivisions as autecology, synecology, insect ecology, and human ecology. To those who regard the cause-and-effect relation as the very es- sence of ecology, the study of man and of human society is obviously a division of the latter, but it is clear that man's importance to him- self will for some time tend to maintain and even emphasize the exist- ing specialization into sociology, economics, behaviorism, psychology, and other fields. This is indicated in particular by the rise of behavior- ism, which had its origin essentially in animal ecology, but has taken its own course with diminishing interest in ecological concepts and methods. The consequent loss of focus and of synthesis has been re- flected in a generally hostile or indifferent attitude to an approach vital to the ecological study of man. As matters stand, it appears that the word ecology will come to be applied to the fields that touch man immediately only as the feel- ing for synthesis grows. The natural procedure will be for its out- look and methods to be adopted gradually by the human sciences and for the use of the term to lag far behind, as is the fate of terms in general (cf. Smuts, 1926; Wells, 1931). Moreover, students of ecology will continue to be trained primarily as botanists, zoologists, sociolo- gists, or economists for some time to come — probably indeed as long as university departments are organized on the present basis. Hence, 2 NATURE AND RELATIONS OF BIO-ECOLOGY to emphasize the proper synthetic approach and to maintain the ideal constantly before specialized workers, the term bio-ecology appears to be well warranted. It possesses the further great merit of being immediately understood, a quality certainly not exhibited at present by ecology with its various uses. This advantage will be correspond- ingly enhanced, as the field becomes on the one hand more analytic, on the other more synthetic. However, it must be admitted that, in respect to terminology especially, habit and point of view will con- tinue to rule for many workers, in spite of the benefits to be procured from uniformity and consistency. SCOPE AND SIGNIFICANCE As indicated previously, bio-ecology is considered to be ecology in the widest sense, but with the recognition that the inclusion of human ecology will be delayed until the feeling for synthesis and experiment becomes more general. In consequence, the application of the term will for the present be largely restricted to the study of biotic communities or microcosms, in which man regularly assumes roles of varying importance. Moreover, it is inevitable that the term ecology will continue to be applied to the study of plant or animal communities separately, as a matter of habit or training, or of predi- lection. Nevertheless, the fragmentation of animal communities on the basis of taxonomic groups is greatly to be deplored, since it destroys the last semblance of unity. Unfortunately, this is such a common practice as to be a matter of much concern to the future of both animal ecology and bio-ecology. This condition can hardly be remedied except by replacing the present highly specialized training with synthetic instruction to a considerable degree. In view of the great diversity of interests and hence of ai)proaches to this vast field, the word ecology will continue to have a number of rivals, in spite of its unique fitness. In accordance with the empha- sis, these range from biology, biogeography, and geobotany to sociol- ogy, biocenology, and biocenotics, and the more specialized limnology, hydrobiology and oceanography. This condition will exist as long as investigators are specialists; it is perhaps less to be deplored since each brings a different point of view to the larger field, and this is probably true likewise of the various efforts at a subdivision of the field. However, the very essence of ecology is the synthesis derived from the exhaustive analysis of the community and its habitat, and bio-ecology must rest upon this principle as its secure foundation. The advent of bio-ecology having been delayed by the separation of SCOPE AND SIGNIFICANCE 3 biology into botany and zoology, its rapid development should not now be hindered by renewed division and philosophical analysis. Nature. Ecology is in large measure the science of community populations. It is concerned with natural communities primarily, and has developed a considerable fund of organized knowledge of plant communities and their dynamics, and a lesser body of similar knowl- edge on the animal side. Because of the synthesis inherent in it, ecology is also to be regarded as a point of view and a method of attack for various great biological problems. Not only does it concern itself more or less with the whole of biology, but also it must borrow largely from chemistry and physics, from climatology, geology, and soil science, and at the same time make basic contributions to the practical sciences of agronomy, horticulture, forestry, grazing, entomol- ogy, conservation, etc., to say nothing of education, economics, sociol- ogy, and politics. It cannot, and does not, venture to draw a line between the past and the present, and it has as significant a role to play in geological as in modern times. More than a quarter of a century ago, the statement w^as made that ecology was to be considered the central and vital part of botany, and this is equally true for biology. It was further stated that plant ecology is physiology carried into the actual habitat, and in conse- quence its paramount theme is stimulus and response. It confines itself primarily and exhaustively with the cause-and-effect relation between the habitat on the one hand, and the organism and the com- munity on the other. All further relations arise out of this, and all other approaches are incomplete unless they lead back to it. With the inclusion of animals in the biotic formation (biome), this rela- tion naturally becomes more complex, but it is none the less valid. Since physiology often finds visible expression in behavior, coaction between the organisms assumes a role often more important than direct response to the habitat. From this springs the view that development is the basic process of ecology, as applicable to the habitat and community as to the individual and species (Clements, 1904, 1905). It recognizes that life constitutes a dynamic system and that static studies are valuable only as they throw light on development or serve some practical purpose in this connection. Furthermore, it was postulated that development is a cyclic process and that the apparent jioints of rest in it are rela- tive to cycles of different rank. At the very outset it was clearly per- ceived that a dynamic system renders measurement indispensable, and hence the past three decades have seen a consistent advance in this respect, especially in plant ecology and to some extent in hydrobiology. 4 NATURE AND RELATIONS OF BIO-ECOLOGY Equally imperative is the thorough-going utilization of experiment, essential not only to finer analysis and more exact measurement, but also to increasingly objective viewpoints. In connection with the preceding, it should be realized that prog- ress in zoo-ecology has been much slower. The natural unity has been obscured by the separate treatment of taxonomic groups and by such faunistic concepts as that of life zone, which, in view of the wide- spread destruction of many species, has rendered synthetic interpreta- tion very difficult. Moreover, although animals are obviously physio- logical in their response to climate, food, etc., much progress can be made in the field of interactions (coactions and reactions) without the use of physiological experiments. Furthermore, the correlations involved are usually to be suggested by studies in the biotic community and then lead properly to physiological experiments that permit more definite control and exact analysis. In sharp contrast to i)lant physiology, animal physiology as taught and applied has little concern with physi- cal factors, while general physiology deals with particular internal processes and physiological ecology with one or more species with- drawn from the community for some particular study. The conse- quence is the ignoring or splitting of the physiology of interactions, since this field finds its inspiration in the study of the biotic com- munity itself. A signal extension of ecological ideas is involved in the applica- tion of climax and succession, that is of development, to lake and ocean. This demands the definition and recognition of climaxes in large bodies of water, and hence of corresponding climates. As indi- cated later in the discussion, this is deemed a logical extension of these terms from land to land and water, and thence into lake and ocean. This further involves questions of dominance, of competition, reaction and coaction, of development and structure, all of which exhibit more or less characteristic differences in deep water. Relations of Paleo-ecology. Development is a continuous process, and hence its division on the basis of time past and present can be justified only on the score of convenience. No radical division exists in geology, where the flow of time is registered chiefly by major and minor events. "With biology and its human subdivisions, however, the technique and usually the evidence also differ so much in nature or form that the distinction appears much greater than it is. This fact has naturally not jMissed unnoticed by paleontologists, but it is the peculiar province of jnileo-ecology to insist upon the basic essence of continuing development and to emphasize the fact that the present is but a passing stage of this. HISTORICAL DEVELOPMENT OF THE CONCEPT 5 From the standpoint of development, miiformity is inevitable and universal, but it is a uniformity of i)roccss and cycle more than of end results. This becomes all the more evident when it is realized that cycles of varying intensity and duration are so telescoped that lesser ones constantly recur within the next larger, producing a complex system in which the respective cycles are difficult to discover. jNIore- over, while cycles in deformation, climate, physiography, soil, climax, migration, and abundance bear an organic relation to one another, response takes place at varying rate and degree, and the mosaic of jn'ocesses becomes correspondingly intricate. The principles and methods of paleo-ecology have been outlined in more or less detail for vegetation (Clements, 1914, 1916, 1918; Clements and Chaney, 1925-35, 1936), and these have been applied to the revaluation of fossil floras with such success as to indicate their fundamental nature (Chaney, 1925, 1933). As with modern ecology, these must necessarily undergo certain extensions and modifications v.-ith the adoption of the biome as the community. Furthermore, while relatively slight changes are needed to fit the case of land climates and climaxes, those of deep water exhibit conditions at once so differ- ent and so uniform as to require much greater modification. As has been emphasized elsewhere (Clements, 1916) , it is an axiom that the key to the past is fashioned by the present, to use these terms in their everyday significance. On the other hand, the present is the sole heir to the past, and no adequate understanding of it is possible without tracing the continuity of developmental processes from the one to the other. In short, there is no more warrant, other than that of convenience and emphasis, for separating paleo-ecology than for dividing bio-ecology, and the best development of ecology demands the synthetic organization of the entire field, even though detailed analyses will continue to be made by specialists. HISTORICAL DEVELOPMENT OF THE CONCEPT The idea of the plant community in general extends backward for nearly two centuries, but the recognition of the biotic community is a recent matter. Post (1867) recognized that the organic world should be dealt with in its entirety, but seems to have had no definite idea of the community as a unit (cf. P. Palmgren, 1928:27). How clearly Mobius perceived the existence of a biotic connnunity can probably never be settled, in spite of his introduction of the term biocenose. He certainly saw something of a community relation in the oyster assemblage (1877), but carried the concept no further, and 6 NATURE AND RELATIONS OF BIO-ECOLOGY his suggestion \Yas practically lost to view for a generation or more. A somewhat similar doubt arises in respect to Dahl's adoption of the word biocenose from JNIobius, for it appears that Dahl employed the term mostly as a synonym of zoocenose (1903, 1904). As indicated later in some detail, Clements, Shelford, France, and Vestal realized the significance of the biotic community more fully and more or less independently, but the distinction of the biome as the basic concept in climax and succession was first made in 1916. Since this time, there has been a slow but gradual recognition of the importance of the concept, exemplified in particular on the animal side by Shelford and his students, on the plant side by Phillips. For the reasons already touched upon, it is not to be expected that this will become the universal approach, and this is probably not desir- able, since some problems require intensive analysis, such as is best secured by working with plants or animals alone. If it becomes gen- erally recognized that the investigation of climax and succession must reckon with the biotic formation as the natural community unit, this will insure the proper perspective and methods. Although of a sec- ondary character, the historical development of the ideas set forth in this volume is important in an understanding of the terms and con- cepts presented. Mobius (1877). Under the title, "An oyster bank is a biocenose or a social community," Mobius gave a detailed account of the ani- mal life of an oyster bed as brought up by the dredge. He stated that very few plants grew upon the banks, namely, a single Zostera and some of the Florideae, while the desmids and diatoms of the plankton served as food for the oysters. Each oyster bed was re- garded to a certain degree as a community of living beings, a collec- tion of species and a massing of individuals, and since science pos- sessed no term for such a grouping, he proposed the word biocenose. Space and food were held to be necessary as the first requisites of every social community, even in the sea, and he clearly perceived that changes of physical factors, and disturbances by man as through over- fishing, often greatly modified the social group. There is little evidence that Mobius regarded the biocenose as constituted by both animals and plants, though such an assumption has long persisted in connection with the use of the term. The single mention of plants, the emphasis upon their role as food, and the com- prehensive discussion of the species of animals all tend to confirm this conclusion. This is supported by Petersen's statement that "Mobius has called the animals living on an oyster bank a biocenosis," and he also employed the term as synonymous with animal community (1913:32). As is shown in the next paragraph, Dahl likewise thought to employ the word in the sense of Mobius, but without rendering his own usage either very definite or consistent. HISTORICAL DEVELOPMENT OF THE CONCEPT 7 Dahl (1903-1908). In three successive editions of his guide for collecting and preserving animals (1903, 1904, 1908), Dahl adopted Mobius's term, but clearly not in the sense of a biotic community, at least in most instances. This is further -shown by the fact that he speaks only of zootopes or animal habitats, and in addition states that the biocenose is for the zoologist what the plant conununity is for the botanist. Three types of biocenose were recognized, namely, phytobiocenose, zoobiocenose, and allobiocenose, composed respectively of the animals to be found on a particular plant or its parts, on an animal, or on inorganic or decaying organic bodies. The subdivisions of the first two and especially the phytobiocenose correspond to all the organs and parts of the host and obviously represent only the most minute animal assemblages. Among the allobiocenoscs were included autonomous communities, but usually without indication of their biotic nature. Clements (1905-1918). In "Research Methods in Ecology" (1905:16), it was stated that plant and animal communities fre- quently coincide. Since animals were regarded as typically motile, their dependence upon the habitat was considered to be less evident. Vegetation as the source of protection and food plays a more obvious if not a more important part. It was stated that the animal ecology of a terrestrial region could be properly investigated only after the habitats and the plant communities have been organized as the basis for studying development and structure. In a study of the life history of the lodgepole pine burn forest (1910), animals were found to play a controlling part in succession. The frequent regeneration in burns, by contrast with the absence of seedlings elsewhere, led to the conclusion that a major effect of fire was to destroy or drive out the seed-eating animals, and permit the establishment of the pure stand of pine (consocies) as a characteristic subclimax. In a monographic discussion of succession (1916), the biotic forma- tion was regarded as an organic unit comprising all the species of plants and animals at home in a particular habitat. Plants w^re con- sidered to exert the dominant influence, although it was recognized that this role might sometimes be taken by the animals. The biotic community is fundamentally controlled by the habitat and exhibits both development and structure. In its development the biome reacts upon the habitat and thus produces a succession. In discussing the scope and significance of paleo-ecology (1918), it was stated that recognition of animals as a part of the community promised to open a new outlook in svnthetic ecology. Adams (1906-1915), Ruthven \l911). In sketching the plan for a survey of Porcupine Mountains and Isle Roj^ale, Michigan (1906), Adams based this upon the relations of the biota to environment, adopting Stcjneger's definition of the biota as "the total of animal or plant life of a region." While there was no definite recognition of the biotic community, the cmjihasis upon the habitat and upon processes in terms of succession, and the use of plant communities as a groundwork, mark the treatment as distinctly synthetic. The 8 NATURE AND RELATIONS OF BIO-ECOLOGY actual survey was carried out by Ruthven upon this broad basis and led to the conclusion that the hardwood forest represents the climax of the region, its habitat increasing at the expense of other societies so that the associated biota tend to become general for the area. Later, a more extensive investigation of Isle Royale was made by Adams and his co-workers, utilizing the same methods (1909). Even greater attention was paid to succession, though this was treated separately with respect to the four animal groups, viz., invertebrates, beetles, birds, and mammals. The biological survey of a sand-dune region in Michigan followed the same general plan (Ruthven, 1911). In a bibliographical treatise Adams presented the conclusion that such projects should deal with the balance within the entire biotic community. It was stated that for any comprehensive study it is necessary to determine the biotic base or optimum toward which con- ditions tend and at which equilibrium occurs. Some uncertainty exists, however, as to the author's use of the term biotic, since he speaks of all this as providing the best method of studying the animals of a region. IMoreover, in the ecological investigation of prairie and forest invertebrates (Adams, 1915) , the animals were treated as separate and the plant associations considered as furnishing the environment for them. Shelf ord (1907-1913). In a preliminary survey, Shelford (1907) traced the relation of Cicindela to the succession of plant commu- nities. The distribution of eight species of tiger beetles was in close correspondence with the zoned habitats and communities, and the conclusion was reached that a similar harmony existed with respect to the fauna in general. In a series of five articles on ecological succession, the same author elaborated the developmental relation between plant and animal com- munities (1911-1912). These were stated to be very generally in agreement. Disagreement was said to be temporary, and to accom- pany rapid successional changes. Succession was stated to be due to an increment of changes in conditions produced by the plants and animals living at a given point. In the treatment of the animal communities of eastern North Amer- ica (1913, a), this theme of the interaction of the two groups of organisms was further developed. Several of the communities were designated by means of a prevalent or characteristic animal and one or more plant dominants, though in general plant communities were treated as constituting the habitat for animal ones. Thus were distin- guished a white tiger beetle or cottonwood association, an ant lion or black oak, a Hyaliodes or black oak-red oak, a green tiger beetle or white oak-red oak-hickory, and a wood frog or beech-maple associa- tion. Succession was emphasized as the chief principle underlying the relations of communities. Plants were recognized as the dominant sessile forms of the land, while animals were considered to be the chief members of the successions in streams, and the primary nature of the climax was stressed. Shelford further endeavored to correlate the l)ehavior of the ani- mal constituents with the life forms of the plants. The terminology HISTORICAL DEVELOPMENT OF THE CONCEPT 9 was based upon the idea of the uniformity of the i)hysiological re- sponses of the important animals in the community (1914, a, b, c; 1915). However, this physiological basis for community classifica- tion was found to be impracticable because of the lack of response data, and the plan was ai)andoned as not yet susceptible of clear expression. Enderlein (1908). Enclerlcin followed Dahl in employing the term biocenose for a wide range of communities, and fui'ther adopted the latter's grouping on the basis of habitats. However, he departed from Dahl's usage by distinguishing areas of more or less unrelated biocen- oses as biosynecies or biosynecic districts, a departure criticized by Dahl in the same year as unwarranted (1908). Enderlein regarded the occurrence of a species in a single biocenose or its extension over two or more as marking a significant distinction, designating the one as homocene, the other as heterocene. The same concept was extended to the biosynecie, for which corresponding terms, stenotope and eury- tope, were proposed. Upon this basis, four groups of species were recognized in accordance with their occurrence in one or more of both types of community: for example, stenotope-homoccne, found in but one biocenose and one biosynecie; stenotope-heterocene, present in a single biosynecie but in two or more biocenoses. These distinctions seem not to have been applied by the author himself in his studies of the insects of moor and dune in west Prussia, though stenotope and eurytope have been utilized in a small degree, while the distinction between biocenose and biosynecie appears to have dropped from view. In fact, the extensive account of the distribution of insects is based upon taxonomic groups and not upon communities, though the com- position of the plant cover is discussed as a background. France (1913). France has advanced the concept of the edaphon, as the counterpart of the plankton, comprising under this term the community of the permanent animal and plant organisms of the soil (geobionts). This consists of the most varied types, but ones mutually tolerant and thus able to hold their own; they are distinguished by a number of adaptations and an entirely distinct and peculiar mode of life. The habitat of the edaphon is characterized by a more or less complete absence of light, periodic limitation of moisture by drought or frost, and an excess of nitrogen. The groups of organisms regarded as belonging to the edaphon are as follows: (1) bacteria, (2) fungi, (3) algae, (4) Protozoa, (5) Rotatoria, (6) worms, (7) arachnids. The inclusion of mycorhiza and earthworms was said to require further consideration, while the subterrene mammals, insect larvae, and rooted plants were ruled out of the communal life. Vestal (1913-1914) . In connection with the successional study of a sand prairie in Illinois, Vestal has tested the assumption that plant and animal associations are coextensive and to a large degree inter- dependent, the animals being entirely dependent upon the plants and the latter partly so upon the animals. In such case, the limits of the animal community are those of the i~)lant association, and both may be spoken of as a single biotic community, composed of plant and ani- 10 NATURE AND RELATIONS OF BIO-ECOLOGY mal assemblages. This relation once established, certain problems in animal ecology would be much simplified, for whereas the animal assemblage is at first obscure, that of the plants is evident, its char- acteristic physiognomy serving as an index to the animals of the com- munity. It was concluded that the evidence drawn from the study of the sand prairie, though very incomplete, was in accord with the theory and justified the treatment of the plant and animal associations together. This theme was further developed in an analysis of the internal relations of terrestrial associations (1914), as a result of which it was concluded that plants and animals agree in similar response to the common environment and in types of geographic distribution. _ It begins to appear that plant and animal assemblages are coextensive parts of a biotic association, which as a whole constitutes the real terrestrial community of living organisms. Plant and animal assem- blages are mutually interdependent, but the plants are dominant in established associations. Such assemblages are composed of ecologi- cally similar groups correlated with the same physical factors or with each other. Gams (1918). Gams considers that no logical ground exists for ex- cluding animals from communities of organisms, and hence he incor- l^orates these in the vegetation. To him, "vegetation research" is synonymous with his new term "biocenology" and with "biocenotics" of the zoo-ecologists, both of which he regards as closely related to ecology, though not identical with it. His discussion, however, is confined largely to plants, the most important exception being his outline of the life forms of the combined plant and animal kingdoms. This is based upon the assumption that the criteria available take rank in the following order: (1) motility, (2) substratum, (3) habitat, (4) nutrition. This is thought to be supported by the general accep- tance of plankton as a biotic community. The three major divisions of his system are as follows: (1) adnate or attached form, EpJiaptome- non; (2) radicate or rooted form, Rhizumenon; (3) errant or free form, Plan omen on. The first group is divided into aquatic, amphibi- ous, aerial, and innate, further subdivisions being autotroph and heterotroph, saprobe, parasitic, and phagont. Gams emphasizes the fact that, while biocenose has been employed by a number of zoo-ecologists, viz., Dahl (1903), Enderlein (1908), Babler (1910), Shelford (1911), Hesse (1912), Doflein_ (1914) , and Thienemann (1918), this has been in connection with animal commu- nities of very unequal rank. He further suggests that phytocenose may be utilized for the plant population of a habitat and zoocenose for the animals, but this suggestion is scarcely in harmony with the concept of the biotic community. HISTORICAL DEVELOPMENT OF THE CONCEPT 11 BIOTIC RESEARCHES The Biotic Formation on Land Vorhies and Taylor (1922) ; Taylor and Loftfield (1924) ; Greene and Reynard (1932). Vorhies and Taylor made a study of the kan- garoo rat in relation to vegetation which brought out various biotic interactions. Taylor and Loftfield determined the amount of forage taken by the Zuni prairie dog, while Greene and Reynard showed the benefits of some rodent reactions to the soil. These studies were a part of a project in grazing research which was organized jointly by the Carnegie Institution, the U. S. Biological Survey, the U. S. Forest Service, and the University of Arizona (cf. Year Books 16-30, Carnegie Institution of Washington, 1917-1931). Palmgren (1928, 1930). In connection with the investigation of the bird life in the forests of southern Finland, Palmgren has dis- cussed the ecological synthesis of plant and animal groups and has recognized that vegetation must form the basis for this. He also subscribes to the principles that animals must be treated as members of the community and that green plants assume the primary role in the latter, with the important corollary that the ecological study of animals must rest in the first instance upon their intimate relations with plants. He has employed the forest types of Cajander and the line surveys of Ilvessalo as the ground plan for his work, which has dealt especially with the numbers and characteristic species of birds. Although he uses the term bird society or association {V og elver ein), it appears evident that he does not intend to set these apart from the biotic community. He finds that the best forest types (Sanicula and Oxalis-Myrtillus) show clearly the influence of the tree species upon the quantitative expression of the bird fauna inasmuch as the numbers are significantly larger in deciduous woods. It appears, however, that the herbaceous layers take the leading role in this and that the nature of the stand of trees comes next- In this connection, his comparisons between deciduous, mixed, and coniferous forests are supported by the rela- tions to be found in North American woods. He gives summaries of bird density for eight different forest types and lists the character species and their abundance for the seven biotopes considered. His methods and results represent the most extensive quantitative attack upon the problem of the role of birds in the biotic community and with the addition of the dynamic outlook will serve as the model for other climaxes. Weese, 1924; Blake, 1926, 1931; Smith, 1925, Smith-Davidson, 1930, 1931. These authors made a series of studies in a forest in cen- tral Illinois composed chiefly of red oak, maple and elm. The work of Weese and the succeeding investigators was essentially quantitative. Weese devoted considerable attention to experiments designed to reveal the factors controlling the position of the prevalents in the layers of the forest; he discussed seasonal communities and described winter movements of invertebrates. Blake (1926) carried on an inves- 12 NATURE AND RELATIONS OF BIO-ECOLOGY tigation of the deciduous forest worked by Weese, and for comparison made studies of biotic communities of the pine-hemlock climax in Maine, as well as those of the upper slopes of IMount Ktaadn, taking the mammals and birds also into account. Smith (1928) utilized the same forest, together with its developmental (serai) stages, while the same author (Smith-Davidson, 1930, 1931) endeavored to evaluate the influence of the various animal species, basing this principally upon their abundance and the division into layers and seasonal groups. Some attention was given to differences between the two years of study, as well as to the characteristics of the climax animals. Blake (1931) has instituted a comparison between the results obtained by himself, Weese, and Smith, finding a good general agreement among them, inasmuch as 36 species were important numerically or otherwise in at least two of the lists. Shackleford (1929); Bird (1930). Shackleford made a study of prairie similar to that of Bird but much farther south; she compared the animal communities of the high and low prairies, treating the sea- sonal aspects in detail. Bird investigated the biotic community of the aspen parkland of western Manitoba in a comprehensive manner. The animals have been dealt with in quantitative fashion, embracing the determination of the food coactions and the evaluation of many of the constituent species. Shelf ord and Olson (1935). The authors showed the close relation of the coniferous forest animals to the plant constituents and evalu- ated the mammals, birds, and a few invertebrates on the basis of size, abundance, and movements through the climax and serai stages. This study followed the senior author's (1932) suggestion that mammals are usually the outstanding influents in communities of this type. Phillips (1930-1935). Phillips has made comprehensive applica- tions of the concept of the biome in two regions in Africa, where biotic communities possess an exceptional wealth of animal forms and still retain much of their primeval character. This was first utilized in the study of the Knysna forests of the Cape region, with especial attention to the coactions of plants and animals in the community proper and to their responses under experimental screens. Even more extensive and important investigations were made on the East African plateau in Tanganyika, where the biotic communities remain essentially primitive. The general relations taken into account com- prised grazing and browsing, fruit coactions, and soil reactions. The biotic projects were focused upon the ecology of the tsetse fly (Glos- sina), constituting altogether the most significant program of research in this vast field. His several projects have led him to the conclusion that the most logical working concept is that of the biotic community. To him the view that the community is a complex organism has defi- nite practical value. Recently, he has given a review of quantitative methods as applied to the animals of the biome, with extensions derived from the re- searches on the tsetse fly (1930), and he has further considered the concept of the biotic community in a series of three critical papers (1934-35). HISTORICAL DEVELOPMENT OF THE CONCEPT 13 Beklemischev (1931). This investigator has discussed the applica- tion of the concepts of bio-ecology to the animal members of the com- munity, with emphasis upon the importance of cycles, succession, and climax. He considers abundance, dominance, frequence, homogeneity, and constancy in relation to animals, defining dominance in terms of comparative abundance, by contrast to the concept employed in the present treatise (cf. p. 234). He distinguishes periodic from non- periodic changes, recognizing daily, annual, and pluriennial cycles, corresponding more or less exactly to diurnation, aspection, annuation, etc. The progressive nature of succession is recognized and the signifi- cance of stabilization perceived for animals as well as plants. Finally, he accepts the view of developmental ecology, namely, that the climax as a living complex includes all its several developmental stages (seres) as essential to its development. Probably no other Conti- nental ecologist has manifested such a clear perception of the funda- mental relations of the biotic community. In a second paper, Beklemischev, Briukhanova and Shipitzina (1931) have summarized the results of studies on the marshes about Magnitogorsk in the Urals, on the basis of the coactions of the organ- isms in the development from water to land (hydrosere) . The Biotic Formation in Water For a number of reasons, it is more difficult to trace the applica- tion of the biotic concept in water than on land. The uncertainty attaching to ]Mobius's use of the term biocenose continues through much of the work of the limnologists, though by some it is definitely limited to the animal community alone (Petersen, 1913; Gajl, 1927). The general dominance of animals in certain types of fresh water and in the sea, coupled with the minuteness of the phytoplankton, furnishes a ready explanation of this. On the other hand, the biotic nature of the plankton and its greater definiteness as a layer often carry the inference of a biotic community when this was not intended. INIore- over, the extensive study of food coactions in the sea especially has in some cases given the impression of biotic unity when no com- munities were recognized or named. The definite limits of the lake in particular have accorded it an obvious unity, both in terms of habitat and community, rarely to be found in any other area. To a certain extent this has long been recognized, but it was perhaps first clearly expressed by Forbes, in referring to the lake as a microcosm. This view has been emphasized by the limnologists, especially Thienemann, Reswoy and AVerestchagin, who consider the lake as a whole to be an organic entity or organism. With tliem this concept seems to have been a more or less independent development, and it suffers from a lack of acquaintance with the similar concept in vegetation, i.e., the complex organism, which antici- pated it by twenty years. In passing, it may be pointed out that to include the habitat in the community obliterates the essential dis- tinctions between the living and non-living, and carries synthesis to the extreme where its very purpose is defeated. 14 NATURE AND RELATIONS OF BIO-ECOLOGY For the reasons given above, it appears desirable to consider here only such contributions as are based intentionally upon the biotic community, supply quantitative materials for it, formulate new prin- ciples, or apply those already proposed by the plant ecologist for land. The details of these, moreover, are considered in the chapters to which they pertain, along with the studies set aside for discussion there. However, no sharp line can be drawn between them, and the arrangement subserves the necessary requirements of brevity nearly as much as it docs that of historical development. Forbes (1887). Forbes was apparently the first to express clearly the unity inherent in a lake. He regarded it as a chapter out of the history of primeval time. The conditions in it are primitive and the forms of life relatively low and ancient, while the system of organic interactions by which these influence and control one another has remained substantially unchanged since a remote period. The animals of such a body of water are remarkably isolated — closely related in all their interests but very largely independent of the land. A single body of water exhibits a far more complete and independent equilibrium of organic life than any land area. It is an islet of older and lower life — a little world within itself, a microcosm in which all the elemental forces are at work and the play of life goes on in full, but on a scale so small as to be easily grasped. Nowhere else is the coherence of such an organic complex so clearly visible; whatever affects one species must sooner or later have some influence on the whole community. One thus perceives that it is im- possible for one form to be completely out of relation to the others, and realizes the need for a comprehensive view of the whole as requisite to the understanding of any part. With the black bass, for instance, one learns but little by limiting himself to this species; he must study also the species upon which it depends and the factors that control them. It is likewise necessary to determine the course and outcome of competition, as well as the conditions involved. When this has been done, the investigator will find that he has run through the whole complicated mechanism of aquatic life, both animal and vegetable, of which the bass forms but a single element. From the title alone, "The Lake as a Microcosm," it may well seem that the author intended to include the habitat in the entity, but this appears not to have been the case, in view of his references to the "organic complex" and to the "equilibrium of organic life." Cleve (1897). As has been previously stated, for a number of rea- sons the study of plankton, especially the microplankton, had, more or less necessarily, a biotic character from the beginning. This is chiefly because the organisms concerned represent both the plant and animal kingdoms, but it is also due to the quantitative nature of hauls, as well as to the strikingly seasonal and annual cycles involved. The situation is perhaps best exemplified by the pioneer essay of Cleve to distinguish types or communities of phytoplankton in the Atlantic and its ti'ibutaries, based for the most part upon one or more preva- lent species of diatoms. The six communities recognized were termed tripos-, styli-, chaeto-, desmo-, tricho-, and sira-plankton, the name HISTORICAL DEVELOPMENT OF THE CONCEPT 15 being drawn from the characteristic genus. The first of these exhibited several neritic subtypes in the seas about the British Isles and Den- mark. In an estimate of Cleve's work, Gran points out certain diffi- culties (1912:359), but concludes that it yields a biological grouping that is satisfactory in the main. By means of seven or eight samples throughout the year in the same general area, Cleve was enabled to follow the changes in the abundance of diatoms and cilioflagellates in particular. These swarms or pulses correspond in several particulars to the aspects exhibited by land biomes. Petersen and Associates (1911-1925). The first organization of the animal communities of the sea bottom was carried out by Petersen (1913, 1914, 1918), as a by-product of the quantitative study of fish food in different areas. Certain species predominated in the bottom samples with such regularity that it proved possible not merely to recognize eight animal communities from the deep water of the Skager- rack to the Baltic, but actually to indicate the distribution of these on a chart of the region. (See Fig. 84, p. 349.) He clearly perceived the great differences between the various groupings and utilized a synoptic method of characterizing these by means of the prevalent animals. The conclusion was drawn that the Macoma community occurred throughout in the shore zone, the Venus community with certain spatangids on sandy bottom in deeper waters, Brissopsis and its associates on soft clay outside these, and other communities in still deeper water. This classic series of quantitative investigations was centered on the food coactions from producent to consument and upon the compo- sition and distribution of the bottom communities. The first mono- graph, by Petersen and Jensen (1911), dealt with the animal life of the sea bottom, its food and quantity; the second discussed the cor- responding animal communities and their importance for marine zoo- geography (Petersen, 1913). A third report (1914) discussed in greater detail the organic matter of the bottom (Boysen Jensen) , and also described the food and conditions of nutrition for the invertebrate communities in Danish waters (Blegvad) , a theme further elaborated by the latter in 1916. Two years later, Petersen (1918) made a com- prehensive account of the so-called valuation studies of the preceding decade, and in 1925 Blegvad gave further data upon the relations of the dominant fishes to the invertebrate communities. Murray and Hjort (1912). In the "Depths of the Ocean," Murray and Hjort have presented an invaluable summary of oceanography, from what is in some respects essentially a bio-ecological viewjioint. The lack of contact between ecology and oceanography at that time serves to explain in part the absence of a definite and comprehensive account of the biotic communities and their relations, though this is due even more to the enormous number of organisms considered and the necessity of treating various great groups from the standpoint of the specialist. In spite of this, the book constitutes the nearest ap- proach to an actual organization of the pelagic communities in the ocean and supplies a vast amount of data for ecological analysis and 16 NATURE AXD RELATIONS OF BIO-ECOLOGY coordination. The discussion of the microplankton by Gran takes account of the usual division into neritic and oceanic communities and further suggests the major regions or climaxes of the Atlantic Ocean. Appelof has described the bottom fauna without defining communities, but with such a treatment of composition and distribu- tion as to indicate their general outlines. Hjort has recognized and described a number of pelagic communi- ties in both the Atlantic and Pacific Oceans. He has dealt with the vertical ranges of dominants in such detail as to suggest the basis for the distinction of the most important layers. The concept of domi- nance is more or less clearly in evidence, thus making it possible to outline a number of associations and faciations in a preliminary manner. Oliver (1915, 1923). In addition to Oliver, Hedley (1915) and Johnston (1917) have studied litoral communities in Australasia from the biotic approach, but the more detailed work of the first will serve to illustrate their general outlook. In his study of the New Zealand shore (1923), Oliver defines the animal-plant formation as a biotic community with its principal ecological groups in definite combina- tion and relation to the habitat. The community is thus based upon growth forms and environment, and formations are distinguished by differences in the dominant ecological forms. The dominants of the littoral formations are attached animals and plants or in some cases sedentary animals. The effect of the substratum is considered to be of major importance. Accordingly, littoral formations are classed as those on rock, with the dominant form varying from algae to shelled animals, and those on sand and mud, ranging from animal to plant by virtue of height above low tide. These two groups are divided into formations, subformations, and associations, but, since this is without reference to climax or successional criteria, it is uncer- tain how closely these accord with the units employed in the present book. Limnology. The rapid development of this field has been an out- standing feature of biological progress during the past two decades. In a recent monograph by Naumann (1932), hardly a tenth of the 350 titles given in the bibliography had appeared before 1917. It represents in some measure a movement independent of ecology, ap- parently deriving its initial impulse largely from practical considera- tions but going far beyond these in its synthesis of related fields. The number of workers concerned has been large, but the organization of the subject and the formulation of concepts are probably to be cred- ited more to Naumann and Thienemann than to any other two men. It scarcely needs to be pointed out that limnology is that portion of ecology which deals with fresh-water biomes and habitats. It is characteristically ecological in its emphasis upon the measurement of factors and has perforce devoted more attention to the biotic com- munity than any other portion of ecology. As indicated previously it has been quick to perceive the significance of the concept of the complex organism, and likewise the importance of its reaction upon HISTORICAL DEVELOPMENT OF THE CONCEPT 17 the habitat. However, it has concerned itself very little with the nature of the community, its composition in terms of dominants and influents, the processes involved in development, and the distinction between climax and serai communities. It uses an adjective nomen- clature which allows a wide latitude in the concepts concerned. Within the scope of the present book, it is impossible to deal ade- quately with the investigations in this field, a subject, moreover, that is covered in encyclopedic manner by Naumann and Thienemann in the contributions mentioned below. In consequence, the treatment will be limited chiefly to basic concepts and units, and the relations of limnology to the larger theme of bio-ecology, especially as a mat- ter of synthesis (cf. Chapter 7). Thienemann (1913-1935). In discussing the progress of limnology, Naumann (1932:13) considers the first major step to have been taken by Thienemann (1913-14), in basing lake types upon oxygen content and the consequent composition of the bottom fauna. This has re- mained a chief interest through a long series of papers, but these have been accompanied by a number of publications dealing with basic concepts and methods of classification in the field of "biocenotics" or bio-ecology. In this connection, the author has emphasized the causal relation between habitat and community, the reaction of the latter upon the former, and the organic unity of the lake as complex organ- ism, all in close accord with the early elaboration of these principles in ecology in 1901 (cf. Clements, 1904, 1905). A general understand- ing of Thienemann's contributions to the organization of the field is most readily obtained from his papers in Abderhalden's "Handbuch," from "Die Binnengewasser INIitteleuropas" (1925), and "Die Sauer- stoff im eutrophen und oligotrophen See" (1928). Naumann (1918-1932). Naumann's earlier researches dealt mainly with pliytoplankton, with more or less special reference to the biology of production, but since 1922 they have been concerned primarily with the broad organization of the field. Regional limnology has occupied the chief place in this program, but physical factors, reac- tions, and methods have also received much attention, and this has involved also the consideration of concepts and terms. Fortunately for both investigator and student, the author's threescore of papers are epitomized in three recent publications. INIethods are discussed in comprehensive fashion in Abderhalden's "Handbuch" (1925), and guiding principles in "Grundziige der regionalen Liranologie" (1932), while his "Limnologische Tcrminologie" (1931) is a combined lexicon and encyclopedia of the subject. Regional limnology, or fresh-water ecology, is considered from the various angles, viz., habitat factors, types of water bodies, plankton, littoral and profundal in regional correlation, types of lakes and their natural succession, modifications in the biology of production, and the relation to applied limnology. The treatment of limnological terminol- ogy is a compendium of the present knowledge in the field, detailed but concise, and arranged in alphabetical order to permit ready refer- ence to the host of terms peculiar to the field or borrowed from related subjects. 18 NATURE AND RELATIONS OF BIO-ECOLOGY Shelf ord and Towler (1925). In their study of communities in the San Juan Channel of Puget Sound, Shelford and Towler found the general principles drawn from plant communities by Clements to be readily applicable. The analysis yielded three benthic formations or climaxes with two associations each and a number of more or less definite serai stages. This investigation w^as carried forward by several other studies, such as one into the relations of the different barnacle dominants by Towner (1930), the value of these as indicators of salinity (Rice, 1930), and the connection between salinity and the size and form of dominants (Worley, 1930). In 1935, Shelford, Weese, Rice, McLean, and Rasmussen brought together the results of their work covering succession to land, describing a fourth bottom forma- tion and mapping the communities of the area. They found only a little evidence of succession in the partially enclosed waters, though Hewatt (1935) described it for the open coast. Eddy (1925-1927); Gersbacher (1937). For a number of years, Eddy (1925-1927) carried on investigations of fresh-water plankton from the standpoint of development and traced the origin of a pelagic community in Lake Decatur, formed by impounding water to pro- duce an urban supply. In six years such a community has developed through the addition of species from year to year, but without the disappearance of any of these, thus affording a basis for dealing with the problem of pelagic climaxes. Gersbacher (1937) presented a de- tailed account of the development of bottom communities in new lakes including fishes (see also Shelford and Eddy, 1929, a). Molander; Gislen (1930). In separate though related investiga- tions of Gullmar Fjord in Sweden, Molander and Gislen have applied the methods of Petersen, employing the bottom sampler to determine numbers and weights. Molander has considered the bottom commu- nities of animals primarily on clay, since the samples from hard- packed sand, coarse gravel, or pebbles are not dependable. He recog- nizes nine associations, several of them with two or three variants or facies, which are regarded as exhibiting a close analogy with many of those of Petersen. Gislen proposes three new terms for biotic communities, viz., epi- biose, endobiose, and hypobiose, the first two corresponding to Peter- sen's onfauna and infavma. He employs facies in a different meaning, epibioses showing soft and hard bottom facies, and endobioses oligo- tropic facies on sand or rock bottoms, eutrophic ones on clay or on substrata with more or less organic material. A system of life forms is outlined, and extensive tables are given of the production in terms of grams per quadrat. Somewhat more than twoscore associations are recognized in accordance with the usage of plant sociologists; many of these are faciations, consociations, or societies in the classification employed by dynamic ecologists. Bio-ecology and Oceanography. It is evident that oceanography is ecology in so far as it measures the physical factors of marine habitats and the reactions of organisms upon them. In its recent development, the growing feeling for quantities and communities stamps it as marine ecology in every significant respect, though, as with all fields of special HISTORICAL DEVELOPMENT OF THE CONCEPT 19 interest, it will probably continue to be known as oceanography. The essential identity of the two has been clearly recognized by Russell (1932) with respect to fishery research in particular. He states that the latter in point of view and methods is simply a branch of ecology, and its special problems are those of marine ecology. The soundness of this view is shown by the topics discussed, each of which represents an important phase of ecology on land, namely: (1) census of fish populations, (2) fluctuation and prediction, (3) distribution and mi- gration of fish in relation to environmental factors, (4) food chains and animal communities. Bigelow (1931) advances a similar point of view in his discussion of the scope and aims of oceanography, even though ecology is not specifically mentioned. This is revealed not only by the emphasis placed upon unity as a basis for research and hence upon the synthesis inherent in ecology, but also by the clear recognition of the para- mount role taken by the habitat in the control of life and by the reaction of organisms on it. He is furthermore in complete accord with modern ecology in its insistence upon dynamics as the guide to all relations but especially to the cause-and-effect interaction of habitat and community. CHAPTER 2 COMMUNITY FUNCTIONS— THE DYNAMICS OF THE BIOTIC FORMATION THE BIOME AS A SOCIAL ORGANISM Introduction. The biome or plant-animal formation is the basic community unit; that is, two separate communities, plant and animal, do not exist in the same area. The sum of plants in the biome has long been known as vegetation, but for animals no similar distinc- tive term has become current. It is obvious, however, that the two do not represent natural divisions of the biotic complex. The plant- animal formation is composed of a plant matrix with the total number of included animals, of which the larger and more influent species may range over the entire area of the biome, including its subdivisions and developmental stages. The extent and character of the biome are exemplified in the great landscape types of vegetation with their accompanying animals, such as grassland or steppe, tundra, desert, coniferous forest, decidu- ous forest, and the like. These commonly represent biotic formations or climaxes, which in their general features have been noted by natu- ralists since the early days of biology. Each of these consists of a great biotic complex of fully developed and developing communities. The mature mass is the final expression of the response of communi- ties to climate. The term biome, as here employed, is regarded as the exact synonym of formation and climax when these are used in the biotic sense. Nature of the Biotic Formation. The concept of the biome is a logical outcome of the treatment of the plant community as a complex organism, or superorganism, with characteristic development and structure. As such a social organism, it was considered to possess characteristics, powers, and potentialities not belonging to any of its constituents or parts. As indicated in the previous chapter, the recognition of the fact that the plant and animal community are generally coextensive natu- 20 THE BIOME AS A SOCIAL ORGANISM 21 rally led to the assumption that the complex of organisms in a par- ticular habitat constituted an entity. It is further evident that the matrix of this entity is composed of the sessile and sedentary individ- uals, which on land are almost exclusively plants, and in the sea, invertebrate animals. On land, this view is supi)orted by the much more intimate connection of plants with the habitat as a consequence of the direct action of the latter upon them and of the universal reaction of plants upon the physical factors concerned. ^Moreover, the food supply of plants is determined by the amounts of energy and raw materials available in the habitat, while all the food of animals is derived directly or ultimately from plants, though in the sea these may grow at a distance. Naturally, these relations had long been known and were to some degree recognized in the general use of the term "biotic factor" by plant ecologists. Nevertheless, the concept involved in this term did not constitute either a logical or natural treatment of plants or animals in a community based also upon the other group of organisms. Such a treatment becomes possible only with the recognition of both organisms as coactors in a complex of effects proceeding from the habitat as the cause. The tardy recognition of the biotic formation as the essential entity was naturally due, for the chief part, to the specialized training of biologists as either botanists or zoologists. However, a small share in this must be ascribed to the characteristic motility of land animals, which obscured their inherent connection with the smaller communi- ties, and also to such processes as metamorphosis, seasonal migration, etc., as a result of which many species regularly traverse community limits. The Biome as a Complex Organism. One of the first consequences of regarding succession as the key to vegetation was the realization that the community, as noted above, is more than the sum of its individual parts, that it is indeed an organism of a new order (Clem- ents, 1901, 1905). For this reason, it was considered to be a complex organism, bearing something of the same relation to the individual plant or animal that each of these does to the one-celled protophyte or protozoan. The novelty of this proposal naturally evoked criti- cism, but in spite of this the concept has slowly grown in favor, with dynamic ecologists in particular, and by an increasing number has come to be regarded as constituting a new basis for almost unlimited development (Jennings, 1918) . However, it is essential to bear in mind the significance of the word "complex" in this connection, since this expressly takes the community out of the category of organisms as represented by individual plants and animals. With the object of 22 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION making this distinction clearer, Tansley has employed the term "quasi-organism" (1920:123) and Wheeler speaks of "real organisms" (1910) and later of "super-organism" (1923) (cf. Clements, Weaver and Hanson, 1929:314). Moreover, significant support for the concept of the complex or- ganism has been afforded by investigators in other fields. In a vague form, this view now seems to have long been held by foresters, espe- cially by Rossmiissler (1863), but it was not definitely formulated in the idea of a "forest organism" until Morozov (1912), and Moller (1922); cf. also Jaczoski (1926), Glinka (1927), and Thatchenko (1930). In a somewhat similar fashion, the life of the soil has been regarded as a distinct entity by Harshberger (1911) and by France (1913), but this is obviously true only in the sense of a layer com- munity. More definite is the view of Forbes (1887; cf. Chapter 1) and of Thienemann (1925), the latter agreeing essentially with the former, as the following excerpts indicate: "Each lake constitutes a life-entity, the parts of which stand in intimate connection. It is a microcosm, an organism of higher rank, the organs of which stand in the closest relation." In its general form, this concept has been followed by a number of hydrobiologists. It is readily seen that the definite limits of a lake lend themselves to a concrete application, though with erroneous implications as to the biome, and also afford some apparent warrant for including the habitat itself in the complex organism. Quite apart from the fact that this carries synthesis to the extreme, the mention of "biological" lake types indicates that Thienemann hardly intends to go so far. As would be expected, the appreciation of the concept of the com- plex organism has been keenest among students of the social insects, notably Wheeler (1910, 1911, 1923), and of group organization in animals, such as Ferriere (1915), Borradaile (1923), Child (1924), Alverdes (1927), and Allee (1931). Under the title, "The Ant-colony as an Organism," AVheeler (1910) says: "We then have left the fol- lowing series: first, the protozoon or protophyte, second the simple or non-metameric person, third the metameric person, fourth the col- ony of the nutritive type, fifth the family, or colony of the repro- ductive type, sixth the coenobiose, and seventh the true, or human society. Closer inspection shows that these are sufficiently heterogene- ous when compared with one another and with the personal organism, which is the prototype of the series, but I believe, nevertheless, that all of these are real organisms and not merely conceptual construc- tions or analogies." Equally penetrating is the statement by Child in "Physiological THE BIOME AS A SOCIAL ORGANISM 23 Foundations of Behavior," as shown by the following excerpt: "In short, whether we are primarily concerned with the organism or with human society, we can not help but see the fundamental similarities in the processes of integration in the two patterns. In fact, the defi- nition of the organism to which the strictly physiological viewpoint of the preceding chapters leads us will serve almost equally well as a definition of society. The organism is a dynamic order, pattern, or integration among living systems or units. A social organization is exactly the same thing. The fundamental difference between the organism and social integrations among human beings is apparently one of degree or order of magnitude" (p. 270). The philosophical development of the concept of holism by Smuts (1926) has much in common with the view of Child, as the following statements indicate: "The plant or animal body is a social commu- nity, but a community which allows a substantial development to its members" (p. 82). "A whole is a synthesis or unity of parts, so close that it affects the activities and interactions of these parts, impresses on them a special character, and makes them different from what they would have been in a combination devoid of such unity or synthesis. It is a complex of parts, but so close and intimate, so unified that the characters and relations and activities of the parts are affected and changed by the synthesis" (p. 122). "The new science of Ecology is simply a recognition of the fact that all organ- isms feel the force and moulding effect of their environment as a whole" (p. 340). The most recent, and in some ways the most significant, contri- bution to the concept has been that of emergent evolution, as em- bodied in the views of Henderson (1917), Spaulding (1918), Sellars (1922), Broad (1925), Morgan (1926), Jennings (1927), Sumner and Keller (1927), and Wheeler (1928, b) . While this development has taken place more or less independently of ecology, it is in practically complete accord with the earlier concept of the complex organism. This essential harmony is well illustrated by the following extracts from Wheeler's discussion. "Non-human societies ... no less than human society, are as super-organisms obviously true emergents, in which whole organisms, i.e., multicellular organisms, function as the interacting determining parts" (p. 25). "Among the heterogeneous associations we can distinguish the innumerable cases of predatism, parasitism, symbiosis and the biocenoses, or animal and plant com- munities, which constitute a vast series of emergents, varying from those of very low to those of very high integration" (p. 27) . A similar conclusion is reached by Summer and Keller (1927) in 24 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION the statement: "Human society then, by the diversity of its parts, their specialization, the distribution of functions, the mutual service and support of the parts, and their solidarity, is a true system or organization. It has a life different from that of the individuals. The quality of a combination is not the sum of the qualities of its com- ponents. There is a body to study as well as a cell, a society as well as an individual; and the body and the society are things with lives and laws of their own. Hence forces arise in the societal organization which are characteristically societal forces." It is evident that this derives much from Spencer's earlier ideas (1866) and that these may have sprung from the germ contained in Comte's positivist philosophy (1830). The most recent and illuminating discussion of the theme of the complex or social organism is that of Phillips (1935; cf. Tansley, 1935), which must be read and pondered by everyone who wishes to obtain a comprehensive outlook upon the world of living things. To the forward-looking biologist, it leaves no doubt that this con- cept is the "open sesame" to a whole new vista of scientific thought, a veritable magna carta for future progress, as Jennings has pointed out. At the most primitive levels, human families and societies are merely integral parts of the biome. It was only with the advent of agriculture and the control of the habitat by culture and especially of urbanization that man achieved such mastery of biome and habitat as to become an outstanding dominant of a new order. Such domi- nance, however, is chiefly the consequence of the development of steel and machinery. In pastoral areas, man perhaps is still to be reckoned as a constituent of the biome rather than the superdominant in it. Although ecology has advanced beyond the simple distinction of the natural and the artificial, it is evident that this still suggests an important difference in the reactions and coactions exerted by man at the various culture levels, a difference, however, that runs the entire gamut from influence to dominance and superdominance. Conse- quently, as suggested earlier, bio-ecology may at present concern itself chiefly with modern man in the role of coactor or reactor in the biome, leaving for sociology and related fields the development and structure of human communities per se. However, in basic stud- ies of social processes and origins, bio-ecology must lay the founda- tion on which the superstructure of the other social sciences can be reared. Status of the Concept. At first thought it might appear that the recognition of the biome as the basic unit would necessitate much modification in dealing with the development and structure of com- THE BIOME AS A SOCIAL ORGANISM 25 munities. However, further consideration discloses that this is not the case, because of the fact that land plants in their community relations have given expression to many of the chief features of com- munity dynamics. This is an outcome of the rule that plants are practically the universal dominants on land and in shallow fresh water, and it derives also from the unity of the biome arising out of the coactions of plants and animals. The fact that the role of animals in both reaction and coaction was either ignored or not definitely evalu- ated merely requires modifying the list of causes involved and the interpretation of community units with reference to one another. As shown in the succeeding chapter, nearly all the reactions on soil, with the occasional exception of those of earthworms and a few rodents, have been ascribed to plants, and the important effects exerted by animals have been mostly overlooked. In general, the field of animal influence in the biotic community from this viewpoint has hardly been touched. When the ocean is taken into purview, it is seen to exhibit nearly every type of dominance to be found on land and in fresh water, and possibly other types still. For example, Zostera and Phyllospadix are submerged dominants essentially identical with their relatives in fresh water, while Ruppia maritvma actually occurs in both coastal bays and saline ponds in the interior. The tropical and subtropical corals assume forms often very like those of plants; they may provide resting and hiding places, shelter and food for other animals, much after the manner of grasses and shrubs on land (Brooks, 1893:30). Corals furnish shade, retard circulation, and modify gases and solutes, reactions more or less parallel to those upon light, wind, and air in forest and thicket. In terms of accumulated material, their reaction may surpass that of land or fresh-water plants (Bourne, 1910) , since borings reveal coral rock hundreds of feet in thickness in some islands of the Pacific. The coralline algae, though much smaller, play a similar part in warm seas, forming deposits often of great thickness, as Howe has recently shown (1932). The food coactions in the ocean differ greatly from those on land, and to a large degree from those in fresh water. The overwhelming number of producent organisms belong to the phytoplankton; the consuments run the entire gamut of animal classes from protozoans to mammals. The food relations are further peculiar in that there is a wide transport of plankton organisms, both living and dead, as well as of organic detritus, and a considerable amount of organic mate- rial in solution, which may enter into the food cycle. 26 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION CYCLE OF CAUSE AND EFFECT Physical Basis of the Biome. Probably the most important modi- fication of concepts that ensues from the recognition of the biotic community operates upon the current meaning of the term "habitat." The accepted division of factors into physical and biotic has been both logical and useful in the past, but with the rise of the biotic concept this no longer holds. With plants and animals regarded as essential constituents of the community, it becomes undesirable, if not actually misleading, to refer to either as biotic factors. The word factor should, in consequence, be restricted to the various physical forces or conditions that constitute the habitat. Such use promotes clarity of thinking as well as of expression, and accordingly is adopted throughout the present treatment. The word habitat is deeply rooted in the practice of plant ecolo- gists, but it has been variously applied by systematists and others. It has been employed somewhat less frequently by zoo-ecologists, and chiefly in application to an area with its plants or to the specific "niche" of an organism. It is used here solely in relation to physical and chemical factors. It would be desirable to secure greater uni- formity of usage with respect to the complex of physical factors, to which have been applied a variety of terms, such as habitat, environ- ment, station, and biotope. A new term, not only free from these objections but also with merits of its own, is suggested. Such a word is "ece," derived from the Greek, oIko?, home, and already familiar in the derivatives eco- nomics, ecology, ecesis, ecad, ecotone, etc. In addition to its brevity, euphony, and significance, it combines readily with both Greek and Latin stems, yields attractive compounds, and may be adopted into any language without change. In actual use during the past seven years, its value has become more and more apparent, and it bids fair to be of distinct service in connection with the comprehensive analysis of the habitat (Clements, 1925:321). At the same time, habitat remains as a desirable synonym for a term in such constant use, while environment still has a proper role in application to the total setting of individual or organism. Nature of the Habitat. In accordance with the preceding, habitat or ece comprises all the physical and chemical factors that operate upon the community. Of these, water, temperature, light, and oxygen are of vast importance to both plants and animals, and carbon dioxide to all holophytes and a few chlorophyll-bearing animals. The raw materials for food making by the plant are obviously ecial factors, but food itself is not, either for animals or hysterophytes. As to the CYCLE OF CAUSE AND EFFECT 27 solutes themselves, some can be used by the animal directly, while others are available only, or usually, in combination. Substratum and bottom are of much significance for great numbers of aquatic animals, and soil is indispensable to most plants and of no little importance to many land animals. It is a significant fact that, though the factor complex differs greatly between land and sea, the same essential factors are present in both. The characteristic distinction is one of degree or quantity rather than of intrinsic constitution. The two extremes are repre- sented by a single medium, air in the case of epiphytes and water for all submerged aquatic organisms. In this respect, rooted plants are more or less intermediate, the roots being essentially aquatic, though imbedded in soil. Between the two extremes lie a series of habitats with diminishing air and increasing water, exemplified by mesophytes, amphibious, floating, and submerged hydrophytes. Amphibious ani- mals exhibit an irregular alternation between the two media; for intertidal plants and animals the alternation is regular, as it is like- wise in the life cycle of many insects with aquatic larvae. Development and Cycles. On land, as in the sea and in some bodies of fresh water, there are two major types of habitats; one of these corresponds to the climax, the other to the sere. Obviously, in the first, climatic factors are paramount; in the second, edaphic, i.e., local, factors are more controlling. Apart from this major dis- tinction, climates are of wide and often vast extent and relatively few in number; conversely, serai communities are for the most part rela- tively small in size and usually recur in great numbers. Both are essentially dynamic rather than static, but edaphic changes are gener- ally more tangible and progressive than variations of climate. This is due primarily to the reaction of the community, as a consequence of which this and the habitat develop pari passu from initial bare area to a climax. In such a dynamic concept, habitat and sere are regarded as correlated processes or stages of a unified development that terminates in the relatively stable climate and biome (Clements, 1916:357). The sere represents the cycle of development of the community, which resembles in many respects the life cycle of the species- individual. Its duration varies within wide limits, from the few years required for the shortest of subseres to the hundreds or thou- sands necessary for priseres in lakes or on lava flows. The phase of development is relatively brief, however, by comparison with that of stabilization in the climax, except in those fairly frequent cases where such an agency as repeated fire produces more than one sere on the 28 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION same area. Moreover, the climate and climax themselves are never entirely static, the relative stability being disturbed in varying degree through cycles of different intensity and duration. The briefest of these are exemplified by seasonal and annual cycles, expressed in aspection and annuation, phenomena that are also exhibited by serai communities, though to a lesser degree. This is likewise true of the less regular effect of the sunspot cycle of 11 years and its double or triple period. The longer solar cycles may comprise thousands of years, as may also such physiographic ones as cycles of erosion, while back of the major climatic and land-form cycles lie the still greater ones of mountain lifting and continent building. To these necessarily correspond the outstanding changes in biomes and the climates that control them. When it is realized that cycles of different kind and length are operating at the same time, with the phases now in con- junction, now in disjunction, it is evident that habitat and climax are in constant fluctuation. Apart from serai areas, however, most of this has to do at any particular moment with the behavior, size, and abundance of the constituent (not from habitat) species, which thus serve as indicators of habitat variations. It is evident that the subdivisions of the climatic feature of the habitat will correspond to the various divisions of the climax itself, though there is no immediate need for a parallel series of terms. In addition, there are not only the serai habitats or sereces, but likewise one to match each distinct successional stage. There are also the small habitats of individuals, ranging from a huge oak or banyan to sedentary aphids and mites, or sessile algae and fungi. Furthermore, the grouping of organisms in layers supplies a certain warrant for dividing the habitat in the case of those limited to a particular layer (Shelford, 1913, a; Yapp, 1922). However, it is obviously illogical to carry such analysis to the extreme of speaking of the root or shoot habitat of a particular individual or species, as has been suggested by some workers. Finally, a large number of animals are concerned with two or more habitats. This is a characteristic relation for insects with aquatic larvae in the hydrosere, and also for migrating birds and fishes and some mammals. These may occupy two or more climates each year or during their life history, and the birds and mammals in particular may live in both climax and serai habitats. It appears significant that in the forest biomes of North America, at least, the larger mam- mals are often best represented in subclimax areas, and the birds in forest margins, where herbs and shrubs alternate in a transition belt or an ecotone, or in serai stages. CYCLE OF CAUSE AND EFFECT 29 Although the question of the biotic habitat presents no serious difficulties, the delimitation of habitats in lake and sea is compli- cated by a lack of visibility. In general, the two major principles of limits of dominants and definite changes in conditions appear to be as applicable in water as on land. The primary divisions of the ocean, for example, should be in close correspondence with the marine communities, and the dominants of the latter should furnish the chief indications of climax limits, with the aid of factor measurements as necessary adjuncts. In the littoral reaches down to 200 meters, or thereabouts, the great density of the medium produces major physical differences in smaller spatial limits, in proportion to the greater density of water as compared with that of air. As a result, the major habi- tats are correspondingly smaller than on land. The deeper bottom ones are known only in a very fragmentary way, but the impression afforded by the great marine expeditions, as that of gradual change over large areas, may not be correct. The pelagic communities of the sea have no counterpart on land, and the greater mobility of the ocean, as expressed in currents, up- welling, tides, storms, icebergs and pack ice, appears to render bound- aries broad or even vague, a consequence possibly augmented by the mobility and motility of pelagic dominants and influents. The vast depths of the ocean further complicate the problem in a fundamental fashion and probably make it necessary to limit pelagic communities both vertically and horizontally (Murray and Hjort, 1912:617). Such features of the ocean floor as the Wyville Thomson or Iceland-Faroe Ridge (1,500 meters above the Atlantic floor at the south) exert a dis- tinct influence on the deeper pelagic communities, but it is hardly com- parable with the striking effects of this ridge upon the benthic com- munities of the same area or of some ridges of similar height on the land communities near the coast of California. AVhether it is possible or desirable to recognize serai habitats in the pelagic realm of the ocean remains an open question at present. How^ever, it appears probable that the movement of great masses of water by currents, or through upwclling, produces areas relatively free of organisms, into which invaders may press, and it is not impossible that similar effects may be produced by drifting ice. On the other hand, while they often result in great variations in abundance, the seasonal and annual cycles of the microplankton are not to be re- garded as successional processes, but are characteristic phenomena of aspection and annuation (p. 315). In the tidal area, the question of habitats is much simpler and with close parallel on land. The importance of surface for attach- 30 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION ment varies inversely with the factors controlling stability. Where wave action is strong, surface for attachment c^uite overshadows the physical factors of both land and water; where it is reduced to a minimum consistent with the deposition of sand, barnacles attach to small pebbles and sea mussels form mats upon which a community usually characteristic of rock may be essentially complete. However, , the building-up of a muddy bottom, as in estuaries and land-locked bays, gradually withdraws the shore from the tidal belt and initiates a halosere from brackish water to land; a somewhat similar transi- tion to land is exhibited by coral atolls and volcanic islands. Small bays may undergo succession to land directly from salt water through the invasion of halophytes, Salicornia, etc. (McLean, 1935). During the past, epirogenic agencies were active in the production of such habitats, especially on the continental shelf, but also in the midst of continents, as illustrated by the withdrawal of the great Mediterranean of North America during the late Cretaceous. Causal Sequence. Inherent in the very name itself is the basic principle of ecology that the habitat is the complex of factors or causes. Ecology is not merely the science of the habitat, but pecu- liarly also of the cause-and-effect relation between this and the biotic community, whether on land or in the sea. Some have assumed that its attention was focused so largely or exclusively on the habitat as to preclude any interest in the life found in it, while others have thought that the study of communities was paramount, with little or no consideration of the habitat. The two views are equally in- complete, and the essence of ecology lies in its giving the fullest possible value to the habitat as cause and the community as effect, the two constituting the basic phases of a unit process. The assump- tion that the habitat is entirely subordinate to the community in value and interest appears to be current in plant sociology, but so far as there is any difference between this and ecology, it resides in the fact that ecology is primarily concerned with causes, but solely by reason of their effects on life. For such researches, the use of quanti- ties is imperative, and hence the cardinal points of ecology, as distinct from its parts, have come to be measurement, experiment, and devel- opment, applied to habitat and biome as inseparable cause and effect. In the plant matrix of the land biotic community, the causal sequence is a fairly simple cycle. The action of the habitat as ex- pressed in stimuli gives rise to responses on the part of the plant or community. These in turn operate on the habitat, producing reactions that modify it, and then again in turn its action on i)Iant life follows. Embraced within this primary cycle is a secondary one of interaction CYCLE OF CAUSE AND EFFECT 31 or coaction between species and between individuals, both plant and animal, well exemplified by plant parasites and saprophytes. The end results of these processes are still other reactions, especially on the soil. Animals too are acted upon directly by the habitat and then react upon it in some degree, but their energy relations are primarily a matter of food supply. In consequence, coaction becomes a response of paramount importance, and plants as middlemen between the supply of solar energy and animals may be regarded as constituting a group of secondary or intermediate causes. Plants likewise exert coactions upon animals, and in the case of lethal parasites these lead to soil reactions through the decomposition of organisms. Hence, the complete cycle of causes, and of effects that become causes in their turn, includes the action of the habitat followed by the responses thereto, which in turn become causes of further change. On land, the plants as dominants and subdominants play the major role in reaction; in the large bodies of fresh water and in the sea the situation is more or less reversed. In the intertidal and subtidal belts of the continental shelf, the animal dominants assume the lead, except occasionally where attached algae become the codominants. In the open ocean, the reactions of the phytoplankton and of the ani- mals are not readily separated or evaluated, as for example in their effect on light. In ponds and shallow lakes, plants are usually the chief reactors. It is obvious that the medium water as the seat of the reaction has much to do with its nature and degree. This sub- ject is discussed in considerable detail in the succeeding chapter. Adjustment and Adaptation. In the case of plants, the immediate response to the action of the habitat is a quantitative change in one or more functions, which is often followed in time by a more or less evident modification of structure or form. The first phase of this process has been termed adjustment; the second, adaptation (Clements, 1907) . Growth is a complex of functions and hence it is to be regarded as adjustment, but when the intensity or duration of a factor is suf- ficient, it results in a change of behavior or structure. In sessile ani- mals, the processes are similar to those of plants (Wood-Jones, 1910). In motile animals, this relatively simple sequence is modified by vir- tue of a more or less effective regulatory mechanism, but it is also possible to trace a connection between habitat and behavior. In spite of the fact that the plant is often more closely dependent upon the land habitat than is the animal, both exhibit much the same or equivalent general adjustments. This is true in broad terms not only of function, growth, and behavior, but also of time of ap- pearance (Clements and Long, 1923), numbers, grouping, and so forth. 32 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION Such adjustments are often correlated with more or less striking adap- tations, clearly so with most plants, but less evident and frequent with animals. When adjustment has once been stabilized as a special adaptation, a certain degree of plasticity or power of reversion is lost, and new adjustments and adaptations follow a different course. A somewhat similar result occurs when correlation or competition be- tween organs or parts enters to produce effects not directly correlated with the habitat and hence apparently opposed to the rule. The viewpoint as regards structural adaptations in sessile animals is similar to the older views held regarding land plants (Wood-Jones, 1910). W'ith land plants, the causal sequence that terminates in adap- tation may operate upon the individual, the species, or the commu- nity. Actually, it affects the individual directly and concretely, and the phyletic and social groups in conseciuence. In respect to the species-individual or specient, these effects are summed up by the life history in terms of adjustment, and in the life form, etc., in so far as they deal with adaptation. With respect to the community, ad- justment is represented by a series of basic processes or functions, and adaptation by the structures expressed in the climax and serai com- munities of different rank. It is obvious, however, that in a dynamic system life history and life form are constantly interdependent, and that the modification of either organism or community carries in- escapable consequences to the other (Clements, 1931). In motile animals, structural adaptations are preeminently related to activity. From the standpoint of community relation, the signifi- cant activities are connected with layers or strata of the community, and hence adaptation is to epiphytic life, especially arboreal in the larger species, to cursorial and to subterranean life. Such modifica- tions are noteworthy, but they may bear no definite relation to the community as a whole: for example, subterranean adaptations in the tundra are hardly distinguishable from those of the tropical grass- land. However, the fact of their existence may be an element of much importance in both communities through the activities corre- lated with them. Animal organisms come into existence with certain innate behavior characteristics. Some of these are simple reflexes, such as backing off and turning in Paramecium; others are complicated activities. In the larger and more influent animals, these innate or instinctive characters are the basis of the selection of food and habitation and the formation of habits, and thus determine the course of reaction and coaction phenomena. Associative memory and intelligence play an important part in the activities, coactions, and reactions of the vertebrates, LIFE HISTORY 33 arthropods, and Mollusca. Homing intelligence is especially impor- tant; thus, ''tradition" plays its part in the choice of areas of winter- ing, as in the Kaibab deer (Rasmussen, in MS) . At the same time the habits of animals during the earlier part of their life histories are commonly molded to some degree by their community associates and habitat conditions. The mores are thus, in part, a community prod- uct. There is unquestionably some teaching of young among birds and mammals, as in the coyote (Bailey, 1930). Social organization of wolves leads to the formation of pack hunts and to the establish- ing of regular routes of travel. Ungulates also assemble in herds with some degree of organization. In Africa, where there are many species with great numbers of individuals and where mixed herds occur, the danger signal of any one species may serve to warn the entire herd. In similar fashion, sheep and goats post sentries in outlying positions to give alarm at the approach of danger (cf. Roosevelt, 1910; Holmes, 1911). In addition to all these activity phenomena, plastic and moldable by community contacts, there are many similar responses which result in "regulating" the organism into a suitable situation. When the organisms find themselves in unsuitable and thereby stimulating or irritating conditions,, random movements and activities take place, some one of which relieves the irritation, and the organism comes to rest. In addition, practically all animals possess a capacity for ad- justment, e.g., metabolism and temperature regulation characterize warm-blooded animals especially. There is also regulation wdth refer- ence to respiration, neutrality, water, and osmotic pressure. All these call into play behavior, muscular activity, and special organs not found in plants, and serve to illustrate the greater emphasis which must be laid on activities and physiological processes in animals as compared with plants (Shelford, 1911, e, 1913, a). LIFE HISTORY Definition and Significance. Life history is the life cycle of the individual; it embraces the entire round of activity or behavior from birth to death. It is not only a cycle in its complete expression, but it also often includes minor cycles corresponding to those of the day, season, or year. These serve to mark the phases or stages of what is essentially a continuing process, and hence organize and illuminate the host of details that constitute the round of life. Embryonic stages, though an intrinsic part of a life history, are best treated in the specialized fields of embryology or morphology, with the possible 34 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION exception of minute or microscopic organisms. Thus, it is most con- venient to limit life histories to the round of growth and behavior observable in nature or in culture, but this should involve, as an essential feature, the use of both cjuantitative and experimental meth- ods. The lack of such methods and measurements has deprived much work in this field of anything more than suggestive value, and it should now be generally recognized that definite and objective results are rarely to be obtained without measuring factors and responses, and also reactions and coactions. To what extent functional response should be included is still to be determined, but the answer is affirma- tive in respect to plants and sessile animals. It is evident that the major features of the life-cycle of plants and animals are similar to the extent of passing through the round of birth, growth, multiplication, senescence, and death (cf. Taylor, 1924, 1930, a). As has been stated, various forms and characteristics of land plants are displayed by certain aquatic animals. In general terms, this becomes significant in connection with the life histories of the larger organisms playing a role in biotic communities. These large and macroscopic multicellular organisms may for present pur- poses be divided into sessile and sedentary ones, as opposed to the motile types. The unicellular and microscopic species of both plants and animals require special treatment, which is beyond the scope of the present discussion. Sessile and Motile Organisms. The former includes land plants generally, the large zoophytes, corals, etc., and a series of smaller hydroids and the like. Most of these attached animals belong to the sea or fresh water and there is also a large group of sedentary forms which have little or no capacity or tendency to move about. Nearly all these sessile and sedentary organisms are producers of disseminules: seeds, spores, etc., are produced by plants; and eggs, free-swimming young or larvae, stages in alternating generations, winter bodies, and specialized parasitic stages, by animals. The disseminules are prob- ably always more widely dispersed than the adults themselves, both as regards space and habitat. Many come to rest more or less acci- dentally in conditions not compatible with continued existence, though the delicate larval stages of some animals that swim about feebly before seating must not be overlooked in the matter of distributional details. The life histories of the vast majority of these organisms may be best considered as starting with the successful seating and begin- ning of growth in the new position. Habitat selection by this means is accompanied by an enormous loss of disseminules before seating, to LIFE HISTORY 35 say nothing of the great mortality among those that find conditions unsuitable for growth before maturity is reached. Only a few are able to grow to maturity under this indirect method of selection. Among the multicellular motile species, with certain notable excep- tions illustrated by a few fishes with pelagic eggs, the eggs or young are very carefully placed in a suitable situation by the parent, and the account of the life history properly speaking begins with the breeding adult. However, land plants and animals differ fundamen- tally as to nutrition, motion, factor control, and complexity, with the result that in detail their respective life histories have little or noth- ing in common. It thus becomes necessary to deal separately with the two groups, though obviously this does not preclude taking into account the intimate relations between plant and animal in the course of their respective cycles. Relation to the Habitat. The relation of the life history to the habitat is direct and intimate in the case of plants, a fact reflected in the close correspondence of the two cycles during the year and embodied in the phenomena of seasonal appearance, or phenology. Such a connection is inherent in the process of aspection, in accord- ance with which both plants and animals exhibit a seasonal rhythm of appearance, growth, and reproduction. It is likewise concerned, though to a less striking degree as a rule, in the related process of annuation, in which presence and number are modified by the climatic cycle. As indicated more fully later, hibernation and estivation are to be regarded as peculiar types of aspection, while diurnation is a some- what similar process operating in a daily cycle. Thus, the flowering of a dandelion shows not only an annual and seasonal maximum, but a marked daily period as well. The metamorphoses and activities of insects and other invertebrates belong in the same general category. In organisms with very short life cycles, such as diatoms, physical factors may bring about two or more maxima of reproduction during the year. One of the most striking examples of direct correlation of habitat and control of life history is that cited by Russell and Yonge for periwinkles (1928:51). The species nearest the low-water mark hatches out in a very early stage as swimmers, the one near the mid- dle of the intertidal belt appears in a later swimming stage, and that near the high-water line produces young like the adult and therefore able to crawl over the exposed rocks at once. 36 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION PLANTS Relation to Life Form and Habitat. The correlation between life form and life cycle is not merely fundamental and comprehensive, but it is likewise reciprocal in a high degree. Not only is the life cycle the dynamic expression of the life form, but, in turn, the round of behavior has a more or less definite and recognizable effect upon the forms assumed by the organism. The first relation is well-nigh universal wlien the phyletic or taxonomic form and the vegetation or biome form are identical, as is often true of invertebrates and crypto- gams. It is little in evidence in flowering plants, except for families with highly specialized shoots, such as the grasses and cacti. Habitat form and growth or competition form bear little or no relation to taxonomic position, with the exception of such rare instances as the water lilies, in which vegetation and habitat form are identical. The influence of form upon the life history is compelling in the phyletic or biome form; it is much diminished in that of the habitat form and disappears more or less completely with the competition form. Con- versely, the effect of life history upon morphology is greater wdth the more recent forms, and it is either absent or little visible in the fixed types. Outline. The following account is designed to serve a twofold pur- pose. In the first instance, it is intended to provide a concise guide to the study of particular life histories in such detail as the biotic approach may warrant. In the second, it is to furnish a basis for the investigation of coaction as the essential bond in the biotic com- munity, as revealed by the interplay of the life cycles of the respective plants and animals. This is illustrated by frequent correspondence between active periods in animal life histories and the flowering of seasonal groups of plants which supply food or shelter. Number of Stages. It is obvious that all plants agree in exhibiting the three cardinal points or stages of a life history, namely, birth, development, and death, or loss of identity at least, as in the case of fission in unicellular algae. Likewise, it is clear that morphological specialization reflects developmental history, with the consequence that stages and activities increase in number from lower to higher forms as a rule. In plants the principle holds without exception, though the alternate generations of mosses and ferns are naturally much more visible than those of flowering plants. In the great majority of plants, the life history begins with the germination of spore and seed, is continued through growth and prop- agation, and terminates in reproduction. In the simplest one-celled PLANTS 37 algae, reproduction does not occur; in others, such as the desmids and diatoms, it has not advanced beyond the fusion of two single cells. Both plant body and reproductive organs undergo some advance in the thallophytes, but this is relatively slight until liverworts and mosses are reached, the mosses exhibiting a threefold differentiation into protonema, leafy gametophyte, and semi-independent sporophyte, The specialization of the shoot in many ferns ajiproximates that of the flowering plants, though the gametophyte is still regularly autono- mous and the disseminule is a spore rather than a seed. AVith the advent of the flowering plants, the shoot began to vuldcrgo a marked differentiation entirely independent of the phyletic form or family, though this process was little felt by the gymno- sperms. In consequence, it is only in the angiosperms that the specialization of life forms becomes a characteristic feature and is accompanied by even greater modification of flower and fruit. Since the flowering plants comprise practically all the dominants of terres- trial vegetation today, it will suffice here to consider their life histories alone. These are treated under the following main heads: germina- tion, growth, movement, propagation, and reproduction, together with the expression of these in the community functions, reaction, compe- tion, and coaction. Germination, Seeds and fruits differ in a number of respects that have a bearing upon that portion of the life history represented by germination. Protection in the form of a hard or bony coat operates against destruction, through digestive fluids, of most fleshy fruits or seeds, though it also may be concerned with rendering them unpala- table. For a few, germination is made possible, or at least is im- proved, by passage through the digestive tract of some animal, and this is likewise true of some fungus spores. Finally, in a few grasses and geranials, the awns of the fruit serve not merely for dissemina- tion, but also for forcing the seed end into the soil, as is notably the case in Stipa and Erodium. Growth. The development of a representative flowering plant ex- hibits three major phases, seedling, juvenile, and adult, though without definite limits between them. Two related processes, propagation and reproduction, are likewise of major significance, but their posi- tion in the sequence of development is often less definite. Flowering and fruiting may mark the last phase of the life cycle, as in the annual, or the final phase for the year, but they may also occur at the outset of the season or during its middle course, to be followed by the development of leafy shoot or underground stem. A consider- able number of herbs do not flower until the second year, and some 38 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION require eight or ten years to reach maturity. This is well exemplified by Erythronium albidum, which each year produces one-leaved flowerless shoots until the contractile roots have drawn the bulb down to the proper level for reproduction. In nature, it is not usual for trees to produce flowers under ten years, and in some soecies the period of youth is doubled or trebled. The life history of the shoot is essentially a matter of the reciprocal development of leaf and bud. Each leafy axis arises from a bud and in its turn gives rise to new buds, typically in the axils of leaves, but also at other places on stems, and even on roots. The further develop- ment of a branching plant, especially a woody one, is determined by the relation of terminal to axillary buds and the outcome of their competition for food. At this point, development passes over into the characteristic features of the life form. Movement. In spite of their stationary nature, flowering plants all possess the power of movement in a restricted sense, for example, growth and the circumnutation of stem and root tips. More pro- nounced and less general are such tropisms as the turning toward light, water, etc., the opening and closing of flowers, and the changes in position displayed by flowers and fruits. Clamberers owe their habit primarily to growth, supplemented by petioles, prickles, spines, etc.; twiners ascend by means of a spiral movement; and climbers, by virtue of tendrils, rootlets, or specialized petioles. Leaves exhibit a variety of movements, from the active ones of sensitive plants and flytraps to the slow but much more common ones resulting in the day and night positions connected with the so-called sleep of plants. These occur especially in compound leaves and hence are of frequent occur- rence in the pea family. Propagation. This term is here employed in its botanical sense to apply to asexual multiplication by natural rather than artificial means. It involves something more than mere increase, inasmuch as duration and migration are also connected with the process. Among flowering plants, it occurs rarely with annuals, though the character- istic tillering of grains and other annual grasses might be included here. It is not a common feature of trees and shrubs, except when the regenerative process has been set up through some accident, and is then largely confined to angiosperms. While present in other eco- logical groups, propagation attains its greatest expression in peren- nial herbs. In fact, these owe their distinctive habit to this process, and their life forms are determined by the manner in which this func- tion is carried out. Process and form are so intimately and obviously related that it is impossible to consider one without the other, but PLANTS 39 in dealing with life histories the dynamic relations are necessarily- emphasized. Propagation has been the outcome of the progressive modification of the shoot, partly through a changing relation to ecial factors and partly through the differential storage of food for the buds. It has also been deeply influenced by the nature of the shoot and especially the bud. Out of this interplay have sprung a number of well-known propagules widely employed by the gardener for artificial multiplica- tion. These range from leafy shoots, modified only to the extent of It*''. ^- ** ««»*^^iififi Fig. 1. — Propagation by root stocks and consequent migration of Co)tvolvulus soldanclla on fore dunes of the strand ; southern Cahfornia. (Photo by Edith Clements.) developing roots where the tip or the nodes touch the ground, as in the stolon, to types so transformed as to be recognizable as shoots only by the presence of buds, such as corms. Between these lie off- sets, runners, scaly and fleshy rhizomes, tubers, caudexes and bulbs (Fig. 1). The nature of the propagule has a direct bearing upon other fea- tures of the life history, such as aggregation, migration, duration, and competition. AVhen the shoot extends in a horizontal direction, as in the scaly root stock of quackgrass or the runner of the strawberry, migration, though slow, is definite and assured. When it is short or 40 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION erect, aggregation is favored and migration is slight or absent. Dura- tion is partly a matter of life form and partly of the type and amount of growth, as is shown by the varied behavior of the species of Erythro- nium. The kind and degree of competition are modified by the rela- tion between aggregation and migration, competition between individ- uals of one species being emphasized in the one instance and between two or more species in the other. For the details of life histories from the morphological standpoint, "Die Lebensgescliichte dcr Bliitenpflan- zen Europas" is a mine of information (Kirchner, Loew and Schroter) ; from the ecological point of view, the life cycle has received atten- tion on an experimental basis (Clements, AVeaver, and Hanson, 1929). Reproduction. By contrast with the preceding processes, sexual multiplication or reproduction is concerned with the flower and its products, fruit and seed. In essence, however, it is but a continuation of the growth of the individual, and the seed is in effect the analogue of the bud. Since the flower is not a food-making organ, it is less intimately related to the habitat than the shoot, though its periodic behavior, both as to season and day, is directly connected with tem- perature, and to a smaller degree with water and light. A number of flowers exhibit a definite cycle of opening and closing, and related movements not infrequently occur in the flower cluster as well. The behavior of a flower is determined in large measure by its structure, which is a matter of its phyletic position or taxonomic form. This controls the type of flower cluster and the kind and ar- rangement of the flowers, and in consequence the major phases of the reproduction cycle, namely, blooming, pollination, fruiting, seed pro- duction, and dissemination. In the present instance, the limitations of space permit only the most concise treatment of these, and to obtain a basis for detailed studies in this field it is necessary to turn to the comprehensive accounts of the several processes. As before, the "Lebensgeschichte" is invaluable for this purpose, while for blooming and pollination, Knuth's "Handbook of Flower Pollination" is of par- ticular importance. The experimental approach, especially from the ecological standpoint, is embodied in "Experimental Pollination" (Clements and Long, 1923), and "Anthokinctics" (Goldsmith and Hafenrichter, 1932). Structure of Flower and Cluster. The life cycle of a flower is dependent upon its structure; the manner of pollination is connected with both structure and arrangement. The daily round of floral be- havior is wrought upon the pattern supplied by the number, position, and structure of the four parts, calyx, corolla, stamens, and pistil. It is intimately connected with the task of securing the proper trans- PLANTS 41 fer of pollen, preferably by means of cross-pollination. Hence, it is the basis of the many and varied coactions exhibited by the flower- loving insects and birds. When plants are one-flowered, it is obvious that cross-pollination alone is possible, while in such clusters as the head of composites, the automatic transfer of pollen between florets may become a regular occurrence. The relative position and develop- ment of the stamens and pistils not only affect the method of transfer, but they also determine the kind of fertilization that results. A de- tailed treatment of the various types of pollination is to be found in Knuth's "Handbook" (pp. 28-60) and various other works. Period of Flowering. The time and duration of flowering bear a fairly definite relation to the adult stage of the individual plant. However, in many perennial herbs and woody plants, the relation is inverted, the flowers appearing before or with the leafy shoot, owing apparently to a delayed bud formation overtaken by winter. A few species blossom more or less throughout the growing period and others are somewhat irregular, but the large majority fall within a fairly definite season. As a consequence, it is possible to distinguish these as prevernal, vernal, estival, autumnal, and hiemal plants, each giving character to a particular aspect. While the flowers of most species open once for all, in a consider- able number there is a marked daily rliythm of opening and closing. This cycle depends primarily upon temperature, but in some cases it is connected with light, as radiant energy, or with humidity. The part actively concerned in the movement is the corolla, the calyx assuming an imitative role; in composites, the involucre may be as much affected as the ray-florets. Although opening and closing may occur at almost any time during the twenty-four hours, the tendency is to open in early morning or evening. Species that open during the daytime are termed hemcranthous or day bloomers, in contrast to nyctanthous or night bloomers. Flower Cycles. AVithin the seasonal cycle of blooming of each species lies the life cycle of the individual flower, essentially alike for all, except where there are two or more kinds of flowers, such as perfect, staminate and pistillate, or open and cleistogamous. In all flowers or heads with movement, there is also a daily cycle as just indicated, with the exception of ephemerals, in which the life period and the daily cycle coincide (Fig. 2). It is evident that the seasonal and the daily period of flowers are intimately connected with the coactions of insects, esi)ecially pol- linating ones. Practically every change of the flower or its parts has some influence upon the procedure in attracting insects and insuring 42 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION the deposit of pollen, as illustrated later under pollination coactions. In the community sense, the complete floral cycle includes not merely the behavior of flower and cluster, but also the interaction of these with the deportment of the pollinator. While the general subject of pollination has received much attention since the time of Darwin especially, complete and detailed life histories have been a matter of recent concern (Clements and Long, 1923; Clements and Clements, 1913, 1928). Fig. 2. — Round-of-life in the flower of wild onion (Allium cernuum) ; Alpine Laboratory, Pikes Peak, Colorado. (Drawn by Edith Clements; courtesy of Carnegie Institution of Washington.) Fruiting and Seed Production. In the great majority of species, the pistil merely enlarges with the developing ovules to constitute the fruit, but in many others another part of the flower shares in its forma- tion. Such changes are not only of interest as a late phase in the life cycle of the flower, but they are likewise of much importance in connection with coactions concerned with food and with dissemination. Dissemination. Plants fall into two general groups, in accordance with the presence or absence of special devices that aid in the dis- tribution of seed or fruit. Many species possess no such modifications, and their dissemination is chiefly a matter of chance operating upon a high seed production. On the other hand, a vast number exhibit some PLANTS 43 feature that promotes migration and a considerable group have be- come highly specialized in this respect. Such specialization has af- fected the fruit as a rule, by virtue of the available material in the wall; seeds are much less frequently modified, hairs and wings con- stituting the usual devices. In fruits, the modification may assume the form of a sac, wings, hairs, parachute, chaff, plumes, awns, spines, hooks, or a fleshy pulp. Most of these are adapted to distribution by wind, but awns, spines, and hooks serve for carriage by attachment, and fleshy fruits are distributed in consequence of their use as food. The i)rincipal agents in dissemination are wind, animals, and man. Although many disseminules are carried by water, especially in ocean currents, few of these remain viable after long immersion, except those of water plants. It is obvious that carriage by the wind and by attachment to animals depends upon the development of a suitable modification. This is true, in part, of fruits and seeds used for food, notably the fleshy ones, but a large number of these are scattered incidentally by animals that seek them. From these interrelations springs a vast group of seed and fruit coactions; though these have received much general attention, their comprehensive and detailed study in various communities awaits further recognition of their importance. Community Relations. It is hardly necessary to emphasize the point that the life history of an isolated individual differs in a number of respects from that of similar individuals in their proper community setting. Hence, complete and detailed life histories can be observed only in the natural habitat, even though garden or other control methods can be profitably employed for the major phases of germina- tion, growth, propagation, and reproduction. In the first place, com- petition is the outcome of the number and spacing of individuals, whether of the same or different species. It depends primarily upon the reaction of these on the habitat, a process that leads generally to a limited supply of some essential factor. When this effect is marked, growth may be seriously hindered or entirely inhibited at any stage in the life cycle. Thus, competition may lead to the sup- pression of branches or propagules; it may prevent the formation of tillers or the production of flowers. On the other hand, it may pro- foundly modify the size, number, or structure of organs or parts, with a more or less corresponding effect upon reaction or coaction. Because of the primary relations of plants and animals in the community, coaction is always an important and often a controlling process in the life cycle. This is particularly true of food coactions and especially of those concerned in pollination. Grazing animals 44 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION may keep grasses more or less permanently in the vegetative condi- tion; browsing ones may in addition change the form of trees and shrubs directly, or indirectly by promoting regeneration, while gall- flies may completely transform shoot, leaf, or flower. It is difficult and often impossible to deal adequately with the life history of either plant or animal without taking their coactions into full ac- count. Indeed, this many-sided interaction within the life cycle of associated plants and animals constitutes the essential bond of the biotic community. ANIMALS In the life histories of animals, considered from an ecological viewpoint, it is the physiological states through which the animal passes rather than the morphological or form stages that are impor- tant. The response systems and instincts where such occur are also of prime importance (cf. Taylor, 1924, 1930, a). This has led to the term "physiological life history," which is unnecessary except for emphasis. Again, the usual morphological procedure of starting the account of the life history in the germ-plasm tissues, or with the egg in the case of sexual reproduction and with the somatic tissue changes in the case of asexual reproduction, must be abandoned. A logical discussion of life history in motile animals usually begins with the mature adult and with the primary emphasis on its response system. The new motile disseminules of sessile organisms do not constitute an actual beginning until seating occurs. Sessile and Sedentary Animals of the Waters. As has already been suggested, disseminules in the form of free-swimming larvae are regarded as the beginning of the life histories. These disseminules are carried far and wide by currents, w^aves, and their own feeble powers of locomotion. Responses to tactile, mechanical, chemical, and physical stimuli largely govern attachment, but this by no means insures survival to maturity. ]\Iany barnacle larvae attach to tidal rock only to be killed after assuming the adult form, by the accident of hot weather falling at the period of extreme low tides and conse- quent maximum exposure to air (Rice, 1935). The existence of a medusa stage which is both free swimming and a disseminule bearer in some coelenterates does not materially alter these facts. In the northern seas, there is a sequence of disseminules of associated seden- tary species (Johnstone, 1908), leading to a season of maximum den- sity and some seasonal groupings (Fig. 3). The reactions of these disseminules upon the substratum for at- tachment consist in covering the surface or changing its character. ANIMALS 45 The ability of many sessile marine animals to attach to each other, however, tends to reduce the effects of the first arrivals on any sur- face, especially if they are shell bearers. The duration of life cycles is of vast importance in determining apparent degree of dominance and the arrangement of species found at any time (Rice, 1935). This is especially true of barnacles and bivalves, which are abundant in the tidal communities and in such subtidal ones as occur in the Danish waters. These short life histories (two to ten years) lead to a rapid replacement of individuals and make the arrangement of subordinate groups and the margins of Jan. Feb. Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec. 3 Copepod nauplii Ascidian larvae Balanus nauplii Balanus cypres Crab zoeae Plutei Crab megalops Fig. 3. — The seasonal sequence of lai\al forms in the plankton of the northeast Atlantic. (After Johnstone.) communities shift back and forth rapidly, to a degree unknown on land. Parasites. Parasites are of importance in communities only as they decrease the vigor, fecundity, abundance, etc., of dominant or influent organisms. In every case in which they do have essential relations, the determination of the life-cycle characters is of great significance. Generally speaking, four types of parasites may be rec- ognized: (a) bacterial parasites that have the simplest of life histories characterized by very rapid development and decline within the or- ganism and are occasionally responsible for malignant infectious dis- eases of influent animals; (6) internal animal parasites that frequently infect more than one organism and do not ordinarily kill the host appear quite generally to have little or no detrimental effect; (c) external i)arasites, usually chiefly arthrojiods, with very simple life histories which become important occasionally when they are cspe- 46 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION cially numerous or carry some form of internal parasite; (d) internal insect parasites that infect only other insects and their eggs and cause the death of the host. The life histories of the external parasites of the mammals and the insect parasites of other insects are very simple and not essentially different from those of animals feeding in some other way, but they are of much importance in any attempt to evaluate their coactive effect. The internal parasites are chiefly worms of the several phyla, protozoans and a few arthropods. The life history of the metazoan parasites is often complicated, as it very commonly involves two hosts. Transfers from host to host are divisible into three chief classes: (a) through contact with feces; (5) through the devouring of herbivores by carnivores and omnivores; (c) through contact with water in drink- ing, bathing, or swimming. Motile Animals. The breeding activities are the center of the environmental relations of such animals (Merriam, 1890; Shelford, 1911, a-e). This does not mean, however, that factors operating at other periods and with reference to other activities may not be more important in some cases (Kendeigh, 1934). Two types of life history resulting from method of reproduction may be recognized, i.e., some animals are oviparous and others are viviparous. From the standpoint of ecology, the life history of an egg-laying animal may well begin with the adult, usually with the laying female. She selects a place for the eggs that is suited not only to them but also to the young at the time of hatching. The adult appears to be in a physiological state similar in many cases to that of the young at hatching. This is a noteworthy characteristic of the tiger beetles investigated by Shelford (1915). JMany fishes construct nests in which the young pass their early sensitive period. In this case both sexes reach a physiological condition similar to that of the young, recurrently each year. The same is true of birds which re- turn each season to the same climatic and habitat complex to breed. The anadromous salmon, however, breeds only once in waters suited to the young, but the young migrate to the sea and back again to the breeding places. In a lesser way, this is true of many animals, notably insects, fishes, amphibians, and reptiles. In the egg-laying organisms with a metamorphosis, each species presents several seasonal forms in its life history. In Amhystoma, the adults, the eggs, the tadpoles, the gilled larvae, and finally the adult form api^ear in turn between February and July. Since many ani- mals without metamorphosis show similar phenomena, there is a gen- eral sequence throughout the year, often made striking by migration ANIMALS 47 to different situations for dormant or unfavorable periods. ]\Iany of the smaller forms, notably insects, produce a number of generations in one season (Glenn, 1915). The different generations are often divergent as to response system and other physiological characters. Other animals, though present as adults each year, require several years to reach maturity, and at a given time the various stages are telescoped together in a somewhat confusing fashion. In fishes, mea- surements of length, scales, and scale rings have served to separate the age classes and illuminate the life history (Walford, 1932). In a few species, such as some cicadas and a few wood beetles, unusu- ally long life histories occur, extending over as much as seven, thir- teen, or seventeen years. Again, the production of eggs is occasion- ally associated with definite astronomical cycles, the palolo worms laying eggs at a definite period of the moon. A correlation with con- ditions is shown by various other marine worms (Mayer, 1908). In any community, a considerable series of important stages in the life histories of different species occur together. This is due to a certain similarity of response or of life histories. Some insects, not conspicuous at other periods, occur in middle latitudes at the time migratory birds are pausing on their w^ay to their northern breeding grounds. At the same time, certain plants are in bloom, giving a sea- sonal aspect to the biotic community, as the result of life history demands. A few motile aquatic animals deposit eggs that float at the sur- face and act essentially like disseminules of the sessile animals. The fishes that produce this type of egg belong to diversified taxonomic groups. For example, the cod moves into shallow water near shore to breed, just as do many other fishes. After the pelagic eggs are hatched, the fishes migrate into the protecting tangles of Zostera, where they live during infancy (Blegvad, 1916). Viviparous species are distributed throughout the more highly organized animal groups. In some cases viviparity does not differ materially from egg laying; e.g., the blowflies and tsetse flies deposit very young larvae instead of eggs. All degrees of adaptation may occur, the condition in the marsupials and placental mammals being more specialized than in the other forms. In these, there is a rutting period often of much importance in that the strongest males fre- quently become the fathers of the next generation, owing to an intense competition among them for mates, as among the seals and certain ungulates. Again the female sheep does not enter into estrus with any certainty, except when stimulated by sharp changes of tempera- ture from day to night (Johnson, 1924). Rutting time bears definite 48 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION relations to the weather ordinate; the period before lambing is im- portant to the females, and that of birth and the few days or weeks following are critical for the lambs. One feature of life histories in general is the occm'rence of dor- mant or quiescent states remarkably well represented in the several groups found in fresh water and on land. The spores and cysts of protozoa, the gcmmules of sponges, the eggs of arthropods, the pupae of insects, and the hibernating ground squirrel afford well-known examples, and suspended development in the embryos of a few mam- mals may be analogous. Such quiescent states have much seasonal significance, and their relations need to be ascertained especially in connection with community aspects. LIFE FORMS Concept and Significance. The concept of the life form came into existence originally as a consequence of the interest of plant geog- raphers in the physiognomy of vegetation. It led logically enough to various systems of classification, usually with much in common, but with the emphasis on different criteria. Some of these were con- structed in great detail, others were more inclusive; in one case, vege- tation was the major objective, in another, floristics. Practically all were static rather than dynamic, and the inductive approach through experiment was entirely neglected, in spite of the fact that life forms afford striking opportunities for the study of adaptation. As a con- sequence, classification became stereotyped with little direct applica- tion to dynamic ecology, though the system of Raunkiaer, with the related biologic spectrum, has been much employed in floristic ac- counts. Nevertheless, life forms do epitomize the adaptation of the plant body under the compulsion of the environment, and hence are of primary importance in connection with climax and succession. For this purpose, however, it is essential to distinguish various categories, based chiefly on the degree of modification and fixity (Clements, 1920:57; 1928:263). Kinds of Life Forms. Probably the most logical and serviceable definition of the life form is that which includes under it all the forms exhibited by plants and animals, such as taxonomic, vegetation or biome, habitat, ecad, growth and competition forms (Clements, loc cit.) . Among plants, the taxonomic and vegetation form are, for the most part, identical in cryptogams; with flowering plants, this is only exceptionally true. For the vast majority of animals, the LIFE FORMS 49 taxonomic and biomc forms are the same; this is especially apparent in invertebrates but holds throughout with few exceptions. Life forms that bear the distinct impress of a particular habitat or some division of it are known as habitat forms, and those of plants have been termed ecads if they can be produced experimentally. Among animals, a group with a characteristic behavior response has been called a inores (Shelford, 1913, a) ; to avoid certain difficulties, especially as to the plural, it is now proposed to employ the word "mune" {munus, function, role). Of more recent impress and hence of less import are the growth forms and competition forms. However, plants often exhibit striking forms of the latter type, both in nature and in culture, and this is true only to a less extent for animals. Bases. The major principles underlying life forms were enunciated by Drude as: (1) the role played by the species in vegetation, and (2) its life history in relation to the habitat, in terms of duration, pro- tection, propagation, and overwintering (1890, 1896). These were later increased to the following five: (1) the basic form, tree, shrub, etc.; (2) form and duration of leaf; (3) protective devices during the resting period; (4) position and structure of the organs of absorption; and (5) reproduction as a single or recurrent process (1913). The system of Warming (1909) took into account three major features, viz.: (1) duration, (2) length and direction of internodes, and (3) position and relations of buds to overwintering; it also took into account five minor ones, namely: (1) structure of buds, (2) size of plant, (3) duration of leaves, (4) adaptation of the green shoot, and (5) capacity for social life (1909). Clements gave more or less equal value to the life period, method of overwintering, conservation of shoots, and success in competition (1920, 1928). Systems of Life Forms. The essential similarity of the systems more or less current is readily perceived from the fact that Drude makes trees, shrubs, perennial, and annual herbs the basic life forms; Warming's major division of land plants is into monocarpic and poly- carpic, essentially annual and perennial, while Raunkiaer's largest groups correspond practically to woody plants and perennial and annual herbs. In accordance with this general agreement, Clements has proposed the following as a simple practicable system, embodying the major features of the others: 1. Annvials 6. Cushion herbs Woody perennials 2. Biennials 7. Mat herbs 11. Halfshriibs Herbaceous perennials 8. Rosette herbs 12. Bushes 3. Sod grasses 9. Carpet herbs 13. Succulents 4. Bunch grasses 10. Succulents 14. Shmbs 5. Bush herbs 15. Trees 50 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION Each of these types is subdivided as is item 3, as illustrated in Figs. 4 and 5. The biologist who wishes to pursue this subject further is referred to Tansley and Chipp (1926) and to the comprehensive monograph on life forms of flowering plants by Du Rietz (1931). Biotic System of Life Forms. Gams has proposed a classification that includes both plants and animals, as an outcome of recognizing the importance of the biotic community (1918). The major bases employed are substratum, motility, nutrition, and duration, and the primary divisions are: (1) the adnate form, Ephaptomenon; (2) the radicant form, Rhizumenon; and (3) the errant form, Planomenon. The difficulties of a combined system are seen in the fact that the radicant form consists exclusively of plants, whereas the other two groups are composed chiefly of animals. Nevertheless, this first essay contains much that is suggestive and may w^ell serve as a basis for future development. Marine Life Forms. In his study of the communities of Gullmar Fjord, Gislen (1930, a, h) , has proposed a system of marine bcnthonic plants and animals, the main features of which are as follows: 1. Crustida: (1) eucrustida, incrusting forms; (2) torida, cushion form; (3) mammida, wart form; (4) digitida, finger form. 2. Corallida: (1) dendrida, slirub form; (2) phyllida, leaf form; (3) umbracu- lida, umbrella form; (4) umbellula form; (5) plume form; (6) rod form; (7) fan form. 3. Silvida: (1) graminida, grass form; (2) foliida, leaf form; (3) sac form; (4) palm form; (5) buoy form; (6) whip form; (7) shrub form; (8) sar- gassus form; (9) radial form. 4. Radiida, radiate form. 5. Valvida, bivalve form. 6. Conchida, snail form. 7. Limacida, slug form. 8. Vermida, worm form. 9. Crustaceida, crustacean form, 10. Piscida, fish form. The advantages in the use of such terms are not very evident. Sessile Multiple-individual Animals. Among plants, life forms have proved very useful in designating and characterizing communi- ties. This is due to the fact that they have segregated themselves into climatic groups that give the essential character to grassland, tundra, desert, deciduous forest, coniferous forest, etc. It is impor- tant to emphasize the fact that plant ecologists are led to expect similar conditions in animal communities in general, and usually LIFE FORMS 51 Fig. 4. — Tall-grass relict (Tnpsacum dactyloides) in mid grasses of the true prairie; eastern Kansas. (Photo by Edith Clements.) Fig. 5. — Buffalo grass (Buchlue ductyluida;), a feud-formniy, .-hon grass, migrat- ing by means of stolons; western South Dakota. (Photo by Edith Clements.) 52 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION where they are not to be found. The limited character of the simi- larity has already been pointed out (p. 34) in connection with a comparison of "zoophytes" and land plants. In a bio-ecological treat- ment, it becomes important to know that the animals of these climatic communities display comparable behavior and physiological charac- ters but lack unity of life-form characters. On the other hand, marine animals may show segregation of characteristic life forms in some communities. Zoophytes have included chiefly the larger upright, treelike delicate corals, but they may well comprise also the more massive corals with similar branching. The life forms of the notably large species include tree forms with radial symmetry, or more rarely fan forms, produced by branching in one plane, like plants of the genus Arcca. On these the zooids are arranged much like leaves, but have a greater tendency to cover the trunk and main branches. A few whip forms have the zooids radially arranged about the trunk like the flowers of the mullein {Verbascum thapsus) . These rigid plantlike animals are typical in warm seas where corals play an important role in the biotic commu- nities. Their life forms probably have value in characterizing these communities, but no studies from this viewpoint are at present known. In addition to the large rigid forms, there are many small delicate hydroids and bryozoans that exhibit the same types of branching and zooid arrangement. The life-form peculiarities of these are usually the taxonomic characters of orders, families, genera, or species. They are apparently of little significance in marine communities, playing a role somewhat similar to that of cup fungi and lichens in a forest. There are also sessile multiple-individual animals that assume an essentially spherical form about a foreign body as an axis (Pectina- tella). Some others approach spherical form, though the body rests upon a substratum; of these the sponges, especially the commercial types (Moore, 1908), are examples. A few compound tunicates as- sume a nearly spherical form, Macroclinum pomum of the North At- lantic being an example. Some of the massive corals are essentially similar, and on the whole a number of community dominants are included in this type. Some of the decumbent animals form fans on the substratum; others make simple plates. Still others are amorphous lumps and irregular aggregations owing in some cases to natural and presumably hereditary tendencies, which would classify them as life forms (Shel- ford, 1914, d). This brief statement concerning the life forms and growth forms of aquatic sessile and sedentary animals by no means exhausts the field either as to detail or types, but it does show that LIFE FORMS 53 the range of life forms in plantlike animals has some resemblance in such land plants as fungi, lichens, liverworts, and even higher plants. However, their segregation into communities so as to give a physiog- nomic aspect, comparable to those of major plant communities, is doubtful except in the case of coral banks. The phenomenon is also essentially limited to warm seas. The significance and usability of these forms in community study are, in any event, much less than among land plants. Several genera of corals (Wood-Jones, 1910) develop a tall straight form in deep still water, a much-branched one in moving water, and Figs. 6-11. — Showing the parallelism in growth form of a sessile plant and a sessile animal. 6-8, Forms of Pinus montana (after Schroter, 1908): 6, from protected vallej-s; 7, from mountain sides; 8, from mountain moors. 9-11, Forms of Madrepora: 9, from deep water; 10, from barrier pools; 11, from rough water. The differences are due to injury to the leader or dominant growing point. (After Wood-Jones, 1910.) amorphous lumps in rough water (Figs. 9-11). These are somewhat parallel to the forms of certain conifers in still valleys, windy moun- tainsides, and timber line (Schroter, 1908). The former is a response to waves and currents, the latter to wind and snow, but both are the result of the injury to a single dominant bud or zooid. The rather striking parallel is shown in Figs. 6-11. The commercial bath sponge shows several forms: a sphere when suspended on a wire, a spheroid when growing on an elevation above the bottom, and a palmate irregular form when surrounded by plants 54 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION or other objects (Moore, 1908). Among the small organisms such as hydroids, some species grow toward the source of light just as plants do. With the small fresh-water types, like Spongilla and Plumatella, one finds frequent reference to growth forms, but rarely any details as to their cause and character. Many of the growth forms noted may be ranked as habitat forms, since they are pro- duced by variation in habitat conditions. Sessile Single-individual Animals. The forms of these are largely taxonomic, as in the sessile barnacle, gooseneck barnacle, serpulid, oyster, sea mussel, and simple tunicate. The growth forms have been little considered. Pilsbry (1916) has noted long pencil types of sev- eral species of barnacles w'hen crowded (cf. Shelford and Towler, 1925). Loeb (1906) has shown that serpulid worms turn toward the light much as do plants, while brachiopods show differences with depth and injury (DuBois, 1916). Sedentary Forms. Sedentary animals are those which rarely move, or which give the impression of being stationary because of very slow or only occasional movements. These are usually the passive mem- bers of active groups, and hence the form is essentially taxonomic, with the exception of the coelenterates. The forms are grouped into types with difficulty, but each of the following represents some degree of geometric likeness: (a) hydra, solitary corals, sea anemones; (6) some chitons and limpets; (c) many worms and a few echinoderms, such as Leptosynapta. Behavior Forms and Taxonomic Forms. In contrast to the zoo- phytes and common plants, the vast majority of animals are in no sense multiple-individual, sessile or sedentary. Their outstanding feature is activity and the forms concerned bear a corresponding impress. In terrestrial communities motile animals ai^e well-nigh universal; by contrast to sessile organisms, in which response is through growth, their primary adjustment to physical factors is by means of movement. The forms of motile animals are usually of direct taxonomic value and at the same time may constitute adaptations determining details of activity. Again, certainly not all the specificities of behavior directly related to structure are of ecological significance. A leaping kangaroo rat may have the same coactions, reactions, and responses to environmental conditions in a grassland community as a ground squirrel which progresses in the more usual way. Accordingly, form in animals is naturally forced into the background. It will therefore not be profitable to go into detail as to form in motile animals. The well-known echinoid, asteroid, snail, bivalve, and vermiform life forms COMMUNITY FUNCTIONS 55 in water often give aspect to marine communities because of a pre- ponderance of one type over another (cf. page 323). Sucii less active groups also show greater growth-form differences than the more active ones. For example, Baker (1928) finds a river form and a lake form of fresh-water mussels, and Humphrey and Macy (1930) report dif- ferences of form and size in tide-pool snails. The more active animals present walking and running, flying and gliding, hopping and looping, burrowing and swimming, and creeping and crawling life forms. These are rather uniformly distributed throughout the phyla, as well as in water and on land. The presence of segregated groups of these types often gives some character to certain communities, though the use of life habits appears more use- ful, owing chiefly to the heterogeneity of adaptation characters. This difficulty is well brought out in a series of papers devoted to the adaptations of mammals to arboreal, cursorial, fossorial, and aquatic life (Osburn, Dublin, Shimer, and Lull, 1903). These discussions indicate that the layer adaptation may be effected in a variety of ways, thus placing the emphasis upon activity rather than structure. Again, since the primary adaptation is to layer or level, this also tends to assign a subordinate role to form. Furthermore, some species lack definite adaptations altogether, while more telling is the fact that certain striking modifications have little ecological meaning, and the activities rather than the structural adaptations are of signifi- cance. In the study of coactions, it is evident that activity must be taken into account with structure, and may often outweigh it. Forbes (1914) indicated another relation of structure to activity in the food-getting apparatus and digestive tract of fishes. He found that the fresh-water fishes of Illinois begin life by feeding upon Entomostraca ; during development from a very early stage to the adult form some become mud-eaters and others insectivorous or pisciv- orous, while only a few continue to feed upon plankton. In each type, the digestive tract and gill rakes become adapted to the special food habits, the mud-eaters developing very long intestines, COMMUNITY FUNCTIONS Nature and Significance. The development and structure of the biome are due to activities that may be properly regarded as func- tions of the community. This is likewise true of its subdivisions, both climax and serai, in which the nature of the processes is even more clearly discernible. The group of organisms which constitute the community is acted upon by the habitat, producing social response 56 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION that leads on the one hand to further reactions upon the habitat and on the other to new coactions between the associated organisms. In succession these processes proceed in a chain or series which finds its summation in the climax. The chain of serai communities has been likened to the series of stages in the life history of an animal undergoing metamorphoses with its final and most perfect stage repre- sented by the adult which is comparable to the climax. The process of succession has also been likened to the growth of plants, but lack of detailed knowledge of both processes renders the comparison ciuite ineffective. The functions of the biome may be viewed from the standpoint of the dynamic processes, such as succession, annuation, aspection, etc., or from that of the causal sequence of processes, beginning with aggregation and terminating in stabilization. Both approaches are desirable for a proper understanding of development and its relation to the consequent structures, but the scrutiny of the single functions and their correlations is much the more essential. In spite of the fact that they are more or less simultaneous in operation, it is pos- sible to separate them experimentally and to a certain extent by observation also. Up to the present, the functions of the community have been stud- ied chiefly with respect to the plant matrix, but it is evident that they also carry over into the biome. Special studies of coactions and com- petitions made from the standpoint of particular species of animals confirm this conclusion. Their significance with respect to animal groups is most clearly exhibited where animals are the dominants, as in the marine climaxes. However, it is also well exemplified in the various minor communities, such as families, colonies, and so- cieties, both plant and animal, which are essential features of the biotic community. The smaller and simpler the community, the more readily can its functions be followed, and, in consequence, initial stages in succession furnish the best opportunity for this in nature, just as similar artificial groups constitute the best cultures for such purposes. The following seven functions are considered to be the basic processes in the plant matrix, and hence in the biome, even when this consists primarily or wholly of animal dominants. These are aggregation, ecesis (establishment), migration, reaction, coaction, com- petition, and cooperation. Out of these arise certain complex proc- esses, such as invasion and succession, while such phenomena as diurnation, aspection, and annuation are more or less closely con- nected with them. For the present purpose, at least, the most signifi- AGGREGATION 57 cant of these are reaction, competition, coaction, and aggregation and ecesis (succession) , and they are in consequence discussed in considerable detail in the following chapters. For the others the general account given here is supplemented by discussion or specific mention of their role in the biome later in the text. AGGREGATION As a technical terra, aggregation was first employed in ecology in the dynamic sense, for the coming together of individuals as a result of multiplication (Clements, 1905, 1928). With respect to ani- mals, it has occasionally been given a similar meaning, but more recently Allee (1931, a) has used it as the inclusive term for the groups that result from the process. In this sense, it is largely synonymous with community, though more exactly with the family or colony of plant ecologists. However, no serious ambiguity is in- volved in the double use of the word, which will probably continue until the study of minor communities becomes much more general on a developmental basis. Aggregation among Plants. In its simplest form, aggregation is the direct consequence of multiplication, though as a rule it is also dependent upon migration in some degree. The first type is exem- plified by such algae as Gloeocapsa and Nostoc, in w^iich the dividing cells are held together by a matrix of mucilage. Such a group of individuals is a family, the relation being essentially that of parent and offspring, even though the parent disappears as a result of fission. Practically the same type of grouping occurs in terrestrial forms, especially flowering plants, when the germules mature and fall to the ground about the parent. A family is also produced when propagation by offshoots leads to a similar disposition. All these are instances of simple or primary aggregation, in which migration is absent or slight. This is often the case in annuals wdth high seed production, and, in consequence, these supply by far the largest number of pure families. Moreover, the conditions for simple aggregation are especially favor- able in bare areas and secondary ones in particular, so that the initial stages of subseres are regularly characterized by annuals (Fig. 12). ]\Iixed or secondary aggregation ensues w^hen seedlings (germules) of two or more species become intermingled to form a colony, in the case of a bare area, or when migration carries propagule or seed into an established family. Every community is an example of this type of grouping to some degree, in view of the fact that association is merely the outcome of the interplay of aggregation and migration. 58 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION With aggregation paramount, families are tlie rule; when the proc- esses are more or less balanced, colonies prevail; with migration emphasized, the mosaic of vegetation results. In closed communities, it is practically impossible for annuals to persist or to enter, and the pattern often reflects the tendency of perennials with offshoots to form families, as illustrated by Antennaria or Erythronium. Aggregation among Animals. In attempting to bring together the knowledge of two fields which have developed as independently as botany and zoology, or more specifically, plant ecology and animal Fig. 12. — Aggregation of a native goosefoot {Chenopodimn IcptophyUum) in a short-grass pasture covered with wind-borne silt; eastern Colorado. (Photo bj- Edith Clements.) ecology, difficulties as to the different uses of the same term arise fre- quently, aside from the fact that aggregation long has been used by plant ecologists to apply solely to the process of assembling in a group. Alice's use of the word introduces an additional general term for the communities of small size. Aggregation is accordingly used here only in the sense of the process. As compared with plants, aggregation through reproduction is comparatively rare or temporary. Temporary aggregation occurs in the case of vertebrates which care for their young. Nest-building MIGRATION 59 fishes, aquatic and gallinaceous birds, and some mammals afford readily observable examples. Permanent aggregation by reproduction occurs in ants and a few other social insects. Doubtless, sessile ani- mals afford examples of aggregation by asexual reproduction, but aside from the corals, noteworthy i)ermanent examples are not outstanding, either in their conspicuousness or ecological significance. As Alice and others have pointed out, the process of aggregation in motile animals is dependent upon sexual forces, upon social forces, and upon common environmental responses. Aggregation by reproduction as cited above is essentially social. In animals with minimal social tendencies the offspring disperse early or may be loosely held together by common environmental responses (cf. Chapter 5). MIGRATION In spite of general agreement in the sense of movement, this term has come to have somewhat different applications in botany and in zoology. This has probably come about as a consequence of the basic contrast in motility, so that it became desirable to distinguish the distant or recurrent movement of animals in mass from local activities. In sessile plants, any movement was of some significance, but the most noticeable ones were those of the individual for a short distance. Moreover, in terrestrial animals the adults are much more motile than the young, while with plants the embryo or seed is often very mobile and the adult immobile, except for the slow and re- stricted spread of offshoots. The general dependence of the flowering plant upon the seed is indicated by the word dissemination, which might well replace migra- tion were it not for two facts. The first is that plants bring about effective change of position by means of propagules (Fig. 13), and the second that vegetation often exhibits great mass movements, in which the associated animals are also involved. In consequence, it seems most logical and convenient to employ migration to denote any and all changes of position, whether of individual or community, single or recurrent, over a restricted or local area, or for great distances. The term would still retain its special application to seasonal, annual, or cyclic movements in mass, characteristic of certain insects, most birds, and some mammals and fishes. Dissemination would continue to apply to the local transport of seeds and fruits in particular, whereas migration would be especially applicable to mass movement in response to climatic change, in which seeds, propagules, and motile animals would all be involved (Clements, 1922:351). 60 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION Migration in Plants. Although migration devices have long been a subject of interest to botanists, the actual process itself has received little attention, especially in terms of experimental study. Such study is peculiarly difficult in nature, and this fact explains in large part the persistence of the idea that the movement of migrules is as effec- tive as it is universal. This view has received much support from the general abundance of weeds and the readiness with which they take possession of disturbed places. However, it finds little warrant in natural communities, in which not only is movement itself much Fig. 13. — Migration of a dune pioneer {Ahronia maritima) by means of creeping stems; seashore, Santa Barbara, California. (Photo by Edith Clements.) more restricted than commonly supposed, but also the establishment of invaders is rendered almost wholly impossible by the competition of the dominants. Transport to a great distance has long possessed dramatic interest, but is rare in fact and even much rarer in effect. When the embryo is not destroyed by the agent of distribution, as regularly happens with water and birds, its establishment becomes possible only in disturbed or bare areas. In consequence, dissemina- tion in nature is of little import to the community, unless a change of climate intervenes. Its chief significance is in the colonization of primary bare areas or secondary disturbed ones and in supplying the newcomers for the stages in the ensuing succession. The mainte- MIGRATION 61 nance of the climax itself is almost exclusively a matter of propaga- tion, supplemented, in a small degree, by regeneration. Leaving aside the consideration of movement in water, which is chiefly due to current and wave, mass migration, as contrasted with the transport of individual migrules, regularly takes place in two fashions. Locally, it operates upon minor communities, utilizing prop- agules in the case of the climax and disseminules in the colonization of bare areas. Regionally, it becomes significant only under the impulse of climatic changes, but the actual advance is due to the slow and repeated movement of dominants and subdominants through both these methods. The migration of ruderals and cultivated species has likewise a mass effect in a large degree, in spite of the fact that trans- port of weeds by man is unintentional. In all these cases, however, the final value of migration as a process is determined by the success attained by ecesis. The Migration of Animals. Migration proper in animals does not differ from that of plants. Sessile and sedentary species, as well as animals of limited activity in water, commonly possess a life-history form that may be carried some distance by currents. On land, small animals, especially insects, spiders, and some mollusks, may be moved into new territory almost as readily as the seeds of plants. The num- ber of these carried out of their homes by wind is evidenced by the line of living drift found about Lake INIichigan after a storm of short duration. However, the habits of the species are regularly so little suited to life on the beach as to bespeak the rarity of establishment. Nevertheless, the effect of such events in populating denuded areas where animals precede plants cannot be neglected (Smith, 1928), nor can the process be overlooked where climatic changes have favored invaders into established communities. For example, species charac- teristic of dry oak-hickory woods appeared in moist oak-maple forests following the dry season of 1930, only to disappear soon after. The random wanderings of the larger motile animals out of their usual range is of no more significance than the movement of the wind- blown insects, since they regularly return and no actual shift of home occurs. Other local or recurrent wanderings occur, but even the more important and definite ones are subordinate to the mass movements involved in biotic migration. Types of Migration. These may be grouped as: (1) recurrent migrations, divisible into (a) annual, (b) seasonal, (c) metamorphic, (d) diurnal; or (2) non-recurrent migrations, divisible into (a) exten- sion of range, (6) local movements within the home area. The annual and seasonal migrations are characteristic of many 62 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION birds, mammals, and fishes, and of a few reptiles, amphibians, and insects and other invertebrates. Practically always, the movement is into a new habitat for reproduction and out again. Some degree of change of place frequently accompanies reproductive activities. In some instances the distance concerned is small, but if it is into a dif- ferent habitat or set of conditions, it is significant and quite com- pletely homologous to that of the salmon or of birds which travel long distances to breeding places. Birds are the most noteworthy migrants, and the distances traveled by many well-known species are remarkable. With the approach of spring in the northern hemisphere, they leave their winter homes in the grassland of Patagonia, the tropical forest of Venezuela, the swamps of Louisiana, or elsewhere, as the case may be, and pass northward. The Kaibab deer journeys from the pinyon and sage- brush to the montane forest for the birth of the young. The salmon, shad, and other fish go many miles to places suitable for spawning. Moreover, the behavior of the black bass which moves from its feed- ing grounds in aquatic vegetation, to a sandy beach is essentially similar. The rose beetle (Microdactylus) leaves its food plant to deposit eggs among grasses. The force that initiates and directs such movements is probably similar in all cases, and the local migrations are sufficiently simple to permit experimental study. There are many local recurrent annual migrations of insects from hibernation quarters to breeding and feeding grounds, and the re- verse, especially between forest edge and grassland, or water and adjacent land. In proportion to size, these flights of small insects are considerable, a few hundred yards for a chinch bug being comparable to miles for a deer. Metamorphic migration, such as the return of the adult to air from water, is typically annual and recurrent, but may be seasonal when two generations occur in one season. Further- more, recurrently migratory species shift their breeding grounds and their winter rookeries with the mass of associated species, but this does not introduce new features into biotic migration. Diurnal recur- rent migration characterizes many insects that move from forest edge to open country, and vice versa, with day and night (Carpenter, 1935) . It is also typical of plankton, which moves down and up in both sea and fresh water in accordance with the alternation of day and night. Non-recurrent migrations are perhaps best illustrated by range extension. The Virginia deer has advanced northward several hun- dred miles since the settlement of eastern North America. It has taken the place of the woodland caribou in the forests about the Great Lakes and for some distance northward. The opossum has ESTABLISHMENT OR ECESIS 63 also moved northward two hundred miles or more from Indiana into Michigan. Both of these extensions are due probably to the release of territory, change of vegetation, reduction of enemies, or other activ- ities of man. Extension of range in insects is likewise frequent. The boxelder bug moves northeastward from Oklahoma to southern Michi- gan every decade or so, and frequently becomes domiciled, until a winter with prolonged low minima destroys the invaders. ESTABLISHMENT OR ECESIS By this term is understood the process of making a new home, involving the adjustment and often the adaptation of organism or community to a new place or habitat. It is both more comprehen- sive and more concrete than acclimatization or naturalization, but differs little in essence. It embraces the widest range of adjustment, from the slight movement of a rhizome in practically uniform condi- tions to the establishment of invaders in a bare area or the advance of forest or prairie along an ecotone. It is a much simpler and surer process when a single medium is concerned, as water or soil, in which migration and ecesis are nearly synonymous. Ecesis in land habitats, with the necessity of adjustment to two media of great variety, be- comes correspondingly complex and difficult. However, this statement applies much more fully to plants than to animals, owing chiefly to their direct dependence upon the ece but also in some part to their sessile nature. It is applicable in varying degree to animals, being fairly simple and direct in wide-ranging species, and more complex in sedentary ones or those with narrow limits as to physical factors or choice of food. By contrast with plants, ecesis in animals involves adjustment not only to the new place or habitat but also to a new group of coactions. Ecesis in Plants. Differences in the manner and success of ecesis are determined by several elements, namely, the plant or part con- cerned, the medium, and the habitat. In free aciuatic forms the in- dividual itself often migrates and ecesis consists merely in its continu- ing to grow and reproduce, a result more or less assured by the greater uniformity of aquatic habitats. For the offshoots of land plants, espe- cially underground ones, conditions are rather similar, and continued growth and multiplication are certain within the limits set by exces- sive competition. However, in the vast migration of seeds and fruits, ecesis requires successful germination, growth, and reproduction, dur- ing which seedling and plant must often withstand unfavorable ecial factors, intense competition, or injurious coactions. As a consequence, a migrule may meet one of four fates: (1) it may never germinate; 64 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION (2) the seedling, or later the adult itself, may die or be destroyed; (3) the individual may persist without reproducing, a frequent event under keen competition; or (4) normal reproduction may occur, asso- ciated in most perennial herbs with propagation. Ecesis, properly speaking, occurs only in the last instance. It regularly involves an expression of the complete life history, though under the influence of marked adjustment this may be modified in details (Fig. 14). ■*m .**J«,*;V. rX' ^n pj- i.'J^\ Fig. \^..— Oenothera caespitosa establishing itself in the sun-baked clay of the Bad Lands; The Great Wall, South Dakota. (Photo by Edith Clements.) As already emphasized, migration becomes effective only when fol- lowed by ecesis. The latter has usually been regarded as a natural if not regular sequel to movement, but experimental studies have shown it to be altogether exceptional (Clements and Weaver, 1924) . This conclusion is reinforced by the slow changes in composition shown by the plant matrix, in spite of the enormous seed production of many species. Not only must the seeds meet the vicissitudes of transport and of germination, but the highly susceptible seedlings must run the gauntlet of untoward conditions, of destructive coactions, and of un- favorable competition. The final survival represents but the merest ESTABLISHMENT OR ECESIS 65 fraction of the initial seed production and would be practically negli- gible were it not for the recurrence of bare or denuded areas in which the barrier of competition is absent. So complete is the control of dominants, in climax communities especially, that the ecesis of in- vaders is all but completely inhibited, becoming possible only in con- sequence of some marked disturbance or climatic change. From this standpoint, the earlier views of more or less constant and widespread migration or of gradual advance, such as that of woodland along val- leys, become entirely untenable, and the great movements of climaxes and subclimaxes are to be explained only on the basis of climatic compulsion, with ecesis as the decisive function of the community (Clements, 1922). Ecesis in Animals. The motility of essentially all land and many aquatic animals leads to an invasion of new territory in their daily rounds for food, in consequence of fright due to enemies or other inci- dents. In addition, many of the smaller forms are borne out of their natural area by currents of wind or water. Thus, there are thousands of temporary invasions of new territory by many species to one inva- sion of significance as biotic migration. The sessile and sedentary animals show a series of phenomena so nearly parallel to those of plants that the essential principles may be found in the preceding section. Motile animals with power of flight, and one or more generations per year, may invade new territory under agricultural conditions and establish themselves until a cold winter or a dry season kills them off. The boxelder bug (see p. 63), harlequin, and cabbage bug are examples. The birds of forest edge and meadow have doubtless in- creased greatly over eastern North America with the increase of such habitats about farms and villages. The introduction of the English sparrow and starling is largely a transfer of a European species of the deciduous forest to similar conditions in America. However, Wetmore (1926:211) states that it took ten years for the starling to establish itself firmly in Central Park, though the responses and coactions in- volved are not known. His account indicates that the starling ranges considerably beyond its breeding area, which is a frequent phenome- non. The instances of the ecesis of animals outside their original ranges in North America have been very numerous under the influence of the rapid modification of the original biomes, but there is scarcely a case in which the detailed causes or processes have been studied. In fact, at present little more can be said of ecesis among animals than that it involves maintaining a population over an adverse year or series of years. 66 COMMUNITY FUNCTIONS— DYNAMICS OF BIOTIC FORMATION Related Processes. A number of functions consist of two or more processes of which ecesis is ruling or decisive. This is particularly true of invasion, which consists of migration and ecesis, but with its final success and effect depending primarily on ecesis. This is the process characteristic of succession, for which it supplies the materials to be organized into the various stages as a result of reaction and competition. The other complex functions are concerned largely with the climax community, though not unknown in the later serai stages especially. The most striking of these is aspection, which is characterized by seasonal maxima of number or developmental behavior, in water as well as on land, and with both plants and animals. Related to this in terms of behavior are hibernation and estivation, ordinarily re- garded as confined to animals but found in plants also, though under other names. When the behavior response operates upon a daily rather than a seasonal cycle, the process may be termed diurnation, illustrated by the vertical movement of plankton and by the "sleep" movements of flowers and leaves. Finally, the change in abundance or prominence may be annual, as an expression of a larger cycle, such as the eleven-year sunspot period. This is known as annuation, in which the response to climatic variation may produce striking changes in abundance, resulting in widespread migration or in marked differ- ences in composition. Because of the importance of their roles in the climax, the discussion of these functions is reserved also for Chapter 6. Interrelations of Community Functions. Like those of the indi- vidual, the functions of the community are not only most intimately connected with one another, but they are also involved in a complex of activities in which their simple causal relation is obscured or com- pletely lost to sight. The normal sequence exists only in the simplest minor communities; in others the interplay of functions is so kaleido- scopic that the operation of each is difficult to discern. This is pecu- liarly true of succession, which exhibits the dynamics of function at a maximum. In the climax, aggregation and migration are at a low ebb, and the directive processes of reaction and competition are diminished and are concerned chiefly w'ith fluctuations in abundance in season and year. The normal sequence comprises aggregation, migration, ecesis in terms of reaction, competition and coaction, succession, diur- nation, aspection, and annuation. It is obvious that the relation of almost any two of these is more or less cyclic, inasmuch as migra- tion makes aggregation again effective, from which further migration proceeds. In the case of reaction, the ensuing competition in turn INTERRELATIONS 67 influences this, and is itself again modified to correspond. In succes- sion, functional activity rises to an optimum until temporary stabiliza- tion is attained in each stage, when it falls off until a new wave of invasion culminates in the succeeding stage. A detailed and compre- hensive account of the various community functions is impossible within the scope of the present book, but the salient features of the major processes, their interrelations, and the significance of each for climax and sere are discussed in Chapters 3 to 6, inclusive. CHAPTER 3 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT Definition and Nature. As has been earlier emphasized, the cause- and-effect cycle in the biotic community comprises the action of the habitat upon the associated organisms, their response to this, and the consequent effect upon the physical factors of the habitat. The last process was termed reaction by Clements (1904:124, 1916:79, 1928; Weaver and Clements, 1929:145), and was defined as the in- fluence exerted by an organism or a community upon its habitat. It is entirely distinct from the response of species or group in the course of adjustment or adaptation. For examjile, the physical factors cause a plant to function and grow, and it then reacts upon the habitat or ece, changing one or more of its factors in an appreciable or decisive manner. The two processes are mutually complementary and often interact in the most complex fashion. Generally, there is a primary reaction with one or more secondary ones, direct or indirect, but not infrequently two or more factors are affected directly and critically. The word interaction has long been used by zoologists to cover all kinds of interrelations between organisms and habitat, but it is obvi- ously too inclusive for adequate analysis, especially in the broader field of bio-ecology. Although it is desirable to retain it in a compre- hensive sense, the need for exactness of reference is best met by recog- nizing two distinct types of interaction. The first of these is reaction, the effect of organisms upon the habitat; the second, coaction, or the influence of organisms upon each other. Such a distinction becomes of paramount importance when the biotic community is made the basis of treatment. The reaction of a community is always more than the sum of the reactions of the component individuals and species. In the case of the plant matrix, though it is the individual that produces the reac- tion in the final analysis, the effect regularly becomes recognizable only through the combined action of the group. In practically all cases, the community accumulates or emphasizes influences that would otherwise be insignificant or transient. This is strikingly illustrated 68 RELATION TO LIFE FORMS 69 by the reaction of trees upon light. The shadow of a single tree shifts with the sun, and, in consequence, the reduced light intensity is permanent only over a small area about the base. Thus, while a com- munity of trees casts less shade than the same number of isolated individuals, the effect is constant and continuous, and hence becomes controlling. The significance of the community is likewise clearly demonstrated in the production of duff and leaf mold. The litter is again only the sum of all the fallen leaves and twigs of the individuals, but its accumulation is dependent upon the practical cessation of wind action. The reaction of plants upon wind-borne sand and silt-laden waters further exemplifies the unique importance of the community. The animal members of the terrestrial community are less effective than plants in producing reactions, as a general rule. In spite of this, waste products and hard parts often accumulate in great amounts, while burrowing animals in particular frequently exert a pronounced effect in disturbing soil or bottom, and sessile and sedentary ones in protecting or perforating the substratum. Moreover, animal reactions may be more or less direct consequences of food coactions, as in the tunnels and mounds of pocket gophers, moles, etc. Relation to Life Forms. Some reactions are the direct consequence of a normal functioning of the organism. AVith respect to plants this is illustrated by the decrease of water content through absorption, the increase of humidity as a result of transpiration, and the weathering of rock by the excretion of carbon dioxide. The amount of oxygen, carbon dioxide, or solutes in the medium is directly affected by both plants and animals, and animals produce many deleterious excreta. Furthermore, such a functional complex as growth may lead to the direct modification of physical factors, but as a rule this is much more strikingly related to life form. Reactions in both plants and animals may be directly connected with form. Growth form in plants, however, is primarily an outcome of reaction as brought about by competition. The plant matrix of the community owes its predominant ability to modify land habitats to the vegetation forms represented by the dominants especially. This is best revealed by the contrast between forest and prairie ; the former exerts a controlling action upon aerial factors, the latter a much slighter effect. On the other hand, the reaction of forest on soil is primarily surficial, while that of grassland is usually profound, owing to the fibrous root systems, which ramify much more completely through the soil. The successful reaction of pioneers in dunes of sand or topsoil, in gravel slides and badlands, is chiefly a matter of the form assumed by the shoot and root, in consequence of which the 70 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT movement of material due to wind, gravity, or water is diminished or eliminated. Relations of this kind are less frequent and less evident with animal forms, though burrowing rodents, earthworms, and ants in particular constitute an important group. In areas of salt marsh exposed to alternating land and sea conditions, it is probable that the special study of reactions will disclose many animals of much importance. Role of Reaction. As has been previously stated, the primary role of reaction is seen in the process of competition. In connection with this, it regularly assumes the directive function in terrestrial succes- sion and in the concomitant development of the habitat, but it may also lead to the production of bare areas as a requisite to succession. In the development of a primary sere, plant reaction begins with the establishment of the first invaders and is narrowly localized about them and the resulting families and colonies. It is largely mechanical at first and results in binding sand or gravel, producing finely weath- ered material or building soil in water bodies, etc. In secondary seres, extensive colonization may occur during the first year, and reaction may at once be set up throughout the entire area. Reaction then progresses with an increasing advantage to each succeeding stage until the climax is attained, when the reaction of the dominants is so decisive as to exclude other invaders. Thus, in one sense, succession is but a series of progressive reactions by which communities are sifted out in such fashion that only the one in closest harmony with the climate ultimately survives. As an inevitable accompaniment, one serai habitat follows another until the climax habitat becomes perma- nent during the persistence of the climate concerned. In the aspec- tion and annuation exhibited by the climax itself, reaction continues to have an influence, but this is usually secondary to the control exerted by season or climatic cycle. In general, animal reactions on land have not been separated from the larger effect produced by plants. However, they are usually pres- ent to some degree, owing to the presence of soil-moving and soil- modifying animals in the climax and all serai stages, even initial ones in which the plants have not yet appeared. In water, reactions are evident but observation is more difficult. Reactions of the animal dominants regularly play a large part, sometimes as in shallow fresh waters through their influence on turbidity and sometimes through disturbing the substratum (see p. 301). The microplankton, however, reacts upon light and dissolved gases and salts in such a manner as to produce distinct conditions, comparable in degree to reaction effects on land. REACTIONS ON LAND 71 Kinds of Reaction. From their very nature, land reactions are most satisfactorily classified in accordance with the effect upon the habitat (cf . Clements, 1928) . However, in extending the scope of the process, the most convenient division is into land and water, with subdivisions into soil and air, fresh water and salt water, bottom, etc. Furthermore, though it is also convenient to refer to them as plant or animal, this distinction often has no corresponding difference in proc- ess or effect. As to the processes concerned, though these differ greatly in detail, all are characterized by the addition or subtraction of material or energy, or by some feature of disturbance. Finally, the life form of the reactor may sometimes be taken into account to some advantage, though this may carry analysis and classification further than present needs warrant. Until recently, the treatment of terrestrial reactions has been mostly qualitative in nature, but the increased emphasis upon soil conservation as a national measure has already placed the reaction of the plant cover upon soil in the forefront of investigation. In addi- tion to such general studies as those of Darwin (1881) and Passargc (1904), a promising start in the direct attack upon the measurement of reaction in relation to competition and to succession has already been made (Sampson and Weyl, 1918; Lowdermilk, 1926, 1930, 1931, 1934; Formosov, 1928; Forsling, 1931; Greene and Reynard, 1932; Weaver and Harmon, 1935; Weaver and Noll, 1935; Kramer and Weaver, 1936; Kraebel, 1936). The most comprehensive attack upon this problem is that which is now being made at the several erosion stations of the Soil Conservation Service. Meanwhile, the increasing attention given to physical factors in the ocean is providing the neces- sary background for evaluating the reactions of the plankton in particular. REACTIONS ON LAND The reactions exhibited by terrestrial communities are logically divisible into the effects exerted upon the soil complex and those that modify aerial factors. In a comprehensive classification, these are further divided on the basis of organism or agent, life-form or life- habit process, effect, and degree. For the present purpose, however, it will suffice to pass reactions in review on the basis of the process chiefly concerned and to discuss the respective parts taken by plants and animals. 72 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT Soil Reactions Reactions upon the substratum may be arranged in three major categories, namely: (1) those that give rise to soil or a new layer of it, or contribute materials that will become soil ultimately; (2) those that protect the soil against erosion, trampling, etc.; and (3) those that change the texture, structure, or character of the soil in an appre- ciable degree. A new substratum may be produced by four different types of reaction: (1) by the accumulation of organic bodies them- selves, regularly under conditions that retard or prevent decay, and usually also of excreta to some degree; (2) by the concretion of min- eral matter into shell, marl, or rock as a consequence of physiologic activity; (3) by the weathering of rock into fine soil, chiefly through the excretion of acids; (4) by the resistance that organisms, especially plants, offer to wind and current, resulting in the deposition of particles in transport. Soil Formation Reaction by Accumulation. As has been indicated, reaction by the accumulation of organic materials becomes possible only in the absence of processes that remove or rapidly decompose them. It is conse- quently at a minimum in open communities where wind and sun are constantly at work, but increases steadily with the height and density of organisms. Accumulation is naturally most pronounced in small water bodies without currents and, by comparison with the atmosphere, provided with a low content of oxygen for producing decomposition. The maximum effect is attained in peat mosses, which possess unique powers of thriving in pools with little oxygen and low pH, optimum conditions for accumulation. Somewhat similar condi- tions as to oxygen deficit occur in reed swamps, and these are likewise sites of rapid accumulation. Marshes are also built up by the accumu- lation of marl or of diatom shells, but these in addition are products of certain chemical activities of the organisms concerned. Usually, plants and animals share in the formation of biogenous soils, plants commonly assuming the leading role on land. The chief exception is that of deposits of guano, which are not only relatively rare but are likewise to be regarded only as potential soils. In the initial stages of the hydroscre, the bodies of minute animals and excrement may play a large or even predominant part, as in the case of coprogcnons deposits. Such sediments are more characteristic of large ponds and lakes; they have been extensively studied and classi- REACTIONS ON LAND 73 fied by Swedish investigators in particular (cf. v. Post, 1862; Lomas, 1905; Naumann, 1922; Lundquist, 1927). A number of general studies have been made of the excreta of animals in terms of accumulation and their gross relation to the soil, such as the guano deposits of Laysan Island where approximately a million birds nest in two square miles of territory (Dill and Bryant, 1911). Errington (1930) has made a considerable study of the pellet contents of raptors, which accumulate in some degree about nests and in rookeries, while Kellogg (cf. Stoddard, 1931:209) has analyzed more than a thousand regurgitated pellets of the marsh hawk from a ''roost" in Florida. Dearborn (1932) has described the diversified nature of mammal droppings, through which materials of slow decomposition, such as hair, feathers, and bones, are also added to the soil mass. This contribution of animal matter, a large part of which is avail- able more or less readily, has for the most part been ignored by stu- dents of soil fertility, probably because their attention has been focused on field soils where animal life is much reduced. Recently, Greene and Reynard (1932) have made a quantitative examination of this question on a grazing range, with especial reference to the kangaroo rat and the wood rat (Fig. 15). Both these rodents defecate more or less throughout their tunnels, thus leading to an increase in soluble salts, particularly the bicarbonates and nitrates of calcium and magnesium, as well as chlorides from urine. The carbon dioxide of respiration was thought to be the probable cause of the increase of calcium bicarbonate, as a result of the conversion of carbonate, and it was also suggested that this gas increases the availability of phos- phorus in the soil. The most outstanding effect was that upon soluble nitrates, which rose from a probable maximum of 15 parts per million for desert soils to 221 and 570 parts per million in two different bur- rows, making a total of 3.65 and 10.26 pounds, respectively. The contribution to the soil by animal chitinous bodies and cal- careous and bony skeletons, though small by comparison with that of plants, is still a matter of significance. This is a field in which quanti- tative determinations are practically unknown, and the annual turn- over as a whole or for any particular group must be left to conjecture at present. The question is also complicated by the coactions of scav- engers and sapronts of all sorts, as a consequence of which the return is indirect or delayed. The effect of any particular species is chiefly a resultant of size and number, and hence it is possible that inverte- brates may often play a larger part than birds or mammals. The approximate number of invertebrates per square meter at the time of the midsummer maximum has been estimated at 3,300 by McAfee 74 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT (1907), or about 1 to each 3 square centimeters. Since many species produce several generations in a year and others do not appear in the summer aspect at all, the total number annually must be much larger, probably reaching 1 or 2 per scjuare centimeter. It seems probable that the contribution made by excreta is more evenly distributed in general than the bodies of animals, though just Fig. 15.— Diagram of a typical den of the banner-tailed kangaroo rat (Dipo- domys spectabilis Mer.). Double shading indicates where one portion of tunnel lies above another and solid black a three-story arrangement; A, B, C, etc., active openings to surface; N, nest chamber; S, storage; OS, old storage; Y, probably an old nest chamber; Z, old, unused, or partially plugged openings. (After Vorhies and Taylor, 1922.) as little is known of its amount, apart from guano and similar deposits. A large ungulate will distribute a considerable amount of excrement in the course of a lifetime, as the "buffalo chips" of the Great Plains demonstrate, but the absence of accumulation renders this much less conspicuous than in the rookeries of birds, bats, etc. Concentration also occurs in respect to many rodents, especially in relation to sani- tation, and the intensity of the reaction can be estimated from pellet REACTIONS ON LAND 75 counts made to determine relative numbers of individuals (Taylor, 1930, b). Even small forms such as insects are not without impor- tance in this connection, since caterpillars are known to add several times their own weight of pellets consisting of partially digested plant material (Jacot, 1936, a, b) . Reaction by Accumulating Shells and Concretions. The shells of animals, whether chitinous or calcareous, regularly play a minor part in this process on land, though quantitative studies may assign them a greater importance than recognizable at present. The sole group of plants with a similar reaction is the diatoms, though their effect is relatively insignificant today in comparison with the geological past. The production of diatomaceous soil on a small scale may be observed along the margin of many pools and small streams, but marshes of this type are rare. The most extensive and best known are found in Yellowstone Park, where the hot waters have apparently promoted the growth of diatoms, and the consequent accumulation has produced a hydrosere, ending in characteristic meadows. Apart from shells, the concretions due to direct physiological activ- ity are limited to aquatic plants found in shallow waters. The result- ing substrata may be calcareous, represented by marl, tufa, and travertine, or siliceous, as in sinter and geyserite. By far the most widespread of these deposits is marl; it is produced chiefly by Chara and occurs more or less regularly as a layer of variable thickness in fresh-water marshes. It is frequently mixed with terrigenous mate- rial and contains small amounts of organic matter from the decaying shoots of the stonewort. Somewhat similar incrustations are pro- duced by a few mosses, while the massive forms known as travertine are the work of microscopic algae, as oolite may be likewise. Sinter and geyserite are also secreted by blue-green and yellow-green algae, but are restricted to the cones and basins of hot springs and geysers, and are consequently of slight importance. Reaction through Weathering. The conversion of rock into soil, in the usual sense, is the combined effect of mechanical forces and plant and animal activities. The former take the more conspicuous if not the more important part, but the production of fine particles is chiefly the work of the organisms. In the case of woody plants, the growth of roots in thickness is an important factor in mechanical weathering, but the paramount reaction is exerted by root secretions, primarily carbon dioxide in solution. Animals apparently have only a small and indirect part in weathering, and then only after cracks have appeared which they can occupy. The corrosion of rock by plant roots is the most significant process 76 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT in the production of fine soil, especially when this accumulates in one particular place. This is a property of all plants from unicellular algae to the largest trees, but its importance depends largely upon the size and extent of the root system. The initial conversion of rock into soil is carried on by the pioneer lichens and their successors, the mosses, in which the hairlike rhizoids assume the role of roots in breaking down the surface into a fine dust. This process is exceedingly slow in granites and lavas, but proceeds more rapidly with sandstones and limestones. It is promoted by the action of frost, as well as wind and water, in forming tiny cracks into which the corroded dust is washed and ants and other animals find space and small herbs may invade. By virtue of their root systems, these carry on the process of weathering more effectually, each successive stage in the xerosere tak- ing a larger part in the process. At the same time, the decay and excrement of each generation add organic matter until a more or less uniform soil is constituted. Reaction upon Wind-borne Material. The major reaction of the plant body upon wind is to lessen its velocity and thus bring about the dropping of its burden of sand or dust. A minor effect results from its constituting a definite obstacle to the movement of particles, a fact often recorded in the abrasion of stems or the etching of trunks. In addition, the plant serves as windbreak for the accumulation at its base and thus renders it difficult for the wind to pick up the grains again. The life form is of the first importance in this reaction, tall plants and especially those with single stems having little or no effect, while mat, bunch, and bush forms attain the greatest success. Roots and rhizomes exert a complementary reaction by binding the accumu- lating material, fibrous ones being naturally the most effective. Of even greater significance than form is the faculty of developing new shoots as the crown is buried, thus permitting plant and community to keep pace with the accretion of dune or ridge. The ability of grasses to produce tillers is peculiarly advantageous in this process and hence the grass form is probably the best adapted to dune formation and stabilization. The action of shoots upon wind-borne snow is essentially identical, but the accumulation is transient, and the reaction is primarily upon the water content of the soil. Reaction upon Water-borne Detritus. The mechanical action of plants upon currents of water is essentially similar to that already noted for air currents. Movement is impeded, and the load is depos- ited in whole or in part. Stems and leaves also make difficult the removal of material once dropped, and root stocks and roots take REACTIONS OX LAND 77 their share in this process. This reaction is often associated with the deposition of sand and silt by the retardation of currents as they enter pond or lake, but the effect of plants is regularly predominant in such deltalike areas. The resultant filling has much of the consequence already indicated for the accumulation of the plant remains, and the two processes usually cooperate to build up the level. However, the movement of water is progressively hindered as the level rises, until the area is overflowed only at times of flood. This sets a limit to the deposition of sediments, and the further reaction is chiefly one of decreasing water content due to the fall of plant parts, to trans- piration, etc. The role of jjlants in impeding runoff and preventing erosion is even more striking and important, though the action itself resembles in some respects that of a shallow stream. In fact, it is the formation of rills and gullies that renders erosion so effective. A good cover of vegetation operates, in the first place, to prevent the direct impact of raindrops on the soil, but much more important is its action in holding back the fallen rain until it can be absorbed. It further restrains both rills and sheet floods, reducing the momentum as well as the surface affected and consequently minimizing both load and erosive power. In the case of wind, the decrease in velocity through the action of cover is the major factor in reducing erosion. Frequently, especially in arid regions, water and wind act together, producing a landscape of hummocks, which are the result of alternating erosion and accretion. The organization of the Soil Conservation Service and the nation- wide installation of projects in soil conservation and flood prevention have served to draw attention to the plant cover as the paramount fac- tor in protection and control. As a consequence, the reactions of cover, both natural and cultural, have come to be regarded as of the utmost significance to economic and social progress, not merely in terms of agriculture, grazing and forestry, but also to urban populations. No field of conservation research equals this in importance or has been more neglected until recently, and the next decade is bound to see an enormous expansion of knowledge in it, together with almost unlimited application to human affairs. Reaction upon Slipping and Sliding. The reaction of a plant cover on the soil of slopes may be exerted upon the mass as well as upon the surface. This is particularly true of loosely aggregated materials, as in talus, steep slopes of gravel, sand, snow, and so forth, and it applies likewise to the faces of cuts and fills in the grades of highways and roadways. In the case of sand, volcanic ash, or gravel, the effect 78 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT is produced by the underground parts, primarily the roots, while that upon snow is due to stem and branches, and to leaves also in the case of conifers. The process known as "slumping" involves, in addi- tion, the saturation of the soil mass so that it flows, producing lava- like streams of mud under extreme conditions. Slumps occur with increasing frequency as highway cuts become deeper with more abrupt sides, and their prevention by means of plant reactions has become a matter of much practical importance from the standpoint of both safety and economy of maintenance. The species best adapted to retaining the soil on slopes are mats or rosettes with tap roots, or long branching ones which anchor the plant firmly, their greatest extension often being uphill, and the cluster of stems or horizontally appressed leaves prevents the slipping of the surface materials. Each plant or colony exerts a stabilizing effect for some distance below its own area, partly by intercepting small slides above it. The primary reaction is a mechanical one, leading to in- creasing aggregation and finally to invasion. Where rain or snow is a factor, as in slumping, the grass or bush forms possess additional advantages, particularly in utilizing artificial succession to hold the slopes. Soil Structure The reactions that build soils regularly continue to act to bring about modification in them to a larger or smaller degree. The struc- ture of a soil may be changed mechanically by superficial accumula- tion or by the inclusion of plant and animal remains, by the penetra- tion of roots, and by the disturbances wrought by animals. With these go a number of chemical changes, often of fundamental impor- tance. In addition, plants react upon the soil profile in such a manner as to protect it against the action of modifying forces, such as weather- ing and erosion by water and wind. The soil is thus a complex of reactions, in which the role and significance of each process can be definitely ascertained only by thorough-going analysis and measure- ment. This applies particularly to the respective parts taken by plants and animals, though it is obvious that the major effect of ani- mals will be exerted through various kinds of disturbance. Reaction by Adding Organic Matter. The most important changes in the structure and texture of the soil are caused by the addition of organic matter or humus. This is derived chiefly from the decay of plant parts, though animal remains usually play some part in it, and its working-over and incorporation are due primarily to animals, everywhere the smaller soil organisms and in dry region the rodents REACTIONS ON LAND 79 also. All plants contribute to the humus in some measure by the death of the entire organism, annually or from time to time, by the annual falling of leaves and the shoots of perennial herbs, and by the exfolia- tion and decay of roots and underground stems. The amount pro- duced depends upon the density and size of the population and upon the rate and completeness of decomposition. It is small in the pioneer stages of a sere, especially in xeric situations, and increases steadily to reach a maximum in or before the climax. AVhatever the contribu- tion made by animals, this is probably greatest in the subclimax or a late serai stage. The admixture of organic matter not only permits the renewed utilization of the nutrients absorbed by previous generations, but it also produces highly important physical effects, especially upon the water content or holard. At first thought it appears a contradiction that humus should have opposite effects upon sand and clay and yet improve the water relations of both. This is explained by its cement- ing action, as a consequence of which it makes one more retentive of water and the other more porous. In general, this tends to increase the water content of dry areas and to decrease that of moist soils, though the decrease is to be ascribed in large measure to raising the level. On the other hand, the non-available water or echard of sand is diminished relatively, while that of loam and clay is augmented. Furthermore, penetration by roots, especially fibrous ones, and the activity of burrowing animals, loosen hard soils and increase absorp- tion, and conversely tend to compact sand and raise the water content correspondingly (cf. Romell, 1921-1935). Reaction by Disturbing the Soil. Practically all the reactions of this group are caused by the activities of animals, negligible excep- tions being furnished chiefly by the growth of underground plant parts. The number of genera and species concerned is very large, represent- ing every major terrestrial group. Man naturally stands preeminent in the variety and magnitude of his effects, mammals generally being much more important than all other groups combined, with the pos- sible exception of ants and earthworms. As to the activities or proc- esses involved, digging of all sorts, with the attendant transfer of material, is paramount, trampling, pawing, wallowing, etc., being of quite secondary importance. In a large number of cases, the reaction itself is not a direct object of the activity, but an outcome of a pur- poseful coaction, as in the rooting of swine. IMoreover, the reaction may be superficial or deep seated, temporary, recurrent, or perma- nent, and in its effect significant or immaterial. As in the case of plants these consequences depend largely upon the degree of aggregation, a 80 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT community of ants often producing a much greater effect than a single large mammal. In the brief outline that follows, the divisions are based upon activity and effect, the subdivisions being made in general correspond- ence with similarity in life form, size, or behavior. The multiform effects exerted by man are reserved for treatment at the end of the section on land reactions. Digging and Burrowing. Digging may produce hollows, holes, or galleries, or a more or less complicated system of tunnels and cham- bers to form a burrow or den. These may serve for nests, shelter and housing, for storage, sanitation, or for various other purposes. The dirt freed may be merely thrown out for a short distance, it may be utilized for diking, or may be carried to some distance to be deposited ; some of it may be compacted into plugs for sealing abandoned bur- rows and entrances as is done by some pocket gophers. Its transport may lead to the formation of paths with the compacting of particles, and its piling, systematic or otherwise, amounts in effect to primitive cultivation, while both processes produce coaction effects in destroying plant cover and the latter by stimulating it also. In general, the con- sequence brought about by a single individual or family is slight (see Fig. 15, page 74), with the exception of such large mounds as those of kangaroo rats, and hence digging coactions are most signifi- cant where aggregation becomes pronounced, as in the so-called towns. By far the most important burrowers are the rodents belonging to the fossorial life habit or mune. While some members of the carni- vores, such as badgers, skunks, and even some wild dogs, do dig holes, they are usually scattered and the importance correspondingly less. In the absence of quantitative studies of burrowing reactions, it is impossible to do more than compare different genera on the basis of size and activity, degree of aggregation, and general effect. Perhaps the most widely important in North America are the pocket gophers, followed more or less closely by marmots and prairie dogs (Fig. 16), ground squirrels, kangaroo rats (Vorhies and Taylor, 1922), rats and mice generally being of much less consequence. Some of these may burrow to a depth of fifteen to twenty feet, translocating a prodigious amount of earth for a relatively small animal, while others, penetrat- ing but a foot or two into the soil, may construct mounds several yards across and two or more feet high, or may group small mounds so closely as to cover more than half the surface. In constructing a system of tunnels, the kangaroo rat is probably the most skillful ; the viscacha of South America develops a unique set of surface trenches a foot or more in depth for conveying loose dirt (Hudson, 1892:294), REACTIONS ON LAND 81 Fig. 16. — A vertical section of a prairie-dog burrow (Cynomys ludovicianus Ord.) showing the bringing of soil from a depth of nearly 5 meters. A, mound; B, funnel-shaped entrance to bun-ow; C, main passage 4^/^ inches (11.4 centi- meters) in diameter, about 15 feet (4.6 meters) in length; D, horizontal passage 9^/^ feet (2.9 meters) in length; E, unused nests filled with earth and refuse; F, unused part of horizontal passage filled with earth, etc. 4 feet (1.2 meters) long; G, niche large enough for one prairie dog; H, nest of grass 11 inches (28 centimeters) in diameter by 9 inches (22.8 centimeters) high; /, absorbent matter carrying bisulphide of carbon; K, position of prairie dogs as found after use of bisulphide of carbon; L, depth of horizontal passage 14 feet 7 inches. (After Merriam, 1901.) 82 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT The number of general studies of , burrowing coactions is of course legion, and one of the major tasks of bio-ecology is to convert these into quantitative terms, as is suggested by some of the more recent researches in this field (Vorhies and Taylor, 1922; Grinnell, 1923, 1933; Formosov, 1928; Greene and Reynard, 1932; Greene and Murphy, 1932). Among the birds, reptiles, and amphibians there are few true bur- rowers, the so-called burrowing owl being often a tenant rather than a builder, and the list comprises chiefly kingfishers, certain swallows, the gopher tortoises, and a few true toads. The burrowing reaction is much more common among insects and spiders, often for shelter or hunting, but, among the former, especially for the deposition of eggs. Notable examples are the gryllids, particularly the mole crickets, locustids or acridids among the Orthoptera, tiger beetles, carabids, and dung beetles in Coleoptera, many termites, and digger wasps and ants among Hymenoptera. The burrowing spiders are chiefly lycosids, mygalids, and agelenids, containing the true and false tarantulas, and the trapdoor forms, while of the Crustacea the only considerable bur- rower on land seems to be crayfish. In nearly all the above examples, while burrowing plays an important part in life history and coaction, significance as a reaction upon the habitat is as yet unmeasured, some termites constituting perhaps the most conspicuous exception. Probably the disturbance reaction of greatest total significance is that of ants and of earthworms in view of their great number, dense aggregation, and widespread occurrence. The large earth-moving worms are restricted to moist areas, but ants are important through- out the globe. Perhaps no other small animal exerts such a variety of influence as these small insects, though unfortunately there have been few or no quantitative studies of the effect of this group. Only the reactions of the mound builders are strikingly evident. Soil is usually brought from a depth of six to eight feet (Fig. 17). Their hills and cleared circles are a conspicuous feature of grassland and desert, where they are sometimes an aftermath of disturbance by cattle or rodents. Part of the earthworm reactions are direct; others accompany or follow food coactions. As to the earthworm burrows, Darwin states that these are built in two ways, either by using the pharynx as a wedge to push the dirt away on all sides, or by actually swallowing the soil and ejecting it as castings. The one is accomplished in a short time in loose soils; the other may require a day or more in compact ones. At first the castings are deposited directly on the sur- face, but as the pit deepens the excreted soil is transported and fre- REACTIONS ON LAND 83 quently built into towers often several inches high by the larger forms; castings are also piled in subterranean chambers or cracks. Two minor reactions of interest have to do with the piling of tiny pebbles about the mouth of the burrow and with their use as gizzard stones. Finally, important results spring from the two chief food coactions, namely, the consumption of plant parts and animal mate- FiG. 17. — A vertical section of a harvester-ant nest {Pogonomyrniex occidcntalis Cres.) in western Kansas. It is nearly 6 feet (2 meters) from the top of the mound to the bottom of the excavation. (Photo by Prof. G. A. Dean.) rial and the utilization of organic matter in rich soils (cf. Jacot, 1936, a and h). It is manifest that earthworms are in essence cultivators of the soil of moist regions, increasing its fertility, rendering it more uniform in texture, and improving its water relations. They also deepen the fertile dark horizon, especially when the penetration is several feet, and frequently tend to counteract acidity by bringing up considerable amounts of lime from the zone of concentration. This process may be 84 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT one of compensation for the acidity of decaying plant material as well as for the acid casts, especially in view of the presence of cal- ciferous glands in these organisms. The large amount of carbon diox- ide given off in respiration must increase the acid reaction, both with respect to the solution of minerals necessary for plants and the neces- sity for neutralization. Salisbury, who has studied these relations (1924), finds that earthworms are most numerous in soils approxi- mately neutral, decreasing in the direction of both acidity and alka- linity; they bring materials up from considerable depths, and the general effect is to modify the horizon and diminish its organic con- tent by mixing coarser material with it. As with ants, coaction is often combined with reaction, and this is especially true of harvester ants (Fig. 17, see page 83). In distribution, earthworms embrace practically all rainy portions of the globe, from Iceland on the north through temperate and tropi- cal zones to Kerguelen in the south, and upward to the alpine climax of lofty mountains. In size, earthworms range from less than a foot in temperate regions to a maximum of six feet in tropical and austral ones, with a girth to correspond. As to number and density, Darwin (1881:158) quotes Hensen to the effect that counts in a measured space indicate a total of more than 50,000 worms to the acre in garden soil and about half this number in fields. Their numbers are, how- ever, greatest in rich cultivated soil, artificial meadows, and rich flood- plain silt. Their numbers in original communities are relatively small. In moist tropical areas these characteristics of earthworms may also be reinforced by that of size, some species attaining lengths of three to six feet, with corresponding relations to soil profile and the amount of earth moved. Surface Disturbances. A host of animal reactions are exerted only on the surface of the soil, or at most in the upper few inches. Obvi- ously, no exact line can be drawn between these and holes or burrows, since digging in some form is regularly involved. However, reactions of this group may be characterized as those in which the surface alone is affected, or in which breadth is increased at the expense of depth, the depth usually being insignificant by comparison wdth the size of the animal concerned. Such effects, though often of much interest in connection with behavior, are rarely of significance in the habitat, apart from the coaction upon vegetation. This is likewise true of trampling, which, as a disturbance, belongs under compacting, in the next section (Fig. 18). The more important reactions upon the surface are caused by rooting, pawing, and trampling, chiefly by mammals. Rooting is char- REACTIONS ON LAND 85 acteristic of swine and their relatives, and produces the maximum local disturbance of this type. Pawing resembles it closely in effect when roots and bulbs are dug out of the soil by this method, but as a rule the effect of pawing is merged in the greater reaction due to trampling. Trampling acts primarily by destroying the plant cover and working the remains into the loosened soil, improving the penetration of rain- fall, and perhaps hastening the incorporation of organic material. On the other hand, the damage done to the plant matrix directly and as a consequence of increased erosion by water and wind far overbalances ■4----'- ••■•^ ..r -»m»t^^- '"mim. Fig. 18. — TeiTaces produced by gi-ound .■^^qmrii 1-, upper ."^lui Joaquin Valley. (Photo by Edith Clements.) any beneficial action. The formation of blowouts in sandhills is a frequent outcome of the trampling reaction, particularly about water- ing places. Somewhat akin to pawing and rooting are the scratching and pecking of most ground birds and some perchers, utilized for the finding of food or gravel, for "dusting," making hollows for nests or "forms," and so forth. Aside from gallinaceous birds, those that nest on the ground away from water are relatively few, the lark bunting being an example. Surface disturbance is also a reaction in the case of reptiles. The effects of all such habits are of much the same nature as those of burrowing, the uppermost layer of the soil being 86 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT modified in structure, water and air content, and organic matter in many cases, but to a much smaller or often imperceptible degree. Related to the surface as a source of material are the nest-building activities of some birds, e.g., swallows and phoebes, and of a large number of "mud daubers" and masons among Hymenoptera especially. Here the amount of mud or pebbles removed and the consequent reac- tion are inconsiderable, but when turrets are built, as by Anthophora and others, the effect is often striking. Reaction by Compacting or Cementing Particles. While roots exert a binding action upon coarse soils and hence compact them in some degree, this consequence is much more characteristic of the activities of animals. It is especially typical of the cursorial life habit, but is also exhibited by fossorial species that make more or less definite runways. The activity regularly concerned is trampling to such an extent that the plant cover is largely or entirely destroyed and the impact is then received directly by the soil surface, the resulting trail often being converted into a gully by erosion. However, it is obvious that compacting results in fine soils only in correspondence with the amount of colloidal material present. In sand, the effect is the same as that produced by trampling, owing to the lack of cohesion between the grains. Other animal activities quite different in nature produce much the same reaction as trampling, for example, rolling, bedding, and wallowing, best illustrated by the "buffalo wallows" of the Great Plains. However, all compacting reactions are narrowly circumscribed, and they are much more striking than important. The property that humus possesses of acting as a weak cement and thus binding together particles of soil has already been noted (Hall, 1908:47). It operates in practically all soils, but its consequences are most pronounced at the two extremes, sand and clay. Humus is also thought to be concerned in the formation of "ortstein" in heath sand, its soluble fraction combining with mineral salts to produce an im- pervious stratum. A somewhat similar result is to be found in grass- land chmaxes, especially in semi-arid or arid regions, where the pene- tration of water is restricted to the depth attained by the roots. The immediate consequence is that the dry soil beneath becomes compacted into a "hardpan," but this is usually secondary to the striking effect produced by the accumulation of minerals at this level, leading to the cementing of the particles into an impure limestone. In its turn, the hardpan limits the downward growth of roots under normal rainfall, but in times of excess it may be sufficiently softened and dissolved to permit the passage of roots and the reformation of the hard layer at a deeper level. REACTIONS ON LAND 87 Soil Water, Solutes, and Gases These three sets of factors are most intimately associated in the soil, and the modification of one leads to the change of others. This is truest of water content, since the amount of this determines in large measure the concentration of the soil solution, as well as the pore space available for air or other gases. Since water is the chief factor in plant as well as community response, it is more or less affected by nearly all reactions. In addition, the increase or decrease of the total water or holard may be a direct outcome of the activity of plants themselves, and this effect may operate upon the available water or chresard, as well as upon the total amount present. Reaction by Increasing the Water Content. No flowering plants are known that increase water content as a direct reaction, though they may bring this about by the formation of dew and the condensa- tion of fog. The sole plants to exert a direct effect are a few mosses, notably Sphagnum, and perhaps such algae as the ground forms of Nostoc. The power of the peat mosses to absorb and retain relatively enormous amounts of rain and dew is unique. Because of this prop- erty, Sphagnum is able to waterlog or flood small areas, with profound effects upon the course of succession and the accumulation of organic material. All reactions that enhance absorption or hamper percolation or evaporation increase water content indirectly. Root systems are every- where of paramount importance in promoting penetration of water into soils, this reaction being most significant in finer or "harder" types. The fibrous roots of grasses are the most effective in augmenting water content, but the deeper-seated ones of perennial forbs and woody plants operate especially in connection with percolation. Humus is likewise a major agent in fostering absorption, and its action is prac- tically universal; even in the initial stages of the xerosere, its small but cumulative effect is decisive. INIuch more obvious, but greatly restricted in extent, are the conse- quences arising from the disturbance of the soil by rodents in particu- lar. Not only do the mounds of loose dirt affect the amount of water that enters and leaves the soil, but the openings and tunnels exert a further action, especially on slopes. It seems to be a common assump- tion that the reactions of burrowing rodents increase erosion by sup- plying loose material and in particular by the wearing of tunnels into gullies. However, constant search for evidence of the latter effect has disclosed but a few doubtful instances, while on the other hand there 88 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT is considerable proof that tunnels and mounds have a beneficial action in promoting absorption (cf. Grinnell, 1923, 1933). Reaction by Decreasing the Water Content. As a direct reaction, plants diminish the water content by absorption and transpiration. The transpiration of a deciduous forest during the summer may be greater than that from a free water surface, and it may be greater still from streamside trees, such as alder, poplar, and willow. Water loss also attains great proportions in the case of most herbaceous crops and amounts to a large total in true and mixed prairie, in spite of the more or less xeric nature of the grass dominants. Probably the highest transpiration in relation to surface is found in emersed water plants and especially those of reed swamps, all of which have permanently open stomata. The reaction is particularly significant in such serai areas, as it materially hastens the drying-out and successful movement set on foot by the shallowing action of plant remains. Animals obviously reduce the water level and remove suspended matter in ponds and playas by drinking, but this is of slight impor- tance except in arid regions, where it is usually secondary to drying by evaporation. They may likewise exert an indirect effect by pack- ing the soil and increasing runoff, and this reaction is turned to advan- tage in the range country for the puddling of earthen reservoirs or "tanks" to insure the retention of impounded waters. Reaction by Returning Plant Nutrients. This reaction is a re- curring one incident upon the annual fall of leaves and the death and decomposition of plants or their parts. A portion of the nutrients may be returned by more or less immediate leaching, but the major part must be unlocked by the coactions that produce decay. The share which animals have in this is unknown. However, the significant fact is that in nature the material returned to the soil corresponds more or less closely to the amount withdrawn, and a fairly definite balance of nutrients is maintained. In crop communities, this balance is dis- turbed to the extent that the individuals are removed, a headed crop of grain contrasted strikingly, in this respect, with one of sugar beets. A severe fire and particularly a complete burn permits the much more rapid incorporation of mineral salts in the soil. Under favoring rainfall, the bulk of these may be returned the first season, as is indi- cated by the exceptional growth made by annuals after a fire. An increase in nutrient content is likewise well known to result from the activity of legumes and other nitrifying organisms, but this is properly considered among coactions. Reaction by Decreasing Plant Nutrients. A progressive or per- manent reduction in soil nutrients, as a consequence of their utilization REACTIONS OX LAND 89 by plants, probably does not occur in nature. A temporary decrease may follow a season of luxuriant growth, such as is noted above after a burn or in consequence of exceptionally favorable climatic condi- tions. Even in the case of crops, the amount absorbed each year may be a very small part of the total present, so that cultivation for long periods may produce no appreciable deficiency (Hall, 1905). The formation of heath sand probably furnishes an example of reduction in nutrient content as a consequence of the formation of acids by humus. These render the mineral nutrients soluble, and they are then removed by the percolating water, beginning at the top. A somewhat similar process takes place in sandy soils in regions of high rainfall, the leaching action of the rain apparently being pro- moted by the acids derived from partial decomposition. Reaction upon Air Content. The amount of air in the soil is known to bear an inverse relation to the water content, decreasing as the latter rises, and the reverse. It increases markedly as a result of all animal activities that disturb and loosen the soil, and particularly so by reason of the fact that these are so often accompanied by tunnel- ing. The loosening effect of plant roots and rhizomes also promotes the entrance of air in some measure. The chief response of plants and of soil animals is to modify the composition of soil air. This involves the absorption of oxygen and the release of carbon dioxide. Since the density of the medium pre- vents ready exchange with the atmosphere above the soil, the air content is regularly lower in oxygen and higher in carbon dioxide than ordinary air. In soils neither wet nor packed, the reduction of oxygen as a consequence of the respiration of roots is rarely serious, though this is not at all true of waterlogged soils. On the other hand, carbon dioxide diffuses less readily through the pores of the soil and may accumulate to a harmful extent in the deeper layers of many compact soils, though the greatest quantity is to be found in w^et soils. Reaction by increasing the amount of soil oxygen is a property of a number of blue-green and yellow-green algae that grow in the upper layer of moist or wet ground, or even on the latter, but the effect is probably too limited to influence any but the minute organisms of the soil. Reaction in Terms of Acids and Toxins. A voluminous literature has grown up around the moot questions of bog xerophytes, toxic exudates, and soil toxins, though the questions themselves have by this time been answered mostly in the negative. It has been shown that the effect of bog water can be largely explained on the basis of deficient aeration, and that the evidence for the secretion of toxic 90 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT exudates by roots is slender, if not altogether wanting. Moreover, the presence of deleterious substances in soils is to be explained chiefly by deficient aeration and resulting anaerobic conditions, as has been emphasized elsewhere (Clements, 1921, b). Even animal excreta ac- cumulate only exceptionally to the extent of becoming deleterious. Reaction and the Soil Profile. The profile of a soil is characterized by the evident differences shown by a cross-section from the surface to country rock or other undifferentiated matrix. Normally, a soil pro- file consists of three horizons or layers, more or less clearly distin- guished by texture, color, structure, and so forth. The uppermost or A horizon is marked by darker color and lighter texture, the middle or B horizon by relatively brighter color and heavier texture. The C horizon is usually set off by a color difference also, owing to the fact that it is the parent rock or sediment, little affected by weather- ing. In a large number of soils, both A and B exhibit a further but slighter differentiation into subhorizons, known as Ai and A2, Bi and B2. In terms of reaction, these three layers show both quantitative and qualitative differences. As the uppermost, A is the level of major reaction, B of minor reaction, and C of little or no effect from the biotic community. The A horizon, as a result of direct contact with the plant cover, is influenced, in some degree, by nearly every one of the reactions described. However, the addition and incorporation of or- ganic material are the characteristic features of it, evoking the chief distinctions between it and the B horizon. In the latter, the outstand- ing process is the concentration of fine particles and of mineral salts, often leading to the formation of hardpan. Because of its depth, horizon C is beyond the reach of practically all reactions, and hence it is not really a component of the soil in the strict sense. Thus, from the standpoint of reaction, A may well be termed the level of accumu- lation, B of concentration, and C of inaction. However, it is necessary to recognize that all three horizons regularly shade into one another, with respect both to processes and to visible criteria. The soil profile further possesses certain important relations to air reactions and consequently to climate, indirectly as well as directly. In fact, from the ecological viewpoint, a soil may well be regarded as a mass of parent rock, more or less consolidated, in which the external portion has been differentiated by climate, biome, and topography. Of these, the influence of the plant matrix is most direct and imme- diate; that of climate is indirect through its control of climax and direct by virtue of rainfall and temperature in particular. Topog- raphy may exert the most striking effects in connection with erosion AIR REACTIONS 91 and deposition, but these are more local and to a large extent condi- tioned by vegetation. In view of these facts and especially the devel- opmental correlation between climax and habitat (Clements, 1905:292; 1916:357) , soils may properly be distinguished on the basis of climaxes, as has already been done to some extent in the recognition of forest and prairie, humid and arid categories. In addition, they may be sub- divided with respect to climax and sere, the role of topography being especially important in connection with the latter. AIR REACTIONS From the very nature of the medium, the reactions of plants upon the air are usually less definite and controlling than upon the soil. Naturally, the chief reason for this lies in the fact that effects are not readily accumulated in a gaseous medium. However, a notable excep- tion exists in respect to light, in which the time element produces results not unlike those of accumulation. The absence of air reac- tions by animals is noteworthy, since the functions that produce their striking reactions in water are almost without effect on land. Reaction upon Light. The leaves of plants react upon light by virtue of reflection and absorption, while the chief role of branches and trunks is interception. The obvious consequence is to reduce the inten- sity, especially of sunlight, and to produce varying degrees of shade. Since the absorption of leaves is selective, it has frequently been assumed that the quality of light is changed under forest canopies especially. It is now known that this takes place in a considerable degree only in dense forests and thickets, owing to the fact that in the great majority of cases the light beneath the crowns is derived from rays reflected by the leaves or passing between and not through them. The same principle holds true for the successive forest layers, the quantity being affected to the extreme point where the ground layer can consist only of mosses and fungi. In the initial stage of the hydrosere, the reduction of light intensity by the water itself may be greatly augmented by the reaction of the plant community. This is most notable for floating leaves, such as those of pond lily and pondweed, but it may sometimes be as great for submerged species, for duckweeds, and, under optimal conditions, for microscopic algae of the plankton. The reaction of the dominants of reed swamps is often much more decisive than it appears, and this is true likewise of grassland, in spite of the more or less complete absence of a canopy. In ponds, the minute animals of the plankton exercise an effect when abundant, and this may likewise be true of 92 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT larger forms under occasional circumstances. In the air itself, animal reaction upon light usually occurs as a secondary effect in the case of phytophagous insects, which destroy foliage, and of other organisms residing upon leaves. Reaction upon Humidity, Temperature, and Wind. These three factors are intimately associated in a complex that determines the water relations of the community in the higliest degree. The energy required to bring about transpiration and evaporation is supplied by incoming radiation, the capacity for taking up the moisture concerned is determined by humidity, and both are modified by the moving and cooling action of wind. The reaction upon all three is practically confined to the plant matrix, since that of animals is essentially negli- gible in spite of the fact that mammals in particular intercept radia- tion and wind, and give off moisture in the form of perspiration. As with light, the reaction upon temperature is due to absorption and interception, together with more or less reflection, and this like- wise increases in intensity from the upper to the lower layers of a community. Conversely, the plant cover, living or dead, may also serve as a blanket to retain the heat that has entered. The effect upon wind is even more obvious as a consequence of interception and correspondingly influences both temperature and humidity. Finally, lunnidity fluctuates directly with the transpiration, and to a less extent with evaporation from plant surfaces of the water condensed or inter- cepted by them. As the ultimate result, water loss is reduced and the holard relatively increased under a canopy, with characteristic effects upon tlie function and structure of shade plants. Reaction upon Carbon Dioxide and Oxygen. Since plants absorb and emit both these gases and animals give off the one and take in the other, it is to be expected that the biotic community will exert some reaction upon the composition of the air. This is an important effect in both soil and water in which diffusion and air movement are much reduced. The mobility of the atmosphere, coupled with the rapidity of diffusion, prevents the accumulation of gases given off and at the same time readjusts the conditions arising from consumi:)tion. Hence, it is only where air movement and diffusion are hindered or the emission of carbon dioxide excessive that accumulation can occur. In nature, such requisites are found only in dense forests and thickets, where a tendency exists to increase the carbon dioxide just above the soil layer especially. This is not true of the oxygen content, since photosynthetic activity is weak in the lower layers, owing to deep shade, and also because this gas is replaced by the augmented carbon dioxide in some degree. AIR REACTIONS 93 Reaction upon Climate. From the preceding account of air reac- tions, it is evident that plant communities exert definite effects upon climate, especially in terms of water relations. These find expression in the processes of precipitation, condensation, and interception, which are consequences of transpiration, cooling, and mechanical action, and hence most marked in the forest. The long debate over the effect of forestation on rainfall has led to a decision in favor of the affirmative, though the amount of increase is still a moot question to be decided only by organized experiments on a much larger scale. One of the basic problems to be settled is the relative transpiration of forest, scrub, grassland, and crops of various sorts. Thus, a possible excep- tion to the rule that forest increases precipitation may be found in the replacement of xerophytic forest and scrub by grass and crops in Australia, which was followed by a rainfall increase of 3 per cent (Quayle, 1922). AVhile the water loss of a deciduous forest is so great as to support the assumption of Briickner that 78 per cent of the pre- cipitation over the continents is derived from this source, the evidence is still too general to warrant its acceptance as more than a plausible working hypothesis (cf. Briickner, 1905; Zon, 1913; cf. Brooks, 1928). Reaction by condensation is partly mechanical and in part due to the lowering of temperature in some degree. It produces striking results in regions much subject to fog and fine mistlike rains, the in- creased precipitation often amounting to twofold or greater. Again the effect is most pronounced in forest and decreases with reduced height and spread in scrub and herbaceous vegetation. Dew belongs in the same general category, but it is much less significant (Marloth, 1903, 1905; Phillips, 1926). Reaction by interception is wholly mechanical in nature and may be exerted by animals as well as plants, though to a much smaller degree. It is produced by all plants, but is of little import in open communities of forbs. It increases with size and density, reaching a maximum in forests, where it may amount to as much as 25 to 50 per cent of a particular rain, bearing an inverse relation to the intensity of the latter (de Forest, 1923; Phillips, 1926; Zon, 1929:24; Brooks, 1928). Reactions Produced by Man. As a superdominant, man may exert all the reactions caused by animals and nearly all those due to plants, working more or less directly through his own activities. When his innumerable coactions enter the scene, he becomes also a superinfluent, with the reactions of plant and animal as well as of the entire commu- nity at his command. Hence, he is unsurpassed in the variety and intensity of his reactions, though many of these are local and inter- 94 REACTION: THE INFLUE^'CE OF COMMUNITY ON HABITAT mittent by contrast with those of the climax. Moreover, his control is conscious and usually intentional, and thus may be extended in space, time, or degree at the behest of need or interest. This is as true of air as of soil reactions, and man has modified or evaded local climates by virtue of shelter, heating and cooling, as well as by a number of minor devices. His effect upon climate in the large has mostly been unintentional or unintelligent, or has dealt with compen- sation, as by the long-distance transport of water for irrigation or urban needs, or the drainage of large areas. However, he is on the threshold of a new era in which the mastery of fallen rain will become more or less complete and even lead to the increasing control of actual rainfall by virtue of great coactions within the plant matrix of the various biomes. This will be brought about by the expanding knowl- edge of climaxes and succession, by which the latter may be widely employed as a unique tool for regulating runoff and erosion. The theme of man as a superdorainant and superinfluent is far too vast even to be outlined in its major features as a part of the present treatment, but some of the chief reactions involved are briefly touched upon in the following chapter. (Cf. Sears, 1937.) REACTION IN WATER Obviously, the change from air and soil on land to water and soil leads to divergence in the manner of reaction, even though the gen- eral processes of adding, subtracting, or modifying are essentially similar. For the most part, the soil becomes merely a substratum for attachment and for the accumulation of detritus, with the loss of its properties as a storehouse of nutrients and gases. At the same time, the air is replaced by a denser and less elastic medium, which must combine in large measure the functions of both media on land. This necessitates a great reduction in the amount of all raw materials in solution, both gaseous and mineral, as compared with soil, for which the slower movement of water provides but slight compensation. Con- sequently, whereas reaction on land centers about water content, in water it is primarily concerned with the amount and distribution of solutes, and suspended matter, and with circulation. Reactions in Fresh Water The transition from land to water reactions is particularly gradual in ponds and lakes, though a similar gradation occurs in estuaries and false bays. The first three stages of the hydrosere are characterized by three types of vegetation, viz., (a) submerged, (5) floating, and REACTION IN WATER 95 (c) emergent. These stages of the hydrosere may be assigned with ahiiost equal propriety to land or water, though developmentally they are an intrinsic part of land climaxes. Since this is largely an out- come of the shallowing effect of plant and animal matter, such accumu- lation has already been considered under land reactions. Reaction upon the medium belongs properly to the consideration of the w^ater. The same is true of influences on the bottom in sluggish rivers and the larger lakes with silt (terrigenous) bottom. The small floating plants and animals are properly considered in relation to both bottom and the medium itself. Small Lakes and Ponds Accumulation and Decomposition. In its general features, accumu- lation in shallow still water resembles that on land, marsh and swamp Pig. 19.— View in Little Barren (Mile 474, 760 kilometers from The Pas, Hudson Bay Railway), showing tundra vegetation over several feet of frozen sphagnum. (Photo by V. E. Shelford.) forming the connection between the two. However, there are several important differences, as is well known. One of these is that detritus is sometimes transported and deposited far beyond its place of origin, another that excrement plays a larger part in consolidation, and a third is the retarding of decomposition and the emphasis upon anae- robic processes. Furthermore, calcareous and chitinous skeletons may accumulate to the point of constituting a definite layer. The nature of the filling process is related to temperature and length of season and is different in different climates. Tundra may overlie deep sphagnum deposits resulting in part from failure of the dead plant bodies to decompose. An area of wet tundra is traversed by the Hudson Bay Railway, and the railway itself rests on frozen sphagnum extending to a depth of as much as 20 feet (6.4 meters) near the southern tundra edge and to 7 or 8 feet (2.3-2.6 meters) near Churchill. The difference in depth is related to topography; Fig. 19 96 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT shows the late stages in the filling of a depression, the Little Barren at mile 474 (Hudson Bay Railway). The filling of small lakes far- ther south, for example in the latitude of the Great Lakes of North America, is often accompanied by floating bogs, the deposition of marl, etc. (Transeau, 1905, p. 364, Fig. 4). Still farther south where decomposition is more rapid, the plant contribution to bottom deposits is most important in the zones of floating and submerged angiosperms. Some of this material is carried out into deeper waters as coarse fragments and detritus. Where the bottom is suitable, much of this material is consumed by crayfish, mussels, worms, insect larvae, fishes, etc., and further modified for incorporation in the deposit. Dead animal bodies, and excrement especially, often accumulate at a relatively rapid rate, A consider- able amount of material arises from the plankton. The phytoplankton and plant fragments quite regularly form a thin brown layer over depositing bottoms in summer, which afford residence for certain types of small organisms. Such deposits have long been studied by Swedish investigators, who have distinguished them especially on the basis of the amount of coprogenous matter in them (von Post, 1862; Naumann, 1929; cf. Gams, 1921). Finally, the bottom is the chief site of decomposition, which is due to the coactions of micro-organisms, but in its turn exerts reactions upon the medium. Reactions upon the Medium. These may operate upon light and heat, the color and transparency of the water, or much more signifi- cantly upon the materials dissolved in it. The penetration of solar energy may be modified by floating or submerged plants, such as Nymphaea, Lemna, and Potamogeton, by the plankton, or usually to a much less degree by the nekton. The first is a frequent result in shallow waters of temperate climates especially, but its importance relative to the aggregate surface of lakes is slight. The influence of plankton depends upon its abundance, being considerable at times of its maximum and of little effect at other periods. Both the quantity and quality of light are affected, the latter especially by the phyto- plankton. The paramount reactions upon the medium are the consequences of metabolism, in the course of which gases are exchanged and nutri- ents absorbed and returned, and of decomposition. The three proc- esses concerned are photosynthesis, respiration, and decomposition, the last involving also the respiration of bacteria. The role of plants in absorbing carbon dioxide and releasing oxygen, and of all living organ- isms in taking up oxygen and emitting carbon dioxide, is too well REACTION IN WATER 97 understood to require comment. However, the ability of green plants to utilize the half-bound carbon dioxide of the bicarbonates is not so generally known, nor is the important consequence in modifying the ion concentration of the water. The detailed reactions are closely related to the times and layers in which the processes occur and espe- cially to the annual cycle of the lake itself in terms of spring and autumn overturn, the relations of epilimnion and hypolimnion, etc. In general, the increase of oxygen and decrease of carbon dioxide pertain to the upper layer in which the phytoplankton is concentrated ; the zone of oxygen deficit is usually near the bottom where decom- position is often limited by the access of this gas. When this occurs, anaerobic processes result, in some measure at least, and a variety of gases may be produced, such as methane and hydrogen sulphide (cf. Birge, 1903; Birge and Juday, 1911). In general, reactions upon the mineral constituents, have to do with their abstraction by plants and their return through decomposi- tion. Related to this is the reciprocal conversion of carbonates and bicarbonates, especially of calcium and magnesium, the first change effected by the carbon dioxide released and the second by the de- mands of the phytoplankton when the free gas is low or absent. Plants alone react upon the medium by reducing the quantity of those minerals that provide essential constituents of the protoplasm, bub the demands of different families and genera are not the same. Thus, among plants, only diatoms reduce the amount of silica materially; they also make heavy demands upon nitrates, according to Pearsall (1922:248), while the reaction of desmids upon the nitrates is much less. Animal reactions by removal are due chiefly to shelled forms which exert their major influence upon calcium carbonate. For the most part, these minerals are carried to the bottom in the bodies of certain dead organisms and are there again rendered available by the decomposition reactions of bacteria in particular. In this process, soluble organic compounds are also produced. Streams Reactions upon medium and bottom are much reduced in streams, by comparison with lakes, owing to the fact that the current renders accumulation difficult and at the same time brings in new materials. At the same time the produccnt phytoplankton is less developed as a rule, and the total quantity of reactors is correspondingly less. As a consequence, the significance of reactions in streams depends largely upon the current and its swiftness, sluggish and swift streams being 98 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT quite dissimilar, though exhibiting various intergrades through mature rivers and "cutoff" lakes. Apart from man, the beaver is the one animal that produces reac- tions in streams on a large scale, though the damming and flooding are an outcome of a coaction. At one time this was a widespread effect of much importance, favorable streams often being converted into a succession of ponds wdth adjacent swamps, but today the reac- tion is practically confined to remote regions. Reactions in Swift Water. It is rare that either plants or animals produce reactions of any significance in rapid streams, though algae, aquatic mosses, and amphibious flowering plants may slacken or deflect the current locally. A number of fish bury their eggs in the loose gravel of moderately swift water, but with little or no significant effect. A characteristic minor reaction but likewise without impor- tant effect is the habit of larvae of caddis flies in binding together tiny pebbles and attaching the cases to the bottom. This may result in increasing the stable area to which other organisms may attach themselves, but it is quite transitory in nature. Reactions in Sluggish Water. As reactors, both plants and animals are of more importance in sluggish streams, the former sometimes affecting the slow current materially and both having some slight effect at least upon the gases and solutes of the medium. Their reac- tion upon the bottom becomes significant only where the current slackens to the point of permitting accumulation, but even in such places, except in baselevel streams, floods continually recur to sweep away the effects. The movements of mussels and snails tend to mix organic matter with the earthy bottom, and the nest-building fishes bury similar materials in the outer rim of the concave nests. Bottom- feeding fishes tend to stir the bottom materials and increase turbidity (see Chapter 9). These are often numerous along the margins of mature rivers, sluggish creeks, and ponds. Crayfish also burrow in such bottoms, bringing up terrigenous material and burying organic matter and other detritus. The reaction of animals which remove plants from the land and increase erosion is evidenced in streams and sometimes in lakes as increased turbidity. The clearing of the land and attendant increase in stream-borne silt has doubtless shifted the fish constituents of stream communities from the trout-bass type toward the buffalo- sucker type with attendant changes in the invertebrates. REACTION IX WATER 99 Reactions in the Sea Reactions in marine habitats closely resemble those of fresh water for the most part, but they are on a much larger scale, owing to the extent and age of the oceans. They also exhibit certain qualitative differences, due to the presence of halides in particular, and are much influenced by currents, tides, and upwelling. Accumulation of effects is regulated by the presence or absence of these to such a degree as to give further warrant to the grouping of marine reactions on the basis of tidal, benthic, and pelagic climaxes. Manifestly, these differ from one another more in degree than in kind of reaction, though each pos- sesses one or more typical effects, such as deposit in the case of benthos. As dominants, the animals are the chief reactors of the ocean, plants assuming this role relatively rarely. Tidal Areas Belt between Mean High and Mean Low Tide. Rocky intertidal areas, and areas covered with coarse gravel or strewn with boulders, are occupied by definite communities, in which barnacles are the chief dominants, associated with sea mussels, sea anemones, and often brown and red seaweeds. These react by virtue of attachment and density, holding water on the rocky surfaces and thus reducing the danger of drying during periods of exposure to the sun. Owing to the water-holding capacity of the bottom materials of sandy and muddy shores, the water withdrawal at low tide has a lesser effect than on rock. This is primarily influenced by the degree of water movement. Strands beaten by waves do not permit the accumulation of the typically small reactions, but in quiet backwaters, where mud and organic matter accumulate, fiddler crabs and various other invertebrates burrow in the substratum, or work it over in ways that differ little from reactions on soil; these communities represent succession to land. However, any area alternately exposed and sub- merged is of the nature of an ecotone between marine and terrestrial connnunitics. Littoral Benthic Belt. In protected mud-bottomed bays the processes are similar to those in lakes. However, on tide-swept rocky bottoms in the littoral belt (0-200 meters deep), great numbers of dominants occur in the form of large showy echinoderms, mollusks, coelenterates, and crustaceans. Relatively few of these are perma- nently attached to the rock bottom, and dredging and sampling show comparatively little skeletal material not belonging to living animals. 100 REACTION: THE INFLUENCE OF COMMUNITY ON HABITAT The general effect of such organisms is to roughen the surface of rocks and thus favor the attachment of Bryozoa, serpudids, barnacles, etc. In the pockets that frequently occur in such areas, the tidal cur- rents are retarded and the skeletons of animals may accumulate in considerable quantities. Shells of barnacles, sea urchins, snails, brachiopods, and bivalves frequently cover much of the surface and exist at considerable depth, in some places overlying layers of mud deposited earlier. Hence, the reaction of shelled animals is to produce a hard bottom suitable for the attachment of sessile forms on top of what was formerly mud or sand. In deeper pockets where the cur- rent is retarded still more, there occurs a deposition of organic matter derived from these animals, as well as from seaweeds. These are merely early stages of a process leading eventually to a hard bottom such as just indicated above. The attached plants that characterize faciations within these com- munities are probably less important while in position than botanists have been inclined to assume. They do produce comparatively dense shade, but their effect upon the carbon dioxide and oxygen content of the water is minimized by the rapid motion of the medium. Shade is a much less important reaction in water than on land, and hence such plants modify the habitat little with respect to animals, and the com- munities are little influenced by them. Their chief effect is probably exerted when they break loose and settle in pockets where they decom- pose and add to the matter accumulated there. Furthermore, when tissues of these plants are broken into fine material, they contribute to the total of suspended organic matter, which is of great importance in connection with the marine climate in different areas. Pelagic and Deep Benthic Areas Reactions on the Medium. The plankton and nekton exercise a far-reaching control over the physical and chemical factors of the marine climates. One of the most striking effects of the swimming and floating organisms, reinforced by organic detritus and silt, is the obstruction of light rays in the lower layers of the ocean and in bays and inlets. The reactions upon the gases dissolved in salt water are, in part, essentially the same as for fresh water. The resemblance extends to the decomposition of material on the bottom, excess of carbon dioxide, and deficiency of oxygen, etc. The occurrence of hydrogen sulphide under conditions of poor circulation and deficient oxygen is more char- REACTION IN WATER 101 acteristic of salt water. The results of the presence of quantities of this substance are several. Colloidal sulphur, which is the most toxic form, often occurs under certain hydroclimatic conditions and kills many of the existing aerobic bottom organisms. Hydrogen sulphide is also acted upon by a remarkable group of sulphur bacteria (John- stone, 1928:147), and a portion of it, after reaching water containing dissolved oxygen, is transformed into sulphur dioxide. This finally becomes sulphurous acid, which often occurs in minute quantities be- low depths of about 50 meters. Reaction also operates necessarily upon the mineral solutes, reduc- ing them as a consec}uence of food making by chlorophyll-bearing organisms, and restoring them through the oxidation exercised by bac- teria, especially the nitrifying ones. Calcium is utilized in large amounts by shelled animals, but the quantity present is constantly renewed by inflow from the land, so that its use is chiefly significant in connection with the reaction of deposit. The situation is quite dif- ferent with respect to nitrates, phosphates, and silica, owing to the relatively small amounts present, and the reduction due to utilization is frequently the limiting factor, both as to species and abundance. Finally, the organic matter in solution in sea water is an outcome of the presence of living organisms, and a somewhat similar reaction may be the basis for the appearance of growth-stimulating substances in the sea (Johnstone, 1928:165). Reaction on the Bottom in Deep Water. The most characteristic reaction upon the bottom of oceans is that of deposit, dead material being contributed by all the pelagic communities above and accumu- lating wherever currents are slight or lacking. Such deposits consist of organic detritus derived from most of the organisms of the sea and their excreta, with which may be mingled more or less terrigenous material, especially in the vicinity of coasts. The continental shelf and adjacent shallower waters are covered with terrigenous deposits of gravel, sand, and mud, but the greater part of the ocean floor is characterized by deposits chiefly of animal origin. From 2,000 to 5,000 meters, approximately, globigerina ooze is the most widely dis- tributed; it consists of the calcareous shells of Foraminifera living in the pelagic climax, and accumulates at the rate of about 2 milli- meters per year. Coral mud and sand occur in the neighborhood of coral reefs and islands, and pteropod ooze is often associated with them, though it develops also on oceanic ridges in warm seas. Radio- larian ooze is restricted to certain tropical waters; diatom ooze is con- fined to colder seas, both in the southern and northern hemisphere. The last two types, by contrast with the others, consist of siliceous 102 REACTION: THE IXFLUE^XE OF COMMUNITY ON HABITAT rather than calcareous material (cf. Murray and Renarcl, 1891; ]\Iur- ray and Hjort, 1912). In Danish waters, Petersen and Jensen (1911) have found that the surface layer of bottonr deposits is 1-2 millimeters in thickness and exhibits a distinct brown color. Petersen made a study of the brown layer and stated that it was composed of fine particles loosely aggre- gated so that the surface was fluffy in texture. In addition to some inorganic particles, it contained the following: (1) shells of diatoms; (2) fragments of tissue of higher plants; (3) chitinous needles and bristles; (4) a few living organisms, comprising bacteria, diatoms, and animals. The part played by excreta in bottom deposits is not definitely known, but it is probably very considerable and may warrant the frecjuent statement that such layers have repeatedly been passed through the alimentary canal of animals living at the bottom. Moore (1931, a, b) has studied the muds of the Clyde and found that as much as 40 per cent of the fine material was consolidated into fecal masses or pellets, though in extreme instances the mud was formed entirely of these. He estimated that these deposits were accumulating at about the rate of a half centimeter a year and that the pellets themselves might persist for a hundred years. The upper 5 centi- meters of mud represented the deposit of ten years and was very loose, with a high water content and a complete deficit of oxygen at the surface, while nitrogen and jihosphorus decreased with depth. As to their origin, the pellets were derived largely from worms, lamelli- branchs, and other bottom forms, though those of the plankton also played an important part, especially of Calanus and several species of euphausids. CHAPTER 4 COACTION: THE INTERRELATIONS OF ORGANISMS Nature and Significance. As has been indicated in Chapter 2, all the activities of the biutic community may be summed up in the action of the habitat upon the organisms, the reaction of these upon the physical factors, and the coaction of the organisms upon each other. In a general sense, the word interaction has been applied to some of these (Forbes, 1880, a) , but the need for exact analysis renders the use of reaction and coaction all but indispensable (cf. Clements, 1916, 1926) . The latter is made peculiarly necessary by the concept of the biome and the consequent dropping of the term biotic factor. The word coaction is especially fitted to designate the enormous range of interactions among plants, plants and animals, and animals alone, since it involves not only the idea of acting together, but also that of urging or compelling. Although the three processes of response, reaction, and coaction are usually sharply delimited, the last two in particular are often closely associated and hence may seem confused. Such a food coac- tion as that of the mole brings about reaction through disturbance, and this may modify the plant matrix, which is usually not directly concerned in the coaction. Similarly, the reactions of a prairie dog in digging its burrow may destroy, stimulate, or change the plant cover, ciuite apart from its consumption as food. The material-shelter coac- tion of the beaver involves a minor reaction in the use of mud, a major one when canals are dug to transport logs, and a combination of coaction and reaction in the destruction of vegetation and modification of the habitat as the consequences of flooding. It has previously been pointed out that the control exerted by land plants is primarily a matter of reaction and related competition, leading to various degrees of dominance and subordination, and that animals enact a somewhat similar role in river, lake, and ocean. By contrast, terrestrial animals usually exert their major effects through coaction, with the resulting gradations in influence. In consequence, it is coaction that constitutes the chief bond in the biotic connnunity, both on land and in water, but on land especially, while reaction is 103 104 COACTION: THE INTERRELATIONS OF ORGANISMS the characteristic process in the plant matrix. Thus, in the study of the biotic community as distinguished from that of separate plant or animal communities, coaction is commonly a paramount theme, though it is regularly to be considered in proper relation to other community functions. BASES OF COACTION Organisms. In its simplest form, each coaction comprises the reciprocal behavior of two individuals of the same or different species ; the more complex coactions involve the interaction of one group or community with another. These may consist of plants or animals alone, or more rarely of both acting together. In the main, the gen- eral nature of each particular coaction is determined by the life form and life habit of the species concerned. The specific quality of this relation is usually derived from behaviors common to families, or genera of animals ; this is frequently true of plants also, but only when life form and taxonomic form are in accord. It is the exception that the organisms concerned in a coaction play equal or similar roles, though this may frequently be true of social interrelations. As between animals and plants especially, the former are largely active, the latter passive. The difference is usually one of motility, though not necessarily so, unless to this is assigned the movement of food-gathering cilia, tentacles, etc. The distinction is primarily one of initiative, the herbivore, for example, being the agent that acts upon the plant matrix or some portion of it. This essential relation is maintained even by plant parasites upon animals, in spite of striking disparity in size and motility. With further use of the term coaction, it may prove desirable to distinguish between the two roles and to designate the initiating or directing organism as the coactor and the receiving one as the coactee. In the large majority of coactions, especially on land, animals take the one part and plants the other, but the behavior is sometimes reversed. In many social and symbiotic relations, the coactive organisms may exhibit more or less parity in behavior, or at least in values received. Such is the situation in a flock or herd where the members are of the same species, and it obtains likewise in certain mixed herds of mammals. Much more striking instances are to be found in the symbiosis of microscopic algae with such animals as Stentor or Hydra, or such plants as Cycas, of bacteria with legumes, and fungi with the roots of orchids, as well as many trees. These are all mutually beneficial, but the transition to pure parasitism is so gradual that no BASES OF COACTION 105 definite line can be drawn between the two types of coaction, the lichen being a case in point. In groupings of two or more species, such as certain ant colonies, the line between symbiosis proper and parasitism is e^'en more vague. Objective or Purpose. It is sufficiently obvious that the most uni- versal of coactions are concerned with shelter and food, directly or indirectly. It is impracticable to evaluate the various coactions as to relative importance, especially in general terms. The food relations of the bottom fauna such as occur in the Danish waters are not all significant coactions in the community, for many species feed largely on detritus of remote origin. However, when these same species are studied in other localities, their food relations take on more of the character of community food coactions because they secure more food from the living and dying plankton organisms. In the propagation of game birds, four essential conditions have usually been noted, depending upon the circumstances, namely: (a) cover or covert defined as shelter, (6) food, (c) suitable nesting con- ditions, and (d) suitable climate. The last, though referring princi- pally to the absence of extremes unfavorable to the species in question, operates with reference to food and shelter and should rarely be con- sidered independently of these relations. The enumeration of needs of game, especially of deer and ciuail (Leopold, 1933), makes clear that certain relations ai'e direct responses to habitat factors, and not coactions or reactions in the strict sense. The deer requires open spaces to play, and the quail selects sparse cover on a well-drained spot with bare ground near by, where the young may dry out after a rain. It is difficult to evaluate food, shelter, nesting and breeding site, social relations, etc., in comparative terms, because they operate in accord with the general principle of Liebig's law of the minimum, which is equally applicable to maxima, as extended and restated by Shelf ord (1913, a) as the law of toleration. In addition to operating in this manner, the amount and kind of food and shelter, especially with reference to specific requirements, vary with weather, climate, and the presence of other organisms. In all studies of relations of species to community and environment, it is necessary to seek a proper bal- ance among these factors and resist the general tendency to over- emphasize one or two. Food coactions have been more often studied than other relations, and there is a large volume of records as regards organisms of economic importance from which stomach contents can readily be obtained and preserved in fluid. This has naturally limited the studies to medium and small animals, such as birds smaller than 106 COACTION: THE INTERRELATIONS OF ORGANISMS the prairie chicken, mammals smaller than the fox, fishes smaller than the full-grown carp, etc. In addition to this, scatology, pellet study, and the observation of browsed plants have contributed important results for a few of the larger forms. Among higher forms occur the various reproductive coactions, in- cluding those of the family as such, which necessarily lead to certain types of social interaction. Naturally, they are likewise part of a composite coaction that includes home making or the securing of food, and they are often combined with disturbance reactions. Out of these basic coactions arise a variety of secondary or correlated ones, more or less distinctive in character but constituting only one feature of a behavior sequence. Such are hunting, storing, combat for the purpose of securing food, materials, territory, slaves or mates, defense and protection, courting, communication, play, etc. In their expression, these are largely an outcome of life form, life history, or life habit, and their development has led to a further specialization of behavior in particular genera and families. Consequences of Coaction. In a broad sense, all interactions be- tween organisms may be characterized as helpful, harmful, or destruc- tive to certain species, to the community as a whole, or to man's selfish interests, though there are many degrees of each, and consequent gradations between them. Quite apart from the inequality of coactor and coactee, moreover, is the fact that the same process frequently produces both helpful and harmful effects. This is notably true of aggregation, in which the consequences may be beneficial or injurious to the species concerned, or the two may be combined in varying degree. When the first outweighs the second, the result is coopera- tion in some measure ; if the scales are reversed, the outcome may well be termed disoperation. This comprises several types, of which com- petition is the most important, ranging from mere subordination or displacement at one extreme of efi'cct to complete destruction at the other. In respect to individuals, destruction is the typical outcome of food coactions, though this may often affect only parts of the coactee. It is but infrequently the result of coactions involving materials, such as those of leaf-cutting ants and the beaver, but with the noteworthy exception of man as a superinfluent. However, even with respect to food, it is evident that symbiosis and slavery exemplify cooperation, often in a high degree, while the destruction wrought by saprophytism is secondary and of a very different type. Parasitism runs the whole gamut from relations that involve at least a modicum of cooperation through an ascending series of disoperations that terminate in the de- BASES OF COACTION 107 struction of the host. In the last case especially, it is worthy of note that the effect is often exerted upon an individual by a simple com- munity of countless members. Direct and immediate, though often partial, destruction is the gen- eral basis of food coactions, best illustrated by the consumption of a smaller coactee by a larger coactor. This interaction embraces such widely different types as the eating of a diatom by an amoeba, the engulfing of quantities of plankton by baleen whales, the capture of a rabbit by a fox, or the eating of water lilies by a moose. Though disparity in size is the rule for eaters, there are striking exceptions in which inequality in size is compensated by number, as with a pack of wolves, or by specialization, as in crotalid snakes and mustelids, for example. Role in the Biotic Formation or Biome. The universal role of coaction is to be seen in the integration of plant and animal relations to constitute an organic complex, which is characterized by a certain degree of dynamic balance in numbers and effects. Obviously, such a balance undergoes a variety of rhythmic changes at different inter- vals, and is never exactly the same after a period of stress (Chapter 5). Nevertheless, it represents a general process of compensation and ad- justment, in which extreme or permanent departures stand out more or less vividly. Hence, it appears entirely desirable to speak of dis- turbances of dynamic balance in the biome, which arise from an emphasis of one or more of the normal coactions. While it is true that at present little is known of the causes and detailed course of such phenomena, this condition is certain to be remedied as the meth- ods of quantitative ecology are focused upon them (cf. Forbes, 1880, a; 1883, a). The nature of the coactions involved in aggregation and competi- tion is reserved for discussion in the next chapter, and it will suffice to point out here certain examples of abnormal intensity which, though not the rule, are far from infrequent. Naturally, the most numerous and important of these have to do with man or his agents, as a consequence of which fire, lumbering, or clearing removes the climax or subclimax in whole or in part and initiates succession. As an indirect human coaction, grazing is usually less thorough in its effects, bringing about modification in various degrees but rarely to the extent of complete destruction. Direct coactions between man and animals also cause changes in abundance and composition by reason of such activities as hunting, fishing, and poisoning, sometimes result- ing in practical extermination over larger or smaller areas and the setting up of a new sequence of effects (Fig. 20). Opposite to these 108 COACTION: THE INTERRELATIONS OF ORGANISMS in character, but similar in producing a new chain of coactions, is the introduction, intentional or otherwise, of exotic plants or animals. In the case of cultivated plants and weeds, this coaction has played the paramount role in every agricultural region, as a sequel to the coac- tions concerned in clearing of land of all kinds. It is likewise seen in the introduction of domestic animals, or of such semi-feral ones as the rat, English sparrow, and numerous insect pests, as well as in that of disease-producing organisms, both plant and animal, of which wheat rust and the bacillus of cholera are examples. — — Wildcat Deer Wolf " " Gray Fox ^^^■^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^H ^^^MB ^^^WHHHmm^mn^^Bi^BB r- II III 1800 1810 1820 1830 1840 1850 1860 1870 1880 1890 1900 1910 Fig. 20. — Showing the effect of settlement on the mammals of central Illinois. The decline of the Wildcat, Lynx rujus (Schreb), and wolf, Canis nubiliis Say, early reduced by trappers and first settlers, was accompanied by an increase in deer, Odocoileus virginianus (Bod.). The gray fox continued in full numbers until about 1850-1860. The decline of this species and of the deer was probably due as much to destruction of the forest habitat as to hunting. (After Wood, 1910.) IModifications of the community by native animals are less wide- spread and on a smaller scale as a rule, but are essentially identical in nature. The grazing coaction of antelope and bison probably dif- fered only in degree and perhaps in slightly different preferences from that of cattle on the open range today. The aggregation of cer- tain rodents in "towns" produces more serious effects, though these are too local and restricted in area to modify the climax materially. Most striking of all such coactions are those caused by grasshoppers in migration, which sometimes leave hardly a vestige of field crops. Successive defoliations by caterpillars have been known to cause the death of an aspen subclimax over many square miles of mountainside SYSTEMS OF COACTIONS 109 (Fig. 21), and similar consequences may follow infestations by other epidemic or endemic insects, notably twig borers and bark beetles. Fig. 21. — Aspens killed after three successive years of defoliation by the larvae of a noctuid moth; Pikes Peak, Colorado. (Photo by Edith Clements.) SYSTEM OF COACTIONS Since processes take the leading part in a dynamic system, the primary division is made upon this basis, as follows: (1) shelter and housing, (2) food, (3) materials, (4) reproduction, (5) social group- ing, and (6) attachment. The logical subdivision of these is first with respect to -the active agent (coactor) and second with reference to the passive organism (coactee), but the difference between land and water is such as to warrant a preliminary grouping into land and water communities, those of the latter being treated incidentally in the chapters on aquatic climaxes. Among coactors, animals are first con- sidered because of their vastly larger number and importance in this 110 COACTION: THE INTERRELATIONS OF ORGANISMS role, followed by plants and then by those partnerships in which each plays the part of coactor in some measure. Coactors differ chiefly in habit and form, which are usually related to the various types of coac- tion. This is true to a large degree of the inactive agents (coactees) likewise. Plant coactees may conveniently be subdivided on the basis of the organ or part used for food, material, shelter, etc. Figs. 22a and b. — A nest of the hooded warbler (Wilsonia citrina, Bod.) show- ing the use of forest floor leaves in construction. Both are of the same nest, built in a small .sprout of tupelo, 32 inches from the ground. The long slim crotch is filled with a loose wad of dead beech leaves upon which the real nest is built. The neatly compacted rim of dead beech leaves is bound in place with strips of the inner bark of chestnut, of which a plentiful supply is available owing to the activities of the "chestnut blight." The lining is of finely shredded strips of grapevine bark — quite hairlike in character. This nest was so well done from the standpoint of camouflage that one could look directly at it without perceiving its nature. (Photo by Arthur B. Williams, Cleveland Museum of Natural History.) In number, coactions are practically countless, and all that can be attempted in a preliminary organization of this vast field is to pass in review the frequent, typical, or outstanding examples and to relate these to the community life of the biome, so far as this is feasible at present. In this connection, composite interactions involving more than two species as individuals and especially as groups are peculiarly SHELTER AND HOUSING MATERIAL CO ACTIONS 111 significant, but these are naturally more complex and at present less understood. SHELTER AND HOUSING MATERIAL COACTIONS The importance of plant shelter has been emphasized chiefly in connection with game management, especially that of game birds. Fig. 23 Fig. 24 Fig. 23. — Meadow mouse (Microtus drummondi, A. & B.) runway at Churchill, Manitoba. The run stands out most clearly where it passes through the water in the center of the upper section. It also shows as a dark area at the right center of the lower section where it passes through dense sedges at the margin of the depression. (Photos by V. E. Shelford.) Fig. 24. — Woodpecker, Colaptes chrysoides (Malh.), holes in Cereus giganteiis, Tucson, Arizona. (Photo by Edith Clements.) Plant cover for shelter during sleep and rest, and during summer heat and winter cold, is a major requirement for game production, and especially for the nesting period. Leopold (1933) describes these in detail for the quail, and brings out the importance of the right density of cover to permit taking flight, of bushes of the forest-edge habitat of the quail to afford refuge when snow is deep, and of open grasslike 112 COACTION: THE INTERRELATIONS OF ORGANISMS vegetation for nesting. In game management, diversity of cover suited to the various needs favors large populations. The small non-burrowing mammals select various types of cover. The snowshoe rabbit prefers a small woody growth so thick that foxes and wolves cannot travel through it with ease. The desert plains blacktailed jack rabbit finds shelter in the mesquite and buck brush and may seek food at some distance. Larger animals also seek shelter in vegetation; the moose frequents dense coniferous forest in winter and hides the young in alder thickets. The great cats, such as Fig. 25 Fig. 26 Fig. 25. — Ravens {Corvus corax sinuatus Wag.) build a nest of old barbed wire in the "Dust Bowl" where other materials are scarce; Dalhart, Texas; 1935. (Photo by Edith Clements.) Fig. 26. — Nest of a lark sparrow {Choiidestes grammacus strigatus, Swains.) made of grasses in mixed prairie near Scotts Bluff, Nebraska. (Photo by Edith Clements.) the jaguar (Bailey, 1931), commonly take refuge in brush thickets. Small rodents, notably Microtus, hide in the grass cover, making run- ways from place to place. Many small ground birds, particularly those nesting in swamps and low ground, take full advantage of the vegetative cover in selecting nesting sites. Even the burrowing mam- mals such as some species of kangaroo rats and ground squirrels prefer to burrow under shrubs, while the nine-banded armadillo selects the center of a thicket or a group of trees for its burrow. The importance of shelter has further been brought out experi- mentally by Gause (1934), who found that paramecia are able to SHELTER AND HOUSING MATERIAL COACTIONS 113 maintain themselves against protozoan predators when cover was provided. The importance of eelgrass in connection with young fishes in the sea is discussed in Chapter 10 (page 336). Home building, with a few exceptions among burrowers, involves the selection of materials which are nearly always parts or products of plants or animals. Burrowers and ground-nesting species com- monly line their nests or breeding chambers with grass or grasslike fibers, sometimes supplemented with hair or feathers from the builder's Fig. 27. — Banner-tailed kangaroo rat (Dipodomys spectabilis Mer.) burrows under mesquite {Prosopis juliflora). (Photo by Edith Clements.) own body. Ground birds commonly choose sites arched over by grasses or forbs. Animals that build nests in trees and shrubs employ a great variety of materials, and the use of the tree or shrub is in itself a coaction. Usually fiber from bark or the stems of forbs, grasses, or sedges, often mixed with leaves from the trees concerned, are employed by the smaller species. The gray and fox squiiTels make summer nests or platforms of green twigs with leaves, and certain apes and lemurs have similar habits. Many of the larger birds use sticks to make a nest platform on the limbs of trees or other high points (Figs. 22 and 25) . A number of insects fasten leaves together to make tem- 114 COACTION: THE INTERRELATIONS OF ORGANISMS porary nests. Examples of this among lepidopterous larvae and spiders are common. (See Figs. 25, 26, and 27.) The trunks of trees when hollow afford home sites for small mam- mals, reptiles, and insects. Comb-making bees often utilize such cavi- ties. A goodly number of Coleoptera and a few Lepidoptera and Hy- menoptera burrow into dead wood, which serves as shelter and for most of the insects it also supplies food. The larvae of click beetles and the larvae and adults of rove beetles, ground beetles, etc., which also are predatory, find shelter in dead wood. A few Hymenoptera make tunnels into wood in which to lay their eggs, but they are not important as regards influence. REPRODUCTIVE AND SOCIAL COACTIONS The reproductive coaction involves mating or the fertilization of the eggs, which calls forth aggregations of individuals. The swarming of marine worms is one of the outstanding types of assemblage for the Fig. 28. — Defense circle of the musk ox {Ovibos moschatus Zim.)- It is an excel- lent defense against wolves and also affords protection to the young. (Sketched from a photograph by D. B. MacMillan in a report by American Committee for International Wild Life Protection, 1934.) lower invertebrates; this brings individuals into close contact and permits fertilization of eggs cast into the water. In terrestrial commu- nities the choosing of mates, sometimes accompanied by fierce contests between males, is a well-known coaction. The care of young is often of much greater importance in the com- munity than nest building in itself, as it involves a greater drain on the food supply. This is especially true among birds, which collect enormous amounts of animal food to nourish their rapidly developing young. The hiding of the young by many mammals is important and varies as to method. Certain rabbits secrete the young individually, the litter being scattered about; this is usually a shelter coaction. The FOOD COACTIONS 115 teaching of the young to fly and hunt food is among the important coactions of birds. The gregarious habit so common among the larger mammals in tundra, grassland, and savannah affords protection from enemies, especially for the young, and constitutes a simple form of cooperation, as in the case of the musk ox (Fig. 28). Social coactions in food getting are exemplified by the wolves, which aggregate in packs for community hunting in the winter and follow more or less regular WOLFITRAILS AND DENS Sfiganaga ^\ % Wolf Trails • Dens ^^■^^ National Forest Boundary I— I— I— I Main Travelled Wolf Trails Fig. 29. — Wolf pack routes in the Suporior-Quctico area. The long axis of ellipse A is approximately 55 miles (89 kilometers), B is 95 miles (153 kilo- meters), and C is 60 miles (97 kilometers). (After Olson, 1938, a, b.) routes that bear a close relation to dens or homes (Fig. 29). These gregarious habits tend to make both reaction and coaction intensive in some areas and consequently irregular in pattern. The detailed descriptions of aggregation and herding in both small and large ani- mals are easily available in the well-known treatise by Allee and hence do not require further discussion. FOOD COACTIONS Elton (1927:56) employs the term "food chain" for a sequence of such coactions and refers to all the food chains in a community as the "food cycle." In view of the specialized use of the term cycle, food nexe {nexus, tie, bond) appears preferable for the interwoven 116 COACTION: THE INTERRELATIONS OF ORGANISMS pattern of food chains, especially because of its basic significance in the biotic community. It further seems desirable at present to employ the term for any particular grouping of food chains rather than all those of a community, owing to the vast number at present in an extensive community. In the treatment that follows, an endeavor is made to keep the dynamic viewpoint constantly to the fore. The chief purpose is to present a flexible arrangement that can be utilized to reveal the signifi- cance of each process in the working of the community as a whole. The length to which food '?oactions are discussed is not to be con- strued as indicating an importance greater than shelter or other coac- tions, but rather that the extensive available facts have been brought together and classified to form a pattern for the study of other coactions. The plant population changes more or less completely with each stage in succession on land. For a number of stages, the species in- crease steadily and there is a corresponding increase in the variety and amount of shelter and food produced. In grassland, this may continue into the climax, but as a general rule, and particularly in coniferous forest, there is a marked reduction in both quantity and variety as the climax is approached. The usual consequence is a similar decrease in the kind and number of animal consuments, so that climax forests are often peculiarly monotonous in terms of bird and mammal or even insect influents. Conversely, the subclimax areas are relatively rich in major influents because of the great variety of shelter and materials, as well as food. Hence, it is sometimes both desirable and convenient to refer to food nexes as climax or serai when significant differences exist between them. ANIMALS AS ACTIVE AGENTS (COACTORS) The major distinctions between animal coactors are founded upon taxonomic life forms primarily, often with important subdivisions on the basis of life-history stages, as in metamorphic insects, and of behavior types such as are found in many groups. With respect to community significance, the general classification into herbivores (phytophaga or plantivores), carnivores, and omnivores assumes new meaning, but at the same time must be carried further in order to provide more definite pathways through the labyrinth of coactions. Choice of Food. With respect to the selection of food, it is helpful to begin with the organism as it comes into free existence, whether through hatching, birth, or transformation from other stages. Such PLANTS AS PASSIVE MEMBERS (COACTEES) 117 organisms usually soon begin to take food, picking up all sorts of material and rejecting those that are distasteful or painful (Holmes, 1911). After a few trials, rejection takes place at sight without test- ing, the animal selecting only those objects that serve as nourishment, and thus quickly learning to distinguish food from all other things. However, many adult insects in particular render such learning un- necessary by laying their eggs on the very material that is to supply food for the young. Some adults, that in the larval stage were forced to feed upon strange food, have been found to lay eggs upon this same substance. Frequently, larvae that have started to feed upon a plant selected by the female moth will not change to another host plant (Picket, 1911; Brues, 1920, 1924). The general principle is that organisms show a preference for a certain kind or kinds of food, which may be selected from a considerable range of materials. Such a choice may be exercised between groups of various kinds, e.g., between species, or organs of food plants. PLANTS AS PASSIVE MEMBERS (COACTEES) The animal coactors of this group may well bear the collective term of plantivores, since the more familiar word herbivore is neither defi- nite nor inclusive. However, it is evident that such a designation is often to be employed in a relative sense for animals whose food is largely but not wholly vegetable, and hence differ only in degree from omnivores. Plantivores sometimes select their principal food from the dominants of a biotic community. Thus, insects on a fioodplain feed in general on a variety of trees, though each kind usually prefers but one or two species of the fioodplain dominants (Felt, 1906). By con- trast, the salt-marsh caterpillar {Estigmene acraea Drury) feeds on 140 different species of herbs (Folsom, 1922). Metcalf (1924) has shown that certain leaf hoppers feed on the plants present where the physical conditions are suitable. A number of Phytophaga are confined to plants belonging to a single family, a preference for willow and Cottonwood being not uncommon (Folsom, loc cit.; Brues, 1924). A striking instance of a similar predilection is furnished by the potato beetle, Leptinotarsa, which passed from the wild Solarium rostratum to the cultivated S. tuberosum to become one of the generally distrib- uted North American pests. The general relations of a pure phytophagous group to its food plants is well illustrated in a recent monograph of the aphids or plant lice of Illinois (Hottes and Frison, 1931), which includes a discussion of 251 species and varieties. Since the food plants and much of the 118 COACTION: THE INTERRELATIONS OF ORGANISMS life histories were known, a compilation of food habits was made from this monograph. Eleven species were thrown out because of restricted catches of new species, or because the host plant was unknown, etc. The percentages of the 240 species considered are shown below: Per Cent A. On food plants belonging to more than 10 genera 2 B. On food plants belonging to 2 to 10 genera 31 C. Only genus named — several species implied 30 D. Genus and one or more species cited 10 E. On a single species 27 100 The food plants of some of these in the last category are known only in Illinois, and thus the percentage in the last item may be very materially reduced with further study throughout their range. In gen- eral, there is a considerable number of coactors that are confined to a single genus or even species of host plant, though the general flexibility of food relations suggests that all supposed instances of such restric- tion demand especially careful and thorough investigation. Seeds and fruits are particularly subject to attack by many species of birds and some small mammals and numerous insects, by reason of the relatively large amounts of food stored in them, but roots, subterrene shoots, stems, leaves, and flowers are each the object of a host of coactions, especially on the part of insects and a few birds. Further distinctions may arise from the nature of the tissue con- cerned, as in woody or herbaceous stems, the pith of a sunflower, or a stone, seed, or pulp of a fleshy fruit. Finally, either living or dead parts of tissues may be utilized, and sometimes this difference in con- dition is immaterial to the coactor. In addition to the central coaction of eating, there are a number of related processes such as collecting, harvesting, storing, and planting. These may be simple and general in character, as with most of the animals concerned, or they may be highly specialized, as with the harvester ants and the fungus cultivators. So far as these are perti- nent to the present treatment, they will be considered under the respective groups. RELATIONS OF FOOD COACTIONS TO THE COMMUNITY A proper ecological approach to the study of food coactions is one that brings out the community interactions. The investigator first learns what foods are present and the quantity of each in the com- munity or communities which the coactor frequents, and then pro- GRAZING AND BROWSING 119 ceeds to determine the items selected from the available food and the quantity in which each is taken. The work of Petersen, Blegvad, and others at the Danish Biological Station is the most thorough of this type, and is discussed in connection with coactions in the sea. Baker (1916) did some similar work in fresh water, but wuth refer- ence to Mollusca. Bird (1930) made community observations rela- tive to the food of a few birds, but the terrestrial studies in general, even some of the more recent ones, lack the full force of the bio- ecological viewpoint. For example, proportions of the different types of plant or animal food may be given, but the relative amounts of each on the range are not indicated. The presentation of coactions from the viewpoint of taxonomic groups, illuminating as it may be to the general biologist trained in this manner, also fails to stress the bio-ecological viewpoint. In addi- tion, it may fail to take account of variations in habits among related species. The American bison {Bison bison L.) is a grassland animal grazing by preference; the closely related European species {Bos bonasus) is a forest dweller, living by browsing. Again, some Carni- vora, for example, the small meerkats in South Africa, have the food habits of prairie dogs, and the small tree hyraces (ungulates) those of raccoons, (cf. Lydekker; he calls the American Bison Bos americanus). GRAZING AND BROWSING As previously suggested, there is no definite line between the graz- ing and browsing habits. Not only do nearly all grazing animals browse in varying degrees, but there is also no clear-cut distinction either in the original meaning or the current usage of the two words. Moreover, forest undershrubs may be grazed practically like grasses and forbs, while tall herbs are often browsed as though they w^re shrubs. Even more significant is the fact that some ungulates may graze in the summer and browse in the winter, that they may change their food plants as a range becomes overgrazed, or their food habits as they pass from one serai stage into another. In spite of all this, however, nearly all ungulates manifest a distinct preference for one type of behavior or the other (cf. Farrow, 1925). Grazing Life Habit Grazing animals fall into three classes, arranged in the order of their importance: (a) large cursorial grazers; (6) small grazers resi- dent underground; and (c) small grazers resident among the grasses. Large Tramping Grazers. The most representative grazing animals 120 COACTION: THE INTERRELATIONS OF ORGANISMS of North America are the bison, pronghorn antelope, musk ox, and tundra caribou. The first three prefer grasses and sedges; the tundra caribou seem to favor lichens, grass, and forbs. Elk, deer, sheep, and goats may shift according to the conditions from the grazing habit through various combinations to a browsing coaction, or the reverse. Quantitative studies of the food coactions of feral grazing animals have been rare, and the scattered observations are for the most part incomplete and undependable. Even the few examinations of stomach contents leave much to be desired, owing to inherent difficulties and the scattered nature of the observations. There is an increasing body of knowledge as to the food habits of domestic cattle, sheep, and goats, all of which are unfortunately of European or Asiatic origin, and some of the observations are both quantitative and specific as to plants used. This knowledge will be steadily augmented by the experimental installations now in existence at the several range reserves and grazing experiment stations. However, these need to be supplemented in detailed manner by extensive observations on the actual process of grazing in terms of life forms and species, closeness of cropping, sea- sonal preference, etc., with reference to the most important wild ungulates. The observed effect of grazing coactions upon the plant matrix is primarily an outcome of the selection and utilization of the con- stituent plant species by domestic animals. Every association of the grassland climax in North America has been thus modified, some of them in most striking and puzzling fashion as an outcome of the choices of domestic stock, but the results of grazing by native animals cannot be expected to be the same. Similar modifications have oc- curred in grassland the world over. Probably the best-known example of such a modified community, viz., the "short-grass plains," was long supposed to be climax in char- acter (Pound and Clements, 1898; Clements, 1920, 1922). Similarly, the bunch-grass prairie of California has been converted almost en- tirely into an associes of annual grasses, chiefly Avena and Bromus, while the true prairie of the Middle West has been largely transformed into a tall-grass postclimax of Andropogons. Under more intense grazing pressure, the grasses have yielded to dominants of adjacent scrub climaxes, such as Artemisia or Larrea, to consocies of such un- dershrubs as Gutierrezia and Haplopappus, or have been replaced by introduced annuals like Salsola. Thus, each kind and degree of overgrazing produces its proper indicators, and in consequence it is possible to reconstruct the history of a range by the indicators that characterize it. GRAZING AND BROWSING 121 Small Grazers Resident Underground. This group includes notably the prairie dogs, marmots, and conies in North America. Grasses and forbs are also taken by certain species of kangaroo rats, ground squir- rels, etc. There is no universal connection between subterranean habit and grazing, but the animals of this group exhibit such a correlation as an important feature of their community relations. Prairie dogs Total Protection PLOT Prairie Dog PLOT Cattle Grazed PLOT Fig. 30. — Fall clippings of blue grama (Boutcloua gracilh) in grazing exclosures at Williams, Arizona. The pile labeled "cattle-grazed plot" is from the open areas where both cattle and prairie dogs grazed. (After Taylor and Loftfield, 1922.) crop herbs and also dig them out, their choice being somewhat the same as that of the native ungulates and domestic animals. Marmots (Marmota) usually choose forbs rather than grasses, owing to their general relation to forest regions, while conies graze and store herbs of all kinds. Another important characteristic of this group of grazers is the occurrence of quiescence in many species during unfavorable seasons. This takes them out of competition with the large grazers 122 COACTION: THE INTERRELATIONS OF ORGANISMS which must eat dead grass and forbs, frequently digging away snow to secure them. Taylor and Loftfield (1922) have measured the coaction of the prairie dog, Cynomys gunnisoni, in northern Arizona in connection with the grazing exclosures and found that this species may destroy as much as 80 per cent of the total potential annual production of forage where the vegetation still persists. Under extreme conditions of crowding, prairie dogs may consume the entire cover and be forced to move elsewhere. Many social burrowers, especially those that form "towns," often bare the surface more or less completely; this is also true in a large degree of the solitary kangaroo rats (Vorhies and Taylor, 1922) and in some measure of the ground squirrels when closely aggregated. Pound and Clements (1898:414) pointed out the characteristic dominants of the extensive "dog towns" in western Nebraska, and the changes involved have been traced in greater detail in and about the grazing exclosures mentioned above (Clements, 1919). Similar stud- ies have been made of the areas denuded by kangaroo rats in the grassland and desert scrub climaxes of southwestern Arizona, where the destruction of the cover is sometimes complete (Clements, 1920:90; 1928:297). Small Surface Resident Grazers. In this group are included rab- bits, mice, etc., which feed on green grass and forbs in summer and their dead tops in winter. The principal animals of this type in North America are voles and jack rabbits. In localities where shrubs or cacti occur, jack rabbits may feed on these in winter or during drought periods. However, it must often be necessary for them to eat dry grasses, though the food records are few as yet (Vorhies and Taylor, 1933). Certain gallinaceous birds may belong here also, but nearly all those that graze do so only for a portion of the year and then not exclusively. In addition to those whose activities have been described, various omnivores such as squirrels, most ground squirrels, many mice, porcu- pines, some^ foxes, and birds compete with the large grazers in a minor way. However, phytophagous chewing insects are often more important in the destruction of herbaceous plants in competition with grazing mammals. This is most strikingly true of grasshoppers, which in general are most abundant in grassland areas, where grazing is the prevalent coaction. GRAZING AND BROWSING 123 Browsing Life Habit This coaction type characterizes chiefly the large mammals (ungu- lates) and some of the larger birds and rodents that inhabit the forest. In North America and probably elsewhere, browsing is the primary coaction during the season unfavorable for plant growth. It alter- nates with grazing of aquatic plants, forbs, fungi, etc. (mainly mam- mals), and with scratching for small ground animals or seeds (some birds). In the coniferous forest of North America, the moose browses chiefly on deciduous trees and shrubs, especially in winter, but eats aquatic plants and some herbs in summer, while the Shiras or moun- tain moose apparently browses the year around. The woodland cari- bou uses lichens in winter and browse similar to that of the moose during the remainder of the year. Likewise, various rabbits and the Hudsonian spruce partridge browse on the growing tops of spruce seedlings or trees, and the ruffed grouse eats buds of deciduous shrubs and trees. The effect of this on the plants is not unlike light browsing by large mammals. The tassel-eared squirrels feed on the bark of terminal twigs (Figs. 31, 32). Deer browse regularly, but in favorable seasons they may also consume large quantities of mushrooms and sometimes forbs. The elk possesses the ability to live both in open forests with grassy parks and in savanna areas, and at one period it ranged across the northern part of the Great Plains. It divided its time, seasonally and daily, between the timber along the streams and the open prairie (Bailey, 1926). Elk browse at all seasons, but especially in winter; they also eat all kinds of herbs, including much grass, thereby differing from the deer. Rabbits browse in the unfavorable season and also take bark from woody plants; the porcupine is similar in this respect but more arboreal, eating the bark at some distance above the ground. Squir- rels, especially the red squirrel, nip off the end buds of conifers in a similar manner (Hatt, 1929). All these rodents resemble the deer in taking herbaceous plants in the growing season, and consequently compete with ungulates in grassy parks as well as in wooded areas. Defoliation and Bud and Twig Injury. This is chiefly the work of insects and arachnids; the lepidopterous and hymenopterous larvae play an important role. In the coniferous forest, the hemlock looper, spruce budworm, and larch and jack pine sawflies are of some small importance in competition with the browsers. The subclimax decidu- ous trees are at times defoliated by sawflies and moth larvae. In the deciduous forest, the cicadas, twig girdlers, and twig-boring beetles have somewhat the same effect as the browsers, but native defoUators 124 COACTION: THE INTERRELATIONS OF ORGANISMS Fig. 31. — The Kaibab squirrel (Sciunis kaibabensis Mer.) feeding. One of its favorite foods is the new bark at the tips of twigs. (Photo by Frasher Photos, Pomona, CaHfornia.) Fig. 32. — Shows needles cut off and piece of peeled twig of the usual length. (Photo by R. R. Hamm.) SEED AND FRUIT COACTIONS 125 are not abundant. Grasshoppers, the army worm, and a few other insects when epidemic remove foliage of all kinds as completely as the large grazers and browsers with which they may compete. Importance of the Browsing-grazing Coaction. Browsing by do- mestic animals (and also by wild ones) has exerted considerable influence upon grassland where this contains certain shrubs or is in contact with them. Species with edible fruits but protected seeds, such as the mesquite (Prosopis) and juniper, are widely scattered by cattle and goats in particular, and frequently increase to a point where the grass dominants are more or less completely replaced by them, espe- cially where fire is a regular process. In addition to such changes of composition, there is usually a striking effect upon the form and branching of species that are regularly browsed, by which they assume more or less globular shapes, though these effects are not frequently due to native species. Recently Vorhies and Taylor (1933) have given a comprehensive account of the food coactions of Lepus alleni and L. calijornicus, as an outcome of the researches on the Santa Rita Range Reserve in Arizona. This deals not only with the quantity of forage consumed, but also with stomach contents, and the utilization of browse, cacti, grass, and forbs. Most of the plants present are eaten to some extent. The percentages for the respective species were as follows, grass, 45 and 24; mesquite, 36 and 56; cacti, 7.8 and 3.3; forbs, 12 and 17. Nevertheless, the authors state that jack rabbits are more abundant where forbs are prevalent than they are in stretches of climax grasses (pages 541, 563), a fact that is more in accord with the food habits of the larger rodents generally. In the Old "World, the common rabbit under agricultural conditions has spread from its original home in the Mediterranean region and is often the most serious of rodent pests (Tansley, 1922; Farrow, 1925). In Australia and New Zealand it is paramount, tens of millions being destroyed in a single year in New South Wales alone (Vorhies and Taylor, 1933:571, 567). SEED AND FRUIT COACTIONS To this group belong the squirrels of the western mountains of North America (except the tassel-eared group), some chipmunks, antelope squirrels, some kangaroo rats, and many wood rats. Outside the tropics this type of coaction is not common among the larger ani- mals; usually some animal food is taken also. The animals belonging strictly to this coaction type are chiefly insects. For example, Kor- stian (1927) found that insects may destroy about 10 per cent of the 126 CO ACTION: THE INTERRELATIONS OF ORGANISMS acorns in white oak and up to a maximum of approximately 50 per cent in black and overcup oak. The nut and fruit destroyers include various weevils, some larvae of other beetles, flies, e.g., apple maggot, various nut weevils, some larvae of other beetles, and moths, e.g., cranberry worm (cf. Weese, 1924; Zazhurilo, 1931). Storage by Mammals. The absence of actual hibernation in the squirrels renders some sort of storage desirable if not imperative in regions with much snow. The Abert squirrel and the flying squirrels are thought not to store food at all, though the former appropriates the stores of the Mexican woodpecker, according to Mearns (1907), as does the California gray squirrel those of other woodpeckers. The red and Fremont's squirrels employ stores almost exclusively, hiding them away in hollow trees, in fallen logs, or in the ground. The bulk of the cones gathered by the Douglas squirrel are placed in sizable hoards. The simplest type of storage is exemplified by the gray and fox squirrels, and to a minor extent by the Douglas squirrel, which merely bury each nut or acorn singly in the soil. It seems clear that the method by which many of these hidden nuts are found should suffice to disclose most of them, as is indicated by the state- ments of Seton, Morris and Merriam (cf. Seton, 1929:33, 92). It is accordingly probable that the debt of hickories, oaks, and cone bearers to the squirrels has been much overestimated, in spite of Seton, who states that there can be little doubt that three out of five nut trees were planted by squirrels, chiefly the gray (cf. Korstian, 1927:35). The nuts that are not stored away are usually eaten by deer, bears, and other animals. In special studies of the reproduction of conifers in the Rocky Mountains, no instance has been seen of buried cones producing sturdy seedlings, owing to the intense competition of the germinules. The seed crop in an even stand of trees, especially a climax, is not of special value as only occasional replacements are needed. It is the cones and nuts in mixed stands at the border lines between the two stages of succession that may be of vital significance. It follows, of course, that they may become effective under various modified conditions in forests. The food coactions of squirrels sometimes produce an effect just the opposite to that which is generally inferred. This has been dem- onstrated by tracing the succession after fire in the montane and subalpine forest of Colorado (Clements, 1910). The maintenance of a burn subclimax of lodgepole pine is due primarily to the fact that the population of squirrels, chipmunks, and nutcrackers is driven out by the fire just before an enormous amount of seed is released by the SEED AND FRUIT COACTIONS 127 opening of the cones. After trees again begin bearing and the ani- mals return, the cones are so completely harvested that seedlings rarely appear, even where space and germination conditions are favorable. Seasonal Coactions in Birds. This group includes the vast majority of gallinaceous and passerine birds, the species and individuals con- cerned being very numerous. In the large forms such as wild turkeys, pheasants, and quail, a scratching reaction on litter and leaf mold is similar to the rooting of peccaries and swine, turning up fruits, seeds, nuts, and invertebrates. The diet of the bobwhite has been studied much more thoroughly than that of other members of the group, espe- cially by Handley (Stoddard, 1931) and by Judd (1905). The food of chicks was found to consist of 84 per cent of animal matter, by con- trast with 22 per cent for adults; the two largest items were beetles 38 per cent and grasshoppers 27 per cent. For adults, the plant and animal material, and the major items in each, fluctuated greatly dur- ing the year. The maximum for the plant material occurred in Janu- ary and February with 98 per cent, contrasting with 2 per cent for animals, but the animal material rose to 38 per cent in October, leav- ing 62 per cent for plants. In nature even these larger birds rarely if ever bring about denudation other than in minute areas, but they may affect composition and invasion directly through eating or disseminat- ing seeds and fruits. Perching Birds. The food coactions of this vast group may be exemplified by the following tables. These have been compiled from several sources, chiefly Forbes, jMcAtee, Henshaw, Beal, and Gabriel- son; although the values are more or less typical, they cannot take account of all regional, annual, and individual variations. The fruit- and seed-eating birds do much under agricultural condi- tions to plant certain shrubs and trees. The prevalence of sumac, trumpet vine, mulberry, etc., along fences is evidence of their work. One of the best demonstrations of the effect of this group of birds on the composition of communities resulted from the controversy as to whether trees would grow on prairie soil. In 1875 and at various subsequent dates, some 18 acres of prairie soil on the campus of the University of Illinois were set with trees of about 30 species. Many of these died, and frequent cutting of the undergrowth largely prevented the development of the forest which would have succeeded. However, under a grove of green ash the recurrence of seedlings was striking, especially of cherry, hackberry, sassafras, grape, Virginia creeper, cur- rant, and other shrubs with fruits having indigestible pits, indicating that the succeeding forest would have been planted by birds. 128 COACTION: THE INTERRELATIONS OF ORGANISMS TABLE 1 Relative Composition of the Food of Common Birds Species Seed In- Fruit sects % % 93 7 90 10 85 15 85 15 85 15 80 20 75 25 75 25 75 25 74 26 74 26 73 27 70 30 70 30 70 30 70 30 67 33 Species Seed Fruit In- sects White-winged crossbUl . Purple finch CaUfornia towhee House finch Phainopepla Horned lark Blue jay Mocking bird Song sparrow White-crowned sparrow Varied thrush Redwing blackbird .... Bobolink Cardinal Indigo bunting White-throated sparrow American goldfinch .... Arkansas goldfinch Brewer's blackbird Lazuli bunting Slate-colored junco Yellow-headed blackbird. . Towhee Chipping sparrow Catbird Bushtit Crow blackbird White-breasted nuthatch . Brown thrasher Robin Black-headed grosbeak . . . Lark sparrow Rose-breasted grosbeak. . . % 67 67 67 67 60 60 58 52 50 50 50 43 42 40 40 40 % 33 33 33 33 40 40 42 48 50 50 50 57 58 60 60 60 TABLE 2 Seasonal Differences in the Food of Granivores (Gabrielson, 1924) Species Evening grosbeak Pine grosbeak . . . . Red crossbill Common redpoll . Pine siskin Snow bunting. . . . Lapland longspur Vesper sparrow. . Winter Seeds 100 0 99 1 99 1 99.6 87 13 97 3 96 4 100 0 Insects .4 Summer Seeds Insects 79 21 84 16 82 18 75 25 72 28 71 29 53 47 0 100 SEED AND FRUIT COACTIONS 129 Scansorial Life Habit. This group comprises those woodpeckers that feed chiefly upon plant materials. However, in spite of the marked structural adaptations of this family, its food habits are fairly generalized, and most of the species are to be regarded as bivores. The most sharply differentiated are the three species of Sphyrapicus, the sapsuckers, which have adapted themselves to a diet of sap and cambium, supplemented in considerable degree by fruits and ants. In Colaptes, the gilded flicker seems to be largely vegetarian, favoring the fruits of cacti; the red-shafted lives on a diet about half ants and half fruits and nuts, while the northern flicker prefers ants to fruits. The red-headed woodpecker mixes plant and animal materials in a ratio of about two to one, but offsets this by a fondness for eggs and nestlings. The California and Lewis woodpeckers prefer acorns, and the former in particular stores these in single caches in the trunks of oaks and pines (cf. Weiss, 1909; Griscom, 1923; Burrt, 1929; Chrysler, 1930). The enormous number of acorns taken by certain species suggests that woodpeckers have some effect upon the reproduction of oaks, but of this there is no definite evidence. However, the sapsuckers not only affect the health of trees and deface them by the production of burls and adventitious buds, but likewise injure some of them, especially young individuals, to the extent that they die. IMcAtee (1911) has listed 267 species of trees and shrubs attacked by the yellow-bellied sapsucker. Dissemination by Animals. In addition to the distribution of fruits and seeds by animals in the course of food coactions, a number of modifications are concerned with wholly unintentional dissemina- tion. There are four types of these, namely, hooks, spines, awns, and viscid excretions. The first are by far the most numerous and im- portant, hooks and barbs of various form occurring in families as far apart as the peas, parsleys, asters, borages, and mints, as illustrated by the familiar sticktights, beggar's ticks, cockleburs, etc. Spines on fruits are fairly common, but only a few are sufficiently stout to bring about attachment, the best known being the sandbur and the caltrop. The spiny heads of thistles are sometimes caught by the hair of animals, as are the fruits of some cacti, but the most effective distribution of the latter is through the food coaction, the fruits and upper joints of cylindric opuntias especially becoming attached to the jowls of cattle and thus spread about locally. Stipa and Erodium are examples of distribution by means of a sharp callus, and Stipa, Aristida, Bromus, Hordeum, and many other grasses of dispersal by virtue of awns. The use of sticky substances is quite exceptional, and 130 COACTION: THE INTERRELATIONS OF ORGANISMS is found only in a few glutinous fruits and in the so-called catchfiies in which the stems may be caught by animals. Finally, there is some dispersion of small seeds and fruits in mud on the feet of mammals and birds, but this is far less important than has been supposed (Clements, 1907). Dissemination by animals is often of much significance in connec- tion with bare areas or those in early stages of the subsere, where there is good opportunity for establishment or ecesis. It is regularly inef- fective when seeds are carried into unfavorable habitats or into com- munities in full occupation of the soil. When this condition obtains in the community to which the species concerned belong, the conse- quence is much the same, since new individuals can rarely be estab- lished until mature ones die out or the turn of annuation brings tem- porarily an enlarged opportunity. Sucking Coaction. There is a large group of food coactions in which the plant is injured or killed by having the sap sucked out by aphids, leaf hoppers, many other Hemiptera, certain larval Diptera, and so forth. The chinchbug affords a notable example of the de- struction of cultivated species by this means, but it is not especially detrimental to native grasses in adjacent areas. Some forms of this group alternate to some extent between plant juices and the blood of animals, as well as that of man. While anthophilous insects secure nectar by sucking, this coaction differs in practically all other respects and hence is considered under symbiotic relations (page 141). Cambium Feeders. This coaction is characteristic of certain in- sects, especially the so-called bark beetles (Scolytidae), which are particularly numerous on conifers. When they occur in epidemic form, they may kill trees over a considerable area, as does the Black Hills beetle (Dendroctonus ponderosae Hopk.). Other borers, usually Coleoptera, also girdle trees occasionally, but a much larger number drill into dead wood or heartwood with little or no effect except to hasten decay (see also Brues, 1920, 1924, and 1930). Galls. While these are not restricted to insects and mites as co- actors and flowering plants as coactees, the overwhelming number are concerned with these groups. The exact nature of the stimulus is not known, but apparently it is due to the injection of a secretion by the insect, though the use of food by the larvae may sometimes be in- volved also. The three chief groups of insects are aphids, gallflies (cecidomyids), and cynipids (Hymenoptera), with the spiderlike mites perhaps next in importance. All plant parts may be more or less affected, but the shoot, stem, or leaf figures in the most bewildering ANIMALS AS PASSIVE MEMBERS (COACTEES) 131 variety of modifications. Though much rarer, flower clusters and even individual flowers exhibit some of the more striking transformations. In exceptional cases where the number of shoots, leaves, or flowers is increased, a certain degree of mutualism appears to enter, but this is more apparent than real, since such parts are rarely quite normal in functioning. Nearly always, the relation is one of pure parasitism, the gall providing both food and shelter for the young of the coactor, regularly with some slight or even considerable disadvantage to the host plant. This rarely has decisive significance, though there may be a minor effect upon the competition between individuals or species, especially when flower and seed production are diminished. Invertebrate Omnivores. As has been pointed out elsewhere, the tendency is for animals to select a wide variety of food from the great diversity present in most habitats. Even in the predaceous beetles, a number prove to be plant eaters in part. Forbes (1883, b) made an exceptionally thorough analysis of the contents of the alimentary tract of common genera of carabids and coccinellids and found them to be more vegetarian than ordinarily supposed (Webster, 1880). Of the 20 genera of ground beetles studied, 8 preferred a diet more than half vegetable, while in Harpalus the percentage rose to 88 and in Amphasia to 97. For the ladybugs, 2 genera fed exclusively on plant material under certain conditions, while the general range was from a half to three-fourths. An unexpected result was the increase in plant food taken in the midst of an infestation of chinchbugs, but this was chiefly due to the concomitant abundance of fungus spores. ANIMALS AS PASSIVE MEMBERS (COACTEES) In the general sense of the term, carnivorous animals appear in all classes and embrace a large majority of the orders among mam- mals. They comprise more than half the families of terrestrial birds, most of the snakes, lizards, and amphibians, and a vast number of insect families, especially if larval coactions are taken into account. The animal-eaters fall into two major divisions, carnivores proper and insectivores, while many omnivores are carnivorous by preference when the food supply permits. The carnivorous habit has led to certain related coactions which may be regarded as offensive or defensive. These may pertain to the individual or the group; in the one case they usually arise out of the structure of the species concerned, in the other from some social habit, especially cooperation. Read (1920) has advanced the idea that hunt- ing in packs was the first social organization of primitive man. He 132 COACTION: THE INTERRELATIONS OF ORGANISMS assumes that the human type separated from the rest of the anthro- poid stock through (a) the adoption of life on the ground, (6) the addition of flesh to a diet of fruit and green plants or the assumption of a more or less complete flesh diet, and (c) hunting in packs. Such hunting would be a necessity only when food from plant sources failed in the dry or cold season. Recourse to the social hunting of large game in a climate with severe winters is exemplified by the wolves. During the summer their food consists of small mammals, birds, bird's eggs, and even insects, but in winter this kind of food is inadequate or wanting and coopera- tion becomes requisite to the securing of large mammals. Olson (1938, a) has mapped wolf dens and hunting-pack routes in the Supe- rior National Forest and Quctico Park. One main traveled trail to the northeast forms a narrow ellipse about 60 miles long and 15 wide, while the southwesterly course constitutes a similar ellipse approxi- mately 90 miles in length. Each of these appears to be hunted over at fairly regular intervals. Family dens are scattered about near the hunting trail, and the size of the pack naturally varies with the num- ber of families participating. Social organization also accompanies hunting habits in other genera (Houssay, 1893), as well as in other groups, such as certain steppe birds in Asia (Brehm, 1896), and South American weasels and birds (Hudson, 1892). It has been noted in a high degree of perfection in fishing squadrons of the white pelican on lakes of Southern California (cf. Bailey, 1917:43). The Prey of Carnivores. The distinction between carnivorous species and insectivorous or omnivorous species is far from absolute. Most of the carnivores eat insects regularly or on occasion, even the cougar being said to take grasshoppers, while mole and shrew feed upon flesh to some degree. ]\Iore than half of the common carnivores of North America eat fruits to some extent, with the consequence that this group passes more or less gradually into the omnivores. Not- withstanding these exceptions, the general habits of the group are well marked and are reflected in dentition, claws, and other structural features. Life habits characteristic of the herbivorous mammals are found in somewhat less degree among the carnivores. The marten is arbor- eal, and its relative, the fisher, rather less so. The foxes and M'olves are cursorial; the weasels and skunks exhibit the ferreting life habit; the hog-nosed skunk is more or less of a rooter, and the badger fos- sorial. The natatorial habit is represented by the otter; the mink is essentially amphibious, and the fisher rather less of a swimmer. Nearly all the group exhibit a strong tendency to be nocturnal, and ANIMALS AS PASSIVE MEMBERS (COACTEES) 133 some of them are strictly so. Practically all of them live in burrows or dens, more rarely in hollow trees, but only a few, such as the badger and the common skunk, hibernate to any considerable extent. As would be expected, the prey of a carnivore is determined largely by relative size and activity, and by the habitat, the choice of which often has some connection with food preference or amount. Thus, the cougar kills deer, elk, mountain sheep, and antelope for the most part, while the foxes and coyotes are largely confined in nature to animals not larger than a jack rabbit or grouse, with emphasis on rodents. The wolverine as the largest of the mustelids regularly catches animals of the size of woodchucks and beaver, and is said to be able to pull down caribou and moose on occasion, but its smaller relatives find the rabbit and muskrat the upper limit in size. As a rule, the lesser mammals and ground birds furnish the bulk of the food of carni- vores, but this is supplemented by snakes, lizards, frogs, insects, car- rion, and fruit, as well as by fish, crustaceans, etc., in some species. The most completely carnivorous are the weasel and mink among the smaller forms, and the gray wolf, lynx, and cougar of the larger ones. The snakes of North America are typically carnivorous, taking chiefly small animals, none of them being known to eat fruit, which is the nearest to flesh in texture. Two genera, the green and worm snakes, are mainly insectivorous, with the addition of earthworms in some instances. However, the great majority restrict their food to larger forms and differ chiefly in the degree of preference for warm- er cold-blooded animals. It is evident that the carnivores may exert a telling effect upon the number of herbivores and through this upon the composition of the biotic community. The relation is necessarily reciprocal and involves the whole question of dynamic balance in nature, which is discussed in the following chapter. Connected with this is that of the indirect effect upon the plant matrix as a consequence of the destruction of herbivorous rodents on a large scale. Campaigns of eradication of flesh-eaters fail to reckon with these complex relations and have some- times brought about an actual increase in rodents, usually detrimental to the human interest that prompted the destruction of the carnivores. Carnivorous birds are not separable from mammals on the basis of any coactional effect, but stand out by themselves on account of their flight and special methods of securing prey. The vultures may be con- sidered exclusively carrion-feeders, a habit in which they are joined by the caracara and the bald eagle. The hawks and owls exhibit less difference than would be expected in view of the nocturnal habits of the owls, though these must be reflected to a considerable degree in 134 CO ACTION: THE INTERRELATIONS OF ORGANISMS the small animals captured. Both live chiefly upon small mammals, birds, and reptiles; about two-thirds of each include insects in the diet. The osprey or fish hawk lives entirely upon fish, and the bald eagle largely so, while fish are a regular feature in the food of several other hawks, but only one owl, the screech owl. The Cooper and sharp-shinned hawks prey chiefly on larger wild birds, as do the American and western goshawks. A few species such as the pigmy owl and the sparrow hawk are mainly insectivorous, 314 out of 410 stomachs of the latter containing insects; 129, small mammals; and 70, small birds (cf. Henshaw, 1921). Among the few carnivorous birds in other North American families, the kingfisher prefers fish, but his tastes cover lizards, frogs, insects and crustaceans. The shrike is said to feed principally upon grass- hoppers, but it captures many small mammals and some birds ; its lack of talons causes it to impale its large prey, and it is also supposed to use this device for al fresco storage. The road runner alone of the bird carnivores employs a mixed diet, adding cactus fruits to a long list of animals ranging from mice and small birds to snails and caterpillars. The examination of more than a thousand pellets of the marsh hawk in Florida disclosed that this bird lives largely upon cotton rats in the particular region. The number for this rat was 925 to 21 for the cottontail and 7 for the common mole. Of more than 40 species of birds taken, only 3 were found in more than 10 instances, namely, song sparrow, 64; meadow lark, 26; savanna sparrow, 23 (Stoddard, 1931). By contrast. Cooper's hawk yielded 38 stomachs with poultry and game birds, 60 with other birds, and 12 with mam- mals, out of a total of 123 (Henshaw, 1921). First and last, the raptores take a prodigious toll of the smaller mammals, birds, reptiles, and insects, both in number and species. This is strikingly shown at the time of lemming migrations, as well as in other cyclic concentrations, but definite knowledge of the direct effect upon the composition of the biotic community is exceedingly difficult to secure. This is even truer of the indirect influence upon the plant matrix, but, in terms of seed- and fruit-eating coactees, this may well be considerable and in some instances locally decisive. The Prey of Insectivorous Animals. Two groups occur, namely, cursorial and aerial. Those possessing powers of flight include many species of small birds, bats, and some insects. Of the birds, prob- ably the swifts and creepers are the only common families that are exclusively insectivorous, though the flycatchers, kinglets, goat- suckers, swallows, vireos, wood warblers, and wrens are predominantly ANIMALS AS PASSIVE MEMBERS (COACTEES) 135 of this habit. Among the well-known species, the brown creeper, bush tit, barn and cliff swallows, chimney swift, house wren, nighthawk, phoebe, wood pewee, purple martin, yellow-billed cuckoo, and yellow- throated vireo rarely if ever consume vegetable matter, as is true in a high degree of the white-headed and arctic three-toed woodpeckers. Fruits and seeds constitute about 15 per cent of the food of king- birds, kinglets, and pipits, though under compulsion this may rise greatly, the last eating as much as 51 per cent in December. Approxi- mately a fourth of the diet of the meadow lark, bluebird, chickadee, and myrtle warbler consists of plant materials, and much the same ratio obtains with the downy and hairy woodpecker and certain ant- eating flickers. Beyond doubt, the more truly insectivorous birds and the omnivorous forms that confine themselves to insects in the summer make vast inroads on the insects of all climax communities and their serai stages, but definite values cannot even be approximated until quantitative studies are much more the rule (cf. McAtee, 1911). In the United States practically all species of bats live upon flying insects, though frugivorous and sanguivorous types occur to the south- ward. Dragonflies, some Hymenoptera (solitary wasps), and Diptcra (robber flies) seize prey on the wing. In any one locality, an opening made through a natural forest by a stream would be frequented by certain birds and dragonflies during sunlight and by other birds and bats soon after sundown and possibly by other bats as darkness comes on or in the night. The different groups are thus out of direct com- petition with one another as they encounter different prey. The cursorial type of insectivorous animals includes mammals, rep- tiles, amphibians, and invertebrates; it is possible that some few birds should be included. They are probably most important in the com- munities of arid areas, though some are found in all regions. The mammals that restrict their diet largely to termites are confined to warm communities in the tropics and subtropics. The lizards are chiefly insectivorous, though a few such as the desert iguana and the chuckwalla are entirely herbivorous, and some, like the collared and leopard lizards, feed upon plants as well as insects and other cold- blooded animals. The larger number confine their attentions to in- sects, though earthworms are sometimes added; some include slugs, frogs, and other small lizards, and others like the "glass snake" and the skunks vary the diet with bird eggs, nestlings, and young mice. Insects carnivorous in the broad sense are termed i)redaceous when they capture other insects, spiders, etc. (Webster, 1880; Forbes, 1883, 6) ; however, many tend to be omnivorous. Those that suck the blood of vertebrates, especially birds and mammals, may be regarded 136 COACTION: THE INTERRELATIONS OF ORGANISMS as truly carnivorous. The free-living bloodsuckers are chiefly Diptera, especially in the tundra and swampy areas of the coniferous forest. Ectoparasites are numerous among insects and arachnids, and an in- significant number of bats are also bloodsuckers. PLANTS AS ACTIVE AGENTS (COACTORS) Plants as Passive Members (Coactees) Like animals, this group is best divided with respect to the type of coactee, whether plant or animal. Apart from the host of para- sites represented by the fungi and bacteria, the number of genera is small, the mosses and ferns having practically none and the flowering plants a few among scattered families of the dicotyledons. To this group are also to be assigned the many saprophytes on dead or decay- ing matter, a few of w'hich occur among flowering plants. Flowering Plants. In this group belong those species that manu- facture no food or but a part of what they require. Like other depen- dent plants, they belong to the great physiological category of hyster- ophytes, and may be more or less definitely divided into partial parasites, parasites proper, and saprophytes. They exhibit practi- cally all possible stages in the evolution of this special habit, from rooted green plants such as Castilleia to chlorophyll-free genera re- duced to flower and haustorium, as in the tropical Rafflesia. Many of them' are more singular than important in the community, but some, like dodder and mistletoe, may exhibit a destructive coaction of signifi- cant effect. Hysterophytes occur in a small number of families, i.e., twelve, some of which contain no holophytic or autonomous genera, though this may be a consequence of basing the family on the food habit. Several of these are tropical, containing such unique forms as Rafflesia, which is reduced to a single flower sometimes three feet across. In temperate regions, the most important families are Loranthaceae, Monotropaceae, and Orobanchaceae, together with scattered genera such as Corallorhiza among orchids and Cuscuta among bindweeds. A large majority of these are root parasites and do not often cause serious injury to the host, but certain of the mistletoes and many of the dodders may exert fatal effects. Cuscuta is especially destructive in California, often producing bare areas of considerable extent, on which succession is initiated. Fungi and Bacteria. The destructive coactions of many of the flowerless hysterophytes are too well known to require comment apart from the role they take in modifying community processes such as ANIMALS AS PASSIVE MEMBERS (COACTEES) 137 competition and ecesis, and hence in changing the composition. On the other hand, the saprophytic forms, especially of bacteria, are in- valuable in breaking down organic matter and converting it into nutrient substances for green plants. Among the most important fungous parasites of plants are the rusts, smuts, and mildews; the other great groups, namely, black, cup, pore, and gill fungi, and the molds, contain many parasitic species along with a much larger num- ber saprophytic on dead leaves, wood, or humus material in the soil. It is exceptional that even rusts and smuts kill their host plants, but they sometimes handicap them sufficiently to lead to their partial elimination through competition or unfavorable climatic conditions. Many smuts, such as those of wheat and corn, destroy the seed and thus have a significant effect upon numbers and through them upon competition. Bacteria play a similar role, but one of relatively little importance by comparison with that in animals and man. Animals as Passive Members (Coactees) Insectivorous Plants. These resemble partial parasites inasmuch as they obtain a portion of their food from other organisms, but they exemplify an entirely different physiological habit. The latter is likewise more unique than socially significant, though it does denote a minor coaction bond in the community, and some of the species are more or less important serai dominants. Practically all the species grow in wet or boggy situations where inorganic nitrogen is deficient, but they differ much in the device for catching and digesting insects and other invertebrates. The modifications concern the leaf and range from ascidia or pitchers in Sarraceniaceae, Nepenthaceae, and Cephalotus in Saxifragaceae to sensitive glandular hairs or leaves in Drosera, Pinguicula, and Dionaea, and bladderlike traps in Utricu- laria. The so-called catchflies, belonging to the genera Silene and Viscaria of the Dianthaceae, entrap insects by means of a viscid secretion on the stem, but it is doubtful that they digest them. Be- cause of its submerged habit, Utricularia is the most important coactor of the entire group; Forbes found 93 animals of 28 species in ten bladders (cf. p. 165), a fact that justifies his contention that the bladdcrwort is a formidable competitor of small fishes. Fungi and Bacteria. Fungi that parasitize animals and man are found scattered through the algal fungi, sac fungi, yeasts, molds, and dermaphytes, the last mostly confined to man. Two groups, Empu- saceae and Laboulbeniales, are restricted to insects, and another, the water molds or Saprolegniaceae, occur chiefly upon small aquatic ani- 138 CO ACTION: THE INTERRELATIONS OF ORGANISMS mals. The genera Empusa and Saprolegnia are known to cause epi- demic diseases, the first in flies, aphids, chinchbugs, grasshoppers, etc., and the second among fishfry, especially in hatcheries. A few molds, such as Siiorotrichum globuliferum and Botrytis cinerea, are peculiarly fatal to true bugs and many larvae, and often become epidemic on a large scale during wet periods or seasons. A sac fungus, Cordyceps, is not uncommon on large grubs and caterpillars, the fruits forming long hornlike projections. The number of bacterial diseases found among insects, birds, and mammals is large; some of these become epidemic and bring about the destruction of flocks and herds on a vast scale. To them has been ascribed the "crash," but the probability of such a happening is dis- cussed in Chapter 5. SYMBIOSIS As stated earlier, the concept of symbiosis has sometimes been so broadened as to become meaningless, while on the other hand it has suffered from superficial observation and vivid imagination. More- over, precise definition is impossible and exact application equally so in the general absence of critical study. At bottom, symbiosis is parasitism in some form or degree, and most so-called examples of symbiosis are little or nothing else, even in such classical illustrations as that of the lichen (Pound, 1892; Clements, 1897; cf. Oltmanns, 1923:501). The coactions involved have chiefly to do with food and, since at least two organisms are concerned, have potential value for the formation of colonies. When one or both are represented by a single individual, no colony results, but in many cases, such as in ants, the production of colonies is the rule. Among water animals, a number of supposed instances of symbiosis have to do with shelter or attachment, and these are found among plants as well (cf. Step, 1913). The following account is confined largely to an enumeration of cases in which there is some evidence of mutual benefit, though often slight on one side at least, and to a brief consideration of the com- munity significance of the various types. These may be conveniently grouped as relations between plant and plant, plant and animal, and between animals. Likewise, for convenience sake, those that deal with food coactions are passed in review here, regardless of whether they occur in land or water biomes. Plant and Plant. In practically all examples of this type, the parasitic nature of one of the symbionts is more or less evident, and the vast majority of these are fungi or bacteria. Even in the pig- mented algae, epiphytic species grade into endophytic ones, some of SYMBIOSIS 139 which arc partial parasites, while others have become more or less completely dependent upon the host without as yet losing their chloro- l)hyll, with the exception of Geosiphon which contains Nostoc as jiroducent. This is almost certainly the relation that exists between blue-green algae and higher plants, as in the coaction of Anabaena with the water fern, Azolla, and Nostoc or its relatives in Si)hagnum, certain liverworts, the Cycadaceae, and an occasional angiosperm, as Gunnera. The outstanding symbiont among the bacteria is Pseud omonoas {Rhizohium) radicicola, which produces the characteristic root- tubercles of nearly all Fabaceae and is probably directly concerned with fixation of atmospheric nitrogen. Similar nodules are to be found in Alnus, Elaeagnus, Myrica, and Ceanothus (Neger, 1913), and in Casuarina and Podocarpus (McLuckie, 1923), and in most cases they are also to be ascribed to the same bacterium, though rarely a fungus may be concerned. Since Pseudomonas seems to be an oblig- atory endoparasite and the legume gains the boon of an added supply of nitrogen, this symbiosis constitutes one of the relatively few con- vincing examples of mutualism among plants, though even here the host grows normally in the absence of its symbiont. A somewhat similar physiological relation is thought to obtain between certain soil algae, Nostoc, Cylindrospermum, etc., and nitrogen-fixing bacteria, especially Azotobacter. Bacteria and yeasts may also exhibit certain characteristic types of symbiotic relation in the fermentation of kephir and ginger beer. The lichen has long been cited as the chief example of mutualism between alga and fungus, but when allowance is once made for the microscopic size and nature of the host, the essential relation is one of parasitism in varying degree. This is clearest in the higher forms especially, in which the fungus sends a haustorium into the algal host, finally destroying it, but destruction of the host is the general result in practically all cases, it seems. Probably all the host algae can, and many of them do, live independently, and this is true also of a considerable number of the fungus parasites among the less inte- grated forms. As would be expected, a score or more of different fungi occur on the same species of algal host, and several of them may have two hosts enwrapped in the thallus. Furthermore, over a hun- dred species of lichens contain in addition to the proper host a second or rarely a third alga near the surface, always blue-green and produc- ing a peculiar structure, the cephalodium, but of unknown function. Finally, there may be a secondary fungus, apparently parasitic on the lichen, but actually deriving its food also from the host algae. 140 COACTION: THE INTERRELATIONS OF ORGANISMS From their life form, lichens also exhibit attachment coactions, as a result of which they may injure bark or leaves by shading, and in the higher forms, the thallus may also live parasitically on the bark, as Phillips has shown for Usnea (1931, d). The association of fungal hyphae, regularly of Hymenomycetes, with roots has long been known as mycorhiza and explained as a rule in terms of mutualism. Its exact nature is still much debated, how- ever, and recent investigators are in disagreement as to the proper interpretation of the majority of cases. This is readily intelligible in the light of Melin's statement that a double parasitism is involved (1925). In the case of conifers, he states that the fungus supplies organic nitrogen to the holophyte, perhaps also potassium and phos- phorus, and in extreme cases serves to absorb all the water and nutri- ents needed by the host. On the other hand, McDougall regards all ectotrophic or external mycorhizas of forest trees as pure parasites (1914, 1922), and Masui (1927) states that it is going too far to say that mycorhiza is in general a symbiotic phenomenon, but that on the contrary it is purely parasitic, or at most only hemi-symbiotic. To the latter he assigns the mycorhizas formed by Boletus, to the former those produced by Armillaria, Polyporus, Hydnum, etc. Mycorhizas are widely distributed through the orders of seed plants, and are also found in some ferns and liverworts. However, they are more characteristic of the roots of conifers, of diclinic trees such as alder, beech, birch, oak, etc., of Ericaceae, Rutaceae, and Orchidaceae. The fungus symbionts belong chiefly to the gill fungi, with some members of the pore fungi and puffballs, and rarely of other groups. Practically all the genera concerned also grow sapro- phytically in the soil and thus exemplify another type of coaction bond in the community. Plant and Animal. The major categories of this type are coac- tions (1) between invertebrates and algae, rarely bacteria or fungi; (2) between insects and fungi; and (3) between flowers and pollinators. The animal symbionts with green algae, such as Zoochlorella, Chlam- ydomonas, Pleurococcus, and Scenedesmus, are represented by infu- soria (Amoeba, Frontonia, Paramecium, Stentor, Vorticella, etc.), a few sponges, hydroids, ophiurids, and the flatworm Convoluta. These coactions have been much studied, and in the Infusoria in particular prove to be comparable with that in the lichens, the alga as a species deriving some benefit but the individual succumbing to parasitism. An identical coaction is exhibited by a yellow algal symbiont, Zooxan- thella, with Foraminifera, Radiolaria, ciliates, sponges, and Bryozoa, and Convoluta as well. From their very structure, sponges are also SYMBIOSIS 141 susceptible of symbiotic relations with filamentous or massive algae of the Chlorophyceae and Florideae, though many of these are quite elementary in nature (Oltmanns, 1923). Pigmented bacteria appear to enter into partnership with the simpler Infusoria, as probably colorless ones also. Probably the simplest combinations of insects with bacteria or fungi are those investigated by Schwartz (1924, 1932) for a scale in- sect, Lecanium, with which a variety of yeasts and molds may live as endosymbionts. ]\Iuch better known are the coactions between the cultivator ants and termites on the one hand and various species of fungi on the other. These have been discussed briefly in another section (p. 152), and for the details the reader is referred to Wheeler's treatment (1923). As to the protection of flowering plants by ants, and the relation of the ants to such epiphytes as IMyrmecodia and to the distribution of seeds with fleshy appendages, none of these appear to involve any real degree of mutualism. "With respect to the sym- biosis between ants and epiphytes described by Ule (cf. Forel, 1930: 518), Wheeler has justly expressed much skepticism {loc. cit., 204). Pollination Symbionts. The universal coaction that involves mutual benefits between plants and animals is found in the process of pollination. In flowers with highly specialized corolla, fertilization and consequent seed production are often impossible without insect aid, while in the vast majority of all flowers, cross-pollination through the agency of animal or wind appears to bring several decisive advan- tages. Even inconspicuous flowers may attract visitors by virtue of nectar, as in willows, or by means of an abundance of pollen. As is well known, the mutualism is all but purely a beneficial one, the insect obtaining food for itself or its young and the plant insuring the pro- duction of seed. The pollen consumed is a minor detail, being much less than the wastage incident to wind pollination, while the removal of the nectar is an advantage, directly as well as indirectly. In detail, the plant profits by the production of more and better seed, and probably better offspring as well, when the flowers are cross- pollinated. In his classic study of the effects of cross- and self- fertilization (1876), Darwin found that the height of crossed morning glories was regularly greater than that of the selfed, the average ratio being 100:75, and the number of seeds was greater in much the same degree, as was the weight also. As between the two treatments, the seeds exhibited much variation in number and weight, but in general there was an advantage of 10-15 per cent in favor of cross-pollination. The greater vigor of the crossed plants was also demonstrated by exposing them to cold or to sudden changes of temperature and like- 142 COACTIOX: THE INTERRELATIONS OF ORGANISMS wise by subjecting them to competition, and was further seen in earlier flowering. The gains to the pollinator have to do entirely with the question of food supply, apart from shelter and protection in the case of lodgers. The food may be nectar for the immediate use of the adult or for storage, or pollen for producing bee bread to feed the larvae Fig. 33. — Insect pollination: The sphinx moth (Protojxircc quinquemaculatus Haw.) visiting evening primrose. (Photo by Edith Clements.) of bees. Both may be gathered from the same species or each one from a different species, but the general effect in pollination is the same. In one-flowered plants, crossing alone can occur, and this is probably the rule with few-flowered ones. However, when the num- ber of flowers rises to hundreds and thousands, the manner of working by bees, butterflies, and hummingbirds in particular renders it prob- able that the great majority will be fertilized by the pollen of the plant that bears them. Furthermore, it is possible for certain sturdy SYMBIOSIS 143 pollinators to pierce the corolla tube and secure the nectar without rendering the proper return, from which a chain of coactions may be set up. In California, the tanager punctures the thick tube of Big- nonia cherere, and various species of hummingbirds that can neither do this nor obtain the nectar directly profit by his fondness for sweets, as do the ants and other insects that follow. On the other hand, nectar may rarely be poisonous, as in Aesculus californica, and tlie symbiotic relation leads to tragedy. These direct effects do not comprise the whole relation between flowers and insects, or other pollinators such as the birds. The experi- mental study of pollination has brought much objective evidence to the support of the views of Darwin, IVIueller, and others, who believed that the two partners have mutually affected the evolution of each other. Flower form and color are most intimately linked with the structure of the preferred visitor, while the form and size of the latter have been reciprocally molded by its flower preferences or by its collecting behavior, as exemplified by the so-called pollen baskets of bees (cf. Clements and Long, 1923; Clements and Clements, 1928). The community consequences of this type of mutualism may be inferred from the usually greater size and vigor of crossed plants and their enhanced seed production. These not only insure a steady and even an augmented supply of nectar and pollen for the animals con- cerned, but also a tangible increase in the food supply of all gramin- ivores and frugivores, from weevils to birds and rodents. This is reflected in the larger number of seeds that escape destructive food coactions and hence are available for germination and the maintenance of the species. Animal Symbionts. The question as to the presence of symbiosis in many animal coactions has been complicated by observation of a general nature and the not infrequent injection of prepossession (cf. Step, 1913). It is manifest that a very large number of assumed symbioses, and especially those that merely involve attachment, shel- ter, or lodging, are not at all mutualistic or only to such a slight degree as to be insignificant. Even in the fresh-water mussels (Anodonta, Unio, etc.) and the bitterling (Rhodeus), the relation ap- pears to be a matter of reciprocal parasitism of a sort rather than symbiosis, at least in the sense indicated by Step {loc cit., page 83). This interpretation is supported by the fact that there is no such mutual relation with other fishes that serve as hosts to the glochidia. ]\Iany examples of symbiosis have been drawn from the social insects, especially ants, but only a relatively small number of these are mutual in any important degree. Most of these are covered by 144 CO ACTION: THE INTERRELATIONS OF ORGANISMS Wheeler's term, "trophallaxis" (cf. page 154) , while the many special trophic relations among ants belong to the general category of para- sitism, or "parasitoidism" (AVheeler, 1923:196, 200). Forel (1930:250) would include under symbiosis "the more or less constant and intimate union of one species with another," but his definition and its applica- tion take in various types of parasitism. The resulting confusion in thought is exemplified by his statement in connection with the tree Cecropia that "on the side of Azteca, symbiosis is complete and suc- cessful, and the plant does not suffer in any way, rather the reverse"! Apart from the symbiotic trophism of adult and young, the most con- vincing examples of mutualism are to be found in the coactions between ants and aphids, coccids, etc., the so-called ant cattle (Forel, loc. cit., page 492; Wheeler, page 178). For a concise but comprehensive account of the food coactions of ants, the reader should consult Wheeler, and further details are to be found in the two volumes of Forel. In the case of the bird-insect nesting relations described by Moreau (1936; Myers, 1929, 1935), an incomplete symbiosis appears to be involved in certain cases, but little is known of the cause and nature of the coaction in which birds build their nests alongside those of social insects. CHAPTER 5 AGGREGATION, CO^IPETITION AND CYCLES General Relations. The process of aggregation lies at the basis of social life in the biotic community, and hence it exhibits the most intimate relations with the other functions of the complex organism. It is the very essence of the association of organisms in the dynamic sense, and is primarily concerned with the integration of all the group- ings, from the simplest family of plants or animals to the most highly differentiated climax. Like all community functions, it is the collec- tive response of organisms to their environment, and in its turn it produces social patterns of all degrees of complexity. For plants, its general features have been elaborated by Clements (1901, 1916) ; for animals, its operation has been treated in much detail by Allee (1931). As with the other concepts of ecology, it now becomes necessary to examine it from the biotic standpoint and to make such modifications in it as the community life of plants and animals renders desirable. The purpose of the present chapter is to discuss aggregation as a social process, to treat its significance in cooperation and competition, and to trace its relation to population numbers and movements and the consequences that flow from this. It is evident that reaction is dependent in the first degree upon aggregation, since this alone makes it possible to combine the effects of individual organisms into a cumu- lative and permanent whole. A somewhat similar relation obtains in respect to coaction. Though the latter may concern but two indi- viduals, as in the case of food or reproduction, this is aggregation in its simplest form, from which all other forms arise directly or indirectly. The kind and degree of aggregation will determine whether coopera- tion or competition will rule in the resulting community, or whether they will alternate in space or time, as in the stages of succession. The connection with migration is even more intimate, since the two processes exhibit constant reciprocal action. All mixed aggregation, that is, every community unit above the rank of family, depends upon the operation of migration, while in the opposite direction the increasing pressure of numbers due to aggregation is probably the chief inciting cause for movement. In turn, ecesis or establishment 145 146 AGGREGATION, COMPETITION AND CYCLES rests in a large measure upon the cooperation of invading individuals or species, while the progression of serai stages is the outcome of the interplay between invaders and occupants in terms of cooperation and competition. Finally, the problem of populations and their fluctuation, of cycles, in short, is essentially a matter of aggregation, first of a particular species in a mounting phase of numbers, and then of its coactors, both predator and parasite, ushering in a second phase of sharp decline in the entire complex. AGGREGATION AS A PROCESS Causes of Aggregation. The basic explanation of aggregation is to be found in growth with consequent multiplication of individuals and their grouping about the parents for a longer or shorter period. The individuals once produced, the course of aggregation will depend upon several considerations, such as the medium, the type of organism, whether motile, mobile, or fixed, and the terrain, whether bare or occu- pied. The process is at its simplest in forms that remain together after fission, such as Merismopcdia and Nostoc among the algae, Vorticella and Fuligo among protozoans, Volvox, and Hydra. Even among flowering plants, the behavior is very similar when the seeds or bulbils germinate on the parent plant, as in some onions. Polygonum vivijKirum, etc. However, the almost universal rule among rooted plants is for the spores or seeds to fall about the parent and give rise to a family in bare areas or a colony in those already occupied. In annuals, the family consists of one generation; in biennials and peren- nials, of two or more. Moreover, aggregation in the latter is promoted by offshoots of various sorts and may come to depend upon them almost wholly, especially in cultivation. In the simple aggregation due to the fall of spores or seeds, gravity takes the primary role, and it has also some part to play when other factors enter. When transport occurs, simple aggregation is hindered and mixed aggregation is favored, in more or less correspondence with the efficiency of the migration device. However, even in the process of migration, simple aggregation recurs frequently when obstacles are interposed to the movement of wind, water, or soil, exemplified espe- cially by windrows of tumbleweeds and wave lines of hydrophytes. On a smaller scale, a similar result ensues when barbed fruits are carried by animals or a rodent hoard is overlooked, though competition between the seedlings usually prevents ecesis in such instances. In the case of free algae, as well as of zoospores, aggregation may result from the combined or separate action of wind, wave, or current, the AGGREGATION AS A TROCESS 147 Sargasso Sea being the outstanding example; and light may have a distinct effect upon motile forms. As with plants, aggregation among animals is regularly a direct outcome of reproduction in the absence of dispersive processes. Like- wise, it may result from the compulsion of such factors as currents of air or water, or from a more definite tropistic response to light, temperature, solutes, etc. More complex and autonomic in nature is aggregation in consequence of the search for shelter or for food, and still more a matter of internal urge is the grouping arising from the quest for mates. Such aggregation not only contains in itself a rudi- ment of social grouping, but, even more important, it leads to the reproduction upon which family aggregation at the various levels of integration is based. It is evident that compulsion, tropism, and self-regulated move- ment may be combined in endless variety and that they may operate to produce or modify communities of all sorts, from the simplest family to the biome itself. In the latter, the plan is naturally most compli- cated and the pattern is to be recognized only through the analysis of the coactions that have led to the integration of the innumerable minor communities. This is well exemplified by the pioneer attempt of Forbes to sketch the coaction bonds operating in the black-bass community of fresh water (1887; Allee, 1931, a:83). In two illuminating chapters (1931:38-80), Allee has discussed the physical factors and the animal responses concerned in the forma- tion of families and colonies, as disclosed by the experimental studies of a considerable number of investigators. He has also summarized the results so far obtained in determining the sense directive in vari- ous types of integration, for example, touch in harvestmen, odor in moths, sight in catfish, and sound in beetles and ants (pp. 88-97). Aggregation on Land. Definite studies of the process of aggrega- tion in connection with the origin or modification of terrestrial commu- nities have dealt chiefly with plants and with primary reference to succession (Clements, 1910, 1916). The investigation of grouping in land animals has been largely incidental to other objectives, though Shelford has described pioneer aggregations concerned in succession (1911, a-e; 1913, a). The first organisms to invade bare areas in sand dunes at the south end of Lake Michigan are the tiger beetle, Cicindela lepida Dj., and the spider, Geolycosa pikei Marx. The en- trance of the adult beetles may occur in autumn, or in spring when the eggs are deposited in the sand at some distance from one another. Upon hatching, each larva remains in position, merely drilling down- ward to a depth of about 45 centimeters. This constitutes an example 148 AGGREGATION, COMPETITION AND CYCLES of simple aggregation, comparable in a general way with that of plants. The spider probably invades as a consequence of the nocturnal wanderings of adults, the two species then forming an open colony as a result of mixed aggregation. At this point, plants enter to give the sand some small stability, the grass Ammophila in particular being quickly followed by a cutworm and this by Microbembex, a solitary wasp with social tendencies. With a steadily increasing number of invaders, both of plants and animals, complex aggregation as- sumes control of the development, to continue until the climax is reconstituted. In the present situation, no definite rule can be laid down as to the type of invaders in bare areas. In certain subseres, the soil com- munity remains in possession more or less intact to constitute the initial stage, which is quickly followed by the visible aggregation of either plants or animals or both. In the case of a severe burn, much of the soil fauna and other animals are destroyed or driven out for a time, and simple or mixed aggregation may follow in a very short time from the wind-blown spores of mosses and liverworts. In pri- mary succession on rock, the process of aggregation concerns lichens alone for many years, the soil algae and fauna and the sparse insects usually appearing with the mosses. On the other hand, the hydrosere exhibits a more complicated type of aggregation inasmuch as plankton and larger aquatic forms are already in occupation, and complex aggregation of a sort operates from the first entrance of the submerged plants characteristic of the initial stage. However, the course and significance of aggregation have received little detailed attention in the past, and this situation will hardly be much improved until the biotic approach to the study of succession becomes more or less the rule. Kinds of Aggregation. In the present scanty knowledge of details and of quantities in the process, a comprehensive analysis of aggrega- tion seems to be unprofitable. As a working basis, it appears sufficient to distinguish simple aggregation, which results in a family with wide variation in numbers and generations. Contrasted with this is mixed aggregation, in which two or more species are concerned, giving rise to a colony of plants, animals, or the two combined, and also varying greatly as to numbers. Less definite as to concept but of even greater importance is complex aggregation, characteristic of most serai stages and of climax units, in which the simple and mixed types play a con- tinuous or recurring part. The distinction between simple and mixed aggregation was also later recognized by Dccgener (1918) in his designation of "associations" and "societies" as homotypic and hetero- AGGREGATION AS A PROCESS 149 typic, in which he was followed by Wheeler (1930). Apart from this agreement, however, the viewpoint of the leading students of social behavior in animals differs materially from that of the bio-ecologist, and this is reflected to a large degree in both concepts and terminology. This divergence is exemplified by Deegener's classification of ani- mal communities, in which he distinguishes "associations" as acci- dental and serving no useful purpose to the individual members, and "societies" as essential and rendering a useful return to the individuals, or at least some of them (1917, 1918; cf. Alice, 1931, a: 15). These are divided and subdivided to yield more than a hundred types, but, as the system is primarily a static one and burdened with a sesquipe- dalian terminology, it possesses little pertinence for the present treat- ment (cf. Allee, loc. cit., page 14). It appears certain that aggrega- tion will sometime be analyzed in considerable detail, especially with reference to the groupings of plants and animals both on land and in water, but this must follow much more extensive c^uantitative and experimental studies in the field. Consequences of Aggregation. It is obvious that the coaction of coming together in a family or other group will set up other coactions as corollaries of this, and each may be of greater or less significance in the life of the community. The community may react upon the habitat, or the individuals may interact with one another, in such manner as to produce either beneficial or harmful effects. Quite fre- quently the two results may be combined in various degrees, though one or the other usually rules. In general, the intensity of effect depends chiefly upon the space relations of the individuals in the group, that is, upon the degree of crowding, so called, but it is also influenced by the qualities of the organisms concerned. In general, helpful coactions are more characteristic of the family and colony, and harmful ones of the more complex communities, but there are striking exceptions in both instances. The property of motility naturally plays a large part in crowding and its consequences, as does also the type of habitat, whether water, soil, or air. In accordance with the above, it becomes necessary to distinguish three types of coaction following upon aggregation, on the basis of mutual effect. Two of these, cooperation and competition, are well known by name, but still too little understood as to fact; the third deals with processes indirectly harmful and may consequently be termed disoperation. It is clear that all three coactions may operate in any community and that they are in fact exhibited in some degree by practically all, though each grouping derives its distinctive charac- ter from the predominant process. 150 AGGREGATION, COMPETITION AND CYCLES COOPERATION Origin and Nature. Cooperation is the universal outcome of simple aggregation; in fact, it appears axiomatic that community life is im- possible \Yithout it in at least some degree (Kropotkin, 1915). Even when the benefits are slight or obscure at the lowest levels, they must outweigh the disadvantages to render the community more than a transient affair. The advantage must be mutual, though often far from equal, and it may exist along with definite, though less critical, handicaps. In essence, then, cooperation is to be considered as a dynamic social process in which mutual benefit of some sort consti- tutes the chief bond and overrules the unavoidable disadvantages of massing or crowding. In the family, this bond is at its strongest, even when the members are counted by the thousands. It is less con- trolling in the colony, except when this has an adoptive pattern, and in communities of higher rank it breaks up into a looser complex of relations between families, colonies, and larger groupings. It is obvious that, while cooperation rests upon mutual tolerance in terms of habits and space, its positive values are derived from the conservation of energy and material, especially food, from division of labor, and from increased care, parental or nutricial. The analysis of any cooperative community must be directed primarily to these processes, as has been so ably exemplified by Wheeler in particular (1923), and the success of community life is to be measured in such terms, with adequate recognition of the attendant disoperation or competition. So vast is this theme, especially in its human connota- tions, that even the barest outline is beyond the scope of the present treatment and little more can be attempted than to point out its major features in the biotic community. Of the extensive literature in this field, none exhibits so much of the spirit of dynamic ecology as Wheeler's "Social Life among the Insects," and the interested reader is referred to this as the most illuminating introduction to the subject. Cooperation in Plant Community and Matrix. Though coopera- tion is generally on a much lower level in plant than in animal com- munities, it does occur and is not without significance. Its beginnings are to be seen in the cenobic algae, such as Gloeocapsa, in which the gelatinous sheaths of the initial cells serve to protect the whole family, or IMicrocoleus, whose outer filaments secrete a similar protection. In Nostoc and its relatives, division of labor appears in addition to a protective matrix, and community functions are assumed by spore and heterocyst, while another type of differentiation takes place in the motile Volvox. Similar phenomena are to be found among the Protozoa and are well exemplified by the plantlike slime molds, in which move- COOPERATION 151 mcnt, protection, spore production, and dissemination arc all more or less specialized functions of the community. With respect to attached plants in general, cooperation is chiefly concerned with reaction, by means of which the community modifies the habitat in some degree to its advantage. This exists in small measure at least with some lichens and most mosses wuth respect to water relations, but is much more important in ferns and flowering plants, which may modify practically any one of the factors of the habitat. Such effects have been considered in some detail in the chapter on reactions, and hence it is necessary here merely to empha- size the cooperative nature of the process. Cooperation also plays a role in dominance and hence in the layering of communities, though the original selection is made by competition. It likewise operates in mass migration and invasion, and its effect is to be seen in both climax and serai stages. To a more limited degree, it is involved in local migration wherever tlie parent plant takes some concern for the fate of its offspring by such devices as catapult fruits or stolons and runners. In symbiotic relations between plants of two species, cooperation is present in varying degrees, but it is rare that two respective families are concerned. In some instances, a single individual of each is involved, as is probably the case in many mycorhizas of trees and the fungi of orchids; in others, the microscopic organism is present in vast numbers in the tissues of a single symbiont, as with Nostoc and cycad, or clover and the nodule bacterium. This may prove to be the rule with lichens, though the fungus element is often derived from more than one germule. There are a few striking instances of sym- biosis between a plant and an animal community, but these can best be treated in connection with similar relations between animals. Cooperation in Animals below the Social Level. In considering the beneficial effects of aggregation, Allee has discussed in several chapters the results of the past decade that bear upon the stimulation of growth and reproduction by crowding, and the effect of crowding upon survival, as well as upon sex determination and morphology (1931, a: 147-334). As a consequence, he reaches the conclusion that interdependence or automatic cooperation is so widespread among animals as to rank as a basic property of animal protoplasm, and probably of all organisms, an opinion supported by what has been said above as to plants. Such a type of cooperation has been more or less definitely demonstrated for tropistic aggregation in more than a hun- dred different groups, from bacteria and Infusoria to fishes and rep- tiles, the great majority of which are far below the level where dis- 152 AGGREGATION, COMPETITION AND CYCLES tinctly social groupings occur. As in plants, such unsocial aggregation is a consequence of the response of the individual to physical factors, and the resulting cooperation arises out of the reaction of the group upon the habitat. It differs essentially from cooperation on the social level, in which coactions among the members of the group are the motive forces that bring about group organization and differentiation. However, the simpler type passes more or less imperceptibly into the other and no hard-and-fast line can be drawn between tropistic and social communities (cf. Kropotkin, 1915). Cooperation in the Family. Although aggregation into families often involves something of the tropistic relation to a physical factor or to food, it is primarily determined by sex. The simplest coopera- tive unit in this category is the potential family, consisting of a single male and female in which the latter is fertilized, as, e.g., in a nuptial flight. A distinct advance in the nature of the social bond occurs when a pair remains mated for a longer period, such as a season or more. Reproduction leads to a second type of family comprising only the young organisms, in which the binding force may be purely tropis- tic or more or less social in nature. The first step toward parental cooperation is taken when one of the parents, usually the female, takes some concern for the fate of the eggs, and true cooperation results when this is shared by its mate. The first step toward actual coopera- tion within the family occurs when one or both parents remain to care for the young for a longer or shorter time, as do many of the vertebrates. However, this is realized only when the offspring as- sumes a certain and often the major share in the family tasks, as is best illustrated below the human family by Hymenoptera and termites (cf. Forel, 1930). In the families of social insects, cooperation finds its chief expres- sion in division of labor and in conservation of food. The former may occur without the origin of castes, as in Belanogaster, in which the older females lay eggs, the younger gather food and materials, and the youngest feed the larvae and tend the nest. Among the social wasps, a distinct worker caste first appears in the vespids, and then remains more or less typical of the three families of social bees, and especially of the honeybee. In certain ants, the division of labor is fourfold, a soldier caste being added to the three, males or drones, queens, and workers found among the social bees. A similar develop- ment of castes has taken place in the termites, but has been carried much further, to the point of producing eight castes, each containing both mules and females, and as many as five or six of these may be found in the termite family (Wheeler, 1923:252). COOPERATION 153 In many desert ants, both division of labor and conservation of food, in the original as well as the derived sense, have been brought about by employing certain workers or soldiers (Wheeler, 1908; 1923: 179,335) as "honey jars." The honey is stored in the crops of such individuals, which become so distended that the ants are unable to walk; when stroked by the workers, they regurgitate droplets to serve as food for them. Such reciprocal feeding, or trophallaxis, as Wheeler terms it, usually concerns larvae and adults in ants, as well as in the social wasps, but is entirely lacking in social bees. In wasps, the larvae are fed with pellets made of caterpillars, flies, etc., and the nurse adults imbibe the sugary saliva that exudes from the mouth of the larva. Ant larvae may be given solid food such as pieces of in- sects or pellets or liquids regurgitated by the workers that nurse them. In turn, the larvae yield secretions that are eagerly sought by the adult; these may be sweet saliva or fatty substances excreted through the integument. With termites, trophallaxis is primarily an adult co- action, in which they feed each other with saliva, with regurgitated food, and with feces. In addition, they also produce fatty exudates, which are consumed by other individuals, the outcome being a com- plex food bond beyond that of any other family group of insects. Outside of the groups of social insects, cooperation occurs but sporadically until the fishes and higher vertebrates are reached. Though there are scattered instances in other groups of care of eggs or young on the part of one parent, it is rare that the two parents cooperate in this respect. In birds, and many groups of mammals, the cooperation of male and female is the rule, as a consequence of which there results much division of labor in terms of behavior. Among the ungulates, the general absence of nest building and the necessity of constant foraging for food affords much less scope for family cooperative behavior. In the large aggregation families, such as flocks of birds and herds of ungulates, there may be a certain de- gree of division of labor in terms of leaders, scouts, and sentinels, but this apparently does not often assume a definite pattern. Finally, cooperation in families is promoted by a means of com- munication among its members. There is no reason to discuss here the moot question of language among bees, ants, and other insects, especi- ally since this hinges largely upon definition. It appears probable that a large number of species possess methods of communicating ob- servations, warnings, and intentions to one another and that these play a large part in the integration of the family group, as well as its protection. One of the most remarkable examples of such cooperation is furnished by squadrons of white pelicans, which perform a number 154 AGGREGATION, COMPETITION AND CYCLES of evolutions with faultless precision in driving fish to shoal waters. An illuminating inquiry into this subject has been made by Stoddard and his associates (1931), who find a dozen distinct calls in the vocabulary of the bobwhite quail {Coli7ius virginianus L.). The best known and most characteristic of these is the "bobwhite" call, which appears to be uttered chiefly by the unmated cocks. The others are the crowing or caterwauling call, the scatter or covey call, the lost call, the decoy ruse call, the distress call, the cackle note, the battle cry, the alarm note, the food call, and the conversational tones, most of them having to do with the guidance of the covey. Cooperation in insect families has been carried to the incidental guests of the family. Wheeler {loc. cit., page 174) says: "I have en- deavored to indicate how trophallaxis, originally developed as a mutual trophic relation between the queen and her brood, has expanded with the growth of the colony, like an ever-widening vortex, till it in- volves, first, all the adults as well as the brood and therefore the entire colony; second, a great number of alien insects that have man- aged to get a foothold in the nest as scavengers, predators and para- sites (symphiles) ; third, alien social insects, that is, other species of ants (social parasites) ; fourth, alien insects that live outside the nest and are 'milked' by the ants (trophobionts)." Wheeler has also named and classified the relations of ants to other organisms {loc. cit. page 200) , of which social parasitism, myrmecophily, and trophobiosis have to do chiefly with families. The term family is here applied to so- called colonies of Hymenoptera and termites as a matter of fact (Read, 1920:35), and its use is in accord with the general implications of the term as applied to plants. However, it is to be understood that various small animals occur on and among the individuals that constitute the plant family just as these alien insects and fungi (usually not noted) occur in the animal family. Cooperation in the Colony. Colony is here used in the sense of a new group of invaders of new territory composed of two or more species. This is the plant-ecological connotation. Cooperation in colonies is generally a matter of symbiotic relation, in view of the fact that two or more species are involved. Naturally, the best examples are found in animal colonies because of their activity and food de- mands, but they occur also among colonies of plants and animals and probably among those of plants alone. The debatable question of the nature of the relation between ants and Acacia, Mymecodia, etc. (cf. Lubbock, 1882:57), may be left to one side, since this is not a matter of a plant-animal community The most familiar examples of cooperation in an animal colony COOPERATION 155 are those in which insects that excrete "honey dew," such as plant lice, mealy bugs, and scale insects, are attended by ants or by beetles such as the silvanids. These gather the sweet excrement as it falls on the leaves of the host plant or take it directly from the bodies as it is made. Some species of ants have developed the habit of stroking individuals of the phytophthora to cause them to excrete more liquid. JNIoreover, they conserve and increase the supply of this food by pro- tecting the producers from marauding enemies, caring for them in special shelters, gathering and distributing the eggs, and transport- ing the adults to their proper host plants (Wheeler, 1923:178,31). Cooperation in Plant-animal Colonies. The simplest cooperation in such colonies is found both in water and in soils that contain algae. The carbon dioxide required by the algae for photosynthesis is sup- plied in large measure by the animals, and in turn the algae give off oxygen for animal respiration. The waste products of the animals as well as the dead bodies are broken down by bacteria and the simple materials elaborated to the point where they can be utilized by the algae. A specific example of such a relation at or near the surface is furnished by Nostoc and Azotobacter. A much more striking behavior cooperation exists between several groups of insects and the fungi they cultivate for food when setting up new colonies and entering new areas. Such a symbiotic relation is exhibited by beetles, ants, and termites, the general features being more or less similar for the three groups. The ''ambrosia" beetles tunnel in twigs or wood, placing the eggs singly in pits and then filling these with chips and mycelium, which is renewed by the mother from time to time. She also clears the refuse away from the pits, and this is utilized for further development of mycelium. When the female leaves her pit, she carries conidia of the particular species of hypho- mycete to her new home. Though there is considerable choice in the selection of a nesting site, each species of beetle makes use of a par- ticular species of mold. By comparison, the fungous gardens of the ants and termites are huge affairs, in keeping with their large compounds, but the members of these two groups are in accord with the ambrosia beetles in selecting a single species of fungus for culture. The ants are known to use the mycelium of agarics, polypores, and black fungi, while the first and last have been found in the cultures of termites. The higher genera of ants cut segments from leaves and carry them to the nest to be comminuted and made into a medium for growing the mycelium. The hyphal threads are manipulated by specialized workers in such fashion as to produce swellings or bromatia, which serve as food for both 156 AGGREGATION, COMPETITION AND CYCLES adults and larvae. The transfer of a hyphal pellet from the old to a new nest is made by a queen, who also fertilizes the growing mycelium with various materials. The fungous gardens of termites are similar to those of ants, but the sowing of conidia is supposed to be through the feces of workers. However, among the adults neither the workers nor soldiers make use of the fungus. Cooperation in Larger Communities. Apart from the families and colonies found within the larger units, cooperation in communities is more or less general or obscure by contrast with the processes discussed in the preceding pages. It is said to occur to some degree in mixed herds of African game (Selous, 1908; Roosevelt, 1910), where several species of ungulates herd together and respond to the signal of any one of them, and to exist between cowbirds and bison (Seton, 1929:3:685). The best-known and most definite type of cooperation in the biome in general is that between plants and anthophilous insects, in which the relation is not only intimate and detailed, but is likewise more or less obligatory for both organisms. In spite of these facts, however, the or- ganization of such cooperative communities is both loose and tem- porary, and follows the kaleidoscopic pattern of most of the smaller biotic units in faciation or association. Cooperation and Human Communities. Like all other social or- ganisms, man is subject to the operation of aggregation and exempli- fies its effects, though he has it much more in his power to modify or escape the results if harmful. As with all social groups, cooperation in rudimentary form first developed in connection with mating and then appeared in the family, to be further emphasized in the super- family or tribe. Division of labor with attendant increase of parental care and conservation of energy and materials must have been present almost from the outset, but necessarily became more marked with each successive stage in culture, from hunting to the pastoral to the agri- cultural. This was not merely because of greater differentiation in each new culture, but also for the reason that the preceding stages persisted in some degree beside each later one. Urbanization placed an enormous emphasis upon division of labor and consequent special- ization, and at the same time insured that the ancient vocations of hunting, war, grazing, and farming should feel a similar impetus, but in lesser degree. As a consequence, while the modern urban community seems to be far withdrawn from kinship with the biome, in fact its dependence upon it has never been greater. DISOPERATION 157 DISOPERATION Nature and Scope. As suggested previously, the harmful effects arising from aggregation or crowding may well be termed disoperation. This stands in direct contrast to cooperation in consequence, but it is less clearly distinguished from competition. However, the essence of competition is the attempt to secure more than a proportionate share of a limited supply of something, e.g., raw materials, food, space, or material for construction. In comparison, disoperation includes chiefly those harmful effects that have to do with changed conditions or behavior, as in the accumulation of carbon dioxide, toxins, or ex- creta. Since all coactions may be classed as beneficial or harmful with respect to the needs of a species, it is evident that no absolute line can be drawn between them, since even cooperation may present disadvan- tages. Nevertheless, the four main types of coaction, namely, coopera- tion, disoperation, competition, and destruction, correspond to definite differences in process and outcome, and hence serve a useful purpose in the analysis and organization of the myriad of interactions between organisms. As with other coactions, disoperation may concern plants or ani- mals, or both may be involved in the same process. IMoreover, it may be combined with other types of coaction in some measure, or it may be a secondary effect of any one of them. Disoperation in Plant Communities. Disoperation among plants is largely an outcome of additive reactions, as in the production of car- bon dioxide or other toxins in the soil. This occurs, as a rule, only in colloidal or waterlogged soils, where it is a concomitant of competition for an inadequate supply of oxygen, with the consequence that the two effects are difficult to separate. Acids and other more or less dele- terious substances are produced by the decay of plant remains in wet climates especially and may serve as a physiological barrier to certain invaders or lead to the actual elimination of some species (cf. Clem- ents, 1921 b) . The accumulation of leaves in forests may be disoper- ative to a high degree in dry climates, or wherever a thick layer of duff is produced or a dense interwoven carpet of pine needles is formed. Such conditions not only render germination difficult or fruitless, but they likewise hinder seedlings from rooting in the mineral soil beneath, with its proper supply of water and nutrients. Disoperation may also act through the canopy of forest or thicket by decreasing the light intensity or the effective rainfall. The light effect is felt in the competition between individuals of the canopy (e.g., Fig. 34) or of the layers below, but it results also in a direct 158 AGGREGATION, COMPETITION AND CYCLES handicap to each successive layer, as well as to the seedlings of the dominants. The last effect in particular is likewise exerted by the progressive interception of falling rain from canopy to the lowermost layer. In regions such as that about Pikes Peak where summer pre- cipitation is mostly in the form of light showers, interception by the coniferous crowns regularly accounts for a large portion of the rain- fall, with a corresponding reduction in ground cover and the germina- tion of tree seeds. Furthermore, though reaction and competition are Fig. 34. — Disoperation between Spanish moss {Tillandsia usneoides) and live-oak {Quercus virginiana), northern Florida. (Photo by J. R. Watson.) regarded as the driving forces in succession, it is clear that disopera- tion plays a regular though secondary role. Disoperation in Animal Communities. With the exception of competition in the proper or strict sense, all coactions that result in discomfort or disadvantage to individual or group may be regarded as disoperative, if the effect falls short of the destruction of the or- ganism. Here again the effect is naturally one of degree, since the same parasite may weaken, cripple, or kill its host in accordance with the intensity of its action. Hence, internal and attached parasites have been considered in the chapter on coactions, leaving for the present treatment the independent parasites, which exemplify the original meaning of the word. Apart from human society, the most COMPETITION 159 striking of these are probably represented by insects and a few birds. In one direction, the beginning of such a rehition is to be seen in cases of trophallaxis where tliere is an actual exploitation of the larvae without an adequate return, as in certain social wasps (Wheeler, 1923:83). An advance upon this relation is made by such ant guests as Lomechusa and its relatives, which beg food from their hosts. The step from beggary to thievery is a short one, as is shown by Antenno- phorus in particular {loc. cit., page 226) , as well as by the thief ants and certain mymecophiles {loc. cit., pages 201, 221). When eggs or larvae are stolen, thievery often leads to slavery in varying degree {loc. cit., page 207). Crowding brings about disoperation among animals, especially in families or colonies of aquatic organisms, and this may be expressed in terms of growth, reproduction, or survival. Aggregation probably produces these effects chiefly through competition for food or oxygen, but toxic substances in excreta also play a large part, and it is at least possible that volume and space as such may be involved in some instances (Allee, 1931, a: 118). There are instances of disoperation of bloodsucking insects which carry fatal diseases and thus destroy their food supply, but all clear cases are associated with human disturbance of natural communities. However, Ricker (1932) has pointed out that, in certain ponds under conditions that might well occur without man's interference, suckers remove submerged vegetation which supports various aquatic inverte- brates and produce a mud bottom in which only bloodworms (chiro- nomid larvae) occur. The suckers thereby decrease the favorite food of trout which pick a considerable part of it from the plants, and the number of trout is decreased. This is a clear example of disoperation, and Ricker points out that at the same time trout and suckers are to some extent in direct competition for the same food (cf, Cahn, 1929) . COMPETITION Nature and Correlation. In contrasting competition with other coactions in preceding sections, it has already been defined in brief, but a comprehensive treatment demands that the lines be drawn with more exactness and in greater detail. The process may be defined inclusively as a more or less active demand in excess of the immediate supply of material or condition on the part of two or more organisms. It may concern a particular object or a set of conditions; it may be exhibited by as few as two individuals, by a vast family horde as with many ungulates, and in communities of every possible size and com- plexity. Its most striking manifestations are associated with crowd- 160 AGGREGATION, COMPETITION AND CYCLES ing in the usual sense, though keen competition frequently occurs in what is visually open spacing, as with desert shrubs and bird terri- tories. Competition is regularly most marked between organisms with the same or similar needs, as within a particular life form of plant or animal, but it may even take place between plants and animals in soil, aquatic, or parasitic communities. In general, competition is to be distinguished from all other co- actions by the test of a common demand upon a limited supply. This criterion applies even to the combat between two males for the same mate. However, the active or passive contest between an animal and its food organisms, as well as combat between two animal families, belong to a different category. This non-competitive type includes in particular the destruction exerted by carnivores, though an active com- petition often exists among these. Similarly, for example, the para- sitism of the cowbird is not competition in the stict sense, in spite of the fact that passive competition occurs among the nestlings. More- over, there is an element of competition in certain types of disopera- tion, instanced by the examples of beggary and thievery cited in the preceding section. Furthermore, though cooperation is the exact antith- esis of disoperation, it is also antithetic to competition, since com- petition is regularly harmful in its effects. On the other hand, when competition leads to dominance and subordination, as it often does, especially among plants, a certain degree of cooperation is established. Consequently, while coaction is regarded as embracing all the inter- actions between organisms, competition comprises only those directed to a common need. Types of Competitors and Objectives. It is evident that organisms compete with one another only when they make the same or similar demands and typically at the same time, in the absence of an ade- quate supply. This may be for one, for several, or for all the essential factors of the habitat. However, there can be no significant competi- tion between an oak and a forb of the forest floor after the latter has become subordinated, though it may exist when the oak is a yearling or when the ground layer is well developed. As a consequence, competi- tion depends in the first instance upon the life forms and life habits involved, and in the second upon the manner and degree of aggregation. Plants and animals will compete least frequently with each other be- cause of certain basic differences in their demands, but when they are similar in size, as in microplankton, or in nutrition, as with leaf parasites, competition does arise. Competition will be keener between mammals than between mammals and birds, as a rule, but there is little between carnivore and herbivore except in so far as some tend COMPETITION 161 to be omnivorous. However, the rivalry among squirrels and nut- crackers for pine seeds may be intense. In other words, similarity in behavior, that is in life habits, may often overrule life form. Since the term itself denotes common seeking, there is no further competition without a proper degree of density or crowding, and the effects increase more or less geometrically with the crowding. Com- petition thus becomes peculiarly a community function, and hence is necessarily affected by the manner of aggregation, the structure in terms of layers and minor communities, and the developmental stage attained. Course and Outcome of Competition. As with other phases of competition, the absence of detailed studies renders it impossible to trace more than its general course in animal communities (cf. Forbes, 1887; Howard, 1920; Allee, 1931, a). On the other hand, plants and plant communities have received considerable attention from this approach, and the nature and course of this function are fairly well understood, as is shown later in this section. The general stages of the processes are epitomized in the outcome, which is represented by dominance in varying degree for the successful competitors and by subordination or elimination for the unsuccessful ones. Subordination may result in subdominance to produce the layers of forest and thicket or the aspect societies of grassland, or it may lead to suppression in the guise of secondary species and communities. When suppression reaches the extreme of elongation or dwarfing, it passes into elimina- tion, which constitutes a universal feature of succession. A similar series of competition phenomena is to be found in animal communities, though in the absence of dominance on land it is less pronounced and visible. It is readily seen in the leadership of old males in polygamous herds, in the culls of broods and the runts of litters, and in such social phenomena as the "peck order" of fowls. It is exemplified in some measure in the drawing of territorial limits by many species, but usually reaches its most characteristic expres- sion among the sessile constituents of marine communities. Reduction or Evasion of Competition. Competition may be reduced in intensity or more or less completely avoided in a variety of ways. It is obvious that such results may be secured by a reversal of the relations or conditions that promote competition, such as similarity of life form or life habit, close spacing, etc. The greater the variety in life forms or behavior, the larger the number of species that can exist side by side in essential harmony. This is well exemplified by sub- ordination, as a result of which a large number of shrubs and herbs may thrive under a forest canopy, or a wealth of forbs flourish amid 162 AGGREGATION, COMPETITION AND CYCLES prairie grasses. A similar adjustment or evasion is evident in the insects and birds of tree trunks by contrast with those of the crowns, and it characterizes also the subterrene moles and gophers. Evasion in time is perhaps even more general than that in space. It is best illustrated by aspect societies of plants or animals, or both, as a consequence of which the maximum demand is distributed through three or four major phases of the growing season or the year. Some- thing of the same advantage, only in a smaller way, accrues from the nocturnal habit and in some degree also from estivation and hibernation. Though less regular in operation, annuation may possess similar value. This is particularly true of winter annuals in the Southwest and desert regions generally, and must apply in a large degree to the animals dependent upon them. It must also play some part in the dynamic balance of animal populations. Similarities and Differences. With respect to the chief prerequisite for competition, namely, a common demand in excess of the supply, all communities, whether plant, animal, or mixed, are in complete accord. But beyond this, striking differences arise in the process as a result of the divergent demands made by autonomous plants and animals. The plant, and hence the plant matrix, as the producer of food from raw materials, makes demands, that are peculiar to it, upon water, carbon dioxide, nutrient salts, and light. The need for oxygen is felt by both plants and animals, and they are likewise in accord as to the essentials of respiration. As to appropriate working condi- tions, both groups of organisms are dependent upon temperature and radiation in varying measure, but there is no actual competition for these, apart from that for light. They may also exhibit competition for certain solutes, as diatoms, chara, Infusoria, and mollusks for lime and silica, though the movement of water or organism may obvi- ate this to a certain extent. Competition for food is characteristic of animals alone, with the exception of plant parasites and saprophytes. Animals are unique in competing for mates, though the rudiments of such competition may be seen in the motile gametes of a few algae. However, a process with a certain similarity is that of insect pollination, in which flowers compete with one another for pollinators. PLANT COMPETITION Nature and Kinds. By contrast with animals, the general lack of motility among plants renders their competition passive and hence inconspicuous, if not invisible. It is based upon reaction rather than coaction and is consequently more or less indirect in operation. Ex- PLANT COMPETITION 163 cept for the early stages in succession, crowding is a regular feature of the plant matrix, and both individual and species regularly bear the impress of competition in some measure. The process begins with increasing aggregation so that shoots or roots occupy the same space to a certain degree and thus make joint demands in excess of the available or immediate supply. However, this effect is really exerted through reaction, each leafy shoot reducing the light intensity and thus affecting its neighbor, while each root system reacts similarly upon the water content and solutes of the soil. No direct coaction is involved except for those rare instances where growth leads to the compression or heaving of tuberous roots, chiefly under cultivation. A similar passivity characterizes the competition among flowers for in- sect visitors, relative success or failure depending upon the form, size, and color of the competing flowers. The experimental study of plant competition as a process was dis- cussed by Clements (1905) and later w^as developed on a comprehen- sive scale in the prairie climax with Weaver (1924) and with Weaver and Hansen (1928). This concerned itself with transplant cultures, sod transplants, and denuded quadrats in subclimax and true prairie, and utilized a number of dominants, subdominants, and ruderals as paired competitors. These represented a variety of life forms and a large number of species, namely, tall, mid, and short grasses, annual and perennial forbs, shrubs, and trees. Similar studies were carried out in the ecotone between woodland and prairie in order to disclose the essential relations between forest, scrub, and prairie, and the nature of competition between individuals of the same species was analyzed in several field crops. The course and outcome of competi- tion were traced in terms of measured reactions, of functions, and of changes in form and structure to afford a detailed and coherent pic- ture of the entire process. The Factors in Competition. AYhile such indirect factors as humidity, pressure, and wind may have some effect upon the process, plants can actually compete only for energy or materials, namely, for light, water, nutrients, oxygen, or carbon dioxide. However, compe- tition for the last two is more or less exceptional, oxygen being at a deficit chiefly in saturated soil and carbon dioxide in pond and lake, the small amount in tlie air being kept fairly uniform through air currents. Of the three major factors, water is regularly first in im- portance in natural communities, light second, and nutrients last, though nutrients may stand first for intensive field crops. However, in temperate humid regions especially, water content may become of relatively little importance, while soil air or nutrients may become 164 AGGREGATION, COMPETITION AND CYCLES paramount, in accordance with the general rule that the factor pres- ent in the smallest amount relative to the demand will be the critical one. "With respect to layered communities, water is the decisive factor in the competition of the dominants of forest, scrub, or grassland. The grouping into the lower layers is largely an outcome of the com- petition for light, but within each layer it is probable that water is more important. However, in all but the most open stands, both water and light are concerned, and their relative significance is to be deter- mined only by a specific study. The Equipment of Plant Competitors. The most significant fea- ture of competing plants is the life form, since this determines the behavior and relations of shoot and root. It bears the ecological impress of climate and soil, and hence largely determines the response to the direct physical factors, as well as to the reaction due to compe- tition. The most telling characteristic of the life form is the duration or length of the life period, as a result of its effect upon occupation and to a large degree upon stature as well. Next in importance comes the rate of growth, which finds its most effective expression in the expanse and density of shoot and root systems, and the depth of the latter. Rate and amount of germination often yield an initial advantage difficult to overcome later, and these are related to the number and kind of seeds produced, which in turn are influenced by the competition among flowers for pollinators. Vigor and hardiness of root or shoot may also play a decisive role, since they frequently determine survival under unfavorable conditions, and especially under the stress of winter. Such qualities may be inherent in the proto- plasm itself, but as a rule they are related to growth and structure, and particularly to ripening and dormancy. In the final outcome, the species with the best equipment will furnish the dominants for the plant matrix, while those with some- what less advantageous features will become subdominants. It is doubtless a matter of primary significance that the dominants of climaxes are drawn almost wholly from the three types of life form, namely, trees, shrubs, and grasses. Competition among Flowers. In contrast to the competition among plants which rests chiefly upon the life form, that between flowers is based in some measure upon the taxonomic form. The actual success in attracting pollinators in large number depends mostly upon the size, color and odor of the flower, but with respect to effective visitors the form of the corolla and the arrangement of stamen, stigma, and PLANT COMPETITION 165 nectary are of decisive influence. Floral competition is at work in many communities throughout the season, but it is probably most in evidence in meadow and prairie in early summer, when it may have a critical effect upon fertilization and seed production. Some species avoid competition to a certain extent by blooming earlier or later, but the number of pollinators is likely to be less at such times also. More effective evasion is secured by species that flower at unusual times or for brief periods, as with nocturnal and many ephemeral blossoms. A decisive advantage may also be obtained by such speciali- zation as will favor a particularly skillful pollinator, such as red flowers which have long tubes especially adapted to hummingbirds. Competition between Plants and Animals. From what has been said previously, it is manifest that plants and animals will compete with one another only when they need the same thing. As a result, such a coaction is hardly to be expected of green terrestrial plants, but may occur with parasites and saprophytes, aquatic forms, and in small degree with soil organisms. Such competition is primarily for food, but it may concern materials, like lime and silica, or working conditions, as oxygen. Dependent plants must secure their food sup- ply from green plants directly or indirectly, much after the fashion of animals, and hence the two will come into competition with one another when they are living on the same host, even though not side by side. This is likewise true of saprobes, for example, bacteria and Infusoria, whether in water or soil, and it obtains in some measure in respect to geophilous fungi and the soil fauna. In both soil and water, there is inevitable competition for oxygen whenever the air content runs low, and a similar result ensues when great numbers of diatoms and radiolarians make excessive demands on the supply of silica, or coralline algae and anthozoans upon calcium carbonate. There are occasional instances of direct competition between plant and animal, such as is exemplified by the flower-spider, Misumena vatia Clerck, which deprives the flower of pollinators. Equally strik- ing, though less evident, is the competition between bladderworts (Utricularia) and young fishes, a relation that Forbes (1883, a, c) has emphasized as tending to decrease the number of fish. Ten bladders from a plant bearing several hundred contained 93 animals representing 28 species ; of the total, 76 belonged to the Entomostraca and 8 were insect larvae. In ponds or lakes with well-defined com- munities of this plant, it is evident that its competition might prove decisive, at least in local areas. 166 AGGREGATION, COMPETITION AND CYCLES ANIMAL COMPETITION Nature and Kinds. It is desirable to stress again the fact that competition comprises a relatively small number of the countless coac- tions among animals, and involves only those in which two or more individuals seek to secure the same object, class of objects, or space. Such competition is an evident coaction when it is direct, but it leads to a wholly different type of interaction in the destruction of one of the competitors. Competition between carnivores may often result in a third coaction, namely, that of combat, also not infrequent among herbivores when competing for mates. It is a well-known principle, emphasized by Darwin, that the struggle for existence is keener the more nearly identical the de- mands, and hence that competition is usually greatest between individ- uals of the same species. However, the investigation of competition by definite methods will doubtless reveal many exceptions. From its nature, competition is determined in the main by life form and in detail by behavior or life habit, though size or peculiarities of activity may also play a large part. All the animals of a particular district are in potential and often direct competition, though the smaller carnivores may take what is left of the kill of the larger ones. In nearly all cases the food preferences are overlapping near their mar- gins, rather than identical at the center or first choice. All examples of supposed competition outside of controlled con- ditions are open to some question. The black rat reached North America about 1775 and became well established before the brown or Norway rat arrived nearly a century later. Upon the arrival of the Norway rat, the black rat began to decrease in numbers and gradually disappeared until it has become rare. In the United States and Canada it appears to have survived in some large buildings in large cities because of its smaller size and has also survived in some one or two remote sections of the country districts. Whether the brown rat attacked and destroyed the black rat, or merely appropri- ated all the nesting places and food, there is no doubt that competi- tion was a factor. The large wolf was early reduced in numbers and extirpated from many areas, and this was followed by a great in- crease in coyotes. Apparently the wolf does not prey upon the coyote, but competition probably involved suitable home sites and hunting territory. Chapman (1931) is probably correct in referring to the limits of population imposed in cultures of Drosophila and of Tribolium in small spaces as due to competition, but has not presented the data TERRITORY 167 on the mechanism of competition and biotic control, as they have not yet been worked out. He called attention to the work of Pemberton and Willard (1918, a and 1918, b), relative to a number of insect parasites of the fruitfly introduced into the Hawaiian Islands. A species of Opius was most effective, as it parasitized a large percentage of the host; a species of Dichasraa was less so, but when both placed eggs in a host larva the less effective Dichasma overcame the Opius and survived. The conclusion was reached that the end result of the operation of both parasites cannot exceed that of the more successful one in any event. The equipment of competitors and the course of the process is generally more evident in animals than in plants, but even in the simpler examples too little is known about these as yet. However, the effect or the outcome is frequently visible in subordination, sup- pression, changes in habit, numbers, and so forth, and hence is felt in varying degree in the composition of the community concerned. Fin- ally, competition, like coaction in general, is sometimes important in connection with food, at other times in connection with shelter, space, or territory. Birds and mammals regularly exhibit a more or less definite competition for mates, and in some form this occurs in the large majority of animals; different herds or flocks in gregarious species not infrequently compete for what may well be termed eco- nomic position. Because of the difficulties attendant upon them, experimental stud- ies of competition among larger land animals are practically unknown, and until extensive exclusion and inclusion areas are available such study will be difficult. Except for the recent inquiries into competi- tion among insects and minute or microscopic aquatic invertebrates (Allee, 1931, a), little experimental work has been done. TERRITORY Territory among Birds. Although but recently reinvestigated, the concept of territory may be traced back for more than a century, but with only occasional mention or consideration until the work of Howard in England (1907, 1914, 1920; cf. Miller, 1931; Nice, 1933; ]\Iichencr and JMichener, 1935). It has now become the favorite theme of many ornithologists and has been taken up in other fields, such as those of mammals and insects. In the most typical instances among birds, it involves both direct and indirect coaction — combat, song, and the choice of a mate all exemplifying the former. In spite of the late emergence of the idea, territory has been much defined and redefined, and will doubtless experience much more re- 168 AGGREGATION, COMPETITION AND CYCLES finement with increasing objectivity. Howard (1920:73) states that each male establishes a territory at the beginning of the breeding sea- son, and there isolates itself from the members of its own sex. But the change is carried further, so that the bird becomes openly hostile toward other males with whom it had previously lived on amicable terms. The seasonal organic condition is responsible for the function- ing of the disposition that results in this intolerance, just as for that concerning the selection of a territory. This intolerance applies also to the selection of a mate. This may be summed up in the later brief statement that the male "isolates himself, makes himself conspicuous, becomes intolerant of other males and confines his movements to a definite area" (1920:64). Nice (1933:91) would limit the term still further: "territory can not mean just the nest spot when the adults feed in common; this may be the 'nest territory,' but is a very dif- ferent matter from a territory in its strict sense, to which the parents confine themselves during the breeding season. Again the very essence of territory lies in its exclusiveness; if a bird's range is not defended, it is not a territory." The extent of territory is supposed to be determined by the space available, as well as the amount of food in it; when food is scarce, the area required is larger. The boundaries are apparently arrived at by both direct and indirect competition, in connection with such fea- tures of the terrain as watercourses, openings, trees, bushes, etc. Once in possession, the male endeavors to keep all other males of the same species out of the area, and when their requirements are much the same, those of other species as well. Nice states that the complete procedure for acquiring a territory consists of four steps, namely, staking out the claim, the chase, the combat, and the final proclama- tion of ownership on the part of each bird {loc. cit., page 94) (Fig. 35). Conspicuousness of the male is regarded as an essential fea- ture of the process, which in passerines is chiefly secured through song, though the author states that the assertions made concerning the latter are pure theory. She further says that the bird students of the world "are in danger of going territory-mad," and it is patent that the present superstructure is out of proportion to its foundation, even Howard admitting in the preface of his book that much is mere speculation (cf. Errington and Hamerstrom, 1936:315, 398; Allen, 1934) . In a recent study of sex rhythm in ruffed grouse, Allen (1934) concludes that this has a direct bearing upon the problem of terri- tory, as the following excerpt indicates: "Bird behavior, including the earlier arrival of males than of TERRITORY 169 females on the nesting ground, and of adults than first-year birds; selection of territory, song, fighting and display of plumage are ex- plainable on the basis of the necessity of synchronizing the mating Fig. 35. — Map of song-sparrow territories. The letters A, B, C, represent the first, second and third nestings. (After Nice, 1931.) cycles of male and female. In order to insure the propagation of the strongest birds, the virile male must keep all other males out of his territory and must drive out all females that are not in the same reproductive cycle as himself, lest another male mate with his female 170 AGGREGATION, COMPETITION AND CYCLES or lest he waste his energy on a female that does not synchronize with him." Territory among Mammals. Red squirrels arc thought by Hatt (1929) to possess territories with a range of about 250 yards, within which they seem to know every tree and hole. They have been seen to drive off intruders, but the limits are evidently not fixed, since they go beyond them for food. Mice of the genus Peromyscus may have a home range about 100 yards in diameter, but P. maniculatus artemisiae (Rho.), has been known to return over distances as great as 5 miles. No dispersal of the young is definitely known, and many individuals find suitable homes roundabout the original one. The porcupine has also been assumed to establish territories with refer- ence to food supply and den sites (Gabrielson, 1928), breeding, shelter, and food all apparently being involved in the territorial coaction (cf. Klugh, 1927; Murie and Murie, 1930). Among the mammals that feed in the sea and breed ashore, as well as in certain sea birds, the selection and establishment of terri- tories are often accompanied by intense competition and fierce com- bats. In such instances food usually has little or no influence; thus, the males of the fur seal do not feed during the period of control of the harem territory, while the females may journey 50 to 100 miles to gorge themselves with fish (Preble, 1923). Howard also notes that in the guillemots the competition is necessarily for space in terms of nesting sites and not of food (1920:215). Heape (1931:28) brought together a fund of information bearing upon the territorial habits of mammals in particular, but much of this is of the nature of general and often isolated observation, and in consequence it possesses little significance. The treatment is far from critical as attested by the statement that wolves respect the territory of caribou when small game is abundant, but do not when the supply of rabbits fails (page 46). In addition, the fable of the happy family of rattlesnake, prairie dog, and burrow owl appears in a new form, in which the voracious Sphenodon and petrel live together amicably in the same burrow (page 47) . The inescapable tendency to broaden the concept of territory in order to fit all the facts is shown by Heape's distinction of a breeding or "home territory" ("almost invari- ably recognized as a sanctuary, though not always respected"!), a much wider "hunting territory," and a "neutral territory." Exclusive- ness is not regarded as essential, and the term territory loses its justifi- cation in all such cases (cf. Nice, 1933:91). Territory among Ants. Elton (1932) has outlined the territories of wood ants [Forniica rufa) in a bird sanctuary in southern England. TERRITORY 171 The ants were chiefly engaged in "farming" the aphids on the trees and shrubs, especially the birches. Trackways extended from each nest to such trees as seemed to determine the size and form of each territory. Some of the trackways persisted in relation to the same trees for the period of three years, but others changed as a result of invading parties or the apjiearance of new trees. Each nest possessed B""~~ -----. ^^'M ©5 Q- ©10 /T"! /'G Fig. 36.— Sketch-map, July 20, 1929, of wood-ant trackways and nests in bird sanctuary at Picket Hill. Black dots are nests; circles with dots are places of former nests; broken hues are trackways; barred lines are fences or hedges; some, but not all, birch trees are put in {B), including majority visited by ants. Track from nest 1 outside the hedge continued 100 feet further west among gorse bushes (G). Approximate positions of willow wren nests in 1929 are showTi by four crosses. (After Elton, 1932.) its own distinct system, but there was normally no hostility among the families, and hence no defense of territorial rights was needed. However, the respect for such rights was not sufficient to prevent raids and the destruction of a nest (Fig. 36) . Elton's account indicates that the territories observed were pri- marily a consequence of convenience and efficiency. Observations by the senior author of a vast aggregation of harvester ants {Messor species) in a community of Aristida, in the Colorado Desert, indi- cated that there w^re no definite trails and no territorial limits (see Fig. 17, page 83). In a neighboring region where four species were busily engaged in collecting grass fruits, the trackways intersected 172 AGGREGATION, COMPETITION AND CYCLES in all directions, so that independent ranges were out of the question in these species. However, in general, -territories and runways are usually distinct and nests spaced well apart. BIOTIC BALANCE The older naturalists expressed the untenable view that a stable, static equilibrium existed among the organisms of any community, and in nature in general. It was further thought that fluctuations in populations of insects pests and other small forms were due to biotic modification by agricultural practices. This appears to have been assumed (Forbes, 1880, a, and others) in the face of locust outbreaks in the undisturbed western grassland to the contrary. Forbes says: "There is a general consent that primeval nature, as in the uninhabited forest or the unfilled plain, presents a settled harmony of interaction among organic groups which is in strong contrast with the many seri- ous maladjustments of plants and animals found in countries occupied by man." In regard to the larger animals whose life histories and life spans are long and whose rate of replacement is slow as compared with the rapidly reproducing rodents and invertebrates, there is some evidence for distortion of equilibrium as regards numbers. Disturbance of bal- ance in the deciduous forest is suggested in a diagram by Wood (1910) , which is reproduced in Fig. 20, showing an increase of deer accom- panying the decline of predators. The fact that prairie dogs increased with the reduction of wolves and coyotes (INIerriam, 1901) is further evidence of some kind of a balance among the larger forms. Increase of deer to a point endangering their food supply has occurred repeat- edly in recent years under protection and the reduction in numbers of predators. Such facts, so far as experience had brought them to atten- tion a half century ago, were perhaps responsible for the idea of a stable equilibrium in regions not affected by man. A natural result of this view has been so much tampering with communities in the name of agriculture, game conservation, and the preservation of rare species that it has been difficult to ascertain what the normal fluctuations are. Custodians of parks, forests and game preserves have usually viewed all declines of popular animals and all increases in unpopular ones with alarm, and immediately proposed and often executed useless or detrimental remedial measures. The difficulty has arisen from the fact that normal fluctuations in abundance in areas not influenced by man had been but little studied. However, in the past decade, investigations have brought BIOTIC BALANCE 173 out the fact that such fluctuations occur in the sea relative to animals little influenced by man's activities (Blegvad, 1925) and in the arctic regions where such influences have affected only some of the larger species. This knowledge has been responsible for a new view of biotic equilibrium which assumes, as normal, a rather wide fluctuation in the number of individuals for many species. Frequently, several species rise to a maximum or sink to a minimum at about the same time. The abundant species react upon the habitat and destroy or provide food for other organisms, but the onslaught on the excess population due to flexibility of food habits, or the pressure of climate and the limitations of shelter and food supply, are the important fac- tors in checking the increase of various species. In addition, disease may become a factor. Elton (1930:17) is a strong advocate of a continuing state of lack of balance in nature, as the following excerpts indicate: " The balance of nature' does not exist, and perhaps never has existed. The numbers of wild animals are constantly varying to a greater or less extent, and the variations are usually irregular in period and always irregular in amplitude. Each variation in the numbers of one species causes direct and indirect repercussions on the numbers of the others, and since many of the latter are themselves independently varying in numbers, the resultant confusion is remarkable. 'T shall take from this region one example, which illustrates very clearly the vast degree of unbalance that nature presents to the un- aided eye. . . . Any animal community that is watched for a number of years presents a restless picture of unending changes in numbers, which are more often than not accompanied by striking changes in their habits of life. "This instability is partly due to the external influences, and partly to the inherent manner in which every animal community is con- structed. The environment (and in particular the climatic factors of the environment) does not remain the same from day to day and year to year. These changes react on the animals either through their direct effect or indirectly by affecting the plant-life of the region. On the other hand, internal factors dependent upon the manner in which animal communities are organized, also play a part in upset- ting the balance of numbers. Epidemics caused by parasites are a very important example of this, while the change of habits consequent on the scarcity of food forms another. Irregular migration is one of the most important of all." Criddle (1930) has pointed out a series of interactions connected 174 AGGREGATION, COMPETITION AND CYCLES with maxima of the sharptailed grouse in southern Manitoba. He states that the maxima for this grouse are preceded and accompanied by grasshopper outbreaks or maxima, the enhanced food supply being the primary cause of the rise. Furthermore, the beginning of a grass- hopper maximum is nearly always preceded or followed by abnormally dry seasons, and the increase may be stopped by excessive rains. The decline in the grouse cycle is attributed mainly to heavy rains and cold, which reduce the amount of food taken to the nest by a third, owing to the inactivity of insects, and thus results in starving the young birds. Disease is regarded as the probable major factor in the reduction of the adults, but they are also decimated by the goshawk, a single predator destroying as many as 50 grouse in a winter. Griddle's explanation ignores possible direct physiological effects of the climatic factors in limiting populations, but nevertheless gives a broad explanation of the observed facts. The view of Uvarov (1931) likewise takes food and predators into account along with climate: "The theory of stable equilibrium is based on the assumption that the numbers of an organism depend mainly on the numbers of their enemies and on the quantity of food, i.e., on factors which in their turn are dependent on other organisms. No one will deny the controlling value of these factors, but the evidence col- lected in this section, as well as in the whole of this paper, should go far towards proving that the key to the problem of balance in nature is to be looked for in the influence of climatic factors on living organ- isms. These factors cause a regular elimination of an enormous per- centage of individuals under so-called normal conditions, which in fact are such that insects survive them, not because they are perfectly adapted to them, but only owing to their often fantastically high re- productive abilities. Any temporary deviations in the climatic factors, however slight they may be, affect the percentage of survival, either directly, or indirectly (through natural enemies and food-plants), and thus influence abundance." Nicholson (1933) has recognized the importance of climate and enemies, but also points out the limitations of climate in rather strong terms, as follows: "We will suppose tliat the animals in a certain population would increase one hundredfold in each generation if un- checked, and also that, on the average, climate destroys 98 per cent of the animals. It is clear that the number of animals would be doubled in each successive generation if no other factors operated. Climate could never check this progressive increase, for it would con- tinue to destroy only 98 i)er cent, its action being uninfluenced by the density of the animals. If, however, there is some other factor. CYCLES AND NUMBERS 175 such as a natural enemy, the action of which is governed by the density of animals, the destruction of the remaining 1 per cent, necessary to check an increase, would soon be accomplished. If this example were observed in nature, one would be tempted to conclude that, because climate destroys 98 per cent of the animals while the natural enemy destroys only 1 per cent, the limitation of the popula- tion is mainly due to the influence of climate. However, it is clear that the natural enemy is wholly responsible for control, because climate, by itself, would permit the density of the population to be- come indefinitely great." He further concludes that there is a particular or "steady" den- sity at which balance exists for each species, and that competition always tends to cause animals to reach and maintain this density. Climate and animal behavior "cannot themselves determine popula- tion densities, but they may have an important effect upon the values at which competition maintains these densities." It appears that these views fail to take into account the climatic cycle and its signal effects, and there is also grave doubt that the statistical approach is applicable to such an intricate complex of causes and effects. Power- ful as competition is in the community, its action may be largely or almost entirely suspended, in the plant matrix at least, by optimum climatic or edaphic conditions. In his studies of the wintering of quail in Iowa in relation to popu- lation, Errington (1934) reaches the following conclusions: ''Food is the first essential constituent of a winter quail territory; cover is the second. The quality, distribution and convenience of food and cover, together with the bobwhite's intolerance of crowding, probably deter- mine in largest measure the carrying capacity of environment for the species. "Cover is of value to the bobwhite chiefly as protection or con- cealment in case of attack by enemies. Lack of cover means vulner- ability to predation, whether enemies are few or many. Cover also has a certain value as shelter during periods of wet or cold weather, or during storms, but the necessity of shelter for the bob-white is usually over-rated about as much as escape cover is under-rated." For the southeastern United States, the earlier account by Stoddard (1931) is a mine of information as to causes of dynamic balance in fiuail populations. CYCLES AND NUMBERS Several important cycles of different character and rank find more or less definite expression in the structure and development of the biome. Chief among these are climatic mass migration and succes- 176 AGGREGATION, COMPETITION AND CYCLES sion, while annuation, aspection (including hibernation and estiva- tion), and diurnation represent a descending scale of effects. All these processes are concerned with numbers in varying form or degree, though this is particularly true of annuation, which comprises the fluctuations from year to year. With respect to the plant matrix, the primary influence is one of structure, and hence these topics are mostly considered in a later chapter (Beveridge, 1921; cf. Taylor, 1934; IMcAtee, 1936) . By contrast, cycles of animal reproduction and migra- tion are characterized by outstanding changes in population, often directed by competition, and are properly treated as more or less correlated results of the same or similar causes. Closely associated with them is the problem of dynamic balance or equilibrium in the biome, a condition that has usually been regarded as a more or less static norm. Since land plants are stationary, fluctuations in their numbers are less dramatic than with animals, but they are of the same order and, as food and shelter, often assume a prior role in the causal sequence. Such phenomena are most evident in annuals, as these are more sus- ceptible to the climatic features of a single year. The most striking instances are afforded by winter annuals in the Southwest; these may be present by billions in arid grassland or in the Colorado and Mohave deserts one year, and all but totally absent the next when the rainfall is seriously deficient. Similar "flushes" are exhibited by phytoplank- ton in small or shallow lakes, particularly by the blue-green algae; fleshy fungi often display great variation also and many parasitic species as well. With perennial forbs and grasses, the departures are naturally much less striking, the annual effect being expressed largely in num- ber and height of shoots and in seed production, since the competition of parents precludes the ecesis of most of the offspring. The produc- tion of dry material, as well as of seed, may vary severalfold, and this is directly reflected in the coactions of grazing animals in par- ticular. With woody plants, the increment of each year is diffused over all or most of the plant in the form of an annual ring and as short twigs, and hence is hardly to be noted. However, more notice- able fluctuations are recorded in the seed crop, especially of conifers, oaks, hickories, etc., and reflected in the ecesis, as well as in the coac- tions of seed-eating animals. All these growth responses bear a more or less definite relation to the sunspot cycle, and it is an interesting fact that this relation was first seen in the annual rings of trees (Douglass, 1909) and was later extended to vegetation in general (Clements, 1916). ANIMAL CYCLES 177 ANIMAL CYCLES The question of animal cycles has been a subject of interest for more than a half-century, though the locust plague, as the most serious expression, has been a matter of concern for hundreds of years. Scien- tific activity in this field has been much stimulated by the work of Collett with the lemming (1895) and the observations of Seton in Arctic America (1911) , and today it constitutes one of the most signifi- cant, as well as most difficult, lines of research in bio-ecology. How- ever, as a field in which quantitative methods are paramount, the study of animal populations in nature still lingers on the threshold. It is manifest that many species have already dwindled beyond the point at which their fluctuations can be profitably investigated, a con- sequence that rules out practically all settled districts. So far as mammals are concerned, only regions in high latitudes hold much promise, but these are the very ones, as a rule, in which the difficulty of resident study over a long period all but eliminates adequate quanti- tative determinations. In the succinct account that follows, it should be constantly borne in mind that numbers and cycles are still based, for the most part, upon general and incidental observations and that discrepancies and contradictions are frequently to be encountered. Moreover, the only records that approximate accuracy are those of the fur returns of the Hudson Bay Company, and it is obvious that even such data as to populations fail in complete accuracy. Nature of Animal Cycles. Cycles are characterized by alternating phases of plus and minus departures that pass more or less gradually into each other, the sunspot cycle being the best-known example. Cycles in populations are rather more variable, the rise to a maximum or the fall to a minimum occasionally occurring in a single year, while a high or low level may be maintained for two or more years. Low levels are the rule with desert annuals, a "flush" appearing only at intervals of several years. Low levels are likewise frequent in animal cycles, but maxima nearly always take the form of sharp peaks, as illustrated by the rabbit curve (Fig. 37). Fig. 38 shows seasonal variation in insect larvae and suggests an unusual abundance for Chironomus bathophilus for 1935. In mammal cycles, the fall to the minimum has been regarded as a catastrophe that signalizes but one or, at most, two seasons, and hence has been commonly known as the "crash." However, an inspec- tion of the curves of furs taken makes it clear that the rise is rapid quite as often as the fall and that the idea of a crash is in part due to the necessarily local, brief or discontinuous and superficial observa- 178 AGGREGATION, COMPETITION AND CYCLES ANIMAL CYCLES IN THE FAR NORTH ANNUAL TAKE OF FURS BY THE HUDSON'S BAY CO., 1821- 1910 VEAR T,,lM,fP?M, 164-0 1 1 1 1 1 1 1 1 1 1850 1 1 1 1 1 1 M 1 llM 1660 M 1 1 1 1 1870 1 1 1 1 1 1 1 1 1 1 1860 1 1 III 1 ml 1890 1 M I 1 M 1 1 1900 1 1 1 1 1 1 I9K 1 1 M 1 1 1 SUNSPOTS M Mm M M M M M M M _ M M M M M M 40 _ r^_^A,.._--— ^-- ^--^V^V_.rv-^-v-Y_^ z . < 250- ,' • t / &200 z / O ISO RABBIT ,' n 100 rAA \ l\ l\ A 50- L / \a \ M \ / \X\ ^ -.^ ^_ / "^ ^\ V J ^^ "^ VAy \ Fig. 37. — Sunspot cycles are shown in connection with Hudson Bay fur receipts. Small capital M indicates minimum and large capital M indicates maximum. 1923 1924 Fig. 38. — Showing variation in the number and weight of the larvae of Chiro- nomus from month to month, April, 1923, through April, 1925, in Flatten Lake (Ploner Becken). The short dashes are for the numbers of C. hathophilus larvae; the long dashes for the numbers of C. qylumoms larvae; and the dot-dash line is for the total weight of larvae of both species. This is the average for the whole lake for the second year and all but the zone 0 to 4 meters for the first. (After Lundbeck, 1926.) ANIMAL CYCLES 179 tions upon the fluctuations of numbers. Such defects in the method appear inescapable, and hence the data derived from the fur trade will probably for some time remain the best quantitative basis for studying cycles among animals. An examination of the rabbit curve (Fig. 37), shows that the greatest change in a year was a drop from about 285,000 to about 20,000 skins during 1845-46, while over against this are two rises of a year each. The following table for the rabbit and lynx permits a TABLE 3 Phases of Rabbit and Lynx Cycles Rabbit Lynx Phase Period, Years Dates Rate M. Phase Period, Years Dates Rate M. Low. . . 5 1821-25 5-10 Rise . . . 5 1826-30 5:35 FaU.... 2 1831-32 85:5 Low . . . 3 1833-35 5-15 Rise . . . 3 1836-38 5:65 FaU.... 4 1839-42 65:5 Low . . . 1 1843 5 Fall 1 1845-46 285:20 Rise . . . 4 1844-47 5:45 Low .... 3 1847-49 15-25 FaU.... 3 1848-50 45:10 Rise .... 4 1850-54 20:90 Low. . . 3 1851-53 10:5 High... 3 1855-57 70-95 Rise. . 3 1854-56 5:30 FaU. . . . 3 1858-60 95:15 High. . 2 1857-58 30 Low. . . 3 1861-63 5-40 FaU.... 4 1859-62 30:5 Rise . . . 1 1864 5:155 Low. . . 2 1863-64 5 FaU.... 5 1865-69 155:5 Rise. . 3 1865-67 5:80 Low . . . 3 1870-72 5-10 FaU.... 4 1868-71 80:10 Rise . . . 4 1873-76 5:105 Low. . . 2 1872-73 5-10 FaU.... 3 1877-79 105:15 Rise. . 4 1874-77 10:40 Low. . . 4 1880-83 10-20 FaU... 5 1878-82 40:5 Rise. . . 4 1884-87 15 140 Rise . . . 5 1883-87 5:80 FaU.... 3 1888-90 140 20 FaU.... 4 1888-91 80:5 Rise . . . 6 1891-96 20 90 Low. . . 1 1892 5 FaU.... 4 1897-1900 CO 5 Rise . . . 4 1893-96 5:55 Low . . . 3 1901-03 5-15 FaU.... 4 1897-00 55:5 Rise. . . 1 1904 5:45 Low. . . 2 1901-02 5 Fall.... 4 1905-08 45:5 Rise . . 4 1903-06 5:60 FaU... 3 1907-09 60:5 Low . . . 1 1910 5- Rise . . . 3 + 1911-13 + 3 + 180 AGGREGATION, COMPETITION AND CYCLES clearer view of the intervals than the curves do, and also makes it possible to determine the average length of rise and fall as approxi- mately 3.3 years. These figures would seem to dispose of the "crash" as anything more than a rare catastrophe. They constitute a direct contradiction of the statements that "in a few weeks usually, the rabbits are wiped out," and that "to explain the variations we must seek not the reason for the increase — that is normal — but for the destructive agency that ended the increase" (Seton, 1911; cf. Leopold, 1931, 1934). CAUSES OF ANIMAL CYCLES In some cases the rise in abundance is important; in others, the decline. There are cases in which the decline affords the key to the explanation, while in others some special factor brings about an increase and the reverse causes a decline. It is customary to view cycles as produced by conditions favor- ing reproduction and survival; however, all plants and animals pro- duce more spores, seeds, eggs, or young than can normally develop to maturity. Under ideal conditions the tendency for any species is in the direction of an almost unlimited population. Such large numbers are unattainable because of various forces which tend to reduce the number of individuals. Small reproductive populations, though fre- quently a contributing factor, are responsible for minima, if at all, only in special types of life histories, such as that of the salmon. The maximum may appear important in one case, the minimum may be equally so in another. For convenience, the problem of fluctuations in abundance, whether these be cyclic or irregular, may be approached more often from the standpoint of the causes of failure to produce large populations of mature individuals or, in other words, causes of small populations. There are eight causes of failure to produce a large number of late juvenile or adult offspring, which means the decrease in numbers of any abundant species. They are (1) decrease in the number of eggs produced or fertilized, owing to various causes, or destruction of eggs and very young stages; (2) death of adults and late juvenile stages from adverse physical conditions; (3) destruction by enemies and dis- ease; (4) quantitative or qualitative insufficiency of food; (5) unsuc- cessful competition for space, shelter, or food; (6) physiological changes in reproductive vigor; (7) initial shortage in reproducing population; (8) cannibalism. To these may be added certain assumptions such as loss of immunity, etc., but of these little is definitely known. Loss of Eggs and Early Stages. The codfish affords a noteworthy example of loss of eggs after fertilization as well as before. Though CAUSES OF ANIMAL CYCLES 181 each female deposits from 3 to 9 million eggs annually, the North Sea is said to contain less than 45 million cod, of which about 23 million are probably females (Johnstone, 1908). The eggs must be Abra Solen Nucula Corbula Recti - naria ^ (£) ^ <^ ^ m ^^ 4S» & 4^ €> fy 9^ ^ ^t €> « «>««««•««> «< ^ ^ o ). A, B, and C, mark clumps of overbrowsed aspen stems. (Courtesy U. S. Forest Sendee, W. G. Mann, Supervisor. Photo by H. L. Andrews, 1936.) Since the equipment of sessile organisms differs more or less in all three respects noted above, there are corresponding differences in the degree of dominance. These are reflected primarily by the life forms and secondarily by size, abundance, or both. On land, at least, the first is peculiarly decisive as to the period of dominance, and hence regularly marks the distinction between the dominants of climax and sere, and the successive stages of sere. By contrast with plants, land animals exhibit very little direct structural response to the habitat, but exert more or less reaction upon it, chiefly through disturbing the soil. Their competition is mainly connected with shelter and food coactions, and not with reaction. On THE STRUCTURE OF CLIMAXES 237 the contrary, aquatic sessile and sedentary animals resemble plants more or less closely in all these respects. Influence. In the case of land animals, the chief effect is exerted through coaction upon plants, and their role is commonly one of in- fluence rather than of dominance. Although burrowing animals regu- larly exercise a definite reaction upon soil, this rarely leads to the destruction of the plant matrix. Modification of it is a more frequent consequence, as exemplified by the hills of mound-making ants anrl Fig. 536. — An exclosure plot .showing the large growth of aspens at the edge of a parklike opening, Kaibab forest, 1936, when protected from deer. (Courtesy of the U. S. Forest Service, W. G. Mann, Supervisor.) The exclosure was similar to the area shown in Fig. 53a at the time of fencing. (Photo by H. L. Andrews.) those in prairie-dog towns. Moreover, though influence may some- times produce striking changes in the appearance of a community, as in the short-grass condition of the mixed prairie, it does not often lead to permanent transformation. Even in the short-grass com- munity or disclimax, the mid grasses are regularly present in sup- pressed form, and attain expression during wet phases at least. Influence is the outstanding characteristic of the animals of the terrestrial biomes, and constitutes the basis for placing them in the proper ecological relation to plants, as well as to each other. This applies likewise to man under primitive conditions, especially before 238 CLIMAX AND SERE dominance resulted from cultural accomplishments such as the produc- tion of steel (Shelford, 1935). But civilized man has also become a reactor through extensive development of human culture. Lumber- ing, as a direct coaction, and grazing, as an indirect one, produce re- action only incidentally, but fire, clearing, cultivation, draining, flood- ing, and construction regularly react on soil conditions and often extend over wide stretches. It is evident that influence, like dominance, depends upon the life form, and in a large degree upon size and abundance as well. This is particularly true of the basic coactions that concern shelter and food material. In all such relations, the animal typically assumes the active role and the plant a passive one, and hence it is not desir- able to treat the plant as an influent, unless it is parasitic or poisonous. Coactions of introduced parasitic plants have at times produced strik- ing results, e.g., the chestnut blight which has practically destroyed the typical dominant of the oak-chestnut association. In water, some animals play the part of dominants, as distinct from that of influents taken by others. However, influence is more commonly exerted upon other animals than on plants, though plankton-eaters devour both the plant and animal members of the microplankton. Kinds of Dominants. Apart from the obvious distinction of dominants as plant or animal, land or sea, climax or serai, they have been distinguished on the basis of their role in the community (Clem- ents, 1916, 1920, 1928; Shelford, 1935). The major division in land communities is into dominants and subdominants, and it is probable that this applies to some aquatic ones also, especially in the benthic climaxes. The term codominant has been variously employed, usually for one of several dominants. In this sense it appears to be super- fluous, and it is here proposed to utilize it for dominant species be- longing to the other kingdom, such as seaweeds in the ocean and carp in ponds. From the standpoint of the food nexe of lake and ocean, the minute forms of the plankton possess an importance quite out of proportion to their size. In recognition of this fact, they have been termed ve- dominants {ve-, small), a treatment further justified by their direct response to the hydroclimate and their reciprocal reaction upon it. Similar small or microscopic organisms take the leading part in the short succession, or senile {-ulus, diminutive), typical of dead plants and animals, logs, food masses, etc. To these, the term dominule is applied, in taking account at the same time of their role and size. The Dominant. According to the prevailing interpretation, a dominant is an organism with such definite relations to climate and THE STRUCTURE OF CLIMAXES 239 such significant reactions upon the habitat, or in water upon the other community constituents, as to control the community and assign to the other species subordinate positions of varying rank. The resulting interrelations have been analyzed in considerable detail for land-plant communities (Clements, Weaver, and Hanson, 1929), but it is quite probable that the zoophytes of coral areas exhibit them in a degree not unlike that of grasses and shrubs. The graded series from these to the motile dominants of marine pelagic and fresh-water biomes pre- sents such relations in constantly diminishing measure, but when more is known of the response, reaction, and coaction of the animals con- cerned, it is probable that pronounced dominants will be found throughout. The major characteristics of dominants may be indicated as fol- lows : 1. Dominants receive the full impact of the climate or of the aerial factors in the case of terrestrial seres. 2. They are the species best adjusted to climate or habitat as the case may be, and hence are regularly most abundant in terms of density or weight, as well as most stable in reproduction. 3. They react directly upon the climate, modifying water and light relations especially on land, and the gas and salt content in the sea. 4. Climax dominants take possession of territory and hold it against all comers as long as the climate oscillates only within its proper range, while the occupation of serai dominants is limited by the succeeding stages. 5. Climax dominants are able to continue to grow and reproduce in the conditions due to their reactions, while serai ones react upon the habitat in such a way as gradually to favor the invasion of their suc- cessors. 6. Dominants on land, by virtue of life form and abundance in particular, are the major sources of food, material for building, and shelter, and usually constitute the basis for the ruling coactions, which serve as a primary bond in the biotic community. 7. Codominants are essentially dominants in terms of reaction or coaction and control, but differ from the typical dominants of the community in the nature of these processes, since they are consti- tuted by plants in communities chiefly dominated by animals, or the reverse. Subdominants. A subdominant has been defined as a species that exhibits a secondary dominance within the area controlled by a dominant. It gives character to pure or mixed societies, either spatial 240 CLIMAX AND SERE or seasonal, in the climax, and to similar socies in the sere. Sub- dominants are the successful competitors among the species that ac- cept the conditions imposed by the dominants. In grassland, they are the outcome of a double competition, namely, among themselves as well as with the dominants; in forest the struggle is chiefly between the species of the layers. They regularly differ from the dominants in life form, consisting of forbs in grassland and desert, and of forbs and shrubs in forest. Their alternation over an area or through the sea- son is largely determined by competition, which is decreased or evaded in some degree by such a disposition. From the nature of their relation to both habitat and dominant, subdominants on land are very generally restricted to plants, the cor- responding groups among animals being termed influents. In water, where the chief dominants are animals, societies, and to a smaller extent socies, are undoubtedly to be found (Eddy, 1934) , but the necessary analysis has barely begun in lake and river, and in the ocean. It is already evident, however, that subdominants occur in the pelagic communities, both fresh-water and marine, and often char- acterize striking seasonal societies. Dominants in Aquatic Communities. In fresh water, no true cli- maxes appear to be established outside of sluggish rivers and large lakes, and the dominants are hence usually serai in character. The rooted marginal vegetation, which produces such notable reactions as the filling of lakes, marshes, and bayous, all belongs to the hydro- sere of the climax of the region in which the body of water occurs. The tidal climaxes exhibit successions (Hewatt, 1935), and both serai and climax dominants occur in them, though the latter are much more numerous and important. Since this includes a belt of the marine algae, it also exhibits codominants, which form faciations or locia- tions in respective climaxes. Serai dominants probably play a small part in the deeper parts of the ocean, owing to the constancy of conditions and the lack of processes that produce bare areas. However, the great physical dif- ferences at various depths appear to dcmark horizontal climates with corresponding climaxes and dominants (Fig. 73, p. 317). The latter differ greatly in life form as a rule and exhibit even greater differences in size. For these reasons in particular, it seems possible to set the phytoplankton or producents and the small zooplankton consuments apart as miniature dominants. The chief organisms of the pelagic and bcnthic climaxes are best characterized as dominants in the usual sense, while those less important but still significant in abundance or importance are miniature dominants. As suggested earlier, it is not THE STRUCTURE OF CLIMAXES 241 unlikely that quantitative studies on a larger and more extensive scale may also render it desirable to distinguish societies of subdominants, especially in the benthos. Kinds of Influents. As indicated previously, the term influent is practicall}' to be restricted to animals because of their role as co- actors. In water climaxes, the effects of animal dominants have not been evaluated as to the relative importance of reaction and coac- tion. Influents fall less definitely into the primary categories of dominants, namely, land and water on the one hand, and climax and serai on the other. They may in time be gi'ouped in accordance with importance of coaction into various categories, such as major influ- ent, minor influent, subinfluent, and veinfluent. Lack of knowledge and opportunity for the study of the more important influences due to extirpation and reduction in numbers, and fluctuation in abundance, renders such classification difficult in some communities at present. Major influents include the larger mammals and birds or intermediate forms of marked coactive significance, the fishes, and other aquatic organisms of considerable size or vast number. Minor influents com- prise the smaller rodents, insectivores, bats, most of the birds, am- phibia and reptiles, and a host of marine forms. Subinfluents embrace the larger insects, arachnids, snails, isopods, etc.; and veinfluents, the disease organisms, micro-insects, the fauna of the soil, and the macro- and microplankton. Though no hard-and-fast line can be drawn be- tween these groups, especially in the present state of our knowledge, they may serve to bring out the comparative roles of coactors in a particular community. On the basis of abundance and time of appearance, smaller influ- ents may be classified as prevalent or predominant when they are present in numbers throughout the several significant seasons, as sea- sonal when they occur during one or two aspects, such as spring, sum- mer, etc., and as cyclics, when they exhibit marked fluctuations or appear only at intervals, like certain cicadas. The larger influents may fall into a similar grouping, though quite possibly their fluctua- tions were less under primeval conditions. In many cases, migratory species are influents in more than one climax and hence must be listed as seasonals in two or more communities. Animals probably do not range outside the biome in which they are influent farther than plants, except when migratory; for example, a few grasses dominant in the prairies may range east into New England in dry sandy spots, but they bear no significant relation to the deciduous forest climax. The difficulty on the animal side arises from lack of evaluation as to abundance and lack of appreciation of the intricate interlacing of 242 CLIMAX AND SERE biomes at their borders. No special terms to apply to the range of animals seem necessary, since the significance of the few exceptions to the usual rule can readily be discussed without them. The most illuminating facts in regard to the animals of a biome are found in the relation to climax and sere and to permanent bodies of water, such as rivers and large lakes that are not necessarily serai. The relations of plants to early serai stages and to watercourses were long ago recognized in Schimper's (1898) distinction between climatic and edaphic communities. This stands in sharp contrast to the at- tempt of Merriam (1890) and his followers to mix the two and use edaphic or local climaxes species as indicators of life zones supposedly based on temperature. Schimper's suggestions laid the foundation for further development of succession and other dynamic ideas, while the life-zone view has served to confuse values. Choice of habitat by each species of animal constitutes an im- portant response, expressed chiefly by the term niche. While Elton (1927) employs this word to sum up the relations to food and enemies, so that it is largely synonymous with coaction, Grinnell (1928) and Park (1931) used it in the sense of place. For purposes of locat- ing the animal in the biotic community and defining its life habit, the space relations, plant matrix, specific plants frequented, and soil and water requirements are of first importance. INIany animals occupy several minor habitats during their life history, a fact well illustrated by the bobwhite, which according to Leopold (1933) requires some- what distinct places for rest, sleep, nesting, drying young, and hiding with and without snow cover, whereas the deer of the Lake States requires five types of places for its different activities. Other animals resemble the deer and bobwhite more or less in this respect, and hence niche is often a compound space concept, to which role of food and enemies must be added, and the term then becomes synonymous with life requirements. The life requirements of many large influent species during the yearly cycle include a series of different places, thus bringing them into contact with most of the serai stages of the region and with the climax. Such influents have been termed permeant. On the basis of size, they may be divided into major and minor permeants. The boundary line between major and minor is based on the inability of the major influents to hide in vegetation, hollow logs, etc., while minor influents can do so readily. Influents that are confined largely to the serai stages may be termed serai, those confined to the climax, climax influents. Further, because of the great difficulty of estimating THE STRUCTURE OF CLIMAXES 243 degrees of influence, the term arthropod influent may well be applied to the numerous insects, arachnids, etc. (Shelford and Olson, 1935). Structure of the Climax. Each climax is the product of climatic differentiation operating upon an original community of vast extent and fairly uniform composition. Such a climax under the compulsion of climatic shifts became a panclimax comprising two or more cli- maxes. The best illustrations of this process today are to be seen in the circumpolar tundra, coniferous forest, and prairie-steppe pan- climax or panformation, each of which is divided into an old and a new world climax. Such a process of community evolution has op- erated alike upon the plant dominants and the animal influents. The old and new world biomes are as closely related in one as in the other respect, while the community bonds in terms of coaction espe- cially are very similar, when not identical. Major Units of the Biome. The climatic factors that produced climaxes or formations have continued to act, with the consequence that each biome has been further differentiated into divisions known as associations. The common origin of the associations of a forma- tion is still attested by the fact that the dominant genera are largely the same throughout and that several species serve as "binders" (or pcrdominants) between the various divisions and especially the con- tiguous ones. This principle is well exemplified by the grassland formation in which the dominants are certain species of Stipa, Bou- teloua, Sporobolus, Agropyrum, Koeleria, and Andropogon that occur over most of the climax area, while such dominants as Stipa comata, Koeleria cristata, Bouteloua gracilis, and Sporobohis cryptandrus re- cur in nearly all six associations. The distribution of influents is comparable to a large degree, as is indicated by such animals as Bison bison, Antilocapra americana, Canis nubilus, Taxidca taxus, and species of Citellus, Dipodomys, and Geomys. In their turn, associations are divided into faciations, on the basis of subclimates as reflected in the entrance or disappearance of one or more dominants. Although faciations have now been recognized in most of the major associations of the continent, such analysis has been carried out most completely in the mixed prairie, which is thought to represent the original matrix of the grassland climax. The presence of Buchloe dactyloides as a major dominant marks a central faciation, Hilaria janiesi and Stipa pennata a southwestern one, and Festuca ovind, one at high altitudes. To what extent animal influents are to be correlated with such units is at present uncertain, but there are at least some examples of agreement. The faciation itself may be char- 244 CLIMAX AND SERE acterized by subordinate groupings of dominants. These minor units are termed lociations, and as the name indicates are relatively local in extent, occupying a few thousand square miles. They have been studied chiefly in the grassland, and their biotic composition is almost untouched as yet. In the sea, all the essential relations described above for the mixed prairie are evident in communities of the sea bottom about Denmark (see Chapter 7) and in Puget Sound. Weese (in Shelford et al., 1935) described a series of faciations in the bivalve-annelid community of a narrow bay. Faciations also occur in the large gastropod-echinoderm communities in the same region. Marine lociations are best illustrated in the Balanus-Littorina biome of the Pacific Coast of North America, where Rice (1930) and Towlcr (1930) have described many peculiar local variations in the arrangement of barnacle dominants. These are explained by Rice (in Shelford et al., 1935) as caused by the com- bination of low tides and warm sunny weather during the seeding and early stages of the barnacles. She points out that the arrangement of the dominant species is controlled by mortality, etc., during accidental combinations of conditions, a fact that leaves the arrangement of adults and nearly grown individuals without meaning unless the series of past events is fully known. Among plants, a concrete community, the consociation, stands by itself as a climax unit consisting of a single dominant. In associations with several dominants, such as grassland and deciduous forest, con- sociations reach expression regularly only in limited areas that are especially favorable to each. However, when the major dominants are but two or three in a particular association, one of these may form an almost pure community over a large area. This is true of Pinus ponderosa and of Picea engclmanni in the Rocky Mountains, of Pseudotsuga mucronata on the Pacific Coast, of Artemisia tridentata in the Great Basin, and of Larrea tridentata in the deserts of the Southwest. In the bunch-grass prairie of California, a similar role was played by Stipa pulchra up to the later historical period, and still more recently by Agropyrum spicatuni in the Northwest. Some subspecies of animals, chiefly subinfluents, find their range wholly or largely in such consociations, and the number of these will probably be increased. Finally, in view of the fact that any major dominant may recur more or less pure in repeated local examples, it has proved convenient to refer to it as a consociation, even though it is part of a particular faciation; that is, the association is divided into faciations, in which the consociation appears only as local expressions. The dense communities of the bivalve, Spisida siibtruncata, in the THE STRUCTURE OF CLIMAXES 245 North Sea (Davis, 1925) , have been referred to as consociations (Shel- ford, 1935), but when compared with plant consociations certain dif- ferences are seen to exist. In view of the apparent dominant func- tion of brittle stars already referred to, and the possible dominance of marine fishes, further investigation may indicate that Spisula is a secondary dominant. Furthermore, while Spisula outnumbers other constituents a thousand to one, the latter are nevertheless present. The sea exhibits other groupings that resemble consociations, the oyster bed constituting an example. The oysters form a substratum which encourages hard-bottom species and hence serves as the basis for a community that would not otherwise occur in the area, espe- cially where water is quite brackish. The bivalve, Modiolus modiolus, forms similar groups and supports hard-bottom communities on the shells, while resting on bottom too soft to support these associates. These are more far-reaching in their effects and relations than the consociation dominant in a plant community. It must further be recognized that, while the oyster and Modiolus communities appear like fragments of other biomes, such as groves of deciduous trees in grassland, they are not so, but are unique certainly so far as the oyster is concerned. However, the Modiolus communities of the North Pa- cific have been regarded as the subclimax stage of the Strongylocen- trotus-Argbuccinum biome because (a) they support this on their shells, and (5) the}^ are climax dominants of the hydroclimate above, regardless of the unfavorable bottom. Minor Units. As has been indicated earlier, the subdominant plants constitute secondary groupings within the community of dominants. In the main, the life form of subdominants is that of the forb, but bush and shrub are also to be included, chiefly in layered forests. Communities of this rank have long been known as societies, being called simple or pure when composed of a single species, and mixed when comprising two or more of similar importance. The two most significant categories are those of aspect or seasonal and layer socie- ties, the former marking the change of tone in the plant matrix through the seasons and the latter being best developed in forest. Communi- ties of small animals, chiefly arthropods, restricted to the layers have been called layer societies. The plants most nearly equivalent to the invertebrates of these societies are the mosses, lichens, and fungi. The vast majority of the arthropod constituents of the layer ani- mal societies of the deciduous forest biotic community (Weese, 1924; Blake, 1926; Smith, 1928) move to the ground surface and under fallen leaves for the winter, greatly increasing the population of that layer and constituting an hiemal layer society. It is not correct to as- 246 CLIMAX AND SERE sume that shrub and tree top hiemal layer societies do not exist, as birds and ants still occupy these levels during the winter (Smith- Davidson, 1930), It is true also that many arthropod inhabitants of herbs do not leave these until they have been broken down by frost and snow. A few of them come up early in spring or even in warm weather in winter and feed on the buds and shrubs before herbs have appeared. The question of the relations of the plants and animals of the sub- dominant communities to the chief dominants of a terrestrial biome, to each other, and to the group as a whole is a difficult one. At the outset of our discussion of this topic, it was thought that the entire group of subordinate organisms could be treated together under the term presociety, in the sense of a prevalent rather than a dominant or controlling group. With further study of the literature and the com- munities of waters, it became impracticable to recognize and separate these two divisions of the biome, and the trend of investigation nat- urally caused the term to be applied to animals only (Smith, 1928; Shackleford, 1929; Bird, 1930), while in general the consideration of plant layers has not concerned itself with the associated animals, or the small and more subordinate lower plants. The problem of a natural or at least a logical classification of so- cieties is connected with the need of modifying the concepts of family and colony. In plant ecology, these have been employed for the first two stages in succession, the family comprising all the individuals of the pioneer species, and the colony, the group constituted when one or more additional species invade the area. In zoology generally, family and colony possess essentially the same significance, though the term colony is more frequent and is usually restricted to invertebrates. In the endeavor to render these terms both definite and distinctive, it is proposed to employ family for the simplest grouping, in which the individuals belong to the same species, whether plant or animal. In the case of animals, they will have sprung from the same parents or parent as a rule, though with plants this will have more frequent ex- ceptions. The family will retain its character as the simplest initial community, but it may appear in the climax as well as constitute the first stage of a sere. In consequence, the colony will be limited to a relatively small community of two or more species, either of plants, plants and animals, or animals alone; in other respects, its position and role in the biome will be much like those of the family. By con- trast, the society has denoted a climax community of higher rank, larger extent, and greater importance in terms of subdominants and influents, but it is now proposed to employ it as a general term LAND AND SEA COMMUNITIES 247 for subordinate communities, including seasonal ones (Clements, 1936) . In connection with the above terms, as well as those later discussed under succession, it should be borne in mind that each has a concrete or local application and, in addition, a general one. Thus, the pioneer family of tiger beetles on a particular dune or sandhill may recur in all identical habitats in the local area, or through an extensive region, to constitute the pioneer family of a dune succession. The community formed in the climax true or mixed prairie by Psoralea tenuijlora exists today in thousands of separate fragments, as a consequence of topographic diversity and especially of disturbance, but the local examples are best regarded as parts of an extensive community. The same is true of nearly all fresh-water communities. The validity of this conclusion is all the clearer in the true prairie, for example, where an originally continuous association of wide extent has been frag- mented by tillage into many thousand pieces, often but a few acres in extent. General Comparison of Land and Sea Communities. It is obvious from the foregoing that size is an important criterion for the rank or the significance of communities. The next paragraph indicates, in very general terms, the comparative magnitude of climax and serai communities of the land and sea bottom. It is based upon grassland as one of the most extensive of North American biomes (Clements, 1920; Weaver and Clements, 1929; Shantz and Zon, 1924), and upon the marine communities of the North Atlantic and North Pacific (Petersen, 1914; Jensen, 1919; Davis, 1923; Shelford and Towler, 1925; Shelford, 1935). The following facts are brought out relative to the size of various units. The biotic formation (biome), such as the North American grassland, may cover as much as 1,000,000 square miles and be divided into five or six associations covering 100,000-300,000 square miles. Although the association is accepted as the most uniform unit, there is still variation which the original workers such as Warming had not discovered. A large association like the mixed prairie may show faciations characterized by the dropping out or addition of species which are as large as 9,000 square miles or even larger, and lociations or local variation may be as large as 900 square miles. The climax is more or less continuous but may be much fragmented at its periphery. Serai communities are generally very much smaller and usually much fragmented. A continuous serai area of 200,000 square miles illustrated by the southeastern pine forest, or still larger areas of 248 CLIMAX AND SERE black spruce at the northern edge of the transcontinental coniferous forest, do exist. The latter may be two or three times as large as the pine area. Perhaps the total area of black spruce consocies is 1,000,- 000 square miles, one-half of which is black spruce forming lace- work, the meshes of which are composed of water and open muskeg. Again the northern and southern large serai areas are only two out of hundreds of types such as those on sand areas, floodplain, rock out- crops, lakes, ponds, and swamps. These are all small, being frag- mented in an almost unlimited manner, so that a continuous area of 25 square miles is out of the ordinary and facies may well be only 2.5 square miles, while local variations (locies) are small and perhaps a quarter section (160 acres). The marine acjuatic communities show various sizes, but near land, 1/100 the size of the North American grassland is to be expected, and other groupings in proportion are likely to be the rule. Fresh-water communities rarely are large; as a rule they are either long narrow strips, or are greatly fragmented, or both. They also possess a mini- mum of decomposed vegetation. The communities of small lakes, ponds, pools, swamps, marshes, bayous, and oxbows associated with streams, bays, and other marginal fragments of large lakes, together wdth the smaller ones about arms of the sea, are serai stages to the land climaxes of the region. The preceding discussion shows size to be important though largely relative, but on the whole communities as described herein are large. They differ strikingly from the communities covering a fraction of a square meter such as are often discussed by plant sociologists and students of animal aggregations. The development of climax com- munities in small denuded or retarded areas has received attention at the expense of broader features or extensive areas of the biome, which makes it unnecessary to treat the subject in detail in this connection. The Dynamic Nature of the Climax. AVhile climaxes may persist and have persisted for thousands or even millions of years, each one is the seat of dynamic processes of varying intensity and extent. The outcome of these is a vast mosaic of great complexity, the under- standing of which can be obtained only by the study of the processes themselves. The motive forces involved are climate, topography and soil, reactions and coactions of all sorts, of which those of man are paramount. Cycles in climate produce a climatic succession (or cli- sere) in which climaxes replace each other in their fixed geographic sequence, a process best exemplified during glacial advance and re- treat. In the course of geological epochs and periods, each climax will leave relict areas of itself in favored situations in the two ad- DYNAMIC NATURE OF CLIMAX 249 jacent climaxes, and these constitute the preclimaxes and postclimaxes that form the most ilhiminating pieces of the mosaic. Next in significance arc the topographic processes that initiate suc- cession and bring about ontogenetic (short successional) changes in the chmax by contrast with the phylogenetic (chmatic) ones just men- tioned. Lake, pond and stream, lava flow, rock fields, dunes and sand hills all break the continuity of the biome and serve as foci for the development of hydrosere and xerosere. Though these finally cul- minate in the climax, the opportunity for their initiation is constantly renewed from time to time and place to place, and this taken with varying rates of progression explains why immature stages of the cli- max are to be found everywhere through it. To the A^ariety wrought in the climax picture by these primary suc- cessions are added, in most communities available for scientific study, the modifications intensified and initiated by man. These are less deep seated but much more frequent and result from disturbances of all kinds, notably fire, trapping, hunting, animal control, clearing, cul- tivation, and grazing. Fire, lumbering, clearing, hunting and trapping have destroyed or modified the climax in practically all forest regions. Cultivation, together with hunting, trapping, and mammal control, has left but scattered and incomplete fragments of the humid prairies, and grazing and mammal control have changed the composition of semi-arid ones by favoring certain dominants and influents at the ex- pense of others. Under natural conditions, the numbers of animals fluctuate greatly, in more or less definite response to climatic cycles, as already indi- cated in Chapter 5. It is true also that the dominants and subdomi- nants of the plant matrix of grassland, for example, undergo gi'eat variations in growth and number of individuals from year to year. This process of annuation often produces striking differences in the composition and appearance of the climax at the wet and dry extremes of the sunspot cycle. The greatest fluctuation in forest is in seed crop and herbaceous growth. Annuations and variations in abundance also operate in fresh-water and marine climaxes (Blegvad, 1925). Quite as pronounced in many instances is the orderly procession of aspects through the biome from spring to fall and winter. In this, the changes in the plant matrix are concerned wtih dominance and pattern rather than with composition, but with the subinfluent and veinfluent animals marked changes in population occur from aspect to aspect. In preparing this book two courses were open to the authors: either to present a description of examples of the natural phenomena with which the book is concerned as a basis for general discussion to fol- 250 CLIMAX AND SERE low, or to reverse the order. The reverse order was chosen, but not without misgiving, and accordingly the last task is to describe enough natural phenomena to illustrate the general principles that have been brought out. This of necessity consists in describing at least three major communities — a terrestrial, a fresh-water, and a marine one. The treatment of all the major communities of northern North America is a major task in itself, though a provisional account is en- tirely possible. Fresh-water communities have not been sufficiently ex- plored from our viewpoint, and the great variety and meager knowl- edge of marine communities make more than a cursory treatment im- possible. The major communities or biomes (usually termed biotic formations, but we have in various earlier papers substituted "biome" as a much more convenient term of the same connotation) are the desert, the chaparral, several in the coniferous forest group, the tun- dra, alpine meadow, deciduous forest, and grassland. The last was chosen to illustrate general principles because it is probably most com- pletely known. CHAPTER 8 THE NORTH AISIERICAN GRASSLAND: STIPA-ANTILO- CAPRA BIOTIC FOR^IATION (BIOME) Introduction. The grassland is well suited to illustrate the charac- tertistic features of the biome and the interdependence of the constit- uents and their relation to chmate. This results not merely from its wide extent and exceptional differentiation structurally, but likewise from the unusual number of striking coactions. From the ecological viewpoint there is no essential distinction be- tween so-called prairie and plains, just as there is also no consistent diversity in topography. Both are uniformly characterized by a cover of perennial grasses in close harmony with the climate and like- wise by a former population of gi-azing animals. The usual concep- tion of a prairie is that of a rolling landscape by contrast with the level expanse of plains, a view that receives much support from the so-called high plains of the West, but over the entire area of the grass- land the exceptions are so numerous as to obscure the rule. The plant life form (grass form) is further to be regarded as the decisive criterion in many districts of sandhills and foothills in which the relief is much bolder than in traditional prairie, though the cover exhibits the usual dominants (Pound and Clements, 1898). The peculiar physiognomy of grassland is well known to all who have visited it. The vegetation itself offers little or no obstruction to vision. Large areas of the central portion of our North American grasslands, green in summer and brown in autumn and winter, stretch away as far as the eye can reach. Generally, however, the uniformity is relieved by slopes, rolling ground, small hills or ranges, and ravines and valleys often marked by relict or serai communities of trees or shrubs. Consequently, strong contrast and sharp delimitation of val- ley and plain are among the striking features. Near the grassland margins where the contacts are with tree or shrub communities, there are small groups of shrubs that break the monotony and afford habi- tations, shelter, or perching places for various animals. In conformity with the biotic concept, animals have a distinct role in the physiognomy of grassland, but this was naturally much more evident before the period of settlement. At that time, an ecologist 251 252 THE NORTH AMERICAN GRASSLAND standing on a small rise of the plain on an August morning might well have seen a large herd of bison grazing to the right, and a smaller herd of antelope to the left, while nearer at hand a coyote or wolf would be seen slipping away to its den. Even today, as one walks about, a long-eared jack rabbit bounds up from behind rock or forb and gallops away, often starting others as it goes. Birds such as the horned lark, lark bunting, Sprague's pipit, and the lark sparrow fly past, singing on the wing. The bee flies and robber flies are unusually conspicuous in flight, and grasshoppers are everywhere in evidence. Such prospects, except for the bison and pronghorn, came into the experience of the authors 30 or more years ago and stand in sharp contrast to the limited outlook in primeval forest. Life Forms and Life Habits. The distinctive life form of the prairie is the perennial grass, and to such a degree that an abundance of annuals is an all but infallible index of disturbance. In exclosures, annual grasses have been found to disappear steadily under the com- petition of perennial ones, at least up to the time when the accumula- tion of dry shoots becomes a handicap, and this has been confirmed by the outcome of competition cultures. Moreover, the grass form is to be understood in the ecological and not the taxonomic sense. In their community and habitat relations, such sedges as Carex filiformis and stenophylla are short grasses in effect, and a number of other sedges and of rushes play the role of grasses locally (cf. Weaver and Fitzpatrick, 1934). As indicated earlier, life habit in animals corresponds in physiog- nomic value to life form in plants; it is expressed by the terms cur- sorial, subterranean, arboreal, etc. The life-habit ratios of different TABLE 10 Number of Common Species Using Different Portions of the Habitat in Breeding, Expressed as Percentages of the Total Number of Species Breeding Places Number of Species Burrows or Pits in Ground Ground Surface Rock Ledges and Fallen Trees Weeds or Shrubs Trees Grassland birds Forest birds 28 41 22 22 2 9 4 0 82 26 0 0 53 20 18 18 0 0 4 5 0 18 100 44 34 7 0 0 0 0 5 68 Grassland mammals * Forest mammals *. . . . Grassland bats Forest bats 0 38 0 56 * Exclusive of bats. LIFE FORMS AND LIFE HABITS 253 taxonomic groups, such as the mammals, birds, or insects, exhibit sig- nificant figures for expressing the characteristics of a particular biome and permitting comparison with others. These data are based on lists by Gary (1917) for Colorado grass- land and Howell (1921) for deciduous forest in Alabama. The two sets of data were gathered for the U. S. Biological Survey at the same period. Comparison can be made only within a natural group, for example grassland birds may be compared with forest birds, mammals with mammals, etc. In the case of grassland birds the majority breed in nests built on or near the ground, 53 per cent contrasting with 20 per cent for the forest. On the other hand, fallen or standing trees are used by 68 per cent of the forest birds. A great preponderance of subterranean spe- cies characterizes the grassland mammals, exclusive of bats. There are other life-habit characteristics which cannot be expressed in tables. For example, Craig (1908) points out that forest birds rarely sing on the wing, but eight species of common North Dakota birds do so, namely: horned lark, bobolink, Smith's longspur, chestnut-collared longspur, lark sparrow, lark bunting, purple martin, and Sprague's pipit. Visibility in grassland is high, and animal habits are adjusted in accordance with it. Eyesight is keen in prairie species, and observa- tion from vantage points takes the place of secretive retreat (Bailey, 1931:307; Seton, 1929:443), which characterizes similar animals in the forest. The prairie dog sitting up on its burrow mound exhibits a habit shared by its ecological equivalents, the Richardson ground squirrel and picket-pin gopher. This outlook habit also characterizes the behavior of one or more burrowing forms of other grasslands, e.g., the viscacha in southern South America; the bobac or tarbagan in central Asia, and the meerkat, a carnivore, in Africa. Several of these live in ''towns" or are aggregated into groups, this particular mode of life evidently fitting well into the grassland com- munity. The large prairie-dog towns, large herds of antelope (400 animals or more reported by early explorers), and the enormous herds of bison (100,000 to 2,000,000; Seton, 1929) bespeak this habit, which is evident also in the grasslands of Eurasia and Africa. In southern South America, where larger game is scarce, the pampas deer is not particularly gregarious, but the weasel or tayra and the ostrichlike rhea assume this habit (Hudson, 1892). As to smaller birds, Hudson also reports the carancho as hunting in bands, and, according to Brehm (1896), flocks of the lesser kestrel and the redfooted falcon seek in- sects on the Asiatic grasslands. Craig (1908) points out the gregari- 254 THE NORTH AMERICAN GRASSLAND ousness of the prairie chicken in contrast to the sohtary habit of its relative, the ruffed grouse. Modern ecology has appeared so late as to require reconstruction to evaluate properly the various species of the grassland, either plant or animal, as well as those of other communities dominated by man. This is especially true of the animals, as few relicts of this biome have remained entirely unmodified in this respect. The habits and habitat relations of each species must be known to interpret its past and pres- ent range. The gradual removal of the generally continuous forest cover of the eastern states and southern Canada for nearly three cen- turies gave abundant time for birds, insects, and other animals of the forest edge, swamp, and moist meadows to invade the eastern United States. Again, the planting of trees in the prairie from 1860 to 1938 has afforded opportunity for forest-edge species to extend westward. This period undoubtedly represents marked expansion of the popula- tions of those animals favored by man directly or indirectly. The community and habitat relations of an animal species can usually be ascertained from good field data, but unfortunately, in the early period of scientific exploration previous to 1890, the ecological results of expeditions were commonly lost by the process of segrega- tion of collections to specialists and by the practice of stressing the description of the species only. In the mid period (1890-1910), taxo- nomic monographs and other papers gave little habitat data in connec- tion with the life-zone work, although any life zone includes many unlike habitats. IVIoreover, all the drier grasslands were confused with desert, and even in typical grass communities few or no grasses were listed as habitat or zone indicators, attention being focused upon the conspicuous woody and succulent forms. With the rise of the eco- logical viewpoint, natural history works of definite ecological value began to appear; those of Seton (1929), the excellent state treatments by Bailey (1931), Hebard (1925-1931), and others are noteworthy. Climate. In harmony with its wide extent, the climatic relations of the prairie exhibit a greater range than those of any other climax on the continent. On the east its boundary lies close to the isohyet of 40 inches from Texas to Indiana, while on the northeast it drops from that of 35 to 25 inches in correspondence with lessened evapora- tion. The extremes of temperature are even more striking, varying from a frost-free season of but three or four months in Canada to one of practically an entire year in southern Texas. The chief explana- tion of this seeming anomaly is to be found for both plants and ani- mals in the evasion of temperature extremes by virtue of the habit of perennation on the one hand and that of burrowing on the other (cf. LIFE FORMS AND LIFE HABITS liiiiii jiiilllill Mixed Prairie PIfll Desert Plains |»{{3 California Prairie ^ ]^o°\ Palouse Prairie |i':i.V;!| Incompletely known grasslands t'lVi'l Aspen Parkland (Savannah) /"^•^^ Contacts with other biomes "*'•'-' Separates different associations Cl^ Mountain masses | | Non- grasslands Fig. 54. — Map of the grassland climax and its associations. The areas in which the climaxes occur outside of low mountains are indicated. TP — true prairie; CP — coastal prairie; MP — mixed prairie; PP — Palouse prairie; BP — California prairie; DP — desert plains. 256 THE NORTH AMERICAN GRASSLAND Savage and Jacobson, 1935; Weaver and Albertson, 1937; Weaver, Stoddart and Noll, 1935). The xeric limit of the grassland confronts the desert in the south- west along the line of 5-6 inches of rainfall, and the sagebrush to the northwestward with an effective rainfall a few inches higher. The as- sumption that grassland is restricted to regions with a spring-summer precipitation of about three-fourths the total, though still more or less prevalent, is no longer tenable in view of the fact that the Pacific and Palouse prairies obtain most of their moisture during the winter. Where freezing temperatures do not obtain, as in southern California, the native bunch grasses may start growth in any month from Sep- tember to February and are not infrequently in bloom in December. STRUCTURE AND UNITY (Fig. 54) The grassland under consideration is divisible into six types or associations, namely (1) the mixed prairie, occupying a large central area lying east of the Rocky mountains and in the main west of the 100th meridian; (2) the true prairie, which lies east of mixed prairie and in contact with forest; (3) the gulf coastal prairie, lying near the Gulf of Mexico; (4) the desert plains, mainly in southern Arizona, New Mexico, and Mexico; (5) the California or Pacific prairie; and (6) the Palouse prairie in the northwestern states. These associations are distinguished by the prevailing dominant grasses and influent animals, as well as by secondary differences in appearance. They are bound together by certain major features of physiognomy and by plants and animals in common, which may be called binding species. Binding Dominants of the Prairie.^ Binding dominants are species of perennial grasses that occur as climax species in three or more as- sociations of the grassland biome and are all found in the ancestral mixed prairie. They are as follows, the sequence indicating a gen- erally decreasing Wideness of range. ^ Sporobolus cryplandrus Boutcloua hirsuta Koeloia cristata Elymus sitanion Stipa comala Poa scabrella Siipa viridula Festuca ovina Agropynim smithi Andropogon scoparhis Boutcloua gracilis Buchloe dactyloidcs Bouleloua curlipendula 1 The names employed are those of long-accepted species of definite eco- logical significance rather than the more recent minor species, or better, sub- species (Clements and Clements, 1913; Hall and Clements, 1923). STRUCTURE AND UNITY 257 It is manifest that these are the dominants that bespeak the unity of the gi-assland as a cHmax formation and constitute the primary pat- tern in which the differentiation into associations has been carried out. Other grasses have similar extensive areas, such as Andropogon sac- charoides and Sporobolus air aides, but the former is chmax in but a single association and the latter is generally a subclimax dominant of the halosere. Binding Influents. Among the influents which give unity to the biome are the bison {Bison bison), the pronghorn antelope {Antilo- capra americana and variety), and the badger {Taxidea taxus and varieties) which covers all the climatic grasslands and is almost re- stricted to them, merely extending into some savanna areas. It is found in all the grassland associations from Indiana to the San Joa- quin valley and from the bunch grass of British Columbia to the desert plains of the Southwest. It invades other biomes only locally in serai stages, as in the saltbush subclimax of the Larrea desert, though maps suggest its presence in the desert generally (Figs. 55-57) . The buffalo wolf [Canis nubilus) , the horned lark (represented by a different va- riety in several of the associations), and a few insects, of which the orthopteran (Mermiria neomexicana) is an example, occur in nearly all the associations. The differences between the associations as to influents are given on pages 264, 273, etc. The genus Geomys (eastern pocket gopher) is largely confined to the moister grasslands likewise, and the smaller Thomomys (western pocket gopher) , is also a grassland influent. Certain species are char- acteristic of climax grassland ; others extend into mountain meadows and into serai communities dominated by a mixture of grasses and trees. The same is true of the several species of Onychomys, the grasshopper mouse, and Citcllus, the ground squirrel. The genus Lepus includes the varying hares and jack rabbits which occupy open and brush-covered areas in grassland and tundra. Jack rabbits comprise two quite distinct groups: (a) the northern white- tailed jack rabbit closely related to the varying hare, and (6) the southern black-tailed jack rabbit. Certain species or varieties of these two groups range through the climatic grassland and into the park- like types of vegetation and grassy serai stages in low altitudes. Some genera of birds divide their time or range between tundra and grassland, such as Calcarius (longspurs), Otocoris (horned lark), and Anthus (pipits). Other genera range between prairie and meadow. Among them are Dolichonyx (bobolink) , Sturnella (meadow- lark) , and Ammodramus (grasshopper sparrow) (Pearson 1923). Of the reptiles two species of bullsnake or gopher snake (Pituophis) 258 THE NORTH AMERICAN GRASSLAND p^ A,^ -"5 STRUCTURE AND UNITY 259 ," '^'^' •:^^^j H ' _^. ^ ^ o Pi o 1— I 4) ' — ;_, cq • S o cc p c H o a ■2 Y ~* H P; '<^ CO "a ^ ^ 9. 3. ^ S. O rt c3 --- TO -^ to 0^ ID ^ ra o O ^ "S -g • s r? ^ i^ ° CO ^ »-i a ■co O "2 O I — I c3 5) 5 ^ > o -f o I 1— Cj a> fi X <» ) positive response to rock as opposed to sand or other bot- tom materials. This was so striking as to constitute a life-habit char- acteristic of the community, which was consequently termed rheotac- tic. This characteristic is easily illustrated by experiment on the common species listed above as belonging to the rapid-water com- munity, such as Etheostomids, Hydropsyche, Heptageninae, Perla, and Corydalis. These forms practically always show an 80 to 100 per cent positive response to a fairly strong water current and a similar one to large stones as opposed to sand. In the study of current, it is necessary to consider only those individuals actually in it, and this may be accomplished by omitting all those resting in contact with ob- jects against which the current strikes at right angles. Many will OTHER COMMUNITIES 311 show the clinging reaction as an expression of their choice of large rough rock surfaces. OTHER COMMUNITIES Intermediate between the swift-water communities and the pool climax are various others, chiefly on sand and gravel bottoms. Those on gravel partake of the general life form, life-habit characters, and, to some degree, of the taxonomic composition of those of the rapids. Sand communities resemble the pool climax. A type of community noted by Gersbacher (1937) on sand is characterized by a predomi- nance of various sphaerids and fresh-water mussels. It lacks sharp distinction from the pool community and its developmental stages, and more study is required to determine its rank. Obviously, animals do not dominate the sand habitat in the way they do in the baselevel mud-bottomed pools (cf. Reighard, 1908). The relation of stream to lake communities is made evident in glaciated areas such as northern Illinois and Wisconsin. Here the very sluggish rivers connect lakes which are in several cases merely broad and sometimes irregular expansions of the river itself. These rivers sometimes contain the climax community, but vegetation grows in them and often covers much of the bottom, which contains much organic matter. Dr. D. H. Thompson (Illinois National History Sur- vey) has observed that during the recent drought period vegetation appeared in the Rock River, which includes areas of climax. He believes this is due to lower turbidity resulting in better light condi- tions. In the Fox River (at Gary, Illinois), vegetation occurs along the margins and the climax at points between the vegetation and the center of the stream. In other words, there is a tension between land and water climaxes which manifests itself in these wide sluggish waters. Streams are in constant state of change from season to season or from year to year, except in the physiographically stable old age or baselevel condition or in other conditions approaching this, due to retarded flow. The small unstable streams likewise show communities in which development may be traced for a time, but which are soon destroyed by flooding and thus rendered difficult to study. The literature deal- ing with the stable or climax communities is cited in connection with the description of them on pages 305 to 307 (see Gole, A. E., 1932). Fresh-water climates and climaxes have only very recently been recognized. One of the earliest ecological classifications of com- munities divided them into edaphic (including water) and climatic. The local character of the edaphic communities and the very exten- 312 AQUATIC CLIMAX COMMUNITIES sive character of the climatic ones was stressed very early. In dy- namic ecology, the edaphic communities become serai stages of the climatic community or climax. The communities of small bodies of water, such as ponds, small lakes, oxbow cut-offs of streams, and swamps, are merely serai stages leading to the climax of the region. They illustrate numerous routes by which such bodies of water may pass to the appropriate climax. Since space permits the consideration of only general principles gov- erning the terrestrial, marine, and fresh-water climaxes, it is not prac- ticable to discuss the hydroseral stages of the terrestrial climaxes. Limnologists have not made use of these distinctions, which are essential to dynamic ecology. The voluminous literature of this field deals largely with lakes and ponds, which are early serai stages of the deciduous and coniferous areas of North America and Europe (Welch, 1935:306). The nomenclature is detailed and characterized by many adjectives. The large dictionary of terms prepared by Naumann (1931:7-776) indicates the extent of the investigations in this field (cf. Ekman, 1911, 1915; Needham and Lloyd, 1916; Shelford, 1918, c; Borner, 1922; Lundbeck, 1926; Thienemann, 1926; Carpenter, 1928). The work on streams has been less extensive, but is treated in the general works cited. CHAPTER 10 MARINE BIOTIC COMMUNITIES INTRODUCTION The marine communities possessing the qualities of land climaxes appear to occupy the greater part of the surface of the globe. Ob- viously, the corals and certain coralline algae produce reactions upon the habitat equal to if not greater than those of forest trees, and doubtless of greater duration in any particular place and set of con- ditions (cf. Herdman, 1906; Bigelow, 1930). Several types of communities occur in the sea. Certain communi- ties are commonly considered as dependent upon the character of the bottom, but it has been pointed out (Shelford et al, 1935) that these are frequently more closely related to the physiographic forces than to the bottom materials. The amount of circulation and the force with which it acts are of great importance in determining the entire marine climatic regime and may sometimes overshadow bottom con- ditions. The tidal community on hard bottom is distinctly marine and has no counterpart in fresh water. It is dominated by acorn barnacles and mussels in the Northern Hemisphere, and by mussels, barnacles, tunicates, and oysters in the Southern Hemisphere (Oliver, 1923). This type of community occurs between the average of the lower half of the low tides and of the higher half of the high tides; it has no counterpart on muddy and sandy shores (cf. Davenport, 1903; South- ern, 1915). Subtidal communities of muddy and sandy shores or clam com- munities on gently sloping beaches do not reach as high above low tide as do the tidal barnacle groups. Clams usually extend about two-thirds of the way between the low tides and the high tides. This distinction prevents confusion and serves to emphasize the fact that the subtidal community reaches up into the tidal area. The areas farther landward from clam beaches on low depositing shores com- monly represent serai stages to land occupied by halophytes mixed with other land plants, or bare sand beaches. On sandy shores pro- truding rocks are occupied by tidal communities. 313 314 MARINE BIOTIC COMMUNITIES The great oceanic or pelagic community is similar in some respects to that of large lakes like the Great Lakes of North America. How- ever, it is infinitely richer in diversity of size and form of animals and in taxonomic groups represented. Hydroclimate. The conditions of existence in the sea differ from those of fresh water in certain important respects. The occurrence of tides is most important in producing circulation; otherwise they have little or no effect on the pelagic or on bottom communities outside the intertidal area. The most important difference in climatic condi- tions lies in the presence of a large amount of salt, principally sodium chloride, and the occurrence of sulphur compounds in the form of hydrogen sulphide, sulphurous acid, and colloidal sulphur, which often have important relations to aquatic life. The salt present increases the density of the water, and hence variations in salt content are credited with playing a very important role in the climate of the sea. The hydroclimatic factors (Wasmund, 1934) are greatly modified by reactions. Greater density of life in the sea produces far greater reaction on the habitat in the way of light reduction, chemical changes, etc., than in lakes. These bioclimatic factors are so important and generally present as to be essentially a part of the hydroclimate itself. The great depths of tlie ocean and the lack of rooted or attached plant life except at irregular intervals along the shore also produce differ- ences between fresh and salt water (cf. Harvey, 1927; Knudsen, 1922). PELAGIC COMMUNITIES The communities of the sea have been so incompletely studied that it is difficult to outline their arrangement in any adequate manner. On account of their outstanding peculiarities, it seems best to begin wnth pelagic communities. Only those of the North Pacific are fa- miliar to the writer, while most of the work has been done on the North Atlantic. The discussion of marine pelagic communities from a biotic viewpoint has not often been attained, but Murray and Hjort (1912) and Bigelow (1924) have made progress in this direction (see Gran, 1912, 1931; Allen, 1921-1932). Pelagic Communities of the Enclosed Waters of the North Pacific The pelagic communities include the plankton or floating organisms taken together with the swimming animals or nekton. The separa- tion into those two groups as a basis for investigation has led to an PELAGIC COMMUNITIES 315 unfortunate failure to recognize the pelagic community proper. The general relations of the various elements of the pelagic community may be brought out for the waters inside the south end of Vancouver Island. This description is, however, handicapped by a lack of in- formation on the food habits of the nekton. Plankton. Studies of the diatoms of this community have been made by Gran and Thompson (1930) and Phifer (1933, 1934); the Protozoa have been treated by Eddy (1925, a), and the Crustacea by Campbell (1929, 1930). The last has found all types of smaller plank- ton organisms most abundant at a depth of about 4 meters, including copepods, peridinia, tintinnids, and diatoms. Phifer (1933, 1934) re- ported diatoms most abundant at 10 meters in the Strait of Juan de Fuca. The depth of maximum abundance differs greatly in various localities and on different dates, but is probably always in accord with physical conditions. In Julj^, 1928, two series of four simultaneous water-bottle samples, separated by 20 minutes at slack tide, were taken over each of the two major bottom communities ( Shelf ord et al., 1935:250). Over the sea urchin-triton snail community (Stron- gylocentrotus-Argobuccinum biome) which usually occurs on rela- tively hard bottoms, counts by Gran of collections distributed from 1 to 225 meters showed that the maximum abundance of diatoms was at 20 meters. They were about 1/10 as numerous at the surface and 1/16 as abundant at 225 meters as at the maximum. The i)lankton over a clam-worm community (Pandora-Yoldia biome) at 28 meters' depth, usually on soft bottom or fine mud, was sampled in a similar manner within an hour. Diatoms were about 10 times as abundant as over the sea urchin-triton community, and the maximum was at 10 meters instead of 20 meters. An examination of the animal plankton taken in the net-haul made at the same time from bottom to surface over the clam-worm com- munity yielded a few copepods, rotifers, and tintinnids, very many dinoflagellatcs, and various larval stages. Over the sea urchin-triton community, it differed chiefly in the lack of dinoflagellatcs and in the presence of a greater variety of the larval stages. A few Sagitta were taken from the deep water here, but none over the Pandora-Yoldia community. Jcllyfishes abundant during the summer months through- out both the inner and outer waters are: Aequorea forskalea (P. and S.), Phialidiu77i gregarium Hacck., and Thaumantias cellularia Haeck. These, together with less abundant species of Sarsia, Stomotoca, Poly- orchis, and the common ctenophores (Mnemiopsis and Pleurobrachia), make up a great part of the volume of the plankton of midsummer. There is a large seasonal element including many eggs and larval 316 MARINE BIOTIC COMMUNITIES stages of invertebrates and a few fishes (Bovard and Osterud, 1919; Weese and Townsend, 1921; Strong, 1925). Nekton. The larger animals with effective swimming powers in this area consist chiefly of fishes and mammals (Shelford and Powers, 1915; Shelford, 1918, a; Powers, 1921). Fishes Culpea pallasii (Cuy. & Val.) Herring Hypomesus pretiosus (Gir.) Surf smelt Thaleichthys pacificus (Rich.) Eiilachon Oncorhynchus nerka (Walb.) Sockeye salmon, anadromous Oncorhynchus kisutch (Walb.) Silver salmon, anadromous Oncorhynchus gorbuscha (Walb.) Hump-back salmon, anadromous Mammals Orcinus rectipinna (Cope) Killer whale Rhachianectes glaucus (Cope) Gray whale Globicephala scammonii (Cope) Pacific blackfin Phocaena phocaena (L.) Porpoise The killer whale appears to be most abmidant and was frequently seen in the San Juan Channel; the blackfin was noted less often. Originally, gray whales congregated in muddy bays and came to the surface daubed with bottom mud (Scammon, 1874). Coaction and Reaction. The food coactions among North Pacific plants and animals are little known, though the work of Lebour (1919-1923) on the North Atlantic makes possible inferences as to the food of plankton animals and young fishes in general. The food habits of only a few adult fishes have been studied. The killer whale is known to prey upon other w'hales and fishes, salmon especially being mentioned by Scammon (1874) ; the same author states that the blackfin feeds upon squids and fishes. The reaction of pelagic organisms in shutting out much light from the waters below has al- ready been noted (Shelford and Gail, 1922; Shelford, 1929, b). In addition to this, plankton organisms, sinking to the bottom at death, absorb oxygen and produce carbon dioxide (Atkins, 1922), as well as sulphur compounds and organic mud, having a profound effect upon bottom conditions, especially in quiet water. Physiological Characters. The independence of the bottom and shores is striking. Most of the work on physiological characters has been concerned w^ith fishes, w^hich are very sensitive to differences in the character of the water. The heri'ing responds to variations of 0.1° C. in temperature and is sensitive to changes of 0.1 pH. The re- sistance of the pelagic herring and surf smelt to carbon dioxide was rated as 10 and 8 respectively, while the viviparous perch,, an in- PELAGIC COMMUNITIES 317 habitant of shore vegetation, had a value of 25 (Shelf ord, 1918, a). Based on sulphur dioxide, the pelagic herring was rated at 10, the perch at 21, and the bottom flounder at 1100. Pelagic Communities of the North Atlantic The only modern consideration of pelagic communities in which the larger organisms and plankton are treated together as a unit is that represented by Murray and Hjort (1912:101-108; 617-704). M 150 500 1000 2000 3000 4000 5000 • Myctophum - Salpa Biome ^Scomber - Calanus^ / Biome } Arevropelecus - Cauliodus Blome C. signata - A. purpurea Association 'iw '^<}^ C. microdon - A multispina ^ '%, Association 40 50 60 Degrees - Latitude North 80 Fig. 73. — Diagrammatical vertical section of the North Atlantic with the several communities described by Murray and Hjort indicated, arranged so as to follow the practice in terrestrial communities. The depths to which the communities occur probably decrease from the equator to 60° N., owing to the difference in the penetration of solar radiation, but this is not indicated. These writers describe various communities of the pelagic waters of the North Atlantic which may perhaps be interpreted as biomes as suggested below. Furthermore, each appears divisible into two or more associations based upon the abundance of certain fishes and other larger animals that may be regarded as making the nearest ap- proach to dominants. The boundaries are apparently less definite than those between major land communities, but this is by no means certain, as the facts are much more difficult to ascertain. The ar- rangement of these (following IMurray and Hjort) is suggested in Fig. 73. While the small amount of observation renders the classifi- cation more or less hypothetical, it serves to illustrate probable 318 MARINE BIOTIC COMMUNITIES comparisons with land communities. To this end, units have been renamed according to the plan followed for the terrestrial and fresh- water communities, and suitable technical names are carried in paren- theses. Slenderfish-red prawn Community (Cyclothone-Acanthephyra Biome) (See Murray and Hjort, Bathypelagic Communities, also Plates I and III, following page 664.) This lies south of the Wyville Thompson Ridge at a depth of 5,000 to 500 meters. It is characterized by slender dark-colored fishes of which Cyclothone is predominant, deep-red prawns of which those of the genus Acanthephyra are outstanding, and some species of peteropods, squids, etc. This community appears to be divisible into two lesser communities (associations), each characterized by a dif- ferent species of Cyclothone and Acanthephyra. The young of vari- ous of the fishes, especially Cyclothone, occur near the surface, forms intermediate in size in the next community below, and the adults in the deep water. Beebe (1929) and Beebe and Hollister (1930) noted Cyclothone in great numbers off the Bermudas from the bathysphere but mainly in the community above this one. They also record scar- let crustaceans of the genera Notostorium and Gnathophansis, and an eel of the genus Serrivomer (Beebe, 1932, a). Telescope-eyed Fish Community (Argyropelecus-Chauliodus Biome) (See Murray and Hjort, Fig. 454, page 603, and 458, page 604.) This community lies above the one containing the red prawns in 500-150 meters. The telescope-eyed fish (Argyropelecus) occurs in large numbers, a fact recorded by both Murray and Hjort and by Beebe (1929, 1932, a, b). According to the former (page 631), the characteristics of the predominants are as follows: "The fishes are as a rule laterally compressed, with a mirror-like silvery skin; when colored, the back is generally blackish brown, and the resplendent mirror-like sides of the body are blue or violet. The eyes are very large, very often telescopic, and the body is usually provided with a number of light organs varying in size. . . . All the silvery fishes of the region between 150 and 500 meters are small, and the same remark applies to the other organisms of the community. These consist al- most exclusively of small crustaceans (coi)epods, ostracods, amphi- pods), sagittids, pteropods, and small medusae. Besides these, we commence to find larvae of squids and fishes, which, however, become PELAGIC COMMUNITIES 319 more numerous in the layer above 150 meters." Beebe and Hollister record numerous shrimp jelly fishes and fishes in great numbers, as • seen from the bathysphere. Two associations are suggested for this community. One, the southern, characterized by fishes of the genera Valenciennellus and Ichthyococcus ; another, more northerly, typified by Stomias boa (Murray and Hjort). Fish-Tunicate Community (Myctophum-Salpa Biome) This community occurs from 0 to 150 meters and lies south of the Wyville Thompson Ridge. It is characterized by numerous animals such as Foraminifera, Radiolaria, Copepoda, and pteropods, and mi- croscopic plants, chiefly diatoms which are most abundant at 10-20 meters and scarce below 100 meters (Gran, 1912). The larger pre- dominant animals include jellyfishes, the Portuguese man-of-war (Physalia), quantities of compound tunicates (Salpa) (cf. Brooks, 1893) and numerous scopelid fishes, e.g., seven species (Myctophum) which are of outstanding importance. The animal grouping also in- cludes cephalopods belonging to seven genera. Sperm whales and cer- tain right and hump-back whales occur. The color characteristics of the community are illustrated by "the minute young of Scombresox living at the very surface, the sides of which are mirror-like, while the backs are intense blue. One group containing seablue forms is represented by the flying-fish. The pilot-fish are also blue, but with some darker transverse bars. In the surface layers most animals are colorless. The eel larvae (Leptocephali) are indeed so transparent that one can only see their small black eyes; even their blood is trans- parent and devoid of haemoglobin" (Murray and Hjort, loc. cit., 669- 670). Mackerel-Calanus Community (Scomber-Calanus Biome) A pelagic community of rather wide distribution in the colder waters of the North Atlantic is suggested in Bigelow's account (1924, a, b) of the plankton of the Gulf of Maine and the work of IVIurray and Hjort on the Norwegian Sea. It is characterized by a great abun- dance of Calanus finmarchicus as the most abundant and uniformly distributed copepod associated with other copepods, Sagitta, jelly- fishes, etc., mackerel (Scomber scombrus L.), herring (Culpea species), and whales of the genera Balaenoptera and Megaptera, which feed upon fishes and pelagic crustaceans. This community appears to exist in the upper 150-200 meters. It illustrates the principle found to 320 MARINE BIOTIC COMMUNITIES characterize terrestrial communities by showing a wide distribution of some of the predominants which bind together two associations, one present in the Norwegian Sea and another well represented in the Gulf of Maine (cf. Hjort and Rund, 1929; Fuller and Clark, 1936). H erring -Calanus Community {Clupea-Calanus Association) This is also well represented in the Norwegian Sea; the species with outstanding abundance of individuals are Calanus, Thysanoessa, the mackerel, herring, and certain whales, all common to both the Norwegian Sea and the Gulf of Maine. In addition, there are present the sprat {Clupea sprattus) and salmon {Salmo trutta), numerous copepods and other crustaceans, as well as certain pelagic Mollusca, fishes, and whales that do not occur in the Gulf of Maine (Murray and Hjort, 1912; Bigelow, 1924, a). Menhaden-Calanus Community {Brevoortia-C alanus Association) The association found in the Gulf of IMaine contains the mackerel {Scomber scombrus) , the copepod {Calanus finmarchicus, Gun.), and several other abundant species that serve to bind the two associations together in one biome. Some of the other species characteristic of the association are Sagitta elegans, certain euphausiid shrimps (spe- cies of the genus Thysanoessa), the menhaden {Brevoortia tyrannus [Latrobe]), and the North Atlantic right whale, together with many others less prominent. In his exhaustive treatise on the plankton of the Gulf of Maine, Bigelow (1924, a) brings out many features that illustrate the character of dominance and the eoactions in pelagic com- munities. Clark (1933) has discussed light relations and distribution of plankton down to 114 meters. Nature of Dominance in the Pelagic Climaxes The oceanic communities present a distinct aspect because of the remarkable adaptations to pelagic life exhibited by the organisms characterizing the different depths. Their permanency is no doubt greater than that of any of the land climaxes. Two or three impor- tant questions arise with regard to the role of microscopic plants and animals, and the nature of the control exercised in the habitat by the organisms. The effect of organisms near the surface on the conditions surrounding those deeper in the water is important and has already been discussed. Bigelow's studies (1924, a) and those reported by other investi- PELAGIC COMMUNITIES 321 gators and summarized by him bring out some features of dominance in pelagic communities in connection with the whales. The whale- bone whales are the largest constituents of the biome in the Gulf of Maine; their food consists of copepods and euphausiids (schizopods), supplemented with fishes. In the long run the crustaceans are appar- ently of greatest importance in most cases (Brooks, 1893; Clark, 1933 a, b, 1936). The food is strained from the water by whales and by some fishes also, and Bigelow stresses the fact that the finer strainers are better adapted to the catching of small forms, and less effective in catching fishes, etc. Bigelow further points out tendencies for particular consuments to seek certain types of plankton or nekton. The menhaden feeds on the unicellular algae (chiefly diatoms) throughout life. Copepods also feed on diatoms, and some other fishes subsist chiefly on Crustacea, chiefly copepods. Sagitta appears more important in reducing cope- pod numbers than fishes. These crustaceans are present in reduced number where Sagitta is abundant. He also states that certain cteno- phores take nearly all living things that come in contact with them. Wherever these creatures abound, most of the small animals tend to be extirpated. On the other hand, ctenophores, themselves, are not eaten by larger animals. The character of dominance, or in other words the control of the community by organisms, is puzzling. One may, however, venture to suggest that dominance by the copepod, Calanus finmarchicus, is indicated in the Gulf of Maine. It is present in outstanding quan- tity, being able to replace population losses so rapidly as to supply the greater part of the food for fishes and many other forms both large and small. It is thereby assimied to serve as the basis for much of the pelagic life of the bay (cf. Brooks, 1893). Again the menhaden may also be regarded as an important dominant because of its ability to utilize diatoms, as well as by reason of its great abundance. The wide distribution of the microscopic plants and the small ani- mals that make up the smallest constituents of plankton, and the relatively non-selective manner in which they are taken by important dominant organisms such as Calanus, hardly puts them in the dom- inant class. They are, however, of fundamental importance as the basis of the food supply of the entire group of pelagic biomes, and constitute a sort of universal mass of food materials for such large crustaceans, mollusks, fishes, etc., as probably may properly be con- sidered as the dominants of pelagic communities. The bathysphere observations of Beebe (1930, 1932, a, b) indicate that pelagic animals are far more numerous than was formerly sup- 322 MARINE BIOTIC COMMUNITIES posed. Such species of fishes as constitute the genera Cyclothone, Storaias, Chauliodus, and Argyropelecus appear to be voracious feed- ers in the oceanic communities south of the British Isles, while squids and the better-known pelagic fishes operate in a similar manner in the Norwegian Sea. Dominance in pelagic communities appears to de- pend upon superior fecundity and numbers, as well as greater ability to hunt or strain out and devour other animals, as well as plants. The principal larger dominants appear to be partially non-competitive in their food relation, which suggests a much finer adjustment of the constituents to one another than is found in terrestrial communities. ECOTONE BETWEEN PeLAGIC AND BOTTOM COMMUNITIES A goodly number of bottom animals swim about, entering the pe- lagic conditions just as the species independent of the bottom and shore do, in a manner comparable to that of birds, bats, insects, etc., in land communities. Some of these motile forms roam over two or more major communities (biomes), using one for breeding, and another for feeding and other activities of a non-breeding portion of the year. The fishes have a mobility of about the same magnitude with refer- ence to major communities as do birds and a few of the largest mam- mals, while bottom crustaceans, mollusks, echinoderms, etc., have a power of movement roughly equal to that of the smaller animals (cf. Hutchinson, 1928; Hutchinson, Lucas, and McPhail, 1929; F. S. Rus- sell, 1928-1932). The ecotone between the benthic communities of the continental shelf and the pelagic ones is also quite evident. It is characterized by fishes and crustaceans dividing their time between the bottom and the water above, though primarily dependent upon the bottom. Fur- thermore, the pelagic community, as the enclosed waters are ap- proached, presents a series of communities characterized by the loss of oceanic species and the addition of larval stages of benthic animals and adult and post-larval fishes of the continental shelf. COMMUNITIES OF THE SEA BOTTOM Sea-bottom communities include both sessile and motile animals, together with plants. Unfortunately, like pelagic communities, these three groups have been considered separately and the community unity and many of the coactions have been passed over or treated in an isolated manner. The sessile, sedentary, and slow-moving inverte- brates of bottom communities have commonly been roughly subdi- vided into three life-habit and life-form groups. The most conspicu- COMMUNITIES OF THE SEA BOTTOM 323 ous of these types is that attached to, or resting upon, the substratum, as exemplified by barnacles, gastropods, large echinoderms, and mus- sels on rock or other hard bottom. These may be called barnacle- gastropod communities. The second life-habit type burrows into soft bottom and includes clamlike mollusks, worms, and a few wormlikc echinoderms.^ These may be called bivalve-annelid communities. A third type is represented by corals, especially those associated with coral reefs; the life forms of these resemble plants, as indicated by the term zoophyte commonly applied to them. The predominants of most communities thus combine two or more sedentary life habits and life forms with those of the strictly motile constituents. From a physiological viewpoint, bottom communities are separable into two principal types: (1) those that do not tolerate exposure to the atmosphere and are practically always submerged in water, and (2) those that tolerate or require exposure to the atmosphere and occupy stable and usually hard substrata exposed to the full force of the air with each important fall of tide. The latter ordinarily be- came subtidal only locally, when under peculiar conditions of salinity or temperature (Huntsman, 1920). The former are divisible into two subgroups: (n) those whose habitat (tidal clam beaches) may be par- tially exposed to the atmosphere during low tides without exposing the community constituents, and (6) those that are always well below low tide. Aside from the corals, the location and relation of the two remain- ing life-form types and the two physiological types are essential to an understanding of marine bottom communities in general. The physio- logical types are readily separated, superficially at least, into two categories, those requiring and those not requiring or tolerating rhyth- mic exposure to the atmosphere. As noted above, strictly speaking, the (clamlike) bivalve-worm communities are never rhythmically exposed to the atmosphere with tidal changes. In the so-called clam beaches, both the bivalves and the worms are restricted to sands having a large water-holding capac- ity (Bruce, 1928). When the tide is out, they retract their fleshy organs and remain in the w^ater held by the sand, and even if this water is partially withdrawn, they are not exposed to the sun and atmosphere. Those bivalve-worm communities that reach above the 1 The first two life-form types are respectively the "on fauna" and "in fauna" of Petersen. Unfortunately, in describing communities Petersen did not stress the motile influents. The term benthic is often applied to the species or com- munities living on or in the bottom, but it is not used here because it seemed confusing. 324 MARINE BIOTIC COMMUNITIES average low-tide line also extend several meters (8-10) below low tide (Petersen, 1918:18; Wisncr and Swanson, 1935). They are es- sentially subtidal, as are all other described communities of this type. The use of the term intertidal is misleading, as are most habitat designations for communities, as it implies that all aggregations ob- A Gastropod -echinoderm Community ( Strongylocentrotus - Argobuccinum biome ) Ecotone A Clam -worm Community (Macoma-Paphia biome) Fig. 74. — A diagram showing the relations of three major marine communities at the north shore of the Straits of Juan de Fuca in the northeast Pacific. Starting at the left the Strongylocentrotus-Argobuccinum biome has its upper limit above the level of the extreme low tides (E), and at the level the aver- age of low tides (D) this boundary is very sharp. The Balanus-Littorina (BL) biome is differentiated between the mean of the lower tides (D) and the mean of the higher tides (A) but does not reach the mean of high tides (B). Toward the right, the Balanus-Littorina biome is bounded at its bottom by sand and its strip becomes narrower. The Macoma-Paphia biome reaches downward through about 8 meters with a wide ecotone between it and the Strongylocentratus-Ai-gobuc- cinum biome. For convenience in making the diagram, it is shown as ending abruptly at a ledge of hard rock at about 6 meters. C indicates the upper limit of this community which is about half way between high and low tides, making it essentially a subtidal community and at average low tide only 1^/^ meters (C-D) of the 8 meter belt is exposed. served between the tide lines are distinct communities, whereas this is not true. The barnacle-gastropod-mussel community might be called intertidal, but since it is evidently adjusted to, and probably requires, tidal rhythm it seems best to call it a tidal community. The primary division with which we have to deal is, however, the two life-form groups noted on page 323, which for convenience may be referred to as COMMUNITIES OF THE SEA BOTTOM 325 the barnacle-gastropod and the bivalve-annelid community types. The latter type, being subtidal, is not subdivisible, while the former is divisible into tidal and subtidal type (cf. Kirsop, 1922). Barnacle-Gastropod Tidal Communities Wherever the substratum materials are not moved by wave action, and the area of the seashore alternately exposed and submerged by the rise and fall of the tide, a tidal community exists. Such com- munities appear to occur on all stable shores, except the icebound ones. They are made up of species tolerating or requiring exposure to the atmosphere at daily intervals. The tidal community proper is a barnacle-gastropod-mussel one, which in the Puget Sound region of the Pacific begins near mean low tide and reaches to a vertical meter or meter and one-half above the upper limit of the large bi- valve-worm community. Its presence may be governed almost as much by water movement as by substratum, since mussels may form a bed in still water, or on the upper portions of a sand beach, and constitute a substratum for the attachment of barnacles. These two species may be followed by others and thus build up the entire barnacle-gastropod-mussel community. The general principles gov- erning this community type may be illustrated in the North Pacific. The community has been sufficiently studied to show its climax na- ture, permanency, etc., and may be termed a biome. Balanus-Littorina Biome The most important dominants include three species of barnacles {Balanus cariosus [Pall.], B. glandula Darw., and Chthamalus dalli [Pil.]) and two species of mussels {Mytilus ediilis L. and M. cali- fornianus Conrad). The gooseneck barnacle [Mitella polymerus [Sow.] ) plays an important role in some parts of the community. A few others, such as the green anemone {Cribrina xanthogrammica Brandt), are local and less important. There is evidently competition for space among the dominants, for, when one is seated on a rock surface through some favorable condition, the others are excluded or may attach to the shells of the true dominants in sparing numbers. The most characteristic motile forms are gastropods of the genus Littorina (L. sitchana Phil., L. scutulata Gould, and other species) and of limpets {Acmaea digitalis Esch., A. cassis Esch., etc.). The food relations of these are not well known but evidently are based upon microscopic plants and animals. Other mobile influents of ir- 326 MARINE BIOTIC COMMUNITIES regular occurrence are gastropods of the genera Thais, Purpurea, and Amphissa, the first two of which feed upon barnacles locally and de- stroy considerable numbers. Rhythmic migrants and ecotone species play a considerable role. The purple shore crab [Hemigrapsis nudis Dana) , the place of which is taken by an equivalent species on the California coast, is signifi- cant. Several fishes, especially blennies such as Xiphister mucosus (Gir.) and Epigcichthys atro-purpiireiis (Kitt), have habits similar to those of the shore crabs. These motile species move into the com- munity and feed when the tide is in and retreat as it falls, stopping under stones near the average low-tide line. They are not present on vertical cliffs, but are numerous on boulder and loose rock-covered slopes and are much more abundant in the more protected waters. A few ecotone species, unable to live long when exposed to air, inhabit the upper portion of the community below and the lower portion of the Balanus-Littorina biome. The starfish, Pisaster ochraceus Brandt, is an example; it may be very destructive of barnacles and mussels lo- cally. Other less influent species such as the six-rayed star are more generally distributed. Extent, Rank, and Boundaries of the Balanus-Littorina Biome. This community occupies an area bounded roughly at the lower limit by the mean of one-half the lowest tides in each month and at its upper limit by the average high tides. It is, therefore, from 2 to 4 meters wide (vertically) in the area studied. The difference in taxo- nomic composition between this and subtidal communities is sharp. Balanus cariosus and glandula cease to be present at a distinct boun- dary, as do all other important species. Subtidal barnacles are almost as definitely distributed and only occasionally overlap the lowest por- tion for a few centimeters. Rasmussen (in Shelford et al., 1935) found a subtidal barnacle overlapping the intertidal species in south- ern California, but waves and constant ocean swells furnish the prob- able explanation. Gislen (1930, a, h) indicates a similar possibility on the Swedish coast (cf. also Hewatt, 1937). In a horizontal direction, the Balanus-Littorina biome is appar- ently widely distributed around the North Pacific. It is narrow be- cause of its dependence upon the rise and fall of the tide, but the sharp difference in 1 meter of height within the belt occupied by the biome may easily be the equivalent of 1,000 meters on a^ mountain side. For example, in the month of August at 48° 30' north latitude where the biome occupies 3 meters' vertical height, its lower edge is exposed to the air about 1 per cent and the upper edge about 96 per cent of the time; hence differences in physical conditions are very COMMUNITIES OF THE SEA BOTTOM 327 great within the biome. Its longitudinal extent is enormous, owing to the sinuate nature of coastlines, and is expressible in thousands of kilometers. Equivalent communities occur along most of the coasts of the northern hemisphere, where not crushed off by shore ice. However, in spite of the general circumpolar occurrence of Mytilus edulis as a dominant, it is not possible to consider the North Atlantic and North Pacific communities as associations of the same biome (Appellof, 1912; Pearse, 1913; Flattely and Walton, 1922; Beauchamp, 1923), although Newcombe (1935, a, b) has applied the same name. The other dominants are not the same, and the motile influents are all dif- ferent. The two biomes, however, are of the same type and life form, and belong to a closely related group similar to that of the coniferous forest biomes of North America and Eurasia (see also Colton, 1916). Associations. The Balanus-Littorina biome of the North Pacific is probably divisible into several associations, but only two appear to have been fully identified in the North Pacific. These are the Bala- nus-M. californianus association of the outer exposed shores and the Balanus-M. edulis association, usually in the more protected places. The former is the more definitely integrated and will be taken up first. Balanus — M. californianus Association. This is best developed on the open exposed shores and headlands of the Pacific coast of the northern United States and southern Canada. Mytilus californi- anus Conrad and Mitella polymerus (Sow.) are the most characteristic species. There is a more vigorous growth of all species and commonly a sharp separation into vertical groupings, termed faciations. This is well shown in the results of a study on the west coast of Vancouver Island (Table 13), where the sessile and motile species are separated as two groups and arranged in the order of abundance. The belts shown are often less definite, and occasionally all the species are mixed together. The variations are therefore properly called faciations. Balanus-M. edulis Association. On the coast where extended studies have been made, this association occupies the more sheltered shores and waters of low salinity. Mytilus edulis and various species of Fucus are most characteristic; Balanus glandula plays a more im- portant role. Cribrina, the green sea anemone, IVIitella, the gooseneck barnacle, and the ribbed mussel do not occur. There are also marked differences in the less abundant species present. The arrangement of the various dominants in this association has been studied by Rice (in Shelford et al., 1935), who found in the case of barnacles that combi- 328 MARINE BIOTIC COMMUNITIES nations of tides, cloudiness, temperature, rainfall, etc., over short periods control the arrangement of dominant species and the conse- quent local variations in community composition. Such local differ- ences have no significance except in the light of knowledge of condi- tions at the time of setting and later survival. Other locations such as tide pools are controlled by conditions evident at the time and place. The usual rock-bottomed tide pool is an example that contains Balanus of two species, both species of Littorina, Mytilus, and limpets, as well as hermit crabs and snails that frequent the intertidal area TABLE 13 Faciations of the Balanus-M. Californianus Association (Shelford, 1935) The term faciation is applied to minor subdivisions of communities characterized by the presence or absence of some of the characteristic species. Here they occur in a very short vertical space. No. per Square Meter Balanus-M. californianus Association (190 cm. wide): 1. Littorina-B. glandula Faciation (20 cm. wide) Balanus glandula Darw., barnacle 2,400 Littorina scutulata Gould, snail 200 2. Littorina-B. cariosus Faciation (45 cm. wide) Balanus cariosus (Pall.), barnacle 3,140 Littorina scutulata Gould, snail 338 Ac7naea digitalis umhonata (Nutt.) Reeve, limpet 70 Thais emarginata Desh., snail or whelk 38 3. Mitella-Mytilus Faciation (65 cm. wide) Mytilus californianus Conrad, Calif oi-nia mussel 1,945 Mitella -polymer us (Sow.), gooseneck barnacle 1,506 Balanus cariosus (Pall.), barnacle 1,363 Acrnaea cassis Esch., limpet 380 Littorina scutulata Gould, snail 225 Thais emarginata Desh., snail or whelk 180 Red sea anemone 120 Acmaea digitalis umhonata (Nutt.) Reeve, limpet 110 Littorina sitchana Phil., snail 50 4. Cribrina Faciation (60 cm. wide) Cribrina xanthogrammica Brandt, green sea anemone 3,140 Mytilus californianus Conrad, California mussel 3,000 Chthamalus dalli Pils. 1,* small barnacle 3,000 Chitons 40 Pisaster ochraceus (Brandt), com.mon starfish 6 Balanus cariosus (Pall.) 3 * Chthamalus does not average this den.sity over the area, but occurs in local clans ha\ing about this number per square meter. COMMUNITIES OF THE SEA BOTTOM 329 and are regularly found out of water at low tide. In addition, there are fishes that stay near the water margin and hence are quasi-resi- dents of the biome. To these are added a few subtidal animals, such as a Cucumaria, serjuilids, and occasional snails and chitons. Relationship of the Associations. Locally, the change from one association to the other maj' be found in passing from the outside of an open coast island to the inner or protected side. At a point on the south shore of the Strait of Juan de Fuca, all the principal species of both associations of the biome appeared on the same shore and were quite generally mixed together. This is the transition between the communities which may contain ]\Iitella and Mytilus calif ornianus as important general dominants, and those in which the former oc- curs in clans and the latter is not abundant. This arrangement simu- lates that of the dominants of the deciduous forest which occur to- gether in certain parts of the Appalachians (Braun, 1935), though in other places they are separated into three associations: oak-hickory, beech-maple, and oak-chestnut, each covering a large area. Community Development or Succession. Pierron and Huang (1926), in a brief study of the Balanus-M. edulis association, con- cluded that all the dominant species were present as juvenile stages on denuded rocks after a few weeks. An examination of pilings of known age in the Balanus-M. edulis area showed that the three prin- cipal dominants, Mytilus edulis, Balanus cariosus, and B. glandida, were all present on piles six months old. Piles one year old merely showed more and larger specimens of the same species. But Rice se- cured suggestions of non-survival of barnacles on planted rocks taken from land. These studies, however, were carried on only in the summer. Hewatt (1935, 1937) has found true succession in the Mytilus calif ornianus area, which he describes as follows: "The results of this investigation seem to indicate that ecological succession in the INIytilus habitat progresses in the following manner: (1) a clean area first becomes covered with a film of algae; (2) those forms which feed on this algal growth, such as the limpets, are the first animals to appear in the area; (3) during their respective spawning seasons, the mussels, gooseneck barnacles and rock barnacles attach themselves to the cleaned surface; (4) these sessile forms gradually come to occupy the greater part of the surface and make the habitat unfavorable for the larger specimens of limpets; (5) the limpets thus move to a higher zone in which the mussels and barnacles cannot exist. The upward migration of the limpets becomes quite evident soon after the appear- ance of the rock barnacles. The concentration of the larger limpets 330 MARINE BIOTIC COMMUNITIES along the upper margin of the Balanus covered area forms a very ob- vious line." He further states that the climax is reached only after more than two and one-half years. The rapid replacement and over- turn in the community constituents, however, stand out in contrast to terrestrial phenomena, and marked changes in the arrangement and abundance of certain constituents take place in short periods of time. In the Bay of Fundy communities, the predation of the starfishes, sea urchins, and whelks limits the downward extent of the biome, while in the North Pacific physical factors appear to control the lower boundary. In the Bay of Fundy and Gulf of St. Lawrence, the corre- sponding biome or many of its constituents extend well below mean low tide (Mossop, 1922; Huntsman, 1924; Newcombe, 1935 a; see also Brandt, 1896). SuBTiDAL Barnacle-Gastropod Communities Marine communities have been so little studied from a quantita- tive standpoint that only one examj^le of this community has been even partially evaluated. It characterizes the sea floor about the San Juan Islands in Puget Sound and on the west shore of Vancouver Island. However, it is to be expected that it occurs over the con- tinental shelf of the North Pacific in the clearer and more open waters. The prevalence of large echinoderms and snails has led to its designation as a sea urchin-gastropod community ( Shelf ord and Tow- ler, 1925; Shelford et ah, 1935; Wisner and Swanson, 1935). Its suc- cession, extent, etc., have been so little studied that it cannot be named with certainty. Green Sea Urchin-Triton Community (Strongylocentrotus-Argobuccinum Biome) The most important sessile dominants are three species of Balanus, of which B. nubilis Darw. is the largest and most conspicuous, along with the sessile cucumber {Psoitis chitinoides H. L. Clark) , the rock oyster {Pododesmus macroschisma Desh.), and scattered brachiopods. These or similar species are always present; they do not, however, cover large areas of bottom to the exclusion of other species, as the tidal barnacles do. The control of the habitat and community is ef- fected by slow-moving forms such as the sea urchins {Strong ylocen- trotus drobachiensis Miill, and franciscanus A. Ag.) which commonly are abundant, snails such as Argobuccinum oregonensis Red., Tricho- tropis cancellata Hinds, Calliostoma costatum Mart., and numerous crepidulas. Two or three sea cucumbers occur, the most noteworthy COMMUNITIES OF THE SEA BOTTOM 331 being the very large Stichopus californicus Ed., and pectens are often abundant. The motile influents include fishes and crabs of the genera Hyas, Cancer, Orcgonia, and shrimps of the genus Pandalus. Of the most regularly occurring fishes are the northern sculpin {Icelinus borealis Gibb), the giant sculpin {Myoxocephalus polyacanthocephalus [Pall.]), and the grunt fish {Rhainphocottus richardsoni [Gunther]). There are also various crabs, shrimps, gastropods, and starfishes, all of relatively large size. Subdivisions. The major community is divisible into two sub- ordinate connnunities in accordance with depth. Tlie first ranges from the surface to 35-50 meters and the other from 35-50 to 225 meters, or even deeper. Green Sea Urchin-Kclpcrab Community {Strong ylocentrotus-Pu- gettia Association) . The biome building influents already enumerated occur throughout and make up a considerable part of the population. The large echinoderms, Stichopus californicus and Strongylocentrotus franciscanus, are abundant and conspicuous in this association and very few in the one in deeper water. Two other cucumbers, several snails, and limpets occur in noteworthy abundance. Various fishes such as rock fishes (Sebastodes), several sculpins, but particularly the blennies, frequent the shallow waters. There are also numerous char- acteristic Mollusca. This association is characterized by algae, both red and green. They are usually irregularly distributed and do not have a marked effect on the animals present. They are hardly to be classed as dominants, but since they occur over only a portion of the bottom, the areas which they cover are best regarded as faciations. A faciation of INIelanophyceae occurs between mean low tide and depths of 15 to 20 meters, and those of Rhodophyceae mainly be- tween depths of 10 and 20 meters, only a very few small animals being characteristic of the latter. Other faciations occur where the bottom soil differs ; thus on mud bottom two or more of the numerous Strongylocentrotus-Pugettia prevalents drop out and Cardium cali- fornense Desh., Yoldia scissurata Dall, and other species of similar habits take their places. The community otherwise retains its biome and association prevalents (see Andrews, H. L., 1925; and Andrews, F. B., 1925). Green Sea Urchin-Cushion Starfish Community [Strong ylocentrotus~ Pteraster Association) . This occurs below 35-50 meters and down to at least 225 meters; the species characteristic of the Pugettia associa- tion either become scarce or drop out. Several large showy echino- derms take their places; these are notably the cushion star [Pteraster 332 MARINE BIOTIC COMMUNITIES tesselatus Ives), the rose star {Crossastcr papposus [L.]), and the basket star {Gorgonocephalus euclenis M. & T.). There are also char- acteristic species of brachiopods, hydroids, pecten, and of crabs and shrimps. The rat-tailed fish {Asterotheca alascona [Gilbert]) and Gilbert's sculpin {Gilbertidia sigolutes [J, & S.]) are perhaps most common among the several species here. The species listed on page 330 as characteristic of the whole major community are usually present in abundance. Faciations and Relations. This association is characterized by a Modiolus faciation, which covers mud bottoms in the deeper parts of the continental shelf in which the hydroclimate is suitable for the biome (Strongylocentrotus-Argobuccinura). The shells form a hard bottom on which the other dominants may rest. Again some depres- sions may have been filled with silt and shells which support the dominants. A sere may be traced beginning with burrowers in the mud of such depressions. These are later smothered out by IModiolus, and this in turn eventually gives way to shells of dead animals which are used as a resting place for the biome constituents. Bivalve-Worm Communities Two major communities of the Puget Sound area in the North Pa- cific belong to this type; one is characterized by mollusks of the genera Macoma and Paphia and the other by two other mollusks be- longing to the genera Pandora and Yoldia, the former being in shal- lower water than the latter. Both stand out in contrast to the bar- nacle-gastropod communities because of the less showy and generally smaller size of most of the constituents, as well as the striking dif- ferences in life form and life habit. However, neither has been studied sufficiently to be named with certainty. Communities of the same two types occur in the partially enclosed waters of both the North Pa- cific and North Atlantic. Petersen's Macoma community (JMacoma- Mya biome) and the Macoma-Paphia community are of the same type, and the known facts regarding the two supplement each other (cf. Huntsman, 1918; Ford, 1923; Hunt, 1925; Stephen, 1931, 1933). COMMUNITIES OF THE SEA BOTTOM 333 shallow- water communities (habitat partially exposed at high tide) Macoma-Paphia Biome In the Pugct Sound waters (North Pacific), this biome is usually found well developed between 8 meters below and 1 meter above mean low tide (the tidal amplitude being 3 and 4 meters). There are about 2 meters of true ecotone between 8 and 10 meters' depth and the com- munity thins out to nothing between 1 and II/2 meters above mean low tide. Clams of four species, Macoma nasuta Con., secta Con., inqui- nata Desh., and Paphia staminca Con., usually make up the great bulk of the population. The clam worm. Nereis virens Sars., is also a regular constituent. Several other species of bivalve mollusks al- ways occur, but in varying numbers. The most important motile in- fluents are several species of flounder (especially Psettichthys melan- ostictus [Gir.] and the tide-pool sculpin {Oligocottus maculosus [Gir.]) (cf. Fraser and Smith, 1928, a, b). Two subdivisions or associations have been recognized, of which the Macoma-Paphia association fits the general description of the biome. The second association (Macoma-Leptosynapta) possesses the same constituents but in different abundance. The butter clam {Paphia staminea) is much less, the cockle {Cardium corbis Mart.) much more, abundant. The lugworm (Arenicola claperedii Lev.) and the wormlike cucumber {Leptosynapta inhaerens Ver.) take the place of various smaller worms of the other associations. Both associations are characterized by eelgrass, usually in re- stricted areas representing depth belts. The eelgrass is quite impor- tant and supports algae, numerous crustaceans such as Caprella, large amphipods, isopods, and snails such as Haminoea and Lacuna, espe- cially in the Macoma-Paphia association. In the Macoma-Lepto- syapta association the additional species are more numerous, and in some cases sand dollars are abundant locally (Shelford et al., 1935). The importance of eelgrass has been brought out by Petersen and associates and will be discussed later. The Pacific oyster evidently represents a fragmented faciation in the southern part of this community, which with overfishing was com- pletely destroyed by the burrowing and earth moving of the large crustacean, Upogebia. The communities of the northeast Atlantic and adjacent Arctic which are similar to Macoma-Paphia community in life forms and position relative to tidal levels have been studied, but their rank in terms of biome and association can only be sug- gested and may prove incorrect. 334 MARINE BIOTIC COMMUNITIES Macoma-Astarte Community (Biome) This is an arctic ocean community with relicts farther south which Spiirck (1935), who calls it the Macoma calcaria community, de- scribes in the following terms: "This community is characterized by the occurrence of Macoma calcaria as the constantly predominating species. Beside this species, forms such as Astarte borealis, ellip- tica, montagui, Portlandia, Yoldia hyperborea, Nucula tenuis, Leda, etc., may occur; also Nephthys ciliata, species of Pectinaria and Har- mothoe, Oyniphis conchylega and several other Polychaeta have been found. Among echinoderms, Myriotrochus rinki and Ophiocten seri- ceurn are the most frequent. This community has been described from the coasts of the East Greenland fjords (Thorson, 1933, 1934; Spiirck, 1933), where it seems to occur everywhere on clay bottoms and on sand mixed with clay. It occurs in different locally and bathy- metrically determined varieties. The lower limit of this community in the East Greenland fjords is about 50 meters. Outside the East Greenland fjords this community has been described from various other arctic waters, namely the Storfjord in Spitzbergen (Brotzky, 1931), where this community is present in the inner part of the fjord, on soft bottoms near the Spitzbergen Bank (Idelson, 1931), in the waters near the Kanin Peninsula (Zenkevitsch, 1931), in parts of the Barents Sea, in the White Sea (Zenkevitsch, 1927), and northern Norway (Soot-Ryen, 1924). In the Barents Sea it occurs at greater depths than in the East Greenland waters, down to 100-150 meters. The Macoma calcaria community occurs at Iceland and the Faroes (Sparck, 1929)." The fragments in the Baltic are regarded as relicts (Fig. 76). Macoma-Mya Community (Biome) (Petersen's Macoma Community) in the North Atlantic (Fig. 75) It occurs slightly above mean low tide to 20 meters' depth in the Baltic. The outstanding bivalves are Mya arenaria, Macoma bal- thica, and Cardium edide, polychaete worms, Arenicola marina, Aricia and Nephthys. Blegvad (1916) divides the community into three parts, essentially based upon dcptlis. We have ventured to call these faciations in accordance with the facts brought out on page 247. The Mya-Cardium-Arenicola faciation occurs in the shoreward side of the Zostera. This is frequented by fishes such as sticklebacks and is the breeding place of gobies, each at the proper season. Blegvad does not record a barnacle-gastropod-mussel community such as is Fig. 75 & <» ^-i^B ^^Wf> 55M5'N :••:•■; -.^^^^^r^ SS'OO'N ■ ■ /^.' . "■ ' '^^i^^^^ ' J>^ . ■ ■ /.'"■ • ^'^'^ " . ■ f . - ■ ' . 54°45'N "■/;y;;>@/' q ■ , 54°30'N ". ■ >^' ■,'■'-','. fj) 1 ■ ■ ■ I ' 1°30'E 2°00'E 2°30'E 3°00'E 3°30'E 4°20'E Fig. 80. — Spisula subtruncata consociations. The oldest areas are solid black; those of medium age, shaded; and the youngest, unshaded. The stippling of areas outside the patches is purely diagrammatic. Each dot represents a large number of individuals of Spisula outside the aggregations because Davis gives only frequency and not spatial relations. (After Davis, 1923.) Brissopsis-Amphiura-Ophiura Ecotone. Sparck (1935) states that Brissopsis-Amphiura chiajei (BCh.) and Brissopsis-Ophiura {Ophio- glypha)* sarsi community appear to represent a transition which (in * Changes in generic names which involve the naming or other designation of communities or their predominant species in the North Atlantic and adjacent waters are as follows: Abra becomes Syndosmya This changes the designation of Petersen's Abra community (Abra with Echinocardium ; b(abc E) and renames the constituents of others. Ophioglypha becomes Ophiura This involves changing Petersen's Brissopsis-(Ophioglypha) sarsii designation as noted above. AxiiiuJi becomes Thyasira Thyasini flexuosa is a common or abundant constituent of two communities which may be united as a biome (see Fig. 84, p. 349). Maclm becomes Spisula The species subtruncata is prominent because of the very dense aggregations in the North Sea (Fig. 80). 344 MARINE BIOTIC COMMUNITIES €) • .^ €) \ \ \ "T. t> Fig. 81. — The Brissopsis-Amphiura ecotone. (After Petersen, 1918.) Fig. 82. — The Amphilepis-Pecten biome. (After Petersen, 1918.) COMMUNITIES OF THE SEA BOTTOM 345 our nomenclature) would lie between the Echinocardium-Thyasira Biome and the Amphilepsis-Pecten Biome. This ecotone appears to occur between about 50 and 380 meters depth in the Danish waters. Haploop's Community {Association or Faciation) . This is a small area northeast of the island of Zealand, omitted from the map. Hap- loop is included here because of its small size and the presence of several predominants of the major community among the Haploops crustaceans. These appear to be another association of the same major community. The arrangement which we venture to present here is in a considerable measure for the purpose of paralleling the phe- nomena found on land. Astarte — Area Community (Biome) This community is characterized by Astarte crenta, by Area gla- cialis, and also by several of the lamellibranchs and annelids which were also found in the Macoma ealearia community, several species of Portlandia, Cardium, Pecten groenlandiciis, for instance. "This com- munity is described from east Greenland waters, inside the fjords and also in the pack-ice belt at depths from about 50 meters to about 250 meters (Sparck, 1933; Thorson, 1934). Further, according to the papers by Zenkevitsch, Brotzky, and Idelson it seems to occur in the central parts of the Barents Sea and in the Kara Sea, and it there- fore appears to occur in arctic seas — in several varieties below the Maeoma ealearia community. It seems also to occur in Ramfjord in northern Norway (Soot-Ryen, 1924)" (cf. Sparck, 1935, 1937). Amphilepsis-Pecten Community (Biome) (Fig. 82) The Amphilepsis-Pecten community occurs in deeper water, ocean- ward from the Echinocardium-Axinus biome (see map, page 349). A more northerly type termed by Sparck (1935) the Astarte crenata community may perhaps be appropriately called the Astarte-Arca biome. Foraminifera Community This occurs in deeper water than the preceding as a rule. Some annelids and mollusks are found with the Foraminifera. The ob- servation of Verrill (1871-72) suggests a series of communities east of Massachusetts resembling those west of Dcnmai'k. Variations in the Bivalve-Annelid Communities. Two types of variation in composition have been described, and called lociations or faciations, depending on the extent. Jensen (1919) describes the for- mer in the various broads of the Limfjord. In the quotation below, 346 MARINE BIOTIC COMMUNITIES Fig. 83a Fig. 83. — Communities of a large protected bay of the northeast Pacific. (After those represented for land in Fig. 54, page 255, which shows the associations or 12 COMMUNITIES OF THE SEA BOTTOM 347 Fig. 83b Shelford, 1935.) The phenomena indicated on the map are in agreement with of the grassland. (One inch on the map equals approximately 6 nautical miles kilometers.) 348 MARINE BIOTIC COMMUNITIES the terms applied to communities of different rank in this discussion are inserted after those used by the author quoted. The variation appears rather small to fit our concept of the association ; the brackets indicate the nomenclature of our system. "1. A Nucula-Corbula-association [faciation], characterized too by its nearly total want of Solen. This association [faciation] is found purest in Nussum Bredning, where the Nucula amount for a series of years has been ca. 30-50 g. per square meter; during the last years it has decreased a little, yet only to ca. 10 g. In the other Brednings, an amount of Nucula exceeding 10 g. only appears as an exception. Corbula, which is found in great amounts in Nissum Bredning together with Nucula, is probably in much smaller degree a characteristic animal; it is, for instance, still found in rather important amounts in Skive Fjord. In the Nucula-Corbula association [facia- tion] , Abra is only found in smaller amounts, Solen is rare and Alya truncata is not found at all. That Abra and Solen appear in such small amounts in Nissum Bredning is probably caused by the fact that they are specially persecuted by the plaices. "2. An Abra-Solon association [faciation], where Nucula and generally also Corbula are of subordinate importance. This associa- tion [faciation] is most typically found in Liv0 Bredning. As men- tioned above, the two bivalves are found in very fluctuating amounts in the various years. "In Lavbjerg and Kaas Brednings transitions between the Nucula- Corbula and Abra-Solen associations [faciations] are found. "3. An Abra-Solen-Mya {truncata) association [ecotone], found in the side-Brednings originating from Liv0-L0gstr0 Bredning, respec- tively Thisted-Visby Brednings and Risgaards and Lovns Brednings. This association is displaced by the occurrence of Mya truncata. "When entering into shallow water or in the very inmost Bred- nings, this association is displaced by the Macoma baltica formation [biome]. One of the characteristic animals of this formation, Mya arenaria, is found together with animals of the Abra-Solen-Mt/a trun- cata association [faciation] in Lovns Bredning as mentioned above." Another important type of variation has been discovered in the Echinocardium-Thyasira community by Davis. On the Dogger Bank, he described several areas dominated by Spisula [Mactra) subtrun- cata (da Costa), from 500 billion to 5 trillion individuals covering several hundred square miles. He believes that these result from fail- ure of the spat to scatter about (Fig. 80, p. 343). Changes from year to year (annuations) are shown in Fig. 40. The near absence of some of the dominants in certain years is notice- COMMUNITIES OF THE SEA BOTTOM 349 able. The variation of non-mobile species in the same community is also illustrated in Fig. 39, page 181. The Nature of Dominance in Bivalve-Annelid Communities All the communities of this type that have been investigated in- clude bottom-feeding, rapid-moving and often migratory fishes, which Fig. 84. — Communities of the North Atlantic interpreted in accord with the principles found among the North American land communities Fig. 54, page 255, and the marine communities of the shore waters of the North Pacific. (Fig. 83 and pages 346-347, modified from Petersen, 1914.) range over two or three major communities as do the birds and large mammals of the land. A second group of slow-moving and relatively stationary, but usually important, influents, are ophiurids in the North Atlantic and both asteriods and ophiurids in the North Pacific. They are in part predatory and play an important role. Gastropods and large crustaceans such as crabs and shrimps are present, but ordinar- ily of lesser influence owing to the small numbers and, in the case of 350 MARINE BIOTIC COMMUNITIES the gastropods, to the relatively small size of the individuals also. The great majority of bivalves and annelids are stationary; they con- stitute the most important constituents as regards competition for space and reaction on the substratum. Blegvad (1914) made a study of the nutrition of the bottom in- vertebrates, classifying the foods as follows: 1. Plant food consists of fresh-growing benthic plants. 2. Detritus is divided into two classes: (a) Plant detritus which is floating plant material; some of it is fresh. (b) Bottom detritus, which consists of fine particles of j^lant and animal material settled on the bottom. He not only examined the stomach contents of the animals, but also made aquarium experiments and observations. The material studied includes the more important representatives from the sta- tionary and slow-moving bottom constituents of the Macoma-Mya, and Echinocardium-Thyasira biomes. The bivalves were found to live entirely upon detritus. A few in- vertebrates are herbivorous detritus-eaters; Rissoa, a small snail abundant on Zostera, is an example. Most Polychaeta are detritus- eaters. All the serpent stars of the genera Ophiopholis and Ophiura (Ophioglypha) , which play a prominent part in the communities, are carnivorous detritus-eaters. Echinocardium belongs here also; it feeds on detritus and young bivalves. Petersen (1918:17) has pointed out the scarcity of bivalves where serpent stars are abundant and credits them with the control of com- munities. In the second paragraph of the quotation, by "grounds near land" he refers to those areas occupied by the Macoma community. He states his conclusions in the following terms: "Most common ma- rine animals living on the bottom commence their existence as minute larvae in the water, and sink to the bottom at a very early stage, as for instance the bivalves. And it is remarkable to note how in those communities where the Amphiura spread their arms abroad, forming a network in the bottom (see PI. IV and V), extremely few bivalves are found at all. The young bivalves will here doubtless as a rule be devoured, while still quite small, by the Amphiura, and only a very few individuals of certain species manage to survive. Both in shallow water near the coasts, and farther out where it is deeper, where few or no Amphiura are found, there are quantities of small bivalves (see PI. VI and I, II and III) of many different species, for instance, Mac- tra, Tellina, as also in summer on grounds near land, where few or COMMUNITIES OF THE SEA BOTTOM 351 no echinoderms at all are found. That the great majority of these young individuals never attain full growth, is doubtless primarily due to the fact that the environment is here unfavorable in the long run; the action of the waves, for instance, will at times be too violent; very low water will kill off numbers of the young, as also severe cold in winter, etc., presumably the same factors which account for the ab- sence of echinoderms in the same localities. It is in such places as these that the species of the jMacoma communities can live and thrive continually; they are the only forms that are able to withstand the severe conditions prevalent in a degree sufficient to ensure the mainte- nance of the species. "It is remarkable, having in mind the hardiness of these Macoma species, that they should not be found deeper out in the Kattegat, throughout the whole of the Venus area, where we might imagine they would find the most favorable environment of all, and where Mytilus also make their appearance on any buoy set out, but hardly ever live on the bottom itself. It cannot be the depth which keeps the Macoma species away from these areas; we find for instance, Mya arenaria, Cardium edule, Macoma baltica and Hydrobia out in at least 20 meters depth in the Baltic where their predominance is undisputed; in the Baltic, however, east of Gedser, there are, as we know, no echinoderms, nor are such found in the low water on the shores of the Kattegat. I must, therefore, suppose that it is just certain echino- derms which prevent the animals of the Macoma community from spreading over larger areas than they occupy in fact." The fishes have potent effects in the communities, but these are greatest in determining abundance, life span, and replacement among those community constituents that are able to exist with them, but their effect in eliminating certain forms from the communities en- tirely has been but little investigated (Jensen, 1919). However, the work of Blegvad (1925) shows the coaction of fishes on the bottom- inhabiting species to be sufficiently great to class them among the dominants. All the community constituents influence the bottom, especially w^here this is little disturbed by waves and currents (Moore, 1931, a, b) ; succession by reaction is to be expected but cannot be followed without great labor over long periods. Here again, as in fresh water, dominance is as much a matter of coaction as of reac- tion, if not more. The relatively short life histories and life span of marine plants and animals and their frequent fluctuations in abundance led Petersen to select single species as indicators of communities. For the selection 352 MARINE BIOTIC COMMUNITIES of a species as a community indicator from this point of view, it must be: 1. Abundant. 2. Uniformly distributed. 3. Always present in considerable abundance when other spe- cies decline almost to zero. 4. The limits of its range must coincide with those of various less stable constituents. The life forms that signalize the most important constituents serve as important criteria, just as they do for land plants. Petersen's use of single species as indicators has led to apparent confusion in the minds of other investigators (Ford, Davis, Stephens, et al.). A closer adherence to the practice of plant ecologists allows a greater latitude. In this, a large series of dominants of a limited number of life forms is recognized, and in some situations nearly all are found mixed together (Clements, 1920; Braun, 1935). They usually segregate into large units or associations, each characterized by a definite group of wide-ranging and restricted species character- istic of the particular association. Toward the outskirts and in local areas some of these drop out and occasionally some species are added. These variations are those called faciations. Petersen's reluctance to consider fishes and other motile forms a part of the bottom community left something to be desired. His work, however, was superior, from a bio-ecological viewpoint, to that of most plant ecologists, because he and his associates were primarily concerned with the food of fishes and worked out the interchange of effect between the motile and sessile constituents. They merely found difficulty in connecting fishes with the communities in mapping, and the fishes, etc., were treated in a somewhat detached manner. They made many facts available; however, our attempt to organize them in the preceding pages is doubtless quite imperfect. The same is true of the endeavor to synthesize the animal constituents of the land com- munities considered. A certain amount of reinvestigation will be necessary to establish definite facts in all cases. COMPARISON OF MARINE AND TERRESTRIAL COMMUNITIES The preceding pages have indicated that the phenomena of dis- tribution of relatively stationary organisms on the sea bottom and on land are quite similar and lend themselves to a similar type of classi- fication for greater ease in description. The failure to find succes- COMMUNITIES OF THE SEA BOTTOM 353 sional phenomena in the faciations of the Balaniis-Littorina biome in the enclosed Puget Sound waters (Shelford et al., 1935) had seemed to offer a difficulty. These studies, however, were carried on only for a short period, and the work of Hewatt (1935) on the Balanus-My- tilus californianus association on the open shore over a long period has demonstrated a clear succession. This fact, and the almost certain occurrence of succession where bottom must develop, covers nearly all the distribution phenomena of the bottom fauna to parallel those de- scribed for plants and considered together on the surface of the land. Since climax and succession have formed the natural basis for classi- fication on land and promises to do so in the sea, the study of com- munity development in connection with public works, especially those in waters of high salinity, where new channels are opened and piers built or dredging done, should be encouraged. The investigation of successional changes in deeper waters is much more difficult but not impossible. Pelagic communities in themselves, which appeared to afford unusual difficulties as regards dominants, have gradually be- come susceptible of analysis as knowledge has advanced, and study of succession or invasion of denuded water is coming into the range of the possible. APPENDIX METHODS General methods of ecological investigations are treated in various refer- ence works (Abderhalden's Handbuch, 1925-1931; Adams, 1913; Shelford, 1913, a; 1929, a), and only a few features of procedure with reference to animals are presented. Let us assume a sample catch of all the organisms from 10 square kilo- meters of primeval grassland (or a similar area of sea bottom). The grassland catch would include everything from the bison to the soil bacteria and Protozoa. The community function of these various organisms could not be determined from inspection. Some of them would be relatively large and con- spicuous, others numerous and made noticeable by their numbers and ex- tension over large areas. Quantitative methods are absolutely necessary. On the basis of size and abundance, various degrees of influence and domi- nance may be roughly recognized, but the actual community functions still have to be determined by long study, both field and laboratory; but no matter what the results may be, the abundance of any organism is a matter of first importance, though often very difficult to ascertain. After all the dominants, subdominants, and influents of various grades have been evaluated as far as is ordinarily practicable in a field investigation, there may remain many small organisms to which no relative value can be assigned. These are small herbs, insects, fungi, bacteria, protozoans, lichens, and various invertebrates. The more abundant of these still have to be called predominant or prevalent among their kind. After evaluation in one locality is completed, organisms have further to be evaluated as to their geographical extent, uniformity of distribution, and stability of mnnbers. This further evaluation is usually accomplished in connection with the recognition of the largest communities of which the local ones are a part. Abundance is always a prime consideration, though ideally the force exerted by the populations is the fact required and sought. In terrestrial communities two principal methods are used in dealing with smaller invertebrates. Placing an inverted can over a known area at the time of minimum activity and killing and recovering the organisms (Wolcott, 1918; Shelford, 1929, a; Beall, 1935) is one standard method. The use of the sweep net to secure invertebrates from the vegetation is a general one and has been discussed especially by Zubareva (1930), Gray and Treloar (1933) and Beall (1935). Gray and Treloar selected an alfalfa field because of its uniformity, but their results indicate that the insect population is more heterogeneous than that of a climax vegetation, and this is to be expected because of the 355 356 APPENDIX youth and agricultural disturbance of the habitat. Beall recommends a square net, a 250-cm stroke, and the studj' and statistical treatment of each sample STATIONARY LINE OF 99 TRAPS ^ ^ 3 Feet MOVING QUADRAT OF 99 TRAPS ooo OOOOOOO oooooooooo \ \ V \ I I I I I I • 111^ A / I I I I I I I I I I ./ / I I I > • ) I I I I I / / / OOOOOOOOOOO I Group of Three Traps, as Indicated at Left O Past or Future Locations Fig. 85. — Showing the Townsend (1935) method of trapping of mice to secure all the regular population. separately. This is justified by the variation in strokes, loss of individual animals, etc. (cf . Graham, 1929, a) . APPENDIX 357 The trapping of small animals has also been given attention. Townscnd (1935) has worked out a plan for such trapping. The Illinois Natural His- tory Survey has used a unique method in estimating fish populations. Num- bers of fishes are caught and marked, and the proportion of these that enter into subsequent catches is used to estimate total populations. For example, if 10 per cent of the subsequent catches were made up of marked individuals, it would be assumed that the number marked was 10 per cent of the total population. The numbers of birds and larger mammals are usually ascertained by cruising. Only experts are really effective in estimating numbers of birds. The person generally best at field identification usually reports most birds. The general impression is that most of the figures published are underesti- mates. All observations should be made at the hour of maximum activity, often early morning, but different for different species. Methods of preserving these animals in natural numbers in public reserva- tion areas too small for their proper support are discussed by Hall (1929) and Shelf ord (1933, 1936). This consists in surrounding the small sanctuary area by buffer zones or zones of protection of animals traveling out of the sanctuary in course of food-getting, seasonal migration, etc. Such areas are of the greatest value to science. They constitute check areas for reservations under management. In dealing with the more strikingly influent animals, for example, mam- mals and birds, one is confronted with the fact that they have commonly been exterminated or suppressed in most of the places where it is desirable to know what their effects may have been under primeval conditions. In order either to reconstruct a former condition or to determine an existing one in regard to these animals, the following operations are necessary: 1. The species of influent animals occurring in a biome should first be listed for several points not too near the biome periphery. 2. The range of these species in and out of the biome areas must be ascertained as completely as possible. 3. The relative abundance of a species in the parts of its range must be ascertained from literature. The records are fragmentary and in obscure publications. 4. The breeding, shelter, and feeding preference must be determined in relation to daily and seasonal cycles. Home range should be ascertained. 5. These habitat preferences must be interpreted in terms of the various serai stages and the climax. a. Water. 6. Water margins. c. Bare areas of all kinds. d. Early serai stages. 6. The distribution of the habitat type occupied or utilized by the animal must be determined. Its local occurrence in other biomes as bare areas, devel- 358 APPENDIX opmental stages, and relicts should be used to interpret extension of range be- yond the limits of the biome. 7. The distribution of the principal food plants or animals must be ascer- tained. The greatest importance is to be attached to habitat relations. This must be learned particularly with reference to early serai stages or climax and late subclimax stages of vegetation, as the primary classification of influents has practically to be based upon these considerations. The quantitative methods used in water are numerous, and the reader should consult Abderhalden's Handbuch; Juday (1916, 1926); Ward and Whipple (1918); Reighard (190S); Ekman (1911); Needham and Christen- sen (1927); Moon (1935); and Williams (1936). BIBLIOGRAPHY Numbers in parenthesis refer to pages on which article in question is cited. A few items carried in the bibliography are not cited; for these, the page numbers are preceded by the word "See." Abderhalden, 1925-31. Handbuch der biologishen Arbeitsmethoden. (Cited under the several authors.) Leipzig and Vienna. (17, 355, 358) Adams, C. C, 1901. Baseleveling and its faunal significance. Am. Nat., 35:839-852. (308) 1906. An ecological survey in northern Michigan. Mich. Board Geol. Surv. Report, 1905:9-12. (7) 1909. Isle Royale as a biotic environment. Mich. Geol. Surv., Ann. Rep., 1908:1-52. (8) 1913. Guide to the study of animal ecology. 183 pp. New York. (355) 1915. An ecological study of prairie and forest invertebrates. Bull. 111. St. N. H. Surv., 11:33-276. (8,274) Ad.\mstone, F. B., 1923. The distribution and economic importance of the mollusca in Lake Nipigon. Univ. Toronto Studies: Biol. Series, 22:69-119. (306, 307) 1924. The distribution and economic importance of the bottom fauna of Lake Nipigon with an appendix on the bottom fauna of Lake Ontario. Univ. Toronto Studies: Biol. Series, 24:3-199. (306, 307) Adamstone, F. B., and W. J. K. Harkness, 1923. The bottom organisms of Lake Nipigon. Univ. Toronto Studies: Biol. Series, 22:123-170. (307) Allard, H. a., 1928. Bird migration from the point of view of light and length of day. Am. Nat., 62:38^-408. (211, 215) Allee, W. C., 1923. Studies in marine ecology: I. The distribution of common littoral invertebrates of the Woods Hole region. II. Some physical factors related to the distribution of littoral invertebrates. Biol. Bull., 44:167-191; 205-253. (336) 1931a. Animal aggregations. 409 pp. Chicago. (22, 57, 145, 147, 149, 151, 159, 167) 19316. Cooperation among animals. Jour. Sociol., 37:386-398. (See 151) Allen, A. A., 1934. Sex rhythm in the ruffed grouse {Bonasa umbellus Linn.). Auk, 51:180-199. (170) Allen, W. E., 1921. Problems of floral dominance in the open sea. Ecology, 2:26-31. (314) 1926a. Remarks on surface distribution of marine plankton diatoms in the East Pacific. Science, 63:96-97. (314) 19266. Investigations on phyto-plankton in the Pacific Ocean. Proc. 3rd Pan- Pac. Congr., Tokyo, 250-263. (314) 1929. Ocean plankton and plankton problems. Sci. Monthly, 28:232-238. (314) 1932. Problems of flotation and deposition of marine plankton diatoms. Trans. Am. Micr. Soc, 51:1-7. (314) Alverdes, F., 1927. Social life in the animal world. New York. (22) 359 360 BIBLIOGRAPHY American Committee for Wild Life Protection, 1934. The present status of the musk-ox. Special Publication, 5. Cambridge, Mass. (114) American Ornithological Union, 1931. Check list of North American birds. Lancaster. (274) Amory, C, 1931. Reports and Minutes of the Matamek conference on biological cycles. MS. unpublished; copy in U. S. D. A. Library, Washington. (195) Andrews, F. B., 1925. Resistance of marine animals of different ages. Pub. Puget Sd. Biol. Sta., 3:361-363. (331) Andrews, H. L., 1925. Animals hving on kelp. Pub. Puget Sd. Biol. Sta., 5:25-27. (331) Antevs, E., 1922. The recession of the last ice sheet in New England. Am. Geog.Soc.Res.Ser.No.il. New York. (192) 1925. On the Pleistocene history of the Great Basin. The big tree as a climatic measure. Carnegie Inst. Wash. Pub., 352:51-153. (192) 1928. The last glaciation with special reference to the ice retreat in northeastern North America. Am. Geog. Soc. Res. Ser. No. 17. New York. (192) Anthony, H. E., 1928. Field book of North American mammals. 625 pp. New York. {See 257 to 289) Appellof, a., 1912. Invertebrate bottom fauna of the Norwegian Sea and North Atlantic. "The Depths of the Ocean," Chap. 8:457-560. London. (16, 327) Atkins, H. A., 1883. American redstart {Setophaga ruticilla). Ornith. and Oologist, 8:31. (224) Atkins, W. R. C, 1922. The hydrogen ion concentration of sea water and its biological relations. Jour. Mar. Biol. Assoc, 12:717-771. (316) Babcock, John P., 1908. Report of the commissioner of fisheries for 1907. Rep. British Columbia Com. Fish., 1907:5-18. (187) 1914a. Sockeye Salmon-pack of Fraser and Puget Sound. 1900 to 1913, inclusive. Rep. British Columbia Com. Fish., 1913:15. (187) 19146. The spawning beds of the Fraser. Rep. British Columbia Com. Fish., App. 1913:17-38. (187) Babler, E., 1910. Die wirbellose terrestrische Fauna der nivalen Region. Rev. Suisse ZooL, 18:761-915. (10) Bailey, F. M., 1917. The white pelican. In F. M. Bailey's "Handbook of birds of the western United States." 690 pp. Boston and New York. (132) Bailey, V., 1905. Biological Survey of Texas, U. S. Dept. Agr. N. Am. Fauna, 25:1-222. (274) 1913. Life zones and crop zones of New Mexico. Ibid., 35:1-95. (274) 1926. Biological survey of North Dakota. Ibid., 49:1-229. (123) 1930. Animal life of Yellowstone Park. Springfield, 111. (33) 1931. Mammals of New Mexico, U. S. Dept. Agr. N. Am. Fauna, 53:1-412. (112, 253, 254, 274) 1936. Mammals and life zones of Oregon. Ibid., 55:1-416. (293) Baker, F. C, 1916. The relation of mollusks to fish in Oneida Lake. Tech. Pub. 4, N. Y. St. Coll. For., Syracuse Univ., 16 (21): 15-366. (119, 307) 1918. The productivity of invertebrate fish food on the bottom of Oneida Lake with special reference to mollusks. Tech. Pub. 9, N. Y. St. Coll. For., Syracuse Univ., 18 (2): 10-264. {See 119, 307) 1922. The molluscan fauna of the Big Vermilion River, Illinois. 111. Biol. Mon., 7 (2):105-224. (5ee 119, 307) BIBLIOGRAPHY 361 1928. The fresh water mollusca of Wisconsin. Wis. Geol. Nat. Hist. Surv. Bull. Pelecypoda, 70 (II):l-482. (55, 307) Baldwix, S. p., 1919. Bird banding by means of systematic trapping. Proc. Linn. See. N. Y., 31 :23-56. (211) Baldwin, S. P., and S. C. Ivendeigh, 1932. The physiology of the temperature of birds. Sci. Pub. Cleveland Mus. Nat. Hist., 3:1-196. (210, 213) Beall, Geoffrey, 1935. Study of arthropod populations by the method of sweep- ing. Ecol., 16:216-225. (355) Beauchamp, p. De, 1923. Etudes de bionomie intercotidale. Les lies de Re et d'Yeu. Arch. Zool. Exper. Gen., 61:455-520. (327) Beebe, Wm., 1929. Deep sea fishes of Hudson Gore. Zoologica, 12:1-19. (318) 1930. A quarter mile down in the open sea. Bull. N. Y. Zool. Soc, 33:201-234. (321) 1932a. A halfmile in the bathysphere. Bull. N. Y. Zool. Soc, 35:143-180. (318, 321) 19326. The depth of the sea. Nat. Geog. Mag., 51:65-88. (318, 321) Beebe, Wm., and G. Hollister, 1930. The log of the bathysphere. Bull. N. Y. Zool. Soc. 33:249-264. (318) Behning, a., 1928. Das Leben der Volga. Die Binnengewasser, 5:1-162. (305) Beklemischev, W. N., 1927. Statistische Untersuchungen iiber die Zusammen- setzung von zwei Biocoenosen der Kamawiesen. Der Organismus und die Biocoenose (Zum Problem Individualitaten der Biocoenologie). Trav. Inst. Rech. Biol. Univ. Perm., 1:127-149. (13) 1931. tJber die Anwendung einiger Grundbegriffe der Bioconologie auf tierische Komponente der Festlandbioconosen. Bulletin of Plant Protection, 1 :277-358 (article in Russian with German summary; Journal with Russian and English title). {See 13) 1934. Die tiiglichen migrationen der Wirbellosen in einem Komplex von Fest- landbioconosen. Trav. Inst. Res. Biol. Perm., 6:120-208. (203) Beklemischev, W. N , A. Briukanova, and N. Shipitzina, 1931. Les premisses de I'epideraiologie et de la prophilaxie du paludisme a Magnitogorsk. Comis- sariat de la Sante Publique; Departement de la Sante Pubhque de Magnitogorsk. Edition du "Magnitostroi," Magnitogorsk (U. S. R.) (In Russian with French title page and summary), 1-49. (13) Belt, T., 1874. The naturalist in Nicaragua, Chapter VIII. London. (Recent edition of Everyman's Library.) {See 143) Bergtold, W. H., 1926. Avian gonads and migration. Condor, 28:114-120. (115, 212) Berry, E. W., 1922. A possible explanation of Upper Eocene cUmates. Proc. Am. Philos. Soc, 61:1-14. (211) 1930. The past climate of the North Polar Region. Smithson. Misc. Coll., 82:1-29. (211) Beveridge, Sir W. H., 1921. Weather and harvest cycles. Econ. Jour., 31:429- 452. (176) BiGELOW, H. B., 1924a. Plankton of the offshore waters of the Gulf of Maine. U. S. Bur. Fish. Bull., 40:1-509. (314, 319, 320) 19246. Physical oceanography of the Gulf of Maine. U. S. Bur. Fish. BuU., 40:511-1027. {See 314) 1930. A developing viewpoint in oceanography. Science, 71:84-89. (313) 1931. Oceanography. New York and Boston. (19) 362 BIBLIOGRAPHY Bird, R., 1927. A preliminary ecological survey of the district surrounding the entomological Station at Treesbank, Manitoba. Ecology, 8:207-220. (276) 1930. Biotic communities of the aspen parkland of central Canada. Ecology, 11:355-442. (12, 119, 246, 276) BiRGE, E. A., 1903. The thermocline and its biological significance. Tr. Am. Micro. Soc, 25:5-33. (97, 297) BiRGE, E. A., and Chancey Juday, 1911. The inland lakes of Wisconsin. The dissolved gases of the water and their biological significance. Wise. Geol. Nat. Hist. Surv. Bull., 22 (Sci. ser. 7):l-259. (97, 296) 1926. Organic content of lake water. U. S. Bur. Fish. Bull., 42:185-205. (297) 1934. Particulate and dissolved organic matter in inland lakes. Ecol. Mon., 4:440-474. (297) BissoNNETTE, T. H., 1930a. Studies on the sexual cycle in birds. I. Sexual maturity, its modification and possible control in the European starling {Sturnus vulg(iris): a general statement. Am. Jour. Anat., 45:289-305. (215) 19306. Studies on the sexual cycle in birds. III. The normal regressive changes in the testis of the European starling {Sturnus vulgaris) from May to November. Am. Jour. Anat., 46:477-492. (215) 1932. Light or exercise as factors in sexual periodicity in birds. Science, 76:253- 255. (See 215) 1933. Light and sexual cycles in starlings and ferrets. Quart. Rev. Biol., 8:201- 208. (215) 1936. Sexual photoperiodicity. Quart. Rev. Biol., 11:371-386. (5ee 215) 1937. Photoperiodicity in birds. Wilson Bull., 49:241-270. (211,215) BissoNNETTE, T. H., and M. H. Chapnich, 1930. Studies on the sexual cycle in birds. II. The normal progressive changes in the testis from November to May in the European starling (Sturnus vulgaris), an introduced, non-migratory bird. Am. Jour. Anat., 45:307-343. (-See 215) Blake, I. H., 1920. A comparison of the animal communities of coniferous and deciduous forest. 111. Biol. Mon., 10:371-520. (11, 245) 1931. Biotic succession on Ivatahdin. Appalachia, 18:409-424. (12) Blegvad, H., 1908. In First report on the oyster and oyster fisheries in the Lim Fjord by C. G. J. Petersen. Rept. Dan. Biol. Sta., 15:1-70. (337) 1914. Food and conditions of nourishment among the communities of inverte- brate animals found on or in the sea bottom in Danish waters. Rep. Dan. Biol. Sta., 22:41-78. (15, 119, 336, 350) 1916. On the food of fishes in the Danish waters within the Skaw. Rep. Dan. Biol. Sta., 24:17-72. (15, 47, 119, 334, 336, 343) 1922. On the biology of some Danish gammarids and mysids {Gammarus locusta, Mysis flexuosa, M. neglecia, M. inermis). Rep. Dan. Biol. Sta., 28:1-103. (341) 1923. Methoden der Untersuchung der Bodenfauna des Meerwassers. Handb. biol. Arbeitsmethoden. Teil 5, 9:311-330. (341) 1925. Continued studies on the quantity of fish-food in the sea bottom. Rep. Dan. Biol. Sta., 31:27-56. (15, 173, 182, 249, 298, 351) 1927. On the annual fluctuations in the age composition of the stock of plaice. Rep. Dan. Biol. Sta., 33:25-42. (341) 1929. Mortahty among animals of the httoral region in ice winters. Ibid., 35:50. (183) 1930. Quantitative investigations of bottom invertebrates in the Kattegat with special reference to the plaice food. Rep. Dan. Biol. Sta., 36:3-55. (340) BIBLIOGRAPHY 363 BoDENHEiMER, F. S., 1929a. A contribution to the study of the desert locust. Hadar, 2:3-12. (206) 19296. Studien zur Epidemiologie, Okologie und Physiologic der afrikanischen \\ anderheuschrecke. Zeit. angevv. Entom., 15:435-537. (206) 1930. Theoretical considerations on the evolution of control measures. Hadar, 3:3-14. (See 177-190) 1938. Problems of Animal Ecology (Chapter IV). London. (.See 172) BoRNER, L., 1922. Die Bodenfauna des St. Moritzer Sees. Arch. Hydrobiol., 13:1-91, 209-281. (312) BoRRADAiLE, L. A., 1923. The animal and its environment. London. (22) Bourne, G. C., 1910. Coral reefs. Ency. Brit., 11th Ed., 7:132-134. (25) BovARD, J. F., and H. L. Osterud, 1919. A partial Hst of animals yielding embryo- logical material at the Puget Sound Biological Station. Pub. Puget Sd. BioL Sta., 2:127-137. (316) Brandt, Karl, 1896. Das Vordringen mariner Thiere in den Kaiser Wilhelm- Canal. Zool. Jahrb. Abt. F. Syst. Geog. Biol. Thiere, 9:387-408. (330) Braun, E. Lucy, 1935. Undifferentiated deciduous forest climax and the associa- tion segregate. Ecology, 16:375-402. (329, 352) Brehm, a. E., 1896. From north pole to equator. Studies of wild life and scenes in many lands. Trans, by Margaret Thomson. Blackie: London. (Un- dated.) (132, 212, 253) Bright, K. M. F., 1938. The South African intertidal zone and its relation to ocean currents. Trans. Roy. Soc. of South Africa, 26:49-88. (See 10) Brimley, C. S., 1917. Thirty-two years of bird migration at Raleigh, North Caro- lina. Auk, 34:296-308. ^ (223) Broad, C. D., 1925. The mind and its place in nature. Inter. Lib. Psych., New York. (23) Brooks, A., 1926. Past and present big-game conditions in British Columbia and the predatory mammal question. Jour. Mam., 7:37-40. (183) Brooks, C. E. P., 1928. The influence of forests on rainfall and run-off. Quart. Jour. Roy. Met. Soc, 54:1-17. (93) Brooks, W. K., 1893. Salpa in its relations to the evolution of life. J. Hopkins Univ. Stud. Biol. Lab., 5:129-211. (125, 230, 298, 319, 321) Brotzky, V. A., 1931. Materials for the quantitative evaluation of the bottom fauna of the Storfjord (E. Spitzbergen). Ber. wiss. Meeresinst., 4:47-61. (334) Brown, Mary Jane, 1931. Comparative studies of the animal communities of oak-hickory forests in Missouri and Oklahoma. Biol. Survey, 3:231-261. Publ. Univ. Okla. {See 243-247) Bruce, J. R., 1928. Physical factors on the sandy beach. Part I. Tidal, climatic and edaphic. Part II. Chemical changes — Carbon dioxide concentration and sulphides. Jour. Mar. Biol. Assoc, 15:535-552 (Part II), 553-566. (323) ^ BRtJCKNER, 1891. Klimaschwankungen seit 1700. Vienna. (192) 1905. Die Bilanz des Kreislaufs des Wassers auf der Erde. Geog. Zeits., 11:436- 445. (93, 192) Brues, C. T., 1920. The selection of food-plants by insects, with special reference to lepidopterous larvae. Am. Nat., 54:313-332. (117, 130) 1924. The specificity of food-plants in the evolution of phytophagous insects. Am. Nat., 58:127-144. (117, 130) 1930. The food of insects viewed from the biological and human standpoint. Psyche, 37:1-14. (130) 364 BIBLIOGRAPHY BuMPtrs, H. C, 1890. The variations and mutations of the introduced sparrow {Passer domeslicus). Biol. Lect. (Woods Hole), 1896-7:1-15. (183) BuRTT, B. D., 1929. Fruits and seeds dispersed by mammals and birds of Tangan- yika Terr. Ecology, 17:351-355. (129) Cahn, a. R., 1925. Migration of animals. Am. Nat., 59:539-556. (212) 1929. The effect of carp on a small lake. The carp as a dominant. Ecology, 10:271-274. (159, 235, 299, 301) 1937. The turtles of Illinois. 111. Biol. Mon., 16:1-218. (266) Campbell, Mildred H., 1929. Free swimming copepods of the Vancouver Island region. I. Trans. Roy. See. Can. Biol. Ser., 323:303-332. (315) 1930. Ibid. II, 24:177-184. (315) Carpenter, J. R., 1935. Fluctuations in biotic communities. I. Prairie forest ecotone of central Illinois. Ecology, 16:203-212. (62, 200, 203) Carpenter, J. R., and J. Ford, 1936. The use of sweep net samples in an ecological survey. Jour. Soc. Brit. Ent., 1:155-161. (-See 355) Carpenter, K. E., 1927. Faunistic ecology of some Cardiganshire streams. Jour. EcoL, 15:33-54. (312) 1928. Life in inland waters. London. (312) Cary, M., 1917. Life zone investigations in Wyoming. U. S. Dept. Agr. N. Am. Fauna, 42:1-95. (253) Casamajor, J., 1927. Experiences sur les facteurs d'orientation chez les oiseaux. Rev. Franc. Orn., 11:259, 345. (227) Cathelin, F., 1920. Les migrations des oiseaux. Paris. (210, 226) Chaney, R. W., 1925. I. A comparative study of the Bridge Creek flora and the modern redwood forest. II. The Mascall flora — its distribution and climatic relation. Carnegie Inst. Wash. Pub., 349:23-48. (5, 211) Chaney, R. W., and E. Sanborn, 1933. I. The Goshen flora of west central Oregon. Carnegie Inst. Wash. Pub. 439. (5,211) Chapman, F. M., 1894. Remarks on the origin of bird migration. Auk, 11:12-17. (212) 1932. Handbook of birds of eastern North America. New York. Id., 3rd edition. (210) Chapman, R. N., 1931. Animal ecology with special reference to insects. New York. (166) 1932. Causes of the fluctuations of population of insects. Proc. Haw. Ent. Soc, 8:279-292. (166) (See 198) Child, C. M., 1924. Physiological foundations of behavior. New York. (22) Chrysler, M. A., 1930. The origin and development of vegetation of Sandy Hook. Bull. Torrey Bot. Club, 57:163-176. (129) Clark, G. L., 1933a. Diurnal migration of plankton in the Gulf of Maine and its correlation with change in submarine irradiation. Biol. Bull., 65:402-436. (320, 321) 19336. The role of copepods in the economy of the sea. Proc. Fifth Pac. Sci. Congr., 1933:2017-2021. (321) 1936. Light penetration in the western north Atlantic and its applications to biological problems. Rapp. Proc- Verb. Cons. Perm. Inter. Expl. Mer., 101:3-7. (321) Clarke, W. E., 1912. Studies in bird migration. 2 vols., 323 pp.; 346 pp. London. (210) BIBLIOGRAPHY 365 Clausen, R. G., 193G. The plant-animal community. Sci. Education, 20:73-75. (See 8-12) Clemens, W. A., and Lucy S. Clemens, 1926. Contribution to the life history of the sock-eye salmon. (No. 12) Rep. British Columbia Cora. Fish App., 1926 :29- 57. (188) Clemens, W. A., J. R. Dymond, N. K. Bigelow, F. B. Adamstone, and W. J. K. Harkness, 1923. Food of Lake Nipigon fishes. Pub. Ont. Fish. Res. Lab., 22:173-188. (306) Clements, F. E., 1897. The polyphyletic disposition of lichens. Am. Nat., 31 :277- 284. (138) 1901. The fundamental principles of vegetation. Am. Assoc. Adv. Sci., Fiftieth (Denver) Meeting, Proc. 50:332. (21, 145) 1904. Developments and structure of vegetation. Rep. Bot. Surv. Nebr., 7. (3, 17, 21, 68) 1905. Research methods in ecology. Lincoln, Nebr. (3, 7, 17, 21, 57, 91, 163) 1907. Plant physiology and ecology. New York. (31,130) 1910. The Ufe history of lodgepole burn forests. For. Serv. Bull. 79. (7, 126, 147) 1914. Plant succession. Year Book Carnegie Inst. Wash., 13:102-103. (5) 1916. Plant succession. Carnegie Inst. Wash. Pub., 242:1-512. (5, 7, 27, 68, 91, 103, 145, 147, 176, 191, 192, 211, 235, 238) 1917-1931. Annual reports. Year Book Carnegie Inst. Wash., 16-30. (See for summaries of researches, 1917-1931.) 1918. Scope and significance of paleo-ecology. BuU. Geol. Soc. Am., 29:369- 374. (5, 7) 1919. Grazing research. Year Book Carnegie Inst. Wash., 18:340. (122) 1920. Plant indicators. Carnegie Inst. Wash. Pub., 290. (48, 49, 120, 122, 192, 235, 238, 247, 292, 352) 1921a. Drouth periods and climatic cycles. Ecology, 2:181-188. (192, 199) 19216. Aeration and air-content. Carnegie Inst. Wash. Pub., 315. (90, 157) 1922. Principles and methods in bio-ecology. Year Book Carnegie Inst. Wash., 21:355. (1, 59, 65, 120) 1925. Evolution of the habitat. Year Book Carnegie Inst. Wash., 24:320. (26) 1926. Community functions. Year Book Carnegie Inst. Wash., 26:357. (See 20-67) (103) 1928. Plant succession and indicators. New York. (48, 49, 57, 68, 71, 122, 238) 1929. Climatic cycles and changes of vegetation. Rep. Confer. Cycles Carnegie Inst. Wash., 3-4, 64-71. (191, 192) 1931. Concept of the specient. Year Book Carnegie Inst. Wash., 30:268. (32) 1934. The relict method in dynamic ecology. Jour. EcoL, 22:39-68. (269) 1936. Nature and structure of the climax. Jour. EcoL, 24:252-284. (247, 269, 285) Clements, F. E., and R. W. Chaney, 1925-1935. Paleo-ecology. Year Books Carnegie Inst. Wash., 24-34. (5) 1936. Environment and life in the Great Plains. Carnegie Inst. Wash. Suppl. Pub., 24. (5, 192) Clements, F. E., and E. S. Clements, 1913. Rocky Mountain flowers. 3rd ed., 1928. New York. (42, 256) 1928. Flower families and ancestors. New York. (42, 143) Clements, F. E., and F. L. Long, 1923. Experimental pollination. Carnegie Inst. Wash. Pub., 336, (31, 40, 42, 143) 366 BIBLIOGRAPHY Clements, F. E., and V. E. Shelford, 1926-1934. Bio-ecology. Year Book Car- negie Inst. Wash., 25-33. (6) Clements, F. E., and J. E. Weaver, 1924. Experimental vegetation. Carnegie Inst. Wash. Pub., 355. (64, 163) Clements, F. E., J. E. Weaver, and H. C. Hanson, 1929. Plant competition. Carnegie Inst. Wash. Pub., 398. (22, 40, 163, 239) Cleve, P. T., 1897. Karaktaristik av Atlantiska Oceanens vatten pa grund av dess mikroorganismer. Overs. K. Vet. Forh., 54:95-102. (14) {See 317, 319) 1901. The seasonal distribution of Atlantic plankton-organisms. Goteborgs Vet. Samh. Handl. {See 317, 319) 1905a. On the plankton from the Swedish Coast-Stations Maseskar and Vilderobod etc. Sv. Hydr. Biol. Komm. Skr., 2:(l-5). {See 317, 319) 19056. Report on tho plankton of the Baltic current . . . at . . . Maseskar and Vaderobod, etc. Ibid., 2:(l-6). {See 317, 319) Cobb, John N., 1922. Pacific salmon fisheries. 3rd ed. Rep. U. S. Com. Fish. 1921 App., 1, 268 pp. (188) CoE, W. R., and W. E. Allen, 1937. Growth of sedentary marine organisms on experimental blocks and plates for nine successive years at the pier of the Scripps Institution of Oceanography. Bull. Scripps Inst, of Oceanography, Tech. Ser. 4:101-136. {See 239) CoKER, R. E., 1929a, h. Keokuk Dam and the fisheries of the upper Mississippi River. Bull. Bur. Fish., 45:87-139; Studies of the common fishes of the Mississippi River at Keokuk. Ibid., 141-225. (301) Cole, A. C, Jr., 1932. The ant: Pogonomyxmex occidentalis Cr., Associated with plant communities. Ohio Jour. Sci., 32:10-20. {See p. 83) Cole, A. E., 1932. Method for determining the dissolved oxygen content of the mud at the bottom of a pond. Ecology, 13:51-53. {See 312) Cole, L. J., 1933. The relation of light periodicity to the reproductive cycle, migra- tion and distribution of the mourning dove {Zenaidura macroura curolinensis) . Auk, 50:284-296. (211) Collett, R., 1895. Myodes lemmus, its habits and migrations in Norway. Vid- Selsk. Forh., 3. (177, 190, 200) 1911-1912. Norges Pattidyr. Christiana. (177, 190, 200) CoLTON, H. S., 1916. On some varieties of Thais lapillus in the Mount Desert sec- tion; a study of individual ecology. Proc. Acad. Nat. Sci. Phila., 68:440-454. (327) CoMTE, A., 1830. Cours de philosophic positive. Paris. (24) Cooke, W. W., 1885. Bird migration. U. S. Dept. Agr. Bull., 185. (210) 1910. The migratory movements of birds in relation to the weather. Yearbook U. S. Dept. Agr., 379-390. (210) 1913. The relation of bird migration to the weather. Auk, 30:205-221. (210, 219, 221, 225) Coward, T. A., 1912. The migrations of birds. Cambridge University Press. 1-137. (1929.) (210) Craig, W., 1908a. North Dakota life: plant, animal and human. Bull. Am. Geog. Soc, 40:321-332; 401-415. (253) 19086. The voices of pigeons regarded as a means of social control. Am. Jour. Soc, 14:86-100. (253) Criddle, N., 1930. Some natural factors governing the fluctuations of grouse in Manitoba. Can. Field-Nat., 44:77-80. (173, 196) BIBLIOGRAPHY 367 1932. The correlation of sunspot periodicity with grasshopper fluctuations in Manitoba. Can. Field-Nat., 46:195-198. (199) 1933. Studies in the biology of North American Acrididae; development and habits. Proc. World's Grain Exhibition and Conference, Canada, 474-494. (202-207) Dahl, F., 1903. Winke fiir ein wissenschaftlisches Sammeln von Thieren. Sitzb. Ges. Naturf. Fr. Berlin, 444-475. (fi, 7, 10) 1904. Kurze Anleitung, etc. 2 ed. Jena. (6, 7) 1908. Grundsiitze und Grundbegriffe der bioconotischen Forschung. Zool. Anzeig. 33:349-353. (7, 9) Darwin, C, 1876. The effects of cross and self fertiUzation in the vegetable king- dom. New York. (141) 1881. The formation of vegetable mould. New York. (71, 84) Davenport, C. B., 1903. The animal ecology of the Cold Spring sand pit, with remarks on the theory of adaptation. Decen. Pub. Univ. Chicago, 10:157-176. (313) Davidson, F. A., 1934. The homing instinct and age at maturity of pink salmon. U. S. Bur. Fish. Bull., 48:27-39. (188, 202) Davidson, F. A., and S. J. Hutchinson, 1938. The geographic distribution and environmental limitations of the Pacific salmon {Genus Oncorhynchus). Bull, of Bur. Fish., 48:667-692. {See 188, 202) Davis, F. AL, 1923. Quantitative studies on the fauna of the sea bottom. No. 1. Preliminary investigation of the Dogger Bank. Fish. Invest. Series II, 6:1-54. (247, 343) 1925. Quantitative studies on the fauna of the sea bottom. No. 2. Results of the investigations in the southern North Sea, 1921-24. Ministry of Agriculture and Fisheries. Fish. Invest. Series II, 8:1-50. (245) Dearborn, N., 1932. Foods of some predatory fur-bearing animals in Michigan. Univ. Mich., Schl. For. Cons. Bull., 1:1-52. (73) Deegener, P., 1917. Versuch zu einem System der Assoziations- und Sozietiits- formen im Tierreiche. Zool. Anzeig., 49:1-16. (149) 1918. Die Formen der Vergesellschaftung im Tierreiche. Ein systematisch- soziologischer Versuch. Leipzig. (148, 149) deforest, H., 1923. Rainfall interception by plants: an experimental note. Ecology, 4:417-419. (93) DeLury, R. E., 1923. Migration in relation to sunspots. Auk, 40:417. (222) 1925. Sunspots and the weather. Jour. Roy. Astron. Soc. Can., 293-298. (223) Dice, L. R., 1923. Mammal associations and habitats of the Flatheatl Lake region of Montana. Ecology, 4:247-260. (293) 1938. Some census methods for mammals. Jour. Wildlife Management, 2:119- 130. {See 357) Dill, N. R., and W. A. Bryant, 1911. Report of an expedition to Laysan Island. U. S. Biol. Surv. Bull., 42:1-30. (73) Dixon, C, 1895. The migration of British birds. (210) Doflein, F., 1914. Das Tier als Glied des Naturganzen. Teubner. Leipzig. (10) Douglass, A. E., 1909. Weather cycles in the growth of big trees. Mo. Weather Rev., 37:225-237. (176, 191) 1919. Climatic cycles and tree-growth. Carnegie Inst. Wash. Pub., 289. (192) 1928. Ibid., Vol. 2. (192) 368 BIBLIOGRAPHY 1936. Climatic cycles and tree growth. III. A study of cycles. Carnegie Inst. Wash. Pub., 289:3. (192) Drude, O., 1890. Handbuch der Pflanzengeographie. Stuttgart. (49) 1896. Deutschlands Pflanzengeographie. Stuttgart. (49) 1913. Die Oekologie der Pflanzen. Braunschweig. (49) DuBois, H. M., 1916. Variations induced in brachiopods by environmental condi- tions. PugetSd. Mar. Sta., 1:177-183. (54) Du RiETZ, G. E., 1931. Life-forms of terrestrial flowering plants. Act. Phytogeog. Suec, 3:1. (50) Eddy, Samuel, 1925a. The distribution of marine protozoa in the Friday Harbor waters (San Juan Channel, Washington Sound). Trans. Am. Micr. Soc, 44:97- 108. (18, 315) 1925&. Fresh water algal succession. Trans. Am. Micro. Soc, 44:138-147. (18) 1927. The plankton of Lake Michigan. Bull. 111. St. Nat. Hist. Surv., 17:203- 232. (18, 306, 307) 1928. Succession of protozoa in cultures under controlled conditions. Trans. Am. Micro. Soc, 47:283-319. (18, 240) 1932. The plankton of the Sangamon River in the summer of 1929. 111. St. Nat. Hist. Surv., Bull., 19(5):469-486. (18, 240) 1934. A study of fresh water plankton communities. III. Biol. Mon., 12:1-93. (240, 298, 299, 301, 303) Eggleton, F. E., 1931. A limnological study of the profundal bottom fauna of certain fresh-water lakes. Ecol. Mon., 1:231-331. (306) 1935. Deep water bottom fauna of Lake Michigan. Mich. Acad. Sci., Arts & Letters, 21:599-^12. (306) EiFRiG, C, 1924. Is photoperiodism a factor in the migration of birds? Auk, 41:439-444. (211) Ekman, S., 1911. Neue Apparate zur qualitativen und quantitativen Erforschung der Bodenfauna der Seen. Int. Rev. Hydrobiol., 3:553-561. (358) 1915. Die Bodenfauna des Vattern, qualitativ und quantitativ Untersucht. Int. Rev. Hydrobiol., 7:146-204. (358) Ellis, M. M., 1931. A survey of conditions affecting fisheries in the upper Missis- sippi River. U. S. Bur. Fish., Fishing Circ, 5:1-18. (300) Elton, C, 1924. Periodic fluctuations in the numbers of animals: their cause and effects. Jour. Exp. Biol., 2:119-163. (190, 192, 193, 196, 200) 1927. Animal ecology. London. (115,242) 1930. Animal ecology and evolution. Oxford. (173) 1931. The study of epidemic diseases among wild animals. Jour. Hyg., 31:435- 456. (190, 192, 193, 196, 200) 1932. Territory among wood ants. Jour. An. Ecol., 1 :69-82. (170) 1933. Abstract of papers and discussions. Matamek Conference on biological cycles. Matamek Factory, Canadian Labrador. (195) 1934. The Canadian snowshoe rabbit enquiry, 1932-33. Can. Field-Nat., 48:73-78; 47:63-69, 84-86. (194, 195) Elton, C, D. H. S. Davis, and G. M. Findlay, 1935. An epidemic among voles {Microtus agrestis) on the Scottish border in the spring of 1934. Jour. An. Ecol., 4:277-288. (185) Elton, C, and G. Swynnerton, 1935-1936. The Canadian snowshoe rabbit enquiry, 1932-33. Can. Field-Nat., 49:79-85; 50:71-81. (194, 195) BIBLIOGRAPHY 369 Enderlein, G., 1908. Biologisch-faunistische IMoor- und Diinenstudien. Danzig. (9, 10) Errington, p. L., 1930. Technique of raptor food habits study. Condor, 32:292- 296. (73) 1934. Vulnerability of bobwhite population to predation. Ecology, 15:110-127. (175) Errington, P. L., and F. N. Hamerstrom, 1936. The northern bobwhite's winter territory. la. Agr. E.xpt. Sta. Bull., 201. (168) Fabre, J. H., 1879. Souvenirs entomologiques. Prem. serie. XIX. (Retour au nid, etc.) Paris. (226) Farrow, E. P., 1925. On the ecology of the vegetation of Breckland. Jour. EcoL, 13:126-137. (119, 125) Faure, J. C, 1932. Phases of locusts in South Africa. Bull. Ent. Res., 23:293-428 (206) 1935. The life history of the red locust, Nomadacris septemfasciata (Serville). Union S. Afr. Dept. Agr. For. Bull., 144. (206) Felt, E. P., 1906. Insects affecting park and woodland trees. N. Y. St. Mus. Mem., 8 (2 vol.). (117) 1928. Dispersal of insects by air currents. N. Y. St. Mus. Bull., 274. (202) Ferriere, a., 1915. La loi du progres en biologie et en sociologie et la question de organisme social. Paris. (22) FiGuiER, L., 1868. The insect world (translated by Y. D.). New York. (203) FiLipjEV, I. N., 1928. Phenology and injurious insects. (In Russian, Izvest.) Ann. State Inst. Agron. Leningrad, 1927, 5:441-456. (198, 206) 1929a. The locust question in Soviet Russia. Inter. Cong. Entom., 11:803-812. (206) 19296. Life-zones in Russia and their injurious insects. Inter. Cong. Entom., 11:813-820. (206) FiNDLAY, G. M., and A. D. Middleton, 1934. Epidemic disease among voles (Microtus) with special reference to Toxoplasma. Jour. An. Ecol., 3:150-160. (185) Flattely, F. W., and C. L. Walton, 1922. The biology of the sea-shore. London. (327) FoLSOM, J. W., 1922. Entomology with reference to its biological and economic aspects. Philadelphia. (117) Forbes, S. A., 1878. Food of lUinois fishes. 111. St. Lab. Nat. Hist. Bull., 2:71-86. (301) 1880. On the food of young fishes. 111. St. Lab. Nat. Hist. Bull., 1 :71-85. (298) 1880a. Some interactions of organisms. 111. St. Lab. Nat. Hist. Bull., 1:3-18. (103, 107, 172) 18806. Notes on insectivorous Coleoptera. 111. St. Lab. Nat. Hist. Bull., 1:167- 176. (131, 135) 1883a. On the food of young fishes. The food of birds. Ibid., 71-161. (107, 165, 299) 18836. Food relations of the Carabidae and Coccinellidac. 111. St. Lab. Nat. HLst. Bull., 1:33-64. (131,135) 1883c. The food of the smaller fresh-water fishes. 111. St. Lab. Nat. Hist. Bull., 1 :65-94. (165, 299) 370 BIBLIOGRAPHY 1887. The lake as a microcosm. Bull. Peoria Acad. Sci., 3rd ed. 111. Nat. Hist. Surv. Bull., 15:537-550. (14, 22, 147) 1888. On the food relations of fresh-water fishes, a summary and discussion. 111. St. Lab. Nat. Hist. Bull., 2:475-538. (299) 1914. Fresh-water fishes and their ecology. 111. St. Lab. Nat. Hist. (Special publication). 19 pp., 10 pis. (55) Forbes, S. A., and R. E. Richardson, 1909. The fishes of Illinois. 111. Nat. Hist. Surv., 3:1-357. (302, 306) 1913. Studies on the biology of the upper lUinois River. III. St. Lab. Nat. Hist. Bull., 9:481-574. (299) 1919. Some recent changes in Illinois River Biology. 111. St. Nat. Hist. Surv. BuU., 13 (6):140-156. (299) Ford, E., 1923. Animal communities of the level sea-bottom in the waters adjacent to Plymouth. Jour. Mar. Biol. Assoc, 13:164-224. (332) FoREL, A., 1930. The social world of the ants compared with that of man. New York. (141, 144, 152) FoRMOsov, A. AL, 1928. Mammalia in the steppe biocenose. Ecology, 9:449-460. (71, 82) 1933. The crop of cedar nuts, invasions into Europe of the Siberian nutcracker {Nucifraga carijocatactes macrorhynchus Brehm) and fluctuations in numbers of the squirrel {Sciurus vulgaris L.). Jour. An. EcoL, 2:70-81. (196) FoRSLiNG, C. L., 1931. A study of the influence of herbaceous plant cover on sur- face run-off and soil erosion in relation to grazing on the Wasatch Plateau in Utah. U. S. Dept. Agr. Tech. Bull., 220. (71) France, R. H., 1913. Das Edaphon, Untersuchungen zur Oekologie der boden- bewonnenden Mikroorganismen. Deut. Mikrolog. Gesellsch. Arbeit, aus d. Biol. Inst. No. 2. Munich. (9, 22) Frankland, E., and H. E. Armstrong, 1874. Sixth report of the (English) com- missioners; pollution of rivers; domestic water supply. 6:501-508 {see also 261-262). (House of Commons Documents, 1874, Vol. 33.) (297) Fraser, C. McLean, and G. M. Smith, 1928a. Notes on the ecology of the little neck clam, Paphia staminea Conrad. Trans. Roy. Soc. Can., Ser. 3, 22:249- 270. (333) 19286. Notes on the ecology of the butter clam, Saxidomus giganteus Deshayes. Trans. Roy. Soc. Can., Ser. 3, 22:271-286. (333) Fuller, J. L., and G. L. Clarke, 1936. Further experiments on the feeding of Calanus finmarchicus. Biol. Bull., 70:308-320. (320) Gabrielson, I. N., 1924. Food habits of some winter bird visitants. U. S. Dept. Agr. Bull., 1249. (128) 1928. Habits and the behavior of the porcupine in Oregon. Jour. Mam., 9:33- 35. (170) Gajl, K., 1927. Hydrobiologischen Studien. I. Bioconosen des Sees Toporowy im polnischen Telle des Tatrabirges. Bull. Acad. Pol., 1926:881-954. (13) Gams, H., 1918. Prinzipienfragen der Vegetationsforschung. Zurich. (10, 50) 1921. Uebersicht der organogenen Sedimente nach biologischen Gesichtspunkten. Naturw. Wochenschr., 20:569-576. (96) Garner, W. W., and H. A. Allard, 1920. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. Jour, of Agri. Res., 18:553-606. (212) BIBLIOGRAPHY 371 Gatke, H., 1900. Heligoland as an ornithological observatory. (German editions, 1890, 1900; English edition, 1895.) (210, 212) Gause, G. F., 1934. Struggle for existence. Baltimore. (112) Gersbacher, W. I\I., 1937. The development of stream bottom communities in central Illinois. Ecology, 18:359-390. (18, 235, 299, 304, 305, 311) Gilbert, C. H., 1914a. Age at maturity of the Pacific Coast salmon of the genus Oncorhynchus. Bull. U. S. Bur. Fish., 1912, 32:1-22. 27 pis. (188) 1914?). Contributions to the life-history of the sock-eye salmon. Rep. British Columbia Com. Fish. 1913, App. 53-78. (188) Gilbert, C. H., and W. H. Rich., 1927. Investigations concerning the red-salmon runs to the Karluk River in Alaska. Bull. U. S. Bur. Fish., Pt. 2, 43:1-69. (188) Gislen, T., 1930. Epibioses of the GuUmar Fjord : I. A study in marine Sociology. Kristinebergs Zool. Sta., 1877-1927. 1-380. (18, 50, 326) Glenn, P. A., 1915. The San Jose Scale, Rep. Sta. Entom. lU., 28:87-106. (47) Glinka, K. D., 1927. The great soil groups of the world and their development. Trans, from the German edition (1914) by Marbut. (22) Goldsmith, G. W., 1922-23. Soil fauna. Yearbook Carnegie Inst. Wash., 21:347; 22:314. {See 72) Goldsmith, G. W., and L. Bonar, 1924. Distribution and behavior of soil algae. Ibid., 23:261. {See 12) Goldsmith, G. W., and A. L. Hafenrichter, 1932. Anthokinetics. The physiol- ogy and ecology of floral movements. Carnegie Inst. Wash. Publ., 420. (40) Graham, S. A., 1929«. The need for standardized quantitative methods in forest biology. Ecology, 10:245-250. (356) 19296. Larch sawfly as an indicator of mouse abundance. Jour. Mam., 10:189- 196. (187) Gran, H. H., 1912. Pelagic plant life. Chapter 6, Murray and Hjort. (15, 314, 319) 1931. On the conditions for the production of plankton in the sea. Cong. Perm. Inter. Explor. Ner. Rapp. Proc.-verb., 75:1-37-46. (314) Gran, H. H., and T. G. Thompson, 1930. The diatoms and the physical and chem- ical conditions of the sea water of the San Juan Archipelago. Pub. Puget Sd. Biol. Sta., 7:169-204. (315) Gray, H. E., and A. E. Treloar, 1935. On the enumeration of insect population by the method of net collections. Ecology, 14:356-367. (355) Green, R. G., 1932. The periodic disappearance of game. Outdoor America, 10:16-17. (184, 187) Greene, R. A., and G. H. Murphy, 1932. The influence of two burrowing rodents, Dipodomys spectabilis spectabilis (kangaroo rat) and Neotoma albigula albigula (pack rat), on desert soils in Arizona. Ecology, 13:358-363. (82) Greene, R. A., and C. R. Reynard, 1932. The influence of two burrowing rodents, Dipodomys spectabilis spectabilis (kangaroo rat) and Neotoma albigula albigula (pack rat), on desert soils in Arizona. Ecology, 13:73-80. (11, 71, 73, 82) Grinnell, J., 1923. Burrowing rodents of California as agents in soil formation. Smithsonian Report, 1923:339-350; Jour. Mam., 4:137-149. (82, 88) Grinnell, J., 1928. Presence and absence of animals. (242) Univ. of Cal. Chron. 30:429^50. 1931. Some angles in the problem of bird migration. Auk, 48:22-32. (208, 210, 226, 227, 242) 372 BIBLIOGRAPHY 1933. Native California rodents in relation to water supply. Jour. Mam., 14:293-298. (88, 290) Grinnell, J., and J. Dixon, 1918. Natural history of the ground squirrels of Cali- fornia. St. Com. Hort. Bull., 7:597-708. (290) Griscom, L. I., 1923. Birds of the New York City region. New York. (129) Groebbels, F., 1928. Zur Physiologic des Vogelzuges. Verh. Ornith. Ges. Bayern, 18:44-74. (See 211) 1931. Der Komplex der Nahrungsinnerwelt des Vogels und seine biologische Bedeutung. Ornith. Cong. Amsterdam, 119-135. (214) Gross, A. 0., 1927. The snowy owl migration of 1926-27. Auk, 44:479. (See 208-12) 1931. The snowy owl migration of 1930-31. Auk, 48:501. (See 208-12) Guthrie, J. E., 1926. The snakes of Iowa. la. Agr. Exp. Sta. Bull., 239:146-192. (265) Hachet-Souplet, p., 1903. Le probleme psychologique du pigeon voyageur. Ann. Psychol. Zool., 3:33-51. (227) Hall, A. D., 1905. The book of Rothamsted experiments. Rothamsted Experi- ment Station, Harpenden. (89) 1908. The soil. 2nd ed., London. (86) Hall, H. M., 1929. European reservations for the protection of natural conditions. Jour. For., 27:667-684. (357) Hall, H. M., and F. E. Clements, 1923. The phylogenetic method in taxonomy. Carnegie Inst. Wash. Pub., 326. (256) Hamilton, A. G., 1936. The relation of humidity and temperature to the develop- ment of three species of African locusts — Locusta migratoria migratorioides (R. & F.), Schistocerca gregaria (Forsk.), Nomadacris septemfasdata (Serv.) Trans. Roy. Entom. Soc. London, 85:1-60. (^^ee 202-207) Hammond, J., 1921. Further observations on the factors controlling fertility and foetal atrophy. Jour. Agr. Sci., 11:337-366. (182) Hancock, J. L., 1911. Nature sketches in temperate America. Chicago. (275) Hankinson, T. L., 1915. The vertebrate life of certain prairie and forest regions. BuU. 111. N. H. Surv., 11:280-303. (274) Hanson, H. C, and L. D. Love, 1931. Effects of different systems of grazing by cattle upon a western wheat-grass type of range. Col. Agr. Exp. Sta. Bull., 377. (See 270) Harshberger, J. W., 1911. The soil a living thing. Science, 33:741-744. (22) Harvey, H. W., 1927. The chemistry and physics of sea water. Cambridge. (314) Hatt, R. T., 1929. The red squirrel. Bull. N. Y. Sta. Col. For. Roosevelt Wild Life Annals, 2:1-146. (123, 170) Haviland, M. D., 1926. Forest, steppe and tundra. University Press: Cam- bridge. (See 11-13) Hayes, W. P., 1927. Prairie insects. Ecology, 8:238-250. (260) Headlee, T. J., 1913. The chinch-bug. Kan. St. Agr. Exp. Sta. Bull., 191. (184) Heape, W., 1931. Emigration, migration and nomadism. Cambridge. (170, 190, 200, 201, 202, 210, 211, 212, 214, 217) Hebard, M., 1925. Orthoptera of South Dakota. Proc. Ac. Nat. Sci. Phila., 77:33-155. (254) 1928. Orthoptera of Montana. Ibid., 80:211-306. (254) 1929. Orthoptera of Colorado. Ibid., 81 :303-425. (254) BIBLIOGRAPHY 373 1930. Orthoptera of Alberta. Ibid., 82:377-403. (254) 1931. Orthoptera of Kansas. Ibid., 83:119-227. (254, 260) 1934. Dermaptera and orthoptera of Ilhnois. Bull. 111. N. H. Surv., 20:125-279. (275) Hedley, Charles, 1915. An ecological sketch of the Sydney beaches. Presi- dential address, 1915: Jour. & Proc. Roy. Soc. N. S. Wales, 49; 1:15-77. (16) Henderson, L. J., 1917. The order of nature. Harvard. (23) Hendrickson, G. 0., 1930. Studies on the insect fauna of Iowa prairies. la. Sta. Col. Jour. Sci., 4:49-179. (274, 275) Henry, A., 1897. The manuscript journals of Alexander Henry and David Thomp- son. Edited by EUiott Eves, New York. (274) Henshaw, H. W., 1910. Migration of the Pacific plover to and from the Hawaiian Islands. Auk, 27:246-262. (210) 1921. The book of birds. Nat. Geog. Soc. Washington. (134, 210) Herdman, W. a., 1906. The problems of the sea. Trans. Liverpool Biol. Soc, 21:1-23. (313) Hesse, R., 1912. Oekologie der Tiere. Biologie. Fischer: Jena. (10) Hewatt, W. G., 1935. Ecological succession in the Mytilus californianus habitat as observed in Monterey Bay, Calif. Ecology, 16:244-251. (18, 240, 329, 353) 1937. Ecological studies on selected marine intertidal communities of Monterey Bay, Calif. Am. Midland Nat., 18:161-206. (326, 329) Hewitt, C. G., 1921. The conservation of wild life. New York. (193) Hicks, L. E., 1932. The snowy-owl invasion of Ohio in 1930-31. Wilson Bull., 44:221. (^ee 208-212) HiLPRECHT, A., 1935. Heimfindeversuche mit Wintervogeln. Vogelzug, 6:188. (227) Hjort, J., and J. T. Rund, 1929. Whaling and fishing in the North Atlantic. Cons. Perm. Inter. Rapp. et Proces-verb. R., 56:5-123. (320) Holmes, S. J., 1911. Evolution of animal intelUgence. New York. (33, 117) Hopkins, S. H., 1934. The papillose Alloceadiidae. 111. Biol. Mon., 13:51-123. (301) HoTTES, C. F., and T. H. Frison, 1931. The plant Hce or Aphididae of Illinois. 111. Nat. Hist. Surv. Bull., 19:123-447. (117) Houssay, F., 1893. Industries of animals. New York. (132) Howard, H. E., 1907, 1914. The British warblers; a history with problems of their Uves. 2 vols., 1, 1907; 2, 1914. (167) 1920. Territory in bird hfe. London. (167, 168, 170) Howe, A., 1932. The geologic importance of lime-secreting algae. U. S. Geol. Surv. Prof. Pap., 170:57-64. (25) Howell, A. H., 1921. Biological survey of Alabama. N. A. Fauna, 45:1-88. (253) Hudson, W. H., 1892. The naturahst in La Plata. London. (80, 132, 253) Humphrey, R. C, and R. W. Macy, 1930. Observations on some of the prol)able factors controlling the size of certain tide pool snails. Pub. Puget Sound. Biol. Sta., 7:205-208. (55) Humphreys, W. J., 1920. Physics of the air. Philadelphia. (296) Hunt, O. D., 1925. The food of the bottom fauna of the Plymouth fishing grounds. Jour. Mar. Biol. Assoc, 13:560-599. (332) Huntsman, A. G., 1918. The vertical distribution of certain intertidal animals. Trans. Roy. Soc. Can., Ser. 3, 12:53-60. (332) 1920. Climates of our Atlantic waters. Proc Am. Fish. Soc, 50:326-333. (229, 294, 323) 374 BIBLIOGRAPHY 1924. Limiting factors for marine animals (1, 2, 3). Cont. Can. Biol., 2:83-88, 91-94, 97-114 (No. 3 with M. D. Sparks). (330) Huntington, E., 1914. The cUmatic factor as illustrated in arid America. Car- negie Inst. Wash. Pub., 192. (192) 1925. Tree growth and climatic interpretations. Ibid., 352:157-212. (192,195) 1932. The Matamek conference on biological cycles. Science, 74:229-235. Report. Matamek Factory, Canadian Labrador. {See 195) Hutchinson, A. H., 1928. A biohydrographical investigation of the sea adjacent to the Fraser River mouth. Paper II. Factors affecting the distribution of phyto-plankton. Trans. Roy. Soc. Can., Ser. 3, 22:293-309. (322) Hutchinson, A. H., C. C. Lucas, and M. McPhail, 1929. Seasonal variations in the chemical and physical properties of the waters of the Strait of Georgia in relation to phyto-plankton. Trans. Roy. Soc. Can., Ser. 3, 23:177-183. (322) Idelson, M. S., 1931. Preliminary quantitative evaluation of the bottom fauna of the Spitzbergen Bank. Ber. wiss. Meeresinst., 4 (3) :27-46. (334) IsELiN, C. O.'D., 1938. Problems in the oceanography of the North Atlantic. Nature, 141:772-780. (See 206) Lean, O. B., 1931. The recent swarming of Locusta migratoroides. R. & F. Bull. Entom. Res., 22:365-378. (206) Leathers, A. L., 1923. Ecological study of aquatic midges and some related insects with special reference to feeding habits. U. S. Bur. Fish. Bull., 38:1-62. (300) Lebour, M. v., 1919a. Feeding habits of some young fish. Jour. Mar. Biol. Assoc, 12 (N. S.):9-21. (298, 316) 19196. The food of post-larval fish. II. Jour. Mar. Biol. Assoc, 12:22-47 (298, 316) 1920. The food of young fish. III. Jour. Mar. Biol. Assoc, 12:261-324. (298, 316) 1921. The food of young clupeoids. Jour. Mar. Biol. Assoc, 12:458-467. (298, 316) 1922. The food of plankton organisms. Jour. Mar. Biol. Assoc, 12:644-677. (316) 1923a. The food of plankton organisms. II. Jour. Mar. Biol. Assoc, 13:70-92. (316) 19236. The food of young herring. Jour. Mar. Biol. Assoc, 13:325-330. (298, 316) Leopold, A., 1931. Report on a game survey of the north central states. Madison, Wis. (180, 196) 1933. Game management. New York. (105, 111, 185, 242) 1934. The game cycle: a challenge to science. Outdoor America, 9:4, 14. (180) Leopold, A., and J. N. Ball, 1931. British and American grouse cycles. Can. Field-Nat., 45:162-167. (196) Lincoln, F. C, 1924. Returns from banded birds, 1920 to 1923. U. S. Dept. Agr. Bull., 1268:1-56. (211) 1927. Returns from banded birds, 1923 to 1926. U. S. Dept. Agr. Tech. Bull., 32:1-95. (211, 226) 1933. Bird banding. Fifty years' prog. Am. Ornith., 1883-1933, 65-87. (209) 1935. The migration of North American birds. U. S. Dept. Agr. Circ, 363:1-72. (200, 207, 208, 209, 210) LoEB, J., 1906. Dynamics of Hving matter. New York. (54) Lomas, J., 1905. The work of organisms in the making and unmaking of rocks. Tr. Liverpool. Biol. Soc, 20:1-14. 1905-06. (73) LowDERMiLK, W. C., 1926. Forest destruction and slope denudation in the province of Shansi, China. China Jour., 4:127-135. (71) 1930. Influence of forest litter on run-off, percolation, and erosion. Jour. For., 28:474-491. (71) 1931. Studies of the role of forest vegetation in surficial run-off and soil erosion. Agr. Eng., 12:107-112. (71) 1934. The role of vegetation in erosion control and water conservation. Jour. For., 32:529-536. (71) Lubbock, J., 1882. Ants, bees, and wasps. London. (154) LucANUS, F. VON, 1922. Die Ratsel des Vogelzuges. (208, 210, 226) BIBLIOGRAPHY 377 LuNDBECK, J., 1926. Die Bodentierwelt norddeutscher Seen. Arch. Hydrobiol. Suppl. Bd., 7:1-473. (178, 30G, 311) LuNDQUisT, G., 1927. Bodenblagerungen und Entwicklungstypen der Seen. Thienemann's, Die Binnengewiisser, vol. II. (73) Lydekker, R., and others. Undated. New natural history. New York. (119) MacLulich, D. a., 1936. Sunspots and abundance of animals., Jour. Royal Astron. Soc. of Canada, 1936:233-246. (223) 1937. Fluctuations in the numbers of the varying hare {Lepus americanus). Biol. Series No. 43, Univ. of Toronto Press. (184, 195) Margery, I. D., 1926. The INlarsham phenological record in Norfolk, 1736-1925, and some others. Quart. Jour. Roy. Meteor. Soc, 52:27-54. (217, 225) Manniche, a. L. v., 1910. The terrestrial mammals and birds of north-east Greenland. Medd. Gronl., 45:1-199. (190) Marcovitch, S., 1924. The migration of the Aphididae and the appearance of the sexual forms as affected by the relative length of daily Ught exposures. Jour. of Agri. Res., 27:513-522. (212) Marloth, R., 1903-05. Results of experiments on Table Mountain for ascertaining the amount of moisture deposited from the southeast clouds. Trans. S. Afr. PhUos. Soc, 14:403-408, 16:97-105. (93) Marshall, F. H. A., 1910. The physiology of reproduction. (Revised, 1922.) London. (212, 215) Masui, K., 1927. A study of the ectotrophic mycorrhizas of woody plants. Mem. CoU. Sci. Kyoto Univ. B, 3:149-279. (140) Mayer, A. G., 1908. The annual breeding swarm of the Atlantic palolo. Papers Tortugas Lab. of the Carnegie Inst., 1 :105-112. (47) Mayr, E., and W. Muse, 1930. Theoretische zur Geschichte des Vogelzuges. Der Vogelzuges, 1:149-172. (5ee 211) McAtee, W. L., 1907. Census of four sq. ft. Science, N. S., 26:447-449. (73) 1911. Woodpeckers in relation to trees and wood products. U. S. Dept. Agr. Biol. Surv. Bull., 39. (129, 135) 1936. The Malthusian principle in nature. Sci. M on., 42:444-456. (176) McDouQALL, W. B., 1914. On the mycorrhizas of forest trees. Am. Jour. Bot., 1:51-74. (140) 1922. Symbiosis in a deciduous forest. Bot. Gaz., 73:200-212; 79:95-102. (140) McLean, A., 1935. Early stages of succession from marine conditions to land. Ecol. Mon., 5:319-324. (In Shelford et al.). (30) McLuckie, J., 1923a. A contribution to the morphology and physiology of the root-nodules of Podocarpus spinulosa and P. elata. Proc. Linn. Soc. N. S. W., 48:82-93. (139) 19236. The root-nodules of Casuarina cunninghamiana and their physiological significance. Proc. Linn. Soc. N. S. W., 48:194-205. (139) MacFarlane, R., 1905. Notes on mammals collected and observed in the northern Mackenzie River district, Northwest Territories of Canada, with remarks on explorers and explorations of the Far North. Proc. U. S. Nat. Mus., 28:673- 764. (193) Mearns, E. a., 1907. Mammals of the Mexican boundary of the United States. U. S. N. Mus. BuU., 56:1-530. (126) Meek, A., 1916. The migration of fish. London. (201) 378 BIBLIOGRAPHY Mblin, E., 1925. Untersuchungen iiber die Bedeutung der Baummykorrhiza. Fischer Jena. (140) Merriam, C. H., 1890. Result of a biological survey of the San Francisco Mountain region and the desert of the Little Colorado, Arizona. U. S. Dept. Agr., N. A. Fauna, 3. (242) 1898. Life zones and crop zones of the United States. U. S. Dept. Agr., Div. Biol. Surv., Bull. 10. (See 242) 1901. Prairie dogs of the Great Plains. Yearbook U. S. Dept. Agr., 1901:257- 270. (81, 172) Merriam, C. H., and L. Stejneger, 1890. Results of a biological reconnaissance of south-central Idaho. U. S. Dept. Agr., N. A. Fauna, 5:1-113. (46, 293) Merriam, J. C., 1899. Report on the expedition to the John Day fossil fields. Univ. of Cal. Chron., 2:217-225. (292) Metcalf, Z. p., 1924. The beach-pool leafhopper complex. Ecology, 5:171-174. (117) Michener, H., and J. R. Michener, 1935. Mocking birds: their territories and \-, individualities. Condor, 37:97-140. (167) Middleton, a. D., 1930. Cycles in the numbers of British voles (Microtus). Jour. EcoL, 18:156-165. (195) 1934. Periodic fluctuation in British game population. Jour. Am. EcoL, 3:231- 249. (196, 197) MiDDLETON, R. G., 1929. Fall migration at Jeffersonville, Penn., 1916-1928 Incl. Cassinia, 27:13. (-See 209-210) MiKESELL, T., 1883. 1873-1912. Phenological dates and meteorological data. Mon. Weath. Rev. Sup., 2:23-93. (221) Miller, A. H., 1931. Notes on the song and territorial habitats of Bullock's oriole. Wilson Bull., 43:102-108. (167) Mobius, K., 1877. Die Auster und die Austernwirtschaft. Berlin. (5, 6, 7, 336) 1883. The oyster and oyster culture. Pre. U. S. Com. Fish., 8:721-729. (336) Moffett, J. W., 1936. A quantitative study of the bottom fauna in some Utah streams variously affected by erosion. Bull. Univ. of Utah 26, Biol. Series, 3:3-33. (307) MoLANDER, A. R., 1930. Animal communities on soft bottom areas in Gullmar fjord. Kristineberg's Zool. Sta., 1877-1927. No. 2:1-90. (18) MoLLER, 1922. Der Dauerwaldgedenke. Sein Sinn und seine Bedeutung. Berlin. (22) Moon, H. P., 1935. Methods and apparatus suitable for an investigation of the littoral region of oligotrophic lakes. Inter. Rev. Ges. Hydrobiol., 32:319-333. (358) Moore, H. B., 1931a. Muds of the Clyde Sea area. III. Chemical and physical conditions; rate and nature of sedimentation; and fauna. Jour. Mar. Biol. Assoc, 17:325-348. (102, 351) 19316. The specific identification of fecal pellets. Ibid., 359-366. (102, 351) Moore, H. E., 1908. Practical methods of sponge culture. Bull. U. S. Bur. Fish., 28:547-583. (52, 54) Moreau, R. E., 1936. Bird-insect nesting association. Ibis, 6:460-471. (144) Morgan, C. L., 1926. Emergent evolution. New York. (23) MoROzov, G., 1912. The knowledge of forest. (22) MoRTENSEN, H. C. C, 1906. Ringfugle. Dansk ornithologisk forenings tidsskrift. Hargangl. Heft 4:144-155. (211) BIBLIOGRAPHY 379 Mossop, B. K. E., 1922. The rate of growth of the sea mussel (Mytilus edulis L.) at St. Andrews, New Brunswick; Digby, Nova Scotia, and in Hudson Bay. Trans. Roy. Can. Inst., 14:3-22. (330) MuRiE, O. J., and A. Murie, 1930. Travels of Peromyscus. Jour. Mam., 12:200- 209. (170) Murray, L., and J. Hjort, 1912. Depths of the ocean. London. (15, 29, 102, 296, 297, 314, 317, 318, 319, 320) Murray, J., and A. J. Renard, 1891. Deep sea deposits. H. M. S. Challenger Rept. Edinburgh. (102) MuTTKOwsKi, R. A., 1918. The fauna of Lake Mendota; a qualitative and quan- titative survey with special reference to the insects. Trans. Wis. Acad. Sci., 19:374-482. (306) Myers, J. G., 1929. The nesting-together of birds, wasps, and ants. Proc. Ent. Soc, London, 4:80-88. (144) 1935. Nesting associations of birds with social insects. Trans. Ent. Soc. London, 83:11-12. (144) Napier, G. P., 1914. Report on the obstructed condition of the Eraser River. Rep. British Columbia Com. Fish. App., 1913:39-42. (187) Naumann, E., 1918. liber die natiirliche Nilhrung des limnischen Zooplanktons. Ein Beitrag zur Kenntnis des Stoffhaushalt im Siisswasser. Lunds Univ. Arssk., neue Folge, Avd. 2, Bd. 14, Nr. 31, pp. 1-48. (17) 1921. Spezielle Untersuchungen liber die Ernahrungsbiologie des tierischen Limnoplanktons. I. tjber die Technik des Nahrungserwerbs bei den Clado- ceren und ihre Bedeutung fur die Biologie der Gewassertypen. Lunds Univ. Arsk. n. f. Avd. 2, Bd. 17, Nr. 4:3-27. (17) 1922. Die Bodenablagerungen des Susswassers. Arch. Hydrobiol., 13:97-165. (73) 1923. Spezielle Untersuchungen liber die Ernahrungsbiologie des tierischen Limnoplanktons. II. tJber den Nahrungserwerb und die natiirliche Nahrung der Copepoden und der Rotiferen des Limnoplanktons. Lunds Univ. Arsk. n. f. Avd. 2, Bd. 19, Nr. 6:3-17. (17) 1925a. See under Teich (Tiefe). Abderhalden's Handb. Biol. Arbeitsmethoden. Abt. 9, Teil 2, H., 1:103-138. (17) 19256. See under Teich (Plankton und Neuston). Abderhalden's Handb. Biol. Arbeitsmethoden. Abt. 9, Teil 2, H., 1:139-228. (17) 1925c. Die Arbeitsmethoden der regionalen Limnologie. Abderha^lden's Handb. Biol. Arbeitsmethoden. Abt. 9, Teil 2, H., 1:544-555. (17) 1925d. Einige Hauptprobleme der modernen Limnologie. Abderhalden's Handb. Biol. Arbeitsmethoden. Abt. 9, Teil 2, H., 1:556-588. (17) 1925e. Methoden der experimentellen Aquarienkunde. Abderhalden's Handb. Biol. Arbeitsmethoden. Abt. 9, Teil 2, H., 1:622-652. (17) 1929. Die Bodenablagerungen der Seen. Verh. Intern. Ver. Limnologie, 4:32- 106. (17, 96) 1931. Limnologische Terminologie. Berlin. (17, 312) 1932. Grundziige der regionalen Limnologie. Die Binnegewiisser. Stuttgart. 11:1-176. (16, 17) Needham, J. G., 1901. Aquatic insects of the Adirondacks. N. Y. Sta. ]Mus. Bull., 47. (309) 380 BIBLIOGRAPHY Needham, J. G., and R. 0. Christensen, 1927. Economic insects in some streams of northern Utah. Utah Agr. Exp. Sta. Bull., 201:1-36. (309, 358) Needham, J. G., and J. T. Lloyd, 1916. Life in inland waters. Ithaca, N. Y. (312) Neger, F. N., 1913. Biologic der Pflanzen auf experimenteller Grundlage. Stutt- gart. (139) Newcombe, C. L., 1935a. A study of the community relationship of the sea mussel, Mytilus edulis L. Ecology, 16:234-243. (327, 330, 336) 19356. Certain environmental factors of a sand beach in the St. Andrews region, N. B., with a preliminary designation of the intertidal communities. Jour. Ecol., 23:334-355, 327) Newton, A., 1874. The migration of birds. Nature, 10:415. (211) Nice, M. M., 1931. Survival and reproduction in a song sparrow population during one season. Wilson Bull., 43:91-102. (169) 1933. The theory of territorialism and its development. In fifty years' prog. Am. ornith., 1883-1933. Am. Ornith. Union: Lancaster, Pennsylvania. (167, 168, 170) 1937. Studies in the life history of the song sparrow. I. A population study of the song sparrow. Trans. Linn. Soc. N. Y., 14:1-247. (See 174, 210, 196) Nicholson, A. J., 1933. The balance of animal populations. Jour. An. Ecol., 2:132-178. (174) Nicholson, E. M., 1929. How birds hve. London. (208, 226) Norton, J. B. S., 1930. The grasses of Maryland. Univ. of Maryland. Agr. Expt. Sta., Bull., 323. {See 260) Oliver, W. R. B., 1915. The moUusca of the Kermadec islands. Trans. Proc. N. Z. Inst. 1914, news issue, 47:509-568. (16) 1923. Marine littoral plant and animal communities in New Zealand. Trans. Proc. N. Z. Inst., news issue, 54:496-545. (16, 313) Olson, S., 1930. The poison trail. Sports Afield, 1930:10-40. (115, 132) 1938a. Organization of the range pack. Ecology, 19:168-170. (115, 132, 200) 19386. A study of the predatory relation with particular relation of the wolf. Sci. Mon., 46:323-336. (115) Oltmanns, F., 1923. IMorphologie und Biologic der Algen. 2nd ed.. Vol. 3. Jena. (138, 141) O'Malley, H., and W. H. Rich, 1920. Migration of adult sockeye salmon in Puget Sound and Eraser River. Bull. U. S. Bur. Fish. App. 8, 1920:1-38. (202) OsBXJRN, R. C., L. I. Dublin, H. W. Shimer, and R. S. Lull, 1903. Adaptation to aquatic, arboreal, fossorial and cursorial, habit in mammals. Am. Nat., 37:651- 665; 731-736; 819-825; 38:1-11 (Jan. 1904). Four separate parts under the same general title. (55) OsTENFELD, C. H., 1908. On the ecology and distribution of the grass wrack (Zostera marina) in Danish waters. Rep. Dan. Biol. Sta., 16:1-62. (336) OsTER, R. H., and G. L. Clarke, 1934. The penetration of the red, green, and violet components of daylight into Atlantic waters. Woods Hole Oc. Inst, and Biol. Lab., Harvard Univ., 25:84-91. (296) Packard, A. S., 1880. Summary of locust flights from 1877-1879. 2nd Rep. U. S. Entom., Com. Ch. 7:160-163. (204, 205) Packard, A. S., and C. Thomas, 1878. Migrations. 1st Rep. U. S. Entom. Com. Ch. 7:143-211. (204) BIBLIOGRAPHY 381 Packard, A. S., and C. V. Riley, 1877. Chronology History (of locust ravages). 1st Rep. Entom. Com. Ch. 2:53-114. (A^ee 198) Palmer, T. S., 1897. The jackrabbits of the United States. U. S. Dept. Agr. Bull., 8:11-88. (290) Palmgren, p., 1928. Zur Synthase pflanzen- und tierokologischer Untersuchungen. Acta Zool. Fenn., 6:1-51. (511) 1930. Quantitative Untersuchungen iiber die Vogelfauna in den Wiildern Siid- finnlands. Acta Zool. Fenn., 7:1-218. (11) Park, Orlando, 1931. Studies in the ecology of Coleoptera. II. Ecology, 12:188- 207. (242) 1935. Studies in nocturnal ecology. III. Recording apparatus and further analysis of activity rhythm. Ecology, 16:152-163. (242) 1937. Studies in nocturnal ecology. Further analysis of activity in the beetle, Passalus cornutus, and description of audio-frequency recording apparatus. Jour. An. EcoL, 6:239-253. (242) Parker, J. R., 1930. Some effects of temperature and moisture upon the Melanoplus mexicanus, Saussure, and Camnula pellucida, Scudder. Mont. Agr. Exp. Sta. Bull., 223:1-132. (182, 198, 199, 203) Passarge, S., 1904. Die Kalahari. Versuch iiber Physisch-geographischen Darstellung der Sixd-Afrikauschen Beckens. (Chapter XVI.) Berlin. (71) Pearl, R., 1925. Biology of population growth. New York. (185) Pearsall, W. H., 1922. A suggestion as to the factors influencing the distribution of free-floating vegetation. Jour. EcoL, 9:241-253; 1922:248. (97) Pearse, a. S., 1913. Observation on the fauna of the rock beaches at Nahant, Mass. Bull. Wis. N. H. Soc, 11:8-34. (327) 1939. Animal Ecology. Chapter 14. New York. (See 68-102) Pearson, T. G. (editor), 1923. Birds of America. 3 Vols. 1:1-272; 2:1-271; 3:1-289. (257) Peckham, G. W., and E. G. Peckham, 1887. On the instincts and habits of the soli- tary wasps. Wis. Geol. Nat. Hist. Surv., 2:3-245. (226) Pemberton, C. E., and H. F. Willard, 1918a. Interrelations of fruitfiy parasites in Hawaii. Jour. Agr. Res., 12:285-295. (167) 19186. Contribution to the biology of fruit parasites in Hawaii. Ibid., 15:419- 465. (167) Petersen, C. G. J., 1908. First report on the oysters and oyster fisheries in the Lim Fjord. Rep. Dan. Biol. Sta., 15, 17:1-41; with map of oyster beds. 2nd Rep., ibid., 1-23. (337) 1913. Valuation of the sea. II. The animal communities of the sea bottom and their importance for marine zoogeography. Rep. Dan. Biol. Sta., 21:1-44, and App., 1-68. (6, 13, 15, 119, 336) 1914. Appendix of report 21:1-7, Rep. Dan. Biol. Sta., 22:89-96. (15, 247, 336, 340, 349) 1915a. On the animal communities of the sea bottom in the Skagerak, the Christiania Fjord and the Danish waters. Rep. Dan. Biol. Sta., 23:3-28. (15, 110, 336, 340) 19156. A preliminary result of the investigations on the valuation of the sea. Rep. Dan. Biol. Sta., 23 (1915):29-32. (119, 336, 340) 1918. The sea bottom and its production of fish food. Rep. Dan. Biol. Sta., 25:1-62. (15, 119, 230, 235, 324, 335, 340, 342, 344, 350) Petersen, C. G. J., and P. B. Jensen, 1911. Valuation of the sea. I. Animal life of the sea-bottom, its food and quantity. Rep. Dan. Biol. Sta., 20:1-76. (15, 102) 382 BIBLIOGRAPHY Petersen, C. G. J., and J. A. L. Lewisohn, 1899. Trawling in the Skagerack and Kattegat, 1897-98. Rep. Dan. Biol. Sta., 9:1-56. (336) Phifer, L. D., 1933. Seasonal distribution and occurrence of planktonic diatoms at Friday Harbor, Washington. Univ. Wash. Pub. Oceanog., 1:39-81. (315) 1934a. Phytoplankton of East Sound, Washington, February to November, 1932. Univ. Wash. Bull. Oceanog., 1:97-110. (315) 19346. Periodicity of diatom growth in San Juan Archipelago. Fifth Pac. Sci. Congr. Victoria and Vancouver, B. C., 1933:2047-2049. (315) 1934c. Vertical distribution of diatoms in the Strait of Juan de Fuca. Univ. Wash. Pub. Oceanog., 1:83-96. (315) Phelps, E. B., and D. L. Belding, 1931. A statistical study of the records of salmon fishing on the Restigouche River. {See Amory) (199) 1933. Trends and cycles among salmon. In Elton "Abstract of papers and dis- cussions, Metamek conference on biological cycles." (199) Phillips, F. J., 1909. The dissemination of junipers by birds. For. Quar., 8:1-16. {See 126) Phillips, J. C., 1913. Bird migration from the standpoint of its periodic accuracy. Auk, 30:191-204. (218) 1932. Fluctuations in numbers of the eastern brant goose. Auk, 49:445-453. (197) Phillips, J. F. V., 1926. Ramfall interception by plants. Nature, 118:837-838. (93) 1930. The application of ecological research methods to the tsetse problem in Tanganyika Territory. Ecology, 9:713-733. (12) 1931a. Forest succession and ecology in the Knysna Region. Bot. Surv. Union S. Agr. Mem. 14, Jour. Ecol. 1935. (12) 19316. The biotic community. Jour. Ecol., 19:1-24. (12) 1931c. Quantitative methods in the study of numbers of terrestrial animals in biotic communities. Ecology, 12:633-649. (12) 1931d. The influence of Usnea (near barbata Fr.) upon the supporting tree. Trans. Roy. Soc. S. Afr., 17:2:101-107. (12, 140) 1934-35. Succession, development, the climax, and the complex organism: an analysis of concepts. Parts I-III. Jour. Ecol., 22:554-571, 23:210-246, 488-508. (12, 24) Picket, A., 1905. Influence de I'alimentation et de I'humidite sur la variation des papillons. ISIem. Phys. Nat. Gen., 35:45-127. (117) 1911. Un nouvel exemple de I'hereditc des characters acquis. Arch. Soc. Phys. Nat. Gen., 31:561-563. (117) Pierron, R. p., and Y. C. Huang, 1926. Animal succession of denuded rocks. Pub. Puget Sd. Biol. Sta., 5:149-157. (329) PiETENPOL, W. B., 1918. Selective absorption in the visible spectrum of the W^isconsin lake water. Trans. Wis. Acad. Sci., 19:562-593. {See 296) PiLSBRY, H. A., 1916. Sessile barnacles (Cirripedia) contained in the collection of the U. S. National Museum. Bull. U. S. Nat. Mus., 93. (54) Piper, C. V., 1906. Flora of the State of Washington. Contrib. U. S. Nat. Herb., 11. (292) Piper, S. E., 1908. Mouse plagues, the control and prevention. Yearbook U. S. Dept. Agr., 1908:301-310. (184) DU Plessis, C., 1938. Locust outbreaks in the Union during the season 1936-37. Dept. of Agr. and Forestry. Sci. Bull., 181 :5-12. {See 198) BIBLIOGRAPHY 383 Pool, R. J., 1914. Vegetation of the sandhills of Nebraska. Minn. Bot. Studies, 4:312. (267) PospELOV, V. P., 1926. The influence of temperature on the maturation and general health of Locusta migratoria Linn. Bull. Entom. Res., 16:363-367. (184) Post, H., von, 1862. Studien liber die koprogenen Bildungen der Jetztzeit.: Gyttja, Dy, Torf und Humus. K. Sv. Vet Akad Hand!., 4. (73, 96) 1867. Forsok till iakttagelser i djur- och viixt-statistik. Ofversikt af Kongl. Vetenskaps-Akad. Forhandlingar No. 2. (5) Pound, R., 1892. Symbiosis and mutualism. Am. Nat., 509-520. (138) Pound, R., and F. E. Clements, 1898. The phytogeography of Nebraska. 2nd ed. 1900. Lincoln. (120, 251) Powers, E. B., 1921. Experiments and observations on the behavior of marine fishes toward the H-ion concentration of the sea water in relation to their migra- tory movements and habitat. Pub. Puget Sd. Biol. Sta., 3:1-22. (316) Preble, E. A., 1908. A biological investigation of the Athabaska-Mackenzie Region. U. S. Dept. Agr. N. Am. Fauna, 27:1-574. (201) 1923. Birds and mammals of Pribilof Isle, Alaska, N. Am. Fauna, 26:1-128. (170) 1925. British Columbia, NaturaUst's Guide to the Americas; Baltimore. See p. 155. (293) Price, W. A., 1929. Calcium and phosphorus utilization in health and disease. Dent. Res. Lab. Cleveland Bull., 79:1-32. (214) PuRCHAS, S., 1657. A theater of political flying insects, wherein especially the nature, the worth, the work, the wonder and the manner of right-ordering of the bee is discovered and described. London. (198) PtJTTER, August, 1908. Die Ernahrung der Wassertiere. Zeits. allg. Physiol., 7:283-320. (297) Quayle, E. T., 1922. Local rain-producing influences under human control in South Australia. Proc. Roy. Soc. Victoria, 34:89-104. (93) Raunkiaer, C, 1934. Life forms of plants and statistical plant geography. Oxford Press, New York. (48, 49) ^ Rasmussen, D. I., 1932. The biotic communities of the Kaibab Plateau. INlanu- script, Univ. of 111. Library. (33, 185, 201) Rawson, D. S., 1928. PreUminary studies of the bottom fauna of Lake Simcoe, Ontario. Univ. Toronto Studies: Biol. Series, Pub. Ont. Fish. Res. Lab., No. 36. (306) 1930. The bottom fauna of Lake Simcoe and its role in the ecology of the lake. Univ. Toronto Studies: Biol. Series, Pub. Ont. Fish. Res. Lab., No. 40. (306) Read, C, 1920. The origin of man and of his superstitions. Cambridge. (131, 154) Rensch, B., 1931. Der Einfluss des TropenkUmas auf den Vogel. Proc. VII Inter. Ornith. Congr. Amsterdam. 197-205. (214) Regnard, p., 1891. Recherches experimentales sur les conditions physiques de la vie dans les eaux. Paris, 500 pp. (297) Reighard, J., 1908. Methods of studying the habits of fishes, with an account of the breeding habits of the horned dace. U. S. Bur. Fish. Bull., 28:1111-1136. (311, 358) 384 BIBLIOGRAPHY Rice, Lucile, 1930. Peculiarities in the distribution of barnacles in commutiities and their probable causes. Pub. Paget Sd. Biol. Sta., 7:249-257. (18, 244) 1935. Controlling factors in the arrangement of barnacle species. Ecol. Mon., 5:293-303. (In Shelf ord et al.) ' (44, 45, 244, 327) Rich, Willis H., 1920. Early history and seaward migration of Chinook salmon in the Columbia and Sacramento Rivers. BuU. U. S. Bur. Fish., 37:1-73, 4 pis. (202) Richardson, R. E., 1921a. The small bottom and shore fauna in the middle and lower Illinois River and its connecting lakes. 111. St. Nat. Hist. Surv. Bull., 13:363-522. (299) 19216. Changes in the bottom and shore fauna of the middle Illinois River and its connecting lakes since 1913-1915 as a result of increase southward of sewage pollution. 111. St. Nat. Hist. Surv. Bull., 14:33-75. (299) 1925a. Changes in the small bottom fauna of Peoria Lake, 1920-1922. 111. St. Nat. Hist. Surv. BuU., 15(5):327-388. (299) 19256. The Ilhnois River small bottom fauna in 1923. 111. St. Nat. Hist. Surv. Bidl., 15:391-422. (299) 1929. The bottom fauna of the middle Illinois River, 1913-1925: its distribution, abundance, valuation and index value in the study of stream pollution. 111. St. Nat. Hist. Surv. Bull., 17(12) :387-475. (299) RiCKER, W. E., 1932. Studies of trout lakes and ponds. Univ. Toronto Studies; Biol. Ser. Pub. Ont. Fish. Res. Lab., 36:146-151 (on Coledon Ponds). (159, 235, 307) Riddle, O., 1927. The cycUcal growth of the vesicula seminahs in birds is hormone controlled. Anat. Rec, 37(1):1-11. (217) 1935. Vitamin E. Contemplating the hormones. Endocrinology, 19:1-13. (217) Riddle, O., G. Christman, and F. G. Benedict. 1930. Differential response of male and female ring-doves to metabolism measurement at higher and lower temperatures. Am. Jour. Physiol., 95:111-120. (217) Riddle, O., and L. B. Dotti, 1936. Blood calcium in relation to anterior pituitary and sex hormones. Science, 84:557-559. (217) Riddle, O., and W. S. Fisher, 1925. Seasonal variation of thyroid size in pigeons. Am. Jour. Physiol., 72:464-487. (217) Riddle, O., G. C. Smith, and F. G. Benedict, 1932. The basal metabolism of the mourning dove and some of its hybrids. Am. Jour. Physiol., 101:260-267. (214, 216) Riley, C. V., A. S. Packard, C. Thomas, et al, 1880. Second report of the United States Entomological Commission for the years 1878 and 1879, relating to the Rocky Mountain locust and the western cricket. Washington. (198) Riviere, B. B., 1929. The "homing faculty" in pigeons. Verh. VI. Int. Orn. Kongr., 535. (227) Roberts, T. S., 1907. A Lapland longspur tragedy. Auk, 24:369-377. (183) 1932. Birds of Minnesota. Minneapolis. (219) Rodenbach, 1895. Zeits. Brieftaubenkunde, 11:134. (227) RoMELL, L. G., 1921. Voles as a factor in plant ecology. Svensk. Bot. Tids., 15:43-45. (79) 1932o. Mull and duff as biotic equihbria. For. Soils Lab. Cornell Univ., 34:161- 188. (79) 19326. Ecological problems of the humus layer in the forest. Cornell Univ. Agr. Exp. Sta. Mem., 170. (79) 1935. Mecanisme de I'aeration du sol. Ann. Agron. (79) BIBLIOGRAPHY 385 Roosevelt, T., 1910. African game trails. New York. (33, 156) RoRiG, G., 1905. Studien liber die wdrtschaftliche Bedeutung der insektfressenden Vogel. Biol. Abteil. Land Forstw., 4:1-50. (214) RossMASSLER, E. A., 18G3. Der Wald. Leipzig und Heidelberg. (22) Rowan, W., 1926. On photoperiodism, reproductive activitj', and the annual migrations of birds and certain fishes. Proc. Boston. Soc. Nat. Hist., 38:147- 189. (211, 212) 1929. Experiments in bird migration. I. Manipulation of the reproductive cycle: seasonal changes in the gonads. Proc. Boston Soc. Nat. Hist., 39:151-208. (212) 1930. Experiments in bird migration. II. Reversed migration. Proc. Nat. Acad. Sci., 16:520-525. (212) 1931. The riddle of migration. Baltimore. (210) 1932. Experiments in bird migration. Proc. Nat. Acad. Sci., 18:639-654. (210, 211, 212) 1933. Fifty years of bird migration. Fifty years' prog. Am. ornith., 1883-1933, 51-63. {See 210-212) RtJBEL, E., 1935. The replaceabihty of ecological factors and the law of the mini- mum. Ecology, 16:336-341. {See 105) RiJppELL, W., 1931. Zug der jungen Storche {Ciconia c. ciconia L.) ohne Fiihrung der Alten; Der Vogelzug, 2:119. (228) 1934. Versuche zur Ortstreue und Fernorientierung der Vogel, II; Der Vogelzug 5, S. 53-59. (227) 1934. Versuche zur Ortstreue und Fernorientierung der Vogel, III; Der Vogelzug 5, S. 161-166. (227) 1935. Heimfindeversuche mit Staren, 1934. Jour. Orn., 83:462-524. (227) Rush, W. ]M., 1931. Northern Yellowstone elk study. Outdoor America, 10:12-13, 29-30. (185) Russell, C. P., 1932. Seasonal migration of mule deer. Ecol. Mon., 2:2-46. (201) Russell, E. S., 1932. Fishery research; its contribution to ecology. Jour. Ecol. 20:128-151. (19) Russell, F. S., 1928a. The vertical distribution of marine macroplankton. VI. Further observations on diurnal changes. Jour. ^lar. Biol. Assoc, 15:81-104. (322) 19286. The vertical distribution of marine macroplankton. VII. Observations on the behaviour of Calanus finmarchicus. Jour. Mar. Biol. Assoc, 15:429- 454. (322) 1928c. The vertical distribution of marine macroplankton. VIII. Further obser- vations on the diurnal behaviour of the pelagic young of teleostean fishes in the Plymouth area. Jour. Mar. Biol. Assoc, 15:829-850. (322) 1930a. The vertical distribution of marine macroplankton. IX. The distribution of the pelagic young of teleostean fishes in the daytime in the Plymouth area. Jour. Mar. Biol. Assoc, 16:639-676. (322) 19306. The seasonal abundance and distribution of the pelagic young of teleostean fishes caught in the ring-trawl in off-shore waters in the Plymouth area. Jour. Mar. Biol. Assoc, 16:707-722. (322) 1931a. The vertical distribution of marine macroplankton. X. Notes on the behaviour of Sagitta in the Plymouth area. Jour. Mar. Biol. Assoc, 17:391-414. (322) 19316. The vertical distribution of marine macroplankton. XI. Further obser- vations on diurnal changes. Jour. Mar. Biol. Assoc, 17:767-784. (322) Russell, F. S., and C. M. Yonge, 1928. The seas. London and New York. (35) 386 BIBLIOGRAPHY RuTHVEN, A. G., 1908. Variation and genetic relations of the garter snake. U. S. Nat. Mus. Bull., 61 :1-193. {See 251-293) 1911. Amphibians and reptiles. A biological survey of the Sand Dune Region on the south shore of Saginaw Bay. Mich. Geol. and Biol. Surv. Pub., 4; 2:257- 272 (8) Salisbury, E., 1924. Influence of earthworms on soil reaction. Linn. Soc. Jour. Bot., 46:415-425. (84) Sampson, A. W., and L. H. Weyl, 1918. Range preservation and its relation to erosion control on western grazing lands. U. S. Dept. Agr., Bull. 675. (71) Sampson, H. C., 1921. An ecological survey of the prairie vegetation of Illinois. lU. Nat. Hist. Surv. Bull., 13:523-577. (273) Saunders, W. E., 1907. A migration disaster in Western Ontario. Auk, 24:108- 110. (183) Savage, D. A., and L. A. Jacobson, 1935. The kilhng effect of heat and drought on buffalo grass and blue grama grass at Hays, Kansas. Jour. Am. Soc. Agron., 27:566-582. (256, 270) ScAMMON, C. M., 1874. The marine mammals of the northwest coast of North America. San Francisco. (316) ScHAEFER, E. E., 1936. The white fungus disease (Beauveria Bassiana) among red locusts in South Africa and some observations on the grey fungus disease {Ein- pusa grylli). Plant Industry Series, 18, Sci. Bull. 160:5-28. {See 184) ScHAFER, N. A., 1907. On the incidence of daylight as a determining factor in bird migration. Nature, 77:159-163. (211, 212, 217) ScHiMPER, A. F. W., 1898 (1903). Plant Geography on a physiological basis. Enghsh translation, 1903. Oxford. (242) Schmidt, J., 1922. The breeding places of the eel. Phil. Trans. B., 211:179-208. (202) 1923. Breeding places and migrations of the eel. Nature, 111:51-54. (202) 1924. The transatlantic migration of the eel-larvae. Nature, 113:12. (202) ScHOUR, Isaac, 1936. The neonatal line in the enamel and dentin of the human deciduous teeth and first permanent molar. Journ. Amer. Dental Assoc, 23:1946-1955. (187) ScHOUR, Isaac, and H. G. Poncher, 1937. Rate of apposition of enamel and dentin, measured by the effect of acute fluorosis. Amer. Journ. Diseases of Children, 54:757-776. (187) ScHOUR, Isaac, and S. R. Steadman, 1935. The growth pattern and daily rhythm of the incisor of the rat. Anatomical Record, 63:4. (187) ScHROTER, C., 1908. Das Pflanzenleben der Alpen. Eine Schilderung der Hochge- birgsflora. Zurich. (53) Schwartz, W., 1924. Untersuchungen liber die Pilzsymbiose der Schildlause. Biol. Zeit., 44. (141) 1932. Neue Untersuchungen liber die Pilzsymbiose der Schildlause (Lecaniinen). Arch. Microbiol., 3:453. (141) Seamans, H. L., 1926. The pale western cutworm. Dom. Can. Dept. Agr. Pam. No. 71 :l-8, new series. (190) Sears, P. B., 1937. This is Our World. Norman, Okla. (94) Seebohm, H., 1888. The geographical distribution of the family Charadriidae, or plovers, sandpipers, snipes and their allies. 524 pp. London. (211) Sellars, R. W., 1922. Evolutionary naturalism. Chicago. (23) BIBLIOGRAPHY 387 Selous, F. C, 1908. African nature notes and reminiscences. London. (156) Seton, E. T., 1909. Life histories of northern animals. 2 vols. New York. (253, 254) 1911. The arctic prairies. New York. (177,180,193,201) 1929. Lives of game animals. New York. (126, 156, 183, 193, 201, 253, 254) Shackleford, M. W., 1929. Animal communities of Illinois prairie. Ecology, 10:126-140. (12, 246, 274, 276) Shantz, H. L., and R. Zon, 1924. Natural vegetation. U. S. Dept. Agr. Atlas of Am. Agr., Part I. Physical Basis of Agr. Sec. E.:l-29. (247) Shelford, M. B., 1913. The decline of primeval communities at the head of Lake Michigan. In Animal communities in temperate America, pp. 13-15. Chicago. (273) Shelford, V. E., 1907. Prehminary note on the distribution of the tiger beetles (Cicindela) and its relation to plant succession. Biol. Bull. 14:9-14. (8) 1910, Ecological succession of fish and its bearing on fish culture. 111. Acad, of Sci., 3:108-110. {See 46, 147, 307, 308) 1911a, h. Ecological succession. I. Stream fishes and the method of physio- graphic analysis. Biol. Bull., 21:9-35. (8,46,147,307,308) 1911c. Ecological succession. II. Pond fishes. Biol. Bull., 21:127-151. (8,46, 147, 307, 308) 191 Id. Ecological succession. III. A reconnaissance of its causes in ponds with particular reference to fish. Biol. Bull., 22:1-38. (8, 46, 147, 307, 308) 191 le. Physiological animal geography. Jour. Morph. (Whitman Vol.), 22:551- 618. (8, 33, 46, 147, 307, 308) 1913a. Animal communities in temperate America. Chicago. Reprinted, 1937 with notes and new bibUography. (8, 28, 33, 49, 105, 147, 232, 274, 306, 355) 19136. The reactions of certain animals to gradients of evaporating power of air. A study in experimental ecology. (With a method of establishing evaporation gradients, by V. E. Shelford and E. O. Deer.) Biol. Bull., 25:79-120. (9) 1914a. An experimental study of the behavior agreement among animals of an animal community. Biol. Bull., 26:294-315. (310) 19146. Modification of the behavior of land animals by contact with air of high evaporating power. Jour. Ani. Behav., 4:31-49. (9) 1914c. A comparison of the responses of sessile and motile plants and animals. Am. Nat., 48:641-674. (52) 1915. Principles and problems of ecology as illustrated by animals. Jour. Ecol., 3:1-23. (9, 46) 1916. Physiological difTerences between marine animals from different depths. Pub. Puget Sd. Mar. Sta., 1:157-176. {See 316-317) 1917. Suggestions as to field and laboratory instruction in the behavior and ecology of animals, with descriptions of equipment. School Sci. Math., 17:388- 409. {See 355-357) 1918a. Relations of marine fishes to acids with particular reference to the Miles acid process of sewage treatment. Pub. Puget Sd. Biol. Sta., 2:97-111. (316) 19186. Conditions of existence. Ward and Whipple, Fresh water biology. Chapter 11:21-60. (312) 1923. The determination of hydrogen ion concentration in connection with fresh- water biological studies. 111. Nat. Hist. Surv. Bull., 14(9):380-395. {See 296) 1926. Terms and concepts in animal ecology. Ecology, 7:389. {See 229-253) 1929a. Laboratory and field ecology. Baltimore. (355) 388 BIBLIOGRAPHY 19296. The penetration of light into Puget Sound waters as measured with gas- filled photoelectric cells and ray filters. Pub. Puget Sd. Biol. Sta., 7:151-168. (296, 316) 1930. Geographic extent and succession in Pacific North American intertidal (Balanus) communities. Pub. Puget Sd. Biol. Sta., 7:217-223. (329-330) 1931. Some concepts of bio-ecology. Ecology, 12:455-467. (12,187) 1932o. An experimental and observational study of the chinch bug in relation to cUmate and weather. 111. Nat. Hist. Survey Bull., 19:487-547. (189) 19326. Basic principles of the classification of communities and habitats and the use of terms. Ecology, 13:105-120. (12) (5ee 243-247) 1933. Preservation of natural biotic communities. Ecology, 14:241-245. (357) 1935. The physical environment. Handb. Soc. Psych., Worcester, Mass., Chapter 14. (230, 235, 238, 245, 246, 347) 1936. Conservation of wild life. Parkins and Whitaker. Our natural resources and their conservation. Chapter 19:485-526. (357) Shelford, V. E., and M. W. Boesel, 1939. Bottom communities of western Lake Erie. Ms. (306) Shelford, V. E., and S. Eddy, 1929a. Methoden zur Untersuchung von Flusslebens- gemeinschaften, Handb. Biol. Arbeitsmethoden, Abt. 9, Teil 22:1525-1549. (18) 19296. Methods for the study of stream communities. Ecology, 10(4):382-391. (18) Shelford, V. E., and F. W. Gail, 1922. A study of light penetration into sea water made with the Kunz photoelectric cell with particular reference to the distribu- tion of plants. Pub. Pug. Sd. Biol. Sta., 3:141-176. (296, 316) Shelford, V. E., and S. Olson, 1935. Sere, chmax and influent animals with special reference to the transcontinental coniferous forest of North America.' Ecology, 16:375-402. (12,243) Shelford, V. E., and E. C. Powers, 1915. An experimental study of the movements of herring and other marine fishes. Biol. Bull., 28:315-334. (316) Shelford, V. E., and E. D. Towler, 1925. Animal communities of San Juan Channel and adjacent areas. Pub. Pug. Sd. Biol. Sta., 5:21-73. (18, 54, 247, 330) Shelford, V. E., A. O. Weese, L. A. Rice, D. I. Rasmussen, and A. MacLean, 1935. Some marine biotic communities of the Pacific coast of North America. Ecol. Mon., 5:250-254. (18, 244, 294, 315, 326, 327, 330, 333, 339, 332) Shimek, B., 1911. The prairies. Bull. Lab. Nat. Hist. State Univ. Iowa, 6:169- 240. (269) Simroth, H., 1908. tjber den Einfluss der letzten Sonnenfleckenperiode auf die Tierwelt. Verh. deut. Zool. Ges., 18:140-153. (196, 199) 1909. Abhiingigkeit der Colias edusa von der Sonnenfleckenperiode in Beziehung zur geographischen Verbreitung. Zeit. Insektbiol, 5:63-65. (See 196-199) Skovgaard, p., 1929. Danske Fugle. 10:215-216. (228) Smith, F., 1930. Records of spring migration of birds at Urbana, Ilhnois. 1903- 1922. 111. St. Nat. Hist. Surv. Bull., 19:105-117. (225) Smith, G. M., 1928. Food material as a factor in growth rate of some Pacific clams. Trans. Roy. Soc. Can., 22:287-291. (245) Smith, J. B., 1909. Insects of New Jersey. N. J. St. Mus. Ann. Rep., 1909:1-888. (260) Smith, J. W., 1915. II. Phenological dates and meteorological data recorded by Thomas Mikesell between 1873 and 1912 at Wauseon, Ohio. Mon. Weath. Rev. Sup., 2:23-93. (221) BIBLIOGRAPHY 389 Smith, V. G., 1928. Animal communities of a deciduous forest succession. Ecology, 9:479-500. (12, 61, 245) Smith-Davidsox, V. G., 1930. The tree layer society of the maple-red oak cHmax forest. Ecology, 11:601-606. (12,246) 1932. The effect of seasonal yariabihty upon species in total populations in a deciduous forest succession. Ecol. Mon., 2:306-323. (12) Smuts, J. C, 1926. Evolution and holism. London. (1, 23) Snow, H. F., 1891. Chinch bugs; experiments in 1890 for their destruction in the field by artificial introduction of contagious disease. Rep. Kan. St. Board Agr., 7:184-188. (184) Soot-Ryen, T., 1924. Faunistische Untersuchungen im Ramfjorde. Tromso Mus. Arshefter, 45. (334, 345) Southern, R., 1915. Marine ecology. Proc. Roy. Irish Acad. (Clare Island Surv.). Sec. 3, Part 67, 31:1-110. (313) Sparck, R., 1929. PreUminary survey of the results of quantitative bottom investi- gations in Iceland and Faroe waters, 1926-1927. Cons. Perm. Inter. Explor. Mer, Rapp. Proc.-verb, Scientific Rep. of the Northwestern Area Com., 47:1-28. (Paged separately.) (334) 1933. Contribution to the animal ecology of the Franz Joseph Fjord and adjacent waters, I-II Medd. om Gronl., 100. (334, 345) 1935. On the importance of quantitative investigation of the bottom fauna in marine biology. Cons. Perm. Inter. Explor. Mer. Jour. Conseil, 10:3-19. (334, 336, 341, 345) 1937. Benthonic animal communities of the coastal waters. The Zoology of Iceland. Copenhagen. 1:6:1-45. (345) Spaulding, E. G., 1918. The new rationaUsm. New York. (23) Spencer, H., 1866. Principles of biology. New York. (24) Steiger, T. L., 1930. Structure of prairie vegetation. Ecology, 11:170-217. (See 269-273) Stejneger, L., 1891. See Merriam and Stejneger. Step, E., 1913. Messmates. A book of strange companionships in Nature. New York. (138, 143) Stephen, A. C, 1930. Studies on the Scottish marine fauna. (1) Additional observations on the fauna of the sandy and muddy areas of the tidal zone. Trans. Roy. Soc. Echn. Part II, 56:80-355. (332) 1933. (2) Natural faunistic divisions of the North Sea as shown by quantitative distribution of mollusca. Part III, 57:601-616. (3) Echinoderms, 777-788. (343) Stephens, F., 1906. The mammals of California. San Diego. (289) Stephens, T. C, 1922. Mammals of the lake region of Iowa. Bull. Okoboji Prot. Assoc, 1922:47-63. (274) Stephenson, T. A., Anne Stephenson, and C. A. du Toit, 1937. The South African intertidal zone and its relation to ccean currents. Trans. Roy. Soc. S. Air., 24:341-382. (See 324r-330) Stevens, B. A., 1926. Callianassidae from the west coast of North America. Pub. Pug. Sd. Biol. Sta., 6:315-369. (338) Stevens, G. A., 1930. Bottom faima and the food of fishes. Jour. Mar. Biol. Assoc, 16:677-706. (5ee 340-342) Stevenson, J., 1933. Experiments on the digestion of food by birds. Wilson Bull., 45:155-167. (214) 390 BIBLIOGRAPHY Stoddard, H. L., 1931. The bob-white quail. Its habits, preservation, and increase. New York. (73, 127, 134, 154, 175) Stone, W., 1891. Bird waves and their graphic representation. Auk, 8:194-198. (225) Strong, L. H., 1925. Development of certain Puget Sound Hydroids and Medusae. Pub. Puget Sd. Biol. Sta., 3:383-399. (316) Sumner, F. B., R. C. Osburn, L. J. Cole, and B. M. Davis, 1911. A biological survey of the waters of Woods Hole and vicinity. Bull. Bur. Fish. U. S., Sects. 1 and 2, 31:1-860. (336) Sumner, W. G., and A. G. Ivelleb, 1927. The science of society. New Haven. (23) SwiNTON, A. H., 1883. Data obtained from solar physics and earthquake commotion applied to elucidate locust multiplication and migration. 2nd Rep. U. S. Entom. Com. Ch., 5:65-85. (198) Szent-Gyorgyi, A., 1933. Identification of vitamin C. Nature, 131:225. (217) Taft, a. C, and Leo Shapovalov, 1938. Homing instinct and straj-ing among steelhead trout (Salmo gairdnerii) and silver salmon {Oncorhynchus kisutch). Cahf. Fish and Game, 24:118-125. {See 201-202) Tansley, a. G., 1920. The classification of vegetation and the concept of develop- ment. Jour. Ecol., 8:118-149. (22) 1922. Studies of the vegetation of the Enghsh chalk. 11. Early stages of the redevelopment of woody vegetation on chalk grassland. Jour. Ecol., 10:168- 177. (125) 1929. Succession. The concept and its values. Inter. Congr. Plant. Sci., 1:677- 686. (22) 1935. The use and abuse of vegetational concepts and terms. Ecologj', 16:284- 307. (24) Tansley, A. G., and T. F. Chipp, 1926. Aims and methods in the study of vegeta- tion. London. (50) Taverner, p. a., 1904. A discussion of the origin of migration. Auk, 21:322-333. (210) Taylor, W. P., 1911. Mammals of the Alexander, Nevada, expedition of 1909. Univ. Cal. Pub. Zool., 7:205-307). (292) 1924. The basic importance of life-history studies. Jour. Mam., 5:44-48. (34, 44) 1930n. Outlines for studies of mammahan life-histories. U. S. Dept. Agr. Misc. Pub., 86:1-12. (34, 44) 19306. Methods of determining rodent pressure on the range. Ecology, 11:523- 542. (75) 1934. Significance of extreme or intermittent conditions in distribution of species and management of natural resources, with a restatement of Liebig's law of minimum. Ecology, 15:374-379. (105, 176) 1935. Significance of the biotic community in ecological studies. Rev. Biol., 10:291-307. (See 229-243) 1936. Some effects of animals on plants. Sci. Mon., 53:262-271. (See 116-126) Taylor, W. P., and J. V. G. Loftfield, 1922. Damage to range grasses by the Zuni prairie dog. U. S. Dept. Agr. Bull., 1227:1-16. (11, 121, 122) Taylor, W. P., and W. T. Shaw, 1929. Provisional hst of the land mammals of the state of Washington. Occ. Pap. Conner Mus. State Coll. Wash., 2 :l-32. (292) BIBLIOGRAPHY 391 Tharp, B. C, 1926. Structure of Texas vegetation east of the 98th meridian. Univ. Te.x. Bull., 2606:1-97. (278) Thatchexko, M. E., 1930. Origin and propagation of forestry ideas. Jour. For., 28:595-617. (22) Thienemann, a., 1913. Der Zusammenhang zwischen dem Sauerstoffgehalt des Tiefenwassers und der Zusammensetzung der Tiefenfauna unserer Seen. Inter. Rev. Hydrobiol., 249-253 (17) (*See 295-297) 1913-1914. PhysikaUsche und chemische Untersuchungen in den Maaren der Eifel. I-II. Verh. Naturh. Ver. preuss. Rheinl., 70-71. (17, see 295-297) 1918. Lebensgemeinschaft und Lebensraum. Naturw. Woehenschr. 17:20-21. (10) 1921. tJber biologische Seetypen und ihre fischereische Bedeutung. Allg. Fisch- ereizeitung (N.F. XXXVI), Nr. 17. 1925. Der See als Lebenseinheit. Naturwiss., 27:589-600. (17,22) 1926. Die Binnengewiisser Mitteleui'opas. I. Stuttgart. (312) 1928. Der Sauerstoff im eutrophen und oligotrophen See. Die Binnegewasser, 4:175. Stuttgart. (17) 1935. Die Bedeutung der Limnologie fiir die Kultur der Gegenwart. 31 pp. Stuttgart. (17) Thomas, C, 1880. Facts concerning and laws governing the migration of locusts in all countries. 2nd Rep. U. S. Entom. Com. Ch., 3:31-71. (198, 203) Thompson, D. H., and F. D. Hunt, 1930. The fishes of Champaign County. Bull. lU. St. Nat. Hist. Surv., 19(1):5-101. (299) Thompson, W. F., 1913. Report on the clam beds of British Columbia. Rep. Com. Fish. British Columbia. 1913. (338) Thomson, A. L., 1926. Problems of bird-migration. New York. (210, 211, 212, 226) 1936. Recent progress in the study of bird-migration: a review of the literature, 1926-35. Ibis, 6:472-530. (210, 211, 227) Thorson, G., 1933. Investigations on shallow water animal communities in the Franz Joseph Fjord (East Greenland) and adjacent waters. Medd. Gronl., 100, No. 2:1-69. (334) 1934. Contributions to animal ecology of the Scoresby Sound Fjord Complex (East Greenland). Medd. Gronl. 100, No. 3:1-68. (334, 345) TowLER, E. D., 1930. An analysis of the intertidal barnacle communities of the San Juan Archipelago. Pub. Pug. Sd. Biol. Sta., 7:225-232. (18, 244) TowNSEND, M. T., 1935. Studies on some small mammals of Central New York, Roosevelt Wild Life Ann. 4:1-120. (357) Transeau, E. N., 1905-06. The bogs and bog flora of the Huron River Valley. Bot. Gaz., 40:351-375; 418-448; and 41:17^2 (1906). (96) 1935. Prairie peninsula. Ecology, 16:423-437. (269, 271) UvAROv, B. P., 1928. Locusts and grasshoppers. London. (198, 199, 203, 205) 1931. Insects and climate. Trans. Entom. Soc. London. 79:1-247. (174, 198, 206) VanDenburg, J., 1922. Reptiles of western America. Occ. Pap. Cal. Acad. Sci., 10:pt. 2:623-1028. (290) Verrill, a. E., 1871-72. Report on the invertebrate animals of Vineyard Sound and adjacent waters. Rept. U. S. Com. of Fish, and Fisheries, 1871-72:295-544. (345) 392 BIBLIOGRAPHY Vestal, A. G., 1913. Local distribution of grasshoppers in relation to plant associa- tions. Biol. Bull., 25:141-180. (9) 1914. Internal relations of terrestrial associations. Am. Nat., 48:413-445. (9, 10) 1938. A subject index for communities, including vegetation-components. Ecol. 19:107-125. {See 229-247) ViSHER, S. S., 1916. The biogeography of the northern great plains. Geog. Rev., 2:89-115. (260) VoRHiES, C. T., 1936. Wild life aspects of range rehabilitation. Hoofs and Horns, 5; No. 8; 6-7, No. 9:10-11. (285) VoRHiES, C. T., and W. P. Taylor, 1922. Life history of the kangaroo rat. U. S. Dept. Agr. Bull., 1091:1-40. (11, 74, 80, 82, 122, 235, 285) 1933. Life histories and ecology of jack rabbits in relation to grazing in Arizona. Univ. Ariz. Agr. Exp. Sta. Tech. Bull., 49:471-587. (122, 125, 285) Wachs, H., 1926. Die Wanderungen der Vogel. Winterstein's "Ergebnisse der Biologie, ' ' 1 :479. (See 207-2 1 1 ) Walford, L. a., 1932. The CaUfornia barracuda. Div. of Fish and Game, California. Fish. Bull., 37:1-121. Walter, H. E., 1908. Theories of bird migration. School Sci. Math., 8:259-266, 359-366. (210) Ward, H. B., 1897. Biological examination of Lake ]\Iichigan in the Traverse Bay Region. Bull. Mich. Fish. Com., 6:1-100. (307) 1921. Some of the factors controlling the migration and spawning of the Alaska red salmon. Ecology, 2:235-254. (202, 256) 1938. Environmental stimuli and salmon migration. Reprinted from the Com- memorative Vol. Grigore Antipa. Monitorui Oficial Si ImprimeriUe Statului Imprimeria Nationala, Bucuresti. 1-11. (See 201, 202) Ward, H. B., and G. C. Whipple, 1918. Freshwater biology. New York. (358) Warming, 1909. Oecology of plants. An introduction to the study of plant com- munities. University Press: Oxford. (49) Wasmtjnd, E., 1934. Die physiologische Bedeutung des limnischen Hydrokhmas, Arch. Hydrobiol., 27:162-198. (229, 294, 314) Watson, J. B., and K. S. Lashey, 1915. An historical and experimental study of homing. Carnegie Inst. Wash. Pub. 211, Dept. of Mar. Biol., 8:1-104. (227) Watson, J. R., 1911. Ecological distribution of the animal life of north central New Mexico with special reference to insects. Nat. Resour. Surv. N. Mex., 67-117. (264) 1925. Florida. Naturahst's Guide, pp. 427-440. Baltimore. (233) Weaver, J. E., and F. W. Albertson, 1936. Effect of the great drought on the prairies of Iowa, Nebraska, and Kansas. Ecology, 17:567-639. (256, 270) Weaver, J. E., and F. E. Clements, 1929. Plant ecology. 2nd Ed., 1938. New York. (68, 247) Weaver, J. E., and T. J. Fitzpatrick, 1934. The prairie. Ecol. Mon., 4:109-295. (252) Weaver, J. E., and G. W. Harmon, 1935. Quantity of hving materials in prairie soils in relation to runoff and erosion. Univ. of Nebr. Conservation and Survey Bull. 8, Div. Bull. 11. (71) Weaver, J. E., and W. C. Noll, 1935. Comparison of runoff and erosion in prairie, pasture and cultivated land. Cons. Dept. Univ. Nebr. Bull., 11. (71) BIBLIOGRAPHY 393 Weaver, J. E., L. A. Stoddart, and Wm. Noll, 1935. Response of the prairie to the great drought of 1934. Ecology, 16:612-629. (256, 270) Webster, F. M., 1880. Notes on the food of predaceous beetles. 111. St. Lab. Nat. Hist. Bull., 1:162-166. (131, 135) Weese, a. O., 1924. Animal ecology of an IlUnois elm-maple forest. 111. Biol. Mon., 9:249-437. (U, 126, 245) 1926. Food and digestive processes in Strongylocentrotus drobachiensis. Pub. Puget Sd. Biol. Sta., 5:177-185. (See 330, 331) 1935. Serai communities in East Sound in relation to physiographic processes. In "Some marine biotic communities of the Pacific Coast of North America." In Shelford, et al., Ecol. Mon., 5:310-318. (244, 339) Weese, A. O., and M. T. Townsend, 1921. Some reactions of the jellyfish, Aequoria. Pub. Puget Sd. Biol. Sta., 3:117-128. (316) Weiss, F. E., 1909. The dispersal of the seeds of the gorse and broom by ants. New Phytol., 8:81-89. (129) Welch, R. S., 1935. Limnology. New York. (312) Wells, H. G., J. S. Huxley, and G. P. Wells, 1931. Science of life. Vol. 3, Book 6, Spectacle of life. Garden City. (1) Wetmore, a., 1926. The migration of birds. Cambridge, Mass. (65, 210, 212, 217) Wheeler, W. M., 1908. Honey ants, with a revision of North American Myrme- cocysti. Bull. Am. Mus. Nat. Hist., 24:345-397. (153) 1910. The ant colony as an organism. Mar. Biol. Lab. (See below.) (22) 1911. The ant colony as an organism. Jour. Morph., 22:307-325. (22) 1923. Social hfe among the insects. New York. (22, 141, 144, 152, 153, 155, 159) 1928a. Insect societies, their origin and evolution. New York. (22) 19286. Emergent evolution and the development of societies. New York. (23) 1930. Societal evolution. In Cowdry, "Human biology and racial welfare." New York. (149) Whitlock, F. B., 1897. The migration of birds: a consideration of Herr Gatke's views. London. (210) Wight, H. M., 1925. Oregon: Animal communities illustrated by mammals. Naturalist's Guide, Baltimore, pp. 185-189. (293) Williams, A. B., 1936. The composition and djTiamics of a beech-maple cUmax community. Ecol. Mon., 6:317-408. (217, 358) Williams, C. B., 1925. The migrations of the painted lady butterfly. Nature, 115:535. (202) Williams, M., 1929. Horizontal upward intensity of light in Puget Sound waters. Pub. Puget Sd. Biol. Sta., 7:129-135. (296) Wilson, O. T., 1925. Some experimental observations on marine algal succession. Ecology, 6:303-311. (-See 333) Wilson, P. T., 1926. A brief stud}'' of the succession of clams on a marine terrace. Pub. Puget Sd. Biol. Sta., 5:137-148. (See 333) Wing, L. W., 1934a. Cycles of migration. Wilson Bull., 46:150-156. (223) 1934b. Migration and solar cycles. Auk, 51:302-305. (223) 1935. Wild life cycles in relation to the sun. Trans. 21st Small Game. Confer., 345-363. (196, 197, 199, 223) Wismer, N. M., and J. H. Swanson, 1935. A study of the animal communities of a restricted area of mud bottom in San Juan Channel, Part II. Mar. Biotic Com. Pac. Coast N. A. Ecol. Mon., 5:333-345. (324, 330) 394 BIBLIOGRAPHY WiTHERBT, H. F., 1920. A practical handbook of British birds. London. (196) WoLCOTT, G. H., 1918. Animal census of two city lots. Sci., 47:366-367. (355) 1927. Animal census of two pastures and a meadow in northern New York. (Abstract, Proc. Entom. Soc. Wash., 29:62-65.) (355) 1937. Ecol. Mon., 7:1-90. (355) Wood, F. E., 1910. A study of the mammals of Champaign, 111. Bull. 111. State Lab. of Nat. Hist., 8:(5) 501-613. (108, 172) Wood, N. A., 1906. Twenty-five years of bird migration at Ann Arbor, Mich. Rep. Mich. Acad. Sci., 8:151-156. (225) Wood, N. A., and A. D. Tinker, 1934. Fifty years of bird migration in the Ann Arbor region of Michigan. Occ. Pap. Mus. Zool. Univ. Mich., No. 280. (219, 220) Wood-Jones, F., 1910. Coral and atolls. London. (31, 32, 53) WoRLEY, L. S., 1930. Correlation between salinity and size of intertidal barnacles. Pub. Pug. Sd. Biol. Sta., 7:233-240. (18) Yapp, R. H., 1922. The concept of habitat. Jour. Ecol., 10:1-17. (28) Zazhurilo, K. K., 1931. Classification of the ornithochoric fruits and seeds. (Russian with German summary.) Jour. Soc. Bot. Russie. 16(f) :169-189. (126) Zenkevitsch, L. a., 1927. Materialien zur quantitativen Untersuchung der Bodenfauna des Barents und des Weissen Meeres (in Russian). Ber. wiss. Meeresinstituts., Pt. 4, 2:1-64. (334) 1930. Ueber den neuen Bodensgreifer von Knudsen. (In Russian, with German summary.) Russ. Hydrobiol. Zeits., 7:201-203. (334) 1931. On the aeration of the bottom waters through vertical circulation. Jour. Cons. Inter. Explor. Mer., 6:402-418. (334) ZoN, R., 1912. Forests and water in the light of scientific investigation. Appendix V, Fin. Rep. Nat. Waterways Com. 2nd Ed. 1929. (93) 1913. The relation of forests in the Atlantic plain to the humidity of the central states and prairie region. Proc. Soc. Am. For., 8:139-153. (93) 1929. The role of the forests in the circulation of water on the earth's surface. Proc. Intern. Cong. Plant Sci., 1926, 1:741-749. (93) Zubareva, S. p., 1930. A statistical evaluation of the method of quantitative entomological collection by sweep nets. (In Russian.) Bull. Inst. Rech. Biol, et Sta. Biol. Univ. Perm., 7:89-104. (355) INDEX Page numbers in bold-faced type refer to pages on which terms are defined or the concept illustrated. Abert squirrel, 126 Abra, 181, 340, 341, 348 Abronia maritima, 60 Absorption, 92 Acacia, 283 Acids, 89, 90 Acipenser fulvescens, 306 Acmaea, cassis, 325, 328 digitalis, 325 digitalis umbonata, 328 Acorn barnacles, 313 Acorns, 129 Acridium acadicum, 267 Acrolophitus hirtipes, 265 Activity, 55 Adaptation, 54, 55 structural, 32 Adelphochorus rapidus, 275 Adenostoma, 288 Adrenalin, 217 Adults, 318 Aequorea forskalea, 315 Aesculus californica, 143 Agave, 283 Ageneotettix doorum, 265 Aggregation, 145-149, 57-59, 66 animal, 58, 59 as a process, 146-149 causes, 146, 147 consequences, 149 general relations, 145, 146 instinct, 206 kinds, 148, 149 on land, 147, 148 permanent, 59 plant, 57, 58 Agoseris, 292 Agropyrum. 243, 272, 279, 290, 292 pauciflonim. 291, 292 smithi, 256, 262, 270, 278, 290-292 Agropyrum, smithi dasystachyum, 291 spicatum, 244, 291, 292 spicatum inerme, 291, 292 Air, 62, 89 reaction, 89, 91 Alaska shrimp, 339 Alegocephalus coeruleus, 308 Algae, 89, 300, 331 blue-green, 75, 300 coralline, 313 microscopic, 91 yellow-green, 75 Algal s.ymbiont, 140 Allium, 287 Allobiocenose, 7 Alnus, 139 Alternating generations, 34 Amblycorypha hamsteca, 280 Ambrosia beetles, 155 Ambush bug, 275 Ambystoma, 46 Ameiurus melas, 300 Ammodramus (grasshopper sparrow), 257 Ammophila, 148 Ammospermophilus harrisii, 285 Amnicola, 306 Amoeba, 140 Amorpha canescens, 272 Amphibians, 62, 82 Amphictcis, 339 Amphilepsis-Pecten biome, 344, 345, 349 Amphiodia urtica, 339 Amphipods, 333 Amphissa, 326 Amphitornus coloradus, 265 Amphiura, 341 filiformis, 341 395 396 INDEX Anabaena, 139 circinalis, 303 Anadromoiis fishes, 201, 202 Andrena, 275 Andropogon. 120, 243, 273, 275 cin-atus, 282 contortus, 278 fiircatus, 278 hirtiflorus, 282 nutans, 278 saccharoides, 257, 278 scoparius, 256, 270, 278. 282 ternarius, 278 Andropogoneae, 278 Anemone, 325 caroliniana, 272 patens, 272 Anemone, sea, 327, 328 Angiosperms, floating. 96 submerged, 96 Animals, 44, 71, 88, 102, 109, 180 as active agents, 116, 117 competition. 166, 167 decumbent, 52 earlier, 251 ecesis, 65 food, 114 grassland, 253, 254 grazing, 119 influence, 237, 238 insectivorous, 134-136 in tidal areas, 99, 100 land, 235 maximum numbers, 194 motile, 31, 32, 46 organisms, 32 oviparous, 46-47 parasites of, 45-46 plankton, 91 reactions, 97 sedentary, 54 seed and fruit coactions, 125-131 sessile, 31, 53 multiple individuals, 50-54 sedentaiy in water, 44-45 single individuals, 54, 55 shelled, 101 symbiosis, 140, 141, 143, 144 trapping, 357 viviparous, 47-48 Annelids, 338, 339, 341 Annuation, 13, 222, 249, 348 Anodonta, 143 grandis, 300 Anosia plexippus, 203 Ant-eating flickers, 135 Antelope, 133, 253 jackrabbit, 285 pronghorn, 120, 264 Antennaiia campestris, 272 Anthus (pipits), 135, 257 Antilocapra americana, 243, 257, 259 Ant lion, 232 Ants, 59, 79, 82, 143, 155, 171, 172 cattle, 144 desert, 153 mound-making, 237 Aphids, 117 Aphodius distinctus, 275 Ajtlodinotus grunniens, 300, 306 Appendix, 354-358 Aquatic climax communities, 294-312 climax, fresh-water, 298-311 introduction, 298 lake, 305, 307 bottom subdominants, 306, 307 dominance of lake fishes, 307 dominants, 306 influents, 307 river, 299-305 biotic development, 303-305 dominants and subdominants, 300 faciations, 305 influents, 301 nature of dominance, 301-303 plankton, 301 properties, 298-299 small river, 299, 300 dominance, 240-241 food relations, 297, 298 fresh-water, 294 hydroclimates, 294, 295 hydroclimatic factors, 295-297 circulation, 295 density, 295 dissolved substances, 296, 297 light and temperature, 296 susjiendcd matter and color, 295, 296 INDEX 397 Aquatic climax communitios, intro- duction, 294 other, 311, 312 stream habitats, 307-311 comparison, 310, 311 swift-water, 308-311 Arboreal adaptations, 55 Areas, deep benthic, 100 pelagic, 100 tidal, 99 Arenicola, claperedii, 333 marina, 334 Argia, 308 Argobuccinum oregonense, 330 Argyropelecus, 322 — Cauliodus biome, 318 Aricia, 341 Aristida, 129, 287 adscensionis, 283 californica, 282 divaricata, 282, 287 purpurea, 278, 282, 287 ternipes, 282 Armillaria, 140 Arphia, conspcrsa, 267 pseudonietana, 265 Artemisia, 120, 272, 288, 293 dracunculus, 273 filifoha, 267 tridentata, 244, 292 vulgaris, 273 Arthropods, 46, 245 Asollus communis, 231 Asilus, 275 Aspection, 13, 35, 222, 225, 226 Aspens, 237 Assemblage, 5 Association, 243, 247, 256, 320, 8, 327, 331, 333 other usages, 18, 148, 149 Associations, Balanus-M. calif orni- anus, 327 edulis, 327 beech-maple, 8 Brissopsis-Amphiura, 345 California prairie, 285-290 coastal prairie, 277-280 Cottonwood, 8 Clymenella-Yoldia, 339 Cucumaria-Scalibregma, 339 Associations, desert plains, 280-285 Echinocardium-Amphiura, 341, 343 general discussion, 243, 247 grassland, 260-293 Haploops, 343, 345 Macoma, -Leptos3'napta, 333 -Paphia, 333 -Tellina, 336 map, 255 marine, Brevoortia-Calanus, 320 Clupea-Calanus, 320 mixed prairie, 260-269 Nucula-Corbula, 348 Palouse prairie, 290-293 relationship, 329 Strongylocentrotus, -Pteraster, 331, 332 -Pugettia, 331 Sj^ndosmya. -Solen, 348 -Solen-Mya, 348 true prairie, 269-277 Venus-Echinocardium, 341 Associative memory, 32 Associes, 232 size, 247, 248 Astarte-Arca biome, 345, 349 Astarte, borcalis, 334 crenata, 345 elliptica, 345 montagui, 334 Aster, 272, 292 ericoides, 272 levis, 272 multifloms, 272 novae-angliao, 272 Asteroidea. 338, 340 Astorotheca alascona, 332 Astragalus, 292 crassicarpus, 272 Atamasco, 279 Atriplcx, 292 Attached plants, 100 Attachment, 109 Attwater prairie chicken, 280 Aulocara elliotti, 265 Autecology, 1 Automatic instinct, 227 Avena, 120, 289 -Bromus disclimax, 289 fatua, 288 398 INDEX Azolla, 139 Azotobacter, 139 Bacillus typhimurium, 184 Bacteria, 97, 102, 139, 184 Bacterial diseases, 138 Badger, 132, 133, 193, 274, 276, 280, 285, 289, 290, 293 holes, 265 Baiomys taylori subater, 280 Balaenoptera, 319 Balance in nature, 173 Balanus, 328, 330 cariosus, 325, 320, 328, 329 glandula, 325, 326, 327, 328, 329 -Littorina biome, 244, 325, 320, 330, 352, 353 -M. calif ornianus, 327, 328, 353 -M. edulis, 327, 329 nubilis, 330 Bald eagle, 133 Balsamorhiza, 292 Bamboo-worm, 339 Banksian pine, 232 Baptisia, 279 leucophaea, 272 Barnacle, 54, 100, 244, 313, 323, 325 community, gastropod, 230, 324, 325- 330 mussel. 230 tidal, 313 goose neck, 325, 327 larvae, 44 Basket star, 332 Bass, 301 Bathophilus, 177 Bathysphere, 318, 319, 321 Bear, 193, 276 Beaver, 98, 133 Beech, 232 Bees, 114, 142, 143 Beetle, 130, 155 ambrosia, 155 bark, 109 cucumber, 275 ground, 131, 266 lady, 275 predaceous, 131 rose, 62 Beetle, tiger, 232, 266, 267 green, 276 white, 232 Behavior, 32, 55 Belanogaster, 152 Borlandiera, 279 Bignonia cherere, 143 Biocenology, 10 Biocenose, 6, 7, 9, 10 Biocenotics, 10 Bio-ecology, 1-19 biotic researches, 11-19 bio-ecology and oceanography, 18, 19 formation, in water, 13-16 on land, 11-13 limnology, 16-18 historical development, 5-10 nature and relations, 1, 2 relations of paleo-ecology, 4, 5 scope and significance, 2-5 Biome, 20, 25, 229, 3, 21-33, 27, 147, 229, 245-247, 250, 251, 315, 330, 332 adjustment and adaptation, 31-33 Amphilepsis-Pecten, 345 as a complex organism, 21-24 as a social organism, 20-25 Astarte-Arca, 345 Balanus-Littorina, 325-330 climate and climax, 229 composition, 234 constituents, 234 development, 231, 232, 27-30 difference, 230 Echinocardium-Thyasira, 340-345 enumeration, 250 fish-tunicate, Scomber-Calanus, 319, 320 functions, 56, 57 habitat, 26, 27 influence, 241-243 life forms, 229-231 Macoma, -Astarte, 334 -Mya, 334-338 -Paphia, 333 major units, 243-245 minor units, 245-247 nature, 20, 21 North American grassland, 251-293 INDEX 399 Biome, Pandora-Yoldia, 339 physical basis, 26 relative size, 247, 248 role of coaction, 107-109 size, 247 slenderfish-red prawn, Cyclothoue- Acanthephyra, 318 status of concept, 24, 25 Stipa-Antilocapra, 251-293 Strongylocentrotus-Argobucciniun, 330-332 Telescope-eyed fish, Argyropelecus- Cauliodus, 318-319 Biotic balance, 172-175 Biotic communities, 18 Biotic development, 303 Biotic formation, 20, 3, 7, 229, 247, 251 in water, 13-19 on land, 11-13 size, 247 Biotope, 11 Birds, 62, 82, 138, 144, 183, 184, 252 carnivores, 133, 134 coastal prairie, 280 cooperation, 153, 154 cycles, 183, 196, 197 dusting, 85 flocks, 153 food of, 128 gallinaceous, 122 grassland, 253, 254, 257 ground, 113, 228 insectivorous, 134-135 migration, 62. 207-211 mixed prairie, 265 nesting, 86, 113 pecking, 85, 127 propagation, 105 scansorial life habit, 129 scratching, 85 seasonal coactions, 127 seed-eating, 127 territoiy, 167, 168, 170 true prairie, 274 waves, 225 Bison, 119, 120. 243. 252. 253. 257. 259. 264, 268, 273, 280, 283, 289, 293 cooperation, 156 European, 119 migration, 201 Bitterling, 143 Bivalves, 54, 230, 334, 338, 339, 340, 341 -annelid community, 230, 244, 323, 340, 345 sphaerid, 306 -worm community, 315, 323, 324, 325, 333, 345, 348 Black-bass, 62, 147 Black bullhead, 300 Black crappic, 301 Black fin, 316 Black game, 197 Blackjack, 279 Black oak, 232 Black-poll warbler, 220 Black rat, 166 Black sucker, 300 Blacktailed jack rabbit, 112, 264 Black-throated blue warbler, 220 Blennies, 326, 331, 336 Bloodworms, 300, 301, 305 Bloomeria, 287 Blowouts, 85 Bluebird, 135 Blue cat, 305 Bluefish, 201 Blue grama, 121 Blue-green algae, 75, 300 Blue jay, 209 Blue racer, 274 Blue violet, 220 Blunt-nosed minnow, 300 Blunt-nosed river carp, 300 Boat-tailed grackle, 280 Bobac or tarbagon, 253 Bobolink, 253, 257 Bobwhite, 127, 175, 242 Bobwhite quail, 154 Bogs, 89, 90, 95, 96 Boletus, 140 Bombus, 275 Bos bonasus, 119 Bosmina longirostris, 301 Botiytis cinerea, 138 Bottom community, 304, 323 Bouteloua, 243 aristidoides, 283 chondrosioides, 282 curtipendula, 256, 270, 278, 282 eriopoda, 282 400 INDEX Bouteloua, gracilis, 121, 243. 256, 261, 271, 282 hirsuta, 256, 271, 278, 282 parry i, 283 radicosa, 282 rothrocki, 282 texana, 278, 279 trifida, 278, 282 Boxelder bug, 63, 65, 183 Brachionus, 301 budapestinensis, 303 havanacnsis, 303 Brachiopods, 330, 332 Brant, 223 Breeding, 46, 47 Breeding areas, 205 Bre\"Oortia-Calanus association, 320 Brevoortia tyrannus, 320 Brewer's sparrow, 265 Brissopsis, 15, 341 -Amphiura association, 344 -Amphiura ecotone, 344 -Amphiura chiajei community, 343 -Amphiura-Ophiura ecotone, 343 lyrifera, 340 lyrifera-Amphiura chiajei community, 340 -Ophiura sarsi community, 343 Brittle stars, 338, 339, 341 Brodiaea, 287 Bromus, 120, 129, 288, 289, 293 carinatus, 287 tectorum, 293 Brown-tail moth, 183 Browsing, 119, 125, 136, 256 Bryozoa, 100, 140 Buchloe, 261, 279 dactyloidcs, 51, 243, 256, 264, 271, 278 Buffalo (fish), red-mouthed, 300 small-mouthed, 305 Buffalo chips, 74 Buffalo grass, 51 Buffalo wallows, 86 Buffalo wolf, 265, 273 Bullsnake, 257, 265, 274 Bimch-grass association, 289 Burgot. 307 Burrowing, 80-84 animals, 69 birds. 82 Burrowing, insects, 82-84 mammals, 80 mayfly nymphs, 300 owl, 82, 265 reptiles, 82 Burrows, 82 Bush tit, 135 Butter clam, 333 Butterflies, 142, 202 Cabbage bug, 65 Cactus, 279 Caddis fly, 98, 308 Calanus, 102, 320, 321 finmarchicus, 319, 320, 321 Calcarius (longspur), 257 Calcium, 101 bicarbonate, 73 carbonate, 97 California ground squirrel, 290 California prairie, 256, 286 Calliostoma costatum, 330 Calls, 154 Calochortus, 287 Cambarus, 308 propinquus, 301 Camel crickets, 285 Campeloma, 300, 301 Canada goose, 209, 220 Cancer, 331 Canis, latrans, 273, 276 mearnsi, 285 nebrascensis, 250, 265, 274 nubilus, 108, 243, 257, 259, 264, 265, 273 ochropus, 289 rufus, 280 Cannibalism, 188 Capparis aphjdla, 205 Caprella, 333 Carabids, 131 Caracara, 133 Carancho, 253 Carbonates, 73, 97 Carbon dioxide, 97 Cardium, californense, 331 corbis, 333 edule, 334, 351 INDEX 401 Carduus, 292 Care of young, 114 Carex, 260 filifolia, 291 filiformis, 252 pennsylvanica, 270, 272 stenophylla, 252, 261 Caribou, 133 migration, 200 tundra, 120 woodland, 123 Carnegiea, 283 Carnivora, 119 Carnivores, 80, 132, 134 Carnivorous habit, 131 Carp, 299. 301, 302, 306 suckers, 302 Carpiodes, difformis, 300 thompsoni, 306 velifer, 300 Carrion, 133 Carj'a buckleyi, 279 Casuarina, 139 Catadromous fishes, 202 Caterpillars, 108, 138 Catfish, 301, 306 channel, 300 Catonotus flabellaris, 308 Catostomus, commersonii, 300, 307 nigricans, 308 Cattle, 125 Ceanothus, 139 Cecropia, 144 Censuses, 196 methods, 355-358 Centrocercus urophasianus, 293 Cephalopods, 319 Ceptocephali, 319 Ceratium hinmdinolla, 301 Cercyonis alope alymus, 275 Cereus giganteus, 110 Chaetoplankton, 14 Chara beds, 307 Chauliodes, 322 rastricomus, 231 Chelydra serpentina, 301 Chenopodium Ipptophyllum, 58 Chestnut blight, 238 Chestnut-collared longspur, 253, 265 Chickadee, 135 Chimney swift, 135, 223, 225 Chinchbug, 130, 181, 182, 187-190, 275 Chipmunks, 126 Chipping sparrow, 220 Chironomidae, 299, 301 Chironomus, 178 bathophilus, 177 plumosus, 300, 305 Chitons, 328 Chlamydomonas, 140 Chlorogalum, 288 Chlorophyceae, 141 Cholera, 108 Chondestes grammacus strigatus, 112 Chortophaga viridifasciata, 267 Chrysemys marginata, 301 Chrysothamnus, 292 Chthamalus dalli, 325, 328 Cicindela, auduboni, 266 denverensis, 267 formosa, 267 formosa generosa, 231, 232 fulgida, 268 lepida, 147, 231 limbalis, 231 obsoleta, 266 pulchra, 266 purpurea graminca, 266 repanda, 267 scutellaris, 267 sexguttata, 231, 276 splendida, 267 succession of, 8 tranquebarica, 267 venusta, 267 Ciliates, 140 Cisco, 307 Citellus, 243, 257 13-lineatus, 274 tereticaudus, 285 Cladocerans, 301 Cladophora glomerata, 308 Clam, 313, 333, 339 beaches, 313 worm, 333 -worm community, 315 Climate, 27, 28, 174, 239 California prairie, 286, 287 coastal prairie, 278 desert plains, 281, 282 402 INDEX Climate, general, 229 grassland, 254-256 limitations, 174 mixed prairie, 262 Palouse prairie, 290, 291 true prairie, 269, 270 types, 233, 234 Climax, 6, 28, 66, 126, 353 beech-maple, 232 lake, 305-307 limits, 29 rivers, 299-305 small river, 300 Climax and sere, 231-232, 229-250 nature and significance, 229-234 climax and climate, 229 life forms, 229-231 tests, 231-233 types, 233, 234 structure, 234-250 characteristics, 239 chmax, 243 comparison, 247, 248 composition of biome, 234 dominance, 235-237 dominants in aquatic communities, 240, 241 dynamic nature, 248-250 dominant, 238, 239 evaluation, 234 influence, 237, 238 kinds of dominants, 238 kinds of influents, 241-243 major units of biome, 243-245 minor units of biome, 245-247 subdominants, 239, 240 Clisere, 248 Closterium acerosum, 303 Clover, 232 Clupea, -Calanus association, 320 sprattus, 320 Clymenella, rubricincta, 339 -Yoldia association, 339 Coactee, 102, 104, 106, 107, 109 plant, 110 Coaction, 68, 103, 102, 104-144, 138, 147, 235, 236, 351 animal coactees, 137, 138 fungi and bacteria, 137, 138 insectivorous plants, 137 Coaction, animals as coactees, 131-136 carnivores, 132-134 insectivorous animals, 134-136 animals as coactors, 116, 117 choice of food, 116, 117 bases, 104-109 consequences, 106, 107 objective, 105, 106 organisms, 104, 105 role, 107-109 browsing life habit, 123-125 defoliation, 123, 125 importance, 125 food, 115, 116 grazing, 108 grazing and browsing, 119 grazing life habit, 119-122 large tramping grazers, 119-120 small grazers resident underground, 121, 122 small surface resident grazers, 122 mixed prairie, 268, 269 nature and significance, 103, 104 pelagic communities, 316 plant coactees, 136, 137 flowering plants, 136 fungi and bacteria, 136, 137 plants as coactees, 117, 118 plants as coactors, 136-138 relations of food, 118, 119 reproductive and social, 114, 115 seed and fruit, 125-131 cambium feeders, 130 dissemination, 129, 130 galls, 130-131 invertebrate omnivorcs, 131 perching birds, 127 scansorial life habit, 129 seasonal in birds, 127 storage by mammals, 126, 127 shelter, 111-114 symbiosis, 138-144 animal symbionts, 143, 144 plant and animal, 140, 141 plant and plant, 138-140 l)ollination symbionts, 141-143 systems, 109-111 Coactor, 104, 21, 106, 107, 109, 110, 116, 117 Coastal prairie, 277 INDEX 403 Coccinellids, 131 Coccobacillus acridiorum, 184 Cockle, 333 Cockroaches, 285 Cod, 199, 201, 336 Codfish, 180, 181, 199 Codling moth, 183 Codominant, 238 Cod plaice, 340 Coclentcratcs, 54, 99 Colaptes, 129 chrysoides, 110 Coleoptera, 130 Colicops, 275 Colinus virginianus, 154 Collembola, 275 Colloidal sulphur, 101, 297, 314 Colony, 154, 246 Columbine, 220 Common mole, 134 Community, 2, 147, 234, 254, 322, 323, 332, 334, 338, 346 Abra, 340 bottom, 304 comparison, land and sea, 247, 248 marine and terrestrial, 352-353 deeper water, 338 development, 353 fresh-water, 294-312 climax, 298 functions, 20, 55-67 aggregation, 57 among animals, 58, 59 among plants, 57, 58 ecesis, in animals, 65 in plants, 63-65 interrelations, 66, 67 related processes, 66 migration, 59 in plants, 60, 61 of animals, 61 types, 61-63 nature and significance, 55-57 general, 2 influence on habitat. 08-102 definition and natiu'e, 68, 69 digging and burrowing, 80-84 kinds, 70 reaction, acids and toxins, 89, 90 accumulating shells, 75 Community, influence on habitat, re- action, adding organic matter, 78, 79 air content, 89 bottom in deep water, 101, 102 cementing particles, 86 climate, 93 COo and O2, 92 decreasing plant nutrients, 88, 89 decreasing water content, 88 disturbing soil, 79 humidity, temperature, and wind, 92 increasing water content, 87, 88 in fresh water, 94-98 in sea, 99-102 in sluggish water, 98 in swift water, 98 in water, 94-102 medium, 97 on land, 71-91 produced by man, 93, 94 returning plant nutrients, 88 role, 70 slipping and sliding, 77, 78 soil, 72 water-borne detritus, 76, 77 weathering, 75, 76 wind-borne material, 75 relation to life forms, 69, 70 soil formation, 72-75 soil structure, 78 surface disturbances, 84-86 North Atlantic, 18, 19, 340-352 North Pacific, 118. 339 Pandora-Yoldia, 315 pelagic, 29, 314-322 sea bottom, 15-19, 322, 353 sea-urchin gastropod, 330 sea-urchin-triton snail, 315 serai, 56 swift-water, 310 tidal, 313, 325, 331-335 tree-top hiemal layer, 246 Venus, 15, 340 Competition, 150, 145, 159-167 animal, 166. 167. 1S5-1S7 nature and kinds. 166, 167 biotic balance, 172-175 404 INDEX Competition, course and outcome, 161 nature and correlation, 159, 160 plant, 162-165, 166, 167 among flowers, 164, 165 between plants and animals, 165 equipment of competitors, 164 factors, 163, 164 nature and kinds, 162, 163 reduction or evasion, 161, 162 similarities and differences, 162 territory, 167-172 among ants, 170-172 among birds, 167, 168 among mammals, 168-170 types of competitors, 160, 161 Complex organism, 22 Condonella crater, 301 Coniferous forest, 12, 20 Conoccphalus fasciatus, 267 Conochiloides natans, 303 Consociation, 244, 245 chaparral, 288 spisula subtruncata, 343 Consocies, 7, 248, 288 Constituent species, 234 Convergence, 231 Convoluta, 140 Cooperation, 150-156 and human communities, 156 in animals, 151, 152 in colony, 154, 155 in family, 152-154 in larger communities, 156 in plant-animal colonies, 155, 156 in plant community, 150, 151 origin and nature, 150 Cooperia, 279 Cooper's hawk, 134 Copepoda, 319 Copepods, 298, 301, 303, 315, 319, 320, 321 Coral communities, 230 Coralline algae, 313 Coral mud, 101 Corals, 25, 34, 52, 53, 313 Coral sand, 101 Corbula, 181, 348 Cordillacris occipitalis occipitalis, 265 Coregonus clupeiformis, 306 Corethra, 305 Corrosion of rock, 75 Corvus, brachyrhynchos, 212 corax sinuatus, 112 Corydalis, 308, 310 Cottontail, 134 Cottonwood, 232 Cougar, 133 Cover, 11, 105, 112, 114, 175 Cowbird, 220 Coyote, 33, 133, 166, 252, 273, 276, 290, 293 Mearn's, 285 Texas, 280 valley, 289 Crabs, 331, 332, 336 shore, 326 Crago alaskensis, 339 Crappie, 188, 301 Crash, 138 Crayfish, 98, 301 Creeper, 134 brown, 135 Crepidulas, 330 Crespidostomum cooperi, 301 Cribrina, 328 xanthogrammica, 325, 328 Cristivomer namaycush, 397 Crossaster papposus, 332 Cross-pollination, 141 Crotalus, confluentus, 265 confluentus oreganus, 290 Crowding, 151, 159 Crows, 212, 215 Crustacea, 321, 326 Crustaceans, 99, 133, 134, 319, 320, 321. 322, 333, 336, 338 Cryptoleon nebulosum, 231, 232 Ctenophores, 315, 321 Cuckoo, 135, 223 Cucumaria, populifera, 339 -Scalibregma association, 339 Cucumber, 330, 331, 339 Cucumber beetle, 275 Culpea, 319 pallasii, 316 Cursorial, 55, 135 Cushion star, 31 Cycadaceae, 139 Cycas, 104 INDEX 405 Cycles, 177, 145, 175-199, 176 among fish, 187, 199 and numbers, 41, 175, 176 animal, 177-180 astronomical, 47 cannibalism, 188 causes, 180-199 competition, 185-187 death, 182, 183 enemies and disease, 183-185 flower, 41, 42 game bird, 196 grouse, 174 in bird numbers, 183, 196, 197 in insect populations, 197-199 in mammal populations, 192-196 irregular fluctuations, 188-190 loss of eggs, 180-182 nature, 177-180 physiological changes, 187-188 qualitative or quantitative failure of food supply, 185 rise to maximum abundance, 190, 191 salmon, 187, 242 sunspot, 28, 191, 192 maximum, 191 minimum, 191 yearly, 242 Cyclops, bicuspidatus, 301, 303 viridis, 303 Cyclothone, 318, 322 -Acanthephyra biome, 318 Cylindrospermum, 139 Cynodon dactylon, 279 Cynomys, gunnisoni, 122 ludovicianus, 81, 259, 285 Dab, 336, 340 long rough, 340 Damsel-fly nymphs, 308 Danthonia, 287 californica, 287, 291 Daphnia longispina, 301 Dasylirion, 283 Death, 182, 183 Deciduous forest, 20 Decline, 182 Decumbent animals, 52 Dedronotus giganteus, 339 Deer, 105, 108, 120, 123, 183, 186, 201, 242 Kaibab, 62, 185, 201 Virginia, 62, 276 Defoliation, 108 Delphinium, 288 Den, 74, 132 Dendroctonus ponderosae, 130 Density of fresh water, 295 Dentition, 132 Desert, 20 Desert horned lark, 265 Desert plains, 256, 281 Desmoplankton, 14 Destroyers, 126 Detritus, 76, 77, 299, 301 Detritus-eaters, 350 Development of community, 309 Diabrotica 12-punctata, 275 Diaptomus, pallidus, 301 siciloides, 301 Diatom, ooze, 101 shells, 102 Diatomaceous soil, 75 Diatoms, 102, 315, 321 Dichasma, 167 Dickcissel, 274 Diet, 127 Digging, 127 of amphibians, 82 of birds, 82 of invertebrates, 82, 83, 84 of mammals, 80 of reptiles, 82 Dinoflagellates, 315 Dipodomys, 243 merriami merriami, 285 nitratoidcs, 290 spectabilis, 74, 113, 283, 284, 285 Diptera, 275 Disclimax, 261, 263, 273, 279, 289 Disease, 174, 183-185 Disoperation, 149, 157-159 in animal communities, 157, 158 in plant communities, 157, 158 nature and scope, 157 Dissemination, by animals, 129, 130 in plants, 42, 59 Disseminules, 34, 44 Dissosteira Carolina, 267 406 INDEX Diurnation, 35 Dobson larvae, 308 Dolichonyx (bobolink), 257 Dominance, 70, 235, 236, 321, 322 Dominant, 238, 302, 321 organisms, 321 Dominants, 238, 239, 29, 99, 238-239, 240, 325, 330, 337, 351, 355 binding, 76, 256, 257 characteristics, 239 in aquatic communities, 240, 241 kinds, 238 of California prairie, 287 of coastal prairie, 278, 279 of desert plains, 282 of lake climaxes, 306, 307 of mixed prairie, 262, 263 of Palouse prairie, 291, 292 of river climaxes, 300 of true prairie, 270-272 Dominule, 238 Dorosoma cepedianum, 300 Douglas squirrel, 126 Doves, 214 Dragnet, 343 Dragonflies, 135 Droppings, 196 Drosophila, 166 Drum, 300 Duckweed, 91, 300, 301 Dynamics, 20 Earthworm, 79, S3, 84, 275 burrows, 82 distribution, 84 Eastern field sparrow, 274 Ecads, 49 Ece, 26 Ecesis, 63, 63-67, 145, 146 in animals, 65 in plants, 63-65 interrelations of community func- tions, 66, 67 related processes, 66 Echard, 79 Echinacea angustifolia, 272 Echinocardium, 341, 350 -Amphiura association, 341, 342, 343 -Axinus biome, 345, 348 Echinocardium, cordatum, 341 -cordatum-Amphiura filiformis, 340 filiformis community, 341 -thyasira biome, 340, 341, 342, 345, 348, 349, 350 -Venus association, 341 Echinoderms, 99, 322, 323, 330, 331, 334, 338 Echinoid, 54 Ecoclines, 232, 233 Ecological succession, 329 Ecology, 30 Ecotone, 28, 233, 260, 322, 341 Abra-Solen — Mya community, 348 Brissopsis-Amphiura, 343 species, 326 Syndosmya, 349 Edaphic communities, 311, 312 Edaphon, 2, 9 Eel, 336, 340 Eel larvae, 319 Eelpout, 339 Eggs, loss of, 180 Elaeagnus, 139 Elk, 120, 123, 133 Elymus, 288, 292 condensatus, 287, 291, 292 glaucus, 287, 291 sitanion, 256, 287, 291 triticoides, 287, 291 Elyonurus, 278 tripsacoides, 278 Emigration, 200 Empusa, 138 Encoptolophus costalis, 265 Endobiose, 18 Endosymbionts, 141 Enemies, 183, 185 Engelmannia, 279 English sparrow, 108 Entomostraca, 55 Ephaptomenon, 50 Ephedra, 283 Epibiose, 18 Epicampps, 287 rigens, 282, 287 Epigeichthj's atropurpureus, 326 Epiphytes, 141 Eragrostis lugens, 282 Ericaceae, 140 INDEX 407 Erigeron ramosus, 272 Erodium, 37, 129, 288 Erogala whipplii, 300 Erythronium albidum, 38 Eschscholtzia, 288 Establishment, 63-67 Estigmene acraea, 117 Estivation, 35 Etheostomidae, 308 Etheostomids, 310 Eudominants, 271, 291 Eudorina elegans, 303 Euglena, acus, 303 viridis, 303 Euiachon, 316 Eumeces obsoletus, 267 Euphausids, 102, 320 Eupogobia, 333, 338 European carp, 301 European herring, 201 Eurytope, 9 Exclosure, 186 Excreta, in sea-bottom deposits, 102 of birds, 73 of insects, 75 of mammals, 73, 74 Extension of range, 63 Fabaceae, 139 Faciation, 247, 328, 100, 244, 327, 331, 332, 334, 336, 339, 348 Faciations, 16 Abra-Solen Association. 348 Balanus, 328 characteristic plants of marine, 100 climax fresh-water, 305 grassland, 243, 244 Buchloe dactyloidcs, 243 Festuca ovina, 243 Hilaria jamesi, 243 Stipa pennata, 243 Haploops, 343, 345 Macoma-Asterias, 336 marine communities, 305 Modiolus, 332 Mya-Cardium-Arenicola, 334, 336 Nucula-Corbula Association, 348 Zostera-Rissoa-Cardium, 336 Failure in population, 180 Falcon, 253 Family, 154, 246 Family dens, 132 Fauna, 323 Feces, 46 Fecundity, 322 Feed, 117 Festuca, 287, 288 idahoensis, 287, 291, 292 occidentalis, 287, 291 o\ina, 243, 256 rubra, 287 Finger-nail shells, 300 Fire, 126 Fisher, 132 Fisher ground squirrel, 290 Fishes, 47, 133, 134, 183, 235, 236, 299, 301, 319, 320, 322, 331 anadromous, 201 bottom-feeding, 98 cannibalism, 188 cycles, 180, 181, 187, 199 dominants, 235, 236, 301, 302 fresh-water, 300, 305 lake, 306, 307 fecundity, 187 fresh-water, 55 fresh-water influents, 300, 301 marine nekton, 316, 317 migration, 201, 202 native, 302 nest-building, 98 pilot, 319 rat-tailed, 332 rock, 331 swift-water communities, 308, 309 white, 306 young, 165 Flatworm, 140 Flexamia, 260 Flicker, 129 Flies, bee, 252 robber, 252, 266, 275, 331 Syrphus, 275 FloatirTg bogs, 96 Flocks of birds, 153 Floodplain, 117 Florideae, 141 Flounder, 333, 336, 340 ^CAi ^. J. 408 INDEX Flourensia, 283 Flowering, 41 Flycatchers, 134 Flying fish, 319 Fontaria corrugatus, 231 Food, 105, 109, 174, 321, 350 birds, 128 chains, 115, 116 choice of, 116-118 coactions, 13, 25 composition, 128 differences, 128 -getting apparatus, 55 nexes, 116 plants, 117, 201 role, 213 supply, 297, 321 Foraminifera, 101, 140, 319 Foraminifera community, 345-348, 349 Forbs, 125 Forest, 11, 20, 172 Form, 69 Formica rufa, 170 Forms of behavior, 55 Fossorial life, 55 Fossorial life habit, 80 Fouquiera, 283 Foxes, 132, 133, 193 gray, 108 kit, 285 red, 195 Fresh-water, see Aquatic Fritillaria, 287 Frogs, 133, 134 Frontonia, 140 Fruit, 126, 133 Fucus, 327 Function, 49 biome, 56 community, 55, 56, 66, 67 Fungous gardens, 155 Fungus, 138 Fur seal, 170 Gadus collaris, 336 Gallinaceous birds, 122 Galls, 130 Game, 183 birds, 104 Game, mammals, 104 needs, 105 Garfish, 201 Gartersnake, 265, 274 Gases, 70, 87 Gastropod, 323, 325, 326, 331, 336 -echinoderm community, 230, 244 Geckos, 285 Geobionts, 9 Geolycosa pikei, 147 Geomys, 243, 257 breviceps sagittalis, 280 bursarius, 274 lutescens, 259 Geosiphon, 139 Germination of plants, 37 Geyserite, 75 Gilbertidia sigolutes, 332 Gilbert's sculpin, 332 Gizzard shad, 300, 305 Gizzard stones, 83 Globicephala scammonii, 316 Globigerina ooze, 101 Glochidia, 143 Glycera, 341 Glycyrhiza lepidota, 272 Gnathophansis, 318 Goats, 120, 125 Goatsuckers, 134 Gobies, 336, 340 Golden plover, 208, 209 Gonads, 211 Goniobasis, 308 Gopher, picket-pin, 253 pocket, 80, 264, 274, 280, 290 Gopher snake, 290 Gooseneck barnacle, 325, 327 Gorgonocephalus euclenis, 332 Grass cover, 112 Grasses, California prairie, 287, 288 coastal prairie, 278-280 desert plains, 282 dominant, 255 mixed prairie, 262, 263 Pulouse prairie, 290-293 proclimax, 263, 264 species, 243 true prairie, 270-273 Grasshopper mice, 264, 285 Grasshopper, migrations, 203 INDEX 409 Grasshopper, outbreaks, 174 years, 198 Grasshoppers, lOS, 132, 199, 204, 252, 267, 274 meadow, 275 Grassland, 251-293 binding dominants, 256, 257 binding influents, 257-260 CaHfornia prairie, 285-290 climate, 286, 287 dominants, 287 influents, 289, 290 nature and extent. 285, 286 proclimaxes, 288 subdominants, 287, 288 climate, 254-256 coastal prairie, 277-280 climate, 278, 279 dominants, 278, 279 influents, 280 nature and extent, 277, 278 proclimaxes, 279, 280 serai stages, 280 subdominants, 279 desert plains, 280-285 climate, 281, 282 dominants, 282 influents, 283-285 nature and extent, 280, 281 proclimaxes, 283 subdominants, 287, 288 introduction, 251, 252 life forms and life habits, 252-254 map, 255 mixed prairie, 260-269 climate, 262 dominants, 262, 203 influents, 264-266 nature and extent, 260-262 proclimaxes, 263, 264 reactions and coactions, 268, 269 river bottoms, 267 sand hills, 267, 268 serai stages, 266, 267 steep banks and ravines, 267 subdominants, 262 Palouse prairie, 290-293 climate, 290, 291 dominants, 291, 292 influents, 293 Grassland, Palouse prairie, nature and extent, 290, 291 proclimaxes, 292, 293 subdominants, 292 jiliysiognomy, 251 structure and unity, 256-260 true prairie, 269-277 climate, 269, 270 contacts, 276, 277 dominants, 270-272 influents, 273-275 nature and extent, 269 proclimaxes, 273 serai stages, 276 subdominants, 272, 273 Gravel bottoms, 311 Gray fox, 108 Gray squirrel, 276 Gray whale, 316 Grazing, 119-125, 238 Grazing coaction, 108 Grazing habit, 120 Great cats, 112 Great Lake trout, 307 Great Lakes, 306, 307 Great Plains, 228, 308 Grebe, 225 Green tiger beetles, 276 Gregarious habit, 115 Ground beetles, 131, 266 Ground birds, 228 Ground squirrels, 265, 274, 289, 293 Grouse, 133 cycle, 174, 197 ruffed, 123 sage, 293 sharptail, 174, 197 Growth, 31, 37 Growth forms, 53, 54 Giubs, 138 Grunt fish, 331 Gunnera, 139 Gutierrezia, 120 Habitat, 26, 27, 329, 338 breeding, 252 choice, 242 relations, 254, 358 stream, 307-311 410 INDEX Haddock, 340 Hake, 201 Halictus, 275 Halophytes, 313 Haploops, 340, 341 community, 343 Haplopappus, 120 Hard bottom, 100 Hardpan, 86, 196 Hare transects, 196 Harlequin, 65 Harlequin cabbage bug, 183 Harmothoe, 334 Harvester ant, 84, 266 nest, 83 Harvest mouse, 265, 280 Haustorium, 139 Haustor lacustris, 306 Hawk, 133, 183, 290 marsh, 73, 134, 220, 265 western red-tailed, 265 Heath sand, 89 Helianthus, 272, 288 grosseserratus, 273 maximiliani, 273 occidentalis, 273 orgyalis, 273 rigidus, 273 Helodrius caliginosus, 231 Hemeranthous bloomers, 41 Hemigrapsis nudis, 326 Hemiptera, 130, 260, 266, 275 Hemi-symbiotic phenomenon, 140 Heptageninae, 308, 310 Herbertia, 279 Herbivores, 133 Herds, bison, 253 mixed, 156 ungulates, 153 Hermit crabs, 328 Herring, 201, 316, 319, 320 European, 201 Heterocene, 9 Heterodon nasicus, 267 Heterogeneity, 55 Hexagenia, 299, 301 Hexagenia nymphs, 305 bilineata, 300 Hibernation, 35 quarters, 62 Hickory, 279 Hilaria, 279 cenchroides, 278, 282 jamesi, 243 mutica, 282 Hii)podamia convergens, 275 Hognosed snake, 267 Hog-sucker, 308 Holard, 79 Holism, 23 Holophyte, 140 Homing, 227 intelligence, 33 pigeons, 227 Homocene, 9 Homoptera, 260 Honey dew, 155 Honey jars, 153 Hooded warbler, 110 Hoppers, 117 Hordeum, 129, 288 nodosum, 287, 291 Hormones, 190 Horned lark, 253 Horned toad, 267 House wren, 135, 213, 214 Housing, 109 Human society, 24 Humidity, 92 Hummingbirds, 142, 143 Hump-back salmon, 316 Hump-back whales, 319 Humus, 87, 294 Hunting, 108 Hunting-pack routes, 132 Huro floridana, 301 Hyaliodes vitripennis, 231, 232 Hyas, 331 Hyborhynchus notatus, 300 Hydnum, 140 Hydra, 104 Hydrobia, 351 Hydroclimate, 294, 295, 314 Hydroclimatic factors, 295-297 density, 295 light, 296 marine, 314, solutes, 296-297 suspended matter, 295-297 temperature, 296 INDEX 411 Hydrogen sulphide, 100, 101, 297, 314 Hydioids, 54, 140, 332 Hjdiopsyche, 308, 310 Hydrosere, 13, 28, 91, 92, 94, 148, 232, 249 Hyla, pickeringii, 231 versicolor, 231 Hynienomycetcs, 140 Hymenoptera, 86, 114, 130, 135, 275 Hyphae, 140 Hypobiose, 18 Hypomosus pretiosus, 316 Hyraces, 119 Icelinus borealis, 331 Ichthyococcus, 319 Ictalums, furcatus, 305 punctatus, 300 Ictiobus, bubalus, 305 urus, 305 Indicators, 351, 352 Infestations, 109 Influence, 237-238 Influents, 241-243, 12, 234, 355 major, 241 minor, 241 prairie, 257, 260 California prairie, 289, 290 desert plains, 283, 285 lake climaxes, 307 mixed prairie, 264-266 Palouse prairie, 293 true prairie, 273-275 Infusoria, 140, 141 Insects, 62, 63. 117, 133, 134, 135, 138, 144, 167 adult, 183 blood-sucking, 159 carnivorous, 135, 136 coastal prairie, 280 cooperation in family, 152-154 cycles, 181-183, 197-199 diseases, 184 fresh-water snbdominants, 300 grassland, 260 homes, 113, 114 larvae, 177 migration, 62, 202-207 mixed prairie, 265-267 Insects, pests, 108 pollination, 142 scale, 155 swift-water communities, 308, 309 true prairie, 274, 275 Instinct, 206 Interaction, 4, 68, 173 Interception, 92 Interrelation of organisms, 103, 104 Invertebrates, 99, 322 Isopods, 333 Jack pine, 232 Jackrabbit, 125, 133, 257, 289 antelope, 285 long-eared, 252 white-tailed, 264 Jaguar, 112 Jellyfishes, 315, 319 Joshua tree, 288 Kaibab deer, 62, 185. 201 Kaibab squirrel, 124. 185 Kangaroo rat, 11, 73, 74, 80. 113, 122, 283, 284, 285, 286, 290 Keratella, 301 Kestrel, 253 Killer whale, 316 Kingbirds, 135, 223 Kinglets, 134, 135 Kit fox, 285 Knysna, 12 Koeleria, 243. 270. 287, 292 crista ta, 256, 270. 278, 287, 291 Lacuna, 333 Lady beetle, 275 Lagopus, 197 Lake carp, 306 Lake climaxes, 305-307 Lake microcosm, 14 Lake sturgeon, 306 Landscape types, 20 Large-mouthed black bass, 301 Lark, 223 horned, 252. 253, 257 desert, 265 412 INDEX Lark, homed, prairie, 274 Texas, 280 meadow, 135, 274 Lark bunting, 252, 253, 265 Lark sparrow, 112, 253 Larrea, 120, 281, 283, 292 desert, 257 tridentata, 244 Larvae, 305, 308 dobson, 308 eel, 319 insect, 177 midge, 306 plumosus, 178 Lasmigonia complanata, 300 Law of minimum, 105 Law of toleration, 105 Layer societies, 245 Lazuli bunting, 265 Lecanium, 141 Leeches, 306 Lemming, 177, 183, 190, 195 Norwegian, 184, 190 Lepidium perfoliatum, 293 Lepidoptera, 275 Leptinotarsa, 117 Leptochloa dubia, 282 Leptosynapta inhaerens, 333 Lepus, 257 alleni, 125, 285 californicus, 125 califomicus californicus, 289 californicus melanotus, 259 richardsonii, 289 Lesions, 184 Leucichthys artedi, 307 Liatris, 272, 279 punctata, 273 scariosa, 273 Lichens, 76, 139, 140 Liebig's law, 105 Life cycles, 45 Life form, 10, 48-55, 76, 229-230, 231, 252-254, 322 bases, 49 behavior and taxonomic, 54, 55 biotic system, 50 concept and significance, 48 kinds, 48, 49 marine, 50 Life form, sedentary, 54 sessile, multiple-individual animals, 50-54 single-individual animals, 54 systems, 49, 50 vermiform, 54 Life habit, 55, 252-254, 312, 323 Life history, 28, 33-48, 172, 351 animals, 44-48 motile, 46-48 parasites, 45, 46 sessile and sedentary animals, 44, 45 definition and significance, 33, 34 physiological, 44 plants, 36-44 community relations, 43, 44 dissemination, 42, 43 flower cycles, 41, 42 fruiting and seed production, 42 germination, 37 growth, 37, 38 movements, 38 number of stages, 36, 37 outline, 36 period of flowering, 41 propagation, 38-40 relation to life form and habitat, 36 reproduction, 40 structure, 40, 41 relation to habitat, 35 sessile and motile organisms, 34, 35 Light, 70, 91, 92 in fresh water, 296 Limnodrilus, 300, 306 Limnology, 16, 17 Limpets, 325, 328, 331 Ling, 307 Litter, 190 Littoral communities, 16 Littorina, 325, 328 Balanus cariosus, 328 Balanus glandula, 328 scutulata, 325, 328 sitchana. 325, 328 Lizards, 133, 134, 135, 285 Lociations, 244 Locies, 248 Locust, 184, 203, 206 lubbery, 274 migrations, 198 INDEX 413 Locust, outbreaks, 198 periodicity, 199 years, 198 Locusta migratoria, 199 Long rough dab, 340 Longspur, 257 chestnut-collared, 253, 265 Smith's, 265 Loon, 223, 225 Lota maculosa, 397 Louisiana vole, 280 Low temperatures, 225 Lugworm, 333 Luidia foliolata, 339 Lupinus, 288, 292 Lycodes brevis, 339 Lycodopsis pacificus, 339 Lyconectes aleutensis, 339 Lynx, 133, 193, 195 rufus, 108 Lysigonium granulatum, 303 Mackerel, 201, 319, 320 Macoma, 332 -Astarte biome, 334, 349 -Asterias, 336 balthica, 334, 348, 351 biome, 341 calcaria community, 334, 345 community, 15, 351 inquinata, 333 -Leptosynapta, 333 -Mya, 333, 334-338, 349, 350 nasuta, 333 -Paphia, 324, 333, 336 secta, 333 Tellina, 336 Macroclinum pomum, 52 Major influents, 241 Major marine communities, 324 Mammalian emigrations, 200 Mammals, 46, 55, 79, 108, 134, 138, 167, 170, 184 age, 187 California prairie, 289, 290 care of young, 114 115 carnivores, 132, 133 competition, 185, 187 coactions, 103 coastal prairie, 280 Mammals, cycles, 177-180, 192-190 desert prairie, 283, 285 enemies and diseases, 183-185 failure in food supply, 185 grassland, 253, 257 grazing, browsing, 119-125 homes, 112, 113 migration, 62, 63 mixed prairie, 264, 265 non-burrowing, 112 Palouse prairie, 293 pawing, 84, 85 storage, 126, 127 territory, 168-170 trampling, 84, 85 true prairie, 274-276 wolves, 132 Man, 93, 94 Manisuris, 278 cylindrica, 278 Manitoba, 12 Man-of-war, 319 Maple, 232 Marcia subdiaphana, 339 Marine biotic communities, 313-353 Amphilepsis-Pecten biome, 345 Argyropelecus-Cauliodus biome, 318, 319 Astarte-Arca biome, 345 Balanus-Littorina biom^?, 325, 326 community development, 329, 330 extent, rank and boundaries, 326- 329 -M. calif ornianus association, 327 -M. edulis association, 327 relationship of associations, 329 subtidal barnacle-gastropod com- munities, 330 bivalve-worm communities, 332 Brissopsis-Amphiura-Ophiura ectone, 343 communities of sea bottom, 322-325 barnacle-gastropod tidal communi- ties, 325 comparison of marine and terrestrial communities, 352-353 Cyclothone-Acanthephyra biome, 318 deep-water communities, 338 ecotone between pelagic and bottom communities, 322 414 INDEX Marine biotic communities, faeiations and lociations, 344 Foraminifera community, 345-348 hydroclimate, 314 introduction, 313, 314 littoral, 324 Myctopum-Salpa biomo, 319 nature of dominance, 349-352 North Atlantic communities, 340-343 Echinocardium-Amphiura associa- tion, 341-343 Echinocardium-Thyasira commun- ity, 340-343 Venus-Echinocardium association, 341 North Pacific communities, 314-317, 339 Pandora- Yoldia biome, 339 Clymcnclla-Yoldia association, 339 Cucumaria-Scalibregma association, 339 pelagic communities, 314-318 enclosed waters, 314-317 North Atlantic, 317, 318 North Pacific, 314-317 coaction and reaction, 316 nekton, 315, 316 physiological characters, 316, 317 plankton, 315, 316 Scomber-Calanus biome, 319, 329 Brevoortia-Calanus association, 320 Clupea-Calanus association, 320 shallow-water communities, 333-338 extent and variations, 336-338 Macoma,-Astarte biome, 334 -Mya biome, 334-336 -Paphia biome, 333 Stronglyocentrotus-Argobuccinum bi- ome, 330, 331 faeiations and relations, 332 -Pteraster association, 331, 332 -Pugettia association, 331 tidal community, 331-332 variations in bivalve-annelid com- munities, 345, 348 Marine life forms, 50 Marine species, 201 Marl, 75, 96 Marmots, 80, 121 Marsh hawk, 220, 265 Marten, 132, 193, 195 Martin, 135, 223, 253, 265 Massasauga, 231, 274, 276 Mayfly nymph, 299, 305 Meadow grasshopper, 275 Meadow lark, 135, 257, 265, 274 Mearn's coyote, 285 Meerkat, 119 Mcgaptera, 319 Megastomatobus cyprinella, 300 Melanophyceae, 331 Melanoplus, 260 atlantis, 203 dawsoni, 275 differentialis, 274, 280 mexicanus, 203, 265 mcxicanus spretus, 266 Melica, 287 harfordi, 287, 291 imperfecta, 287 Menhaden, 320, 321 Mephitis hudsonica, 259 Mermiria neomexicana, 257 Mesquite, 113, 279 Metabolism, 190 Methods ecological investigation, 355- 358 quantitative, 355, 358 Microcosm, 2, 13, 14, 22 Microcystis aeruginosa, 303 Microdactylus, 62 Microplankton, 14, 70 Microscopic algae, 9 Microtus, 112, 185 drummondi, 110 ochrogastcr, 274 Midge, 305 Migration, 59. 60, 61, 190, 200-208, 216, 225, 226 animal, 61 bird, 207-211 Canada goose, 209 diurnal, 62 factors and stimuli, 211-228 aspection, 225, 226 historical, 211, 212 orientation, 226-228 present status, 215-217 regularity of return, 217-222 time of arrival, 222-225 INDEX 415 Migration, fish, 201, 202 general 59-63 insects, 202-207 locust, 198 mammal, 62, 63 metamorphic, 62 plant, 60, 61 research, 212-217 types, 61-63 Mimosa, 283 Minima, 63 Mink, 132, 133, 193 Minnows, 301 Minor influents, 241 Misumena vatia, 165 Mitella, 327, 329 -Mytilus, 328 polymerus, 325, 327, 328 Mixed herds, 156 Mixed prairie, 261 Mnemiopsis, 315 Mobility, 322 Modiolus, 245, 332 modiolus, 245 Moina aiBnis, 301 Mole, 132 common, 134 Texas, 280 Mollusca, 119, 300, 306, 313-353 var., 182 Mollusks, 99, 322, 332, 333 Mongrel buffalo, 305 Moose, 112, 123, 133 Mores, 33, 49 Morphology, 151 Mosses, 76 Motility types, 230 Mound builders, 82 Mound-making ants, 237 Mountain sheep, 133 Mouse, 184, 187 meadow. 111, 274 plagues, 184 pocket, 265, 290 white-footed, 280 Movement, 322 plant, 38 Moxostoma, aureolum, 300 breviceps, 300 Mud-bottomed pools, 308 Mud cat, 305 Mud daubers, 86 Muds, 102 Muhlcnbcrgia, 272 arenicola, 282 cuspidata, 270, 272 emersleyi, 282 monticola, 282 portcri 282 Mulberry, 127 Muillia, 287 Mune, 40, 80 Munus, 49 Musculinum, partumeium, 231 transversum, 300 Mushrooms, 123 Muskox, 114, 120 Muskrat, 133 Mussels, 98, 143, 299, 300, 301, 305, 313, 323, 325 Mustela, nigripes, 259 sp., 259 Mustelids, 107 Mutualism, 140 Mya, arenaria, 334, 248, 351 -Cardium-Arenicola faciation, 334 truncata, 348 Mycorhizas, 140 Myctopum-Salpa biome, 319 Myoxocephalus polyacanthocephalus, 331 Myrica, 139 Myriotrochus rinki, 334 Myrmecodia, 141 Myrtle warbler, 135 Mytilus, 328, 329 californianus, 325, 327, 328, 329 edulis, 325, 327, 329 Nanostoma zonale, 308 Native fishes, 302 Needs of game, 105 Nekton, 314. 316, 321 Neoconocephalus ensiger, 274 Neotoma floridana rubida, 280 Nephthys, 341 ciliata, 334 hombcrgi, 341 Nereis vircns, 333 Neritic subtypes, 15 416 INDEX Nesting, 112 conditions, 105 Nests, 46, 110, 112 Nexe, 115, 116, 238 Niche, 26, 242 Nighthawk, 135 Nitrates, 73 Nitrogren-fixing bacteria, 139 Noddies, 227 Nolina, 283 Northern flicker, 129 Norway lemming, 184, 190 Norway rat, 166 Nostoc, 139 Notostorium, 318 Nucula, 181, 348 -Corbula association, 348 tenuis, 334, 341 Nudibranch, 339 Numbers, 322 bird, 357 Nut, 126 Nutcrackers, 126 Nut weevils, 126 Nyctanthous or night bloomers, 41 Nymphs, mayfly, 299 stonefly, 308 Oak, red, 232 white, 232 Oak-hickory association, 277 Odocoileus virginianus, 108 Oenothera caespitosa, 64 Old age, 187 Oligocottus maculosus, 333 Olneya, 283 Omnivores, 131, 161 Oncorhynchus, gorbuscha, 316 kisutch, 316 nerka, 316 Onychomys, 257 leucogaster articeps, 259 Onuphis conchylega, 334 Ophiocten scriceum, 334 Ophioglypha, 350 Ophiopholis, 350 aculeata var. kennerlyi, 339 Ophiura, 341, 350 Ophiurids, 140, 340, 349 Ophulella pelidna, 280 Opladelus olivaris, 305 Opossum, 62 Opuntia, 279 Orchelimum vulgare, 275 Orchidaceae, 140 Orcinus rectipinna, 316 Oregonia, 331 Organic detritus, 100 Organism, 22 coaction, 104, 105 motile, 34 quasi, 22 real, 22 sedentary, 34 sessile, 34 super, 22 Orphulella pelidna, 267 Orthoptera, 260, 275, 280 Oryzomys palustris texensis, 280 Oryzopsis hymenoides, 291 Ostrea, edulis, 337 lurida, 338 virginica, 338 Otocoris (horned lark), 257 alpestris leucodaema, 259 Otospermophilus, beecheyi, 290 fisheri, 290 grammurus, 290 Otter, 132 Ovenbird, 220 Ovibos moschatus, 114 Owl, 133, 183 short-eared. 190 snowy, 190 Oxbow, 302 Oxygen, 165, 296 Oyster, 6, 313, 333, 337 rock, 330 Pacific blackfin, 316 Paleo-ecology, 4 Palm warbler, 220 Panclimax, 243 Pandalus, 331 Pandora, 332 filosa, 339 -Yoldia biome, 338, 339 Panformation, 243 Panicum, halli, 282 obtusum, 282 INDEX 417 Panicum, scribnerianum, 270 virgatum, 278 Panorpa venosa, 231 Paphia, 332 staminea, 333 Paramecium, 140 Parasite, 45-46, 165 animal, 45 bacterial, 45 external, 45, 46 insect, 46 trematode, 301 types, 45 Parasitism, 143 Parasitoidism, 144 Parkinsonia, 283 Parks, 172 Paspalum plicatulum, 278 Passer domesticus, 213 Pawing, 79, 85 Pecking, 85 Peck order, 161 Pecten groenlandicus community, 345 Pectens, 331, 332 Pectinaria, 181, 334 koreni, 182 Pectinatella, 52 Pelagic, 15 areas, 100-102 climaxes, 18 communities, 29, 314-322 eggs, 35 Pelican, 153-154 Pellet, 134 counts, 74 Pentstemon, 261, 288 Perdominants, 243 Peregrine falcon, 190 Perennial forbs, 261 Peridinia, 315 Period of flowering, 41 Perla, 308, 310 Permeant, 242 Perognathus californicus, 290 Peromyscus, 169 maniculatus artemisiae. 169 maniculatus nebrascensis, 259 Pctalostemon, 279 candidus, 272 purpureus, 272 Petrel, 170 Pewee, 135 Phacoides tenuisculptus, 339 Phenacobius mirabilis, 308 Phenologj^ 35 Phialidium gregarium, 315 Phlibostroma quadrimaculatum, 265 Phlox pilosa, 272 Phocaena phocaena, 316 Phoebe, 86, 135 Phosphorus, 73 Phrynosoma cornutum, 267 Phyllospadix, 25 Phymata erosa fasciata, 275 Physiognomy, 229 grassland, 251 Physiologic orientation, 228 Physiological types, 323 Phytobiocenose, 7 Phytoplankton, 14, 96 Picea engelmanni, 244 Pied-billed grebe, 223 Pigeons, 214, 226 Pilchard, 201 Pilot fish, 319 Pinus, ponderosa, 244 sabiniana, 288 Pioneer family, 247 Pipe fish, 340 Pipit (Anthus), 135, 257 Sprague's, 252 Pisaster ochraceus, 326, 328 Pisidium sp., 300 Pituophis, 257 catenifer, 290 sayi, 265, 274 Plaice, 336 Plains, 120 Plains gartersnake, 265 Plains weasel, 265 Plankton, 14, 91, 301, 307, 314, 321 animals, 91 communities, 315-316 fresh-water, 301 marine, 315, 316 organisms, 303 Plants, 49, 77. 180 active agents, 136-138 aggregations, 57, 58 community relation, 43, 44 418 INDEX Plants, competition, 162-165 consociation, 244 cooperation, 155, 156 cover, 110 disoperation, 157, 158 dominants, 235, 236 ecesis, 63 ecology, 3 flowering, 136 functions, 36-44 fungi, bacteria, 136, 137, 138 grassland, 251-293 importance of shelter, 111 influents, 238 insectivorous, 137 migration, 60, 61 passive members, 117, 118 symbiosis, 138-143 tidal areas, 99, 100 Plethodon cinercus, 231 Pleurobrachia, 315 Pleurococcus, 140 Plover, 208 Plumosus larvae, 178 Pluvialis dominica, 208 Poa, 287, 288 nevadensis, 291 scabrella, 256, 287 scabrella secunda, 291, 292 Pocket mouse, 290 Podocarpus, 139 Pododesmus macroschisma, 330 Pogonomyrmex occidentalis, 83 Pollination, 141-143 Polyarthra, 301 Polychaeta, 334 Polygyra monodon, 231 Polyodon spathula, 305 Polyorchis, 315 Polyponis, 140 Pomoxis sparoides, 301 Pool, community, 301 mud-bottomed, 308 Population, 180, 185, 186 Porpoise, 336 Portlandia, 334 Portuguese man-of-war, 319 Postclimax, 233, 200, 262, 273 Prairie, bunchgrass, 120 California, 285 chicken, 196, 254, 274 Prairie, coastal, 277 gulf, 256 desert, 280 dog, 11, 80, 119, 122, 172, 253, 264, 268, 285 burrows, 81 towns, 122, 237, 253 falcon, 265 horned lark, 274 mixed, 256, 260 mouse, deer, 274 meadow, 274 Palousc, 256, 290, 291 peninsula, 270 sand, 9 rattlesnake, 265 true, 256, 269 Preclimax, 233 Predaceous beetles, 131 Predaceous insects, 135 Prcdation, 330 Predators, 174 Predominance, 351 Predominant influents, 241, 318, 319, 320 Presociety, 246 Prevalence, 330 Prevalent influents, 241 Prey, 316 Primary seres, 232 Primitive man, 131 Procladius, 305 Proclimax, 263, 283 California prairie, 288 coastal prairie, 279, 280 desert prairie, 283 mixed prairie, 263, 264 Palouse prairie, 292, 293 true prairie, 263, 264 Production of eggs, 182 Promachus, 275 Pronghorn, 252 Pronghorn antelope, 120, 264, 273 Propagation, 38, 39 game birds, 105 Propagule, 39 Proptera alata, 300 Prosopis, 279, 283, 292 juliflora, 113 Protoparce quinquemaculatus, 142 Protozoa, 301, 315 Protozoans, 46 INDEX 419 Psettichthys melanostictus, 333 Pseudomonas radicicola, 139 Pseudotsuga mucronata, 244 Psoloessa delicatula, 265 Psolus chitinoides, 330 Psoraloa, argophylla, 272 tenuifloi'a, 247, 272 Pterastcr tesselatus, 331 Pteropods, 319 Purpurea, 326 Purshia, 292 Pyrameis atlanta, 203 cardui, 203 Pyramidula striatella, 231 Quadrats, of droppings, 196 of trapping, 356 Quail, 105, 175, 185 Quantitative methods, 355, 358 Quasi-organism, 22 Quercus marilandica, 279 stellata, 279 Quetico Park, 132 Quill back, 300 Rabbit, 114, 123, 133, 193 common, 125 curve, 177, 179 cycle, 177-180 grassland, 257, 264, 285, 289, 290 population, 187 problem, 125 snowshoe, 112, 192, 194, 195 swamp, 280 Raccoons, 119 Radiolaria, 140, 319 Ranunculus, 288 Raptors, 73, 134 Rat, 108 black, 166 Norway, 166 rice, 280 wood, 72 swamp, 280 Rat-tailed fish, 332 Rattlesnake, 274, 285, 290 Pacific, 290 prairie, 256 retreats of, 285 swamp, 276, 274 Ravens, 112 Reaction, 68, 4, 69-102, 235, 236, 248 air, 91-94 carbon dioxide and oxygen, 92 climate, 93 humidity, temperature and wind, 92 light, 91, 92 produced by man, 93, 94 definition and nature, 68, 69 kinds, 71 land, 71-91 relation to life forms, 69, 70 role, 70-71 soil, 72 accumulation, 72-75 shells and concretions, 75 adding organic matter, 78, 79 air content, 89 compacting particles, 86 decreasing plant nutrients, 88, 89 decreasing water content, 88 digging and burrowing, 80-84 disturbing, 79, 80 formation, 72-75 increasing water content, 87, 88 profile, 90, 91 returning plant nutrients, 88 slipping and sliding, 77, 78 surface disturbances, 84-86 terms of acids and toxins, 89, 90 water-borne detritus, 76, 77 weathering, 75, 76 wind-borne material, 76 water, 94-102 fresh, 94, 95-98 pelagic and deep benthic areas, 100, 102 bottom in deep water, 101, 102 medium, 100, 101 sea, 99-102 small lakes and ponds, 95-97 accumulation and decomposition, 95, 96 medium, 96, 97 streams, 97, 98 sluggish-water, 98 swift-water, 98 tidal areas, 99, 100 belt between mean high and low tide, 99 littoral benthic belt, 99-100 420 INDEX Real organisms, 22 Reciprocal, 153 Reciprocal parasitism, 143 Red devil, 339 Red fox, 195 Red horse, 300 Red oaks, 232 Red Sea anemone, 328 Regurgitation, 153 Reithrodontomys megalotis dychei 259 Reproduction, 109, 151 plant, 40 Reptiles, 25, 62, 72, 82, 265, 267, 268, 274, 290 California prairie, 290 carnivores, 133 desert plains, 285 fresh-water influents, 301 grassland, 257, 258 migration, 62 mixed prairie, 265, 267 true prairie, 274 Rhachianectes glaucus, 316 Rhamphocottus richardsoni, 331 Rhea, 253 Rheotactic characteristic, 310 Rhizomes, 76 Rhizumenon, 50 Rhodeus, 143 Rhythmic migrants, 326 Richardson ground squirrel, 253, 264 Right whale, 320 River carp, 300 River climaxes, 299-305 development, 303-305 Roa, 340 Road runner, 134 Robber flies, 266, 275 Rock fishes, 331 Rock oyster, 330 Rodents, 78 Role, 49 Rookeries, 62 Rooting, 84, 85 swine, 79 Roots, 76 Root systems, 87 Rose beetle, 62 Rose star, 332 Rotifers, 315 Routes of wolves, 115 Ruffed grouse, 123 Ruppia maritima, 25 Rutaceae, 140 Rutting, 47, 48 Sage grouse, 293 Sagitta, 315, 319, 321 elegans, 320 Salmon, 62, 199, 320, 340 cycle, 187 hump-back, 316 silver, 316 sockeye, 316 Salmo trutta, 320 Salsola, 120 Salt-marsh caterpillars, 117 Salvia, 279, 288 pitched, 273 Sand bottoms, 308, 311 Sandhill crane, 223 Sand turtle, 268 Saprobes, 165 Saprolegnia, 138 Sapsucker, 129, 220 Sarsia, 315 Scale insects, 155 Scalibregma, 339 inflatum, 339 Scalopus aquaticus texanus, 280 Scaphirhj^nchus platorhynchus, 305 Scatology, 106 Scenedesmus, 140 Schistocerca gregaria, 205, 206 Sciurus kaibabensis, 124 Scleropogon brevifolius, 282 Scolopax, 197 Scomber, -Calanus biome, 319, 320 scombrus, 319, 320 Scombresox, 319 Scopelid, 319 Scratching, 85 Scudderia texensis, 280 Sculpin, 331, 333 Sea anemone, 327 Sea cucumber, 330 Sea scoi"pion, 336 Seasonal sequence, 45 INDEX 421 Seasonal variation, 177 Sea urchin, 330, 340 Seaweeds, 238 Sebastodes, 331 Sedentary, 61, 322 constituents, 335 organisms, 34 Seed, crop, 126, 180 -eating birds, 127 Seeds and fruits, 118 Serai-pools with gravel bottoms, 308 Senecio aureus, 272 Sense of direction, 227 Serai, 12 communities, 27, 247 stages, 231, 232, 260-286, 312 coastal prairie, 280 mixed prairie, 266, 267 true prairie, 276 Sere, 6, 27, 56, 229-250 Serpulid, 54, 100 worms, 54 Serrivomer, 318 Serule, 238 Sessile, 61, 322 animals, 53 organisms, 34 plants, 53 Setaria macrostachya, 282 Settlement, 108 effect, 108 Shad, 300, 305 Shadbush, 232 Sharks, 201 Sharp-tailed grouse, 174, 197 Sheep, 120 Sheepshead, 300, 306 Shelled animals, 101 Shells, 75, 100 Shelter, 11, 109, 112, 119 Shifting sand-bottomed pools, 308 Shore crab, 326 Short-eared owl, 190 Short-grass disclimax, 261 Short-grass plains, 120 Short-headed red horse, 300 Shrew, 132 Shrimp, 319, 320, 331, 332 Siberian nutcracker, 196 Sidalcea, 288 Silphium, 272, 279 Sinter, 75 Siraplankton, 14 Sistrurus, catenatus, 231, 274 Sisymbrium altissimum, 293 Sisyrinchium bcllum, 287 Skeletons, 73 Skink, 267 Skuas, 190 Skunk, 132, 193, 265 common, 133 hog-nosed, 132 spotted, 280 Slumping, 7, 78 Small-mouthed buffalo, 305 Small-river climax, 300 Smith's longspur, 253, 265 Snail, 54, 98, 275, 300, 306, 308, 328, 330, 331, 333, 336, 339 Snakes, 133, 265, 274 blue racer, 274 bull, 257, 290 crotalid, 107, 231, 274, 276, 285, 290 garter, 256, 274 gopher, 290 hog-nosed, 267 Snapping turtle, 301 Snowshoe rabbit, 112, 192, 194 Snowy owl, 190 Social community, 6 Social grouping, 109 Social hunting, 132 Social life, 206 Social organization, 131, 132 Socies, 240 Society, 245, 148 human, 24 layers, 245-246 seasonal, 240 Soil, 78, 84 profile, 90, 91 structure, 78 water, 87 Solanum, rostratum, 117 tuberosum, 117 Solen, 181. 348 pellucidus, 182 Solidago, 288, 292 nemoralis, 273 422 INDEX Solidago, rigida, 273 speciosa, 272 Solutes, 87 mineral, 101 Soodland caribou, 62 Sooties, 227 Sparrow, Ammodramus (grasshopper), 257 chipping, 220 eastern field, 274 English, 108, 213 lark, 112, 252, 253 migration, 213 song, 169 Spartina, patens, 280 spartinae, 280 Spatangoidea, 340, 341 Spatangus, 341 Species, omnivorous, 132 secondary, 234, 300 Sperm-whales, 319 Sphaerid, 299, 301, 305 bivalves, 306 Sphaerium striatinum, 300 Sphagnum, 87, 95, 139 Spharagemon equale, 265 Sphenodon, 170 Sphinx moth, 142 Sphyrapicus, 129 Spiders, 135 Spilogale interrupta, 259 Spisula, 245 subtruncata, 244, 341, 348 subtruncata consociation, 343 Sponge, 53, 140 Spoon-bill cat, 305 Sporobolus, 243 airoides, 257, 282 asper, 270, 272, 278 berteroanus, 278 cryptandrus, 243, 256, 262, 282 cryptandrus contractus, 282 cryptandrus flexuosus, 282 cryptandrus giganteus, 282 heterolepis, 270 virginicus, 280 Sporotrichum globulifcrum, 138 Sprague's pipit, 252, 253, 265 Sprat, 320 Spruce partridge, 123 Squids, 322 Squirrel, 122, 125, 126 Abert, 126 Douglas, 126 flying, 126 fox, 113 gray, 113, 276 California, 126 ground, 274, 285, 289, 293 fisher, 290 Kaibab, 124 red, 123, 168 Starfish, 230, 326, 330, 331, 336, 338, 339, 340 Starling, 65, 227 Steel-colored minnow, 300 Stenotope, 9 -heterocene, 9 -homocene, 9 Stentor, 104, 140 Sternaspis, 339 Stichopus californicus, 331 Stipa, 37, 129, 243 -Antilocapra biome, 251-293 comata, 243, 256, 261, 262, 290, 291, 292 coronata, 287 lepida, 287 leucotricha, 278 occidentalis, 291, 292 occidentalis elmeri, 291 occidentalis thurberiana, 291 pennata, 243, 262 pulchra, 244, 287, 288 spartea, 270, 272 speciosa, 287, 288 viridula, 256, 262, 291 Stomach contents, 125 Stomias, 322 Stomiasoa, 319 Stomotoca, 315 Storks, 227-228 Stream, 97, 98, 311 dominants, 309-310 habitat, 307-311 small unstable, 311 Strongyloccntrotus, -Argobuccinum biome, 245, 315, 324, 330-332 drobachiensis, 330 franciscanus, 330, 331 INDEX 423 Strongylocentrotus, -Pteraster associa- tion, 331, 332 -Pugettia association, 331 Structural adaptations, 32 Structure, 55 animal, 55 biome, 55 plant, 40 Sturgeon, lake, 306 shovel-nosed, 305 Sturnella (meadow lark), 257 neglecta, 259 Sturnus vulgaris, 227 Styliplankton, 14 Subclimates, 243 Subclimax, 16 Subdominants, 234. 239, 300, 355 California prairie, 287, 288 coastal prairie, 279 desert plains, 283 lake climaxes, 306 mixed prairie, 262 Palouse prairie, 292 river climaxes, 300 true prairie, 272, 273 Subinfluents, 234, 241, 249 Subseres, 232 Substages, 232 Subtidal communities, 313 Subtidal type, 325 Succession, 4. 56, 61, 66, 70. 126, 329, 330, 353 Successional development, 231, 304 Succinea ovalis, 231 Sucker, 159, 301. 307 Sucker-mouthed minnow. 308 Sucking habit, 300 Sulphur, bacteria, 101 compounds, 314 dioxide, 297 Sulphurous acid, 101, 314 Sumac, 127 Sunspot, cycle, 28, 191, 192. 194 numbers, 222 relation to migration, 222-225 years, 194 Superdominant. 148 Superorganism, 22 Surface layers, 319 Surf smelt, 316 Swallows, 86, 134, 223 barn, 135 cliff, 135 Swamp rabbit, 280 Swamp rattlesnake, 276 Swamp wood rat, 280 Swamps, 112 Swifts, 134 Swift-water community, 310 Swine rooting, 79, 85 Sword bearer, 274 Sylvilagus aquaticus littoralis, 289 Symbiosis, 138-144 Sj'mbiotic relation, 155 Symbiotic trophism, 144 Symphiles, 154 Synchaeta, 301 pectinata, 303 stylata, 303 Syndosmya, 336 alba (abra), 341 community, 340 ecotone, 349 nitida, 341 -Solen association, 348 -Solen-Mya association, 349 Synecology, 1 Syrphus flies, 275 Tanager, 143, 210 Tanganyika, 12 Tarpon, 201 Taxidea, taxus, 243, 257, 259 taxus berlandieri, 285 taxus neglecta, 289 Teaching in mammals, 33 Techniques, ecological, 355-35S Teeth, mammal, 187 Tellina fabula, 341 Temperature, 92 fresh-water, 296 rutting and, 47-48 Tenebrionidae, 266 Termites, 152, 155 Terrapene ornata, 268 Terrestrial plants, 302 Terrigenous bottom, 298 Territorial limits, 171 Territory, 167-172 ant, 170-172 424 INDEX Territory, bird, 168, 169, 170, 176 home, 170 hunting, 170 mammal, 168-170 neutral, 170 song-sparrow, 169 Tetragnatha laboriosa, 231 Tetrao, 197 Texas coyote, 280 Texas horned lark, 280 Texas mole, 280 Texas wolf, 280 Thais, 326 emarginata, 328 Thaleichthj's pacificus, 316 Thamnophis radix, 265, 274 Thaumantias, cellularia, 315 Thermocline, 297 Thistles, 129 Thomomys, 257 bottae, 290 Thyrasira flexuosa, 340 Thysabiessa, 320 Thysanoessa, 320 Thysanura, 275 Tidal, areas, 99, 100 belts, between high and low, 99 littoral benthif. 99. 100 communities, 313, 325, 331, 332, 333- 358 Tide pool, 328 Tiger beetle, 232, 266, 267, 268 Timber rattler, 276 Tintinnidium fluviatile, 303 Tintinnids, 315 Toad, horned, 267 Toleration, law, 105 Toxins, 89, 90 Toxoplasma, 185 Trachelomonas volvocina, 303 Trachypogon, 278 montufari, 278 Tradcscantia virginiana, 272 Tramping grazers, 119 Trampling, 79, 85 Transpiration, 88 Trapping, 196 animals, 357 mice, 356 Tree rings, 192 Tree trunks, 114 Tribolium, 166 Trichachne californica, 282 Trichoplankton, 14 Trichotropis cancellata, 330 Trimerotropis, 260 pallidipennis, 267 Triodia, mutica, 282 pilosa, 278, 282 pulchella, 282 Triposplankton, 14 Tripscum, 51 Troglodytes, aedon, 213 Trophallaxis, 153, 154 Trophobionts, 154 Tropism, 147, 151 Trout, 159, 307 Trumpet vine, 127 Tsetse fly, 12 Tularemia, 187 Tundra, 20, 95, 96 Tunicate?, 313, 319 Tunnels, 114 Tunny, 201 Turbidity, 70, 98, 235, 236, 302 Turritella, 341 Turtle, box, 267, 268 painted, 301 sand, 268 snapping, 301 Twig borers, 109 Tympanuchus, cupido americanus, 259, 274 Unbalance, 173 Ungulates, 74, 153 Unio, 143 Usnea, 140 Utricularia, 165 Valenciennellus, 319 Valvata, 306 Variation, 177 Varying hare, 195 Vedominants, 238 Veinfluents, 241, 249 Venus, -Echinocardium association, 341, 342, 343, 349 gallina, 341 Verbascum thapsus, 52 INDEX 425 Vernonia, 272 fasciculata, 273 Viola, 288 pedata, 272 pedatifida, 272 Virco, 134 yellow-throated, 135 Viscacha, 80, 253 Visibility, 253 Vitamins, 190, 211 Viviparous animals, 46 Viviparous perch, 316 Vole, 195 Louisiana, 280 Vorticella, 140 Vulpes, macrotis neomexicana, 285 velox, 259 velox velox, 265 Vultures, 133 Wallowing, 79 Warbler, black-poll, 220 black-throated blue, 220 hooded, 110 myrtle, 135 palm, 220 wood, 134 Warnings, 153 Wasps, 267 ^ Water, 62 lilies, 107 reaction, 94-102 decreasing content, 88 increasing content, 87 Weasel, 132, 133, 253, 265 Weathering. 75, 76 Weevils, .126 Whales, 319, 320 baleen, 107 blackfin, 316 gray, 316 hump-back, 319 killer, 316 right, 320 sperm, 319 Wheat rust, 108 Whelks, 330 White fish, 306 Whiting, 343 W^ildcat, 108 Wilsonia citrina, 110 Wind, 92 Wingless cockroaches, 285 Winter bodies, 34 Wolf, 33. 108. 112, 114, 132, 166, 193, 252, 285, 298, 293 bufTalo, 257, 264, 265, 273, 274, 280 gray, 133 pack, 107, 115 Texas, 280 Wolverine, 133, 193 Woodchucks, 133 Woodcocks, 197 Woodland caribous, 62, 123 Woodpeckers. 126. 135 California. 129 Lewis, 129 Mexican, 126 Wood pewee, 135 Wood rat, 73 Worm, 230, 300, 306, 334, 339 serpulid, 54 Wren, 134 house, 135 Wyethia, 292 Xerosere, 249 Xiphister mucosus, 326 Yellow adder's tongue, 220 Yellow-bellied sapsucker, 220 Yellow-green algae, 75 Yoldia, 332 hyperborea. 334 limatula. 339 scissurata, 331 Yucca, 283, 288 brevifolia, 288 Zoobiocenose, 7 Zoocenose, 6 Zoochlorella, 140 Zooids, 52 Zoophytes, 34, 52 Zootope, 7 Zooxanthclla, 140 Zostera, 25, 336, 350 -Rissoa-Cardium faciation, 336 Zygadenus, 287