Specificity and Behavior in Symbioses

INTRODUCTION S ince earliest imes naturalists have been intrigued with the intimate and so often highly specific associations between species which we speak of as symbioses. They have asked: "What factors bring symbiotic organisms together?" and "How are they maintained in partnership?" Yet until recently few efforts to answer these questions have been made. It has, of course, long been recognized that separate disciplines within a science progress historically in a remarkably parallel way. We are all familiar with the more or less orderly progression: "taxonomy-morphology-physiology-behavior" in the development of so many of the Life Sciences. The study of animal associations appears to be now in somewhat the same state as such a science as entomology was at the beginning of this century. At that time a great body of literature had appeared on the taxonomy and morphology of insects, while the study of behavior based on a knowledge of physiology was in its infancy. So far, as one might perhaps expect, our most noteworthy advances in the study of associations have been made in the investigation of truly social organisms. In our study of insect societies we have passed through the great, but in the main descriptive, work of such men as Fabre, Forel, and William Morton Wheeler, to the dramatic experimental contributions of Karl von Frisch. As a result of these observations and the continuing ones of Schneirla and others, we have today an extensive knowledge of the integrative factors, both physiological and behavioral, which knit together the "organs" and "cells" of the hymenopterous society. Likewise our understanding of the mechanisms controlling vertebrate social behavior is at present rapidly increasing as a result of the investigations of Konrad Lorenz, N. Tinbergen, and their colleagues in Europe. The same cannot be said of our understanding of symbioses; we are at the present time in the formative years of the investigation of the mechanisms of control of these partnerships. As Maurice Caullery in his classic Parasitism and Symbiosis (1952) has so clearly seen: "The question is really one of analyzing by precise experiments the relations of [the partners] ... and of careful comparison of their behavior in an isolated state and in association." It is the primary aim of this review to point out the number of fascinating problems that confront us in the investigation of behavior in symbioses, as well as to show that most of these problems, with the passage of time, can undoubtedly be solved by careful experimentation. As will be seen, one can often, by the use of relatively simple techniques, precisely identify in symbionts those stimnli which control adaptive behavior serving to bring the partners together or to maintain them in partnership. Throughout, we shall direct our attention to that behavior of symbionts which is directly related to their unique habit; such behavior must be absent in their free-living relatives. In what is to foflow, a number of very different types of associations will fall under discussion. With no intention whatever of being all-inclusive, these have been selected primarily to illustrate how a careful analysis of the adaptive behavior of their members may further elucidate not only the