DEVELOPMENTAL PHASES OF THE BIOCOENOSIS* BY CLYDE E. GOULDEN ACADEMY OF NATURAL SCIENCES OF PHILADELPHIA AND UNIVERSITY OF PENNSYLVANIA Communicated by G. Evelyn Hutchinson, January 31, 1969 Abstract.-Species number and diversity increase log-linearly with time during the early development of a biocoenosis. This period may be divided into three phases. In the first phase, diversity increases with the rapid immigration of species into the newly established habitat. In the second phase, diversity in- creases as common species become less common and rare species less rare. This period ends with the attainment of a maximum diversity pattern. In the third phase, rare species continue to invade the habitat until it is saturated. In each phase there is a maximal number of species that can invade the habitat. There are three aspects of species diversity: (1) number of species, S; (2) their relative abundances, commonly designated as H in the most-often-used diversity index; and (3) the pattern of relative abundances of all species. The second aspect is generally measured by the Shannon-Wiener information theory equation, H = - Xpi log Pi. The pattern of relative abundances for a taxocene (a set of closely related species) varies for different groups of organisms, changing with the maturity of the association under study as shown below, and is probably related to the number of competing species composing the taxocene. We are concerned here with a description of the historical changes in species number and diversity characteristic of early developmental stages of the biocoen- Os's. The organisms considered here are all members of the Family Chydoridae (Order Cladocera, Class Crustacea). The species are found concentrated in weed beds in the littoral zone of lakes. All appear to feed on plant detritus, algae, and bacteria. Our initial studies indicate that the species have substrate preferences. All species produce recognizable chitinous exuviae that are pre- served in lake sediments. A single sample of surface sediment can be used to identify the entire chydorid fauna of a lake,1 and samples from a single sediment core suffice to describe for a given lake age the relative abundances of the micro- fossil population.2 We have shown elsewhere that the pattern of relative abundances of fossil chydorid populations that represent stable, mature periods of a lake's history tends to conform with predicted values from the MacArthur Type 1 distribu- tion3-5 (the fact that it fits this particular model is unimportant-any biological model will suffice for the present discussion). t Chydorid populations represent- ing the early stages of development of the lake biocoenosis tend to be poor fits to the Type 1 distribution, with successively better fits as the habitat "matures." This trend has now been found for five lakes: Aguada de Santa Ana Vieja, Guatemala ;5 Lago di Monterosi, Italy ;6 Esthwaite Water, England ;3 Lake Lacawac, Pennsylvania; and Lake Nojiri, Japan.7 1066 Downloaded by guest on September 29, 2021 VOL. 62, 1969 ZOOLOGY: C. E. GOULDEN 1067 After attainment of a good fit to the Type 1, additional species may be added- thus further increasing diversity-but the basic pattern of relative abundances remains the same. There appears to be an upper limit or asymptotic number of species, so that diversity H tends toward an asymptote. This can best be seen in Esthwaite Water, England, in which the association of chydorids remained essentially constant over the last 4000 years of the lake's history.8 However, if the environment is disturbed significantly, there is an immediate decrease in diversity and usually in number of species, with an accompanying poorer fit to the Type 1 distribution.5' 7 9 When this occurs, one species becomes superabundant while the other species become rather rare. As long as the dis- turbance persists, the number of species and diversity H will remain low. But at its cessation, assuming that the habitat is not totally destroyed, diversity and the number of species will again increase as in the early stages of biocoenosis develop- ment. so~~~~~~~~~_ 2.0 +1.0~~~~~~ f~~~~~~ FIG. 1.-Changes in species S _ number S and diversity H with H 0 regression line for chydorid Cla- docera in sediment core from the Aguada de Santa Ana Vieja, 0 l l l Guatemala. DC". I0 20 DEPTH To illustrate and describe the changes occurring during the early stages of biocoenosis development, I have plotted the logarithm of number of species S and of diversity H against sediment depth (Figs. 1 and 2); sediment depth was mea- sured in centimeters from the bottommost sample in which reliable population sizes were encountered. The increases in both species numbers and diversity appear to be almost log-linear, and in fact give significant linear regressions, as measured by the F test. It is apparent that the points do not form a straight line if connected and are more convex curvilinear. Part of the explanation for this is that an error is in- troduced in the time scale used, which in this case is sediment levels. Without an absolute dating scale we must assume that the sedimentation rate is constant. This is a weak assumption. We do have an almost absolute time scale based on Downloaded by guest on September 29, 2021 1068 ZOOLOGY: C. E. GOULDEN PRoc. N. A. S. 0 +3.0 .* 0 0 * 0 +2.5 t- 0 S *2.0F 0 +1.5 I *1.0 0 20 40 60 +1.0 0 __-- ~~~~~2-- & .':~~~~~~~~~ :- - O h H 6 0 -.5 - -I.0 0 20 40 60 DEPTH FIG. 2.-Changes in species number S and diversity H for chydorid Cladocera in sediment core from Lake Lacawac, Pennsylvania. Solid line represents linear regression for all points; dashed line, linear regression for points above 30 cm; dotted line, esti- mated regression for points below 5 cm. closely spaced radiocarbon dates for Lago di Monterosi, Italy (Fig. 3), and have compared the increase in diversity during and following a period of Roman dis- turbance of the drainage basin with both the sediment-level time scale and the absolute time scale. The regression of diversity on time is slightly more signif- icant (with a higher F-test value) than that of diversity on sediment depth. Since this is a semilogarithmic plot, we would conclude that both species num- ber and diversity increase exponentially, but tend toward an asymptote. If we assume diversity and species number to be in equilibrium with the environment, then these changes must reflect structural changes in the environment probably associated with decreasing unpredictability of the environment.10 One more point can be added to Figures 1 and 2, a point representing the earli- est of lake development, just before animals migrated into the newly formed lake. Downloaded by guest on September 29, 2021 VOL. 62, 1969 ZOOLOGY: C. E. GOULDEN 1069 +1.0 H *50 O YR& 50000 TIME to.0 FIG. 3.-Changes in diversity H .50 H for chydorid Cladocera with sediment depth and time (see text for explanation) in Lago di __ __ __ __ __ _ Monterosi, Italy. 0 cs 20 DEPTH This point would be to the left of zero on the abscissa, since the zero represents the first point where microfossils were encountered in sufficiently large numbers to be counted. In Figure 2 we have added a dotted line on the left, a suggested re- gression line, that could be extrapolated back to the time when the lake lacked a cladoceran fauna. We have added a dashed line that represents the linear re- gression for diversity H and species number S values minus the initial set of points. These two "regression" lines (as given in Fig. 2) describe the data much better than would a single line since they suggest that there are in fact two phases of biocoenosis development and that both are probably exponential.t The first phase is associated with the immigration of species into the newly formed habitat. The increase in species occurred very rapidly, so rapidly that our techniques are not sensitive enough to measure it. This increase may be exponential, which would correspond with the suggestion by MacArthur and Wilson" that immigra- tion onto islands occurs at an exponential rate. The second phase, as indicated in Figures 1, 2, and 3, has a more gradual slope covering a much longer period of time and is not associated with as significant an increase in species numbers. The increase in diversity results not only from an increase in species numbers but also from the rearrangement of the relative abundance of species in which the common species become less common and the rare species less rare. This should lead to the ultimate, most equitable division of the environment wherein all species are equally common; however, this rarely, if ever, occurs in nature. Instead, as mentioned above, the relative abundance of species in this case attains a pattern similar to that described in MacArthur's Type 1 distribution or similar models suggested by Cohen.'2 This pattern appears to represent the "most equitable" diversity of resources that can occur in nature.'3 We can see this more clearly in Figure 4. Here we have put together all data for species number and diversity available from our own studies and from one study by Frey'4 on Schleinsee, Germany, from which the data could readily be obtained. Essentially all the points in Figure 4 are concentrated between two Downloaded by guest on September 29, 2021 1070 ZOOLOGY: C. E. GOULDEN PRoc. N. A. S. 30 r / I/ / II //I// I / ~~~~~~~~~~~// / ~~~~~~~~~~~~~// / ~~~~~~~~~~~// / ~~~~~~~~~// 20 /~~~~~+ +0 A.. S / a~~~xx .O0^ x x x x OX 0+3+ A +A /xXXXX X XX oX 0o/ X ~~~~~~~~~~//0 tx xx xx x 0 XX XX oXX 0 0 0 0++0e, 10 _ yX X ~~XX X 00 X 0 'ow xxxxox A at + ESTHWAITE WATER, EINLAI,ND 0 x OX Xo + A 0a LAGO DI MONTEROSI, ITALY /xxx ax XX% LAKE LACAWAC, PENN., U.S.,A.