BIRD SPECIES DIVERSITY: COMPONENTS OF SHANNON'S FORMULA

ELLIOT J. TRAMER*
Department of Biology, Princeton University, Princeton, New Jersey
(Accepted for publication May 28, 1969)

Abstract. Shannon's diversity index H' = ~^pi Iog2 pt was calculated for 267 breeding bird
censuses. The index was resolved into its components, species richness and relative' abundance,
to determine which components played a larger role in the determination of diversity patterns.
Changes in diversity were correlated closely with species richness (r = 0.972), while the-
relative abundance component remained stable. Among the nine community types represented,
diversity and species richness increased with the foliage height diversity. The relative abun-
dance component was strikingly low in the marshes due to the presence of gregarious birds
which nest in colonies and feed outside the community. Photoplankton differ from birds in
that the relative abundance component is not stable from one collection to the next. This
is attributed to differences in the environmental uncertainty encountered by the two groups,
plankton inhabiting relatively uncertain environments and being "opportunistic," while birds
occupy predictable environments and are therefore "equilibrium" species. The distribution
of relative abundances in birds is more even than in trees, herbaceous-shrub communities, or
phytoplankton. Since this is in part the result of intraspecific terriloriality, it is predicted
that in nonbreeding bird populations, species' relative abundances will be less even than they
are during the breeding season. It is suggested that the regulation of diversity by either the
species richness or relative abundance components represent alternative strategies which are
suited to predictable/nonrigorous and unpredictable/rigorous environments, respectively. There-
fore, differences similar to those observed between birds and phytoplankton might be expected
in other groups of organisms.

INTRODUCTION The purpose of this paper is to present evidence that

To describe species diversity in natural communities, in breeding bird populations diversity patterns are strongly
ecologists have made widespread use of Shannon's func- correlated with variation in the species richness com-
tion (Shannon and Weaver 1963). This expression is ponent, the relative abundance component being relatively
stable. Furthermore, it will be shown that in most com-
munities the distribution of species abundances in breed-
H'=- (1) ing bird populations is unusually even. Some ecological
implications of these findings are discussed, particularly
where pi is the proportion of individuals in the ith spe- regarding the relative effects of the two components on
cies (i = 1, 2, ...,S). Lloyd and Ghelardi (1S64) have diversity patterns in various types of organisms.
pointed out that this measure has two separate com-
ponents, species richness and the "equitability" or "even- PROCEDURES
ness" of species abundances. Species richness is simply
5", the number of species in the sample. Several expres- Most of the 267 breeding bird censuses used in this
sions have been employed to measure the relative abun- study were taken from Audubon Field Notes (1937-1966;
dance component: here we will use the index formerly 'Bird Lore and Audubon Magazine). Other
/' = #'/#'„„ (2) sources were Odum (1950), Johnston and Odum (1956),
Cody (1966), MacArthur, Rechcr, and Cody (1966), and
in which H'max is Iog2 $• This index represents the seven censuses conducted by the author on forested moun-
ratio of the observed diversity to the maximum diversity tain watersheds .at the Coweeta Hydrologic Laboratory
possible for the same number of species. It has a max- near Franklin, N. C. The data included here represent only
imum value of unity when all species arc equally abun- a fraction of the total number of censuses reported in
dant, while the minimum value is denned by the situation Audubon Field Notes. This is because many of the
in which all species save the most abundant are repre- censuses in that journal are of heterogeneous vegetation
sented by only one individual; the more individuals in stands or of tracts containing more than one habitat;
the sample, the closer y' mill approaches zero. homogeneity of vegetation structure was the primary
Since the components of the Shannon formula can vary criterion applied in the selection of censuses for use here.
independently of one another it is obvious that two sam- In addition, tracts censused in more than one year were
ples having identical H' values may in fact be very dif- used only the first time they appeared in the journal.
ferent. Therefore, I resolve the formula into its com- Complete lists of the censuses used are available from
ponents when analyzing diversity patterns. the author.
1
Present address: Department of Biology, The Univer- Values of H' and /' were determined for each census
sity of Toledo, Toledo, Ohio 43606. and a regression of H' against the logarithm of the num-
928 REPORTS Ecology, Vol. 50, No. 5
DISCUSSION
An obvious consequence of the results is that in a
given community, breeding bird diversity can be ade-
quately described by merely counting the number of spe-
cies present; i.e., their relative abundances can be dis-
regarded. Therefore, we can conclude that the factors
which regulate bird species diversity do so by determin-
ing the number of species which can coexist in a given
habitat.
MacArthur and MacArLhur (1961) showed that in
temperate regions, bird species diversity is correlated to
foliage height diversity. Thr.t is, diversity increases -with
the number of layers in the vegetation and with the even-
ness of foliage apportionment among the layers. Apply-
ing this relationship to the data in Table 1, we find that
marshes and grasslands (one-layered) are less diverse
than shrublands and deserts (essentially two-layered) ;
log 2 S coniferous forests (up to three-layered) often have some-
FIG. 1. Regression of diversity, H' = — S/>i 'og2 t>i, what diversities
sparse shrub and herbaceous layers and therefore
against the' logarithm of number of species for 267 breed- have in between those of two-layered and other
forested (three-layered) communities. Therefore, it is
ing bird populations. possible that the foliage height diversity determines the
number of available niches (at least in the physical sense)
ber of species was then calculated. The censuses were and thus the number of species which can coexist within
then divided among the following nine community types: a given community.
marshes, grasslands (including early successional fields), Unfortunately the concept of foliage height diversity
shrublands (including overgrown fields), deserts, conif- does not seem to account for the diversity of tropical
erous forests, mixed (hardwood-coniferous) forests, up- woodlands, since it appears that birds in tropical forests
land deciduous forests, floodplain deciduous forests, .and tolerate narrower niches than their temperate zone coun-
tropical woodlands. Means and two standard errors of terparts (Klopfer and MacArthur 1961; MacArthur,
the mean of H', S, and /' were calculated for each com- Recher, and Cody 1966). The high bird species diversity
munity type. in the tropics is part of a general biological phenomenon
RESULTS which may have a general explanation. Hypotheses as to
The regression of H' against Iog2 S (Fig. 1) shows the causes of tropical diversity have been reviewed by
that changes in diversity are closely correlated to vari- Pianka (1966) and will not be considered here.
ations in species richness. The relationship is expressed While foliage height diversity may explain the correla-
by the equation tion of species richness to diversity in temperate commu-
H' — 0.941 (log.j.S1) -0.251. nities, it is still not clear why the species abundance
component remains so stable. This stability is especially
The data show extremely close fit to the linear form interesting in light of the finding by Sager and Hasler
(;- = 0.972). Since the slope of the regression is (1969) that diversity patterns in lacustrine phytoplankton
H'/log2S = H'/H'maix = J' [formula (2)] the figure are correlated to variations in species relative abundance,
demonstrates the stability of the relative abundance com- while species richness remains stable. Since exactly the
ponent as well as the correlation between H' and species opposite situation obtains in birds, this implies a funda-
richness. mental difference in the control of diversity between
Table 1 shows means ± two standard errors of H' S, birds and phytoplankton which reflects the very different
and /' for the nine community types (arranged in order modes of existence in the two groups.
of increasing H'). Trends in //' and 5" from one com- Plankton are "opportunistic" (sensu MacArtliur 1960) ;
munity to the next are identical (marshes have lower i.e., a given species can reproduce quickly and become
mean H' and higher mean 5" than grasslands, but these extremely abundant when conditions are favorable. Since
differences are not statistically significant). Marshes their environment is characterized by relatively high cli-
and, to a lesser degree, grasslands and shrublands, have matic and nutrient variability, a species can only achieve
somewhat lower mean /' than the temperate zone forest high numbers temporarily, and equilibrium numbers only
types, while tropical woodlands are slightly higher. exist as long-term averages taken over a period of many

TABLE 1. Means ± 2 standard errors of //', 6", and /' for breeding bird populations in nine community types. « =
number of censuses in sample; H'= —S^j log.,p t ; S = number of species; /' = H'/\og2S

Community n //' S J'

Marshes 15 1 79 + 0 34 6 33+ 1 32 0 718 + 0 OSO '"
Grasslands 38 1 93 + 0 24 5 74+ 1 00 0 842 + 0 034
Phrublands 26 3 14 + 0 10 14 08+ 2 31 0 843 + 0 024
Deserts (3 3 25 + 0 GO 14.17+ 5 08 0 884+0 048
Coniferous forests 51 3.S3 + 0 14 17.43+ 1 92 0 8SO + 0 014
Upland dccidious forests 62 3 82 + 0 OS' 20 94+ 1 34 0 879+0 012
A[i\ed forests . ... 30 3 92 + 0 14 21 87+ 2 76 0 893 + 0 016
FIoc.dpla.in deciduous forests 18 4 07 + 0 lf> 24 22+ 2 84 0 898+0 020
Tropical woodlands 21 5 23 + 0 21 55 14 + 11 24 0 921+0 012
 Late Summer 1969 REPORTS 929
generations. Therefore, a series of plankton samples taken ACKNOWLEDGMENTS
either at different times or in different communities is
likely to have highly variable species abundance distribu- I am especialh' grateful to Eugene P. Odum for guid-
tions. ance. Robert H. MacArthur provided useful criticism of
Birds, on the other hand, are mostly "equilibrium" the manuscript, and discussions with Steve D. Fretvvell,
species whose physical environment and resources are Henry S. Horn, John T. McGinnis, Carl D. Monk, and
relatively stable from one generation to the next, and Bernard S. Patten were also helpful. James E. Douglass,
whose densities are partly determined by intraspecific Norman Miner, and others at the Coweeta Hydrologic
tcrritoriality. They lay virtually the same size and num- Laboratory gave generous assistance in the course of my
ber of clutches year after year, and the numbers of birds fieldwork. Financial support was provided by a prcdoc-
appear to be more or less at equilibrium from one gener- toral traineeship from the National .Aeronautics and
ation to the next, implying death rates which are also Space Administration and by a Ford Foundation post-
stable. The result is that in most avian communities the doctoral fellowship.
available species partition the breeding space in a charac-
teristic way, and a series of samples from the same or LITERATURE CITED
from different localities will yield similar distributions
of species abundance. Audubon Field Notes. 1937-1966; formerly Bird Lore
Sager and Hasler (1969) give no tables of /', but from (1937-1938) and Audubon Magazine (1939-1946). An-
their graphs it appears that most /' values for plankton nual breeding bird censuses. No. 6 in each volume.
are well below those of birds. Pielou (1966a, b) has National Audubon Society, New York, N.Y.
measured the "evenness" component for trees and herba- Cody, Martin L. 1966. The consistency of infra- and
ceous-shrub vegetation (less than 2 cm in diameter) in intercontinental grassland bird species counts. Amer.
Quebec. Her tree plots ranged in evenness from 0.499 Naturalist 100: 371-375.
to 0.791, while for the herbaceous-shrub community the Horn, Henry S. 1968. The adaptive significance of
value was 0.727. These values are also well below those colonial nesting in the Brewer's Blackbird (Euphagns
given in Table 1 for breeding birds. The high /' values cyaiioccphaliis). Ecology 49: 682-693.
in Table 1 may be due in part to the well-developed Johnston, David W., and Eugene P. Odum. 1956.
intraspecific territoriality exhibited by breeding birds. Breeding bird populations in relation to plant suc-
Assuming a limit to the compressibility of territories, cession on the Piedmont of Georgia. Ecology 37:
effect of this behavior would be to place an upper limit 50-62.
on the density of the commonest species in a given census Klopfer, Peter H., and Robert H. MacArthur. 1961.
area. No such mechanism is known in the phytoplank- On the causes of tropical species diversity: niche
ton or in terrestrial'plant communities. overlap. Amer. Naturalist 95: 223-226.
It is interesting to note that the only avian community Lloyd, Monte, and Robert J. Ghelardi.. 1964. A table
having /' values comparable to those of plant communi- for calculating the equitability component of species
ties is the marshes. The reason is that marshes are diversity. J. Animal Ecol. 33: 217-225.
characterized by gregarious and often polygamous birds MacArthur, Robert H. 1960. On the relative abun-
which defend only the immediate area of the nest against dance of species. Amer. Naturalist 94: 25-34.
others of the same species, and which feed largely outside MacArthur, Robert H., and John W. MacArthur. 1961.
of the census area'(Snelling 1968; Horn 1968). This On bird species diversity. Ecology 42: 594-598.
results in high densities of the most abundant species, and MacArthur, Robert H., Harry Recher, and Martin L.
therefore lower values of J'. Cody. 1966. On the relation between habitat selec-
Birds occupying a given area in the winter or during tion and species diversity. Amer. Naturalist 100:
the migratory season can be expected to have lower 319-325.
valucs of /' than breeding populations, in part because Odum, Eugene P. 1950. Bird populations of the High-
..for most species there is no territorial behavior. It is lands (N.C.) plateau in relation to plant succession
therefore possible that diversity will be correlated more and avian invasion. Ecology 31: 587-605.
closely to relative abundance and less to species richness Pianka, Eric R> 1966. Latitudinal gradients in species
in nonbreeding bird populations as resources become less diversity: A review of concepts. Amer. Naturalist
predictable in their abundance and distribution. 100: 33-46.
The difference in the importance of the two diversity Pielou, E. C. 1966a. Species diversity and pattern
components in birds and phytoplankton is significant, since diversity in the study of ecological succession. J.
it implies two alternative strategies by which diversity Theoret. Biol. 10: 370-383.
can be regulated. It is suggested that these arc responses . 1966b. The measurement of diversity in dif-
to two general types of environments, rigorous ones which ferent types of biological collections'. J. Theoret.
vary widely and often unpredictably in climate and/or Biol. 13: 131-144.
resources, and nonrigorous ones in which these variations Sager, Paul E., and Arthur D. Hasler. 1969. Species
are small and/or relatively predictable. Although phyto- diversity in lacustrine phytoplankton.I. The compo-
plankton and birds probably represent the extremes of nents of the index of diversity from Shannon's for-
these two situations, it is possible to predict that collec- mula. Amer. Naturalist 103: 51-60.
tions of organisms from rigorous environments will vary Shannon, C. E., and W. Weaver. 1963. The mathe-
in diversity according to their relative abundance distri- matical theory of communication. University of Illi-
butions while diversity patterns in collections from non- nois Press, Urbana.
, rigorous environments will be a function of the numbers Snelling, John C. 1968. Overlap in feeding habits of
of species. Evidence is currently being gathered to lest Redwinged Blackbirds and Common Crackles nesting
this prediction. in a cattail marsh. Auk 85: 560-585.