AMER. ZOOL., 34:48-56 (1994)
Systematics and Natural History, Foundations for
Understanding and Conserving Biodiversity1
HARRY W. GREENE
Museum of Vertebrate Zoology and Department of Integrative Biology,
University of California, Berkeley, California 94720
SYNOPSIS. Enhanced by recent technical and conceptual advances, two
classical endeavors in biology play vital roles in understanding, appreciating, and managing biodiversity. Systematics defines the fundamental
units and relationships among living things; natural history chronicles the
lifestyles of organisms in relation to environments. For example, analyses
of evolutionary relationships emphasize the uniqueness of certain taxa,
help prioritize groups of organisms for conservation, and enable us to
estimate the biology of unstudied taxa. Radiotelemetry permits repeated
location of snakes and other stealthy animals, facilitating previously
impossible behavioral studies and thus laying the groundwork for effective
management. Natural history in a systematic and geographic context provides a "rule-of-thumb" for predicting extinction due to global climate
change. Educators should emphasize the urgency of the biodiversity crisis,
inform debates about priorities for funding and other conservation matters, and teach about the goals, methods, and applications of systematics
and natural history.
INTRODUCTION
UNDERSTANDING AND APPRECIATING
BIODIVERSITY
An environmental crisis is upon us, not
just looming on the horizon. More than six
billion humans will burden the earth by the
end of the 20th Century, regardless of our
best efforts, and extinction of many plant
and animal species is underway now. In
addition to ameliorating the harmful effects
of population growth and pollution, we must
rapidly influence public opinion and save
portions of the remaining biotas (Wilson,
1992). Here I briefly review the broad goals
and methods of modern systematics and
natural history, then illustrate how these
activities contribute to our understanding,
appreciation, and conservation of biodiversity. I focus on the applications of phylogenetic analysis and on telemetry studies of
stealthy vertebrates, illustrating how new
techniques enhance traditional approaches.
What are systematics and natural history?
Systematics encompasses the characteristics, genetic status, and evolutionary histories of organisms. Once devoted mainly
to describing obvious phenotypic variation
and coining formal names, systematists now
evaluate samples from throughout the geographic distribution of living things with
morphological, biochemical, multivariate
statistical, and other sophisticated techniques. Phylogenetic systematics, in particular, strives to infer the evolutionary histories of independent lineages (species and
higher taxa), and to determine relationships
between geography and the divergence of
organisms (Cracraft, 1994; O'Hara, 1994).
Natural history focuses on where organisms are and what they do in their environments, including interactions with each
other. The building blocks of natural history
are descriptive ecology and ethologydetailed accounts of organismal biology in
natural settings—followed by experimental
studies of factors that affect distribution,
abundance, and interactions.
1
From the symposium Science as a Way of Knowing—Biodiversity presented at the Annual Meeting of
the American Society of Zoologists, 27-30 December
1992, at Vancouver, Canada.
48
BASIC BIOLOGY AND BIODIVERSITY
Conserving and appreciating nature
Systematics and natural history define the
boundaries and contours of biodiversity;
they elucidate the fundamental kinds of
organisms (species and higher taxa) as well
as their interactions with each other and
their environments. Areas are chosen for
conservation based on, among other criteria, the kinds and numbers of organisms
they encompass; effective captive breeding
and reintroduction depend on knowledge of
a species' ecology and behavior; and popular films and books translate research findings about nature into public education
(Greene and Losos, 1988). I will elaborate
on two roles for systematics and natural history, the first ubiquitous but widely unrecognized and the other relatively new.
If wild organisms and places are to be
conserved, they must have value in human
societies. Interactions among plants and
animals hold countless solutions to natural
problems with analogues in human welfare;
the skin toxins of dart-poison frogs and other
natural products with pharmaceutical applications are well known examples (e.g., Wilson, 1992). Equally important in the long
run, systematics and natural history also
underlie esthetic evaluation, cultural acceptance, and prioritization for management.
Beyond intrinsic cuteness, we regard the
giant panda as special because of its controversial relationships with bears and raccoons, strange thumblike dewclaws, and diet
of bamboo. In the economic and political
arenas of conservation, efforts to save rainforests are based on their demonstrably
incomparable biodiversity, not just the
emotional responses some of us have to
those places. Striking resemblances of unrelated organisms from distant, similar habitats are a common theme in exhibit labels
and other forms of environmental education, yet without phylogenetic evidence that
similar traits indeed were acquired independently we could not marvel at convergent evolution (Luke, 1986). Systematics and
natural history even facilitate the transfer
and evaluation of knowledge about nature
among human societies, since ethnobiology
is based on their results (e.g., Patton et al,
1982).
49
The uncertain but potentially serious consequences of rapid climate change are a new
challenge for conservation in the coming
decades. Ideally, the predicted impact of
temperature and moisture shifts (via organismal physiology) on population viability
will be incorporated into management strategies (Kareiva et al., 1992). Such detailed
knowledge requires years of research and is
available for relatively few species, so indirect methods are potentially useful. For
example, McDonald and Brown (1992) used
presence or absence of montane mammals
on isolated ranges of different sizes in the
Great Basin to estimate minimum refuge
areas for each species. The resulting thresholds for refuge area were then compared with
estimates of habitat shrinkage from climate
change to predict future extinctions. That
technique is limited to fairly large samples
of habitat islands with well-documented
biotas; a less precise but more broadly applicable "rule-of-thumb" approach based on
systematics and natural history is illustrated
later in this paper: Terrestrial species with
fragmented geographic ranges and narrow
elevational tolerances are especially at risk
under changing regimes of temperature and
moisture.
STUDYING STEALTHY VERTEBRATES
The information on ecology and behavior
necessary for conservation, management,
and nature appreciation are available for
only a tiny fraction of species, generally those
that are large, common, or otherwise relatively easy to study (Greene, 1986).
Advances in telemetry during the past two
decades, however, have greatly enhanced
research on stealthy and otherwise cryptic
animals. Early workers mostly localized
radio signal coordinates on a map, but
recently biologists have used telemetry to
study undisturbed animals more directly in
nature (e.g., Emmons, 1987, for rainforest
cats). Our research on pitvipers in Arizona
illustrates the use of miniaturized, surgically
implanted transmitters (Reinert, 1992) to
facilitate repeated encounters and behavioral observations.
Since 1986 my colleagues and I have followed 17 blacktailed rattlesnakes (Crotalus
molossus) in the Chiricahua Mountains, for
HARRY W. GREENE
FIG. 1. Vignettes from the natural history of blacktailed rattlesnakes (Crotalus molossus) in the Chiricahua
Mountains, Cochise Co., Arizona. Courtship behavior in a juniper tree, 24 August 1991; telemetered male's
head (#8, total length ca. 1 m) is pressed against the smaller female's neck (photograph by D. L. Hardy, ST.).
periods of a few days to more than four or by following previously telemetered indiyears. Despite bright colors and a total length viduals, and during ca. seven months of
of ca. 1 m, these snakes are indeed cryptic fieldwork at the site I encountered only one
and difficult to locate. Most of our study blacktail by visual scanning in the habitat.
animals were found as they crossed a road With telemetry, we have documented pat-
BASIC BIOLOGY AND BIODIVERSITY
51
FIG. 2. Vignettes from the natural history of blacktailed rattlesnakes (Crotalus molossus) in the Chiricahua
Mountains, Cochise Co., Arizona. Telemetered male (#6, total length ca. 80 cm) basking on a woodrat (Neotoma)
nest, 29 September 1990; a suspiciously rat-sized bulge is visible on the left side of the snake. In each case
observations commenced when the male was located initially by radiotelemetry.
terns of daily and seasonal movements,
ambush hunting tactics, late autumn feeding, courtship, copulation, shifts in retreat
sites during the winter, and various maintenance behaviors in the field (Figs. 1, 2).
In 1992 we extended radiotelemetry to a
poorly known species with special conservation status, the ridgenosed rattlesnake
{Crotalus willardi, total length ca. 40 cm) in
the Huachuca Mountains. During the first
year's work with four telemetered C. willardi we have observed hunting, courtship,
copulation, and winter activity (Fig. 3). Our
findings on mating patterns and seasonal
movements, among other factors, eventually will help identify critical habitat for that
species.
Two SMALL RATTLESNAKES: SYSTEMATICS,
NATURAL HISTORY, AND DIVERGENT
CONSERVATION PROSPECTS
Ridgenosed rattlesnakes (Crotalus willardi) inhabit the Sierra Madre Occidental
of Mexico and nearby mountains in the U.S.
(Fig. 4). The New Mexico ridgenosed rattlesnake (C w. obscurus) is on the U.S.
Endangered Species List and the Arizona
ridgenosed rattlesnake (C. w. willardi) is state
listed as threatened. The relatively wellstudied systematics of ridgenosed rattlesnakes (Barker, 1992) provides important
insights for their conservation. First, information on the natural history of some taxa
can be used to estimate that of their unstudied or unstudiable relatives (Brooks et ai,
HARRY W. GREENE
1992). Although only C. w. obscurus is officially "endangered," systematics provides
strong support for Arizona's strict protection of C. w. willardi; three alternative phylogenies and two ranking methods agree that
the latter is evolutionarily more distinctive
than the former (Fig. 5).
Massasauga rattlesnakes (Sistrurus catenatus) inhabit seasonally wet grasslands,
bogs, and adjacent forests from Arizona and
northern Mexico to New York and southern
Canada, a distribution indicative of postPleistocene expansion of prairie into northeastern North America (Schmidt, 1936). In
contrast to Crotalus willardi, geographic
variation in S. catenatus is so incompletely
studied that we lack a basis for prioritizing
any particular segment of the range in terms
of phylogenetic significance; three subspecies are based on vaguely defined clinal variation in coloration and a few scale counts,
and relationships among populations are
unknown (Gloyd, 1955). Most massasauga
populations are isolated by land conversion
for agriculture, and the species is threatened
or endangered throughout much of its range
(Seigel, 1986). The status ofS. catenatus in
the southwestern U.S. is especially precarFIG. 3. Courting ridgenosed rattlesnakes (Crotalus ious; there are no recent records from west
willardi) in the Huachuca Mountains, Cochise Co., Ari- of the Pecos River in Texas or from southzona, 21 July 1992. The snakes are coiled and the western New Mexico. A few small populatelemetered male (# 1, total length ca. 60 cm) is tapping
the female's back (#7) with his chin (photograph by F. tions remain in Arizona, where massasauWilson); this species is difficult to locate in its typical gas are seen above ground only during the
microhabitat of oak leaves and bunch grass (note dia- late summer rainy season and their persisgram).
tence might be dependent on the stable high
humidity in kangaroo rat burrows (Kay and
Whitford, 1978).
1992). Four subspecies of C. willardi feed
Systematics and natural history enhance
on centipedes and lizards as juveniles and appreciation for these small pitvipers and
on rodents (rarely birds) as adults, but only suggest divergent prospects for conservaone natural prey item (a warbler) is known tion. Neither species constitutes a threat to
for the New Mexico race (Greene et ah, human welfare and both are regarded as
unpublished). Lacking direct information, attractive by naturalists (some Native
management can precede on the conser- Americans called massasaugas "pictures of
vative assumption that C. w. obscurus has the sun," alluding to the large, silver-edged
not diverged in diet from other ridgenosed dorsal blotches). Both are living icons for
rattlesnakes. Second, all members of a group landscape history, ridgenosed rattlesnakes
{e.g., species in a genus) usually have been for fragmentation of ancient mountain
valued equally, thus ignoring their differ- ranges and massasaugas for more recent
ential evolutionary significance if particular vagaries of grassland ecosystems. Biogeogtaxa must be slighted when funds, person- raphy, based on systematics and natural hisnel, and other resources are scarce (Vane- tory, suggests that these two species would
Wright et al, 1991; Greene and Campbell, respond differently to anthropogenic cli-
53
BASIC BIOLOGY AND BIODIVERSITY
Desert
Grassland
Encinal
Pine-Oak Woodland
Coniferous Forest
willardi
• I / •>
Peloncillo
Mts.
Douglas/ / _ ; J ;
Agua Prieta
PhobscUrus
xd.?.
j
Sierra de
(.Los Ajos
CHIHUAHUA
silus
50 miles
FIG. 4. Distribution of three subspecies of the ridgenosed rattlesnake (Crotalus w. willardi, C. w. obscurus, and
C. w. silus) in the northern Sierra Madre Occidental and outlying ranges of Mexico, Arizona, and New Mexico;
two Mexican subspecies are not shown (based on Marshall, 1957; Barker, 1992; Thirkhill and Starrett, 1992).
Ridgenosed rattlesnakes occur in evergreen oak woodland ("encinal"), pine-oak woodland, and coniferous forest.
mate change during the coming decades.
Crotalus willardrs wide attitudinal range (ca.
1,475-2,770 m, Lowe et ai, 1986) spans
several major vegetation belts; closely
related populations are separated by unsuitable habitat {e.g., grassland between the
Huachucas and Sierra de Cananea for C. w.
willardi, Fig. 4), suggesting that their wood-
54
HARRY W. GREENE
B
a.
b.
c.
amabilis
meridionalis
obscurus
silus
willardi
amabilis
meridionalis
obscurus
silus
willardi
amabilis
meridionalis
obscurus
silus
willardi
U
R,
1
.143
1
1
1
.143
.143
3
.429
4
1.5
.231
4
1.5
.231
6
6
4
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.154
1.5
.231
.17
.17
5
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1
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.176
1
.17
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.176
1
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.17
5
5
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.176
1
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.125
.50
6
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.25
2 .25
1 .125
1 .125
2 .25
1
1
.125
.125
.125
.33
.143
.154
.176
.295
FIG. 5. Three alternative hypotheses of evolutionary relationships (based on Barker, 1992) and two phylogenetic
methods for assessing conservation priorities (May, 1990; Vane-Wright et ai, 1991) for five subspecies of the
ridgenosed rattlesnake (Crotalus willardi). A simple method weights "sister taxa" (e.g., amabilis and meridionalis)
equally and converts their scores (C) to proportions (P,). A second method totals for each taxon the number of
branches from each node between the taxon and the tree's origin (B), takes the inverse of B as a measure of
phylogenetic distinctiveness (U), and converts scores for U into proportions (P2). For example, phylogeny (a)
indicates that C. w. willardi represents one half of the initial divergence event in this species by P, and about
43% of overall phylogenetic distinctiveness by P2; phylogeny (b) suggests that C. w. willardi should be prioritized
only at values of 25% and about 23%, respectively. Larger groups would not always yield identical rank orders
of importance by P, and P2, and more refined approaches are possible with some data sets (e.g., Crozier, 1992;
Faith, 1992).
land habitats repeatedly have contracted
upward and expanded downward in the past
{cf. Van Devender and Spaulding, 1979).
Under moderate global warming ridgenosed rattlesnakes probably will persist at
higher elevations in several mountain
ranges, as they have during previous glacial
cycles. Sistrurus catenatus has a narrow elevational range and populations have been
separated by human impact over the past
two centuries rather than by natural, longterm habitat shifts. Subjected to moderate
climate change and without heroic manage-
ment, the massasauga might survive only
in moister, eastern segments of its distribution. Southwestern populations would dry
up like water drops on a griddle.
BIOLOGY, CONSERVATION, AND
EDUCATION
Unfortunately, despite the irrevocable,
imminent realities of extinction, support for
systematics and natural history continues to
dwindle. Current levels of funding imply
that understanding and conserving biodiversity are far less important than space
BASIC BIOLOGY AND BIODIVERSITY
travel, sequencing the human genome, and
other multi-billion dollar activities (e.g., ca.
10 million dollars/year for systematic biology at the National Science Foundation, vs.
30 million dollars for a single toilet on the
Space Shuttle). Underlying such disparities
are our failure to comprehend the urgency
of the biodiversity crisis, the view prevalent
in some circles that those branches of biology are outmoded, and a widespread belief
among lay people that knowledge is already
available or can be gained easily.
The realities are straightforward. Behind
all the facts, interpretations, and impressions in nature programs and field guides
are thousands of biologists: collecting and
curating specimens, weighing nestling eagles,
sketching fern leaves, and recording the
behavior of ants. Practical applications of
those and countless other seemingly esoteric
tasks range from developing new pharmaceuticals to designing wildlife refuges and
detecting pesticides in eggshells. Nevertheless, we are surprisingly ignorant of life on
earth. Scientists have learned how many
atoms are in a molecule and how many craters are on the moon, but not how many
species of birds, butterflies, or trees live in
Brazil. A new species of amphibian or reptile is found about every other year in California (Greene and Losos, 1988), one of the
world's best explored places, and only two
of 69 species of snakes in the western U.S.
have been analyzed phylogenetically (Barker, 1992; Grismer, 1990). The biotas of
tropical regions are even more incompletely
studied, and newly discovered organisms
there are literally disappearing faster than
they can be described.
Artists, teachers, politicians, journalists,
citizen activists, and scientists all have vital
roles to play in saving biodiversity. Of foremost importance is convincing everyone
that a crisis is underway now, that solutions
must be found soon. With that recognition,
we need to provoke and inform debates
about priorities at all levels of government,
for in a monetary sense conservation competes with other scientific endeavors as well
as broader societal needs. Systematists and
natural historians must refine their own goals
and techniques, as well, for solving these
urgent problems (Soule, 1990). Finally, we
55
should take every opportunity to teach about
modern systematics and natural history,
especially their implications for appreciating and managing nature. Complexities of
the biodiversity crisis and roles for science
in conservation are appropriate topics for
discussion in every high school and undergraduate biology course.
ACKNOWLEDGMENTS
I thank D. L. Hardy, Sr., C. W. Painter,
C. J. Schneider, T. A. Snell, B. R. Tomberlin, and F. Wilson for their collaboration on
research projects discussed herein; the Arizona and New Mexico game and fish departments for encouraging our studies; U. C.
Berkeley Committee on Research for financial support; K. Klitz for preparing the figures; and an anonymous, grizzled reviewer
for helpful criticisms of the manuscript.
REFERENCES
Barker, D. G. 1992. Variation, infraspacific relationships, and biogeography of the ridgenose rattlesnake, Crotalus willardi. In J. A. Campbell and E.
D. Brodie, Jr. (eds.), Biology of the pitvipers, pp.
89-105. Selva, Tyler, Texas.
Brooks, D. R., R. L. Mayden, and D. A. McLennan.
1992. Phytogeny and biodiversity: Conserving our
evolutionary legacy. TREE 7:55-59.
Cracraft, J. 1994. Species diversity, biogeography,
and the evolution of biotas. Amer. Zool. 34:000000.
Crozier, R. H. 1992. Genetic diversity and the agony
of choice. Biol. Conserv. 61:11-15.
Emmons, L H. 1987. Comparative feeding ecology
of felids in a neotropical rainforest. Behav. Ecol.
Sociobiol. 20:271-283.
Faith, D. P. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61:1-10.
Gloyd, H. K. 1955. A review of the massasauga,
Sistrurus catenatus, of the southwestern United
States (Serpentes: Crotalidae). Bull. Chicago Acad.
Sci. 10:83-98.
Greene, H. W. 1986. Natural history and evolutionary biology. In M. E. Feder and G. V. Lauder
(eds.), Predator-prey relationships: Perspectives and
approaches from the study of lower vertebrates, pp.
99-108. Univ. Chicago Press, Chicago.
Greene, H. W. and J. A. Campbell. 1992. The future
of pitvipers. In J. A. Campbell and E. D. Brodie,
Jr. (eds.), Biology of the pitvipers, pp. 421-427.
Selva, Tyler, Texas.
Greene, H. W. and J. B. Losos. 1988. Systematics,
natural history, and conservation. BioScience 38:
458^62.
Grismer, L. L. 1990. A new long-nosed snake (Rhinocheilus lecontei) from Isla Cerralvo, Baja California Sur, Mexico. Proc. San Diego Soc. Nat. Hist.
4:1-7.
56
HARRY W. GREENE
Kareiva, P. M., J. G. Kingsolver, and R. B. Huey. (eds.)
1992. Biotic interactions and global change. Sinauer Assoc, Sunderland, Massachusetts.
Kay, F. R. and W. G. Whitford. 1978. Burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in south-central New Mexico.
Amer. Midi. Nat. 99:270-279.
Lowe, C. H., C. R. Schwalbe, and T. B. Johnson. 1986.
The venomous reptiles of Arizona. Arizona Game
and Fish Dept., Phoenix.
Luke, C. 1986. Convergent evolution of lizard toe
fringes. Biol. J. Linnean Soc. 16:1-16.
Marshall, J. T. 1957. Birds of pine-oak woodland in
southern Arizona and adjacent Mexico. Pacific
Coast Avifauna 32:1-125.
May, R. M. 1990. Taxonomy as destiny. Nature 347:
129-130.
McDonald, K. A., and J. H. Brown. 1992. Using
montane mammals to model extinctions due to
global change. Conserv. Biol. 6:409-415.
O'Hara, R. J. 1994. Evolutionary history and the
species problem. Amer. Zool. 34:12-22.
Patton, J. L., B. B. Berlin, and E. A. Berlin. 1982.
Aboriginal perspectives of a mammal community
in Amazonian Peru: Knowledge and utilization
patterns among the Aguaruna Jivaro. Spec. Publ.
Pymatung Lab. Ecol. 6:111-128.
Reinert, H. K. 1992. Radiotelemetry. In J. A. Campbell and E. D. Brodie, Jr. (eds.), Biology of the
pitvipers, pp. 185-197. Selva, Tyler, Texas.
Schmidt, K. P. 1936. Herpetological evidence for the
postglacial eastward extension of the steppe in
North America. Ecology 19:396-407.
Seigel, R. A. 1986. Ecology and conservation of an
endangered rattlesnake, Sistrurus calenalus, in
Missouri, USA. Biol. Conserve. 35:333-346.
Soule, M. 1990. The real work of systematics. Ann.
Missouri Bot. Gard. 77:4-12.
Thirkhill, L. J. and B. L. Starrett. 1992. Geographic
distribution. Crotalus w. willardi. Herp. Review
23:124.
Van Devender, T. R. and W. G. Spaulding. 1979.
Development of vegetation and climate in the
southwestern United States. Science 204:701-710.
Vane-Wright, R. I., C. J. Humphries, and P. H. Williams. 1991. What to protect? Systematics and
the agony of choice. Biol. Conserv. 55:235-254.
Wilson, E. O. 1992. The diversity of life. Harvard
Univ. Press, Cambridge, Massachusetts.