DECEMBER1990
Mpnroarer,
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ARTICLES
CLASSICALTAXONOMYOF MOSQUITOES-AMEMORIALTO
JOHN N. BELKIN 1,'
THOMAS J. ZAVORTINK
Department of Biology, Uniuersity of San Francisco,Ignatian Heights, San Francisco,CA 94117-1080
ABSTRACT. The major contributions of John N. Belkin to the field of mosquito systematicsare
noted. Hallmarks of his publications are presentedand his hypothesesabout the evolution, speciation,
competition, distribution and classification of mosquitoesare summarized. The current status of the
field of mosquito systematicsis examined. It is argued that mosquito systematicsis still largely at the
alpha taxonomy level, that at best only 25-50% of mosquito speciesare known, and that we have not
even begun to develop a natural classification for the Culicidae. It is concludedthat there will be little
improvement in the status of mosquito taxonomy unless there is increasedsupport for systematics.
an interest in entomology also, they told me
about a fantastic systematist in the Zoology
The scientist we honor this year is John N. Department, a man who studied mosquitoes.
Belkin, one of the finest systematists ever to That man was,of course,John Belkin. Sincehis
work with mosquitoes. He was a painstaking coursein "Principles of SystematicZoology" was
worker, a perfectionistif you wish, whosepub- required of all students in systematic botany,
Iications set the standard for accuracyand com- the older graduate students were very familiar
pletenessthat others must now strive to reach. with him and his work. I met John the next
He made major contributions to the field of year, and after discussinghis researchwith him,
mosquito systematics, contributions that will
I decided to pursue my doctoral studies under
influence the field for decadesto come. Among his direction. I finished my master'sin botany
these are the development of: field and labora- and joined his researchgroupshortly thereafter.
tory techniques for studying mosquitoes; a John suggestedseveralprojects that I could unstandard descriptive terminology for all stages dertake for my dissertation. Among these were
of mosquitoes; an explicitly stated taxonomic a c5rtotaxonomicstudy of the Anophelesspecies
methodology for mosquitoes; a classification in California, a revision ofthe crab hole breeding
scheme for all culicids; and hypothesesto ex- genus Deinocerites, and a revision of the tree
plain the evolution, speciation and distributions hole breeding genusOrthopodomyia.AII of these
of mosquitoes. Belkin amassed the finest re- wereprojectsin which John was interested.Besearchquality collection of mosquitoesin exist- causeof my fascination with tree hole mosquience.If it is properly curated,it will be a price- toes, I choseto work on Orthopodomyia.I comless heritage for future generations.In recogni- pleted my doctorate in 1967. Instead of leaving
tion of his outstanding contributions to UCLA, I stayed and worked with John on his
mosquito systematics,the American Mosquito "Mosquitoes of Middle America" project. BeControl Association awarded Belkin the Medal causeof my Iong associationwith John, it is
of Honor-the highest honor given by the So- perhaps appropriate that I present this memociety-at the Annual Meeting in Salt Lake City rial to him.
in April 1980.Two weeks Iater he died.
I entered UCLA as a graduate student in
systematicbotany in 1961.As soon as the older
JOHN BELKIN AND HIS SCIENTIFIC
graduate students in botany learned that I had
CONTRIBUTIONS
INTRODUCTION
'Twelfth Annual AMCA Memorial Lecture delivered at the 56th Annual Meeting of the American
Mosquito Control Association, Lexington, Kentucky,
April 2, 1990.
2Acknowledgmentsare made to the Lowndes EngineeringCompany for their participation in sponsoring the 1990Memorial Lecture.
On the personal side, John was a kind and
generousman. He could, however,be a difficult
man to work for. He demandeda lot of himself,
and he acceptedno lessof others.On occasion,
he would be brusque, irascible, obstinate. His
demeanorand his encyclopedicknowledgewere
intimidating to many. But if a person wasn't
deterred by John, and proved himself to be
596
JouRNar,oF THEAurRrcarvMosqurro Cor.nnor.Assocrerron
cations.Someof theseideasor hypotheseswere
developed by Belkin himself; some were borrowed from other biological disciplines.Some
are controversial views that have not gained
widespreadacceptanceamong culicidologists or
zoologistsin general. All these themes demonstrate, though, his overriding concern with
analysis and explanation. One hypothesis that
Belkin developedwas that the intercontinental
regions in both the OId World and New World
tropics were "Centers of Origin" where major
new adaptivetypes of mosquitoesoriginated. He
saw the intercontinental regions as geologically
unstable areaswhere land bridees were formed
and fragmentedrepeatedly.Duiing fragmentation, populations of mosquitoes would be reducedin size and isolated,creatingthe kind of
situation that could lead to the rapid fixation of
new adaptive types. These would becomebetter
adapted with time, and would disperseto adjacent regionswhen Iand bridgesreformed. Belkin
also saw evidencefor other methods of speciation in mosquitoes.He proposedsympatric speciation as the explanation for the existence of
flocks of closelyrelatedspeciesin groupsutilizing specialized,
restrictedbreedingsites such as
leaf axils and pitcher plants. Without doubt, the
single most controversial proposition advanced
by Belkin was that hybridization was a major
factor in the speciation and evolution of mosquitoes. He saw evidence for hybridization in
taxa of all ranks-species, subgenera,genera,
tribes. At the specieslevel, he considered hybridization as the most parsimonious explanation for the combinationofblocks ofcharacters
from 2 speciesin the different sexesor stagesof
a third species.In the caseof higher taxa, he
believed that hybridization in the distant past
was the explanation for the annectent gtoups
that exist today. He reasonedthat taxa that had
formed in isolation on fragments of former land
bridges may have been morphologically distinct
but not reproductively isolated, and that they
may have hybridized when the fragments rejoined. Belkin's familiarity with the role of hybridization in the speciation of flowering plants
undoubtedly played a part in his willingness to
embracethis conceptfor mosquitoes.More than
40% of flowering plant species are of hybrid
origin. They are fertile tetraploids formed by
doubling the chromosomenumber of partly or
completelysterile hybrids between2 diploid species. Belkin believedthat he saw the same kind
of morphological evidence for hybridization in
mosquitoesthat botanists sawin plants. He once
told me that the only distinction between the
situation in plants and the situation in mosquitoes was that botanistsknew the mechanismby
which hybrid speciesof plants formed,whereas
Vor-.6,
we did not yet know that mechanism for mosquitoes.
Belkin was strongly influenced by ecological
thought, particularly that related to competition. He did not believe that there could be 2 or
more speciesof the samespeciescomplexbreeding in the same habitat in the samearea. In the
section on methodologyin his Mosquitoesof the
South Parific, he stated that he used data from
morphology, bionomics and distribution. The
bionomical data to which he referred were the
habitats of the immatures. The first steps in his
taxonomic procedure were to sort material to
geographicalsourceand habitat. His belief that
2 or more speciesof the samecomplex could not
coexist in the same habitat went a long way in
preventing the description of intraspecific variants, particularly hairy larval and pupal
morphs,asdistinct species.Belkin alsosawcompetition as shapingentire mosquitofaunas.His
commentsabout the tribes Aedini and Sabethini
are relevant in this regard. The greater number
of sabethinelineagesin the New World tropics
relative to the Old World tropics could be interpreted as indicating that the tribe originated in
the New World and radiated there in the absence of competition from aedines. Alternatively, if the sabethines originated in the Old
World tropics, which was, by the way, what
Belkin believed,then they had been largely replacedthere by the more recently evolvedplantbreeding aedine mosquitoes.
In interpreting distributional data, Belkin
consideredcommon, widespread mosquitoes to
be the most recently evolved species in their
group. He envisionedthem as arising in a source
area,which, for the faunas he was interested in.
was an intercontinentalareain the tropics.
then
-dispersal
spreading into adjacent areas when
routes became available and eliminating previously evolvedspecies.Specieswith limited distributions were consideredto be relicts, or paleoendemics,particularly if they occurredin unusual habitats for their group or occurred near
the limits of distribution for their group. Belkin
believed most of the mosquitoesendemic to the
islands of the South Pacific were older than
their relatives in the source area to the west.
They were relicts whose absencein the source
area was due to extinction. Incidentally, Belkin
consideredthe mosquitoesof New Zealandto be
an ancient continental fauna, and the speciesof
this fauna to be the most primitive living representatives in their phyletic lines to be found
anywhere in the world. This belief profoundly
influenced his ideas about the evolution of the
Culicidae.
In the classification of mosquitoes,Belkin
placed emphasison characters of the immature
DECEMBER1990
MBtr.roRrelLncrune
597
large at the alpha taxonomy level. Emphasis is
still on recognizing,characterizing and naming
species,Even many who utilize nonmorphological techniques, like electrophoresis,are alpha
taxonomists whose primary concern is the recogrrition and characterization of species.How
many species of mosquitoes are there? How
many more remain to be discovered?The rate
at which speciesare discoveredin any group of
organisms can be depicted as a sigmoid curve
(Fig. 3). The rate is slow initially, increases
exponentially as interest in the group rises,
starts to slow when more than half the species
are known, and finally approachesasymptotically the total number of speciesin the group.
The graph showing the total number of presently valid speciesof Aedes known at 2l-year
intervals from 1750to 1975 showsthe expected
upturn, but gives no hint of slowing (Fig' a)' A
bar graph showingthe number of presently valid
speciesof Aedesdescribedin each5-yearperiod
from 1900to 1980 shows more variation in the
rate of taxonomic work (Fig. 5). Those periods
of time in which relatively few species were
describedgenerally coincide with times of warfare or economic depression. However, the
period in which the fewest species were described is 1975-80. Does this slowing down indicate that we have found more than half the
speciesof Aedes, or does it indicate only a decrease in taxonomic effort? I suspect it shows
only the latter. If the rate of description of Aedes
has not started to slow and if our knowledgeof
this genus is representative of the Culicidae in
CURRENT STATUS OF MOSQUITO
general,then we know lessthan halfthe species
TAXONOMY
in the family at this time. Belkin believed that
Where is the field of mosquitotaxonomy to- the 155 named zoologicalspeciesof true mosday? The taxonomy of every group passes quitoes that he treated in the Mosquitoesof the
through 3 overlapping and intergrading Ievels
commonly called alpha, beta and gamma taxonomy. At the alpha level of taxonomy, the main
concernsare the discovery,characterizationand
naming of species.These speciesare placed into
o
large, comprehensivegenera. At the beta level
of taxonomy,the primary concernis the devel- .9
opment of a natural classification. The species o
are studied in greater detail and are reclassified
into smaller and more numerous genera that
o
indicate their genetic relationships more accurately. At the gamma level of taxonomy, the
primary concernsare various biologicalaspects E
F
of organisms, such as the structure of natural
populations, the genetic basis of phenotypic
characteristics, the nature of isolating mechaTime
nisms, and the rates of evolution and speciation.
This Ievel of taxonomy emphasizesthe interpreFig. 3. Sigmoid curve showing the increase in the
tation ofbiological diversity. So, where doesthe number of speciesknown for any group of organisms.
field of mosquito taxonomy stand in this classi- The broken line representsthe total number ofspecies
fication of taxonomies? Sadly, it is still by and in the group.
stagesrather than on the generalornamentation
of adults or the secondarysexual characters of
males. He believed larvae preserved phyletic
charactersbetter than adults. He went so far as
to say that we needed to study all instars of
Iarvaein order to developa natural classification
for the family. In the true mosquitoes Belkin
recognized12 tribes. This arrangementwas a
marked departure from recognizing only 3 coordinate groups,the anophelines,toxorhynchitines and culicines.It was Belkin's conviction,
though, that the unusual featuresof anophelines
and toxorhynchitines had been overemphasized,
and that these gtoups were no more distinct
than many of the lineages traditionally placed
in the culicines.Furthermore,he did not believe
that the culicineswere a monophyletic group. In
his Mosquitoesof the South Pacific, Belkin presented a list of the 12 tribes, placing the more
generalizedtribes centrally and the more specializedand annectenttribes at the ends of the
"phylogenetic
Iist. This can be interpreted as a
bush," with the more specializedtribes radiating
out in several lines from the central core of
generalizedforms. Groups considered to be
primitive in more traditional classifications,Iike
the anophelinesand sabethines,were considerei
highly specializedtribes by Belkin. Although his
classification is radical in its arrangement of
genera, it continues the conservative tradition
of recognizing only a relatively few genera for
mosquitoes,
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1975
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Fig. 4. Number of presently valid speciesof Aedes
known at 25-yearintervalsfrom 1Tb0to 1g7b.
90
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3 7 0
o 6 0
VoL.6, No. 4
about 3,146.The squareroot of this is 56. Theoretically, for mosquitoesthere should be 56
monotypic genera and the largest genus should
have 56 species.How different is the real situation! The graph for mosquitoesis almost a
straight line (Fig. 7). We recognizeonly 3 monotypic generaand no more than 2 generaof any
other particular size. At the rieht end of the
graph, 6 generawith over 100 to nearly 1,000
specieseach are way off scale. The graph for
mosquitoes is clear evidence that we have not
even begun to develop a natural classification
for the family. Incidentally, an estimate of the
total number of genera that should, theoretically, be recognizedin a family the size of the
Culicidae can be obtained by integration of the
equation XY : 56. The number is 225. We
recognizejust 37 at this time.
Not all taxa are studied at the same rate.
Although study of mosquitoesis still at the alpha
taxonomiclevelfor the mostpart, thereare some
groupswhere study has reachedthe gammalevel
of sophistication.Includedamongt[ese are sev-
- 5 0
E 4 0
2 z a
20
10
0
1915
1925
1935
1945
1920
J930
1940
IgEO
Date
Fig. 5. Number of presently valid species of Aedes
described in each 5-year period from 1900 to 1980.
South Pacific represented less than half the
fauna,becausepracticallyno collectinghad been
done in the interior of any of the islands.Because Belkin describedas new or resurrected
from synonymy77,or 50%,of these 155species,
the number of speciesknown from the region
before his studiesmay havebeen as little as 25%
ofthe actualfauna.I would estimate,then, that
we know at best only somewherebetween 25
and 50% of mosquito species.
In those groups of organisms that have
achieved the beta level of taxonomic work. it
has been noted that a graph of the number of
genera to the number of speciesper genus is a
hollow curve that approachesboth axes asymptotically (Fig.6).At oneextreme,there are many
monotypic or ditypic genera. At the other extreme, there are only one or 2 large genera. In
the middle, there are relatively few generawith
just a few species.Mathematically, this curve is
a hyperbolawith the equation XY : K. For any
group of organisms,K is the square root of the
number of speciesin that group.For mosquitoes,
the number of valid speciespresently known is
Speci€sper gsnus
Fig. 6. Hollow curve showingthe decreasein the
number of generaas the number of speciesper genus
increasesfor any group of organisms with a sound,
natural classification.
45
2
5
3
5
4
5
S
65
100-1000
species
Sp€oies per g6nus
Fig. 7. Number of mosquito generawith the number
of speciesindicated.
DEoEMBER1990
MEMORIAL
LECTURE
larger community of biologists wants it to be. If
no value is given to systematic studies and the
field of systematicscontinues to be understaffed
and underfunded, then there will be little progressin mosquito taxonomy' There will be some
ievisionary work, but no major syntheses, no
development of a natural classification and no
major faunal studies. Gamma level taxonomic
studieswill continue, but a point will be reached
where such studies will be hindered by the lack
of a modern classifrcation for mosquitoes.If' on
the other hand, support for mosquito systematics increases,then the kinds of studies that will
lead to the development of a natural classification of the family will be possible.Faunal studies
"Mosquitoes of Middle America" and
FUTURE OF MOSQUITO TAXONOMY
like the
"southeast Asia Mosquito Project" should
the
taxonomy?
What is the future for mosquito
Systematicsis a much misunderstoodand ma- be resurrectedand continued. It is only through
ligned science.As noted by Simpsonyears ago major projects like these that the diversity of
(1945),systematicsis both the most elementary mosquitoesbecomesknown. Taxonomic revisionsproducedby projects like theseprovide the
and most inclusive of the biological sciences.It
is the most elementarybecauseorganismsmust data that will ultimately lead to the development
be discoveredand named before we can study of a natural classification. That classification
them and record information about them. It is will, in turn, suggest innumerable hypotheses
the most inclusive becauseeverything that is that can be tested by studies at the gammalevel
eventually learned about organisms is utilized of taxonomy, and may provide some basis for
in systematicsto help recogrrizetaxa and under- understanding the interrelationships between
stand the relationships among them- Too many mosquitoes and the disease-causingorganisms
biologists have equated systematics with only they vector.
the description and naming of species' They
have failed to seethe central role of systematics
CONCLUSION
in the interpretation of biological diversity. As
dein
long-term
has
been
a result, systematics
In conclusion. let me note that we all stand
cline. The field is understaffedand underfunded, on the shoulders of our predecessors.The field
and relatively few students are being trained' of mosquito systematicsis fortunate to have had
The situation in mosquito systematicsis essen- a man with the intellect and motivation of John
tially the sameas that in systematicsas a whole' Belkin. He showed us the kind of studies that
The scientific community seemsto be awaken' could be done and left us explicit instructions
ing to the fact that we know only a very small on how to do them. AII that remains is to compercentageof the specieson earth. Some biolo- plete
the work that Belkin had hoped to do
gists estimate that the 1.5 million species of
himself.
organismswe know are only 5% of the total that
exist. The scientific community seemsalso to be
awakening to the fact that the number of sysACKNOWLEDGMENTS
tematists is inadequateto perform the work that
is stil needed. In recent years a number of
I thank Bruce F. Eldridge and John D. Edman
scientists have called for national or global bio- for their suggestionsin preparing the Memorial
logical surveysand have arguedfor gteater sup- Lecture, Sharon L. Belkin for providing photoport of systematicsthrough the creation of po- graphs,and Sandra S. Shanks and Mary Ann
sitions, the funding of researchand the training Tenorio for preparation ofthe graphs.
of students. Many biologists attach great urgencyto these matters becausethe growing huREFERENCES CITED
man population is acceleratingthe rate at which
habitats are being destroyed and species are
S. J. and J. H. Belkin.1978.Collection
Heinemann,
going extinct. Some estimate that 25 to 50% of.
of MiddleAmerrecordsof the project"Mosquitoes
the
within
the specieson earth will be extinct
ica." 10. Panama,includingCanalZone(PA,GG).
next 30 years. Some even seethis mass extincMosq.Syst.10:119-196.
tion of biological diversity as a threat to the Simpson,G. G. 1945.The principlesof classification
and a classificationof mammals.Bull. Am. Mus.
survival of human civilization.
Nat. Hist.85:1-350.
The future will be, I believe,exactly what the
eral speciesgroupsin the generaAedes,Anophelesand Culex. lntercstingly, most gamma level
taxonomic work done in the United States is
done by individuals who do not consider themselvesto be taxonomists. They are instead vector biologists,geneticists,evolutionistsor ecologists. I used the genusAedes as an example
earlier, so let me use it again by saying that the
various studies of groups of Aedes that have
been done in the laboratoriesof GeorgeB. Craig
and Karamjit S. Rai at the University of Notre
Dame are among the finest gamma level taxonomic studies ever done on mosquitoes.