Comments on Population Dynamics of Exotic Insects
By
ROBERT VAN DEN BOSCH
Division of Biological Control, University
of Califorttia, Ber~>eley
This paper is a commentary on the recent article
"Population Dynamics of Exotic Insects" by A. D. Turnbull (1967) which treats largely of the competitive displacement principle, DeBach (1966), DeBach and Sundby
(1963). Dr. Turnbull has used this latest publication as
a vehicle to reiterate his concern over the possible adverse
effects of competition on biological control agents. In an
earlier publication, Turnbull and Chant (1961), this concern was expressed in relation to the multiple introduction of entomophagous species which they considered bad
practice. Now competitive displacement has been seized
upon as perhaps another illustration of the unfavorable
effects of competition. But in exploiting a situation that
seemingly supports this position the author appears to
entomophages introduced against indigenous pests. If this
is the case then his argument bears considerable legitimacy
for exotic entomophages are generally poorly adapted to
indigenous hosts and the latter are often attacked by complexes of native natural enemies with clear competitive
advantage. But there is nothing in the paper to indicatc
that the author is talking to this obvious point (i.e. the
introduction of exotic enemies against indigenous pests),
and whatever his objective, his discussion contains unfortunate statements and implications that cannot be left
unanswered.
have
The inordinate amount of failure in natural enemy introductions deserves discussion because there appears to
be considerable misunderstanding concerning the factors
that contribute to it.
sacrificed
perspective,
\vhich
in
turn
has
led
into
serious error. Honest error is understandable, even excusable, and Dr. Turnbull's errors would not be particularly
bothersome if they comprised the only flaw in his paper.
But error in this case has led to certain statements and
implications concerning biological control which if left
unchallenged stand to do considerable and perhaps permanent harm to that highly important field of pest control. This is what has induced me to expend time and
effort in rebuttal.
In the introduction to the paper (Turnbull, 1967) various types of invading exotic species including deliberately
introduced biological control agents are discussed. The
author correctly points out that among the many introduced entomophagous species, relatively few have become
established (about 1 in 10). He then states that the
causes of such failure are unknown but that "speculative"
reasons given for failure are (I) climate ("the usual
scape-goat") and (2) lack of some requisite in the environment ("another favorite explanation").
Quite obviously he does not place much credence in these explanations, the arguments for which he dismisses as lacking
conviction (climatic explanations)
or as not being very
satisfactory (lack of essential requisites). Following this
the author moves very quickly into a treatment of the
competitive displacement principle which he discusses in
considerable detail. Finally he arrives at his main point,
the relevance of competitive displacement to biological
control. It is here that he commits a fundamental error
with his astonishing assumption that exotic entomophages
are typically introduced into areas already populated
by highly competitive incumbent natural enemies. This,
he suggests, might be the reason why so many biological
control projects have failed. This is, of course, wrong
because exotic pests characteristically are not attacked by
effective natural enemies in the invaded environments and
therefore competition from such species is rarely a factor
where exotic entomophages are colonized. This is the
basis of classical biological control (i.e. natural enemy
introduction)
which typically involves an invading pest
species that has escaped its natural enemies and flourishes
because incumbent enemies do not meet and effectively
attack it. Thus, exotic entomophages obtained from the
pests' area of indigineity are introduced to fill the vacuum
and do this with reasonable frequency, DeBach (1964).
It is possible that I have misinterpreted Dr. Turnbull's
intent and that he is directing his discussion to exotic
FACTORS AFFECTING
ESTABLISHMENT
OF
EXOTIC ENTOMOPHAGES
I do not contest the obvious fact that failures have far
outnumbered successes. The record is clear. But this
record is misleading for it does not show that a significant, perhaps even major, proportion of the introduccd
entomophages never had a chance of establishment and
never should have been introduced. This relates in considerable measure to the fact that a great many of these
species though originating in foreign lands, often in the
pest's native habitats, were really poorly adapted or not
at all adapted to the species against which they were
introduced.
This point can be illustrated by analyzing the natural
enemy introductions made against the citrus black scale,
Saissetia oleae (Bern) in California. By 1955 thirty-eight
species of natural enemies had been introduced against
this pest, fifteen of which had become established, van den
Bosch et al' (1955). However, today only one of these
species, M etaphycl/s heivolus (Compere), is of major importance as an enemy of the scale. The genus Saissctia
is indigenous to East Africa and presumably this is the
area where its adapted natural enemies occur. Yet in the
course of the biological control campaign against S. olcae,
parasites and predators were imported from such remote
(and improbable) places as Brazil, Argentina, Australia
and Tasmania. Almost surely many of the species which
were obtained in these latter areas attacked black scale
adventitously and were principally associated with other
homopterous species. Their introduction into California
was pretty much a predestined exercise in futility and yet
they appear on the record as failures or at best partially
effective introductions. There is even the probability that
some of the parasites obtained in Africa, ostensibly frol11
S. oleae, were not from that species at all. For example,
in my own experience in Eritrea, I collected abundant
parasite material from what I thought to be S. oleae infesting bark fissures and wound scars on Vernonia
a11ljlgdalina Del. Fortunately while in East Africa I was
able to consult with the coccidologist, Giovanni De Lotto,
who was then working on the systematics of Saissetill.
Doctor De Lotto expressed considerable
doubt that
the population of Saissetia found in cryptic situations on
V. amygdalilla, though morphologically very similar to
S. oleae, was indeed that species. Information contained
112
in a paper on East African Saissetia, De Lotto (1956),
strongly indicates that the Verollia infesting scale was
Suisse/ia persimilis (Newst.).
Thus, had I not visited
Doctor De Lotto the chances are that a variety of
parasites of S. persimi/is might have been sent to Califomia on the premise that they were from S. oleae.
There is reason to believe that throughout the history of
hiological control parasite material of this sort has been
recurrently colonized against a wide range of pest species.
One has only to look to the wide spectra of species introduced against pests such as the gypsy moth, the brown
tail moth, the European com borer, and the citrus red
scale to have his suspicions aroused.
The important point is that a considerable portion of
the natural enemies introduced against S. oleae, and an
array of other pests, had little or no chance of establishment and never should have been introduced. But these
"born losers" are all charged to the negative side of the
ledger and they fatten the statistics which show that the
practice of natural enemy introduction is largely futile.
A number of other factors have doomed natural enemy
introductions in a variety of biological control programs.
These factors include inadequate information, indifference,
lack of persistence, and technical difficulty.
TIHldeqllu/e illformation.' I am sure that all of us in the
field of biological control have made mistakes through
ignorance. For instance a colleague and I once made a
futile effort to establish Apantcles flavicollcllOe Riley on
the alfalfa caterpillar, Colias el/rythellle Boisd. in central
and southem California. The A. flm,ieo/lchae material
had been obtained from Colias philodice Latr. in the
southern U.S.A. What we did not know was that C.
philo dice and A. flavicollchae already existed in the north
eastern (Great Basin) part of Califomia (Hagen and
van den Bosch, unpublished data). We still do not know
the reasons why C. Phi/odice and A. flm'icollchae have not
moved into the lowland areas of California, but without
question ecological factors (perhaps even competitive displacement of C. pllilodice by C. ellrytheme) have played
an important role in this situation. In trying to introduce
.-1. flavicollclrae into these areas we were probably beaten
from the start but didn't know it. We are embarrassed
by our ignorance but this doesn't alter the fact that A.
flaviconchae appears on the list of failures in parasite
introduction.
Of course, ignorance has had its real impact on natural
enemy introduction where persons totally unprepared to
do so have undertaken such activity. It is difficult to
estimate how widespread this has been and I am certainly not going to cite specific cases (although this could
be done). Suffice to say, ignorance has contributed its
bit to the failure of natural enemy introductions.
[ndif!erellce.' This factor has largely occurred where persons or agencies normally involved in other aspects of
applied entomology have been charged with the responsibility of colonizing natural enemies. Again, for discretionary reasons I will not cite specific cases. But I cannot resist recounting how a former colleague (essentially
concerned with citrus pests) once described his efforts
to colonize parasites of a vegetable pest in one of the
torrid California desert valleys. His technique was to
drive (slowly?) by the colonization site letting the wasps
dribble into tlle furnace heat as he held the containers
out the car window. Needless to say this was another
failure in parasite introduction. Admittedly this anecdote
describes an extreme case but it also symbolizes indiffer-
ence which has contributed
natural enemy introduction.
to a number of failures
in
Lack of persistence.' This factor is not simply the trait
of the sloven. Indeed, even the most dedicated and energetic person becomes discouraged when after months or
even years of effort to establish seemingly promising species success is not attained. A point arrives in any program when a decision must be made to cease colonizations, either because establishment has occurred or because the weight of evidence indicates that it will not.
In many, perhaps most, cases when the latter decision is
made it is probably correct. But one is often left with
the uncomfortable feeling that if things had only been
done differently or if the effort had been carried on a bit
longer success might have been attained.
An experience from my own career might serve to
illustrate this point. This concerns thc program against
the spotted alfalfa aphid, T herioaphis trifolii (Monell).
In the first year of parasite colonization against this pest
only negative results were obtained. This was puzzling
because seemingly adequate numbers of parasites had been
released in a variety of locations under reasonably favorable conditions. But quite obviously something was wrong.
Either the California environment was unsuitable for the
parasites or our colonization technique was faulty. We
were at a point of decision to quit or go on. We decided
on the latter but changed thc colonization tactic from that
of rather random distribution of wasps in commercial
alfalfa fields, to one of heavy and repeated colonization in
limited plots over which complete control was exercised.
This proved to be the right decision and it quickly changed
gloom to elation as the wasps established themselves and
spread with incredible swiftness out of the colonization
sites, van den Bosch et al. (1959). But I still shudder
when I think that our decision might have been to give
up and I wonder how many times such a wrong decision
has been made in biological control programs.
Tee/mical problems.' If entomophagous species cannot be
produced in sufficient numbers to assure adequate colonization stocks, their chances for establishment are essentially doomed. Some species simply are not amenable to
insectary propagation, others are obligate parasites or
predators of hosts which cannot be grown under artificial
conditions. Diapause in host and parasite stocks can severely limit or even preclude effective propagation of the
latter. These factors and others (e.g. complex biologies,
lack of proper facilities or qualified insectary personnel)
have, in the past, affected success in natural enemy introduction and will continue to do so in the future.
The climatic "scapegoat" alld other "favorite exPlallatiolls." From the preceding discussion it should be apparent that a varicty of factors work against successful natural encmy introduction even before the animals are turned
loose or at the time of their release. Then when they are
thrown into the natural environment they have to run a
gamut of hazards as do all invading species.
Climate, of course, is of paramount importance. This
can be illustrated by the fate of the introduced parasites
of the spotted alfalfa aphid in California. This program
involved three species, Trioxys complallOtlls Quilis and
PraOl~ exsoletllm Nees (Aphidiidae) and Aphelilllts asychis Walk. (Aphelinidae).
All three became established
in California but not in all areas where their host thrives.
For example P. exsoletlt1n and A. asychis cannot survive
the torrid heat of summer in the low desert valleys of
California since they do not have the ability to diapause
113
during that hostile time of year. Thus, these two species
have not become established in the Imperial, Palo Verde
and CoacheIla VaIleys. By contrast, T. complanatus
which is also sensitive to high temperature, Force and
Messenger (1964), survives the summer period in diapause and by virtue of this attribute has become an abundant and effective parasite of T. trifolii in the desert
valleys, van den Bosch, et al. (1964).
The important point here is not that T. complanatus
survives and thrives in the desert environment, but that
P. exsoletum and A. asychis cannot. In other words this
is clearly an instance in which climate has prevented the
establishment of two fuIly (host) adapted parasites even
where their host is abundant. It takes little imagination
to realize that if these two species were the only ones
colonized in California there would not now be parasitization of the spotted alfalfa aphid in the important alfalfa
growing vaIleys of the low desert.
I feel it unnecessary to expend time and effort to discuss additional cases in which climate has precluded establishment of natural enemies since the case just cited estab-
lishes the point.
Similarly, I wiIl only aIlude to a single case in discussing that "favorite explanation";
(the absence of) key
requisites.
Since the key requisite of any imported natural enemy
is the availability of a suitable host, perhaps it is best to
discuss the subject in this context. To do so we have
only to look to the program involving the Mexican bean
beetle, Epilachna varivestis Muls. Here a parasite, Paradexoides epilachnae Ald., obtained in Mexico performed
most promisingly during several seasons of liberation.
But invariably during the ensuing winters when its host
passed into diapause P. epilachnae, which did not do so,
faded away because the environment lacked an alternative
host (key requisite) on which the parasite could bridge
the period when E. varivestis was not available to it,
Landis and Howard (1940).
Other requisites such as food for parasite adults, shelter,
hibernating or aestivating places, etc. can undoubtedly
affect the fortunes of introduced entomophages. For example, it is difficult to envisage certain coccinellid species,
that require special diapause quarters being established
in areas devoid of such piaces (e.g. mountain peaks).
CONCLUSIONS
In the preceding discussion an attempt has been made
to illustrate through examples from personal experience
and from published accounts, the considerable array of
factors that legislate agail1st establishment of introduced
natural enemies. I tried, in particular, to point out that
these limiting factors are only in part characteristic of
the new environment and that they come into effect in
significant degree even before the parasite or predator is
colonized.
It should be apparent to all that the feeble record of
natural enemy establishment is an inaccurate measure of
the establishment potential of highly adapted species. The
poor results of record largely reflect the fact that we
oftentimes have l:olonized the wrong animals, handled
them inefficiently or indifferently, or released them in inadequate' numbers or under improper circumstances. Inimicable factors in the environment have also taken their
toll. But competitive disPlacement has not contributed
importantly to this record of failure because in the overwhelming nttlllber of cases the introduced nat1trat enemies were colonized against species that were free of sig-
nificant highly-adapted Ifatural memies. This is why introductions were attempted; it is the very basis of natural
enemy introduction.
Even in the one authenticated case of competitive displacement, this factor did not preclude establishment of
the newly introduced species. Instead, it resulted in the
replacement of the incumbent species or caused their populations to recede to ecologically optimum areas. The end
result was beneficial (from man's standpoint) because it
brought about better overaIl biological control of a serious
pest, De Bach et al. (1962).
The introduction of natural enemies is a complex affair
and no matter how hard we try or how sophisticated our
methods a considerable degree of failure can be expected.
But the flat statement in TurnbuIl (1967) that "The
chances of establishing a foreign entomophage in a new
environment are always small" is clearly wrong. The
record shows that the right species colonized in the right
way have considerable chance of establishment and furthermore that they have the potential to do substantial
good, DeBach (1964).
This discussion cannot be terminated without treating
of Mr. Turnbull's closing remarks. He states that in the
introduction of exotic entomophages, "We are not concerned with population diversity but with maximizing a
single species-our
crop; not with stabilizing pests, but
with suppressing them. For these purposes we need specific agents to carry out specific tasks. The chances of
finding such agents without knowing what characteristics
they should possess are not impossible, but they are certainly remote. In fact, we have little reason to suspect
that such organisms exist."
The last sentence is absurd. The record of successful
natural enemy introduction, as poor as it is, clearly shows
that quite a few such organisms do indeed exist. The
challenge before us is to increase our efficiency in seeking
out the right species and through a variety of techniques
and manipulations, maximize their chances for establishment in the new environments.
'
REFERENCES
CITED
DeBach, P. 1964. Biological Control of Insect Pests and
Weeds. Chapman and Hall Ltd., London. 844 pp.
DeBach, P. 1966. The competitive displacement and
coexistence principles. Ann. Rev. Entomol. 11: 183212.
DeBach, P., J. Landi, and E. B. White.
1962. Parasites
are controlling red scale in southern California citrus.
Calif. Agric. 16(12) : 2-3.
DeBach, P., and R. A. Sundby.
1963. Competitive displacement between ecological homologues. Hilgardia
34: 105-166.
De Lotto, G. 1956. The identity of some East African
species of Saissetia (Homoptera,
Coccidae).
Bull.
Entomol. Res. 47: 239-249.
Force, D. c., and P. S. Messenger.
1964. Fecundity, reproductive rates and innate capacity for increase of
three parasites of Therioaphis maculata (Buckton).
Ecology 45: 706-715.
Landis, B. ]., and N. F. Howard.
1940. Paradexodcs
epilachllae, a tachinid parasite of the Mexican bean
beetle. U.S. Dept Agric. Tech. Bull. 721, 32 pp.
Turnbull, A. D. 1967. Population dynamics of exotic
insects. Bull. Entomol. Soc. Amer. 13: 333-337.
Turnbull, A. D., and D. A. Chant.
1961. The practice
and theory of biological control of insects in Canada.
Canad. Jour. Zool. 39: 697-753.
114
van den Bosch, R., B. R. Bartlett, and S. E. Flanders.
1955. A search for natural enemies of lecaniine scale
insects in northern Africa for introduction into California. Jour. Econ. Entomol. 48: 53-55.
van den Bosch, R., E. I. Schlinger, E. J. Dietrick, K. S.
Hagen, and J. K. Holloway.
1959. The colonization and establishment of imported parasites of the
spotted alfalfa aphid in California. Jour. Econ. Entomol. 52: 136-141.
van den Bosch, R., E. I. Schlinger, E. J. Dietrick, J. C.
Hall and B. Puttler.
1964. Studies on succcession,
distribution and phenology of imported parasites of
Thl'rioaphis trifolii (Monell) in southern California.
Ecology 45: 602-621.
AN ANNOTATED LIST OF SELECTED DEALERS
IN ANTIQUARIAN
ENTOMOLOGICAL
LITERATURE
ANDR.FRED.IIj!lST & sj!lN, 35 Bredgade, Copenhagen, Denmark. Large insect section in their frequent Zoology
catalog. American and European publications, mostly
books of recent date.
II. E. KNOWLES,23 Hemberton Road, London S.W.9, England. Small independent book dealer with good selections of European invertebrate literature. Moderatelypriced selections, Remittance not required with order.
OTTOKOELTZANTIQUARIAT,P.O.B. 129, 624 KoenigsteinTsjWestern Germany.
II. K. LEWIS & co., Ltd" Scientific Books, 136 Gower
Street, London W.e. 1, England. New scientific books,
very large stock, quick delivery on new English books.
No antiquarian department, small second-hand department. Not really good on entomology. Payment with
order.
ANTHONYD. LILLY, Charenton, Cliff Road, Hythe, Kent,
England. Very small antiquarian dealer, sells from own
home, personal service, travels frequent!y .and .will look
for out-of-the-way items. Actually specializes 111 botany
and zoology other than entomology, but often has very
nice entomological items. Prices very low.
ERICLUNDBERG,
Ashton, Maryland 20702. General natural
history, good used and antiquarian. Reasonable prices,
personal service. Often very fine antiquarian entomology items at low prices.
MULLER& GRAFF,Stuttgart-N,
Calwer Strasse 54, Germany.
NATURALIIISTORYBOOKS,John Johnson, R.F.D. 2, North
Bennington, Vermont 05257. General natural history,
few really antiquarian items, good "used." Not too
many entomological books.
J. P. DONAHUE,R. J. SNIDER,ANDR. S. WILKINSON'
East Lansing, Michigan
This list of dealers in antiquarian (old) entomological
publications has been compiled to assist .individuals in locating sources of old, rare, or out-of-pnnt books and reprints in the field of entomology.
All the dealers noted here provide free catalogs and
price-lists-simply
tell them what your particular interests
are for some have more than one catalog. If you can not
find the book you want, most of these dealers will be
pleased to file your order and notify you when the book
becomes available.
Orders should be placed IMMEDIATELY
after you receive
a catalog-choice
items go very quickly, and a telephone
call often assures success. For less rare items, an order
on a letterhead is usually sufficient-you
will be invoi~ed
with the shipment. This method is preferred by foreign
dealers, so that they will not have to bother with refu?ding dollars if part of your order cannot be filled. Foreign
dealers often have rare American publications at bargain
prices.
Annotations are given below only for those dealers with
which the compilers are personally familiar.
ANTIQUAIUAATJUNK, Postbus 5, Lochem, Holland. A
very large stock of antiquarian items; good supplier
for new Continental books. General natural history
with a specialty in entomology. Antiquarian prices tend
to be slightly high. Payment on invoice unless account
established.
PIERCE BOOK COMPANY,
A. ASIIER & CO.,386 Herengracht, Amsterdam-C, Holland.
J. N. BARTFIELD,
Natural History Books, 45, We~t 57th St.,
New York, N.Y. 10019. A general antlquan~n dealer,
library specialist, not a really large entomologJca stock,
but often has nice antiquarian items, color-plate books.
Prices can be high but are usually reasonable for the
items handled. Payment with order.
E. J. BRILL, Oude Rijn 33a-35, Leiden, Holland. Large
Dutch publisher, specializing in new mon,ographs and
reprints. Numerous African works on agnculture, botany entomology, archeology, natural history available.
A ;ather select offering of old reprints offered from
time to time. Book lists sent monthly.
E. W. CLASSEY,353 Hanworth Road, Hampton, Middlesex,
England, Small dealer, personal service. Laq~e stock
of antiquarian entomology; very reasonable pnces, can
supply new and in-print English books at !ower. than
American prices. Many hard-to-get Amencan Items,
good on want lists, will purchase at sales. Normally
entomology only. Payment with order unless arranged
otherwise.
R. FRIEDLANDER
& SOliN, Berlin-Charlottenburg
2, Knesebeckstrasse IS, Germany. Predominantly North European selections. Prices moderate to high. Or~ers fill.ed
with restrained dispatch. Remittance not reqUIred With
order.
'This Ii.t was compil<d for the Entomological Society of
Michigan. Copies are available free by sending a self.addressed
.tamped envelope to the Michigan .Ento.mological Societr, Dept.. 0l
Entomology, Michigan State Umverslty, East Lan.lOg, Mich.
48823.
Winthrop,
Iowa 50682.
BERNARDQUARITCHLtd., 11 Grafton Street, New Bond
Street, London W. I, England. A famous general antiquarian dealer with a very large natural history stock,
much entomology in all price ranges. Catalogs are very
useful bibliographically.
QUIVIRASCIENTIFICCOMPANY,P.O. Box 2029 (4204 West
21st St.), Topeka, Kansas. Large midwest book dealer.
Most of the material offered is of recent vintage. Very
little European literature. Catalog published occasionally, with supplements.
STECHERT-HAFNER,
INC., 31 East 10th Street, New York,
New York 10003. Large publisher of major zoological
classics. Catalog sent once or twice yearly. Very few
old singles available.
HENRY TRIPP 92-06 Jamaica Ave., Woodhaven, New
York 1142i. Very reasonable prices, good stock of
hard-to-get American antiquarian items in entomology,
large stock of recent and in-print books and journ!1ls.
Good on want lists. (Member of the EntomolOgical
Society of America.)
JACK WEINSTEIN,P.O. Box 4, New Lots Station, Brooklyn, New York 11208.
WIiELOON& WESLEY, Lytton Lodge, Codicote, Hitchin,
Herts., England.
England's largest. natural hist«;>ry
dealer, antiquarian and good used. Pnces can be high
but in most cases are reasonable. Very useful catalogs.
One of largest stocks of antiquarian entomology in
world.
CII. DE WYNGAERT,
296 Avenue Georges Henry, Bruxelles
15, Belgium.
115