Вы находитесь на странице: 1из 16


Scope and Significance of Biological Control

Center for Biological Control
201 Wellman Hall
University of California
Berkeley, California

The amount of food for each species of course gives the as relatively fixed or subject to [and altered by] evolution-
extreme limit to which each can increase, but very fre- ary change?" These are questions various authors in this
quently it is not the obtaining of food, but the serving as book have considered and have offered some insights.
prey to other animals, which determines the average num- DeBach's usage of biological control in the antecedent vol-
ber of a species. Darwin on the Origin of Species (1859) ume to this book (DeBach, 1964a) was "demographic and
ecological in context but does not explain the mechanisms
of control or regulation."
Biological control when considered from the ecological Bellows and Fisher's preface to this book discusses the
viewpoint as a phase of natural control can be defined as various concepts of biological control and its implications
the action of parasites, predators or pathogens in maintain- in practice. This section also details the beginning of curric-
ing another organism's population density at a lower av- ular biological control at the University of California and
erage than would occur in their absence discusses the antecedent volume on this subject edited by
P. DeBach (1964, p. 6) DeBach (1964b) for its historical relevance. Readers of this
chapter should be sure to read that preface as a prelude to
this introductory chapter and the rest of the book.
There are some rather basic differences among some
chapter authors relative to what is meant by biological
Biological control has commonly had both pure and control, and in other cases the value of different approaches
applied definitions and connotations. In this book the au- to evaluating the role of natural enemies. For example,
thors adhere mostly to DeBach's quotation, with the pro- Federici in Chapter 21 includes as biological control certain
viso that parasites, predators, and pathogens include "antag- biotechniques not accepted as such by the authors of many
onists" of plant pathogens. The significance of biological of the chapter. Also, the methods of evaluation of natural
control is clear in the quotations from both Darwin and enemies utilized by certain authors in the book Critical
DeBach, residing in the roles such natural enemies have in Issues in Biological Control edited by Mackauer, Ehler,
determining the densities of other organisms in nature and and Roland (1990) differ distinctly from those described in
thus their impacts on their environments. Chapter 2 by Bellows and Hassell, in which they consider
Huffaker and Rabb (1984) considered, "Nature as a that theories of interactions "accord well with observed
complex of interacting systems is widely accepted, but outcomes of experimental populations in both laboratory
many questions remain as to how these systems are ar- and natural settings," especially so for simpler systems.
ranged and to what degree they are interdependent. To what DeBach and Rosen (1991) give data on some 164 spe-
extent are structure and function deterministic or probabilis- cies of insect pests being permanently controlled by intro-
tic? To what degree should we treat elements of the system duced natural enemies (classical biological control): for 75

Copyright 9 1999 by AcademicPress.

Handbookof BiologicalControl All rights of reproduction in any form reserved.
2 C.B. Huffaker and D. L. Dahlsten

species "complete," for 74 species "substantial," and for 15 does not describe the discipline of biological control, which
species "partial" control. Because many of these species is broader and includes what the profession must do (see
were also controlled in more than one country, they noted Chapters 40 and 41). In that same antecedent volume the
that up to 1988 there had been some "384 successful proj- density-regulating roles of natural enemies and the mecha-
ects worldwide." They also state: "This is by far the greatest nisms were discussed by Huffaker and Messenger (1964),
number of successes achieved by any one non-chemical including interdependencies and deterministic or probabilis-
method, with the possible exception of cultural control, tic features, for different types of habitats and weather.
which to our knowledge has not been tabulated." All other These ideas are used and modified by various authors in
nonchemical methods combined would add only a few pest this book.
species up to now. It was noted that nearly one-third of the Biological control of other organisms is exemplified far
species first controlled in a country were again controlled beyond entomology. Its research and practice have been
in other countries. Information is drawn from works of greatly expanded relative to plant and animal diseases and
DeBach (1964a), Clausen (1978), Laing and Hamai (1976), weed control. It was also utilized very early in attempts to
and Luck (1984); and from BIOCAT information furnished control rats, for example, by use of the mongoose. Davis et
by D. J. Greathead in 1988 and "some additions from their al. (1976) also dealt with the use of other vertebrates to
own records." control vertebrates, and with the use of disease for control
With the preceding records of "4 successes in 10," di- of European rabbit hordes in Australia. Since then, biolog-
rected against only 415 pest species, it is an indictment of ical control has become an increasingly strong component
environmentally interested sponsorship worldwide that in a broader vital area, that of conserving and promoting a
none of the others among some 10,000 species of insect viable, sustainable agriculture, forestry, and biosphere (see
pests (95%) have been investigated for possible importa- Chapters 26, 29, 34, and 36 to 39).
tions. Moreover, DeBach and Rosen (1991) note that of To regulate a population, factors (singly or in combina-
some "4226 natural enemy species introduced worldwide, tion) must act either in a direct density-dependent way
1251 have become established, 2038 failed, and the fate of (Huffaker et al., 1971; Huffaker et al., 1984) or in an
932 is still unknown." This gives an establishment rate of inverse density-dependent way associated with prey patches
"38% of those with known outcome." Yet, clearly it is not within a host generation (Hassell, 1986). Huffaker et al.
the percentage, or number, of species established, but the (1984) dealt at length with the functioning of natural con-
success of the project that is important. As often happens, trol in general, and with the roles of the specific density-
a highly effective species may displace or prevent establish- dependent regulating performance of various natural ene-
ment of less effective competing species, and better biolog- mies or other negative feedback processes. They noted that
ical control commonly results (see "competitive displace- even while some such natural control factors may be re-
ment," Huffaker & Messenger 1976; also DeBach & sponsible for density regulation in a specific limited time
Sundby, 1963; Huffaker & Kennett, 1969). Also, Huffaker and place frame, evolutionary processes may be operating
et al. (1971) present specific cases where competitive dis- to alter the case in time (see Chapters 12, 13, 15, and 23).
placements have improved biological control, often with They presented a chart illustrating that intraspecific com-
reductions in the complex of enemy species in the system. petition of predators for prey and the linked intraspecific
Successes worldwide have been directly related to the competition of the prey for hiding places or predator-free
effort expended; for this reason only, such areas as Hawaii space can explain the various manifestations of density
(31), California (24), the rest of the United States (20), regulation for specific biotic and abiotic conditions. They
Chile (16), Australia (13), New Zealand (13), Canada (11), also cited several authors who refer to competition for en-
Israel (11), France (11), and Mauritius (10) have had cor- emy-free space as a means of reducing the species diversity
responding degrees of success. Moreover, DeBach and Ro- of herbivorous insects on a particular plant species. Yet,
sen (1991) conclude that the costs of biological control most of the authors of chapters in this book dealing with
importations are very low compared to the costs of devel- theory of natural-enemy control of prey (or host) species
oping pesticides, which are offering declining rewards, and look at it as linked predator,prey population interaction
that if all countries expended the effort on biological con- and do not consider it one of prey competing for predator-
trol that "the leading twelve [do now] the number of prob- free places. We also present here in Fig. 1, Huffaker et al.'s
lems solved would jump enormously." As seen in this vol- illustrations of various density-related performance func-
ume, classical importations include only a part of modem tions for insects and other relevant factors.
biological control. Nechols (1995) discusses the accom- In this volume, considerable general attention is given to
plishments and benefits of a number of W-84 control proj- the question of evolutionary processes, for example, in
ects in the western United States from 1964 to 1989. Rosen Chapters 15 and 23, and to the question of pesticide resist-
and DeBach (1991) discuss the importance foreign explo- ance in Chapters 13 and 24.
ration plays in classical biological control. It is important now to place the forms of biological
DeBach's definition of biological control (cited earlier) control in the context of animal and plant protection
Chapter 1 S c o p e a n d Significance of Biological Control 3

40 E 1 2 4 8
10 5O C
3 (a) i~ 0 . 8 -3

40 N
2O <m 0 . 6 , ,,z,
ao o.4
< b) ~z -3
2s so _

20 >0.2
D ~ (b)
r.n 0
10 0 50 100 150 200
(c) % ~ # ~ o ~ "
i l , llll,l ' ' ' I .... l . . . . . . . . I . . . . . . I
i i
00 I0
5 1 oo 150 ~ -41 10 100 1000

! D
.< ~ 0.6 v 40
o <
~-k (b) o
~ 0.02 o= ao o
I1. 0 . 4
kU ~ 0 0 0 0 I-.
0 o 20
C) 0.01
,,,,,I ~ ~ o.2 u.
I,U (a) '~, olo
LU w
oo , , , I . i , , 00
100 200 300 400 ' 2~5 ' 50 % 4'0 ' 8'0

FIGURE 1 Some density-related performance functions of various insects. Effect of population density (abscissa) on (A) the number of eggs laid by a
bark beetle, (a) Dendroctonus pseudotsugae (McMullen & Atkins, 1961), a flour beetle, (b) Cryptolestes (Varley et al., 1973), and a psyliid, (c) Cardiaspina
albitextura (Clark, 1963); (B) the developmental rate of Endrosis sarcitrella (Anderson, 1956); (C) the probability of survival of a grain beetle, (a)
Rhizopertha dominica (Crombie, 1944) and the blowfly, (b) Lucilia cuprina (Nicholson, 1954); (D) the proportion of females of (a) Bracon hebetor
(Benson, 1973) and (b) Nasonia vitripennis (Walker, 1967); (E) the host-searching efficiency (logl0a) of (a) Pseudeucoila bocheri parasitizing Drosophila
larvae (Bakker et al., 1967), and (b) Nemeritis canescens parasitizing Anagasta kuhniella (Hassell & Huffaker, 1969); and (F) the sigmoid relation in
number of hosts attacked by (a) Aphidius uzbeckistanicus parasitizing the aphid Hyalopteroides humilis (Dransfield, 1975), and (b) mosquito larvae attacked
by the waterboatman, Plea atomaria (A. Reeve, unpubl., from Hassell et al., 1977). Note: These latter show the effect of increase in prey density in
attracting a greater intensity of predation. (After Huffaker, C. B., Berryman, A. & Laing, J. E. [1984]. In C. B. Huffaker, & R. L. Rabb (Eds.), Ecological
entomology, (p. 375). New York: John Wiley & Sons.

schemes often discussed today. Figure 2 from Garcia et al. We also reproduce in Fig. 3 a diagram from Krebs
(1988) presents this in terms of biological, cultural, and (1972) of the general areas of biology that interact and
chemical control methods. It is seen that we view true overlap in the ecology of any organism. The four areas of
biological control as that which is self-sustaining or par- genetics, physiology, behavior, and evolution impinge
tially so; and that which is achieved by parasites, predators, strongly as shown. Behavior is often directly classed as
and pathogens, including antagonists of plant pathogens. ecology, and physiology and ecology interact in ecophy-
There are three forms r e c o g n i z e d - - t h a t which is naturally siology. Genetics lies at the roots of each of the other
self-sustained, that in which augmentation is utilized, and expressions and evolution is the product of change in any
that which uses conservation of natural enemies through of these over time. We define ecology as the total relation-
management practices. While "autocidal" methods and ships of organisms with their e n v i r o n m e n t - - w i t h their own
breeding for host-plant resistance are biotechniques, they kind, with other organisms, and with the abiotic factors.
do not utilize parasites, predators, or pathogens and they Huffaker et al. (1984) noted: "Ecology's special domain
are not self-sustaining. Note, too, that breeding, selection, has become the analysis of a great variety of e c o s y s t e m s :
and genetic engineering may result in improvements that subdivisions of the global environment containing a re-
could become useful in several of the plant protection meth- stricted number of living species adapted to survive within
ods, including that of true biological control. well defined abiotic and biotic conditions." Often, the pop-
4 c . B . Huffaker and D. L. Dahisten

ulations inhabiting an ecosystem can only be estimated species occurring in patches that differ in density, or to
from samples and mathematical estimates of densities, and switching in multiple prey species (complexes) as a fre-
spatial distribution tends to be abstract and probabilistic. quency-dependent response, and competition in the prey
Yet these methods sometimes offer enough prediction to be species." It was only through the exploitation of prey
useful in making pest control decisions. patches that such stabilization was envisioned. Luck, Shep-
The question of risks and conflicts of interest in intro- ard, and Kenmore see little of value in any of the mathe-
ducing biological control agents presents a variety of con- matical approaches, but see their Chapter 9 in this book.
cerns, greater in the case of biological control of weeds Huffaker (1988) also reviewed in a general way the
than of insect pests, but of concern in any case (e.g., Cal- question of ecology of insect pest control. Theoretical pred-
tagirone & Huffaker, 1980; Price et al., 1980; Batra, 1982; ator-prey models were not dealt with, but the work of
Julien, 1982; Howarth, 1983; Clarke et al., 1984; Maws, Teng (1985) was considered a supplemental and different
1984; Pimentel et al., 1984; Turner, 1985; U.S. Congress, approach. Huffaker and Rosen (1990) dealt with the attrib-
1995; and others). Because of a variety of concerns a sem- utes of effective natural enemies, and Huffaker (1990) re-
inar was organized in 1996 by the United States Depart- viewed the role of weather factors as they may influence
ment of Agriculture (USDA) to draft a plan for the coordi- the host-parasite regulation process. Van Driesche and
nation, regulation, and accountability of biological control Bellows (1996) covered the principles behind biological
within the USDA (Carruthers & Petroff, 1997). Choice of control techniques and their implementation, and incorpo-
target plants and choice of specific biological control orga- rated practical examples from the biological control of a
nisms to introduce against plants are the key decisions for variety of pests.
resolving any conflict of interest. Three major mechanisms
suggested by Turner (1985) are (1) authoritative decision,
(2) mediation, and (3) litigation. Each method has been
Chapter 2
used; for example, litigation over the E c h i u m project in
Australia went to the High Court of Australia before it was The authors Bellows and Hassell deal with theories and
resolved in favor of introducing biological control agents, mechanisms of natural population regulation, starting with
which led to the passage of an enabling act for biological single-species populations; and leading on to interspecific
control. Gutierrez et al. (see Chapter 10) also note the competition, host-parasitoid systems, host-pathogen sys-
difficulty of including in the costs and benefits of biological tems, and multispecies systems. They state that the princi-
control introductions, not only the poorly assessed direct pal aim of biological control is the reduction of negative
costs and benefits (in our projects) but also those to which impact of pest species, including both pest suppression and
the external costs, risks, and benefits can only be surmised. pest regulation. The dynamic behavior involved can be of a
Various chapters in this volume go considerably further in density-dependent nature for the pest and the natural en-
establishing real costs, benefits, and risks of conflicts than emy; and can involve specific search behavior, more than a
was possible in DeBach (1964b). single natural enemy, the patchiness of the environment,
and both behavioral and stochastic interactions (particularly
related to stabilizing populations). The authors develop
PRINCIPLES A N D PROCESSES their chapter according to an analytical framework of dif-
ference equations, but in cases consider also continuous-
Ecology and biological control has had such a long his- time systems. They deal primarily with insect parasitoids,
tory and has been handled in such a diversity of ways that predators, and pathogens, for which there is a large body of
it is not possible to present an exhaustive discussion in one data; and do not deal with insect herbivory effects on plant
chapter. Luck (1984) reviewed the use of three general populations because of the scarcity of suitable data (Craw-
types of mathematical models, "those that treat continually ley, 1989).
growing predator-prey populations (overlapping genera-
tions), those that treat predator-prey populations with non- Chapters 3 through 14 deal rather more specifically with
overlapping generations, and those that view the predation the processes in biological control, although certain other
process as one of resource exploitation (i.e., foraging the- chapters throughout the book bear on such principles and
ory)." Luck concluded that all are "to one degree or another processes and are used for illustrations. Topics dealt with
inadequate." Yet he pointed to the value of such models in in this section are taxonomic and evolutionary closeness
focusing attention on certain assumptions and processes (Chapter 3), molecular methods (Chapter 4), foreign explo-
associated with predation (or parasitism). He noted that ration (Chapter 5), quarantine (Chapter 6), culture and col-
several assumptions appear capable of stabilizing the pred- onization (Chapter 7), evaluation (Chapters 8, 9, and 10),
ator-prey process: "predator aggregation on dense prey manipulation (Chapter 11), genetic improvement (Chapter
patches, spatial and temporal habitat heterogeneity, pres- 12), and enhancement of biological controls (Chapters 13
ence of a sigmoid functional response to a surge of prey and 14).
Chapter 1 Scope and Significance of Biological Control 5




,, , [
.. [
Crop Rotation
Multicropping 4 BIOLOGICAL
Tillage ri CONTROL ~ l
Water M a n a g e m e n t 2 OF NATURAL (Cottony- OF NATURAL
(Others) 3 Klamath Beetle ( M a n a g e m e n t
Screwworm Wheat .Tm'c'h o g r a m, m a
(Klamath Weed) Practices)
(Hessian Fly) (Cornborer)
Fruit Flies
GraDe Encaraia Rust
(Others) (Fhylloxera) (Whitefly) ( C h o n d r i l l a ]unce~
(Others) Virus (granulosis, NP)
l 1

(Plant pathogens)

J /\ Some baculoviruses
I (Rhinoceros beetle)
Some protozoa
Sulfur Copper Sulfate Chlorinated Hydrocarbons Semiochemicals
(Others) (Others) Organophosphates Pyrethrums

Carbamates Rotenone
Pyrethroids Toxins (Bacillus lhuringiensis)
(Others) (Others)
(e. g. breeding and selection, genetic engineering)

1. List not inclusive - Integrated Pest M a n a g e m e n t is not included b e c a u s e it draws f r o m all m e t h o d s .

2. Placed by s o m e experts u n d e r Cultural Control.
3. S o m e varieties have retained r e s i s t a n c e for decades, while o t h e r s lose r e s i s t a n c e sooner.
4. S o m e f o r m s are s e l f - s u s t a i n i n g .
5. Partially s e l f - s u s t a i n i n g .

FIGURE 2 Methods for animal and plant protection, with some specific examples. (After Garcia, R., Caltagirone, L.E., & Gutierrez, A. P. [1988].
BioScience, 35(10), 692-694.)

Chapter 3 era Aphytis and Marietta are very similar morphologically,

but Aphytis species are primary parasites of armored scales
Gordh and Beardsley point to the confusion and mislead- while Marietta species are hyperparasites, and generally
ing inferences about an organism if it is not properly clas- viewed as harmful to biological control. The highly signifi-
sified. A correct name, alone, furnishes much information. cant problems of the identity of various species of Tricho-
Seemingly minor structural differences "can mean the dif- gramma, crucial to their use, are also discussed.
ference between pest and non-pest, or establishment or fail-
ure for a natural enemy." For example, of the species of
Chapter 4
Pectinophora, only P. gossypiella is of major importance
and its ability to diapause within cotton seeds is a major Unruh and Woolley consider molecular methods for bio-
reason for its widespread distribution. logical control, with particular reference to their utility in
Confusion of Aonidiella aurantii and A. citrina in early biosystematics and the study of field populations of insect
work led to many introductions of A. citrina parasites that biotypes. This chapter reviews isozyme electrophoresis; re-
were unsuitable for A. aurantii. The incorrect identification striction fragment analysis; and sequencing of ribosomal
of the coffee mealybug, Phenococcus kenyae, led to years RNA, mitochondrial DNA, and genomic DNA. D N A -
of fruitless effort to achieve biological control from import- DNA hybridization and immunological distances are also
ing ineffectual parasites of two Asiatic Planococcus, discussed.
whereas effective parasites of P. kenyae were already in Very little has been done, for example, on enzyme elec-
Africa and when established in Kenya quickly effected trophoresis of natural enemies of insects, but possibilities
complete biological control. Confusion concerning natural are illustrated by work on the systematics of insects. Insect
enemies is also of great importance. For example, the gen- biological control agents have not been studied using mo-
6 C.B. Huffaker and D. L. Dahlsten

assessment of their capabilities prior to colonization are

The mechanics of organizing and executing foreign ex-
ploration for beneficials are described. Bureaucratic require-
ments at home and abroad for permits, shipping methods,
etc., must be anticipated and followed to expedite safe
arrival of shipments at home quarantine receiving facility.
Personal and technical problems faced by explorers in
the field are briefly discussed.

FIGURE 3 Relation of ecology to other biological sciences. (After This chapter by Fisher and Andrrs on quarantining or
Krebs, C. J. (1972). Ecology: The Experimental Analysis of Distribution
isolation work contains concepts, including principles, fa-
and Abundance. New York: Harper & Row.)
cilities needed, and procedures to be used. They note that
Kahn in 1988 presented a solid and up-to-date review of
the quarantine exclusion process. The authors cover these
lecular techniques for nucleic acids but a few have been areas fully, citing both the important older and newer
studied using the isozyme method. Considerable study has works.
been done on insect viruses and entomogenous bacteria. The principal function of the biological control quaran-
Primarily, this chapter illustrates a methodology for study- tine operation is to fumish a safe area and competent staff
ing natural-enemy species and biotypes with reference to to screen incoming material to exclude unwanted organisms
their ecological capabilities and roles in managed and nat- and determine the identities and biologies of those desired
ural settings. These genetic approaches are needed in bio- to be propagated and colonized. Proving the environmental
logical control to more fully understand and utilize the safety of herbivorous organisms for the biological control
adaptive diversity in populations of insects as natural ene- of weeds can be very demanding and crucial. It is desirable
mies. to conduct these studies in the country of origin; otherwise,
This section deals also with the essentials of classical the entry country must conduct the necessary testing under
biological control: exploration, introduction, culture, colo- quarantine.
nization, and evaluation. The material on this "backbone" Other references cited in Chapter 6 include Coulson and
of biological control work is covered in Chapters 5 to 7 Soper, who in 1989 presented an excellent review of the
and 10, and is outlined briefly here. role of quarantine in biological control. Fisher and Andrrs
deal with (1) national, state, and county regulations; (2)
quarantine laboratory design and equipment; (3) personnel;
Chapter 5
and (4) operating procedures. The authors note that the
Legner and Bellows describe criteria that will help delin- mechanics have not changed appreciably for entomopha-
eate search areas of choice before exploration for ento- gous species since Fisher's account in 1964 (see DeBach,
mophagous organisms begins. Ascertaining region or origin 1964b); thus, the emphasis in this chapter is on weed-
of the target pest or its plant hosts, if possible, will priori- feeding candidates, the area undergoing much expansion
tize areas to be searched. Key considerations are taxonomy, and ever-more-demanding concems for environmental
distribution, hosts of record, biologies of closely related safety and involving close consideration of pathogens.
species, and input from foreign colleagues in the proposed
areas of search. The authors also cite several successful
Chapter 7
biological control programs by organisms secured in areas
other than the native home of the target pest. This chapter by Etzel and Legner is primarily, but not
A generalized categorization of environmental risk fac- exclusively, on insect parasites and predators and relates to
tors associated with introduction of exotic natural enemies three major purposes: (1) permanent establishment, (2) pe-
is presented. Terrestrial vertebrates present the greatest po- riodic colonization and augmentation, and (3) inundative
tential risk, followed by phytophagous arthropods, phyto- releases. The programs needed vary with each of these
pathogens, and terrestrial scavengers. Because of their re- purposes and with the types of organisms. The first goal is
strictive habits, uses of parasitic and predaceous arthropods that associated with successful classical biological control
and pathogens of arthropods are considered the least risky through introductions. The second is illustrated by the phe-
introductions, but even they require careful evaluation from nomenal success with yearly (periodic) spring releases of
several perspectives before being released. Criteria to aid in the parasitoid Pediobius foveolatus for control of the Mex-
Chapter 1 Scope and Significance of Biological Control 7

ican bean beetle in southeastern United States, and by re- distribution). Mortalities from natural enemies and other
leases of the fish Tilapia zillii in irrigation canals for aquatic causes are typically measured as rates and their relative
weed and mosquito-habitat control in southeastern Califor- influences in population growth can be expressed as im-
nia. The third is where very large releases are made to pacts on the net reproductive rate (Ro) of the target popula-
achieve quick reduction of the pest, as with releases of a tion; this rate must be reduced to below unity for the pop-
tachinid parasite of the sugarcane borer, and of hydra ulation to decrease. They note that the marginal attack rate
against mosquito larvae. is the only measure whose calculation permits correct inter-
Host foods used in production are living plants, har- pretation of the impact of factors, even contemporaneous
vested plant parts, vegetables or fruits, and prepared diets. mortality factors, between different systems.
The choice to be made depends on the species of the host The authors also discuss various means of using methods
and its intended use. Prepared diets have perhaps been the for analyzing joint host-parasitoid systems, for dealing
most researched new approach, and 22 multiple species with both discretely breeding populations and continuously
rearing diets have been used for dozens of insect species. breeding ones, and for analyzing sequentially acting and
Etzel and Legner also discuss both production and colo- contemporaneously acting factors. Indispensable mortality,
nization of host and natural-enemy production in detail. a most important concept, is unfortunately rather neglected,
Contamination of cultures by insects or disease-producing perhaps because of problems in its establishment. Indis-
organisms is a common problem, and methods of handling pensable mortality is an important aspect that bears on the
such a problem are dealt with. The authors also discuss question of multiple versus single introductions. They deal
advantages and disadvantages of high or low genetic com- with horizontal life table construction [based on real mor-
position in a natural enemy, with the former desired for talities of a given group (cohort)] over a period of time,
field testing of effectiveness and the latter desired for in- and with vertical life table construction by examining age
sects used for assay purposes. The questions of diapause structures at given times. The notion of vertical life tables
forms, rearing conditions (temperature, light, and humid- has its origins in the work of R. D. Hughes in 1963 (see
ity), mating, and other behaviors are covered. Most of their Southwood, 1966).
extensive references are recent. Changes in laboratory cul- The authors detail extensive studies on tests for density
ture are also discussed, and the problems (including in- dependence (employing, e.g., Monte Carlo simulation), and
breeding, sex ratios, founder effects, laboratory environ- cite methods of Pollard et al. (1987) and Reddingius and
ment, genetic drift, mating type, mutation, etc., with van den Boer (1989). Many problems of solid evaluation of
suggested solutions) are considered. Finally, the authors density-dependent performance for many situations remain.
include an addendum that provides an invaluable list of
important reviews coveting in detail the necessary infor-
Chapter 9
mation on entomophage biologies, production problems,
and techniques and facilities so important in all culture and Luck, Shepard, and Kenmore update and suggest meth-
colonization programs. (Extensive references are cited.) ods to achieve greater precision in the evaluation of natural-
enemy effectiveness (components of Chapter 14 in DeBach,
1964b, and especially of Chapter 11 in DeBach et al.,
Chapter 8
1976). In the former DeBach book, the superior place of
The authors Bellows and Van Driesche discuss the con- using experimental "check methods" (exclusion, inclusion,
struction and analysis of field life tables in the evaluation additions, and interference), including removal methods, to
of biological control agents9 They describe the types of life evaluate the efficacy of natural enemies was closely consid-
tables and use them to evaluate natural enemy actions to ered; the same subject was covered in a long series of
answer two basic questions; the first deals with their impact papers by DeBach and associates (some cited in Chapter
on their hosts (prey), and the second considers their ecolog- 9). DeBach et al. (1976) noted that although key-factor and
ical roles, particularly in stabilizing populations. K-factor analyses may offer some possibilities of assessing
The construction of life tables for these purposes re- the regulatory power of a natural enemy, "In the field there
quires good estimates of numbers entering the different are so many other contemporaneously interacting factors
stages and numbers dying within them due to the various 9 . that use of these life tables and regression techniques

specific causes. Methods they describe to obtain such esti- gives little assurance that the true role of a natural enemy
mates include stage-frequency or age-frequency analysis, will necessarily be discovered by their use. We reiterate
recruitment, growth rate analysis, and death rate analysis; that the best, the closest, and only reliable means of evalu-
the measure of recruitment of both hosts and parasites is ation is through experimental or comparison methods."
the most direct means. For any of these methods, sampling Chapter 8 in this book goes a great deal farther, especially
programs "must avoid potential biases caused by behavioral in delineating appropriate sampling schemes and experi-
changes of parasitized hosts and by host patchiness" (in mental designs to achieve such improved evaluations.
8 C.B. Huffaker and D. L. Dahlsten

C h a p t e r 10 available methods, such as selective use of pesticides, use

of semiochemicals and/or supplements of natural enemies."
Gutierrez, Caltagirone, and Meikle present an economic
Earlier background manipulations to enhance parasitoid ac-
evaluation of biological control efforts. The authors start
tivity as reviewed by Powell in 1986 were cited. The chap-
with an enlightening preamble from DeBach, who in 1974
ter includes an up-to-date review of augmentative releases
stated that farmers have become convinced they "must use
of Trichogramma spp., the most extensively employed or-
pesticides regularly or perish" and notes that this conviction
has had biased origins and little solid economic evaluation.
The wind tunnel flight chamber is considered a useful
The work relates to classical and naturally occurring biolog-
tool for examining flight behavior and foraging. Elzen and
ical control by natural enemies. They follow the scheme in
King also discuss methods of assessing augmentative re-
Fig. 2, considering Bacillus thuringiensis (B.t.) toxins, ry-
leases and other management procedures, for example,
ania, pyrethrum, and other pesticides derived from orga-
those in Chapters 8 and 9. They discuss selective use of
nisms; and other biotechniques, such as sterile male re-
chemicals and the increasing problem with chemical pesti-
leases, as being outside of the traditional biological control
cides. For example, even low doses may reduce parasitoid
concept. Yet they go beyond the traditional use of the term
fecundity and egg viability. They emphasize the need to
and include not only parasites, predators, and pathogens but
integrate biological control with needed chemicals to con-
also competitors, possibly to include antagonists in the con-
serve natural enemies by using selective pesticides and min-
trol of plant pathogens.
imal dosages integrated with cultural practices and host-
The authors note that most of the benefits of naturally
plant resistance, and improved methods of assessing
occurring biological control have come to light from use of
abundance and effectiveness of the enemies. They point to
pesticides that have interfered with natural enemies. Many
the need to use the best biotypes, genetically improved
examples (see review of DeBach & Rosen, 1991) are dis-
stocks, use of behavior-modifying substances, and in vitro
cussed and referenced.
techniques for culturing.
Costs and benefits are discussed fully, including both the
direct ones (assessable) and certain indirect, external ones.
The latter are assignable to the cost-benefit equations, both C h a p t e r 12
negatively and positively (e.g., benefits society derives from
Whitten and Hoy deal with breeding and selection for
not using objectionable pesticides as a result of biological
genetic improvements of natural enemies mmites are
control). The authors also discuss various case histories,
stressed because more work has been done on mite preda-
some with measurable economic gains and others with vast
tors of mites than on other groups. They review the "over-
benefits that are still not adequately definable (e.g., cottony-
whelmingly favorable record" for biological control in the
cushion scale on citrus worldwide).
classical sense, with reference to cost effectiveness; envi-
The authors also present mathematical formulations for
ronmental acceptability; and safety record for control of
assessing costs and benefits. They discuss in dollar values,
arthropods, nematodes, weeds, and plant pathogens. They
for example, the biological control of ice plant scales along
note, too, that biological control has been attempted on less
California highways as reported by Tassan et al. in 1982,
than 5% of the 5000 or so arthropod pests, and that a
and note the biological control of wheat aphids in South
substantial proportion of efforts have had limited or no
America and of cassava pests in Africa, where economic
success, as various others have noted. They cite reviews on
analyses have not been conducted but the net benefits are
genetic improvements of pathogens and nematodes but do
nevertheless impressive. Cassava mealybug was solved at a
not deal with them.
cost of 8 cents per affected person over a vast region of
Whitten and Hoy consider the rather low success rate for
Africa. (See references in Chapter 10.)
introductions, and consider the question of genetic im-
provement. They state, however, that "the track record of
Applications of "Enhancements of Biological Control"
achievement of genetic improvement of arthropod natural
is reviewed in Chapter 11 by Elzen and King on manipula-
enemies by 1971 was sufficiently unimpressive to elicit in
tion of natural enemies, in Chapter 12 by Whitten and Hoy
1971 the pithy but fair assessment of Messenger and van
on genetic improvements; in Chapter 13 by Johnson and
den Bosch: 'artificial selection of natural enemies has been
Tabashnik on improving the use of chemicals; and in Chap-
considered by many, attempted by few, and, unfortunately,
ter 14 by Letourneau and Altieri on environmental manage-
proven practicable by no one.'" They question whether any
species had been "actually improved" and proved of value
in the field. Whitten and Hoy then consider 14 cases since
Chapter 1 1
1971 of parasites and predators being genetically improved
Elzen and King consider the use of natural enemies in a in the laboratory. They consider three categories: (1)cases
"rational insect management program that considers all where the pest status is due to lack of effective enemies;
Chapter 1 Scope and Significance of Biological Control 9

(2) cases involving biological control of secondary pests may influence natural-enemy efficacy such as nutrition
triggered to pest status by pesticides; and (3) cases in ill- (Chapter 22), sex ratios (Chapter 23), and pesticide resist-
defined, novel, or disturbed situations, where over time ance of natural enemies (Chapter 24) are also dealt with.
stocks have become better adapted to the conditions and Phytophagous insects used in the biological control of
presumably could be hastened to that end by genetic im- weeds are discussed in Chapter 17, and the various agents
provements. and strategies used in the rapidly expanding field of the
biological control of plant pathogens are dealt with in
Chapters 19, 20, and 25.
C h a p t e r 13
Johnson and Tabashnik discuss how pesticides can dis-
C h a p t e r 15
rupt biological control through both direct and indirect ef-
fects. Sublethal effects may lead to poor searching or habi- Gordh, Caltagirone, and Legner deal specifically with
tat orientation, for example. Short-term direct mortality and the biology and mechanisms of parasitoids and parasitism.
reduction of hosts have the greatest impact. Due to cumu- A parasitoid lives in or on a single host organism, unlike
lative uptake of toxins, biological control agents that are true predators. Seven basic criteria that distinguish parasi-
better searchers (more mobile) may be at a disadvantage. toids from other parasitic animals are listed (but there are
The authors propose that pesticide companies furnish infor- exceptions to each criterion). They develop internally or
mation on the detrimental effects of pesticides on natural externally, or initially as one and then the other. The clas-
enemies relative to the specific crop and locality. They note sical forms of parasitism are defined and differentiated.
also that there are relatively few documented pest popula- Hyperparasitism is highly developed in Hymenoptera com-
tion thresholds for initiating pesticide treatments, even pared to Diptera and Coleoptera. Anatomical features re-
though such thresholds are vital to this issue. lated to their modes of life are specified.
The Parasitica (Hymenoptera) is the largest group and
most important to biological control. The various superfam-
C h a p t e r 14
ilies and families are categorized briefly as to their biology
Letourneau and Altieri discuss various aspects of envi- and in some cases their biological control potential. Devel-
ronmental management to enhance biological control. This opment from egg to adult is outlined and differences be-
naturally overlaps with other chapters, especially Chapters tween various developmental forms are noted, as are the
12, 28, and 33. general physiologies and behaviors of adults. It is noted
They note especially that trends in agriculture toward that "parasitoids have ovipositional strategies which are
decreasing environmental heterogeneity, increasing use of essential in optimizing lifetime performance." Interestingly,
chemicals and machinery, and decreasing genetic diversity gregarious parasitoids may estimate host size and adjust the
in the crops have increased problems for effective action by number of eggs accordingly.
natural enemies. They note, too, the increasing need for Sex regulation, host feeding, habitat and host location,
integrated pest management (IPM) programs in view of the and host acceptance and suitability are also considered.
"cumulative restrictions on various pesticides and of public
concerns about their use." Effects of reduced tillage and
C h a p t e r 16
vegetational diversification have received much attention,
while other approaches have been minimal, except for the Hagen, Mills, Gordh, and McMurtry discuss the biology
"novel advances in the use of food sprays and kairomones of predators and mechanisms of predation.
to enhance natural enemy action" (see Chapters 16 and 22). The authors note that predaceous arthropods have impor-
The authors list Grigg's (1974) main types of agricul- tant roles in the three main tactics employed in biological
tural systems in the world: (1) shifting cultivation systems; control of pests: through importation, manipulation, or con-
(2) semipermanent, rain-fed cropping systems; (3) perma- servation. Each tactic has a relevance in our overall inte-
nent rain-fed cropping systems; (4) arable irrigation sys- grated approach to pest management. Brief biologies of the
tems; (5) perennial crop systems; (6) grazing systems; and families represented are given, including eggs and imma-
(7) systems alternating arable cropping and sown pasture. ture stages. The prey range of immature and adult forms,
and the cues that are employed to find prey are also pre-
AGENTS, BIOLOGY, AND METHODS The roles of behavioral chemicals and some of the se-
miochemicals that often involve tritrophic interrelationships
In this section the biology of parasitoids, predators, and are discussed, as are the basic nutritional requirements of
pathogens used for the biological control of insects are these predators. The roles of generalist and specialist pred-
discussed (Chapters 15, 16, 18, and 21). Other factors that ators in biological control are compared, and the contro-
10 C.B. Huffaker and D. L. Dahlsten

versy over releasing polyphagous species in new regions is logical control, particularly if control of weeds (aquatic and
discussed. The authors consider that in the future an in- terrestrial) is included along with insect pests. Federici con-
crease in periodic releases of natural enemies is likely as siders Bacillus thuringiensis (B.t.) to have had the greatest
the curtailments in use, or the effectiveness, of chemicals success, pointing out that it kills via a toxin, which places
develop further. They also see an increased need to mass this tactic in a category different from biological control in
culture natural enemies on natural or artificial diets, along the sense used in Fig. 2 and most other chapters. Also, he
with use of food supplements and shelters in field situa- includes as biological control other biotechniques not ac-
tions. cepted as such by the other authors of this book.
The authors review the Chelicerata and the Uniramia, Federici notes the paradox that the greater specificity
excluding the Crustacea of the former phylum Arthropoda. that gives these agents (pathogens) their biological utility
In the Chelicerata, the most important to applied biological also makes them less marketable than chemicals, even oth-
control is the Arachnida; only the spiders (Araneae) and the ers derived from organisms. He considers that recombinant
mites (Acariformes) are considered here. The spiders are DNA technology to improve the use and efficacy of micro-
considered to be more regulators of complexes in the eco- bial insecticides (or to produce crops resistant to the pests)
system than of individual species. Of the 331 known fami- will have an increasing role in the future. He then discusses
lies of Acariformes, at least 20 include predaceous species the development, current usage, limitations, and likely
but only 11 are dealt with. The Phytoseiidae are the princi- modes for improvement for each major pathogen group
pal predators of phytophagous mites. Their roles in biolog- (bacteria, viruses, fungi, and protozoa).
ical control are discussed, as well as examples of attempts Several B.t. strains are promising, including B.t. israe-
to improve their qualities through genetic manipulation, lensis for mosquito and blackfly larvae, and B.t. tenebrionis
selection, and periodic releases. There also has been some for Coleoptera, the latter now used for Colorado potato
utilization of Tydeidae, Bdellidae, Chyletidae, and Stig- beetle in the United States and Russia and also being devel-
maeidae. oped for use against the elm leaf beetle. The cloning of a
In the phylum Uniramia, the insects (Hexapoda) are of gene encoding the B.t. toxin has resulted in transfers to
crucial importance both as predators and as parasitoids. The tobacco, potato, and tomato, with others to follow. This
different foraging strategies of predators, such as random gives protection to the plant from specific insects, and the
search in hunting, ambush, and trapping, are all represented possibilities seem to be mushrooming. Studies suggested by
in the insects. Some are generalists and others highly prey the new genetic technologies are also discussed for viruses,
(and host) specific. The authors review the main orders of where registration problems exist. While there are no fungi
importance, including the historical significance of preda- currently registered for use in the United States, some pos-
tory Coccinellidae in establishing the significance of pred- sibilities are suggested. Protozoans are discussed, but the
atory insects in controlling pest species. prospects are not considered very promising.
The authors also discuss the sequence patterns of prey
finding and generalist versus specific predators. They also
C h a p t e r 19
compare the nutritional requirements of predators and her-
bivores and suggest the most likely avenues for improving Dodds provides a review of two vital plant processes
biological control. that limit the disease process. Systemic acquired resistance
occurs when a plant is inoculated with a virulent pathogen
against which it is able to mount a resistance reaction.
C h a p t e r 17 (and C h a p t e r 34)
Later, should the plant be inoculated by a pathogen to
These chapters deal with biological control of weeds. In which it is normally susceptible, infection is greatly limited
the former, Bellows and Headrick discuss the attributes of by the resistance in the plant induced by the first pathogen.
insects used to control alien weeds. The second pathogen may or may not be related to the first.
There has been a great increase in the number of biolog- Cross protection is a more specific protection, when prior
ical control projects against weeds (Chapters 17 and 34). challenge by a microbe limits the disease caused by later
The number of species established has been proportional to infection with a related microbe.
the number of agents introduced, but not necessarily suc-
cessful as controllers.
Chapter 20
A variety of mechanisms are currently being investigated
C h a p t e r 18 a n d 21
to genetically engineer plants to be resistant to pathogenic
Federici considers the use of insect pathogens in biolog- viruses. Cooper shares insights into several of these mech-
ical control. Emphasis is not on biological control per se, anisms, including coat-protein mediated protection, RNA
but on its use in IPM. He takes a pessimistic view of mediated protection, and several mechanisms that relate to
introduction of pathogens to achieve lasting (classical) bio- the pathogen genome or to changes in plant enzymes relied
Chapter 1 Scope and Significance of Biological Control I i

on by the pathogen for reproduction. A simple, widely eradicate or substantially reduce the culture or may produce
effective resistance mechanism that can be engineered into a thelytokous result, is discussed at length. When cultures
plants in general has thus far eluded researchers, and a of parasitoids attenuate or start yielding proportionately
combination of several mechanisms may turn out to be more males than females, it is important that the insectary
important in achieving resistance to a broad spectrum of supervisor understands the possible explanations for it to
heterologous viruses. take corrective action.
The most important factors controllable within a con-
C h a p t e r 22 fined rearing program that contribute to quality (i.e., highest
parasitization in the field) are the number of females and
Thompson and Hagen deal with the principles of nutri-
their size and individual heterozygosity, especially in out-
tion of entomophagous insects. They note many nutritional
breeding species such as those of Ichneumonoidea, in
advances since the reviews by Doutt (1964) and Hagen
which the effect of inbreeding on female function may be
(1964) cited in DeBach (1964b). Rearing some of these
insects artificially has revealed that their nutritional needs
embrace a "complex of behavioral, physiological, and nu-
tritional factors as cited by Slansky (1982, 1986)." The host Chapter 24
may influence development, sex ratio, fecundity, longevity,
Tabashnik and Johnson note that natural enemies ac-
and vigor of the subsequent adult parasitoids. This is often
count for only 3% of insect and mite species reported as
the result of the nutrition afforded by the host. Compara-
resistant to pesticides. They review three main hypotheses
tively few similar studies have been conducted with preda-
proposed to explain this pattern: (1) documentation bias,
torsmlimited work has been reported on 10 coccinellid
(2) differential preadaptation, and (3) differences in popu-
species. Thompson and Hagen also report that numerous
lation ecology.
studies show that entomophagous insects have "no unusual
Analysis of studies of 14 species of natural enemies
qualitative nutritional requirements," but that dietary suit-
published from 1979 to 1987 showed that with the excep-
ability involves a "quantitative balance" beyond mere qual-
tion of phytoseiid mites, substantial resistance development
itative essentials. They also note that "nutritional require-
in field populations of natural enemies was rare. High levels
ments of adult entomophagous insects remain obscure."
of resistance in Hymenoptera were virtually absent. The
The addition of semiochemicals to supplemental foods
authors conclude that pesticide resistance is more likely to
attracts Chrysoperla carnea adults and causes them to "set-
be documented in pests than in natural enemies, yet the
tle down." Flight patterns and attraction to prey are affected
lack of resistance in several carefully studied natural enemy
by tryptophan breakdown products from honeydew. Cocci-
species suggests that resistance does evolve faster in pests
nellids and other predators aggregated around artificial hon-
than in natural enemies.
eydew. Spraying of corn with sugar or molasses increased
The authors report that intrinsic levels of detoxification
predation on, and lowered populations of, aphids and corn
enzymes were not consistently lower in natural enemies
borers. Currently, practical applications are "restricted to
than in pests. They suggest that various preadaptation hy-
use of food and food supplements to enhance entomopha-
potheses based on differences in detoxification enzymes
gous insects in the fields where synchrony is lacking or the
have limited explanatory power. Differences in intrinsic
enemies are isolated from environments having nectars and
tolerance to pesticides and differences in genetic systems
honeydew they commonly use." Feeding of Trichogramma
were also found to be unlikely general explanations for why
prior to release markedly increased fecundity and longevity,
pests become resistant more readily than their arthropod
and feeding Bracon brevicornis honey solution sprayed on
natural enemies.
sorghum stalks in winter increased parasitoid cocoons,
Tabashnik and Johnson suggest that food limitation due
while hosts declined. (See extensive citations by Thompson
to reduction in host or prey densities caused by pesticides
and Hagen.)
is a major factor that retards resistance development in
natural enemies (see also Huffaker, 1971). To maintain
C h a p t e r 23
biological control, they recommend sparing and judicious
Luck, Nunney, and Stouthamer deal more specifically use of selective pesticides. (Extensive references are cited.)
with the evolutionary ecology of parasitoids. They discuss
the impact of culturing techniques on sex ratios and quality
C h a p t e r 25
of the insectary product, the natural enemy, both from a
theoretical perspective of first principles and from a practi- Fulbright outlines the history and findings of the re-
cal perspective of the insectary workers. search that has followed the fate of chestnut blight, a dev-
The genetic (hence evolutionary) significance of factors astating disease of chestnuts in both North America and
such as male diploidy and son-killer bacteria, which may Europe. Following widespread destruction of chestnut after
12. C.B. Huffaker and D. L. Dahisten

the introduction of the pathogenic fungus, a few stands of occurring between those used on the aerial parts of plants
chestnut were discovered that were recovering from infec- (Chapter 32), and those found in the soil or rhizosphere
tion. Milder, nonlethal strains of the fungus appeared to (Chapter 26).
outcompete, or at least to moderate the impact of, the viru-
lent strain. The hypovirulent trait appears transmittable to
C h a p t e r 27
virulent strains through transfer of genetic material inside
an infected tree. This work holds promise that chestnut may Kennett, Beardsley, and McMurtry discuss tropical and
someday be recovered as an important forest tree in decid- subtropical crops and provide by far the most examples of
uous forests, and indicates that hypovirulence may be a solid classical biological control. They also illustrate a wide
promising area for future developments against other fungal diversity of the principles in ecology and natural enemy
diseases. behavior, particularly in relation to results from introduced
natural enemies. This is not unexpected because the vast
majority of efforts have been centered in the tropical and
APPLICATIONS subtropical areas against the armored and unarmored scale
insects, mealybugs, whiteflies, psyllids, and mites. Included
It was intended that the principles would largely have are work on citrus (the earliest and most researched), coco-
been handled in the preceding sections; yet, inevitably there nut, banana, coffee, tea, and olive. These illustrate some of
are in this section various possibilities and consequences the more striking successful examples and include the more
from applications that bear on, and contribute examples of, recent efforts. However, sugarcane, pineapple, macadamia
principles from classical or manipulative biological controls nut, and passion fruit are not covered (but see Bennett et
or enhancements. Some examples relate to broader ecolog- al., Chapter 15, in Huffaker & Messenger, 1976).
ical aspects than to just biological control, for example, in Examples include those where competitive displacement
general resource, agroecosystem, crop, forest, or range has improved biological control, and the culture and release
management. These areas embrace an enormous spread of of mycelia of a pathogenic fungus was used to control the
environments and human enterprise B for the simplest row- citrus red mite.
crop situation and multicrop interplantings in single-objec-
tive agriculture, multiobjective small farm units, green-
Chapter 28
house cultures; and perhaps the most complex of all, for
that of urban multiplantings of great complexity, objectives, AliNiazee and Croft review biological control work on
and vague potentials for estimating cost-benefit functions. pests of deciduous tree fruits and the use of natural enemies
Also, there are medical and veterinary problems that in- and IPM for these crops. These crops are characterized by
clude solutions involving management of disease vectors in large pest complexes; since biological control agents are
ways that utilize biological control, but are not classifiable inadequate against some of these, integrated programs are
specifically to the environmental categories. Biological con- generally needed, and in some cases strictly chemical con-
trol of soil-borne and foliar plant pathogens are discussed trol programs are necessary. The authors discuss their pro-
(Chapters 26 and 32) as well as the use of plant pathogens grams in terms of key, sporadic, and secondary pests. Suc-
to control weeds (Chapter 35). Biological control of verte- cessful introductions of exotic natural enemies have been
brate pests is considered in Chapter 38. Chapter 40 deals few, but striking results from introducing pesticide-resistant
with social and economic factors of human orientation, and phytoseiids into Australia for control of mites (a pesticide-
omits the basic ecological underpinnings. triggered problem) are reported. Otherwise, classical bio-
logical control introductions for these crops have been lim-
ited mainly to efforts on woolly apple aphid, winter moth,
C h a p t e r s 2 6 a n d 32
and codling moth.
Controlling plant pathogens through biological control
or manipulation of microbial populations is the subject of
Chapter 29
Chapters 26 and 32. As Bellows points out, this area of
biological control is essentially ecological management at In this chapter on biological control of forest insects,
the microbial level. Manipulations of microbial populations Dahlsten and Mills discuss the great differences between
to favor nonpathogenic types and limit pathogens can take forest management and agricultural crop management. For-
place in a variety of ways, through conservation of popula- ests are a multiple-use resource and differ widely from
tions, manipulating the environment to favor saprotrophic single-crop agriculture. Time to harvest is 20 to 30 years at
organisms over pathogens, or by adding organisms directly the shortest and 50 to 100 years in other cases. The cost of
to a cropping environment. The groups of organisms and treating such a long-term crop annually would be impossi-
the ways in which they are manipulated vary with the ble economically. Some 78% of biological control impor-
system that they are targeted for, with principal differences tations for forest use have involved parasitoids (Hymenop-
Chapter 1 Scope and Significance of Biological Control |3

tera and tachinids); 40 species of enemies have been used increase since 1968. Yet it is estimated that biological con-
in unsuccessful efforts against the balsam woolly aphid, trol is used regularly on only about 3000 ha, excluding
Adelges piceae. Augmentation and conservation of natural some undocumented use in Russia.
enemies are promising routes. Cucumbers and tomatoes are by far the most important.
The effort on the larch casebearer has been a long one m It is interesting that "the intensive harvesting (2 to 3 times
from 1928--and is continuing. Cited are Ryan et al. a week) is difficult to coordinate with statutory re-entry and
(1987), who report a steady decline of the casebearer since pesticide residue restrictions for pesticide usage. Phytotox-
releases of Chrysocharis laricinellae and Agathis pumila. icity from pesticides, especially young plants in winter, also
favors biological control."
The high tolerance of cucumbers to spider mite damage
Chapter 30
and the very high and quick efficiency of Phytoseiulus
Kogan, Gerling, and Maddox review the methods of persimilis account for its widespread usage for cucumbers.
enhancing biological control on several transient crops. It is a welcome "solution to increasing problems" with
They note that disturbances in such crops are difficult to resistance of Trichogramma urticae to acaricides. The ini-
correct, but nevertheless many less disturbed crops benefit tial density of pest mites and the rate of introduction are
from a high level of resident natural enemies. Such crops critical. Cucumbers are deliberately infested with spider
are also susceptible to secondary pest outbreaks triggered mites immediately after planting, or both spider mites and
by pesticide use. P. persimilis are introduced at the first natural appearance
These circumstances make transient crops "particularly of spider mites.
suited for augmentative releases of natural enemies and use Greenhouse whitefly was controlled on cucumbers and
of microbial pesticides or methods to trigger natural epizo- tomatoes by Encarsia formosa in the United Kingdom from
otics of pathogens." 1927 until the 1940s when synthetic organic pesticides be-
Much of the treatment is based on soybean as a model. gan to be used instead. The development of resistance in T.
The instability of the tritrophic interactions is a major prob- urticae to pesticides ushered in biological control on these
lem for classical biological control. Hence, colonization crops and this necessitated a return to biological control for
(addition) of natural enemies is stressed, including "(1) greenhouse whitefly. Encarsia has many desirable traits for
native host-specific enemies that overwinter in or near the achieving good control on tomatoes in greenhouses, but
fields, (2) polyphagous species that develop in various less so for cucumbers. Leaf miners on cucumbers, toma-
nearby habitats and move in as opportunists, and (3) mi- toes, and melons have also been controlled by three species
grant colonizers from more subtropical areas." The authors of parasitoids in the Netherlands, United Kingdom, and
also state, "Despite the inherent ecological instability-- Sweden. Related problems in other countries and on other
most [of the] herbivore populations are effectively regu- greenhouse crops are also receiving attention. (See refer-
lated by a complement of natural enemies." They use ex- ences in Chapter 31.)
amples for predators, parasites, and disease pathogens (e.g.,
Nomurea) and discuss cotton, soybean, corn, melon, alfalfa,
C h a p t e r 33
and cassava.
The microsporidian Nosema pyraustae (inadvertently in- In this chapter on insects and mites of grapes, Flaherty
troduced) is the major enemy of corn borer in many areas and Wilson review the culture and pest problems of culti-
and may have displaced a previously significant introduced vated grapes worldwide, noting their origin in Asia Minor.
tachinid, Lydella thompsoni. Trichogramma spp. are used Included is consideration of the various groups of pests;
in inundative and augmentative releases for various crops: they note that for so valuable a crop, very little work on
rice, millet, crucifer, beet, corn, cassava, and others. Many biological control has been done. In California (where most
successes have been documented, but the potential for even work has been done), the egg parasitoid Anagrus epos is a
greater successes exists. key factor in biological control and IPM. In favorable
places this parasitoid parasitizes about 80% of the native
grape leafhopper, but only 20% of the variegated grape
C h a p t e r 31
leafhopper, which now poses additional problems. Proper
Parrella, Hansen and van Lanteren deal with biological integration of chemicals for control of primary pests is
control in greenhouse environments, some 100,000 to crucial to avoid major problems with pesticide-generated
150,000 ha worldwide. Manipulations in greenhouses are pests, such as spider mites.
easier than those outdoors--for the pests, the natural ene-
mies, the environment, and IPM in general. Greenhouses
Chapter 34
offer food, warmth, protection from weather, and physical
barriers to prevent dispersal by drift. Work has been mostly Goeden and Andr6s cover the biological control of
on vegetables and flowers, but there has been a dramatic weeds, both terrestrial and aquatic. They detail the meth-
14 c.B. Huffakerand D. L. Dahlsten

odology in choosing and carrying out a project (reviews ronment, and also by programs that seek a pathogen that
cited are those by Goeden, 1978 in Clausen, 1978, Zw/31fer can be mass-reared and then added to a particular system
& Harris, 1971, and Turner, 1985). For importations, (1) in an inundative way. Some opportunity for commercial
project selection, (2) search for natural enemies, (3) tests development of pathogens may find fruition in this field.
and biological studies of host range, (4) evaluation of host-
range studies, (5) importation and release, and (6) evalua-
tion form the components of a program. They also deal C h a p t e r 36
with conserving and augmenting existing biological control
In this chapter on urban environments, Dahlsten and
agents. They noted more than 80 projects in biological
Hall note that these environments are the most complex,
weed control in the United States and Canada alone, and
diverse, and discontinuous due to the many introduced or-
cite Julien (1982), who states that 101 species of weeds
namental plants in fragmented patches. These environments
have been targeted worldwide for 174 projects. They note
offer special opportunities for IPM and biological control.
that while insects have been used mostly, phytopathogens
There are problems in assessing aesthetic and nuisance
are showing promise and some success. Their chapter and
pests. There is a higher and more diversified pesticide usage
Chapter 17 cover details with the Coleoptera, Lepidoptera,
per acre than in any crop or forest, especially prior to the
Diptera, and Hemiptera-Homoptera being the main agents
1970s, with no regard for IPM or biological controls. Over-
introduced; and 19 to 44% of these providing effective
lapping problems include medical, psychological, architec-
control (not just being established).
tural, agricultural, silvicultural, floricultural, and horticul-
Goeden and Andrrs also detail the histories of early
tural concerns. Improved incentive for biological control
projects. They detail work on alligator weed in the United
comes from public concerns for clean air and water and
States and Australia; puncture vine in the southwestern
fear of pesticide exposure.
United States, Hawaii, and St. Kitts; water hyacinth in the
For example, in Berkeley, California, 10 tree species
southeastern United States; and three other successes (i.e.,
constitute the native tree flora; now there are 123 species,
for Cuscuta in China, Ambrosia (ragweed) in Russia, and
with nearly 300 on the University of California at Berkeley
Salvinia in Australia and New Guinea). In the latter case
campus alone. They have come from most moderate cli-
the significance of solid taxonomy and host relationship
mate regions of the world and have a wide variety of
was found to be crucial. Two other points are worth noting
introduced pests. Most of the successes with introduced
here: (1) the authors downplay the promise of genetic im-
natural enemies have been with homopterous insects on
provements in natural enemies, but in Chapter 12 on this
perennials, as in agriculture, for example, woolly whitefly
subject, considerable promise is suggested; (2) the authors
on citrus, acacia psyllids on acacia, and aphids on elm.
state that before undertaking an introduction effort, "there
That urban fly and mosquito control with chemicals can
must be assurances that the weed has few, if any, redeeming
interfere with biological controls on urban trees is illus-
virtues and that there is little or no public opposition to the
trated by outbreaks of Lecanium corni on fruit trees on
project," citing Turner (1985). Yet Turner's paper is a
Mackinac Island, Michigan; and of pine needle scale in
closely considered, comprehensive analysis, not just the
South Lake Tahoe, California. There is currently a Berkeley
cautions to be considered. It also gives suggestions on how
campus program on control of cockroaches using two egg
apparent conflicts of interest may be resolved, even where
there is not complete public acceptance and there may be
some redeeming virtue. There is now a closer concern about
making unwise releases; more kinds of agents are being
C h a p t e r 37
used, adverse environmental consequences are being posed,
and many more personnel who have different views and In this chapter on biological control of medical and
qualifications concerning these complex risks are involved. veterinary pests, Garcia and Legner deal with earlier re-
So it is proper that protocols are being tightened and eco- views and bring in newer developments. A few references
logically disruptive possibilities are being more closely to snail vectors of digenetic trematodes are made, but most
considered (see Turner, 1985). of the work has been against pest Diptera.
The agents used for mosquito control have been mostly
fish, insects, and other arthropods; and the microbial insec-
C h a p t e r 35
ticide B. thuringiensis var. israelensis (H-14). Several nem-
Pathogens in weed control is the subject of Chapter 35 atodes and fungi are being tested. Interest at the turn of the
by Rosskopf, Charudattan, and Kadir. In this chapter they century on dragonflies quickly waned. Soon thereafter the
discuss the opportunities for biological control of weeds mosquito fish, Gambusia affinis, was intensively used for
using pathogens. Pathogens, with the possibility of high some 40 years. Synthetic organic insecticides curtailed all
selectivity, may be viewed with favor both in programs that this work shortly after World War II, and it was revived
seek to permanently introduce new pathogens into an envi- only when the problems of resistance to the chemicals
Chapter 1 Scope and Significance of Biological Control 15

loomed ever greater. Gambusia is not now widely accepted Chapter 40

but is still used in some situations; it is better against non-
Perkins and Garcia discuss the general social, political,
anophelines. There is a real problem with fixing mosquito
economic, and philosophical factors that affect research and
tolerance levels, but more important is the temporary, un-
implementation of biological control. They define biologi-
stable habitat of the pest species, which is not conducive to
cal control as "the identification of indigenous and exotic
sustained biological control (Legner & Sjogren, 1984
natural enemies, the importation and release of exotic nat-
ural enemies, and the evaluation of the abilities of natural
Of the synanthropic Diptera, muscoid species, including
enemies to suppress a pest." This is an excellent discipli-
the housefly, are the most important. In Australia, dung-
nary expression in that it specifies the identification, thus
burrowing beetles introduced for bush fly control have aided
the taxonomic relevance, and the e v a l u a t i o n - - w h a t work-
agriculture through their manure mixing in the soil, but
ers must do. They also summarize the various economic
appear not to have much affected densities of the bush fly.
and social factors discussed and give recommendations.
For snails, biological control is very limited and re-
These relate, not to the basic ecological factors, for exam-
stricted to special situations. Sciomyzid flies are highly
ple, weather, allies, and competition, that affect natural en-
specific and have shown some success in Hawaii (Bay et
emy success, but to those social, political, and economic
al., 1976; Garcia & Huffaker, 1979) to control the inter-
factors so important to biological control and other resource
mediate host snail of the giant liver fluke of cattle. Suppres-
management efforts.
sion of Biomphalaria glabrata, the intermediate host of
human schistosomiasis, through competitive displacement
by Marisa cornuarietis and also Helisoma duryi, shows C h a p t e r 41
promise. In this final chapter, Bellows provides a view toward the
future of where biological control can take us, or more
precisely, where it will likely fit in our world's future. He
Chapter 38 covers possible developments in combating adventive and
native pests, advances in use of microbial agents, possibili-
Biological control of vertebrates is a challenging and ties of protecting natural environments from invading spe-
important area worldwide. Hoddle provides in this chapter cies, the roles of experts and institutions, and the impor-
a review of the types of damage exotic vertebrates can tance of training future biological control scientists.
cause to both natural and agricultural ecosystems. Historical
approaches, employing vertebrate predators, are reviewed,
and the risks and benefits of such programs are discussed.
Other techniques that include biological sterilization, and The authors wish to express appreciation of the cooperation of all
use of specific pathogens, are reviewed as perhaps more subsequent chapter authors in preparing this introductory chapter, espe-
likely to be implemented in the future than would be addi- cially to A. P. Gutierrez for insightful suggestions; and to David L. Row-
ney and the secretarial staff for much patience and help.
tional movement of vertebrate predators.


Chapter 39 Batra, S. W. T. (1982). Biological control in agroecosystems. Science,

215, 134-139.
Altieri and Nicholls utilize programs in Latin America Bay, E. C., Berg, C. O., Chapman, H. C., & Legner, E. F. (1976). Biolog-
as a model for dealing with these types of problems in ical control of medical and veterinary pests. In C. B. Huffaker & P. S.
countries where assessment technology is limited; or pesti- Messenger (Eds.), Theory and practice of biological control (pp. 457-
479). New York: Academic Press.
cide laws are lax or even favor pesticide abuses, o r allow Caltagirone, L. E., & Huffaker, C. B. (1980). Benefits and risks of using
the "dumping" of disallowed pesticides from more environ- natural enemies for controlling pests. In B. Lundholm & M. Stuckerud
mentally conscious countries (e.g., the United States). The (Eds.), Environmental protection and biological forms of control of
authors deal with these questions and with the complex pest organisms. Stockholm: Ecol. Bull.
factors associated with using biological and cultural con- Carruthers, R. I., & Petroff, J. K. (Eds). (1997). Proceedings of the Invi-
tational Workshop on USDA Activities in Biological Control. Oct. 8-
trois. Of the biological control work considered, Chile has 11, 1996, Riverdale, Maryland and Washington, D. C. USDA, Agr.
had the most introductions, with 66 introductions being Res. Service 1997-01, 109 pp.
made from 1903 to 1984 against pests of citrus, grape, Clarke, B., Murray, J., & Johnson, M. S. (1984). The extinction of en-
peach, apple, tomato, and other crops. They report that demic species by a program of biological control. Pac. Sci., 38, 97.
some 42 species of natural enemies were established; and Clausen, C. P. (ed.). (1978). Introduced parasites and predators of arthro-
pod pests and weeds: A world review. Agriculture Handbook No. 480.
60% of the targeted host species are under complete or Washington, DC: USDA.
substantial biological control, 38% by introduced predators Crawley, M. J. (1989). Insect herbivores and plant population dynamics.
and 24% by introduced parasites. Annual Review of Entomology, 34, 531-564.
16 c.B. Huffaker and D. L. Dahlsten

Davis, D. E., Myers, K., & Hoy, J. B. (1976). Biological control among entomology (pp. 359-398). New York: Wiley-Interscience, John Wi-
vertebrates. In C. B. Huffaker & P. S. Messenger (Eds.), Theory and ley & Sons.
practice of biological control (pp. 501-519). New York: Academic Huffaker, C. B., Gordon, H. T., & Rabb, R. L. (1984). Meaning of
Press. ecological entomology--The ecosystem. In C. B. Huffaker & R. L.
DeBach, P. (1964a). The scope of biological control. In P. DeBach (Ed.), Rabb (Eds.), Ecological entomology (pp. 3-17). New York: Wiley-
Biological control of insect pests and weeds (pp. 3-20). London: Interscience, John Wiley & Sons.
Chapman & Hall. Huffaker, C. B., Messenger, P. S., & DeBach, P. (1971). The natural
DeBach, P. (Ed.). (1964b). Biological control of insect pests and weeds. enemy component in natural control and the theory of biological con-
London: Chapman & Hall. trol. In C. B. Huffaker (Ed.), Biological control (pp. 16-67). New
DeBach, P., & Rosen, D. (1991). Biological control by natural enemies York, London: Plenum Press.
(2nd ed.). Cambridge, England: Cambridge Univ. Press. Julien, M. H. (Ed.). (1982). Biological control of weeds. A world cata-
DeBach, P., & Sundby, R. A. (1963). Competitive displacement between logue of agents and their target weeds. Slough, England: Common-
ecological homologues. Hilgardia, 34, 105-166. wealth Agricultural Bureau, Commonwealth Institute of Biological
DeBach, P., Huffaker, C. B., & MacPhee, A. W. (1976). Evaluation of the Control.
impact of natural enemies. In C. B. Huffaker & P. S. Messenger (Eds.), Krebs, C. J. (1972). Ecology: The experimental analysis of distribution
Theory and practice of biological control (pp. 255-285). New York: and abundance. New York: Harper & Row.
Academic Press. Laing, J. E., & Hamai, J. (1976). Appendix. In C. B. Huffaker & P. S.
Garcia, R., & Huffaker, C. B. (1979). Ecosystem management for sup- Messenger (Eds.), Theory and practice of biological control (pp. 685-
pression of vectors of human malaria and schistosomiasis. Agro-Eco- 743). New York: Academic Press.
systems, 5, 295- 315. Luck, R. F. (1984). Principles of arthropod predation. In C. B. Huffaker
Garcia, R., Caltagirone, L. E., & Gutierrez, A. P. (1988). Comments on a & R. L. Rabb (Eds.), Ecological entomology (pp. 497-527). New
redefinition of biological control. BioScience, 38, 692-694. York: Wiley-Interscience, John Wiley & Sons.
Gilbert, N. E, Gutierrez, A. P., Fraser, B. D., & Jones, R. E. (1976). Mackauer, M., Ehler, L. E., & Roland, J. (Eds.). (1990). Critical issues in
Ecological relationships. London: Freeman. biological control. Andover, Herts: Intercept.
Hassell, M. P. (1986). Parasitoids and population regulation. In J. Waage Maws, M. G. (1984). Ambrosia artemisiifolia L., common ragweed (Com-
& D. Greathead (eds.), Insect parasitoids (pp. 201-224). London: positae). In J. S. Kelleher & M. A. Hulme (Eds.), Biological control
programmes against insects and weeds in Canada 1969-1990 (pp.
Academic Press.
Howarth, F. G. (1983). Classical biocontrol: Panacea or Pandora's box? 111-112). Commonwealth Agric. Bureau.
Nechols, J. R. [Exec. Ed.]. (1995). Biological control in the western
Proceedings of the Hawaiian Entomological Society, 24, 239-244.
United States. Univ. of Calif., Div. of Agric. and Nat. Res. Pub. 3361.
Huffaker, C. B. (1971). The ecology of pesticide interference with insect
Pimentel, D., Glenister, C., Fast, S., & Callahan, D. (1984). Environmental
populations (upsets and resurgences). In J. E. Swift (Ed.), Agricultural
risks of biological pest controls. Oikos, 42, 283-290.
chemicals--harmony or discord for food, people and the environment
Price, P. W., Bouton, C. G., Gross, P., McPheron, B. A., Thompson,
(pp. 92-104). Proceedings of Symposium, Univ. of Calif., Div. of
J. N., & Weiss, A. E. (1980). Interactions among three trophic levels:
Agric. Sci.
influence of plants on interactions between herbivores and natural
Huffaker, C. B. (1988). Ecology of insect pest control (Vol. 3). In R.
enemies. Annual Review of Ecology & Systems, 11, 41-65.
Goren & K. Mendel (Eds.), Proceedings, Sixth International Citrus
Reynolds, H. T. (1971). A world review of insect population upsets and
Congress, Tel-Aviv, Israel, March 6-11, 1988 (pp. 1047-1066). Phil-
resurgences caused by pesticide chemicals. In J. E. Swift (Ed.), Agri-
adelphia, Rehovot: Balaban Publ. cultural chemicalsnharmony and discord for food, people and envi-
Huffaker, C. B. (1990). Effects of environmental factors on natural ene- ronment (pp. 108-112). Proceedings of Symposium, Univ. of Calif.,
mies of armored scale insects (Vol. 4B). In David Rosen (Ed.), The Div. of Agric. Sci.
armored scale insects, their biology, natural enemies and control (pp. Rosen, D., & DeBach, P. (1991). Foreign exploration: The key to classical
205-220). Amsterdam: Elsevier. biological control. Florida Entomology, 75,409-413.
Huffaker, C. B., & Gutierrez, A. P. (1990). Evaluation of efficiency of Ryan, R. B. (in press). Evaluation of biological control: introduced para-
natural enemies in biological control (Vol. 4B). In David Rosen (ed.), sites of larch casebearer (Lepidoptera: Coleophoridae) in Oregon. En-
The armored scale insects, their biology, natural enemies and control vironmental Entomology,
(pp. 443-495). Amsterdam: Elsevier. Southwood, T. R. E. (1966). Ecological methods. London: Methuen &
Huffaker, C. B., & Kennett, C. E. (1969). Some aspects of assessing Co., Ltd.
efficiency of natural enemies. Canadian Entomology, 101,425-447. Teng, P. S. (1985). Integrating crop and pest management: the need for
Huffaker, C. B., & Messenger, P. S. (1964). The concept and significance comprehensive management of yield constraints in cropping systems.
of biological control. In P. DeBach (Ed.), Biological control of insect Journal of Plant Prot. Tropics, 2(1), 15- 26.
pests and weeds (pp. 45-117). London: Chapman & Hall. Turner, C. E. (1985). Conflicting interests and biological control of weeds.
Huffaker, C. B., & Messenger, P. S. (Eds.). (1976). Theory and practice In E. S. Delfosse (Ed.), Proceedings, VI, International Symposium on
of biological control. New York: Academic Press. Biological Control of Weeds, Vancouver, Canada (pp. 203-225).
Huffaker, C. B., & Rabb, R. L. (Eds). (1984). Ecological entomology. U.S. Congress, Office of Technology Assessment (1995). Biologically
New York: Wiley-Interscience, John Wiley & Sons. based technologies for pest control (OTA-ENV-636). Washington,
Huffaker, C. B., & Rosen, D. (1990). The attributes of effective natural D.C.: U.S. Government Printing Office.
enemies (Vol. 4B). In D. Rosen (Ed.), The armored scale insects, their Van Driesche, R., & Bellows, T. S., Jr. (1996). Biological control. Lon-
biology, natural enemies and control (pp. 197-204). Amsterdam: El- don: Chapman and Hall.
sevier. Zw61fer, H., & Harris, P. (1971). Host specificity determination of insects
Huffaker, C. B., Berryman, A., & Laing, J. E. (1984). Natural control of for biological control of weeds. Annual Review of Entomology, 16,
insect populations. In C. B. Huffaker & R. L. Rabb (Eds.), Ecological 159-178.