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Biological control of locusts and grasshoppers using a

fungal pathogen: the importance of secondary cycling
M A T T H E W B. T H O M A S 1, S I M O N N. W O O D 1 and

C H R I S T O P H E R J. L O M E R 2
1Natural Environmental Research Council Centre for Population , Imperial ,> ,
Ascot SL5 7PY,U.K.
2International Institute of Biological ,C
ontrl Silwood , Buckhurst ,
Ascot, SL5 7TA, U.K.

SUMMARY

Persistent chemical pesticides can provide an effective means of control against locusts and grasshoppers
due to prolonged activity of the spray residue. However, use of these pesticides is now prohibited, and non-
persistent chemical alternatives are substantially less successful. Here we show why it is expected that
biological pesticides based on the fungal pathogen Metarhizium will be highly effective in the
control of both locust and grasshopper. We demonstrate, using novel population dynamic models
containing measured estimates of horizontal transmission coefficients, that secondary cycling of the
pathogen after a single spray application provides a biological substitute for chemical persistence. This has
significant consequences for the economics of biopesticide use in pest control. Furthermore, by identifying
that secondary cycling acts in a density—dependent manner, this study also highlights fundamental
differences between conventional pesticides and biopesticides and how they might be used.

1. I N T R O D U C T I O N
The devastation of crops by locusts and grasshoppers
has been recorded since biblical times, and many
millions of U.S. dollars are spent annually on their
control, throughout the world. For example, during
the period of 1986-1989 the total cost of locust and
grasshopper control programmes (mainly in the Sahel
and northwest Africa) amounted to over 400 million
U.S. dollars (OTA 1990).
Until the mid-1980s the principle strategy for
controlling locusts and grasshoppers was to use
persistent synthetic chemical insecticides. Because of
the long activity of the spray residue, persistent
insecticides are effective even when direct contact rate
between spray and target insect is low (as occurs in
some environments occupied by grasshoppers in the
Sahel (Lomer et al. 1995a) and with some aerial
application (Prior & Streett 1995)) (Brader 1988;
Prior & Streett 1995). However, because of concern
about environmental damage and hazards to human
health and livestock, persistent chemical insecticides
are no longer applied. Non-persistent chemicals, with
virtually no residual activity, are now used instead
(Brader 1988). Because these chemicals kill largely as a
result of direct spray contact only, they are much less
effective and often require several applications within
a season or extensive blanket spraying to achieve
satisfactory control (Brader 1988). This results in
increased cost and environmental damage of the
control programe (Brader 1988; OTA 1990; Kremer
1993).
In response to the problems outlined above, the
IIB C /IITA /D FPV collaborative research programme
on the biological control of locusts and grasshoppers
(LUBILOSA) has been developing alternative tech­
nologies for locust and grasshopper control. In this
programme, strains of the entomopathogenic fungus
Metarhizium flavoviride Gams & Rozsypal (Deutero-
mycotina: Hyphomycetes) have been isolated from
several locust and grasshopper species (Bridge al.
1993), and oil-based biopesticides suitable for ap­
plication using ultra-low volume techniques are being
developed and tested (Bateman et al. 1993; Lomer et
1993; Lomer et 1al.995£). Field trials with the
biopesticides have demonstrated effective control of
both locusts and grasshoppers under natural field
conditions (Douro-Kpindou et al. 1995; Kooyman &
Godonou 1995; Lomer et 1al.995a, b).
It has been shown that spray residues from the
biopesticide have only limited persistence (Carruthers
et al. 1995). However, secondary cycling of the
pathogen (i.e. horizontal infection) after a spray
application has been measured in the field during
biopesticide trials on sahelian and Australian grass­
hoppers (Lomer et al. 1995a; Baker et al. 1995;
C. Lomer, M. Thomas & S. Wood, unpublished data;
respectively). Here, we investigate the importance of
this for both locust and grasshopper control using two
novel population dynamics models. One model pre­
dicts the effects of the biopesticide on the grasshoppers,
Hieroglyphus daganensis Krauss and Zonocerus variegatus
(L.), two key pest species from slightly different
ecological zones in sahelian and subtropical Africa

Proc. R . Soc. Lond. B (1995) 259 , 265-270 265 © 1995 T he Royal Society
Printed in Great Britain
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266 M. B. Thom as and others Biocontrol o f locusts and grasshoppers
(Steedman 1990). The second model predicts the
effects of the biopesticide on the Desert Locust,
Schistocerca gregaria (Forskal). Mathematical details are
kept to minimum because the aim of this paper is to
examine the consequences of the host-pathogen in­
teraction for biological control. A more thorough
presentation and in-depth analysis of the models will
be published elsewhere (M. Thomas, S. Wood &
C. Lomer, unpublished data).
2. H O R I Z O N T A L T R A N S M I S S I O N
A key parameter in host-pathogen models is the
transmission coefficient. This describes the probability
of a successful infection resulting from contact between
a susceptible host and an infective propagule (i.e. free
living spore or virus particle, or infective host in the
case of directly transmitted diseases) (Anderson 1981).
Unfortunately, few models contain measured estimates
of this parameter because of problems with manipu­
lating and monitoring both insect and pathogen
populations (but see Dwyer 1991; Dwyer & Elkinton
1993; Goulson et 1al.995). In the presentdetailed in figure 1, these infectivity profiles after death
defining cadavers as the infective units, we were able to
capture the essential temporal and spatial aspects of
disease transmission under field conditions without
monitoring the pathogen population per se. This
enabled us to measure transmission coefficients for the
two grasshoppers in their natural environments during
held trials in Benin and for Desert Locust in held cages
in southern Niger. The experimental procedure
(described in detail in Carruthers et al. 1995) used
sequential exposure of populations of uninfected hosts
in held cages to bioassay for changes in infectivity
time / d
Figure 1. The transmission coefficient or infectivity profile for
H. daganensis. Infectivity profiles for this and the other species
were fitted with a first- or second-order gamma function,
= /?d+U e_ct, where j = 0 or 1, /?It(t)
magnitude of infection and c controls the timescale of the
infectivity profile. Best-fit parameters (least-squares objec­
tive) for the grasshoppers were: H. daganensis = 0.4±0.006,
c = 0.11+0.01 and j = 1; Z. variegatus /? = 1.8+ 0.5,
c = 0.03 + 0.01 and j = 0. For the desert locust, S. gregaria,
measured infectivity was not unequivocally declining by the
end of the experiment, we therefore fitted a gamma function
to our data, but chose the value of c at the upper end of its
95 % confidence interval and refitted /?. This yields a very
conservative infection profile, with c = 0.037, ft = 3.0 and
j = 1-
Proc. R. Soc. Lond. B (1995)
through time of infected cadavers placed on the soil
surface. This technique did not affect the rate of
cadaver break up and decay (M. Thomas, S. Wood &
C. Lomer, unpublished data) but effects on host
behaviour, as with most cage experiments, cannot be
discounted.
From these experiments, the transmission coefficient
for an individual cadaver was observed to change
through time (see figure 1). This pattern of infectivity
relates in part to variations in spore availability as the
cadaver breaks up and decays but the exact pattern of
the infection profile is determined by both biotic and
abiotic factors and the interactions are complex
(M. Thomas, S. Wood & C. Lomer, unpublished
data). However, these measured infection profiles do
provide a phenomenological representation of the net
infectivity of a cadaver under real field conditions (and
thus include the effects of factors such as microclimate,
pathogen isolate and host susceptibility on infection).
The essential features of these profiles are that the
infectivity of an individual cadaver has both build up
and decay phases, and lasts for several weeks. As
study, by
are well characterized by a gamma function multiplied
by a constant, and enter the models described below
accordingly.
3. H O S T - P A T H O G E N M O D E L S
H. daganensis, like many sahelian grasshoppers, has
just one generation per year. In the model for this
species, we assume that nymphs hatch at the onset of
the rains. The pathogen is sprayed 30 days after
eclosion when insects are 3-4 instar (the normal stage
at which a chemical pesticide might be applied). Those
insects contacted directly by the spray take 12 days to
die and as cadavers then become infective and initiate
new infections. This process continues until the end of
the wet season (90 days) when any surviving grass­
hoppers lay eggs and die. Grasshoppers pass through
the dry season in egg diapause during which time
pathogen is lost from the system. For Z. ,
which has essentially the same life history, we use the
same model but the timing of the seasons differ because
this species occupies more humid zones. The key
biological differences between these species and differ­
ences between environments with respect to disease
transmission, are contained within the individual
infection profiles. For both species, infection risk per
healthy individual t days after spraying in season i is
therefore given by:
determines the total
= f j G(t— x)fii(x— t ) dx. (1
Jo
f and G(. ) are defined in the legend of figure 1 and r
is the time from infection to death. The infection rate
of healthy grasshoppers is:
H,(t)I,(t)+ 5 ( 0, 0)H,(0)k, < » 0
0
where 5(0,0) is a Dirac delta function, Hf(t) is the
population of healthy grasshoppers t days after spray­
 Downloaded from http://rspb.royalsocietypublishing.org/ on June 7, 2018
Biocontrol o f locusts and grasshoppers
ing in season i,and k( is the proportion hit directly by
the spray (initial spray contact rate). The population
of healthy hosts within a season is governed by:
dHi/d t = - p i(t). (3)
Differentiation of (1) turns the within season system
into a numerically tractable set of delay differential
equations, by the ‘linear chain trick’ (MacDonald
1978; Blythe et al. 1983).
We describe between season dynamics from the end
of season i to the time of spraying in season / + 1 by:
HM ( 0 ) = r t Ht{ T ) + f ti (4) j mass divided by adult mass. Individuals within a
where riand f are normally distributed random
variables representing host reproduction and immi­
gration with mean R and F, respectively, and standard
deviation 20% of the mean (the standard deviation
allows for some between-year variation in these
variables that is likely to occur in response to changes
in weather and food quality). T is the duration of the
wet season after spraying. We neglect exogenous
density dependence on the grounds that for control we
want to keep numbers well below those at which this
becomes important.
For the desert locust we use a second model to
investigate the potential of the biopesticide for use in a mortality of grasshopper populations when sprayed
‘preventative control’ or ‘upsurge elimination’ strat­
egy (Bennett 1976), as opposed to swarm control (see
Prior & Streett (1995) for an up to date analysis of
strategies in locust and grasshopper control). In this
model we target a population of desert locusts in a
restricted breeding area (i.e. the build-up phase of a
discrete gregarious population before migration). We
assume that adults arrive at a site and start to breed.
We apply the pathogen after 30 days (allowing time for
detection of the population and for a spray team to be
deployed) and assume that sprayed individuals become
infective cadavers. We follow the course of the epizootic
for three continuous locust generations (the possible
number of breeding generations at the same site
(Roffey & Stower 1983)) and examine what effect the
biopesticide has on the size of the peak population;
reducing the size of populations and hence restricting
migration of large populations is likely to reduce the
spread of outbreaks (Bennett 1976; Prior & Streett
1995). This strategy could also apply to other locust
species, such as the red locust and the African
migratory locust, which have well defined permanent
breeding areas where damaging swarms first develop
(Joyce 1985).
In the locust model the infection mechanism is the
same as that for grasshoppers, but we explicitly
included the six nymphal instars, because infection
caused by the cadavers of different instars may be very
different. The final instar is divided into a pre-
reproductive (27 days) and a reproductive (23 days)
stage (Norris 1952; Steedman 1990). Pre-adult instar
durations were 6, 6, 6, 7 and 13 days (Steedman 1990),
and pathogen independent mortality risk was 0.04 per
day for the pre-adult instars (Roffey & Stower 1983).
Instar masses were 35, 65, 160, 600, 1100 and 1750 mg
(Steedman 1990). Eggs took 12 days from laying to
hatching (Norris 1952; Steedman 1990) and the time
Proc. R. Soc. Lond. B (1995)
M. B. Thom as and others 267
from infection to death was eight days. Mature adults
are modelled as laying some fixed number of eggs per
day, b. Instantaneous daily infection risk for any
individual is therefore given by:
rt 7
/(£ )= /? G{t—x) 2P
j Fj(x ~ 8) Ajdx, (5)
J 0 j= 1
where P, is the proportion of infected locusts which
survive other sources of mortality long enough to
expire from infection, fift) is the number of stage
locusts infected per unit time at time t and A-} is the stage
stage are treated as identical except for their age,
which determines their time of maturation from the
stage only. The instar populations are then governed
by the fundamental balance equations for structured
populations (Gurney et al.1983), and can be
numerically tractable by the same method used for the
grasshopper equations (MacDonald 1978; Blythe et al.
1983).
4. R E S U L T S AND D I S C U S S I O N
We use equations (1)—(3) to examine the total
with a biopesticide with different initial spray contact
rates (see figure 2). This figure illustrates two important
points. First, the biopesticide acts in a density-
dependent manner. This results in high density
populations suffering proportionately greater mortality
for any given spray contact rate. Second, for both
grasshopper species, the pathogen is extremely efficient
and even very low spray contact rates result in high
mortality by the end of the season. This suggests the
possibility for developing novel control strategies based
on low-level pathogen applications.
The long-term consequences of this additional
mortality (see figure 3) are measured by the relative
advantage of the biopesticide over a chemical assuming
that the chemical pesticide and biopesticide have the
same initial spray contact rate of 50% and the contact
with either spray is lethal (i.e. a simplifying assumption
ignoring sublethal effects of either spray). The relative
advantage is measured as the ratio of the predicted
frequency of spraying with a non-persistent chemical
pesticide to the frequency of spraying with a Metarhi-
zium-based biopesticide for a spray action threshold of
10 m-2 (there are no good estimates of economic
threshold densities for Sahelian grasshoppers; 10 m“2 is
an arbitrary figure representing intermediate to high
grasshopper densities). This ratio is examined as a
function of R\the mean finite rate of increase, and F\
the mean number of grasshoppers that arrive in an
area independent of the grasshopper density last year.
There are few estimates of R for Sahelian grasshoppers.
However, population dynamic studies of Z. variegatus
have suggested a range of values up to 10
(Chapman et al. 1979, 1986) so this was selected as an
upper limit for both species. Similarly, no accurate
estimates of F are available so a range of 0—1 m-2 was
selected to represent localized movement of these
species which exist in relatively discrete populations in
 Downloaded from http://rspb.royalsocietypublishing.org/ on June 7, 2018
268 M. B. Thom as and others Biocontrol o f locusts and grasshoppers

(a) (b)

Figure 2. ( a)The expected proportion of H.daganensis killed 90 days after spra

fungus, Metarhizium flavoviride, as predicted by the model given in the text and using the experimentally determined
parameters, c and ft. The proportion killed is shown as a function of the proportion hit directly by spraying, k, and
the initial grasshopper density H0.(b) Is the same as (a) but for the grasshopper species Z. v

Figure 3. Predicted frequency of spraying with a non-persistent chemical pesticide divided by frequency of spraying
with a Metarhizium flavoviride based biopesticide, as a function of R, the mean finite rate of increase, and F, the mean
number of grasshoppers that arrive in an area independent of the grasshopper density last year. ( ) Is for H. daganensis
assuming spraying occurs when the density is above a spray action threshold of 10 m-2. {b) Is for Z. variegatus again
assuming spraying occurs above a density of 10 m-2.

specific habitats (C hapm an^ al.1979, 1986;
1990; M. Thomas, S. Wood & C. Lomer, unpublished
data).
For this range of values, the biopesticide is between
6-13 times more efficient than the non-persistent
chemical pesticide for both grasshopper species. The
spray frequency of the chemical pesticide is insensitive
to F but increases proportionally with R, necessitating
several sprays a year at higher The frequency of
biopesticide applications increases with both F and R
but always reduces the grasshopper population below
the threshold by the end of the season so that it never
requires application more than once a year. The
contour plots are complicated by the fact that although
application of a conventional non-persistent pesticide
varies smoothly with R, the system controlled by a
biopesticide tends towards multi-year cycles, the
frequencies of which change quite sharply as F and R
vary: we will explore this issue in more detail elsewhere
(M. Thomas, S. Wood & C. Lomer, unpublished
data).
For desert locust we use equation (5) to investigate
how control efficiency varies with initial spray contact
rate and reproductive potential of the pest (weather
and vegetation type can cause large variation in
Steedman
fecundity and survival of desert locust (Ashall & Ellis
1962; Jackson etal. 1978). As expected, pe
lations increase as reproduction increases and as spray
efficiency falls (see hgure 4 a). Note, however, that the
estimates are if anything too high because of the very
conservative nature of the infection profile estimation.
Figure 4 b shows how many times a non-persistent
chemical pesticide would have to be applied to achieve
the same level of control as a single application of the
biopesticide. As with the grasshopper studies, this
figure shows the biopesticide to be far more effective
than a non-persistent chemical. An important extra
advantage of the biopesticide is that peak densities do
not persist for very long and for the range of parameters
shown in figure 4, expected final densities were
substantially less than 1 m~2 except at very low
fecundity and high initial hit rate, where expected final
densities were higher but less than 5 m-2.
These theoretical and experimental results dem­
onstrate that locust and grasshopper control with the
Metarhizium-based biopesticide could be highly effec­
tive. A key component in this is the fact that
grasshoppers and locusts infected with go

Proc. R. Soc. Lond. B (1995)

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Biocontrol
(a)
Figure 4. (a) Peak population densities (as adult equivalents, by mass) shown as a function of fecundity; b (the number
of viable eggs per adult per day), and initial spray contact rate, k\ for a population of Desert Locust,
allowed to reproduce for three generations and sprayed with pathogen on day 30.
population would have to be sprayed with a conventional non-persistent pesticide to keep densities below the peak
level achieved by the pathogen.
on to provide secondary sources of pathogen. The long
infection profile of infected cadavers, together with
subsequent cycles of infection provide a biological
mechanism for enhancing the persistence of the
biopesticide. Thus, under natural field conditions
where the direct impact of a spray is often limited, the
biopesticide is expected to be far more effective than
the non-persistent chemical pesticides currently avail­
able for use. As mentioned in the introduction,
biopesticide trials at appropriate scales (i.e. operational
field scales) are now beginning to provide evidence in
support of this theoretical prediction. However, further
experimental studies are required to validate the
model. Investigations into non-linearity between
pathogen and host density and the rate of infection,
sublethal and behavioural responses to infection and
the fate of infected hosts and cadavers in the held are
currently underway. Modification of any of these from
the current model could potentially reduce the
impact of the pathogen. Nonetheless, the results of this
study do highlight the possibility of exploiting the
biological properties of relatively ineffective indigenous
pathogens to develop biopesticides that act in a density
dependent manner. This possibility has rarely been
considered in the development or strategic use of
entomopathogens in biological control. Identifying this
fundamental difference between biopesticides and
conventional pesticides has significant consequences
for the economics of biopesticide use and should
provide new opportunities for biological pest control.
We thank C. Briggs, C. Godfray, D. Greathead, R. Holt,
J. Lawton, J. Magor, D. Moore, P. Neuenschwander,
C. Prior and J. Waage for helpful comments on the manu­
script. We also thank other members of the LUBILOSA
team, particularly Ignace Godonou and Comlan Gbongboui
for assistance in the field. This work forms part of the research
programme of the NERC Centre for Population Biology and
the LUBILOSA programme. LUBILOSA is a research
programme on the biological control of locusts and grass­
hoppers executed by the International Institute of Biological
Control, of CAB INTERNATIONAL; the International
Institute of Tropical Agriculture Plant Health Management
Division; the Department de Formation en Protection des
Proc. R. Soc. Lond. B (1995)
o f locusts and grasshoppers onM.
B.7,Thom
June 2018 as and others 269
(
gregaria,
The number of times the same
Vegetaux of CILSS, the Comite Inter-Etat de Lutte contre la
Secheresse au Sahel and funded by CIDA, ODA, DGIS and
SDC.
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behaviour. Desert Locust Field Research Stations Technical
Series. LAO Report No. AGP/DL/TS/24. LAO, Rome.
Steedman, A. (ed) 1990 Locust handbook, 3rd edn, p. 204.
Chatham: Natural Resources Institute.
Received 31 October 1994; accepted 5 December 1994