important aspect of the brown locust lifecycle for survival in the semi-arid Karoo is the egg
stage, which is highly resistant to drought involving a complex of diapause and quiescent
stages [14]. Solitaria phase females only lay diapause eggs, with the obligate diapause being
broken after 9–45 days under dry soil conditions, while gregaria swarming females only lay
non-diapause eggs that develop continuously under moist soil conditions. Transient phase
females lay egg pods containing various proportions of diapause and non-diapause eggs
depending upon factors including day length, phase, age and nutrition of the female [14].
Under extended dry conditions in the Karoo, the non-diapause eggs, as well as the diapause
eggs that have exited the diapause state, stop further development and enter a state of
quiescence just before the embryonic stage of katatrepsis takes place [14]. Quiescent eggs
are known to be very drought tolerant and small numbers of egg pods have been known
to survive for up to 2–3 years in the field [9,15], Price, *pers. obs.*, but the contribution of
any eggs surviving for more than 12 months was dismissed as being irrelevant to the
population dynamics of the brown locust [15]. Eggs are typically laid in dry soil and
hatch after 10–14 days following summer rainfall, with 20–25 mm of rain required for
widespread hatching [10]. There are five hopper instars, with solitaria hoppers developing
within 21–30 days depending upon temperature, while gregaria phase hoppers are much
larger with the hopper bands typically taking 42–45 days to develop in summer [10,16].
Gregarious phase females in the field mature within 2–3 weeks after fledgling and will
then lay 3–4 egg pods containing a mean of 45 eggs at weekly intervals [17], but under
laboratory conditions the females mature more quickly and can lay up to 10–15 egg pods
each [8]. Adult locusts live for 2–3 months under summer conditions, but live a lot longer
during the cooler autumn season [8]. The multivoltine lifecycle along with a high fecundity
of the brown locust allows a rapid rate of population increase with two or three generations
normally possible per year from September to May [10], with four generations recorded
during some of the more climatically favourable years [3], Price, *pers. obs*.

The brown locust is predominantly graminivorous and hoppers and adults prefer to feed on a range of Karoo grasses, but under dry field conditions the hoppers and adults can be frequently observed nibbling on the leaves and bark of Karoo bushes and anything else that is edible [10,11,16]. Eruptions of the brown locust pose a direct pest threat to the sheep grazing rangeland within the Karoo, to crops planted under irrigation within the Karoo, and more especially to the main maize and wheat cereal cultivation areas of the country that are within range of swarms escaping from the eastern Karoo. The brown locust therefore is a formidable pest problem and has been the target of chemical control campaigns waged by the South African Department of Agriculture since 1906 [18,19].

The historic periodicity of brown locust plague periods from 1797 to 1915 were re-
ported by Lounsbury [20] as lasting an average of 13 years with a recession period of
approximately 11 years between the plagues. After the introduction of Government-
funded chemical control in 1906, the periodicity of outbreak cycles was considered to
have shortened to 7–11 years of swarming activity followed by a similar period of re-
cession [3,5,12,21,22]. However, gregarious brown locust populations requiring chemical
control could be found somewhere or other in the Karoo in approximately 90% of years
throughout the entire twentieth century, although the intensity and extent of outbreaks
varied greatly [19]. The outbreak and invasion areas of the brown locust in southern Africa
as described by different authors are depicted for reference in Figure 1.
<figure><img src="image_87.png" /><figcaption>**Figure 1.** Outbreak area of the brown locust in southern Africa, as defined by Faure and Marais [1], Lea [3], Kieser [4]. Invasion area as defined by Lea [3].</figcaption></figure>

**2. History of Brown Locust Outbreaks and Control**

**2.1. Outbreak Cycles of the Brown Locust**

Incipient outbreaks develop following the successful breeding and aggregation of solitary and transient phase adults leading to rapid gregarization of the next generation of hatching hoppers. Under favourable rainfall conditions over one or more summer seasons, such incipient outbreaks often develop simultaneously over a vast area of the Nama Karoo [5]. The scattered outbreaks rapidly develop into gregaria-phase population eruptions, which then have been traditionally combated at source within the Karoo [3], in a suppressive control strategy that can be described as upsurge elimination [23] before migrating swarms can escape and threaten cereal crop production areas outside the Karoo. Since the mid-1940s, when synthetic insecticides first became available, this control strategy has largely restricted outbreaks to the Karoo with only brief invasions of surrounding countries being recorded [19]. Long-term plague cycles have been prevented and food security within the southern African region has not been seriously threatened.

The distribution and abundance of brown locust populations for the period 1906–1969 were described by Lea [12,21,22], with the relative abundance per year based on figures of control expenditure. However, financial comparisons become inaccurate over time and a more comparative analysis of brown locust outbreaks was considered to be the number of Magisterial Districts that reported locust control action per year in South Africa, Namibia and Botswana [19], although this number gave no indication of the actual intensity of the outbreaks within each of the districts. An updated graph of the number of Magisterial Districts where control action was undertaken between 1941 and 2005 is shown in Figure 2.
<figure><img src="image_88.png" /><figcaption>**Figure 2.** Number of Magisterial Districts that reported brown locust campaigns per locust season in South Africa, Namibia and Botswana between 1941 and 2005. Data obtained from Lea [3,22] for the period 1941–1954, from Lea [13,22] for the period 1954–1969, from annual reports of the South African National Dept. Agric. between 1970 and 1984, and from weekly locust control reports from the South African Dept. Agric. for the period 1984–2005. Data for Namibia and Botswana from Lea [22] and from Dept. Agric. reports from 1985 to 2005.</figcaption></figure>

Figure 2, shows the high outbreak frequency and occurrence of major eruptions or 'plague' periods over a wide area, namely during the periods 1950–1951, 1963–1964, 1970–1975, 1985–1978, 1988–1990, 1993–1997 and 1999–2001. The actual intensity of the brown locust control campaigns can be demonstrated from more recent records of the number of individual locust targets chemically controlled during each 'locust outbreak season' (September–June) over the 22 year period in South Africa between 1983–1984 and 2004–2005 (Table 1).

Intense outbreak seasons can be clearly seen (Table 1), with 'plague' eruptions, as defined by the Southern African Regional Commission for the Conservation and Utilization of the Soil (SARCCUS) sub-committee for the control of migratory pests [24] as seasons with >5000 adults swarms being controlled, being evident in 1985–1986, 1988–1989, 1993–1994, 1995–1996, 1996–1997 and 1999–2000. The continual chemical control campaigns waged against the brown locust have evidently not dampened the ability of this locust species to produce serious eruptions on a regular basis [22], with enough of the gregarious populations surviving to lay eggs before winter to ensure the ongoing eruption into the next season [19]. It is evident that the preventative control action, in the sense of stopping the plagues from developing, has utterly failed [22]. The ever increasing economic costs of the almost annual control campaigns, as well as the environmental contamination that is inevitably caused by the application of broad-spectrum insecticides in the ecologically unique Nama Karoo biome, is a serious cause for concern and introspection.
<table><caption>**Table 1.** The number of individual locust targets (roosting hopper bands and adult swarms) controlled during each outbreak season (September to June) in South Africa between 1983–1984 and 2004–2005 (data from the weekly reports of the locust control officers of the South African National Department of Agriculture).</caption><thead><tr><td>Outbreak Season</td><td>No. Hopper Bands Controlled</td><td>No. Adults Swarms Controlled</td></tr></thead><tbody><tr><td>1983–1984</td><td>61</td><td>34</td></tr><tr><td>1984–1985</td><td>633</td><td>65</td></tr><tr><td>1985–1986</td><td>175,500</td><td>38,600</td></tr><tr><td>1986–1987</td><td>68,902</td><td>14</td></tr><tr><td>1987–1988</td><td>5618</td><td>1123</td></tr><tr><td>1988–1989</td><td>85,935</td><td>1642</td></tr><tr><td>1989–1990</td><td>36,553</td><td>1392</td></tr><tr><td>1990–1991</td><td>1142</td><td>357</td></tr><tr><td>1991–1992</td><td>18,131</td><td>1603</td></tr><tr><td>1992–1993</td><td>72</td><td>0</td></tr><tr><td>1993–1994</td><td>34,581</td><td>9565</td></tr><tr><td>1994–1995</td><td>20,895</td><td>663</td></tr><tr><td>1995–1996</td><td>24,489</td><td>6577</td></tr><tr><td>1996–1997</td><td>75,890</td><td>8081</td></tr><tr><td>1997–1998</td><td>1018</td><td>80</td></tr><tr><td>1998–1999</td><td>2</td><td>0</td></tr><tr><td>1999–2000</td><td>40,115</td><td>9021</td></tr><tr><td>2000–2001</td><td>28,642</td><td>1135</td></tr><tr><td>2001–2002</td><td>1905</td><td>137</td></tr><tr><td>2002–2003</td><td>0</td><td>0</td></tr><tr><td>2003–2004</td><td>128</td><td>154</td></tr><tr><td>2004–2005</td><td>1167</td><td>20</td></tr></tbody></table>

## 2.2. Control Strategy against the Brown Locust in South Africa

Due to the devastation caused to agriculture in South Africa at the turn of the 20th century by incessant locust plagues, the South African Government first took over the coordinated responsibility for locust control in 1906 using sodium arsenite solutions ('arsenite of soda' dissolved in warm water with sugar added) applied using spray pumps [18]. Sodium arsenite aqueous and dusting formulations were used for brown locust control for the next 30 years, even though the toxicity of arsenic compounds to the spray operators and livestock was already well known with safe handling and operator protection regulations being issued [25]. Plague locusts were declared as National Pests in South Africa in 1911 in one of the first legislations promulgated by the new Government of the Union of South Africa [20]. The national pest status of locusts and the legal responsibility of landowners to report the presence of locusts on their land and for the Minister of Agriculture to be responsible for combatting locust outbreaks was ratified under Article 6 of the South African Migratory Pests Act (Act No. 36 of 1983). The principles guiding locust control in South Africa were updated and consolidated in a new policy for the management of the locust problem in South Africa [26]. The National Department of Agriculture, Land Reform and Rural Development: Directorate of Disaster Management, who are responsible for locust control, currently maintains two locust control depots in the Nama Karoo, namely at De Aar in the Upper Karoo region and at Upington in the arid Bushmanland region, managed by a
senior locust control officer at each depot who controls the stores of application equipment and pesticide stocks.

The pro-active control of incipient sub-swarming brown locust concentrations has historically been considered as being uneconomic and impractical [5,12,22] and brown locust control has always relied on an emergency response to swarming populations. Due to the seasonal nature and unpredictable location of brown locust outbreaks, the operational management of outbreaks has relied for decades on what is locally known as the “Commando system”, which activates during outbreaks with an army of temporarily employed locust officers and spray machine operators tracking down and controlling individual hopper band or roosting swarm targets. The Directorate maintains a network of District Locust Control Officers in each of the Magisterial Districts within the brown locust outbreak region, who are usually farmers with previous experience with locust control campaigns and who are re-appointed during outbreaks in order to coordinating the control campaigns in their District by directing control teams and managing pesticide and equipment resources. These officers report any control actions directly to the Senior Officers at the two locust control depots. Farmers and town residents from the local communities within each of the districts are then appointed on a temporary basis as ‘supervisors/drivers’, who use their own private pick-up vehicles for undertaking the locust control operations and who then claim a mileage allowance rate. The supervisor/drivers then appoint a small team of pest control operators (usually local farm assistants) to manage the spray machines. The district locust officers, supervisors and assistants also claim day-wage allowances when on active duty [27]. The supervisors and assistants receive protective clothing and training on the effective and safe operation of the spray equipment.

Brown locust control currently relies on the ground-based spot application of broad-spectrum, fast-acting synthetic pyrethroid insecticides, such as deltamethrin (Decis®) UL 6g a.i./ℓ, and more recently esfenvalerate (Sumi-Alpha®) UL 8g a.i./ℓ), applied at an area dosage rate of 2.5 ℓ/ha as low-volume drift sprays from motorised knapsack sprayers (Solo Port 423®) or vehicle mounted (Power Solo®, Francisco 'Bakkie' pump® and Micron Ulvamast®) equipment [27]. The vehicle-mounted sprayers are used to control the larger-sized targets. In some areas, esfenvalerate (Sumi-Alpha DP®) dusting powder is applied at rates of 5–20 kg/ha using manual backpack dusters or motorized powder dusters (Osbornbirds®). Individual hopper band and fledgling swarm targets are located by the mobile control teams and are spot-treated early in the morning while still densely aggregated on their overnight roosts and while basking in the morning sun. Hopper control is focussed on the later instar (L4–L5) gregarious hopper bands which are red and black in colour, known locally in Afrikaans as 'rooibaadjies' (red jackets). Roosting band targets can be readily spotted with the naked eye or through binoculars over a distance of up to 1–2 km in the early morning sunshine as red-coloured masses roosting on the low Karoo bushes (usually 0.3–1 m high). Adult swarms are usually tracked by the locust officers and farmers during the afternoon until they roost on the Karoo bushes in the evening and are then controlled from vehicles during the night as this provides more time to complete the control operations against these often large targets [19].

Brown locust hopper band targets are usually small and discrete, measuring between 5 m² and 0.5 ha in extent when roosting over the Karoo bushes, with >90% of hopper band targets being <0.25 ha in extent [28]. The Department of Agriculture classifies small band targets as <120 m², medium targets as 121–2500 m² and large targets as >2500 m², while roosting adult swarms average 10–14 ha in extent, but can sometimes cover 2–3 km². The aerial spraying of locust targets using spray helicopters and fixed-wing aircraft is generally unsuitable for use against the typically small-sized brown locust targets, but aerial control is employed during emergencies if the ground teams are being overwhelmed by the numbers of locust targets or if they occur in terrain which is difficult to access, or if fast-flying swarms are starting to exit the Karoo and to potentially threaten crops. The Department of Agriculture maintains a spray aircraft and spray helicopter on a stand-by contract, but emergency aerial support is also contracted from commercial crop spraying
companies when required. The aerial control of flying swarms (air-to-air spraying) is not undertaken in South Africa.

The history of the methods and insecticide products used for brown locust control are described in Table 2. Apart from the insecticides used operationally for locust control in the Karoo, a wide range of insecticide products have also been screened as possible acridicides since 1975 against the brown locust [19,28]. Please note that mention of trade names of spray equipment and commercial insecticide products in this review publication is for the purpose of providing specific information only.

<table><caption>**Table 2.** History of the methods and insecticide products used for brown locust control operations in South Africa (from the South African National Department of Agriculture and [19,28]).</caption><thead><tr><th></th><th></th></tr></thead><tbody><tr><td>Before 1906</td><td>Mechanical and cultural control methods<br>(trampling, beating, burning pastures, digging up of egg beds, collecting adult locusts in sacks, spraying soap solutions)</td></tr><tr><td>1906–1934</td><td>Application of sodium arsenite<br>(supplied free of charge to farmers and applied as aqueous or dusting formulations using hand-operated pumps)</td></tr><tr><td>1934–1944</td><td>Sodium arsenite baits<br>(moistened bran bait applied by hand to roosting hopper bands)</td></tr><tr><td>1945–1986</td><td>Benzene hexachloride (BHC)<br>(applied first as a bait agent and as aqueous spray, but mainly as a dust formulation (mainly 7% gamma isomer, but also as Lindane dust with 99% gamma BHC formulation), applied as a dusting powder from hand-operated or motorised dusting machines at area application rates of 15–20 kg/ha)</td></tr><tr><td>1975–1994</td><td>Organophosphate insecticides<br>(diazinon and fenitrothion applied as an ultra-low-volume (ULV) sprays from a range of motorised mist-blower and stacked-disc sprayers). A standard 400 g/ℓ fenitrothion formulation was applied at a volume rate of 2.5 ℓ/ha, giving an area dose rate of 1 kg a.i./ha</td></tr><tr><td>1990–to date</td><td>Synthetic pyrethroid insecticides<br>(deltamethrin and esfenvalerate applied as ULV spray at a volume rate of 2.5 ℓ/ha from motorised back-pack or vehicle-mounted sprayers). Esfenvalerate UL 8g a.i./ℓ formulation is now mainly employed in the Karoo</td></tr><tr><td>Future</td><td>New products already registered or trial work completed<br>(e.g., alpha-cypermethrin, fipronil, <i>Metarhizium myco-insecticide</i>)</td></tr></tbody></table>

## 2.3. Outbreak Early Warning Systems

The complicated relationship between the patchy rainfall distribution typical in the semi-arid Karoo areas and the development of incipient outbreaks has been studied for decades [2,3,10,12], but no conclusive patterns were found to enable an effective outbreak early warning system to be developed. Both Smit and Lea clearly thought that drought conditions of dry winters and dry early-summers, followed by widespread rainfall in late-summer, supported large-scale population increases, whilst fewer outbreaks were recorded following wet winters and wet early-summer periods. By analysing the correlations between rainfall data and swarming activity for the development of an outbreak simulation model [29], the data supported the view that dry winters followed by good early rains in the Karoo were conducive to years of locust eruptions, while wet winters were conducive to years of reduced locust numbers. The hypothesis was that the dry conditions over several months, with no rain on any one day of more than 6 mm, ensured that both diapause and quiescence in the overwintering egg populations was broken and allowed the eggs to respond to rainfall events in early summer (October–December). However, this simulation model relied on estimates of egg populations to generate outbreaks and the reliability of such detailed field data will always be problematic. However, other studies could find no statistical evidence of any connection between brown locust eruptions and previous austral winter rainfall [30], but instead found a high correlation between rainfall over
the previous 12 months prior to the locust season and in particular with rainfall during December. The hypothesis was that the high-frequency outbreak cycles were related to the El Nino/Southern Oscillation (ENSO) climatic patterns and that high-frequency locust activity was clearly evident during La Niña events (wet cycles in southern Africa) and with low locust activity during El Nino dry events. A dominant outbreak frequency of 17.3 years was proposed, with these extended cycles strongly related to the sea-surface temperatures and ENSO events [30].

The monitoring of farms with a known history of producing locust outbreaks was also employed for many years in the past as an early warning system of the build-up of solitary adult populations and the development of impending outbreaks [10,12]. The foot survey counts accurately predicted the development of incipient swarming populations based on critical population levels for phase transformation [12], but the monitoring was very time consuming and became redundant once widespread outbreaks developed.

## 2.4. Environmental Impact of Synthetic Pyrethroid Insecticides

Modern synthetic pyrethroid insecticides are safer to apply and pose less environmental risk than the arsenic, organochlorine and organophosphate compounds used for locust control in the past [31,32]. The tactics of the spot application of insecticide to densely aggregated, roosting brown locust targets also minimizes the area treated, compared with the aerial blanket-spraying undertaken against some other locust and grasshopper species.

As discussed previously, the roosting brown locust hopper band and swarm targets are usually relatively small and discrete, so only a limited area is actually spot-sprayed during control operations. Over a 20-year period, an estimated average of 75,000–90,000 ha were sprayed each year against the dense roosting targets during locust control operations in the Karoo, which is less than 0.25% of the total brown locust outbreak area [27]. Spot spraying with synthetic pyrethroids in the Karoo also has a relatively short-term environmental impact as most non-target arthropods recolonize the small treated areas within a few weeks in summer [33], while the chance that exactly the same areas are sprayed every year is also low [28]. Nevertheless, the intensity of the spraying campaigns and the negative impact that the repeated application of broad-spectrum insecticides may have on the rich diversity of endemic invertebrates and reptiles found in the Nama-Karoo biome is of concern to landholders and conservationists. How to reduce the insecticide load and minimize the environmental impact in the Karoo and yet at the same time control this serious agricultural pest has become a controversial issue. There is thus a need for more target specific and environmentally benign methods of controlling the brown locust as an alternative to the current spraying of broad-spectrum insecticides.

# 3. Alternative Control Methods

Various alternative methods of controlling the brown locust were evaluated against gregarious hopper populations in the Agricultural Research Council—Plant Health and Protection (ARC-PHP) laboratories in Pretoria and in small-scale field trials in the Nama Karoo between 1994 and 2003 [34].

## 3.1. *Natural Enemies*

A wide range of natural enemies are known to prey upon the various life stages of the brown locust [9,21,35,36] and their impact can sometimes be locally high [9]. The predation of egg pods by larvae of the woolly bee fly, *Systoechus* sp. (Bombyliidae) and the digging up of egg beds by small mammals and birds sometimes caused up to 12% mortality of egg pods [34]. The voracious ants, *Camponotus fulvopilosus* and *Anoploepis custodiens*, were also sometimes important predators of hatching hoppers, while various species of robber flies, ground beetles, hunting wasps, scorpions, spiders, lizards, mammals (e.g., jackals, mongooses, feral dogs) and a wide range of bird species are opportunistic predators of all life stages of the brown locust [34]. Of particular interest was the impact of the sarcophagid fly, *Wohlfarhtia pachytyli* (Walker), which is a generalist scavenger as well as a facultative
parasite of moulting L5 brown locust hoppers and fledglings [37]. The fly larviposits on moulting locusts when they are immobilised and unable to defend themselves from fly attack. In contrast, no parasitism of active hoppers or adults was observed [37,38]. The fly was common throughout the Karoo and highest fly populations were always associated with brown locust outbreaks. Locusts parasitised by fly maggots were regularly found at roosting sites where hopper bands had moulted, or where fledgling had occurred. However, intensive sampling showed that *W. pachytyli* failed to cause more than 0.1% mortality of hoppers and 6% mortality of fledgling swarms [38]. These figures suggest that the potential of *W. pachytyli* as a biological control agent may have been overestimated in the past [38]. Despite the wide range of opportunistic predators and parasites reported, their impact on brown locust populations was usually very low. On no occasion were natural enemies observed in sufficient numbers to dampen the intensity of brown locust outbreaks [34].

## 3.2. *Mechanical Control*

Before the first insecticides became available at the turn of the 20th century, farmers had to resort to beating, trampling, trenching and burning to protect their crops and pastures from the ravages of locusts [18,39]. Turning back the clock, the destruction of locust egg beds and the harvesting of locusts were re-examined as control methods. Brown locust egg beds proved very difficult to locate in the remote Karoo, but once found, the excavation of locust eggs with picks and garden forks gave excellent control. However, the disturbance of the friable soils in the Karoo would cause severe erosion problems and is therefore not advocated. Harvesting of live locusts using nets or vacuum machines was not practical as locusts either scattered upon disturbance, or retreated into the interior of the spiny Karoo bushes to avoid capture. However, the harvesting of locust cadavers lying on the soil surface following insecticide spraying, once they had dried out and insecticide residues had broken down, was possible. With their high protein and fat content, the processing of locust cadavers into animal feed may become economically viable in future.

## 3.3. *Insecticide Baits*

Bran bait containing 2–3% sodium arsenite was extensively used for the control of brown locust and red locust hopper bands in South Africa during the 1930s [40]. The baiting technique was re-evaluated as a more target-specific, low cost method of locust control using two modern insecticides, the non-ester pyrethroid, silafluofen (Neophan®), and the phenyl-pyrazol, fipronil (Regent®). Bioassays showed that these insecticides, when dissolved in water and mixed into wheat bran as the edible carrier, had a potent stomach action and were effective in minute quantities against the brown locust. Bran baits containing 0.2% Neophan 80EC and 0.02% Regent 200SC were prepared in the field and were broadcast by gloved hand onto the soil surface around bushes occupied by hopper bands as overnight roosting sites [34,41]. The densely aggregated hoppers descended from their roosts to bask at the base of the bushes and fed avidly on the bait. Hoppers became visibly affected within 2–3 h and usually died within 24 h.

Batches of 5 and 10 kg of both baits gave excellent control (>95%) of small and medium sized hopper bands roosting over an area of 10–100 m² and 101–250 m², respectively. However, baiting was only effective if undertaken shortly after sunrise, before hoppers descended from their roosts and scattered from the baited area. Baiting large bands or diffuse targets, or baiting later in the day once hoppers became active, was not effective [41]. Baiting was more practical under autumn conditions in the Karoo when there was more time during the cool mornings to locate and bait bands before they descended from their roosts. Baiting was inexpensive and was easy to prepare and apply, requiring basic equipment and limited training. Baiting was also a more target-specific method of controlling locusts as there was no off-target drift of insecticide and it only killed the hoppers and some other insects that ate it. Baiting could thus be effectively used for small-scale locust control by rural communities, or in conservation areas where more target-specific
locust control is required [34]. However, the logistics of the bulk transport, preparation and application of locust baits under large-scale operational conditions appear daunting.

### 3.4. Insecticide Barrier Treatments

Barrier treatments, based on the application of the organochlorine insecticide, dieldrin, applied to narrow strips of vegetation were extensively used in North Africa to control marching bands of the desert locust [42]. Following the withdrawal of dieldrin during the 1970s due to its high persistence and bio-accumulation in the environment [43], the most promising candidates to have emerged as a replacement for dieldrin in barrier treatments have been various insect growth regulator (IGR) compounds and the phenyl pyrazole insecticide, fipronil. These compounds provide moderate persistence in the environment without the bio-accumulation problems of dieldrin [23]. In recent years, fipronil (Adonis UL®) barriers have been successfully applied from aircraft under operational conditions against hopper bands of the Malagasy locust, the Australian plague locust and the desert locust. However, insecticide barrier treatments have never been used operationally against the brown locust.

The high efficacy of fipronil against the brown locust was established in laboratory bioassays and in small-scale field trials of ULV cover sprays. Field trials of fipronil (Adonis® 5UL) barriers, applied to 21 m-wide strips of Karoo vegetation at a volume rate of 2.5 l/ha (giving an area dose rate of 12.5 g a.i./ha) from motorized 'Solo 432' knapsack sprayers, were used to intercept marching gregarious brown locust hopper bands. Barriers of Adonis® applied at 12.5 g a.i./ha proved very effective against L2–L3 bands and against small-size L4–L5 bands, giving >90% control within 48 h [34]. However, a lower dose rate of 7.5 g a.i./ha in similar barrier strips proved largely ineffective against L3–L5 marching bands. Even at the high 12.5 g a.i./ha dose rate, the barriers sometimes failed to adequately control large and mobile L5 hopper bands that maintained cohesion and had sufficient momentum to march quickly through the relatively narrow barrier strips before the majority of hoppers acquired a lethal dose. For maximum efficacy it was vital that hoppers consumed fipronil-treated vegetation and barriers proved less effective where the vegetation density was sparse or where the vegetation was less palatable to hoppers [34].

Despite these factors, Adonis® barriers were considered to have potential for the passive control of brown locust hopper bands in the more remote western areas of the Karoo, especially during the early stages of an outbreak when young-instar hopper bands become mobile. The high mobility of the hopper bands, which can march at least 1–3 km per day in summer, would suggest that even a low-density network of insecticide barriers, set 5–10 km apart, would soon be intercepted by marching bands. However, the fipronil product has a comparatively high environmental impact against non-target organisms, with the product assigned a high-risk rating by the FAO against terrestrial non-target organisms and a medium risk against mammals, reptiles and aquatic arthropods [44]. This is a similar environmental risk rating as malathion, which is extensively applied as an area treatment against the desert locust. The FAO Pesticide Referee Group recommends a dose rate of 4.2 g/ha Adonis® for wide barrier treatments applied from aircraft against other locust and grasshopper species [44]. Any barrier treatments would have to be judiciously applied to restrict the environmental impact of Adonis® against non-target organisms in the Nama Karoo environment.

### 3.5. Insect Growth Regulators (IGRs)

The benzoylphenyl urea IGR products only affect the juvenile stages of insects and are thus relatively target specific with a limited environmental impact [45]. Various IGRs have been used operationally as barrier treatments or cover sprays against a number of locust and pest grasshopper species [23]. Laboratory bioassays with the IGRs, flufenoxuron and teflubenzuron, applied to maize leaf discs and fed to L5 brown locust hoppers at dose rates of 3–15 µg/g per hopper, gave variable mortality of 30–70% after a single ingestion [34]. However, when diflubenzuron (Dimilin OF6®), was sprayed onto maize
plants at volume rates of 1–3 l/ha and subsequently fed to L2 hoppers, 100% mortality of hoppers was produced within 11 days at all application rates as long as the hoppers were continuously exposed to treated vegetation. However, irregular exposure to Dimilin® during the inter-moult period produced unsatisfactory mortality, as the product is evidently non-accumulative and is readily excreted [46]. The fact that brown locust hoppers have to feed regularly on IGR-treated vegetation during the entire inter-moult period, combined with the high mobility of hopper bands, would probably make IGR barriers unsuitable for brown locust control operations. To increase the likelihood of hoppers ingesting treated vegetation, large areas would have to be block-treated from aircraft, or multiple barriers would have to be applied in parallel across vast tracts of the Karoo. These application strategies are clearly uneconomic and are not environmentally acceptable.

### 3.6. *Metarhizium Myco-Insecticide*

Myco-insecticides, comprising the aerial conidia of certain isolates of the entomopathogenic fungus, *Metarhizium acridum* ((Driver and Milner) J.F. Bisch., Rehner and Humber), formulated in oil and applied through conventional spray equipment, have proved effective against a range of locust and pest grasshopper species [47,48]. Myco-insecticides have a low environmental impact and are recommended for locust control in environmentally sensitive areas as replacements for synthetic insecticides [49]. Commercial myco-insecticide products have been shown to be effectively in large-scale operational use against the Australian plague locust, as well as against locust outbreaks in China [50]. Such products have also been used on occasion against the red locust and desert locust.

Under suitable application conditions the *M. acridum* (LUBILOSA isolate IMI 330189) myco-insecticide, applied at a standard dose of 100 g conidia/ha from hand-held ULV spinning disc apparatus, or from microlight aircraft fitted with micronair AU 4000 atomisers, regularly produced >90% mortality of L5 brown locust hoppers sprayed in the field and then maintained in cages [51,52]. However, speed of kill was slow, with median lethal times of 10–13 days for the ground and aerial application trials, respectively. In most cases, acceptable >90% mortality was not achieved for at least three weeks after application, although affected hoppers did show reduced feeding behaviour [53]. Despite the slow speed of kill in the small-scale trials, the myco-insecticide agent was considered a significant advance in brown locust control and was commercially registered as Green Muscle® in South Africa in 1998 under the South African Agricultural Remedies Act (Act 36 of 1947). However, subsequent studies showed that various factors negatively affected the performance of Green Muscle® against the brown locust. The hot and dry Karoo environment, combined with the high ultra-violet radiation typical of the latitude and altitude of the Karoo, is detrimental for the survival and transmission of fungal conidia. The most important constraint, however, proved to be the unusually active thermoregulation behaviour of brown locust hoppers in the field that enabled them to elevate and maintain their body temperature 2–3 °C above normal [54]. This ‘behavioural fever’ elevated the body temperature of the locust above the threshold for optimum growth of the fungal pathogen and effectively suppressed the development of mycosis under certain field conditions for up to 70 days [55]. The great variability of performance of the myco-insecticide was not evident in the cage samples taken during the earlier trial work, as the caged locusts were unable to thermo-regulate to the same extent to defer the onset of mycosis. This unfortunately gave a false impression of the true speed of kill in the field.

The lack of a rapid knock-down action and the slow speed of kill currently makes Green Muscle® unsuitable for spot spraying operations in the Karoo. The thousands of individual hopper bands treated during control campaigns, and the high mobility of marching bands, would make the easy recognition of treated and untreated targets by locust officers impossible. Its use in conservation areas is also currently not practical, as treated bands would soon march out of these relatively small and fragmented areas. An alternative application strategy to manage the slow speed of kill needs to be developed and tested, before Green Muscle® can be considered for brown locust control.
3.7. *Pathogenic Micro-Organisms*

Apart from entomopathogenic fungi, a range of other pathogenic micro-organisms
have been isolated from locusts and grasshoppers, including bacteria, entomopoxvirus,
microsporidia, protists and nematodes [56]. Biological control of locusts and grasshoppers
using the augmentative release of pathogens has met with mixed success [57] and has been
considered as being impractical because of the technical problems and expense involved in
the mass production and application of pathogens.

Various strains of the spore forming bacteria, *Bacillus thuringiensis* Berliner (Bt), have been commercialised world-wide as microbial insecticides against various Lepidoptera, Coleoptera and Diptera pests. However, none of the commercially available Bt strains has proved sufficiently pathogenic against locusts because of the acid pH of the Orthoptera gut which prevents the Bt endotoxin crystals from dissolving [58]. In bioassays against the brown locust, four Bt strains that showed an enhanced acid-tolerance were fed to L3 and L4 brown locust hoppers as freeze-dried Bt spores mixed into bran bait at a dose rate of 1mg spores/g dry bran. However, none of the Bt baits produced any significant mortality compared with the untreated controls [34].

Another pathogenic micro-organism evaluated against the brown locust was an en-
tomopoxvirus (EPV) isolated from a West African grasshopper, *Odaleus senegalensis* (De
Geer), which had shown potential for the control of some rangeland grasshopper pests
in the western USA [59]. However, bioassays of the virus suspension applied to maize
leaf discs and fed to different brown locust hopper instars at a range of dosage rates did
not produce any observed infection or mortality compared with untreated controls [34].
Entomopoxviruses are known to be relatively host specific [60] and the virulence of the
imported EPV against acridids other than its direct grasshopper host may be low.

4. Alternative Control Strategies

The regular and often intense outbreaks of the brown locust present a formidable pest control problem. Locust control operations have evidently failed as they have been unable to stop the regular plague cycles from developing [22]. The typical large-scale incipient upsurges over a wide area of the Karoo are impossible to prevent and once the populations develop into gregaria phase eruptions then the only option is to undertake a large-scale and expensive chemical control campaign. However, chemical control operations are rarely able to subdue the large-scale eruptions on their own and such extensive control campaigns are usually assisted by the onset of unfavourable dry or cold climatic conditions that restricts further locust breeding and supresses the eruptions. Fipronil (Adonis®) barrier treatments and insecticide baits were considered to have sufficient potential to be incorporated into an integrated management strategy against brown locust hopper bands in certain areas of the Karoo. Although there is concern regarding the environmental impact of fipronil, the barriers could have potential if judiciously applied to intercept marching hopper bands in the more remote areas of the Karoo, while insecticide baits could have application in specific areas where a low environmental impact was required. However, no alternative control method was considered sufficiently flexible and effective enough under all field conditions to entirely replace the application of synthetic pyrethroid insecticides in the Karoo. Fast-acting ULV insecticides will hence continue to provide the backbone of the brown locust control programme for the foreseeable future.

The current 'Commando' system of ground-based locust control has been in operation for decades in the Karoo, partly because it has provided a relatively cost-effective strategy against the unpredictable intensity and distribution of brown locust outbreaks across the Karoo, while also ensuring that Government finances are channelled to pay local inhabitants to fight the locusts as temporary employees when needed. However, the tracking down and spraying of thousands of individual hopper bands and roosting swarms has long been considered as an inefficient use of manpower and resources. Records dating back to the mid-1960s and again confirmed in the 1990s showed that the targeting the hopper bands accounted for up to 90% of the locust control budget, but only accounted for 10%
of the actual number of locusts controlled, whereas the targeted spraying of roosting adult swarms accounted for an estimated 90% of the locust population [61,62]. In recent years, the traditional Commando system has also become more difficult to sustain due to the spiralling costs of transport and insecticides, as well as the costs of hiring the large temporary labour force. The ongoing depopulation of farms in the more remote and arid areas of the Karoo means that there is a very low density of resident farmers left to report the locusts. In addition, the changing attitudes of some landholders towards reporting locusts due to their conservation views on the spraying of pesticides, or more especially regarding the security concerns on the farms, has therefore limited access to farms for locust surveys and has negatively impacted the efficacy of the locust reporting and control network. Outbreaks on the large-sized farms in the remote Central Karoo and Bushmanland areas therefore often go undetected and the local control capacity can be suddenly overwhelmed by swarm escapes.

Alternative strategies of combatting outbreaks in the remote areas of the Karoo are required as an alternative to the traditional active location and spot spraying of individual locust targets. There is therefore a need to discuss possible alternative strategies based on sound economic and logistical principles.

## 4.1. Abandoning Brown Locust Control Entirely

Historical records showed that the uncontrolled brown locust plagues in the past (before 1940) all eventually collapsed due to a combination of factors including the build-up of natural enemies and diseases, the onset of unfavourable climatic conditions, or as a result of the exodus of swarms into areas that were unsuitable for further breeding, e.g., the mountain Kingdom of Lesotho. Earlier plague cycles were then always followed by a long recession period since the swarming populations had all vacated the optimal breeding areas in the Karoo [12,22]. By not controlling locust outbreaks, it can be argued that the outbreaks will always come to an end naturally and the money saved on control operations could be used instead to compensate for crop losses. However, the uncontrolled brown locust plague cycles between 1890 and 1940, as well as the various invasions of red locust and African migratory locust plagues into South Africa during this time, posed a devastating threat to agricultural production throughout southern Africa, causing the threat of starvation amongst rural communities. The South African and other African Governments will not tolerate this threat to food security again.

There is still an economic and environmental debate on whether locusts and grasshoppers should be chemically controlled to protect rangeland grazing [32], especially in the Karoo where the cost of locust control per hectare is usually far more than the grazing value of the land [63]. However, other studies estimated the amount of grass consumed by the brown locust hoppers and correlated this with the consumption by sheep, suggesting that it was economically viable to control the locusts in the Karoo to save the available grazing for the sheep flocks [64]. To counter these findings, it can be argued that most of the locust control operations are undertaken against late instar hopper bands and fledgling swarms when the damage to the local grazing has already been done. There is no doubt, however, regarding the need to control locust and grasshopper outbreaks within the rangeland areas to protect vulnerable staple food crops such as maize, wheat and millet grown outside the rangeland areas [32,65]. Likewise in the Karoo, the brown locust problem will have to be continually managed and contained within the outbreak area so that damage to food crops outside the Karoo is prevented as much as possible.

## 4.2. Update the Current "Commando System"

Within the Upper Karoo region (e.g., area containing the Districts of Prieska, Douglas, Strydenburg, Britstown, De Aar, Philipstown, Hopetown, Hanover, Richmond, Victoria West), as well as the adjacent Districts to the east and south-east, there is a higher population of resident farmers and farm workers on the relatively smaller-size farms (2000–5000 ha), as well as a good communication network. In these areas, the traditional Commando system
of locust control can still work well once the manpower and operational resources are in place and is generally considered to be a viable and cost-effective strategy for brown locust control. However, in the more remote western areas of the arid Bushmanland and the Central Karoo, the Commando system has become ineffective due to the demographic and economic factors discussed earlier. If the Commando system is still to be applied throughout the Karoo it will have to be modernised and substantially resourced to improve the capacity to locate locust targets by implementing an effective locust monitoring and outbreak early warning system. This implies a substantial investment in regular monitoring of known locust outbreak 'hot-spot' areas, as well as resources for the implementation of technologies for effective target location and mapping systems to support the Commando teams. It is also highly recommended that the control teams should focus on the spraying of the fledgling swarms as they coalesce, as well as the larger-sized hopper bands as they aggregate, rather than spending most of their time and resources tracking down and spraying individual small-sized hopper band targets.

There are various digital field tools and GIS mapping systems used in locust control forecasting and field control operations in other parts of the world, such as the FAO's recently introduced 'eLocust3' system used in the desert locust campaigns. Survey teams can log the local survey observation data, as well as information on local climatic and vegetation conditions, onto a digital tablet that then transmits the data via satellite to a national locust command centre. All the data is precisely GPS geo-referenced and the survey or control data is then automatically downloaded onto the FAO's 'RAMSESV4' database software application and GIS mapping platform, which can combine multiple observation inputs along with dedicated layers of GIS spatial information to generate visual maps of the target areas. The GIS maps are then a powerful tool for early warning forecasting, or for directing field control operations.

Climate monitoring and vegetation greening index satellites are also employed for wide-scale desert locust forecasting in order to monitor rainfall events, soil moisture conditions and vegetation greening in remote desert regions. Such technology is readily available in South Africa and should be adopted by the brown locust management strategy to assist with outbreak forecasting. Likewise, there are sophisticated climatic models used in crop yield forecasting that could be readily adopted to model and predict rainfall conditions in the Karoo over the medium-term. The use of unmanned aerial vehicles (drones) is also showing potential for locust survey work in desert locust campaigns and can be used to locate green vegetation zones in desert areas where locusts are likely to aggregate and oviposit. The survey and location of isolated ecotone areas of tall grass and open bare patches of soil typically suitable for brown locust adult aggregation and for nearby oviposition, defined as the locust 'concentration belts' [16], could certainly benefit the locust survey teams in the Karoo by reducing the need for the extensive foot surveys.

### 4.3. Abandon Hopper Control and Target Adult Swarms Only

Using modern spray aircraft to target young swarms as they mill around and aggregate into large-size targets is standard control strategy in various countries, such as Australia and Madagascar. The similar convergence and coalescence of brown locust swarms into large swarm targets has also been regularly observed in the Karoo [61], Price, pers. obs. Apart from the high work rate of spray aircraft and the large areas that can be quickly spayed, adult locusts are also known to be more susceptible targets to kill with insecticides than late instar hoppers, which has important consequences for reduced insecticide application and environmental impact. Aircraft would only be brought into operation once a threshold number or size of swarms had developed and once cereal crops were threatened. The co-ordinated air-to-air spraying of flying swarms using low dosages of synthetic pyrethroid insecticides, accurately applied from aircraft fitted with GPS systems can effectively control even large-scale plagues. The active spotting and tracking of swarms could be done along strategically placed observation stations.
A limited number of small to medium capacity spray aircraft, such as the Piper Pawnee, Gippsland GA200C and the Air Tractor series, could intercept large-size swarms as they aggregated and migrated along their traditional seasonal flyways out of the Central and Upper Karoo. The active spotting and tracking of swarms could be done along strategically placed observation stations. Aircraft operating from the larger towns in the Upper Karoo, such as De Aar, Britstown and Hopetown, could attack swarms once they entered a 100–150 km wide buffer zone stretching along the Orange River. Outbreaks in the Great Karoo could be controlled with aircraft stationed at Beaufort West or other suitable locations. Small-scale outbreaks may even be managed with microlight aircraft equipped with appropriate spray gear for ULV application, as has been demonstrated in earlier trial work carried out by the ARC-PHP.

## 5. Conclusions

The current Commando system of managing the brown locust is only considered as being viable and effective in the Upper and eastern Karoo regions where there is a sufficient density of resident farmers and farm workers who can report outbreaks and where good communications exist to be able to rapidly respond and obtain access to the locust targets. However, the Commando system is not currently effective over a vast area of the Central and Great Karoo and Bushmanland. The scattered outbreaks throughout these areas should be left to fledge into adult swarms, which would then soon aggregate into large-sized swarms that would make viable targets for spray aircraft. The benefits (pros) and constraints (cons) of the alternative brown locust control strategies discussed are summarized in Table 3.

<table><caption>**Table 3.** Comparison of current and alternative strategies to manage the brown locust.</caption><thead><tr><td>Control Strategies, Current and Alternatives</td><td>Benefits (pros)</td><td>Constraints (cons)</td></tr></thead><tbody><tr><td>0-‘Commando’ system</td><td>Current strategy. Long history, community-based system, local knowledge and communication networks, per diem payments to local people for operations, good control of small outbreaks and able to dampen large upsurges. Spray roosting swarms at night so more time to control large-size targets.</td><td>Not effective in some areas, weak reporting from remote farms, reduced access to all farms, mainly target L5 bands so not cost effective, not able to stop large upsurges or prevent plague cycles. No central coordination of operations or situation over-view, no early warning or mapping of outbreaks, sub-optimal use of strategic resources.</td></tr><tr><td>1-Abandoning brown locust control entirely</td><td>With natural enemies and diseases, unfavourable climatic conditions, exodus of swarms into unsuitable areas, outbreaks will always end naturally. Ecologically sustainable. Money saved on control operations could be used to compensate for crop losses. No environmental damage from pesticides.</td><td>Large-scale outbreaks cause severe damage to Karoo grazing, widespread damage to commercial cereal crops outside the Karoo, threat of starvation amongst smallholder farmers and rural communities. Swarm invasions into neighbouring countries, political pressure on South Africa to contain locust outbreaks.</td></tr><tr><td>2-Update the current “Commando system”</td><td>Adoption of modern GIS technology for target reporting and campaign management, more focus on control of aggregating swarms, more effective deployment of resources, better planning and direction of operations, more tactical use of spray aircraft when required. A viable and cost-effective strategy for brown locust control in some areas, such as the Upper and eastern Karoo. Will work well once the manpower and operational resources are in place.</td><td>Outdated and not currently effective over a vast area of the Central and Great Karoo and Bushmanland. Substantial investment necessary in new technologies. Will still have weak reporting of targets in remote areas, risk of sub-optimal adoption and use of technologies. Fewer locust control teams required—loss of income for communities. Availability, coordination and high costs of spray aircraft.</td></tr></tbody></table>
<table><caption>Table 3. *Cont.*</caption><thead><tr><th>Control Strategies, Current and Alternatives</th><th>Benefits (pros)</th><th>Constraints (cons)</th></tr></thead><tbody><tr><td>3-Abandon hopper control and target adult swarms only</td><td>Adult swarms naturally coalesce to form large targets. Adult locusts are known to be more susceptible targets to kill with insecticides than late instar hoppers. Farmers and locust officers spot and report the swarms, limited number of small to medium capacity spray aircraft required. Sophisticated commercial aerial spray companies in South Africa. Reduced insecticide application and environmental impact.</td><td>During large outbreaks adult populations develop simultaneously over wide areas, swarm spotting capacity and spray aircraft resources overwhelmed, massed swarm escapes from the Upper and eastern Karoo. More locust damage to Karoo grazing and increased threat to cereal crops outside Karoo. Political pressure from commercial farmers and rural communities, swarm invasion of neighbouring countries.</td></tr><tr><td>4-Necessity of an IPM approach Modernised and well-resourced Commando system in the Upper Karoo and eastern Karoo, spraying fledgling swarms and large hopper bands. + Stop using ground-based 'Commando' system in remote areas of central and western Karoo where ineffective and switch mainly to aircraft control of aggregating swarms.</td><td>Modernize and support Commando system in Upper and eastern Karoo. Stop wasting finances and resources with current ineffective system in remote areas. Locust officers now employed to spot and track aggregating swarms and to direct spray aircraft to targets. Use modern technology to map outbreaks and to direct ground operations and aircraft campaign. More effective allocation of manpower and resources. More effective kill of locusts (dead locusts per litre of insecticide).</td><td>Farmer political pressure that remote areas of Karoo are being 'neglected', loss of potential income for locust officers and spray teams. Manpower for spotting and tracking swarm targets in remote areas. Availability and coordination of aircraft for swarm control. High costs of hire aircraft capacity. New ULV formulations required for aircraft. Short window to spray roosting swarm targets in the morning.</td></tr></tbody></table>

When reviewing possible options for controlling the brown locust, the most effective strategy probably lies with an integrated locust management strategy, with a modernised and well-resourced Commando system in the Upper Karoo and eastern Karoo that focusses on the spraying of coalescing fledgling swarms and the larger hopper band targets, supported by the judicious use of aircraft for the aerial control of swarms developing in the more remote regions of the Karoo. Such an integrated strategy combining ground and aerial tactics would have the flexibility and the capacity to deal effectively with all locust emergencies. It is also vital to invest more resources in technology for the early-warning forecasting of brown locust outbreaks in relation to climatic conditions, along with timely surveys of known outbreak hot-spot farms early in the season. The use of digital technology data gathering and mapping systems would also enhance the ability to manage the outbreaks as they developed and would allow resources to be deployed more judiciously.

**Funding:** Received from the ARC-Plant Health and Protection.

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** None applicable.

**Data Availability Statement:** Data sharing not applicable.

**Acknowledgments:** To my late colleagues and mentors, Dick Brown and Peter Napier-Bax, for their camaraderie on our numerous locust field trips throughout the Karoo. Thanks to the many hospitable Karoo farmers who allowed us to work on their land and to the locust officers who enthusiastically guided us to the locust targets. Thanks to the ARC-Plant Health and Protection for the financial and administrative support, as well as the various Agro-Chemical companies and to CABI for financial support for specific projects within the study. Thanks to the South African Department of Agriculture for providing the weekly locust control data and to my colleague, Margaret Kieser, for analysing and computing the locust data.

**Conflicts of Interest:** The author declares no conflict of interest.
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Review

# A Review of the Biology, Ecology, and Management of the South American Locust, *Schistocerca cancellata* (Serville, 1838), and Future Prospects

Eduardo V. Trumper <fnref n="1" />,* ID, Arianne J. Cease <fnref n="2" />, María Marta Cigliano <fnref n="3" />,<fnref n="4" />, Fernando Copa Bazán <fnref n="5" />, Carlos E. Lange <fnref n="4" />, Héctor E. Medina <fnref n="6" /> ID, Rick P. Overson <fnref n="2" />, Clara Therville <fnref n="2" /> ID, Martina E. Pocco <fnref n="3" />,<fnref n="4" />, Cyril Piou <fnref n="7" />, Gustavo Zagaglia <fnref n="8" /> and David Hunter <fnref n="9" /> ID

**Citation:** Trumper, E.V.; Cease, A.J.; Cigliano, M.M.; Copa Bazán, F.; Lange, C.E.; Medina, H.E.; Overson, R.P.; Therville, C.; Pocco, M.E.; Piou, C.; et al. A Review of the Biology, Ecology, and Management of the South American Locust, *Schistocerca cancellata* (Serville, 1838), and Future Prospects. *Agronomy* 2022, 12, 135. https://doi.org/10.3390/agronomy12010135

Academic Editor: Stefano Bedini

Received: 22 October 2021

Accepted: 24 December 2021

Published: 6 January 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

<figure><img src="image_91.png" /></figure>

Copyright: © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

**Abstract:** In the first half of the twentieth century, the South American Locust (SAL), *Schistocerca cancellata* (Serville, 1838), was a major pest of agriculture in Argentina, Bolivia, Paraguay, Uruguay, and Brazil. From 1954–2014, a preventive management program appeared to limit SAL populations, with only small- to moderate-scale treatments required, limited to outbreak areas in northwest Argentina. However, the lack of major locust outbreaks led to a gradual reduction in resources, and in 2015, the sudden appearance of swarms marked the beginning of a substantial upsurge, with many swarms reported initially in Argentina in 2015, followed by expansion into neighboring countries over the next few years. The upsurge required a rapid allocation of resources for management of SAL and a detailed examination of the improvements needed for the successful management of this species. This paper provides a review of SAL biology, management history, and perspectives on navigating a plague period after a 60-year recession.

**Keywords:** locust plagues; population dynamics; management

## 1. Introduction

Locusts are among the most devastating pests globally and leave clear imprints in memories and historical records. The substantial impact of the South American Locust (SAL), *Schistocerca cancellata* (Serville, 1838), on agriculture and cattle production shaped the early stages of the government agricultural service in Argentina. Going back at least to the first half of the nineteenth century and during the first half of the twentieth century, there were frequent plague periods where SAL invaded other countries, including Bolivia,

<footnote n="1">¹ Estación Experimental Agropecuaria Manfredi, Instituto Nacional de Tecnología Agropecuaria (INTA), Manfredi X5988, Argentina</footnote>

<footnote n="2">² School of Sustainability, Arizona State University, Tempe, AZ 85287, USA; acease@asu.edu (A.J.C.); roverso@asu.edu (R.P.O.); clara.therville@gmail.com (C.T.)</footnote>

<footnote n="3">³ División Entomología, Museo de La Plata, FCNyM-UNLP, La Plata 1900, Argentina; cigliano@fcnym.unlp.edu.ar (M.M.C.); martinapocco@fcnym.unlp.edu.ar (M.E.P.)</footnote>

<footnote n="4">⁴ Centro de Estudios Parasitológicos y de Vectores, UNLP-CONICET-CICPBA, La Plata 1900, Argentina; carlosl@cepave.edu.ar</footnote>

<footnote n="5">⁵ Instituto de Investigaciones Agrícolas El Vallecito, Universidad Autónoma Gabriel René Moreno, Km 7 1/2 Carretera al Norte, Santa Cruz de la Sierra, Santa Cruz, Bolivia; anfecopa@gmail.com</footnote>

<footnote n="6">⁶ Servicio Nacional de Sanidad y Calidad Agroalimentaria (SENASA), Av. Paseo Colón 367, Buenos Aires C1063ACD, Argentina; hmedina@senasa.gob.ar</footnote>

<footnote n="7">⁷ Unité Mixte de Recherche Centre de Biologie pour la Gestion des Populations (UMR CBGP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), 755 Avenue du Campus Agropolis, CS 30016, F-34398 Montpellier, France; cyril.piou@cirad.fr</footnote>

<footnote n="8">⁸ Servicio Nacional de Sanidad y Calidad Agroalimentaria (SENASA), España 366 Piso 3, Salta A4400, Argentina; gzagaglia@senasa.gob.ar</footnote>

<footnote n="9">⁹ Locust and Grasshopper Control, 125 William Webb Drive, McKellar, Canberra, ACT 2617, Australia; davidmhunter100@gmail.com</footnote>

<footnote>* Correspondence: trumper.eduardo@inta.gob.ar</footnote>
Paraguay, Uruguay, and Brazil [1]. The available historic records show that recession periods were the exception rather than the rule [1], but between 1954 and 2014, coinciding with the implementation of a preventive management program, there were no large-scale upsurges, with only localized outbreaks from time to time within Argentina [2,3]. However, there was an upsurge in the number of swarms in Argentina in 2015, and by early 2017, swarms reached Bolivia and Paraguay [3]. This rapid expansion of the locust populations meant that the infrastructure for managing locusts had to be quickly rebuilt.

Locusts differ from most agricultural pests. They are sporadic, have the capacity to rapidly expand across borders, and then contract to localized pockets that act as reservoirs for future outbreaks [4]. The key to successful management is not only knowledge of locust biology and design of sound management strategies but also a robust organization and maintenance of stakeholder engagement. In the case of SAL, a preventive strategy was established by the Argentinean government during the mid-1950s. Organizations for permanent surveillance and control of locusts were established as part of Departments of Plant Health and Acridology of a number of provinces in northwest Argentina [1]. The preventive management system successfully kept SAL populations quite low and generally limited to Catamarca and La Rioja, where preventive management actions were systematically conducted by field teams. The preventive management went largely unnoticed so that the general public thought that the pest had been eradicated, and with no obvious outbreaks, political support and funding gradually declined [2,3]. Thus, the recent resurgence of SAL, six decades after the last major plague, meant public agencies as well as private stakeholders faced the challenge of recovering capacities to deal with an almost forgotten problem.

Across six decades, many things changed, with the most relevant and apparent being land use and the emergence of a more complex matrix of stakeholders. Additionally, there was a change in the way complex problems were dealt with, with a clear worldwide claim for and trend of more participatory approaches for diagnosis, research, and innovation. Naturally, the key questions are (1) “why” and “how” did SAL re-emergence happen, and (2) how to best manage the system into the future. The answer to the first is likely a complex combination of factors including changes in the natural system (land use and convergence of favorable meteorological conditions likely attributable to climate change), and a reduction in monitoring and control operations. To begin to answer these questions, we need to revisit what we know about the problem from different perspectives, considering the new context in terms of the scientific, technological, agricultural, and social matrix.

The present article reviews SAL biology, including a description of typical habitats, temporal changes, and migration, as well as how management changed during the twentieth century. With the sudden and unexpected resurgence of SAL in 2015 [3], a whole new process began, characterized by a steep learning curve in the face of a dramatic upsurge in locust numbers. This process involved the engagement of new stakeholders and cooperation on different fronts that had not been experienced previously: research and development, governance of the emergency, and management of the pest. The review also identifies old and new knowledge gaps, highlighting research and development needs, and thus provides a contribution to redesigning a robust management strategy.

## 2. Biology and Ecology of S. cancellata

Locusts are grasshoppers in the family Acrididae that have a phenotypic plasticity known as phase polyphenism in that they behave as solitarious individuals at low densities but shift to a completely different behavior and morphology when at high density [5]. At low density, locusts are *solitarious*: they avoid each other and are generally cryptic green or brown. Crowded locusts are *gregarious*: they tend to have darker or aposematic coloration and their attraction to each other leads to marching bands of nymphs and migrating swarms of adults. The genus *Schistocerca* (Acrididae, Cyrtacanthacridinae) includes about 50 species, and at least four are considered highly swarming locusts: the desert locust (*S. gregaria*); the Central American locust (*S. piceifrons*); *S. interrita*, which had several major outbreaks in
Perú; and the South American Locust (S. cancellata) [6]. *Schistocerca cancellata* is similar to the three others in coloration and body size and can be differentiated by the male cercus, with the lower lobe larger than the upper lobe; by the subgenital plate of males with a notch almost parallel sides; and by the presence of a waxy secretion on the abdomen on mature adults [7,8].

## 2.1. *Phenotypic Plasticity Traits in S. cancellata*

### 2.1.1. Nymphs

**Morphology.** In the laboratory, the nymphal body size is affected by rearing density, and there is a sex-dependent pattern. Crowded final instar female nymphs are smaller than those reared isolated, while crowded male nymphs are larger, resulting in a less pronounced body size difference between crowded males and females [9] (Table 1). In the field, sexual dimorphism has not been thoroughly studied, though recent observations in Argentina (Piou et al., unpublished data) suggest that female nymphs are larger than males. In both sexes, isolated nymphs have higher density hair on the outer surface of the hind femur, suggesting that this species might use the same mechanism as the desert locust (stimulation of these hairs from bumping into other locusts [10] to detect changes in density) [9].

**Coloration.** Solitarious nymphs are generally green, with variations from light brown to light green, and small black dots over part or all of the body (e.g., hind femur) (Table 1, Figure 1). At high density, gregarious nymphs exhibit the contrasting pattern of striking yellow, red, or reddish orange and black though some bright yellow nymphs are seen [9] (Figure 1). Between the two extreme colorations typical of the solitarious and gregarious phases, transitional colorations are commonly observed, corresponding to the "transiens" phase [9]. In the laboratory, recently hatched nymphs are generally light green with or without darker areas, and with nymphs kept in isolation, the greenish or light brown coloration is maintained [9]. With nymphs kept at high density, the black pattern is evident within a few hours of hatching. The first two instars are rather pale with the orange-red color of the head and the bright black and yellow becoming more evident after the third instar. However, nymphs crowded for several hours and then isolated initially developed coloration typical of crowding but lost their coloration after the first molt.

**Behavior.** In its natural habitat, after hatching, solitarious SAL nymphs disperse in the vegetation and develop in isolation, hiding in the plants protected by their cryptic coloration [11]. After hatching, gregarious nymphs are much more active and form dense groups that eventually constitute bands of marching nymphs [8]. Gregarious nymphs display 'hectic' behavior, with higher individual irritability and more ingestion of food [11]. When food is available and the temperature is high enough, nymphs feed almost continuously [12]. The gregarious bands display circadian cycles of activities: (1) going down their roosting plants and basking in the early morning; (2) basking in groups in the ground until body temperature is high enough to initiate marching; (3) marching and eventually jumping by late morning; (4) when the ground temperature is too high, hoppers climb on plants, jump, or hide in the shade from midday to mid-afternoon; (5) they resume marching in the late afternoon; and (6) they climb up trees or bushes at sunset to find high roosting plants to spend the night [12]. The marching bands can cover several hundreds of meters per day and display a large front of high density in a similar way as desert locust [12]. In the laboratory, Pocco et al. [9] demonstrated that crowded final instar nymphs are more active and more attracted to conspecifics than those reared in isolation, regardless of sex.
## Schistocerca cancellata

<figure><img src="image_92.png" /><figcaption>**Figure 1.** *Schistocerca cancellata*, (A,B) final instar nymphs and (C,D) adults. (A,C) solitarious phase (isolated locusts in laboratory); (B,D) gregarious phase (B) crowded nymph in laboratory; (D) adult female in nature). (Photographs: M. Pocco).</figcaption></figure>

### 2.1.2. Adults

**Coloration.** SAL adults (Figure 1) are in general brownish, with a contrasting pattern of stripes in the pronotum, two brown dorsal bands delimited by dark brown lines, and a wide median longitudinal light-brown stripe extending from the fastigium along the tegmina. In the lateral lobes of the pronotum, there is a pattern of light brown, brown, and whitish stripes. The tegmina exhibit a pattern of dark maculae, and the hind wings are hyaline to light yellowish, with brownish veins in the remigium area. On the hind femur, there is a white stripe in the outer face, below the pinnae, and the hind tibia is purple on its dorsal face, with white spines and black tips. The coloration of SAL adults is quite similar in solitarious and gregarious individuals, although slight differences can be seen in the pattern of stripes in the pronotum. In gregarious mature adults, the contrasting coloration of stripes in pronotum is faintly evident, turning homogenously pale yellow, keeping the narrow dark brown stripes. In natural conditions, immature gregarious adults have a reddish coloration, turning to a general pale-yellow color as they mature [11].

**Morphology.** SAL is a large acridid: female adults range from 39 to 66 mm in length and males range from 28 to 49 mm [13]. In the laboratory, crowded male adults are significantly larger than isolated males (mean value of body length for crowded males: 58.1 mm and isolated males: 52.7 mm). The size of the female adults does not differ as much between the two density conditions (mean value of body length for crowded females: 67.2 mm and isolated females: 66.0 mm), although the head is significantly wider and the pronotum slightly larger in crowded females than in isolated ones [9].

The classic measures of phase change seen in *Schistocerca gregaria* [14] are the morphometric ratios F/C (where F is the length of the hind femur and C is the maximum width of the head) and E/F (where E is the length of the fore wing over the length of the hind femur (F)). Pocco et al. [9] found that the F/C ratio is significantly lower in crowded than in isolated adults, indicating that the head width is wider in crowded individuals, which
could be related to the voracious feeding capability of the gregarious locusts [15]. However,
there was no significant difference in the E/F ratio between isolated and crowded adults.

## 2.2. Habitats and Feeding Preferences

As with most locusts [4,16,17], SAL outbreaks tend to originate in arid regions, which are marked by low levels of human presence, so that early outbreaks are mostly detected by government surveys. Typical habitat in the central permanent gregarization zone of Catamarca and La Rioja (Figure 2: Outbreak Area) is largely desert and semi-desert, where mountain ranges alternate with basins containing inland drainage, saltpans, extensive silt deposits, and sand dunes [18]. The dominant vegetation is wooded steppe of *Prosopis* and *Larrea* bushes, with tufts of *Sporobolus* and *Panicum* grasses or with *Atriplex* or *Suaeda* where the soil is salty [19]. The mosaic of vegetation types associated with these soil types was considered by Köhler [11,18] to be of particular importance to locusts and was termed "Acridoflora". "Acridoflora" consists mainly of annuals that spring up following rain: (Poaceae: *Bouteloua aristidoides* (Kunth), *Aristida murina* Cav., *Trichloris* sp.; Amaranthaceae: *Gomphrena martiana* Gillies; Nyctaginaceae: *Boerhavia spicata* Choisy; Portulacaceae: *Portulaca* sp.; *Heliotropium* sp.). Indeed, SAL is highly polyphagous and eats plants from many different families. The reported list for Argentina includes nearly every cultivated plant from pasture grass and cereal crops such as maize and sorghum to soybeans, peanuts, and citrus [17]. In Bolivia, the identified host range of SAL includes *Amaranthus retuflenxus*, *Sida cordifolia*, *Cassia tora*, *Nicandra physaloides*, *Panicum maximum*, *Alternanthera* sp., *Zea mays*, *Croton argenteos* L., *Cynodon dactylon*, *Schinus* sp., *Sorghum sudanense*, *Braquiaria plantaginea*, *Echinochloa colonum*, and *Digitaria sachariflora* [20,21].

Studies on field populations have revealed that SAL marching bands are carbohydrate (not protein) hungry and that access to carbohydrates is likely important for supporting long-distance migration. Teams of researchers and practitioners set artificial diets in front of oncoming bands at eight unique sites across Argentina, Bolivia, and Paraguay and found that individuals stopped and ate most often at dishes high in carbohydrates [Cease et al. unpublished data]. In the Paraguay study [22], juveniles collected from a marching band and fed artificial diets differing in a protein-carbohydrate (p:c) ratio in the laboratory had increased survival as diets became more carbohydrate biased. When fed single diets of plants that they were seen eating in the field, locusts only gained weight on the plant with the lowest p:c ratio. The plants were from the genera *Paspalum* sp., *Celtis* sp., *Mikania* sp., *Grabowskia* sp., *Prosopis* sp., and *Digitaria* sp. and one from the subfamily Celastraceae. Most of these local plants had a p:c higher than optimal, suggesting that marching locusts must actively seek out carbohydrates, or their growth and survival would be carbohydrate limited.

In contrast to the general pattern of herbivores being nitrogen or protein limited [23], SAL's carbohydrate demand and preference are similar to what has been shown for field populations of other locust species [16]. Land management practices, such as heavy livestock grazing, that deplete soil nitrogen promote outbreaks of these species by lowering plant p:c ratios [24-26]. Lower p:c diets (high carbohydrate) are likely required to support migration. Locusts rely on lipids to fuel long-distance adult flight [5,27], and while the energetic costs of locust marching have not been measured, terrestrial locomotion increases metabolic rates by 2-12-fold above resting for other insects [28,29]. In the Talal et al. [22] study, for both artificial and plant diets, SAL body lipid content increased with decreasing dietary p:c. similar to that shown for migratory locusts (*Locusta migratoria*) eating low p:c meals [30,31]. Both migratory locusts and SAL elevate CO₂ production following a low p:c meal. Talal et al. [22] showed that this is likely due to de novo lipid synthesis, as indicated by a respiratory exchange ratio above 1 (ratio of CO₂ produced in metabolism to O₂ used). Further studies on *Oedaleus* spp. in Senegal and China corroborate the hypothesis that high carbohydrate diets support locust migration [32,33].
<figure><img src="image_93.png" /><figcaption>**Figure 2.** South American locust distribution map. Adapted from de Wysiecki and Lange, 2005.</figcaption></figure>

## 2.3. *Population Dynamics*

### 2.3.1. Life Cycle Parameters

In natural conditions, gregarious *S. cancellata* has five nymphal instars and the total period of nymphal development is about 36–57 days [17]. Under laboratory conditions, six nymphal instars are recorded in both isolated and crowded conditions [9]. At constant 30 °C, nymphal development is 47.9 days for isolated nymphs but only 35.6 days for crowded nymphs (Table 1). As in other locusts, the number of eye stripes for both isolated and crowded nymphs is the same as the number of instars from hatching to adult [9].

Typically, there are two generations (spring and summer) per year. Adults from the second generation spend the dry season in a reproductive diapause until rains fall in spring [2,8]. During the summer non-diapause period, adults live for at least 6 weeks with maturation and laying occurring from the third week onwards when rain has fallen. During the diapause period, overwintering adults can live for up to 6–8 months from the beginning of the diapause period in autumn until the rains of the following spring [2,17]. Gregarious females lay eggs in dense groups on bare ground, laying up to six egg-pods over their lifetime, usually with 60–120 eggs per pod [17]. Egg development is continuous, and the incubation period in Argentina varies from 50–61 days for eggs laid in early spring when it is cool to 15–20 days for eggs laid in late spring or summer [2,19,34]. In Bolivia, laboratory studies found that the period from egg-laying to adult emergence of SAL in the
gregarious phase at 25 °C (normal conditions of Santa Cruz, Bolivia) is 85–95 days, with the adults living an average of a further 114 days [20].

<table><caption>**Table 1.** Summary of the main differences between solitarious and gregarious phases for the nymphal and adult stages of *Schistocerca cancellata*.</caption><thead><tr><th colspan="7">Schistocerca cancellata</th></tr><tr><th rowspan="2">Traits</th><th colspan="3">Solitarious Phase</th><th colspan="2">Gregarious Phase</th><th rowspan="2">References</th></tr><tr><th>Nymphs</th><th>Adults</th><th>Nymphs</th><th>Adults</th></tr></thead><tbody><tr><td>Size</td><td>Final instar: males smaller; females larger</td><td>Males smaller; females similar size, narrower head</td><td>Final instar: males larger; females smaller</td><td>Males larger; females similar size, wider head</td><td></td><td>[9]</td></tr><tr><td>Coloration</td><td>Green, varying from light brown to light green, with small black dots</td><td>General brownish, contrasting pattern of stripes in pronotum</td><td>Pattern of striking yellow, red, or reddish orange & black</td><td>General brownish; pattern of stripes in pronotum<br>faintly evident<br>In nature: reddish (immature)<br>pale yellow (mature)</td><td></td><td>[9,11]</td></tr><tr><td>Behavior</td><td>Sedentary, disperse in the vegetation and develop in isolation</td><td>Sedentary, disperse in the vegetation and develop in isolation</td><td>Active; dense groups (marching bands)</td><td>Active; dense groups (swarms)</td><td></td><td>[9,11]</td></tr><tr><td>Femur hairs (%)</td><td>Higher</td><td></td><td>Lower</td><td></td><td></td><td>[9]</td></tr><tr><td>F/C ratio</td><td></td><td>Higher</td><td></td><td>Lower</td><td></td><td>[9]</td></tr><tr><td>Life cycle: N° instars</td><td>6 (in lab.)</td><td></td><td>6 (in lab.); 5 (in nature)</td><td></td><td></td><td>[9,17]</td></tr><tr><td>Mean duration of stage</td><td>47.9 days</td><td>87 days</td><td>35.6 days</td><td>58 days</td><td></td><td>[9,34]</td></tr></tbody></table>

In the laboratory, at constant 30 °C, the mean duration of the adult stage is about 87 days for isolated individuals compared with the significantly shorter 58 days for crowded adults [9] (Table 1). In crowded conditions, adults take about two to three weeks after molting before mating. Sanchez et al. [34] recorded 73 eggs per pod (mean value) and a mean fecundity of 161 eggs/female in crowded locusts. Based on observations made in the laboratory, the number of hatchlings per pod was higher in the crowded than in the isolated locusts (mean 85.1 for crowded; 51.8 for isolated). In the laboratory, egg incubation takes about 15–20 days.

Similar to many other locust species [4], SAL demonstrates dramatic swings in both its abundance and its occupied geographic range [3]. The population dynamics of this species are characterized as having both recession and outbreak areas sensu Uvarov [35]. In most years, there are low to moderate populations in a localized area in northwest Argentina (Figure 2) and periodic treatment of the bands and swarms that appeared in this area [2,18] helped to prevent plagues for more than 60 years [1–3]. However, SAL shows a pattern of population fluctuation that fits into Berryman's [36] sustained irruption type of population dynamics, where a period of unusually favorable conditions [36,37] can lead to rapid population increases. Once populations reach high densities, even less than ideal conditions are sufficient to maintain the population, resulting in a stable equilibrium at high densities that can result in plagues lasting many years. In the past, dense bands and swarms spread to cover more than 1.5 million km² in Argentina, Bolivia, Paraguay, Brazil, and Uruguay [1], and the current upsurge has expanded to cover a significant
proportion of this maximum area [3,20] (Figure 2). The stable equilibrium at high densities has profound effects on locust management efforts: if locust populations reach high levels, even substantial control efforts are often unable to reduce a population and end a plague unless aided by unfavorable climatic conditions [38].

Different factors influencing or determining insect outbreaks have been hypothesized including physiological [39] or top-down mechanisms [40]. Unfortunately, limited research on SAL has been carried out on the mechanisms underlying outbreaks. However, joining some known features of SAL and environmental conditions concomitant to recession and outbreak periods, a plausible hypothesis can be stated as follows.

### 2.3.2. The Third Generation Hypothesis

As mentioned earlier, under normal meteorological conditions, SAL has two generations [1,9]. As with the red locust *Nomadacris septemfasciata* (Audinet-Serville, 1883) in Africa and the spur throated locust *Austracris guttulosa* (Walker, 1870) in Australia [41], SAL has an adult diapause during the winter dry season. Oviposition only occurs between September and March and, then, only if rain has fallen to produce green vegetation [2]. During the June to August winter period, rainfall is very low in northwest Argentina, with an average of <7 mm per month in Catamarca and La Rioja and <15 mm per month in adjacent provinces. Rainfall during summer (December–February) is much higher, averaging > 60–90 mm/month in Catamarca and La Rioja and >100 mm/month elsewhere. Adult diapause ends around August, but adults remain immature until the first rains of the spring, which is often in October or even November. Oviposition begins a week or so after the rains, leading to the normal two (spring and summer) generations during the late spring/summer rainy period.

Importantly, rain sometimes falls during the June–September period, providing green vegetation for post-diapause adults to begin maturation and laying in September. Using a developmental model based on Barrera and Turk [42], Hunter and Cosenzo [2] found that after winter/early spring rain, three generations per year were possible: (1) early spring to early summer, (2) early summer to late summer, and (3) late summer+. In this scenario, the second-generation adults mature in late summer, just before the late March initiation of diapause, enabling a third (autumn) generation. However, only a few locations in Catamarca and La Rioja provinces were found to be hot enough to allow for these three generations [2]. Rainfall is low in Catamarca and La Rioja during winter, and for the 80 years after accurate records began for both provinces, there was significant rain (>25 mm) during any of the months between June and September for 20% of the years for Catamarca and 16% for La Rioja. Interestingly, in 1943, during the winter before the gregarization leading to the last plague of the twentieth century (1944–1954), rain fell during July in Catamarca (27.6 mm) and La Rioja (31.9 mm). Running of the model revealed that the bands of young nymphs seen during January 1944 [1] would have been nymphs of the second generation. These nymphs would have reached the adult stage by March and laid their eggs, allowing a third generation to produce the substantial number of swarms seen during winter 1944. To confirm the hypothesis of three generations and its possible importance in leading to the current upsurge, further studies should be conducted on how the higher temperatures and alterations in rainfall resulting from climate change might lead to an expanded area favorable for a third generation beyond the current Catamarca and La Rioja outbreak area. In particular, an analysis of the conditions throughout northern Argentina, Bolivia, and Paraguay that led to the resurgence of swarms in 2015 is needed.

### 2.4. *Natural Enemies and Biological Control*

SAL has many natural enemies or antagonists including predators, parasitoids, and pathogens. Numerous invertebrates, from nematodes to insects and spiders, and vertebrates, particularly insectivorous or opportunistic birds, are known to consume either embryonic or postembryonic stages of SAL [43]. Daguerre [44,45] found that *Sarcophaga* spp. parasitoid flies inflicted the highest levels of mortality in Argentina. In Bolivia, López
and Copa Bazán [20] found that natural enemies included lizards, hawks, cuckoos, spiders, and different insects such as reduvids, carabids, ants, wasps, predatory mites, and the entomopathogenic fungus *Beauveria* sp. [46]. Although such predators or parasitoids may reduce locust populations or contribute to earlier collapses [47], their actual impact has not been studied for SAL. As for other locusts [48], heavy, widespread chemical campaigns against locusts may also have had serious negative effects on natural enemies but is so far understudied.

Pathogens are the only natural enemies that have so far received some attention as possible biocontrol agents of SAL. In fact, SAL in North Argentina was among the first targets (along with Australia) of using natural enemies for control: Bruner introduced a fungus from South Africa in 1898, and the microbiologist d'Hérelle [49] applied the bacterium *Coccobacillus acridiorum*, which he had isolated from diseased locusts in Mexico. Although some good results were reported, there was little success overall [50]. Under laboratory conditions, SAL proved to be susceptible to the amoeba *Malameba locustae* and the *Entomopox* virus of *Melanoplus sanguinipes* (MsEPV) [51]. However, both pathogens are unlikely to be useful. *Malameba locustae* cysts lose viability under storage, and the MsEPV is not a native natural enemy. Species of Eugregarines (Apicomplexa) are also known to occur in SAL populations [43,52] but normally do not seem to harm the host. Among the fungi, there are old records of *Sporotrichum paranenese*, *Fusarium* sp., and *Aspergillus parasiticus* [43] and new isolates of *Beauveria bassiana* and *Cordyceps locustiphila* that are under study as possible biocontrol agents [53,54]. In China, a species of *Aspergillus* has shown high virulence against locusts [55]. The naturalized microsporidium *Paranosema locustae*, which appears to continue causing epizootics and expanding its host range in grasshopper communities of the Pampas and Patagonia [56], turned out to be not infective for crowded gregarious nymphs of SAL in the laboratory as opposed to relatively uncrowded gregarious nymphs of earlier studies [57]. It remains to be determined if *P. locustae* may prevent phase transformation when it is administered to solitary nymphs of *S. cancellata* as observed in the Migratory locust *Locusta migratoria* [58,59].

# 3. Management of SAL: An Historical Perspective

## 3.1. *Early Management Efforts against SAL Plagues*

The first records of locusts in Argentina date from the 1500s, with swarms damaging crops of cassava (*Manihot esculenta*) [1]. While there were reports of locusts in the following centuries, including plagues in Córdoba and Santa Fe provinces during 1833–1840 and 1844–1849 [50], detailed records of the extent of locust infestations began in the late 1800s with the continuous record of the size of locust infestations from 1897–1968 as summarized by Gastón [1]. These detailed records were a response to an increasing realization that SAL caused a great deal of damage to Argentinian agriculture, even though early damage estimates were vague and indirect. The problem led to the gradual development of specific pest control policies, characterized by a strong interventionist profile. These policies underscore SAL's seriousness and importance for the national economy [60] and led the Argentine government to create an agency to implement the first locust control campaigns. This mission was assigned in 1891 to the National Commission for Locust Extinction (CNEL) [61], which having “extinction” in its name, was based on the idea that the problem could be solved for good by a short-term campaign. In 1898, the control of SAL was declared mandatory by law (https://www.argentina.gob.ar/normativa/nacional/ley-37 08-284864 accessed on 17 December 2021) and the first agricultural pest in which control was declared compulsory in Argentina. SAL was a problem of such an impact, and the difficulties experienced were so deep that the government decided in 1912 to transform this low-level and temporary office into a permanent department, named the General Directorate of Agricultural Defense, which then turned into the National Direction for Agricultural Defense and Plant Health [61]. The NDADPH was first appointed with the task of controlling SAL attacks on crops, pastures, and trees in public places, but their role widened to include all kinds of pests as agriculture advanced throughout the country.
In those first years, there was little understanding of the true nature of the population dynamics of SAL, and this contributed to a lack of effectiveness in its management. The locust problem was widespread such that, between the first detailed records in 1897 until the late 1930s, more than half of the years had SAL invasions in >20% of the whole territory of Argentina, with a maximum invasion of 57% of Argentina in 1932 [1]. There were only five years when <5% of Argentina was invaded, leading to the idea that swarms were a permanent condition of this species [18,45]. All recorded expeditions were organized during periods of large-scale locust invasions, 1908, 1917, and 1934–1936 [18,62], so studies of the gregarious swarming phase predominated. While the occurrence of a solitarious phase consistent with Uvarov's phase theory [63] began to be considered by the late 1930s, its presence was initially not generally recognized [18,62].

There were similar early misunderstandings concerning the source of invasions. In 1880 and 1892, there were observations leading to the hypothesis that invasions came from the Great Chaco in Argentina and Bolivia [63]. The belief that the "permanent region" was in northern Argentina and especially southeast Bolivia was built on the expeditions that Enrique Lynch Arribálzaga and Carlos A. Lizer y Trelles carried out in Jujuy, the northernmost province of Argentina during 1908 and 1917, respectively, coinciding with periods of very expanded invasions [1,62]. However, even though these source area ideas were erroneous, what was recognized very early was the importance of migration. D'Hérelle [49] reported widespread swarm movements: from the north towards the south in winter months and from the center of Argentina towards the north at the end of the summer months, effectively a migratory circuit later found in other locusts such as the desert locust [64–67] and Australian plague locust [68]. He mentioned that migrations were at night during the summer but only seen during the day in winter. The importance of long-distance migrations would later be further elaborated for swarm movements in the 1930s to 1950s [17] and again during the recent 2015–2021 upsurge.

Before the first systematic surveys, it was believed that SAL could reproduce anywhere and therefore every region was suspected to be a potential source of new invasions. Initially, it was also thought that SAL persisted in winter refuges, based on the frequent observations that swarms came southward to agricultural areas from northern regions. To try to locate these refuges, the Central Commission for Locust Research was established in 1933 and conducted expeditions lasting 3–4 months that explored the north and the west. These expeditions were led by three entomologists and served not only for describing dispersion paths, behavior, meteorological factors affecting swarm dispersion, feeding preferences, and natural enemies but also to test different inorganic insecticides and application equipment [69]. These expeditions were unable to find overwintering swarms, leading to the rejection of the winter refuge hypothesis [18].

During this period, there were several hypotheses concerning the wide fluctuation in the extent of the invaded area including correlations with sunspot numbers [63]. This idea may have derived from the proposition by Archibald [70] that periodical invasions of *Locusta migratoria migratoria* (L.) into the temperate zone are apparently regulated by certain meteorological conditions, which in turn seem correlated with variations in sunspots. There were similar hypotheses for the Rocky Mountain Locust ((*Melanoplus spretus* (Walsh, 1866)) in North America [71]; for *Locusta migratoria migratorioides* (Reiche & Fairmaire), still referred to as *Locusta migratoria manilensis* (Meyen) in eastern China [72,73]; and for the desert locust, *S. gregaria* [73].

The initial misunderstandings about the population dynamics of SAL combined with the widespread nature of swarming populations and an inability to locate source areas meant that management efforts during the first three decades of the twentieth century were "primitive", to use the terminology of Lizer and Trelles [62]. The locust commissions were initially established with the appointed task of exploring territories affected by swarms or bands and of recording habitat characteristics and crops affected. Control of the swarms was generally limited to treating adults settled on trees or fences. Most control measures were aimed at containing nymphal bands, a "defensive" strategy [1] aimed at preventing
bands from invading crops. The strategy was to interrupt band marching with perimetral metal barriers fixed to the ground. “Funnels” or collectors used the organized and uniform movement of the gregarized bands to direct the bands to deep trenches, where the millions of nymphs that accumulated were torched with flame throwers. Other methods included plowing to destroy the eggs, and allegedly, the adults as they lay. Hand or mechanical picking was promoted with economic compensation per bag of locusts collected. There are anecdotal records of turkeys and chickens released in the vineyards and orchards as a complementary control measure [60]. Additionally, setting fire to pastures and fallow fields was sometimes practiced but abandoned because of the low efficacy and risk of spread of uncontrolled fires [74].

During one of the long-lasting plagues in the 1920s, mechanical collection of locusts reached industrial proportions. In eastern Argentina, five hundred metal fences were installed, totaling 50 km of barriers to herd the nymphs towards corrals where locusts were sun-dried and then sold as fertilizer. The production of locust powder reached 95 million tonnes, but this practice was abandoned due to high costs [60].

## 3.2. *The Offensive Management Period*

The Locust Control Service was established in 1945 and was characterized by the heavy use of insecticides applied with blowers mounted on trucks, backpacks, airplanes, and helicopters either hired or specifically assigned to the aerial Aviation Department of the Agricultural Ministry [1]. This move was enabled by improvements in control techniques including more effective chemical pesticides (e.g., DDT) and aerial campaigns as has started in Africa [75]. While the environmental impacts had yet to be uncovered, these technical advancements allowed for the rapid treatment of large areas through offensive operations [1]. The Locust Control Service treated locusts as the upsurge increased after locusts invaded from Paraguay and Brazil in early 1945, and the infested area then expanded to 35° South by 1946–1947 [43]. In 1948, the large scale of the plague led to the formation of international cooperation between countries affected by SAL: Brazil, Uruguay, Paraguay, Bolivia, and Argentina. By 1952–1954, there was an extensive control campaign involving 12,000 tons of pesticide [17,43], and by early 1955, few locusts remained. While it was uncertain whether this decline was solely a result of the intensive treatment programs or in combination with unfavorable environmental conditions, by 1956, no gregarious locusts were detected, and this great plague period came to an end [1,3,43].

## 3.3. *Advances That Formed the Basis for Preventive Management*

The 1944–1954 plague was monitored closely not only regarding the efficiency of methods of control but also concerning the biology and population dynamics of SAL [18]. These observations led to substantial breakthroughs and to a new strategy for SAL: preventive management. The aim of preventive management was to have teams equipped for surveillance and control operations so that any gregarizing groups of nymphs or adults found early in an outbreak could be treated as a way of preventing an upsurge.

The first breakthrough was applying the phase theory of Uvarov [63] to SAL, indicating that SAL exhibited phenotypic plasticity by switching between solitarious (non-outbreak) and gregarious (outbreak) phases. The commonly encountered gregarious swarms and the scattered solitarious locusts found in northwestern drylands had been thought to be a different species [18,62]. Detailed observations in the late 1930s to early 1940s showed that they were different density-dependent phenotypes of the same species [18]. Rearing experiments demonstrated phase transformation when locusts were crowded [76]. Subsequent careful field observations revealed that the scattered locusts present during the population decline of the late 1930s started to change their behavior as numbers increased during the 1943–1944 season. Together, these advancements demonstrated that the isolated forms seen in northwest Argentina and the gregarious swarming forms of SAL were the same species [18].
The second breakthrough was that phase change (from solitarious to gregarious SAL) occurred in specific arid areas of La Rioja and Catamarca provinces [18]. This led to the realization that plagues occurred in the past because of a failure to control these newly gregarized nymphs and the resulting swarms that followed, leading to enormous costs from damage to agricultural production. The identification of localized outbreak areas meant that early targeted treatment might prevent plagues, as had been proposed by Uvarov [35] for other locusts with outbreak areas. Thus, regular surveillance for signs of gregarizing locusts and treatment of any bands or swarms found within the 100,000 km² outbreak area formed the basis of the preventive management program for SAL [1,18]. SAL invasions reaching Bolivia, Paraguay, Brazil, and Uruguay were correlated with swarms originating in the Argentinian outbreak area including the presence of SAL in Bolivia in 1947, 1949 [77,78] and in the recent upsurge during 2017 and 2020, where they were reported in the Bolivian Chaco region, Santa Cruz, Tarija, and Chuquisaca [79,80]. In Brazil, recorded invasions occurred in its southeast region in 1906, 1932–1933, and 1946–1948 [81], while in Uruguay, there were nine invasions that caused significant damage between 1890 and 1948 [82].

The third breakthrough was recognition that SAL had a migratory circuit. Locusts originating in the La Rioja and Catamarca regions initially as small bands and then adult groups transitioned into large migrating swarms that headed towards northern Argentina with converging winds [18]. These northward dispersions were called "concentration flights" [62], with a proposed hypothesis that summer/autumn wind currents and topography contributed to making swarms converge during this northward dispersion [11,18]. The swarms reached northern Argentina and even Bolivia and Paraguay at times. During the winter, the swarms returned south, and in the first waves of swarms, adults were reddish and tended to fly long distances following the prevailing northerly winds. As the southerly migratory movement continued, the locusts mature irregularly in pulses and disperse into ever smaller masses and begin the spring and summer breeding period.

The final breakthrough to support preventative management was uncovering the relationship between precipitation patterns and multiple SAL generations in one year. It had long been realized that SAL adults remained immature over winter, and it was thought that they matured and laid with warm weather of spring, with asynchronous and sporadic laying and hatching continuing from October to March as part of a single generation per year. However, Köhler [11,18] observed that the transition from solitarious to transiens to gregarious occurred over a period of two generations in a season. The existence of a second generation was further confirmed in February 1945, when new swarms invaded northern Argentina from Paraguay [1]. Due to a drought in the area, there was no maturation and laying despite the hot weather that was thought to lead to maturation and laying, but there was then heavy rain, which was followed by widespread oviposition and an "extraordinary quantity of nymphs" [1]. This meant not only that there was more than one generation per year [1,18] but also that rainfall was important in allowing maturation and laying, a finding reinforced by Hunter and Cosenzo [2]. Therefore, during rainy periods, adults matured rapidly and laid, allowing for more than one generation in a season, and since a female could lay 100 eggs or more, a substantial population increase was possible.

### 3.4. *The Preventive Management Program*

Uvarov [35] had suggested preventive management be implemented for locusts with outbreak areas. Such a program had begun to be implemented in the outbreak areas of the red locust, *N. septemfaciata* in Africa [83], and so, a similar preventive program was envisaged for the outbreak areas of SAL [1]. In 1954, the Service to Police and Prevent Locusts was established, which consisted of permanent scouting commissions with the aim of locating and controlling locust infestations [1,43]. At first, these commissions were deployed in an area of 300,000 Km², covering Catamarca, La Rioja, and adjacent provinces of northwest Argentina. Surveillance followed pre-established routes and occurred throughout the spring and summer generations. Teams were equipped for control operations so
that any gregarizing groups of nymphs or adults found could be treated [1]. Treatments were carried out usually by ground equipment such as backpack sprayers or sprayers attached to Unimogs [2] though some years had slightly larger outbreaks requiring the use of aircraft [1,2,60]. With the information gathered in the first 14 years of implementation of the preventive management strategy, it became clear that there was an area of approximately 100,000 Km² where the build-up of SAL population was permanent, particularly during the summer [1]. The intensity of the scouting and control process was adjusted to concentrate more on this 100,000 Km² area, mainly in Catamarca and La Rioja [1,2].

Following the implementation of the preventive management program in the 1950s and 1960s, outbreaks of SAL were small, with treatments on the order of a few thousand hectares or less, reaching 10,000–30,000 ha at times [1,2], much less than the hundreds of thousands of hectares requiring treatment during plagues. The resulting long recession was a complete contrast to the first half of the twentieth century when locusts were in recession for only 10 of the 55 years from 1900 and 1954 [1,2]. However, the very success of the program in containing outbreaks before they could expand to agricultural areas meant that there was little impetus for studies to increase the understanding of SAL population dynamics. Research was limited to studies by Barrera and Turk [42] on aspects of SAL biology including development rates and by Waloff and Pedgley [19], who reviewed the biology of SAL in comparison with the South African desert locust, including mention of an Argentina–Bolivia/Paraguay migratory circuit for SAL. However, the successful preventive management strategy in Argentina caught the attention of locust workers in Australia and visits to Argentina led to a detailed analysis of the plague and contrasting preventive management recession periods. Hunter and Cosenzo [2] found that, when rain fell between June and September in one or both of Catamarca/La Rioja, three generations were possible in a season, resulting in a larger than normal treatment program, which turned out to be critical in preventing the population to further upsurge to plague proportions.

In a similar way, the very success of the preventive management program led to a gradual decline in finances and resources due to the “vicious cycle” of successful prevention, leading to loss of the memory of how damaging plagues had been and gradual erosion of management effectiveness [84]. During the 1960s, there were field teams for locust surveillance and control with substantial amounts of ground equipment and access to helicopters and airplanes for treatments of larger infestations [1,60]. In 1970, Daguerre [85] warned about not enough effort being put into controlling reproduction foci before SAL reaches the reproductive stage. By the late 1980s, budget constraints led to a reduction in staff and equipment such that Hunter and Cosenzo [2] reported that, during the 1987–88 season, there were few surveys in spring and no band treatments in summer, leading to an unusually large treatment campaign against adults that included the use of aircraft. An international workshop held in February 2020 [86] confirmed the importance of a gradual reduction in financial and political support as the recession progressed, which reduced the effectiveness of the preventive management system. Participants identified the lack of a budget and a strong and continuous state policy as major explanations of the current crisis: surveillance activities became increasingly restricted in location and timing so that, when conditions favorable for an outbreak occurred, the initial outbreak populations were not located and controlled. These reductions in resources are similar to the ‘vicious governance cycle’ described for the desert locust [87–89]: long recessions induce a loss of interest, coordination, and institutional memory such that the human, social, material, and financial infrastructure accumulated during and immediately following plague periods, slowly decreases in the face of other political priorities.

The result was a dramatic reduction in the amount of locust survey and control [3,90–92]. Surveys were largely limited to Catamarca and La Rioja, with a dramatic reduction in access to the permanent gregarization area by closure of access trails and legal difficulties of SENASA teams being allowed to enter private property (HM, unpublished). With locusts rarely being present in numbers to cause economic damage [3], there was little institutional resistance to these increasing restrictions, thus limiting the ability of field officers to effec-
tively locate and control localized gregarious infestations [86], a key requirement of any
preventive management program. Compounding these limitations was a gradual loss of
institutional knowledge and experience [86], including the loss of the detailed records of the
extent of bands and swarms and their treatment, so that the only records remaining were
those retained in Australia by the Hunter and Cosenzo [2] study. With such decreases in
knowledge and capacity to respond, it is not surprising that there was a sudden appearance
of swarms in 2015 that marked the onset of the current upsurge.

4. Management under A New Plague Period

4.1. *The Resurgence of SAL*

The new upsurge of SAL began with the sudden appearance of in north-central
Argentina during July 2015 [90,91]. In the years prior to 2015, the surveillance and control
actions focused on a small area of Argentina [3], and so at present, there is no certainty
about the geographical source of the original outbreak that triggered the subsequent
regional emergency.

Following the appearance of swarms during July 2015, a program of widespread surveys was introduced, which found a number of swarms during spring 2015 [3]. Widespread control of nymph bands was instituted during the 2015–2016 season [90]. There was a small nymphal treatment program in Argentina during late 2016, and following sightings of swarms migrating at night in northern Salta province and at Tarija in Bolivia [HM, unpublished], many swarms were seen in Bolivia during January 2017 [91]. These northward migrations had not been documented during the 60-year period of preventive management [3].

Overall, the 2015–2021 plague was characterized by periods of breeding in Argentina alternating with breeding in Bolivia/Paraguay [3]. As a result, instead of bands and swarms being mainly limited to the outbreak area, they were present in a much larger area (Figure 2: “Transition Area During Plague Periods”) [90,91] though not as large an area as sometimes occurred in the past (Figure 2: “Maximum Historical Invasion Area”) [19]. During the years of migrations north (2016–2017, 2018–2019, and 2019–2020), there were generally two generations per year: a spring generation in Argentina, followed by a summer generation in Bolivia/Paraguay [3,90–92].

While there was the widespread treatment of nymphs in Argentina whenever they
were present, treatment of swarms proved much more difficult: during 2015 and 2019,
there was little or no treatment of swarms, and during 2017, treatments were conducted
but were limited by social and governance factors [88,89]. Chemical control in horticultural
areas was very difficult because the long recession period without locusts meant that
there were few insecticides registered for use on such crops, and even for insecticides
that were registered, strict regulations further limited their use, leading to substantial
economic impacts on horticultural production [90]. When high-value fruit tree production
was threatened [90,91], swarms were controlled with the decisive participation of local
crisis committees that included the producers affected by the pest [86].

The new plague forced very fast learning and decision-making processes adapted
to conditions that were very different from those existing in the previous plague period
during 1944–1954 [60]. After 60 years, the situation changed significantly: there were
many new stakeholders [93], evolving interests and priorities of citizens, farmers, and local
decision-makers [86], huge changes in land use [94] particularly the extension of agricul-
tural land [95], and greatly increased environmental concerns associated with large scale
treatment programs using chemical pesticides [86]. The management program required
an extremely rapid increase in tools and resources, so it was not surprising, therefore, that
it took some time to facilitate the governance and oversight capable of coping with the
resurgence, including the coordination of efforts and construction of links to ensure control
was effective [86].
## 4.2. Re-Establishing a Sustained SAL Preventive Management Program

As stated by a participant to the 2020 workshop on SAL governance [86]: "the key to work with locusts in the long term is to go back to preventive management (...) so we don't have another crisis ... We need preventive management, not reactive and palliative". An effective preventive strategy should be the way to manage locusts [38], but it requires first getting out of the crisis and building back a preventive system that includes international best practices.

As part of adapting SAL management to the twenty-first century, some important improvements have been made: there have been substantial improvements in the overall organization of SAL management in that collaborations between State agencies in charge of locust management, the provinces, and producers have been strongly reinforced since 2015 [84]. This improvement has mostly relied on personal commitment, "good interpersonal relationships" that emerged in the context of emergency protocols implementation and crisis committees. To maintain this commitment and improvements beyond individuals and during recession, interactions and collaboration arenas need to be institutionalized and maintained as part of a preventive management program.

To ensure the successful implementation of a new preventive management system, there also needs to be improved efficiency of data collection and analysis. In 2020, a locust alert system that notified farmers, beekeepers, researchers, and members of government about the advance of the pest was implemented. Currently, work is underway to implement this system used in Argentina throughout the region affected by SAL as it was recognized that data collection needs to be harmonized between countries to ensure that outbreaks are detected quickly and reported, so they can be controlled.

Critical to efficient preparation and planning of treatment programs is to have a better forecasting system based on an improved understanding of factors leading to outbreaks [67]. Both field and laboratory studies are needed and should utilize the latest technologies including remote sensing to accurately identify suitable locust breeding habitats and habitat conditions [96], wind analyses for migration patterns, and rates of development under different environmental conditions. Such data lead to more accurate development models that forecast the extent and timing of outbreaks so that surveys can be concentrated in areas where outbreaks are more likely. The influence of climate change on outbreaks of different locust species in the world has been debated [97], and for SAL, there needs to be an analysis of altered rainfall and temperature patterns on the location and timing of gregarization processes leading to outbreaks. However, probably, a more parsimonious explanation is that effective preventive strategies put in place for different locust species in the world in the sixties [1,83], play key roles in long recession periods. The gregarization process in SAL has been compared with that of *S. gregaria* in the laboratory [9], but there needs to be field studies such as those already conducted for *S. gregaria* [67,98–102]. A detailed analysis of ways to improve methods of treatment are required, not only an investigation of the latest chemical treatments appropriate for governments and landholders but also an integration of biological control, as has been already accomplished in Australia [103], Mexico [104], China [55], Tanzania [105], and Somalia [106] as part of complete implementation of Integrated Pest Management programs. Increasing constraints on the widespread use of chemical pesticides mean a biological alternative is essential to ensure that locusts are treated wherever they are, including in environmentally sensitive areas and where restrictions make the use of chemical pesticides difficult. To facilitate treatments in sensitive areas, the environmental sector should be more involved, including better coordination between the ministries of environment and agriculture [92].

## 5. Conclusions

The very success of SAL preventive management program led to less survey and control, but even more importantly, there was a virtual absence of research into the latest developments in locust biology and management. An update on locust biology is critical in view of climate change effects on rainfall and temperature, possibly altering the location
and intensity of initial SAL outbreaks, which might make regions outside the traditional provinces of Catamarca and La Rioja [1,2] important in the initiation of upsurges. Management of SAL has begun to implement some of the world's best practice, but many aspects need to be investigated and then implemented in ways relevant to the political and managerial system prevalent in the affected countries. The re-establishment of effective preventive management will rely on harmonizing coordination between Argentina, Bolivia, and Paraguay, but this "slow pace of regional coordination" encounters "obstacles coming from institutional instabilities" [86], including changing administrations. Only by "putting the three countries together" [86], through a regional plan, will an effective preventive management system be ensured and further be locust upsurges avoided.

**Author Contributions:** Conceptualization E.V.T., A.J.C., M.M.C., D.H.; methodology, all authors; formal analysis, all authors; writing—original draft E.V.T., M.M.C., C.E.L., M.E.P., C.P., D.H.; writing—review and editing, all authors; supervision, E.V.T., funding, A.J.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was supported in part by the Foundation for Food and Agricultural Research, grants no. 593561 to A.J.C.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** Special thanks to Michel Lecoq for the invitation to write this review and suggestions to improve the graphical abstract.

**Conflicts of Interest:** The authors declare no conflict of interest.

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Article

# New Technology for Desert Locust Control

Graham A. Matthews

Faculty of Life Sciences, Imperial College, Ascot SL5 7PY, UK; g.matthews@imperial.ac.uk

**Abstract:** Locust outbreaks usually begin in remote unpopulated areas following higher than average rainfall. The need to survey such areas has suggested that unmanned aerial vehicles (UAVs), often referred to as drones, might be a suitable means of surveying areas with suitable detection devices to survey areas and detect important locust concentrations. This would facilitate determining where sprays need to be applied at this early stage and would minimise the risk of swarms developing and migrating to feed on large areas of crops. Ideally, a drone could also spray groups of hoppers and adults at this stage. To date, tests have shown limitations in their use to apply sprays, although it has been suggested that using a fleet of drones might be possible. The use of biopesticide in these areas has the advantage of being more environmentally acceptable as the spray has no adverse impact on birds.

**Keywords:** locust; drone; unmanned aerial vehicle; early warning; preventive control; biopesticide

## 1. Introduction

Since biblical times, vast numbers of desert locusts (*Schistocerca gregaria* Forskål, 1775) have periodically increased to such an extent that the plagues cause extensive damage to major crops. Locust upsurges occur infrequently and during a recession period, international organisations have not prioritized research, nor have governments in countries subject to locust plagues maintained in-country research, due to years of under-funding, so they are not prepared for locust surveillance and the control of locust swarms when they do occur.

Over the last 60 years, the onset of a plague has been detected at an early stage, but in 2019, the early onset of locusts was following cyclones in 2018 which resulted in heavy rain in the inhospitable deserts of Arabia. This allowed locusts to breed unseen in the wet sands. Strong winds in 2019 blew the growing swarms into the Yemen where they were undetected as the country was beset with a war.

Initially, the solitary insects typically occur at low densities across a recession area, but following a period of good rainfall, the locusts thrived and soon aggregated and formed swarms, which spread both eastwards to Iran, India and Pakistan, and westwards to East Africa, with Kenya experiencing its worst outbreak in 70 years. Back in the 1950s, despite vast areas being invaded by swarms, it was possible to use aircraft to spray insecticides, including dieldrin to protect crops and eventually reduce the plague [1] (Figure 1). Dieldrin was used to kill hopper bands that crossed barrier strips and as a very low dose in very fine sprays to kill swarms of desert locust. However, due to increased concern over persistent insecticides affecting non-target species, the use of dieldrin was banned at meeting organised by FAO in 1988 [2]. Following this meeting, the FAO Pesticide Referee Group was established to advise which insecticides could be used. At the same time, CABI organised the international LUBILOSA Programme project, which led to the production of a biopesticide, based on *Metarhizium acridum*, to control locusts. This major development provides control of locusts that does not harm people or the environment [3,4]. Today, we need to bring together new technology to improve the detection of locusts in remote areas and use biopesticide to control locusts before populations build up and swarms invade extensive farming areas. Once swarms arrive in new areas, the control

**Citation:** Matthews, G.A. New Technology for Desert Locust Control. *Agronomy* 2021, *11*, 1052. https://doi.org/10.3390/agronomy11061052

Academic Editors: Michel Lecoq, Arianne Cease and Beatriz Gámiz

Received: 20 April 2021

Accepted: 21 May 2021

Published: 24 May 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

<figure><img src="image_94.png" /></figure>

**Copyright:** © 2021 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
of adult locusts is rapidly needed before crop damage occurs. Biopesticide acts slowly so insecticides that can achieve high mortality within 24 h are needed. Nevertheless, the least hazardous insecticides should be selected in terms of mammalian toxicity and environmental protection.

<figure><img src="image_95.png" /><figcaption>**Figure 1.** The number of countries in which desert locusts were detected since 1950, with fewer countries having an onset of major desert locust activity (i.e., major upsurges and plagues) since 1965. Control has been achieved sufficiently early to avoid a major plague, but in 2019/20 the locusts spread without early detection (updated from [5,6]).</figcaption></figure>

## 2. The Initial Signs of a New Upsurge

During a recession, locusts survive in small numbers as solitary insects in arid areas in sparsely populated areas from the Atlantic Ocean to Northwest India, but particularly in the Middle East. After a period of above average rainfall that provides the vegetation, the locust population in these areas can increase rapidly, which translates into spectacular hopper band movements and swarms which migrate. Using phenomenological models using gridded monthly data, Tratalos et al. [7] suggested that desert locust dynamics are influenced by endogenous factors and rainfall, and that broad patterns of locust upsurges and declines can be forecast with some degree of success using data on only these factors.

Locust monitoring has relied on ground-based surveys, which have required individual searches in areas with a history of locust activity, albeit at long and irregular intervals to notify the national locust control units and share the information with neighbouring countries and international agencies [8]. As the population increases, and desert locusts often aggregate to lay eggs, and as they are extremely sensitive to density changes, this rapidly triggers their phase transformation, resulting in their movement in swarms to new areas. The phase transition is a continuous, cumulative, and easily reversible process that can take place within a short period (from 4 h to 32 h) in the desert locust [9,10]. Studies in China have indicated the presence of an aggregation pheromone in the migratory locust, *Locusta migratoria* (Linnaeus, 1758) [11], but as Vosshall [12] discusses, it is not clear whether pheromone traps could assist in detecting the presence of locusts, or whether a chemical could be found to block the receptor to prevent aggregation. The latter may not be desirable as it would not reduce locust populations but rather disperse large numbers of locusts over even larger areas, making the control of locust concentrations nearly impossible.
3. Detecting Where the Locusts Can Be Found after a Recession Period

Satellite imagery has been used for finding and mapping emerging vegetation in the desert. Data collected by the Moderate Resolution Imaging Spectroradiometer (MODIS) on NASA's Terra Satellite and the Normalized Difference Vegetation Index (NDVI) are measures of the health and greenness of vegetation based on how much red and near-infrared light is reflected. According to Tratalos and Cheke [13], there is evidence of a positive relationship between NDVI and the presence of grasshopper populations, probably because grasshoppers were found in areas with higher rainfall. This helps to monitor and forecast the desert locust [14] by assessing whether the ecological conditions are favourable to locust survival, breeding, and gregarization, but needs to be accompanied by thorough observations on the ground for making decisions regarding control interventions against the initial locust congregations. This significantly reduces the costs and contributes towards changing the paradigm of locust control from curative to preventive [15]. According to FAO, current satellites can provide continuous estimates of rain-producing clouds and ecological conditions, such as vegetation development and soil moisture, which are important factors for monitoring desert locust habitats and forecasting locust development. Related to soil moisture, observed differences in grass abundance and size contribute to locust gregarization [16]. The temporal, spectral and spatial characteristics of the sensor instruments onboard these earth observation satellites provide a wide range of sensing capabilities [17].

In 2018, the FAO initiated trials with a long-range fixed-wing drone to examine areas where locusts could be present by mapping areas of green annual vegetation. Ideally, the drone needs a range of at least 100 km or more and should be solar powered. Searching vegetation is possible with lightweight multispectral sensors with near-infrared (NIR) and/or red-edge bands, as well as hyperspectral sensors that provide spectral separability [18]. For locust work, the drone initially needs to detect green vegetation by flying at optimal heights to obtain imagery that can be processed easily and rapidly in the field, so the team can decide where to intensify survey efforts, again with the drone, to detect locust concentrations using optical images that could warrant control [19,20]. The drones need to be easy to operate both manually and automatically, as well as be robust, affordable and simple to maintain locally in locust-affected countries. As a result of three years of trials and refinement, the dLocust drone developed by HEMAV (Figure 2) became available for use in locust-affected countries in 2020 [21]. Imagery is processed in-flight so that when dLocust completes its long-distance survey, the results are immediately available and handed over to the eLocust3 tablet used by field teams for recording and transmitting survey and control data in real time [22,23]. In this way, the team does not need to carry an additional computer to the field. The eLocust3 tablet was also used to plan the dLocust flight and operate the drone. Using drones for surveillance with appropriate detection equipment will enable larger areas to be surveyed in contrast to using ground teams which may only be able to survey limited accessible areas.

Small multi-rotor drones with propellers positioned parallel to the ground may pro-
vide a more stable flight and vertical take-off ability, but these are liable to damage from
flying locusts. At present, small drones are restricted to carry a limited quantity of spray
(only 10 kg) and have a limited endurance of around 10–15 min productivity for locust
control, due their small size and limited battery life. The drones need to be easy to control
both manually and automatically, as well as be robust, affordable and easy to maintain
locally in locust-affected countries.
<figure><img src="image_96.png" /><figcaption>**Figure 2.** Fixed wing drone for desert locust monitoring (source: FAO [24]).</figcaption></figure>

**4. Applying the Biopesticide in Remote Areas at the Initial Stage of Hopper Development**

Studies have been carried out in West Africa to establish the importance of using the biopesticide known as “Green Muscle®”, and based on the entomopathogenic fungus *Metarhizium acridum* [25,26]. The storage methods for fungi would be as dry conidia, perhaps with clay diluents, or in oils [27]. The LUBILOSA project focused on developing an oil formulation [28] suitable for ultra-low volume (ULV) application, a technique already well established for locust control. Early studies in South Africa in trials against Vth instar Brown locusts (*Locustana pardalina* Walker, 1870) used a large micro-light aircraft fitted with Micronair AU7000 atomisers to apply *Metarhizium flavoviride* isolate IMI 330189. Dry conidial powder was formulated in a paraffinic oil to apply approximately 2.0 × 10¹² conidia per hectare with volume application rates of 1.0 and 2.5 L/ha with the atomiser blades set at three angles (25, 35 and 45°). Up to 98% mortality was obtained where locusts were in open top field enclosures, with the 2.5 L/ha apparently obtaining more consistent results [29]. As pointed out by Bateman [30], the key problems for further research and development would be the logistics and supply of consistently reliable formulations for application at a large scale, and the determination of mechanisms for effective dose transfer in the field. Since the development of the mycopesticide known as “Green Guard®”, more than 100,000 ha have been treated with the FI-985 isolate of the fungus *Metarhizium anisoplae* var. *acridum*, since operational use began in Australia in 2000 [31].

At present, attempts to control locusts have been limited to using ground equipment with hand-carried spinning disc sprayers or using truck mounted equipment. Developments with ground equipment now include a ground positioning system (GPS) on truck-mounted sprayers to provide precision while applying ULV insecticide sprays along parallel tracks whilst also recording the position of the sprayer so that a record of the treatment is obtained and analysed.
The biopesticide, now marketed as Novacrid® from Elephant Vert (isolate EVCH077 of *Metarhizium acridum*), is a dry powder supplied in sachets, which is mixed with an appropriate oil before application at ULV rates of 1 L/ha and 0.5 L/ha. Oil formulations were tested in a range of commonly used spinning-disk sprayers, including the hand-held Micron Ulva-Plus and vehicle-mounted Ulva-Mast [3].

The enormous advantage of using the biopesticide for locust control is that it lacks adverse side-effects on biodiversity. In a study in Niger, Green Muscle® was sprayed operationally, using 107 g viable conidia per hectare, where the population of adult locusts, birds and vegetation greenness were previously simultaneously assessed along two transects from 12 days until 23 days after treatment [32]. Locusts started dying five days post-spray and the biopesticide reached its maximum effect one-two weeks after the spray, with 80% efficacy at day 21. After spraying, kestrels took significantly more of the larger female (75-80%) than smaller male (20-25%) locusts. This indicated that avian predation increased the impact of the biopesticide by removing more of the adult female locusts. No direct or indirect adverse side-effects were observed on non-target organisms including locust predators, such as ants and birds.

Where areas are accessible, ground equipment can spray up to 300 ha a day at a fraction of the cost and logistical effort. Similarly, aircraft can spray large areas at relatively low cost, but substantial logistics are required to support aerial operations.

Using a drone at present requires a trained operator, transportation for the drone with the spray formulation, an engine-powered generator and fuel for recharging the batteries. Drone battery technologies are expensive, and the number of charges is limited with existing technologies to less than an estimated 500 charges or only 75 h actual spraying before new batteries are required. Clearly, more research and development are needed to determine the most effective design, and operating procedures are needed to facilitate the control of hoppers prior to the expansion of the locust reaching plague status, with appropriate guidance and standard operating procedures (SOPs) for training to enable drones to be used effectively in certain situations to minimise the formation of swarms.

At present, there is little information available on how to treat desert locusts with drones in a safe and effective way. Solid scientific-based field testing is required. From there, guidelines and standard operating procedures (SOPs) can be developed, and training provided before using drones. The FAO is clear that these are very important steps that cannot be omitted.

# 5. Current Trials

## 5.1. Kenya

Drones were tentatively used in 2020 to determine whether their use would be effective. In Kenya, the main focus was to target hoppers and roosting locusts with better efficiency to develop SOPs for the optimal use of the technology. A DJI Agras T16 drone, fitted with a 16 L tank, six rotors, and programmed for operation in Auto and manual modes, was used to treat a 6.5 m swath applying 4.8 L/minute and treat 10 hectares. According to the manufacturer, the drone was fitted with either XR11001VS or XR110015VS fan nozzles which can apply 3.6 to 4.8 L/min, respectively.

The drone (Figure 3) can be operated at up to 3 km at a flight altitude of 2.5 m from the operator and spray at a maximum operational flight speed of 7 m/s. There were 16 nozzles operating from the height of 2.5 m above the canopy, so the drones automatically adjusted to maintain this height. As per the manual, the pilot controls the flight and the volume sprayed. The intention was to spray as per the recommendation on the pesticide label, so various flight parameters to determine which one results closest to the recommended dosage were tried with different heights and flying speeds.
<figure><img src="image_97.png" /><figcaption>**Figure 3.** Drone spraying locusts in trees in Kenya (source: CABI [33]).</figcaption></figure>

5.2. India

The operation of drones was examined by deploying them initially for spot application, including high trees, dense plantation and inaccessible areas in association with ground control teams for effective control operation. Fifteen drones were each equipped with a 10 L tank and supplied with eight batteries so that 1 hectare could be treated in 15 min, and a drone could cover 12–15 hectares during a day. Flat fan nozzles were used for spraying a mixture of two insecticides, supplied as per EC formulations. They contained 5% lambdacyhalothrin and 2.8% deltamethrin. Insecticide in the range of 100–120 mL was mixed with 10 L of water. A total of 1753 L of the mixture was applied using 15 drones over 60 days, covering 7017 hectares in a total of 2007 h.

The flight height was 12.2–13.7 m. Flying speed depended on the whether the target was in a tree or in fields and ranged from 10 to 20 km/h. Swath width depended on wind speed and ranged from 1 to 5 m. The volume of spray applied was 10 L per ha. The mortality of locusts was between 50 and 90% at various locust stages.

No ULV formulations were sprayed and no ULV nozzles were used in drone spraying, but if used, the area coverage would increase 10 times.

The overall indications to date are that:

(a) The small multi-copter drones do not have an adequate lifting and endurance capacity to treat more than a small area;

(b) Most have hydraulic pressure nozzles that spray too high a volume so the area that can be treated is very limited. The power requirement to pump the volume of water would be better deployed by using ULV sprays applied with a rotary atomiser;

(c) Even when applying a ULV spray with rotary atomisers, the small payload (10–15 kg) carried by drones limits the area that can be treated with significantly higher operating costs than existing ground sprayers. Spraying small areas of trees on which locusts can be resting is one example as the target is not easily accessible with ground equipment;
(d) Most commercial drones are not designed for ULV products, as pumps, hoses and plastic materials are not compatible with the formulations being used;

(e) There is a question over durability in desert environments with sand and dust drawn across exposed electric motors from multi-rotor types;

(f) Battery cost and operating costs are high with limited duty cycle—400 × before they need to be changed;

(g) A larger payload drone (100 kg+) may offer better potential to fill the gap between using ground equipment and manned aircraft.

Ideally, locusts are controlled by the aerial application of ultra-low volume (ULV) sprays from c. 10 m height applied at one litre per hectare, using a spray with droplets of 120 µm volume median diameter (VMD) [34], while smaller droplets using 70–100 µm VMD sprays are applied with ground equipment. A narrower and more effective droplet spectrum is provided by rotary atomisation.

**6. Conclusions**

At present, the main use of drones will be to improve the surveillance of remote areas where locust populations can increase following more intense rainfall, especially when improvements in the effectiveness of deep learning and computer vision algorithms facilitate the efficiency of spotting the build-up of locusts to form swarms so that appropriate measures can be taken sooner [35]. Further research is needed to examine the effectiveness of drones which carry an increased payload of spray and are equipped with rotary nozzles to apply ultra-low volume sprays in remote areas and extend surveillance over larger areas, but also target sprays at hoppers to reduce the development of swarms. Where swarms have invaded new territories, rapid action insecticides applied as ULV sprays will continue to be needed. With concerns over climate change, surveillance and the ability to minimise the formation of swarms will be more important. In addition, in war or insecurity zones, any control of locusts will remain difficult and realistic mitigation measures will need to be carefully designed and implemented [36].

**Funding:** This research received no external funding.

**Acknowledgments:** The author gratefully acknowledges Keith Cressman (FAO, Desert Locust Information Service, Rome) for his guidance regarding recent work by FAO, as well as Ivan Rwomushana (CABI, Nairobi, Kenya) and K.L. Gurjar (Locust Unit, Faridabad, Haryana, India) for information about locust control and drone use in their respective countries.

**Conflicts of Interest:** The author declares no conflict of interest.

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Short Biography of Authors

**Graham A. Matthews** is a Professor Emeritus at Imperial College, Silwood Park (UK). His research within the International Pesticide Application Centre (IPARC) was on the application of pesticide technology, involving testing equipment suitable for vector control for the WHO and on applying pesticides for crop protection. Early in his career, he was involved in cotton pest research in Africa. Prof. G.A. Matthews was a member of the Pesticide Advisory Committee of the UK Department for Environment, Food and Rural Affairs from 2000 to 2004, and Chairman of the FAO Expert Panel on Locust Pesticides from 1989 to 2015. He is the author of numerous publications and books, including *Pesticide Application Methods* in 1979, now in its fourth edition, and most recently *Pesticides, Health, Safety and the Environment* (second edition—2016) and a *History of Pesticides* (2018).
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Article

# Regional Differences in Control Operations during the 2019–2021 Desert Locust Upsurge

Renata Retkute <fnref n="1" />,*, Rebekah G. K. Hinton <fnref n="1" />,<fnref n="2" />,*, Keith Cressman <fnref n="3" /> and Christopher A. Gilligan <fnref n="1" />

**Abstract:** The desert locust remains a major threat to global food security. Control operations are a crucial tool to manage crisis; this research investigated the nature of control operations conducted between 2019–2021. Historical data on desert locust and control operations were obtained from the survey reports at the FAO Locust Hub and analysed with respect to survey reports, land cover types, cropland/rangeland extent and crop productivity data. We found that 16.1% of the grid cells with locust presence and 14.9% of the grid cells with control operations had a proportion of rangeland higher than 0.75; while 13.3% of the grid cells with locust presence and 13.2% of the grid cells with control operations had a proportion of croplands higher than 0.75, highlighting that locust presence and control operations were reported in both rangeland and cropland. Control operations continue to be used both to reduce overall locust numbers and to protect crops. Furthermore, through identifying which crops were most at risk, our analyses indicate that wheat production was under the highest strain during periods of increased locust infestations.

**Keywords:** desert locusts; control; crop loss; pastureland; land cover

## 1. Introduction

Desert locusts (*Schistocerca gregaria*) continue to pose one of the most severe threats to agricultural and rangeland crops, making their control a priority to food security in many regions [1]. Timely and precise early warning, and rapid response can be achieved through sustaining monitoring efforts [2], orienting surveys towards historical hotspots [3], increasing the areas accessed by field teams [4], integrating the roles of stakeholders [5], and by more efficient monitoring and control techniques [1]. Symmons [6] outlines three strategies in desert locust control: control during the upsurge for plague prevention, eliminating a plague through destroying all desert locusts, and allowing the plague to continue but protecting crops. The method of control applied and intensity of the control operation varies in accordance with the aim of the control operation and the stage in the desert locust outbreak in which it is applied. The United Nations Food and Agriculture Organisation (FAO) coordinates preventative and reactive control strategies through locust surveys and control operations, and providing early warning [7–12].

Prior to 1965, plagues of desert locust were common in East and West Africa, the Middle East and parts of Pakistan and India [13]. The availability of effective pesticides, together with an integrated programme for surveillance, monitoring and control, developed and advocated by FAO, has prevented local outbreaks and more widespread upsurges from developing into plagues in many regions since 1965 [14,15]. Pesticide application using ultra low volume (ULV) spraying formulations, originally developed in the 1950s and 1960s, remains one of the most extensive control methods [6,16]. Three types of sprayer platforms are utilised in a field, with each having specific control related characteristics:

**Citation:** Retkute, R.; Hinton, R.G.K.; Cressman, K.; Gilligan, C.A. Regional Differences in Control Operations during the 2019–2021 Desert Locust Upsurge. *Agronomy* **2021**, *11*, 2529. https://doi.org/10.3390/agronomy11122529

Academic Editors: Michel Lecoq and Arianne Cease

Received: 30 October 2021
Accepted: 7 December 2021
Published: 13 December 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

<footnote n="1">¹ Epidemiology and Modelling Group, Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK; cag1@cam.ac.uk</footnote>

<footnote n="2">² Department of Civil and Environmental Engineering, University of Strathclyde, Glasgow G1 1XJ, UK</footnote>

<footnote n="3">³ Food and Agriculture Organization of the United Nations, Viale delle Terme di Caracalla, 00153 Rome, Italy; Keith.Cressman@fao.org</footnote>

<footnote>* Correspondence: rr614@cam.ac.uk (R.R.); rgkh2@cam.ac.uk (R.G.K.H.)</footnote>
portable ULV sprayers (slow work rate and up to 10 ha target size), vehicle-mounted sprayers (medium work rate and 1–100 ha target size), and aircraft-mounted sprayers (fast work rate and over 25 ha target size) [17]. The dispersal of the pesticide into small droplets for ULV application ensures efficient use of the pesticide and effective dispersal on the wind. Restrictions of resource and availability of aerial spraying mean that handheld and especially vehicle-mounted spraying to control desert locust remain common.

However, the control of desert locusts can have negative ecological consequences on non-target organisms [18–20]. Organophosphates and carbamates have historically been the most commonly used insecticides as they are fast acting and relatively non-persistent [16]. The non-persistence minimises their impact on non-target insects as they do not remain biologically active for long after application. Nevertheless, organophosphate and carbamate insecticides are broad spectrum compounds, exhibiting toxic effects on other arthropods that risk causing unintended ecological damage. Biopesticides represent an alternative method for the control of desert locusts, providing specific control [19]. For example, *Metarhizium anisopliae* var. acridum is a biopesticide specific to the family Acrididea, containing desert locusts [20]. However, despite the benefits in minimising the ecological consequences of desert locust control, *Metarhizium anisopliae* is often not used due to slow action, variable locust mortality and challenges in its production and storage [16]. Nevertheless, good results were achieved in Somalia where it was used exclusively during the 2019–2021 upsurge. Whilst pesticides with adverse ecological consequences remain in use, monitoring and managing the extent and location of control operations will be an important method in minimising negative ecological consequences for non-target insects.

In May and October 2018, the tropical cyclones Mekunu and Luban caused heavy rainfall and intense precipitation events in the Arabian peninsula, which provided suitable environmental conditions for breeding, multiplication and gregarization of the desert locust [21,22]. In January 2019, desert locust swarms spread to Yemen, Saudi Arabia and Iran, eventually crossing the Red Sea to East Africa [23]. From June 2018 to June 2020, desert locust swarms were observed in more than 22 countries [23].

The current research was designed to investigate the nature of control operations conducted during the 2019–2021 desert locust upsurge. The work is part of wider project, designed to evaluate the potential for epidemiological models, coupled with meteorological models for swarm dispersal, to optimise the deployment of control in order to minimise the impacts of desert locust on agricultural crops and rangeland. Here we describe an empirical analysis of control practices. Specifically, we investigate properties of control operations under the following aspects: survey reports, land cover types, cropland/rangeland presence and crop productivity. The primary objective is to assess the extent to which control occurs on crop and pastureland (i.e., control aimed directly at desert locusts to minimise economic loss) compared with bare ground and shrubs (i.e., control aimed directly at desert locusts and indirectly at preventing economic loss and hardship). Our analysis indicates that control operations in East Africa, the Middle East and an Eastern Region (comprising, Iran, Pakistan, India and Nepal) were qualitatively different in terms of the type of control used for locust management and how desert locust infestations affected the livelihoods of the communities in these regions.

## 2. Materials and Methods

### 2.1. Data

Historical data on desert locust presence and control operations were obtained from survey reports and archives at the FAO Locust Hub website [24]. We have extracted the records dated between 1 January 2019 and 1 June 2021.

We used land cover classification from Copernicus global map of land cover at 100 m resolution data (CLC100) [25,26]. Maps of an area fraction that represent the percentage of the pixel occupied by cropland and rangeland at 1 km resolution were downloaded from EU Science Hub [27]. The global crop production statistics data for 2010 [28] and data in