for males < 1.402), and the tegmina of the typical gregarious adults are visibly longer (E/F for females > 1.608; for males > 1.625).

Numerous publications describing the Italian locust spatio-temporal distribution in different parts of its range were also analyzed.

## 3. Results

### 3.1. Distribution Patterns of the Italian Locust over the South-Eastern Part of West Siberian Plain and the Adjacent North-Eastern and Eastern Parts of the Kazakh Uplands

A comparative analysis of three gradient transects crossing the eastern part of the Italian locust range from the forest-steppes of West Siberian Plain to Central Asia: (1) mainly along the 77–79th meridians east [4,9,12]; (2) along the 80th meridian east (Figure 4B), and (3) along the Irtysh River (Figure 4A)—allowed to reveal the general patterns of the species populations’ distribution in the periods between outbreaks.

<figure><img src="image_67.png" /><figcaption>**Figure 4.** Population distribution of the Italian locust along two gradient (transzonal) transects crossing the south-eastern part of West Siberian Plain and the adjacent north-eastern and eastern parts of the Kazakh Uplands along the Irtysh River (A) and near the 80th meridian east (B). N—north; E—east.</figcaption></figure>
In the southern forest-steppes and in the northern steppes of West Siberia [23], the Italian locust is distributed sporadically, especially during years without outbreaks. Its local colonies occur mainly in dry habitats of watershed plains, including overgrazed pastures and road-sides, while its abundance may be very low. Sometimes a surveyor may spend more than an hour to find one adult. The species is more common in the typical steppes. Its populations are also associated with the steppe habitats on watershed plains, but they are more or less common over terraces and dry parts of upper flood-plains. In the dry steppes of the Kulunda Plain [23], there is the local optimum of the Italian locust. Its populations are in almost all applicable habitats, from flood-plains to watershed plains [6,12,24,25]. In the southernmost steppes and in the northern parts of the semi-deserts, the species colonies occur either in watershed plains and southern slopes of hills or along upper flood-plains. The main optimal area of the Italian locust is in the southern parts of the semi-deserts. Its populations occur in all or almost all favorable habitats, and the abundance level is usually moderate (Figures 3 and 4). Further south, its populations are again sporadic and scarce. In the deserts, they are commonly associated with some parts of watershed plains, mountain slopes, and upper floodplains. The sketchy pattern of the Italian locust distribution along the Irtysh River in the 1920s described by G.Ya. Bey-Bienko [26] corresponds mainly to our data (Figure 5).

<figure><img src="image_68.png" /><figcaption>**Figure 5.** Population distribution of the Italian locust along the Irtysh River in the 1920s (after [26]).</figcaption></figure>

## 3.2. *Long-Term Dynamics of the Italian Locust in the Central and Eastern Parts of Its Range: General Patterns*

General trends of the Italian locust long-term dynamics were mainly evaluated on the basis of published data [10,11,27–31]. Recently many of them were described for the main regions of the former USSR countries [9].

In the 19th century, the situation with the Italian locust and other grasshoppers in the Russian Empire was relatively calm. Many acridid outbreaks were registered in 1821–1830 and 1841–1850. However, K. Lindemann [27] described in detail a series of outbreaks of the Italian locust per se in the forest-steppes of European Russia. The situation changed during the next century. Some serious outbreaks occurred in 1921–1940. However, the Italian locust had remained the secondary pest.

For instance, in the comprehensive report on the acridid pests of the USSR for 1925–1933 [29], authors described the problems associated with the migratory locust, *Lo-custa migratoria* (Linnaeus), on 32 pages, with the Moroccan locust, *Dociostaurus maroccanus* (Thunberg)—on 33 pages, and even with the desert locust, *Schistocerca gregaria* (Forskål)—on four pages, while the part concerning the Italian locust took up slightly more than one page only. As a rule, the breeding areas of *C. italicus* were localized and limited by hundreds or thousands hectares, mainly in the semi-deserts [28]. For instance, during the
outbreak in 1932–1933 in Kazakhstan, the general infested area was less than 190,000 ha (cf. with the area infested in 2000—more than 8 million ha [1]). However, its local bands and swarms were characterized by very high densities and active migrations, especially in the semi-deserts.

From 1940 until 1990 upsurges had been more or less common but remained highly localized. However, at the end of the 20th century, the outbreaks became extremely serious and common. For the North Caucasus—Lower Volga area, M.V. Stolyarov [10,11] described four outbreaks of the Italian locust (in 1954–1957, 1972–1974, 1982–1984, and 1992–1998). However, in the southern part of West Siberia, the outbreaks occurred in 1952–1956, 1967–1971, 1977–1982, and 1999–2002 [9]. Thus, the outbreaks of the Italian locust did not exactly coincide in the different part of its range. In many cases, outbreaks in West Siberia started earlier than in the North Caucasus—Lower Volga region, but, as a rule, were relatively weak and sporadic. However, the last and worst outbreak had begun in 1991 in the North Caucasus—Lower Volga region. After that, the outbreak spread over a huge area from Azov Sea to the eastern part of Kazakhstan (1996–1998). In 1998–2001 the main breeding areas moved northward and eastward. On the last stage (2002–2014), these areas became smaller and occupied the territory from south Ukraine to Caspian Sea and to the Ural Mts. [9]. The last decade is characterized by some sporadic outbreaks of the Italian locust in the central and eastern parts of its range, e.g., mainly in some regions of the North Caucasus [32–34].

Thus, the long-term population dynamics of the Italian locust can be very distinct in the different part of its range. Such pattern may be determined by regional climatic peculiarities, by variations in soils and vegetation covering, and by some changes in human activities.

### 3.3. Peculiarities of Long-Term Dynamics of the Italian Locust in the South-Eastern Part of West Siberian Plain and in the Adjacent Parts of the Kazakh Uplands

The south-eastern part of West Siberian Plain and the adjacent parts of the Kazakh Uplands are the typical territories where outbreaks of the Italian locust began and may begin [1, 4, 6, 9, 30, 35, 36]. First data on its local outbreaks appeared in the 1910–1930s [29,30,37,38]. However, these outbreaks were sporadic and restricted by one or a few years [29,30]. In the 1930s I.A. Chetyrkina [36] studied the Italian locust distribution in the semi-deserts and in the dry steppes of the eastern part of Kazakhstan. She revealed the main peculiarities of its population distribution when its colonies were found in almost all habitats except pine forests and some plots with halophytes. Actually, her observations showed the Italian locust preferred habitats with sagebrush dominance, including abandoned fields. These shifts in the Italian locust distributions could be associated with some transformation of the territory, because in the beginning of the 20th century, many areas had been plowed, and after that, many fields had become abandoned.

Later, in the middle of the 1950s, during the co-called Virgin Land campaign, vast steppe areas have been plowed and many remaining steppe habitats have become over-grazed. As a result, many habitats of *C. italicus* have been destroyed or damaged. Such regional and local transformations and/or also climate changes could and can result in some shifts in its population dynamics and spatial distribution (Figure 6). Extensive plowing often resulted in very significant decreasing of grasshopper abundance, especially over steppe regions [39].
<figure><img src="image_69.png" /><figcaption>**Figure 6.** Long-term dynamics (1960–2015) of the Italian locust infestations in West Siberia (Altaj, Novosibirsk and Omsk Regions of Russia) and in the Pavlodar and East Kazakhstan Regions of Kazakhstan (% of the maximal registered infested areas [9]).</figcaption></figure>

Later, in the 1960–1980s, some development of technologies preventing soil erosion caused again local but relatively weak and rare outbreaks of grasshoppers and locust, including *C. italicus* [6], but mainly in the semi-deserts of East Kazakhstan. The last and most devastating outbreak of the Italian locust started in 1998. The maximal infested areas were registered in 1999 in the Pavlodar Region and in the south-eastern parts of West Siberia (i.e., mainly in the steppes) and in 2000 in East Kazakhstan (i.e., in the semi-deserts). This outbreak may be qualified as a plague, because the large-scale infestation occupied huge areas and continued at least three years [1,9,16]. Besides, there were numerous bands and swarms in almost all parts of the territory, except local forests and the upper altitudinal belts of mountains. Some swarms actively migrated and could cross the state and regional borders. This extreme outbreak might be promoted either by economical transformations in the former USSR countries in the 1990s, while plant protection services were partly destroyed, trans-boundary cooperation in breeding areas was limited, and abandoned fields spread over huge territories, or by climatic changes of recent decades as well [1].

3.4. *Dynamics of the Italian Locust Populations in the Kulunda Steppe in 2000–2008*

In the Kulunda steppe, the last outbreak started in 1999. This area might be colonized by a specific mixture of local and vagrant populations [19,35], but our observations showed the low possibility of long migrations (cf. [36]). The Italian locust occurred in natural, semi-natural and anthropogenic habitats, including cultivated and abandoned fields. In 1999–2000, the average densities of the Italian locust were usually about 0.3–9.6 adults/m², but in some places, the density was significantly higher (~24 adults/m²) [16,19]. Swarms of this species were common in 2000 and 2001. In 2000, they had occupied about 84 km (from 337 km) along a road from Ust-Volchikha to Aleksandrovskij (see Section 2.2), while in 2001 the swarms were observed over a distance of 60 km. Later, in 2002–2008, there were no swarms along this route. However, in 2015, very small bands (up to several square meters) were observed near Severka and Bor-Forpost.

Dynamics patterns were different in all observation sites (Table 1). One can formally split them into four groups based on the position of the maximum average population density. The first group includes the majority of studied populations (Aleksandrovskij,
Burla, Yarovoe, Platovka, and Mikhaylovskoye). They were at maximum levels during 2000. This group includes mainly the populations from the northern part of the Kulunda steppe, except Mikhaylovskoye. The other groups had the maximum densities of the Italian locust in 2001 (Severka), in 2002 (Bor-Forpost and Ust-Volchikha), and in 2000 and 2002 (Pokrovka), respectively.

This grouping is partly supported by the Spearman rank order correlation analysis (Rs from 0.900 up to 0.975 at the significance level *p* < 0.05) for 2000–2004 (Figure 7) [19]. The analysis of relatively long rows of data (from 2000–2005 to 2000–2008) allows to gradually combine almost all populations (except Bor-Forpost) but with less significant support (Rs > 0.7, *p* < 0.05) (Figure 7). Such similarity is determined by low levels of population densities from 2003 until 2008 in almost all sites. The population near Bor-Forpost only was characterized by more or less gradually increasing from 2003 until 2008 (actually this trend continued in 2009, with the average density 2.69 ± 0.54).

<figure><img src="image_70.png" /><figcaption>**Figure 7.** Associations between the long-term dynamics of the Italian locust populations in the Kulunda steppe for 2000–2004 and 2000–2008 (levels of the Spearman rank order correlation—Rs, *p* < 0.05).</figcaption></figure>

The Kruskal–Wallis ANOVA and median tests show significant inter-annual difference for each site studied at *p* < 0.0001 for all tests. Thus, in all cases, the null hypotheses (the different samples are from the same distribution) should be rejected. The Mann–Whitney U test calculated for every consecutive pair of years for each population (Table 2) reveals significant differences between years with high densities and the adjacent ones for almost all populations [19]. In all cases, variations between consecutive years with densities lower than 3.0 ind. per m² are insignificant.
<table><caption>**Table 1.** Dynamics of the average densities (ind. per m² ± s.e.) of the Italian locust in the Kulunda steppe.</caption><thead><tr><th>Year</th><th>Aleksandrovskij</th><th>Burla</th><th>Yarovoe</th><th>Platovka</th><th>Severka</th><th>Pokrovka</th><th>Mikhaylovskoye</th><th>Bor-For-post</th><th>Ust-Volchikha</th></tr></thead><tbody><tr><td>1999</td><td>?</td><td>?</td><td>0.48 ± 0.27</td><td>0.80 ± 0.33</td><td>0.32 ± 0.22</td><td>~1</td><td>3.2 ± 0.61</td><td>?</td><td>0.32 ± 0.22</td></tr><tr><td>2000</td><td>24.32 ± 2.34</td><td>9.60 ± 0.85</td><td>6.40 ± 0.65</td><td>4.48 ± 0.48</td><td>2.88 ± 0.67</td><td>5.28 ± 0.86</td><td>6.56 ± 0.80</td><td>0.96 ± 0.35</td><td>0.48 ± 0.27</td></tr><tr><td>2001</td><td>2.77 ± 0.70</td><td>5.60 ± 0.73</td><td>4.16 ± 0.63</td><td>3.04 ± 0.53</td><td>7.36 ± 0.82</td><td>4.00 ± 0.65</td><td>0.96 ± 0.35</td><td>0.08 ± 0.08</td><td>1.60 ± 0.46</td></tr><tr><td>2002</td><td>0.16 ± 0.16</td><td>3.20 ± 1.31</td><td>0.16 ± 0.16</td><td>1.28 ± 0.89</td><td>1.92 ± 1.06</td><td>6.40 ± 1.85</td><td>0.32 ± 0.32</td><td>1.92 ± 0.74</td><td>1.92 ± 1.06</td></tr><tr><td>2003</td><td>+</td><td>0.16 ± 0.16</td><td>+</td><td>0.16 ± 0.16</td><td>0.32 ± 0.23</td><td>0.13 ± 0.13</td><td>0.16 ± 0.16</td><td>0.32 ± 0.23</td><td>0</td></tr><tr><td>2004</td><td>0.32 ± 0.32</td><td>+</td><td>+</td><td>0.96 ± 0.54</td><td>+</td><td>0</td><td>0</td><td>0.40 ± 0.27</td><td>0.32 ± 0.32</td></tr><tr><td>2005</td><td>0.32 ± 0.23</td><td>0</td><td>0.38 ± 0.22</td><td>0.53 ± 0.37</td><td>0.05 ± 0.05</td><td>0</td><td>0</td><td>0.85 ± 0.29</td><td>+</td></tr><tr><td>2006</td><td>+</td><td>0.64 ± 0.45</td><td>0.21 ± 0.15</td><td>0.43 ± 0.30</td><td>1.28 ± 0.62</td><td>0.21 ± 0.21</td><td>0</td><td>0.75 ± 0.028</td><td>0.16 ± 0.16</td></tr><tr><td>2007</td><td>0.32 ± 0.23</td><td>0.96 ± 0.54</td><td>0.64 ± 0.32</td><td>1.16 ± 0.69</td><td>1.92 ± 0.74</td><td>1.07 ± 0.46</td><td>0</td><td>1.15 ± 0.37</td><td>+</td></tr><tr><td>2008</td><td>0.48 ± 0.27</td><td>0.16 ± 0.16</td><td>0.51 ± 0.25</td><td>0.96 ± 0.54</td><td>0.64 ± 0.45</td><td>0.32 ± 0.32</td><td>0</td><td>1.54 ± 0.46</td><td>0</td></tr></tbody></table>

+—One or several specimens were found beyond counts; ?—no data for this year.

<table><caption>**Table 2.** Mann–Whitney U test (U/p < 0.05) for the status of Italian locust populations for every consecutive pair of years in the Kulunda steppe.</caption><thead><tr><th>Year</th><th>Aleksandrovskij</th><th>Burla</th><th>Yarovoe</th><th>Platovka</th><th>Severka</th><th>Pokrovka</th><th>Mikhaylovskoye</th><th>Bor-Forpost</th><th>Ust-Volchikha</th></tr></thead><tbody><tr><td>1999–2000</td><td>?</td><td>?</td><td>41.5</td><td>85</td><td>202.5</td><td>125</td><td>167.5</td><td>?</td><td>n.s.</td></tr><tr><td>2000–2001</td><td>469</td><td>195.5</td><td>0.0000</td><td>0.00001</td><td>0.0328</td><td>0.0003</td><td>0.000</td><td>166</td><td>n.s.</td></tr><tr><td>2001–2002</td><td>0.0000</td><td>0.0024</td><td>0.0250</td><td>n.s.</td><td>126.5</td><td>n.s.</td><td>0.0045</td><td>n.s.</td><td>n.s.</td></tr><tr><td>2002–2003</td><td>n.s.</td><td>165.5</td><td>84.5</td><td>153.5</td><td>94</td><td>n.s.</td><td>n.s.</td><td>n.s.</td><td>n.s.</td></tr><tr><td></td><td>n.s.</td><td>n.s.</td><td>0.00001</td><td>0.0020</td><td>0.00002</td><td>n.s.</td><td>1012</td><td>n.s.</td><td>n.s.</td></tr><tr><td></td><td>n.s.</td><td>n.s.</td><td>n.s.</td><td>n.s.</td><td>n.s.</td><td>n.s.</td><td>0.0055</td><td>n.s.</td><td>n.s.</td></tr></tbody></table>

?—no data for this pairs; n.s.—not significant difference.
The seasons with the high locust abundance can be considered as outbreak periods. Our data showed that, in the region, the outbreaks were characterized by the average densities of adults more than 3 ind. per m². However, intensity and duration of each local outbreak may be quite different. For instance, the maximal registered densities varied very significantly between the populations studied (Tables 1 and 2). As for duration, 5 from 9 populations were characterized by the explicit one-year maximum, while one population (near Platovka) showed the high levels both in 2000 and 2001, and the population near Pokrovka was distinguished by the relatively long outbreak from 2000 until 2002. Two other stages in long-term dynamics of the Italian locust populations can be revealed as well:

(1) A recession, when adults' abundance in a local population in the middle and the end of a summer varies between relatively low and moderate (according our estimation, in the Kulunda steppe, from 0.1 up to 2.0 ind. per m², perhaps in some cases—up to 3.2). This means that recommendations of some published manuals concerning monitoring and management of pest locusts and grasshoppers [40,41] to organize partial treatments in the next year, when the density of the Italian locust adults is more than 1 ind. per m², are based on too conservative estimations.

(2) A depression, when density is very low, commonly significantly less than 0.1 ind. per m². In this case, a population may be stable, but scarce locusts are distributed very sporadically. For instance, in 31 July 2019, I spent about two hours on our main model site in the northern part of the Kulunda steppe (near Aleksandrovskij) finding only 10 adults of the Italian locust and estimated their average density as about 25 ind. per ha (Figure 2).

Besides, there were no evident correlations between species abundance, its morphological characteristics (actually the E/F ratio), and its behavior (Table 3). In 2000, when the Italian locust was very abundant on our main model plot near Aleksandrovskij settlement and there were numerous and dense bands and small swarms, the average level of the E/F ratio corresponded to the transiens status [19]. In 2008, when its abundance was low and there were no bands or swarms, the E/F ratio for females corresponded to transiens again (moreover, one female morphologically looked like the gregarious one). Similar discords could be likewise observed on other sites (Table 3) [19]. Our data for 1999–2000 also show that presence of the gregarious form was limited (for all samples—about 4.9% of females and 7.1% of males) [19]. This also means that the rate of long (including transborder) migrations during the outbreaks was low.

Thus, the adjacent local populations of the Italian locust could differ significantly in their long-term dynamics patterns. In the south-eastern part of West Siberian Plain, these changes often look like some waves of spatial redistribution of maxima and minima of abundance [19,20]. The akin peculiarities of the Italian locust population dynamics were described for the North Caucasus as well [42].

<table><caption>**Table 3.** Changes of the average densities (ind. per m² ± s.e.) and average tegmen length/posterior femur length ratios (E/F ± s.e.) of the Italian locust on two plots with quite different long-term dynamics.</caption><thead><tr><th rowspan="2">Year</th><th colspan="5">Aleksandrovskij</th><th colspan="3">Ust-Volchikha</th></tr><tr><th>Density</th><th>Species Behavior</th><th>E/F Females</th><th>E/F Males</th><th>Density</th><th>Species Behavior</th><th>E/F Females</th><th>E/F Males</th></tr></thead><tbody><tr><td>1999</td><td>?</td><td>?</td><td>?</td><td>?</td><td>0.32 ± 0.22</td><td>No bands and swarms</td><td>1.576 ± 0.004</td><td>1.609 ± 0.006</td></tr><tr><td>2000</td><td>24.32 ± 2.34</td><td>Numerous bands, small swarms, active local flights</td><td>1.514 ± 0.016</td><td>1.539 ± 0.013</td><td>0.48 ± 0.27</td><td>Very small and scarce swarms</td><td>1.368 ± 0.010</td><td>1.392 ± 0.012</td></tr><tr><td>2001</td><td>2.77 ± 0.70</td><td>No bands and swarms</td><td>1.395 ± 0.013</td><td>1.406 ± 0.018</td><td>1.60 ± 0.46</td><td>Very small and scarce swarms</td><td>1.473 ± 0.011</td><td>1.479 ± 0.009</td></tr><tr><td>2008</td><td>0.48 ± 0.27</td><td>No bands and swarms</td><td>1.484 ± 0.038</td><td>1.384 ± 0.024</td><td>0</td><td>No bands and swarms</td><td>?</td><td>?</td></tr></tbody></table>

In bold—the average E/F ratios correspond to the intermediate (transiens) status of the local population; in italics—the solitarious status of the population; ?—no data for this year.
3.5. *Seasonal Dynamics and Distribution of the Italian Locust Local Population in the Northern Steppe in 2000–2019*

We started to study the dynamics of the Italian locust population in the northern part of the Kulunda steppe (near Aleksandrovskij settlement) in 2000, on 20 June. The steppe areas and the edges of agricultural fields were occupied by numerous hopper bands. These bands mainly consisted of the first stage hoppers (about 95%) [16]. The average density of locusts was 24.67 ± 4.42 ind. per m² on the steppe plot and 430.4 ± 161.6 ind. per m² on the field edge where some bands concentrated. The density in bands could be more than 1000 ind. per m², while band areas varied between 2 and 300 m² [16].

After a week, the bands included the hoppers of all five instars, while the second and third instars dominated. On 5 July, the main part of the population consisted of the fourth instar hoppers; however, it also included many nymphs of the third and fifth instars [16]. The hopper band areas varied between 4 and 3500 m². On 20 July, adults comprised almost half of the population. The second half included mainly the fifth instar hoppers and a few fourth stage hoppers [16]. Some bands occupied more than 5 ha. On the control plot, the average density was relatively stable [16]. Adults tried to fly, but their flights were limited to meters to dozens of meters. Besides, there were several huge colonies of rooks. Our estimations show that these birds can withdraw about 10–15% of the locust population [9].

Treatments with fipronil showed very high effectiveness within the 15 m of the treated swaths—more than 95% after several days, while on the untreated 15 m swaths only some weak effects (17–33% reduction) could be observed only after a week or two [16,43]. This pattern can be explained by extremely low rates of young hopper migrations till the end of June, because there were sufficient quantities of preferred foods. In July, insects (last instars and adults) started to move more actively [16,43].

In 2001, general abundance of the Italian locust decreased, and there were no bands. In the beginning of our studies, on 5 June, the average density of the Italian locust was only 3.41 ± 0.54 ind. per m², while the population mainly consisted of the first stage hoppers (about 87%). The early fourth instar hoppers were observed on 15 June, and the first adults—on 5 July. On 15 July, adults comprised about 64% of the population. Besides, there were also the fourth instar (about 21%) and fifth instar nymphs (about 15%). On the control plot, the average density was relatively stable and remained almost the same during the season (on 15 July—2.77 ± 0.70 ind. per m²).

Experiments with teflubenzuron showed that this IGR was highly effective in blanket treatments and also within the treated 15 m swaths (Table 4). Effectiveness was most obvious after about a week which corresponds to the molting rates of hoppers—every 5–7 days [9]. The high levels of effectiveness were observed on treated plots. Untreated swaths were characterized by moderate effectiveness of treatments, usually about 80–84%.

<table><caption>**Table 4.** Effectiveness (%) of teflubenzuron treatments (6 June) on the experimental site in the northern part of the Kulunda steppe (near Aleksandrovskij settlement) in 2001.</caption><thead><tr><th colspan="2">Plot</th><th>7 June</th><th>12 June</th><th>13 June</th><th>15 June</th><th>16 June</th><th>23 June</th><th>26 June</th><th>5 July</th><th>15 July</th></tr><tr><th>Type</th><th>Treated/Untreated</th><th>D1</th><th>D6</th><th>D7</th><th>D9</th><th>D10</th><th>D17</th><th>D20</th><th>D29</th><th>D39</th></tr></thead><tbody><tr><td colspan="2">Blanket</td><td>31.4</td><td>70.0</td><td>100</td><td>93.7</td><td>100</td><td>100</td><td>76.0</td><td>100</td><td>86.1</td></tr><tr><td rowspan="2">1:1</td><td>Treated</td><td>57.2</td><td>81.3</td><td>100</td><td>100</td><td>93.2</td><td>100</td><td>100</td><td>91.7</td><td>100</td></tr><tr><td>Untreated</td><td>35.7</td><td>43.8</td><td>77.5</td><td>80.3</td><td>79.5</td><td>70.8</td><td>55.0</td><td>50.0</td><td>65.4</td></tr><tr><td rowspan="2">1:2</td><td>Treated</td><td>46.4</td><td>81.3</td><td>100</td><td>96.1</td><td>100</td><td>100</td><td>100</td><td>100</td><td>82.7</td></tr><tr><td>Untreated</td><td>57.2</td><td>62.5</td><td>70.0</td><td>56.6</td><td>86.4</td><td>66.7</td><td>-</td><td>8.3</td><td>56.7</td></tr><tr><td rowspan="2">1:3</td><td>Treated</td><td>14.3</td><td>70.0</td><td>76.0</td><td>81.1</td><td>90.1</td><td>86.8</td><td>100</td><td>33.3</td><td>86.1</td></tr><tr><td>Untreated</td><td>14.3</td><td>10.0</td><td>52.0</td><td>36.9</td><td>78.2</td><td>33.9</td><td>4.0</td><td>-</td><td>58.4</td></tr></tbody></table>

These experiments showed that teflubenzuron (like other IGRs) could be very suitable for the Italian locust management in the steppes of South Siberia. However, the efficacy
of the barrier treatments with relatively wide untreated swaths was low. Hence, blanket application and barrier treatments with narrow equal alternating swaths may be optimal.

### 3.6. *The Italian Locust and Rare Orthopteran Species*

Among local species of Orthoptera, *Saga pedo* (Pallas), *Gampsocleis glabra* (Herbst), and *Onconotus servillei* (Fischer de Waldheim) are on the IUCN Red List of Threatened Species [44]. The first species is also in the Red Book of the Russian Federation. Besides, in the south-western part of West Siberian Plain, there are several rare species of Orthoptera. Recently, we analyzed shifts in rare acridid species distribution over the Baraba and Kulunda steppes [45]. At least two grasshoppers, namely, *Notostaurus albicornis* (Eversmann) and *Mesasippus arenosus* (Bey-Bienko), could be found in the habitats where the Italian locust may be very abundant. *Miramiola pusilla* (Miram) (Tettigoniidae) and *Aeropedellus baliolus* Mistshenko. (Acrididae) may be observed on these plots as well. This means, in the steppe habitats, anti-locust treatments can result in decreasing and even elimination of rare species populations.

Rare species were found on almost all sites studied or just nearby (see Section 2.2), except vicinities of Platovka and Pokrovka (Table 5). *G. glabra* was the most common rare species in the steppe habitats. *M. pusilla* was found on four sites, both *Saga pedo* and *A. baliolus*—on two, and *N. albicornis* occurred only in one place.

<table><caption>**Table 5.** Occurrence of rare Orthoptera on sites studied in the Kulunda steppe.</caption><thead><tr><th>Year</th><th>Aleksandrovskij</th><th>Burla</th><th>Yarovoe</th><th>Platovka</th><th>Severka</th><th>Pokrovka</th><th>Mikhaylovskoye</th><th>Bor-Forpost</th><th>Ust-Volchikha</th></tr></thead><tbody><tr><td>1992</td><td>?</td><td>?</td><td>AB,<br>NA</td><td></td><td></td><td></td><td></td><td>?</td><td>?</td></tr><tr><td>1999</td><td>?</td><td>?</td><td>MP</td><td></td><td></td><td></td><td></td><td>?</td><td></td></tr><tr><td>2000</td><td>GG, MP<sup>b</sup></td><td></td><td>AB,<br>NA</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>2001</td><td>AB, GG<sup>c</sup>, MP</td><td>GG</td><td>NA</td><td></td><td></td><td></td><td>GG, SP<sup>a</sup></td><td></td><td></td></tr><tr><td>2002</td><td>AB, MP<sup>d</sup></td><td></td><td>AB</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>2003</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>2004</td><td>GG, MP<sup>e</sup></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>2005</td><td>GG</td><td>GG</td><td>AB</td><td></td><td></td><td></td><td></td><td>GG, SP</td><td></td></tr><tr><td>2006</td><td>GG</td><td></td><td>AB,<br>MP</td><td></td><td>MP<sup>a</sup></td><td></td><td></td><td></td><td></td></tr><tr><td>2007</td><td></td><td></td><td>MP</td><td></td><td></td><td></td><td></td><td></td><td>GG<sup>a</sup></td></tr><tr><td>2008</td><td>GG<sup>e</sup>, MP<sup>e</sup></td><td></td><td>GG</td><td></td><td></td><td>GG</td><td>GG</td><td></td><td></td></tr><tr><td>2015</td><td>GG</td><td></td><td>MP</td><td></td><td></td><td></td><td>MP</td><td></td><td></td></tr></tbody></table>

AB—*Aeropedellus baliolus* Mistsh.; GG—*Gampsocleis glabra* (Hbst.); MP—*Miramiola pusilla* (Miram); NA—*Notostaurus albicornis* (Ev.); SP—*Saga pedo* (Pall.); <sup>a</sup>—the species was found on some adjacent plot; <sup>b</sup>—the species was also found after the fipronil treatment (30 days since—20 July); <sup>c</sup>—the species was also found after the teflubenzuron treatment (39 days since—15 July); <sup>d</sup>—the species was found only on the plot treated by the synthetic pyrethroid in 2001; <sup>e</sup>—the species was also found on the plots treated by the synthetic pyrethroid in 2001; <sup>?</sup>—no data for this year.

In 2000 and 2001 anti-locust treatments in the northern part of the Kulunda steppe (near Aleksandrovskij settlement) did not result in elimination of the local populations of rare Orthoptera. Three species, namely, *A. baliolus*, *G. glabra*, and *M. pusilla*, were found more or less often. Moreover, in 2000, the last species was observed on the treated swath after a month. In 2001, a similar situation was registered for *G. glabra*. Later, in 2002, 2004, and 2008, *M. pusilla* was also found on the plots treated by the synthetic pyrethroid in 2001. This means some localized treatments with acridicides (especially the barrier ones) do not destroy significantly populations of rare Orthoptera.
**4. Discussion**

Our studies of the Italian locust ecology and distribution as well as studies of our colleagues during last two decades resulted in revealing several dilemmas concerning approaches to monitor, manage, and forecast its population dynamics in time and space.

4.1. *May We Use for the Italian Locust Approaches and Technologies Developed for the Desert and Migratory Locusts or Not?*

Nowadays, the Italian locust is the only locust species mainly associated with temper-
ate grasslands, namely, steppes and northern semi-deserts. The main breeding (outbreak)
areas of the desert and migratory locusts as well as some other important pests are in the
tropical and subtropical regions [2,3,9,46]. This is why many ecological and biological
peculiarities of the Italian locust are quite different [1,2,9]. The species is univoltine and is,
even during depressions (see Section 3.4), often widely distributed across different ecosystems, especially in the dry steppes and the semi-deserts. Its behavior during outbreaks
is common for locusts, but areas occupied by bands and swarms and ranges of dispersal
rates are relatively limited, while outbreaks are relatively short and commonly can last for
one or several years. This means that, in steppes and semi-deserts, it is almost impossible
to identify precisely preferred breeding areas of the Italian locust [47]. In the 1950s K.A.
Vasil'ev [5] tried to delimit some such breeding areas in Central Kazakhstan, but in reality,
he described several plots where gregarization already had started.

In the steppes, the species occurs usually in all applicable habitats, but their local
populations are often scarce and characterized by low abundance, while, in the semi-deserts,
its populations may be usually relatively abundant for many decades [4,9,12,36]. Besides,
the Italian locust long-term dynamics may be described as quite specific. In the dynamics
of the migratory and desert locust, several main periods, namely, plagues, outbreaks, and
recessions (and sometimes—also peak plagues, upsurges, and deep recessions), may be
often distinguished [48–50]. In the dynamics of the Italian locust, plagues are extremely
rare. Only last huge outbreaks in the end of 20th century can be qualified as the plague.
Actually, numerous outbreaks of *C. italicus* were and are usually limited in space and time,
and their decline may result in either the recession or the depression characterized by stable
populations with extremely low average densities and scarce individuals’ distribution (see
Section 3.4). If a population drops off, the recession may transform into the depression.
On the contrary, if a population with very low abundance begins to increase (and may be
crowding), the depression may transform into the recession.

One may suggest that, in this situation, we should monitor all habitats colonized by
the Italian locust across huge territories of its range and, inside the range, try to check
carefully populations with relatively high densities of adults (probably, more than 1 ind.
per m² in the steppes and 5-7 ind. per m² in the semi-deserts). Therefore, many (or all)
approaches developed to monitor and control the desert and migratory locusts are not
applicable for the Italian locust, or they should be adapted for the situation.

4.2. *Monitoring, Management, and Forecasting: Is the Regional Level of Exploration Enough or Not?*

The environmental factors and the biological and ecological characteristics of each
species can significantly vary in time and space so that their relations can be revealed only
by consistent explorations of species populations across its total range [3]. This is important
for both potential pest species and rare forms. Actually, in many cases, pest infestations can
be small-scale events, localized in space and time and dependent on local conditions [51].

Local outbreaks of the Italian locust usually start after several years with warm and relatively dry periods in the end of spring and in the beginning of summer, while their regressions are mainly associated with cool and rainy summers [3,5,10,11]. However, rates of increasing and decreasing, gregarization and dissociation in local populations may be quite different [4,9,16] and look like depending on local environmental conditions.
As a result, the local outbreak in one population can develop faster (or slower) than the outbreaks in adjacent colonies. Some similar trends can be revealed for regression.

However, forecasting systems are usually based on the regional generalization and simplification of assessment data [32,33,40,41], while local colonies of *C. italicus* can be significantly different in their ecology (including dynamics) and diversity (including intrapopulation characteristics) [4,9,19,52]. This means that we should use often different management procedures for two neighboring local populations of this species; moreover, in many cases, we are not able to delimit a local population without special studies [52].

We should reveal seasonal and long-term dynamics of local populations (ideally, all such populations) and try to evaluate their temporal patterns relative to climatic and ecosystem changes and to peculiarities of each colony. We should reveal also spatial structures (patches and gaps, distances, population connections, barriers and corridors) and local dispersal systems (parameters of emigration and immigration).

These substantial localized variations in population dynamics mean large scale forecasting of Italian locust upsurges and declines is very difficult. Local forecasting and management may be possible based on increased understanding of local population dynamics, but having local knowledge in the many parts of its vast range and in quite different habitats would require substantial effort that at present is just not possible. However, if we eventually understand the exact patterns of spatial population structures, we will be able to understand, at least, some peculiarities of dynamic patterns in each local population.

### 4.3. Monitoring, Management, and Forecasting: When Should We Begin (or End) to Trouble or When Not?

National and international plant protection services usually use one or several parameters to determine when and where control operations should start. J.A. Lockwood [53] designated this approach as the administrative one. For example, in the USA and in Russia, these operations usually begin when population densities of grasshoppers reach more than 9–10 ind. per m² [1,40,41]. In the case of the Italian locust, according different authors [1,9,40,41], the critical values for hoppers are about 2–5 and for adults—about 1 ind. per m². However, these levels of density are actually too low [53,54]. For instance, in the dry steppes of Central Kazakhstan, the average adult density of solitarious populations of *C. italicus* could be more than 2–7 ind. per m² [5], while in the semi-deserts and the mountain steppes of East Kazakhstan, this density might reach 26 ind. per m² [36]. This means that the critical values for the Italian locust may vary remarkably from one population to another and from one year to another and can depend on numerous parameters (climatic fluctuations, vegetation and soil dynamics, human resources, etc.) Moreover, density effects can be also very notable [55]. They may be rather complicated and more or less unpredictable due to complex nature of ecosystem and population dynamics. Besides, according the catastrophe theory [56], small variations in weather may result in different population dynamics. There are no exact criteria to distinguish consecutive stages of long-term dynamics of locusts as well [50].

This means in many cases we do not have applicable criteria where, when, why and how to monitor and control early infestations [57]. This is especially important for the Italian locust, since its populations between outbreaks are sprawling and scarce. Some formal criteria (densities, band formation, morphometric indices, etc.) may mean almost nothing, because (1) critical values can vary significantly between different ecosystems and between different periods, (2) some traits of gregarization may be revealed during regressions when a population density is relatively low, (3) small changes can result in different dynamics [55,56], and (4) at least in some cases usual criteria do not correlate [19] (see also Section 3.4).

### 4.4. Treatments: When Do Barriers Work and When Not?

Barrier treatments are widely used for locust populations management in different regions. The so-called reduced area and agent insecticide treatments (RAATs) technology often result in evident decline of locust densities, preserve some level of biological diver-
sity, and significantly decrease direct expenses [58,59]. However, the experimental barrier treatment with fipronil showed that its general efficacy was low [16] (see also Section 3.5). The hopper bands usually stayed on the steppe plots with well-developed vegetation, did not move or moved only over the very short distances (about several meters per day) and, thus, did not actively cross over the treated areas. In 2001 the experimental treatments with teflubenzuron showed the similar pattern. The maximal effect on the untreated swaths was observed in the middle of June (after 9–10 days since the treatment) (Table 4), and it was relatively significant only for the experiment with equal narrow swaths. When hopper bands begin to move more or less rapidly [5,60], barrier treatments, especially with low dosage, may be very effective. Besides, the developmental stages of hoppers are also important, because one can use low dosage of an insecticide against young hoppers [16,60,61], but such hoppers usually move slowly [5,60]. This means that we should take into consideration not only pest abundance, situations with biodiversity, and management costs but also general conditions of ecological systems and local population statuses.

### 4.5. Treatments: Can We Preserve Local Populations of Rare Orthoptera or Not?

Steppes and other grasslands are ecosystems where both pest acridids and rare Orthoptera are distributed [62–65]. This means there is a clash between approaches to manage pest populations (to monitor, forecast and control their outbreaks) and to preserve rare forms and their populations. In the steppes of the south-eastern part of West Siberian Plain, some rare species may occur in the same habitats and for the same time as the Italian locust, especially its bands [20,45,62]. Thus, acridicide treatments against the bands could result in damage or full elimination of local populations of rare Orthoptera, such as *S. pedo*, *M. pusilla* or *A. baliolus*. However, our observations show that the harmful effects of acridicides on rare steppe species of Orthoptera may be relatively weak (cf. Section 3.6), when treatments are localized in space, i.e., do not cover all area of a habitat, e.g., the RAATs type or even simple variants of barrier applications.

## 5. Conclusions

The Italian locust is characterized by populations, which are widely distributed across its range and through quite different types of grasslands. In the dry steppes and especially in the semi-deserts, it may colonize all or almost all applicable habitats and may be abundant, while in the forest-steppes and the northern and typical steppes, between outbreaks, its abundance is commonly low or extremely low, and often surveyors may observe very few specimens during several hours of observations. Its local populations often respond differently to climatic fluctuations and changes of human activity. In the steppes, hopper bands often move very slowly, or they stay in one place during several days or even weeks, while adults prefer very short local flights. Besides, the Italian locust often colonize the same grasslands as rare orthopteran species. This is why we cannot use many of the ideas, approaches, and technologies suggested for the desert and migratory locust to monitor, supervise, and control populations of *C. italicus*.

Recently we suggested to change considerably the strategy and tactics to avoid the Italian locust outbreaks [66]:

(1) Crucial parts of the range, habitats, and time lapses should be determined for the species across all species range, each region, and landscape.

(2) New approaches have to be elaborated to manage populations on the landscape scale and to treat agricultural fields and rangelands.

(3) Agricultural technologies per se ought to be modified significantly. For instance, in grasslands, overgrazing should be minimized, and restoration of abandoned fields that commonly harbor *C. italicus* should be accelerated.

(4) Information technologies, especially associated with big data storage and analysis, ecologo-geographic modeling, global information systems, and remote sensing, should become the main basis for monitoring, supervising and forecasting (see also [67–69]).
(5) New approaches should be very important for field assessments of the Italian locust populations as well. For instance, real time observations by using unmanned aerial vehicles are very hopeful.

Besides, one should consider that the Italian locust is the member of grasshoppers'
group (Acridoidea), and these insects are common inhabitants of all or almost all grass-
lands. They often considered as one of the most important consumers in steppes, prairies,
savannas, semi-deserts, and even deserts [70–72]. Moreover, grasshoppers may enhance
net primary production over years [73]. In the dry steppes and the semi-deserts, even
between outbreaks, the Italian locust may consume significant part of aboveground vegeta-
tion, to damage growing points of sagebrushes and to accelerate their growth [36]. During
outbreaks the species can also change considerably fluxes of some chemical elements in the
steppe ecosystems [74]. One may also hypothesize that the Italian locust can also interact
with other species of Orthoptera in ecosystems, and some variations in its populations
should result in changes of orthopteran assemblages and populations, including colonies of
rare species. In any case, attempts to control the Italian locust populations affect colonies of
other species, either positively or negatively. This means we should alter widely distributed
common management approaches to the holistic ones arising not only from exploration of
species populations or their assemblages but also from investigations of ecosystemsper se
and their changes in space and time.

**Funding:** These studies were financially supported by the joint programme of the Russian Foundation for Basic Researches and the Government of Novosibirsk Region (18-416-540001 and 20-416-540004) and also by the Federal Fundamental Scientific Research Programme (FWGS-2021-0002).

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

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** I thank all my colleagues and students (especially O. Denisova, O. Efremova, O. Ermolaeva, K. Popova, and I. Vanjkova) for their valuable help during collecting field data. I am also indebted to all companions during our numerous field trips. I wish to express special thanks to the late L.L. Mistshenko and the late I.V. Stebaev for their advices and cooperation and to L.B. Pshenitsyna for indentification of plant species. Finally, to the late V.I. Strizhak, K.K. Musinov, N.I. Vastshenko, and A.N. Shedenko, I am indebted for helping us with organization of experimental treatments in 2000 and 2001. I also thank two anonymous reviewers for their valuable comments and proposals.

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

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<figure><img src="image_71.png" /></figure>
Review

# Locust and Grasshopper Outbreaks in the Near East: Review under Global Warming Context

Battal Çiplak

Department of Biology, Faculty of Science, Akdeniz University, 07058 Antalya, Turkey; ciplak@akdeniz.edu.tr

**Abstract:** Plagues of locust possibly date back to before humanity, as they evolved before humans. Following the Neolithic revolution and the permanent settlement of humans in Mesopotamia, locusts and grasshoppers have become a serious problem for people, as imprinted on archaeological remains. In the Near East, desert locust may be an important problem during invasion periods, in addition to various local species of locusts and grasshoppers. Past plagues caused serious disasters in the region, but there has been a pause since the 1960s, thanks to more effective monitoring and control. However, global warming and other anthropogenic activities change ecosystems, and these increase the potential for locust outbreaks, upsurges and plagues for the region. Outbreaks of some local species could also be a serious problem. Pest species of the locust and grasshopper of the Near East mainly belong to Caelifera and some to Ensifera. Global warming and extended agricultural activities can increase the potential for outbreaks of local species and create suitable conditions for desert locust invasions. This review is an attempt to (i) provide a historical background for locust invasions/outbreaks in the Near East, (ii) assess the potential for outbreaking of local species and (iii) define a perspective for future actions regarding global changes.

**Keywords:** locust swarms; Near East; Mesopotamia; swarming potential of resident species; *Schistocerca greraria*; *Dociostaurus maroccanus*

**Citation:** Çiplak, B. Locust and Grasshopper Outbreaks in the Near East: Review under Global Warming Context. *Agronomy* **2021**, *11*, 111. https://doi.org/10.3390/agronomy11010111

Received: 3 December 2020

Accepted: 5 January 2021

Published: 8 January 2021

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

<figure><img src="image_72.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/).

## 1. Introduction

Phylogenetically, the origin of the desert locust, *Schistocerca gregaria* Forskål, dates back to around eight million years ago [1], but that of humans as the genus *Homo* to date back to 2.5 million years and modern human *Homo sapiens* to about 200 thousand years [2]. As desert locust and *Homo sapiens* are both native to Africa, we can speculate that modern humans evolved under the selection pressures of the disasters caused by the desert locust plagues. Whether or not *Homo sapiens* has managed to adapt to this selection pressure is a provocative question, but the available data points to the side of “no”. For instance, in recorded history, there are indications of a locust problem in Assyrians and New Testament of the Bible [3–5]. All these histories come from the Middle East and this study aims to present a review of the locust problem in a part of this region, starting from Sinai in the south, extending as far as to the Caucasus in the north, to the Aegean Sea in the west and Zagros Mountain range in the east (Figure 1). The southern part of the Arabian Peninsula is left out because this region is within the recession area of the desert locust and has already received considerable interests from locust experts (for a review see [6]). Comparing to North Africa and Southern part of the Arabian Peninsula, the locust and grasshopper problem in the Near East has other peculiarities, and thus requires a separate evaluation. In this region, the desert locust plagues have been relatively rare. The area is outside recession range of the species and is only contaminated during significant plague periods [7]. In addition, there have been no desert locust swarms in the region since 1960s. However, there are other outbreaking species, such as *Dociostaurus maroccanus* (Thunberg), *Locusta migratoria* Linnaeus and some species of *Calliptamus* Serville. Moreover, there have been occasionally and locally outbreaking species, such as *Heteracris pterosthica* (Fischer
de Waldheim), *Notostaurus anatolicus* (Krauss) and *Arcyptera labiata* (Brulle), especially in Anatolia, and an assessment of their potential in the context of global warming seems of particular importance. Some species of Barbististini—*Isophya* Brunner von Wattenwyl, *Poecilimon* Fischer and *Phonochorion* Uvarov—will also be considered, although none of these long-horned Orthoptera could be considered a locust and there is no significant report on their outbreaks. The review will begin by summarizing the locust problem in the previous century, especially before the 1960s. In the second section, common and locally outbreaking species as well as their management will be considered, especially in Anatolia and Mesopotamia. Finally, an assessment of the possible impact of global warming and other anthropogenic activities on the locust and grasshopper problem will be discussed. The conclusion aims to provide a management perspective.

<figure><img src="image_73.png" /><figcaption>**Figure 1.** The geographic area considered in this review.</figcaption></figure>

## 2. History of the Locust and Grasshopper Problem in the Near East—First Half of the 20th Century

Considering the Near East (Figure 1), publications on locust plagues in the 20th century can easily be assembled into two groups according to their dates. Publications included in the first group are rarely after 1960 [8–18] and if so, they review plague events of the past [19]. Rainey et al. [20] clearly defines ending of a period as no plagues reached to this
region after 1962. A new period of the studies begins after 2000, although the publications by orthopterists or locust experts are scant among them (e.g., 6). The new period is mainly characterized by publications of historians [21–32], also dealing with locust invasions of the first half of the 20th century. They combine information from archives of governments and old newspapers and provide a significant amount of knowledge about the history of locust invasions in the Near East. For example, thanks to these publications, we discovered the acceptance of a special law for locust control by the Ottoman Parliament in 1912, which seems to be a unique event in this regard [28,29]. The law consists of nine articles. The first article defines responsibilities of local peoples in monitoring their district and informing the local governmental officers and regulate awarding of peoples who supply accurate information. The second article defines how to treat the areas contaminated with eggs and hoppers. The third article lists responsibilities of persons in a hierarchical way in destroying the eggs or hoppers. Later, six articles define the rules for offices and staffs of the government, the budget to be provided and its usage. This law was updated in subsequent years by Parliaments of Ottoman and Turkish Republic. Almost all of these publications report or discuss the plagues caused by two species—*S. gregaria* and *D. maroccanus*—indicating they were main locust pests in this area, and these will mainly be considered below. Damage to agriculture by other species such as *Calliptamus italicus* (Linnaeus) (or other species of the genus), *Gryllus campestris* Linnaeus, *Platycleis intermedia* (Serville), *Platycleis affinis* Fieber and *H. pterosthica* are negligible [14,16,29].

### 3. Desert Locust Plagues in the Near East

The range of the desert locust is variable depending on plague period. Regarding the present recession area [7], the desert locust range is between latitudes 10° N–35° N and longitudes 15° W–72° E, mainly associated with the Sahara Desert in North Africa, the Arabian Desert in the Arabian Peninsula and the Thar Desert in Pakistan/India. However, the extent of the range can double during periods of invasion. The Near East remains outside the recession area and constitutes a marginal part of the of invasion area [6,7,33]. The history of desert locust plagues during the last two centuries was summarized in Table 1 and the maximum northward extension of the invasions during the 20th century was shown in Figure 2. The extent of the past plagues in the Near East depended on some other peculiarities such as the severity of the plague, rain regime and the control efforts. Several desert locust plagues were reported for the period before the First World War (Table 1) [19,23,33], in particular for Mesopotamia and the Levant. Although data on the severity and extent of plagues are limited and mainly concern human aspects due to the destruction of food resources and control management by the Ottoman Government [12,22,31], they allows us to estimate that at least the Levantine and the Mesopotamian regions have been invaded on several occasions. According to reports, possibly the greatest plague occurred during First World War and its peak was in 1915 and ended in 1917. As controlling actions were primitive and ineffective, such as destroying the locusts by hand (Figure 3); its consequences were catastrophic. It resulted in a great famine, which was considered one of the greatest tragedies in the region, with the death toll attributed to it estimated at around 500,000 in 1918 [15,24,29–31]. Existing records, based on certain governmental documents, indicate that there was also a significant control effort (see [12,23,29,31] and references therein), but not sufficient to prevent a disaster. During these years, a local reproduction regularly took place, particularly in the Levant and Mesopotamia, leading to successive outbreaks and increasing the impact of the plague.
<table><caption>**Table 1.** History of *Schistocerca gregaria* plagues in the last two centuries (those in the 20th century are shown in Figure 2).</caption><thead><tr><td>Year/Period</td><td>Invasion Area in Near East</td><td>Reference</td></tr></thead><tbody><tr><td>1729</td><td>Aleppo</td><td>[22,32]</td></tr><tr><td>1865</td><td>Levant (from Sinai to Turkey), including Cyprus</td><td>[19]</td></tr><tr><td>1878</td><td>Sinai, Palestine, Syria (Levant)</td><td>[19]</td></tr><tr><td>1890</td><td>Sinai, Palestine, Syria (Levant)</td><td>[19]</td></tr><tr><td>1902</td><td>Sinai, Palestine, Syria (Levant)</td><td>[19]</td></tr><tr><td>1911–1915</td><td>Arabian Peninsula plus Mesopotamia (Syria, Lebanon, Iraq and Turkey) up to Southern Caucasian Plateau</td><td>[8,12,15,19,24,29,31]</td></tr><tr><td>1928–1930</td><td>Arabian Peninsula plus Mesopotamia (Syria, Lebanon, Iraq and Turkey) up to Southern Caucasian Plateau</td><td>[8,19,29]</td></tr><tr><td>1945</td><td>Arabian Peninsula plus Mesopotamia (Syria, Lebanon, Iraq and Turkey) up to Southern Caucasian Plateau</td><td>[8,19]</td></tr><tr><td>1952</td><td>Arabian Peninsula and a very small part of the Mesopotamian Turkey</td><td>[8,19]</td></tr><tr><td>1953</td><td>Arabian Peninsula and large parts of the East plus South East Turkey</td><td>[8,19]</td></tr><tr><td>1958</td><td>Arabian Peninsula and large parts of the East plus South Turkey</td><td>[19]</td></tr><tr><td>1959</td><td>Arabian Peninsula plus a small part of Mesopotamian Turkey</td><td>[19]</td></tr><tr><td>1960</td><td>Arabian Peninsula plus a small part of Mesopotamian Turkey</td><td>[19]</td></tr><tr><td>1962</td><td>Arabian Peninsula plus Mesopotamian Turkey</td><td>[19]</td></tr></tbody></table>

<figure><img src="image_74.png" /><figcaption>**Figure 2.** Northern invasion borders of *Schistocerca gregaria* plagues in the 20th century in the Near East (figure prepared using data by Balamir [19]).</figcaption></figure>
<figure><img src="image_75.png" /><figcaption>**Figure 3.** Locust destruction by sticks at hand in Palestine (from the newspaper *Serveti Fünun*, 269, 1896, page 140).</figcaption></figure>

Balamir [19] presented an extensive review of desert locust invasions in the Near East after the First World War, including extent, control activities and consequences of the invasions. Eight different plagues have been reported in the years 1930, 1945, 1952, 1953, 1958, 1959, 1960 and 1962 (Table 1). The size of these invasions and their northern boundaries were variable (Figure 2). The plagues extended to northern Syria and Iraq, but not to Turkey (or only into a small part), in 1952, 1959 and 1960. In 1962, the plagues invaded the Mesopotamian lowlands of Turkey, as well as, further south, the Levant, Jordan and Iraq. In the remaining years, plagues reached to mountain belts in the northern Mesopotamia. The two most extensive plagues were those of 1930 and 1958, and the invasion margin reached the Caucasus Plateau in north-eastern Turkey. Various preventive actions were taken. The use of sheet metal dams (made of zinc plates) for the management of hopper bands was the main control method. Hoppers were channeled into ditches and then crushed, burned or buried. For example, a total of 67,690,000 kg and 603,142,000 kg nymphs were destroyed in Turkey by this method during the 1930 and 1958 plagues, respectively [19]. Spraying insecticide (mainly the gamma-hexachlorocyclohexane preparations) by air became a dominant method after mid of the 20th century. Great success was achieved by this method and none of the 20 swarms of 1960 succeeded in laying eggs in Turkey [19]. Other control methods implemented in the past were ploughing egg-laying sites, collecting nymphs and adults by hand or spraying liquid soap or some other chemicals, such as arsenic [19,29,32,33].

There are no records of desert locust swarms in the Near East after the years mentioned above, which corresponds to the general trend in other parts of the invasion area [20]. This is possibly the reason why the countries in the region have halted governmental units for locust control or not established new ones [6]. Why did such a period of successive plagues, observed since at least the last quarter of the 19th century, end in the last half of the 20th century? In fact, after 1965, effective control activities, mainly in Africa and southern Arabia—efficient survey and timely response in desert locust breeding areas— appear to be the main reasons for this improvement and the absence of swarms in the Near East [7,20,34–39]. This is also applicable for the peripheral invasion areas, as using spraying aircrafts after 1950 prevented the spread of the swarms to the borders of Caucasus.
Although, in recent years, some swarms entered in the Near East, none of them were able to become harmful.

4. Moroccan Locust Plagues in the Near East

Considering the Near East, one of the most harmful locust species was the Moroccan locusts. This species seems to have recently lost its economic importance to the point that conservation measures have been suggested only for certain localities [40]. However, it was a serious problem for the Near East in the first half of the 20th century, especially important in West Anatolia and moderate highlands of Mesopotamia, including south-eastern Turkey and the northern regions of Iraq and Syria for around a hundred-year period. Several very harmful plagues of this species have been reported in the Near East during the period of 1847–1945 [12,18,25,29,31] (Table 2). Although there are no reliable reports for more archaic time, this locust species may have been a serious problem at all times in the Near East. West Anatolia, Mesopotamia and Southern Caucasus also were three important outbreak areas for this species (Figure 4). The outbreak periods were mostly different, although sometimes overlapping, from one region to another.

Seven plague periods have been reported in West Anatolia for a century, from the mid-19th century to the mid-20th century. Each plague lasted for 2 to 7 years. The plague extent varied from a few km² to the whole West Anatolia, from the Marmara Sea to the Mediterranean Sea, excluding narrow coastal areas. Some plagues also spread to the European part of Turkey. The three plagues of the second half of the 19th century—1847–1851, 1852–1864 (especially in 1861) and 1875–1881—invaded large parts of West Anatolia [25,29]. The plague in 1904–1905 was restricted to the eastern parts of the Manisa and Uşak provinces of Turkey and possibly played a significant role in the development of the next one, which lasted for about seven years from 1910 to 1917. It was possibly the largest in terms of extent and impact. The upsurge period started in 1909–1910 in Eşme and Kula, then reached its peak in 1916 and declined in 1917. All these stages were well monitored and documented [12,19]. As the Moroccan locust was a persistent problem for West Anatolia, Uvarov [18] was invited to study this species in the region; he considered the 1910–1917 plague as a reference with which to define the bio-ecology of the Moroccan locust. In addition, a considerable effort had been devoted to the prevention of future plagues [12]. Karabağ [16] reported that 125,000,000 kg nymphs and 12,500,000 kg egg pods were destroyed during the period of 1915–1917. Although it was largely controlled in West Anatolia, local swarms in the Marmara region, including parts of Thrace in 1919, were likely the aftershock of this plague period. For the aforementioned reasons, studies on this plague constitute a reference for understanding the upsurges characteristics of species in relation to ecology and for developing effective control strategies. These experiences have provided significant knowledge for the prevention of subsequent plagues. The later plagues, in 1930–1932 and 1939–1941, were also widespread and invaded large parts of West Anatolia up to Marmara Sea in the north, the Konya province-central Anatolia in the east and the north of Antalya in the south. However, both were controlled within one or two years and their damage was limited. Later, especially after 1962, only a few local swarms occurred and these were successfully controlled.

Mesopotamia (Syria, Iraq and Turkey) was another outbreak area for the Moroccan locust in the Near East (Figure 4). There are no data regarding plagues of this species for earlier periods; however, four plague periods are well known in first half of 20th century [12,13,29]. Those in 1919 and 1945 were one-year plagues affecting a restricted part of Mesopotamia. The two others, in 1931–1932 and 1939–1941, lasted at least two years each and invaded larger areas in the region. In addition, the plague of 1925 in Iraq was reported to cause serious damage [40]. The South Caucasus lowlands in the Basins Aras and Kura rivers appear to be a separate outbreak area, and the plague of 1920–1921 in Armenia and Azerbaijan caused significant damage to the region [29,40].
<table><caption>**Table 2.** History of *Dociostaurus moroccanus* plagues in the last two centuries (those in the first half the 20th century are shown in Figure 4).</caption><thead><tr><td>Year/Period</td><td>Invasion Area</td><td>Reference</td></tr></thead><tbody><tr><td>1830</td><td>West Anatolia, local swarms</td><td>[25,29]</td></tr><tr><td>1847–1851</td><td>Aegean Region and south Marmara</td><td>[25]</td></tr><tr><td>1852–1864 (peak in 1861)</td><td>Large parts of West Anatolia</td><td>[25,29]</td></tr><tr><td>1875–1881</td><td>Antalya, Inner part of Aegean Region up to Balıkesir Province</td><td>[29,31]</td></tr><tr><td>1904–1905</td><td>Manisa (inner parts) and Uşak provinces</td><td>[25,29,31]</td></tr><tr><td>1909</td><td>Local swarm in Eşme in Manisa Province</td><td>[18,29,31]</td></tr><tr><td>1910–1911</td><td>Swarms in Manisa province (Eşme, Kula, Demirci, Alaşehir)</td><td>[13,18,29]</td></tr><tr><td>1911–1912</td><td>West Anatolia (Denizli, Manisa, Aydın and İzmir provinces)</td><td>[13,18,29]</td></tr><tr><td>1915–1916, declined in 1917</td><td>Large parts of western Anatolia up to Antalya and Konya provinces</td><td>[13,18,29]</td></tr><tr><td>1919</td><td>Marmara Regions of Turkey</td><td>[13,18,29]</td></tr><tr><td>1919</td><td>A restricted part of Mesopotamian Turkey, Iraq and Syria</td><td>[29]</td></tr><tr><td>1920–1921</td><td>Armenia and Azerbaijan</td><td>[40]</td></tr><tr><td>1930–1932</td><td>Large parts of West Anatolia including Marmara Basin plus Konya province in Central Anatolia</td><td></td></tr><tr><td>1931–32</td><td>Mesopotamian Turkey (from Siirt to Mersin), Iraq and Syria</td><td>[13,29]</td></tr><tr><td>1934–1938</td><td>Local swarms in several location especially in West Anatolia</td><td>[13,29]</td></tr><tr><td>1939–1941</td><td>Aegean and Southern Marmara regions, and local swarms in Mesopotamian Turkey, Iraq and Syria</td><td>[13,29]</td></tr><tr><td>1945</td><td>A restricted part of Mesopotamian Turkey and Syria</td><td>[29]</td></tr></tbody></table>

<figure><img src="image_76.png" /><figcaption>**Figure 4.** Outbreak areas of *Dociostaurus moroccanus* in the Near East: West Anatolia, Mesopotamia and Caucasus. Development of the most intense plague during 1909–1917 in West Anatolia is outlined by years. The borders for 1917–1918 also define the West Anatolian outbreak area. Figure is based on data mainly provided by Bücher [12] and Uvarov [18]).</figcaption></figure>

The Moroccan locust plagues in the Near East exhibit some peculiarities. It seems that they are several independent outbreak areas and these can be classified as West Anatolia, Mesopotamia and the Caucasus (see Figure 4) [12,18,40]. In West Anatolia, the plains of the Inner Aegean Basin, especially those in Manisa, Uşak and the surrounding parts of the neighboring provinces of Denizli and Aydın, were the main outbreak areas.
Swarms that originated in these regions spread in subsequent years and extended to the surrounding parts of Aegean, Marmara, the Mediterranean and central Anatolia (Figure 4). The Mesopotamian outbreak area may include two places of origin: one in northern Syria and the other in northern Iraq. Uvarov [18] stated that the outbreak area of this species in West Anatolia exhibits special environmental conditions: (i) it is restricted to altitudes of 400–1000 m, (ii) it has a certain precipitation regime and (iii) it harbors a well-defined vegetation (the presence of *Plantago* spp. and *Hordeum* spp. is of particular importance). The determinative aspects of these environmental conditions have been reported from other parts of the species range [40]. This combination of factors restricts the species to parts of West Anatolia, but arising upsurges can invade the surrounding parts of the regions in Anatolia.

The Moroccan locust does not occur in Euro-Siberian vegetation along the Black Sea Basin up to the Great Caucasus. The average elevation of central Anatolia is around 1000 m and that of eastern Anatolia is around 1500 m [41], and these heights possibly prevent the species from colonizing these areas. Consistent with this viewpoint, no swarm or outbreak areas have been reported from central and eastern Anatolia, although the solitary form has been recorded frequently [9,42,43]. For similar reasons, the south-eastern Taurus Mountains and the Syrian Desert constitute the northern and southern borders of the Moroccan locust outbreak area in Mesopotamia, respectively. Thus, this outbreak area of the Moroccan locust in this region constitutes an arc starting from Mediterranean Syria and extending to Zagros. The differences between the West Anatolian and Mesopotamian outbreak areas are mainly altitudinal, with altitudes of 400–1000 m and 200–400 m, respectively [14,18], indicating that the latter outbreak area is less suitable. This is possibly the reason why the Moroccan locust plagues in this region were less severe than those in West Anatolia.

The moderate highlands of the inter-montane basins of the Aras and Kura rivers in southern Caucasus were the third important outbreak area in the Near East (Figure 4). Past reports indicate that this is a less significant outbreak area compared to the two others. It should be noted that these three outbreak areas are independent: no swarms in one area spread to another. The periodic overlap of some past plagues of these three distinct areas needs an explanation, but periodic climate changes lasting several years may be the main reason.

An issue worth highlighting is that there has been a pause in the Moroccan locust plagues since the mid-20th century. Although there have been a few local swarms ([44,45]; N. Babaroğlu—personal communication), none of them were invasive and they were controlled in their local outbreak area. This pause may be the result of a combination of several factors. The bio-ecology of the species is surely one of them, as indicated by Uvarov [18] and Latchininsky [40]. The reasons for the pause may be different for West Anatolia, Mesopotamia and the Caucasus. However, the topographic and ecological heterogeneity of the biogeographic Anatolia (see [41]) offers opportunities for the species to compensate for environmental changes. The most plausible reason for the pause seems to be the intense control of swarms in the outbreak areas, preventing upsurges in subsequent years. The swarm in 1996 in Eynif Plain in Akseki (Antalya, Turkey) was controlled by the application of 40,000 kg of insecticide [44,45]. Several similar local swarms occurred in the Aegean part of Turkey (A. Yüzbaş and N. Babaroğlu—personal communication), but none of them succeeded in invading other areas in the following years. This also indicates that control in the outbreak areas is the key reason for preventing long-lasting plagues.

**5. Other Pest Orthopteran Species**

The desert locust and the Moroccan locusts were the two most important agricultural pests in the Near East in 20th century. However, limiting to these two species seems insufficient for the region, especially for Anatolia. Although their characteristics are different from these two species, many other orthopteran pests have been reported in past studies [10,11,14,16,46–48]. We can cite some Acrididae species, such as *L. migratoria*, *Calliptamus* spp. (namely *C. italicus*, *C. barbarus* (Costa) and *C. tenuicercis* (Tarbinsky)), *H. pterosticha* (Costa).
and *Arcyptera labiata*; Ensifera species, such as *Melanogryllus desertus* (Pallas) and *P. intermedia*; and some species of *Poecilimon*, *Isophya* and *Phonochorion* (without certain specific identification). Of all these species, *L. migratoria* and *C. italicus* were the most important, corresponding to Uvarov's definition of locust [17] and requiring control measures [14,48].

The author himself observed many local swarms of orthopteran species during his field studies since 1990 across Anatolia. As mentioned above, the swarm of *D. maroccanus* in 1996 in the Eynif Plain (near Antalya) was observed from the merging of dense patches of hoppers into larger bands and then into migrating adults. Swarms of other species were also observed, but their swarming characteristics were different from typical locusts. These species present a great taxonomical variety, but mainly belong to Acrididae and Phaneropterinae. Among Acrididae, *L. migratoria*, *C. italicus*, *C. barbarus*, *C. tenuicercis* and *H. pterosticha* are the species reported in previous publications. *N. anatolicus* (Krauss), which coexists mainly with *Calliptamus* spp., is another species to be added to this list. *L. migratoria* is the model species on which Uvarov [17] based his phase theory. Local swarms of the species have been reported ([10]; N. Babaroğlu—personal communication) and control measures have been applied locally by the Turkish Ministry of Agriculture (by central and local plant protection institutions). *L. migratoria* is common in its solitary form and can pullulate in paddy fields, but there is no record of invasive plagues extended to other places. *H. pterosticha* occurs in humid plains irrigated by humans below 1000 m elevation. For example, its population showed a significant increase in 1961–1962 in Diyarbakır and was prevented by the application of chemical insecticide [11]. The author observed a similar case in the province of Malatya in Mesopotamian Turkey. The population density gradually increased in 2017–2020 in the plain part of the province. The increase in population density caused significant damage on crops and fruit trees. Apricot cultivation is the main agricultural activity in the region and these grasshoppers climb to apricot trees and consume both leaves and fruits, as complained about by farmers. This case should be monitored in the coming years. *Calliptamus* spp. and *N. anatolicus* can reach high densities, especially in arid agricultural fields in Central Anatolia, Mesopotamia and some plains of eastern Anatolia. The damage caused by *Calliptamus* spp., especially *C. italicus*, and insecticide application to manage their populations is known for a long time [48]. Although Tutkun ([48]; see also [29,31]) states that the species is the third most harmful locust species in the area, there has been no recent report of outbreaks or preventive control measures. However, monitoring seems to be a necessity.

The case of the phaneropterid species is more interesting. Highly dense populations of *Poecilimon* spp. and *Isophya* spp. have been reported in previous publications [47] or observed by the author himself. Only the two most striking cases are mentioned here. *Isophya hakkarica* Karabağ, whose range covers the south-eastern Taurus and the Anatolian Diagonal [49], reached to very high population densities in the Malatya, Elazığ and Adıyaman provinces of Turkey in 2016. Rural people asked the local government to control the pest as it caused extensive damage to pasture and destroyed animal feed. Residents observed that the increase in population density began in 2015 and peaked in 2016. Local governmental agencies provided partridges to be release into the wild to try to control the pest, but no insecticide was applied. A similar case has been observed with *Poecilimon celebi* Karabag in the Kastamonu province. During a field study in 2012, an extremely dense population was observed in the forest clearing areas with Euro-Siberian steppe vegetation (Figure 5). Locals complained about the destruction of fields and meadows where animal feed was produced. Many other similar cases with species belonging to *Poecilimon*, *Ispohya* and *Phonochorion* (all from Barbitistini) have been observed, especially in northern Anatolia along the Black Sea Basin and the highlands of the eastern Anatolia with a high grassland vegetation. The conclusion is that several Barbitistini species may reach high population densities, cause significant damage and require various control measures.
<figure><img src="image_77.png" /><figcaption>**Figure 5.** Collecting specimens of *Poecilimon celebi* in an outbreak area in North Anatolia.</figcaption></figure>

The reports on the locust and grasshopper management from the Agriculture Ministry of Turkey since the second half of the 20th century, as well as the author's observations during last 30 years, allow us to make some general statements that could guide future plans and actions. Among the previously mentioned species, both *S. gregaria* and *D. moroccanus* show locust characteristics with phase polyphenism (shift from solitary to gregarious phase according to population density), as defined by Uvarov [18,50], and can invade new areas by migrating from the outbreak areas where the initial increase in density occurs. *L. migratoria* and *Calliptamus* spp. (specifically, *C. italicus*, *C. barbarus* and *C. tenuicercis*) were also reported as locusts; however, in previous Near East studies or reports, no specific phase changes or long-distance migration leading to invasions of new areas were observed. Instead, they were reported to be harmful only by reaching high densities in their regular distribution range (N. Babaroğlu—personal communications). This statement is undoubtedly valid for the other acridid species: *A. labiata*, *H. pterosticha* and *N. anatolicus*.

The case of long-horned species requires a distinct assessment. All the long-horned or
ensiferan species mentioned above have a limited range or are endemic to a specific location.
In addition, they are short-winged and lack the ability to migrate. They can exhibit various
pigmentation forms, such as green or black as in some *Isophya* and *Phonochorion*, or green
and yellow/brown as in some species of *Poecilimon* [51], but these colors do not indicate
phase polyphenism due to population density. Although they may pullulate and cause
significant damage locally, their outbreaks are only local and population density increases
within their regular range. This does not mean that they do not require monitoring and
control measures. Several species of Barbitistini and, in addition, some other tettigoniids
species can reach unexpectedly high population densities in their local range depending on
annual environmental conditions, which may possibly require survey and control measures
if a density threshold is exceeded.

**6. Locust and Grasshopper Management in Turkey in Recent Years**

Locust and grasshopper management activities in Turkey are organized under the authority of the Directorate of Plant Protection Central Research Institute (DPPCRI) a branch of the Ministry of Agriculture and Forestry (N. Babaroğlu, M. Çulcu and E. Akci from DPPCRI—personal communication). The main management activity is applying
insecticide over outbreak areas. Releasing partridges is an uncommon practice; there is no report on the efficiency of this method. For the period of 2013–2020, the control of grasshopper outbreaks required, yearly, on average, an application of insecticides of over 55 km², in several locations, throughout 81 provinces of Turkey (Figure 6). During the period of 2013–2020, in some provinces, insecticide application has only been conducted in one year, while in some other provinces it has been conducted in two, three or more years. These data have some specific indications for the recent condition for outbreaks in Turkey. Although the grasshopper species are not generally identified and non-locust species are possible, most of the insecticide applications for the period of 2013–2020 are located in the Moroccan locust outbreak areas, i.e., in West Anatolia and Mesopotamian Turkey. This can be considered as an indication of the potential danger of the Moroccan locust for present and the future. Insecticide application in other areas is rare, just in restricted locations and only for one or two years, for the period 2013–2020. Rare application areas are mostly scattered along the one-third of Anatolia, in northern part. From previous publications and personal observation during the last 30 years, we assume that the species outbreaks in these districts are non-locust species mentioned above. In particular, the release of partridges in the provinces of Çorum and Kastamonu in northern Anatolia is consistent with this assumption. Comparison of these recent control activities with earlier records indicates that the potential of outbreak by resident species has increased and may increase further under global warming (see below). Overall, the data indicate that the outbreak potential of the non-locust species requires special attention.

<figure><img src="image_78.png" /><figcaption>**Figure 6.** Insecticide application by the Directorate of Plant Protection Central Research Institute (DPPCRI) during the period of 2013–2020 throughout Turkey, indicated by the number of years (open circle application in ≤2 years, square in 3 years and triangle in ≥4 years).</figcaption></figure>

**7. Climate Change and Its Possible Impacts on Locust/Grasshopper Problem in the Near East**

Global changes/warming directly or indirectly affect locust and grasshopper species [52–57]. The direct effects are those related to the auto-ecology (e.g., specific thermal thresholds for their development) and therefore to phenology, including changes in life history traits such as the hatching time, instar durations, adult emerging time, reproduction period, egg lying time and number of annual generations [53,54,58,59]. Such phenological changes depend on the resilience and adaptive capacity of the species [54,58–61]. The indirect effects of global warming on insect species are represented by changes in habitat as well as changes in food preferences. Changes in habitat characteristics can be particularly
serious for phytophagous insects, as their presence is correlated with plant communi-
ties [53,54]. Locusts, generally phytophagous, may have some preference for a limited
plant spectrum or may preferentially feed on some certain plant species. For example,
Uvarov [18] reported that *Plantago* spp. and *Hordeum* spp. were determining plants for the
presence of the Moroccan locust in western Anatolia. Thus, global warming will produce
new conditions for locusts and grasshoppers and adaptation to the new conditions will
require high resilience and/or adaptive plasticity, especially for the locally outbreaking
species [41,54–57].

Depending on the adaptive capacity of a species, three main consequences may be
expected: (i) change of ecological niche/habitat or phenology, (ii) dispersal to new areas
with conditions similar to those of the original habitats (range shift) and (iii) extinction, if
there is no capacity to adapt to the new conditions and/or to disperse into new areas [52–57].
A change in ecology/phenology of the pest orthopteran species is very likely. If their
long-term adaptations provide the capacity for a broad ecological tolerance, they can
overcome altered environmental conditions and continue to live in their regular range and
outbreak if they meet favorable conditions. In the case of outbreaking species, one issue
to be considered in the context of phenological changes is the number of generations per
year. The lengthening of the warm period, a consequence of global warming [62,63], can
lead to an increase in the number of generations. Shifting their ranges either diffusely over
several generations or migrating long distances within a generation can be expected when
the previous habitat becomes unavailable [41] or newly available areas appeared [57,61,63].
Regarding outbreaking and invasive locusts, the new conditions produced by global
warming may also mean an increase in the available area to be invaded, in addition to their
regular ranges [56,57]. Extinction or even range size reduction is less likely for common
locusts but may be probable for locally outbreaking non-locust orthopteran. On the other
hand, the severity or impacts of global warming/changes are expected to be different
depending on geographic location [60,64]. The Mediterranean in general and the Near
East in particular are among the places experiencing a high rate of warming [64] and the
possible consequences for the species in this area are likely to be more serious.

The possible impact of global changes/warming on outbreaking species can be as-
sessed according to four criteria: (i) phenological changes, including the number of annual
generations, (ii) habitat/niche change, (iii) range shift and (iv) extinction. Although each
species may be affected differently, a generalization may be possible for the locally outbreak-
ing species, such as those of Barbitistini belonging to *Poecilimon*, *Isophya* and *Phonochrion*.
Unfortunately, studies specifically examining the bio-ecology of the species belonging
to these genera are scarce [51] and do not provide a basis with which to evaluate the
possible impact of global warming for their future. Some speculations can be made from a
phylogeographic point of view regarding the location of their range and habitat preference.
These species are univoltine and this feature seems to be fixed evolutionarily; therefore,
additional generations are unexpected. However, their hatching, nymph and adult periods
may shift to earlier times of year. Outbreaking species of these genera prefer certain vege-
tation, mainly wet grasslands, and their ranges are mostly restricted to certain fragments
in the heterogeneous topography of the Black Sea Basin and of the highlands of East
Anatolia [41,65–67]. Furthermore, they are flightless, with a low dispersal capacity, and
we believe that invasion of new areas by these species is unlikely. On the other hand, they
can vertically shift their range and benefit from the buffer role of altitudinal heterogeneity
to overcome the effect of global warming [68]. This is another reason why extinction is
also unlikely. These species are likely to experience fluctuation in population density from
year to year or at certain years and become harmful when the appropriate combination of
ecological factors is met. Thus, they may require special monitoring and necessary control
measures must be taken in the event of an increase in population density.

A generalization may also be possible for the locally outbreaking acridid species,
i.e., *L. migratoria*, *H. pterosticha*, *N. anatolicus*, *C. italicus*, *C. barbarus*, *C. tenuicercis* and
*A. labiata*. Different than all others, the last species is found in mountainous habitats and
will not be considered. The other species are mainly associated with anthropogenic or
agricultural habitats and prefer a relatively warm climate and moderate altitudes below
1000 m [43]. The first two species are found in humid and irrigated agricultural plains,
while the last four in arid plains or arid habitats contiguous to humid plains. These species
are known to be univoltine. However, our observations on *H. pterosticha* indicate that
it can be multivoltine as nymphs and adults have been observed together at different
periods from June to October. From the perspective of the above four criteria, the following
statements can be made. The probability of extinction is less likely. Range shifting and an
enlargement of the regular range is highly likely as warming provides new opportunities
for these species. An additional generation seems less likely for most of the species, but this
is probable for *L. migratoria* and *H. pterosticha*. *N. anatolicus*, and three species of *Calliptamus*,
namely, *C. italicus*, *C. barbarous* and *C. tenuicercis*, occur in arid and mostly agricultural
areas (48). Publications on locust generally report *C. italicus* as the main pest species in the
genus; the author observed that these three species reach high population densities in the
arid areas adjoining to irrigated plains. Modelling studies [56,57] estimate that *C. italicus*
may benefit from global warming and enlarge its range or become a more serious pest
in West Palearctic. Estimating the same consequences for *C. barbarous*, *C. tenuicercis*, and
*N. anatolicus* will not be an exaggeration as their habitat preferences are quite similar. All
these species may become more serious pests as temperatures and agricultural activities
increase, and control measures may be an unavoidable necessity.

The two most important species showing real locust characteristics are *S. gregaria* and *D. moroccanus* and they should be considered separately. The first species, the desert locust, live in desertic habitats and the above model cannot be applied. Aridification due to global warming is an expectation for the whole region and especially Mesopotamia [62,64] and this can be considered as new opportunities for the desert locust. The Near East is not an outbreak area for this species, not even in its recession area, but it is on the margins of the invasion area. Larger breeding areas may become available for this locust, offering new opportunities to increase its populations in the case of new invasions. In particularly, enlargement of the dry desert-like areas in Central Anatolia requires special attention in the event of a new plague. Additionally, the inter-mountain plains that develop in Mesopotamia and eastern Anatolia also require caution. However, in any case, preventive or proactive control in the outbreak areas (far from Near East) is more important than the regional measures, which can only be considered during plague episodes.

The four criteria given above can be strictly applied to the Moroccan locust, the most
economically important locust species in the region. Uvarov [18], also supported by other
studies [40], constitutes a hallmark background for the bio-ecology of the species, to be
used as a basis for the four criteria given above. This species is univoltine and a change in
this characteristic due to new conditions seems unlikely. However, some climate changes,
such as the lengthening of the warm season, can shorten various stages of the life cycle and
cause earlier outbreaks. Shift of the distribution area is another parameter of our model.
This species occurs in certain altitudes: 400–1000 m altitude in western Anatolia [18] and
200–400 m in Mesopotamia [13]. Thus, dispersing to higher altitudes along the outbreak
areas that are suitable for other conditions is likely. However, species composition of
vegetation constitutes another determinant of the outbreak. Thus, change in vegetation
composition either in outbreak areas or in areas to be invaded further is also important.
In addition, the precipitation regime is another significant factor in the ecology of this
species, so fluctuation in the precipitation regime will be another determinant for the future
outbreaks by the species. However, it should be noted that aridification in the region is an
expectation [64] and this may interplay a role in an outbreak. Together, these conditions
may further delimit the expansion and outbreaking of this species, as has been the case
since the 1960s. As a result, it may become a less important pest, as observed in several
other places [40]. Plagues of the species are possible in the case of upsurges during a few
successive years. Thus, monitoring the species in local outbreak areas, as has been done
during 2013–2020 by the DPPCRI, especially in the cases of random overlapping of the conditions mentioned above, remains the best practice to prevent possible plagues.

**8. Conclusions**

The above assay includes data gathered from studies in various scientific fields ranging from the humanities to phylogeography and such a rich combination indicates that locust plagues are natural events with a high impact on human life. As witnessed in the 20th century in the Levant, Mesopotamia and Anatolia, every society or state has to pay attention to it in order not to pay the price. In the light of past plagues, it can be stated that the two most important and damaging species were true locusts: *S. gregaria* and *D. moroccanus*. For *S. gregaria*, although the Near East does not include any outbreak area and remains just on the margins of the invasion area, societies living in this region have had to endure tremendous suffering and have paid hundred thousand lives. These two species prevailed in the region for nearly 100 years, between the mid-19th and 20th centuries, but large plagues came to a halt from the 1960s. *S. gregaria* is still a serious pest for North Africa and the Southern Arabian Peninsula, as well as in many other regions of its invasion area, but effective control in its outbreak areas [37,69] keeps the Near East apart of the disaster of this species. *D. moroccanus* was probably the most harmful species especially for West Anatolia and Mesopotamia, particularly in the first half of the 20th century. However, effective control in its outbreak areas/plains scattered in West Anatolia and Mesopotamia subsequently prevented large-scale plagues. As for *S. gregaria*, only a few local swarms were encountered after the 1960s. Although they lack the typical locust characteristics and do not swarm in extensive areas, other species pullulate locally and may cause significant damage in crop fields and pastures, especially in Anatolia. This is the case with *L. migratoria*, *C. italicus*, *C. barbarus*, *C. tenuicercis* and *H. pterosthica*, all from Acrididae, which should be closely monitored for early prevention. Outbreak of species belonging to the Ensifera, namely those of Barbitistini, is an event rarely reported. However, these species may cause significant damage to grasslands and require monitoring. Global changes, especially climate warming, can affect these species in various ways, changing the outbreak probability, as well as the course of invasions and migrations. We can assume that most of these species will benefit from these changes to invade new areas, enlarge their range or increase their population sizes, at the disadvantage of humans. Such global changes may present opportunities for the pest species of Acrididae, both in the irrigated and arid agricultural plains of Mesopotamia and Anatolia. Scientific attention on the part of local authorities is essential not to face such disasters as experienced during the First World War.

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

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

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** This review would not have been possible without invitation, encouraging and valuable contributions by Michel Lecoq. Numan Babaroğlu, Mehmet Çulcu and Emre Akci from Directorate of Plant Protection Central Research Institute (Ankara) spent a great time and effort to provide data on grasshopper management for the period 2013–2020. Onur Uluar and Özgül Yahyaoğlu assisted during preparation of the review. Designer Helin Çıplak Palabıyık (helin@wodern.com) prepared the maps. Hasan H. Başıbüyük reviewed the manuscript for linguistic editing. We are grateful to all for their valuable contributions.

**Conflicts of Interest:** The author declares no conflict of interest.
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<figure><img src="image_79.png" /></figure>
Review

# State of the Art Management of the Central American Locust
## *Schistocerca piceifrons piceifrons* (Walker, 1870)

Ludivina Barrientos-Lozano <fnref n="1" />,* [ID], Hojun Song <fnref n="2" /> [ID], Aurora Y. Rocha-Sánchez <fnref n="1" /> and Jorge Ariel Torres-Castillo <fnref n="3" />

**Citation:** Barrientos-Lozano, L.; Song, H.; Rocha-Sánchez, A.Y.; Torres-Castillo, J.A. State of the Art Management of the Central American Locust *Schistocerca piceifrons piceifrons* (Walker, 1870). *Agronomy* **2021**, *11*, 1024. https://doi.org/10.3390/agronomy11061024

Academic Editors: Michel Lecoq and
Arianne Cease

Received: 21 April 2021

Accepted: 18 May 2021

Published: 21 May 2021

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

<figure><img src="image_80.png" /></figure>

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

**Abstract:** The Central American locust (CAL), *Schistocerca piceifrons piceifrons* (Walker, 1870), is a transboundary pest that is distributed from Mexico to Panama. It is a true locust species characterized by density-dependent phase polyphenism. The ancient record of the CAL is found in the Popol Vuh, the Mayan sacred book, demonstrating how it has affected humans for millennia. In Mexico, the CAL have been declared a national threat to agriculture since 1824. Serious locust plagues occurred in 1882–1883 when swarms of 20 km<fnref n="2" /> in size invaded the Yucatán Peninsula and neighboring states in southern Mexico and, since then, management actions to suppress populations and economic damage have been implemented. A better understanding of the biology, ecology, and behavior of the CAL replaced a manual and mechanical collection of locust swarms, hopper bands, and egg pods with modern techniques such as the use of safer chemical products and environmentally friendly bioinsecticides. Presently, biomodels and GIS support the monitoring and forecasting of outbreaks. Currently, studies are conducted to investigate environmental factors that trigger locust gregarization, the evolution of phase polyphenism, and CAL bioactive compounds and nutritional contents, envisioning its potential use in biotechnological industries. Findings will be crucial to improve the management strategies of the CAL.

**Keywords:** locust plagues; ecology; field monitoring; outbreaks management

## 1. Introduction

The Central American locust (CAL), *Schistocerca piceifrons piceifrons* (Walker, 1870), is a menacing pest that has affected humanity for millennia [1]. It is believed that climate changes and recurrent locust plagues could have caused the decline of the Mayan civiliza- tion in Mesoamerica in the period 740–930 A.D. [1–3]. It is a transboundary migratory pest that is distributed throughout Mexico and Central America, affecting at least ten countries during outbreaks [4]. It is a true locust species characterized by density-dependent phase polyphenism [1,4–8]. At low density, individuals are solitary, avoid each other, and are harmless, and this phenotype is called the “solitary phase”; when environmental conditions promote population density increase, they transform into gregarious and conspicuous locusts that can form large migrating groups of nymphs (bands) or adults (swarms), and this phenotype is called the “gregarious phase”. Solitarious locusts differ from gregarious locusts not only in behavior, but also in color, morphology, and physiology [4,7–9]. Locust bands march in compact groups in the same direction and in a cohesive way, while swarms may contain millions of individuals that migrate long distances in a few days, causing severe damage to agriculture and livestock. The phenomenon that triggers polyphenism is not “unknown”, but it must be considered a very complex multifactorial process involving different mechanisms [10].

<footnote n="1">¹ Tecnológico Nacional de México-I. T. Ciudad Victoria. Blvd. Emilio Portes Gil No.1301, C.P. 87010 Cd. Victoria, Tamaulipas, Mexico; auro_3110@hotmail.com</footnote>

<footnote n="2">² Department of Entomology, Texas A&M University, College Station, TX 77843, USA; hsong@tamu.edu</footnote>

<footnote n="3">³ Ciudad Victoria-Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas-Campus, División del Golfo 356, Col. Libertad, C.P. 87019 Cd. Victoria, Tamaulipas, Mexico; jorgearieltorres@hotmail.com</footnote>

<footnote>* Correspondence: ludivinab@yahoo.com</footnote>
Throughout its distribution, permanent reproduction and gregarization areas for the CAL are located at 100 masl or below, which are characterized by optimal climatic conditions (27 °C average annual temperature, and at least 1000 mm annual precipitation) [4,5,9,11,12]. In modern Mexico, the first official report on the CAL plague dates back to 1882-1883 when swarms of 20 km² in size invaded the Yucatán Peninsula and other states of southern Mexico [1-4,7]. Along with its history of massive reproduction and invasions, different management actions have been used to suppress infestations and economic damage [2-4,9]. A better understanding of the biology, ecology, and behavior of the CAL has gradually replaced the manual and mechanical collection of locust swarms, hopper bands, and egg pods performed during the 19th century with more appropriate management techniques [4,9,11-16]. At present, the use of biomodels and Geographic Information Systems Technology (GIS) support CAL monitoring and the forecasting of outbreaks [17-19]. During the most recent outbreak in 2018-2020, the National Service of Agri-food Health, Safety and Quality (SENASICA) introduced the potential use of unmanned aerial vehicles (UAVs) or drones for the monitoring of locust populations in addition to land monitoring [20,21]. Currently, several research lines elucidate on the evolution of phase polyphenism, the environmental factors that trigger gregarization and swarm formation, the bioactive compounds and nutritional contents of the CAL, and the improvement of an early warning system (EWS) [8,15,19,21-26]. Hopefully this work will provide novel information and knowledge that helps to improve the management and control strategies of the CAL.

This work aims to provide a general view on the current knowledge of the CAL, management strategies, present research, and future work.

## 2. Life History of the Central American Locust

It is well established that in continental Mexico and Central America, the CAL exhibit two generations per year [4,11-13,23,27-29]. Interestingly, only one generation per year is reported to occur in Socorro Island, Archipelago Revillagigedo by the Mexican Pacific Coast, 480 km southwest of Baja California, Mexico where a locust invasion was reported in 2006 [5,30]. In this review, we will refer to the life history of the CAL populations that occur in continental Mexico and Central America. In these regions, the second generation overwinters as sexually immature adults from November to April-May, undergoing a reproductive diapause. This physiological state is a response to the onset of the autumn-winter dry season that brings about a decrease in temperature and shorter days [4,9,23,27,28]. Adults remain sexually immature until the onset of the rainy season around mid-April. As climatic conditions improve, and when environmental conditions become suitable for reproduction, adults of the second generation become sexually mature and start mating and laying eggs from May through June. Sexually mature adults turn yellow and mate en masse on bare sandy-clay soils, where each female lays one to four egg pods at a depth of approximately 3 to 10 cm. Each egg pod may contain 40-75 eggs based on field observations [29]. These eggs will hatch from mid-May through June and give rise to the first generation. First-generation nymphs are present from May-June through July, and adults from mid-July to the end of September. The first generation develops very rapidly, given the favorable climatic conditions (27 °C average temperature, 50-80% relative humidity, and 13L: 11D period, as well as abundant and lush vegetation for feeding); it may take 55-60 days to progress from egg through to sexually mature adult. Mating and oviposition occur from mid-September through October. Second-generation nymphs may occur from mid-September through mid-December. By the end of November, 70-80% of the second-generation nymphs will have reached the adult stage and will remain sexually immature. There is an overlap between second-generation adults and nymphs of the first generation, and also between adults of the first generation and second-generation nymphs. The second generation has a longer duration, 155-180 days since the adult enters diapause in response to a drier season, lower temperature, and shorter day length that occurs in the region from November through April [4,7,9,11,12,17,20,23,27,28]. Under these unfavor-
able environmental conditions, the CAL may not resume development, though relative humidity occasionally may be high at 70-85% [4,9,27-29]. If the population density is high (>25-30 adults/m²) and environmental conditions become suitable, four to six weeks after reaching the adult stage, scattered populations may join to form swarms ready for migration. The first swarms in the region are observed and located from the second half of December onwards. The period, from December through April, is appropriate to undertake control measures since adult populations of the CAL remain sexually immature and in large aggregations (up to 5000 adults/m²) [9]. When the first rains begin in April-May, the adults then enter the process of sexual maturation and changes in their behavior and color continue to occur. The solitary young adult is brown with light-brown tones, and has a great capacity for flight over short distances of 15-20 m when disturbed; while the gregarious young adult is brown with dark brown tones and moves in a cohesive manner in large groups or swarms. As they reach sexual maturity, this coloration disappears and turns yellow, observed first in males and later in females, and is more conspicuous in gregarious than in solitary populations [4,9,27,28]. During this period, large numbers of locusts are observed flying against the wind, which helps to increase their body temperature and strengthen their flight muscles [4,9,11].

### 3. Habitat and Ecology

The CAL is a polyphagous species throughout its distribution area. It has been recorded to feed on up to 400 plant species, feeding on both cropped and grazing areas, including dry vegetation [4,9,27,28]. Feeding ecology of the CAL is not fully understood, but a recent study on the effect of plant volatiles and feeding preference of the CAL showed that the CAL in the Yucatán Peninsula was highly attracted to the odor of *Pisonia aculeata* L., which it uses as a refuge but not for feeding [22]. As for the feeding preference, the study revealed that the CAL showed marked feeding preference for two native plant species, *Leucaena glauca* Benth and *Waltheria americana* L. [22]. However, it is not clear if this observation can be applied to other regions where the CAL is present. In Mexico and Central America, the breeding areas for the CAL are cultivated and natural grasslands that have replaced the low and thorny forests. For instance, in the coastal plain of the Gulf of Mexico and the Yucatán Peninsula, 80% of the areas of reproduction and gregarization occur in these agroecosystems [19]. The habitat of solitarious populations is characterized by grassland and vegetation patches that do not exceed 2.5 m in height [4]. Its distribution depends upon the vegetation pattern and, if the vegetation is homogeneous, locust populations may remain scattered. However, anthropogenic activities, such as burning or abandonment of cultivated areas, and environmental factors (convergent winds, droughts, flooding, and food shortage) may lead to gregarization and swarm formation [4,19,28,29]. In recent years, changes in land use through the conversion of forested areas into agricultural areas have aggravated the locust problem, since the area suitable for reproduction and gregarization has increased. For example, in the Yucatán Peninsula, which represents the most important breeding area in Mexico, the agricultural area increased from 394,236 ha in 1981 to 579,643 ha in 2014; in a 30 year period, 47% of the forested area was converted to livestock activities [31]. Recent studies found that the burning of grassland and agricultural areas that are ideal for feeding, reproduction, and oviposition of the CAL are associated with the emissions of methane (CH4) and carbon dioxide (CO2), and these greenhouse gases increase soil temperature up to 3 °C which favors locust breeding and gregarization, as occurs in northern Mexico, north of the Huasteca Potosina and southern Tamaulipas, where locust populations have increased [19,32].

### 4. Permanent Breeding Areas

Solitarious populations of the CAL reproduce and develop in permanent breeding areas located in the lowlands that provide suitable climatic conditions for reproduction, uncovered land or with little vegetation cover, and close to cultivated areas. The invasion area extends south of the Tropic of Cancer (23°26′), at no more than 2000 masl and 700-2500 mm
annual precipitation [28,33,34]. The onset of the spring rains is critical to induce sexual maturation, mating, and oviposition of second-generation adults [4,9,16,28,33,34]. Four permanent breeding areas have been recognized [4,11,13] (Figure 1): (1) the Yucatán Peninsula in Mexico; (2) the Valley of Rio Aguan in Northern Honduras; (3) the Gulf of Fonseca in El Salvador, Honduras, and Nicaragua; and (4) the Province of Guanacaste in Costa Rica. Recently, four additional breeding areas have been identified in Mexico [34,35] (Figure 1): (5) the State of Veracruz, municipalities of Medellín, Boca del Río, Alvarado, Tlalixcoyan, and Tierra Blanca, which is second in importance after the Yucatán Peninsula; (6) Chahuites-Tepanatepec, located on the limits of Oaxaca and Chiapas, where the CAL becomes gregarious, causing invasions into the Isthmus of Tehuantepec and other localities in the state of Oaxaca; (7) the border of San Luis Potosí-Tamaulipas states, in the Valleys of the Sierra Nahola, the smallest of the four additional permanent breeding areas, which currently has given rise to serious invasions into the Huasteca region (East of San Luis Potosí, South Tamaulipas, and North of Veracruz); and (8) Tabasco, located on the banks of the Usumacinta River on the border with Guatemala, where it is considered that environmental conditions can lead to the development of CAL populations.

<figure><img src="image_81.png" /><figcaption>**Figure 1.** Central American locust, *Schistocerca piceifrons piceifrons* (Walker, 1870), permanent breeding areas: (1) Yucatán Península, México, (2) Valley of Rio Aguan, Northern Honduras, (3) Gulf of Fonseca in El Salvador, Honduras, and Nicaragua, (4) Province of Guanacaste, Costa Rica, (5) State of Veracruz, México, (6) Chahuites-Tepanatepec, on the limits of Oaxaca and Chiapas, Mexico, (7) Border of San Luis Potosí-Tamaulipas states, México, and (8) Tabasco, on the banks of the Usumacinta River, border with Guatemala.</figcaption></figure>

Seasonal migration between habitats does not seem to be part of the life-cycle of the solitarious phase, although conclusive studies have not been made. Plagues occur when swarms form and migrate outside of the permanent breeding sites. The ecological factors that cause outbreaks are poorly understood; nonetheless, the extent of a suitable habitat created by anthropogenic activities plays a major role [4,9,11–13,16,19]. Several works have associated CAL outbreaks with the event of El Niño Southern Oscillation (ENSO) (a drought period followed by abundant rain) and La Niña [19,36]. Recent studies found that solitarious populations of the CAL in the Yucatán Peninsula are high in the rainy season and correlated with the abundance of the grass *Panicum maximum* Jacq. and
precipitation [37]. Indeed, precipitation is one of the most influential factors in determining locust activities, such as mating and oviposition periods. Humidity is required in the soil to ensure the hatching of the eggs and to satisfy the water requirements of nymphal development [4,9,11–13,16,17,23,38]. Regarding the CAL plagues and invasions, the coastal lowlands of Mexico have been invaded as far north as the Tropic of Cancer by swarms originating in the Yucatán Peninsula or the Pacific Coast of Guatemala [13,39]. In 1923, a CAL plague invaded the state of Veracruz [13,40]. Swarms occupied the hot coastal plain (Tierra Caliente) where they bred. However, adults moved to the west, up the valleys towards the cooler highlands where they bred, but hoppers perished because of the cool weather. Prevailing winds and the occurrence of rain all contributed to determining the direction of swarm movements. It has been shown that, in the Yucatán Peninsula, the migration direction of the first-generation swarms is northeast and of the second-generation swarms is southwest [37].

**5. Band and Swarm Formation**

Solitarious nymphs of the CAL are green or tan in color, avoid encounters with other individuals, and cause no economic damage. As the local population density increases due to favorable environmental conditions, they become gregarious and attracted to each other. Soon they develop a pink to orange background color with intense black patterns (Figure 2) [4–6,9,41].

<figure><img src="image_82.png" /><figcaption>**Figure 2.** Central American locust, *Schistocerca piceifrons piceifrons* (Walker, 1870), solitarious (a,b) and gregarious (c) nymphs showing different color patterns.</figcaption></figure>

Prolonged high-density conditions may result in an exponential population growth, which can lead to the formation of bands consisting of millions of individuals that march in the same direction in a cohesive manner [4,5,9,11–13,41]. Displacement of locust bands depends upon developmental stages and environmental factors; the first and second nymphal instars of the gregarious phase may remain on the host plant for a few days, but older nymphal instars (third-sixth) form bands and may displace 15–50 m per day [4,11,28]. It is reported that the black pigmentation allows the insects to be more efficient at absorbing solar radiation, raising their body temperature and metabolic activity; this is important during the winter (diapause stage) [4,11]. Other adaptive significance of the black patterns, such as aposematic coloration, which was shown in the desert locust [42], has not yet been demonstrated in the CAL. Gregarization is also associated with drastic changes in the insect's habitat or unusual climatic changes, such as convergent air currents. If the population density is high (>5 nymphs/m²) and harvesting, burning of crop remnants, or soil preparation activities are performed, the nymphs gather and form compact groups (bands) on patches of vegetation nearby the cultivated land [9,29,41]. Upon reaching the adult stage, these small groups, which can vary in size from a few m² to several hectares, join with others and form swarms. This behavior may be observed at the end of crop
harvest in the spring-summer cycle. At this stage, there is an opportunity to undertake
control measures since it is easier to deal with small areas already located than large areas
of land when the population is dispersed [4,9,16,27–29]. Further research is necessary to
understand the gregarization mechanism and factors involved in the displacement of locust
bands and swarms.

6. Phase Polyphenism, Gregarization, and Migration

The CAL is a true locust species that shows an extreme form of density-dependent phenotypic plasticity [4–6,9,16,27–29,41]. While the proximate mechanisms of phase transformation in the CAL are less understood than its congener *S. gregaria*, recent laboratory research has shown that the rearing density has a dramatic impact in resulting phenotypes including color, morphology, and behavior. Similar to other locust species, the solitarious CAL avoid each other, are inconspicuous, and harmless, while the gregarious CAL are attracted to each other, are conspicuously colored, and form large aggregations of nymphs (bands; Figure 3) or adults (swarms; Figure 4) that migrate long distances causing severe damage to agriculture and humankind [4–6,11–13,27–29,41].

<figure><img src="image_83.png" /><figcaption>**Figure 3.** Central American locust, *Schistocerca piceifrons piceifrons* (Walker, 1870), 1st (a) and 6th (b) instar bands.</figcaption></figure>

<figure><img src="image_84.png" /><figcaption>**Figure 4.** Central American locust, *Schistocerca piceifrons piceifrons* (Walker, 1870), swarms.</figcaption></figure>

It is unclear at this point what the relative importance of tactile, olfactory, and visual stimuli is in detecting changes in density in the CAL, but the preliminary laboratory data seem to suggest that the proximate mechanisms of phase transformation may be slightly different from what is known in the desert locust [43]. For example, the relative rates of gregarization and solitarization are different from the desert locust (Foquet et al., unpublished). This is not surprising given the fact that the CAL has evolved phase polyphenism
independently from the desert locust [44]. The molecular basis of phase polyphenism in the CAL is currently being studied using transcriptomics and RNA interference. Phenotypic plasticity is often considered to be an adaptation to heterogeneous environment [45], but whether the phase polyphenism in the CAL is adaptive or not has not yet been formally studied. Currently, it is not known whether the conspicuous coloration of the gregarious nymphs is aposematic, because it is frequently observed in the field that vertebrate predators readily consume gregarious nymphs. However, it is possible that these insects may prefer to feed on toxin plants at the early stage of gregarization, which will provide a certain level of chemical protection. This is an untested hypothesis, but a previous study on the desert locust demonstrated that at the early stage of gregarization, the nymphs would preferentially feed on toxic plants, which makes their yellow and black coloration aposematic [42]. Other adaptive features of the nymphal coloration, such as thermoregulation or heightened immunity [45], have not yet been studied in the CAL [Song, pers. comm.]. Likewise, the adaptive nature of cryptic coloration and solitary behaviors associated with the solitarious phase have not been tested, but it would be quite easy to imagine that they would be adaptive.

The solitarious nymphs in the field setting are often green with small black dots and markings on the pronotum, abdomen, and hind legs, while the gregarious nymphs have a pink or peach background color with an extensive black pattern on the head, pronotum, abdomen, pads, and legs (Figures 2 and 3) [4,5]. Newly fledged adults are brown to pinkish in color, with abundant light black marks on the tegmina. Sexually immature adults in the solitarious phase are brown with light-brown tones and have a great capacity for flight. Sexually immature adults in the gregarious phase exhibit a darker pink color with darker marks on the tegmina and turn bright yellow on sexual maturity, the latter being observed first in males and later in females (Figure 5) [4,5,9,11,12,27–29,41].

<figure><img src="image_85.png" /><figcaption>**Figure 5.** Central American locust, *Schistocerca piceifrons piceifrons* (Walker, 1870), sexually immature adults in the solitarious (a,b) and gregarious phase (c); sexually mature adult in gregarious phase showing bright yellow color (d).</figcaption></figure>

Sexual maturity is closely related to precipitation and relative humidity, with second-generation adults beginning this process with the onset of rains in April–May; during the next three to four months, thousands of yellow adult couples will mate and lay eggs
simultaneously in bare, rich-clay soils [4,5,9,11,12,27–29,41]. Under laboratory conditions, a similar pattern has been observed, with small differences [4,9,11,12,27–29]: rearing density affected the hopper coloration greatly. Those reared in crowds invariably had a heavy black pattern on a pink or peach ground color; those reared in isolation had little or no black pattern and the ground color was green, brown, pink, or straw. The type of food also affected the coloration of the isolated hoppers, but had no effect on the crowded specimens. The color of fledgling adults was not correlated with nymphal coloration; all had a rather somber, brown appearance. Sexually mature males kept in crowds became predominantly yellow, but crowded females developed only a little yellow coloration, and isolated adults developed none at all upon maturity. In captivity, density also affected the length of the pre-oviposition period, which averaged 36 days from fledging to the production of the first egg pod by females kept in crowds and 61 days for those reared in isolation. Crowded adult females averaged six egg pods each, with 70 eggs per pod; while isolated females averaged eight pods, with 62 eggs per pod. Egg pods were produced at 6- to 7-day intervals, regardless of density. The incubation period was 18–19 days at 32 °C and 25 days at 28 °C. It is documented that adults of the CAL strengthen their flight muscles four to six weeks after reaching the adult stage, and if population density is high (>10–15/m²) and environmental factors suitable, scattered populations join forming swarms that start migrating [4,9,16]. Swarm migration occurs mainly during the day, but occasionally swarms have been seen flying at night when the temperature is high (25 °C ± 2 °C) and on light moon nights. Second-generation swarms are observed and located in the region from the second half of December onwards [4,9,27–29]. During this stage, it is advisable to undertake all possible control actions since adults have not mated or oviposited and remain at very high population densities (up to 5000 adults/m²) in large aggregations (Figure 4).

Large numbers of locusts are frequently observed flying against the wind to increase their body temperature [4,9,28]. In regard to environmental factors, such as temperature, precipitation, day length, distribution of vegetation patterns, and land use, it is well established that all play a major role in influencing and inducing gregarization and phase transformation [4,9,13,16,18,19,23,27,28]. Recent work showed that in the Yucatán peninsula, which represents the most important breeding area in Mexico, environmental factors associated with the population density of the CAL are, in order of importance, the relative species density of vegetation, the isotherm and isohyets, maximum precipitation, temperature, and land use; the population density of the CAL is influenced primarily by the abundance of the grass *P. maximum* and precipitation [23].

## 7. Central American Locust Outbreaks

The CAL, like its congeners, has caused fear and destruction throughout its distribution area for centuries. In Mexico, the most ancient records come from pre-Hispanic times [1–3,14] and the locust swarms are believed to be one of the causes that led to the decline of the Maya-Quiché cultures in the Yucatán Peninsula and the Toltec in the Anahuac Valley. The Mayan sacred book, the Popol-Vuh, mentions that the ancient people migrated out of hunger brought about by the agricultural losses inflicted by the locust plagues. During the colonial time, written records on locust plagues date back to the seventeenth century, when the first invasion in the territory currently occupied by the Yucatán Peninsula, Tabasco, Chiapas, Oaxaca, and Veracruz, was reported [38,39,46,47]. In Mexico, the CAL was declared a national pest in 1824 and provisions were established to fight off bands and swarms [47]. In 1924–1926, there was a great invasion and, since then, the presence of locust plagues has occurred without interruption in one or another part of its distribution area, especially in the Yucatán Peninsula and Central America [4,9,14,19,21]. The National Plant Protection Service in Mexico created a permanent locust control campaign in 1949 [48,49]. The OIRSA (Organismo Internacional Regional de Sanidad Agropecuaria) was created in 1947 as the CICLA (Comité Internacional Contra la Langosta), and in 1955 the CAL was declared a transboundary pest that required the coordinated efforts of Central American
countries to deal with it. At present, the OIRSA represents the Central American anti-locust
organization and continues to be in charge of coordinating the regional control efforts,
funding anti-CAL campaigns, training, and providing information on the current locust
situation [21,49,50]. From 2016 to date, there have been significant population increases
of the CAL in the OIRSA Region. For example, in Nicaragua in 2016, locust swarms
were controlled by the Institute for Agricultural Protection and Health (IPSA). There were
outbreaks in the Yucatán Peninsula, Mexico (2014–2020), El Salvador (2016 and 2018) and,
at present, after a long recession period, outbreaks were registered in Belize. Significant
populations of the CAL have been reported in Guatemala, suggesting that there are factors
that favor the development of this pest. On 2 July 2020, OIRSA issued a regional alert for
the prevention of the CAL swarms [50].

**8. Central American Locust Management Strategies**

Considerable progress has been made on the management of the CAL during recession and outbreak periods [9,16–19,36,51–62]. Management techniques have evolved from the manual and mechanical collection of egg pods, hopper bands, and adult swarms [1–4,14] to the use of prediction models that aim to understand how population dynamics of the CAL relate to environmental factors and local conditions. For instance, a study [36] on the relationship between sea surface temperatures, the El Niño Southern Oscillation (ENSO), and the potential of the CAL plagues found a 72% coincidence between years of massive CAL attacks and ENSO years in the North Pacific of Costa Rica; an increase of environmental temperature and irregular distribution of precipitation, as occurs during the ENSO years, may result in vigorous copulation and oviposition in the CAL. A population increase is the first step for phase change and eventual plagues. A subsequent work assessed the risk of next-generation nymph-populations, considering an initial adult population and each instar mortality rate [51]. In another study, a Thermal Time Locust Development Clock (TTLDC) was built considering average values of temperature, day length, diapause cool hours, and calendar dates; this model helped to predict the CAL timing of phenological stages. This model implies a starting date (Bio-fix) established experimentally after quality data on population dynamics and the life cycle of the CAL. When the model was compared with field observations, the differences were relatively small. The reliability of predictions depends upon the accuracy of the starting date and deviations in weather conditions from the average year [17]. More recently, an early warning system (EWS) for monitoring and management of the CAL habitat in permanent breeding areas in the Huasteca region (Mexican Coastal Plain) and the Yucatán Peninsula was implemented by SENASICA-UASLP (Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria-Dirección General de Sanidad Vegetal-Universidad Autónoma de San Luis Potosí). This EWS applies multicriteria models and NOAA-AVHRR satellite images [15,19,32]. The model is based on two variables of the meteorological mesoscale: the presence of the ENSO and drought monitoring; it also takes the CAL behavior into account. Accordingly, the process of band or swarm formation begins when solitarious populations face environmentally unfavorable conditions (grass or crop remnant burning, convergent winds, droughts, or food shortage) and converge in places where vegetation is available. The increase in population density of individuals per unit area leads the insect to gregarize and prepare to migrate in search of food and oviposition sites. Hence, climatic effects are among the fundamental cause of behavioral change, and the host distribution pattern reflects spatially the areas of gregarization and oviposition (greater stress), and the areas of migration in search of food (higher biomass production in agricultural areas). Currently, this EWS proposes that not only the ENSO, but also the La Niña, affects locust breeding and gregarization. Furthermore, there is evidence that as a consequence of the increase of greenhouse gas emissions such as CH₄ and CO₂ in gregarious areas, in the last four years (2017–2020), the drought monitor showed an increase of more than 3 °C in soil temperature in areas proximate to the Gulf of Mexico. These greenhouse gas emissions (CH₄ and CO₂) are produced by anthropogenic livestock activity, which creates more favorable environmental conditions for the repro-
duction of the CAL [32]. An additional dynamic simulation model [18] showed that the growth and development of the CAL in the Yucatán Peninsula was associated with daily rainfall, temperature, and physical soil properties, such as texture and depth. In regard to the growth of non-cultivated grass in breeding zones and oviposition rates, the model estimated both variables as a function of soil moisture. The latest work [23] focused on a deeper analysis of the environmental factors that affect population dynamics of the CAL and it was found that plant species richness (PSR) and relative species density (RSD) in the Yucatán Peninsula were higher during the rainy season than in the dry season, with RSD the most important variable associated with locust density, followed by isotherm and isohyets, maximum precipitation and temperature, and land use. Locust density was positively correlated with the abundance of the grass *P. maximum*. Therefore, surveys for early detection and control of the CAL on the Yucatán Peninsula may focus on areas with the grass *P. maximum* to predict risk areas and target survey efforts. In the most recent outbreak (2014–2020) in the Yucatán Peninsula, the possibility of using drones or unmanned aerial vehicles (UAVs) for locust surveying was introduced [49,50,52]. Hopefully, the Mexican National Plant Protection Service and the OIRSA will have trained technicians in the near future to incorporate this tool in the surveying of locust populations and into the CAL campaigns. All these efforts have provided novel information and additional techniques for the CAL surveying and management. However, future research integrating multiple disciplines is needed to obtain finer data on the ecological factors and their correlation with the population dynamics of the CAL. Moreover, all information generated must be incorporated into the CAL management strategy since, at the moment, the use of the available techniques and tools is limited.

## 9. Control Measures

Control campaigns in Mexico and Central America aim to prevent swarm formation or migration by undertaking timely control of locust bands and swarms through the continuous surveying and monitoring of breeding areas in the Mexican Coastal Plain, southern Mexico, and six Central American countries [4,7,11–13,19–21,27,34,35,47]. This preventive control strategy is occasionally halted due to a lack of economic resources, shortage of personnel, or climatic conditions. In addition, deforestation, grassland burning, and livestock activity have intensified in recent years, increasing the area with suitable conditions for reproduction and growth of the CAL [22,23,41,49]. Up to the present, chemical control is perhaps the main alternative during outbreaks. Previous to 1998, most control operations against the CAL were carried out using methyl parathion. However, beginning in 1999–2000, chemical control was diversified with the validation and introduction of additional products such as phenylpyrazole, pyrethroids, insect growth regulators, and, above all, bioinsecticides [16,28,50,52–62]. From 2000–2010, a successful biological control program was established. This program employed searching for local strains of entomopathogenic fungi, screening for the most pathogenic and virulent strains, development and formulation of a biological insecticide supported in laboratory and field trials, and the transference of technology to the National Plant Protection Service to produce the bioinsecticide [16,28,53–62]. *Metarhizium anisopliae acridum*, a native isolate, is produced at present by the National Plant Protection Service in two state-run laboratories in Guanajuato and Yucatán, and a privately-owned business in Puebla [16,28,53–62]. Field trials in the Huasteca region and the Yucatán Peninsula (4 × 10¹² conidia per hectare) in a mineral oil formulation provided up to 90% mortality in swarms following applications of the pathogen. At present, this biological insecticide is used to suppress locust bands to prevent swarm formation and, during the winter season, it is used to suppress locust swarms over grassland areas. In 2010, the fungus was applied to over 4000 ha of locust at a cost of approximately USD 10 per hectare [60]. Neem extracts (*Azadirachta indica* Juss) are recommended by OIRSA as a viable alternative to suppress nymph and adult populations of the CAL that invade forest or urban areas. It is reported that at a dose of 1 L/ha applied in 1–2 L of vegetable oil, neem extracts cause 67% mortality after 48 h and 100% after 7 days [34,50].
Safer chemical products, bioinsecticides, and neem extracts, as well as the introduction of new technologies, have been integrated into the locust preventive management strategy, making the Integrated Pest Management approach, adopted in 2005, possible [61,62].

## 10. Current Research

There are several ongoing research lines aiming to have a better understanding of major behavioral, ecological, environmental, and evolutionary factors that favor CAL reproduction, growth, gregarization, migration, and phase change. The main goal is to provide a multidisciplinary approach that strengthens and deepens current knowledge on the CAL. This may help improve preventive strategies and the suppression of locust plagues during outbreaks, as well as generate alternative management practices. Laboratory and field studies are performed to understand the molecular mechanisms that sustain the behavioral and physical changes in the CAL and how the environment influences phase polyphenism [8]. Research using remote sensing technology is being conducted to gain insight into the environmental factors that determine the CAL distribution and trigger concentration, reproduction, and gregarization [19,32,46]. This project encompasses the Huasteca Region and the Yucatán Peninsula. To date, an early warning system (EWS) that provides timely information on possible concentration and reproduction areas has been developed. Currently, it has been found that the CAL is distributed in areas of high CH₄ and CO₂ emissions north of the Huasteca Potosina and South Tamaulipas [19,32]. Livestock activity and the burning of grasslands are among the major variables that are modifying the CAL habitat. Additional research is being conducted to study the nutritional contents and bioactive compound levels of the CAL [24–26], aiming to incorporate this information into its management. The presence of phenolic compounds, alkaloids, tannins, saponins, flavonoids, and quantity of antioxidants against the DPPH (2, 2-diphenyl-1-picrylhydrazyl) and ABTS (2, 2'-azino-bis, 3-ethylbenzothiazoline-6-sulfonic acid) free radicals was reported. Proximate analysis showed that *S. p. piceifrons* has a high protein content (80.26%), low-fat content (6.21%), and fiber content (12.56%) similar to other Orthoptera species. The chitin and chitosan contents of the CAL were 11.88 and 9.11%, respectively, and the recovery percentage of chitosan from chitin was 76.71%. Among the Orthoptera, the protein content of the CAL is among the highest while its contents of chitin and chitosan are similar to those of other insect species, e.g., *Bombyx mori* Linnaeus (Lepidoptera: Bombycidae). Results suggest that this locust species is a potential source of bioactive compounds of biotechnological interest for use by pharmaceutical and food industries. A more recent work [26] assessed the digestibility of proteins of the CAL and the content of antioxidants from the peptides resulting from proteolysis. It was found that digestion with trypsin allowed the recovery of 0.68 and 0.055 mM TE/mg of protein, with a digestion time of 1 and 3 h, respectively. This work documents the potential of the CAL as a source of protein for the food industry and provides additional evidence on the potential use of this natural resource. Studies on the inhibition of intestinal proteases by plant species such as the fruit of hardy parlor palms (*Chamaedorea radicalis* Mart.) and its effect on the intestinal proteolytic activity of adult Orthoptera, the CAL and *Pterophylla beltrani* Bolívar and Bolívar, provided encouraging results [63]. The intestinal proteolytic activity of both orthopteran species was related to serine and cysteine proteases. Total proteolytic activity was 98,930.56 ± 7544.46 PAU/g (proteolytic activity units per gram) of intestinal tissue in the CAL and 52,847.22 ± 8509.11 PAU/g in *P. beltrani*. Fruit of hardy parlor palms is considered a strong candidate in future studies for identification and characterization of the inhibitors and their potential use in biological control.

These innovative research topics will enhance our understanding of the CAL plagues and may contribute substantially to the development of more effective and sustainable management mechanisms.
## 11. Future Work

In the last 20 years, a large amount of information has been generated to improve the management of the CAL. The integration of a bioinsecticide and the diversification of chemical products into the CAL campaign are, perhaps, among the most outstanding, for two reasons: (a) the development or introduction of these products allowed the opportunity of an integrated pest management approach for solitarious populations that might be of risk and improved management of locust outbreaks; and (b) the environmental impact caused by locust operations was considerably reduced. However, it is necessary to have a better understanding of the CAL population dynamics in relation to environmental factors, physical and physiological traits that promote gregarization, and swarm formation. its nutritional ecology, and new technologies that will contribute to a more efficient and effective management of this pest. Taking these remarks into account, some aspects for future research are outlined below.

To date, the proximate mechanisms of phase change are relatively unknown. However, we are in the beginning stage of understanding locust phase polyphenism in the CAL better. A long-term laboratory colony was established, which allows the possibility of manipulative experiments that can yield detailed understanding of the phase change in the CAL. Currently, the effect of rearing density on behavior, color, and morphology has been studied. Specifically, the behavioral polyphenism has been quantified using the same behavioral assay used in the desert locust. Density-specific transcriptomes from the CAL were generated and the number of differentially expressed genes between the density conditions were identified. The whole genome sequencing with chromosome-level assembly is currently underway for the CAL. These new developments will allow us to have a better understanding of density-dependent phase polyphenism in the CAL.

The environmental factors that affect the population dynamics of the CAL have not been sufficiently studied. It is necessary to carry out more in depth and systematic studies in critical areas where the CAL lives and reproduces. Environmental information generated (climatic variables: temperature, precipitation, relative humidity, photoperiod, soil types, vegetation types and its distribution patterns; and cultural practices such as the burning of grasslands and crop residues, and radiation, among others) must be integrated into biomodels that consider the largest possible number of environmental variables and their relationship with the presence of this pest. This will provide reliable information for locust surveying, monitoring, and the prediction of locust outbreaks to allow for timely and effective decisions.

The use of new technologies, such as remote sensing and unmanned aerial vehicles (UAVs), for the monitoring of sensitive areas is equally important. As is the training of field technicians in the use and management of these and other new technologies for surveying the CAL habitat and populations that might generate risky conditions.

Studies on the nutritional ecology vs. the population dynamics of the CAL will provide useful information on its distribution and habitat preferences; and this information will be a useful tool in its management.

The potential effect of climate change and land use or cover change on the CAL biology and outbreak frequency needs to be addressed. This is a promising research field that may provide insight into the development of gregarious populations, density-dependent phase polyphenism, and migration [64].

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

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

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** To Tecnológico Nacional de México-I. T. Cd. Victoria for providing facilities to undertake this work. Special thanks to Michel Lecoq for the invitation to write this review.
**Conflicts of Interest:** The authors declare no conflict of interest.

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Review

# Alternative Strategies for Controlling the Brown Locust, *Locustana pardalina* (Walker)

Roger Price

Insect Ecology Division, ARC-Plant Health and Protection, Private Bag X134, Queenswood, Pretoria 0121, South Africa; pricer@arc.agric.za

**Abstract:** Regular and often intense outbreaks of the brown locust, *Locustana pardalina* (Walker), in the semi-arid Nama Karoo region of South Africa present a formidable pest control problem. Outbreak patterns over a 64-year period (1941–2005) were reviewed indicating a very high frequency of outbreak years with regular ‘plague’ periods being experienced, while a more detailed analysis of the numbers of locust targets controlled during a 22-year period (1983–2005) described the intensity and scale of the outbreaks. The operational constraints associated with the traditional ground-based control strategy employed against the thousands of individual roosting brown locust hopper band and swarm targets in the Karoo are discussed. A brief review of laboratory and field trials of alternative methods of controlling the brown locust, such as insecticide baits, barrier treatments and the Green Muscle® myco-insecticide, as an alternative to broad-spectrum pyrethroid insecticides are described. In addition, alternative control strategies to the current ‘Commando’ system of ground-based control operations are discussed. The recommendation is for a modernised and technology-equipped integrated brown locust management strategy (IPM), combining ground and aerial tactics that will have the flexibility and the capacity to deal effectively with outbreaks. The integrated management strategy should focus on ground-based control of hopper bands and fledgling swarms in the Upper and eastern Karoo, while outbreaks over most of the Central Karoo and arid Bushmanland areas should be left to fledge and coalesce into large-sized swarms that could then be targeted by spray aircraft as they migrate along their known swarm flight paths. The introduction of electronic reporting and GIS mapping technologies for brown locust campaign management is essential.

**Keywords:** brown locust; *Locustana pardalina*; Karoo; outbreak patterns; control strategy; integrated pest management

## 1. Introduction

The aim of this review article is to summarise the outbreak history of the brown locust, *Locustana pardalina* (Walker) along with the control tactics currently employed and alternative control methods evaluated, and to then discuss possible alternative strategies for more effective management of outbreaks. The brown locust has a recognised outbreak area that covers approximately 250,000 km² of the semi-arid Nama Karoo biome region of South Africa and southern Namibia [1–4], from where plagues have developed that have overrun the entire southern African sub-continent up to the Zambezi River [3]. The Nama Karoo occupies the central plateau of the western half of South Africa at an altitude of 500–2000 m, so frost is common in winter. The rainfall mainly falls in late summer and autumn, with a rainfall gradient ranging from approximately 100 mm in the western arid areas to 400 mm per annum in the eastern Karoo, although rainfall is typically erratic and extended droughts are common. The brown locust displays a wide range of phase polymorphism and sexual dimorphism [5], with the differences measured between the extreme solitaria and gregaria phases being more pronounced than with any other locust species [6,7]. The field biology and population dynamics of the brown locust have been extensively studied [2,8–13]. An

**Citation:** Price, R. Alternative Strategies for Controlling the Brown Locust, *Locustana pardalina* (Walker). *Agronomy* 2021, 11, 2212. https://doi.org/10.3390/agronomy11112212

Academic Editors: Michel Lecoir and Arianne Cease

Received: 27 July 2021
Accepted: 31 August 2021
Published: 31 October 2021

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**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/).