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History of locust phase change research

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Early locust research

In earlier centuries, only the individuals living in areas affected by locust outbreaks were aware of the phenomenon. On an international level, travelers, missionaries, naturalists, and the like were aware of the existence of locusts. [1] In regard to Africa, it is impossible to separate early locust research from the colonial interests of the British, French, and others.


French entomologist, Hippolyte Lucas, authored one of the initial scientific reports on locusts in the mid-19th century.[1] Jules Kunckel d'Herculès, French locust control delegate in Algeria, was influential in the early days of locust research.[2] [1] From 1888 to 1905, Kunckel d'Herculès conducted thorough investigations on the desert locust in North Africa, predating the identification of the locust phase phenomenon. He described plagues and control operations in great detail in his 1905 publication[3], filling up a 3-volume document weight 10 kg. [4] During that era, the theory of phase polymorphism had not yet emerged, and only the gregarious phase of locusts was recognized. Kunckel d'Herculais offered an initial explanation for the color evolution observed in gregarious desert locusts: immature adults were red, while mature adults were yellow. Even during this early period, he pioneered using color to identify potential swarm origins and attempted the first preventive control measures.[4]

In 1868, Charles Valentine Riley was appointed as Missouri's inaugural state entomologist, marking the inception of this position in the United States.[2] Riley's research primarily centered on investigating outbreaks of the Rocky Mountain locust (Melanoplus spretus). His seminal publication in 1877, titled "The Locust Plague in the United States," significantly contributed to the establishment of the United States Entomological Commission. Notably, his recommendations for locust management even included recipes for consuming locusts.

Integrating https://horizon.documentation.ird.fr/exl-doc/pleins_textes/pleins_textes_7/carton07/010008856.pdf

Sir Boris Petrovitch Uvarov and a brief history of phase change research

Sir Boris Petrovitch Uvarov © National Portrait Gallery, London

Boris Petrovich Uvarov (1886-1970) was born in 1886 in Uralsk, located in southeast Russia, and is often regarded as the pioneer of acridology. His research primarily revolved around the taxonomy, behavior, and ecology of locusts. Uvarov made significant contributions to the field by classifying and identifying numerous locust species, thereby enhancing our comprehension of their diversity and geographic spread. Additionally, he delved into the physiological and environmental factors that instigate locust swarms, as well as their behavioral traits during solitary and gregarious phases.[2]

At the age of 23, Boris Petrovich Uvarov assumed the role of director at the Entomological Bureau in Stavropol. During this time, he gained his first practical experience in managing locust populations, specifically the migratory locust (Locusta migratoria) and the Moroccan locust (Dociostaurus maroccanus). Uvarov observed mixed populations of migratory locusts and Locusta danica grasshoppers with intermediate (phase change) characteristics. In 1913, Uvarov's colleague Plotnikov conducted crowding experiments, while Faure (1923) studied the brown locust (Locustana pardalina) in the field. These early experiences laid the foundation for Uvarov's future contributions to locust research. His observations and collaborations during this period were pivotal in shaping the comprehension of locust biology, population dynamics, and the factors that influence their behavior. [2]

The findings inspired Uvarov to publish his theory of "phase polymorphism" [5] which later became "phase polyphenism". [6] [7] This work revealed that the migratory locust and L. danica are two phases of the same species (L. migratoria). He demonstrated that the transition between these phases is influenced by population density, with the solitarious phase prevailing at low densities and the gregarious phase occurring when favorable ecological conditions sustain high-density populations. [2]

Uvarov went on to extend his theory to the desert locust (Schistocerca gregaria) and the red locust (Nomadacris septemfasciata). While studying the specimens in the British Museum of Natural History, he realized from field records that the individual living Acridium flaviventre (now considered Schistocerca gregaria flaviventris) never co-occurred with S. gregaria and Acridium coangustatum (now a synonym of Nomadacris septemfasciata) never co-occurred with N. septemfasciata. He proposed these were likely to be their respective solitarious forms.[8] Uvarov's phase theory was further supported by field observations of S. gregaria by King [9] and Johnston [10] [11] and the closely related, Central American locust, Schistocerca piceifrons (then called S. paranensis) by Dampf (1926), who isolated wild-caught individuals and observed their transition towards a solitarious phenotype.[2] In the 1930s, Faure conducted caged experiments on the species L. pardalina, exploring various factors such as population densities, parentage, humidity, and background. These experiments marked a significant turning point in the understanding of locust invasions, contributing to the foundation of knowledge in this field. The subsequent development of phase theory became a prominent paradigm that has facilitated the advancement of locust research over the last century.[12]

In 1920, Uvarov relocated to London and joined the Imperial Bureau of Entomology, which later became the Imperial Institute of Entomology. Then, in 1929, Uvarov assumed leadership of the International Unit of Locust Research, initially consisting of himself and his assistant Zena Waloff. Subsequently, in 1931, France established the Committee for the Study of Locust Biology under the guidance of Professor Pasquier, which operated out of Algeria. This committee was later succeeded in 1943 by the Office National Antiacridien (ONAA), chaired by Zolotarevsky and supported by Pasquier and Rungs.[2] The ONAA ceased its activities following Algeria's independence in 1962. [13]

The "locust problem" becomes global

In the 1930s, numerous scientists, in addition to Boris Uvarov, played significant roles in establishing the foundations of what would become the new discipline of acridology.[2] This era witnessed notable milestones, including a series of international conferences organized to address the locust problem.[14] These conferences convened in Rome in 1931, Paris in 1932, London in 1934, Cairo in 1936 (a pivotal step in the internationalization of the issue), and Brussels in 1938 (Ministère des Colonies, 1938). These conferences brought together an increasing number of countries: the Union of South Africa, Saudi Arabia, Argentina, Australia, Belgium, Bulgaria, Canada, Chile, China, Egypt, Ethiopia, France, Greece, Guatemala, India, Iran, Iraq, Mexico, the Philippines, Portugal, Romania, Spain, Uruguay, the United Kingdom, the United States and Yugoslavia, plus many representatives of other countries in Africa and Asia colonized by English, French, Italian and Portuguese. Among the many scientists who participated in these conferences (or played an important role in locust research during this decade), were D. Imms (UK), H.B. Johnston (UK), O.B. Lean (UK), R.C. Maxwell-Darling (UK), B.P. Uvarov (UK), H.J. Brédo (Belgium), P. Vayssière (France), R. Pasquier (France), L. Chopard (France), B.N. Zolotarevsky (France), J.C. Faure (South Africa), Y. Ramachandra Rao (India), M. Afzal Husain (India, later Pakistan).[2] The list of countries participating in the conferences showcased the extensive global impact of the locust problem. However, the composition of scientists attending these conferences, predominantly European and exclusively male, highlighted the limited social and political diversity within the field of locust research during that period.

Read about women in acridology

The Anti-Locust Research Centre (ALRC) was established in 1945 in London, UK with Uvarov as director. The ALRC emerged with the primary objectives of coordinating research in acridology and fostering international collaboration in locust control, driven mainly by the economic interests of the British Empire's colonial ventures.[2] Similar motivations influenced the French Empire as well. [15] [16] During this era, extensive field studies were conducted on the major locust species of economic significance. Significant progress was made in understanding their life histories, migrations, behavior, and natural predators. However, the foremost goal of these field investigations was undoubtedly the identification of gregarious areas—the regions serving as the origins of outbreaks and migratory swarms. Zolotarevsky's work in 1937 demonstrated that the accumulation of solitarious individuals in outbreak areas appeared to be the primary factor in phase transformation, influenced by a range of ecological factors such as climate and vegetation, which varied across species and regions. By the decade's end, outbreak areas had been roughly identified for key locust species including the desert locust, migratory locust, red locust, and brown locust.[2]

Post World War II

Uvarov emphasized the importance of establishing permanent initiatives to monitor regions prone to outbreaks and fostering global collaboration to tackle the formidable migratory capabilities of these insects. After World War II and the decline of European empires and the subsequent emergence of numerous independent nations, necessitated a new approach to managing locusts. The creation of the Food and Agriculture Organization of the United Nations (FAO) in 1945 provided a framework to do so. In the 1950s, concrete cooperation materialized as the FAO facilitated the establishment of the Desert Locust Control Committee, aimed at promoting international collaboration in locust control efforts.

Food and Agriculture Organization of the United Nations (FAO UN)

Since 1955, the FAO ensures the coordination of desert locust monitoring and control activities and plays a major role in the early warning system via its Desert Locust Information Service (DLIS) (managed by the ALRC in London from 1943 to 1978, then by the FAO in Rome). Over time, there was a gradual implementation of international monitoring, control, and cooperation measures, accompanied by the establishment of dedicated international organizations for permanent surveys. [17] [18] [19] [13]

During the post-world-war period, in the 1950s and 1960s, Uvarov’s recommendations to develop inter-state cooperation on locust problems were implemented through various other international organizations. These organizations, mainly operational in nature to control invasions more effectively, have nevertheless played a key role in improving our understanding of the biology and ecology of locusts.[2]

See the FAO organization page for more information on the role of the DLIS and other FAO commissions established around this time.

Prominent locust phase-change researchers

Despite retiring in 1959, Uvarov continued his work at the ALRC until his passing in 1970. A comprehensive obituary and the history of the ALRC during his directorship can be found in the publication by Waloff and Popov.[20] Following Uvarov's death, the ALRC's scope expanded to encompass broader aspects of plant and animal protection in developing countries. In 1971, it was renamed as the Centre for Overseas Pest Research (COPR). Under Uvarov's leadership, the ALRC and later COPR served as a hub for numerous renowned researchers studying locust phase-change phenomena, with many joining during or shortly after his tenure.[2]

John Stodart Kennedy conducted field observations of encounters that resulted in aggregation and subsequent gregarization in S. gregaria.[21] In a later study, Kennedy examined the role of phase change in swarm formation relative to ecological factors.[22] Peggy Ellis played a pioneering role in the development of arena-based behavioral assays. She conducted highly comparative side-by-side testing of S. gregaria and L. migratoria nymphs. These circular arenas test the temporal and spatial dynamics of phase-dependent aggregation [23] [24] [25] [26], the onset and continuance of marching after group formation [27] [28] [29] [30], and the effect of tactile stimulation on gregarization, which Ellis achieved using small pieces of wire and crowding with woodlice (Ellis, 1959).[2] Behavioral work was continued by Sylvia Gillett [31] [32] [33], including some of the earliest work on locust aggregation pheromones, which was investigated independently by Nolte and colleagues in South Africa.[34]

At the ALRC, Peggy Ellis collaborated with Graham Hoyle and David Carlisle to investigate the physiology of phase change. [35] [36] Additionally, Hoyle played a crucial role in establishing locusts as a model organism in neurophysiology, following Uvarov's advocacy to promote locusts as excellent experimental animals.[2] Jeremy Roffey, George Basil Popov, and L.V Bennett explored the spatial and environmental processes that promoted the survival, multiplication, and gregarization of S. gregaria.[2] Meir Paul Pener spent a postdoctoral year at the ALRC in 1964, going on to an eminent career investigating the physiology and endocrinology of locust phase polyphenism in Israel (reviewed in [6] [37] [7]).

Prominent locust phase-change organizations

Fieldwork conducted in the 1950s and 1960s built upon earlier research from the 1920s and 1930s. In Mali, significant studies took place within OICMA, importantly, the gregarization process of the migratory locust in the Niger River floodplain. Researchers investigated population movements and dynamics, with notable contributions from Descamps [38], Remaudière [39], Davey [40], and Farrow [41], among others.[2]

Similarly, fieldwork was conducted on the red locust during outbreaks in Madagascar by Têtefort and Wintrebert [42] and within the IRLCO (International Red Locust Control Organization) in the African Great Lakes region, particularly in Tanzania's Rukwa valley by Chapman [43], Dean [44], Morant [45], Scheepers and Gunn [46], Symmons [47], and Vesey-Fitzgerald [48]. During the same timeframe, from 1959 to 1964, the FAO played a significant role in a major project focused on the desert locust, directed by Belgian entomologist Hans Brédo and financed by the United Nations Development Programme (UNDP). This comprehensive project significantly advanced our understanding of the desert locust's ecology across its entire range. Notable contributions were made by Popov [49] [50] in improving knowledge of the habitats that facilitate gregarization.[2] Jean Roy was responsible for the operational research aspect of the FAO project, focusing on enhancing strategies and methods for intervention and control [13].

A few years later in Madagascar, another research project aimed at improving the strategy for controling the migratory locust, funded by the UNDP and FAO took place from 1971 to 1973. Led by J.P. Têtefort, this project made it possible to better understand the functioning of the outbreak area of this species in the extreme south-west of the island. [2] The project quantified the significant influence of rainfall, emphasized the role of solitarious population movement in gregarization, and proposed a monitoring and warning system. [51] [52] [53] Following this project, the Programme de recherche interdisciplinaire français sur les acridiens du Sahel, better known by its acronym Prifas, was created within the Groupement d’étude et de recherche pour le développement de l’agronomie tropicale (GERDAT) which later became The French Agricultural Research Centre for International Development (CIRAD).

Centre de coopération Internationale en Recherche Agronomique pour le Développement

[2] This was one of the first works to research Odaleus senegalensis the Senegalese grasshopper in West Africa following major outbreaks in 1974. The research allowed for a comprehensive understanding of the species' annual south-north migrations, influenced by rainfall patterns driven by the dynamics of the inter-tropical convergence zone. As a result, the first attempt was made to develop a model using this species as a monitoring tool.[54] Then, Prifas, in collaboration with monitoring and control agencies, dedicated over two decades to studying the bio-ecology, population dynamics, and risk modeling of locusts in tropical regions worldwide. Key species investigated included the desert locust, migratory locusts in Madagascar and Indonesia, Mato Grosso locust, Rhammatocerus schistocercoides in Brazil, and the red locust in Madagascar. In 1998, Prifas turned into a research unit under CIRAD, known as "Locust Ecology and Control". In addition to its extensive research endeavors, the unit actively participated in FAO's EMPRES program in West and North Africa for approximately 15 years. Presently, the CIRAD locust unit is integrated into a joint research unit known as the Centre de Biologie pour la Gestion des Populations (CBGP). The CBGP continues to carry out ongoing research, including locust genetics and risk modeling, leveraging nearly 50 years of expertise and a vast network of field contacts. [2]

In 1983, the amalgamation of COPR in the UK and the Tropical Products Institute led to the establishment of the Tropical Development and Research Institute (TDRI). This institute further merged with the Land Resources Development Centre in 1988, forming the Overseas Development Natural Resources Institute (ODNRI). Subsequently, in 1990, the ODNRI became known as the Natural Resources Institute

Natural Resources Institute (NRI)

and was later transferred to the University of Greenwich in 1996. [2] During this transitional period, S. gregaria stocks from COPR were utilized to initiate a colony in the Department of Zoology at Oxford. Initially, they were employed by Steve Simpson's research group for comparative studies on feeding and nutrition in conjunction with L. migratoria. [55] However, the focus soon shifted towards a renewed effort to investigate locust phase polyphenism. Building upon the previous work by Ellis and Gillett, Roessingh et al. [56] introduced a novel behavioral assay involving tracking individual S. gregaria nymphs for 5-10 minutes in relation to a group of conspecifics positioned at one end of a rectangular arena. Unlike the group assays pioneered by Ellis, the Roessingh assay emphasized studying one insect at a time and placed greater emphasis on understanding the underlying organismal basis of behavioral gregarization. [2]

The history of locust research reflects a predominant focus and funding from the global north. Many countries heavily impacted by locust outbreaks have limited native research programs, with funds primarily directed towards practical control measures rather than speculative research. [2] However, there have been notable contributions from scientists in diverse regions. One such scientist is Thomas Risley Odhiambo from Kenya, who pursued his training at the University of Cambridge in the early 1960s under the guidance of entomologist and physiologist V.B. Wigglesworth. During this time, Odhiambo conducted research on reproductive physiology in the desert locust and authored fourteen papers, including a letter to Nature. [57] Following a review of the current status of Science in Africa [58] Odhiambo started envisioning the establishment of an African research center focused on African, and more broadly pantropical, research with the aim of increasing agricultural production, and combating tropical and vector-borne diseases. He strongly believed that science conducted in Africa should have at its heart improving the livelihoods of smallholder farmers. [2]

International Center of Insect Physiology and Ecology

In 1970, his vision became a reality with the creation of the International Centre of Insect Physiology and Ecology (ICIPE) in Nairobi, Kenya. Odhiambo's aim was for ICIPE to serve as a focal center of excellence, offering training and a research platform for African scientists across the continent. Since the 1990s, ICIPE has contributed significantly to research on locust behavior and ecology, with a particular emphasis on the desert locust. [2] Their work has explored various aspects of locust chemical ecology and investigated the potential of biocontrol methods involving entomopathogens. [59] [60] [61] [62]

References

  1. ↑ 1.0 1.1 1.2 Buj A (1995) International experimentation and control of the locust plague. Africa in the first half of the 20th century, pp. 93–105. In: Chatelin Y., Bonneuil C. (Eds). Nature et Environnement. Vol. 3, Les sciences hors d'Occident au XXe siècle, ORSTOM, Paris.
  2. ↑ 2.00 2.01 2.02 2.03 2.04 2.05 2.06 2.07 2.08 2.09 2.10 2.11 2.12 2.13 2.14 2.15 2.16 2.17 2.18 2.19 2.20 2.21 2.22 2.23 2.24 2.25 Ries MW, Adriaansen C, Aldobai S, Berry K, Bal AB, Catenaccio MC, Cigliano MM, Cullen DA, Deveson T, Diongue A, Foquet B, Hadrich J, Hunter D, Johnson DL, Pablo Karnatz J, Lange CE, Lawton D, Lazar M, Latchininsky AV, Lecoq M, Le Gall M, Lockwood J, Manneh B, Overson R, Peterson BF, Piou C, Poot-Pech MA, Robinson BE, Rogers SM, Song H, Springate S, Therville C, Trumper E, Waters C, Woller DA, Youngblood JP, Zhang L, Cease A (2024) Global perspectives and transdisciplinary opportunities for locust and grasshopper pest management and research. Journal of Orthoptera Research 33(2): 169–216. doi:10.3897/jor.33.112803.
  3. ↑ Künckel d'Herculais J (1905) Invasion des acridiens, vulgo sauterelles, en Algérie (1893–1905). Imprimerie administrative et commerciale Giralt, Alger. 3 Vols.
  4. ↑ 4.0 4.1 Lecoq M (2005) Desert locust management: from ecology to anthropology. Journal of Orthoptera Research: 179–186. https://doi.org/10.1665/1082-6467(2005)14[179:DLMFET]2.0.CO;2
  5. ↑ Uvarov, B.P. (1921) A revision of the genus Locusta, L. (=Pachytylus, Fieb.), with a new theory as to the periodicity and migrations of locusts. Bulletin of Entomological Research 12: 135–163. https://doi.org/10.1017/S0007485300044989
  6. ↑ 6.0 6.1 Pener MP (1991) Locust phase polymorphism and its endocrine relations. Advances in Insect Physiology 23: 1–79. https://doi.org/10.1016/S0065-2806(08)60091-0
  7. ↑ 7.0 7.1 Pener MP, Simpson SJ (2009) Locust phase polyphenism: an update. Advances in Insect Physiology 36: 1–272. https://doi.org/10.1016/S0065-2806(08)36001-9
  8. ↑ Uvarov BP (1923) Notes on Locusts of Economic Importance, with some new Data on the Periodicity of Locust Invasion. Bulletin of Entomological Research 14: 31–39. https://doi.org/10.1017/S0007485300028182
  9. ↑ King HH (1921) The migratory locust (Schistocerca peregrina Oliver). Wellcome Tropical Research Laboratories Entomology Section Bulletin 12: 14 pp. figs. 7.
  10. ↑ Johnston HB (1926a) A further contribution to our knowledge of the bionomics and control of the migratory locust, Schistocerca gregaria Forsk. (peregrina Oliv.), in the Sudan. Welcome Tropical Research Laboratory Entomology Section Bulletin 22: 14 pp.
  11. ↑ Johnston HB (1926b) New facts regarding the phases of migratory locusts. Nature 118: 10–11. https://doi.org/10.1038/118010b0
  12. ↑ Lecoq M, Cease AJ (2022) Are Mycopesticides the Future of Locust Control? Agronomy 2022, 12, 2344. https://doi.org/10.3390/agronomy12102344
  13. ↑ 13.0 13.1 13.2 Roy J (2001) Histoire d’un siècle de lutte anti-acridienne en Afrique. Contributions de la France. Paris: L’Harmattan Edition. 294 pp.
  14. ↑ Buj Buj A (2016) Plagas de langosta: De la plaga bíblica a la ciencia de la acridología. Serbal ed., Barcelona, Spain, 164 pp.
  15. ↑ Péloquin C (2013) Locust swarms and the spatial techno-politics of the French Resistance in World War II. Geoforum 49: 103–113. http://doi.org/10.1016/j.geoforum.2013.06.005
  16. ↑ Péloquin C (2014) Unruly Nature and Technological Authority: Governing Locust Swarms in the Sahel. University of Arizona. https://repository.arizona.edu/handle/10150/321308
  17. ↑ FAO (1968) Desert locust Project. Final Report. Report no. FAO/SF:34/DLC. Food and Agriculture Organization ​​of the United Nations, Rome.
  18. ↑ Hafraoui A, McCulloch L (1993) Present practices of controlling desert locust outbreaks. In: Atelier International de la FAO sur la recherche et la planification en matière de lutte contre le Criquet pèlerin tenu à Marrakech (Maroc). 24–28 May. Food and Agriculture Organization, Rome.
  19. ↑ Magor JI, Ceccato P, Dobson HM, Pender J, Ritchie L (2005) Preparedness to prevent desert locust plagues in the Central region, an historical review. Report No. AGP/DL/DS/35. desert locust Technical Series. Food and Agriculture Organisation, Rome.
  20. ↑ Waloff N, Popov GB (1990) Sir Boris Uvarov: the father of acridology. Annual Review of Entomology 35: 1–24.
  21. ↑ Kennedy JS (1939) The behaviour of the desert locust (Schistocerca gregaria) (Forskål) (Orthoptera) in an outbreak centre. Transactions of the Royal Entomological Society of London 89: 385–542. https://doi.org/10.1111/j.1365-2311.1939.tb00735.x
  22. ↑ Kennedy JS (1956) Phase transformation in locust biology. Biological Reviews 31: 349–370. https://doi.org/10.1111/j.1469-185X.1956.tb01595.x
  23. ↑ Ellis PE (1956) Differences in social aggregation in two species of locust. Nature 178: 1007. https://doi.org/10.1038/1781007a0
  24. ↑ Ellis PE (1963a) The influence of some environmental factors on learning and aggregation in locust hoppers. Animal Behaviour 11: 142–151. https://doi.org/10.1016/0003-3472(63)90022-8
  25. ↑ Ellis PE (1963b) Changes in the social aggregation of locust hoppers with changes in rearing conditions. Animal Behaviour 11: 152–160. https://doi.org/10.1016/0003-3472(63)90023-X
  26. ↑ Ellis PE, Pearce A (1962) Innate and learned behaviour patterns that lead to group formation in locust hoppers. Animal Behaviour 10: 305–318. https://doi.org/10.1016/0003-3472(62)90054-4
  27. ↑ Ellis PE (1950) Marching in locust hoppers of the solitary phase. Nature 166: 151. https://doi.org/10.1038/166151b0
  28. ↑ Ellis PE (1951) The marching behaviour of hoppers of the African migratory locust (Locusta migratoria migratorioides R. & F.) in the laboratory. Anti-Locust Bulletin 7: 1–46.
  29. ↑ Ellis PE (1964a) Marching and colour in locust hoppers in relation to social factors. Behaviour 23: 177–192. https://www.jstor.org/stable/4533088
  30. ↑ Ellis PE (1964b) Changes in marching of locusts with rearing conditions. Behaviour 23: 193–202. https://www.jstor.org/stable/4533089
  31. ↑ Gillett SD (1968) Airborne factor affecting the grouping behaviour of locusts. Nature 218: 782-783.
  32. ↑ Gillett SD (1972) Social aggregation of adult Schistocerca gregaria and Locusta migratoria migratorioides in relation to the final moult and ageing. Animal Behavior 20: 526-533. https://doi.org/10.1016/S0003-3472(72)80017-4
  33. ↑ Gillett SD (1973) Social determinants of aggregation behaviour in adults of the desert locust. Animal Behavior 21: 599–606. https://doi.org/10.1016/S0003-3472(73)80022-3
  34. ↑ Nolte DJ, Eggers SH, May IR (1973) A locust pheromone: Locustol. Journal of Insect Physiology 19: 1547–1554. https://doi.org/10.1016/0022-1910(73)90084-X
  35. ↑ Ellis PE, Hoyle G (1954) A physiological interpretation of the marching of hoppers of the African migratory locust (Locusta migratoria migratorioides R. & F.). Journal of Experimental Biology 31: 271–279. https://doi.org/10.1242/jeb.31.2.271
  36. ↑ Ellis PE, Carlisle DB (1961) The prothoracic gland and colour change in locusts. Nature 190: 368–369. https://doi.org/10.1038/190368a0
  37. ↑ Pener MP, Yerushalmi Y (1998) The physiology of locust phase polymorphism: an update. Journal of Insect Physiology 44: 365–377. https://doi.org/10.1016/s0022-1910(97)00169-8
  38. ↑ Descamps M (1953) Observations relatives au criquet migrateur africain et à quelques autres espèces d’Acridae du Nord-Cameroun. Agronomy Tropical, Nogent 8: 567–613.
  39. ↑ Remaudière G (1954) Etude écologique de Locusta migratoria migratorioides Rch. Et Frm. (Orth. Acrididae) dans la zone d’inondation du Niger en 1950. Locusta 2: 248 pp.
  40. ↑ Davey JT (1959) The African Migratory Locust (Locusta migratoria migratorioides Rch. & Frm. Orth.) in the Central Niger Delta. Part two: The ecology of Locusta in the semi-arid lands and seasonal movements of populations. Locusta 7: 180 pp.
  41. ↑ Farrow R (1975) The African Migratory Locust on its main outbreak area of the Middle Niger: quantitative studies of solitary populations in relation to environmental factors. Locusta 11: 198 pp.
  42. ↑ Têtefort JP, Wintrebert D (1967) Ecologie et comportement du criquet nomade dans le Sud-Ouest malgache. Annales de la Société entomologique de France 3: 3–30.
  43. ↑ Chapman RF (1959) Field observations on the behaviour of hoppers of the red locust (Nomadacris septemfasciata Serville). Anti-Locust Bulletin 33: 51 pp.
  44. ↑ Dean GJW (1968) Studies of factors affecting the formation of hopper bands of the Red Locust (Nomadacris septemfasciata) in an outbreak area. Journal of Applied Ecology 5: 273–290.
  45. ↑ Morant V (1947) Migrations and breeding of the Red locust (Nomadacris septemfasciata Serville) in Africa, 1927​​–1945. Anti-Locust Memoir 2: 1–60.
  46. ↑ Scheepers CC, Gunn DL (1958) Enumerating populations of adults of the Red Locust Nomadacris septemfasciata (Serville), in its outbreak areas in East and Central Africa. Bulletin of Entomological Research 49: 273–285. https://doi.org/10.1017/S0007485300053608
  47. ↑ Symmons PM (1963) The patterns of distributions of adults of the Red Locust (Nomadacris septemfasciata Serville) in an outbreak area. Entomologia experimentalis et Applicata 6:123–132. https://doi.org/10.1111/j.1570-7458.1963.tb00609.x
  48. ↑ Vesey-Fitzgerald DF (1964) Ecology of the Red Locust. Monographiae biologicae 14:255–268.
  49. ↑ Popov GB (1965) Review of the work of the Desert Locust Ecological Survey June 1958–March 1964 and the considerations and conclusions arising from it. Rome. FAO Rep. no. UNSF/DL/ES/8: 80 pp.
  50. ↑ Popov GB (1997) Atlas of Desert Locust Breeding Habitat. Food and Agriculture Organization of the United Nations, Rome.
  51. ↑ Launois M (1974) Influence du facteur pluviométrique sur l’évolution saisonnière du Criquet migrateur en phase solitaire et sur sa grégarisation à Madagascar. Ministère de la coopération, Paris. 272 pp.
  52. ↑ Lecoq M (1975) Les déplacements par vol du Criquet migrateur malgache en phase solitaire : leur importance sur la dynamique des populations et la grégarisation. Ministère de la Coopération (Paris): 272. https://doi.org/10.13140/RG.2.2.35380.55683
  53. ↑ Lecoq M (1995) Forecasting systems for migrant pests. III. Locusts and grasshoppers in West Africa and Madagascar. In: Drake VA and Gatehouse AG (Eds) Insect migration: physical factors and physiological mechanisms. Cambridge University Press, Cambridge. 377–395.
  54. ↑ Maiga IH, Lecoq M, Kooyman C (2008) Ecology and management of the Senegalese grasshopper Oedaleus senegalensis (Krauss 1877) (Orthoptera: Acrididae) in West Africa: review and prospects. Annales de la Société entomologique de France 44: 271–288. https://doi.org/10.1080/00379271.2008.10697563
  55. ↑ Roessingh P, Simpson SJ (1984) Volumetric feedback and the control of meal size in Schistocerca gregaria. Entomologia Experimentalis et Applicata 36: 279–286. https://doi.org/10.1111/j.1570-7458.1984.tb03440.x
  56. ↑ Roessingh P, Simpson SJ, James S (1993) Analysis of phase-related changes in behaviour of desert locust nymphs. Proceedings of the Royal Society B: Biological Sciences 252: 43–49. https://www.jstor.org/stable/49916
  57. ↑ Odihambo TR (1965) Metabolic effects of corpus allatum hormone, in the desert locust, Schistocerca gregaria. Nature 207: 1314. https://doi.org/10.1038/2071314b0
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  59. ↑ Torto B, Obeng-Ofori D, Njagi PGN, Hassanali A, Amiani H (1994) Aggregation pheromone system of adult gregarious desert locust, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae). Journal of Chemical Ecology 20: 1749–1762. https://doi.org/10.1007/BF02059896
  60. ↑ Torto B, Njagi PGN, Hassanali A, Amiani H (1996) Aggregation pheromone system of nymphal gregarious desert locust, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae). Journal of Chemical Ecology 22: 2273–2281. https://doi.org/10.1007/BF02029546
  61. ↑ Hassanali A, Torto B (1999) Grasshoppers and locusts. In Pheromones of NonLepidopteran Insects Associated with Agricultural Plants, ed. J Hardie, AK Minks, pp. 305–28. Oxon: CABI Publication
  62. ↑ Hassanali A, Njagi PGN, Bashir MO (2005) Chemical ecology of locusts and related Acridids. Annual Review of Entomology 50: 223–45 doi:10.1146/annurev.ento.50.071803.130345
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