Behavioral thermoregulation in Locusta migratoria manilensis (Orthoptera: Acrididae) in response to the entomopathogenic fungus, Beauveria bassiana

• Published in: PloS one Vol. 13; no. 11; p. e0206816
• Main Authors: Sangbaramou, Rouguiatou, Camara, Ibrahima, Huang, Xin-Zheng, Shen, Jie, Tan, Shu-Qian, Shi, Wang-Peng
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 28.11.2018; Public Library of Science (PLoS)
• Subjects: Acrididae; Agriculture - methods; Animals; Ascomycota; Beads; Beauveria - pathogenicity; Beauveria - physiology; Beauveria bassiana; Behavior; Behavior, Animal - physiology; Biology; Biology and Life Sciences; Body temperature; Body Temperature Regulation - immunology; Entomopathogenic fungi; Environmental conditions; Environmental impact; Environmental quality; Fever; Fluorescein; Fluorescein isothiocyanate; Fungi; Germination; Grasshoppers; Hemocytes; Hemocytes - immunology; Hemolymph; Hemolymph - cytology; Hemolymph - immunology; Host Microbial Interactions - immunology; Hyphae - physiology; Immune system; Immunology; Infections; Inoculation; Insects; Locusta migratoria; Locusta migratoria - microbiology; Locusta migratoria - physiology; Locusts; Locusts (Insects); Medical research; Medicine and Health Sciences; Mycoses; Mycoses - immunology; Mycoses - microbiology; Mycoses - veterinary; Mycosis; Nymph - microbiology; Nymph - physiology; Orthoptera; Orthopterans; Parasites; Pathogenic microorganisms; Peptides; Pest Control, Biological - methods; Pesticides; Phagocytes; Phagocytes - immunology; Phagocytosis; Silica; Silicon dioxide; Temperature; Temperature effects; Thermoregulation; Thermoregulatory behavior; Thorax; Beijing China; China
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0206816

Insects such as locusts and grasshoppers can reduce the effectiveness of pathogens and parasites by adopting different defense strategies. We investigated the behavioral thermopreference of Locusta migratoria manilensis (Meyen) (Orthoptera: Acrididae) induced by the fungus Beauveria bassiana, and the impact this behavior had on the fungal mycosis under laboratory conditions. By basking in higher temperature locations, infected nymphs elevated their thoracic temperature to 30-32.6 °C, which is higher than the optimum temperature (25°C) for B. bassiana conidial germination and hyphal development. A minimum thermoregulation period of 3 h/day increased survival of infected locusts by 43.34%. The therapeutic effect decreased when thermoregulation was delayed after initial infection. The fungus grew and overcame the locusts as soon as the thermoregulation was interrupted, indicating that thermoregulation helped the insects to cope with infection but did not completely rid them of the fungus. A significant enhancement in the number of haemocytes was observed in infected thermoregulating locusts, reaching levels that were even higher than those observed in the controls. In contrast, haemocyte concentration was severely reduced in infected insects that did not thermoregulate. In infected non-thermoregulating locusts, the reduction in haemocyte number was accompanied by an increase in fungal blastospore concentration that was obvious in the haemolymph by day four. In contrast, no circulating blastospores were found in the haemolymph of infected thermoregulating locusts three days post-inoculation. We also examined the phagocytic activity of infected insects in vivo by using fluorescein isothiocyanate (FITC)-labelled silica beads. The proportion of beads that was engulfed by haemocytes in infected, thermoregulating insects was similar to that in the controls throughout the experiment, whereas the rate of phagocytosis in infected, non-thermoregulating insects progressively decreased after infection. These findings demonstrated that behavioural thermoregulation can adversely affect B. bassiana mycosis in infected L. migratoria manilensis, thereby limiting the development of lethal entomopathogenic fungi in locusts. This is apparently accomplished through an increase in the levels of haemocytes, leading to greater phagocytic activity under certain environmental conditions.