Metamorphosis is an important developmental stage for holometabolous insects, during which adult morphology and physiology are established. Proper development relies on optimal body temperatures, and natural ambient temperature (Ta) fluctuations, especially in spring or in northern latitudes, could result in interruptions to development. It is unclear how low-Ta exposure may affect insects that are actively developing. To understand how suboptimal Ta may affect metamorphosing insects, we used the alfalfa leafcutting bee, Megachile rotundata (Fabricius), a solitary, cavity-nesting bee that spends its juvenile and pupal stages within a brood cell. We characterized suites of physiological traits, rather than just using a singular parameter to determine effects of sublethal Ta stress. Metamorphosing M. rotundata were exposed to either constant or fluctuating low-Ta stress and compared to control bees allowed to develop normally. All bees survived and emerged as adults, but the constant low-Ta-stressed bees were affected most severely. Male constant low-Ta-stressed bees had decreased flight performance (lower metabolic rate, shorter flight bouts, decreased wing length), suggesting that the stress altered muscular or neurological development. Constant low-Ta-stressed bees also had altered activity levels, providing more support for the hypothesis that low-Ta stress causes long-term neurological defects. Exposure to fluctuating low Ta also delayed development time for both sexes; males had decreased adult life span, and both sexes had shortened wings. Together, these results provide evidence for a critical developmental window during metamorphosis and suggest that there may be severe implications for bees in the wild that are exposed to low-Ta stressors.
Photoperiod is considered the universal zeitgeber, regulating physiological processes in numerous animals. However, for animals in light-restricted habitats (e.g. burrows or cavities), thermoperiod may be a more important cue. Our study tested this hypothesis in the alfalfa leafcutting bee, , which nests in cavities and undergoes development within a brood cell. We assessed the role of environmental cues (thermoperiod and photoperiod) on the process of adult emergence by examining: (1) whether those cues direct circadian rhythms, (2) which cue is more dominant and (3) how sensitive developing bees and emergence-ready adults are to cues. Although we found that 20% of light penetrates the brood cell, and bees respond to photoperiod by synchronizing emergence, thermoperiod is the dominant cue. When presented with a conflicting zeitgeber, bees entrained to the thermophase instead of the photophase. When temperature cues were removed, we observed free-running of emergence, indicating that underlying circadian mechanisms can be synchronized by daily fluctuations in temperature. We also found that emerging bees were highly sensitive to even small increases in temperature, entraining to a ramp speed of 0.33°C h The response and sensitivity to temperature cues suggest that evolved a temperature-mediated clock to time emergence from light-restricted cavities.
The alfalfa leafcutting bee, Megachile rotundata (F.), is a solitary, cavity-nesting bee and is the primary pollinator for alfalfa seed production. Bee management practices include cold storage during the prepupal stage. Fluctuating thermal regimes during cold storage increases survival of cold storage and allows a doubling of the cold storage period with no decrease in survival. However, survival, characterized as successful adult emergence, is not qualitative. In this study, we determined whether extended storage affects adult bee respiration or flight physiology. We overwintered bees for a single winter (current management protocol) or for 12 mo longer (extended storage). We used resting and tethered flight metabolic rates and resting critical PO2 (the oxygen partial pressure below which metabolism can no longer be sustained) as indices of adult bee quality. We found no significant differences in body mass, resting or flight metabolic rates, or critical PO2 between the two groups. Together these data indicate that extended storage of M. rotundata produces bees of similar respiratory capacity and flight ability. These findings could increase the use of M. rotundata as an alternative pollinator, allowing for extended storage to time adult emergence with early blooming crops.
Among animals, insects have the highest mass-specific metabolic rates; yet, during intermolt development the tracheal respiratory system cannot meet the increased oxygen demand of older stage insects. Using locomotory performance indices, whole body respirometry, and X-ray imaging to visualize the respiratory system, we tested the hypothesis that due to the rigid exoskeleton, an increase in body mass during the intermolt period compresses the air-filled tracheal system, thereby, reducing oxygen delivery capacity in late stage insects. Specifically, we measured air sac ventilation frequency, size, and compressibility in both the abdomen and femur of early, middle, and late stage sixth instar Schistocerca americana grasshoppers. Our results show that late stage grasshoppers have a reduced air sac ventilation frequency in the femur and decreased convective capacities in the abdomen and femur. We also used X-ray images of the abdomen and femur to calculate the total proportion of tissue dedicated to respiratory structure during the intermolt period. We found that late stage grasshoppers had a lower proportion of their body dedicated to respiratory structures, especially air sacs, which convectively ventilate the tracheal system. These intermolt changes make oxygen delivery more challenging to the tissues, especially critical ones such as the jumping muscle. Indeed, late stage grasshoppers showed reduced jump frequencies compared to early stage grasshoppers, as well as decreased mass-specific CO(2) emission rates at 3 kPa PO(2). Our findings provide a mechanism to explain how body mass changes during the intermolt period reduce oxygen delivery capacity and alter an insect's life history.
Individual heterogeneity within societies provides opportunities to test hypotheses about adaptive neural investment in the context of group cooperation. Here we explore neural investment in defense specialist soldiers of the eusocial stingless bee (Tetragonisca angustula) which are age sub-specialized on distinct defense tasks, and have an overall higher lifetime task repertoire than other sterile workers within the colony. Consistent with predicted behavioral demands, soldiers had higher relative visual (optic lobe) investment than non-soldiers but only during the period when they were performing the most visually demanding defense task (hovering guarding). As soldiers aged into the less visually demanding task of standing guarding this difference disappeared. Neural investment was otherwise similar across all colony members. Despite having larger task repertoires, soldiers had similar absolute brain size and smaller relative brain size compared to other workers, meaning that lifetime task repertoire size was a poor predictor of brain size. Together, our results are consistent with the specialized but flexible defense strategies of this species, broadening our understanding of how neurobiology mediates age and morphological task specialization in highly cooperative societies.
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