Isotopic (δ2H and δ13C) tracing the provenance and fate of individual fatty acids fueling migrating animals: A case study of the monarch butterfly (Danaus plexippus) (original) (raw)
Related papers
Conservation Physiology
The eastern population of the North American monarch butterfly (Danaus plexippus) overwinters from November through March in the high-altitude (3000 m+) forests of central Mexico during which time they rely largely on stored lipids. These are acquired during larval development and the conversion of sugars from floral nectar by adults. We sampled fall migrant monarchs from southern Canada through the migratory route to two overwintering sites in 2019 (n = 10 locations), 2020 (n = 8 locations) and 2021 (n = 7 locations). Moderate to extreme droughts along the migratory route were expected to result in low lipid levels in overwintering monarchs but our analysis of lipid levels of monarchs collected at overwintering sites indicated that in all years most had high levels of lipids prior to winter. Clearly, a significant proportion of lipids were consistently acquired in Mexico during the last portion of the migration. Drought conditions in Oklahoma, Texas and northern Mexico in 2019 resu...
2019
Using stable isotope measurements of inert tissues to determine origins and migratory patterns is well established. However, isotopically determining nutritional origins of lipids, the primary fuel of migration, has not been attempted. I explored isotopic links between diet and stored lipids in captive White-throated Sparrows (Zonotrichia albicollis) and true armyworm moths (Mythimna unipuncta) using δ 13 C and δ 2 H measurements. Isotopic discrimination between body lipids and diet was established as linear calibration functions. Isotopic uptake following a diet switch in moths was used to trace lipid accumulation over time. Isotopic correlations between breath metabolic by-products of fed and fasted sparrows were explored as indicators of lipid use. This study established isotopic (δ 13 C, δ 2 H) linkages between diet and stored lipids for migratory insects and passerines and advocates the use stable isotopes in lipids as a tool to evaluate nutrient origins and allocation strategies in a variety of migratory species.
Fueling the fall migration of the monarch butterfly
Integrative and Comparative Biology, 2006
Synopsis Monarch butterflies in eastern North America accumulate lipids during their fall migration to central Mexico, and use them as their energy source during a 5 month overwintering period. When and where along their migratory journey the butterflies accumulate these lipids has implications for the importance of fall nectar sources in North America. We analyzed the lipid content of 765 summer breeding and fall migrant monarch butterflies collected at 1 nectaring site in central Virginia over 4 years (1998)(1999)(2000)(2001), and compared them with 16 additional published and unpublished datasets from other sites, dating back to 1941. Virginia migrants store significantly more lipid than summer butterflies, and show significant intraseason and between-year variation. None of the Virginia samples, and none of the historical samples, with one exception, had lipid levels comparable with those found in migrants that had reached Texas and northern Mexico. This evidence suggests that upon reaching Texas, the butterflies undergo a behavioral shift and spend more time nectaring. The one exceptional sample led us to the discovery that monarchs that form roosts along their migratory routes have higher lipid contents than monarchs collected while nectaring at flowers. We propose that for much of their journey monarchs are opportunistic migrants, and the variation within and between samples reflects butterflies' individual experiences. The stored lipids appear to be of less importance as fuel for the butterflies' migration than for their survival during their overwintering period, in part because soaring on favorable winds reduces the energetic cost of flying. The conservation of nectar plants in Texas and northern Mexico is crucial to sustaining the monarch's migratory spectacle, and nectar abundance throughout eastern North America is also important. As generalists in their selection of nectar sources and nectaring habitats, monarchs are unlikely to be affected by small changes in plant communities. Agricultural transformations of natural communities in the eastern United States and Great Plains, however, and especially the extensive planting of genetically modified herbicide-resistant soybeans and corn, may be changing the availability of nectar for monarchs and other pollinators. This new technology is eliminating virtually all forbs in and surrounding agricultural fields, including the monarch's larval hostplants (milkweeds) and native and nonnative nectar sources. To evaluate whether changes in nectar availability are altering the butterflies' ability to accumulate energy, we recommend that monarchs' lipid contents be assayed annually at sites throughout eastern North America.
Naturwissenschaften, 1997
1. Gadagkar, R., in: Social Biology of Wasps, p. 149 (KG Ross, RW Mat-thews, eds.) Ithaca, New York: Cornell University Press 1991 2. Reeve, HK, in: Social Biology of Wasps, p. 99 (KG Ross, RW Matthews, eds.). Ithaca, New York: Cornell Univer-sity Press 1991 3. West-...
Comparative Biochemistry and Physiology Part A: Physiology, 1992
Phospholipid fatty acid compositions of whole animals from all life stages of the gypsy moth Lymanrria dispar and the fatty acid compositions of total lipids of their larval culture medium were determined. 2. The major components of the larval diet and the insect tissues were the Cl6 and Cl8 saturated and unsaturated fatty acids that are expected in plant and insect lipids. 3. The fatty acid profiles of the insects and of their larval diet were different. 4. There were small differences in fatty acid profiles of phospholipids and triacylglycerols from different life stages of the gypsy moths, and substantial differences between phospholipids and triacylglycerols within life stages. 5. Certain Cl8 and C20 polyunsaturated fatty acids (PUFAs) that were not present in the diets were detected in the insect tissue phospholipids. 6. Biosynthesis of certain PUFAs from 18:2n-6 and from 18: 3n-3 is inferred from these observations. help in rearing the gypsy moths, and Arthur Bridgeford for diet processing. This is paper 9681, journal series, Nebraska Agricultural Research Division, and contribution 771 of the Department of Entomology, University of Nebraska-Lincoln. These investigations were supported by the University of Nebraska Agricultural Research Division, the
2005
It is a nutritional challenge for nectar-feeding insects to meet the amino acid requirements of oviposition. Here we investigate whether egg amino acids derive from larval diet or are synthesized from nectar sugar in four species of butterfly: Colias eurytheme, Speyeria mormonia, Euphydryas chalcedona, and Heliconius charitonia. These species exhibit a range of life history and differ in degree of shared phylogeny. We use 13 C differences among plants to identify dietary sources of amino acid carbon, and we measure amino acid 13 C using compoundspecific stable isotope analysis. Egg essential amino acids derived solely from the larval diet, with no evidence for metabolic carbon remodeling. Carbon in nonessential amino acids from eggs derived primarily from nectar sugars, with consistent variation in amino acid turnover. There was no relationship between the nonessential amino acids of eggs and host plants, demonstrating extensive metabolic remodeling. Differences between species in carbon turnover were reflected at the molecular level, particularly by glutamate and aspartate. Essential amino acid 13 C varied in a highly consistent pattern among larval host plants, reflecting a common isotopic "fingerprint" associated with plant biosynthesis. These data demonstrate conservative patterns of amino acid metabolism among Lepidoptera and the power of molecular stable isotope analyses for evaluating nutrient metabolism in situ.
Frontiers in Ecology and Evolution
The measurement of naturally occurring stable hydrogen (δ 2 H) and carbon (δ 13 C) isotopes in wings of the eastern North American monarch butterflies (Danaus plexippus) have proven useful to infer natal origins of individuals overwintering in Mexico. This approach has provided a breakthrough for monarch conservation because it is the only viable means of inferring origins at continental scales. Recently, routine simultaneous analyses of tissue δ 2 H and δ 18 O of organic materials has emerged leading to questions of whether the dual measurement of these isotopes could be used to more accurately infer spatial origins even though the two isotopes are expected to be coupled due to the meteoric relationship. Such refinement would potentially increase the accuracy of isotopic assignment of wintering monarchs to natal origin. We measured a sample of 150 known natal-origin monarchs from throughout their eastern range simultaneously for both δ 2 H and δ 18 O wing values. Wing δ 2 H and δ 18 O values were correlated (r 2 = 0.42). We found that wing δ 2 H values were more closely correlated with amount-weighted growing season average precipitation δ 2 H values predicted for natal sites (r 2 = 0.61) compared to the relationship between wing δ 18 O values and amount-weighted growing season average precipitation δ 18 O values (r 2 = 0.30). This suggests that monarch wing δ 2 H values will be generally more useful in natal assignments than δ 18 O values. Spatial information related to the use of deuterium excess in environmental waters was similarly found to be not useful when applied to monarch wings likely due to the considerable variance in wing δ 18 O values. Nonetheless, we recommend further testing of monarch wing δ 2 H and δ 18 O values from known natal sites with an emphasis on field data across a strong gradient in precipitation deuterium excess.
Frontiers in Ecology and Evolution
Emergent insects represent a key vector through which aquatic nutrients are transferred to adjacent terrestrial food webs. Aquatic fluxes of polyunsaturated fatty acids (PUFA) from emergent insects are particularly important subsidies for terrestrial ecosystems due to high PUFA contents in several aquatic insect taxa and their physiological importance for riparian predators. While recent meta-analyses have shown the general dichotomy in fatty acid profiles between aquatic and terrestrial ecosystems, differences in fatty acid profiles between aquatic and terrestrial insects have been insufficiently explored. We examined the differences in fatty acid profiles between aquatic and terrestrial insects at a single aquatic-terrestrial interface over an entire growing season to assess the strength and temporal consistency of the dichotomy in fatty acid profiles. Non-metric multidimensional scaling clearly separated aquatic and terrestrial insects based on their fatty acid profiles regardles...
Chemoecology, 2017
The application of fatty acids (FAs) as biomarkers in food web ecology is based on the concept of dietary routing, i.e., FA assimilation as entire molecule and transfer into consumer tissue with no or minor modification. However, the lack in knowledge in lipid metabolism of the soil fauna hampers the FA trophic marker approach. This study used labeled palmitic acid (13 C16:0, 99 atom%) as tracer in lipid pathways of two common soil Collembola, Heteromurus nitidus and Protaphorura fimata. The incorporation and dietary routing of this precursor were determined by 13 C: 12 C FA analysis (gas chromatographycombustion-isotope-ratio-monitoring), while metabolic modifications were assessed with isotopologue profiling (mass spectrometry with single ion monitoring). The 13 C enrichment in FAs assigned the transfer of the labeled precursor predominantly into the neutral lipid fraction of Collembola. Thereby, isotopologue profiling demonstrated that dietary routed FAs are marginally metabolically modified. In contrast, the phospholipid fraction showed a considerable degree of FA modification, most markedly a fast degradation of palmitoleic acid. Further, de novo synthesis of linoleic acid was approved for both Collembola species. While 16:0 and 18:0, and their descendants 16:1x7 and 18:1x9, followed the concept of dietary routing and thus are good markers, arachidonic acid showed a different metabolism. This comprised elongation/desaturation of 13 C16:0 and de novo synthesis, including 13 C labeled acetyl-CoA from degradation of the precursor, indicating its utility to assign carbon flow but not as trophic marker. We propose isotopologue profiling as a valuable tool for evaluation of the lipid metabolism in small soil animals to disentangle trophic interactions.