Minimally invasive collection of adipose tissue facilitates the study of eco‐physiology in small‐bodied mammals

Abstract

Summary Adipose tissue is the primary fuel storage for vertebrates and is an important component of energy budgets during periods of peak energetic demands. Investigating the composition of adipose tissue can provide information about energetics, migration, reproduction and other life‐history traits. Until now, most field methods for sampling adipose tissue of small‐bodied vertebrates have been destructive. Therefore, investigations of adipose tissue in small‐bodied vertebrates have been limited in their broadscale application. We developed a field‐ready micro‐adipose biopsy method for sampling adipose tissue of small‐bodied vertebrates, by adopting fine‐needle adipose aspiration. We applied the method to silver‐haired bats (Lasionycteris noctivagans) and then quantified the resulting fatty acid signatures of a summer group and an autumn group to demonstrate one possible application of the method. We successfully obtained interpretable fatty acid signatures from 74·5% of micro‐adipose biopsy attempts, with success positively correlated with body mass index. Summer and autumn groups of bats had different fatty acid signatures likely representing varied available dietary compositions at resident sites (the habitat where adipose deposits are accumulated prior to migration). The fatty acid profile of autumn silver‐haired bats was largely characterized by 16:0, 18:1 and 14:0, and the summer group was characterized by 16:0, 16:1 and 18:0. Our results suggest that fatty acid signatures have the potential to characterize the origins of migrating individuals, or the number of unique subpopulations being supported by a migration route. This field‐ready fine‐needle adipose aspiration method can be used on small‐bodied mammals and modified for application to other small‐bodied vertebrates. This non‐destructive approach to sampling adipose tissue has great value because it allows for robust sample sizes, longitudinal studies of the same individuals across space and time, and sampling of rare, threatened and endangered species.

White adipose tissue remodeling in Little Brown Myotis (Myotis lucifugus) with white-nose syndrome

“…Sample collection has typically included wing biopsies/wipes [56, 57], blood [58], saliva [59], and fecal samples [60]. In addition, adipose tissue biopsies have been used to measure changes in lipid content by fatty acid profiling via chemical derivatization to fatty acid methyl ester (FAME) analysis [25, 45]. Although derivatization can increase sensitivity that is useful for low tissue masses, a limitation inherent to FAME analysis is that structural information is lost after fatty acid cleavage from their headgroup (e.g., glycerol, sphingosine, cholesterol), and fractionation of lipid subclasses prior to analysis is a tedious process [61].…”

“…The optimal tissue weight for analysis fell between ∼0.5 – 10 mg, at which we see a loss of linearity (primarily in TAGs) with tissue weights over 10 mg (Supplementary Fig 1). Excellent linearity (R 2 > 0.99, ePE R 2 = 0.97) was observed between 0.62 – 6.29 mg tissue weights; however, for the broad classes that are found in naturally lower proportion in WAT (e.g., CERs, CEs, acylcarnitines, and minor GPs and LGPs), several compounds will not be detected in smaller tissue biopsies, which needs to be considered if attempting to analyze small micro-adipose samples from nonlethal sampling [25]. Although, it is important to note that these results are highly instrument specific and newer platforms offer improved sensitivity and dynamic range for detecting lower concentration compounds in biological samples.…”

Rates of seasonal fuel loading do not differ by sex or overwintering strategy in three species of bats

“…Northern California is a unique study system because its relatively mild climates allow some species to be active year-round. Though silver-haired bats are considered migrants, some individuals may be year-round residents but the majority of the autumn and winter population, particularly females, are expected to be composed of individuals that migrate from elsewhere (Clerc et al 2017) and both sexes are active during winter (Falxa 2007; Weller and Stricker 2012). Although their winter ecology is not well understood, California Myotis are more active than Yuma Myotis during winter (Falxa 2007; Weller and Stricker 2012).…”