Comprehensive Screening Links Halogenated Organic Compounds with Testosterone Levels in Male Delphinus delphis from the Southern California Bight

Abstract

While environmental pollutants have been associated with changes in endocrine health in cetaceans, efforts to link contaminant exposure with hormones have largely been limited to a list of known, targeted contaminants, overlooking minimally characterized or unknown compounds of emerging concern. To address this gap, we analyzed a suite of potential endocrine disrupting halogenated organic compounds (HOCs) in blubber from 16 male short-beaked common dolphins ( Delphinus delphis) with known maturity status collected from fishery bycatch in the Southern California Bight. We employed a suspect screening mass spectrometry-based method to investigate a wide range of HOCs that were previously observed in cetaceans from the same region. Potential endocrine effects were assessed through the measurement of blubber testosterone. We detected 167 HOCs, including 81 with known anthropogenic sources, 49 of unknown origin, and 37 with known natural sources. The sum of 11 anthropogenic and 4 unknown HOC classes were negatively correlated with blubber testosterone. Evidence suggests that elevated anthropogenic HOC load contributes to impaired testosterone production in mature male D. delphis. The application of this integrative analytical approach to cetacean contaminant analysis allows for inference of the biological consequences of accumulation of HOCs and prioritization of compounds for future environmental toxicology research.

Figure 1:

A) The overall number and average relative abundance of halogenated organic compounds (HOCs) classified by origin (gray scale) among all samples. B) The average relative abundance (in log scale) and standard error of all compound classes by maturity type (black circles and gray triangles represent data from immature and mature animal samples, respectively). The * denotes compound classes with significantly different abundance between mature and immature animals, as determined by randomForest permutation tests.

Figure 1:

A) The overall number and average relative abundance of halogenated organic compounds (HOCs) classified by origin (gray scale) among all samples. B) The average relative abundance (in log scale) and standard error of all compound classes by maturity type (black circles and gray triangles represent data from immature and mature animal samples, respectively). The * denotes compound classes with significantly different abundance between mature and immature animals, as determined by randomForest permutation tests.

Figure 2:

A principal components analysis (PCA) plot of the loadings for all compound classes according to origin (anthropogenic, mixed, natural, or unknown). The drawn circle highlights the anthropogenic compound group and the compound classes contributing to this group are listed on the right. Within the group, compound classes with significant higher relative abundance according to the Random Forest are marked with an asterisk (*).

Figure 3:

Difference in average total number and relative abundance of compounds detected in confirmed immature and mature individuals. Compound classes that differed between immature and mature individuals were mostly of anthropogenic origin and some of unknown origin. No compound classes of natural origin differed between maturity groups.

Figure 4:

Regressions examining the relationship between the sum of the compound abundances in the anthropogenic contaminant group (AC group) compounds and blubber testosterone for age-corrected data combined (a) and the log-transformed mature-only, non-age-corrected contaminant sum (b). Black circles and triangles represent data from immature (I) and mature (M) animal samples, respectively) and color represents the age of mature individuals. Individuals below the dotted line have less testosterone than expected given the same gonad weight (and age for the age-corrected graph)

Figure 5:

The relative abundance of compound classes that increased predictive power of gonad weight adjusted testosterone concentration. Variable importance metrics (I) and p-values (p) are provided for each compound, where p-values below 0.05 were considered significant (*). Color denotes the origin of the compound (anthropogenic, unknown, or natural).