Can the stable isotope variability in a zooplankton time series be explained by its key species?

Abstract

Stable isotope (SI) analysis is a standard tool to study marine food webs, usually based on the measurement of a few individuals from a small list of subjectively pre-defined species. The main objective of this study was to find out which species are significantly associated with the temporal variability of the SI composition of zooplankton in a tropical marine ecosystem. We investigated this by means of a novel species-biomass-isotopes-mixture (SBIM) approach that uses a relative biomass matrix to explain the SI signature of the zooplankton community. Furthermore, SBIM was applied to detect key taxa that can be considered bioindicators for important descriptors of ecosystem state (e.g., oligotrophy, carbon sources, mean trophic level). Plankton samples (64 μm mesh size) were obtained in Tamandaré Bay (northeastern Brazil) from June 2013 to August 2019. One aliquot of each sample was taken for stable isotope measurements and one for taxonomic identification and estimation of size and relative biomass. Total zooplankton biomass differed significantly between years, seasons and stations. Total zooplankton δ13C values ranged from −21.0 to −18.2‰ (mean ± standard deviation: −19.7 ± 0.7‰ in the dry season, and −19.4 ± 0.8‰ in the rainy season). Total zooplankton δ15N values ranged from 3.8 to 9.0‰ (7.0 ± 1.0‰ in the dry season, and 6.5 ± 1.2‰ rainy season). Total zooplankton C/N ratios ranged from 3.5 to 5.0 (4.2 ± 0.4 in the dry season and 4.2 ± 0.3 in the rainy season). The sparsely abundant and relatively large-sized copepod Pseudodiaptomus acutus was the most important species for explaining the variability in δ15N (22% of the total variability). Relative biomass (%) of P. acutus showed a strong positive correlation with δ15N, indicating a high trophic level (TL). Our results highlight the importance of less abundant taxa for marine food webs. Small-sized invertebrate larvae were negatively correlated with δ15N, indicating a TL below average. The copepod Dioithona oculata was the most important organism in explaining the δ13C of zooplankton (17.7% of the total variability, positive correlation with δ13C), indicating possible selective use of a13C-enriched food source (e.g., diatoms) by this cyclopoid copepod. Oithona spp. juveniles showed a negative relationship with zooplankton C/N ratio, which can be indicators of an oligotrophic ecosystem state and lipid-poor zooplankton. The tintinnid F. ehrenbergii showed a positive correlation with C/N, being an indicator for turbid “green waters'', during the rainy season, when the ecosystem was in a eutrophic state, with high lipid contents in the zooplankton community. The proposed SBIM approach opens up a novel pathway to understanding the factors and species that shape the temporal variability of food webs.