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High parasite diversity in the amphipod Gammarus lacustris in a subarctic lake

Citation

Shaw, Jenny et al. (2021), High parasite diversity in the amphipod Gammarus lacustris in a subarctic lake, Dryad, Dataset, https://doi.org/10.25349/D9B89T

Abstract

Amphipods are often key species in aquatic food webs due to their functional roles in the ecosystem and as intermediate hosts for trophically transmitted parasites. Amphipods can also host many parasite species, yet few studies address the entire parasite community of a gammarid population, precluding a more dynamic understanding of the food web. We set out to identify and quantify the parasite community of Gammarus lacustris to understand the contributions of the amphipod and its parasites to the Takvatn food web. We identified seven parasite taxa: a direct life cycle gregarine, Rotundula sp., and larval stages of two digenean trematode genera, two cestodes, one nematode, and one acanthocephalan. The larval parasites use either birds or fishes as final hosts. Bird parasites predominated, with trematode Plagiorchis sp. having the highest prevalence (69%) and mean abundance (2.7). Fish parasites were also common, including trematodes Crepidostomum spp., nematode Cystidicola farionis, and cestode Cyathocephalus truncatus (prevalences 13, 6, and 3%, respectively). Five parasites depend entirely on G. lacustris to complete their life cycle. At least 11.4% of the overall parasite diversity in the lake was dependent on G. lacustris, and 16% of the helminth diversity required or used the amphipod in their life cycles. These dependencies reveal that in addition to being a key prey item in subarctic lakes, G. lacustris is also an important host for maintaining parasite diversity in such ecosystems.

Methods

Study area and collection

Takvatn (69o07’N, 19o05’E) is a subarctic, oligotrophic, and dimictic lake in northern Norway that has been the focus of intensive ecological and food web studies for more than 30 years (details in Amundsen et al., 2009, 2013, 2019). The lake is situated 214 m above sea level with a surface area of 15 km2 and a maximum depth of ca 80 m. There is little macrovegetation in the lake, but the littoral zone (3-10 m depth) has dense beds of the grass-like macroalgae Nitella sp., which contain the highest abundances of G. lacustris (Frainer et al., 2016).

We sampled gammarids in the littoral zone (0-8 m depth) by dragging a benthic sled along Nitella sp. beds as described in Knudsen et al. (2001). Gammarids were collected from each haul, placed in buckets with lake water and vegetation, and brought back to the lab for dissection within 48 hours. Individuals not dissected within 24 hours were kept cool overnight in the refrigerator or outdoors (at approx. 4-8 oC). To obtain a broader range of parasite diversity in G. lacustris in the lake, gammarids were collected from five sites (L1-L5), including two in the vicinity of an important nesting area for birds (L4 and L5; Klemetsen and Knudsen, 2013). Sampling was carried out over three years during different times of the ice-free period (August and October 2012, June and September 2013, and August 2015). Not all sites were sampled every year.

Dissection and parasite identification

We blotted 474 amphipods on paper towels, measured length (eye to end of telson; mm) and wet weight (g). Due to potential variation in length measurements, we generated a length-weight regression from a subsample (y = 132.17x + 5.62, R2=0.95) and used weight-based estimates of length for all analyses. We compressed whole gammarids between glass plates (150 mm × 100 mm × 3.5 mm) and examined them under a stereo microscope (Leica Wild M3, maximum magnification of 40X). Parasites were counted and transferred for further inspection under a compound microscope if needed. Parasites were identified to the nearest taxonomic level based on morphology, and select specimens were preserved in 95% ethanol for genetic analysis in a separate study (trematodes only; details in Soldánová et al., 2017) or formalin for further identification (all other parasites).

Statistical analyses

We characterized the parasitism in G. lacustris samples by calculating prevalence, mean intensity, and mean abundance (defined in Bush et al., 1997) and assessed parasite infra-community composition using the 7-set Venn diagram “Adelaide” (Dusa, 2020). We investigated whether the infections of parasites with indirect life cycles varied between sampling locations and sampling period, using two analyses. To analyze if the abundance of Plagiorchis sp. differed between sampling locations and periods, we used a mixture model (zero-inflated negative bionomial generalized linear model (ZINB GLM); R (version 3.5.1; R Core Team, 2018), with G. lacustris size (length) as a covariate (Zuur et al., 2009). The ZINB GLM contains two parts; a negative binomial GLM that models parasite counts and a binomial GLM that models the probability of observing excess zeros above those of the count process (Zuur et al., 2009). Other parasite species were low in intensity so we used infection status (infected versus uninfected) rather than abundance as the binomial response variable in logistic regressions with the same predictor variables (sampling location, period, and G. lacustris size).

Funding

Norwegian Research Council, Award: NFR 213610