Predator and prey biodiversity relationship and its consequences on marine ecosystem functioning-interplay between nanoflagellates and bacterioplankton

Abstract

The importance of biodiversity effects on ecosystem functioning across trophic levels, especially via predatory-prey interactions, is receiving increased recognition. However, this topic has rarely been explored for marine microbes, even though microbial biodiversity contributes significantly to marine ecosystem function and energy flows. Here we examined diversity and biomass of bacteria (prey) and nanoflagellates (predators), as well as their effects on trophic transfer efficiency in the East China Sea. Specifically, we investigated: (i) predator diversity effects on prey biomass and trophic transfer efficiency (using the biomass ratio of predator/prey as a proxy), (ii) prey diversity effects on predator biomass and trophic transfer efficiency, and (iii) the relationship between predator and prey diversity. We found higher prey diversity enhanced both diversity and biomass of predators, as well as trophic transfer efficiency, which may arise from more balanced diet and/or enhanced niche complementarity owing to higher prey diversity. By contrast, no clear effect was detected for predator diversity on prey biomass and transfer efficiency. Notably, we found prey diversity effects on predator-prey interactions; whereas, we found no significant diversity effect on biomass within the same trophic level. Our findings highlight the importance of considering multi-trophic biodiversity effects on ecosystem functioning in natural ecosystems.

Fig. 1

Conceptual diagram illustrating the studied hypotheses associated with diversity effects on trophic interactions. Hypothesis I: predator diversity (I-1) increases predator consumption and consequently prey biomass, which in turn elevates predator/prey biomass ratio (PPBR, a proxy for trophic transfer efficiency), or (I-2) weakens grazing pressure, and as a consequence releasing prey biomass from depression and reducing PPBR. Hypothesis II: prey diversity (II-1) promotes predator biomass and thus increases PPBR or (II-2) reduces predator production and biomass by hindering predation through diluting the proportion of edible prey and thus decreases PPBR. Hypothesis III: (III) prey diversity promotes predator diversity

Fig. 2

Relationships used to evaluate the aforementioned Hypotheses in Fig. 1. Hypothesis I: effects of predator diversity (Shannon diversity) on (a) prey (heterotrophic bacteria) biomass and (b) predator-prey biomass ratio (PPBR). Hypothesis II: effects of prey diversity on (c) predator biomass and (d) PPBR. Hypothesis III: (e) predator and prey diversity relationship. Note in a–d, the Y-axis is in log-scale with the base of 10. The circles and triangles represent the samples collected in the summer and spring seasons, respectively. The line indicates the best-fit linear regression line with significant (P < 0.05) relationship based on GLMM analysis with season as the random effect

Fig. 3

Bar-plot summarizing the relative strength (Pearson’s correlation, r) and its P-value of biodiversity effect on trophic interaction based on different diversity indices: richness (OTU), Shannon, Simpson, and phylogenetic diversity (PD), for the heterotopic bacterial prey. Hypothesis I: effects of predator diversity on (a) prey biomass and (b) predator-prey biomass ratio (PPBR). Hypothesis II: effects of prey diversity on (c) predator biomass and (d) PPBR. Hypothesis III: (e) predator and prey diversity relationship. Filled and open bars indicate positive and negative effects, respectively

Fig. 4

PLS-SEM analysis deciphering (a) the effect of Shannon diversity of heterotrophic nanoflagellates (HNFD, predator) and heterotrophic bacteria (HBD, prey) on their biomasses (HNFB and HBB), as well as (b) the effect of Shannon diversity of heterotrophic nanoflagellates (HNFD, predator) and autotrophic bacteria (ABD, prey) on their biomasses (HNFB and ABB). Both of the two analyses account for the effects of temperature (Tem), nutrient (Nut), and the interaction within individual trophic level (e.g., the relationship between HBD and HBB, as well as between HNFD and HNFB). Black and gray lines indicate the significant (P < 0.05), and non-significant (P > 0.05) relationships, respectively. The “gof” indicates the goodness of fit