Food quality of anemophilous plant pollen for zooplankton

Abstract

Pollen rain can lead to considerable allochthonous particulate organic carbon input into freshwater systems. However, the importance of allochthonous pollen deposition for zooplankton production has not so far been considered. Here, standardized growth experiments were performed to assess the quality of pollen from three species (Alnus sp., Populus sp., and Cedrus sp.) as a food source for two cladocerans (Daphnia longispina and Simocephalus vetulus). Although lipid analysis revealed high polyunsaturated fatty acid (PUFA) contents in pollen, both cladoceran species exhibited suboptimal development when directly fed on pollen (ranging from 0.2 d 21 to 0.3 d 21 ). The low food value of pollen was attributed to the presence of a refractory wall reducing its digestibility. In a second set of experiments, cladocerans were fed on a mixture of heterotrophic microorganisms (bacteria, chytrids, and protozoa) that had grown on pollen grains (Cedrus sp.). The introduction of microorganisms as an intermediate trophic level resulted in cladoceran growth rates that were about double those obtained on pollen alone. Hence, our findings suggest that pollen carbon could sustain zooplankton growth indirectly, and highlight the key role of microorganisms, and especially of chytrids, in transferring and upgrading pollen PUFA to higher trophic levels.

How pollen organic matter enters freshwater food webs

“…Thus, we can reasonably assume that accumulation of pollen grains at the water-air interface and development of key microorganisms such as zoosporic chytrid fungi may have initiated a pollen-based microbial food web in the neustonic compartment. In a previous experimental study, such a pollen-based microbial food web was shown to transfer pollen carbon and upgrade its quality to promote zooplankton growth, especially by adding some long-chain PUFA, such as eicosapentaenoic acid (20:5v3; Masclaux et al 2011). Trophic upgrading of food quality by microorganisms has been associated with increasing digestibility and essential lipid compound production (such as C20 and C22-PUFA; Bec et al 2006).…”

“…The method used for lipid analysis was fully described in Masclaux et al (2011). Once extracted, FA were converted into FA methyl-esters (FAME) by acid-catalyzed transesterification and analyzed on an Agilent technologies 6850 gas chromatograph.…”

“…All three characteristics have been used as criteria for high-quality food source for zooplankton (Sterner and Hessen 1994;Brett and Mü ller-Navarra 1997). A recent experimental study (Masclaux et al 2011), however, showed that anemophilous plant pollen alone could not promote zooplankton growth, and its poor food quality has been attributed to its low digestibility. Pollen grains are protected by an extracellular wall (the exine) that makes them highly resistant even to microbial degradation (Stanley and Linskens 1974).…”

“…The strong tendency of these fungi to form multiple infections of individual pollen grains weakens the wall and undoubtedly facilitates their further decomposition by other biological agents (Goldstein 1960). Therefore, in aquatic ecosystems, chytrid infection of pollen grains could initiate the formation of a microbial food web composed of chytrid zoospores, heterotrophic bacteria, and protozoan grazers, all of which have been shown to transfer pollen carbon and upgrade their quality to zooplankton in controlled experiments (Masclaux et al 2011).…”

“…The mineral and biochemical composition of pollen is characterized by a high content of phosphorus (Banks and Nighswander 2000) and polyunsaturated fatty acids (FAs), such as linoleic acid, 18:2v6, and a-linoleic acid, 18:3v3 (Masclaux et al 2011). In addition, most pollen grains are within the size range of particles consumed by filter-feeding zooplankton.…”