Elsevier

Protist

Volume 170, Issue 3, July 2019, Pages 283-286
Protist

Original Paper
Filter-feeding in Colonial Protists

https://doi.org/10.1016/j.protis.2019.04.002Get rights and content

Many protists form cell colonies. Among them several are filter-feeders depending on suspended food particles such as bacteria. It has been suggested that the formation of colonies enhances feeding efficiency and implied that – in the case of colonial choanoflagellates – it was an adaptive trait that led to the evolution of metazoans. Here it is shown experimentally – for a colonial peritrich ciliate and for a choanoflagellate – that colony-formation does not enhance the efficiency of filter-feeding relative to solitary cells and that the adaptive significance of cell colony-formation must have some other explanation.

Introduction

Many protists form cell colonies: cells do not separate following mitotic division, but remain attached in close contact or via branching stalks. The colonies reproduce by forming motile cells that detach from the colonies to form new colonies. It is clear that colony-forming protists potentially represent a step towards true multicellularity; that is, with a germline consisting of potentially immortal cells (the germ line) and somatic cells that are specialized for different functions, but have a limited lifespan thus allowing formation of tissue with special functions (e.g., Woodland 2016). With respect to some phototrophic lineages among the eukaryotes such as green algae and rhodophytes the evolution to multicellularity in this sense is well understood. With respect to the origin of metazoans it was more than a century ago suggested that choanoflagellates, among which several are colonial, represent the ancestors of sponges and by implication other metazoans due to the similarity of these flagellates to the choanocytes of sponges. More recently, molecular evidence and some structural details at the cellular level have shown that the choanoflagellates do, in fact, constitute a sister group to the metazoans and so the evolutionary role of choanoflagellates has drawn renewed interest (Leadbeater 2015). However, even in colonial choanoflagellates all cells retain the potential to form new colonies and are not “multicellular” in the above sense.

In this context it has been suggested that the efficiency of suspension feeding is enhanced if the cells form colonies and so – by implication – that this was a selective force that resulted in colony-formation among a number of choanoflagellate species (Cavalier-Smith, 2017, Roper et al., 2013) although this result was based only on theoretical considerations without experimental evidence. In the present contribution this is examined for a colonial peritrich ciliate (Zoothamnium dublicatum Kahl) and a species of colonial choanoflagellates: Codosiga botrytis Ehrenberg.

Section snippets

Peritrich Ciliates

Zoothamnium dublicatum forms stalked, branching colonies where the cells form a single slightly curved layer (canopy) with up to 15–20 cells. Since the spherical food vacuoles have a very uniform volume (115.0 μm3, SD = 14.2) they can, for comparative purpose, be used as a measure of feeding rate. Figure 1 shows the formation of food vacuoles formed in colonies with different cell numbers incubated in a suspension of 0.2 μm latex beads with a concentration of 2.1 × 106 ml−1. It is seen that the number

Discussion

The present results show that colony formation does not enhance the efficiency of filter feeding as previously suggested by Cavalier-Smith (2017) and by Roper et al. (2013). It is in all cases only a question of a number of pumps that work in parallel. A somewhat similar conclusion was drawn by Kirkegaard and Goldstein (2016) on a theoretical basis. The essential problem is that the cell colonies must have a structure so that a given parcel of water is not strained of food particles by more

Methods

Zoothamnium dublicatum was collected on the thallus of the rhodopyte Ceramium virgatum growing in shallow water in Aarhus Bay (East coast of Jutland, Denmark) and the algae were maintained in aerated seawater (salinity: ca. 20 ppt). Codosiga botrytis was collected on filamentous green algae growing in a freshwater tropical fish tank.

The measure of feeding efficiency referred to as clearance is the volume of water cleared of food particles per unit time. At low particle density this is equivalent

Acknowledgement

This study was supported by a research grant (no. 9278) from the Willum Foundation, Denmark.

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