Sediment tolerance mechanisms identified in sponges using advanced imaging techniques

Brian W Strehlow; Mari-Carmen Pineda; Alan Duckworth; Gary A Kendrick; Michael Renton; Muhammad Azmi Abdul Wahab; Nicole S Webster; Peta L Clode

doi:10.7717/peerj.3904

Sediment tolerance mechanisms identified in sponges using advanced imaging techniques

PeerJ. 2017 Nov 16:5:e3904. doi: 10.7717/peerj.3904. eCollection 2017.

Authors

Brian W Strehlow^{1

2

3

4

5}, Mari-Carmen Pineda^{4

5}, Alan Duckworth^{4

5}, Gary A Kendrick^{1

3

5}, Michael Renton^{1

6}, Muhammad Azmi Abdul Wahab^{4

5}, Nicole S Webster^{4

5

7}, Peta L Clode^{1

2

3}

Affiliations

¹ School of Biological Sciences, University of Western Australia, Crawley, WA, Australia.
² Centre for Microscopy, Characterisation and Analysis, University of Western Australia, Crawley, WA, Australia.
³ Oceans Institute, University of Western Australia, Crawley, WA, Australia.
⁴ Australian Institute of Marine Science, Cape Ferguson, QLD, Australia.
⁵ Western Australian Marine Science Institution, Crawley, WA, Australia.
⁶ School of Agriculture and Environment, University of Western Australia, Crawley, WA, Australia.
⁷ Australian Centre for Ecogenomics, University of Queensland, Brisbane, QLD, Australia.

Abstract

Terrestrial runoff, resuspension events and dredging can affect filter-feeding sponges by elevating the concentration of suspended sediments, reducing light intensity, and smothering sponges with sediments. To investigate how sponges respond to pressures associated with increased sediment loads, the abundant and widely distributed Indo-Pacific species Ianthella basta was exposed to elevated suspended sediment concentrations, sediment deposition, and light attenuation for 48 h (acute exposure) and 4 weeks (chronic exposure). In order to visualise the response mechanisms, sponge tissue was examined by 3D X-ray microscopy and scanning electron microscopy (SEM). Acute exposures resulted in sediment rapidly accumulating in the aquiferous system of I. basta, although this sediment was fully removed within three days. Sediment removal took longer (>2 weeks) following chronic exposures, and I. basta also exhibited tissue regression and a smaller aquiferous system. The application of advanced imaging approaches revealed that I. basta employs a multilevel system for sediment rejection and elimination, containing both active and passive components. Sponges responded to sediment stress through (i) mucus production, (ii) exclusion of particles by incurrent pores, (iii) closure of oscula and pumping cessation, (iv) expulsion of particles from the aquiferous system, and (v) tissue regression to reduce the volume of the aquiferous system, thereby entering a dormant state. These mechanisms would result in tolerance and resilience to exposure to variable and high sediment loads associated with both anthropogenic impacts like dredging programs and natural pressures like flood events.

Keywords: 3D X-ray microscopy; Scanning electron microscopy; Sediments; Sponge.

Grants and funding

This research was funded by the Western Australian Marine Science Institution (WAMSI) as part of the WAMSI Dredging Science Node, and made possible through investment from Chevron Australia, Woodside Energy Limited, BHP Billiton as environmental offsets and by co-investment from the WAMSI Joint Venture partners. The views expressed herein are those of the authors and not necessarily those of WAMSI. Nicole S. Webster was funded by an Australian Research Council Future Fellowship FT120100480. Brian W. Strehlow was supported by a University of Western Australia (UWA) Scholarship for International Research Fees, University International Stipend, and UWA Safety-Net Top-Up Scholarships. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.