Effect of Suspended Sediments on the Pumping Rates of Three Species of Glass Sponge in Situ

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Vol. 615: 79–100, 2019 MARINE ECOLOGY PROGRESS SERIES Published April 18§ https://doi.org/10.3354/meps12939 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Effect of suspended sediments on the pumping rates of three species of glass sponge in situ N. Grant1, E. Matveev1,5, A. S. Kahn1,6, S. K. Archer2, A. Dunham2, R. J. Bannister3, D. Eerkes-Medrano4, S. P. Leys1,* 1Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada 2Fisheries and Oceans Canada, Pacific Biological Station, 3190 Hammond Bay, Nanaimo, British Columbia V9T 6N7, Canada 3Institute of Marine Research (IMR), Bergen 5005, Norway 4Marine Scotland Science, Aberdeen AB11 9DB, UK 5Present address: Department of Ocean Sciences, Memorial University of Newfoundland, St, John’s, Newfoundland and Labrador A1C 5S7, Canada 6Present address: Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA ABSTRACT: The largest known glass sponge reefs in Canada are within the Hecate Strait and Queen Charlotte Sound Glass Sponge Reefs Marine Protected Area (HSQCS-MPA) in British Columbia. However, human activities outside the core MPA boundaries, such as trawling, can cre- ate plumes of suspended sediments capable of travelling large distances. We studied the response of 3 glass sponge species to changes in suspended sediment concentrations (SSCs) at 170 m depth inside the HSQCS-MPA. Two species reduced excurrent flow rate in response to natural and experimentally induced increases in suspended sediment. Background suspended sediment levels were low and showed little variation (2.71 ± 0.09 mg l−1, mean ± SD). Species varied in the threshold of SSCs that triggered arrests. Sediment concentrations of 2.8− 6.4 mg l−1 caused arrests in Rhabdocalyptus dawsoni, while Heterochone calyx did not arrest until concentrations reached 5−10 mg l−1. Very small, but prolonged increases of suspended sediments (<1 mg l−1 for R. dawsoni and 3.2 mg l−1 for H. calyx) caused arrests of several hours in R. dawsoni and prolonged periods of reduced flow in H. calyx. No arrests were observed in Farrea occa, even after repeated exposures up to 57 mg l−1. A sediment transport model showed that sediment concentrations can remain high enough to affect sponge behaviour as far as 2.39 km from the source of the plume. The results highlight the importance of understanding the biology of different species for establishment of adequate boundaries in MPAs. KEY WORDS: Glass sponges · Reefs · Pumping Rate · Suspended sediments · Porifera · Trawling · Marine protected areas 1. INTRODUCTION managed is critical for effective conservation. One ex ample is Canada’s recently established Hecate Globally, marine ecosystems are challenged by Strait and Queen Charlotte Sound Glass Sponge multiple human-caused stressors. In response, the Reefs MPA (Fisheries and Oceans Canada 2017). This United Nations has set targets to protect 10% of the MPA was established to protect the globally unique oceans by 2020 and more thereafter (MacKinnon et ecosystems formed by glass sponges, but as suspen- al. 2015). Establishing marine protected areas (MPAs) sion feeders, sponges are sensitive to any activity that is fundamental to meeting these targets, but how the changes the water properties around them, including areas are chosen and how boundaries are set and those that occur outside the MPA boundaries. *Corresponding author: [email protected] © N. Grant, E. Matveev, A. S. Kahn, R. J. Bannister, D. Eerkes- Medrano, S. P. Leys and Fisheries and Oceans Canada 2019. §Article length was adjusted from p. 79–101 to p. 79–100 after Open Access under Creative Commons by Attribution Licence. publication. Use, distribution and reproduction are un restricted. Authors and original publication must be credited. This corrected version: April 24, 2019 Publisher: Inter-Research · www.int-res.com 80 Mar Ecol Prog Ser 615: 79–100, 2019 Glass sponge reefs occur in depths of 30−200 m on lida) are the only group that instantly arrest pumping the continental shelf of British Columbia, Canada, activity, using an action potential, in response to sed- and Alaska, USA (Conway et al. 1991, 2001, Krautter iments (Leys et al. 1999, Tompkins-MacDonald & et al. 2001). The reefs are built by 3 glass sponge spe- Leys 2008, Grant et al. 2018). cies that provide extensive habitat for many commer- Arrests of pumping are triggered by action poten- cially important fish and invertebrates, such as Pacific tials travelling throughout the glass sponge’s syncy- halibut, rockfish and spot prawn (Conway et al. 2001, tial tissues (Mackie et al. 1983, Leys et al. 1999). Cook et al. 2008, Chu & Leys 2010). This has brought These action potentials, and the ensuing arrests of fishing pressure, including bottom-contact trawl fish- pumping behaviour, have been recorded in Rhabdo- ing, to the sponge reefs, resulting in visible physical calyptus dawsoni in laboratory experiments (Leys & damage prior to MPA establishment (Conway et al. Mackie 1997, Leys et al. 1999). Tompkins-MacDon- 1991, 2001, Jamieson & Chew 2002, Austin et al. ald & Leys (2008) later found similar arrests of excur- 2007). Bottom-contact fishing also resuspends large rent flow in Aphrocallistes vastus in response to sus- amounts of sediment, but the impact of these sedi- pended sediments added to the water. More recently, ment plumes on the glass sponges is still unknown. the arrest response of A. vastus was studied in the In February of 2017, Fisheries and Oceans Canada naturally turbid waters of the Strait of Georgia, established a 2410 km2 MPA around 4 glass sponge British Columbia. That study found that A. vastus reef complexes in Hecate Strait and Queen Charlotte stopped pumping in response to suspended sediment Sound (Fisheries and Oceans Canada 2017). The MPA concentrations that were far lower than those gener- consists of a core protection zone (CPZ), which ex - ated by trawling (Grant et al. 2018). cludes all human activities, and an adaptive manage- Reefs in the northern complex of the Hecate Strait ment zone (AMZ) or buffer zone bordering the reef MPA are made by different glass sponge species and complexes, which is currently closed to fishing activity are in a less turbid environment than reefs in the but may be opened in the future. However, it is unclear Strait of Georgia (reviewed by Leys 2013). To deter- if these measures protect the reefs from indirect mine how other reef-building glass sponge species impacts of trawling (e.g. resuspended sediments) are affected by suspended sediments, and how effec- when such activities occur adjacent to the AMZ. tive the MPA might be in terms of protecting the Sponges are highly efficient water filterers capable sponges from resuspended sediments, we conducted of processing up to 900 times their body volume in experiments in situ at the northern sponge reef com- 1 h (reviewed by Yahel et al. 2003, their Table 3). plex in the Hecate Strait and Queen Charlotte Sound Generally, they filter constantly and take in both Glass Sponge Reefs MPA (HSQCS-MPA). Our spe- organic and inorganic particles alike. While they can cific aim was to determine whether the sponge spe- excrete inedible detritus (Wolfrath & Barthel 1989, cies at the reef are adapted, through variations in Yahel et al. 2007, Kahn et al. 2018), too much of it arrest responses and their thresholds to sediment dis- can be detrimental (reviewed by Bell et al. 2015). turbance, to specific environments and environmen- Sponges are sensitive to minute changes in water tal conditions. We hypothesized that either glass quality and respond to changes in seasonal charac- sponges in Hecate Strait would be sensitive to teristics of the water column (Reiswig 1971), food smaller increases in suspended sediment concentra- availability (Reiswig 1975, Kahn et al. 2012), ocean tions than those in the Strait of Georgia, or alterna- acidification (Bates & Bell 2018) and suspended sedi- tively, that Hecate Strait sponges would not be used ments (Gerro dette & Flechsig 1979, Carballo 2006, to higher suspended sediment concentrations and Tompkins-MacDonald & Leys 2008). Sediments may thus would not respond by arresting pumping smother and clog a sponge (Airoldi 2003, Tompkins- activity. MacDonald & Leys 2008, Strehlow et al. 2017), and We also studied the size fractions of sediment smaller grain sizes can fit through the incurrent pores found at the northern reef complex in Hecate Strait on the sponge surface (<20 µm) (Kilian 1952, Reiswig as well as current velocities above the sponges at the 1974) potentially damaging their aquiferous system. reef. These parameters were used to model the reach To deal with sediments, most demosponges contract of sediment plumes under different transport scenar- to prevent entry of sediment or to expel already in - ios. Our analyses underscore the importance of gested sediments (Prosser et al. 1962, Elliott 2004, understanding the biology of animals to be protected Elliott & Leys 2007); others secrete mucus to slough by an MPA. They also highlight the importance of sediments off their surface (Kowalke 2000). Of all adequate protective buffer zones around the conser- sponges, however, glass sponges (Class Hexactinel - vation targets within MPAs. Grant et al.: Glass sponge sensitivity to sediment 81 2. MATERIALS AND METHODS (ROV) (Remotely Operated Platform for Ocean Sci- ences, ROPOS; http://ropos.com) in the northern 2.1. Study site and study species reef complex. Sediment experiments were carried out at the eastern corner of this complex, at a site Experiments were carried out on a sponge reef dominated by large, patchily distributed bushes of at approximately 170 m depth in the HSQCS-MPA Farrea occa. Goblet-shaped Heterochone calyx during 2 cruises of the Canadian Coast Guard sponges were found growing between and out of Ship (CCGS) ‘JP Tully’ in October 2015 and May F. occa bushes, while small chalice-shaped Aphro- 2017 (2015: 53° 11’ 37.2” N, 130° 28’ 27.7” W; 2017: callistes vastus and tube-shaped Rhabdocalyptus 53° 11’ 38.0” N, 130° 28’ 29.4” W; Fig.
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