Contraction Dynamics and Respiration of Small Single-Osculum Explants of the Demosponge Halichondria panicea

Abstract

Sponges pump large amounts of seawater through their water canal system, providing both food and oxygen to the sponge body. Sponge pumping activity may show considerable variation as a consequence of contractile behavior, which includes contraction and expansion of the exhalant opening (osculum) in regular or irregular time intervals. The present study unravels short-and long-term effects of contractionexpansion events on the respiration rate of small single-osculum explants of the demosponge Halichondria panicea. Based on simultaneous video-microscopic timelapse recordings of osculum cross-sectional area (OSA) and projected area (A), combined with respiration rate measurements, we further evaluate the role of pumping activity for oxygen uptake in the explants. Pumping dynamics were expressed by cyclic contraction-expansion events of the OSA and A, including osculum closure with a mean duration of 37.5 ± CI 95% 13.7 min. The respiration rate of sponge explants remained relatively constant at 0.046 ± CI 95% 0.014 µmol O 2 h −1 (i.e., 7.41 µmol O 2 h −1 g −1 DW sponge) during contraction-expansion cycles, but with a marginal decrease of 9.6% during osculum closure. Periods of pumping cessation during osculum closure likely caused reduced oxygen levels in the sponge body, increasing the oxygen gradient between the environment and the sponge interior, allowing enhanced diffusion of oxygen across the explant surface. This is a key mechanism for balancing respiratory demands during sponge contractions. While contractile behavior is only marginally associated with decreased respiratory demands in small single-osculum H. panicea explants, it may control the degree of internal oxygen depletion and thereby ensure maintenance of sponge-associated microorganisms during non-pumping periods.

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

“…The difference between the microbial communities in G. barretti and those in anoxia-tolerant species from Lough Hyne might be due to differences in morphology, as G. barretti is a massive species, or environment, since it occurs more under constant oxygenation than under seasonal anoxia. Thus, the "anoxic microecosystems" observed in G. barretti (49) may result from its morphology, and the thin, encrusting sponges of Lough Hyne could be comparatively more oxygenated most of the year, even if pumping ceases (91). Periods of pervasive oxygenation would restrict symbioses with obligate anaerobes and favor microbes with flexible metabolic strategies.…”

Size Is the Major Determinant of Pumping Rates in Marine Sponges

“…Reiswig found that sponge-pumping behavior was more complex than previously thought and might be driven by both abiotic (e.g., storms, sedimentation, and temperature) and intrinsic factors (e.g., daily cycles and behavioral pattern). More recent studies focused on the effect of a single parameter on the sponge pumping in either laboratory conditions (e.g., Annandale, 1907;Stuart and Klumpp, 1984;Huysecom et al, 1988;Riisgård et al, 1993;Larsen and Riisgård, 1994;Tompkins-MacDonald and Leys, 2008;Pfannkuchen et al, 2009;Schläppy et al, 2010;Massaro et al, 2012;Lavy et al, 2016;Strehlow et al, 2016;Kumala et al, 2017;Kumala and Canfield, 2018;Goldstein et al, 2019) or in situ (e.g., Gerrodette and Flechsig, 1979;Savarese et al, 1997;Bell et al, 1999;Trussell et al, 2006;Tompkins-MacDonald and Leys, 2008;Schläppy et al, 2010;Leys et al, 2011;McMurray et al, 2014;Lewis and Finelli, 2015;Ludeman et al, 2017;Grant et al, 2019;Wooster et al, 2019). Unfortunately, most studies were short term or small scale and thereby failed to provide a comprehensive view of the long-term in situ natural pumping behavior of the studied sponges.…”

The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (Lough Hyne, Ireland)

“…The difference in the microbial communities in G. barretti compared to anoxic-tolerant species from Lough Hyne could be due to differences in morphology as G. barretti is a massive species, or environment, since it is found under more or less constant oxygen rather than seasonal anoxia. Thus, the 'anoxic micro-ecosystems' observed in G. barretti (49) may result from its morphology, and the thin, encrusting sponges of Lough Hyne could be comparatively more oxygenated most of the year, even if pumping ceases (90).…”