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 contraction-expansion events on the respiration rate of small single-osculum explants of the demosponge Halichondria panicea. Based on simultaneous video-microscopic time-lapse 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 ± CI95% 13.7 min. The respiration rate of sponge explants remained relatively constant at 0.046 ± CI95% 0.014 µmol O2 h-1 (i.e., 7.41 µmol O2 h-1 g-1 DWsponge) 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.

Highlights

  • Sponges are sedentary filter-feeding invertebrates characterized by a simple body plan composed of numerous pores on the outer surface and a water canal system merging into one or more exhalant openings

  • Except for an initial increase in the oxygen consumption of sponge explants ID1 and ID2 (Figure 2), respiration rates remained relatively constant throughout the entire study period

  • Neither state of the osculum cross-sectional area (OSA) (LM, t = 0.128, P = 0.898, see diagnostic plots in Supplementary Figure S3) and A (LM, t = 0.260, P = 0.795), nor temporal changes in OSA (LM, t = 0.348, P = 0.701, see diagnostic plots in Supplementary Figure S4) and A (LM, t = 0.628, P = 0.530), affected respiration rates significantly when taking into account differences among individual sponge explants

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Summary

Introduction

Sponges are sedentary filter-feeding invertebrates characterized by a simple body plan composed of numerous pores (ostia) on the outer surface (exopinacoderm) and a water canal system merging into one or more exhalant openings (oscula). Muscles (Pavans de Ceccatty, 1986, 1989) and a nervous system (Jones, 1962; Pavans de Ceccatty, 1974), but they possess coordinated contractile behavior as a response to external (Elliott and Leys, 2007) and internal stimuli (Reiswig, 1971a) This behavior includes contraction and inflation of the sponge body as well as the inhalant (ostia) and exhalant (oscula) openings (Prosser et al, 1962; Reiswig, 1971a; Gaino et al, 1991; Nickel et al, 2006; Elliott and Leys, 2007; Strehlow et al, 2016). Pumping cessation may further result in temporal anoxia in the sponge body (Hoffmann et al, 2005b; Schläppy et al, 2007), which serves as a habitat for highly diverse microbial consortia (Taylor et al, 2007; Thomas et al, 2016)

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