Osculum dynamics and filtration activity in small single-osculum explants of the demosponge Halichondria panicea

Kumala, Lars; Riisgård, Hans Ulrik; Canfield, Donald E.

doi:10.3354/meps12155

Cited by 38 publications

(57 citation statements)

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“…We observed active pumping (i.e., OSA > 0 mm 2 ) of starved explants over extended periods t P = 7.0 ± CI 95% 2.2 h and cyclic osculum closure for t C = 37.5 ± CI 95% 13.7 min ( Table 1). Similar contraction-expansion dynamics were observed for continuously fed H. panicea explants during laboratory experiments (Kumala et al, 2017) and other sponge species (e.g., Verongia gigantea) under natural conditions (Reiswig, 1971a). From a mean initial oxygen concentration of 271 µmol L −1 (i.e., 271 nmol cm −3 ; Supplementary Figure S1) and a mean volume-specific respiration rate of 0.52 µmol O 2 h −1 cm −3 sponge (i.e., 520 nmol O 2 h −1 cm −3 sponge ) as determined in the present study, an oxygen drawdown time, i.e., the time until complete reduction of oxygen within the sponge, of (271/520 =) 0.5 h can be estimated for the present H. panicea explants.…”

Section: Contraction-expansion Behavior In Single-osculum Halichondrisupporting

confidence: 80%

“…Generally, as previously suggested for sponges with rigid, spicule-rich skeletons (Nickel, 2010), contraction-expansion behavior in H. panicea is mainly expressed in contractions of the osculum as well as water canal system (cf. Kumala et al, 2017). The more pronounced body contractions (i.e., changes in A) in T. wilhelma probably reflect a larger collapse of the aquiferous system during contractions than for H. panicea.…”

Section: Contraction-expansion Behavior In Single-osculum Halichondrimentioning

confidence: 91%

“…Experiments were performed using single-osculum explants of the demosponge H. panicea, which were prepared and cultivated according to Kumala et al (2017). Explant volume (mL) was determined from the volume equation for a hemisphere (V sp = 2/3 × πr 3 ).…”

Section: Preparation and Cultivation Of Sponge Explantsmentioning

confidence: 99%

“…The present study reveals that the sponge respiration is not appreciably affected by osculum dynamics and the pumping activity of H. panicea explants. Pumping dynamics do, however, influence filter-feeding (Kumala et al, 2017) and the internal redox state of the sponge body (Hoffmann et al, 2008). Both aerobic and anaerobic metabolic processes of associated microorganisms play an important role for several sponge species (Wilkinson and Fay, 1979;Weisz et al, 2007;Hoffmann et al, 2009;Maldonado et al, 2012;Lavy et al, 2016).…”

Section: Contraction-expansion Behavior In Single-osculum Halichondrimentioning

confidence: 99%

“…Small single-osculum explants are well-suited for exploring the relationship between sponge physiology and contractile behavior (Kumala et al, 2017), which is difficult to assess in large sponges that may display asynchronous closure and opening of their multiple oscula . Recent studies on single-osculum explants of the demosponge Halichondria panicea revealed a clear relationship between osculum opening dynamics and the filtration rate (=pumping rate), where no water was pumped during periods of osculum closure (Kumala et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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

Kumala

Canfield

2018

Front. Mar. Sci.

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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.

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Section: Contraction-expansion Behavior In Single-osculum Halichondrisupporting

confidence: 80%

Section: Contraction-expansion Behavior In Single-osculum Halichondrimentioning

confidence: 91%

Section: Preparation and Cultivation Of Sponge Explantsmentioning

confidence: 99%

Section: Contraction-expansion Behavior In Single-osculum Halichondrimentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Kumala

Canfield

2018

Front. Mar. Sci.

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Spatial and temporal anoxia in single-osculum Halichondria panicea demosponge explants studied with planar optodes

et al. 2021

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The water flow through sponges is regulated by their contractile behaviour including contraction and expansion of the aquiferous system, which leads to shifting oxygen levels in the sponge interior. Still, knowledge of spatial and temporal anoxia in sponges is lacking, but important in elucidating interactions between sponge hosts and their microbiomes. We combined 2-D luminescence lifetime imaging of oxygen with simultaneous time-lapse recordings of the sponge exhalant opening (osculum) to unveil temporal as well as spatial oxygen dynamics caused by contractile behaviour in single-osculum explants of the demosponge Halichondria panicea. The present study reveals an intrinsic concentric deoxygenation pattern in explants during episodes of osculum contraction generating an oxygen gradient with increasing concentrations towards the explant periphery. Four sponge explants faced 25 episodes with substantial changes in internal oxygen and anoxia which prevailed for 4.4 h of the total 92.0 h observation period. The 2-D images revealed that the total area of the explant experiencing anoxia during periods of osculum contraction–expansion varied between 0.01 and 13.22% and was on average 7.4 ± 4.4% for all sponge explants. Furthermore, oxygen respiration, as approximated by the rate of change of oxygen concentration during deoxygenation of the explant interior, was similar throughout the oxic parts of the explant base. The resolved 2-D dynamics provide an unprecedented insight into the internal O2 distribution of sponges and complement the traditional point measurements of oxygen sensors.

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Eating and Cognition in Two Animals without Neurons: Sponges and Trichoplax

Bechtel,

Bich

2024

Biol Theory

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Eating is a fundamental behavior in which all organisms must engage in order to procure the material and energy from their environment that they need to maintain themselves. Since controlling eating requires procuring, processing, and assessing information, it constitutes a cognitive activity that provides a productive domain for pursuing cognitive biology as proposed by Ladislav Kováč. In agreement with Kováč, we argue that cognition is fundamentally grounded in chemical signaling and processing. To support this thesis, we adopt Cisek’s strategy of phylogenetic refinement, focusing on two animal phyla, Porifera and Placozoa, organisms that do not have neurons, muscles, or an alimentary canal, but nonetheless need to coordinate the activity of cells of multiple types in order to eat. We review what research has revealed so far about how these animals gather and process information to control their eating behavior.

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Osculum dynamics and filtration activity in small single-osculum explants of the demosponge Halichondria panicea

Cited by 38 publications

References 75 publications

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

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

Spatial and temporal anoxia in single-osculum Halichondria panicea demosponge explants studied with planar optodes

Eating and Cognition in Two Animals without Neurons: Sponges and Trichoplax

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