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Hydrodynamic Characteristics of Aquiferous Modules in the Demosponge Halichondria Panicea

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Hydrodynamic Characteristics of Aquiferous Modules in the Demosponge Halichondria Panicea Downloaded from orbit.dtu.dk on: Sep 27, 2021 Hydrodynamic characteristics of aquiferous modules in the demosponge Halichondria panicea Kealy, Rachael A.; Busk, Thomas; Goldstein, Josephine; Larsen, Poul S.; Riisgård, Hans Ulrik Published in: Marine Biology Research Link to article, DOI: 10.1080/17451000.2019.1694691 Publication date: 2019 Document Version Peer reviewed version Link back to DTU Orbit Citation (APA): Kealy, R. A., Busk, T., Goldstein, J., Larsen, P. S., & Riisgård, H. U. (2019). Hydrodynamic characteristics of aquiferous modules in the demosponge Halichondria panicea. Marine Biology Research, 15(10), 531-540. https://doi.org/10.1080/17451000.2019.1694691 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. 1 file: Sponge module ms - submitted to Marine Biology Research 18 December 2018 2 3 Hydrodynamic characteristics of aquiferous modules in the 4 demosponge Halichondria panicea 5 Rachael A. Kealy1, Thomas Busk1, Josephine Goldstein1, Poul S. Larsen2, Hans Ulrik 6 Riisgård1* 7 1Marine Biological Research Centre, University of Southern Denmark, Hindsholmvej 11, DK-5300 8 Kerteminde, Denmark 9 2DTU Mechanical Engineering, Fluid Mechanics, Technical University of Denmark, Building 403, DK- 10 2800 Kgs. Lyngby, Denmark 11 *Corresponding author 12 ______________________________________________________________________ 13 Abstract: Multi-oscula sponges are organisms composed of aquiferous modules, each 14 of which draws water through its canal system by means of pumping units (choanocyte 15 chambers, CC) such that the filtered water leaves the module as an exhalant jet through 16 the osculum of the module. Here we compare relations between the characteristic 17 parameters of sponge volume (V), osculum cross-sectional area (OSA), exhalant jet 18 speed (U0), and filtration rate (F) of single-osculum explants and individual aquiferous 19 modules of multi-oscula explants of the demosponge Halichondria panicea. The latter 20 modules are identified by observing from which part of the surface administered dye 21 will emerge from its osculum. There is fair agreement in results between the two types 22 of modules. For both types, the filtration rate is a linear function of the modules volume, 23 with average values of volume-specific filtration rate of 1.8 and 1.5 ml min-1 cm-3 for 24 single- and multi-oscula sponge explants, respectively. This supports the hypothesis that 25 the density of CCs is approximately constant for a given species. Although the 26 individual modules in a multi-oscula sponge operate as separate aquiferous systems, the 27 present study has shown that modules nevertheless communicate in response to external 28 stimuli. Thus, when one module was exposed locally to ink particles, both the exposed 29 module and its neighbouring modules reduced their OSA, U0, and F. 30 Keywords: Exhalant jet speed; Filtration rate; Osculum area; Scaling; Aquiferous 31 module; Contraction 32 ______________________________________________________________________ 33 Introduction 34 Sponges (Porifera) are among the oldest groups of multicellular organisms in the animal 35 kingdom (Metazoa) with fossil records dating back to over 700 million years (Brian et 36 al. 2012) They are comprised of at least eight cell types and the entire body is 37 specialized for filter-feeding on suspended organic particles (i.e. free-living bacteria and 38 phytoplankton) in the ambient water (Jørgensen 1966; Reiswig 1971, 1974, 1975; 39 Bergquist 1978; Simpson 1984; Larsen and Riisgård 1994; Elliott and Leys 2007; Leys 40 et al. 2011; Ludeman et al. 2014; Strehlow et al. 2016; Lüskow et al. 2018). Sponges 41 lack nerves and muscles, but have muscle-like cells (myocytes) resembling smooth 42 muscle cells which, along with chemical messenger-based systems enable sponges to 43 react to environmental stimuli in a coordinated way of contraction-inflation behavior 44 (Parker 1910; Bagby 1966; Perovic et al. 1999; Nickel 2004, 2011; Nickel et al. 2006; 45 Elliott and Leys 2007, 2010; Ellwanger et al. 2007; Ludeman et al. 2014; Leys 2015). 46 Sponges are modular organisms in which each "aquiferous module" is a functional 47 unit that draws ambient water through numerous small inhalant openings (ostia) into an 48 inhalant canal system by means of pumping units (choanocyte chambers, CC). These 1 49 CCs filter the water for bacteria, phytoplankton and other suspended food particles 50 before the water leaves the module via an exhalant canal system through a single 51 exhalant opening (osculum) to the surrounding water (Fry 1970, 1979; Ereskovskii 52 2003). In a recent study, Goldstein et al. (2019) stated that a constant density of CCs in 53 sponges would imply that the theoretical scaling of sponge volume (Vs), osculum cross- 54 sectional area (OSA), exhalant jet speed (U0), and filtration rate (F) could be expressed 2/3 1/2 3/2 55 as OSA ~ Vs , U0 ~ OSA and F ~ OSA . Experimental data obtained on single- 56 osculum sponge explants (i.e. single aquiferous modules) of the demosponge 57 Halichondria panicea Pallas, 1766 showed that the observed scaling with size was close 58 to that inferred from the hypothesis of constant CC density (Goldstein et al. 2019). 59 Thus, the increase of U0 with increasing OSA may be expressed by a power function 60 with an exponent of 0.5 and (based on literature data, Goldstein et al. 2019, Fig. 10 -1 61 therein) reach a maximum value of U0 = 6 to 8 cm s . This suggests that U0 approaches 62 an upper limit which in turn implies that a sponge module of the species in question 63 may increase only to a certain size. 64 According to Fry (1970, 1975) the development of an osculum may be in response to 65 expel drawn in water from a certain volume of sponge, referred to as an aquiferous 66 module. Thus, a multi-oscula sponge may be regarded as a "population of aquiferous 67 modules" (Fry 1970). Because the size of the OSA seems to be closely correlated with 68 both sponge volume and filtration rate it has been of interest in the present study to 69 determine the size of individual modules and their filtration rate in both single-osculum 70 and multi-oscula sponge explants. Although the aquiferous systems of the individual 71 modules in a multi-oscular sponge are separate functional units this may not exclude - 72 communication between modules leading to coordinated oscular contractions triggered 73 by inorganic particles, and therefore it has been of interest to study the effect of 74 inorganic particle overloading in multi-oscula sponges. 75 76 Materials & Methods 77 Sponges were sourced from larger colonies of the demosponge Halichondria panicea at 78 the inlet to Kerteminde Fjord, Denmark (55°26'59"N, 10°39'40"E) and transported to 79 the Marine Biological Research Centre laboratory. Small cuttings ranging from 0.03 to 80 1.68 cm3 were placed on glass slides in temperature-controlled (16.1±0.9 °C) flow- 81 through aquaria with bio-filtered (blue mussels, Mytilus edulis Linneaus, 1758) 82 seawater (23.0±0.9 PSU). Development of a single osculum (or several oscula) was 83 regularly monitored. In addition, multi-oscula explants were produced from larger 84 sponge fragments with several oscula and were attached to substrate plates with 85 whipping twine. All explants were kept in flow-through aquaria and fed lab-cultured 86 Rhodomonas salina Wislouch, Hill and Wetherbee, 1989 algal cells (~5000 cells ml-1) 87 for 6 h every 1 to 3 days. 88 Osculum diameter (D, mm) of the aquiferous modules in explants were measured 89 video-microscopically using the software ImageJ v5.0.3 to determine the osculum 90 cross-sectional area (OSA, mm²) as: 91 92 OSA = π(D/2)² . Eq. (1) 93 94 To serve as a reference, the oscula of 69 sponges were photographed in situ in the 95 inlet to Kerteminde Fjord 4 October 2018 to determine the size distribution of OSA in 96 the field. For single-osculum explants, i.e. individual aquiferous modules, the side-view 97 projected area (A, mm²) and height (h, mm), were measured for volume estimates (Vest, 98 mm³) using the cone equation (Goldstein et al. 2019): 99 2 100 Vest = πA²/3h . Eq. (2) 101 102 For multi-oscula explants, the boarders of aquiferous modules were identified 103 through observations of incurrent and excurrent water flow using fluorescence. 104 Fluorescein dye (20 PSU, 12°C) was deposited on the exopinacoderm in small doses 105 (~0.1 ml) using a micromanipulator. The micromanipulator was repositioned over the 106 sponge explant (distance from explants ~0.5 mm) to determine where fluorescein 107 stopped exiting one osculum and began exiting another. Exhalant jets were visualized 108 with fluorescein dye while all oscula were open to ensure water flow through the entire 109 sponge. The volume of each aquiferous module in a multi-oscula explant was directly 110 measured (Vmea, mm³) by cutting along the invisible boarders of an aquiferous module 111 and weighing each module individually. Comparative volume estimates (Vest, mm³) 112 were obtained based on the relative contribution of each aquiferous module to the total 113 volume flow through the entire explant, based on the hypothesis that volume-specific 114 filtration rate is constant and the same for all modules, leading to the equation: 115 116 Vest = Fest/∑Fest × ∑Vmea , Eq.
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