Hydromechanical mechanisms of colony organization and cost of hefense in an encrusting bryozoan, Membranipora membranacea

Abstract

In bryozoans, hydrodynamic interactions among colony members can substantially affect filtering rates and access to food-rich water for zooids within a colony and for the colony as a whole. Hydrodynamic theory suggests that highly integrated (area-filling) colony architectures lead to strong interference bctwccn neighboring zooids, whereas less integrated architectures do not. The highly integrated bryozoan Membrunipora membranacea displays two morphological specializations that modify hydrodynamic interactions: internal excurrent zones (chimneys) and inducible defensive spines. In this study, possible hydrodynamic mechanisms underlying the cost of inducible defense and chimney organization were tested experimentally by culturing spined and unspined colonies under controlled flow conditions. Spines reduced colony growth rate when growth was limited by clearance rates, but not when transport of particles from upstream limited growth. This supports the hypothesis that the cost of inducible defense is primarily a reduction in clearance rate (i.e. spines cause hydrodynamic interference with feeding currents) rather than metabolic investment in spine construction. Chimneys were more closely spaced in spined than unspined colonies, consistent with a mechanism for organizing chimney formation based on responses by zooids to local hydromechanical cues rather than a rigid, colony-level control of zooid growth form (astogeny). Direct manipulation of hydrodynamic cues resulted in substantial changes in chimney morphology, again supporting the hydromechanical organization mechanism. More generally, these cxpcrimental results support the theoretical assessment that the highly integrated architecture is hydrodynamically unfavorable. The success of Membruniporu in some habitats suggests that its architecture confers compensating advantages, such as improved ability to compete for space. This tradeoff in growth habit may explain shifts in relative prevalence of bryozoan architectures with depth and across other environmental gradients.Bryozoans are a group of colonial suspension feeders for which there is strong evidence that flow patterns are important in determining feeding success. Bryozoan colonies consist of small modules (zooids), which feed by everting ciliated tentacular structures (lophophores) that induce water currents, from which food particles are extracted. Observations of flow rates through lophophores and particle capture rates of individual zooids have shown that the feeding success of zooids varies with extrinsic factors such as external flow speed (Cancino and Hughes 1987;Hughes and Hughes 1986; Okamura 1992) and food content (Best and Thorpe 1983, 1986a;Okamura 1987), the presence of neighboring con-and heterospecific colonies (Best and Thorpe 1986b;Okamura 1988), as well as with intrinsic colony characteristics such as colony growth form (Okamura 1984(Okamura , 1985 and the specialization of zooid morphologies (McKinney and I Present address:

An inducible morphological defence is a passive by-product of behaviour in a marine snail

“…However, the conclusion of costs or trade-offs requires careful scrutiny with regard to the exact causal chain between the predator cue and the phenotypic response. For example, in bryozoans, spines cause hydrodynamic interference with feeding currents, suggesting that costs of inducible defence are primarily a reduction in clearance rate rather than metabolic investment in spine construction (Grunbaum 1997). Moreover, growth costs associated with predatorinduced defences in larval anurans are due in part to environmentally induced changes in feeding morphology rather than direct allocation shifts between growth and defence (Relyea & Auld 2005).…”

Flow and conduit formation in the external fluid-transport system of a suspension feeder

“…The hypothesis that high excurrent flow speed induces chimney formation directly might explain the effects of ambient flow (Okamura and Partridge, 1999) and the presence of spines (Grünbaum, 1997) on chimney spacing, and the responses of lophophores to injury of adjacent zooids (Dick, 1987;von Dassow, 2005). Both high ambient flow speed (Okamura and Partridge, 1999) and the presence of defensive spines (Grünbaum, 1997) result in reduced chimney spacing.…”

“…Both high ambient flow speed (Okamura and Partridge, 1999) and the presence of defensive spines (Grünbaum, 1997) result in reduced chimney spacing. High ambient flow speed also resulted in smaller lophophores in field studies of M. membranacea (Okamura and Partridge, 1999).…”

“…The spines stick up between the lophophores, so they may affect chimney spacing by interfering with the flow under the canopy (Grünbaum, 1997). The shape of the chimneys is also affected by the shape of the substrate (which determines the shape of the colony), possibly because the pattern of flow around and through the colony depends on the substrate shape (Grünbaum, 1997). However, the position of existing chimneys does not appear to be affected by either changes in the ambient flow speed or by injury to the colony (von Dassow, 2005).…”

“…the colonies are grown (Okamura and Partridge, 1999) and on the presence or absence of spines (Grünbaum, 1997), an inducible defense produced by the bryozoans against predatory nudibranchs (Harvell, 1984). The spines stick up between the lophophores, so they may affect chimney spacing by interfering with the flow under the canopy (Grünbaum, 1997).…”