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Invertebrate zoogeomorphology: A review and conceptual framework for rivers

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Abstract Invertebrates are important sediment engineers, making up for their small body size with abundance and behavioral diversity. However, despite the recognized importance of invertebrates as sediment engineers in terrestrial and marine environments, zoogeomorphology in rivers has primarily considered larger taxa, such as fish and beaver. This article reviews the zoogeomorphic effects of invertebrates in freshwater habitats, with a focus on rivers. To better synthesize current zoogeomorphic research and to help guide future studies we build a conceptual model considering biotic (behavior, abundance, body size, life history, and species invasions) and abiotic (geophysical energy and sediment grain size) controls on the direction and magnitude of zoogeomorphology. We also incorporate invertebrate engineers into conceptual sediment entrainment models, to understand their geomorphic role in the context of hydraulic power and sediment size. We structure our review around invertebrate behavior as a key control on whether invertebrates have a sediment destabilizing or stabilizing impact. Invertebrate zoogeomorphic behavior are diverse; the majority of research concerns bioturbation, a result of locomotion, foraging, and burrowing behaviors by many taxa. Similarly, burrowing into bedrock by a caddisfly and non‐biting midge larvae promotes bioerosion. Attachment to the substrate, (e.g., silk nets by caddisfly larvae or byssal threads by some mussels) can stabilize sediment, providing bioprotection. Bioconstructions (e.g., caddisfly cases and mussel shells) may have either stabilizing or destabilizing effects depending on their density and abiotic context. Interactions between lotic invertebrates and fluvial processes are complex and understudied, requiring further research across a greater range of taxa, behaviors, and spatiotemporal scales. This article is categorized under: Water and Life > Nature of Freshwater Ecosystems Water and Life > Conservation, Management, and Awareness
Mechanisms of bioturbation (adapted from Kristensen et al., 2012 with D added to suit lotic environments). (a) Biodiffusion—movement of particles short distances in effectively random directions, vertically or horizontally. (b) Upwards conveyors—behaviors resulting in a net movement of sediment upwards. (c) Downwards conveyors, (d) bank to channel conveyors—taxa which burrow into river banks and increase bank erosion and fine sediment input into the channel
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Hierarchical scale of river systems, representing top down controls of abiotic geomorphology and bottom up controls of zoogeomorphology (Modified from Frissell et al., 1986). Geomorphic drivers influence the form and function of rivers from catchment scale (stream system) down to the microhabitat scale. Less well understood are the zoogeomorphic feedbacks which provide a reciprocal control on larger scale processes. For example, small scale locomotion and burrowing behaviors by crayfish supply fine sediment into the river channel at the reach scale, affecting sediment budgets for catchments, at least during baseflow (Rice et al., 2016). Individual nets and retreats of Hydropsychidae caddisfly stabilize sediment particles, resulting in stable patches of sediment at the reach scale (Albertson et al., 2019) but measuring the effects of stabilization at the catchment scale is yet to be achieved
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Effects of aquatic invertebrates on the force required to entrain sediment, based on the empirical work of Shields (1936). Particle Reynolds number is Re* = (u*D)/v, where u* is the shear velocity, D particle size, and v the kinematic viscosity of water. Particle Reynolds number can be interpreted as scaled particle size (Church 2006). Shields parameter is , where τc is the critical shear stress, ρs and ρ the density of sediment and water respectively and g, acceleration due to gravity. Shields threshold (based on the empirical work of Shields, 1936) and the threshold for sediment suspension (from Church 2006) in gray. Zoogeomorphic studies included in this review that considered the effects of invertebrates on critical shear stress are included. Studies must report either incipient shear stress or Shields values for both invertebrate treatments and controls. Surprisingly few studies consider critical shear stress with many measuring mass of sediment transported instead. Arrows indicate approximate increase and decrease in sediment stability between the mean value of the control and treatment with the largest difference. We assumed all sediment had a density of 2,650 kg m−3. Values are approximate, as in some cases values had to be interpreted from graphs within these published articles. The environmental ranges of key zoogeomorphic behaviors (Figure 6) are conceptualized based on literature reviewed in this article. (1) Biofiltration only affects very fine sediment in suspension, (2) burrowing affects fine‐medium grain sizes above and below the threshold for motion, (3) locomotion and foraging moves sediment across a wide range of grain sizes, (4) attachment consolidates sediment, which is only important above the threshold for motion. More research which considers changes to threshold shear stress due to taxa with different behaviors is required to quantify these groups. At higher and Re* it is expected that abiotic forces will dominate over biotic forces
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Conceptual Hjulström (1935) curve modified to include the influence of zoogeomorphology. Fine grained sediments require high flow velocities to entrain due to cohesive bonds between grains (high erosion threshold), but once eroded require very little flow to remain entrained in the water column (low settling velocity). For coarser particles sizes (>0.1 mm), critical flow velocity and settling velocity increase with particle size. Plotted zoogeomorphic‐adjusted flow velocity thresholds are a conceptual representation and have not been empirically quantified. (a) Biology increases the erosion threshold via biostabilization (e.g., Hydropsyche caddisfly nets increase flow velocity to erode 2–10 mm grains by 30%; Cardinale et al., 2004 and stabilize up to about 65 mm diameter sediment; Albertson, Sklar, et al., 2014). Microbes and aquatic macrophytes also increase the erosion threshold of clay, silt and sand particles (not reviewed here, but see Le Hir et al., 2007 in marine systems and Gurnell, 2014; Wharton et al., 2006 for aquatic vegetation). (b) Above the biostabilization threshold, high flow velocities break up stabilizing structures. (c) Bioturbation reduces the erosion threshold of sediment and is largely independent of flow velocity. However, when flow velocity is below the settling threshold of that sediment, sediment will only be moved locally (e.g., rolled by crayfish; grain size up to 38 mm; Johnson et al., 2010). (d) When the settling threshold is exceeded, bioturbated sediment will be transported downstream with larger scale impacts
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Linking organism behavior traits to zoogeomorphic effects (see Box 1; Figure 5). Organism behavior has the potential to affect geomorphology via a number of specific mechanisms, which may destabilize (blue boxes) or stabilize sediment (orange boxes). Burrowing and locomotion bitoturbate and bioerode sediment (e.g., Mermillod‐Blondin, 2011; Rice et al., 2019). Attachment to the bed surface may consolidate sediment via filtration and provide bioprotection (e.g., caddisfly filter feeding nets). Feeding activities may have different zoogeomorphic affects based on activity. Foraging may increase bioturbation (e.g., crayfish; Johnson et al., 2010 and stonefly; Statzner et al., 1996) while filtering removes sediment from the water column (e.g., Mussels; Tuttle‐Raycraft & Ackerman, 2018). Both autogenic and allogenic construction are forms of bioconstruction and can provide bioprotection and biofiltration (e.g., caddisfly nets and mussel shells; Zimmerman & de Szalay, 2007)
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Conceptual model for the zoogeomorphic effects of animals highlighting the importance of organism traits (gray boxes). Adapted from Moore (2006) who considered how behavior, body size and abundance are mediated by abiotic context to influence zoogeomorphic affects. (1) The spatial distribution of zoogeomorphic engineers is controlled by both abiotic (e.g., physical habitat) and biotic variables (e.g., species interactions). (2) The zoogeomorphic effects of an organism are a result of the behavior, biomass (body size * abundance) and life history of that individual. We build on previous models by explicitly considering the importance of organism behavior as a key control, not just on the magnitude, but also on the direction of zoogeomorphic effects (Figure 6). In contrast, we consider biomass and life history to be primarily controls on the magnitude of zoogeomorphic activity (over space and time respectively). (3) The activities of the organism are mediated by the abiotic environment. (4) Zoogeomorphic effects may modify habitat and species distributions through zoogeomorphic feedback (ecosystem engineering, Jones et al., 1994)
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Examples of bioprotection and bioconstruction by invertebrate animals in rivers. (a) Nets of Hydropsychidae caddisfly nets fluorescing under UV light (image: Matthew Johnson). (b) Case‐building caddisfly larvae (Glossosomatidae) move sand around the sediment–water interface. (c) Quagga mussels attach to bed sediment and other mussels using byssal threads, River Wraysbury, UK. (d) Populations of freshwater mussels may stabilize sediment and filter suspended sediment from the water column (image: freshwater pearl mussels with Glossosomatidae caddisfly living on them). (e) Layers of caddisfly cases form calcium carbonate bioherms. Each caddisfly case is orientated vertically: reproduced from Leggitt and Cushman (2001)
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Mechanisms for sediment stabilization by aquatic animals. (a) Bioconstruction using self‐generated tissue, for example mussel shells or caddisfly nets. (b) Bioconstruction using other materials, for example the construction of cases by many caddisfly species. (c) Bioconstructions may stabilize bed sediments via bioprotection (e.g., caddisfly filter feeding nets tie gravel particles together). (d) Filtration of fine sediment from the water column by feeding organisms
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Examples of lotic invertebrate bioturbation and bioerosion. (a) Bioturbation by mayfly larvae (Pseudiron centralis) which uses body positioning to create hydraulic structures eroding sand furrows to excavate prey (reproduced from Soluk & Craig, 1990). (b) Galleries of Tubificidae worms (Tubifex sp. and Limnodrilus sp.) increase hydraulic connectivity of the subsurface and convey fine sediment to the surface (reproduced from Nogaro et al., 2006). (c) Bioerosion by caddisfly larvae, which build Y‐shaped burrows which extend 40 mm into mudstone (white outline) accompanied by smaller U‐shaped Chironomidae burrows (white arrows; scale bar = 1 cm; reproduced from Savrda, 2019). (d) Burrows of signal crayfish (Pacifastacus leniusculus) in Gaddesby Brook, UK
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