Predation and the associated behavior of both predator and prey are important drivers of evolutionary change (Vermeij ), with predator–prey interactions receiving considerable research attention (e.g., Heck and Crowder , Chivers and Smith , Schmitz et al. ). Many species display a repertoire of strategies and defense mechanisms to reduce the risks associated with predation that reflect adaptations developed over millennia (Strauss et al. , Belgrad and Griffen , Alberti et al. ). For instance, prey may respond to the presence of a predator by reducing activity levels and by increasing or timing their use of safe microhabitats to reduce the risk of predation (Lima and Dill , Sih and McCarthy ). However, the rapid spread of non‐native species across the globe (Early et al. ) may disrupt the behavioral response of indigenous native taxa. The overall effect of non‐native predators may therefore be enhanced if they possess predation strategies that prey do not recognize or are ill‐equipped to counter (Sol and Maspons , Segev et al. ). Understanding the behavioral adaptions that taxa employ to successfully evade and survive predation pressures by native and non‐native taxa is therefore important in the context of managing contemporary ecosystems.
Crayfish (order Decapoda) are one of the most widely translocated groups of aquatic organisms (Kouba et al. ). Where crayfish invade they typically reduce biodiversity and biomass of the wider faunal community (Twardochleb et al. , Mathers et al. ). The most widely recorded taxa affected by invasive crayfish colonization are Mollusca, with reductions in species richness, abundances, and biomass (e.g., Dorn , Ruokonen et al. ). Despite a large number of studies centered on crayfish–prey interactions (Crowl and Covich , Alexander and Covich ), studies examining the behavioral response of ubiquitous prey taxa within crayfish invaded ecosystems are limited (but see Haddaway et al. ). In response to predation by non‐native crayfish, several natural avoidance strategies have been observed in macroinvertebrate species, including rapid locomotion, increased voluntary drift, and vertical migration into the subsurface sediments (Alexander and Covich , Nyström , Haddaway et al. ). However, utilization of subsurface sediments as a refuge is dependent on the availability of open, interstitial pore spaces.
River bed gravels typically form a structural framework within which finer sand (<2.0 mm) and silt (<0.063 mm) particles are stored (Church et al. ). The amount of available pore space depends on (1) the grain size distribution of the framework gravels and their packing density (Frostick et al. , Cui and Parker ), and (2) the amount and size of fine sediment delivered to and stored within the framework. The relative size of the framework and fine sediment is a key control on bed porosity because it directly affects the propensity of fine sediment to infiltrate into or block (clog) gravel interstices (Frings et al. , Wooster et al. ). If interstitial space is sufficient, particles infiltrate and infill from the base of the substrate in a process called unimpeded static percolation (Lunt and Bridge ). In contrast, where interstitial spaces are small, large sand grains may block pore throats, impeding the infiltration of fine sediments in a process known as bridging (Gibson et al. ). The availability of interstitial refugia for prey species (e.g., freshwater amphipods) in riverine systems is therefore linked to the bed sedimentology and the fine sediment regime (Gayraud and Philippe , Jones et al. ).
Anthropogenic modifications have altered the quantity and composition of fine sediment delivered to rivers globally (Walling and Collins ), with sediment yields of many rivers currently exceeding background levels (Owens et al. , Collins and Zhang ). Consequent filling (or colmation) of interstitial spaces within the river bed can lead to the disconnection of river bed (benthic) and subsurface (hyporheic) habitats (Descloux et al. , Mathers et al. ). Where this occurs, taxa that possess predator avoidance adaptations that rely on vertical movement into the river bed may be subject to reduced refuge availability and therefore enhanced predation pressure.
However, the classic view of fine sediment dynamics at the water–substrate interface has been conceived entirely around geophysical principles in which bed shear and fluid turbulence drive entrainment, transport, and deposition of fine sediment (Beschta and Jackson , Diplas and Parker , Kuhnle et al. ). There is a growing body of literature demonstrating that animals including fish and macroinvertebrates can also alter the accumulation and distribution of fine sediment (Statzner et al. , Zanetell and Peckarsky , Nogaro et al. , Pledger et al. ) via the expenditure of biotic energy (Rice et al. ). For example, macroinvertebrate prey may winnow fine sediment from interstitial spaces and thereby maintain and/or re‐establish vertical connectivity and migration pathways within the river bed (Visoni and Moulton , Mermillod‐Blondin et al. , Mermillod‐Blondin and Rosenberg , Nogaro et al. , Stumpp and Hose ). This is an example of fluvial zoogeomorphology (Butler ) the process through which animals alter the geomorphology and sedimentology of their environment (Rice et al. , Statzner , Albertson and Allen , Vu and Pennings ). Crayfish are widely recognized zoogeomorphic agents that manipulate coarse sediments and bedload flux (Johnson et al. ), recruit fine sediment to rivers via their burrowing activities (Faller et al. , Rice et al. ), entrain detritus into the flow when foraging and fighting (Usio and Townsend , Harvey et al. ), and increase the suspended sediment load in rivers (Rice et al. , ). It is therefore likely that crayfish may also have a direct influence on the infiltration of sediment into subsurface habitats, a process which has yet to be tested for any biota.
This research therefore sought to examine the engineering of a shared physical environment by a predator and its prey, and the effect of their geomorphological work on predator–prey interactions. These interactions are situated within a broader framework in which ecosystems are subject to multiple external stressors (Sih et al. , Strayer , Jackson et al. ) that may drive and/or mediate the interactions between predator, prey, and the physical environment, in this case biological invasions and increased fine sediment loading. Predator–prey interactions are a recurrent theme in ecology, but the typical assumption (conceptualized in Fig. A) is that the physical environment is a fixed template in which predation occurs. The growing recognition that organisms can engineer their environments (Jones et al. , Moore , Wright and Jones ), in this case via zoogeomorphological processes (Rice et al. , Statzner ), means that both predator and prey may modify their shared habitats (Fig. B).
Enlarge this image.Conceptual framework of the interactions between predator–prey relations, the physical environment, and the addition of an external stressor. Panel (A) represents the traditional view of predator–prey interactions; panel (B) characterizes the additional processes and interactions between biotic and abiotic factors which take place in the natural environment. Red arrows represent the additional mediating factors considered in this study for the first time.
In this study, we examine the effect that predators (invasive crayfish) and prey (freshwater amphipods) have on the ingress of contrasting surface fine sediment treatments into experimental substrates and how changes in the physical environment influence predator–prey interactions. Amphipods are diverse and keystone organisms in marine and freshwater systems with over 2000 freshwater species recorded to date (Väinölä et al. ). Gammarus pulex (L.) (Amphipoda: Crustacea) is the most widely distributed and abundant amphipod species in the UK (Gledhill et al. ), often dominating macroinvertebrate communities by biomass and abundance (MacNeil et al. ). G. pulex are a highly mobile taxon, capable of burrowing into fine sediment to find trophic resources and habitat (Vadher et al. ) and are therefore an ideal model prey organism. The North American signal crayfish (Pacifastacus leniusculus; Dana) is one of the most prevalent non‐native decapod species globally (Kouba et al. ), including in UK freshwaters (Holdich et al. ), and was therefore chosen as the model predator organism.
We address the following research questions: (1) Does the presence of G. pulex and P. leniusculus (alone and in combination) modify fine sediment infiltration rates? (2) Does G. pulex display predator avoidance behavior in the presence of P. leniusculus in the form of vertical movement into subsurface sediments? (3) Does elevated sediment ingress into subsurface habitats result in reduced survivorship of G. pulex due to predation? Each of these questions were examined across a gradient of infiltration scenarios, as defined by sediment loading and grain size, thereby providing different environmental conditions in which to examine the interaction of predator–prey relationships and zoogeomorphic activity. Fine sand treatments were used to assess the role of pore infilling and therefore reduction in refuge volume, while coarse sand allowed the assessment of surface‐pore bridging and therefore a reduction in refuge access. Differentiation between these processes is ecologically important as pore space may still be available but inaccessible should coarse sand bridge pathways, prohibiting the transfer of resources and organisms below the level of clog development. In contrast, a reduction in pore volume renders the interstitial space unusable regardless of the grain size present (Mathers et al. ).
Experiments were undertaken in three identical sediment columns (following Mathers et al. ) comprising two interlocking substrate sections representing surface (benthic) and subsurface (hyporheic) substrates (Fig. ). Each section was 32 cm in diameter and contained a 50 mm thickness of coarse fluvial sediment (gravel particles 20–64 mm in diameter). This size distribution is consistent with natural coarse river framework gravels and included particles that Pacifastacus leniusculus are known to displace (up to 38 mm in diameter; Johnson et al. ). The two sections were stacked vertically to provide a total substrate depth of 100 mm. Six mm holes (at a density of 0.06 cm−1) allowed water, fine sediment and Gammarus pulex to move between the sections. The bottom section (50–100 mm) was perforated with smaller holes (2 mm diameter at a density of 0.09 cm−1) to prevent emigration of G. pulex and limit fine sediment loss from the base of the column, while also permitting vertical hydrological exchange. In addition, 0.25‐mm netting was secured around the base of the column and a 5‐mm rubber seal created around the base of the top section. The column was covered to prevent movement of crayfish out of the column. Experiments were conducted under natural ambient light conditions as G. pulex are phototactic and display negative migration behavior in response to light (movement away from the light source; MacNeil et al. ) and P. leniusculus activity is strongly diurnal with most activity occurring at night (Guan and Wiles , Nyström ).
Enlarge this image.Conceptual diagram of the experimental setup consisting of a coarse surface layer and finer subsurface layer. The red arrow represents the migration pathways available to Gammarus pulex, and the black arrow represents the flow of downwelling water and direction of sediment transport. Photographs illustrate the grain size matrix prior to sediment addition.
Downwelling flow conditions were employed during all experiments. Previous experiments using the mesocosm facility have documented the affinity of G. pulex for surface substrates under downwelling hydrological exchange (Mathers et al. ). Application of downwelling flow conditions therefore provided a baseline distribution of G. pulex for this set of experiments and facilitated the detection of avoidance behavior as increased occupancy of subsurface substrates. The sediment columns were placed inside separate cylindrical water containers (97 × 57 cm, volume = 210 L). External pumps delivered flowing water to the columns which passed through the column under gravity. A sprinkler rosette was attached to the end of the pump outlet to disperse water (2.7–2.8 L/min). Preliminary observations indicated that this flow of water was sufficient to maintain low interstitial flow through the sediments but was not great enough to initiate sediment transport. Consequently, any vertical movement of fine sediment during the experimental period was primarily a function of gravity or the direct activity of G. pulex and/or P. leniusculus.
The experimental containers were aerated throughout the experiments using an aquarium pump and temperature was held constant (15 ± 0.4°C) via an external water cooler (Aqua Medic, Titan 150, Bissendorf, Germany). The temperature selected for the experiments corresponds with peaks in crayfish activity under field conditions in the summer months within the UK (Bubb et al. , Johnson et al. ) and is comparable to that employed during other laboratory studies (Basil and Sandeman ). Experiments were undertaken during late spring and summer (May–July) to coincide with the main period of crayfish activity in the Northern Hemisphere.
The fine sediments used in the experiment consisted of two prewashed fluvial size fractions: fine sand (0.125 μm–1 mm) and coarse sand (1–4 mm). Finer fractions (<0.125 μm) were removed by wet sieving to ensure that turbidity did not vary between experimental trials. Prior to each experimental run, fine sediment was applied evenly to the surface of wet gravel in the top section of the column using a 1 or 4 mm sieve, respectively. Preliminary tests indicated that the application of 5 kg/m2 filled all interstices (100% of pore framework volume) under the fine sediment treatment and covered the surface of all gravel particles. In addition to this heavy sediment loading, a moderate sediment loading of 3 kg/m2 was used. The two size fractions were chosen to include grains with a low propensity to clog interstitial spaces (0.125 μm–1 mm) and grains with a high propensity to bridge between framework clasts and thus limit further infiltration (1–4 mm). Appropriate grain sizes were determined using calculations based on studies by Gibson et al. () and Frings et al. (), who provide ratios to discriminate between pore filling loads and bed structure (framework) clasts. For each experimental trial, a mixture of both fine sand fractions (equivalent to 2 kg/m2 of each size fraction) was mixed thoroughly with the gravel matrix and placed in the bottom section. This poorly sorted grain size mixture acted as sediment trap but did not reduce interstitial space sufficiently to preclude G. pulex from migrating into the subsurface layer.
Five sediment treatments were examined: (1) an open gravel framework without application of fine sediment; (2) 3 kg/m2 fine sand sedimentation in the surface section; (3) 5 kg/m2 fine sand sedimentation in the surface section; (4) 3 kg/m2 coarse sand sedimentation in the surface section and; (5) 5 kg/m2 coarse sand sedimentation in the surface section. These treatments represented a gradient of fine sediment loading (Appendix S1). Each treatment was undertaken for four different scenarios: (1) no organisms present; (2) 75 G. pulex; (3) one P. leniusculus; and (4) one P. leniusculus and 75 G. pulex. The sediment treatments (n = 5) and organism presence/absence (n = 4) were combined in a full factorial design giving 20 treatment combinations. Each combination was replicated five times to give a total of 100 experimental runs. Treatments were randomly allocated to an experimental trial.
All crayfish were collected from a local stream (Wood Brook, Loughborough, UK; 52°75′69″ N., −1°22′74″ W.) using baited traps and immediately transported to the laboratory. To limit variability that might be associated with differing size and age, only medium‐sized individuals with a carapace length of 40 ± 5 mm were selected. Selected individuals did not display any obvious injury (such as damaged carapace or loss of chelae, legs, or antennae), or regenerating chelae which might have affected their foraging behavior (Basil and Sandeman , Koch et al. ). The sex was recorded, although males and females have been documented as exhibiting no significant differences in behavior (Guan ), so this influence was not considered in experiments. Only intermolt individuals were used in the experiments (Kuhlmann et al. ) because activity and feeding behavior is known to be modified during ecdysis (molting; Reynolds ).
Each crayfish was housed individually between experiments and lettuce was provided ad libitum and supplemented with crayfish pellets (Tetra: TetraCrusa Menu) every other day when not involved in experiments. Preliminary tests indicated that when P. leniusculus were not fed in the days prior to experiments, insufficient numbers of G. pulex survived the experimental trials to enable analysis. All G. pulex specimens were collected from a local stream (Burleigh Brook, Loughborough, UK; 52°76′09″ N., −1°24′58″ W) where they occurred at high abundances (>100 individuals per m2) using a standard pond net (mesh size, 1 mm) prior to each experimental trial. Individuals used in the experiments consisted of mixed size classes; 1–10 mm length.
For experiments in which no organisms were present (control application experiments), sediment was applied to the surface of the top section and left for 24 h. Experiments with P. leniusculus present were initiated in the same manner but with the addition of one crayfish on the surface section immediately after the application of the sediment treatment. For experimental trials which included only G. pulex, seventy‐five individuals were released onto the top section of the columns and left for 24 h to redistribute themselves. Preliminary experiments indicated that this was a sufficient number for appropriate survival rates at the termination of the experiments to enable the detection of an avoidance behavior if present. In experimental trials where P. leniusculus and G. pulex were present at the same time, all G. pulex individuals were placed in the experimental facility and left to acclimatize for an hour prior to the addition of crayfish. A single pre‐conditioned (soaked in water) horse chestnut (Aesculus hippocastanum) leaf was placed in both sections of the sediment columns as a food source for the G. pulex to reduce intraspecific predation (Dick ). A slice of carrot (~10 g) and crayfish pellets were provided as alternative food sources for P. leniusculus (following Bubb et al. , Kuhlmann et al. ), to avoid excessive predation due to the absence of an alternate sedentary food source (Dorn , Ruokonen et al. ). Shelter, in the form of an open‐ended cylinder (110 × 100 mm), was provided for the crayfish in order to reduce pit digging behavior triggered by the absence of refuge (Johnson et al. ). This allowed the direct effect that foraging activities had on the ingress of fine sediment to be identified. New G. pulex specimens were used for each experimental trial. One crayfish was used per experimental trial, and each individual was used once for each treatment.
At the end of each experimental run (24 h), G. pulex individuals were collected and counted from each of the two substrate sections by washing the contents of each section through 4‐mm sieves. All fine sediment was removed from the column and subsequently oven dried at 60°C until a constant weight was recorded to determine mass per section. For the subsurface section, the mass of fine sediment initially placed in the section was subtracted from the total fine sediment mass to calculate the fraction which had infiltrated down into the subsurface. These masses were converted to infiltration rates (kg·m−2·day−1) as a measure of the amount of sediment mobilized.
Differences in infiltration rates between organism combinations for each sediment treatment were examined via a linear model using the function lm in the stats package in R version 3.12 (R Development Core Team ). Differences between all experimental treatments were tested using a Tukey post‐hoc test via the glht function in the multcomp package (Hothorn et al. ).
Differences in the abundance of G. pulex in the subsurface as a function of sediment treatment, P. leniusculus presence, and the interaction of the two factors were examined via a linear model and tested using a Tukey post‐hoc test. To assess differences in the vertical distribution of G. pulex (associated with avoidance behavior) within each sediment treatment and each organism combination (P. leniusculus presence or absence), a linear mixed effects model was employed with treatment specified as a fixed factor and substrate section nested within the experimental replicate (column) as a random factor (reflecting the fact that sections within individual columns were not independent). Post‐hoc tests were conducted using a Tukey post‐hoc test to determine the effect of the different sediment loadings on G. pulex movement patterns with and without P. leniusculus. Survivorship of G. pulex (number of individuals retrieved at the termination of the experimental trial) in the presence and absence of P. leniusculus and as a function of the sediment treatment was examined within a general linear model using the glm function in the stats package. A Poisson error distribution and log link structure were fitted to account for non‐normal residuals.
Infiltration rates of fine sand into the subsurface layer were greatest in experiments with P. leniusculus present (mean 1.93 kg/m2 ± SEM 0.10, 63.3% of the sediment initially applied on the surface of the upper layer). These rates were significantly greater (P = 0.026 Tukey) than under control conditions with no organisms present (1.61 kg/m2 ± SEM 0.06, 53.6%; Fig. A).
Enlarge this image.Mean infiltration rates (kg·m−2·day−1 ± 1 SE) for each biotic treatment: (A) 3 kg/m2 fine sedimentation; (B) 5 kg/m2 fine sedimentation; (C) 3 kg/m2 coarse sedimentation; and (D) 5 kg/m2 coarse sedimentation. Treatments where infiltration rates were not significantly different are denoted with the same letter (Tukey post‐hoc test P < 0.05). Note the order of magnitude reduction in vertical (infiltration rate) scale between fine (upper row) and coarse (lower row) sediment treatments.
Fine sand sedimentation experiments with P. leniusculus present had the greatest infiltration rates (mean 3.06 kg/m2 ± SEM 0.37, 61% of initial sediment, Fig. B); however, none of the pairwise comparisons were statistically different (Table ).
Tukey post‐hoc comparisons of sediment infiltration rates over the 24‐h experimental period for each sediment treatment| Organism by sediment treatment | Gammarus pulex | Pacifastacus leniusculus | G. pulex and P. leniusculus |
| 3 kg/m2 fine sedimentation | |||
| Control | 0.609 | 0.026 | 0.343 |
| G. pulex | 0.172 | 0.926 | |
| P. leniusculus | 0.497 | ||
| 5 kg/m2 fine sedimentation | |||
| Control | 0.998 | 0.098 | 0.673 |
| G. pulex | 0.110 | 0.774 | |
| P. leniusculus | 0.546 | ||
| 3 kg/m2 coarse sedimentation | |||
| Control | 0.955 | 0.992 | 0.902 |
| G. pulex | 0.996 | 0.998 | |
| P. leniusculus | 0.978 | ||
| 5 kg/m2 coarse sedimentation | |||
| Control | 0.821 | 0.275 | <0.001 |
| G. pulex | 0.062 | <0.001 | |
| P. leniusculus | 0.009 |
P values are presented for pairwise comparisons between organisms. Significant (P < 0.05) results appear in boldface.
No significant differences between infiltration rates with or without organisms were determined (Table ). All organism treatments displayed similar low sediment infiltration rates with surface clogging being evident (range 0.095–0.111 kg/m2, 3.1–3.7% of initial sediment application Fig. C).
Univariate linear model (LM) analysis for the abundance of Gammarus pulex within the subsurface associated with the presence of Pacifastacus leniusculus, sediment treatments (n = 5), and the interaction between these factors| Factor | df | F | P |
| P. leniusculus presence | 1, 40 | 22.14 | <0.001 |
| Sediment treatment | 4, 40 | 13.42 | <0.001 |
| Sediment treatment × P. leniusculus presence | 4, 40 | 1.42 | 0.247 |
Infiltration of sand into the subsurface was greatest when both P. leniusculus and G. pulex were present, and the rate was statistically greater than for control conditions (P < 0.001 Tukey), G. pulex (P < 0.001 Tukey), and for an individual crayfish (P = 0.009 Tukey; Table ). However, infiltration rates for all organism treatments were low when compared to fine sand treatments (range 0.082–0.286 kg/m2, representing only 1.6–5.7% of the initial sediment application; Fig. D).
The distribution of G. pulex between layers was dependent on the presence of P. leniusculus (P < 0.001) and fine sediment treatment (P < 0.001) but did not vary as a function of the interaction of these factors (P = 0.247; Table ; LMM).
In the absence of P. leniusculus, the majority of G. pulex remained in the surface layer, but in the presence of P. leniusculus, G. pulex were more equally distributed between the surface and subsurface layers (Fig. ). Statistical differences were apparent in the number of G. pulex recorded in the surface or subsurface layers for treatments when P. leniusculus were absent with a greater number of G. pulex recorded in the surface layer (t1,8 = −6.770, P = <0.001; Table ). The presence of P. leniusculus resulted in no differences between the layers.
Enlarge this image.Mean number of Gammarus pulex (± 1 SE) recorded at the end of the 24‐h experiment within surface (black) and subsurface (red) substrates for each sediment treatment in: (A) the absence and (B) presence of Pacifastacus leniusculus. For post‐hoc tests see Tables and .
| Sediment treatment | t | P |
| Crayfish absent | ||
| Open framework | −6.770 | <0.001 |
| 3 kg/m2 fine | −6.856 | <0.001 |
| 5 kg/m2 fine | −5.815 | <0.001 |
| 3 kg/m2 coarse | −11.109 | <0.001 |
| 5 kg/m2 coarse | −12.411 | <0.001 |
| Crayfish present | ||
| Open framework | −1.199 | 0.972 |
| 3 kg/m2 fine | −0.390 | 1.000 |
| 5 kg/m2 fine | −0.240 | 1.000 |
| 3 kg/m2 coarse | −4.197 | <0.001 |
| 5 kg/m2 coarse | −4.587 | <0.001 |
P values are presented for pairwise comparisons in the presence/absence of Pacifastacus leniusculus for each sediment treatment. Significant (P < 0.05) results appear in boldface.
The presence of P. leniusculus resulted in a greater number of G. pulex migrating into the subsurface (Fig. ). In the absence of P. leniusculus, 25% of individuals were located in the subsurface layer at the end of the experiment, but when crayfish were present, this proportion increased significantly to 50%. During experiments without P. leniusculus, there were significant differences in the vertical distribution of G. pulex (t1,8 = −6.856, P = <0.001), but no differences were evident when P. leniusculus were present (P > 0.05; Table ).
There were no significant differences in surface and subsurface abundances of G. pulex when crayfish were present (P > 0.05), but when P. leniusculus were absent the surface layer contained a greater number of individuals (t1,8 = −5.815, P = <0.001; Table ; Fig. ).
Unlike the control and fine sand treatments, when coarse sand was applied the majority of amphipods remained in the surface layer whether or not P. leniusculus was present (Fig. ). The number of G. pulex in surface and subsurface layers was significantly different in experiments with (t1,8 = −11.109, P = 0.010) and without P. leniusculus (t1,8 = 4.197, P = <0.001; Table ).
The greater loading of coarse sand was associated with the highest counts of G. pulex in the surface layer irrespective of P. leniusculus presence (Fig. ; Table ). The surface layer contained significantly greater numbers of G. pulex than the subsurface layer with (t1,8 = −4.587, P = <0.001) and without crayfish (t1,8 = −4.587, P = <0.001; Table ).
Overall, there were significant differences in the number of G. pulex in subsurface substrates when comparisons between sediment treatments, with or without P. leniusculus (Table ), were considered. In the absence of P. leniusculus, only the addition of the greatest loading of coarse sand (5 kg/m2) resulted in significant differences in the distribution of G. pulex compared to 3 kg/m2 fine sand (P = 0.022) and 5 kg/m2 fine sand (P = 0.005; Table ). In contrast, in the presence of P. leniusculus, the addition of 3 and 5 kg/m2 coarse sand treatments resulted in reduced numbers of G. pulex in the subsurface layer compared to clean gravel (P = 0.030 and P < 0.001, respectively), 3 kg/m2 fine sand (P = 0.006 and P < 0.001, respectively), and 5 kg/m2 fine sand (both instances P = <0.001; Table ).
Tukey post‐hoc comparisons of Gammarus pulex abundance in the subsurface layer. P values are presented for pairwise comparisons between sediment treatment| Sediment treatment | 3 kg/m2 fine | 5 kg/m2 fine | 3 kg/m2 coarse | 5 kg/m2 coarse |
| Pacifastacus leniusculus absent | ||||
| Open framework | 1.000 | 0.989 | 0.069 | 0.073 |
| 3 kg/m2 fine | 1 | 0.380 | 0.022 | |
| 5 kg/m2 fine | 0.140 | 0.005 | ||
| 3 kg/m2 coarse | 0.942 | |||
| P. leniusculus present | ||||
| Open framework | 1.000 | 0.942 | 0.030 | <0.001 |
| 3 kg/m2 fine | 1.000 | 0.006 | <0.001 | |
| 5 kg/m2 fine | <0.001 | <0.001 | ||
| 3 kg/m2 coarse | 0.651 |
Significant (P < 0.05) results appear in boldface.
Survivorship rates of G. pulex averaged 80% for all experiments but were highly variable as a function of crayfish presence/absence (Fig. ). Experiments conducted in the absence of P. leniusculus had a mean survivorship of 89% ± SEM 1.59 (range = 80–100%) compared to 70% ± SEM 3.52 when crayfish were present (range = 45–100%). The survivorship of G. pulex was dependent on the sediment treatment (P < 0.001) and the interaction of sediment treatment and P. leniusculus presence (P = 0.003; Table ; LMM). Pairwise comparisons across all treatment combinations indicated that the addition of 5 kg/m2 of coarse sediment in the presence of crayfish resulted in significantly lower survivorship (mean 56.27% ± SEM 5.04) of individuals compared to all substrate conditions when P. leniusculus were absent (all P ≤ 0.001; Table ; Fig. ). The addition of 3 kg/m2 of coarse sand and 3 kg/m2 fine sand in the presence of P. leniusculus resulted in significantly lower survivorship than both coarse sand treatments in the absence of crayfish (all P < 0.05; Table , Fig. ).
Enlarge this image.Survivorship of Gammarus pulex (n = 75) at the end of the 24‐h experiment in the absence (solid squares) and presence (dashed rhombus) of Pacifastacus leniusculus.
| Factor | df | z | P |
| P. leniusculus | 1, 40 | −0.190 | 0.850 |
| Sediment treatment | 4, 40 | 2.449 | <0.001 |
| Sediment treatment × P. leniusculus | 4, 40 | −2.949 | 0.003 |
Significant (P < 0.05) results appear in boldface.
| Substrate | P. leniusculus absent | Control | P. leniusculus present | ||||||
| Fine | Coarse | Fine | Coarse | ||||||
| 3 kg/m2 | 5 kg/m2 | 3 kg/m2 | 5 kg/m2 | 3 kg/m2 | 5 kg/m2 | 3 kg/m2 | 5 kg/m2 | ||
| P. leniusculus absent | |||||||||
| Control | 1.000 | 1.000 | 0.906 | 0.996 | 0.870 | 0.702 | 0.989 | 0.373 | <0.001 |
| 3 kg/m2 fine | 1.000 | 1.000 | 1.000 | 0.418 | 0.241 | 0.763 | 0.075 | <0.001 | |
| 5 kg/m2 fine | 0.993 | 1.000 | 0.582 | 0.376 | 0.883 | 0.140 | <0.001 | ||
| 3 kg/m2 coarse | 1.000 | 0.080 | 0.032 | 0.262 | 0.007 | <0.001 | |||
| 5 kg/m2 coarse | 0.277 | 0.144 | 0.610 | 0.039 | <0.001 | ||||
| P. leniusculus present | |||||||||
| Control | 1.000 | 1.000 | 0.999 | 0.060 | |||||
| 3 kg/m2 fine | 1.000 | 1.000 | 0.132 | ||||||
| 5 kg/m2 fine | 0.959 | 0.012 | |||||||
| 3 kg/m2 coarse | 0.361 |
Significant (P < 0.05) results appear in boldface.
This research sought to examine the behavioral strategies prey may use to evade predation, the engineering of a shared physical environment by a predator and its prey, and the impact that modifications to the prey's habitat as a result of biotic engineering and anthropogenic sediment loading may have for predator–prey interactions. In this study, freshwater amphipods utilized vertical avoidance behavior by actively moving into subsurface substrates to evade crayfish predation. However, the deposition of coarse fine sand clogged the surface layers of the substrate and reduced the effectiveness of this behavioral strategy resulting in increased predation (Fig. ). When considering the zoogeomorphic potential of taxa, crayfish influenced fine sand ingress but predator–prey interactions themselves were found to be a primary mediating factor, with the availability of prey resources controlling the foraging activity of crayfish and subsequently their direct effect on the sedimentology of the physical environment (Fig. ). The extent of this effect was, however, dependent on differences in the amount and grain size of the sediment loads applied. In the current experiments, large pore spaces prevented crayfish‐initiated infiltration of sand from reducing refuge habitat availability to the point that prey capture was more likely than for clean gravels. However, within a mixed, poorly sorted framework it is likely that crayfish‐augmented infiltration may have the potential to reduce interstitial refuge availability and as a result prey avoidance behavior (Fig. ). These ideas are captured in Fig. , which develops predator–prey–environment interactions (Fig. ) into a more complex model in which the fuller sets of interactions are recognized (Fig. ). This conceptual model emphasizes that predator–prey interactions should not be studied in isolation from the physical environment, and that the role of zoogeomorphic activity should be considered in the context of resource availability and other biotic drivers. The results also highlight the tantalizing prospect that predators may increase foraging success by inadvertently engineering changes in the environment (crayfish may increase fine sediment infiltration sufficiently to reduce available pore space), which requires further investigation in future studies. Each of the research questions we sought to address will be considered in the following sections where we examine the complex and three‐way relationship between predator–prey and the physical environment and the critical role that external factors may play.
Enlarge this image.Conceptualization of the work conducted in this study examining the interactions between predator–prey relations, the physical environment, and the addition of an external stressor building on the traditional concepts presented in Fig. . Specific examples in relation to fine sediment dynamics, Pacifastacus leniusculus and Gammarus pulex, are provided. Dashed arrows indicate processes which require further investigation to fully understand the implications for predator–prey–environment dynamics.
Many studies have examined the ingress of fine sands into gravel beds (e.g., Beschta and Jackson , Frostick et al. , Wooster et al. , Franssen et al. ), but to date none have examined how this process is affected by the zoogeomorphic activity of a single organism or the interaction(s) among multiple organisms. This study provides direct evidence that the presence of P. leniusculus alone and of G. pulex and P. leniusculus together can increase infiltration rates depending on the characteristics of the sediment involved. For fine sand treatments (grain size 0.125 μm–1 mm), the greatest geomorphic effect was associated with crayfish foraging and resulted in ~10% increase in fine sediment infiltration into the bed compared to control conditions (no organisms present) or when 75 G. pulex were present. The significant effect of a single crayfish suggests that under field conditions, and where interstitial spaces in the subsurface exist, sediment infiltration may occur at greater rates if crayfish densities are high. Given that P. leniusculus can reach densities up to 15 m−2 (Guan and Wiles ), the presence of this organism may significantly modify fine sediment movements between river bed surface and subsurface layers. No significant difference in infiltration rates was detected for G. pulex when in isolation, most likely associated with their relatively small body size (Moore ).
When both predator and prey were present (P. leniusculus and 75 G. pulex), sediment infiltration rates were on average 5% higher than control conditions or when only 75 G. pulex were present. It is likely that infiltration rates were reduced during these experiments because of direct prey–predator interactions that affected the zoogeomorphic behavior of prey and predator. First, for experiments without crayfish, the majority of G. pulex were in the surface layer and therefore had a greater opportunity to cause ingress of fine sediment over the course of the experiment. In contrast, in the presence of P. leniusculus, on average 25% more G. pulex migrated into subsurface habitats, and consequently, the sum influence on ingress was reduced. Second, in experiments where P. leniusculus were the only organism present, a large proportion of energy was expended in foraging for food. In a number of experiments, P. leniusculus exhibited bulldozing behavior by piling and moving the substrate (Helms and Creed , Johnson et al. ). This foraging behavior and the disturbance of surface sediments significantly affected the vertical movement of fine‐grained sediments into the bed. The addition of prey (G. pulex) resulted in a reduction in foraging activity due to the greater availability and number of encounters with food resources. It is assumed that during the experiments foraging activity would gradually decline over the 24‐h period as prey were consumed (Haddaway et al. ) and time between foraging activity would have increased. The overall effect was a reduction in bed disturbance caused by foraging, and therefore, a reduction in fine sediment ingress compared with that when P. leniusculus were alone. Prey availability may therefore be a key driver of zoogeomorphic activity. Reductions in prey availability may increase foraging behavior and inter‐species competition (especially for P. leniusculus which exhibits a high degree of intraspecific aggression; Pintor et al. ); this in turn may enhance fine sediment mobilization (suspension and ingress). These results support findings of other studies on predaceous stoneflies, which surmise that prey scarcity increases predator movement and thus the stability of fine sediments (Statzner et al. , Zanetell and Peckarsky ).
In contrast to fine sand deposition, the greater propensity of coarse sand to form a bridge between clasts and thus prevent further infiltration meant that biota had little effect on overall infiltration rates. Under 3 kg/m2 loadings, no significant differences in infiltration rates were recorded for any of the organism combinations, with only 3–4% (0.1 kg/m2) of the initial sediment application infiltrating into the subsurface. Application of 5 kg/m2 coarse sand resulted in limited differences in infiltration rates when animals were present, and although significant, the total mass of sediment was low compared to fine sand treatments (mean 0.14 kg/m2 ingress). For coarse sand sediment treatments, P. leniusculus generated significantly greater infiltration rates (an extra 0.1 g/m2 on average) compared to control or 75 G. pulex treatments. However, in contrast to fine sand applications, the combination of both G. pulex and P. leniusculus resulted in the greatest infiltration rates. With clogging of the surface layers of the substrate by coarse sands (Mathers et al. ), G. pulex were unable to migrate into the subsurface, and therefore, around 95% of individuals remained in the surface layer. This had a significant effect on infiltration rates in the coarse sediment experiment but at an order of magnitude lower than for the fine sand treatments.
The application of fine sediment (grain size 0.125 μm–1 mm) under both loadings (3 and 5 kg/m2) resulted in high infiltration rates under control conditions (gravity and downwelling flow) and all organism combinations. However, vertical connectivity was maintained due to the large interstitial spaces between gravel particles relative to the sand grain size (Xu et al. , Mathers et al. ). As a result, around 50% of G. pulex were able to migrate vertically into the subsurface when predatory crayfish were present. In the equivalent treatments without the predator, the majority of prey remained in the surface layer, probably reflecting the rheophilic preferences of G. pulex (Gledhill et al. ). The results therefore indicate that the presence of the crayfish predator significantly modified the vertical distribution of G. pulex and provides evidence of predator avoidance behavior.
In contrast, the addition of coarse sand sediments (1–4 mm) resulted in bridging of interstitial spaces within the surface layer of the substrates and clogging that disconnected the surface and subsurface layers regardless of zoogeomorphic activity. Infiltration rates were significantly lower for coarse sand than for fine sand treatments, with the majority of sand particles being retained in the surface layer for both organism combinations. As a result, no significant difference in the vertical distribution of G. pulex (with or without P. leniusculus) was observed. The formation of surface‐layer clogs probably restricted the ability of G. pulex to migrate into subsurface sediments (sensu Mathers et al. ) and influenced predator–prey relationships, in this instance through survivorship of G. pulex (Figs. B, ). In experiments where G. pulex could easily migrate, survivorship averaged 77% (± SEM 4.5) with no significant differences evident for any of the fine sand sediment or control treatments. The addition of coarser sand clogged the substrate interstices and prevented vertical avoidance behavior resulting in lower survivorship rates. 3 kg/m2 coarse sand resulted in moderately lower survivorship (70% ± SEM 5.1) and 5 kg/m2 reduced G. pulex survival to 56% (± SEM 4.5); a reduction of 28% compared to the control treatment (open gravel framework).
Despite P. leniusculus being a significant zoogeomorphic agent within fine sand treatments, in this set of experiments only the coarse sand treatment affected the vertical avoidance behavior and subsequent predation rates. This result is predominately a function of the open gravel framework used in the experiments (Xu et al. ) and we therefore hypothesize that under natural conditions, where poorly sorted mixed gravel frameworks exist, ingress of sand augmented by P. leniusculus may influence pore space sufficiently to affect avoidance behavior in many instances. If this is the case, P. leniusculus may inadvertently improve their predatory success by increasing fine sediment content within the river bed, an example of extended phenotype engineering, whereby the organism creates structures or effects that directly influence their fitness and survival (Jones et al. , Wright and Jones ). This hypothesis requires further detailed investigation to fully understand the feedbacks between predator–prey and the physical environment (sensu Fig. ).
This research illustrates how the structure of the physical environment potentially influences predator–prey interactions (Figs. B, ). In each experiment, the nature of the physical environment was a key control on these interactions and feedback, with different outcomes dependant on the amount and grain size of the fine sediment applied. The deposition of coarser sand grains has the potential to reduce the effectiveness of a prey's avoidance behavior and render them susceptible to enhanced predation. This suggests that in nature, spatial and temporal variations in fine sediment dynamics will partly regulate these interactions and further field experimentation is required to test this more rigorously. Sediment dynamics in rivers vary as a function of the abiotic hydro‐geomorphological regime, but anthropogenic activities (agriculture, urbanization, forestry, construction, mining) increase sediment loading (Owens et al. ) and, in the UK, sediment recruitment to rivers may be further increased in the presence of P. leniusculus through burrowing activities (Faller et al. , Rice et al. ). It is therefore possible that anthropogenic sedimentation has facilitated the success of invasive P. leniusculus by reducing the availability of hyporheic refugia for prey species.
The results of this study demonstrate that fine sediment ingress into gravel river beds can be caused by expenditure of biological energy under certain environmental conditions; that prey utilize avoidance strategies to evade predation; that predator–prey interactions themselves mediate the zoogeomorphic effectiveness of an organism and that these interactions and feedbacks are dependent on the environmental context. We present a new conceptual model that captures the interactions between predator, prey, zoogeomorphic processes, and habitat availability (Fig. ) highlighting that interactions between ecosystem processes may be strongly mediated by dynamic bi‐directional interactions between organisms and the physical environment they inhabit. Ecological (predation, avoidance) and geomorphological processes (sediment infiltration) are intrinsically linked and should not be studied in isolation.
KLM acknowledges the support of a Glendonbrook doctoral studentship and co‐funding from the Environment Agency to undertake this study. Thanks go to Stuart Ashby and Richard Harland for providing technical and laboratory support and to Nigel Wilby and Nicholas Clifford for useful discussions pertaining to the study outcomes. The comments of two anonymous reviewers have significantly improved the clarity of this study.
© 2019. This work is published under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Details
; Rice, S P 2 ; Wood, P J 2 1 Eawag, Swiss Federal Institute of Aquatic Science and Technology, Department of Surface Waters Research and Management, 6047 Kastanienbaum, Switzerland
2 Geography and Environment, Centre for Hydrological and Ecosystem Science, Loughborough University, Loughborough, Leicestershire, UK