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Inter-patch connectivity and intra-patch structure differentially alter prey consumption by multiple predators KRISTOPHER A. PITCHER AND DANIEL A. SOLUK Department of Biology, University of South Dakota, 414 E. Clark Street, Vermillion, South Dakota 57069 USA Citation: Pitcher, K. A., and D. A. Soluk. 2016. Inter-patch connectivity and intra-patch structure differentially alter prey consumption by multiple predators. Ecosphere 7(11):e01598. 10.1002/ecs2.1598

Abstract. Structural habitat complexity (SHC) and functional habitat connectivity (FHC) have important effects on predator–prey interactions and exert a strong influence on community structure/dynamics in terrestrial and aquatic ecosystems. Although these factors vary simultaneously in most systems, their interactive effects are poorly understood. Using artificial pond mesocosms and multiple prey types, we manipulated plant density (SHC: low, high) and inter-patch distance (FHC: short, long) in a full factorial design to test for potential interactive effects of these factors on competition and predation by a dragonfly larva (Anax junius) and fish predator (Lepomis cyanallus). When inter-patch distances (FHC) were short, A. junius consumed more amphipods (36% 4.6%) compared with long treatments (19% 4.8%). We detected no significant effects of plant density (SHC) on prey consumption by A. junius. There were significant interactive effects of FHC and SHC on Lepomis cyanellus consumption of amphipods and damselflies. The most counterintuitive of these effects was that sunfish consumed more larval damselflies at high plant density (64% 6.0%) than at low plant density (38% 8.6%) but only in short connection treatments. This interactive effect of SHC and FHC on damselfly predation by L. cyanellus was likely because damselflies exhibited riskier behavior at higher SHC. Prey consumption with both predators present was additive, but no significant effect of either SHC or FHC on interspecific predation was detected, suggesting compensatory foraging responses. Structural habitat complexity and FHC interactively influence predator foraging behavior in complex, non-intuitive ways that are highly dependent on the predator/prey combination in question. Structural habitat complexity and FHC are currently being influenced by anthropogenic factors in multiple ways (e.g., habitat loss, global climate change), and being able to predict the responses of biotic communities to these changes should be an important consideration in restoration and conservation efforts. Key words: Anax junius; functional habitat connectivity; habitat structure; inter-patch distance; Lepomis cyanellus; multiple predator; spatial complexity; structural complexity. Received 6 October 2016; accepted 14 October 2016. Corresponding Editor: Debra P. C. Peters. Copyright: © 2016 Pitcher and Soluk. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected]

INTRODUCTION

Warfe and Barmuta 2006, Yee 2010) oviposition (Sadeh et al. 2009), competition (Hampton 2004), and dispersal/colonization (Huffaker 1958, Yee et al. 2009). In turn, these effects on behavior can influence trophic cascades (Grabowski et al. 2008), community assemblages (Wesner et al. 2012), nutrient cycling (Atwood et al. 2014), the impacts of invasive species (Ruokonen et al.

In most terrestrial and aquatic habitats, organisms have to interact with a complex and dynamic structural maze of plants, substrates, and other abiotic and biotic features. This structural matrix can have important effects on animal behaviors, such as foraging (Huffaker 1958, ❖ www.esajournals.org

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The relationship between SHC and predation rates can be either negative or positive depending on the behavioral responses of both the prey and the predators that are present (Giller and McNeill 1981, Briers and Warren 1999, Saha et al. 2012). Structural habitat complexity can reduce predation rates by providing refuge for prey (Crowder and Cooper 1982, Lewis and Eby 2002) or can increase predation rates by providing cover for ambush predators (James and Heck 1994, Flynn and Ritz 1999, Yee 2010). The behaviors of multiple predators can also be modified by SHC and result in non-additive (i.e., synergistic or interference) effects on prey populations (Soluk and Collins 1988, Soluk 1993, Swisher et al. 1998). In streams, for example, stoneflies exploit the fish-free refuge within rocky substrates and this prompts their prey to move to exposed surfaces or escape into the water column, where they can then be preyed upon by fish (i.e., a non-additive synergistic effect; Soluk and Collins 1988, Soluk 1993). Structural habitat complexity has also been theorized as a possible mechanism that mitigates competition among conflicting predators and may promote coexistence (Schoener 1974). By increasing spatial complexity as well as promoting higher diversity and abundance in prey resources, SHC should allow more species to coexist within a habitat (Briers and Warren 1999, Hampton 2004, Warfe and Barmuta 2006). Finally, the effects of SHC on the dispersal responses of aquatic invertebrate predators have been theorized as important mechanisms influencing community structure both within and among aquatic habitats (Goodwin and Fahrig 2002, Yee et al. 2009). However, when compared to the effects of SHC on either competition or predation, the effects of SHC on dispersal, especially within habitat patch movement, are poorly understood. Depending on the hunting mode of the predator in question (e.g., active, sit-and-wait), SHC may promote or dissuade an individual from making the behavioral choice to move between habitat patches. For example, an active predator that has higher hunting success in low vegetation patches, where prey have less places to hide, may be less likely to disperse from this type of patch when compared to patches that have higher SHC. Functional habitat connectivity at both the landscape and local scales also influence

2014), and other ecosystem dynamics. Although there are a myriad of terms describing the physical architecture of an ecosystem, habitat structure is often defined by two main components: structural habitat complexity (SHC; e.g., vegetation, substrate, size of habitat) and functional habitat connectivity (FHC; e.g., distance between discrete habitat patches; McCoy and Bell 1991, Beck 2000). Both SHC and FHC can rapidly change in a number of different habitat types due to shortterm seasonal variations such as flooding, drought, and plant growth (Sousa et al. 2011). For example, as plants grow outward in either terrestrial or aquatic systems (e.g., forests, marine grass beds, ponds), stem densities and patch size increase and distance between patches decreases. Floods and droughts both can be strong influences on these patterns of growth in both terrestrial and aquatic plants. Flooding can also decrease inter-patch distances and create connections between isolated aquatic habitats (e.g., wetlands, streams, rivers) while having the opposite effect on terrestrial habitats (e.g., prairies, forests; Junk et al. 1989). Drought in aquatic systems can increase inter-patch distances between aquatic habitats (e.g., wetlands, streams). The short-term dynamics of SHC and FHC are especially apparent within temporary and semi-permanent pond habitats that undergo repeated inundation and drying events along with repeated cycles of plant growth and die back (Welborn et al. 1996, Williams 1996). Such environments present unique opportunities to empirically test how these factors independently and interactively influence predator/prey dynamics. The effects of SHC on species interactions (e.g., predation, competition), and the dispersal/colonization responses of aquatic predators and prey in pond habitats are thought to be one of the most important variables influencing the structure of aquatic invertebrate communities (Benke 1978, McCoy and Bell 1991, Kovalenko et al. 2012). The term “habitat complexity” has been used in a number of ways in the literature (Kovalenko et al. 2012), but for this study we are referring to SHC (a.k.a. architectural complexity; Atilla et al. 2005) specifically as the surface area and density produced by different structural components within a habitat patch (e.g., vegetation, substrate, coarse woody debris), which is usable by the organisms in question (Beck 2000). ❖ www.esajournals.org

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may discourage dispersal. In complex habitat units, such as ponds and wetlands where changes in plant growth and water level can alter patch sizes and overall spatial arrangement of patches, it seems especially likely that FHC will strongly influence the distribution of aquatic invertebrate predators. Ultimately it is important to consider that organisms in dynamic habitats experience changes in both SHC and FHC simultaneously. Because both of these variables can affect species interactions and movement, it is important to understand how SHC and FHC may directly and interactively alter predator–prey dynamics and multiple predator effects, and indirectly influence community structure and ecosystem function. Through a series of mesocosm experiments, this study attempts to understand how both FHC and SHC interactively influence multiple predator foraging behaviors and competitive interactions among habitat patches and how this in turn might alter the patterns of abundance in prey communities. Specifically, we focused on the foraging behaviors of two co-occurring predators with different hunting modes (i.e., active, ambush), green sunfish (Lepomis cyanellus; Rafinesque 1891), and common green darner dragonfly larvae (Anax junius; Drury 1773), on multiple prey types under different plant densities (a.k.a. SHC) and between patch distances (a.k.a. FHC). We predicted that: (1) for the active fish predator, increasing FHC will increase both prey consumption and interspecific competitive interactions because the predator will spend less time moving between more connected patches and more time hunting and interacting with conspecifics; (2) for the less mobile dragonfly predator, increasing FHC will also increase interspecific interactions, but it will have a diminished influence on prey consumption because the predator will use the inter-patch connections less frequently; (3) increasing SHC will negatively affect prey consumption by active predators because it provides better refuge for the prey, while at the same time increasing prey consumption by ambush predators because it provides better cover; (4) increasing SHC will reduce competition and possibly promote positive interactions between the two predator types because the ambush predator can better avoid detection and interaction with the active predator, while

predator–prey interactions and community structure in pond habitats, but its effects are less understood. In this study, the term FHC is defined as the measurable physiographic attributes of the landscape (e.g., inter-patch distance, number of patches, dispersal barriers), which can constrain the movement of a specific organism among habitat units or patches (Tischendorf and Fahrig 2000, Bilton et al. 2001). Functional habitat connectivity can affect competition and predation in multiple ways. Habitat units within a landscape that are more isolated, and thus have lower FHC, often exhibit a negative relationship with species richness (Ficetola and Bernardi 2004, McCauley 2006). This negative relationship suggests that predation or competition may either be: (1) weaker in isolated units (i.e., low FHC) because only a few predators or competitors can colonize the units from source populations, or (2) initially stronger because predators or competitors are less likely to leave the units increasing the intensity of interactions. The effect of FHC on the dispersal of organisms has received substantially more attention, and theoretical models suggest the decision to disperse to other habitat units in a landscape is determined in part by unit isolation (i.e., low FHC), with less isolated units having more individuals dispersing and colonizing them (Gustafson and Gardner 1996). This relationship is empirically apparent between the isolation of aquatic habitat units in a landscape and the colonization rates of dominant aquatic predators such as backswimmers (notonectids), dragonfly larvae (odonates), and predacious diving beetles (dytiscids) (Wilcox 2001, McCauley 2006). Habitat choice by organisms may also interact with FHC resulting in situations where organisms avoid suitable habitat units because other nearby habitat units in the landscape are unsuitable (Kneitel and Chase 2004, Resetarits and Binckley 2009, Wesner et al. 2012). This suggests FHC can have a significant effect on movement behaviors of predators and prey among habitat units within a larger landscape. This movement of organisms among habitat units in the landscape is also likely influenced by internal inter-patch connectivity within these habitat units. For example, high inter-patch distances between patches within a habitat unit may encourage dispersal to a new habitat unit, whereas low inter-patch distances ❖ www.esajournals.org

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habitats in North America, actively use vegetation for cover, and are readily consumed by at least one (i.e., snails by A. junius) or both of the predators (i.e., amphipods, damselflies; A. junius: Folsom and Collins 1982, Turner and Chislock 2007; Lepomis: Sadzikowski and Wallace 1976, Savino et al. 1992).

each predator type forces prey into or out of the structural refuge; and finally (5) FHC and SHC will interact creating complex non-intuitive outcomes as predators balance the costs of remaining in a patch that may be suboptimal or spending time moving to a new patch.

METHODS

Mesocosm design and arrangement

This study uses an experimental mesocosm approach to separate out the effects of SHC and connectivity. These mesocosms provide a simplified but realistic model of a natural pond habitat that can be easily manipulated, controlled, and replicated.

Sixteen mesocosms were set up evenly in four rows in an open field at the Illinois Dragonfly Research Facility located at the Waterfall Glen Forest Preserve near Lemont, Illinois. Each mesocosm was constructed from two 320-L plastic trashcans (0.7 m diameter) each filled with 120 L of filtered well water and connected via 7.62 cm diameter PVC pipes creating two habitat patches (Fig. 1). The volume of the connections either 5.4 or 0.5 L, for the long or short connection, respectively. This minor difference in volume was considered negligible. Air stones were placed into each patch of the mesocosm and were run for the duration of each run of the experiment to prevent mesocosms from becoming anoxic during high temperature days. In the middle of the PVC connectors, a video camera with motion detection was mounted to a Y-bend in order to determine predator movement between patches. Before predators or prey were added, and during the experiment, mesocosms were entirely covered with 40% shade cloth to prevent invertebrate colonization and allowed to sit for at least 24 h to stabilize temperature and dissolved oxygen before running the experiment. In order to initially determine whether the predators would cross through the pipe connections, we video-recorded predator movement of both predators in multiple 4- to 6-h sessions using clear PVC. The video footage showed that both predators readily exploited the pipe connection and remained within the pipe for no longer than 1.5 min at a time. Additionally, A. junius only swam through the pipes using jet propulsion from their specialized rectal chamber, a behavior used most typically to escape from a dangerous situation. These responses indicate that both predators identify the pipe as a vulnerable location (e.g., open water) rather than a safe one (e.g., a vegetated patch). At the end of the experiment we also analyzed a sub-sample of the recorded video movement footage between the white PVC

Study organisms

Anax junius dragonfly larvae and first-year L. cyanellus used in this study were collected using minnow traps and a seine from nearby pond habitats where they co-occur. These predators were chosen because they are respectively voracious for a dragonfly and fish predator, and they both are commonly found in vegetated pond habitats throughout North America. In order to prevent cannibalization, A. junius were kept inside at ambient temperatures in individual 473-mL plastic containers along with a stem of vegetation for a perch. Between trials, dragonfly larvae were fed prey items from nearby ponds (e.g., midge larvae, snails, amphipods) every other day and kept on a normal summer light regime (i.e., 14-h:10-h light: dark). Lepomis cyanellus were kept together in two aerated 166-L holding tanks located next to the experimental mesocosms. Lepomis cyanellus were fed similar aquatic prey items (e.g., midge larvae, worms, amphipods) and consumed terrestrial insects that fell into the tanks. Bladder snails (Physa spp.), amphipods (2–4 mm TL; Malacostraca: Amphipoda), and damselfly larvae (3–6 mm TL; Enallagma geminatum and Ischnura verticalis) were collected from the field and cultured in the laboratory. The size of the amphipods relative to the damselflies should have eliminated any possible effects of intraguild predation among prey. Prey were fed right until they were placed in mesocosms, preventing any potential starvation behaviors that may have enhanced consumption during experimental runs. These prey were chosen because they co-occur widely in pond ❖ www.esajournals.org

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Fig. 1. Dual patch mesocosm layout. Long and short lengths of PVC pipe connected the individual barrels (patches). A “y” connector was used to house a motion-activated camera to capture crossing events by predators. Polyolefin rope was used to simulate erect plant stem.

1956). The sizes of sunfish used were between 60 and 80 mm fork length. To test for the effects of SHC and functional connectivity on predator competition and foraging behavior, we used two densities of artificial plants connected by either long or short distances. Strands of 4 mm diameter, polyolefin fiber rope, eight cm long, and weighed down in the middle with a stainless steel mass were used to create patches of high (40 stems per patch) and low (20 stems per patch) stem densities (Fig. 1). PVC pipe (3 inches) was used to create either a long (1.5 m), or short (0.3 m) connection between patches (Fig. 1). We used four predator treatments (19 A. junius, 19 L. cyanellus, 19 A. junius + 19 L. cyanellus, no predator) resulting in 16 possible treatment combinations that were assigned to each mesocosm group using a latin square design. Video cameras recorded movement of predators from one patch to another over a 24-h period. After 24 h, predators were removed and remaining prey removed using a dip net. Mesocosms were then emptied, scrubbed, rinsed, and refilled before each run of the experiment. The 24-h time period was chosen because it was short enough to prevent predators from consuming all the prey at the tested densities, while at the same time encompassing both diurnal and nocturnal behaviors of the predators. Water temperature, conductivity, dissolved oxygen, and pH were also recorded at the end of the experiment. A

connections for each replicate from 09:00 hours to 10:00 hours and 21:00 hours to 22:00 hours. Within these two time periods, we recorded how many crosses were observed per hour, as well as the average time it took a predator to cross in order to confirm that the connections were used and that neither predator exploited this artificial connection as a refugee for a prolonged period of time (i.e., >1.5 min).

Testing effects of SHC and connectivity on competition and foraging behavior Each trial was begun by introducing 10 snails (26.3 individuals/m2), 10 amphipods (26.3 individuals/m2), and five damselflies (13.2 individuals/m2) into each mesocosm patch. A single predator (2.6 individuals/m2) was randomly added to one of the mesocosm patches in their respective treatment 30 min after prey were introduced. Prey and predator densities were within the natural range of nearby pond densities (K. A. Pitcher, personal observation). Before each trial, predators were starved for 24 h in the laboratory, measured, and photographed. In the case of the dragonfly larvae, new individuals were used for each run of the experiment. Head widths of dragonfly larvae used varied between 5.0 and 8.2 mm (instars F-5 to F-1). Due to limited numbers, sunfish were used multiple times throughout the experiment, but were randomly selected from a pool of 16 individuals to diminish possible effects of individual learning (Hale ❖ www.esajournals.org

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RESULTS

complete replicate was run once a week for five weeks between 22 July 2014 and 26 August 2014, resulting in a total of four to five replicates for each treatment combination.

Predator crossing behavior No crossings were recorded for A. junius. Lepomis cyanellus averaged between seven and 17 crosses per hour, but we detected no significant difference between treatments (Fig. 2). The majority of crosses lasted under 15 s, with the longest crossing behavior taking approximately 1 min. This confirms our preliminary findings that there is no evidence that the fish predator used the connection as a refuge and that the connection tubes did not create additional SHC in the mesocosm.

Analysis All statistical analyses were run using JMP version 12.1.0 (SAS Institute, Cary, North Carolina, USA). For the crossing data, we ran a three-factor ANOVA with a full factorial design to determine whether there was an interactive or independent effect of inter-patch distance, stem density, or predator treatment on the mean number of crosses per hour by the fish predator. Sampled prey densities in predator treatments were adjusted by subtracting their respective daily controls to account for random mortality and create a more accurate predator consumption value hereafter referred to as adjusted prey consumption. For each predator type, we ran three separate two-factor ANOVAs with a full factorial design that tested the separate and interactive effects of vegetation density and connection length on the percent adjusted prey consumption (e.g., amphipod, snail, damselfly). If a significant interactive effect was found, a post hoc Fisher’s least significant difference (LSD) (a = 0.05) test was then used to determine which treatments were significantly different than one another. We did not use predator treatment as a third factor in our ANOVA model because (1) we were not interested in testing whether dragonflies eat less than sunfish because this is already well established and would not likely to be influenced by the factors we tested, and (2) the interspecific predator treatments are additive and would confounded predator identity with predator density. Instead, to compare between intra- and interspecific treatments, we used an additive probability model (Soluk and Collins 1988, Soluk 1993) to calculate expected prey consumption when both predators are present. We ran three two-factor ANOVAs to determine whether there was an interactive effect, or an independent effect of connection distance or stem density on the mean adjusted proportion of prey consumption for each prey type. We then used a three-factor nested design ANOVA with vegetation density, connection length as the main factors, expected vs. actual as the nested factor and mean adjusted proportion of prey consumption as the dependent variable. ❖ www.esajournals.org

Effect of SHC and FHC on individual prey mortality Week that that trial was run was initially incorporated as a blocked factor but consistently had a P-value > 0.40, so it was dropped from the model. Densities of each prey type were adequate to prevent total consumption within 24 h in all treatments. Assumptions of normality and homoscedasticity were met for all ANOVA comparisons. For A. junius, the results of the two-factor ANOVAs showed that there was a significant effect of FHC on adjusted amphipod

Fig. 2. Influence of stem density (structural habitat complexity), inter-patch distance (functional habitat connectivity), and the presence of an interspecific competitor on the between patch crossings per hour (mean SE) by sunfish (Lepomis cyanellus). Intraspecific treatments are in gray, and interspecific are in white.

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PITCHER AND SOLUK Table 1. Results of ANOVAs for the effects of SHC, FHC, and SHC by FHC interaction on adjusted prey consumption by Anax junius. Prey Damselfly

Factor

SHC (stem density) FHC (inter-patch distance) SHC 9 FHC Amphipod SHC (stem density) FHC (inter-patch distance) SHC 9 FHC Snail SHC (stem density) FHC (inter-patch distance) SHC 9 FHC

df F ratio P value 16 16 16 16 16 16 16 16 16

4.072 0.602 0.024 1.852 7.910 3.630 0.091 0.495 0.091

0.061 0.450 0.879 0.192 0.013* 0.075 0.767 0.492 0.767

Note: FHC, functional habitat connectivity; SHC, structural habitat complexity. * denotes significance.

mortality (F1,16 = 7.91, P = 0.013), with all other factors (i.e., SHC, interaction) being insignificant (Table 1, Fig. 3). For L. cyanellus, there was an interactive effect of SHC and FHC on damselfly mortality (F1,16 = 9.14, P < 0.01), and amphipod mortality (F1,16 = 10.89, P = 0.01), but no effect of SHC or FHC on snail mortality (Table 2). Post hoc analysis indicated specific differences between treatments for each prey mortality response (Fig. 4).

Effect of SHC and FHC on interactions between predators Assumptions of normality and homoscedasticity were met for all ANOVA procedures. The initial two-factor ANOVAs on the interspecific predator consumption data found no effect of SHC or FHC on any of the adjusted prey mortalities (Table 3). The three-factor nested ANOVA found no effect of SHC or FHC on the actual vs. expected prey consumption comparisons suggesting that interspecific predation was additive regardless of the treatment or prey type (Table 4, Figs. 5–7). Fig. 3. Effects of stem density (SHC, structural habitat complexity) and inter-patch distance (FHC, functional habitat connectivity) on adjusted predation rates (mean SE) of dragonfly larvae (Anax junius) on amphipod and damselfly prey. Results are grouped by levels of FHC and then sub-grouped by levels of SHC on the x-axis. Treatments with the same letters were not significantly different.

DISCUSSION The effects of both SHC (Huffaker 1958, Crowder and Cooper 1982, Diehl 1992), and to a lesser extent FHC (Huffaker 1958, Wilcox 2001, McCoy et al. 2009), on predator–prey dynamics have received substantial attention by ecologists.

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has been found in other aquatic predators (James and Heck 1994, Lombardo 1997, Warfe and Barmuta 2006), and may either suggest (1) that the higher stem density treatment may not have been high enough to provide adequate refuge, (2) the densities of prey were too low to elicit an effect, or (3) the observations of higher A. junius abundance in high SHC in the wild is a result of increased refugia from predators rather than an optimal habitat for ambushing prey (Lombardo 1997). Although there were no apparent strong effects for the dragonfly larvae, the interaction between

Table 2. Results of ANOVAs for the effects of SHC, FHC, and SHC by FHC interaction on adjusted prey consumption by Lepomis cyanellus. Prey Damselfly

Factor


df F ratio P value 16 0.063 16 0.571 16 9.142 16 2.371 16 0.091 16 10.887 16 0.672 16 0.000 16 1.058

0.804 0.461 0.008* 0.143 0.355 0.005* 0.423 1.000 0.319

Note: FHC, functional habitat connectivity; SHC, structural habitat complexity. * denotes significance.

However, while ecologists have some understanding of the independent importance of SHC and FHC on predation and competition, our understanding of how they interact to alter predator/prey dynamics and behavior is very limited, especially if we are considering assemblages with multiple predators and prey. As predicted, the results of our study suggest that SHC and FHC do have a significant interactive influence on predator foraging behavior and this interaction depends on the particular predator/ prey combination in question. In the case of A. junius, no interactive effect was detected, but higher FHC (i.e., shorter patch connections) did increase consumption of benthic prey (i.e., amphipods) regardless of SHC (Fig. 3). Consistent with the predictions of optimal foraging theory (e.g., MacArthur and Pianka 1966, Pyke et al. 1977), these results suggest that longer patch connections do in fact cause either the amphipod prey or the dragonfly predator to spend more time moving between patches, thus effectively reducing fatal encounters between the two in the short term. In preliminary studies, using a clear PVC tube connection, we did document several crossings by A. junius using high-definition video cameras; however, the security cameras were visually restricted by the solid white PVC and their motion sensors were not sensitive enough to detect A. junius or prey movement. Thus, we were not able to determine whether it was the behavior of the predator or prey that was the driving mechanism for this FHC effect. The lack of an effect of SHC on prey consumption by the dragonfly larvae was surprising, but ❖ www.esajournals.org

Fig. 4. Interactive effects of stem density (SHC, structural habitat complexity) and inter-patch distance (FHC, functional habitat connectivity) on adjusted predation rates (mean SE) of sunfish (Lepomis cyanellus) on amphipod and damselfly prey. Results are grouped by levels of FHC and then sub-grouped by levels of SHC on the x-axis. Treatments with the same letters were not significantly different.

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PITCHER AND SOLUK Table 3. Results of ANOVAs for the effects of SHC, FHC, and SHC by FHC interaction on adjusted prey consumption by Anax junius and Lepomis cyanellus. Prey

Factor

Damselfly


df F ratio P value 14 3.175 14 0.794 14 0.286 14 0.557 14 0.008 14 0.001 14 0.1462 14 1.600 14 0.458

0.097 0.388 0.601 0.468 0.928 0.990 0.708 0.227 0.510

Note: FHC, functional habitat connectivity; SHC, structural habitat complexity.

SHC and FHC on prey consumption was apparent for the active predatory sunfish. Lepomis cyanellus exhibited a positive relationship between FHC and prey consumption of amphipods and damselflies at high SHC (Fig. 4). The longer time spent in the artificial patch connections seems to significantly reduce successful prey capture as it did for the dragonfly predators. However, when SHC was low the increased traveling cost associated with the longer inter-patch distance seemed to become relatively insignificant. As predicted, higher SHC did significantly

Fig. 5. Interactive effects of stem density (SHC, structural habitat complexity) and inter-patch distance (FHC, functional habitat connectivity) on actual and expected, combined predation (mean SE) by dragonfly larvae (Anax junius) and fish (Lepomis cyanellus) on amphipod prey. Expected values were calculated using an additive probability model to calculate expected prey consumption when both predators are present. Results are arranged by levels of SHC on the top x-axis, levels of FHC treatments on the left y-axis, and actual vs. expected values sub-grouped on the bottom x-axis.

Table 4. Results of ANOVAs for the effects of SHC, FHC, and SHC by FHC interaction on expected vs. actual comparisons of adjusted prey consumption by Anax junius and Lepomis cyanellus. Prey

Factor

df

F ratio

P value

Damselfly

Expected vs. Actual (E vs. A) SHC (stem density) 9 E vs. A Depth 9 E vs. A SHC 9 Depth 9 E vs. A Expected vs. Actual (E vs. A) SHC (stem density) 9 E vs. A Depth 9 E vs. A SHC 9 Depth 9 E vs. A Expected vs. Actual (E vs. A) SHC (stem density) 9 E vs. A Depth 9 E vs. A SHC 9 Depth 9 E vs. A

28

0.331

0.570

28

1.798

0.184

28 28 28

0.890 1.272 0.005

0.422 0.296 0.944

28

1.469

0.248

28 28 28

0.989 1.970 3.393

0.385 0.158 0.076

28

0.723

0.494

28 28

0.559 0.752

0.578 0.781

Amphipod

Snail

decrease fish consumption of amphipods, but this effect was lost when FHC was higher (Fig. 4). This suggests that the benefit of increased refugia from higher SHC may become insignificant for prey when shorter inter-patch distances increase predator visitation and occupation of a patch. In contrast, more damselfly larvae were consumed in high SHC treatments compared with low SHC when FHC was higher. This result appears counterintuitive, as the majority of studies that have looked at the effects of SHC on prey capture rates by predators at varying levels almost always suggest that there is a negative relationship between the two (Huffaker 1958, Crowder and Cooper 1982, Gilinsky 1984, Diehl 1992). Our result is possibly explained if increasing SHC alters how the damselfly responds to the presence of the fish predator. Species of damselfly larvae similar to those used in this study have been observed to significantly reduce conspicuous movement when placed in an open tank with a fish and/or

Note: FHC, functional habitat connectivity; SHC, structural habitat complexity.


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facilitation within any of the treatment combinations (Figs. 5–7). Furthermore, the fact that the effects of SHC or FHC were lost in the multiple predator treatments is surprising (Figs. 5–7). This loss of a significant effect of either SHC or FHC on combined prey consumption may suggest that while the predators are not benefiting each other (causing higher prey consumption than expected), they do seem to at least complement each other in these different environmental arenas so that any negative influence of SHC of FHC is moderated by having a second predator that has a different hunting mode. This is consistent with findings that larger aquatic invertebrate predators (e.g., dragonfly larvae) may still play an important role in overall food-web dynamics even in systems where fish exhibit a comparably stronger predatory force on the prey community (Diehl 1992). Our study suggests that incorporating both SHC and FHC into predation experiments may

Fig. 6. Interactive effects of stem density (SHC, structural habitat complexity) and inter-patch distance (FHC, functional habitat connectivity) on actual and expected, combined predation (mean SE) by dragonfly larvae (Anax junius) and fish (Lepomis cyanellus) on damselfly prey. Expected values were calculated using an additive probability model to calculate expected prey consumption when both predators are present. Results are arranged by levels of SHC on the top x-axis, levels of FHC treatments on the left y-axis, and actual vs. expected values sub-grouped on the bottom x-axis.

dragonfly predator (McPeek 1990, Schaffner and Anholt 1998). However, at high SHC the risk of detection and predation is decreased and the cost of damselfly larvae moving within a patch normally decreases (Dionne et al. 1990). Theory suggests that at higher SHC, prey (e.g., damselfly larvae) become more emboldened, shifting to a more optimal foraging strategy, especially when patches are distantly connected and the threat of predation is decreased (MacArthur and Pianka 1966, Pyke et al. 1977, Brown et al. 1999). However, our findings suggest that this increased behavior in high SHC becomes suboptimal in closely connected habitats because the threat of predation is misinterpreted by the prey that are unable to perceive the larger scale spatial risk (i.e., closer connected habitats increase predator encounters). Counter to our predications, the interspecific treatments containing both A. junius and L. cyanellus did not exhibit any non-additive ❖ www.esajournals.org

Fig. 7. Interactive effects of stem density (SHC, structural habitat complexity) and inter-patch distance (FHC, functional habitat connectivity) on actual and expected, combined predation (mean SE) by dragonfly larvae (Anax junius) and fish (Lepomis cyanellus) on snail prey. Expected values were calculated using an additive probability model to calculate expected prey consumption when both predators are present. Results are arranged by levels of SHC on the top xaxis, levels of FHC treatments on the left y-axis, and actual vs. expected values sub-grouped on the bottom x-axis.

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in many ecosystems (e.g., global climate change, habitat loss, invasive species, agriculture; Samson and Knopf 1994, Mulholland et al. 1998, Amezaga et al. 2002). Understanding how the changing physical environments influence predator–prey dynamics is especially important in such systems and can have both economic and environmental benefits. For example, in wetlands and agricultural landscapes the control of medically and economically important insects by natural predators (e.g., mosquitoes, crop pests; Saha et al. 2007, Culler and Lamp 2009, Lundgren and Fergen 2014) could be enhanced by simultaneously reducing inter-patch distances through habitat creation, and by altering vegetation structure within patches through planting. For conservation, the creation/restoration of habitats with higher structural complexity (Alsfeld et al. 2009, Viol et al. 2009) as well as longer inter-patch distances should promote lower predation and competition pressures and thus promote higher biodiversity. The scale of such modifications will be dependent on the ecological neighborhoods of the predators and prey involved (Addicott et al. 1987), but overall our results suggest that the interactive effects of SHC and FHC should be considered to a much greater extent and that such consideration will enhance our understanding of many structurally complex ecosystems.

result in conclusions that would not be predicted had either variable been considered alone. For example, two different field enclosure studies looking at the effect of plant stem densities on the growth of Bluegills (Lepomis macrochirus) have shown either that fish grew better at an intermediate stem density, because there was enough refuge to keep prey abundances high over time but not enough to significantly inhibit prey capture (Crowder and Cooper 1982), or that there was no change in growth as the result of a threshold effect (Savino et al. 1992). However, as our damselfly consumption results show that the influence of SHC on predation may not always be so straightforward. We suggest that the conflicting results in these studies may be partially attributed to variation in the distances among vegetated patches within the enclosures. Although FHC was not considered in either of these studies, if it had been Crowder and Cooper (1982) may have found an intermediate stem density effect because their distances between patches were great enough not to counteract the refuge benefit of the higher stem density (i.e., the cost of increased prey activity at high SHC was low). For Savino et al. (1992), the distance between patches may have been shorter, increasing predator presence within patches and counteracting the refuge benefit of the higher stem density for certain prey types (i.e., the cost of increased prey activity at high SHC was elevated). Our results suggest that understanding how changes in SHC and FHC influence biodiversity, community structure, and ecosystem function over time requires us to acknowledge the complex interactive effects that a physically dynamic environment has on predator/prey interactions. Although the combined effects of SHC and FHC have the potential to modify interactions within biological communities in many complex ways, we think the strongest impacts will be on predator and prey foraging behaviors and overall predator–prey dynamics. These impacts of SHC and FHC on predator–prey dynamics will be most pronounced in landscapes where habitats show substantial spatial and structural heterogeneity. Such landscape features are not unique to pond environments, but occur commonly in marine, terrestrial, and freshwater ecosystems. The structure and distribution of habitats are rapidly changing due to anthropogenic influences ❖ www.esajournals.org

ACKNOWLEDGMENTS We want to thank Hugh Britten, Steve Chipps, Mark Dixon, and Jacob Kerby for input in design and analysis of this study. The GrEBE doctoral writing group members, Drew Davis, Laura Jackson, Erica Mize, and Gretchen Newberry, provided much appreciated comments that greatly improved this manuscript. We also want to thank Amber Furness, Tristan Soluk, and Ruth Wollman for their assistance in the construction and implementation of this experiment. This study would not have been possible without the facilities at the Illinois Dragonfly Research Center that were graciously made available to the authors by Tom Valet the Ecology Coordinator for the Forest Preserve District of Dupage Forest County. The primary author wants to especially thank Elizabeth Pitcher for her support throughout the project and her much appreciated technical edits on early drafts of this manuscript. This study was made possible by funding from the University of South Dakota Foundation: Raymond D. Dillion Memorial Travel Grant, and the University of South Dakota Foundation: Cable Research Assistantship.

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SUPPORTING INFORMATION Additional Supporting Information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/ ecs2.1598/full


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