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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information

Theoretical treatments of intraguild predation and its effects on behavioral interactions regard the phenomenon as a size-structured binary response wherein predation among competitors is completely successful or completely unsuccessful. However, intermediate outcomes occur when individuals escape intraguild (IG) interactions with non-lethal injuries. While the effects of wounds for prey include compromised mobility and increased predation risk, the consequences of similar injuries among top predators are not well understood, despite the implications for species interactions. Using an amphibian IG predator, Ambystoma opacum (Caudata: Ambystomatidae), we examined associations between non-lethal injuries and predator body size, foraging strategy, microhabitat selection, and intraspecific agonistic interactions. Wounds were common among IG predators, generally increasing in frequency throughout larval ontogeny. Non-lethal injuries were associated with differences in predator body size and behavior, with injured predators exhibiting smaller body sizes, increased use of benthic microhabitats, reduced agonistic displays, and increased risk of intraspecific aggression. While such effects were not ultimately associated with reduced foraging success, non-lethal injury could contribute to niche partitioning between injured and healthy predators via habitat selection, but injured predators likely continue to exert predatory pressure on IG and basal prey populations. Our results indicate that studies of top-down population regulation should incorporate injury-related modifications to both prey and predator behavior and size structure.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information

Intraguild predation (IGP), or the killing and eating of potential competitors (Polis et al. 1989), is a ubiquitous phenomenon in terrestrial and aquatic systems. Theoretical models of IGP predict ecological consequences including: (1) immediate benefits to intraguild (IG) predators through reduced competition, wider prey diversity, and increased growth and reproduction; (2) superior exploitative competitive ability of IG prey; (3) increased basal prey densities via reduced densities of IG prey; (4) coexistence of IG predator and prey at intermediate levels of production; and (5) multiple stable equilibria of predator and prey densities (Polis 1981; Polis et al. 1989; Holt & Polis 1992). Empirical evidence has supported these predictions (Eaton 1979; Diehl & Feissel 2001) and documented roles of IGP in weakening trophic cascades and ultimately altering ecosystem functions (Fincke & Denno 2004).

While the impacts of IGP are substantial, theoretical treatments typically model the interaction as an ‘all or nothing’ event, wherein predation and/or cannibalism are completely successful, completely unsuccessful, or not attempted (Polis et al. 1989; Polis & Holt 1992). Intermediate outcomes occur, however, when IG predators or prey survive attempted predation while sustaining injuries (Vermeij 1982; Harris 1989). Even among gape-limited, suction-feeding predators where ‘all or nothing’ responses are anticipated due to feeding kinematics, injuries do not necessarily result in mortality (Semlitsch & Reichling 1989). Under such conditions, IG predators and prey are vulnerable to damage inflicted by larger or smaller conspecifics, heterospecific IG predators, or IG prey (Hokit et al. 1996; Mott & Maret 2011).

Non-lethal injuries have been hypothesized as a mechanism of population regulation (Harris 1989), though largely via injury-related mortality. The ecological consequences of injuries within feeding guilds are largely unknown (but see Semlitsch & Reichling 1989), but the ultimate fate of injured predators should dictate the top-down effects of injury on trophic cascades and help determine whether injuries can ultimately be considered merely a ‘delayed form’ of IGP as it relates to its ecological impacts. If injured IG predators die, then strict density-dependent consequences for trophic cascades would include competitive release among surviving predators (Rudolf 2007), increased IG prey survival, and subsequent decreases in basal prey abundance (Polis et al. 1989; Polis & Strong 1996). However, if wounded predators do not ultimately die, top-down effects of injury on IG predator, IG prey, and basal prey populations are highly dependent on the ability of injured predators to survive and compete effectively with healthy conspecifics (i.e. trait-mediated effects; Abrams 1995). If injured predators alter their behavior or diet, such effects would likely impact IG prey or basal prey. Therefore, the survival and/or performance of injured top predators may dictate associated trophic cascades as being predominantly density-dependent in the case of predator mortality, predominantly trait-mediated if predators survive, or a combination of these mechanisms if injuries do not result in a single predictable outcome.

The ecological impacts of non-lethal injury are well documented for prey species (Smith 1995; Downes & Shine 2001; Segev et al. 2009) yet, our understanding of similar wounds among top predators is lacking. To characterize associations between non-lethal injury, foraging behavior, and species interactions of IG predators, we examined the influences of injury on body size, diet, microhabitat selection, and intraspecific agonistic behavior among larval salamanders (Ambystomatidae, Caudata). Larval ambystomatids are a feeding guild employed frequently as a model IG system (Wilbur 1972; Cortwright 1988) because larvae are gape-limited predators that compete for shared prey (Petranka 1998). Larvae of earlier breeding species are IG predators and therefore superior interference competitors but less successful at exploitative competition than smaller larvae of later breeding IG prey species (Walls 1996; Holt & Polis 1997; Diehl & Feissel 2000, 2001; Amarasekare 2008). Although smaller in size, later hatching species exhibit rates of aggression toward larger IG predators that can exceed rates of intraspecific aggression (Mott 2010; Mott & Maret 2011) and prey species can injure predators by biting off legs, gills, and tails (Semlitsch & Reichling 1989; Wildy et al. 2001). It is possible that such injuries may be a significant source of mortality for larval populations of Ambystoma, given that larval mortality in nature often exceeds 95% (Shoop 1974; Semlitsch 1987; Petranka 1989). However, previous mesocosm studies indicate that injured larvae can survive to metamorphosis (Semlitsch & Reichling 1989), and thus, we cannot predict whether the community impacts of predator injury can be attributed solely to density dependence associated with mortality or trait-mediated effects of surviving, yet potentially compromised predators.

To determine whether injury prevalence varied with trophic status, we monitored injuries among an IG predator, A. opacum, a sympatric IG predator/prey, A. tigrinum, and their shared IG prey, A. maculatum. We hypothesized that damage incurred during aggressive interactions would negatively impact wounded IG predators in any one or combination of the following ways: (1) injured IG predators exhibit smaller body sizes than uninjured conspecific; (2) injured IG predators are forced to inhabit pond microhabitats of lesser quality with respect to food availability; (3) injured IG predators alter their diet based on their ability to pursue and capture prey of varying mobility, body size, or microhabitat use; (4) injured IG predators reduce aggression toward conspecifics due to risks of reciprocal aggression; or (5) injured IG predators become increasingly targeted by conspecifics during agonistic interactions or increasingly unable to escape such attacks.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information

Injury Prevalence in Ambystoma

All statistical analyses were conducted using R, version 2.15 (R Core Team 2013). Non-lethal injury prevalence among all focal species was monitored throughout the larval period in 14 ephemeral ponds in the Shawnee National Forest (SNF), southern Illinois, from 2005 to 2008. Each month following hatching of A. opacum and until all focal species had metamorphosed, 30 larvae of each species were inspected for injuries to the front and rear limbs, gills, and tail and then released. We assigned individuals to injury categories of: (1) uninjured = no visible injuries; (2) tail injured = missing all or portions of the tail; (3) gill injured = missing one or multiple gill filaments; (4) limb/digit injured = missing digits, feet, or entire limbs; or (5) multiple injury = exhibiting two or more different injuries. Due to extreme interannual variation in dates of hatching and metamorphosis within species, often by several months, we were unable to utilize repeated measures analyses due to an abundance of missing values that, when omitted following listwise deletion, would reduce the total data set by over 50%. We therefore assessed seasonal changes in injury frequency (% larvae injured/pond) by species, month, and pond using ANOVA. We initially analyzed each year separately to account for yearly variation in hatching phenology; however, based on similar results for all years, we subsequently pooled data for all years. Significant pairwise differences by month and species were identified using Tukey's HSD Tests.

Correlations between Injury Prevalence, Body Size, and Behavior in A. opacum

The relationship between injury, larval body size (i.e. snout-vent length), and microhabitat association of A. opacum was assessed in three ponds total between 2006 and 2008 in SNF and the Touch of Nature Environmental Education Center (TONEC), Carbondale, Illinois. Ponds were selected based on the absence (1 pond) or extremely low density (2 ponds) of large, predatory macroinvertebrates that could cause injuries similar to those inflicted by salamander larvae. The average density among all three ponds was 0.13 predators/m2 as determined by ten sediment core samples per pond (Mott 2010; Mott & Sparling 2010), while observed densities of larval odonate and dytiscid predators commonly exceed 50/m2 (Benke & Benke 1975; Van Buskirk 1989; Pearman 1995). Between April and May, we examined larvae from four microhabitats within ephemeral ponds: (1) benthos = > 1 m from pond edge on or among the leaf litter at the pond bottom; (2) littoral = < 1 m from pond edge in or among leaf litter; (3) water column = > 1 m from pond edge, > 10 cm above pond benthos and > 10 cm below the pond surface; and (4) surface = > 1 m from pond edge, head at pond surface. Microhabitats were designated based on the different dominant prey types in these pond regions (C. L. Mott, unpubl. data), which were examined in a subsequent analysis. A minimum of 35 larval A. opacum were collected from each region in each pond, and body sizes were measured using ImageJ (Abramoff et al. 2004). Large ponds were selected so that sampling of one region of the pond would not disturb subsequent sampling in additional regions, and sampling was conducted after larvae had stratified in the water column at night (Anderson & Graham 1967; Branch & Altig 1981).

We assigned each larva to one of five injury categories: (1) no injury; (2) one minor injury (a single injury consisting of a missing gill, digit, limb, or < 10% tail loss); (3) two minor injuries; (4) three minor injuries; or (5) major injury (any combination of missing gills, digits, or limbs with > 20% tail loss). These categories differed slightly from those utilized for identifying aforementioned seasonal trends in larval injury because the former were a component of a previous study (Mott 2010), while the latter were developed specifically for this study. Injury categories were based on observed patterns and the assumption that tail injuries would most severely limit foraging abilities (Hassinger et al. 1970).

Although we collected data on injuries and body size from the same individuals, body sizes were determined ex situ via digital photographs. However, we could not assign both injury categories and body sizes simultaneously to individual larvae as intended due to difficulties in diagnosing which injuries were observed among which larvae from photographs due to low camera resolution. Larvae were also photographed in groups of 2–4 individuals, such that we could obtain the injury scores and body sizes within these small groups, but not for any single larva, thereby preventing us from stating whether smaller larvae in particular exhibited the most severe injuries. Therefore, we conducted separate one-way ANOVAs for the effect of microhabitat and pond on (1) body size and (2) average injury level, as such an approach pools data for each microhabitat among larvae and does not require matching size and injury data for each larva individually. Essentially, the first analyses determined whether larval injury categories decreased with size and the second whether larval injury categories are associated with microhabitat selection. Given that this analysis may be inaccurate due to our inability to directly link injury with body size, we also measured body sizes and diagnosed injuries for 162 larvae preserved for gut content analyses (see below). The effects of pond and injury category on body size were assessed for preserved specimens using ANOVA, with significant pairwise differences within each analysis identified using Tukey's HSD Tests.

To determine the impact of injuries on prey selection by IG predators, we examined gut contents from 162 larval A. opacum (< 5% of each population; Mott 2010); samples sizes for each injury category were uneven due to the rarity of some injury combinations (N for injury categories 1–5 = 28, 40, 51, 12, and 31, respectively). Larvae were euthanized using a 250 mg/l aqueous solution of benzocaine and preserved in 10% buffered formalin. Stomachs were excised and examined under 10–40 × magnification, and larvae and prey items were dried at 70°C for 24 h and weighed. Micro- (< 1 mm) and macroinvertebrate (> 1 mm) prey were enumerated and identified to order and family, respectively. To account for variation in prey capture based on predator size, we utilized predator body size as a covariate in our analysis. The influence of larval injury category on diet was analyzed using MANCOVA, with response variables of prey diversity, number of prey items, and prey mass, with random and fixed factors of pond and injury category, respectively. Prey diversity was the combined numbers of orders and families for micro- and macroinvertebrates, respectively.

We assigned prey to one of three mobility categories, hypothesizing that predators with severe tail injuries would be unable to capture highly mobile prey. Prey categories were as follows: (1) high mobility = dipteran larvae, corixids, gerrids, coleopterans, (2) medium mobility = ostracoda, cladocera, copepoda, hydrachnida, nematoda; (3) low mobility or immobile = amphibian eggs, rotifera, oligochaeta, mollusca. Proportions of dietary items from each category were calculated for A. opacum, and the effects of injury on dietary proportions of each category were examined via MANOVA with random and fixed factors of pond and injury category, respectively.

We also identified pond zones in which prey were likely captured by predators based on typical patterns of prey microhabitat use. Prey items were defined as: (1) benthic = rotifera, chironomidae, oligochaeta, nematoda, physidae; (2) water column = ostracoda, cladocera, copepoda, chaoboridae, coleopteran larvae; or (3) surface = culicidae, amphibian eggs, gerridae. To link predator injury with changes in microhabitat and associated prey choice, proportions of dietary items from each microhabitat were calculated for injured and uninjured A. opacum. Response variables of prey proportions from each microhabitat were quantified with respect to larval injury categories via MANOVA using random and fixed factors of pond and injury category, respectively.

To identify size-based foraging trade-offs associated with injury, we also categorized prey by size, with the hypothesis that injured predators consume large numbers of smaller prey that are easily captured. Dietary items were assigned to size categories of small (< 1 mm; ostracoda, cladocera, copepoda, nematode, rotifera) or large (> 1 mm; amphibian eggs, chaoboridae, chironomidae, coleopteran larvae, culicidae, gerridae, oligochaeta, physidae), with proportions of prey items from each size category recorded. The effects of injury category on dietary proportion of large prey size were assessed via ANOVA with random and fixed factors of pond and injury category, respectively.

Agonistic Behavior between Injured and Uninjured A. opacum

Ambystoma opacum consume conspecifics in addition to IG and basal prey (Petranka 1998); therefore, we utilized laboratory observations of agonistic behavior to determine how previous injury affects subsequent intraspecific interactions. Injured and uninjured A. opacum were collected from SNF and TONEC in May 2008 and transported to the animal care facilities at the Cooperative Wildlife Research Laboratory, Southern Illinois University Carbondale. Larvae were housed individually in 15 × 12 × 5 cm plastic containers filled with 600 mL of reconstituted water under a 12:12 L:D photoperiod. Ambient temperature ranged from 16 to 19°C, larvae were fed daily with the amount of Artemia spp. nauplii hatching from 0.015 g of eggs, and all individuals remained under laboratory conditions for at least 1 wk prior to behavioral observations.

Larval head width was measured using ImageJ (Abramoff et al. 2004), and larvae were assigned to conspecific pairs based on equal head width because size asymmetry can skew the results of behavioral observations (Mott & Maret 2011). Uninjured larvae were assigned to competitors consisting of either another uninjured larva or a naturally injured larva, the latter of which exhibited 2–3 minor injuries including missing gills, feet, or tail tips. After pairwise assignment, larvae were returned to individual containers and denied access to food for 24 h to standardize hunger levels.

Nocturnal behavioral observations were video-recorded in a circular arena (diameter = 19 cm, depth = 3.5 cm) using infrared lighting. For each larval pair, individuals were placed in separate plastic cylinders, acclimatized for 5 min, and released. For both larvae over the following 30 min, we calculated combined totals of the behaviors: MOVE TOWARD – one salamander moves toward in the direction of another such that continued movement would result in contact; LUNGE – one salamander rapidly and abruptly moves toward another but does not intersect with any part of the other individual's body; BITE – one salamander grabs another with the mouth (definitions from Walls & Jaeger 1987) and MUTUAL APPROACH – ‘move toward’ performed by both larvae simultaneously (Mott & Sparling 2009), all of which served as indicators of ‘individual aggression’. For both control (two uninjured larvae) and treatment (one uninjured and one injured larva) conditions, we conducted 25 behavioral trials, and each larva was utilized for a single trial. ‘Total aggression’ for uninjured:uninjured and uninjured:injured larval pairs were calculated as the summed values of ‘individual aggression’ for both larvae in a trial, and these values were square-root-transformed to satisfy assumptions of normality. We subsequently analyzed ‘total aggression’ exhibited by control vs. treatment trials using a t-test. To determine whether differences in aggression observed between control and treatments larval pairs were due to increased aggression directed specifically toward injured larvae in treatment trials, we also assessed differences in ‘individual aggression’ between injured and uninjured larvae strictly from treatment trials using a paired t-test.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information

Injury Prevalence in Ambystoma

We observed 2147, 227, and 485 larval Ambystoma opacum, A. tigrinum, and A. maculatum, respectively, over 66 pond-months of sampling, with injury prevalence ranging from 0 to 91% of individuals in ponds. Injury prevalence was influenced by month, pond, and species, but interaction terms were not significant (Table 1). Injuries increased through ontogeny in A. opacum, although slight decreases in injuries occurred near metamorphosis, and the primary species differences were between the peak and minimum levels of injury between A. opacum and A. maculatum (Fig. 1). Among all species and months combined, gill injuries accounted for the greatest percentage all of all larval injury categories (27.4%), followed by tail injuries (11.4%), multiple injuries (7.9%), and limb injuries (5.5%). A significant pond effect without significant interactive effects with species or month (Table 1) illustrates general differences in average injury levels among ponds, but with relatively similar temporal injury trends within each species among all ponds through time.

Table 1. ANOVA of injury through ontogeny for larval Ambystoma opacum, A. tigrinum, and A. maculatum based on month, pond, and species
Factordf F p
Month712.51< 0.001
Species216.31< 0.001
Pond125.410.002
Month × Species31.640.225
Month × Pond252.020.081
Species × Pond20.560.583
Month × Species × Pond511.330.289
image

Figure 1. Seasonal patterns of average injury prevalence (± SE) among larval Ambystoma opacum, A. tigrinum, and A. maculatum observed among 14 forested ephemeral ponds from 2006 to 2008 in the Shawnee National Forest, southern Illinois. Letters designate pairwise differences from Tukey's HSD Tests among all combinations of month and species. Letters for A. tigrinum and A. maculatum are positioned above and below the error bars, respectively.

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Correlations between Injury Prevalence, Body Size, and Behavior in A. opacum

Differences in intraguild predator body size and microhabitat selection were associated with increasing severity of non-lethal injuries. Among preserved specimens of A. opacum, increasing injury severity was associated with consistent decreases in body size across all injury categories (Table 2; Fig. 2), with each additional increase in injury category associated with a decrease in body size of 2.6–6.6%. The interaction of injury × pond was non-significant, indicating that, despite overall difference in body size among larvae from different ponds, the general trend of decreasing body size with increasing injury severity was preserved across all ponds.

Table 2. Results of ANOVA for body sizes of larval Ambystoma opacum based on pond and injury category among preserved specimens
Factordf F p
Injury112.55< 0.001
Pond259.57< 0.001
Injury × Pond26.550.402
Error156  
image

Figure 2. Snout-vent length (mm ± 1 SD) of larval Ambystoma opacum based on injury category for 162 individuals collected from three ephemeral ponds. Injury designations are: (1) no injury; (2) one minor injury (missing gill, digit, limb, or < 10% of the tail); (3) two minor injuries; (4) three minor injuries; or (5) major injury (any combination of missing gills, digits, or limbs, AND > 20% tail loss). Sample sizes for each category are shown within each bar, and letters indicate significant pairwise differences as indicated by Tukey's HSD tests.

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Based on larvae collected from ponds, body size of A. opacum increased across pond microhabitats in the order benthos < littoral < column < surface (Fig. 3a–c; Table 3A). Larvae in littoral and benthic habitats exhibited increased incidence of injury, and average injury categories of larvae from these microhabitats were 31.8% higher than larvae from surface and column microhabitats (Fig. 3d; Table 3B). Significant effects of pond and a significant interaction term between pond and microhabitat for the response of body size reflect a pattern wherein two of three ponds exhibited a significant association between microhabitat and size (Fig. 3a–b), while the third pond exhibited a similar, albeit non-significant pattern (Fig. 3c). The lack of a significant effect of pond or interaction for pond x microhabitat for the response of average injury severity indicates that associations between injury and microhabitat held across all ponds (Tables 3B).

image

Figure 3. (a–c) Snout-vent length (mm ± 1 SE) and (d) average injury score (from 1 = uninjured to 5 = major injury ± 1 SE) of larval Ambystoma opacum based on microhabitat for 490 individuals collected from three ponds in southern Illinois; snout-vent lengths are shown for each pond separately, while injury scores are collectively shown for all ponds. Pond microhabitats were defined as: (1) benthos = > 1 m from pond edge on or among the leaf litter at the pond bottom; (2) littoral = < 1 m from pond edge in or among leaf litter; (3) water column = > 1 m from pond edge, > 10 cm above pond benthos and > 10 cm below the pond surface; and (4) surface = > 1 m from pond edge, < 2 cm from pond surface. Sample sizes for each category are enclosed within bars, and letters indicate significant pairwise differences following Tukey's HSD Tests (within ponds for larval SVL, among all ponds for injury score). Response variables of body size and average injury score were examined using separate ANOVAs due to the inability to measure both size and injury severity from digital images at the level of individual larvae.

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Table 3. Results of ANOVA for (A) body size and (B) average injury category of larval Ambystoma opacum based on pond and pond microhabitat, with response variables examined using a separate analyses due to the inability to measure both size and injury severity from digital images at the level of individual larvae
ResponseFactordf F p
(A) Body sizeMicrohabitat153.15< 0.001
Pond2216.27< 0.001
Microhabitat × Pond115.88< 0.001
Error483  
(B) Injury categoryMicrohabitat124.84< 0.001
Pond20.680.409
Microhabitat × Pond12.550.111
Error483  

Increasing injury severity did not influence predator diet as measured by number, mass, or diversity of prey items captured when accounting for predator size and pond, and injuries were not associated with any differences in the size, microhabitat, and/or mobility of invertebrate prey consumed (Tables S1–S4).

Agonistic Behavior between Injured and Uninjured A. opacum

Larval injuries were associated with changes in both the intensity and direction of intraspecific aggression. Trials consisting solely of uninjured larvae were characterized by over 195% higher aggression than pairs with one injured larva (Fig. 4a; = −5.36, df = 35.42, p < 0.001). Furthermore, in injured:uninjured behavioral trials, aggression was highly asymmetric; injured larvae were commonly targeted by uninjured conspecifics, with the latter exhibiting 59% greater aggression (Fig. 4b; paired t-test = −2.52, df = 24, p = 0.018).

image

Figure 4. Average larval aggression among paired Ambystoma opacum (combined counts for both individuals of the behaviors move toward, lunge, bite, and mutual approach ± 1 SE) between (a) control (N = 25) and treatment (N = 25) trials and (b) uninjured (N = 25) and injured (N = 25) larvae from only the treatment trials.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information

This study indicates that non-lethal injuries are common within IG predator populations, and such wounds, while not ultimately resulting in decreased foraging success, were associated with differences in body size, microhabitat selection, and intraspecific interactions. While the effects of non-lethal injury on prey populations are well documented (Morin 1985; Nunes et al. 2010), to our knowledge, this study is the first to quantify effects of similar injuries on top predators. Injuries in this study, which were widespread among three species of salamanders, were associated with decreased body sizes, shifts to benthic microhabitats, decreased performance of agonistic behavior, but increased risk of being the victim of conspecific aggression. Consequently, theoretical treatments of IGP that only consider cases where it leads to immediate death underestimate the importance of these complex interactions. The seasonal increases in the incidence of injury in this system suggest that predators survive with wounds, and thus density-dependent effects of injury, such as competitive release among IG predators, may be low while trait-mediated effects of predator performance may be prevalent and influence trophic cascades.

Injuries should be least prevalent among the highest trophic levels, as the risks of reciprocal aggression are negatively correlated with trophic status and/or body size (sensu Polis et al. 1989). Surprisingly, IG predators in this study (A. opacum) exhibited maximum injury frequencies higher than their IG prey (A. maculatum), and empirical evidence points to temporal patterns in resource abundance as a potential cause of this counterintuitive pattern. Intraspecific aggression among A. opacum is more intense than in sympatric species, yet rarely results in cannibalism (Mott & Maret 2011), leaving non-lethal injury as an alternative outcome. Increased intraspecific aggression has been attributed to the prolonged duration in which A. opacum occurs in ponds at high densities prior to the arrival of later breeding prey species, as well as low invertebrate prey densities that cause intense competition (Walls 1998; Mott 2010). Conversely, reduced injury among IG prey may result from shorter larval periods, given that our results indicate that injuries accumulate in populations over time, and A. tigrinum and A. maculatum in our study completed development in nearly half the time of A. opacum. Alternatively, due to differences among species in their ability to cope with injury, reduced instances of injury among IG prey may simply reflect efficient predation by A. opacum that does not frequently produce wounded survivors.

While injuries may not appear to result in direct mortality among IG predators, the association between health and body size is of considerable consequence, for predation is highly dependent on body size in aquatic communities (Wellborn et al. 1996; Brose et al. 2006). Reduced body size of injured predators increases risks of cannibalism by larger, uninjured conspecifics and predation by macroinvertebrates. Smaller, injured predators also experience increased risks of reciprocal aggression when attempting to capture IG prey (sensu Brunkow & Collins 1998), and increased desiccation risk may occur for predators if they cannot metamorphose before the pond dries (Werner 1986; Wilbur 1987). Injuries incurred during non-reproductive, larval life stages in this study may therefore have fitness consequences for aquatic predators similar to those of previously studied adult organisms lacking biphasic life cycles (Harris 1989; Bernardo & Agosta 2005).

Although predator foraging success was not associated with increasing injury severity, observed effects on microhabitat selection suggest a shift in foraging strategy in association with non-lethal injuries. Intraguild predators with no or few injuries foraged predominantly in open water microhabitats, while IG predators exhibiting the most severe injuries foraged predominantly in benthic microhabitats. Predators in each microhabitat were equally successful with respect to prey intake, and therefore, it does not appear that individuals are necessarily relegated to ‘suboptimal’ microhabitats following non-lethal injuries. Although the results of field and mesocosm studies of larval salamander competition have varied tremendously, some studies have indicated that food may not be a limiting resource (e.g. Ireland 1989). Our results tend to provide support to this hypothesis, given that larvae of all sizes, injury statuses, and microhabitats exhibited equivalent foraging success, despite the known influences of one of these factors (i.e. body size) on the intensity of competitive interactions and foraging success (Wilbur 1972; Maret & Collins 1994; Brunkow & Collins 1998).

Based on patterns of larval microhabitat selection, non-lethal injury may facilitate niche partitioning among injured and uninjured IG predators in terms of spatial organization even if predators are not partitioning based on dietary preferences. The selection of benthic microhabitats by injured predators may represent an attempt to minimize the future likelihood of encountering aggressive conspecifics, given that the results of laboratory trials indicate injured larvae would be the preferred targets of conspecific aggression. Benthic microhabitats often provide cover that, while typically utilized by IG prey species in ephemeral ponds (Nyman 1991; Brodman & Jaskula 2002), would also provide camouflage for IG predators seeking to avoid detection. The availability of ample cover and food resources could explain why rates of injury among IG predators can remain so high throughout larval ontogeny, while seemingly not resulting in extensive mortality wherein the prevalence of injury would drop over time.

Harris' (1989) model of population regulation via injury predicts that growth of uninjured individuals must exceed that of injured individuals, which receives support in that the smallest larvae exhibited severe injuries. In addition, the greatest potential to regulate population size under this model is achieved when injuries are predominantly intraspecific as opposed to resulting from heterospecific predator–prey interactions. The prevalence of injuries among our IG predators prior to the emergence of IG prey indicates intraspecific aggression may be a potent source of non-lethal injury in this system, and that injury may ultimately constitute an important influence on spatial dynamics and size structure of predator populations. Furthermore, this model assumes that injured individuals avoid conspecifics until they are repaired, which may occur given our observations of altered microhabitat selection following injury. According to Harris (1989), injured individuals are also predicted to be less likely to inflict injuries upon other conspecifics; this was clearly demonstrated by our laboratory observations.

While this model was explicitly derived in the context of a reproducing active population, we have provided evidence that many of the key tenets are supported for non-reproductive larval amphibian populations, supporting hypotheses that non-lethal injury can direct population dynamics in pre-reproductive life stages. In addition, we suggest that future theoretical treatments of population regulation through non-lethal injury should incorporate two key aspects of foraging ecology observed in the present study. The first, changes in intra- and interspecific contact rates as a result of microhabitat shifts, will ultimately affect rates of cannibalism and heterospecific predation, as well as subsequent changes in community size structure, species composition, and niche partitioning. Microhabitat partitioning even in small, ephemeral aquatic habitats is common (Wellborn et al. 1996; Van Buskirk 2003) yet, investigations of species interactions that alter microhabitat selection and resultant trophic cascades are generally lacking. The second key addition is the recognition that both predator and prey behavior and fitness can be altered by non-lethal injury; both the Harris (1989) model and numerous empirical studies have examined behavioral changes among prey species, but as supported by the present study, predator behavior can be equally modified by non-lethal injury.

Associations between body size, behavior, and non-lethal injuries observed in this study indicate that the intensity, size structure, and function of IG interactions are highly dependent upon predator injury and associated microhabitat selection. Upon being injured, IG predators assume many of the traits shared by IG prey, including microhabitat preference and vulnerability to predation. As such, the functional roles of IG predators are largely dependent upon severity of non-lethal injuries. However, given that our experiments were not designed to test priority effects, it is unclear whether changes in habitat selection are preceded by injuries or whether initial habitat selection influences an individual's likelihood for subsequent injury. Similarly, we lack direct evidence that small body size leads to individuals becoming injured, when it is equally likely that individuals, once injured, may simply grow slower. Future studies that examine the mechanistic basis of patterns in injury, size, and habitat selection in wild populations will be beneficial in clarifying such relationships. When compared to existing theoretical treatments on non-lethal injury, the relationships associated with injury in this study indicate that this phenomenon may play a central role in population dynamics in size-structured communities.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information

We thank S.A. Albert, C.H. Haas, B.K. Willey, and J.M. Uzzardo for assistance in the field and T.A. Anderson, S.D. Martin, and H.H Whiteman for their comments on a previous version of the manuscript. All components of this research were performed in accordance with Southern Illinois University animal care guidelines (SIUC IACUC #05-036 and #05-037) and Illinois Scientific Collecting Permit No. A08.4048. Permission for this research was granted by the United States Forest Service, Illinois Department of Natural Resources, and Touch of Nature Environmental Center, and funding was provided by a Delyte and Dorothy Morris Doctoral Fellowship awarded to Cy L. Mott. The authors declare that they have no conflict of interest.

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  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
  9. Supporting Information
FilenameFormatSizeDescription
eth12178-sup-0001-TableS1-S4.docxWord document20K

Table S1. Results from MANCOVA and subsequent ANCOVAs of prey number, mass, and diversity in larval Ambystoma opacum based on pond and injury class of larvae and larval body size as a covariate.

Table S2. Results from MANOVA and subsequent ANOVAs of prey of fast, intermediate, and slow mobility classes as dietary components of larval Ambystoma opacum based on pond and injury class of larvae.

Table S3. Results from MANOVA and subsequent ANOVAs of prey of benthic, water column, and surface microhabitats as dietary components of larval Ambystoma opacum based on pond and injury class of larvae.

Table S4. Results of ANOVA for prevalence of large prey taxa in the diets of larval Ambystoma opacum based on pond and injury level among preserved specimens.

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