Oecologia (2015) 179:117–127 DOI 10.1007/s00442-015-3324-4
POPULATION ECOLOGY - ORIGINAL RESEARCH
Reciprocal transplant reveals trade‑off of resource quality and predation risk in the field Clifton B. Ruehl1,2 · Joel C. Trexler1
Received: 13 January 2015 / Accepted: 15 April 2015 / Published online: 28 April 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Balancing trade-offs between avoiding predators and acquiring food enables animals to maximize fitness. Quantifying their relative contribution to vital rates in nature is challenging because predator abundance and nutrient enrichment are often confounded. We employed a reciprocal transplant study design to separate these confounded effects on growth and reproduction of snails at wetland sites along a gradient of predator threats and phosphorus (P) enrichment associated with a canal. We held snails in mesh bags that allowed the passage of waterborne predator cues and fed them local or transplanted periphyton. Molluscivores were more abundant near the canal, and snails tethered near the canal suffered 33 % greater mortality than those tethered far from it (far sites). The greatest difference in snail growth rates was at the far sites where growth on far periphyton was 48 % slower than on P-enriched (near canal) periphyton. Close proximity to the canal reduced growth on near periphyton by 21 % compared to growth on the same periphyton far from the canal; there was no difference in growth rate on either periphyton type when snails were raised near the canal. Snails laid 81 % more egg masses at far sites than at near sites, regardless of periphyton origin. Top–down and bottom–up processes were elevated near the canal, and their effects canceled on growth, but not reproduction. Phenotypic
Communicated by Roland A. Brandl. * Clifton B. Ruehl [email protected] 1
Department of Biological Sciences, Florida International University, 3000 NE 151st Street, North Miami, FL, USA
2
Present Address: Department of Biology, Columbus State University, Columbus, GA 31907, USA
trade-offs such as these may explain why some taxa show little response to nutrient enrichment, compared to others, or that the effects of nutrient enrichment may be context dependent. Keywords Nonlethal · Predator–prey · Phosphorus enrichment · Pulmonate snails · Everglades
Introduction Animals face trade-offs between the need to acquire food and the need to avoid predators in order to survive, grow, and reproduce (Abrams 1984). Life history theory predicts that natural selection should favor individuals which balance this growth versus predation risk trade-off in ways that optimize individual growth and reproduction to maximize fitness (Sih 1980; Gilliam and Fraser 1987). Food quality and threats of predation alter the conditions of the trade-off by jointly influencing individual prey growth and reproduction. Nutrient enrichment lowers carbon:phosphorus (C:P) ratios and improves food quality by altering composition in favor of more edible groups (Sterner and Elser 2002; Gérard et al. 2008; Trexler et al. 2015). Higher food quality provides consumers with more resources to allocate toward competing life functions, such as growth and reproduction. In contrast, threats of predation typically decrease energy intake because prey move to refuges and forage less, resulting in slower growth and less reproduction (Relyea 2001; Benard and Fordyce 2003; Turner 2004; Hoverman et al. 2005; Ruehl and Trexler 2013). Threats of predation also stimulate allocation of resources toward producing defensive structures that alter the trade-off by increasing the chances of survival, but further limit energy available for growth and reproduction, potentially slowing prey
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population growth (Brown and Kotler 2004; Peckarsky et al. 2008; Brönmark et al. 2012; Ruehl and Trexler 2013). High-quality food in the presence of predators increases the nonlethal effects of predators on prey through opportunity costs to scared prey that miss out on the potential growth enjoyed by individuals without the threat of predation (Turner 2004; Werner and Peacor 2006; Ruehl and Trexler 2013). Therefore, nonlethal threats of predation may cancel the positive effects of high-quality food on the vital rates and population growth of prey species. Understanding how nutrient enrichment, in particular P enrichment in freshwater ecosystems, modifies species interactions like predation is critical for quantifying the impact that human activities, such as fertilizer runoff, have on natural populations and communities. Much of the literature testing the effects of nutrient enrichment on the nonlethal interaction strength between predators and prey has been conducted in laboratory and outdoor mesocosms that enable the easy separation of nutrient enrichment effects from nonlethal predator effects (Werner and Peacor 2003, 2006; Preisser et al. 2005; Ruehl and Trexler 2013). Tests of the conclusions from these controlled experiments in natural settings are needed because the threat of predation can vary over space and time (Turner and Montgomery 2003), suggesting that laboratory and mesocosm studies may overestimate the strength of nonlethal effects of predators. However, determining the relative importance of the nonlethal effects of predators and the effects of nutrient enrichment on prey in nature is difficult because the effects of predators and nutrient enrichment are often confounded. For example, theory and experiments indicate that nutrient enrichment drives strong bottom–up effects that support strong top–down effects (Rosenzweig 1973; Oksanen et al. 1981; Wootton and Power 1993; Forrester et al. 1999; Moran and Scheidler 2002; Cross et al. 2006; Peckarsky et al. 2013). Similarly, isolating the nonlethal effect of predators from food quality in nature is difficult because slow individual prey growth and diminished reproductive rates could result from low food quality rather than the nonlethal effects of predators and obscure the relative importance of each on prey populations (Creel and Christianson 2008). Therefore, study design is a central challenge for tests of food quality and the nonlethal effects of predators in nature. We propose the use of a reciprocal transplant study design, similar to that used by evolutionary ecologists to study gene-by-environment interactions (Clausen et al. 1940; Kawecki and Ebert 2004; Hereford 2009), as one solution for isolating the confounded effects of food quality and predator threats on prey populations in field settings. However, unlike the traditional reciprocal transplant study design which places a focal organism in both environments, we propose moving either the predator or the resource to
13
Oecologia (2015) 179:117–127
experimentally isolate one from the other. We illustrate this concept by the reciprocal transplant of a food source (periphyton). Prior research indicates that the food source, periphyton, varied in quality along the gradient (Gaiser et al. 2006) and that its cohesive mat structure enabled transporting periphyton between sites that facilitated the separation of nutrient enrichment effects from nonlethal effects of predators. In the study reported here, we used Planorbella duryi (Seminole ramshorn) as the focal prey species. Planorbid snails are good candidates for exploring the mechanisms behind the complex effects of overlapping environmental drivers such as predation and resource quality. Snails typically do not move far during their life (Dillon 2000) and exhibit life history plasticity that is easily quantified in response to threats of predation and nutrients (Turner 2004; Hoverman et al. 2005). A prior mesocosm study in the Everglades that separated nonlethal effects from nutrient enrichment effects found that nonlethal crayfish (Procambarus fallax) limited per-capita F1 P. duryi standing stock by slowing individual growth, while nutrient enrichment mitigated these effects by stimulating growth of individuals and their offspring (Ruehl and Trexler 2013). Based on these mesocosm results, we predicted that snails maintained near the canal (near sites) and fed local periphyton mat would grow and produce egg masses at similar rates to those raised far from the canal (far sites) and fed local periphyton because the elevated predator threats and elevated nutrients near the canal would cancel each other out (Fig. 1a). Further, we predicted that moving the periphyton mat between near and far sites would reveal that growth and egg-mass production would be highest for snails raised far from the canal (fewer threats of predation) on the periphyton mat from near the canal (high-quality food). Similarly, growth and egg-mass production would be lowest for snails raised near the canal (greater threats of predation) and fed periphyton mat that originated far from the canal (low-quality food).
Methods Study system The Everglades is a large oligotrophic subtropical wetland with high annual periphyton production (Ewe et al. 2006). Everglades’ periphyton forms cohesive floating mats, benthic mats, and epiphytic mats depending on the mineral content of the substrate, elevation in the water column, and hydroperiod (Browder et al. 1994; Vymazal 1995; Gaiser et al. 2011). Thick floating periphyton mats dominate sloughs and long-hydroperiod marshes where this study was conducted (Gaiser et al. 2006, 2011). Canals, dredged
Oecologia (2015) 179:117–127
in the Florida Everglades to store water and mitigate flooding, increase the P content of nearby periphyton mats by leaching P-rich water that runs off agricultural fields (Gaiser et al. 2006). Canals provide an extensive network of deepwater refuges for large predatory fishes (including molluscivorous fishes) during drying events and an additional habitat for small and large consumers throughout the year, resulting in greater numbers of consumers in canals and adjacent marshes compared to areas distant from canals (Rehage and Trexler 2006; Parkos and Trexler 2014). Procambarus fallax is the numerically dominant crayfish in the Everglades and serves as the most important mollusciovore in the system based on tethering studies and long-term sampling (Dorn and Trexler 2007; Ruehl 2010). Interestingly, many primary consumers and omnivores of the Everglades exhibit mixed responses to nutrient enrichment from canals (Turner et al. 1999; McCormick et al. 2004; Gaiser et al. 2005). These mixed responses suggest that there may be interplay between top–down and bottom–up processes that impact population growth of these consumer groups.
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Some canal and marsh sediments in South Florida have elevated metal concentrations from agricultural runoff, including copper, which can have acute effects on gastropods (Hoang et al. 2009). However, we chose a study area (25°45′55.70″N, 80°45′35.50″W; Fig. 1b) along a canal (L-29) and marsh (Water Conservation Area 3A) that has low levels of these contaminants and is distant from sites directly receiving runoff (Rand and Schuler 2009; sites CA3-15, S355A, S355B).
We established two 3-km transects separated by 6 km that ran perpendicular to the canal into the marsh. Along each transect, we chose two sites near the canal ( 0.05, in all cases). SIMPER analysis revealed that the average dissimilarity between periphyton that originated near the canal compared to that which originated far from the canal was 31 % regardless of where it was placed. Desmids accounted for 39.7 % of this dissimilarity, diatoms for 29.2 %, and coccoid bluegreens for 25.5 %. NMDS plots reflected the PerMANOVA (add-on package for PRIMER) and SIMPER results that periphyton composition primarily depended on where the periphyton originated (Fig. 2). At the end of the experiment, periphyton from far sites that was placed near the canal was more similar to periphyton at far sites than to periphyton from near sites. Similarly, periphyton from near sites that was placed far from the canal more closely matched periphyton from near the canal compared to composition far from the canal. Diatoms in particular displayed a higher relative abundance near the canal than far from it, while filamentous cyanobacteria (bluegreens) had a higher relative abundance far from the canal. Periphyton edibility (diatoms + nonfilamentous greens) was 21 % greater near the canal than far from the canal regardless of origin (site: F1,37 = 5.71, P = 0.02). However, periphyton origin also affected edibility. Periphyton that originated near the canal had 37 % more diatoms and non-filamentous algae than periphyton that originated far from the canal (origin: F1,37 = 18.01, P
POPULATION ECOLOGY - ORIGINAL RESEARCH
Reciprocal transplant reveals trade‑off of resource quality and predation risk in the field Clifton B. Ruehl1,2 · Joel C. Trexler1
Received: 13 January 2015 / Accepted: 15 April 2015 / Published online: 28 April 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Balancing trade-offs between avoiding predators and acquiring food enables animals to maximize fitness. Quantifying their relative contribution to vital rates in nature is challenging because predator abundance and nutrient enrichment are often confounded. We employed a reciprocal transplant study design to separate these confounded effects on growth and reproduction of snails at wetland sites along a gradient of predator threats and phosphorus (P) enrichment associated with a canal. We held snails in mesh bags that allowed the passage of waterborne predator cues and fed them local or transplanted periphyton. Molluscivores were more abundant near the canal, and snails tethered near the canal suffered 33 % greater mortality than those tethered far from it (far sites). The greatest difference in snail growth rates was at the far sites where growth on far periphyton was 48 % slower than on P-enriched (near canal) periphyton. Close proximity to the canal reduced growth on near periphyton by 21 % compared to growth on the same periphyton far from the canal; there was no difference in growth rate on either periphyton type when snails were raised near the canal. Snails laid 81 % more egg masses at far sites than at near sites, regardless of periphyton origin. Top–down and bottom–up processes were elevated near the canal, and their effects canceled on growth, but not reproduction. Phenotypic
Communicated by Roland A. Brandl. * Clifton B. Ruehl [email protected] 1
Department of Biological Sciences, Florida International University, 3000 NE 151st Street, North Miami, FL, USA
2
Present Address: Department of Biology, Columbus State University, Columbus, GA 31907, USA
trade-offs such as these may explain why some taxa show little response to nutrient enrichment, compared to others, or that the effects of nutrient enrichment may be context dependent. Keywords Nonlethal · Predator–prey · Phosphorus enrichment · Pulmonate snails · Everglades
Introduction Animals face trade-offs between the need to acquire food and the need to avoid predators in order to survive, grow, and reproduce (Abrams 1984). Life history theory predicts that natural selection should favor individuals which balance this growth versus predation risk trade-off in ways that optimize individual growth and reproduction to maximize fitness (Sih 1980; Gilliam and Fraser 1987). Food quality and threats of predation alter the conditions of the trade-off by jointly influencing individual prey growth and reproduction. Nutrient enrichment lowers carbon:phosphorus (C:P) ratios and improves food quality by altering composition in favor of more edible groups (Sterner and Elser 2002; Gérard et al. 2008; Trexler et al. 2015). Higher food quality provides consumers with more resources to allocate toward competing life functions, such as growth and reproduction. In contrast, threats of predation typically decrease energy intake because prey move to refuges and forage less, resulting in slower growth and less reproduction (Relyea 2001; Benard and Fordyce 2003; Turner 2004; Hoverman et al. 2005; Ruehl and Trexler 2013). Threats of predation also stimulate allocation of resources toward producing defensive structures that alter the trade-off by increasing the chances of survival, but further limit energy available for growth and reproduction, potentially slowing prey
13
118
population growth (Brown and Kotler 2004; Peckarsky et al. 2008; Brönmark et al. 2012; Ruehl and Trexler 2013). High-quality food in the presence of predators increases the nonlethal effects of predators on prey through opportunity costs to scared prey that miss out on the potential growth enjoyed by individuals without the threat of predation (Turner 2004; Werner and Peacor 2006; Ruehl and Trexler 2013). Therefore, nonlethal threats of predation may cancel the positive effects of high-quality food on the vital rates and population growth of prey species. Understanding how nutrient enrichment, in particular P enrichment in freshwater ecosystems, modifies species interactions like predation is critical for quantifying the impact that human activities, such as fertilizer runoff, have on natural populations and communities. Much of the literature testing the effects of nutrient enrichment on the nonlethal interaction strength between predators and prey has been conducted in laboratory and outdoor mesocosms that enable the easy separation of nutrient enrichment effects from nonlethal predator effects (Werner and Peacor 2003, 2006; Preisser et al. 2005; Ruehl and Trexler 2013). Tests of the conclusions from these controlled experiments in natural settings are needed because the threat of predation can vary over space and time (Turner and Montgomery 2003), suggesting that laboratory and mesocosm studies may overestimate the strength of nonlethal effects of predators. However, determining the relative importance of the nonlethal effects of predators and the effects of nutrient enrichment on prey in nature is difficult because the effects of predators and nutrient enrichment are often confounded. For example, theory and experiments indicate that nutrient enrichment drives strong bottom–up effects that support strong top–down effects (Rosenzweig 1973; Oksanen et al. 1981; Wootton and Power 1993; Forrester et al. 1999; Moran and Scheidler 2002; Cross et al. 2006; Peckarsky et al. 2013). Similarly, isolating the nonlethal effect of predators from food quality in nature is difficult because slow individual prey growth and diminished reproductive rates could result from low food quality rather than the nonlethal effects of predators and obscure the relative importance of each on prey populations (Creel and Christianson 2008). Therefore, study design is a central challenge for tests of food quality and the nonlethal effects of predators in nature. We propose the use of a reciprocal transplant study design, similar to that used by evolutionary ecologists to study gene-by-environment interactions (Clausen et al. 1940; Kawecki and Ebert 2004; Hereford 2009), as one solution for isolating the confounded effects of food quality and predator threats on prey populations in field settings. However, unlike the traditional reciprocal transplant study design which places a focal organism in both environments, we propose moving either the predator or the resource to
13
Oecologia (2015) 179:117–127
experimentally isolate one from the other. We illustrate this concept by the reciprocal transplant of a food source (periphyton). Prior research indicates that the food source, periphyton, varied in quality along the gradient (Gaiser et al. 2006) and that its cohesive mat structure enabled transporting periphyton between sites that facilitated the separation of nutrient enrichment effects from nonlethal effects of predators. In the study reported here, we used Planorbella duryi (Seminole ramshorn) as the focal prey species. Planorbid snails are good candidates for exploring the mechanisms behind the complex effects of overlapping environmental drivers such as predation and resource quality. Snails typically do not move far during their life (Dillon 2000) and exhibit life history plasticity that is easily quantified in response to threats of predation and nutrients (Turner 2004; Hoverman et al. 2005). A prior mesocosm study in the Everglades that separated nonlethal effects from nutrient enrichment effects found that nonlethal crayfish (Procambarus fallax) limited per-capita F1 P. duryi standing stock by slowing individual growth, while nutrient enrichment mitigated these effects by stimulating growth of individuals and their offspring (Ruehl and Trexler 2013). Based on these mesocosm results, we predicted that snails maintained near the canal (near sites) and fed local periphyton mat would grow and produce egg masses at similar rates to those raised far from the canal (far sites) and fed local periphyton because the elevated predator threats and elevated nutrients near the canal would cancel each other out (Fig. 1a). Further, we predicted that moving the periphyton mat between near and far sites would reveal that growth and egg-mass production would be highest for snails raised far from the canal (fewer threats of predation) on the periphyton mat from near the canal (high-quality food). Similarly, growth and egg-mass production would be lowest for snails raised near the canal (greater threats of predation) and fed periphyton mat that originated far from the canal (low-quality food).
Methods Study system The Everglades is a large oligotrophic subtropical wetland with high annual periphyton production (Ewe et al. 2006). Everglades’ periphyton forms cohesive floating mats, benthic mats, and epiphytic mats depending on the mineral content of the substrate, elevation in the water column, and hydroperiod (Browder et al. 1994; Vymazal 1995; Gaiser et al. 2011). Thick floating periphyton mats dominate sloughs and long-hydroperiod marshes where this study was conducted (Gaiser et al. 2006, 2011). Canals, dredged
Oecologia (2015) 179:117–127
in the Florida Everglades to store water and mitigate flooding, increase the P content of nearby periphyton mats by leaching P-rich water that runs off agricultural fields (Gaiser et al. 2006). Canals provide an extensive network of deepwater refuges for large predatory fishes (including molluscivorous fishes) during drying events and an additional habitat for small and large consumers throughout the year, resulting in greater numbers of consumers in canals and adjacent marshes compared to areas distant from canals (Rehage and Trexler 2006; Parkos and Trexler 2014). Procambarus fallax is the numerically dominant crayfish in the Everglades and serves as the most important mollusciovore in the system based on tethering studies and long-term sampling (Dorn and Trexler 2007; Ruehl 2010). Interestingly, many primary consumers and omnivores of the Everglades exhibit mixed responses to nutrient enrichment from canals (Turner et al. 1999; McCormick et al. 2004; Gaiser et al. 2005). These mixed responses suggest that there may be interplay between top–down and bottom–up processes that impact population growth of these consumer groups.
119
Some canal and marsh sediments in South Florida have elevated metal concentrations from agricultural runoff, including copper, which can have acute effects on gastropods (Hoang et al. 2009). However, we chose a study area (25°45′55.70″N, 80°45′35.50″W; Fig. 1b) along a canal (L-29) and marsh (Water Conservation Area 3A) that has low levels of these contaminants and is distant from sites directly receiving runoff (Rand and Schuler 2009; sites CA3-15, S355A, S355B).
We established two 3-km transects separated by 6 km that ran perpendicular to the canal into the marsh. Along each transect, we chose two sites near the canal ( 0.05, in all cases). SIMPER analysis revealed that the average dissimilarity between periphyton that originated near the canal compared to that which originated far from the canal was 31 % regardless of where it was placed. Desmids accounted for 39.7 % of this dissimilarity, diatoms for 29.2 %, and coccoid bluegreens for 25.5 %. NMDS plots reflected the PerMANOVA (add-on package for PRIMER) and SIMPER results that periphyton composition primarily depended on where the periphyton originated (Fig. 2). At the end of the experiment, periphyton from far sites that was placed near the canal was more similar to periphyton at far sites than to periphyton from near sites. Similarly, periphyton from near sites that was placed far from the canal more closely matched periphyton from near the canal compared to composition far from the canal. Diatoms in particular displayed a higher relative abundance near the canal than far from it, while filamentous cyanobacteria (bluegreens) had a higher relative abundance far from the canal. Periphyton edibility (diatoms + nonfilamentous greens) was 21 % greater near the canal than far from the canal regardless of origin (site: F1,37 = 5.71, P = 0.02). However, periphyton origin also affected edibility. Periphyton that originated near the canal had 37 % more diatoms and non-filamentous algae than periphyton that originated far from the canal (origin: F1,37 = 18.01, P
