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Fear of predation alters soil carbon dioxide flux and nitrogen content Michael I. Sitvarin and Ann L. Rypstra Biol. Lett. 2014 10, 20140366, published 25 June 2014

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Community ecology

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Fear of predation alters soil carbon dioxide flux and nitrogen content Michael I. Sitvarin1 and Ann L. Rypstra2 1 2

Research Cite this article: Sitvarin MI, Rypstra AL. 2014 Fear of predation alters soil carbon dioxide flux and nitrogen content. Biol. Lett. 10: 20140366. http://dx.doi.org/10.1098/rsbl.2014.0366

Received: 7 May 2014 Accepted: 30 May 2014

Department of Biology, Miami University, Oxford, OH 45056, USA Department of Biology, Miami University, Hamilton, OH 45011, USA Predators are known to have both consumptive and non-consumptive effects (NCEs) on their prey that can cascade to affect lower trophic levels. Non-consumptive interactions often drive these effects, though the majority of studies have been conducted in aquatic- or herbivory-based systems. Here, we use a laboratory study to examine how linkages between an aboveground predator and a detritivore influence below-ground properties. We demonstrate that predators can depress soil metabolism (i.e. CO2 flux) and soil nutrient content via both consumptive and non-consumptive interactions with detritivores, and that the strength of isolated NCEs is comparable to changes resulting from predation. Changes in detritivore abundance and activity in response to predators and the fear of predation likely mediate interactions with the soil microbe community. Our results underscore the need to explore these mechanisms at large scales, considering the disproportionate extinction risk faced by predators and the importance of soils in the global carbon cycle.

Subject Areas: ecology Keywords: predation, non-consumptive effects, detrital system

Author for correspondence: Michael I. Sitvarin e-mail: [email protected]

Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2014.0366 or via http://rsbl.royalsocietypublishing.org.

1. Introduction Predators can affect prey populations directly by consuming individuals and indirectly by causing changes in prey traits (e.g. behaviour) as prey exhibit a fear response to the risk of predation [1]. These interactions between predators and prey have been termed consumptive and non-consumptive effects (NCEs), respectively. Surprisingly, NCEs often have an equal or greater magnitude than consumptive effects (CEs) on both prey and prey resources [2], and the importance of NCEs has been widely demonstrated [3]. The vast majority of research into predator effects on prey and their resources has focused on the ‘green pathway’ that links predators to plants via herbivores. By contrast, the ‘brown pathway’ linking predators to detrital pools via detritivores has received considerably less attention [1], despite the applicability of ‘green’ theory to ‘brown’ systems [4] and the importance of soils in the global carbon cycle [5]. Although predation studies in detrital systems are becoming more common, most experiments manipulate only predator presence [6–8], thus failing to understand the contribution of NCEs to observed predator effects. The few studies that have investigated the role of NCEs in detrital systems were either aquatic or focused on by-products of predator–herbivore interactions [9–12]. There is clearly a need to explore NCEs in terrestrial detrital systems to understand the degree to which control of soil properties can be attributed to the effects of predators on detritivores. This gap in our knowledge is particularly relevant considering that predators may be more strongly linked to detritivores than to herbivores [13]. We examined the role of CEs and NCEs in a detrital system using the predatory wolf spider Pardosa milvina and the detritivorous collembolan Sinella curviseta. Collembola are frequently consumed by wolf spiders, and can alter soil carbon and nutrient dynamics [14,15]. Specifically, collembolans can increase CO2 flux [14,16,17] and soil nitrogen [14,17,18], so we predicted that interactions between predators and detritivores

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would cascade to dampen these effects and that NCEs would be comparable to CEs.

2

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2. Material and methods

3. Results (a) Detritivore survival Predators consumed detritivores, as only 61.7% + 4.1 (mean + s.e.) of the detritivores survived in the predator treatment, whereas in the absence of a predator, detritivore survival was high (detritivore treatment: 97.4% + 0.8, cue treatment: 94.4% + 1.3). Statistically significant differences between treatments were driven by the mortality imposed by predators, as cues alone had only a weak effect on detritivore survival (table 1).

(b) Carbon dioxide flux All treatments started at a similar state and fluctuated over time, creating an interaction between time and treatment (F3,54 ¼ 23.8, p , 0.01) with no overall treatment effect (F2,55 ¼ 0.5, p ¼ 0.62; figure 1). Differences between treatments were greatest on the last day of the experiment, and corrected values revealed an increase in CO2 flux from detritivores that was absent in the predation and cue treatments (figure 2a, table 2 and the electronic supplementary material).

0

−0.05

cues predation detritivore

−0.10

1

2

3

4

day

Figure 1. Corrected CO2 flux dynamics (mean + s.e.).

Table 1. Effects of cues and predation on the survival of detritivores. Treatments: cues (C), predation (P), detritivore (D). Symbols between treatment letters indicate relationships based on effect sizes. Cohen’s d

95% CI

C¼D

20.4

(20.9, 0.1)

P,D C.P

21.8 1.8

(22.4, 21.2) (1.2, 2.4)

Fd.f.

p

37.52,65.2

,0.01

sample sizes: D (26), C (43) and P (39)

(c) Soil chemical content We found an effect of detritivore activity on soil nitrogen, representing a 6% increase compared with the blank treatment (figure 2b and the electronic supplementary material). As predicted, adding either predator cues or an actively foraging predator had cascading effects on the soil; nitrogen values in the predation and cue treatments were intermediate between the blank and detritivore treatments (electronic supplementary material). Corrected values illustrate increased soil nitrogen content in the detritivore treatment and how both predation and cues alone moderate that effect (figure 2b and table 2). There was no significant effect of treatment on soil total carbon or organic carbon, thus changes in C : N were driven by effects on soil nitrogen (electronic supplementary material).

4. Discussion We have demonstrated that predators can indirectly affect soil properties via consumptive and non-consumptive interactions with detritivorous prey, and that the risk of predation had effects comparable to those from actual predation. Specifically, the presence of predators or their cues led to a decrease in total CO2 flux as well as reduced N inputs to the soil. Predator cues had a large impact on soil properties despite not being renewed throughout the experiment and causing no appreciable prey mortality. Because these cues were also present in the predator treatment, it appears that consumptive

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Additional methods and results are available in the electronic supplementary material. We used four treatments to examine how consumptive and nonconsumptive interactions affect soil CO2 flux and nitrogen content: blank treatment (B) did not receive any arthropods and served as a control, detritivore treatment (D) was identical to B except for the addition of 15 detritivores, cue treatment (C) was identical to D except that it contained cues (i.e. silk, faeces and other excreta) deposited by a single predator over a 24 h period prior to the removal of the predator, and predation treatment (P) was identical to C except that the predator was not removed before adding detritivores. Experiments were conducted in laboratory microcosms. We quantified daily CO2 flux for 4 days, and at the end of this period, we removed and counted all remaining detritivores before we analysed soil chemical content (total nitrogen, carbon, organic carbon, C : N). We isolated the impact of detritivores on CO2 flux and soil chemical content by subtracting the mean values of the blank treatment from the values measured in the detritivore treatment. We performed similar corrections for the cue and predation treatments by subtracting the mean values from the detritivore treatment from both the cue and predation treatments. We tested treatment effects on the proportion of detritivores recovered at the end of the experiment and on soil chemical content using separate one-way ANOVAs. Flux in CO2 was analysed using repeated-measures ANOVA. We also used a one-way ANOVA to analyse CO2 flux on the last day of the experiment, as this represents the cumulative effect of the treatments and coincides with measurements of soil chemical content. All analyses were conducted on unmanipulated and corrected values (see above), and Welch’s tests were used instead of ANOVA when groups had unequal variances. Additionally, we calculated Cohen’s d and 95% confidence intervals (CIs), using suggested guidelines to interpret effect sizes (small ¼ 0.2, medium ¼ 0.5, large ¼ 0.8) [19]. All analyses were carried out using JMP (v. 9.0; SAS Institute, Inc., Cary, NC, USA).

CO2 (ml 24 h−1)

0.05

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(a)

(b)

3 0.0018

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% nitrogen

CO2 (ml 24 h−1)

0.75

0

0

–0.0018 cues

predation

detritivore

cues

predation

detritivore

Figure 2. (a) Corrected total CO2 flux and (b) soil nitrogen, on the last day of the experiment. Box plots show median, first and third quartiles, greatest values within 1.5 interquartile range, and outliers.

Table 2. Effects on corrected CO2 flux and soil N content. Treatments: blank (B), cues (C), predation (P), detritivore (D). Symbols between treatment letters indicate relationships based on effect sizes. CO2 (ml 24 h21)

% nitrogen

Cohen’s d

95% CI

Fd.f.

p

C,D

20.7

(21.3, 0.0)

13.62,27.5

,0.01

P,D C¼P

20.7 20.1

(21.3, 0.0) (20.7, 0.5)

sample size: B (20), D (21), C (20) and P (17)

and NCEs are not simply additive. Furthermore, the effects of predators seem to be largely attributable to their cues alone, as demonstrated in grazing systems [11]. This result is significant when considering that most studies to date investigating the impact of predators on detrital food webs have only manipulated the presence of predators, thus lacking the ability to highlight the importance of NCEs. These indirect interactions may be manifest as changes in prey behaviour or physiology that cascade through the soil community. The presence of collembolans has been shown to increase CO2 flux, an effect often attributed to collembolan stimulation of fungi and bacteria [16,18]. Reduced CO2 flux in the predator and cue treatments likely reflects decreased detritivore activity, a common response of prey to the presence of predators and the fear of predation [2]. Indeed, collembolans are capable of altering activity in response to predators and their cues [20]. Induced reductions in activity could consequently decrease stimulation of microbe respiration, creating a system wherein predation or fear of predation cascades through prey to the soil microbe community, ultimately altering soil processes. Our system appears to have a relatively simple structure (e.g. spiders–collembolans–microbes), as predators can reduce CO2 flux in odd-numbered food chains and, conversely, are expected to increase flux in even-numbered food chains [8]. Increased soil nitrogen content in response to adding detritivores is attributable to a combination of direct inputs and interactions with soil microbes [18]. Because all collembolans were removed prior to quantifying soil chemical

Cohen’s d

95% CI

C¼D

20.5

(21.1, 0.2)

P¼D C¼P

20.4 0.1

(21.0, 0.3) (20.5, 0.7)

Fd.f.

p

12.52,54

,0.01

sample size: B (20), D (20), C (19) and P (18)

content, nitrogen increases are limited to substances left behind by individuals. Collembolans excrete N and may egest N-containing compounds as well [21] and, because adults continue to moult [22], exuviae may also contribute nitrogen. S. curviseta is particularly fecund, and deposition of spermatophores by males and eggs by females likely contributed to increased soil nitrogen. Importantly, the nitrogen content of collembolan eggs is largely derived from body reserves, not diet, providing another potential source for the observed increase in soil nitrogen [21]. Finally, collembolans can increase N-fixation by interacting with free-living N-fixers that are abundant in soil systems [17]. The presence of predators or their cues may have reduced these nitrogen inputs by consuming individuals or changing detritivore behaviour [6], metabolic rate [21], assimilation efficiency [23] or reducing reproductive inputs. These mechanisms are not mutually exclusive and require further study to elucidate the impacts of predators on detrital systems. In conclusion, predators can have both consumptive and NCEs on detritivorous prey with cascading impacts on soil content and function. The importance of these indirect connections is twofold, because declines in biodiversity disproportionately affect predators [24], and soils are important regulators of the global carbon cycle [5]. Anthropogenic disturbances may weaken or eliminate links between predators and detritivores, with potentially negative consequences for numerous ecosystem services provided by soil arthropods [25]. Studies conducted at broader spatio-temporal scales will

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further enhance our understanding of the influence predators can have on detrital systems.

Data accessibility. Data available in the electronic supplementary material. Funding statement. Funding provided by Miami University’s Department

4

Acknowledgements. We are grateful to our research group, Melany Fisk

of Biology and Hamilton Campus and Arachnological Research Fund grant from the American Arachnological Society to M.I.S.

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and Michael Vanni for assistance.

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Fear of predation alters soil carbon dioxide flux and nitrogen content.

Predators are known to have both consumptive and non-consumptive effects (NCEs) on their prey that can cascade to affect lower trophic levels. Non-con...
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