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Community ecology
rsbl.royalsocietypublishing.org
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
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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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
Biol. Lett. 10: 20140366
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
Biol. Lett. 10: 20140366
−0.75
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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.
rsbl.royalsocietypublishing.org
and Michael Vanni for assistance.
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