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Community ecology
rsbl.royalsocietypublishing.org
Detritivores ameliorate the enhancing
effect of plant-based trophic cascades on
nitrogen cycling in an old-field system
Research
Robert W. Buchkowski and Oswald J. Schmitz
Cite this article: Buchkowski RW, Schmitz OJ.
2015 Detritivores ameliorate the enhancing
effect of plant-based trophic cascades on
nitrogen cycling in an old-field system. Biol.
Lett. 11: 20141048.
http://dx.doi.org/10.1098/rsbl.2014.1048
Received: 10 December 2014
Accepted: 22 March 2015
Subject Areas:
ecology
Keywords:
trophic cascade, nitrogen mineralization,
above-ground – below-ground interactions
School of Forestry and Environmental Studies, Yale University, 370 Prospect Street, New Haven CT 06511, USA
Nitrogen (N) cycling is a fundamental process central to numerous ecosystem
functions and services. Accumulating evidence suggests that species within
detritus- and plant-based food chains can play an instrumental role in regulating this process. However, the effects of each food chain are usually examined
in isolation of each other, so it remains uncertain if their effects are equally
important or if one chain exerts predominant control. We experimentally
manipulated the species composition of detritus-based (isopods and spiders)
and plant-based (grasshoppers and spiders) food chains individually and in
combination within mesocosms containing plants and microbes from an
old-field ecosystem. We tested: (i) their relative impact on N cycling, and
(ii) whether interactions between them moderated the influence of one
group or the other. We found that spiders in plant-based food chains exerted
the only positive effect on N cycling. Detritus-based food chains had no net
effects on N cycling but, when combined with plant-based food chains,
ameliorated the positive effects of plant-based species. Our results suggest
that detritus-based food chains may ultimately limit rates of N cycling by eroding the enhancing effects of plant-based food chains when antagonistic
interactions between detritus- and plant-based species exist.
1. Introduction
Author for correspondence:
Robert W. Buchkowski
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2014.1048 or
via http://rsbl.royalsocietypublishing.org.
Nitrogen (N) cycling is an important ecosystem process that determines production rates, levels of biodiversity and the trophic structure of ecosystems
[1]. Classical theory holds that in terrestrial ecosystems soil macrofauna
within detritus-based food chains play a key role in determining N cycling
rates, owing to their critical role in breaking down detrital inputs and priming
that detritus for microbial decomposition [2,3]. These indirect effects may in
turn feed back up the plant-based food chain to control the level of primary
and secondary productivity and community structure [2– 5]. Theory and emerging evidence shows that carnivores and herbivores within plant-based chains
can also control N cycling. These effects can be propagated through predatordriven changes in the feeding behaviour of herbivores, which influences the
composition of the plant community and hence plant inputs to the soil through
litter fall or root exudation [6 –9]. Furthermore, predators can alter herbivore
physiology by causing chronic stress and increasing the N excreted by herbivores in their faeces [10]. It follows that net N cycling rate should reflect the
combined effects of interactions among species in plant- and detritus-based
food chains [6,11]. Yet, research examining trophic effects on N cycling typically considers the effects of these trophic chains in isolation [6]. It therefore
remains uncertain if trophic effects propagating along each chain will be maintained if both chains are present. Understanding interactions and feedbacks
within and between plant- and detritus-based food chains is needed to offer
a complete picture of the impact of species composition on N cycling in ecosystems [12]. To this end, we report here on an experimental evaluation of the
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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experimental treatments: food chain configurations
2
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B
F
D
A
two trophic levels
C
G
H
I
E
three trophic levels
Figure 1. Illustration of the experimental treatments in which the number of trophic levels and the species composition of the trophic levels were systematically
manipulated to test for the effects of species interactions and feedbacks on N cycling. The treatments include a plant-only control (treatment A), plant-based chains
(treatments B and C), detritus-based chains (treatments D and E) and mixtures of plant- and detritus-based chains (treatments F –I). Each was replicated five times.
The plant species are the grass Poa pratensis and the goldenrod herb Solidago rugosa. The animal species are listed in figure 2. (Online version in colour.)
relative importance of species interactions within and between
plant- and detritus-based food chains for controlling N cycling
over a single season.
2. Material and methods
Methodology is explained in detail in the electronic supplementary
material.
the field offer a working hypothesis of direct interactions among
the species, as portrayed in figure 2a.
The experiment involved nine treatments across different
degrees of trophic complexity (figure 1). The treatments were
replicated five times using a randomized block design and isolated the effects of each animal species within each food chain,
with the proviso that predators were not added without their
primary prey (figure 1).
(b) Data collection
(a) Experimental design
The experiment was conducted using mesocosms designed to
explore the mechanisms of interaction among a circumscribed set
of species (figure 1) that are dominant members of plant- and detritus-based food chains of a New England old-field ecosystem [6].
Our explicit goal in using this particular set of species was to
systematically resolve mechanisms governing plant- and detritus-based feedbacks on N cycling using a factorial experimental
design (figure 1). This mechanistic, factorial approach would not
be feasible if we used a broader complement of animal species
that normally comprise the old-field system. Hence, our approach
reflects a compromise in which we use functionally representative
species to capture some biological realism, yet allow for experimental tractability in order to resolve mechanisms [6,13–15].
The soil was hand sorted and mixed with sand in order to exclude
soil macrofauna, so our plant communities were grown from
rhizomes and seed before the start of the experiment. Natural
history observations of plant- and detritus-based food chains in
Forty-six days after adding the animals to experimental mesocosms, we captured all the surviving animals, collected plant
biomass (roots and shoots) and took soil samples to measure
soil N content and to conduct laboratory incubations for net N
mineralization potential and microbial biomass.
(c) Data analysis
We analysed net N mineralization potential and soil N using linear
mixed-effects models with treatment as the fixed effect and block
as the random effect ([16], R v. 3.1.1). We used a linear mixed
model analysis with a categorical independent variable and a control treatment. In such an analysis, a significant treatment effect
indicates that the treatment deviated significantly from the control
after block effects are taken into account. Net N mineralization
potential and soil N data were log transformed to meet normality
requirements and we removed two replicates from our analyses
in which the grass did not successfully seed (final cover less
than 10%).
Biol. Lett. 11: 20141048
one trophic level
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(a)
Pisaurina mira
+
Melanoplus femurrubrum
+/–
(b) Plant and microbial biomass
0.04
Although grasshoppers and isopods typically prefer N-rich
grass in the absence of stress [6,17], we saw no differences in
plant community composition or plant biomass across our
treatments (electronic supplementary material, figures S2
and S3).
N
difference
(b)
net N mineralization potential
(µg g–1 d–1)
0.08
*
0.06
0.02
(c) Block effects
0
–0.02 B C D E F G H I
0.04
0.02
4. Discussion
0
(c)
0.20
0.5
difference
0.6
soil N (µg g–1)
Block effects accounted for a large portion of the withintreatment variability in our data and were largely driven
by a single block, wherein net N mineralization potential
( p ¼ 0.009, d.f. ¼ 37) and soil N ( p , 0.001, d.f. ¼ 38) were
significantly higher for all treatments.
**
0.4
0.10
0
–0.10 B C D E F G H I
*
0.3
0.2
0.1
0
A
B
C
D
E
F
G
H
I
treatment
Figure 2. (a) Hypothesized interactions among species used in our experiment.
Solid lines represent direct interactions, dashed lines represent positive (þ) or
context-dependent (+) indirect effects on soil N. (b) Effects of experimental treatment on net N mineralization potential and (c) soil N. Symbols
indicate treatments that were significant predictors of variation in net N
mineralization potential or soil N (*p , 0.08, **p , 0.01). Insets show the
net directional change in treatment effect. Grey, control; green, plant-based
chain; brown, detritus-based chain; gold, mixed treatments. (Online version
in colour.)
3. Results
(a) Net nitrogen mineralization potential and soil
nitrogen
The fully intact plant-based chain treatment (treatment C)
composed of plants, grasshoppers and sit-and-wait spiders
was the only significant predictor of differences in net N mineralization potential or soil N ( p ¼ 0.0314, d.f. ¼ 29, figure 2b;
We found that the sit-and-wait spiders in the three trophiclevel plant-based chain had the only significant impact on
net N mineralization potential and soil N. The effect of this
particular species on N cycling is consistent with previous
work conducted in field plots within our old-field ecosystem
[6]. The presence of sit-and-wait spiders is known to alter
grasshopper habitat use and feeding behaviour in a manner
that increases the grasshopper feeding on goldenrod [6] and
causes the grasshoppers to shed extra N in their faeces [10].
This spider species generally does not [6,10,18] and was not
found here (electronic supplementary material, figure S5) to
increase grasshopper mortality (i.e. mortality was compensatory to natural mortality). The stress-induced changes in
grasshopper physiology are likely to have increased soil N
and net N mineralization potential, because goldenrod dominance slows N mineralization [18] and grasshopper fecal
inputs increase soil N stocks [19].
The detritus-based species alone had no net effect on net N
mineralization potential or soil N. One potential explanation
is that the soils we used had 26% less soil N (x + s.e.; 0.24 +
0.016 mg g dry mass equivalent soil21) than soils where topdown control on N cycling in detritus-based food chains has
been documented (90 mg g dry soil21 [20]; 25.5 mg g dry
soil21 [21]). Thus, in our experiment, microbes may have
been strongly limited by N so that grazing by isopods had
little impact on their biomass or functional capacity (electronic
supplementary material, figure S4; [22]). Furthermore, isopod
survival to the end of the experiment was low, most probably
in response to predation and moisture stress (electronic supplementary material, table S3). Low isopod survival and a
microbial community limited by low soil N means that the conditions in our experiment probably were outside of the range
where top-down feedbacks in the detritus-based chain might
predominate [22].
Classic approaches typically consider how plant-based food
chains might influence belowground species and associated
processes through biomass inputs of detritus to soil [8,19].
The recent appreciation for interactions between detritus- and
Biol. Lett. 11: 20141048
+/–
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+
Rabidosa rabida
Oniscus asellus
p ¼ 0.0082, d.f. ¼ 30, figure 2c) by enhancing the process
(figure 2, insets). The plant-based chain with grasshoppers
and plants (treatment B) had a marginally significant effect
on soil N ( p ¼ 0.074, d.f. ¼ 30, figure 2c). None of the other
treatments differed significantly from the plant-only control
treatment ( p . 0.4).
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Ethics statement. All methods adhered to Yale University standards and
required no permits.
Data accessibility. All raw data are available in the electronic supplemental material, table S3.
Acknowledgements. We thank B. Crowley, T. Crowther, M. Bradford,
K. Burghardt, M. Lambert, E. Lazo-Wasem, D. Lopes, J. Smith,
A. Trainor and K. Urban-Mead for help and advice and three
anonymous referees for helpful comments.
Funding statement. Funding was provided by the Schiff Fund of Yale
University and the Edna Bailey Sussman Fund and a Natural Science
and Engineering Research Council of Canada grant to R.W.B. and
NSF grant no. DEB-0816504 to O.J.S.
Author contributions. R.W.B. conceived of the idea and conducted the
experiments. R.W.B. and O.J.S. designed the experiments and wrote
the manuscript.
Conflict of interests. We declare no competing interests.
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