# “Brown” World Invertebrates Contradict “Green” World Biodiversity Theory

Authors: L. Brian Patrick; Lauchlan H. Fraser; Mark W. Kershner
Journal: Research Letters in Ecology
 (2008)

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## Abstract

Biodiversity-productivity theory predicts that ecosystems with increased productivity due to excessive limiting-nutrient loading will have decreased taxonomic diversity.  In this 4-year study, we elevated productivity by adding NPK fertilizer to 20 m diameter plots in an old-field grassland to test the effects of anthropogenically mediated nutrient loading on plant and epigeal arthropod communities. While plants responded as predicted by the biodiversity-productivity theory, the epigeal arthropod community had highest species richness within the fertilized high-productivity treatments. We conclude that the contradictory response of the largely detrital-based epigeal community should alter conventional biodiversity-productivity theory and could affect terrestrial biodiversity conservation strategies.


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## Body

## 1. Introduction

The
biodiversity-productivity theory stating that local richness declines from
mesotrophic to eutrophic systems has received considerable empirical and
theoretical support [1–5]. Although most empirical studies examined plant communities,
studies of invertebrates have also shown that reduced plant diversity caused by
high productivity corresponds to reduced diversity in the primary-producer-based
(or “green” world) herbivore community as well as higher trophic levels [5, 6]. Hutchinson
[7] referred to
this as the diversity-trophic structure hypothesis, where a reduced diversity
and concomitant architectural structure within the plant community will
correspond with a reduced diversity in the herbivore community and upper
trophic levels.The relationship
between biodiversity, productivity, and trophic interactions is understudied [3],
especially considering that humans have significantly altered the global
nitrogen (N) pool causing nutrient loading into ecosystems and degradation of
biodiversity in a variety of habitats [2, 4]. Especially little attention has
been given to the detritus-based (or “brown” world) component of the
invertebrate community [3, 5, 6], but see [8–10], despite the
fact that detritivores can alter nutrient cycling and trophic interactions [3, 8].
Ungrazed or unmown temperate grasslands can produce an abundance of plant
litter [11], which provides an opportunity for controlled manipulative
experiments to test the effects of litter on the epigeal community.Here we report
results of a large-scale 4-year study in which plant litter and nutrient
loading were manipulated with NPK fertilizer to elucidate the response of the plant
and epigeal invertebrate communities in a temperate old-field grassland [12].
Our goal was to test the biodiversity-productivity theory with respect to the epigeal
invertebrate community. Our hypothesis was that invertebrate species richness would
be reduced by fertilization and by plant litter.


## 2. Materials and Methods

A
complete description of the field site and the plant sampling are described
elsewhere [12], though a brief description of the general experimental design
and invertebrate sampling procedure are given below.In August 2001,
twenty-four 20 m diameter circular plots (314 m2) were established.
These experimental plots were separated by at least 20 m and were at least 30 m
away from any other habitat (e.g., roads, forest). Treatments were applied in a
2×2 factorial design of fertilizer (+F  =  fertilizer added, −F  =  no
fertilizer) and plant litter (−L  =  litter removed, +L  =  litter left in situ after yearly mowing) with the
control plots characterized as no fertilization and plant litter left in situ (+L /−F), resulting in six
replicates per treatment. In April 2002 and continuing each April through 2005,
Scotts brand Osmocote 8-9 month slow release fertilizer 19-6-12 (NPK; Scotts,
Marysville, Ohio, USA) was applied at 20 g N m-2 in fertilized plots.
Within two days of annual mowing of the whole site with a large tractor and
brush hog mower (autumn 2001–2004), litter was
removed from litter removal treatments using a small 23 hp lawn tractor with a
pull-behind 8 hp Agri-Fab Mow-N-Vac trailer attachment (Agri-Fab, Sullivan, Ill,
USA).  After litter removal, loads of
removed litter were left standing for at least 10 minutes to allow
inadvertently vacuumed arthropods to return to the site.Beginning
in 2002, invertebrates were collected using four pitfall traps in each plot (n=96 total pitfall traps). Within each
plot, a single trap was placed 5 m from the center of the plot at each of four
magnetic compass directions (northeast, northwest, southeast, and southwest).
Each trap consisted of a 10 cm diameter, 18 cm tall PVC sleeve into which a
710-mL plastic cup was inserted and filled to approximately 4 cm with a 50/50
water/propylene glycol mixture. To deter trap raiders (e.g., microtine
mammals), to prevent captured invertebrates from climbing out of the trap, and
to prevent precipitation from directly flooding the trap, an 8 cm powder funnel
with a base enlarged to approximately 3 cm was inserted into the trap and
covered by a 15 cm × 15 cm board, leaving approximately 3 cm clearance.
Starting in May and continuing through August, traps were alternately left open
for two weeks and closed for two weeks. When closed, the plastic cups were
removed, the contents collected and preserved in 70% EtOH, and the PVC sleeve
was tightly capped. This resulted in 3 sampling periods each year from 2002 to 2005,
with no overlap between sampling, mowing, and vacuuming. We only report on our
final 2005 harvest because the trends were similar in earlier years and 2005
results had the greatest treatment effects.Invertebrates were
identified to species when possible, otherwise to the lowest possible taxonomic
level, and the numbers within each taxonomic identification unit (TIU) in each
trap were recorded. Each TIU within a trap was dried at 70°C for 72 hours, then
TIU biomass to the nearest 0.0001 g was determined. Because some extremely
small TIUs did not register a biomass at 0.0001 g, their biomass was recorded
as “0.0000 g,” unless caught in number sufficient to register a mass.


## 3. Results and Discussion

While the plant
community largely responded to our treatments as predicted by the
biodiversity-productivity theory (Figure1(a)) [12], the epigeal invertebrate
community did not. Invertebrate species richness increased with invertebrate
biomass (Figure 1(b)). Moreover, invertebrate species richness also increased as
plant biomass increased (Figure 1(c)) and was inversely related to plant
species richness (Figure 1(d)).  These
results are contrary to previous research [5, 6] and predictions [4, 7], and instead
support the idea of a bottom-up control of diversity in the epigeal invertebrate
community [8–10]. Our results suggest that the present
biodiversity-productivity theory does not adequately describe the dynamics of
the predominately “brown” portion of terrestrial ecosystems [8–10].Scatter plots with linear regressions of the average of the three
sampling periods in 2005 data for (a) plant species richness versus
standing crop plant biomass (g/m2), (b) invertebrate richness
versus invertebrate biomass (g), (c) invertebrate richness versus
plant biomass (g/m2), and (d) invertebrate richness versus plant species
richness.  Invertebrate data represent three 14-day sampling periods
(4032 “traps nights,” or 96 traps × 14 nights open × 3 sampling
periods) during which 46208 invertebrates were captured. –L
and +L indicate plant litter biomass removed and plant litter
biomass left in situ, respectively, and –F versus +F indicate
no fertilizer and fertilized at 20 g N/m2,
respectively.
** indicates
regression significant at P<.0001.
(a)(b)(c)(d)We acknowledge that pitfall trap sampling does not represent the entire epigeal community. Only the most active epigeal invetebrates are sampled by pitfall traps. Furthermore, pitfall trapping is not simply a representation of just the detrital-based community. Combining pitfall traps with litter
extraction using Berlese funnels or D-Vac sampling would have given a more
complete picture, with the inclusion of many important litter arthropods that
might not have been adequately counted.Why does epigeal
invertebrate species richness increase with productivity? If we were to assume
a direct causal connection between plant productivity and the species richness
of the detrital community it would seem that dead plant material limits
detritivore diversity.  However, epigeal richness
was equally high in fertilized plots where litter was removed compared to fertilized
plots with litter left in situ.
Perhaps the limitation to epigeal invertebrate richness was nitrogen since the
fertilizer was a high-N mix. High quality, N-rich detritus, from both
above-ground (even if it were minimal) and below-ground (e.g., fine root
turnover) may regulate epigeal richness. If nitrogen, through fertilization,
was the major factor that controlled detritivore richness, we could say that
bottom-up effects were important within the epigeal food web. Another possible
controlling factor is through indirect predator-prey interactions mediated by the
increased flow of energy through the “green” trophic levels (primary producer
to herbivore to carnivore) caused by fertilization. For example, Fraser and Grime [13, 14] reported evidence to support
top-down cascading effects in highly productive plant communities (carnivores
controlled herbivores, thus releasing herbivore pressure on vegetation), but
little signs of herbivore activity at high productivity, which begged the
question: What are the carnivores feeding on? One possible explanation is that the carnivores
also prey on a large detritivore community, which increases carnivore abundance
well above the levels that could be supported by the herbivores alone; these
elevated carnivore populations in turn suppress the herbivores to extremely low
levels [15, 16]. A knowledge of the detritivore population and the extent to
which carnivores are generalized enough to prey on detritivores and herbivores
is needed.We suggest the
causal link between productivity and biodiversity is bidirectional [3], and is
also potentially complicated by trophic interactions: productivity can control
diversity, but diversity can also regulate productivity. In the first case, a productivity-driven
reduction in plant diversity may be positively correlated with herbivore diversity
[5], but may also have the potential to indirectly affect the detritivore
trophic level. In the second case, a diverse detritivore-based community may
affect nutrient cycling, thereby influencing both plant and animal productivity
[8–10]. This influence of the “brown” community on the “green” community’s
productivity is largely ignored by current biodiversity-productivity theory,
despite theoretical and empirical evidence suggesting a potentially strong
feedback from the detritus-based community to the producer-based community [8–10].Another
interesting finding that emerged from our study was that our results do not
support the diversity-trophic structure hypothesis posed by Hutchinson
[7]. A reduction in plant species
richness was inversely related to invertebrate species richness.  We think this suggests that productivity and
energy flow has a greater control on invertebrate richness than does plant
richness. However, more work is needed to elucidate the relative affects of
bottom-up and top-down control on detritivores.The relationships highlighted
by our study are of particular importance given the negative human influences
on biodiversity and ecosystems. Humans are altering ecosystems and accelerating
biodiversity loss at an alarming rate [3, 4, 12]. As a result, terrestrial
biodiversity conservation strategies have largely focused on the primary producer
and the primary producer-based portions of biological communities. These
community components are often more easily sampled and identified, and are
typically more visible to the general public. Thus, producers and visible
consumers lend themselves readily to the rapid biological assessments required
for conservation policy, especially in ecosystems with charismatic threatened
species. However our results suggest that more comprehensive studies that include
the animal component of the “brown” world are needed, lest we ignore significant
portions of the biological community which can substantially affect nutrient cycling
and trophic dynamics.



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