OIKOS 93: 429–438. Copenhagen 2001
Allochthonous aquatic insects increase predation and decrease
herbivory in river shore food webs
Joh R. Henschel, Dieter Mahsberg and Helmut Stumpf
Henschel, J. R., Mahsberg, D. and Stumpf, H. 2001. Allochthonous aquatic insects
increase predation and decrease herbivory in river shore food webs. – Oikos 93:
429–438.
Rivers produce an abundance of aquatic insects that traverse land, where they can
have bottom-up effects on predators, who, in turn, can have top-down effects on
terrestrial herbivores. This effect can cascade down to plants. These trophic relationships were demonstrated in a field of stinging nettles, Urtica dioica, along a river in
Germany. At the shore compared to similar microhabitats 30 – 60 m away the
abundance and biomass of: midges were highest, spiders were also highest, while
herbivorous leafhoppers were lowest. At the shore, nettle plants were less damaged by
herbivores and thus had less regrowth. Spiders regularly captured both aquatic
midges as well as terrestrial leafhoppers and they captured more individuals of both
groups at the shore than further away. Midges supported high densities of shore
spiders. This was inferred from correlation of distribution and diet in the absence of
other environmental gradients. Removal of spiders from experimental plots caused
leafhoppers to increase at the shore, causing more plant damage. These effects were
not evident at spider-removal sites away from the shore. This demonstrated that
spiders depressed leafhoppers and decreased herbivory on plants only at the shore. It
is concluded that aquatic insects had a bottom-up effect on spiders and that this
subsidy facilitated a top-down effect that cascaded from spiders to leafhoppers to
plants. Similar effects would explain the distribution of arthropods along many
rivers. Allochthony connects river food webs with shore food webs, making both
components essential for each other.
J. R. Henschel, Desert Research Foundation of Namibia, Gobabeb, P.O. Box 20232,
Windhoek, Namibia ( [email protected]). – D. Mahsberg and H. Stumpf, TheodorBo6eri-Institut für Biowissenschaften der Uni6ersität, Lehrstuhl für Tierökologie und
Tropenbiologie, Biozentrum: Am Hubland, Uni6. Würzburg, D-97074 Würzburg, Germany.
Movements of resources from one habitat to another
(respectively, donor and recipient) can affect the food web
in the recipient habitat by enriching some consumers. Such
allochthonous resources, also termed subsidy (Polis and
Hurd 1995), are typically subject to donor control.
Subsidized consumers in the recipient habitat are consequently less dependent on in situ resources, but can exert
higher effect strength (consumer pressure) on these
resources (Jeffries 1988, Holt and Lawton 1993, Polis et
al. 1997). The subsidy hypothesis was proposed by Polis
and Hurd (1995) and Bustamante et al. (1995) to explain
why some animals maintain extraordinarily dense popula-
tions even though their in situ resource base is apparently
poor (Readshaw 1973, Lawton et al. 1975, Spiller 1992).
This hypothesis predicts that if the subsidized consumers
are polyphagous, they can depress the in situ resources.
Rivers are places of origin of many aquatic animals that
move across land. For example, imagoes of aquatic insects
such as midges, caddis flies and mayflies, sometimes occur
in high densities in terrestrial environments. Terrestrial
predators, such as spiders, may capitalize on such booms.
For such predators, aquatic insects represent a subsidy.
This paper focuses on whether and how subsidized
shoreline predators affect the food web.
Accepted 2 January 2001
Copyright © OIKOS 2001
ISSN 0030-1299
Printed in Ireland – all rights reserved
OIKOS 93:3 (2001)
429
In this paper, we elucidate the hypothesis (Henschel
et al. 1996a) that abundant flying insects of aquatic
origin (hereafter referred to as aquatic insects) subsidize
arthropod predators living on river shores, thus increasing the capacity of these polyphagous predators to
depress terrestrial prey populations. Furthermore, it is
suggested that, as a result of this depression, shore
plants should be less damaged by herbivorous insects.
First we compared arthropod populations at various
distances from a river in southern Germany and then
we experimentally tested the strongest causal links. To
reduce the number of variables affecting community
composition and to facilitate comparison, we focused
on insects and spiders occupying greater stinging nettles, Urtica dioica L. (Urticaceae). Nettles often dominate shore plant communities in Europe and harbor
characteristic fauna (Richards 1948, Davis 1983, 1989,
Sommaggio et al. 1995, Henschel et al. 1996a, Zabel
and Tscharntke 1998). Stinging nettles respond to herbivory by increasing defense and regrowth, i.e. they
grow new leaves and side branches that often bear
higher densities of stinging trichomes (Pullin 1987, Van
der Meijden et al. 1988, Pullin and Gilbert 1989, Mutikainen et al. 1994). Degree of regrowth is correlated
with herbivory and it integrates effects of herbivory on
plant performance. Thus, by examining relative degrees
of regrowth, we could estimate relative degrees of
herbivory.
From spatial variation of aquatic insects, arthropod
predators, terrestrial insects and nettle damage, we
could detect correlation, but the strength of causal
relationships required experimental confirmation. A direct test is to reduce the density of aquatic insects at the
shore, but it was impermissible in the water reserve and
impractical to remove aquatic insects from a sufficient
length of shore for the entire spring and summer seasons. Nevertheless, the same effect was attained by
comparing the edge of a nettle field facing the shore
with the edge of the same nettle field some distance
away from the shore in otherwise similar microclimatic
conditions. The above-ground development of riparian
nettles undergoes a complete cycle every year, beginning with almost bare ground and no resident herbivores and predators in spring each year. Differences in
aquatic insect abundance at different edges of a nettle
field with similar microclimatic conditions for the duration of the growth season thus represent a natural
experiment as effective as a manipulative experiment.
Furthermore, we conducted a manipulative experiment to test causal relationships of predators to terrestrial prey at places differing in the abundance of
aquatic insects. Physical removal of predators is a
common method for testing predation effects (e.g.,
Clarke and Grant 1968, Eickwort 1977, Henschel 1986,
Spiller and Schoener 1988, 1990, 1994, Dial and
Roughgarden 1995, Holland and Thomas 1997, Lang et
al. 1999). We removed all polyphagous arthropod
430
predators from sites at the river and some distance
away. Response variables were biomass of predators
and herbivores, and plant regrowth. We predicted that
at places where aquatic insects were most abundant,
removal of predators results in increases in terrestrial
insects. By contrast, we predicted that at places where
aquatic insects were not abundant, removal of predators would have little or no effect on terrestrial insects.
In this way, the predator-removal experiment could
also reveal whether aquatic insects affected the relationship of predators on terrestrial prey. In other words,
while treatment served to elucidate the effect of predation, repetition of the experiment at different distances
from the shore revealed the effect of aquatic insects on
predation pressure for terrestrial insects.
Methods
Study area
Fieldwork was conducted during 1994 and 1995 in the
Würzburg riparian forest (Wasserschutzgebie Würzburg
Mergentheimerstraße: 49°37%N; 09°57%E), an 18-ha area
along the western shore of the Main River within the
town of Würzburg, Bavaria, Germany. The 70-m-wide
river has an average discharge during low water in the
order of 100 m3 s − 1. The study area on the shore was
a strip of riparian forest, 900 m long and 60 m wide,
comprising silver willow Salix alba, black poplar Populus nigra, and black elderberry Sambucus nigra, and
lay 1–3 m above the river level. Tree canopies covered
about half of the forest floor, which was dominated by
a near-continuous patch of stinging nettles, Urtica
dioica. Nettles were selected as standard substrate for
investigating terrestrial arthropod assemblages. On the
landward side, the edge of the nettle field bordered a
meadow 60 m from the river.
Sample sites
Sample sites were selected so as to minimize variability
of sun, shade, and stand size between samples of a set.
Three sample sites were demarcated in a line at distances of 1, 30 and 60 m from the river, designated as
shore, midfield and meadow-edge sites. Nine such sets
of sites traversed the forest perpendicular to the river,
giving 27 sample sites.
Habitat condition
In order to determine whether there were environmental gradients and to assess plant damage, the following
parameters of microclimate, physical characteristics,
and nettle structure were measured at each study plot
on the day/night preceding sampling: temperature (°C),
relative humidity (%), shelter index (number of halfquadrants of sky covered), light intensity at 14.00 (klx),
plant cover (%), plot volume (m3), nettle density (m − 2),
OIKOS 93:3 (2001)
proportion of other herbs (%), distance of the plot from
a willow tree trunk (m), mean nettle height (m), maximum nettle height (m), number of primary leaves of six
nettles (nettle − 1), number of regrowth leaves of six
nettles (nettle − 1), and number of regrowth branches of
six nettles (nettle − 1). Nettle plant regrowth was determined by counting small new leaves and branches that
emerged along the stem well below the apical bud,
where primary leaves arise.
No microclimatic gradient was detectable in the relatively narrow study area that was only 1–3 m above the
river level. At night, relative humidity was typically
100% throughout the area and air temperature differed B1oC between sites. By day (mid-afternoon), humidity and temperature also did not differ significantly
between the shore and 30 m away (relative humidity:
t =0.81, df=34, p\0.05; temperature: t=1.00, df=
34, p\0.05).
In a multiple regression, nettle density contributed
significantly to the regression with arthropod abundance (r 2 =0.59, p =0.005) and biomass (r 2 = 0.60,
p= 0.007) and it was correlated with all but one environmental variable (r= 0.44–0.81), the exception being
proportion of other herbs. Although nettle density
varied between sites (range=30–101 nettles m − 2,
CV =27.6%), this variable was normally distributed
(Kolmogorov-Smirnov D=0.104, pB 0.05) and did not
differ between shore, 30 m and 60 m sites (ANOVA
with season as repeated measure: F=0.48, df= 72,
p \0.50).
trapping rate on 14-d traps minus the trapping rate by
night.
Arthropod distribution
Predator reduction
All spiders, opilionids and predacious insects (ca 70
species) seen at night in the herb layer of 18 treatment
plots were removed. Nettles were searched from top to
bottom, but ground predators were ignored. Predators
were captured with a small electric D-vac (Henschel
1995) that left non-target animals undisturbed. Removed predators were preserved in 75% alcohol for
identification. Each plot was searched for 18.99 SD 9.9
min (range 10–81 min), during which time 299SD 33
arthropods were removed (0–175). Spiders represented
78.2% of 4931 predators removed. No predators were
removed from control plots, but an equal length of time
was spent at these plots (by a second person) as at the
treatment plots.
Arthropods were sampled with sticky traps and by
beating nettles. One set of these samples was taken at
each of 27 sample sites during 18–30 June 1994, again
during 9 – 16 August 1994, 11–13 October 1994, and
22–24 May 1995, giving a total of 108 sets of samples.
Beating samples were collected at night (21.00–02.00)
when weather was relatively stable and when most web
spiders had their period of maximum foraging activity.
An umbrella (86 cm diameter) was placed into a 1-m2
area of nettles and opened onto the ground. Nettles
(n=20 –60) were vigorously beaten over this tray for 1
min with a stick. Arthropods were captured with a
modified D-vac (Henschel 1995) and preserved in 75%
ethanol.
Sticky traps were made of clear plastic plates of
10 ×10 cm coated on both sides with insect glue. These
were placed vertical, with the base 10 cm above nettles.
The sampling period was 14 d, beginning one week
before taking beating samples. Another set of 169
sticky traps was deployed in a similar fashion for
several hours (mean 9SD 4.491.0 h) during 27 nights.
While the night traps monitored pterous aquatic insects
at night, their activity by day was estimated from the
OIKOS 93:3 (2001)
Predator removal
Experimental protocol
Predators were removed during 74 fieldwork nights
during the period 29 May– 10 August 1995 and abundance of arthropods was determined on the nights of
16–19 August 1995. Plots consisted of strips of nettles
of 1× 2 m that were oriented parallel to the shoreline
and were surrounded by 1-m-wide paths that were kept
clear of vegetation. String fencing prevented nettles
from encroaching into the path and new growth in the
path was cut weekly to maintain the gap as a hurdle for
movements of terrestrial arthropods, while not hindering movements of flying aquatic insects. However, with
only 1 m distance separating the experimental plots
from the habitat pool (a large patch occupying several
hectares), plots did not become small habitat patches,
which could have changed animal community composition (Davis 1975, Zabel and Tscharntke 1998). Thirtysix plots were situated in pairs, 3–5 m apart, \ 10 m
between pairs. One plot of a pair was designated initially (by coin flipping) for predator removal. Fauna
was not manipulated in control plots. Each pair of
shore plots was matched with a pair of midfield plots
(30 m away from the river) with similar microclimatic
conditions. The experimental design thus comprised
nine replicate sets of four plots: removal and control at
shore, and removal and control away from shore.
Final collection
At the end of the experiment, predator removal efficiency was tested by first removing predators as usual,
before collecting by beating (as above, pooled double
samples to collect off 2 m2). Dislodged material was
poured into plastic bags, preserved with 75% ethanol,
and arthropods (454–2681/sample) were separated.
Treatment removed 61% of spider biomass and 48% of
other predators.
431
Predator diet
Feeding arthropod predators were observed for 323 h
using an Eschenbach binoscope with a 0.4-m focal
distance. Only actual feeding was recorded, and insects
trapped in spider webs, but not fed upon were ignored.
Whenever possible without interfering with the study,
feeding predators and their prey were collected for close
examination, especially to improve identification. Prey
capture rates by spiders were estimated by comparing
records of feeding with non-feeding spiders. Based on
observations and literature, all spiders collected in the
current study were categorized by species according to
their time of foraging activity as crepuscular/nocturnal
(ca 18.00 –06.00), diurnal or diel. 82.0% of the individuals were crepuscular/nocturnal, 16.7% diel, and only
1.3% were diurnal. This indicated that predation was
more intense at night than by day and supports the
nocturnal emphasis of the current study.
Analyses
Analyses of samples
A total of 102 095 arthropods with a body length ] 0.6
mm were collected and preserved in the distribution,
diet, and experimental parts of the study. Sampling and
the study questions did not focus on smaller
arthropods, nor on Acari and Pulmonata and these
were not analyzed. The following groups were ignored
from the beating samples, but were analyzed for the
sticky traps: Diptera: Nematocera and Brachycera, Trichoptera, Hymenoptera other than Formicidae, Lepidoptera imagoes. Collected arthropods were later
examined and measured (90.01 mm) by microscope.
Identification was to species or to the highest possible
taxonomic category. Total length was measured excluding terminal projections or appendages. From this,
biomass (dry mass) was calculated using equations of
Rogers et al. (1976) for insects (mass= 0.0305×
length2.62), and of Henschel et al. (1996b) for spiders
(mass = 0.076×length2.245) and opilionids (mass=
0.058×length2.559).
Pterous insects with aquatic larvae (referred to as
aquatic insects) had a high diversity of 51 species of
Nematocera, Trichoptera and Ephemeroptera, numerically dominated by midges, Chironomidae, Chironomus
spp. and Rheotanytarsus spp. (W.-D. Schmidt 1994
unpubl. report, Government of Lower Frankonia). In
our analysis, we grouped the most abundant chironomids (95.9% of the benthic Diptera; Schmidt op cit.)
with several other less abundant families of aquatic
Nematocera (mainly Culicidae, Simuliidae, Ephydridae), and for convenience refer to them collectively as
midges (Chironomidae), with the understanding that
some 4% are not chironomids. The remaining major
groups in our study were 158 taxonomic categories of
432
terrestrial herbivorous insects, termed herbivores
(Collembola, Coleoptera, Heteroptera, Homoptera,
Hymenoptera: Formicidae, Lepidoptera larvae, and
Psochoptera), 55 taxa of predatory insects (Coleoptera,
Heteroptera, Pseudoscorpionida, Dermaptera, Odonata,
Ensifera,
Mecoptera,
Neuroptera,
and
Thysanoptera), 5 harvestmen (Opiliones), and 72 spiders
(Araneae). Spiders amounted to 47.5% of all predators
and comprised wandering spiders (Clubionidae, Lycosidae, Philodromidae, Salticidae, Thomisidae, the
linyphiid Gongylidium rufipes), and web spiders
(Araneidae, Dictynidae, Mimetidae, Tetragnathidae,
Theridiidae, other Linyphiidae), with Tetragnathidae
accounting for 43.8% of spider abundance. Of the other
predators, only the opilionids, representing nearly 6.0%
of all predators, were important polyphagous predators, while the remainder were either uncommon or
stenophagous (e.g. 36.0% were Anthocoridae, pirate
bugs, that are specialist predators of homopteran eggs
and nymphs; Anderson 1962), and none appeared to
have a key role.
Data analyses
Abundance and biomass were standardized against nettle density and transformed with log(x+ 1). Means are
given 9 SD and significance levels were pB 0.05 unless
stated otherwise. Differences in distribution of
arthropods (not the experiment) were tested with
ANOVA with season as the repeated measure, using
the Tukey honest significant difference test to derive
probabilities (Zar 1996). The experiments were designed
pair-wise (treatment vs control, shore vs away from
shore), and Wilcoxon signed rank test was applied.
Results
Distribution of arthropods
Aquatic insects
Most of the aquatic insects (86.4%) were Nematocera
(of which 95% were Chironomidae) and these were
2.8 times as abundant at night than by day. Night traps
caught 0.319 0.41 midges dm − 2 h − 1, significantly
more at the shore than at 30 m (t =2.00, df= 167,
p B0.05). The biomass of aquatic insects on 14-d traps
differed with distance from the shore (F=31.3, df=2,
pB 0.001), being 4.5–7.4 times higher at the shore than
at 30 m and 60 m (Tukey: pB0.005), with no difference
between the latter sites (Tukey: p\0.05) (Table 1, Fig.
1a).
Predators
In beating samples, predators represented 48.3% of biomass of terrestrial arthropods. Predators comprised spiders (57.3% of biomass), Opiliones (12.1%), with the remainder being Heteroptera, Coleoptera, Thysanoptera
OIKOS 93:3 (2001)
and Tettigoniidae (30.6%). Biomass of predators other
than spiders did not differ significantly with distance
from the shore (FB2.25, df=2, p\ 0.05). Spider
biomass differed with distance from the shore (F= 6.26,
df=2, p=0.0065) (Table 1, Fig. 1b), being 2.5– 6.9
times higher at the shore than at 30 m (Tukey: p=
0.0198). There were no significant differences between
30 m and 60 m (p\0.05). The spiders Tetragnatha
montana and Clubiona (C. lutescens and C. phragmites)
represented 42.0% and 24.4% of the spider biomass,
respectively. T. montana had 2.3 times more biomass at
the shore than at 30 m (F\11.9, df= 2, pB 0.005).
Likewise, Clubiona had 3.1 times more biomass at the
shore (Friedman test: x2 =10.1, df=2, pB0.01).
Terrestrial herbi6ores
Biomass of herbivorous terrestrial insects was very variable and did not differ significantly with distance (F=
2.35, df =2, p=0.117). Homoptera, which represented
52.8% of biomass, was the only order that differed with
distance (F=5.12, df= 2, p=0.014). The difference
was due to the dominant leafhoppers, Cicadellidae
(F =5.92, df=2, p=0.0081, Fig. 1c) that were less
abundant at the shore compared to 30 m (Tukey:
p=0.0064), but did not differ between 30 and 60 m
(Tukey: p\0.05).
Predator-herbi6ore ratios
Overall, predators were more abundant at the shore
than 30 m away, while herbivores were less abundant.
This resulted in an overall predator–herbivore ratio 2.6
times higher at the shore than at 30 m (Table 1).
Predator diet
Arthropod predators were observed feeding on 779
occasions at the shore and 30 m away (Table 2). Of 128
feeding opilionids, 15.1% consumed aquatic insects,
with no significant difference between the shore and
30m (x2 = 1.47, df= 1, p \0.05). Predatory insects ate
37 prey, of which 16% were aquatic, captured by
polyphagous Nabidae (Heteroptera). Spiders fed (n =
545) mostly on Homoptera (46.8%) and midges
(39.3%). The proportion of spiders observed feeding did
not differ with distance (x2 = 3.84, df= 1, p\ 0.05). At
the shore, 53.6% of spider prey were of aquatic origin,
while this prey category represented only 24.2% at 30 m
(x2 = 21.3, df=1, pB0.001). The relative contribution
of aquatic insects in the diet did not differ from the
relative abundance of aquatic insects in sticky traps
(x2 = 0.61, df= 1, p\ 0.05), indicating that spider diet
tracked availability. The species recorded feeding most
often (47.5% of occasions) was Tetragnatha montana,
with 57.8% of its prey at the shore being aquatic
compared to 31.5% at 30 m (x2 = 4.91, df=1, pB
0.05). Herbivores represented 36.7% and 54.3% of its
diet at the shore and at 30 m, respectively. Aquatic
insects formed a lower proportion of the diet of Clubiona spp. at the shore (27.1%) and at 30 m (16.9%).
This spider preferred cicadellids (65.3%). Another common spider, Gongylidium rufipes, was never seen feeding
on aquatic insects, while 58.8% of its food items were
cicadellids.
We estimated relative predation rate from diet, abundance of spiders and proportion of spiders feeding. The
T. montana population captured 4.4 times as much
Table 1. Mean9 SD biomass of arthropods at river shore, midfield (30 m from river) and meadow edge (60 m) sites. Ratio
1 = mean biomass at shore } midfield; Ratio 2= shore } meadow edge. Subscript letters indicate grouping determined with
repeated measures ANOVA.
Nettle site
Ratio
Arthropods
at shore
midfield
meadow edge
1
2
Aquatic Insects (mg dm−2 sticky trap)
Nematocera
Trichoptera
Predators (mg m−2 nettles)
Spiders
T. montana
Clubiona
Opiliones
Insects
Herbivores (mg m−2 nettles)
Coleoptera
Miridae
Homoptera
Aphididae
Psyllidae
Cicadellidae
Imagoes
Nymphs
4.493.1a
2.59 2.7a
1.8 9 2.4a
36.0 9 30.5a
21.9 9 21.1a
9.1 9 7.5a
6.0 97.8a
3.6 9 3.1a
10.59 7.9a
20.4 9 5.8a
5.995.4a
5.59 4.1a
9.09 4.1a
1.49 1.1a
0.99 0.8a
3.1 90.3a
1.79 1.3a
1.59 1.4a
1.0 91.0b
0.9 91.0b
0.08 90.14b
21.8 9 8.4a
10.5 9 8.1b
4.5 92.7b
1.9 92.2b
3.3 92.7a
8.0 94.1a
32.1 9 22.7a
7.7 98.7a
5.7 95.1a
18.7 9 16.5b
5.2 98.7a
1.1 90.8a
9.1 99.1b
3.1 90.8b
6.0 99.9b
0.8 90.7b
0.7 90.7b
0.09 90.21b
19.0 9 7.9a
9.2 97.1b
2.7 92.8b
2.0 91.9b
1.5 91.0a
8.3 99.3a
25.9 911.5a
4.1 92.2a
6.8 95.9a
15.0 9 10.0b
3.3 95.2a
1.0 90.7a
6.1 95.8ab
1.8 90.5a
4.3 96.1b
4.2
2.6
22.9
1.7
2.1
2.0
3.1
1.1
1.3
0.6
0.8
1.0
0.5
0.3
0.8
0.3
0.5
0.2
5.2
3.4
20.8
1.9
2.4
3.3
3.1
2.3
1.3
0.8
1.4
0.8
0.6
0.4
0.9
0.5
0.9
0.3
2.6
2.4
Predator : herbivore ratio
OIKOS 93:3 (2001)
1.8
0.7
0.7
433
Terrestrial herbi6ores
Homoptera, the dominant terrestrial herbivores
(biomass: 51.8%; Table 3), were affected by the treatment at the shore. There, their biomass increased by
26.2% (T=42, pB0.05) in removal plots compared to
control plots. This pattern was evident for leafhoppers,
particularly the cicadellids Eupteryx spp. (E. urticae, E.
cyclops, E. aurata; biomass: 52.2% of Homoptera) (T=
41, p B0.05) (Fig. 2). By contrast, leaf bugs (Miridae)
and beetle biomass did not change. At 30 m there were
no significant differences in herbivores between treatments (T539, p \0.05).
Nettle regrowth
Degree of regrowth was 43.0% higher at distant control
plots than at the shore (T= 41, pB 0.05). Regrowth
was 17.7% higher at removal plots than control at the
shore (T =42, pB0.05), but not significantly different
at 30 m (Fig. 2).
Discussion
Fig. 1. Log mean biomass (mg m − 2, n= 9) of (a) midges on
sticky traps, (b) spiders in beating samples, and (c) leafhoppers
in beating samples collected at Würzburg riparian forest in
different months at the river shore (0 m, shaded) compared to
30 m away (clear).
aquatic prey and 1.5 times as much terrestrial prey at
the shore than did the population at 30 m. For Clubiona these two ratios were 6.4 and 3.7, respectively.
This indicated that these spiders exerted a higher predation pressure on herbivores at the shore.
Predator removal
Predators
Removal treatment reduced spider populations
(Wilcoxon test on nine pairs at shore and nine pairs at
30 m: T\39, pB0.05; Table 3). In ten weeks, 3857
spiders were removed, causing a decline in biomass of
T. montana by 35–61% and of other spiders by 26–28%
(Fig. 2). Many small G. rufipes were overlooked, while
small pirate bugs (Anthocoridae) increased at shore
removal sites (T\40, pB 0.05). Removal effort did not
affect other predatory insects nor mobile harvestmen
(T539, p \0.05).
434
Several trophic levels were correlated along the Main
River in Würzburg. At the shore, midges of aquatic
origin were most abundant and so were polyphagous
spiders. Abundant aquatic insects appeared to be the
reason why shore spiders were so abundant. This conclusion is based on the correlation of the distribution of
these taxa as well as the declining representation of
aquatic insects in spider diet with distance from the
shore. This is furthermore reinforced by the results of
the natural situation identical to an experiment: comparison of the edge of the nettle field facing the shore
and a similar edge facing away from the shore. There
was no gradient of microclimate and nettle characteristics across the low-lying study area that would have
influenced these results. We conclude that allochthonous aquatic insects caused a bottom-up effect
on spiders at the shore and that this effect declined with
distance from the shore.
Consistent with our result, Henschel et al. (1996a)
found that the pattern of higher abundance of spiders
in nettles along river shores and lower abundance at
similar sites away from shores is widespread in southern
Germany. Indeed, spiders are conspicuously abundant
in many habitats along river shores elsewhere (Jackson
and Fisher 1986, Jadranka 1992, Malt 1995, Williams et
al. 1995, Power et al. 1998) and ocean coasts (e.g.,
Schoener and Toft 1983, Spiller 1986, Polis and Hurd
1995, 1996a, b, Schoener and Spiller 1995). This is
because of their ability to concentrate at resource-rich
places (Riechert 1976, Greenstone 1978, Kronk and
Riechert 1979, Gillespie 1981, Janetos 1982, Morse and
Fritz 1982).
At the Würzburg shore compared to some distance
away, we found that the herbivorous leafhopper popuOIKOS 93:3 (2001)
lation was reduced. Diet indicated that there was a
causal link between abundant, polyphagous shore spiders and reduced leafhoppers, with predation rate of
spiders on leafhoppers being much higher at the shore.
The manipulative experiment confirmed this causal
link. It also demonstrated that spiders depressed
leafhoppers only at shore sites and did not significantly
affect them away from the shore. This was a further
indication that shore spider abundance was related to
bottom-up effects other than terrestrial herbivores,
namely abundant midges.
It is well established that polyphagous spiders can
depress insect prey populations in certain circumstances
(e.g., Kajak 1965, 1978, Riechert and Lockley 1984,
Nyffeler and Benz 1987, Riechert and Bishop 1990,
Wise 1993). Especially in agroecosystems, where Homoptera are pests, it has been noted that spiders can
significantly depress aphids and leafhoppers (e.g., Kiritani et al. 1972, Edwards et al. 1979, Chiverton 1986,
Oraze and Grigarick 1989, Holland and Thomas 1997,
Lang et al. 1999). In a comparison of spider predation
in a maize field with fallow land, Lang (1998) found
that leafhopper populations were depressed only in the
maize, where there were high numbers of flies and
aphids. This appears to be a situation analogous to our
river shore, where alternative prey enabled the spiders
to increase predation. In addition to polyphagy, the
ability of spiders to concentrate at prey-rich sites, to
adjust rapidly to changes in prey availability with a
functional response, and to change their reproductive
rate to give a numerical response (Wise 1979, 1993)
facilitate their ability to depress resident prey
populations.
In our study, the reduction of leafhoppers at the
shore also reduced damage to nettles. Herbivores are
known to have top-down effects on nettles (Fraser
1998) and to increase regrowth (Van der Meijden et al.
1988, Pullin and Gilbert 1989, Mutikainen et al. 1994).
We found that higher regrowth occurred in those shore
plots where spiders were removed and leafhoppers increased. By comparison, nettles in control plots at the
shore had less regrowth, reflecting less damage by herbivores. Damage increased away from the shore where
leafhoppers were more abundant. Other nettle characteristics did not differ consistently with distance from
the shore. We conclude that the high abundance of
midges enabled an increase in spider abundance at the
shore, which caused an apparent top-down trophic
cascade that affected leafhoppers and, ultimately, nettles (Fig. 2). For practical reasons, it was possible for us
to demonstrate this trophic cascade at the species-level
(or assemblage). We suggest that the trophic cascade
may extend to the community-level (according to the
distinction made by Polis 1999, Polis et al. 2000), given
that there are indications that both aquatic insects as
well as generalist terrestrial predators tend to be abundant along shores in general.
Although the 70-m-wide Main River is a fairly substantial water body, aquatic insects and their trophic
effects declined surprisingly quickly in only a few tens
of meters from the shore, although the habitat did not
change. Intensive management and use of the Main
River as well as the near-lack of shallow mudflats along
its shore embankments will have reduced the productivity of this river from its pristine state (however, the
condition of the Main River is believed to be improving, Anon. 1991). This situation may not allow us to
comment on the relationship, if any, of the size of the
river to the extent of its influence over land, except to
note that the relative rate of change in the assemblage
Table 2. Percent diet of arthropod predators at the shore and 30 m or further away.
Predator
Spiders
Prey
shore
Aquatic insects
Nematocera
Trichoptera
Terrestrial herbivores
Cicadellidae
Psyllidae
Aphididae
Heteroptera
Coleoptera
Other
Brachycera
Hymenoptera
Araneae
Opiliones
Nettle seeds
Other
Identified
Unidentified
OIKOS 93:3 (2001)
Harvestmen
\30 m
shore
Other
\ 30 m
shore
\30 m
51.0
2.6
23.8
0.4
16.9
2.6
7.9
2.6
28.6
0.0
0.0
0.0
19.0
6.9
11.4
5.2
1.3
34.0
15.6
8.2
5.3
4.1
3.9
1.3
28.6
2.6
1.3
5.3
2.6
18.4
2.6
0.0
14.3
4.8
28.6
14.3
0.0
0.0
0.0
83.3
8.3
0.0
1.0
0.7
0.3
0.0
0.0
0.7
5.7
0.8
0.8
0.0
0.0
1.2
0.0
0.0
0.0
6.5
32.5
3.9
10.5
2.6
0.0
5.3
26.3
15.8
0.0
0.0
0.0
4.8
0.0
4.8
0.0
0.0
0.0
0.0
0.0
8.3
77
10
38
3
306
27
244
37
21
3
12
1
435
Table 3. Total abundance (biomass) of predators removed during week 1–10 of the experiment and predators and herbivores
collected during week 11 in nine plots of each treatment.
Shore
30 m
Control
n
Predators removed in week 1–10
T. montana
Other spiders
Harvestmen
Pirate bugs
Other predatory insects
Predators collected in week 11
T. montana
Other spiders
Harvestmen
Pirate bugs
Other predatory insects
Herbivores collected in week 11
Cicadellidae
Other Homoptera
Leaf bugs
Beetles
Removal
mg
n
mg
1680
578
474
2
146
(1774)
(576)
(1080)
(1)
(2338)
n
Removal
mg
mg
n
877
722
286
0
166
(630)
(601)
(622)
(0)
(2571)
710
1052
178
1973
100
(799)
(247)
(749)
(370)
(385)
487
1129
166
2267
126
(515)
(178)
(418)
(500)
(375)
608
1063
99
2013
169
(647)
(592)
(262)
(349)
(429)
277
887
68
2147
248
(255)
(438)
(167)
(343)
(671)
3845
395
351
322
(1363)
(226)
(424)
(95)
4596
675
366
364
(1681)
(254)
(380)
(90)
3992
536
460
520
(1522)
(284)
(420)
(125)
3790
720
465
597
(1368)
(445)
(487)
(133)
with distance from the Main River did not appear to be
very different in scale from that found along streams
(B10 m wide) in southern Germany (Henschel et al.
1996a). Individual aquatic insects emerge from water
and return to it, sometimes crossing between different
water bodies. They therefore most frequently cross
shorelines and less frequently traverse particular areas
further from shores, where their density is consequently
Fig. 2. Median9 quartile of arthropod biomass (mg m − 2,
same linear scale for all) and of nettle regrowth (number of
secondary branches and secondary leaves per nettle) at predator-removal and control plots at the shore and 30 m distant
from it. Differences at a site for Tetragnatha, other spiders and
harvestmen were caused by the treatment, while the rest are
response variables. Asterisks indicate that differences between
treatments (below graph) or between the shore and 30 m plots
(below centre) were significant according to the Wilcoxon test
(p B 0.05, n = 9 pairs).
436
Control
lower than at shores. The density of aquatic insects at a
distance from the shore will very likely be affected by
the productivity of the water body as well as by the
behavior of particular species of aquatic insects in
crossing land, which will also be influenced by the
nature of the terrestrial habitat. To deepen our understanding of the effects of trophic relationships in rivers,
where turnover rate is high, towards trophic relationships in adjacent terrestrial environments, where
turnover is expected to be comparatively slower (Cyr
and Pace 1993, Chase 2000), both more detailed behavioral, as well as broader, spatio-temporal ecological
studies are required (Power 2000, Holt 2000).
Our investigation elucidates one way how distinctive
habitats, water and land, are interconnected. The
aquatic food web becomes part of the surrounding
terrestrial environment and affects the terrestrial food
web in a way analogous to apparent competition (Holt
1984). Midges originating from the water cause a numerical response in spiders and enable them to depress
leafhoppers and thereby to reduce herbivory on nettles.
This case study contributes to the growing concept of
spatial subsidies (Polis et al. 1997) that is fundamental
for the landscape ecology of rivers.
Acknowledgements – The late Gary Polis suggested and guided
this study and the Alexander-von-Humboldt Foundation
funded JRH. The Wasserwerk Würzburg, Würzburger Versorgungs- und Verkehrs GmbH, Government of Lower Frankonia and Municipality of Würzburg gave permission and
facilitated this study in Würzburg riparian forest. Inge Henschel assisted extensively in the field and laboratory. Peter
Buchacher, Günther Eppinger, Jutta Hoffmann, Annette Hoh,
Konstantin König, Norbert Schneider, Lisa Stumpf and Gerhard Vonend provided help, tools and advice. For valuable
comments we thank Andreas Lang, Eduard Linsenmair, Mary
OIKOS 93:3 (2001)
Power, Mark Robertson, John Sabo, Thomas Schmidt, Mary
Seely and David Ward.
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