J o u r n a l o f A nimal
E c o l o g y 2 0 07
B
Slackwell Pubplishing Ltid ders and subsidies: results
from the riparian zone
76, 687–694
of a coastal temperate rainforest
LAURIE B. MARCZAK and JOHN S. RICHARDSON
Department of Forest Sciences, University of British Columbia, 3041-2424 Main Mall, Vancouver, British Columbia,
Canada, V6T 1Z4
Summary
1. Aquatic insects emerging from streams can provide an important energy subsidy to
recipient consumers such as riparian web-building spiders. This subsidy has been
hypothesized to be of little importance where the primary productivity of the recipient
habitat exceeds that of the donor habitat.
2. To test this hypothesis, we manipulated emerging stream insect abundance in a
productive riparian rainforest in a replicated design using greenhouse-type exclosures,
contrasted with unmanipulated stream reaches (four exclosures on two streams).
3. Experimental exclosures resulted in a 62·9% decrease in aquatic insect abundance in
exclusion reaches compared with control reaches. The overall density of riparian spiders
was significantly positively correlated with aquatic insect abundances. Horizontal orb
weavers (Tetragnathidae) showed a strong response to aquatic insect reduction –
abundance at exclosure sites was 57% lower than at control sites. Several spider families
that have not been associated with tracking aquatic insect subsidies also showed significantly decreased abundance when aquatic insects were reduced.
4. This result is contrary to predictions of weak subsidy effects where recipient net
primary productivity is high. These results suggest that predicting the importance of
resource subsidies for food webs requires a focus on the relative abundance of subsidy
materials in recipient and donor habitats and not simply on the total flux of energy
between systems.
Key-words: aquatic insect emergence, land–water interface, streams, trophic subsidies.
Journal of Animal Ecology (2007) 76, 687–694
doi: 10.1111/j.1365-2656.2007.01240.x
Introduction
Resource flows between habitats (hereafter referred to
as subsidies) can have important implications for food
web dynamics in recipient environments (Bastow et al.
2002; Collier, Bury & Gibbs 2002; Sabo & Power
2002b). The movement of energy, nutrients or prey
between systems is ubiquitous, although it is not yet
clear how strong the effects of these subsidies are in all
systems (Polis, Anderson & Holt 1997). In this context
it is critical to understand how different characteristics
of subsidies (e.g. trophic level of a subsidy, subsidy type,
variability in space or time), habitats (e.g. permeability,
seasonality of in situ production) or consumers (e.g.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society
Correspondence: L. B. Marczak, Department of Forest
Sciences, University of British Columbia, 3041-2424 Main
Mall, Vancouver, British Columbia, Canada, V6T 1Z4. Tel.:
(604)822 8927. Fax: (604)822 9102. E-mail:
laurie@interchange.ubc.ca
trophic level, functional feeding group) might determine
the relative importance of cross-habitat subsidies.
Explicit in the definition of resource subsidies has
been the idea of recipient benefit. We follow Polis et al.
(1997) in defining subsidies as any movement of energy
and materials across a habitat boundary that provides
benefit to a recipient consumer. Although not implicit or
required by this definition, the vast majority of studies
have supposed that cross-habitat subsidies move predominantly into less productive systems, and there
strongly influence abundance and distribution of
consumers (Polis & Hurd 1996; Sears, Holt & Polis
2004; Paetzold, Bernet & Tockner 2006). This premise
is based on the assertion that passive dispersal or
movement will occur by diffusion from areas of higher
to lower density, and that these flows will have strong
effects in lower productivity recipient habitats, and by
extension negligible effects in productive recipient
habitats (Sears et al. 2004). Indeed, examples of strong
effects of resource subsidies in low productivity
688
environments are well known, particularly in deserts, dry
L. B. Marczak & coastlines and arctic systems (Polis & Hurd 1996). In Polis &
J. S. Richardson Hurd’s (1996) island food webs, marine algae and carrion
beached on the shores of small, very dry islands
supported extremely large populations of detritivorous
arthropods that formed greater than 90% of the food
available to web-building spider populations. Spiders
were 1–2 orders of magnitude greater in abundance than
in similar areas without detrital inputs. Marine-derived
material has similarly been found to subsidize coyotes
along desert coastlines in Baja, California (Rose & Polis
1998). Similarly, emerging aquatic insects have been
found to affect the growth and fitness of lizards on dry
cobble bars in California (Sabo & Power 2002) and to
alter the distribution of ground-dwelling arthropods on
low productivity gravel bars in Italy (Collier et al. 2002;
Paetzold et al. 2006).
How do consumers respond to subsidies in highly
productive recipient habitats? It has been supposed that
the effect of subsidies arriving in high productivity
habitats will be small in magnitude. However, empirical
studies in such habitats are scarce – researchers have
understandably focused on systems with strong edges
and where the ability to detect a response to subsidies is
correspondingly large. The emphasis on studying
systems where strong responses to resource subsidies
are anticipated has limited our ability to ascertain the
variables that determine the strength of responses, or to
appreciate the ubiquity of subsidy effects.
Aquatic-terrestrial contrasts have been popular in
studies of subsidy effects, at least in part because of the
distinct boundary between these habitats. In particular,
the study of forest contributions to headwater streams
was fruitful long before it was framed in the context of
resource subsidies (e.g. Mason & Macdonald 1982;
Jackson & Fisher 1986; Richardson 1991). More recent
investigations have highlighted the potential contribution of streams to forest habitats in the form of salmon
(Wipfli 2005), algal mats (Bastow et al. 2002), and
Table 1. Comparison of physical and hydrological characteristics of East Creek and
Spring Creek. Mean ± 1 standard error
East Creek
Spring Creek
Gradient (%)*
1·9
1·8
Elevation (m asl)
Watershed area (ha)
Channel wetted width (m) (mean ± SE)*
Mean water depth (m) (mean ± SE)
Mean velocity during experiment (m s–1)
Mean annual discharge (L s–1)†
Substrate size (% distribution ± SE)‡
Sand and silt (< 2 mm)
Gravel (2–64 mm)
Cobble (64–130 mm)
154
35·0
2·4 ± 0·2
0·18 ± 0·01
< 0·14
32 ± 3
160
44·0
3·0 ± 0·6
0·14 ± 0·02
< 0·10
n/a
6·3 ± 1·3
70·3 ± 3·0
22·3 ± 3·7
70 ± 10·8
26·3 ± 9·7
3·75 ± 1·3
emerging aquatic invertebrates (Sanzone et al. 2003).
Recipient consumers for these subsidies include riparian
vegetation (nutrient addition from salmon carcasses),
invertebrates (decomposer fauna for carcasses, algae
and detritus) and spiders, birds, bats and similar
organisms (emerging aquatic invertebrates). In keeping
with the suppositions above, such work has focused on
systems with large contrasts in donor to recipient primary productivity and strongly oligotrophic recipient
habitats. In this study, we conducted a manipulative
field experiment to test whether the abundance of
emerging aquatic insects affected the distribution and
abundance of riparian web-building spiders in a highly
productive rainforest of coastal British Columbia,
Canada. Given the high net primary productivity of the
recipient habitat at our study site, we predicted that the
response of web-building spiders to aquatic insect
subsidy exclusion would be small and limited to those
spiders with a strong dependence or specialization on
adult aquatic insects.
Methods
STUDY SITE
The field experiment was conducted from May through
July of 2004 in two similar headwater streams (Spring
Creek and East Creek; Table 1) within the Malcolm
Knapp Research Forest (MKRF; 49° 18'40"N,
122°32'40"W). The forest is located in the Pacific
coastal rainforest of south-western British Columbia.
Average mean air temperature ranges from a low of 2 °C
in January to a high of 16 °C in July. Precipitation is
approximately 2500 mm annually. More than 70% of
this precipitation falls between October and March. The
coastal temperate rainforests of British Columbia are
substantially more productive (above-ground NPP
estimated at 1050-1300 g C m–2 year-1 from a model
calibrated for the MKRF, Forest Ecosystem Modelling
2006) than the headwater streams that flow through
them (production of algal biomass estimated at 3·64 g C
m–2 year-1; data adapted from Kiffney, Richardson &
Feller 2000). The dominant vegetation surrounding these
streams included red alder Alnus rubra and vine maple
Acer circinatum with a canopy composed largely of
western hemlock Tsuga hetero-phylla, western redcedar
Thuja plicata and Douglas-fir Pseudotsuga menziesii.
Understorey vegetation immediately adjacent to the
streams consisted of 1-2 m tall shrubs, particularly
salmonberry Rubus spectabilis and huckleberry
Vaccinium ovatum. The immediate riparian cover of
East Creek is more strongly deciduous than Spring
Creek, with large numbers of red alder dominating the
stream banks.
FIELD EXPERIMENT
*Kiffney, Richardson & Feller 2000. †J.
Caulkin, unpublished data. ‡Boss &
Richardson 2002.
Between 16 May and 19 May 2004 two greenhousetype exclosures were constructed on each of the two
689
Spiders and
subsidies
Fig. 1. (a) Upstream exclosure along 50 m of East Creek, Malcolm Knapp Research Forest (photo credit Y. Zhang). (b)
Diagrammatic representation of exclosure placement and experimental design.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76, 687–694
streams in the MKRF (Fig. 1a). Exclosures were constructed from transparent plastic sheeting supported by
semicircular PVC frames that were anchored to the
banks. The edges of the plastic sheeting were partly dug
into the stream bank to form a complete seal over the
streambed. Each exclosure covered a 50 m long stream
reach, and was separated by 50 m long stream reaches
that served as controls. Controls and exclosures alternated from the upstream direction (Fig. 1b).
W e sampled orb-weaving spider abundance by using
timed vegetation shake samples (Costello & Daane
1997). We used a 0·3 m2 tray with steep sides and shook
vegetation directly over this tray for 20 s. Individual
spiders were removed from the tray using an aspirator
and stored in 75% ethanol until identified. Orb-weaving
spiders were collected in this fashion in the week prior
to construction of the exclosures and every week for 10
weeks following construction of the exclosures with
four subsamples taken in the middle 15 m of each reach
within 2 m of the stream wetted edge, two on each side
of the stream (Fig. 1b). Precise collecting locations
within a reach varied between weeks. The abundances
of flying aquatic and terrestrial insects were estimated
each month by sticky trap sampling. Traps were composed of Tanglefoot (The Tanglefoot Company, Grand
Rapids, MI, USA) thinly spread on one side of an acetate sheet (each sheet represents a 600 cm2 surface area)
and suspended between two garden stakes approximately
1·5–2 m above the ground facing the stream in roughly
the same locations as spider shake samples. Sticky trap
samples were set for 7 days in the middle of each month
(May, June and July), and collected samples were
frozen until sorted.
Adult spiders were sorted and identified to species.
Insects were identified to Order, or to Family in the case
of Diptera, and assigned to either an aquatic or
terrestrial group based on published life-history details
(Merritt & Cummins 1996). Length and width measurements of insects were determined with an optical
micrometer to the nearest 0·01 mm. Biomass estimates of
spiders were based on measurements of the length of the
tibia-patella of the first pair of walking legs (Higgins
1992). We used published length-mass regression equations to determine biomass of spiders and aquatic and
terrestrial insects (Rogers, Hinds & Buschbom 1976;
Sample et al. 1993; Sabo, Bastow & Power 2002).
STATISTICAL ANALYSES
Repeated measures and nested designs involve spatial
and temporal autocorrelation that violate assumptions of
independence of data points necessary for conventional
general-linear modelling (Buckley, Briese & Rees
2003). We used mixed-effects models that can account
for the correlated error structures present in our data. By
combining both repeated measures and spatially nested
random effects in a general linear mixed effects
(GLME)
model
we
mitigate
problems
of
nonindependence and pseudoreplication - the combination of random spatial effects and repeated measures
made the use of this technique necessary.
The abundance and biomass of flying aquatic and
terrestrial insects were each analysed using repeated
measures ANOVA with treatment (ambient and reduced
insects) and stream (East and Spring Creeks) as main
factors, date as the repeated measure (three sampling
periods) and sticky trap samples as replicates. As
multiple samples from each 50 m stream segment were
not independent, these data were combined to expand
the total area of habitat sampled (four subsamples in
each stream segment combined into one weekly sample,
n = 8 per sampling period) for both insect and spider
abundances. We also used repeated measures ANOVA
with the abundance of all spiders as the response variable,
treatment and stream as factors and date (10 sampling
periods) as the repeated measure. Only adult spiders were
utilized in statistical analyses as the identification of
juveniles is less reliable. Subsequent repeated measures
690
L. B. Marczak &
J. S. Richardson
ANOVAs were performed separately for the most abundant spider families (five families each representing > 5%
of total abundance). We applied a sequential Bonferroni procedure to correct for multiple tests. Stream was
considered a random factor in all models as this has the
advantage of using fewer degrees of freedom. We used
the Satterthwaite approximation to estimate denominator degrees of freedom for both fixed and random
effects as recommended by Schabenberger & Pierce
(2002). The hypothesized time correlation structure used
for these models was heterogeneous autoregres-sive (i.e.
correlation between samples is assumed to decrease as
separation in time increases). The assumption of a
correct covariance model was examined using a
likelihood ratio test (with a x2 distribution) against
models with compound symmetry. Heterogeneous
autoregressive was the better covariance model for all
insect and spider data. We also used likelihood ratio tests
to assess the contribution of the two spatial correlation
parameters included as random factors (stream and the
stream by treatment interaction). For each model, we
first checked that the assumptions of normally distributed data and linearly related fixed-effects means
were met by examining residual vs. predicted plots and
normal probability plots. All data required ln transformation to meet these assumptions. All analyses were
conducted using PROC MIXED in the statistical package
SAS v 9·0 (SAS Institute Inc., Cary, NC, USA).
Results
FLYING AQUATIC
ABUNDANCE
AND
TERRESTRIAL
INSECT
The greenhouse cover significantly reduced the abundance and biomass of flying insects of aquatic origin in
exclusion reaches relative to control reaches (abundance, F1,5·23 = 15·07, P < 0·01; biomass F1,2·1 = 16·35, P
= 0·05; Table 2; Fig. 2a). Adult aquatic insect biomass
in the exclusion reaches was 55·9% lower than in
control reaches when all dates were combined while
adult aquatic insect abundance was 62·9% lower. Flying
terrestrial insect abundance and biomass were
unaffected by the exclusion treatment (abundance,
F1,5·36 = 0·08, P = 0·79; biomass, F1,5·82 = 0·02, P = 0·89;
Table 2; Fig. 2c). Neither time, stream nor the treatment
by stream interaction were significant factors for either
aquatic or terrestrial insects, although there was a trend
towards overall greater abundances of emerging aquatic
invertebrates at East Creek (deciduous canopy). There
was no significant change in terrestrial insect abundance
or biomass over the sampling period. In control reaches
(representing ambient conditions) flying aquatic insects
were 6·49 times more abundant than flying terrestrial
insects across the entire sampling period and had 4·25
times greater biomass. This pattern did not change over
the sampling period; there was no evidence of
alternating peaks in abundance between these two prey
sources over the 3-month study period (Fig. 2b,d).
SPIDER DENSITY
There was no effect of future exclosure site, stream or
the stream by exclosure site interaction on spider
abundance in the week prior to construction of experimental exclosures (effect of future exclosure site: F1,5 =
0·50, P = 0·51). A total of 26 spider species, representing
nine families were collected during the experiment
(Table 3). The experimental reduction of aquatic insects
depressed the overall abundance of spiders adjacent to
exclusion reaches (treatment, F1,16·1 = 11·59, P < 0·01).
There was no significant effect of time or the interaction
of time and treatment. The random effect of stream was
not significant across all adult spiders and there was no
significant interaction between stream and treatment,
although there was a trend towards greater overall
spider abundance at East Creek. Five families were
present in abundances large enough to merit further
analyses
(Araneidae,
Hahniidae,
Linyph-iidae,
Tetragnathidae, Theridiidae, each representing > 5% of
total abundance). Repeated measures ANOVAs for mean
abundances of the most common families showed that
four of the five families included in the analysis were
significantly depressed by the exclusion of aquatic
insects (Table 4; Fig. 3). There was no
Table 2. Repeated measures ANOVAs for mean of abundance and biomass per trap (n = 8) of flying aquatic and terrestrial insects.
Contributions of random effects (stream, stream x treatment) to the model were assessed using a %2 test (d.f. = 1) of the difference
in residual log likelihood for the full and reduced model. Significant P-values are highlighted in bold text
P
Flying aquatic insects
Biomass
Abundance
Test
Flying terrestrial insects
Effect
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76, 687694
P
Test
Treatment
Time
Time × treatment
Stream
Stream × treatment
F1,5·23 = 15·07
F2,9·99 = 3·46 F29·99
= 4·25 %2 = 0
z2 = 0
Abundance
P
0·01
0·07
0·06
1·00
1·00
F12·1 = 16·35
F2,13·5 = 0·87
F2,135 = 1·00
%2 = 0 Z2 =
0·9
0·05
0·44
0·39
1·00
0·34
Test
F 1,5·36 = 0·08
F2,10·3 = 0·09
F2,10·3 = 0·57 %2
=0
z2
=0
P
Biomass
Test
0·79
0·92
0·58
1·00
1·00
F1,5·82 = 0·02
F2,109 = 0·15
F2,10·9 = 0·72 %2
=0
z2 = 0
0·89
0·87
0·51
1·00
1·00
691
Spiders and
subsidies
Aquatic
invertebrates
July
June
control exclosure
y
(d)
control exclosure
Terrestrial
(c)
60
2
40
1-8
•S35
16
I 30
1-4
£25
8 20 a
1-2
E 15 o
1
to 10
5
08
0-6
0-4
0-2
0
0
control
e
-A
i
xclos 9
ur
\ /v
■,
i~~ i
control exclosure
I
Density [ins ects/tr
45
invertebrates
— 50
12
CO
I,40
^
E 30
CO
E 20
m 10
0
May
Fig. 2. Effect of exclosure treatments on the (a) overall mean biomass and density of aquatic invertebrates (b) monthly mean
biomass of aquatic invertebrates at control (filled bars) and exclosure (open bars) reaches (c) overall mean biomass and density of
terrestrial invertebrates and (d) monthly mean biomass of terrestrial invertebrates at control (filled bars) and exclosure (open bars)
reaches. Values are least-squares means (± 1 standard error for the individual lsmean relative to zero).
Table 3. List of families and species of vegetation-dwelling spiders collected at Spring Creek and East Creek in the Malcolm Knapp
Research Forest indicating relative percentages (%) of abundance
% of total
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76, 687–694
Trap type
Family
Species
Vertical orb webs
Araneidae
Araneus nordmanni
Active hunters (with silk retreat)
Dwarf sheet-webs
Clubionidae
Hahniidae
Sheet-webs
Linyphiidae
Active hunters (no web)
Active hunters (no web)
Horizontal orb webs
Philodromidae
Salticidae
Tetragnathidae
Tangle-webs
Theridiidae
Hackled orb webs
Uloboridae
Araniella displicata
Cyclosa conica
Larinioides sclopetarius
Clubiona pacifica
Cryphoeca exlineae
Dirksia cinctipes
Helophora sp.
Linyphiid morphospecies
Microlinyphia mandibulata
Neriene digna
Pityohyphantes costatus
Walckenaeria kochi
Philodromus rodecki
Salticid spp.
Tetragnatha versicolor
Metellina curtisi
Emblyna peragrata
Enoplognatha ovata
Pholcomma sp.
Theridiid morphospecies
Rugathodes sexpunctatus
Theridion varians
Hyptiotes gertschi
abundance (adults)
0·14
0·01
0·14
4·8
3·5
0·9
4·1
3·8
0·3
5·2
1·0
3·7
0·3
1·7
0·1
1·7
14·2
0·3
7·0
0·1
0·1
43·3
0·4
3·3
692
L. B. Marczak &
J. S. Richardson
Table 4. Results of separate repeated measures ANOVAs for mean abundance of adult spiders in five families each representing
> 5% of total spider abundance. Contributions of random effects (stream and stream by treatment) to the model were assessed
using a χ2 test (d.f. = 1) of the difference in residual log likelihood between the full and reduced model. Significant P-values are
highlighted in bold text. All P-values were adjusted using a sequential Bonferroni procedure
Araneidae
Treatment
Time
Time × treatment
Stream
Stream ×
treatment
Hahniidae
Linyphiidae
^ 1
a
£0.8
P
Test
P
Test
P
Test
F1,18·9 = 9·38
F,34·4 = 0·82
F934·4 = 0·75
< 0·01
0·61
0·75
1·00
0·75
F1,26·9 = 17·45
F9,33·4 = 1·28
F9,33·4 = 1·00
< 0·01
0·28
0·46
0·40
0·40
F1,15·4 = 4·53
F9,37·7 =
2·04
F9,37·7 = 0·82
0·05
0·06
0·60
0·04
0·08
F1,19·8 = 4·69
F9,36·2 = 2·22
F9,362 = 0·83
χ2 = 0 χ2 =
0·1
χ2 = 0·7 χ2
= 0·7
(0
■ control □ exclosure
T
*
Theridiidae
Hahniidae
*
Araneidae Tetragnathidae Linyphiidae
£.0.6
Fig. 3. Effect of aquatic insect exclosure on
the abundance of spiders in five families.
Stars indicate significant differences
0
between control and exclosed reaches. Values are
least-squares means (± 1 standard error for the individual
lsmean relative to zero).
W
g 0.4
Q 0.2
significant interaction between stream and treatment for
any of the spider families. Tetragnathids did significantly decrease in abundance over the sampling period
(F9,36·2 = 2·22, P = 0·04), while only linyphiids showed a
family level difference in abundance between the two
streams (P = 0·04). Hahniids and araneids showed the
largest magnitude responses to aquatic insect exclusion,
being 89·1% and 85·7% lower in exclosure reaches
relative to control reaches, while linyphiids and tetragnathids were 50·1% and 42·9% lower, respectively.
Discussion
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76, 687694
Theridiidae
Test
1.4
ST 1-2
E
Tetragnathidae
This study demonstrates that predators in highly
productive terrestrial habitats can respond strongly to
trophic subsidies. Most previous studies have focused
on the case where local production is largely absent and
consumers are obligately dependent on allochthonous
contributions. For example, Paetzold et al. (2006) noted
that large differences in productivity, such as occurred
at their river cobble bar study site, should result in greater
transfers of energy from donor to recipient habitats (via
incorporation of subsidies by recipient habitat dwelling
consumers). They found that ground-dwelling
arthropods showed a substantial numerical response to
the exclusion or addition of drifting and emerging
aquatic invertebrate subsidies. Polis & Hurd (1995)
found that, in most years allochthonous marine
χ2 = 4·1 χ2 =
3·8
χ2 = 1·0
χ2 = 0·1
P
0·04
0·04
0·59
0·32
0·75
Test
F1,17·9 = 1·20
F9,32·9 =
1·75
F9,329 = 0·58
χ2 = 2·2 χ2 =
0·1
inputs controlled the dynamics of web-building spiders
on dry Gulf of California islands – allowing large
populations of consumers to persist despite terrestrial
primary productivity fluctuations. These and other
empirical results have led to an assumption that the
effects of subsidies will only be significant when
recipient primary productivity is lower than that of the
donor system. Our results are the first to test that
assumption in a highly productive terrestrial setting.
Although yearly aquatic NPP was substantially lower
than terrestrial NPP, the average emerging aquatic
insect abundance was 5·9 times higher than terrestrial
insects. This indicates that assumptions about subsidy
movements based purely on ratios of NPP may be
misleading. Large subsidies (relative to terrestrial production) of emerging aquatic insects occurred despite
low stream NPP. This is perhaps not entirely surprising
given the well-known relationship between secondary
production in these headwater streams and detrital
inputs (from the surrounding forest). In these systems it
appears that detrital inputs from the forest to streams is
driving growth and development of aquatic invertebrates, which feeds energy back into the surrounding
forest. Within the stream environment, these detrital
inputs may be converted to insect biomass at a substantially higher rate than would occur for the equivalent
material on the forest floor (Shurin, Gruner & Hillebrand 2006). Streams may therefore be important
bioreactors for converting relatively recalcitrant forest
litter into energy sources that are available to higher
trophic levels in terrestrial settings.
Results from our system showed that spiders in
diverse families, with widely divergent web morphologies and capture techniques, tracked aquatic insect
subsidies for some portion of their diet. In their study of
the effects of aquatic insect exclusion on riparian
spiders in Horonai, Japan, Kato et al. (2003) found that
horizontal orb weavers were noticeably affected while
vertical orb-weaving and sheet-web weaving spiders
were not. They attributed this result to the different
feeding strategies implied by the web morphologies and
thus prey preferences of these distinctive families.
Sheetweb weavers (Linyphiidae) have a high investment
in three-dimensional web structures that make it
P
0·29
0·12
0·81
0·14
0·75
693
Spiders and
subsidies
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76, 687–694
costly to move in order to track spatially and temporally
ephemeral resources. Vertical orb weavers (Araneidae)
construct large vertical webs that are structurally more
suited to catching larger, faster-flying terrestrial prey
(Olive 1982; Foelix 1996). In contrast, the large open
webs and nonsticky silk of horizontal orb weavers are
often viewed as adapted to the capture of small or
weakly flying insects (Olive 1982) and represent a lower
investment that may promote resource tracking. The
insect exclusion in this study generated a response in a
larger number of spider groups, including those that are
not associated with resource tracking of aquatically
derived insects. This unexpected pattern of response by
nonspecialists on aquatic resources suggests that, in the
riparian habitats of the MKRF, adult aquatic insects
play a disproportionately large role in determining the
distribution of many web-building spiders. This may be
particularly true when subsidy resources form a large
fraction of total available resources or more broadly
when the ratio of subsidy to equivalent local resources is
greater than 1. The high abundance of aquatic insects
evidently supports groups of spiders with a broader
range of capture techniques than may be occurring
where aquatic insects form a much smaller proportion of
the overall prey base.
Recent studies have emphasized the importance of
alternating periods of productivity between habitats,
creating seasonally reciprocal flows of energy (Nakano
& Murakami 2001; Takimoto, Iwata & Murakami 2002;
Kato et al. 2003). At the interface between streams and
forests, the seasonal emergence of aquatic insects may
be temporally offset from the time of maximum
secondary terrestrial productivity – influencing the
distribution and abundance of generalist consumers such
as riparian spiders (Kato et al. 2003) and birds (Nakano
& Murakami 2001; Uesugi 2002). Terrestrial
invertebrate production should be greatest during the
spring and early summer as deciduous trees leaf out,
coniferous trees put on new growth and understorey
vegetation is flush. While previous studies have shown
strong variability in the relative availability of aquatic
and terrestrial insect prey, this pattern was not detectable in the 3 months (spring through mid-summer) of
this experiment. In our study, availability of emerging
aquatic insect prey was always greater than terrestrial
insect abundance in the riparian forest. It seems probable that, in the highly productive rainforests of the
Pacific Northwest, emerging aquatic insects are more
abundant than flying terrestrial invertebrates at most
times in the year. However, this production and export
of material to the riparian forest is itself a consequence
of terrestrial detrital inputs. The high secondary productivity of headwater streams in this region supports a
diverse group of invertebrate predators. This secondary
productivity is itself created by the higher trophic
efficiency within streams, based on terrestrially derived
materials indicating that for small headwater streams
and their adjacent forests, the land–water boundary is
particularly porous.
Conclusions
In our system, existing theory predicted that responses
to subsidy exclusion would be weak, or constrained to
family groups known to specialize on aquatic insects as
a subsidy resource. Contrary to this expectation, the
overall abundance of several spider families decreased
with subsidy exclusion, including families not thought
to be particularly sensitive trackers of aquatic insect
abundance. This suggests that even in highly productive
settings, specific subsidy types can have important
effects on fauna. Although allochthonous resources may
indeed contribute close to 100% of productivity in some
habitats (e.g. headwater streams, caves, snow-fields,
islands, etc.; Vanni et al. 2004), the importance of
subsidies appears nearly as great in habitats with
substantial in situ primary productivity, such as that
described here.
This study provides direct evidence that the local
distribution of multiple families of riparian orb weavers
can be controlled by changes in inputs of emerging
aquatic insects, particularly when that input to adjacent
terrestrial habitats is sufficiently large compared with
equivalent terrestrial resources (terrestrial insects). The
high relative abundance of aquatic insects in headwater,
temperate rainforest streams may impact riparian food
web dynamics particularly where terrestrial insect
production is limited, even though riparian forest
primary productivity is relatively high. Subsidy effects
appear to be largest when they subsidize a system with
comparable resources that are at low levels – the pool of
labile or available carbon is often not equivalent to the
overall contrast in donor and recipient habitat primary
productivity, particularly when the focal consumer is a
predator. The development of predictions about where
subsidies are likely to produce the greatest effects in
recipient habitats will require more specific studies that
examine the nature of the subsidy relative to the nature
of available resources in the recipient habitat.
Acknowledgements
W e thank Yixin Zhang, Deirdre Leard, Conan Phelan,
Tatiana Lee, Trent Hoover and other members of the
Stream and Riparian Research group (StaRR) for
assistance in the field and lab. Ross Thompson and
Rebecca Best provided statistical guidance. The authors
acknowledge funding assistance from the Natural
Sciences and Engineering Research Council (Canada)
and the Forest Sciences Program (British Columbia).
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Received 28 September 2006; accepted 28 February 2007