(93)

J. Env. Bio-Sci., 2018: Vol. 32 (1):93-98 ISSN 0973-6913 (Print), ISSN 0976-3384 (On Line)

IMPACTS OF ALTERED PRECIPITATION ON SPIDER MEDIATED TROPHIC CASCADE

Kashmeera N. A. and Sudhikumar A. V.*
Centre for Animal Taxonomy and Ecology, Department of Zoology, Christ College, Irinjalakuda, Kerala, 680125
[Corresponding author*:avsudhi@rediffmail.com]

Received: 06-04-2018 Accepted: 16-04-2018

Planet earth is facing unprecedented changes like a warmer atmosphere, a warmer and more acidic ocean, higher sea levels, and
larger changes in precipitation patterns. The magnitude and stability of ecosystem functioning are likely to be significantly altered
by these changes. Here, alteration in litter decomposition rate mediated by spider Pardosa sumatrana was studied in the field
under manipulated rainfall conditions. Results of this study indicate that changes in rainfall patterns can alter the rate of litter
decomposition mediated by spiders. Understanding how organisms provide ecosystem services to humans is essential for
continued ecosystem development.
Key words: Trophic cascade, Altered precipitation, Spider

Climate change projections show that global annual
precipitation rate will rise significantly, due to the pronounced
rainfall events in tropical and high-latitude regions (IPCC, 2013).
Projected ramifications of climate change also show that these
changes have the potential to aggravate the water scarcity in
some areas, but mitigate them in others (Arnell, 1999). Many
studies show that these changes in climate altering the
structure and functioning of tropical ecosystems, as it is in
the rest of the world (Corlett, 2012). Ecosystem functions or
processes are the biological, geochemical and physical
processes and components that take place or occur within an
ecosystem (Maynard et al., 2010). These processes such as
productivity, decomposition, nutrient cycling, fluxes of nutrients
and energy are indispensable for the welfare of mankind. So
understanding how alterations happen to ecosystem functions
is key to efforts to foresee all the consequences of climate
change (Millennium Ecosystem Assessment, 2005).
Ecosystem processes like decomposition and recycling of
nutrients plays critical role in maintaining persistence and
stability of ecosystem through continuous productivity.
Decomposition also plays key role in pedogenesis, energy
release to higher trophic levels and successive perpetuation
of faunal and floral diversity (Swan and Kominoski, 2012). The
soil and leaf litter constitutes a spatially diverse habitat for soil
faunal community, which plays vital role in decomposition of
litter. Besides the abundance and diversity of soil fauna
especially fungi, bacteria and invertebrates (Swift et al. 1979;
Seastedt, 1984; Gonzalez and Seastedt, 2001) the rate of
decomposition of the leaf litter is also determined by several
factors including the climatic and seasonal conditions (García-
NAAS Rating (2017)-4.43
Palacios et al.2013) and the physical and chem ical
composition of leaves (Aerts, 1997; Meentemeyer, 1978;
Cleveland et al. 2006; Kaspari et al. 2008; Guendehou et al.
2014).
Regular and consistent cycling of nutrients is also necessary
for maintaining sustained productivity of natural ecosystems
(DeBano et al., 1998). Through decomposition and
mineralization a vast variety of organisms enable nutrient
cycling. This process enables an adequate and balanced
supply of several key elements like Carbon, Phosphorous,
Nitrogen, Sulphur which are essential for life (Millennium
Ecosystem Assessment, 2005).
Maintenance of these ecosystem functions are of paramount
importance because it is found that the areas with better
functioning of ecosystems can also contribute the perpetual
supply of ecosystem services, which are vital for the survival
of human beings (Maynard et al., 2010).
Climate change studies on fungi, bacteria and invertebrates
like protozoans, nematodes, annelids, arthropodsetc are
significant since they are the prime mediators of important
ecosystem processes, such as litter decomposition and
nutrient cycling (Seastedt, 1984). A review on invertebrate
response to climate change indicates that climate change
can affect ecosystem services by altering invertebrate
populations (Prather et al., 2013). Invertebrates deserve more
attention because they dominate several niches and are the
most abundant and diverse animal group (Brusca and Brusca,
2002).
 KASHMEERA AND SUDHIKUMAR (94)

Despite their ecological importance soil arthropods like spiders roaming in the field with cocoons attached to spinnerets
are comparatively ill-considered under climate change (Sebastian and Peter, 2009).
perspective. Many investigations have revealed that the
Litter preparation was done by collecting fallen leaves of different
influence of spiders as predators could cascade through detritus
plant species from the floor of the study site. To make the
based food web, indirectly affecting ecological process like
experiment more realistic, mixture of canopy-species leaves
litter decomposition. For example, a short-term study
reflecting their abundance were used to make litter bags.
conducted in deciduous forest showed that spider removal
Petioles and any hard veins of the leaves were disposed and
from forest-floor resulted in increased numbers of collembolans
the rest was broken into roughly 2 cm diameter pieces. Then
there by increasing the rate of litter loss, whereas a long term
the litter was air dried to a constant weight before use. Ten
study reported opposite effect (Lawrence and Wise,
grams of leaf litter were weighed and filled in 2 mm nylon
2000;Lawrence and Wise, 2004). Another study showed that
mesh bags (15X10 cm).
higher rainfall decreased the strength of the trophic cascade
mediated by spiders (Lensing and Wise, 2006). Liu et al. 2014 Three 4X3 m2 experimental plots were established in the Herbal
observed negative trophic cascade effects on litter garden. They were assigned to three rain fall treatments:
decomposition mediated by spiders under drought conditions. Heavy, Low and Ambient. Each 4X3m 2 plot was divided into
These studies indicate the chances for radical changes in eight 0.5m2 subplots and half of it was assigned as high density
ecosystem processes as a result of intense hydrological cycle plots and other half as low density plots. Each subplot was
predicted to occur with global climate change. fenced with 50 cm aluminium flashing, with 10cm buried under
ground. Rains out shelters were constructed over the High
The purpose of field experiments reported here was to reveal
and low rainfall plots and ambient rainfall plots were left
the response of an important ground dwelling Asian spider
uncovered. Rainout shelters were made of PVC frame topped
Pardosa sumatrana (Thorell, 1890) to predicted changes in
by a funnel of uncoated polyethylene that direct the rainwater
climate. Changes in litter decomposition rate mediated by
into a PVC pipe that diverted it away from the plot. These
spider were studied under altered rainfall conditions. These
rainout shelters are removable and were removed at the time
experiments also yield information about response of
of rainfall treatment. Shelters extended by 0.25m on each side
collembolans to altered precipitation and spider density.
beyond edge of the subplots.
MATERIAL AND METHODS
One litterbag was placed at the centre of each subplot and
This study was conducted in Herbal Garden at Christ college,
was covered with leaves. Each high density subplots stocked
Irinjalakuda, Kerala (10o23'N, 76o11'E). This region has a humid
with 4 spiders and low density plots with 2 spiders. Spiders
tropical climate. Annual precipitation averages 2469 mm. Mean
were collected by handpicking method. Rainfall treatments
annual air temperature ranges from 25.3oC to 30.8oC. The mean
were done for two months. The plots were irrigated using a
relative humidity is 86.7 %. Canopy is composed mainly of
hand held watering can. Low rainfall plots were irrigated in
Anacardium occidentale, Azadrachta indica, Tectona grandis,
alternating weeks so that it received 30% below the mean
Swietenia mahagoni and Aegle marmelos. The study area was
rainfall of last five years and high rainfall plots were irrigated
gifted with scrub jungle, open grassland and mixed type
weekly so that it received rainfall 30% above the mean rainfall
plantation. It is also endowed with a well littered floor, which
of last five years. Ambient rainfall plots were left un-irrigated.
encourage the thriving of wandering spiders like Lycosids. Spider
Pitfall traps were used at the beginning and end of rainfall
used in this study is Pardosa sumatrana (Thorell, 1890). It is
treatments to measure activity density of collembolans. Pitfall
an active hunting spider common in grasslands. They are also
traps were 7 cm deep, 6cm diameter plastic containers. The
found abundant in damp leaf litter and are the most dominant
traps were buried in the soil such that the upper rim was at the
spiders in the study site. They are ground runners, which
level of ground. Following Gisin, (1960), 20ml of fixing fluid
mainly feed on ground layer of the field and rarely come to the
(14.52ml alcohol, 4.84ml ether, 0.58ml glacial acetic acid and
foliage or canopy of plants for prey capture. Females range 8-
0.058ml formalin (40%)) was added to each trap to prevent the
10mm in size and males 6-8mm. Sometimes females are seen
(95) IMPACTS OF ALTERED PRECIPITATION ON SPIDER MEDIATED TROPHIC CASCADE
collembolans from escaping.
Activity densities (number per trap) of collembolans were
measured at the beginning and end of experiment using pitfall
traps. Traps were opened for 24 hour period before and after
the experiment. Then the samples were taken to laboratory
for counting and calculating activity density.
Three months after rainfall treatment, litterbags retrieved from
each subplot were sealed in plastic bags and immediately
taken to lab. Any mud or debris on the litterbags were removed
gently. After that, litterbags were dried in oven at 60OC to a
constant weight. Remaining mass was noted to calculate
percentage litter loss and Trophic Cascade Index. Trophic
Cascade Index was calculated following Lensing and Wise,
(2006.)
Trophic cascade index = rate at natural spider density - rate
at low spider density
rate at low spider density
where, rate is the rate of litter disappearance calculated by
averaging proportion of litter disappearance in all replicates of
each spider density treatment.
Statistical analyses: First a two-way analysis of variance
(ANOVA) was conducted to study the influence of two
independent variables (Rainfall, Spider density) on the activity
density of Collembola. Rainfall included three levels (High
rainfall, Low rainfall, Ambient rainfall) and Spider density
consisted of two levels (High density, Low density).
Then to determine if varying levels of rainfall and spider density
effect percentage of litter loss, a two-way Analysis of variance
was performed.
RESULTS AND DISCUSSION
Impact of rainfall and spider manipulation on activity
density of Collembola: A two-way analysis of variance was
conducted on the influence of two independent variables
(rainfall, spider density) on the activity density of collembola.
All effects were statistically significant at the 0.05 significance
level except for the activity density. The main effect for rainfall
yielded an F ratio of F (2, 18) = 90.49, p = 4.06e-10, indicating
a significant difference between high rainfall (M = 13.625, SD
= 3.23), low rainfall (M = 8.43, SD = 3.31) and ambient rainfall
(M = 2.5, SD = 1.035). The main effect for spider density
yielded an F ratio of F (1, 18) = 32.88, p =1.95e-05, indicating
significant difference between high density (M = 6.25, SD =
4.37) and low density (M = 10.125, SD = 5.92). The interaction
effect was not significant, F(2, 18) = 3.31, p = 0.059 (Table 1)
as natural densities may change according to rainfall but
experimental density of spiders do not. Activity density of
collembolans was higher in high rainfall plots compared to low
and ambient rainfall plots (Fig.1)
Table 1: Two-way analysis of variance on the influence
of rainfall and spider density on the activity
density of collembola.
Source SS df MS F p
Between groups
18.1875 2 9.09375 3.319392 0.059276
Within groups
49.3125 18 2.739583
Total 653.4063 23
Fig.1: Impacts of different rainfall treatments (HR-High
Rain fall, LR- Low Rain fall,AR- Ambient Rain
fall) on activity densities of Collembolans.
Collembola can play a crucial role via their impacts on the
primary and most common decomposers of litter in many
ecosystems which are the saprophytic fungi. Presence and
density of Collembola depend on environmental factors, such
as humidity, temperature, organic matter and their predators
(such as spiders). There was marked environmental variation
between the different habitats, following the modification
gradient. Plot location had little impact on Collembola
abundance or activity. Number of Pardosa spider were
successfully manipulated. Densities of Pardosa were not
affected by rainfall treatment. Altering rainfall affected
Collembola densities and also by the spider treatment. The
 KASHMEERA AND SUDHIKUMAR
activity density of Collembolans was higher in high rainfall plots,
with the highest in high rainfall, low density plot followed by
high rainfall high density plot. We can also observe a significant
increase in activity density of Collembolans in the low rainfall
low density plot (Fig.1). This may be due to reduced predatory
risk from spiders.
Fig. 2: Effect of spider manipulation on activity density
of collembolan
In marked contrast, differences in Spider density had little
impact on overall Collembola densities. The activity density of
Collembolans was observed higher in low density plots than
high density plots (Fig. 2). But also a marked increase of
activity density can be observed in high density high rainfall
treatment plot. The interaction effect was not significant as
natural densities may change according to rainfall but
experimental density of spiders do not as it is manipulated or
controlled.
Effect of different rainfall treatments and spider density
on percentage of litter loss: Different levels of rainfall
treatments and density of spiders affected the percentage loss
of litter in different ways. A two-way analysis of variance on the
influence of two independent variables (rainfall and spider
density) on the percentage loss of litter was conducted. All
effects were statistically significant at the 0.05 significance
level except for the percentage of litter loss. The main effect
for tainfall yielded an F ratio of F (2, 18) = 152.85, p = 5.08e-
12, indicating a significant difference between high rainfall (M
= 28.94, SD = 3.21), low rainfall (M = 12.42, SD = 8.42) and
ambient rainfall (M = 2.88, SD = 3.13). The main effect for
spider density yielded an F ratio of F (1, 18) = 30.36, p =3.12e-
(96)
05, indicating significant difference between high density (M =
18.14, SD = 11.17) and low density (M = 11.35, SD = 12.68).
The interaction effect was significant, F(2, 18) = 10.89, p =
0.0079 (Table 2).
Table 2 : Two-way analysis of variance on the
influence of rainfall and spider density on the
percentage loss of litter.
Source SS df MS F p
Between groups
198.3965 2 99.19826 10.89756 0.000792
Within groups
163.8503 18 9.102796
Total 3421.542 23
Fig. 3: Percentage loss of leaf litter under different
treatment levels of rainfall (HR-High Rain fall,
LR- Low Rain fall,AR- Ambient Rain fall)
Effect of different rainfall treatments on percentage of
litter loss: Changes in the behavior, abundance, and predator/
prey interactions of spiders and Collembola could have
important consequences for this system by impacting rates
of leaf-litter decomposition. The percentage of litter loss was
higher in the high rainfall high density plot followed by the low
density high rainfall plot. Increased rainfall likely increased
fungal growth, leading to higher rates of reproduction by
Collembola, and possibly higher collembola survival rates. There
was also a marked increase in percentage of litter loss in the
high density low rainfall plot. Suggesting that limited resources-
water or food led them to be active regardless of predation
(97) IMPACTS OF ALTERED PRECIPITATION ON SPIDER MEDIATED TROPHIC CASCADE

risk. The percentage of litter loss was observed minimum in
the ambient rainfall low density plot (Fig. 3) due to low moisture
availability.
Understanding and predicting the climate change impacts on
ecosystem processes is essential for planning mitigation
efforts to reduce vulnerability to climate change. For the
continued ecosystem development a clear understanding of
how organisms provide ecosystem services to humans and
how these organisms will be altered with a changing climate
is needed. This study meets this need to a great extent.

ACKNOWLEDGEMENTS

Authors are grateful to late Fr. Dr. T. M. Jose, CMI, Principal,

Christ college, Irinjalakuda, Kerala for the support and
encouragement. We would like to acknowledge all the labmates
for valuable comments and suggestions. We are also grateful
to Kerala State Council for Science, Technology and
Environment for the financial support.
Fig. 4: Percentage loss of leaf litter under different spider
densities (HD-High density, LD-Low Density)

Effect of spider density on percentage of litter: After the

litter addition, most of the subplots in experiment contained
an average amount of leaf litter. Addition of litter to the plots
may have decreased the ability of wolf spiders to prey on smaller
individuals like collembola. Likewise, this increased habitat
complexity could have hampered the ability of wolf spiders to
find and capture Collembola, indicating higher percentage of
litter loss in high rainfall high density plot (Fig. 4). The
percentage of litter loss was also higher in low density high
rainfall plot. The percentage of litter loss was minimum in low
density ambient rainfall plot. This may be as a result of low
moisture availability and low predation risk.
PLATE A: Fenced experimental plots covered
This study shows that climate change induced alterations in with Rainout shelters
availability of water can significantly affect the interaction
strength between spiders and its prey. It also reveals that
changes in precipitation patterns can alter the rate of litter
decomposition mediated by spiders. The result of this and
other studies (Lawrence and Wise,2000,2004, Shultz et al.
2006, Liu et al. 2014) denote that spiders affect litter
decomposition rates indirectly by reducing number of
collembolans.While this study indicates an increase in litter
decomposition rate with increase in spider density, certain
studies have reported opposite effect (Lawrence and
Wise,2000; Kajak et al., 1991; Kajak, 1997). This may be due
to the difference in duration of experiment or peculiarity of
study site. Plate B: Subplot fenced with Aluminium flashing
 KASHMEERA AND SUDHIKUMAR (98)

REFERENCES 15. Guendehou, G.S., Liski, J., Tuomi, M., Moudachirou, M., Sinsin, B.
and Makipaa, R.(2014). Decomposition and changes in chemical
1. IPCC (2013). In: Climate Change 2013: The Physical Science Basis.
composition of leaf litter of five dominant tree species in a West
Contribution of Working Group I to the Fifth Assessment Report of
African tropical forest. Trop Ecol, 55(2), 207-220.
the Intergovernmental Panel on Climate Change Cambridge University
16. DeBano, L.F., Neary, D.G. and Ffolliott, P.F. (1998). Fire effects on
Press, Cambridge, United Kingdom and New York, NY, USA.
ecosystems.John Wiley & Sons.
2. Arnell, N.W. (1999). Climate change and global water resources.
17. Prather, C.M., Pelini, S.L., Laws, A., Rivest, E., Woltz, M., Bloch,
Global Environ. Chan., 9, S31-S49.
C.P., Del Toro, I., Ho, C.K., Kominoski, J., Newbold, T.A. and Parsons,
3. Corlett, R.T. (2012). Climate change in the tropics: the end of the
S. ( 2013). Invertebrates, ecosystem services and climate change.
world as we know it?. Biol. Conser., 151(1), 22-25.
Biol. Revi., 88(2), 327-348.
4. Maynard, S., James, D. and Davidson, A.(2010). The development
18. Brusca,R.C. and Brusca, G. J. (2002). In: Invertebrates.Second
of an ecosystem services framework for South East Queensland.
Edition.Sinauer Associates, Sunderland.
Environ. Manag., 45(5), 881-895.
19. Lawrence, K.L. and Wise, D.H. ( 2000). Spider predation on forest-
5. Millennium Ecosystem Assessment (2005). In: Ecosystems and
floor Collembola and evidence f or indirect effects on
Human Well-being: Biodiversity Synthesis. World Resources Institute,
decomposition.Pedobiologia, 44(1),33-39.
Washington, DC.
20. Lawrence, K.L. and Wise, D.H. (2004). Unexpected indirect effect
6. Swan, C.M. and Kominoski, J.S. (2012). In: Biodiversity and
of spiders on the rate of litter disappearance in a deciduous
ecosystem function of decomposition. eLS.
forest.Pedobiologia, 48(2), 149-157.
7. Swift, M.J., Heal, O.W. and Anderson, J.M. (1979). In: Decomposition
21. Lensing, J. R., and Wise, D. H. (2006). Predicted climate change
in terrestrial ecosystems (Vol. 5). Univ. of California Press.
alters the indirect effect of predators on an ecosystem process.
8. Seastedt, T.R.(1984). The role of microarthropods in decomposition
Proc. Natl. Acad. Sci. USA103: 15502-15505.
and mineralization processes. Annual Rev. Entomol., 29(1), 25-46.
22. Liu, S., Chen, J., He, X., Hu, J. and Yang, X. (2014). Trophic cascade
9. Gonzalez, G. and Seastedt, T.R.(2001). Soil fauna and plant litter
of a web-building spider decreases litter decomposition in a tropical
decomposition in tropical and subalpine forests. Ecol., 82(4), 955-
forest floor. Europ.Jour. Soil Biol., 65, 79-86.
964.
23. Sebastian, P. A. and Peter, K. V. (Eds.). (2009). In: Spiders of India.
10. García, Palacios, P., Maestre, F.T., Kattge, J. and Wall, D.H.(2013).
Universities press.
Climate and litter quality differently modulate the effects of soil
24. Gisin, H. (1960). Collembolen fauna Europas (pp. 243-243). Geneva,
fauna on litter decomposition across biomes. Ecol. Lett., 16(8),
Switzerland: Museum d'histoirenaturelle.
1045-1053.
25. Shultz, B.J., Lensing, J.R. and Wise, D.H. (2006). Effects of altered
11. Aerts, R. (1997). Climate, leaf litter chemistry and leaf litter
precipitation and wolf spiders on the density and activity of forest-
decomposition in terrestrial ecosystems: a triangular relationship.
floor Collembola.Pedobiologia, 50(1), 43-50.
Oikos:439-449.
26. Kajak, A., Chmielewski, K., Kaczmarek, M. and Rembialkowska, E.
12. Meentemeyer, V. ( 1978.) Macroclimate and lignin control of litter
(1991). Experimental studies on the effect of epigeic predators on
decomposition rates. Ecol., 59(3), 465-472.
matter decomposition processes in managed peat grasslands. Polish
13. Cleveland, C.C., Reed, S.C. and Townsend, A.R. ( 2006). Nutrient
Ecol. Stud, 17, 289-310.
regulation of organic matter decomposition in a tropical rain forest.
27. Kajak, A. (1997). Effects of epigeicmacroarthropods on grass litter
Ecol., 87(2),492-503.
decomposition in mown meadow. Agricul., Ecosys. Environ., 64(1),
14. Kaspari, M., Garcia, M.N., Harms, K.E., Santana, M., Wright, S.J.
53-63.
and Yavitt, J.B. (2008). Multiple nutrients limit litterfall and
decomposition in a tropical forest. Ecol. Lett., 11(1), pp.35-43.