Transcript Slide 1

The good, the bad, and the slimy:
Analyzing the net ecological effects of invasive slugs on an urban forest
Hillary Z.G. Lauren* & W. Lindsay Whitlow
Department of Biology, Seattle University, 2009
Introduction
Invasive species often have striking primary negative effects on native species, in such a manner that secondary effects
can be overlooked. Some studies have shown that although invasive species impact new ecosystems negatively, they can
also have positive secondary effects, for example by increasing selective pressures on natives and driving evolutionary
diversification (Vellend, 2007) or controlling the presence of other invasive species through competition (Zavaleta, et al.
2001).
Terrestrial mollusks can have negative and positive effects on ecosystems. Slugs have been found to have negative
effects on seedling establishment (Scheidel, 2005; Hanley 1995), vegetation biomass and diversity (Buschmann 2004)
and positive effects on litter consumption and nutrient cycling (Jennings and Barkham 1979). Specifically, Arion spp.
consumed approximately 8.4% of leaf litter input in a Virginia forest (Jennings and Barkham 1979) and their mucus and
feces significantly increased nutrient leeching from beech leaf litter and microbial biomass (Theenhaus, 1996a). Other
studies suggest higher abundances of slugs increase soil invertebrate populations (Ferguson, 2004), which can positively
affect understory plants through increased nutrient availability. As an example, plants increased growth rates in soil with
bacteria and nematodes compared to bacteria alone because of increased nitrogen availability (Ingham et al. 1985).
Although these studies stress the importance of either negative (herbivory) or positive effects (increased litter
decomposition and nutrient leeching), few studies have simultaneously looked at both.
Results
Conclusions
Plant growth analyses
Since the invasive slugs had a significant negative effect on leaf area in plots with high slug densities (Fig. 3)
while positive effects on litter invertebrates (Fig. 5) or nutrients did not differ between plots, we conclude that
A. ater has a negative net ecological effect on M. nervosa. In addition, M. nervosa in plots with low slug
density had more new growth, and therefore higher final number of leaves, compared to those with higher slug
density (Fig. 4a).
Plants in plots where there was a lower slug density showed less herbivory damage than those where slugs had higher densities (Fig. 3). Data
analyses showed that change in leaf area per plant had a significant interaction between site and treatment (p<0.05) but no significant differences for
either main effect. The change in leaf area per leaf showed that slug exclusion plots were significantly different from the none (p<0.005), inclusion
(p<0.01), and control (p<0.05) plots (Fig. 3). Although there was also a significant difference between sites (p<0.01), there was no interaction effect.
Number of branches per plant was inconsistent between high and low slug density (Fig. 4a), but number of leaves per plant was highest in plots of
low slug density (Fig 4b). There was a significant difference between treatments concerning number of leaves (p<0.05) and branches (p<0.01), but
neither showed significance between sites or an interaction effect. Leaf length showed no significant differences between sites or treatments, and
branch length showed a significant difference between sites (p<0.01) but not treatments.
The final number of branches was significantly higher for Inclusion and Exclusion plots when compared to
None plots (Fig. 4a). This same significance was found at the beginning of the experiment (data not shown)
and can only be explained by random chance because the seedlings were planted at random. As M. nervosa
grows, it produces new branches which subsequently have more and more leaves. Therefore a plant with more
branches is more likely to produce a branch with more leaves. While this may be the case, inclusion plots
showed significantly more loss in leaf area than exclusion plots—in other words, the herbivory effect is so
strong that any additional variables produced by number of branches have no significance.
This study attempted to examine the ecological impacts of an invasive slug on native understory plants to determine the
relative magnitudes of positive and negative effects. Because understory plants benefit from nutrients released into the
soil from slug feces regardless of whether they are a result of herbivory or the consumption of leaf litter, it was
hypothesized that slugs have a positive effect on plants.
Soil and litter analyses
Interestingly, there was a higher relative abundance of litter invertebrates in inclusion plots (Fig. 5a) which
supports previous findings that slugs positively affect the presence of other invertebrates (Ferguson, 2004). The
difference cannot be attributed to the existence of the fence, as the abundances in the Control (with fence) and
None (without fence) plots were very similar.
a
Figure 1. Illustration of the ecological
effects of slugs, including negative such
as herbivory (a) and positive such as litter
decomposition (b), nutrient leeching (c),
and effect on litter invertebrates (d).
b
a
c
b
Percent moisture content did not differ significantly
between treatments or sites. All other measurements
showed significant differences between sites, including
pH (p<0.001), dry leaf litter mass (p<0.001), change in
nitrate (p<0.05), and abundance (p<0.01) and diversity
(p<0.001) of litter invertebrates per gram litter. None of
these showed differences between treatments.
Interestingly, the abundance of invertebrates in the
inclusion plot was relatively high compared to the other
plots (Fig. 5a), though not significantly.
Ten sites were chosen in Seward Park, Seattle. Each site had
four treatment 0.25m2 plots for controlling slug presence
(Figure 2) using fences with or without copper tape. Each plot
had three Mahonia nervosa (Cascade Oregon grape) seedlings.
None: no fence
Experiments in the lab included calculating the consumption
and assimilation rate of fresh M. nervosa leaves and Acer
macrophyllum (Big leaf maple) litter.
Figure 2. Four plot treatments at each
field site. Inclusion and exclusion plots
had copper tape to discourage slugs
from crossing the barrier.
Laboratory experiments
The non-significant differences in dry litter mass indicate that slugs do not consume large amounts of litter, a
fact which is supported by the lab consumption rates (Fig. 4A). More slugs ate leaf litter than those which ate
fresh leaves, suggesting that although the mean consumption of fresh leaves was significantly higher, litter is
more universally palatable among individuals. These conclusions cannot be absolute, because the food types
were presented separately to slugs and preference cannot be determined.
The insignificance for positive effects such as change in nitrate may be explained because it takes more time
before they are evident. Herbivory affects the plant through loss of leaf area and therefore photosynthetic
potential immediately. However, the digestion of plant matter and subsequent “recruitment” of bacteria and
nitrate availability take a longer time to become evident.
Soil and litter analyses
Materials and methods
At the end of the trial period (August 2008 – April 2009),
measurements were taken of
• dry leaf litter mass
• soil pH
• change in soil nitrate
• % soil moisture, and
• litter invertebrate abundance and diversity.
• number and length of leaves and branches
• change in leaf surface area
Figure 4. Effect of slug density on number of leaves and branches per M.
nervosa plant. (a) There was an increasing amount of leaves from none,
inclusion, control to exclusion plots, significant between None and Exclusion
plots (p=0.106). (b) Exclusion plots had a significantly higher number of
branches than None and Control plots but not Inclusion plots (p<0.05).
**p<0.005 *p<0.05
Figure 3. Effect of slug density on change in M. nervosa leaf area
per leaf. There was a significant decline in M. nervosa leaf area in
treatment areas of high slug density. (p<0.05)
***p<0.005 **p<0.01 *p<0.05
d
Plant growth analyses
The greatest difference in plant measurements occurred between None and Exclusion plots, where significant
differences were observed in change in leaf area (Fig. 3, p<0.005), number of branches (Fig. 4a, p<0.005), and
number of leaves (Fig. 4b, p<0.05). Although plots without fences were not significantly different from control
plots, this indicates that the presence of fences has some effect on slug foraging behavior.
Literature cited
Buschmann, H, et al. 2005. The effect of slug grazing on vegetation development and plant species diversity in an
a
b
Figure 5. Effect of slug density on litter invertebrate abundance and diversity.
Inclusion plots showed higher mean litter invertebrate (a) abundance (p=0.421) and
(b) diversity per gram litter than other treatment groups (p=0.731).
Inclusion: slugs enclosed
Laboratory experiments
The slugs showed a significantly higher consumption rate
of fresh leaves than litter (Fig. 6a, p<0.01), and a slightly
higher assimilation rate for leaf litter, though not
significantly (Fig. 6b).
Control: free movement
Exclusion: slugs excluded
a
b
Figure 6. Slug consumption and assimilation rates on leaf
litter and fresh leaves. There was a significantly higher (a)
consumption rate (p<0.01) of fresh leaves than gram leaf litter
per live slug weight per day but no significant differences
concerning (b) assimilation (p=0.223).
experimental grassland. Functional Ecology 19: 291-298.
Hanley, ME, Fenner, M, & Edwards, PJ. 1995. An experimental field study of the effects of mollusk grazing on seedling
recruitment and survival. Journal of Ecology 83: 621-627.
Ingham, RE, et al. 1985. Interactions of bacteria, fungi, and their nematode grazers: Effects on nutrient cycling and plant growth.
Ecological Monographs 55: 119-140.
Jennings, TJ, & Barkham, JP. 1979. Litter decomposition by slugs in mixed deciduous woodland. Holarctic Ecology 2: 21-29.
Scheidel, U & Bruelheide, H. 2005. Effects of slug herbivory on the seedling establishment of two montane Asteraceae species.
Flora 200: 309-320.
Theenhaus, A & Scheu, S. 1996. The influence of slug (Arion rufus) mucus and cast material addition on microbial biomass,
respiration, and nutrient cycling in beech leaf litter. Biology and Fertility of Soils 23: 80-85.
Vellend, M, et al. 2007. Effects of exotic species on evolutionary diversification. Trends in Ecology and Evolution 22: 481-488.
Zavaleta, ES, Hobbs, RJ, & Mooney, HA. 2001. Viewing invasive species removal in a whole-ecosystem context. Trends in
Ecology & Evolution 16: 454-459.
Acknowledgments
We would like to thank the M.J. Murdock Charitable Trust for funding, the Seattle Parks and
Recreation Department for permission to study Seward Park, and our colleagues at Seattle
University, especially John Vincent, for technical and field assistance.
Contact
*Please contact Hillary Lauren at [email protected]. More information on this and
related projects are available at www2.seattleu.edu/scieng/biology/