Elucidating the Relationship Between Indirect Effects and Ecosystem Stability

Jessica Robbins
University of California Berkeley Department of Molecular and Cell Biology
Motivation
As global temperatures rise, extreme weather events become frequent, and human settlement encroaches into previously undisturbed areas, it is clear that the worlds ecosystems are in a precarious position. As such, the importance of understanding which factors support ecosystem stability in the face of environmental change cannot be understated.

Methodology
We begin by constructing a model food web according to the niche model algorithm established by Williams and Martinez. Of the resultant networks, those containing no basal species, predators who did not ultimately derive their biomass from basal species, and segmentation are eliminated. Self-cycling is not permitted. Networks were created containing 5, 10, and 15 species, and with expected connectance of levels of .10, .15, .20, .25, and .30. 10 networks with each combination of parameters were created. The biomass of each species changes according to the following set of differential equations: For basal species: =
=

Results

Conclusions
There is a strong correlation between an ecosystems connectance and its indirect effects ratio. This means that it will be difficult to delineate the effects of these factors in future studies and invites the possibility that stability previously ascribed to connectance may also be due in part to indirect effects. In addition, indirect effects may be a more informative descriptor of ecosystem behavior, as it takes both structure and dynamics into account. Both indirect effects and connectance can help promote ecosystem stability. However, this is not a guarantee that ecosystems with the highest indirect effects ratio or highest level of connectance will always be the most stable or vice-versa. In contrast, increasing the abundance of basal species tends to promote ecosystem instability. Increasing the size of the network tends to both promote instability and increase the range of ecosystem response to perturbation. These results may be due in part to a discrepancy between empirical and simulated ecosystems. The study of ecosystem dynamics is at its heart a deeply holistic science, and as such it is difficult---and possibly ill-advisedto analyze the effects of one variable in isolation.

Background
A number of factors play a role in shaping ecosystem stability. In 2000, McCann posited the insurance hypothesis, which claims that species diversity can give rise to functional diversity within ecosystems, making the system more stable to environmental change. Predator-prey body mass ratios are also known to have an influence on ecosystem stability, with the most stable ratios being between 10 and 100 for ectotherm vertebrates and between .1 and 10 for invertebrates. Connectivity is also known to promote stability, especially in the presence of weak interactions. According to the principle of the weak interaction effect, food webs that exhibit a high proportion of weak interactions tend to be more stable than those that do not.
Connectance Indirect Effects System Size

For consumer species:

() ()

The relationship between indirect effects ratio and mean of the norm difference of biomass for all networks, indicating the presence of a relationship between indirect effects ratio and stability. Red shades indicate 15-species networks, green 10 species, and blue 5 species.

Stability Body Sizes

Where Bi is the biomass of species i, xi is its mass-specific metabolic rate, yij is the maximum ingestion rate of prey species j by predator species i, eij is the fraction of biomass of species j lost due to consumption by species i that is actually metabolized, Gi(B) is the normalized growth rate of primary producer species, and Fij(B) is the functional response of consumer species i and resource species j. Once network dynamics had reached steady state, one species was chosen at random and its biomass was multiplied by a factor between 0 and 5. The perturbed network was then allowed to go to steady state, and the norm biomass difference between the original and altered networks was calculated. This process was repeated 50 times for each network. The indirect effects ratio for each network was calculated according to the following formula:
+ + ] [ = = = =

= +
=

References
1. Allesina, S., Tang, S., 2012. Stability criteria for complex ecosystems. Nature 483, 208-208. 2. Bellingeri, M., Cassi, D., Vincenzi, S., 2013. Increasing the extinction risk of highly connected species causes a sharp robust-to-fragile transition in empirical food webs. Ecological Modeling 251, 1-8.

The relationship between indirect effects and connectance for all networks. There is a strong positive correlation between the two metrics. However, the existence of many high connectivity, low indirect effects networks indicates that the indirect effects of a network, which take the weights of flows into account, may be more informative measures of ecosystem behavior

3. Brose, U., 2008. Complex food webs prevent competitive exclusion among producer species. Proceedings of the Royal Society B: Biological Sciences 275, 2507-2514. 4. Brose, U., Williams, R.J., Martinez, N.D., 2006. Allometric scaling enhances stability in complex food webs. Ecology Letters 9, 1228-1236. 5. Dunne, J.A., Williams, R.J., Martinez, N.D, 2002. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology Letters 5, 558-567. 6. Grimm, V., Schmidt, E., Wissel, C., 1992. On the application of stability concepts in ecology. Ecological Modeling 63, 143-161. 7. Kalinkat, G., Scheider, F.D., Digel, C., Guill, C., Rall, B.C., Brose, U., 2013. Body masses, functional responses and predator-prey stability. Ecology Letters 1-9. 8. Lin, Y., Sutherland, W.J., 2013. Color and degree of interspecific synchrony of environmental noise affect the variability of complex ecological networks. Ecological Modeling 263, 162-173. 9. Ma, Q., Kazanci, C., 2012. Analysis of indirect effects within ecosystem models using pathway-based methodology. Ecological Modeling 252, 238245. 10. Martinez, N.D., Williams, R.J., Dunne, J.A., 2005. Diversity, complexity, and persistence in large model ecosystems. Santa Fe Institute. 11. McCann, K.S., 2000. The diversity-stability debate. Nature, 405 228-233. 12. Rall, B.C., Guill, C., Brose, U., 2008. Food-web connectance and predator interference dampen the paradox of enrichment. Oikos 117, 202-213. 13. Rip, J.M.K., McCann, K.S., 2011. Cross-ecosystem differences in stability and the principle of energy flux. Ecology Letters, 14 733-740. 14. Williams, R.J., 2008. Effects of network and dynamical model structure on species persistence in large model food webs. Theoretical Ecology 3, 285-294. 15. Williams, R.J., Anandanedesan, A., Purves, D., 2010. The probabilistic niche model reveals the niche structure and role of body size in complex food webs. PLoS ONE 5, e12092. 16. Williams, R.J., Martinez, N.D., 2000. Simple rules yield complex food webs. Nature 404, 180-183. 17. Williams, R.J., Martinez, N.D., 2004. Stabilization of chaotic and non-permanent food-webs dynamics. European Physical Journal B 38. 297-303. 18. Woodward, G., Ebenman, B., Emmerson, M., Montoya, J.M., Olesen, J.M., Valido, A., Warren, P.H., 2005. Body size in ecological networks. Trends in Ecology & Evolution, 20 402-409

Basal Species

If indirect effects, flows of energy or matter between species that have a path length greater than one, can be thought of as a type of weak interaction, it is conceivable that an abundance of indirect effects may promote ecosystem stability as well.

.5

.5

Where Gij is the fraction of species js flow material that goes directly to species i, Ti is all the flow material species i obtains by consuming other species plus all the flow material i obtains from the environment, and fij is the rate of direct flow from species j to species i. .25 A visualization of indirect effects: If 50% of Species As flow material goes to Species B, who in turn gives 50% of its flow material to Species C, the indirect flow between Species A and Species C is .25 Inference from confounding variables was minimized by grouping networks by connectance value, number of species, and abundance of basal species prior to analysis. Similar distributions of body mass ratio and functional response were maintained throughout the simulations.

The relationship between basal species abundance and mean of the norm of the biomass difference. The positive correlation between these two metrics runs somewhat contrary to traditional biological thought, and may point to a disparity between empirical ecosystems and computational methods

Objective
Investigate the connection between the indirect effects ratio of an ecosystem and the degree of its response to environmental perturbation.

Acknowledgements
This work would not have been possible without the advice and support of Dr. Caner Kazanci, Qianqian Ma, Dr. Rosalyn Rael, Dr. Kevin Lafferty, Dr. Alice Boit, Linh Huynh, The University of Georgia, and The Mathematical Biosciences Institute.

Inquiries can be directed to Jessica Robbins at jmrobbins92@gmail.com

The relationship between system size and stability. The finding that increased system size increases the variability in system response indicates that larger ecosystems may be more sensitive to variables such as connectance, indirect effects ratio, and basal species abundance than smaller systems.