Michelle Chow
 

Brett, M.T. and C.R. Goldman. 1996. A meta-analysis of the freshwater trophic cascade. Proceedings of the National Academy of Sciences 93:7723-7726.

The authors conducted a meta-analysis of 54 separate enclosure and pond experiments. The results of the data analysis showed that in general zooplanktivorous fish addition resulted in greatly decreasing zooplankton biomass; median=29% of the control value. These treatments also resulted in increased phytoplankton biomass, median=176% of control value. These experiments endeavor to solve the debate by providing unequivocal support for the trophic cascade hypothesis in freshwater ecosystems.

Brett, M.T. and C.R. Goldman. 1997. Consumer versus resource control in freshwater pelagic food webs. Science 275:354-386.

A review paper of previous work on meta-analysis of freshwater communities. The meta-analysis was conducted of 11 fish-by-nutrient factorial plankton community experiments. Results showed that zooplankton biomass was under strong consumer control but was weakly stimulated by nutrient additions. Phytoplankton biomass was under strong resource control with moderate control by fish. Therefore both top-down and bottom-up influences were at work in each freshwater community. Top-down control was stronger at higher trophic levels while bottom-up control was stronger at the base of the food web. They attribute the lack of nutrient control on zooplankton to unpalatable algae which prevent the transfer of the nutrients further up the food chain.

Carpenter, S.R., J.F. Kitchell, and J.R. Hodgson. 1985. Cascading trophic interactions and lake productivity. BioScience 35:634-639.

A review paper of trophic cascade theory and population regulation. All case studies reviewed are freshwater lake systems. The purpose of the paper is to suggest that perhaps knowledge of these regulation patterns can be used in conservation ecology. Enhanced piscivory can decrease planktivore densities, increase grazer densities, and decrease chlorophyll concentrations. The authors state that stocking piscivores has promise as a tool for rehabilitating eutrophic lakes. The concept of trophic cascading links limnology and fisheries biology and suggests a biological alternative for lake management.

 Carpenter, S.R., J.F. Kitchell, J.R. Hodgson, P.A. Cochran, J.J. Elser, M.M. Elser, D.M. Lodge, D. Kretchmer, X. He, and C.N. von Ende. 1987. Regulation of lake primary productivity by food web structure.

Classic paper demonstrating trophic cascade theory in lakes. Whole lake manipulations were performed in Tuesday, Peter, and Paul Lakes near University of Notre Dame. In Paul Lake (the reference lake) productivity varied between years. This demonstrates the effects of physical factors on communities. In Tuesday Lake the addition of bass (top carnivore) and the removal of minnows (primary carnivores) resulted in higher zooplankton biomass and lower phytoplankton biomass compared to control. In Peter Lake, removal of bass and addition of minnows resulted in decreased zooplankton and an initial increase in phytoplankton followed by decrease. The results of Tuesday Lake illustrate the trophic cascade hypothesis however data from Peter Lake is contradictory. The authors’ explanation for Peter Lake is that enough bass remained to effectively eliminate minnow densities, thereby removing the predation pressure on zooplankton and decreasing phytoplankton. Eventually young of the year bass were able to feed on zooplankton and allowed the phytoplankton to increase by the termination of the experiment. The contradictory data and the authors’ explanations make this paper difficult to read. However, it is also cited in almost all trophic cascade papers and is worth struggling through.

Carpenter, S.R. and J.F. Kitchell. 1988. Consumer control of lake productivity. BioScience 38:764-769.

A review paper of the authors’ previous work in 1987. Again the article emphasizes the role of the trophic cascade. In cases where the secondary carnivore was removed, the primary carnivores increased in density causing a decrease in zooplankton and an increase in phytoplankton. Since the authors have shown by their study in 1987 that whole lake manipulations can have predictable results, lake management procedures should be easy to employ.

Estes, J.A. and J.F. Palmisano. 1974. Sea otters: Their role in structuring nearshore communities. Science 185:1058-1060.

A good example of trophic cascades in the marine community, thereby widening the theory to aquatic systems in general. A natural experiment is performed by measuring kelp biomass in areas visited or not visited by otters. Where otters are present, urchins are scarce and kelp becomes plentiful. A lack of otters allow urchins to graze down the subtidal kelp. Although this paper gives, in my opinion, substantial evidence, it still is considered only a "potential" trophic cascade by several ecologists.

Hairston, N. G., F.E. Smith, and L.S. Slobodkin. 1960. Community structure, population control, and competition. American Naturalist 94:421-425.

A classical paper that questions what methods control natural populations not only for a single species but for communities. This paper developed three hypotheses based upon observations and logical statements. 1) Any population which is not resource limited must be limited to a level below that set by resources. 2) Herbivores are seldom food limited and appear most often to be predator limited. 3) Since predators control the populations of herbivores, thereby limiting their own resource, they are food limited. The first hypothesis pertains to all systems where as the last two hypotheses were designed primarily for terrestrial communities.

The authors believed the world was green because predators kept herbivore populations below the level set by primary productivity. This paper is often cited as the beginning theory of trophic cascades and should be read as part of the history of ecology.

Hairston, N.G. Jr., and N.G. Hairston, Sr. 1997. Does food web complexity eliminate trophic-level dynamics? American Naturalist 149:1001-1007.

A reply to Strong’s Are trophic cascades all wet? paper. In contrast to Strong’s view that terrestrial communities are too complex to show general patterns, the authors argue that trophic levels do exist and general interactions occur between them. One pattern can be seen between consumption efficiencies of herbivores in terrestrial and aquatic communities. In aquatic systems, consumption by herbivores is much higher (32%) compared to terrestrial systems (3%). They equate this difference to the role that primary and secondary predators play in the two systems. In freshwater lakes, secondary predators are an important component by reducing the numbers of primary carnivores. This reduces predation pressure on herbivores. In terrestrial communities, secondary carnivores are quantitatively an unimportant part of the mortality of primary carnivores. Primary predation is a major source of herbivore mortality, allowing primary producers to increase. Therefore the authors still find evidence for top down control of communities.

Hunter, M.D. and P.W. Price. 1992. Playing chutes and ladders: Heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724-732.

Prior to this paper, ecologist were in disagreement about whether top-down or bottom-up forces structure a community. The authors propose that the null model used should be donor control with top-down effects superimposed in the case of trophic cascades.

Marquis, R.J. and C.J. Whelan. 1994. Insectivorous birds increase growth of white oak through consumption of leaf chewing insects. Ecology 75:2007-2014.

This study showed that the presence of birds enhances the growth of juvenile oaks in the Ozarks by bird consumption of leaf-damaging insects. Oaks that were caged to exclude birds had two times as many herbivorous insects as control plants. The authors suggest that birds could alter the relative abundance of tree species in any forest where insects affect plant growth and seed production differentially. I think that this study, along with Strong’s current work, are two of the few clear examples of terrestrial trophic cascades.

Mikola, J. and H. Setala. 1998. No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79:153-164.

This experiment tests the trophic cascade hypothesis in a soil food web: predatory nematodes microbivorous nematodes bacterial and fungi. The authors tested for biomass and productivity of each trophic level starting with microbes only and continued as they added higher trophic levels. The strong top-down regulation of microbivore biomass was demonstrated by the reduction of these nematodes in the presence of predators. However the abundance of microbes did not significantly change with an increase in the food chain from 2 to 3 levels. This result might be due to the ability of bacteria to increase production using the excretory products of the nematodes themselves. This would allow microbes to keep pace with an increase in grazing pressure. The authors believe that their study indicates that true trophic cascades of biomass regulation do not frequently appear in decomposer food webs.

Oksanen, L. 1983. Trophic exploitation and arctic phytomass patterns. American Naturalist 122:45-52.

A terrestrial example of an herbivore suppressing above ground phytomasses of tundra communities. A site visited by the herbivore, Lemmus sp., had 5 times the amount of moss meadows as a site not visited by the lemmings. Data taken after a substantial population crash of lemmings showed a 8.4 fold increase in moss phytomass from a previously impoverished site. Although this study is an example of top-down control, the results are based on only a comparison of two sites. Also no mention is made of potential lemming predators, an essential component to investigate before this is classified as a trophic cascade.

Paine, R.T. 1974. Intertidal community structure. Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15:93-120.

This paper coined the phrase "keystone species", a species which upon its addition or removal causes substantial changes in the community. The research examined possible biological and physical factors that could control the zonation of the mussel, Mytilus californianus, in the rocky intertidal. Mytilus californianus is a superior space competitor, therefore any limit to its territory allows higher species diversity. Results showed that the starfish, Pisaster ochraceus, preys on M.californianus thus establishing a lower distributional limit for the mussels. When Pisaster was removed, mussels "migrated" downwards, increasing their habitat and removing inferior space competitors. The author concluded that Pisaster was a keystone species which directly controlled mussel populations and indirectly influenced other intertidal species as well.

Paine, R.T. 1980. Food webs: linkage, interaction strength, and community structure. Journal of Animal Ecology 49:667-685.

A review paper of Paine’s previous work with emphasis on strong and weak species’ interactions. The paper states that the strength or importance of a trophic relationship cannot be assumed equivalent for all web species. Some species will be a strong interactor and will have pronounced effects on the community. An example is Pisaster ochraceus’ predation on Mytilus californianus. Other species will have little or no effect on the community upon removal. Therefore just enumerating links of a food web provides little information on species’ importance or role in the community. What counts instead is the interaction strength of the predator or the competitive stature of the preferred prey. Paine suggests that the next generation of food web ecologists be more sensitive to interaction strength and less so to trophic complexity.

Power, M.E. 1990. Effects of fish in river food webs. Science 250:811-814.

This study involves experimental manipulations of fish in Eel River (Mendocino County) to demonstrate trophic cascades in freshwater systems. The food web under study consisted of California roach and steelhead which feed on predatory insects and fish fry which feed on algivorous chironomid larvae. 12 cages were constructed to allow development of the food web with and without the top carnivores. Results showed that in the presence of California roach and steelhead, algal assemblages were significantly reduced by chironomid infestations. Where fish were excluded, Cladophora glomerata cover was substantial and devoid of chironomids. This
experiment elucidates a four tiered trophic cascade in which primary productivity increases in the presence of a secondary carnivore. The paper is concisely written and has served as a model for classic top-down control.

Spiller, D.A. and T.W. Schoener. 1990. A terrestrial experiment showing the impact of eliminating top predators in foliage damage. Nature 347:469-472.

This paper focuses on the effects of top predators which consume both carnivorous and herbivorous arthropods. Thus unlike a classical trophic cascade, these top carnivores consume not just the nonbasal level below them. Anolis lizards in the Bahamas feed on herbivorous arthropods and web spiders, which also prey on herbivores. The impact on primary production is predicted to be positive if herbivorous arthropods are more prone to be eaten by lizards than spiders and negative if visa-versa. This study seems to contain two possible trophic cascades: lizards spiders insects plants or lizards insects plants. The results showed that overall removal of lizards increased herbivorous scar damage. This paper seems to address Strong’s claim to terrestrial complexity. Predation on multiple trophic levels can have top-down effects depending on the relative strengths of those interactions.

Strong, D.R. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems.

A controversial paper that questions whether control of herbivores is through top-down forces. While the author agrees that top-down forces (trophic cascades) operate in aquatic systems, he disagrees that top-down forces dominate terrestrial communities. Strong brings up four reasons why the original Hairston, Smith, and Slobodkin theory does not apply to terrestrial communities. 1) Simple top-down dominance is not the norm. Instead changes in productivity, availability, or the quality of food have effects which propagate upward. 2) Although the world is green, not all of it is edible. Secondary chemical defenses allow plants to buffer the runaway consumption of herbivores. 3) Neither shifts in vegetation nor energy flow do a trophic cascade make. Even if one plant species is removed by herbivory, several other plant species are able to fill the niche and thus the world remains green. 4) There is insufficient experimental evidence for understanding speciose food webs in any general sense. The evidence that supports trophic cascades in lakes is missing from terrestrial systems. Although in 1997 this paper is still debated, it served its purpose in questioning functional importance of trophic cascades in terrestrial communities.

Strong, D.R., J.L. Maron, P.G. Connors, A. Whipple, S. Harrison, and R.L. Jefferies. 1995. High mortality, fluctuation in numbers, and heavy subterranean insect herbivory in bush lupine, Lupinus arboreus. Oecologia 104:85-92.

Mass mortality of Lupinus arboreus on the Bodega Marine Reserve is caused by root damage from the ghost moth caterpillar, Hepialus californicus. Aerial photographs of the reserve (1955-present) show that several areas have substantial lupine coverage one year only to have 90% of the lupines die two to three years later. This cycle repeats approximately every five years. Other parts of the reserve have consistent lupine cover of about 70%. Studies showed that lupine mortality was correlated with the intensity of ghost moth caterpillars in the roots. Sites with massive die-offs had the highest number of caterpillars where sites with little mortality had few caterpillars. At the highest caterpillar density measured (mean=37.5, maximum=62 caterpillars/root), a stand of L. arboreus suffered 41% mortality. The massive die-offs were not correlated with folivory as leaf damage was nil to moderate in dying stands. Instances where L. arboreus was completely defoliated by the tussock moth, Orgyia vetusta, did not result in mortality but only in the replacement of leaves by secondary growth. This paper begins the investigation of Strong et al. of a potential terrestrial trophic cascade.

Strong, D.R., H.K. Kaya, A.V. Whipple, A.L. Child, S. Kraig, M. M. Bondonno, K. Dyer, and J.L. Maron. 1996. Entomopathogenic nematodes: natural enemies of root-feeding caterpillars on bush lupine. Oecologia 108:167-173.

This paper continues the research of Strong, et al. 1995. The patchy die-offs of Lupinus aboreus on the Bodega Marine Reserve are due to the root boring caterpillar, Hepialus californicus. Prevalence of the caterpillar is controlled by a species of soil dwelling entomopathogenic nematode, Heterorhabditis hepialus. A single nematode after entering the caterpillar kills the host within 48 hours. The nematode begins reproduction, ultimately producing as many as 420,000 offspring in one caterpillar. The authors believe that the nematodes can effectively control H. californicus thereby preventing the die off of lupine. Where the nematodes are absent, L. arboreus cycles between substantial coverage and mass mortality. This study is among the few examples of a potential trophic cascade in a terrestrial community.

Strong, D.R., J.L. Maron, and P.G. Connors. 1996. Top down from underground? The underappreciated influence of subterranean food webs on above-ground ecology. In Food webs: Integration of patterns and dynamics, eds G.A. Polis and K.O. Winemiller, pp 170-175. Chapman and Hall, New York.

Another review article describing Strong’s terrestrial trophic cascade. The main point of the paper is to show how important below ground food webs are to the community. Many below ground species are involved in decomposition and nutrient cycling, among other processes. Although many ecologists have passed over top carnivores located in the soil as potential herbivore controllers, Strong encourages a revisitation of the underappreciated influence of subterranean food webs on above-ground ecology.

Strong, D.R. 1997. Quick indirect interactions in intertidal food webs. Trends in Ecology and Evolution 12:173-174

A small review article that details the indirect interactions in trophic cascades. It covers a lot of material found in his previous work and is not an essential reading for understanding food webs in general. The paper’s intent is to bring awareness to how indirect interactions are now one nexus of contemporary food webs.

Strong, D.R. Submitted to Oecologia. Predator control in terrestrial ecosystems: the underground food chain of bush lupine.

This paper provides circumstantial evidence that the 3 tiered trophic cascade (nematodes, caterpillar, and lupine) has been increased to include nematophagous fungi. This possibly creates a 4 tiered system where the fungi are able to control the nematode populations locally. Studies of fungi consuming the H. hepialus in the laboratory is documented. However since the nematophagous fungi is a generalist and H. hepialus only constitutes a small fraction of nematodes in the soil, it is debated how much of an effect the fungi imposes on the food chain. Further experimental studies need to be done before this fourth level is included in the terrestrial trophic cascade.

Strong, D.R., A.V. Whipple, A. L. Child, and B. Dennis. Submitted to Ecology. Model selection for a subterranean trophic cascade: Root-feeding caterpillars and entomopathogenic nematodes.

While past Strong papers only provided circumstantial evidence for the terrestrial trophic cascade, this paper provides the experimental evidence. Lupinus arboreus seedlings were planted in pots with or without nematodes and with 0, 8, 16, or 32 Hepialus californicus caterpillars (fully factorial design). Seedlings with nematode protection had high probability of survival regardless of caterpillar density. Seedlings without nematodes had increased mortality directly related to number of H. californicus present. Although this paper contains experimental evidence, it also contains advanced statistics and modeling of the data. This makes a majority of the paper difficult to understand without substantial statistical background.