- Top of page
- Materials and Methods
- Strength of Tropic Interactions and Environmental Gradients
- Supporting Information
Plant productivity, or the shades of green in the world, is limited by abiotic factors such as light, temperature and precipitation, and biotic factors such as herbivory and the biotic cycles that determine nutrient availability. Herbivores and predators are also limited by abiotic factors such as temperature and precipitation (Hodkinson, 2005). The close relationship between plant productivity and strength of trophic interactions was summarized by the Hairston, Smith and Slobodkin (HSS) hypothesis which proposed that herbivores control plant populations and predators in turn control herbivores; thus predation on herbivores increases plant biomass through the depletion of plant consumers (Hairston et al., 1960). However, it is not just predators that control herbivores; the apparent verdant tropical and temperate forests are actually primarily brown by weight (i.e. trees are primarily composed of woody lignin and cellulose) (Polis, 1999). Further, there is also population control of herbivores through plant defences that either limit resources to herbivores or force them to cope with a wide array of defences. Control of herbivores by predators is thought to increase towards the equator (Jeanne, 1979; Dyer & Coley, 2002); however, the traditional notion that control of herbivores by plant defences is stronger in the tropics (i.e. Coley & Aide, 1991) has been recently challenged by a thorough meta-analysis (Moles et al., 2011). However, this study found a latitudinal gradient in which the effect of alkaloids on herbivores was stronger at tropical latitudes.
Biogeographically, evidence suggests that trophic cascades are stronger in aquatic ecosystems (Strong, 1992; Polis, 1999; Halaj & Wise, 2001). In terrestrial ecosystems, Oksanen et al. (1981) argued that predators may be able to regulate herbivores in productive ecosystems but fail to do so in the most unproductive, arctic and alpine ecosystems (i.e. the ecosystem exploitation hypothesis EEH). However, empirical evidence has generated controversy on the EEH hypothesis: Borer et al. (2006) reviewed research on trophic cascades and found that herbivore biomass declined and plant biomass increased in the presence of predators, regardless of the productivity levels of the ecosystem. In contrast, a recent literature review on effects of intraguild predation on the ability of intermediate predators to control herbivores found this relationship was not dependent on latitude but was dependent on primary productivity, hence supporting EEH (Mooney et al., 2010).
Spatial and temporal heterogeneity in abiotic factors, such as climate, can often alter the deterministic outcome of interactions between plants, herbivores and predators (Andrewartha & Birch, 1954; Menge & Sutherland, 1976; Hunter & Price, 1992). The varying effect of climate on the strength of interactions makes it difficult to determine if weak bottom-up or top-down control of trophic interactions is due to a biotic factor or the conditions at the particular location where the interaction is studied (Ovadia & Schmitz, 2004). In addition, when responses of individual species are studied, factors such as plant phenology and metabolic rates are known to change across the species geographic range (Fox & Morrow, 1981; Hodkinson, 2005).
The distribution of herbivore abundance and their ability to outbreak is not necessarily a function of bottom-up and top-down forces but is confounded by the climatic conditions determining variations in plant quality, plant defences and predation at a landscape scale (reviewed by Gripenberg & Roslin, 2007). Despite of all these efforts to understand variation in trophic cascade strength, how global climatic gradients will affect trophic interactions remains elusive.
Global warming is perhaps the most dramatic anthropogenic disturbance to natural ecosystems (Thomas et al., 2004). Effects of climate change have already been documented as shifts in species geographical distribution (e.g. Parmesan & Yohe, 2003; Chen et al., 2009). However, in order to understand the magnitude of the effect and possible biological feedbacks is important to understand how changes in temperature and precipitation will affect the biology of organisms. Predictions of how trophic interactions will change are not straight forward since high thermal tolerance is similar for ectotherms across latitudinal gradients (Addo-Bediako et al., 2000). Thus, unprecedented temperatures in rain forests and the narrow temperature tolerance ranges of tropical organisms increases the risk of biotic attrition in the lowland rain forests (Deutsch et al., 2008; Colwell et al., 2008). In the face of climate change, increasing our understanding of the effects of global climate gradients on trophic interactions is imperative.
Landscape and global level studies of plant–herbivore–predator interactions are rare because of the difficulties in conducting species exclusions simultaneously at different sites. In this case a meta-analysis where location and strength of trophic interactions are recorded and analysed may enable testing for the climatic effects on strength of interactions across broad spatial scales (Cooper, 1998). Here I review publications on trophic cascades published in the past 50 years and georeference each study's location in order to address how global temperature and precipitation gradients affect trophic interactions between plants, herbivores and predators. Further, I ask if the same climatic factors facilitating primary productivity are correlated with stronger trophic interactions.
- Top of page
- Materials and Methods
- Strength of Tropic Interactions and Environmental Gradients
- Supporting Information
In this meta-analysis, five out of the six trophic interactions studied exhibited significant relationships across MAT, TAP or both climatic gradients (Table 3). Latitude explained 79% of the variation in MAT, (Fig. 2a); hence correlations between strength of trophic interactions and MAT were not independent from latitude. Thus, relationships between MAT and the strength of trophic interactions may be caused by factors covarying with latitude. For instance, tropical interactions may have had longer historical and coevolutionary time than those trophic interactions occurring in temperate ecosystems (Schemske et al., 2009). In contrast, only 35% of the variation in TAP was explained by latitude, with the greatest variation in TAP found at tropical latitudes (Fig. 2b); hence correlations between TAP and strength of trophic interactions were less dependent on latitude than the correlations between MAT and latitude.
Responses of plant growth to resources were stronger in warm and wet ecosystems (Figs 3a & 4a); empirical studies also demonstrate that adding resources to plants consistently resulted in enhanced growth or increased biomass (e.g. Gruner et al., 2008). My finding that plants at a global scale accumulate more biomass in environments with high MAT and TAP is in concurrence with multiple global studies in which primary productivity was found to be a function of both temperature and precipitation (Woodward et al., 1995; Knapp & Smith, 2001). However I also show a plant's responses to added resources depend on the latitudinal location of the studies (tropical/temperate) and the duration of the manipulations (Appendix S2, Fig. S1). This may mean that tropical plants are generally more limited by nutrient and light availability than plants in temperate soils (Chadwick et al., 1999; Reich & Oleksyn, 2004). Warm temperatures were also associated with stronger control of herbivores as suggested by (1) stronger negative effects of predators (Fig. 3c) and (2) stronger negative effects of plant defences (Fig. 3f) at biomes with high temperatures. Stronger herbivore control at higher temperatures, typical of tropical latitudes, provides some insight into the greater dietary specialization of herbivores observed at tropical latitudes (Dyer et al., 2007), since the tri-trophic niche concept states that herbivores, by specializing, would not only cope better with stronger plant defences (Cornell & Hawkins, 2003) but would also gain enemy free space (Singer & Stireman, 2005). Damage by herbivores was highest in wet ecosystems (Fig. 3b and Appendix S2 & S3b) but this effect depended on whether entire herbivore communities or single species were studied (Appendix S2, Table S3). This interaction may be due to a bias in the number of studies conducted with specialist versus generalist herbivores. Single species studies generally concern effects of specialists whereas entire communities of herbivores concern the global damage of herbivores on plants.
Top-down trophic cascades and predation were strongest in ecosystems with MAT > 25 °C and TAP > 2000 mm year–1 (Figs 3 & 4c,d); suggesting that climatic conditions of rain forests, favoured ant activity so that rain forests had the strongest suppression of herbivore damage, and a positive effect on plants. The effectiveness of ants in controlling herbivore damage in these ecosystems may explain why there is a higher proportion of plants investing in nutrient rewards such as food bodies and nectar in rain forests (Rosumek et al., 2009). Interestingly, top-down trophic cascades were also strong in cold and dry ecosystems (Table 3); strong top-down effects may thus not only be a result of high MAT and TAP but also extreme environments harbouring specialist interactions whose exclusion may have stronger top-down effects (Rodríguez-Castañeda, 2009). The interaction between duration of the top-predator exclusions and strength of top-down trophic interactions and TAP (Appendix S2, Fig. S4) call for long term exclusions of top-down predators in places with high annual precipitation so that we can determine whether the strong top-down control observed at TAP > 2000 mm is due to the climatic conditions or the strong immediate response of plants to top predator exclusions.
No climatic or latitudinal trend was found in bottom-up trophic cascades (Figs 3 & 4f), which may be due to the high number of secondary factors that may play a role in this interaction and the low sample size. In fact, bottom-up trophic cascades were stronger in dry ecosystems in which perhaps lower predation, competition and plant defences due to the harsh climatic conditions allow herbivores to take advantage of the effect that adding resources has on plants.
Plant defences increased with MAT (Fig. 3f and Appendix S2, S2f). Even though warmer temperatures enabling plants to invest more in defences to have a stronger negative effect on herbivores cannot be ruled out, it is more likely that stronger effects of defences on herbivore biomass is a result of warm ecosystems containing plants with stronger toxins, such as alkaloids, that negatively affect herbivore biomass (Moles et al., 2011).
Results from this study also provide partial support for the ecosystem exploitation hypothesis, which predicts predation to be highest in sites with climatic conditions favouring high primary productivity (Oksanen et al., 1981) and is consistent with experimental findings of predation being stronger under high primary productivity conditions (Forkner & Hunter, 2000; Gruner et al., 2008). However top-down trophic cascades in this study were also strong the lower end of the primary productivity gradient. Some of the strongest top-down control studies at low temperatures were studies conducted with plant–ant interactions (i.e. Warrington & Whittaker, 1985; Kelly, 1986). Even though, more studies would need to confirm this theory; ant–plant interactions may become more important at extreme temperature/precipitation regimes.
These results have relevancy when thinking about ecosystem changes under future climate regimes. For instance, control of herbivore abundance by predation and plant defences is predicted to increase in warmer conditions (Table 3c,f); this effect will be detrimental to herbivore taxa whose diversity peaks in tropical montane ecosystems such as geometrids (Brehm et al., 2005), where species thrive because of lower predation (Rodríguez-Castañeda, 2009). Experimental studies on the direct effect of temperature and precipitation on animal physiology and its effects on strength of trophic interactions are needed in order to distinguish effects of climatic variation from the effects trophic interactions on plants. For instance, from 2000 to 2009, global plant primary productivity was reduced as a response to increased drought in the southern hemisphere (Zhao & Running, 2010). These results make specific predictions on herbivore and predator performance under dry conditions (Fig. 4b,c); however, the question of what is the relative contribution of NPP versus the physiological effects of drought on herbivore and predator populations remains open.
According to Hillyer & Silman (2010), low seed predation allowed Amazonian trees to migrate upslope. It would be interesting to study the effects of having Amazonian plants with increased plant defences and higher predation rates on the herbivore communities currently living in the upslope Andean forests. In temperate zones, increased trophic interactions as a result of warming may also affect the geographic distribution of species. For instance, the composite Arnica montana is currently restricted in its altitudinal distribution by slug herbivory (Bruelheide & Scheidel, 1999); so that stronger control of herbivory would allow the species to expand its altitudinal distribution. Moreover, changes in strength of trophic interactions will likely affect the distribution of the holly leafminer Phytomiza ilicis since current geographical variation in host plant quality and parasitism rates rank as the main determinants of its geographic distribution (Brewer & Gaston, 2003; Gaston et al., 2004). These are some the studied examples that show the importance of understanding how climate impacts trophic interactions and the geographic distribution of plant species. Further, results from this study show that globally, trophic interactions are strongest in tropical ecosystems where species have high niche conservatism, small geographic ranges (Crisp et al., 2009), and are physiologically sensitive to changes in temperature regimes (Addo-Bediako et al., 2000; Deutsch et al. 2008).
Literature synthesis is the most feasible tool to understand how global climatic gradients affect strength of interactions. However, while literature syntheses can detect hidden correlations, this approach cannot estimate the magnitude of the effects of climatic gradients on the strength of trophic interactions since they are bound to be subject to other driving factors (Cooper, 1998). Therefore these results should be used to guide macroecological experiments that add knowledge to some of the patterns found in this study. A novel aspect of this study was georeferencing the studies from which measurements were taken because trophic interactions observed in individual experiments could then be placed in a spatially explicit framework.
Ideally the effect size of strength of trophic interactions observed under specific environmental conditions could be used to explore how trophic interactions affect the geographic distribution of species and the plasticity of functional traits in plants, herbivores and predators across their geographical distributions. Further, expected climate change and the strong effects of MAT and TAP on trophic interactions make it imperative to incorporate effects on ecological interactions to understand the impact of global warming not only on future biodiversity but also on crop production.