Nathan P. Lemoine

Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales

Losses of corals worldwide emphasize the need to understand what drives reef decline. Stressors such as overfishing and nutrient pollution may reduce resilience of coral reefs by increasing coral–algal competition and reducing coral recruitment, growth and survivorship. Such effects may themselves develop via several mechanisms, including disruption of coral microbiomes. Here we report the results of a 3-year field experiment simulating overfishing and nutrient pollution. These stressors increase turf and macroalgal cover, destabilizing microbiomes, elevating putative pathogen loads, increasing disease more than twofold and increasing mortality up to eightfold. Above-average temperatures exacerbate these effects, further disrupting microbiomes of unhealthy corals and concentrating 80% of mortality in the warmest seasons. Surprisingly, nutrients also increase bacterial opportunism and mortality in corals bitten by parrotfish, turning normal trophic interactions deadly for corals. Thus, overfishing and nutrient pollution impact reefs down to microbial scales, killing corals by sensitizing them to predation, above-average temperatures and bacterial opportunism.

Nutrient supply from fishes facilitates macroalgae and suppresses corals in a Caribbean coral reef ecosystem

On coral reefs, fishes can facilitate coral growth via nutrient excretion; however, as coral abundance declines, these nutrients may help facilitate increases in macroalgae. By combining surveys of reef communities with bioenergetics modeling, we showed that fish excretion supplied 25 times more nitrogen to forereefs in the Florida Keys, USA, than all other biotic and abiotic sources combined. One apparent result was a positive relationship between fish excretion and macroalgal cover on these reefs. Herbivore biomass also showed a negative relationship with macroalgal cover, suggesting strong interactions of top-down and bottom-up forcing. Nutrient supply by fishes also showed a negative correlation with juvenile coral density, likely mediated by competition between macroalgae and corals, suggesting that fish excretion may hinder coral recovery following large-scale coral loss. Thus, the impact of nutrient supply by fishes may be context-dependent and reinforce either coral-dominant or coral-depauperate reef communities depending on initial community states.

Variable effects of temperature on insect herbivory

Rising temperatures can influence the top-down control of plant biomass by increasing herbivore metabolic demands. Unfortunately, we know relatively little about the effects of temperature on herbivory rates for most insect herbivores in a given community. Evolutionary history, adaptation to local environments, and dietary factors may lead to variable thermal response curves across different species. Here we characterized the effect of temperature on herbivory rates for 21 herbivore-plant pairs, encompassing 14 herbivore and 12 plant species. We show that overall consumption rates increase with temperature between 20 and 30 °C but do not increase further with increasing temperature. However, there is substantial variation in thermal responses among individual herbivore-plant pairs at the highest temperatures. Over one third of the herbivore-plant pairs showed declining consumption rates at high temperatures, while an approximately equal number showed increasing consumption rates. Such variation existed even within herbivore species, as some species exhibited idiosyncratic thermal response curves on different host plants. Thus, rising temperatures, particularly with respect to climate change, may have highly variable effects on plant-herbivore interactions and, ultimately, top-down control of plant biomass.

Differing nutritional constraints of consumers across ecosystems

Stoichiometric mismatches between resources and consumers may drive a number of important ecological interactions, such as predation and herbivory. Such mismatches in nitrogen (N) or phosphorus (P) content between resources and consumers have furthered our understanding of consumer behavior and growth patterns in aquatic systems. However, stoichiometric data for multiple consumers from the same community are lacking in terrestrial systems. Here, we present the results of a study designed to characterize nutritional constraints within a terrestrial arthropod community. In order to place our results in a broader context, we compared our data on resource–consumer stoichiometry to those of stream and lake ecosystems. We found that N and P varied among trophic levels, and that high N:P content of herbivores suggests that herbivores might experience strong N-limitation. However, incredibly low P-content of plant foliage leads to potential P-limitation in herbivores that is nearly as strong as potential N-limitation. Moreover, arthropod predators may also be strongly P-limited. In fact, potential nutrient limitation of terrestrial herbivores in our study is similar to nutrient limitation from streams and lakes, suggesting that similar nutritional constraints may be operating across all three study systems. Importantly, our data suggest that consumers in lakes experience a trade-off between N- and P-limitation, while terrestrial consumers experience simultaneous strengthening or weakening of N- and P-limitation. We suggest that P may be overlooked as an important limiting nutrient in terrestrial ecosystems.

Nutrient loading alters the performance of key nutrient exchange mutualisms.

Nutrient exchange mutualisms between phototrophs and heterotrophs, such as plants and mycorrhizal fungi or symbiotic algae and corals, underpin the functioning of many ecosystems. These relationships structure communities, promote biodiversity and help maintain food security. Nutrient loading may destabilise these mutualisms by altering the costs and benefits each partner incurs from interacting. Using meta-analyses, we show a near ubiquitous decoupling in mutualism performance across terrestrial and marine environments in which phototrophs benefit from enrichment at the expense of their heterotrophic partners. Importantly, heterotroph identity, their dependence on phototroph-derived C and the type of nutrient enrichment (e.g. nitrogen vs. phosphorus) mediated the responses of different mutualisms to enrichment. Nutrient-driven changes in mutualism performance may alter community organisation and ecosystem processes and increase costs of food production. Consequently, the decoupling of nutrient exchange mutualisms via alterations of the worlds nitrogen and phosphorus cycles may represent an emerging threat of global change.

Underappreciated problems of low replication in ecological field studies

The cost and difficulty of manipulative field studies makes low statistical power a pervasive issue throughout most ecological subdisciplines. Ecologists are already aware that small sample sizes increase the probability of committing Type II errors. In this article, we address a relatively unknown problem with low power: underpowered studies must overestimate small effect sizes in order to achieve statistical significance. First, we describe how low replication coupled with weak effect sizes leads to Type M errors, or exaggerated effect sizes. We then conduct a meta-analysis to determine the average statistical power and Type M error rate for manipulative field experiments that address important questions related to global change; global warming, biodiversity loss, and drought. Finally, we provide recommendations for avoiding Type M errors and constraining estimates of effect size from underpowered studies.

Asymmetric responses of primary productivity to precipitation extremes: A synthesis of grassland precipitation manipulation experiments

Climatic changes are altering Earths hydrological cycle, resulting in altered precipitation amounts, increased interannual variability of precipitation, and more frequent extreme precipitation events. These trends will likely continue into the future, having substantial impacts on net primary productivity (NPP) and associated ecosystem services such as food production and carbon sequestration. Frequently, experimental manipulations of precipitation have linked altered precipitation regimes to changes in NPP. Yet, findings have been diverse and substantial uncertainty still surrounds generalities describing patterns of ecosystem sensitivity to altered precipitation. Additionally, we do not know whether previously observed correlations between NPP and precipitation remain accurate when precipitation changes become extreme. We synthesized results from 83 case studies of experimental precipitation manipulations in grasslands worldwide. We used meta-analytical techniques to search for generalities and asymmetries of aboveground NPP (ANPP) and belowground NPP (BNPP) responses to both the direction and magnitude of precipitation change. Sensitivity (i.e., productivity response standardized by the amount of precipitation change) of BNPP was similar under precipitation additions and reductions, but ANPP was more sensitive to precipitation additions than reductions; this was especially evident in drier ecosystems. Additionally, overall relationships between the magnitude of productivity responses and the magnitude of precipitation change were saturating in form. The saturating form of this relationship was likely driven by ANPP responses to very extreme precipitation increases, although there were limited studies imposing extreme precipitation change, and there was considerable variation among experiments. This highlights the importance of incorporating gradients of manipulations, ranging from extreme drought to extreme precipitation increases into future climate change experiments. Additionally, policy and land management decisions related to global change scenarios should consider how ANPP and BNPP responses may differ, and that ecosystem responses to extreme events might not be predicted from relationships found under moderate environmental changes.

Climate change may alter breeding ground distributions of eastern migratory monarchs (Danaus plexippus) via range expansion of Asclepias host plants.

Climate change can profoundly alter species’ distributions due to changes in temperature, precipitation, or seasonality. Migratory monarch butterflies (Danaus plexippus) may be particularly susceptible to climate-driven changes in host plant abundance or reduced overwintering habitat. For example, climate change may significantly reduce the availability of overwintering habitat by restricting the amount of area with suitable microclimate conditions. However, potential effects of climate change on monarch northward migrations remain largely unknown, particularly with respect to their milkweed (Asclepias spp.) host plants. Given that monarchs largely depend on the genus Asclepias as larval host plants, the effects of climate change on monarch northward migrations will most likely be mediated by climate change effects on Asclepias. Here, I used MaxEnt species distribution modeling to assess potential changes in Asclepias and monarch distributions under moderate and severe climate change scenarios. First, Asclepias distributions were projected to extend northward throughout much of Canada despite considerable variability in the environmental drivers of each individual species. Second, Asclepias distributions were an important predictor of current monarch distributions, indicating that monarchs may be constrained as much by the availability of Asclepias host plants as environmental variables per se. Accordingly, modeling future distributions of monarchs, and indeed any tightly coupled plant-insect system, should incorporate the effects of climate change on host plant distributions. Finally, MaxEnt predictions of Asclepias and monarch distributions were remarkably consistent among general circulation models. Nearly all models predicted that the current monarch summer breeding range will become slightly less suitable for Asclepias and monarchs in the future. Asclepias, and consequently monarchs, should therefore undergo expanded northern range limits in summer months while encountering reduced habitat suitability throughout the northern migration.

Increased temperature causes protein limitation by reducing the efficiency of nitrogen digestion in the ectothermic herbivore Spodoptera exigua

For insect herbivores, rising temperatures lead to exponentially higher metabolic rates. As a result, basic nutritional demands for protein and carbohydrates can be altered at high temperatures. It is hypothesized that temperature‐driven increases in metabolic nitrogen turnover will exacerbate protein limitation by increasing metabolic nitrogen demand. To test this hypothesis, the present study examines whether metabolic nitrogen turnover at higher temperatures causes protein limitation of a generalist herbivore, the beet armyworm Spodoptera exigua Hübner (Lepidoptera : Noctuidae). Third‐instar S. exigua larvae were reared at 25 and 30 °C on three artificial diets of varying protein : carbohydrate ratios (23 : 26, 17 : 26 and 6 : 26 %P : %C, respectively) and their growth rates, metabolic nitrogen demand and consumption rates were measured. Warming was found to lead to temperature‐induced protein limitation of the S. exigua larvae by increasing metabolic nitrogen demand at the same time as reducing nitrogen digestion efficiency. Because climate change is increasing atmospheric temperatures rapidly worldwide, it is suggested that a better understanding of how temperature change can influence metabolic demands will provide key information for predicting herbivore growth rates and foraging strategies in the future.

Bidirectional trophic linkages couple canopy and understorey food webs

Summary 1. Cross-system resource flux is a fundamental component of ecological systems. Allochthonous material flows generate trophic linkages between adjacent food webs, thereby affecting community structure and stability in recipient systems. 2. We investigated cross-habitat trophic linkages between canopy and understorey food webs in a terrestrial, wooded, ecosystem in South Florida, USA. The focal community consisted of three species of Anolis lizards and their prey. We described interspecific differences among Anolis species in the strength and routing of these cross-habitat flows using stable isotope analysis, stomach content analysis and habitat use data. 3. All three Anolis species in this study consumed different prey and occupied vertically distinct arboreal habitats. Despite these differences, carbon isotope and stomach content analysis revealed strong integration with understorey and canopy food webs for all Anolis species. Modes of resource flux contributing to the observed cross-habitat trophic linkages included prey movement and the gravity-driven transport of detritus. 4. Our study shows that terrestrial systems are linked by considerable bidirectional cross-system resource flux. Our results also suggest that considering species-specific interactions between predator and prey is necessary to fully understand the diversity of material and energy flows between spatially separated habitats.