Predicting changes in abundance and juvenile proportions of earthworms in the field using glmmADMB in R

The study aimed at investigating effects of three differently acting biocides; the insecticide esfenvalerate, the fungicide picoxystrobin and the bactericide triclosan, applied individually and as a mixture, on an earthworm community in the field. A concentration-response design was chosen and results were analyzed using univariate and multivariate approaches. Effects on juvenile proportions were less pronounced and more variable than effects on abundance, but effects in general were species- and chemical-specific, and temporal variations distinct. Esfenvalerate and picoxystrobin appeared to elicit stronger effects than triclosan at laboratory-based ECx values, which is in accordance with our previous laboratory study on Eisenia fetida. The mixture affected abundance and juvenile proportions, but the latter only at high mixture concentrations. Esfenvalerate and picoxystrobin appeared to be the main drivers for the mixture's toxicity. Species-specific toxicity patterns question the reliability of mixture toxicity predictions derived on E. fetida for field earthworms. Biocide concentrations equaling EC50s (reproduction) for E. fetida provoked effects on the field earthworms mainly exceeding 50%, indicating effect intensification from the laboratory to field as well as the influence of indirect effects produced by species interactions. The differing results of the present field study and the previous laboratory study imply that lower- and higher-tier studies may not be mutually exclusive, but to be used in complementary.

Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales)

Understanding the ecological implications of global climate change requires investigations of not only the direct effects of environmental change on species performance but also indirect effects that arise from altered species interactions. We performed CO2 perturbation experiments to investigate the effects of ocean acidification on the trophic interaction between the brown seaweed Fucus vesiculosus and the herbivorous isopod Idotea baltica. We predicted faster growth of F. vesiculosus at elevated CO2-concentrations and higher carbon content of the algal tissue. We expected that I. baltica has different consumption rates on algae that have been grown at different CO2 levels and that the isopods remove surplus carbon metabolically by enhanced respiration. Surprisingly, growth of F. vesiculosus as well as the C:N-ratio of the algal tissue were reduced at high CO2-levels. The changes in the elemental composition had no effect on the consumption rates and the respiration of the herbivores. An additional experiment showed that consumption of F. vesiculosus by the isopod Idotea emarginata was independent of ocean acidification and temperature. Our results could not reveal any effects of ocean acidification on the per capita strength of the trophic interaction between F. vesiculosus and its consumers. However, reduced growth of the algae at high CO2-concentrations might reduce the capability of the seaweed to compensate losses due to intense herbivory.

Experiment: Food availability outweighs ocean acidification effects in juvenile Mytilus edulis

Ocean acidification is expected to decrease calcification rates of bivalves. Nevertheless in many coastal areas high pCO2 variability is encountered already today. Kiel Fjord (Western Baltic Sea) is a brackish (12-20 g kg-1) and CO2 enriched habitat, but the blue mussel Mytilus edulis dominates the benthic community. In a coupled field and laboratory study we examined the annual pCO2 variability in this habitat and the combined effects of elevated pCO2 and food availability on juvenile M. edulis growth and calcification. In the laboratory experiment, mussel growth and calcification were found to chiefly depend on food supply, with only minor impacts of pCO2 up to 3350 µatm. Kiel Fjord was characterized by strong seasonal pCO2 variability. During summer, maximal pCO2 values of 2500 µatm were observed at the surface and >3000 µatm at the bottom. However, the field growth experiment revealed seven times higher growth and calcification rates of M. edulis at a high pCO2 inner fjord field station (mean pCO2 ca. 1000 µatm) in comparison to a low pCO2 outer fjord station (ca. 600 µatm). In addition, mussels were able to outcompete the barnacle Amphibalanus improvisus at the high pCO2 site. High mussel productivity at the inner fjord site was enabled by higher particulate organic carbon concentrations. Kiel Fjord is highly impacted by eutrophication, which causes bottom water hypoxia and consequently high seawater pCO2. At the same time, elevated nutrient concentrations increase the energy availability for filter feeding organisms such as mussels. Thus M. edulis can dominate over a seemingly more acidification resistant species such as A. improvisus. We conclude that benthic stages of M. edulis tolerate high ambient pCO2 when food supply is abundant and that important habitat characteristics such as species interactions and energy availability need to be considered to predict species vulnerability to ocean acidification.

Sea urchin response to rising pCO2 shows ocean acidification may fundamentally alter the chemistry of marine skeletons

Ocean acidification caused by an increase in pCO2 is expected to drastically affect marine ecosystem composition, yet there is much uncertainty about the mechanisms through which ecosystems may be affected. Here we studied sea urchins that are common and important grazers in the Mediterranean (Paracentrotus lividus and Arbacia lixula). Our study included a natural CO2 seep plus reference sites in the Aegean Sea off Greece. The distribution of A. lixula was unaffected by the low pH environment, whereas densities of P. lividus were much reduced. There was skeletal degradation in both species living in acidified waters compared to reference sites and remarkable increases in skeletal manganese levels (P. lividus had a 541% increase, A. lixula a 243% increase), presumably due to changes in mineral crystalline structure. Levels of strontium and zinc were also altered. It is not yet known whether such dramatic changes in skeletal chemistry will affect coastal systems but our study reveals a mechanism that may alter inter-species interactions.

Functional consequences of prey acclimation to ocean acidification for the prey and its predator

Ocean acidification is the suite of chemical changes to the carbonate system of seawater as a consequence of anthropogenic carbon dioxide (CO2) emissions. Despite a growing body of evidences demonstrating the negative effects of ocean acidification on marine species, the consequences at the ecosystem level are still unclear. One factor limiting our ability to upscale from species to ecosystem is the poor mechanistic understanding of the functional consequences of the observed effects on organisms. This is particularly true in the context of species interactions. The aim of this work was to investigate the functional consequence of the exposure of a prey (the mussel Brachidontes pharaonis) to ocean acidification for both the prey and its predator (the crab Eriphia verrucosa). Mussels exposed to pH 7.5 for >4 weeks showed significant decreases in condition index and in mechanical properties (65% decrease in maximum breaking load) as compared with mussels acclimated to pH 8.0. This translated into negative consequences for the mussel in presence of the predator crab. The crab feeding efficiency increased through a significant 27% decrease in prey handling time when offered mussels acclimated to the lowest pH. The predator was also negatively impacted by the acclimation of the prey, probably as a consequence of a decreased food quality. When fed with prey acclimated under decreased pH for 3 months, crab assimilation efficiency significantly decreased by 30% and its growth rate was 5 times slower as compared with crab fed with mussels acclimated under high pH. Our results highlight the important to consider physiological endpoints in the context of species interactions.

Mixing effect on volume growth of Fagus sylvatica and Pinus sylvestris is modulated by stand density

Despite the increasing relevance of mixed stands due to their potential benefits; little information is available with regard to the effect of mixtures on yield in forest systems. Hence, it is necessary to study inter-specific relationships, and the resulting yield in mixed stands, which may vary with stand development, site or stand density, etc. In Spain, the province of Navarra is considered one of the biodiversity reservoirs; however, mixed forests occupy only a small area, probably as a consequence of management plans, in which there is an excessive focus on the productivity aspect, favoring the presence of pure stands of the most marketable species. The aim of this paper is to study how growth efficiencies of beech (Fagus sylvatica) and pine (Pinus sylvestris) are modified by the admixture of the other species and to determine whether stand density modifies interspecific relationships and to what extent. Two models were fitted from Spanish National Forest Inventory data, for P. sylvestris and F. sylvatica respectively, which relate the growth efficiency of the species, i.e. the volume increment of the species divided by the species proportion by area, with dominant height, quadratic mean diameter, stocking degree, and the species proportions by area of each species. Growth efficiency of pine increased with the admixture of beech, decreasing this positive effect when stocking degree increased. However, the positive effect of pine admixture on beech growth was greater at higher stocking degrees. Growth efficiency of beech was also dependent on stand dominant height, resulting in a net negative mixing effect when stand dominant heights and stocking degrees were simultaneously low. There is a relatively large range of species proportions and stocking degrees which results in transgressive overyielding: higher volume increments in mixed stands than that of the most productive pure pine stands. We concluded that stocking degree is a key factor in between-species interactions, being the effects of mixing not always greater at higher stand densities, but it depends on species composition.

Analyzing size-symmetric vs. size-asymmetric and intra-vs. inter-specific competition in beech (Fagus sylvatica L.) mixed stands

In mixed stands, inter-specific competition can be lower than intra-specific competition when niche complementarity and/or facilitation between species prevail. These positive interactions can take place at belowground and/or aboveground levels. Belowground competition tends to be size symmetric while the aboveground competition is usually for light and almost always size-asymmetric. Interactions between forest tree species can be explored analyzing growth at tree level by comparing intra and inter-specific competition. At the same time, possible causes of niche complementarity can be inferred relating intra and inter-specific competition with the mode of competition, i.e. size-symmetric or sizeasymmetric. The aim of this paper is to further our understanding of the interactions between species and to detect possible causes of competition reduction in mixed stands of beech (Fagus sylvatica L.) with other species: pine?beech, oak?beech and fir?beech. To test whether species growth is better explained by size-symmetric and/or size-asymmetric competition, five different competition structures where included in basal area growth models fitted using data from the Spanish National Forest Inventory for the Pyrenees. These models considered either size-symmetry only (Reineke?s stand density index, SDI), size-asymmetry only (SDI of large trees or SDI of small trees), or both combined. In order to assess the influence of the admixture, these indices were introduced in two different ways, one of which was to consider that trees of all species compete in a similar way, and the other was to split the stand density indices into intra- and inter-specific competition components. The results showed that in pine?beech mixtures, there is a slightly negative effect of beech on pine basal area growth while beech benefitted from the admixture of Scots pine; this positive effect being greater as the proportion of pine trees in larger size classes increases. In oak?beech mixtures, beech growth was also positively influenced by the presence of oaks that were larger than the beech trees. The growth of oak, however, decreased when the proportion of beech in SDI increased, although the presence of beech in larger size classes promoted oak growth. Finally, in fir?beech mixtures, neither fir nor beech basal area growth were influenced by the presence of the other species. The results indicate that size-asymmetric is stronger than size-symmetric competition in these mixtures, highlighting the importance of light in competition. Positive species interactions in size-asymmetric competition involved a reduction of asymmetry in tree size-growth relationships.

Variation in per capita interaction strength: Thresholds due to nonlinear dynamics and nonequilibrium conditions

I measured the strength of interaction between a marine herbivore and its growing resource over a realistic range of absolute and relative abundances. The herbivores (hermit crabs: Pagurus spp.) have slow and/or weak functional and numerical responses to epiphytic diatoms (Isthmia nervosa), which show logistic growth in the absence of consumers. By isolating this interaction in containers in the field, I mimicked many of the physical and biological variables characteristic of the intertidal while controlling the densities of focal species. The per capita effects of consumers on the population dynamics of their resource (i.e., interaction strength) were defined by using the relationship between hermit crab density and proportional change in the resource. When this relationship is fit by a Weibull function, a single parameter distinguishes constant interaction strength from one that varies as a function of density. Constant interaction strength causes the proportion of diatoms to fall linearly or proportionally as hermit crab density increases whereas per capita effects that increase with density cause an accelerating decline. Although many mathematical models of species interactions assume linear dynamics and invariant parameters, at least near equilibrium, the per capita effects of hermit crabs on diatoms varied substantially, apparently crossing a threshold from weak to strong when consumption exceeded resource production. This threshold separates a domain of coexistence from one of local extinction of the resource. Such thresholds may help explain trophic cascades, resource compensation, and context-dependent interaction strengths, while indicating a way to predict trophic effects, despite nonlinearities, as a function of vital rates.

Jugar a extinguir ensambles: importancia de las oquedades de los árboles para la biodiversidad de insectos saproxílicos

The assessment of the relation between species diversity, species interactions and stability is a major goal for conservation strategies of saproxylic insects in Iberian Mediterranean woodlands. In these woodlands, tree hollows in standing living trees are key microhabitats for saproxylic biodiversity. We assess the variation in the tree hollow-saproxylic insect network among three woodland sites in the Cabañeros National Park (Spain), and evaluate their implications for saproxylic assemblages’ persistence, through simulations of three possible scenarios of loss of tree hollow microhabitats. The composition of tree hollows is closely related to biotic and ecological complexity of saproxylic networks, and together exhibit positive effects on network stability. By other side, different scenarios entail different reorganizations of saproxylic diversity of species and interactions, and the variation of the main interacting attributes. Woodlands providing higher proportion of large tree hollows are less sensitive to microhabitat loss. Conservation strategies for saproxylic insects in Iberian Mediterranean woodlands should consider woodland composition and configuration as key factors in the selection of priority conservation areas.

Association Patterns in Saproxylic Insect Networks in Three Iberian Mediterranean Woodlands and Their Resistance to Microhabitat Loss

The assessment of the relationship between species diversity, species interactions and environmental characteristics is indispensable for understanding network architecture and ecological distribution in complex networks. Saproxylic insect communities inhabiting tree hollow microhabitats within Mediterranean woodlands are highly dependent on woodland configuration and on microhabitat supply they harbor, so can be studied under the network analysis perspective. We assessed the differences in interacting patterns according to woodland site, and analysed the importance of functional species in modelling network architecture. We then evaluated their implications for saproxylic assemblages’ persistence, through simulations of three possible scenarios of loss of tree hollow microhabitat. Tree hollow-saproxylic insect networks per woodland site presented a significant nested pattern. Those woodlands with higher complexity of tree individuals and tree hollow microhabitats also housed higher species/interactions diversity and complexity of saproxylic networks, and exhibited a higher degree of nestedness, suggesting that a higher woodland complexity positively influences saproxylic diversity and interaction complexity, thus determining higher degree of nestedness. Moreover, the number of insects acting as key interconnectors (nodes falling into the core region, using core/periphery tests) was similar among woodland sites, but the species identity varied on each. Such differences in insect core composition among woodland sites suggest the functional role they depict at woodland scale. Tree hollows acting as core corresponded with large tree hollows near the ground and simultaneously housing various breeding microsites, whereas core insects were species mediating relevant ecological interactions within saproxylic communities, e.g. predation, competitive or facilitation interactions. Differences in network patterns and tree hollow characteristics among woodland sites clearly defined different sensitivity to microhabitat loss, and higher saproxylic diversity and woodland complexity showed positive relation with robustness. These results highlight that woodland complexity goes hand in hand with biotic and ecological complexity of saproxylic networks, and together exhibited positive effects on network robustness.

Mollusca Non-Grata: The influence of top-down control and residence time on the abundance, distribution, and behavior of non-native marine snails in Washington State

Thesis (Ph.D.)--University of Washington, 2016-06

Local impacts of global change: shifting range limits, advancing phenology, and communicating research

Thesis (Ph.D.)--University of Washington, 2016-06

Responses of neotropical mangrove seedlings grown in monoculture and mixed culture under treatments of hydroperiod and salinity

We investigated the combined effects of salinity and hydroperiod on seedlings of Rhizophora mangle and Laguncularia racemosa grown under experimental conditions of monoculture and mixed culture by using a simulated tidal system. The objective was to test hypotheses relative to species interactions to either tidal or permanent flooding at salinities of 10 or 40 g/l. Four-month-old seedlings were experimentally manipulated under these environmental conditions in two types of species interactions: (1) seedlings of the same species were grown separately in containers from September 2000 to August 2001 to evaluate intraspecific response and (2) seedlings of each species were mixed in containers to evaluate interspecific, competitive responses from August 2002 to April 2003. Overall, L. racemosa was strongly sensitive to treatment combinations while R. mangle showed little effect. Most plant responses of L. racemosa were affected by both salinity and hydroperiod, with hydroperiod inducing more effects than salinity. Compared to R. mangle, L. racemosa in all treatment combinations had higher relative growth rate, leaf area ratio, specific leaf area, stem elongation, total length of branches, net primary production, and stem height. Rhizophora mangle had higher biomass allocation to roots. Species growth differentiation was more pronounced at low salinity, with few species differences at high salinity under permanent flooding. These results suggest that under low to mild stress by hydroperiod and salinity, L. racemosa exhibits responses that favor its competitive dominance over R. mangle. This advantage, however, is strongly reduced as stress from salinity and hydroperiod increase.

Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non-consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non-native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non-native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non-consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non-native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter-related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non-native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non-native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.

Human-driven benthic jellyfish blooms: Causes and consequences for coastal marine ecosystems

Coastal marine ecosystems are among the most impacted globally, attributable to individual and cumulative effects of human disturbance. Anthropogenic nutrient loading is one stressor that commonly affects nearshore ecosystems, including seagrass beds, and has positive and negative effects on the structure and function of coastal systems. An additional, previously unexplored mechanistic pathway through which nutrients may indirectly influence nearshore systems is by driving blooms of benthic jellyfish. My dissertation research, conducted on Abaco Island, Bahamas, focused on elucidating the role that benthic jellyfish have in structuring systems in which they are common (i.e., seagrass beds), and explored mechanistic processes that may drive blooms of this taxa. ^ To establish that human disturbances (e.g., elevated nutrient availability) may drive increased abundance and size of benthic jellyfish, Cassiopea spp., I conducted surveys in human-impacted and unimpacted coastal sites. Jellyfish were more abundant (and larger) from human-impacted areas, positively correlated to elevated nutrient availability. In order to elucidate mechanisms linking Cassiopea spp. with elevated nutrients, I evaluated whether zooxanthellae from Cassiopea were higher from human-disturbed systems, and whether Cassiopea exhibited increased size following nutrient input. I demonstrated that zooxanthellae population densities were elevated in human-impacted sites, and that nutrients led to positive jellyfish growth. ^ As heightened densities of Cassiopea jellyfish may exert top-down and bottom-up controls on flora and fauna in impacted seagrass beds, I sought to examine ecological responses to Cassiopea. I evaluated whether there was a relationship between high Cassiopea densities and lower benthic fauna abundance and diversity in shallow seagrass beds. I found that Cassiopea have subtle effects on benthic fauna. However, through an experiment conducted in a seagrass bed in which nutrients and Cassiopea were added, I demonstrated that Cassiopea can result in seagrass habitat modification, with negative consequences for benthic fauna. ^ My dissertation research demonstrates that increased human-driven benthic jellyfish densities may have indirect and direct effects on flora and fauna of coastal marine systems. This knowledge will advance our understanding of how human disturbances shift species interactions in coastal ecosystems, and will be critical for effective management of jellyfish blooms.^