John J. Stachowicz

Inclusion of facilitation into ecological theory

Investigations of the role of competition, predation and abiotic stress in shaping natural communities were a staple for previous generations of ecologists and are still popular themes. However, more recent experimental research has uncovered the largely unanticipated, yet striking influence of facilitation (i.e. positive species interactions) on the organization of terrestrial and aquatic communities. Modern ecological concepts and theories were well established a decade before the current renaissance of interest in facilitation began, and thus do not consider the importance of a wide variety of facilitative interactions. It is time to bring ecological theory up to date by including facilitation. This process will not be painless because it will fundamentally change many basic predictions and will challenge some of our most cherished paradigms. But, ultimately, revising ecological theory will lead to a more accurate and inclusive understanding of natural communities.

THE INVASION PARADOX: RECONCILING PATTERN AND PROCESS IN SPECIES INVASIONS

The invasion paradox describes the co-occurrence of independent lines of support for both a negative and a positive relationship between native biodiversity and the invasions of exotic species. The paradox leaves the implications of native-exotic species richness relationships open to debate: Are rich native communities more or less susceptible to invasion by exotic species? We reviewed the considerable observational, experimental, and theoretical evidence describing the paradox and sought generalizations concerning where and why the paradox occurs, its implications for community ecology and assembly processes, and its relevance for restoration, management, and policy associated with species invasions. The crux of the paradox concerns positive associations between native and exotic species richness at broad spatial scales, and negative associations at fine scales, especially in experiments in which diversity was directly manipulated. We identified eight processes that can generate either negative or positive native-exotic richness relationships, but none can generate both. As all eight processes have been shown to be important in some systems, a simple general theory of the paradox, and thus of the relationship between diversity and invasibility, is probably unrealistic. Nonetheless, we outline several key issues that help resolve the paradox, discuss the difficult juxtaposition of experimental and observational data (which often ask subtly different questions), and identify important themes for additional study. We conclude that natively rich ecosystems are likely to be hotspots for exotic species, but that reduction of local species richness can further accelerate the invasion of these and other vulnerable habitats.

Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions.

The spread of exotic species and climate change are among the most serious global environmental threats. Each independently causes considerable ecological damage, yet few data are available to assess whether changing climate might facilitate invasions by favoring introduced over native species. Here, we compare our long-term record of weekly sessile marine invertebrate recruitment with interannual variation in water temperature to assess the likely effect of climate change on the success and spread of introduced species. For the three most abundant introduced species of ascidian (sea squirt), the timing of the initiation of recruitment was strongly negatively correlated with winter water temperature, indicating that invaders arrived earlier in the season in years with warmer winters. Total recruitment of introduced species during the following summer also was positively correlated with winter water temperature. In contrast, the magnitude of native ascidian recruitment was negatively correlated with winter temperature (more recruitment in colder years) and the timing of native recruitment was unaffected. In manipulative laboratory experiments, two introduced compound ascidians grew faster than a native species, but only at temperatures near the maximum observed in summer. These data suggest that the greatest effects of climate change on biotic communities may be due to changing maximum and minimum temperatures rather than annual means. By giving introduced species an earlier start, and increasing the magnitude of their growth and recruitment relative to natives, global warming may facilitate a shift to dominance by nonnative species, accelerating the homogenization of the global biota.

Biodiversity, Invasion Resistance, and Marine Ecosystem Function: Reconciling Pattern and Process

A venerable generalization about community resistance to invasions is that more diverse communities are more resistant to invasion. However, results of experimental and observational studies often conflict, leading to vigorous debate about the mechanistic importance of diversity in determining invasion success in the field, as well as other eco- system properties, such as productivity and stability. In this study, we employed both field experiments and observational approaches to assess the effects of diversity on the invasion of a subtidal marine invertebrate community by three species of nonindigenous ascidians (sea squirts). In experimentally assembled communities, decreasing native diversity in- creased the survival and final percent cover of invaders, whereas the abundance of individual species had no effect on these measures of invasion success. Increasing native diversity also decreased the availability of open space, the limiting resource in this system, by buffering against fluctuations in the cover of individual species. This occurred because temporal patterns of abundance differed among species, so space was most consistently and completely occupied when more species were present. When we held diversity constant, but manipulated resource availability, we found that the settlement and recruitment of new invaders dramatically increased with increasing availability of open space. This suggests that the effect of diversity on invasion success is largely due to its effects on resource (space) availability. Apart from invasion resistance, the increased temporal stability found in more diverse communities may itself be considered an enhancement of ecosystem func- tion. In field surveys, we found a strong negative correlation between native-species richness and the number and frequency of nonnative invaders at the scale of both a single quadrat (25 3 25 cm), and an entire site (50 3 50 m). Such a pattern suggests that the means by which diversity affects invasion resistance in our experiments is important in determining the distribution of invasive species in the field. Further synthesis of mechanistic and ob- servational approaches should be encouraged, as this will increase our understanding of the conditions under which diversity does (and does not) play an important role in deter- mining the distribution of invaders in the field.

Global patterns in the impact of marine herbivores on benthic primary producers

Despite the importance of consumers in structuring communities, and the widespread assumption that consumption is strongest at low latitudes, empirical tests for global scale patterns in the magnitude of consumer impacts are limited. In marine systems, the long tradition of experimentally excluding herbivores in their natural environments allows consumer impacts to be quantified on global scales using consistent methodology. We present a quantitative synthesis of 613 marine herbivore exclusion experiments to test the influence of consumer traits, producer traits and the environment on the strength of herbivore impacts on benthic producers. Across the globe, marine herbivores profoundly reduced producer abundance (by 68% on average), with strongest effects in rocky intertidal habitats and the weakest effects on habitats dominated by vascular plants. Unexpectedly, we found little or no influence of latitude or mean annual water temperature. Instead, herbivore impacts differed most consistently among producer taxonomic and morphological groups. Our results show that grazing impacts on plant abundance are better predicted by producer traits than by large-scale variation in habitat or mean temperature, and that there is a previously unrecognised degree of phylogenetic conservatism in producer susceptibility to consumption.

Invasions and Extinctions Reshape Coastal Marine Food Webs

The biodiversity of ecosystems worldwide is changing because of species loss due to human-caused extinctions and species gain through intentional and accidental introductions. Here we show that the combined effect of these two processes is altering the trophic structure of food webs in coastal marine systems. This is because most extinctions (∼70%) occur at high trophic levels (top predators and other carnivores), while most invasions are by species from lower trophic levels (70% macroplanktivores, deposit feeders, and detritivores). These opposing changes thus alter the shape of marine food webs from a trophic pyramid capped by a diverse array of predators and consumers to a shorter, squatter configuration dominated by filter feeders and scavengers. The consequences of the simultaneous loss of diversity at top trophic levels and gain at lower trophic levels is largely unknown. However, current research suggests that a better understanding of how such simultaneous changes in diversity can impact ecosystem function will be required to manage coastal ecosystems and forecast future changes.

Managing for ocean biodiversity to sustain marine ecosystem services

Managing a complex ecosystem to balance delivery of all of its services is at the heart of ecosystem-based management. But how can this balance be accomplished amidst the conflicting demands of stakeholders, managers, and policy makers? In marine ecosystems, several common ecological mechanisms link biodiversity to ecosystem functioning and to a complex of essential services. As a result, the effects of preserving diversity can be broadly beneficial to a wide spectrum of important ecosystem processes and services, including fisheries, water quality, recreation, and shoreline protection. A management system that conserves diversity will help to accrue more “ecoservice capital” for human use and will maintain a hedge against unanticipated ecosystem changes from natural or anthropogenic causes. Although maintenance of biodiversity cannot be the only goal for ecosystem-based management, it could provide a common currency for evaluating the impacts of different human activities on ecosystem functioning and can...

REDUCING PREDATION THROUGH CHEMICALLY MEDIATED CAMOUFLAGE: INDIRECT EFFECTS OF PLANT DEFENSES ON HERBIVORES

Herbivores often specialize on particular hosts that provide both food and shelter from natural enemies. It is thus often unclear whether a plant’s value as a food or its value as a safe shelter has played a larger role in selecting for specialization. Decorator crabs offer a novel opportunity to investigate the relative effects of diet vs. natural enemies in selecting for specialization because these crabs place plant “shelter” on their backs as camouflage but need not use these plants as food, thus decoupling the plant’s value as a food from its value as a shelter. In this study, we show that juveniles of the decorator crab Libinia dubia selectively decorate with the chemically defended brown alga Dictyota menstrualis but treat this plant as a low-preference food. Common omnivorous fishes that are potential predators of Libinia avoid consuming Dictyota due to the alga’s potent chemical defenses. In the field, juvenile crabs decorated with Dictyota experience significantly less predation than crabs decor...

Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium.

The consequences of declining biodiversity remain controversial, in part because many studies focus on a single metric of ecosystem functioning and fail to consider diversitys integrated effects on multiple ecosystem functions. We used tide pool microcosms as a model system to show that different conclusions about the potential effects of producer diversity on ecosystem functioning may result when ecosystem functions are measured separately vs. together. Specifically, we found that in diverse seaweed assemblages, uptake of either nitrate or ammonium alone was equal to the average of the component monocultures. However, when nitrate and ammonium were available simultaneously, uptake by diverse assemblages was 22% greater than the monoculture average because different species were complementary in their use of different nitrogen forms. Our results suggest that when individual species have dominant effects on particular ecosystem processes (i.e., the sampling effect), multivariate complementarity can arise if different species dominate different processes. Further, these results suggest that similar mechanisms (complementary nutrient uptake) may underlie diversity-functioning relationships in both algal and vascular-plant-based systems.

DIVERSITY ENHANCES COVER AND STABILITY OF SEAWEED ASSEMBLAGES: THE ROLE OF HETEROGENEITY AND TIME

Generalizations regarding the mechanisms underlying the effects of plant diversity on ecosystem processes, and whether the patterns transcend study systems remain elusive. Many terrestrial plant diversity manipulations have found that plant biomass increases with diversity, but most marine studies find little or no effect of seaweed diversity on producer biomass or production. However, differences in experimental approach (field vs. mesocosm) and duration (years vs. weeks) between published terrestrial and marine experiments confound the interpretation of these differences in response to changing diversity. We conducted a three-year field manipulation of seaweed diversity on intertidal rocky reefs in central California, USA, to examine the effect of diversity on seaweed cover. We found that diversity increased standing algal cover and decreased the availability of free space relative to monocultures, but this effect took nine months to materialize. Furthermore, diverse assemblages did not consistently exceed the best performing monocultures until 18 months after the experiment was initiated, suggesting that the effect of diversity strengthens over time. Overall, diversitys effect was consistently stronger than that of individual species and not attributable to the influence of any particular species (sampling effect) because (1) polycultures eventually achieved higher cover than even the best performing monoculture and (2) monocultures rarely differed much, precluding a strong sampling effect. Instead, mechanisms such as facilitation and differential use of microhabitats in a heterogeneous environment likely caused the higher cover in polycultures. Our findings contrast with short-term experiments with other seaweeds but are similar to longer-term experiments with terrestrial plants, suggesting that experimental design and approach, rather than inherent differences between marine and terrestrial ecosystems, underlie contrasting responses among systems. We argue that experiments conducted in the field, and for a greater length of time, allow for the manifestation of a greater number of potential mechanisms of overyielding in diverse communities, increasing the likelihood of observing a strong diversity effect.