Ecosystem engineering as an energy transfer process: a simple agent-based model

Ecosystem engineers are defined as organisms who modulate the availability of resources for themselves and other organisms by physically changing the environment. Ecosystem engineering is a well-recognised ecological interaction, but there is a limited number of general models due to the recent development of the field. Agent-based models are often used to study how organisms respond to changing environments and are suitable for modelling ecosystem engineering. To our knowledge, agent-based methodology has not yet been used to model ecosystem engineering. In this paper, we develop a simple agent-based population dynamics model of ecosystem engineering as an energy transfer process. We apply energy budget approach to conceptually explain how ecosystem engineers transfer energy to the environment and define various types of energy transfers relative to their effects on the engineers and other organisms. We simulate environments with various levels of resource abundance and compare the results of the model without ecosystem engineering agents to the model with ecosystem engineering agents. We find that in environments with higher levels of resources, the presence of ecosystem engineers increases the average carrying capacity and the strength of population fluctuations, while in environments with lower levels of resources, ecosystem engineering mitigates fluctuations, increases average carrying capacity and makes environments more resilient. Finally, we discuss about the further application of agent-based modelling for the theoretical and experimental development of the ecosystem engineering concept.     

Using ecosystem engineers to restore ecological systems

Ecosystem engineers affect other organisms by creating, modifying, maintaining or destroying habitats. Despite widespread recognition of these often important effects, the ecosystem engineering concept has yet to be widely used in ecological applications. Here, we present a conceptual framework that shows how consideration of ecosystem engineers can be used to assess the likelihood of restoration of a system to a desired state, the type of changes necessary for successful restoration and how restoration efforts can be most effectively partitioned between direct human intervention and natural ecosystem engineers.     

Ecosystem engineering effects on species diversity across ecosystems: a meta‐analysis

Ecosystem engineering is increasingly recognized as a relevant ecological driver of diversity and community composition. Although engineering impacts on the biota can vary from negative to positive, and from trivial to enormous, patterns and causes of variation in the magnitude of engineering effects across ecosystems and engineer types remain largely unknown. To elucidate the above patterns, we conducted a meta‐analysis of 122 studies which explored effects of animal ecosystem engineers on species richness of other organisms in the community. The analysis revealed that the overall effect of ecosystem engineers on diversity is positive and corresponds to a 25% increase in species richness, indicating that ecosystem engineering is a facilitative process globally. Engineering effects were stronger in the tropics than at higher latitudes, likely because new or modified habitats provided by engineers in the tropics may help minimize competition and predation pressures on resident species. Within aquatic environments, engineering impacts were stronger in marine ecosystems (rocky shores) than in streams. In terrestrial ecosystems, engineers displayed stronger positive effects in arid environments (e.g. deserts). Ecosystem engineers that create new habitats or microhabitats had stronger effects than those that modify habitats or cause bioturbation. Invertebrate engineers and those with lower engineering persistence (<1 year) affected species richness more than vertebrate engineers which persisted for >1 year. Invertebrate species richness was particularly responsive to engineering impacts. This study is the first attempt to build an integrative framework of engineering effects on species diversity; it highlights the importance of considering latitude, habitat, engineering functional group, taxon and persistence of their effects in future theoretical and empirical studies.     

Ecosystem engineering in space and time

The ecosystem engineering concept focuses on how organisms physically change the abiotic environment and how this feeds back to the biota. While the concept was formally introduced a little more than 10 years ago, the underpinning of the concept can be traced back to more than a century to the early work of Darwin. The formal application of the idea is yielding new insights into the role of species in ecosystems and many other areas of basic and applied ecology. Here we focus on how temporal, spatial and organizational scales usefully inform the roles played by ecosystem engineers and their incorporation into broader ecological contexts. Two particular, distinguishing features of ecosystem engineers are that they affect the physical space in which other species live and their direct effects can last longer than the lifetime of the organism – engineering can in essence outlive the engineer. Together, these factors identify critical considerations that need to be included in models, experimental and observational work. The ecosystem engineering concept holds particular promise in the area of ecological applications, where influence over abiotic variables and their consequent effects on biotic communities may facilitate ecological restoration and counterbalance anthropogenic influences.     

Functional domains in soils

Soil processes are significantly regulated by biological activities. Soil ecosystem engineers (predominantly termites, earthworms and ants) and roots produce biogenic structures, aggregates or pores that determine the structure and architecture of soil. The sum of structures produced by a population or community of invertebrate engineers creates a specific environment defined here as a functional domain. Functional domains are characterized by (i) the nature and spatial array of the biogenic structures, solid aggregates, mounds or constructs and pores of different shapes or sizes; (ii) the specific communities of smaller organisms from the meso- and microfauna and micro-organisms that they host; and (iii) the spatial and temporal scales at which soil processes operate. The regulation of processes caused by the physical organization of the soil environment and the redistribution of organic resources have been described and quantified in several studies. In soil, the relative importance of regulation imposed by ecosystem engineering is likely to be greater than regulation by trophic relationships because of the specific ecological constraints observed in this environment when compared to above-ground conditions.     

Effect of Season on the Impact of Ecosystem Engineers in the New River, NC

The importance of biotic interactions in structuring communities can depend on seasonal changes in abiotic context. The crayfish and benthic-feeding fish of the headwaters of the New River have been shown to be ecosystem engineers due to their ability to reduce the amount of sediment accumulation in cobble beds during the summer. However, the temperature-driven seasonal reduction in the activity level of these organisms may reduce their impacts during the colder months. I measured the impact of benthic-feeding fish and crayfish on sediment accrual in the headwaters of the New River during the winter using a field exclosure experiment. I found that during the winter there was no effect of benthic-feeding fish and crayfish on the amount of sediment accumulating in cobble beds in the headwaters of the New River. These findings suggest that seasonal changes in the effect of ecosystem engineers need to be quantified for a complete understanding of the effect of these organisms.     

Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers

Invasions by exotic species represent both threats to ecosystems as well as opportunities to learn more about them. Among the invaders that will have the largest impacts are those that directly modify ecosystems and thus have cascading effects for resident biota. Exotics can affect ecosystems by altering system-level flows, availability, or quality of nutrients, food, and physical resources (e.g. living space, water, heat or light). The invader-mediated control of physical resources, typically achieved through the modification of habitats, has received limited attention in invasion biology. This reflects a general trend in ecology, and only recently has the concept of ecosystem engineering been developed to account for the role of species that shape habitats. Plants and animals in terrestrial and aquatic systems can both create and destroy structure. When introduced into ecosystems, these exotic engineers cause physical state changes with effects that ramify throughout the system. Although the consequences of these modifications are varied and complex, insight gained from general ecological principles offers an opportunity to predict what invaders will do upon their integration into systems. Examples from the literature suggest that introduced ecosystem engineers that increase habitat complexity or heterogeneity tend to cause abundances and/or species richness to rise, while those that decrease complexity tend to have the reverse effect. In assessing such patterns, however, it is critical to also consider spatial scales and the life habits of resident organisms. In addition to providing predictive power, recognition of engineering as a major means by which invasive species affect ecosystems provides a unifying theme for invasion biology and offers a chance to consider more fully the general role of species in ecosystems.     

Are hippos Africa's most influential megaherbivore? A review of ecosystem engineering by the semi-aquatic common hippopotamus

Megaherbivores perform vital ecosystem engineering roles, and have their last remaining stronghold in Africa. Of Africa's remaining megaherbivores, the common hippopotamus (Hippopotamus amphibius) has received the least scientific and conservation attention, despite how influential their ecosystem engineering activities appear to be. Given the potentially crucial ecosystem engineering influence of hippos, as well as mounting conservation concerns threatening their long-term persistence, a review of the evidence for hippos being ecosystem engineers, and the effects of their engineering, is both timely and necessary. In this review, we assess, (i) aspects of hippo biology that underlie their unique ecosystem engineering potential; (ii) evaluate hippo ecological impacts in terrestrial and aquatic environments; (iii) compare the ecosystem engineering influence of hippos to other extant African megaherbivores; (iv) evaluate factors most critical to hippo conservation and ecosystem engineering; and (v) highlight future research directions and challenges that may yield new insights into the ecological role of hippos, and of megaherbivores more broadly. We find that a variety of key life-history traits determine the hippo's unique influence, including their semi-aquatic lifestyle, large body size, specialised gut anatomy, muzzle structure, small and partially webbed feet, and highly gregarious nature. On land, hippos create grazing lawns that contain distinct plant communities and alter fire spatial extent, which shapes woody plant demographics and might assist in maintaining fire-sensitive riverine vegetation. In water, hippos deposit nutrient-rich dung, stimulating aquatic food chains and altering water chemistry and quality, impacting a host of different organisms. Hippo trampling and wallowing alters geomorphological processes, widening riverbanks, creating new river channels, and forming gullies along well-utilised hippo paths. Taken together, we propose that these myriad impacts combine to make hippos Africa's most influential megaherbivore, specifically because of the high diversity and intensity of their ecological impacts compared with other megaherbivores, and because of their unique capacity to transfer nutrients across ecosystem boundaries, enriching both terrestrial and aquatic ecosystems. Nonetheless, water pollution and extraction for agriculture and industry, erratic rainfall patterns and human–hippo conflict, threaten hippo ecosystem engineering and persistence. Therefore, we encourage greater consideration of the unique role of hippos as ecosystem engineers when considering the functional importance of megafauna in African ecosystems, and increased attention to declining hippo habitat and populations, which if unchecked could change the way in which many African ecosystems function.     

Ecosystem engineering and biodiversity in coastal sediments: posing hypotheses

Coastal sediments in sheltered temperate locations are strongly modified by ecosystem engineering species such as marsh plants, seagrass, and algae as well as by epibenthic and endobenthic invertebrates. These ecosystem engineers are shaping the coastal sea and landscape, control particulate and dissolved material fluxes between the land and sea, and between the benthos and the passing water or air. Above all, habitat engineering exerts facilitating and inhibiting effects on biodiversity. Despite a strongly growing interest in the functional role of ecosystem engineering over the recent years, compared to food web analyses, the conceptual understanding of engineering-mediated species interactions is still in its infancy. In the present paper, we provide a concise overview on current insights and propose two hypotheses on the general mechanisms by which ecosystem engineering may affect biodiversity in coastal sediments. We hypothesise that autogenic and allogenic ecosystem engineers have inverse effects on epibenthic and endobenthic biodiversity in coastal sediments. The primarily autogenic structures of the epibenthos achieve high diversity at the expense of endobenthos, whilst allogenic sediment reworking by infauna may facilitate other infauna and inhibits epibenthos. On a larger scale, these antagonistic processes generate patchiness and habitat diversity. Due to such interaction, anthropogenic influences can strongly modify the engineering community by removing autogenic ecosystem engineers through coastal engineering or bottom trawling. Another source of anthropogenic influences comes from introducing invasive engineers, from which the impact is often hard to predict. We hypothesise that the local biodiversity effects of invasive ecosystem engineers will depend on the engineering strength of the invasive species, with engineering strength defined as the number of habitats it can invade and the extent of modification. At a larger scale of an entire shore, biodiversity need not be decreased by invasive engineers and may even increase. On a global scale, invasive engineers may cause shore biota to converge, especially visually due to the presence of epibenthic structures.     

Patch dynamics in a landscape modified by ecosystem engineers

Ecosystem engineers, organisms that modify the environment, have the potential to dramatically alter ecosystem structure and function at large spatial scales. The degree to which ecosystem engineering produces large-scale effects is, in part, dependent on the dynamics of the patches that engineers create. Here we develop a set of models that links the population dynamics of ecosystem engineers to the dynamics of the patches that they create. We show that the relative abundance of different patch types in an engineered landscape is dependent upon the production of successful colonists from engineered patches and the rate at which critical resources are depleted by engineers and then renewed. We also consider the effects of immigration from either outside the system or from engineers that are present in non-engineered patches, and the effects of engineers that can recolonize patches before they are fully recovered on the steady state distribution of different patch types. We use data collected on the population dynamics of a model engineer, the beaver, to estimate the per-patch production rate of new colonists, the decay rate of engineered patches, and the recovery rate of abandoned patches. We use these estimated parameters as a baseline to determine the effects of varying parameters on the distribution of different patch types. We suggest a number of hypotheses that derive from model predictions and that could serve as tests of the model.     

Multi‐scale habitat modification by coexisting ecosystem engineers drives spatial separation of macrobenthic functional groups

By changing habitat conditions, ecosystem engineers increase niche diversity and have profound effects on the distribution and abundances of other organisms. Although many ecosystems contain several engineering species, it is still unclear how the coexistence of multiple engineers affects the physical habitat and the structure of the community on a landscape scale. Here, we investigated through a large‐scale field manipulation how three coexisting engineers on intertidal flats (cockles Cerastoderma edule; lugworms Arenicola marina; blue mussels Mytilus edulis) influence the functional composition of the local macrobenthic community and what the consequences are at the landscape level. By using biological trait analysis (BTA), we show that on the local scale biogenic changes in sediment accumulation and organic matter content translated into specific shifts in the distribution of functional traits within the community. At a landscape scale, the co‐occurrence of multiple ecosystem engineers resulted in the spatial separation of different functional groups, i.e. different functional groups dominated unique complementary habitats. Our results emphasize the role of co‐occurring multiple engineers in shaping natural communities, thus contributing to a better knowledge of community assembly rules. This understanding can profitably be used to improve ecosystem‐based management and conservation actions.     

Ecosystem engineering moving away from just-so stories

The concept of ecosystem engineering has been proposed recently to account for key processes between organisms and their environment which are not directly trophic or competitive, and which result in the modification, maintenance and/or creation of habitats. Since the initial reporting of the idea, little work has been undertaken to apply the proposed concept to potential ecosystem engineers in the marine environment. Biological and ecological data for the burrowing ghost shrimp Callianassa filholi (Decapoda: Thalassinidea) allowed for a formal assessment of this species as an ecosystem engineer, in direct accordance with published criteria. Despite a low population density and the short durability of its burrow structures, Callianassa filholi affected a number of resource flows by its large lifetime per capita activity. Ecosystem effects were evident in significant changes in macrofauna community composition over small spatial and temporal scales. Seasonal variation in the effects of ghost shrimp activity were associated with changes in seagrass (Zostera novazelandica) biomass, which revealed the probability of interactions between antagonistic ecosystem engineers. The formal assessment of Callianassa filholi provides the opportunity to aid discussion pertaining to the development of the ecosystem engineering concept.     

Ecosystem services provided by armadillos

Awareness of the natural ecological processes provided by organisms that benefit human well‐being has significantly progressed towards the goal of making conservation a mainstream value. Identifying different services and the species that provide them is a vital first step for the management and maintenance of these so‐called ecosystem services. Herein, we specifically address the armadillos, which play key functional roles in terrestrial ecosystems, including as ecosystem engineers, predators, and vectors of invertebrates and nutrients, although these roles have often been overlooked. Armadillos can control pests, disperse seeds, and be effective sentinels of potential disease outbreaks or bioindicators of environmental contaminants. They also supply important material (meat, medicines) and non‐material (learning, inspiration) contributions all over the Americas. We identify key gaps in the understanding of ecosystem services provided by armadillos and areas for future research required to clarify their functional role in terrestrial ecosystems and the services they supply. Such information will produce powerful arguments for armadillo conservation.     

Engineering role models: do non-human species have the answers?

A shift from traditional engineering approaches to ecologically-based techniques will require changing societal values regarding ‘how and what’ is defined as engineering and design. Non-human species offer many ecological engineering examples that are often beneficial to ecosystem function and other biota. For example, organisms known as ‘ecosystem engineers’ build, modify, and destroy habitat in their quest for food and survival. Similarly, ‘keystone species’ have greater impacts on community or ecosystem function than would be predicted from their abundance. The capacity of these types of organisms to affect ecosystems is great. They exert controlling influences over ecosystems and communities by altering resource allocation, creating habitats and modifying relative competitive advantages.Species’ effects in ecosystems, although context-dependent, can be evaluated as ‘beneficial’ or ‘detrimental’. The evaluation depends on whether effects on other species or ecosystem function are more or less desirable from a given perspective. Organisms with beneficial impacts facilitate the presence of other species, employ efficient nutrient cycling, and are sometimes characterized by specific mutualisms. In contrast, many cases of detrimental engineering are found from introduced (i.e., exotic) species and are characterized by a loss of species richness, a lack of nutrient retention and the degradation of ecosystem integrity. Species’ impacts on ecosystems and community traits have been quantified in ecological studies and can be used similarly to understand, design and model human engineering structures and impacts on the landscape. Emulation of species with beneficial impacts on ecosystems can provide powerful guidance to the goals of ecological engineering. Using role model organisms that have desirable effects on species diversity and ecosystem function will be important in developing alternatives to traditional engineering practices.     

Ecosystem engineering affects ecosystem functioning in high-Andean landscapes

Ecosystem engineers are organisms that change the distribution of materials and energy in the abiotic environment, usually creating and maintaining new habitat patches in the landscape. Such changes in habitat conditions have been widely documented to affect the distributions and performances of other species but up to now no studies have addressed how such effects can impact the biotically driven physicochemical processes associated with these landscapes, or ecosystem functions. Based on the widely accepted positive relationship between species diversity and ecosystem functions, we propose that the effects of ecosystem engineers on other species could have an impact on ecosystem functions via two mutually inclusive mechanisms: (1) by adding new species into landscapes, hence increasing species diversity; and (2) by improving the performances of species already present in the landscape. To test these hypotheses, we focused on the effects of a high-Andean ecosystem engineer, the cushion plant Azorella monantha, by comparing the accumulation of plant biomass and nitrogen fixed in plant tissues as species richness increases in landscapes with and without the engineer species. Our results show that both ecosystem functions increased with species richness in both landscape types, but landscapes including A. monantha cushions reached higher outcomes of plant biomass and nitrogen fixed in plant tissues than landscapes without cushions. Moreover, our results indicate that such positive effects on ecosystem functions could be mediated by the two mechanisms proposed above. Then, given the conspicuousness of ecosystem engineering in nature and its strong influence on species diversity, and given the well-known relationship between species diversity and ecosystem function, we suggest that the application of the conceptual framework proposed herein to other ecosystems would help to advance our understanding of the forces driving ecosystem functioning. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

European rabbits as ecosystem engineers: warrens increase lizard density and diversity

Mammals that build extensive open burrow systems are often classified as ecosystem engineers, since they have the potential to modulate the availability of resources for themselves and other organisms. Lizards may benefit from the heterogeneity created by these structures, especially if coupled with an increased offer of sites for refuge and thermoregulation. However, information about these engineering effects by burrowing animals is scarce. We investigated the influence of European rabbit burrows on several parameters of a Mediterranean lizard community (abundance, density, diversity and body condition) in three different habitats (open pastures, holm oak and scrub patches). We found that lizards were positively associated with burrows, and that burrows determined lizard presence at otherwise unfavourable habitats. Moreover, community parameters such as density and species richness were higher in sites with burrows. Burrows influenced lizard species in different ways, and were also relevant for other Mediterranean vertebrates, as revealed by questionnaires to experts. We also explored the possible resources provided by burrows for lizards. Warrens offer relatively abundant prey and appropriate retreat sites for refuge and thermoregulation. Warrens may have further implications within the ecosystem, acting as stepping stones, allowing lizards to reach otherwise inaccessible habitat patches. This study shows that European rabbit warrens have a positive influence on lizard density and diversity, and confirms the role of rabbits as ecosystem engineers. This reinforces the need for appropriate conservation measures for rabbits, especially given their threatened status in the Iberian Peninsula. Furthermore, our study highlights that taking into account the influence of engineering activities increases our awareness of species interactions, and may translate into more adequate conservation measures for the preservation of biodiversity.     

Shellfish Reefs Increase Water Storage Capacity on Intertidal Flats Over Extensive Spatial Scales

Ecosystem engineering species can affect their environment at multiple spatial scales, from the local scale up to a significant distance, by indirectly affecting the surrounding habitats. Structural changes in the landscape can have important consequences for ecosystem functioning, for example, by increasing retention of limiting resources in the system. Yet, it remains poorly understood how extensive the footprint of ecosystem engineers on the landscape is. Using remote sensing techniques, we reveal that depression storage capacity on intertidal flats is greatly enhanced by engineering by shellfish resulting in intertidal pools. Many organisms use such pools to bridge low water events. This storage capacity was significantly higher both locally within the shellfish reef, but also at extensive spatial scales up to 115 m beyond the physical reef borders. Therefore, the footprint of these ecosystem engineers on the landscape was more than 5 times larger than their actual coverage; the shellfish cover approximately 2% of the total intertidal zone, whereas they influence up to approximately 11% of the area by enhancing water storage capacity. We postulate that increased residence time of water due to higher water storage capacity within engineered landscapes is an important determinant of ecosystem functioning that may extend well beyond the case of shellfish reefs provided here.     

Insects as stem engineers: interactions mediated by the twig-girdler Oncideres albomarginata chamela enhance arthropod diversity

Background

Ecosystem engineering may influence community structure and biodiversity by controlling the availability of resources and/or habitats used by other organisms. Insect herbivores may act as ecosystem engineers but there is still poor understanding of the role of these insects structuring arthropod communities.

Methodology/Principal Findings

We evaluated the effect of ecosystem engineering by the stem-borer Oncideres albomarginata chamela on the arthropod community of a tropical dry forest for three consecutive years. The results showed that ecosystem engineering by O. albomarginata chamela had strong positive effects on the colonization, abundance, species richness and composition of the associated arthropod community, and it occurred mainly through the creation of a habitat with high availability of oviposition sites for secondary colonizers. These effects cascade upward to higher trophic levels. Overall, ecosystem engineering by O. albomarginata chamela was responsible for nearly 95% of the abundance of secondary colonizers and 82% of the species richness.

Conclusions/Significance

Our results suggest that ecosystem engineering by O. albomarginata chamela is a keystone process structuring an arthropod community composed by xylovores, predators and parasitoids. This study is the first to empirically demonstrate the effect of the ecosystem engineering by stem-boring insects on important attributes of arthropod communities. The results of this study have important implications for conservation.     

Context dependence of marine ecosystem engineer invasion impacts on benthic ecosystem functioning

Introduced ecosystem engineers can severely modify the functioning on invaded systems. Species-level effects on ecosystem functioning (EF) are context dependent, but the effects of introduced ecosystem engineers are frequently assessed through single-location studies. The present work aimed to identify sources of context-dependence that can regulate the impacts of invasive ecosystem engineers on ecosystem functioning. As model systems, four locations where the bivalve Ruditapes philippinarum (Adams and Reeve) has been introduced were investigated, providing variability in habitat characteristics and community composition. As a measure of ecosystem engineering, the relative contribution of this species to community bioturbation potential was quantified at each site. The relevance of bioturbation to the local establishment of the mixing depth of marine sediments (used as a proxy for EF) was quantified in order to determine the potential for impact of the introduced species at each site. We found that R. philippinarum is one of the most important bioturbators within analysed communities, but the relative importance of this contribution at the community level depended on local species composition. The net contribution of bioturbation to the establishment of sediment mixing depths varied across sites depending on the presence of structuring vegetation, sediment granulometry and compaction. The effects of vegetation on sediment mixing were previously unreported. These findings indicate that the species composition of invaded communities, and the habitat characteristics of invaded systems, are important modulators of the impacts of introduced species on ecosystem functioning. A framework that encompasses these aspects for the prediction of the functional impacts of invasive ecosystem engineers is suggested, supporting a multi-site approach to invasive ecology studies concerned with ecosystem functioning.     

Mollusks as ecosystem engineers: the role of shell production in aquatic habitats

Mollusk shells are abundant, persistent, ubiquitous physical structures in aquatic habitats. Using an ecosystem engineering perspective, we identify general roles of mollusk shell production in aquatic ecosystems. Shells are substrata for attachment of epibionts, provide refuges from predation, physical or physiological stress, and control transport of solutes and particles in the benthic environment. Changes in availability of these resources caused by shell production have important consequences for other organisms. Colonization of shelled habitat depends on individual shell traits and spatial arrangement of shells, which determine access of organisms to resources and the degree to which biotic or abiotic forces are modulated. Shell production will increase species richness at the landscape level if shells create resources that are not otherwise available and species are present that use these resources. Changes in the availability of resources caused by shells and the resulting effects on other organisms have both positive and negative feedbacks to these engineers. Positive feedbacks appear to be most frequently mediated by changes in resource availability, whereas negative feedbacks appear to be most frequently mediated by organisms. Given the diversity of species that depend upon resources controlled by shells and rapid changes in global shell production that are occurring due to human activities, we suggest that shell producers should not be neglected as a targets of conservation, restoration and habitat management.