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      The Multiple Impacts of Tropical Forest Fragmentation on Arthropod Biodiversity and on their Patterns of Interactions with Host Plants

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          Abstract

          Tropical rain forest fragmentation affects biotic interactions in distinct ways. Little is known, however, about how fragmentation affects animal trophic guilds and their patterns of interactions with host plants. In this study, we analyzed changes in biotic interactions in forest fragments by using a multitrophic approach. For this, we classified arthropods associated with Heliconia aurantiaca herbs into broad trophic guilds (omnivores, herbivores and predators) and assessed the topological structure of intrapopulation plant-arthropod networks in fragments and continuous forests. Habitat type influenced arthropod species abundance, diversity and composition with greater abundance in fragments but greater diversity in continuous forest. According to trophic guilds, coleopteran herbivores were more abundant in continuous forest and overall omnivores in fragments. Continuous forest showed a greater diversity of interactions than fragments. Only in fragments, however, did the arthropod community associated with H aurantiaca show a nested structure, suggesting novel and/or opportunistic host-arthropod associations. Plants, omnivores and predators contributed more to nestedness than herbivores. Therefore, Heliconia-arthropod network properties do not appear to be maintained in fragments mainly caused by the decrease of herbivores. Our study contributes to the understanding of the impact of fragmentation on the structure and dynamics of multitrophic arthropod communities associated with a particular plant species of the highly biodiverse tropical forests. Nevertheless, further replication of study sites is needed to strengthen the conclusion that forest fragmentation negatively affects arthropod assemblages.

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          Confounding factors in the detection of species responses to habitat fragmentation.

          Robert M. Ewers, Raphael Didham (2006)
          Habitat loss has pervasive and disruptive impacts on biodiversity in habitat remnants. The magnitude of the ecological impacts of habitat loss can be exacerbated by the spatial arrangement -- or fragmentation -- of remaining habitat. Fragmentation per se is a landscape-level phenomenon in which species that survive in habitat remnants are confronted with a modified environment of reduced area, increased isolation and novel ecological boundaries. The implications of this for individual organisms are many and varied, because species with differing life history strategies are differentially affected by habitat fragmentation. Here, we review the extensive literature on species responses to habitat fragmentation, and detail the numerous ways in which confounding factors have either masked the detection, or prevented the manifestation, of predicted fragmentation effects. Large numbers of empirical studies continue to document changes in species richness with decreasing habitat area, with positive, negative and no relationships regularly reported. The debate surrounding such widely contrasting results is beginning to be resolved by findings that the expected positive species-area relationship can be masked by matrix-derived spatial subsidies of resources to fragment-dwelling species and by the invasion of matrix-dwelling species into habitat edges. Significant advances have been made recently in our understanding of how species interactions are altered at habitat edges as a result of these changes. Interestingly, changes in biotic and abiotic parameters at edges also make ecological processes more variable than in habitat interiors. Individuals are more likely to encounter habitat edges in fragments with convoluted shapes, leading to increased turnover and variability in population size than in fragments that are compact in shape. Habitat isolation in both space and time disrupts species distribution patterns, with consequent effects on metapopulation dynamics and the genetic structure of fragment-dwelling populations. Again, the matrix habitat is a strong determinant of fragmentation effects within remnants because of its role in regulating dispersal and dispersal-related mortality, the provision of spatial subsidies and the potential mediation of edge-related microclimatic gradients. We show that confounding factors can mask many fragmentation effects. For instance, there are multiple ways in which species traits like trophic level, dispersal ability and degree of habitat specialisation influence species-level responses. The temporal scale of investigation may have a strong influence on the results of a study, with short-term crowding effects eventually giving way to long-term extinction debts. Moreover, many fragmentation effects like changes in genetic, morphological or behavioural traits of species require time to appear. By contrast, synergistic interactions of fragmentation with climate change, human-altered disturbance regimes, species interactions and other drivers of population decline may magnify the impacts of fragmentation. To conclude, we emphasise that anthropogenic fragmentation is a recent phenomenon in evolutionary time and suggest that the final, long-term impacts of habitat fragmentation may not yet have shown themselves.
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            The architecture of mutualistic networks minimizes competition and increases biodiversity.

            Ugo Bastolla, Miguel A. Fortuna, Alberto Pascual-García … (2009)
            The main theories of biodiversity either neglect species interactions or assume that species interact randomly with each other. However, recent empirical work has revealed that ecological networks are highly structured, and the lack of a theory that takes into account the structure of interactions precludes further assessment of the implications of such network patterns for biodiversity. Here we use a combination of analytical and empirical approaches to quantify the influence of network architecture on the number of coexisting species. As a case study we consider mutualistic networks between plants and their animal pollinators or seed dispersers. These networks have been found to be highly nested, with the more specialist species interacting only with proper subsets of the species that interact with the more generalist. We show that nestedness reduces effective interspecific competition and enhances the number of coexisting species. Furthermore, we show that a nested network will naturally emerge if new species are more likely to enter the community where they have minimal competitive load. Nested networks seem to occur in many biological and social contexts, suggesting that our results are relevant in a wide range of fields.
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              Plant responses to insect herbivory: the emerging molecular analysis.

              André Kessler, Ian Baldwin (2002)
              Plants respond to herbivore attack with a bewildering array of responses, broadly categorized as direct and indirect defenses, and tolerance. Plant-herbivore interactions are played out on spatial scales that include the cellular responses, well-studied in plant-pathogen interactions, as well as responses that function at whole-plant and community levels. The plant's wound response plays a central role but is frequently altered by insect-specific elicitors, giving plants the potential to optimize their defenses. In this review, we emphasize studies that advance the molecular understanding of elicited direct and indirect defenses and include verifications with insect bioassays. Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses. Such organizational elements could help elucidate the molecular control over the diversity of responses elicited by herbivore attack.
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                Author and article information

                Contributors
                Tadashi Fukami: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 5 January 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 1
                Electronic Location Identifier: e0146461
                Affiliations
                [1 ]Laboratorio de Ecología del Hábitat Alterado, Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México (UNAM), Morelia, Michoacán, Mexico
                [2 ]Instituto de Ecología AC, Red de Ecoetología, Xalapa, Veracruz, Mexico
                [3 ]Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Apartado postal 69–1, 42001 Pachuca, Hidalgo, Mexico
                [4 ]Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, A.P. 70–153, México, Distrito Federal C. P., 04510
                [5 ]Instituto de Ecología AC, Red de Ecología Funcional, Xalapa, Veracruz, Mexico
                [6 ]Universidad Intercultural de Chiapas, Unidad Académica Multidisciplinaria Las Margaritas, Chiapas, Mexico
                Stanford University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JBM. Performed the experiments: APMF RL. Analyzed the data: WD APMF. Contributed reagents/materials/analysis tools: JBM WD CD SL JV RL. Wrote the paper: JBM WD. Conceived of the study, designed the study, coordinated the study and drafted the manuscript: JBM. Carried out the ecological network analyses and helped draft the manuscript: WD. Collected field data, helped draft the manuscript and carried out statistical tests: APMF. Identified the arthropod species: CDB JV SL. Collected the specimens RL. Gave final approval for publication: JBM WD APMF CD SL JV RL.

                Article
                Publisher ID: PONE-D-15-32878
                DOI: 10.1371/journal.pone.0146461
                PMC ID: 4701723
                PubMed ID: 26731271
                SO-VID: 0e4c3197-e6c1-4ae9-8c11-ba66ee04d9b3
                Copyright © © 2016 Benítez-Malvido et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 29 July 2015
                Date accepted : 17 December 2015
                Page count
                Figures: 4, Tables: 1, Pages: 15
                Funding
                This work was supported by financial and logistic support from Universidad Nacional Autónoma de México (UNAM) Project PAPIIT IN214014 to JBM and for a sabbatical grant to JBM at the Instituto Mediterráneo de Estudios Avanzados (IMEDEA). WD was supported by CNPq grant 237339/2012-9, and APMF by a postdoctoral scholarship from UNAM. The Comisión Nacional de Áreas Naturales Protegidas (CONANP), permission number SGPA/DGVS/07830)) granted permits to work in the MABR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
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                Data Availability All relevant data are within the paper.

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