High-order interactions maintain or enhance structural robustness of a coffee agroecosystem network

Abstract The capacity of highly diverse systems to prevail has proven difficult to explain. In addition to methodological issues, the inherent complexity of ecosystems and issues like multicausality, non-linearity and context-specificity make it hard to establish general and unidirectional explanations. Nevertheless, in recent years, high order interactions have been increasingly discussed as a mechanism that benefits the functioning of highly diverse ecosystems and may add to the mechanisms that explain their persistence. Until now, this idea has been explored by means of hypothetical simulated networks. Here, we test this idea using an updated and empirically documented network for a coffee agroecosystem. We identify potentially key nodes and measure network robustness in the face of node removal with and without incorporation of high order interactions. We find that the system's robustness is either increased or unaffected by the addition of high order interactions, in contrast with randomized counterparts with similar structural characteristics. We also propose a method for representing networks with high order interactions as ordinary graphs and a method for measuring their robustness.

[1]  B. Cai,et al.  Corrigendum: Epidemiology study of HBV genotypes and antiviral drug resistance in multi-ethnic regions from Western China , 2016, Scientific Reports.

[2]  Yong Liu,et al.  Cyanobacterial bloom induces structural and functional succession of microbial communities in eutrophic lake sediments. , 2021, Environmental pollution.

[3]  F. Jordán,et al.  Non‐trophic key players in aquatic ecosystems: a mesocosm experiment , 2020 .

[4]  J. Vandermeer,et al.  Contrasting bee foraging in response to resource scale and local habitat management , 2009 .

[5]  S. Savary,et al.  Effects of crop management patterns on coffee rust epidemics , 2004 .

[6]  Hamid Reza Pourghasemi,et al.  A machine learning framework for multi-hazards modeling and mapping in a mountainous area , 2020, Scientific Reports.

[7]  Ted J. Case,et al.  Higher Order Interactions in Ecological Communities: What Are They and How Can They be Detected? , 1994 .

[8]  César A. Hidalgo,et al.  Scale-free networks , 2008, Scholarpedia.

[9]  F. Jordán,et al.  Combining centrality indices: Maximizing the predictability of keystone species in food webs , 2021, Ecological Indicators.

[10]  L. Lawlor.  A Comment on Randomly Constructed Model Ecosystems , 1978, The American Naturalist.

[11]  J. Vandermeer,et al.  Ants defend coffee from berry borer colonization , 2013, BioControl.

[12]  Duanbing Chen,et al.  Vital nodes identification in complex networks , 2016, ArXiv.

[13]  Stacy M. Philpott,et al.  Ecological Complexity and Pest Control in Organic Coffee Production: Uncovering an Autonomous Ecosystem Service , 2010 .

[14]  Paul J. Laurienti,et al.  The Ubiquity of Small-World Networks , 2011, Brain Connect..

[15]  Joseph S. Wright.  Plant diversity in tropical forests: a review of mechanisms of species coexistence , 2017, Oecologia.

[16]  M. Loreau,et al.  Resilience, reactivity and variability: A mathematical comparison of ecological stability measures. , 2015, Journal of theoretical biology.

[17]  P. Guimarães,et al.  The structure of ant-plant ecological networks: is abundance enough? , 2014, Ecology.

[18]  A. Damon,et al.  A review of the biology and control of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). , 2000, Bulletin of entomological research.

[19]  Jody M. Webster,et al.  Erratum: Intensification of the meridional temperature gradient in the Great Barrier Reef following the Last Glacial Maximum (Nature Communications (2014) 5 (4102) DOI: 10.1038/ncomms5102) , 2016 .

[20]  P. Chesson.  Mechanisms of Maintenance of Species Diversity , 2000 .

[21]  ROBERT M. MAY,et al.  Will a Large Complex System be Stable? , 1972, Nature.

[22]  H. Liere,et al.  Cascading trait‐mediation: disruption of a trait‐mediated mutualism by parasite‐induced behavioral modification , 2010 .

[23]  Stefano Allesina,et al.  Beyond pairwise mechanisms of species coexistence in complex communities , 2017, Nature.

[24]  Albert-László Barabási,et al.  Error and attack tolerance of complex networks , 2000, Nature.

[25]  Ferenc Jordán,et al.  Food web dynamics in trophic hierarchies , 2018 .

[26]  D. Gonthier,et al.  Cryptic biodiversity effects: importance of functional redundancy revealed through addition of food web complexity. , 2012, Ecology.

[27]  I. Perfecto,et al.  Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico , 2003 .

[28]  Stephen H. Levine,et al.  Competitive Interactions in Ecosystems , 1976, The American Naturalist.

[29]  H. Manns,et al.  Cropping system yield stability in response to plant diversity and soil organic carbon in temperate ecosystems , 2018 .

[30]  Daniel B. Stouffer,et al.  Higher-order interactions capture unexplained complexity in diverse communities , 2017, Nature Ecology &Evolution.

[31]  Teja Tscharntke,et al.  Fruit set of highland coffee increases with the diversity of pollinating bees , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  S. Philpott,et al.  Parasite Lost: Chemical and Visual Cues Used by Pseudacteon in Search of Azteca instabilis , 2010, Journal of Insect Behavior.

[33]  Jean-Gabriel Young,et al.  Networks beyond pairwise interactions: structure and dynamics , 2020, ArXiv.

[34]  H. Caswell,et al.  ALTERNATIVES TO RESILIENCE FOR MEASURING THE RESPONSES OF ECOLOGICAL SYSTEMS TO PERTURBATIONS , 1997 .

[35]  M. Benítez,et al.  Combined effect of matrix quality and spatial heterogeneity on biodiversity decline , 2018, bioRxiv.

[36]  Gary P. Griffith,et al.  Identifying important species that amplify or mitigate the interactive effects of human impacts on marine food webs , 2018, Conservation biology : the journal of the Society for Conservation Biology.

[37]  E. Kalko,et al.  Bats Limit Arthropods and Herbivory in a Tropical Forest , 2008, Science.

[38]  Serguei Saavedra,et al.  A structural approach for understanding multispecies coexistence , 2017 .

[39]  J. Cusack,et al.  Integrating conflict, lobbying, and compliance to predict the sustainability of natural resource use , 2020 .

[40]  J. Vandermeer,et al.  Ants (Azteca sp.) as potential biological control agents in shade coffee production in Chiapas, Mexico , 2002, Agroforestry Systems.

[41]  J. Grilli,et al.  Higher-order interactions stabilize dynamics in competitive network models , 2017, Nature.

[42]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[43]  J. Montoya,et al.  Small world patterns in food webs. , 2002, Journal of theoretical biology.

[44]  Ivette Perfecto,et al.  A Keystone Mutualism Drives Pattern in a Power Function , 2006, Science.

[45]  I. Perfecto,et al.  Impacts of major predators on tropical agroforest arthropods: comparisons within and across taxa , 2004, Oecologia.

[46]  W. Deen,et al.  Increasing Crop Diversity Mitigates Weather Variations and Improves Yield Stability , 2015, PloS one.

[47]  K. McCann.  The diversity–stability debate , 2000, Nature.

[48]  Kon Shing Kenneth Chung,et al.  Quantifying topological robustness of networks under sustained targeted attacks , 2013, Social Network Analysis and Mining.

[49]  J. Vandermeer,et al.  GREATER PREDATION IN SHADED COFFEE FARMS: THE ROLE OF RESIDENT NEOTROPICAL BIRDS , 2004 .

[50]  J. Vandermeer,et al.  Hypothenemus hampei (Coleoptera: Curculionidae) and its Interactions with Azteca instabilis and Pheidole synanthropica (Hymenoptera: Formicidae) in a Shade Coffee Agroecosystem , 2013, Environmental entomology.

[51]  S. Philpott.  Trait-Mediated Effects of Parasitic Phorid Flies (Diptera: Phoridae) on Ant (Hymenoptera: Formicidae) Competition and Resource Access in Coffee Agro-ecosystems , 2005 .

[52]  R. Macarthur.  Fluctuations of Animal Populations and a Measure of Community Stability , 1955 .

[53]  Amedeo Caflisch,et al.  The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. , 2010, Ecology letters.

[54]  J. Vandermeer,et al.  Spatial and Temporal Dynamics of a Fungal Pathogen Promote Pattern Formation in a Tropical Agroecosystem , 2009 .

[55]  David P. M. Lam,et al.  Research pathways to foster transformation: linking sustainability science and social-ecological systems research , 2020 .

[56]  S. Carpenter,et al.  Stability and Diversity of Ecosystems , 2007, Science.

[57]  Serguei Saavedra,et al.  Structural forecasting of species persistence under changing environments. , 2020, Ecology letters.

[58]  J. Vandermeer,et al.  Hysteresis and critical transitions in a coffee agroecosystem , 2019, Proceedings of the National Academy of Sciences.

[59]  Daniel B. Stouffer,et al.  Keystoneness, centrality, and the structural controllability of ecological networks , 2019, Journal of Ecology.

[60]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[61]  U. Dieckmann,et al.  Complexity and stability of ecological networks: a review of the theory , 2018, Population Ecology.

[62]  S. Carpenter,et al.  Global Consequences of Land Use , 2005, Science.

[63]  M. Uriarte,et al.  Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Peter B Adler,et al.  Trait-based tests of coexistence mechanisms. , 2013, Ecology Letters.

[65]  W. Worthen,et al.  Higher-Order Interactions and Indirect Effects: A Resolution Using Laboratory Drosophila Communities , 1991, The American Naturalist.

[66]  V. de Crécy-Lagard,et al.  A network approach to elucidate and prioritize microbial dark matter in microbial communities , 2020, The ISME journal.

[67]  J. Vandermeer,et al.  The dynamics of the coffee rust disease: an epidemiological approach using network theory , 2018, European Journal of Plant Pathology.

[68]  Alvaro Sanchez,et al.  Defining Higher-Order Interactions in Synthetic Ecology: Lessons from Physics and Quantitative Genetics. , 2019, Cell systems.

[69]  D. Gruner,et al.  Interactions among predators and the cascading effects of vertebrate insectivores on arthropod communities and plants , 2010, Proceedings of the National Academy of Sciences.

[70]  T. Schoener,et al.  PREDATION ON A COMMON ANOLIS LIZARD: CAN THE FOOD-WEB EFFECTS OF A DEVASTATING PREDATOR BE REVERSED? , 2002 .

[71]  S. Philpott,et al.  Cascading Indirect Effects in a Coffee Agroecosystem: Effects of Parasitic Phorid Flies on Ants and the Coffee Berry Borer in a High-Shade and Low-Shade Habitat , 2011, Environmental entomology.

[72]  J. Vandermeer,et al.  The effect of an ant-hemipteran mutualism on the coffee berry borer (Hypothenemus hampei) in southern Mexico. , 2006 .

[73]  B. Krasnov,et al.  Species abundance and the distribution of specialization in host–parasite interaction networks , 2005 .

[74]  H. Liere,et al.  Cascading trait-mediated interactions induced by ant pheromones , 2012, Ecology and evolution.

[75]  Erik E. Westlund,et al.  Ecological Networks over the Edge: Hypergraph Trait-Mediated Indirect Interaction (TMII) Structure. , 2016, Trends in ecology & evolution.

[76]  Eyal Bairey,et al.  High-order species interactions shape ecosystem diversity , 2016, Nature Communications.

[77]  J. Bernal,et al.  Impact of natural enemies on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics in Chiapas, Mexico. , 2009 .

[78]  M. Picanço,et al.  Insecticide use and organophosphate resistance in the coffee leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae) , 2002, Bulletin of Entomological Research.

[79]  Matthew D. Johnson,et al.  Pest reduction services by birds in shade and sun coffee in Jamaica , 2010 .

[80]  S. Philpott,et al.  Arboreal Ant Abundance and Leaf Miner Damage in Coffee Agroecosystems in Mexico , 2008 .

[81]  O. Schmitz,et al.  Linearity in the aggregate effects of multiple predators in a food web , 2002 .

[82]  G. R. Young.  Recent work on biological control in Papua New Guinea and some suggestions for the future , 1982 .

[83]  S. Peacor,et al.  A REVIEW OF TRAIT-MEDIATED INDIRECT INTERACTIONS IN ECOLOGICAL COMMUNITIES , 2003 .

[84]  M. Benítez,et al.  Cognitive Maps Across Multiple Social Sectors: Shared and Unique Perceptions on the Quality of Agricultural Soils in Mexico , 2021, Frontiers in Sustainable Food Systems.

[85]  L. Lawlor,et al.  Structure and Stability in Natural and Randomly Constructed Competitive Communities , 1980, The American Naturalist.

[86]  J. Timothy Wootton,et al.  Indirect Effects and Habitat Use in an Intertidal Community: Interaction Chains and Interaction Modifications , 1993, The American Naturalist.

[87]  J. Vandermeer,et al.  Bats Limit Insects in a Neotropical Agroforestry System , 2008, Science.

[88]  J. Vandermeer,et al.  Clusters of ant colonies and robust criticality in a tropical agroecosystem , 2008, Nature.

[89]  A. Larsen,et al.  Twig‐Nesting Ants: The Hidden Predators of the Coffee Berry Borer in Chiapas, Mexico , 2010 .

[90]  Piraveenan Mahendra,et al.  On the Influence of Topological Characteristics on Robustness of Complex Networks , 2013, J. Artif. Intell. Soft Comput. Res..

[91]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[92]  Jiming Liu,et al.  The robustness of ecosystems to the species loss of community , 2016, Scientific Reports.

[93]  Neo D. Martinez,et al.  Network structure and biodiversity loss in food webs: robustness increases with connectance , 2002, Ecology Letters.

[94]  K. Gurney,et al.  Network ‘Small-World-Ness’: A Quantitative Method for Determining Canonical Network Equivalence , 2008, PloS one.

[95]  Stephen Muggleton,et al.  Provided for Non-commercial Research and Educational Use Only. Not for Reproduction, Distribution or Commercial Use. Networking Agroecology: Integrating the Diversity of Agroecosystem Interactions , 2022 .

[96]  Neal M. Williams,et al.  Species abundance and asymmetric interaction strength in ecological networks , 2007 .

[97]  H. Liere,et al.  Cheating on a Mutualism: Indirect Benefits of Ant Attendance to a Coccidophagous Coccinellid , 2008, Environmental entomology.

[98]  H. Liere,et al.  Evidence for hyperparasitism of coffee rust (Hemileia vastatrix) by the entomogenous fungus, Lecanicillium lecanii, through a complex ecological web , 2009 .

[99]  Sonia Kéfi,et al.  More than a meal… integrating non-feeding interactions into food webs. , 2012, Ecology letters.

[100]  J. Vandermeer,et al.  Ecological complexity and contingency: Ants and lizards affect biological control of the coffee leaf miner in Puerto Rico , 2021 .