Rewiring and indirect effects underpin modularity reshuffling in a marine food web under environmental shifts

Abstract Species are characterized by physiological and behavioral plasticity, which is part of their response to environmental shifts. Nonetheless, the collective response of ecological communities to environmental shifts cannot be predicted from the simple sum of individual species responses, since co‐existing species are deeply entangled in interaction networks, such as food webs. For these reasons, the relation between environmental forcing and the structure of food webs is an open problem in ecology. To this respect, one of the main problems in community ecology is defining the role each species plays in shaping community structure, such as by promoting the subdivision of food webs in modules—that is, aggregates composed of species that more frequently interact—which are reported as community stabilizers. In this study, we investigated the relationship between species roles and network modularity under environmental shifts in a highly resolved food web, that is, a “weighted” ecological network reproducing carbon flows among marine planktonic species. Measuring network properties and estimating weighted modularity, we show that species have distinct roles, which differentially affect modularity and mediate structural modifications, such as modules reconfiguration, induced by environmental shifts. Specifically, short‐term environmental changes impact the abundance of planktonic primary producers; this affects their consumers’ behavior and cascades into the overall rearrangement of trophic links. Food web re‐adjustments are both direct, through the rewiring of trophic‐interaction networks, and indirect, with the reconfiguration of trophic cascades. Through such “systemic behavior,” that is, the way the food web acts as a whole, defined by the interactions among its parts, the planktonic food web undergoes a substantial rewiring while keeping almost the same global flow to upper trophic levels, and energetic hierarchy is maintained despite environmental shifts. This behavior suggests the potentially high resilience of plankton networks, such as food webs, to dramatic environmental changes, such as those provoked by global change.

[1]  D. Mason,et al.  Compartments revealed in food-web structure , 2003, Nature.

[2]  J. Lawton.  Structure of food webs , 1978, Nature.

[3]  F. Lombard,et al.  Mammoth grazers on the ocean's minuteness: a review of selective feeding using mucous meshes , 2018, Proceedings of the Royal Society B: Biological Sciences.

[4]  Laurent Dubroca,et al.  Stability and resilience in coastal copepod assemblages: The case of the Mediterranean long-term ecological research at Station MC (LTER-MC) , 2012 .

[5]  Dominique Gravel,et al.  The dissimilarity of species interaction networks. , 2012, Ecology letters.

[6]  Luis Pedro Coelho,et al.  Community‐Level Responses to Iron Availability in Open Ocean Plankton Ecosystems , 2019, Global Biogeochemical Cycles.

[7]  Ferenc Jord,et al.  Network ecology: topological constraints on ecosystem dynamics , 2004 .

[8]  Guadalupe Peralta,et al.  Non-random food-web assembly at habitat edges increases connectivity and functional redundancy. , 2017, Ecology.

[9]  Mathieu Bastian,et al.  Gephi: An Open Source Software for Exploring and Manipulating Networks , 2009, ICWSM.

[10]  Ferenc Jordán,et al.  Network ecology: Topological constraints on ecosystem dynamics , 2004 .

[11]  Dominique Gravel,et al.  Beyond species: why ecological interaction networks vary through space and time , 2014, bioRxiv.

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

[13]  P. Cury,et al.  Indicators quantifying small pelagic fish interactions: application using a trophic model of the southern Benguela ecosystem , 2004 .

[14]  G. Daily,et al.  Double keystone bird in a keystone species complex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[15]  C. Duarte,et al.  Oligotrophication and Metabolic Slowing-Down of a NW Mediterranean Coastal Ecosystem , 2017, Front. Mar. Sci..

[16]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[17]  D. D’Alelio.  Biological complexity behind plankton system functioning: Synthesis and perspectives from a marine Long Term Ecological Research , 2017 .

[18]  Neo D. Martinez,et al.  Food webs: reconciling the structure and function of biodiversity. , 2012, Trends in ecology & evolution.

[19]  Victoria J. Coles,et al.  Modelling the complexity of plankton communities exploiting omics potential: From present challenges to an integrative pipeline , 2019, Current Opinion in Systems Biology.

[20]  G. Paffenhöfer,et al.  From small scales to the big picture: persistence mechanisms of planktonic grazers in the oligotrophic ocean , 2007 .

[21]  Martin Rosvall,et al.  Maps of random walks on complex networks reveal community structure , 2007, Proceedings of the National Academy of Sciences.

[22]  J. Bascompte,et al.  Compartmentalization increases food-web persistence , 2011, Proceedings of the National Academy of Sciences.

[23]  Carl J. Walters,et al.  Ecopath with Ecosim: methods, capabilities and limitations , 2004 .

[24]  Stefano Allesina,et al.  Food web models: a plea for groups. , 2009, Ecology letters.

[25]  H. Charles J. Godfray,et al.  Experimental evidence for apparent competition in a tropical forest food web , 2004, Nature.

[26]  Carsten F. Dormann,et al.  Identifying Causes of Patterns in Ecological Networks: Opportunities and Limitations , 2017 .

[27]  Neil Rooney,et al.  A landscape theory for food web architecture. , 2008, Ecology letters.

[28]  P. Abreu,et al.  Human activities and climate variability drive fast‐paced change across the world's estuarine–coastal ecosystems , 2016, Global change biology.

[29]  Edward M. Reingold,et al.  Graph drawing by force‐directed placement , 1991, Softw. Pract. Exp..

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

[31]  M. Mello.  Keystone Species , 2019, Ecology.

[32]  G. Barabás,et al.  Self-regulation and the stability of large ecological networks , 2017, Nature Ecology & Evolution.

[33]  Ferenc Jordán,et al.  CoSBiLab Graph: The network analysis module of CoSBiLab , 2010, Environ. Model. Softw..

[34]  Temporal variation of keystone species and their impact on system performance in a South African estuarine ecosystem , 2017 .

[35]  J. Bascompte,et al.  Ecological networks : beyond food webs Ecological networks – beyond food webs , 2008 .

[36]  Olga Mangoni,et al.  Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends , 2004 .

[37]  J. Bascompte.  Networks in ecology , 2007 .

[38]  T. F. Hansen,et al.  Increased appendicularian zooplankton alter carbon cycling under warmer more acidified ocean conditions , 2017 .

[39]  Andrew J. Watson,et al.  Ecosystem dynamics based on plankton functional types for global ocean biogeochemistry models , 2005 .

[40]  U. Sommer,et al.  Warming and Acidification Effects on Planktonic Heterotrophic Pico- and Nanoflagellates in a Mesocosm Experiment. , 2016, Protist.

[41]  F. Jordán,et al.  Quantifying the importance of species and their interactions in a host-parasitoid community , 2003 .

[42]  R. Levins,et al.  Identifying keystone trophic groups in benthic ecosystems: Implications for fisheries management , 2013 .

[43]  D. Caron,et al.  Mixotrophy in the Marine Plankton. , 2017, Annual review of marine science.

[44]  V. Cardin,et al.  Evidence of zooplankton vertical migration from continuous Southern Adriatic buoy current-meter records , 2017, Progress in Oceanography.

[45]  Jens M. Olesen,et al.  Ecological networks in motion: Micro- and macroscopic variability across scales , 2016 .

[46]  F. Jordán.  Keystone species and food webs , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  Carl T. Bergstrom,et al.  The map equation , 2009, 0906.1405.

[48]  A. Ellis,et al.  Invariant antagonistic network structure despite high spatial and temporal turnover of interactions , 2017 .

[49]  Stefano Allesina,et al.  Modularity and stability in ecological communities , 2016, Nature Communications.

[50]  S. Dupont,et al.  Increased fitness of a key appendicularian zooplankton species under warmer, acidified seawater conditions , 2018, PloS one.

[51]  J. Memmott,et al.  Functional group diversity increases with modularity in complex food webs , 2015, Nature Communications.

[52]  Peer Bork,et al.  Determinants of community structure in the global plankton interactome , 2015, Science.

[53]  Ferenc Jordán,et al.  Weighting, scale dependence and indirect effects in ecological networks: A comparative study , 2007 .

[54]  Carsten F. Dormann,et al.  Ecological networks - foodwebs and beyond , 2009 .

[55]  Maurizio Ribera d’Alcalà,et al.  Ecological-network models link diversity, structure and function in the plankton food-web , 2016, Scientific Reports.

[56]  Robert Belshaw,et al.  The structure of an aphid–parasitoid community , 1999 .

[57]  Jordi Bascompte,et al.  Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. , 2009, Ecology letters.

[58]  Colin Fontaine,et al.  Stability of Ecological Communities and the Architecture of Mutualistic and Trophic Networks , 2010, Science.

[59]  Manuela Hartmann,et al.  Mixotrophic basis of Atlantic oligotrophic ecosystems , 2012, Proceedings of the National Academy of Sciences.

[60]  Andrea Lancichinetti,et al.  Community detection algorithms: a comparative analysis: invited presentation, extended abstract , 2009, VALUETOOLS.

[61]  H. Godfray,et al.  The structure of a leafminer–parasitoid community , 2000 .

[62]  Mercedes Pascual,et al.  The multilayer nature of ecological networks , 2015, Nature Ecology &Evolution.

[63]  J. Link,et al.  Emergent Properties Delineate Marine Ecosystem Perturbation and Recovery. , 2015, Trends in ecology & evolution.

[64]  D. Sarno,et al.  The green–blue swing: plasticity of plankton food-webs in response to coastal oceanographic dynamics , 2015 .

[65]  Oswald J. Schmitz,et al.  Trophic cascades : the primacy of trait-mediated indirect interactions , 2004 .

[66]  Jason M. Tylianakis,et al.  Ecological Networks Across Environmental Gradients , 2017 .

[67]  Luis Pedro Coelho,et al.  Plankton networks driving carbon export in the oligotrophic ocean , 2015, Nature.

[68]  S. Borgatti,et al.  Defining and measuring trophic role similarity in food webs using regular equivalence. , 2003, Journal of theoretical biology.

[69]  D. Pauly,et al.  A method for identifying keystone species in food web models , 2006 .

[70]  Adriana Zingone,et al.  Disentangling physical and biological drivers of phytoplankton dynamics in a coastal system , 2017, Scientific Reports.

[71]  D. Sarno,et al.  Plankton food-webs: to what extent can they be simplified? , 2016 .

[72]  H. Godfray,et al.  Indirect interactions in aphid–parasitoid communities , 1999, Researches on Population Ecology.

[73]  Santo Fortunato,et al.  Community detection in networks: A user guide , 2016, ArXiv.

[74]  Scott T. Grafton,et al.  Dynamic reconfiguration of human brain networks during learning , 2010, Proceedings of the National Academy of Sciences.

[75]  B. Patti,et al.  Benthic-pelagic coupling mediates interactions in Mediterranean mixed fisheries: An ecosystem modeling approach , 2019, PloS one.

[76]  T. F. Hansen,et al.  Copepods act as a switch between alternative trophic cascades in marine pelagic food webs , 2004 .

[77]  Michael Kaufmann,et al.  yFiles - Visualization and Automatic Layout of Graphs , 2001, Graph Drawing Software.

[78]  M. Aschan,et al.  Food‐web structure varies along environmental gradients in a high‐latitude marine ecosystem , 2018, Ecography.

[79]  Craig E. Nelson,et al.  Synchronous shifts in dissolved organic carbon bioavailability and bacterial community responses over the course of an upwelling‐driven phytoplankton bloom , 2015 .