Abstract
Mutualistic systems can experience abrupt and irreversible regime shifts caused by local or global stressors. Despite decades of efforts to understand ecosystem dynamics and determine whether a tipping point could occur, there are no current approaches to estimate distances (in state/parameter space) to tipping points and compare the distances across various mutualistic systems. Here we develop a general dimension-reduction approach that simultaneously compresses the natural control and state parameters of high-dimensional complex systems and introduces a scaling factor for recovery rates. Our theoretical framework places various systems with entirely different dynamical parameters, network structure and state perturbations on the same scale. More importantly, it compares distances to tipping points across different systems on the basis of data on abundance and topology. By applying the method to 54 real-world mutualistic networks, our analytical results unveil the network characteristics and system parameters that control a system’s resilience. We contribute to the ongoing efforts in developing a general framework for mapping and predicting distance to tipping points of ecological and potentially other systems.
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Data availability
All network and abundance data can be accessed through https://doi.org/10.5281/zenodo.6784072.
Code availability
All code used in this study is available on Zenodo at https://doi.org/10.5281/zenodo.6784072.
References
Aizen, M. A., Sabatino, M. & Tylianakis, J. M. Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335, 1486–1489 (2012).
Aanen, D. K. et al. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl Acad. Sci. USA 99, 14887–14892 (2002).
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. & Hudson, P. J. Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840–844 (2004).
Jaeggi, A. V. & Gurven, M. Natural cooperators: food sharing in humans and other primates. Evol. Anthropol. 22, 186–195 (2013).
Van Der Maas, H. L., Kan, K.-J., Marsman, M. & Stevenson, C. E. Network models for cognitive development and intelligence. J. Intell. 5, 16 (2017).
Bascompte, J. & Jordano, P. Plant-animal mutualistic networks: the architecture of biodiversity. Annu. Rev. Ecol. Evol. Syst. 38, 567–593 (2007).
Bastolla, U. et al. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018 (2009).
Valverde, S. et al. The architecture of mutualistic networks as an evolutionary spandrel. Nat. Ecol. Evol. 2, 94–99 (2018).
Vizentin-Bugoni, J. et al. Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai’i. Science 364, 78–82 (2019).
Bascompte, J. Disentangling the web of life. Science 325, 416–419 (2009).
Liu, X. et al. Network resilience. Phys. Rep. 971, 1–108 (2022).
Rezende, E. L., Lavabre, J. E., Guimarães, P. R., Jordano, P. & Bascompte, J. Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448, 925–928 (2007).
Pocock, M. J., Evans, D. M. & Memmott, J. The robustness and restoration of a network of ecological networks. Science 335, 973–977 (2012).
Fowler, J. H. & Christakis, N. A. Cooperative behavior cascades in human social networks. Proc. Natl Acad. Sci. USA 107, 5334–5338 (2010).
May, R. M., Levin, S. A. & Sugihara, G. Complex systems: ecology for bankers. Nature 451, 893–894 (2008).
Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856 (2010).
Berdugo, M. et al. Global ecosystem thresholds driven by aridity. Science 367, 787–790 (2020).
Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929 (2008).
Biggs, R. O., Peterson, G. & Rocha, J. C. The regime shifts database: a framework for analyzing regime shifts in social-ecological systems. Ecol. Soc. 23, 3 (2018).
Walker, B. & Meyers, J. A. Thresholds in ecological and social-ecological systems: a developing database. Ecol. Soc. 9, 2 (2004).
Hirota, M., Holmgren, M., Van Nes, E. H. & Scheffer, M. Global resilience of tropical forest and savanna to critical transitions. Science 334, 232–235 (2011).
Barnosky, A. D. et al. Approaching a state shift in earth’s biosphere. Nature 486, 52–58 (2012).
Dakos, V. & Bascompte, J. Critical slowing down as early warning for the onset of collapse in mutualistic communities. Proc. Natl Acad. Sci. USA 111, 17546–17551 (2014).
Lever, J. J., van Nes, E. H., Scheffer, M. & Bascompte, J. The sudden collapse of pollinator communities. Ecol. Lett. 17, 350–359 (2014).
Lever, J. J. et al. Foreseeing the future of mutualistic communities beyond collapse. Ecol. Lett. 23, 2–15 (2020).
Hillebrand, H. et al. Thresholds for ecological responses to global change do not emerge from empirical data. Nat. Ecol. Evol. 4, 1502–1509 (2020).
Dudney, J. & Suding, K. N. The elusive search for tipping points. Nat. Ecol. Evol. 4, 1449–1450 (2020).
Scheffer, M. et al. Anticipating critical transitions. Science 338, 344–348 (2012).
Martin, S., Deffuant, G. & Calabrese, J. M. in Viability and Resilience of Complex Systems (eds. Deffuant, G., & Gilbert, N.) 15–36 (Springer, 2011).
Cohen, R., Erez, K., Ben-Avraham, D. & Havlin, S. Resilience of the internet to random breakdowns. Phys. Rev. Lett. 85, 4626–4628 (2000).
Gao, J., Barzel, B. & Barabási, A.-L. Universal resilience patterns in complex networks. Nature 530, 307–312 (2016).
Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).
Boettiger, C. & Hastings, A. Quantifying limits to detection of early warning for critical transitions. J. R. Soc. Interface 9, 2527–2539 (2012).
Blanchard, J. L. A rewired food web. Nature 527, 173–174 (2015).
Campbell, C., Yang, S., Shea, K. & Albert, R. Topology of plant-pollinator networks that are vulnerable to collapse from species extinction. Phys. Rev. E 86, 021924 (2012).
Revilla, T. A., Encinas-Viso, F. & Loreau, M. Robustness of mutualistic networks under phenological change and habitat destruction. Oikos 124, 22–32 (2015).
Vizentin-Bugoni, J. et al. Ecological correlates of species’ roles in highly invaded seed dispersal networks. Proc. Natl Acad. Sci. USA 118, (2021).
Whanpetch, N. et al. Temporal changes in benthic communities of seagrass beds impacted by a tsunami in the Andaman Sea, Thailand. Estuar. Coast. Shelf Sci. 87, 246–252 (2010).
Orth, R. J. et al. Restoration of seagrass habitat leads to rapid recovery of coastal ecosystem services. Sci. Adv. 6, eabc6434 (2020).
Veraart, A. J. et al. Recovery rates reflect distance to a tipping point in a living system. Nature 481, 357–359 (2012).
Dai, L., Vorselen, D., Korolev, K. S. & Gore, J. Generic indicators for loss of resilience before a tipping point leading to population collapse. Science 336, 1175–1177 (2012).
Dakos, V., van Nes, E. H., d’Odorico, P. & Scheffer, M. Robustness of variance and autocorrelation as indicators of critical slowing down. Ecology 93, 264–271 (2012).
van Belzen, J. et al. Vegetation recovery in tidal marshes reveals critical slowing down under increased inundation. Nat. Commun. 8, 15811 (2017).
Rohr, R. P., Saavedra, S. & Bascompte, J. On the structural stability of mutualistic systems. Science 345, 1253497 (2014).
Wright, D. H. A simple, stable model of mutualism incorporating handling time. Am. Nat.134, 664–667 (1989).
Newman, M. E. J. Networks: An Introduction (Oxford Univ. Press, 2010).
Jiang, J. et al. Predicting tipping points in mutualistic networks through dimension reduction. Proc. Natl Acad. Sci. USA 115, E639–E647 (2018).
Gao, J., Buldyrev, S. V., Stanley, H. E. & Havlin, S. Networks formed from interdependent networks. Nat. Phys. 8, 40–48 (2012).
May, R. M. Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature 269, 471–477 (1977).
Moreno, Y., Pastor-Satorras, R., Vázquez, A. & Vespignani, A. Critical load and congestion instabilities in scale-free networks. Europhys. Lett. 62, 292–298 (2003).
Martinez, N. D., Williams, R. J., Dunne, J. A. & Pascual, M. in Ecological Networks: Linking Structure to Dynamics in Food Webs (eds. Pascual, M., Dunne, J. A., & Dunne, J. A.) 163–185 (Oxford University Press, 2006).
Chen, S., O’Dea, E. B., Drake, J. M. & Epureanu, B. I. Eigenvalues of the covariance matrix as early warning signals for critical transitions in ecological systems. Sci. Rep. 9, 1–14 (2019).
Suweis, S., Simini, F., Banavar, J. R. & Maritan, A. Emergence of structural and dynamical properties of ecological mutualistic networks. Nature 500, 449–452 (2013).
Mariani, M. S., Ren, Z.-M., Bascompte, J. & Tessone, C. J. Nestedness in complex networks: observation, emergence, and implications. Phys. Rep. 813, 1–90 (2019).
Staniczenko, P. P., Kopp, J. C. & Allesina, S. The ghost of nestedness in ecological networks. Nat. Commun. 4, 1–6 (2013).
Marsh, H. et al. Optimizing allocation of management resources for wildlife. Conserv. Biol. 21, 387–399 (2007).
Dakos, V. et al. Slowing down as an early warning signal for abrupt climate change. Proc. Natl Acad. Sci. USA 105, 14308–14312 (2008).
Reyer, C. P. et al. Forest resilience and tipping points at different spatio-temporal scales: approaches and challenges. J. Ecol. 103, 5–15 (2015).
Dakos, V. et al. Ecosystem tipping points in an evolving world. Nat. Ecol. Evol. 3, 355–362 (2019).
Hurwicz, L. The design of mechanisms for resource allocation. Am. Econ. Rev. 63, 1–30 (1973).
Almeida-Neto, M. & Ulrich, W. A straightforward computational approach for measuring nestedness using quantitative matrices. Environ. Model. Softw. 26, 173–178 (2011).
Atmar, W. & Patterson, B. D. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96, 373–382 (1993).
Kéfi, S. et al. Spatial vegetation patterns and imminent desertification in Mediterranean arid ecosystems. Nature 449, 213–217 (2007).
Dakos, V., van Nes, E. H., Donangelo, R., Fort, H. & Scheffer, M. Spatial correlation as leading indicator of catastrophic shifts. Theor. Ecol. 3, 163–174 (2010).
Buldyrev, S. V., Parshani, R., Paul, G., Stanley, H. E. & Havlin, S. Catastrophic cascade of failures in interdependent networks. Nature 464, 1025–1028 (2010).
Web of Life, Ecological Networks Database (Bascompte Lab, accessed 12 June 2017); http://www.web-of-life.es/map.php?type=5/
Gleeson, J. P., Melnik, S., Ward, J. A., Porter, M. A. & Mucha, P. J. Accuracy of mean-field theory for dynamics on real-world networks. Phys. Rev. E 85, 026106 (2012).
Strogatz, S. H. Nonlinear Dynamics and Chaos: with Applications to Physics, Biology, Chemistry, and Engineering (CRC Press, 2018).
Vázquez, D. P. Interactions Among Introduced Ungulates, Plants, and Pollinators: a Field Study in the Temperate Forest of the Southern Andes PhD thesis, University of Tennessee (2002).
Kaiser-Bunbury, C. N., Vázquez, D. P., Stang, M. & Ghazoul, J. Determinants of the microstructure of plant-pollinator networks. Ecology 95, 3314–3324 (2014).
Memmott, J. The structure of a plant-pollinator food web. Ecol. Lett. 2, 276–280 (1999).
Dicks, L., Corbet, S. & Pywell, R. Compartmentalization in plant-insect flower visitor webs. J. Anim. Ecol. 71, 32–43 (2002).
SMITH-RAMÍREZ, C., Martinez, P., Nunez, M., González, C. & Armesto, J. J. Diversity, flower visitation frequency and generalism of pollinators in temperate rain forests of Chiloé Island, Chile. Bot. J. Linn. Soc. 147, 399–416 (2005).
Dupont, Y. L., Hansen, D. M. & Olesen, J. M. Structure of a plant-flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands. Ecography 26, 301–310 (2003).
Dupont, Y. L. & Olesen, J. M. Ecological modules and roles of species in heathland plant-insect flower visitor networks. J. Anim. Ecol. 78, 346–353 (2009).
Acknowledgements
W.Z. acknowledges support from the National Natural Science Foundation of China (grant nos. 61702200, 61473183, U1509211 and 61627810) and National Key R&D Program of China grant no. 2017YFE0128500. J.G. acknowledges the support of the USA National Science Foundation under Grant No. 2047488, and the Rensselaer-IBM AI Research Collaboration.. Q.W. was partially supported by the US National Science Foundation (grant no. 1761950 and 2125326). We sincerely thank J. Bascompte for early discussion and detailed suggestions that helped improve our paper.
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All authors designed and conducted the research. H.Z. and J.G. performed the analytical and numerical calculations. H.Z., Q.W. and J.G. carried out analysis and interpreted the data. J.G. led the writing of the manuscript.
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Extended data
Extended Data Fig. 1 54 real ecological networks with abundance values from 8 locations.
We obtained 54 pollination networks with real proportional abundances from references listed above (‘Ref.’), including 51 weighted networks (Table S3) and 3 unweighted ones (Table S4), spread in 8 locations world-wide. We sorted the effective abundance ratio decently as A - H. ‘ID’ is the network’s code shown in ‘web of life’66, ‘LAT’ refers to the latitude of one location, and ‘LONG’ refers to its longitude.
Extended Data Fig. 2 The characteristics of the real networks analysed in the paper.
‘ID’ is the identity of one network recorded in the website66. ‘∣P∣’, ‘∣A∣’ denotes the number of plant and animal species respectively. ‘∣links∣’ is the number of links in a network. ‘C’ is the connectivity of a network. ‘HP’ and ‘HA’ are the heterogeneity of the plant and animal sub-networks respectively. ‘γ’ is the effective mutual strength. ‘\(\left\langle {{{\rm{err}}}}\right\rangle\)’ is the prediction error of our method for each network. For data sources and references, see Supplementary Prediction error.
Extended Data Fig. 3 The robustness of the proposed resilience function for non-transition case.
The proposed resilience function (the gray curve, theoretical prediction obtained from equation (1) with βs = 100 and β = 10) predicts well the resilience of 28 weighted networks (see supplementary Table S2) without transition, under different parameters: α = 2, α = 1, α = − 1, h = 0.8, h = 0.5 and h = 0.2. Moreover, it is robust to competition typologies by assigning three different linking probabilities: 20% (light blue), 50% (blue), and 100% (red).
Extended Data Fig. 4 Prediction fails with large inter-competition strengths and high heterogeneity.
a-b, Test how inter-competition strength influence the prediction on a synthetic system with a plants’ inter-competition network A (a 100*100 ER network), an animals’ inter-competition matrix C (a 150*150 ER network), and a mutualistic network (a 100*150 ER network), with homogeneous inter-competition βij and mean degree 5. a, The simulation results of the effective abundance for all species (‘S’, obtained by solving the high-dimensional equations equation (2)) fit well with the theoretical prediction (‘T’, obtained by numerically solving 1D function \(\frac{dx}{dt}=x(\alpha -{\beta }_{w}x+\frac{\gamma x}{1+h\gamma x})\) directly) when the inter-specific competition strength βij is small (βij < 0.2 for certain mutual strength γ0 = [3, 5, 15]). However, the prediction fails with large inter-competition βij. b, For one γ0, we calculate the prediction error (difference between ‘S’ and ‘T’) for βij = [0.1, 0.2, 0.5, 1] respectively. In each box, there are 15 points (γ0 = [1: 15]). The central mark indicates the median, the bottom and top edges of the box indicate the 25th and 75th percentiles respectively, while the whiskers extend to the most extreme data points not considered outliers (the outliers are marked with ‘+’). c, We show how the heterogeneity of a mutualistic network influences the prediction accuracy applied to 39 real mutualistic networks in Fig. 2q. Firstly, we project each system into two networks31 and then calculate the heterogeneity of the two networks that is, HP and HA, respectively. d, We compare the calculation time between the full system (equation (1)) and the decoupled system (first solve equation (3) and then put xeff and xeco into equation (4)), for 10 random graphs. Data are presented as mean values +/- SEM. CPU: Single core in Intel(R) Xeon(R) CPU E5-2683 v4 @ 2.10GHz. Parameter setting: h = 0.2, \({\alpha }^{(P)}=-0.{3}_{{N}^{{{{\rm{I}}}}}\times 1}\), \({\alpha }^{(A)}=-0.{3}_{{N}^{{{{\rm{II}}}}}\times 1}\), \({\beta }_{S}^{(P)}={{{\rm{diag}}}}({3}_{{N}^{{{{\rm{I}}}}}\times 1})\), \({\beta }_{S}^{(A)}={{{\rm{diag}}}}({3}_{{N}^{{{{\rm{II}}}}}\times 1})\), \({\gamma }_{ij}={\varepsilon }_{ij}{\gamma }_{0}/{({s}_{i})}^{\delta }\), δ = 0.5.
Extended Data Fig. 5 The prediction of resilience in supply chain networks.
The resilience is tested against: (1) perturbation in links (a-d, for mutualistic network), and (2) perturbation in nodes (e-h). Link perturbation has two variations: increasing/decreasing (that is competition/mutualism) the average weight to a fraction fw of their original value; and extinction of a fraction fL of links. Node perturbation also has two variations: extinction of a fraction fsN of suppliers; extinction of a fraction fmN of manufacturers. i, All data (red points) in a-h uniformly collapse onto the resilience function (blue surface), indicating that regardless of the network structures and the forms of perturbation, the state of the system is captured by β and γ (see dynamics for supply chain networks in Supplementary Note 7).
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Supplementary Figs. 1–26, Discussion and Tables 1–6.
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Zhang, H., Wang, Q., Zhang, W. et al. Estimating comparable distances to tipping points across mutualistic systems by scaled recovery rates. Nat Ecol Evol 6, 1524–1536 (2022). https://doi.org/10.1038/s41559-022-01850-8
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DOI: https://doi.org/10.1038/s41559-022-01850-8