Mechanisms promoting biodiversity in ecosystems

Abstract

Explaining biodiversity is the central focus in theoretical ecology. A significant obstacle arises from the competitive exclusion principle (CEP), which states that two species competing for the same type of resources cannot coexist at constant population densities, or more generally, the number of consumer species cannot exceed that of resource species at steady states. The conflict between CEP and biodiversity is exemplified by the paradox of the plankton, where a few types of limiting resources support a plethora of plankton species. In this review, we introduce mechanisms proposed over the years for promoting biodiversity in ecosystems, with a special focus on those that alleviate the constraints imposed by the CEP, including mechanisms that challenge the CEP in well-mixed systems at a steady state or those that circumvent its limitations through contextual differences.

Keywords

biodiversity / competitive exclusion principle / paradox of the plankton

References

[1] Daniel R . The metagenomics of soil. Nat Rev Microbiol. 2005; 3 (6): 470- 8.

[2] Pennisi E . What determines species diversity? Science. 2005; 309 (5731): 90.

[3] Hoorn C , Wesselingh FP , ter Steege H , Bermudez MA , Mora A , Sevink J , et al. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science. 2010; 330 (6006): 927- 31.

[4] de Vargas C , Audic S , Henry N , Decelle J , Mahé F , Logares R , et al. Eukaryotic plankton diversity in the sunlit ocean. Science. 2015; 348 (6237): 1261605.

[5] Gause GF . Experimental analysis of Vito Volterra's mathematical theory of the struggle for existence. Science. 1934; 79 (2036): 16- 7.

[6] Volterra V . Variations and fluctuations of the number of individuals in animal species living together. ICES (Int Counc Explor Sea) J Mar Sci. 1928; 3 (1): 3- 51.

[7] MacArthur R , Levins R . Competition, habitat selection, and character displacement in a patchy environment. Proc Natl Acad Sci USA. 1964; 51 (6): 1207- 10.

[8] Levin SA . Community equilibria and stability, and an extension of the competitive exclusion principle. Am Nat. 1970; 104 (939): 413- 23.

[9] McGehee R , Armstrong RA . Some mathematical problems concerning the ecological principle of competitive exclusion. J Differ Equ. 1977; 23 (1): 30- 52.

[10] Park T . Experimental studies of interspecies competition Ⅱ. Temperature, humidity, and competition in two species of Tribolium. Physiol Zool. 1954; 27 (3): 177- 238.

[11] Ayala FJ . Experimental invalidation of the principle of competitive exclusion. Nature. 1969; 224 (5224): 1076- 9.

[12] Wang X , Liu YY . Overcoming competitive exclusion in ecosystems. iScience. 2020; 23 (4): 101009.

[13] Lotka AJ . Analytical note on certain rhythmic relations in organic systems. Proc Natl Acad Sci USA. 1920; 6 (7): 410- 5.

[14] MacArthur R . Species packing and competitive equilibrium for many species. Theor Popul Biol. 1970; 1: 1- 11.

[15] Rohr RP , Saavedra S , Bascompte J . On the structural stability of mutualistic systems. Science. 2014; 345 (6195): 1253497.

[16] Coyte KZ , Schluter J , Foster KR . The ecology of the microbiome: networks, competition, and stability. Science. 2015; 350 (6261): 663- 6.

[17] Kingsland S , Alfred J . Lotka and the origins of theoretical population ecology. Proc Natl Acad Sci USA. 2015; 112: 9493- 5.

[18] Bashan A , Gibson TE , Friedman J , Carey VJ , Weiss ST , Hohmann EL , et al. Universality of human microbial dynamics. Nature. 2016; 534 (7606): 259- 62.

[19] Angulo MT , Kelley A , Montejano L , Song C , Saavedra S . Coexistence holes characterize the assembly and disassembly of multispecies systems. Nature Ecology & Evolution. 2021; 5 (8): 1091- 101.

[20] Remien CH , Eckwright MJ , Ridenhour BJ . Structural identifiability of the generalized Lotka-Volterra model for microbiome studies. R Soc Open Sci. 2021; 8 (7): 201378.

[21] Hu J , Amor DR , Barbier M , Bunin G , Gore J . Emergent phases of ecological diversity and dynamics mapped in microcosms. Science. 2022; 378 (6615): 85- 9.

[22] Hutchinson GE . The paradox of the plankton. Am Nat. 1961; 95 (882): 137- 45.

[23] Levins R . Coexistence in a variable environment. Am Nat. 1979; 114 (6): 765- 83.

[24] Levin SA . Dispersion and population interactions. Am Nat. 1974; 108 (960): 207- 28.

[25] Koch AL . Competitive coexistence of two predators utilizing the same prey under constant environmental conditions. J Theor Biol. 1974; 44 (2): 387- 95.

[26] Goldford JE , Lu N , Bajić D , Estrela S , Tikhonov M , Sanchez-Gorostiaga A , et al. Emergent simplicity in microbial community assembly. Science. 2018; 361 (6401): 469- 74.

[27] Kerr B , Riley MA , Feldman MW , Bohannan BJM . Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature. 2002; 418 (6894): 171- 4.

[28] Posfai A , Taillefumier T , Wingreen NS . Metabolic trade-offs promote diversity in a model ecosystem. Phys Rev Lett. 2017; 118 (2): 028103.

[29] Adler PB , HilleRisLambers J , Kyriakidis PC , Guan Q , Levine JM . Climate variability has a stabilizing effect on the coexistence of prairie grasses. Proc Natl Acad Sci USA. 2006; 103 (34): 12793- 8.

[30] Watt AS . Pattern and process in the plant community. J Ecol. 1947; 35 (1/2): 1- 22.

[31] Kane VR , Gersonde RF , Lutz JA , McGaughey RJ , Bakker JD , Franklin JF . Patch dynamics and the development of structural and spatial heterogeneity in Pacific Northwest forests. Can J For Res. 2011; 41 (12): 2276- 91.

[32] Angino EE , Armitage KB , Tash JC . Chemical stratification in lake Fryxell, Victoria land, Antarctica. Science. 1962; 138 (3536): 34- 6.

[33] Richerson P , Armstrong R , Goldman CR . Contemporaneous disequilibrium, a new hypothesis to explain the “Paradox of the Plankton”. Proc Natl Acad Sci USA. 1970; 67 (4): 1710- 4.

[34] Sunagawa S , Coelho LP , Chaffron S , Kultima JR , Labadie K , Salazar G , et al. Structure and function of the global ocean microbiome. Science. 2015; 348 (6237): 1261359.

[35] Villa Martín P , Buček A , Bourguignon T , Pigolotti S . Ocean currents promote rare species diversity in protists. Sci Adv. 2020; 6 (29): eaaz9037.

[36] Gupta D , Garlaschi S , Suweis S , Azaele S , Maritan A . Effective resource competition model for species coexistence. Phys Rev Lett. 2021; 127 (20): 208101.

[37] Huisman J , Weissing FJ . Biodiversity of plankton by species oscillations and chaos. Nature. 1999; 402 (6760): 407- 10.

[38] Becks L , Hilker FM , Malchow H , Jürgens K , Arndt H . Experimental demonstration of chaos in a microbial food web. Nature. 2005; 435 (7046): 1226- 9.

[39] Benincà E , Huisman J , Heerkloss R , Jöhnk KD , Branco P , Van Nes EH , et al. Chaos in a long-term experiment with a plankton community. Nature. 2008; 451 (7180): 822- 5.

[40] Goyal A , Maslov S . Diversity, stability, and reproducibility in stochastically assembled microbial ecosystems. Phys Rev Lett. 2018; 120 (15): 158102.

[41] Lopez JG , Wingreen NS . Noisy metabolism can promote microbial cross-feeding. Elife. 2022; 11: e70694.

[42] Laird RA , Schamp BS . Competitive intransitivity promotes species coexistence. Am Nat. 2006; 168 (2): 182- 93.

[43] Czárán TL , Hoekstra RF , Pagie L . Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci USA. 2002; 99 (2): 786- 90.

[44] Kirkup BC , Riley MA . Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature. 2004; 428 (6981): 412- 4.

[45] Buss LW , Jackson JBC . Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am Nat. 1979; 113 (2): 223- 34.

[46] Sinervo B , Lively CM . The rock-paper-scissors game and the evolution of alternative male strategies. Nature. 1996; 380 (6571): 240- 3.

[47] Kelsic ED , Zhao J , Vetsigian K , Kishony R . Counteraction of antibiotic production and degradation stabilizes microbial communities. Nature. 2015; 521 (7553): 516- 9.

[48] Bairey E , Kelsic ED , Kishony R . High-order species interactions shape ecosystem diversity. Nat Commun. 2016; 7 (1): 12285.

[49] Grilli J , Barabás G , Michalska-Smith MJ , Allesina S . Higher-order interactions stabilize dynamics in competitive network models. Nature. 2017; 548 (7666): 210- 3.

[50] Xue C , Goldenfeld N . Coevolution maintains diversity in the stochastic “kill the winner” model. Phys Rev Lett. 2017; 119 (26): 268101.

[51] Gammaitoni L , Hänggi P , Jung P , Marchesoni F . Stochastic resonance. Rev Mod Phys. 1998; 70 (1): 223- 87.

[52] Paine RT . Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol. 1980; 49 (3): 667- 85.

[53] Wang S , Brose U , Gravel D . Intraguild predation enhances biodiversity and functioning in complex food webs. Ecology. 2019; 100 (3): e02616.

[54] Neutel A-M , Heesterbeek JAP , van de Koppel J , Hoenderboom G , Vos A , Kaldeway C , et al. Reconciling complexity with stability in naturally assembling food webs. Nature. 2007; 449 (7162): 599- 602.

[55] Thingstad TF . Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr. 2000; 45 (6): 1320- 8.

[56] Brose U . Complex food webs prevent competitive exclusion among producer species. Proc Biol Sci. 2008; 275 (1650): 2507- 14.

[57] Ceulemans R , Guill C , Gaedke U . Top predators govern multitrophic diversity effects in tritrophic food webs. Ecology. 2021; 102 (7): e03379.

[58] Hubbell SP . The unified neutral theory of biodiversity and biogeography (MPB-32). Princeton University Press; 2001.

[59] Behrenfeld MJ , Bisson KM . Neutral theory and plankton biodiversity. Ann Rev Mar Sci. 2024; 16 (1): 283- 305.

[60] McGill BJ . A test of the unified neutral theory of biodiversity. Nature. 2003; 422 (6934): 881- 5.

[61] Stanley Harpole W , Tilman D . Non-neutral patterns of species abundance in grassland communities. Ecol Lett. 2006; 9 (1): 15- 23.

[62] Fuentes M . Slight differences among individuals and the unified neutral theory of biodiversity. Theor Popul Biol. 2004; 66 (3): 199- 203.

[63] Barabás G , D'Andrea R , Stump SM . Chesson's coexistence theory. Ecol Monogr. 2018; 88 (3): 277- 303.

[64] Chesson P . Mechanisms of maintenance of species diversity. Annu Rev Ecol Evol Syst. 2000; 31 (1): 343- 66.

[65] Chesson P , Huntly N . The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am Nat. 1997; 150 (5): 519- 53.

[66] Letten AD , Ke P-J , Fukami T . Linking modern coexistence theory and contemporary niche theory. Ecol Monogr. 2017; 87 (2): 161- 77.

[67] Chesson PL , Warner RR . Environmental variability promotes coexistence in lottery competitive systems. Am Nat. 1981; 117 (6): 923- 43.

[68] Stander PE . Cooperative hunting in lions: the role of the individual. Behav Ecol Sociobiol. 1992; 29 (6): 445- 54.

[69] Merron GS . Pack-hunting in two species of catfish, Clavias gariepinus and C. ngamensis, in the Okavango Delta, Botswana. J Fish Biol. 1993; 43 (4): 575- 84.

[70] Boesch C . Cooperative hunting in wild chimpanzees. Anim Behav. 1994; 48 (3): 653- 67.

[71] Creel S , Creel NM . Communal hunting and pack size in African wild dogs, Lycaon pictus. Anim Behav. 1995; 50 (5): 1325- 39.

[72] Bshary R , Hohner A , Ait-el-Djoudi K , Fricke H . Interspecific communicative and coordinated hunting between groupers and giant moray eels in the Red Sea. PLoS Biol. 2006; 4 (12): e431.

[73] Muro C , Escobedo R , Spector L , Coppinger RP . Wolf-pack (Canis lupus) hunting strategies emerge from simple rules in computational simulations. Behav Process. 2011; 88 (3): 192- 7.

[74] Vail AL , Manica A , Bshary R . Referential gestures in fish collaborative hunting. Nat Commun. 2013; 4 (1): 1765.

[75] Geisen S , Rosengarten J , Koller R , Mulder C , Urich T , Bonkowski M . Pack hunting by a common soil amoeba on nematodes. Environ Microbiol. 2015; 17 (11): 4538- 46.

[76] Seccareccia I , Kost C , Nett M . Quantitative analysis of Lysobacter predation. Appl Environ Microbiol. 2015; 81 (20): 7098- 105.

[77] Kang J , Zhang S , Niu Y , Zhong F , Wang X . Intraspecific predator interference promotes biodiversity in ecosystems. eLife. 2024; 13: RP93115.

[78] Beddington JR . Mutual interference between parasites or predators and its effect on searching efficiency. J Anim Ecol. 1975; 44 (1): 331- 40.

[79] DeAngelis DL , Goldstein RA , O'Neill RV . A model for trophic interaction. Ecology. 1975; 56: 881- 92.

[80] Cantrell RS , Cosner C , Ruan S . Intraspecific interference and consumer-resource dynamics. Discrete Contin Dyn Syst -B. 2004; 4: 527- 46.

[81] Hsu S-B , Ruan S , Yang T-H . On the dynamics of two-consumers-one-resource competing systems with Beddington-DeAngelis functional response. Discrete Contin Dyn Syst -B. 2013; 18 (9): 2331- 53.

[82] Huisman G , De Boer RJ . A formal derivation of the “Beddington” functional response. J Theor Biol. 1997; 185 (3): 389- 400.

[83] Fuhrman JA , Steele JA , Hewson I , Schwalbach MS , Brown MV , Green JL , et al. A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA. 2008; 105 (22): 7774- 8.

[84] Ser-Giacomi E , Zinger L , Malviya S , De Vargas C , Karsenti E , Bowler C , et al. Ubiquitous abundance distribution of non-dominant plankton across the global ocean. Nature Ecol Evol. 2018; 2 (8): 1243- 9.

[85] Terborgh J , Robinson SK , Parker Iii TA , Munn CA , Pierpont N . Structure and organization of an Amazonian forest bird community. Ecol Monogr. 1990; 60 (2): 213- 38.

[86] Cody ML In: Cody ML, Smallwood JA, editors. Long-term studies of vertebrate communities. Academic Press; 1996. p. 291- 342.

[87] Martínez AE , Ponciano JM , Gomez JP , Valqui T , Novoa J , Antezana M , et al. The structure and organisation of an Amazonian bird community remains little changed after nearly four decades in Manu National Park. Ecol Lett. 2023; 26 (2): 335- 46.

[88] Clarke FM , Rostant LV , Racey PA . Life after logging: post-logging recovery of a neotropical bat community. J Appl Ecol. 2005; 42 (2): 409- 20.

[89] Descamps-Julien B , Gonzalez A . Stable coexistence in a fluctuating environment: an experimental demonstration. Ecology. 2005; 86 (10): 2815- 24.

RIGHTS & PERMISSIONS

The Author(s). Quantitative Biology published by John Wiley & Sons Australia, Ltd on behalf of Higher Education Press.