Mutualism (biology)

This article is about the biological term. For the economic theory and other uses, see Mutualism (disambiguation).

Hummingbird hawkmoth drinking from Dianthus , with pollination being a classic example of mutualism

Mutualism describes the ecological interaction between two or more species where each species has a net benefit. ^[1] Mutualism is a common type of ecological interaction, one that can come from a parasitic interaction. ^[2] Prominent examples include most vascular plants engaged in mutualistic interactions with mycorrhizal fungi, flowering plants being pollinated by animals, vascular plants being dispersed by animals, and corals with zooxanthellae, among many others. Mutualism can be contrasted with interspecific competition, in which each species experiences reduced fitness, and exploitation, or parasitism, in which one species benefits at the expense of the other. ^[3]

The term mutualism was introduced by Pierre-Joseph van Beneden in his 1876 book Animal Parasites and Messmates to mean "mutual aid among species". ^{[4] [5]}

Mutualism is often conflated with two other types of ecological phenomena: cooperation and symbiosis. Cooperation most commonly refers to increases in fitness through within-species (intraspecific) interactions, although it has been used (especially in the past) to refer to mutualistic interactions, and it is sometimes used to refer to mutualistic interactions that are not obligate. ^[1] Symbiosis involves two species living in close physical contact over a long period of their existence and may be mutualistic, parasitic, or commensal, so symbiotic relationships are not always mutualistic, and mutualistic interactions are not always symbiotic. Despite a different definition between mutualistic interactions and symbiosis, mutualistic and symbiosis have been largely used interchangeably in the past, and confusion on their use has persisted. ^[6]

Mutualism plays a key part in ecology and evolution. For example, mutualistic interactions are vital for terrestrial ecosystem function as about 80% of land plants species rely on mycorrhizal relationships with fungi to provide them with inorganic compounds and trace elements. ^[7] As another example, the estimate of tropical rainforest plants with seed dispersal mutualisms with animals ranges at least from 70 to 93.5%. ^[8] In addition, mutualism is thought to have driven the evolution of much of the biological diversity we see, such as flower forms (important for pollination mutualisms) and co-evolution between groups of species. ^[9] Mutualism has also been linked to major evolutionary events, such as the evolution of the eukaryotic cell (symbiogenesis) and the colonization of land by plants in association with mycorrhizal fungi.

Types

Resource-resource relationships

Mutualistic relationships can be thought of as a form of "biological barter" ^[10] in mycorrhizal associations between plant roots and fungi, with the plant providing carbohydrates to the fungus in return for primarily phosphate but also nitrogenous compounds. Other examples include rhizobia bacteria that fix nitrogen for leguminous plants (family Fabaceae) in return for energy-containing carbohydrates. ^[11] Metabolite exchange between multiple mutualistic species of bacteria has also been observed in a process known as cross-feeding. ^{[12] [13]}

Service-resource relationships

The red-billed oxpecker eats ticks on the impala's coat, in a cleaning symbiosis.

Service-resource relationships are common. Three important types are pollination, cleaning symbiosis, and zoochory.

In pollination, a plant trades food resources in the form of nectar or pollen for the service of pollen dispersal. However, daciniphilous Bulbophyllum orchid species trade sex pheromone precursor or booster components via floral synomones/attractants in a true mutualistic interactions with males of Dacini fruit flies (Diptera: Tephritidae: Dacinae). ^{[14] [15]}

Phagophiles feed (resource) on ectoparasites, thereby providing anti-pest service, as in cleaning symbiosis. Elacatinus and Gobiosoma , genera of gobies, feed on ectoparasites of their clients while cleaning them. ^[16]

Zoochory is the dispersal of the seeds of plants by animals. This is similar to pollination in that the plant produces food resources (for example, fleshy fruit, overabundance of seeds) for animals that disperse the seeds (service). Plants may advertise these resources using colour ^[17] and a variety of other fruit characteristics, e.g., scent. Fruit of the aardvark cucumber (Cucumis humifructus) is buried so deeply that the plant is solely reliant upon the aardvark's keen sense of smell to detect its ripened fruit, extract, consume and then scatter its seeds; ^[18] C. humifructus's geographical range is thus restricted to that of the aardvark's.

Another type is ant protection of aphids, where the aphids trade sugar-rich honeydew (a by-product of their mode of feeding on plant sap) in return for defense against predators such as ladybugs.

Service-service relationships

Ocellaris clownfish and Ritter's sea anemones live in a mutual service-service symbiosis, the fish driving off butterflyfish and the anemone's tentacles protecting the fish from predators.

Strict service-service interactions are very rare, for reasons that are far from clear. ^[10] One example is the relationship between sea anemones and anemone fish in the family Pomacentridae: the anemones provide the fish with protection from predators (which cannot tolerate the stings of the anemone's tentacles) and the fish defend the anemones against butterflyfish (family Chaetodontidae), which eat anemones. However, in common with many mutualisms, there is more than one aspect to it: in the anemonefish-anemone mutualism, waste ammonia from the fish feeds the symbiotic algae that are found in the anemone's tentacles. ^{[19] [20]} Therefore, what appears to be a service-service mutualism in fact has a service-resource component. A second example is that of the relationship between some ants in the genus Pseudomyrmex and trees in the genus Acacia , such as the whistling thorn and bullhorn acacia. The ants nest inside the plant's thorns. In exchange for shelter, the ants protect acacias from attack by herbivores (which they frequently eat when those are small enough, introducing a resource component to this service-service relationship) and competition from other plants by trimming back vegetation that would shade the acacia. In addition, another service-resource component is present, as the ants regularly feed on lipid-rich food-bodies called Beltian bodies that are on the Acacia plant. ^[21]

In the neotropics, the ant Myrmelachista schumanni makes its nest in special cavities in Duroia hirsute . Plants in the vicinity that belong to other species are killed with formic acid. This selective gardening can be so aggressive that small areas of the rainforest are dominated by Duroia hirsute. These peculiar patches are known by local people as "devil's gardens". ^[22]

In some of these relationships, the cost of the ant's protection can be quite expensive. Cordia sp. trees in the Amazonian rainforest have a kind of partnership with Allomerus sp. ants, which make their nests in modified leaves. To increase the amount of living space available, the ants will destroy the tree's flower buds. The flowers die and leaves develop instead, providing the ants with more dwellings. Another type of Allomerus sp. ant lives with the Hirtella sp. tree in the same forests, but in this relationship, the tree has turned the tables on the ants. When the tree is ready to produce flowers, the ant abodes on certain branches begin to wither and shrink, forcing the occupants to flee, leaving the tree's flowers to develop free from ant attack. ^[22]

The term "species group" can be used to describe the manner in which individual organisms group together. In this non-taxonomic context one can refer to "same-species groups" and "mixed-species groups." While same-species groups are the norm, examples of mixed-species groups abound. For example, zebra ( Equus burchelli ) and wildebeest ( Connochaetes taurinus ) can remain in association during periods of long distance migration across the Serengeti as a strategy for thwarting predators. Cercopithecus mitis and Cercopithecus ascanius , species of monkey in the Kakamega Forest of Kenya, can stay in close proximity and travel along exactly the same routes through the forest for periods of up to 12 hours. These mixed-species groups cannot be explained by the coincidence of sharing the same habitat. Rather, they are created by the active behavioural choice of at least one of the species in question. ^[23]

Mathematical modeling

Mathematical treatments of mutualisms, like the study of mutualisms in general, has lagged behind those of predation, or predator-prey, consumer-resource, interactions. In models of mutualisms, the terms "type I" and "type II" functional responses refer to the linear and saturating relationships, respectively, between benefit provided to an individual of species 1 (y-axis) on the density of species 2 (x-axis).

Type I functional response

One of the simplest frameworks for modeling species interactions is the Lotka–Volterra equations. ^[24] In this model, the changes in population densities of the two mutualists are quantified as:

${\displaystyle {\begin{aligned}{\frac {dN_{1}}{dt}}&=r_{1}N_{1}-\alpha _{11}N_{1}^{2}+\beta _{12}N_{1}N_{2}\\[8pt]{\frac {dN_{2}}{dt}}&=r_{2}N_{2}-\alpha _{22}N_{2}^{2}+\beta _{21}N_{1}N_{2}\end{aligned}}}$

where

• ${\displaystyle N_{i}}$ = the population density of species i.
• ${\displaystyle r_{i}}$ = the intrinsic growth rate of the population of species i.
• ${\displaystyle \alpha _{ii}}$ = the negative effect of within-species crowding on species i.
• ${\displaystyle \beta _{ij}}$ = the beneficial effect of the density of species j on species i.

Mutualism is in essence the logistic growth equation modified for mutualistic interaction. The mutualistic interaction term represents the increase in population growth of one species as a result of the presence of greater numbers of another species. As the mutualistic interactive term is always positive, it may lead to unrealistic unbounded growth as it happens with the simple model. ^[25] So it is important to include a saturation mechanism in the formula to avoid this occurring.

Type II functional response

In 1989, David Hamilton Wright modified the above Lotka–Volterra equations by adding a new term, βM/K, to represent a mutualistic relationship. ^[26] Wright also considered the concept of saturation, which means that with higher densities, there are decreasing benefits of further increases of the mutualist population. Without saturation, species' densities would increase indefinitely. Because that is not possible due to environmental constraints and carrying capacity, a model that includes saturation would be more accurate. Wright's mathematical theory is based on the premise of a simple two-species mutualism model in which the benefits of mutualism become saturated due to limits posed by handling time. Wright defines handling time as the time needed to process a food item, from the initial interaction to the start of a search for new food items and assumes that processing of food and searching for food are mutually exclusive. Mutualists that display foraging behavior are exposed to the restrictions on handling time. Mutualism can be associated with symbiosis.

Handling time interactions In 1959, C. S. Holling performed his classic disc experiment that assumed the following: that (1), the number of food items captured is proportional to the allotted searching time; and (2), that there is a variable of handling time that exists separately from the notion of search time. He then developed an equation for the Type II functional response, which showed that the feeding rate is equivalent to

${\displaystyle {\cfrac {ax}{1+axT_{H}}}}$

where

• a = the instantaneous discovery rate
• x = food item density
• T_H = handling time

The equation that incorporates Type II functional response and mutualism is:

${\displaystyle {\frac {dN}{dt}}=N\left[r(1-cN)+{\cfrac {baM}{1+aT_{H}M}}\right]}$

where

• N and M=densities of the two mutualists
• r=intrinsic rate of increase of N
• c=coefficient measuring negative intraspecific interaction. This is equivalent to inverse of the carrying capacity, 1/K, of N, in the logistic equation.
• a=instantaneous discovery rate
• b=coefficient converting encounters with M to new units of N

or, equivalently,

${\displaystyle {\frac {dN}{dt}}=N[r(1-cN)+\beta M/(X+M)]}$

where

• X=1/aT_H
• β=b/T_H

This model is most effectively applied to free-living species that encounter a number of individuals of the mutualist part in the course of their existences. Wright notes that models of biological mutualism tend to be similar qualitatively, in that the featured isoclines generally have a positive decreasing slope, and by and large similar isocline diagrams. Mutualistic interactions are best visualized as positively sloped isoclines, which can be explained by the fact that the saturation of benefits accorded to mutualism or restrictions posed by outside factors contribute to a decreasing slope.

The type II functional response is visualized as the graph of ${\displaystyle {\cfrac {baM}{1+aT_{H}M}}}$vs.M.

Structure of networks

Mutualistic networks made up out of the interaction between plants and pollinators were found to have a similar structure in very different ecosystems on different continents, consisting of entirely different species. ^[27] The structure of these mutualistic networks may have large consequences for the way in which pollinator communities respond to increasingly harsh conditions and on the community carrying capacity. ^[28]

Mathematical models that examine the consequences of this network structure for the stability of pollinator communities suggest that the specific way in which plant-pollinator networks are organized minimizes competition between pollinators, ^[29] reduce the spread of indirect effects and thus enhance ecosystem stability ^[30] and may even lead to strong indirect facilitation between pollinators when conditions are harsh. ^[31] This means that pollinator species together can survive under harsh conditions. But it also means that pollinator species collapse simultaneously when conditions pass a critical point. ^[32] This simultaneous collapse occurs, because pollinator species depend on each other when surviving under difficult conditions. ^[31]

Such a community-wide collapse, involving many pollinator species, can occur suddenly when increasingly harsh conditions pass a critical point and recovery from such a collapse might not be easy. The improvement in conditions needed for pollinators to recover could be substantially larger than the improvement needed to return to conditions at which the pollinator community collapsed. ^[31]

Humans

Dogs and sheep were among the first animals to be domesticated.

Humans are involved in mutualisms with other species: their gut flora is essential for efficient digestion. ^[33] Infestations of head lice might have been beneficial for humans by fostering an immune response that helps to reduce the threat of body louse borne lethal diseases. ^[34]

Some relationships between humans and domesticated animals and plants are to different degrees mutualistic. For example, agricultural varieties of maize provide food for humans and are unable to reproduce without human intervention because the leafy sheath does not fall open, and the seedhead (the "corn on the cob") does not shatter to scatter the seeds naturally.^{[ citation needed ]}

In traditional agriculture, some plants have mutualist as companion plants, providing each other with shelter, soil fertility and/or natural pest control. For example, beans may grow up cornstalks as a trellis, while fixing nitrogen in the soil for the corn, a phenomenon that is used in Three Sisters farming. ^[35]

One researcher has proposed that the key advantage Homo sapiens had over Neanderthals in competing over similar habitats was the former's mutualism with dogs. ^[36]

Intestinal microbiota

The microbiota in the human intestine coevolved with the human species, and this relationship is considered to be a mutualism that is beneficial both to the human host and the bacteria in the gut population. ^[37] The mucous layer of the intestine contains commensal bacteria that produce bacteriocins, modify the pH of the intestinal contents, and compete for nutrition to inhibit colonization by pathogens. ^[38] The gut microbiota, containing trillions of microorganisms, possesses the metabolic capacity to produce and regulate multiple compounds that reach the circulation and act to influence the function of distal organs and systems. ^[39] Breakdown of the protective mucosal barrier of the gut can contribute to the development of colon cancer. ^[38]

Evolution of mutualism

Evolution by type

Every generation of every organism needs nutrients – and similar nutrients – more than they need particular defensive characteristics, as the fitness benefit of these vary heavily especially by environment. This may be the reason that hosts are more likely to evolve to become dependent on vertically transmitted bacterial mutualists which provide nutrients than those providing defensive benefits. This pattern is generalized beyond bacteria by Yamada et al. 2015's demonstration that undernourished Drosophila are heavily dependent on their fungal symbiont Issatchenkia orientalis for amino acids. ^[40]

Mutualism breakdown

Mutualisms are not static, and can be lost by evolution. ^[41] Sachs and Simms (2006) suggest that this can occur via four main pathways:

1. One mutualist shifts to parasitism, and no longer benefits its partner, ^[41] such as headlice ^[42]
2. One partner abandons the mutualism and lives autonomously ^[41]
3. One partner may go extinct ^[41]
4. A partner may be switched to another species ^[43]

There are many examples of mutualism breakdown. For example, plant lineages inhabiting nutrient-rich environments have evolutionarily abandoned mycorrhizal mutualisms many times independently. ^[44] Evolutionarily, headlice may have been mutualistic as they allow for early immunity to various body-louse borne disease; however, as these diseases became eradicated, the relationship has become less mutualistic and more parasitic. ^[42]

Measuring and defining mutualism

Measuring the exact fitness benefit to the individuals in a mutualistic relationship is not always straightforward, particularly when the individuals can receive benefits from a variety of species, for example most plant-pollinator mutualisms. It is therefore common to categorise mutualisms according to the closeness of the association, using terms such as obligate and facultative. Defining "closeness", however, is also problematic. It can refer to mutual dependency (the species cannot live without one another) or the biological intimacy of the relationship in relation to physical closeness (e.g., one species living within the tissues of the other species). ^[10]

See also

• Arbuscular mycorrhiza
• Co-adaptation
• Coevolution
• Ecological facilitation
• Frugivore
• Greater honeyguide – has a mutualism with humans
• Interspecies communication
• Müllerian mimicry
• Mutualisms and conservation
• Mutual Aid: A Factor of Evolution
• Symbiogenesis
• Plant–animal interaction

References

1. Bronstein, Judith (2015). Mutualism. Oxford University Press.
2. "Yale researchers show that mutualism can come from parasitism". 6 February 2018.
3. "IXL | Classify symbiotic relationships | 7th grade science". IXL Learning. Retrieved 4 December 2023.
4. Van Beneden, Pierre-Joseph (1876). Animal Parasites and Messmates. London: Henry S. King.
5. Bronstein, J. L. (2015). The study of mutualism. Oxford University Press. ISBN   9780199675654.{{cite book}}: |work= ignored (help)^{[ page needed ]}
6. Douglas, Angela E. (December 2014). The Symbiotic Habit. United States: Princeton University Press. ISBN   9780691113425.
7. Wang, B. (2006). "Phylogenetic distribution and evolution of mycorrhizas in land plants". Mycorrhiza. 16 (5): 299–363. Bibcode:2006Mycor..16..299W. doi:10.1007/s00572-005-0033-6. PMID   16845554. S2CID   30468942.
8. Jordano, P. 2000. Fruits and frugivory. pp. 125–166 in: Fenner, M. (Ed) Seeds: the ecology of regeneration in plant communities. CABI.
9. Thompson, J. N. 2005 The geographic mosaic of coevolution. Chicago, IL: University of Chicago Press.
10. Ollerton, J. 2006. "Biological Barter": Interactions of Specialization Compared across Different Mutualisms. pp. 411–435 in: Waser, N.M. & Ollerton, J. (Eds) Plant-Pollinator Interactions: From Specialization to Generalization. University of Chicago Press.
11. Denison, RF; Kiers, ET (2004). "Why are most rhizobia beneficial to their plant hosts, rather than parasitic". Microbes and Infection . 6 (13): 1235–1239. doi:10.1016/j.micinf.2004.08.005. PMID   15488744.
12. Schink, Bernhard (1 December 2002). "Synergistic interactions in the microbial world". Antonie van Leeuwenhoek. 81 (1): 257–261. doi:10.1023/A:1020579004534. ISSN   1572-9699. PMID   12448724. S2CID   9310406.
13. Chacón, Jeremy M.; Hammarlund, Sarah P.; Martinson, Jonathan N.V.; Smith, Leno B.; Harcombe, William R. (2 November 2021). "The Ecology and Evolution of Model Microbial Mutualisms". Annual Review of Ecology, Evolution, and Systematics. 52 (1): 363–384. doi: 10.1146/annurev-ecolsys-012121-091753 . ISSN   1543-592X. S2CID   239694099.
14. See also Attractant related to synomone; and references therein
15. Tan, K. H. and Nishida, R. (2000) Mutual reproductive benefits between a wild orchid, Bulbophyllum patens, and Bactrocera fruit flies via a floral synomone. Journal of Chemical Ecology, 26: 533-546. doi.org/10.1023/A:1005477926244
16. M.C. Soares; I.M. Côté; S.C. Cardoso & R.Bshary (August 2008). "The cleaning goby mutualism: a system without punishment, partner switching or tactile stimulation" (PDF). Journal of Zoology. 276 (3): 306–312. doi:10.1111/j.1469-7998.2008.00489.x.
17. Lim, Ganges; Burns, Kevin C. (24 November 2021). "Do fruit reflectance properties affect avian frugivory in New Zealand?". New Zealand Journal of Botany. 60 (3): 319–329. doi:10.1080/0028825X.2021.2001664. ISSN   0028-825X. S2CID   244683146.
18. van Rheede van Oudtshoorn, Karen; van Rooyen, Margaretha W. (1998). Dispersal Biology of Desert Plants. Berlin; New York: Springer. p. 118. ISBN   978-3-540-64886-4 . Retrieved 28 January 2023.
19. Porat, D.; Chadwick-Furman, N. E. (2004). "Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival". Hydrobiologia . 530 (1–3): 513–520. doi:10.1007/s10750-004-2688-y. S2CID   2251533.
20. Porat, D.; Chadwick-Furman, N. E. (2005). "Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthella content and tissue regeneration". Mar. Freshw. Behav. Phys. 38 (1): 43–51. Bibcode:2005MFBP...38...43P. doi:10.1080/10236240500057929. S2CID   53051081.
21. "Swollen Thorn Acacias". www2.palomar.edu. Archived from the original on 27 June 2018. Retrieved 22 February 2019.
22. Piper, Ross (2007), Extraordinary Animals: An Encyclopedia of Curious and Unusual Animals, Greenwood Press.
23. Tosh CR, Jackson AL, Ruxton GD (March 2007). "Individuals from different-looking animal species may group together to confuse shared predators: simulations with artificial neural networks". Proc. Biol. Sci. 274 (1611): 827–32. doi:10.1098/rspb.2006.3760. PMC   2093981 . PMID   17251090.
24. May, R., 1981. Models for Two Interacting Populations. In: May, R.M., Theoretical Ecology. Principles and Applications, 2nd ed. pp. 78–104.
25. García-Algarra, Javier (2014). "Rethinking the logistic approach for population dynamics of mutualistic interactions" (PDF). Journal of Theoretical Biology . 363: 332–343. arXiv: 1305.5411 . Bibcode:2014JThBi.363..332G. doi:10.1016/j.jtbi.2014.08.039. PMID   25173080. S2CID   15940333.
26. Wright, David Hamilton (1989). "A Simple, Stable Model of Mutualism Incorporating Handling Time". The American Naturalist . 134 (4): 664–667. doi:10.1086/285003. S2CID   83502337.
27. Bascompte, J.; Jordano, P.; Melián, C. J.; Olesen, J. M. (2003). "The nested assembly of plant–animal mutualistic networks". Proceedings of the National Academy of Sciences. 100 (16): 9383–9387. Bibcode:2003PNAS..100.9383B. doi: 10.1073/pnas.1633576100 . PMC   170927 . PMID   12881488.
28. Suweis, S.; Simini, F.; Banavar, J; Maritan, A. (2013). "Emergence of structural and dynamical properties of ecological mutualistic networks". Nature. 500 (7463): 449–452. arXiv: 1308.4807 . Bibcode:2013Natur.500..449S. doi:10.1038/nature12438. PMID   23969462. S2CID   4412384.
29. Bastolla, U.; Fortuna, M. A.; Pascual-García, A.; Ferrera, A.; Luque, B.; Bascompte, J. (2009). "The architecture of mutualistic networks minimizes competition and increases biodiversity". Nature. 458 (7241): 1018–1020. Bibcode:2009Natur.458.1018B. doi:10.1038/nature07950. PMID   19396144. S2CID   4395634.
30. Suweis, S., Grilli, J., Banavar, J. R., Allesina, S., & Maritan, A. (2015) Effect of localization on the stability of mutualistic ecological networks. "Nature Communications", 6
31. Lever, J. J.; Nes, E. H.; Scheffer, M.; Bascompte, J. (2014). "The sudden collapse of pollinator communities". Ecology Letters. 17 (3): 350–359. Bibcode:2014EcolL..17..350L. doi:10.1111/ele.12236. hdl: 10261/91808 . PMID   24386999.
32. Garcia-Algarra, J.; Pasotr, J. M.; Iriondo, J. M.; Galeano, J. (2017). "Ranking of critical species to preserve the functionality of mutualistic networks using the k-core decomposition". PeerJ. 5: e3321. doi: 10.7717/peerj.3321 . PMC   5438587 . PMID   28533969.
33. Sears CL (October 2005). "A dynamic partnership: celebrating our gut flora". Anaerobe. 11 (5): 247–51. doi:10.1016/j.anaerobe.2005.05.001. PMID   16701579.
34. Rozsa, L; Apari, P. (2012). "Why infest the loved ones – inherent human behaviour indicates former mutualism with head lice" (PDF). Parasitology. 139 (6): 696–700. doi:10.1017/s0031182012000017. PMID   22309598. S2CID   206247019.
35. Mount Pleasant, Jane (2006). "The science behind the Three Sisters mound system: An agronomic assessment of an indigenous agricultural system in the northeast". In Staller, John E.; Tykot, Robert H.; Benz, Bruce F. (eds.). Histories of Maize: Multidisciplinary Approaches to the Prehistory, Linguistics, Biogeography, Domestication, and Evolution of Maize. Amsterdam: Academic Press. pp. 529–537. ISBN   978-1-5987-4496-5.
36. Shipman, Pat (2015). The Invaders: How Humans and Their Dogs Drove Neanderthals to Extinction. Cambridge, Maryland: Harvard University Press.
37. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005 Mar 25;307(5717):1915-20. doi: 10.1126/science.1104816. PMID 15790844
38. Genua F, Raghunathan V, Jenab M, Gallagher WM, Hughes DJ. The Role of Gut Barrier Dysfunction and Microbiome Dysbiosis in Colorectal Cancer Development. Front Oncol. 2021 Apr 15;11:626349. doi: 10.3389/fonc.2021.626349. PMID 33937029; PMCID: PMC8082020
39. Gerard Clarke, Roman M. Stilling, Paul J. Kennedy, Catherine Stanton, John F. Cryan, Timothy G. Dinan, Minireview: Gut Microbiota: The Neglected Endocrine Organ, Molecular Endocrinology, Volume 28, Issue 8, 1 August 2014, Pages 1221–1238, https://doi.org/10.1210/me.2014-1108
40. Biedermann, Peter H.W.; Vega, Fernando E. (7 January 2020). "Ecology and Evolution of Insect–Fungus Mutualisms". Annual Review of Entomology . Annual Reviews. 65 (1): 431–455. doi: 10.1146/annurev-ento-011019-024910 . ISSN   0066-4170. PMID   31610133. S2CID   204704243.
41. Sachs, JL; Simms, EL (2006). "Pathways to mutualism breakdown". TREE. 21 (10): 585–592. doi:10.1016/j.tree.2006.06.018. PMID   16828927.
42. RÓZSA, LAJOS; APARI, PÉTER (6 February 2012). "Why infest the loved ones – inherent human behaviour indicates former mutualism with head lice" . Parasitology. 139 (6): 696–700. doi:10.1017/s0031182012000017. ISSN   0031-1820. PMID   22309598. S2CID   206247019.
43. Werner, Gijsbert D. A.; Cornelissen, Johannes H. C.; Cornwell, William K.; Soudzilovskaia, Nadejda A.; Kattge, Jens; West, Stuart A.; Kiers, E. Toby (30 April 2018). "Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown". Proceedings of the National Academy of Sciences . National Academy of Sciences. 115 (20): 5229–5234. Bibcode:2018PNAS..115.5229W. doi: 10.1073/pnas.1721629115 . ISSN   0027-8424. PMC   5960305 . PMID   29712857. S2CID   14055644.
44. Wang, B.; Qiu, Y.-L. (6 May 2006). "Phylogenetic distribution and evolution of mycorrhizas in land plants". Mycorrhiza. International Mycorrhiza Society (Springer). 16 (5): 299–363. Bibcode:2006Mycor..16..299W. doi:10.1007/s00572-005-0033-6. ISSN   0940-6360. PMID   16845554. S2CID   30468942.

Further references

• Angier, Natalie (22 July 2016). "African Tribesmen Can Talk Birds into Helping Them Find Honey". The New York Times .
• Bascompte, J.; Jordano, P.; Melián, C. J.; Olesen, J. M. (2003). "The nested assembly of plant–animal mutualistic networks". Proceedings of the National Academy of Sciences . 100 (16): 9383–9387. Bibcode:2003PNAS..100.9383B. doi: 10.1073/pnas.1633576100 . PMC   170927 . PMID   12881488.
• Bastolla, U.; Fortuna, M. A.; Pascual-García, A.; Ferrera, A.; Luque, B.; Bascompte, J. (2009). "The architecture of mutualistic networks minimizes competition and increases biodiversity". Nature. 458 (7241): 1018–1020. Bibcode:2009Natur.458.1018B. doi:10.1038/nature07950. PMID   19396144. S2CID   4395634.* Breton, Lorraine M.; Addicott, John F. (1992). "Density-Dependent Mutualism in an Aphid-Ant Interaction". Ecology . 73 (6): 2175–2180. doi:10.2307/1941465. JSTOR   1941465.
• Bronstein, JL (1994). "Our current understanding of mutualism". Quarterly Review of Biology . 69 (1): 31–51. doi:10.1086/418432. S2CID   85294431.
• Bronstein, JL (2001). "The exploitation of mutualisms". Ecology Letters . 4 (3): 277–287. Bibcode:2001EcolL...4..277B. doi: 10.1046/j.1461-0248.2001.00218.x .
• Bronstein JL. 2001. The costs of mutualism. American Zoologist 41 (4): 825-839 S
• Bronstein, JL; Alarcon, R; Geber, M (2006). "The evolution of plant-insect mutualisms". New Phytologist . 172 (3): 412–28. doi: 10.1111/j.1469-8137.2006.01864.x . PMID   17083673.
• Denison, RF; Kiers, ET (2004). "Why are most rhizobia beneficial to their plant hosts, rather than parasitic?". Microbes and Infection . 6 (13): 1235–1239. doi:10.1016/j.micinf.2004.08.005. PMID   15488744.
• DeVries, PJ; Baker, I (1989). "Butterfly exploitation of an ant-plant mutualism: Adding insult of herbivory". Journal of the New York Entomological Society. 97 (3): 332–340.
• Hoeksema, J.D.; Bruna, E.M. (2000). "Pursuing the big questions about interspecific mutualism: a review of theoretical approaches". Oecologia . 125 (3): 321–330. Bibcode:2000Oecol.125..321H. doi:10.1007/s004420000496. PMID   28547326. S2CID   22756212.
• Jahn, G.C.; Beardsley, J.W. (2000). "Interactions of ants (Hymenoptera: Formicidae) and mealybugs (Homoptera: Pseudococcidae) on pineapple". Proceedings of the Hawaiian Entomological Society. 34: 181–185.
• Jahn, Gary C.; Beardsley, J. W.; González-Hernández, H. (2003). "A review of the association of ants with mealybug wilt disease of pineapple" (PDF). Proceedings of the Hawaiian Entomological Society. 36: 9–28.
• Lever, J. J.; Nes, E. H.; Scheffer, M.; Bascompte, J. (2014). "The sudden collapse of pollinator communities". Ecology Letters . 17 (3): 350–359. Bibcode:2014EcolL..17..350L. doi:10.1111/ele.12236. hdl: 10261/91808 . PMID   24386999.
• Noe, R.; Hammerstein, P. (1994). "Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating". Behavioral Ecology and Sociobiology . 35: 1–11. doi:10.1007/bf00167053. S2CID   37085820.
• Ollerton, J. 2006. "Biological Barter": Patterns of Specialization Compared across Different Mutualisms. pp. 411–435 in: Waser, N.M. & Ollerton, J. (Eds) Plant-Pollinator Interactions: From Specialization to Generalization. University of Chicago Press. ISBN   978-0-226-87400-5
• Paszkowski, U (2006). "Mutualism and parasitism: the yin and yang of plant symbioses". Current Opinion in Plant Biology . 9 (4): 364–370. Bibcode:2006COPB....9..364P. doi:10.1016/j.pbi.2006.05.008. PMID   16713732.
• Porat, D.; Chadwick-Furman, N. E. (2004). "Effects of anemonefish on giant sea anemones:expansion behavior, growth, and survival". Hydrobiologia . 530 (1–3): 513–520. doi:10.1007/s10750-004-2688-y. S2CID   2251533.
• Porat, D.; Chadwick-Furman, N. E. (2005). "Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthella content and tissue regeneration". Mar. Freshw. Behav. Phys. 38 (1): 43–51. Bibcode:2005MFBP...38...43P. doi:10.1080/10236240500057929. S2CID   53051081.
• Thompson, J. N. 2005. The Geographic Mosaic of Coevolution. University of Chicago Press. ISBN   978-0-226-79762-5
• Wright, David Hamilton (1989). "A Simple, Stable Model of Mutualism Incorporating Handling Time". The American Naturalist . 134 (4): 664–667. doi:10.1086/285003. S2CID   83502337.

Further reading

• Boucher, D. G.; James, S.; Keeler, K. (1984). "The ecology of mutualism". Annual Review of Ecology and Systematics . 13: 315–347. doi:10.1146/annurev.es.13.110182.001531.
• Boucher, D. H. (editor) (1985) The Biology of Mutualism : Ecology and Evolution London : Croom Helm 388 p.  ISBN   0-7099-3238-3