The effect of climate change on plant mutualistic interactions · plant protection and nutrition,...

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The effect of climate change on plant mutualistic interactions Irene Calderón-‐Sanou1*, Emilie Isasa2*

Abstract Mutualisms play a major role in ecosystems functioning and maintenance. Plant mutualisms are crucial for plant nutrition, reproduction and survival. Climate change, including increased atmospheric CO2 levels and temperatures, and changes to precipitation patterns, are already affecting biological systems in different ways. These changes may affect the evolution and maintenance of mutualisms that are temporally and spatially dynamic. Some mutualisms will be disrupted, while others will persist depending on the nature of environmental changes. Here, we review the effects of climate change on plant mutualisms. We focused on two plant mutualisms: firstly ant-‐plant symbiotic mutualisms, implicated in plant protection and nutrition; secondly plant-‐pollinator transitory mutualisms, implicated in pollen transportation for plant reproduction. We found that drought promotes ant–plant symbioses. Water stress increases herbivory and therefore plants host and feed ant colonies as defense against herbivores. For plant-‐pollinator mutualisms, phenological shifts to plants and their pollinators are leading to a spatial and temporal mismatch, causing mutualism breakdowns. Modeling, together with life-‐history traits and population ecology has allowed prediction of pollination systems based on interaction characteristics. Generalists are likely to maintain the functioning of pollination in the community by shifting partners, while specialists are more likely to become extinct if mis-‐matches are significant. These examples illustrate two possible outcomes of mutualisms under climate change, but many other mutualisms need to be taken in consideration to understand how ecosystems will respond to global changes.

Keywords Mutualisms, Climate change, Ant-‐plant, Plant-‐pollinator, symbiotic/non-‐symbiotic

1 AgroParisTech, UMR EcoFoG, Master EcoTrop, F-‐97310 Kourou, French Guiana. 2 Université de Guyane, UMR EcoFoG, Master EcoTrop, F-‐97310 Kourou, French Guiana. * Corresponding author: [email protected], [email protected]

Contents Contents 1 Introduction 1 1 Mutualism reinforcement under climate change: the case of ant-plant interactions 2 1.1 Herbivory explosion: why herbivores eat stressed plants? 2 1.2 Ant-‐plant mutualism get stronger under climate change 2 1.3 Case study 3 2 Mutualism breakdown under climate change: the case of plant-pollinator networks 4 2.1 How can climate change disrupt plant-‐pollinator interactions? 4 2.2 Modeling the outcomes of plant-‐pollination systems 5 2.3 The vulnerability of obligate mutualisms 6 Conclusion 6 Acknowledgements 6 References 6

Introduction Plants are engage in multiple and simultaneous in-

teractions with other species occurring within the same community. Antagonist interactions (e.g. herbivory, com-petition) reduce plant performance while mutualisms

results in benefits related to plant protection, pollination, seed dispersal, nutrition and stress tolerance. Based on Boucher et al. (1982) classification, mutualisms are “symbiotic” when the interacting species live together in close association or with physiological integration (e.g. mycorrhizas, myrmecophily), or “non-symbiotic”, when interactions involve simple contact or superficial ex-change between species (e.g. pollination, seed dispersal). Mutualisms can also be characterized by the dependence of the interaction (facultative or obligate), and the number of species interacting (oligophilic or polyphilic). To sum-marize, some symbionts are highly host-specific and oth-ers associate with multiple hosts. In general, symbiotic mutualisms are the result of coevolution and involve obli-gate interactions, while non-symbiotic mutualisms are facultative and transitory.

Evolution of mutualism is dynamic in space and time, with mutualism being constantly formed, trans-formed, or dissolved (Sachs & Simms 2006). Understand-ing and predicting how mutualisms evolve remains chal-lenging because of the complexity of interaction dynam-ics. The outcomes of mutualisms can depend on environ-mental fluctuations and their evolution can vary in space across abiotic and biogeographical gradients (based on the geographical mosaic theory of coevolution; Thompson 1999; Gomulkiewicz et al. 2000). Species interacting in symbiotic mutualisms are expected to evolve in the same direction by maintaining the mutualism, shifting to para-sitism or getting co-extinct. The direction taken would depend on environmental conditions (Neuhauser & Fargione 2004). On contrast, free-living partners from

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non-symbiotic mutualisms are more likely to display dif-ferential responses to environmental fluctuations (Rafferty et al. 2015).

Global climate change generates non-negligible en-vironmental fluctuations that have significant impacts on biological systems (Sagata & Gibb 2016). Climate change includes increases in the frequency, intensity and duration of drought, temperature rise and higher atmospheric CO2 levels (Walther et al. 2002). These environmental fluctua-tions may have repercussions for biodiversity by directly affecting community structure (i.e. through species extinc-tion and geographical distribution shifts) and by changing mortality rates and phenological cycles at the scale of individuals or populations (Walther et al. 2002). Those changes can directly or indirectly affect the species inter-actions in the community (Tylianakis et al. 2008). Mutual-istic interactions involving plants contribute to multiple ecosystem functions by driving processes such as disper-sal, pollination, ecosystem regeneration and nutrient trans-fer. Indeed, plant mutualisms are crucial for understanding species survival because they enhance plant adaptation to stressful environments.

Given the complexity of plant network interactions, predicting the effect of climate change on plant mutual-isms remains a challenge. Predicting the ecological conse-quences of climate change requires a deep understanding of how plant interactions work and which factors influ-ence them. Here we review the predicted effects of cli-mate change (drought, increased temperature and in-creased CO2 levels) on mutualistic interactions in plants. Two possible and opposite outcomes of mutualisms could be expected: first, interactions are maintained and/or rein-forced; second, mutualism break down, when the interac-tion ends or leads to species extinction. To illustrate these possible outcomes we focused on two particular mutual-isms: 1) the symbiotic ant-plant mutualism, related to plant protection and nutrition, and 2) the transitory plant-pollinator mutualism, related to pollen transportation and reproduction success. At the same time, ant-plant and plant-pollinator mutualisms allow studying the effect of climate change on mutualisms at individual and communi-ty scales, respectively.

1 Mutualism reinforcement under climate change: the case of ant-

plant interactions

1.1 Herbivory explosion: why herbi-vores eat stressed plants?

As many ant-plant mutualisms provide protection against herbivores, understanding the effect of climate change on these mutualisms requires accounting for the effect of climate change on herbivore populations. One predicted consequence of climate change is the increase of herbivory.

According to Mattson & Haack (1987), outbreak of herbivorous insects occurs generally on plants affected by environmental stress. Indeed, it has been noticed that factors inducing drought stress in plants also promote insect population growth because plant nutrients are more concentrated under plant stress. More precisely, the C:N ratio increases on leaves, and to compensate the nitrogen imbalance. Moreover we can observe many plant physio-logical modifications. For example, at the molecular level, chlorophyll production decreases significantly and induc-es leaf yellowing that attracts insects (Mattson & Haack 1987). Similar modifications to plant physiology and herbivore behavior have been observed with increases in atmospheric CO2 levels and temperature. Global warming may also accelerate herbivores life cycles producing an increase in number of generations per year (DeLucia et al. 2012). Major mechanisms by which climate change may affect insect behavior are summarizes in Figure 1. As a strategy to fight against elevated herbivory, plants may favor another biotic interaction, namely, ant-plant symbio-ses.

Figure 1: Hypothetical representation of how drought/ climate change influences host plants, phytophagous insects, and their

natural enemies to provoke insect outbreaks. Based on Mattson & Haack (1987).

1.2 Ant-plant mutualism get stronger under climate change

Ant–plant symbioses are a good example of protec-tion mutualism (Rico-Gray & Oliveira 2007). These ant-plant symbioses are restricted to the Tropics, for example


ant-gardens and myrmecophytic plants (Orivel & Leroy 2011).

Water limitation, together with the risk of herbivory, can increase the strength of carbon-based mutualisms (Thrall et al. 2007). Also, nutrient-poor environments should amplify mutualism if the cost for each partner to obtain a limited resource alone is higher than that of ob-taining the resource from the mutualistic partner (Bronstein 1994). As a consequence, mutualistic interac-tion between species is often stronger when resources are limited. The costs of herbivory under water stress are particularly high, and leaves are harder to replace when resources are rare. Plants may invest more in ant defense when they are water stressed (Coley et al. 1985). To this end, myrmecophytic plants provide specialized nesting and housing structures for ants called domatia. Directly, plants can also offer nutrients such as carbohydrate-rich nectar, food bodies, or indirectly through honeydew aphids (Heil & McKey 2003).

González-Teuber et al. (2012) showed that Acacia produced more extra-floral nectar in the dry season com-pared to the rainy season. Increases in nectar productivity directly resulted in higher ant activity and aggression against herbivores.

Ants may also prevent epiphyte desiccation under water stress. Schmit-Neuerburg & Blüthgen (2007) stud-ied a neotropical ant garden during a dry period. They showed that in the absence of ants, epiphyte substrates become dry, increasing plant wilting and seedling mortali-ty. Climate change may modify precipitation patterns and may increase the duration of dry seasons in lowland tropi-cal rain forests. Ant-plant mutualism could be expected to increase epiphytic survival during dry periods by main-taining the moisture and stability of the substrate. The effect of CO2 concentrations on ant-plants and their inter-actions with ants, and the effect of nutrient enrichment because is poorly documented.

Variations in ant-plant protective mutualism are generally associated with other biotic interactions. One known interaction includes hemiptera. As previously said, hemiptera feeds ants through honeydew, which is directly produced by plant sap. The importance of ant-hemiptera mutualism likely depends on the availability of honeydew or another sources of carbohydrates in sap. In return, ants protect the plant against herbivory and sometimes provide them with nutrients from their waste, mostly deposited inside the domatia.

This mutualism Ant-Hemiptera-plant is important and ensure ant may benefit from honeydew nutrients that contain proteins, amino acids and carbohydrates (Fischer et al. 2002). As previously said, honeydew attract herbiv-orous insects too, resulting in an increase of insect prey on plant surfaces that are a good source of proteins for ants. At the same time, the predation activity of mutualistic ants stimulates food body production (Linsenmair et al. 2001).

1.3 Case study An older study proved that ant-plant mutualism is

stronger under water stress. They studied Camponotus fastigatus and Crematogaster quadriformis that are the main ant species associated with Inga vera (Kersch & Fonseca 2005). Later the study of Pringle et al. (2012) focused on Cordia alliodora and the ant Azteca pittieri and the mechanism of plant defense. Recently, Pringle et al. (2013) tested whether the strength of an ant-plant mu-tualism was related to water availability. They focused on specialist interaction between Cordia alliodora and Azteca that shows a stronger mutualism in drier sites. This plant species can be found from Mexico to Argentina in dry tropical forests.

Cordia alliadora individuals are protected by spe-cialized ants and an indirect exchange of carbon occurs between them (Fig. 2). Firstly, the tree produces carbohy-drates and uses them for leaf growth, seed production, fabrication of extra-floral nectaries or to support the scale-insects that feed the defending ant colony. Water is an essential component in this cycle. Secondly, ants use the carbohydrates obtained from scales to feed workers, who defend leaves from herbivory and protect the carbon source, and to feed reproductive ants.

Figure 2: Schematic of relationships among water, carbon, and mutualistic carbohydrate allocation strategies (Pringle et al.

2013).

On the one hand, the authors wanted to know if pre-cipitation, carbon and herbivory were correlated with mutualistic investments by trees and ants and investigated the relationships between water, carbohydrates, and mutu-alistic traits. On the other hand they tested if water stress leads to carbon stress, and whether carbon stress affects carbohydrate strategies by the mutualist partners.

They proved that ants defended more plants in drier sites than in wetter sites (Fig. 3B). Moreover, an ant-exclusion experiment conducted at different sites in dif-ferent gradients of precipitation, showed that herbivory was significantly lower on leaves with ants in dry sites than on leaves without ants in wet sites (Fig. 3C). They propose that precipitation and herbivory determine togeth-er the patterns in the strength of a plant–ant mutualism by an indirect effect on plant carbon availability.


Figure 3: Mutualism strength increases as water availability decreases (Pringle et al. 2013). a- Relationship between annual precipitation of a site and the density of scale insects for all 26 sites. b- Relationship between annual precipitation of a site and ant colony size (density of worker ants) for all 26 sites. c- Dif-ference in percent leaf area eaten between when ants were pre-sent and when ants were experimentally excluded at three dry-forest sites along the annual-precipitation gradient from driest (Chamela) to wettest (Santa Rosa). Bars represent mean differ-

ences from matched-pair experiments within trees.

Regarding the chemical differences in honeydew, ants received significantly more carbohydrates at drier sites than at wetter sites, because scale insects are more presents in wet sites (Fig. 3A). On the whole of this study, drought and carbon deficiency in plants affect the results of an ant-plant mutualism.

These results suggest that in this system the tree can decrease herbivory by promoting ant-colony growth, maintaining space and food investment in ants, as long as the tree continues to grow.

To sum up, ant-plant symbiosis is a complex interac-tion involving generally other biotic interactions (as he-mipterans) so is difficult to predict under interacting fac-tors of climate change. However, as it represent a protec-tion for the plant (and sometimes nutrients supply), is likely to be reinforced. In the future, increased droughts and generally climate changes could affect mutualistic interactions between plants and other species.

2 Mutualism breakdown under climate change: the case of

plant-pollinator networks

2.1 How can climate change disrupt plant-pollinator interactions?

Plant-pollinator interactions include a diverse range of mutualism types, from facultative polyphilic interac-tions to obligate oligophilic symbiosis. In general, plant-pollinator mutualisms involve many species interacting in complex networks and are therefore studied at community level. Most plant-pollinator networks are asymmetric and nested with generalist pollinators interacting with special-ist plants and specialist pollinator interacting with general-ist plants. Obligate interactions are more rare but no less important for ecosystem functions (e.g. Fig-wasp interac-tion).

There are significant concerns regarding the effects of climate change on plant-pollinator systems because of the importance of pollination for maintaining wild plant communities, ecosystem stability and crop production (Fontaine et al. 2005). Interacting factors of climate change may produce different responses in plant-pollinator interactions (Hoover et al. 2012). Spatial and temporal synchrony between plant flowering and pollina-tor activity is requisite for the existence of plant-pollinator mutualism (Elzinga et al. 2007). However, climate change may disrupt plant-pollinator interactions by producing phenological shifts or changes to species distribution ranges, leading to temporal and spatial mismatches (Heg-land et al. 2009).

Shifts of plant and animal phenologies as a conse-quence of climate change have been well documented (Walther et al. 2002; Parmesan 2007). For example, a delay in seasonal migrations of butterflies has being rec-orded as a response to increased temperatures (Sparks et al. 2006) and changes on precipitation regimes (Srygley et al. 2010). Earlier flowering of plants has been exhaustive-ly reported all over the world (e.g. Parmesan 2007). How-ever, shifts in life cycles are not necessarily synchronized between plants and pollinators, leading to phenological mismatches and eventually to the disruption of interac-tions (Rafferty et al. 2013). Direct consequences of phe-nological decoupling on plants and pollinators are summa-rized in Figure 4.

Climate change also has an impact on species distri-bution range (Walther et al. 2002). Rapid changes to plant species distribution have been reported but great variation of the extent of range modifications are observed between different species (Chen et al. 2011). Historical evidence based on pollen records suggests that it is unlikely that inter-related species shift distribution in the same direc-tion, allowing for the maintenance of mutualistic interac-tions (Dunn et al. 2009). Therefore the disassembling of communities by individualistic range shifts is predicted


(Walther et al. 2002). However, the effects of this spatial mismatch on plant-pollinator interactions has been poorly studied (Hegland et al. 2009).

Figure 4: Schematic showing how climate change can affect

plant-pollinator interactions. A direct effect on species phenolo-gy and distribution causes spatial and temporal mismatches

disrupting plant-pollinator interactions. The cascade effects that may have this disruption on plants and pollinators are shown on left (plant) and right (pollinator) panels. Modified from Hegland

et al. (2009).

2.2 Modeling the outcomes of plant-pollination systems

Predicting the future of plant-pollinator system is challenging because of its complexity and local condition variability (Wolkovich et al. 2012). Changes to climate conditions may lead to a mutualism breakdown when mutualism is not resilient or flexible enough, dependent on the characteristics of the interaction. Mathematical models combined with knowledge of life history traits have been used to predict the effect of environmental fluctuations on plant-pollination interactions (Gilman et al. 2012; Rafferty et al. 2013; Fagan et al. 2014). These models provide a general view on how diverse plant-pollinator systems will respond to climate change based on endogenous and exogenous characteristics.

Most models study the response of plant-pollinator interactions to plant phenological shifts (tem-poral mismatch). Stronger phenological shifts increase the probability of mismatch between flowering and pollinator activity. This temporal disruption affects both partners (Fig.3). Temporal mismatch reduces potential food re-sources for pollinators (Memmott et al. 2007; Gilman et al. 2012), and reduces reproduction success for plants (Vilela et al. 2017; Fig. 4). Generally, survival of at least one of the partners is predicted for generalist or facultative mutualisms, while co-extinctions usually imply mutual-isms with more specialized and obligate species (Rafferty et al. 2015).

Memmott et al. (2007) found that interactions in-volving generalist species tended to persist, but with a

decrease in food resources for pollinators, while specialist pollinators were more likely to become extinct in the total absence of food supply. Gilman et al. (2012) found simi-lar results suggesting that generalist species were more likely to survive if other resource supplies were available, and survival was then related to flowering abundance and timing of all plant species from the community. In cases where mutualism persists at the community level, some plant-pollination interactions are disrupted but immediate-ly replaced by the formation of new ones, but this is only likely if species are generalist. This redundancy is linked to the nested characteristic of plant-pollinator networks. Nestedness may provide plant-pollinator mutualisms more resistance to climate change and species loss (Bascompte et al. 2006). Memmott et al. (2004) confirmed the im-portance of nestedness by simulating the consequences of species removal from pollination interaction networks. They highlight the importance of generalist species on the maintaining of mutualisms but concluded that generalist pollinators loss could unleash extinction cascades across multiple trophic levels causing immeasurable damage to ecosystems.

Fagan et al. (2014) studied how plant population dynamics change as a consequence of phenological mis-matches. They predicted changes to population growth rates in different temporal mismatch scenarios and found that plant-pollinator systems are more sensitive when flowers or pollinators are short-lived or present high with-in-population synchrony in emergence/arrival dates (Fig. 5). Asynchrony within populations can reduce the pheno-logical decoupling by extending the net overlap time be-tween flowering and pollinator activity.

Figure 5: Predicted changes on plant population growth rate (ρ100) in function of phenological mismatch measured as the

separation between peak pollinator emergence and peak plant flowering for two scenarios: long-lived pollinators and long-

lived flowers (right; e.g. orchids and oligolectic bees) and short-lived pollinators and short-lived flowers (left; e.g. bromeliads

and birds). When ρ100=1 the population size stay constant. Line types represent different phenological distribution of plants and

pollinators: (i) broad, (ii) medium, and (iii) narrow. Broader distributions are related to within population synchrony and

narrow distributions to asynchrony. Modified from Fagan et al. (2014).


2.3 The vulnerability of obligate mutual-isms

Many studies agree that probability of extinction is more likely to occur in obligate interactions and when plant or pollinator population size decreases below a threshold. This is because small populations can suffer an Allee effect leading to the extinction of at least one of the partners (Gilman et al. 2012; Fagan et al. 2014).

Fig-wasp extinction on Borneo is an example of how obligate interactions can be vulnerable to climate change (Harrison 2000). Following a severe drought linked to the El Niño episode in Borneo, eight Ficus spe-cies suffered from prolonged shifts on its reproduction phenology. As a result, the wasp that pollinates figs be-came locally extinct. The frequency and severity of droughts has increased significantly in the last decades as a result of climate change and extinctions of coevolved mutualisms could be expected.

In a nutshell, climate change may lead to tem-poral and spatial mismatches between plant flowering and pollinator activity. Such shifts most likely result in the interaction disruption. This can be caused by a reduction on pollinator’s food supply and (crossed-) pollination rates for plants or by a decreased on population leading to an Allee effect. As must plant-pollinator networks are nested, the presence of both generalist plants and general-ist pollinators may promote the formation of new interac-tions allowing the maintenance of plant-pollinator system at the community level. However, specialist and obligate species might be more vulnerable to extinction.

Conclusion Plant mutualisms play a major role in ecosystems

functioning and maintenance. Predicting the trajectory of existing mutualisms is crucial to prevent negative irre-versible consequences on world ecosystems. Some pat-terns in the response to climate change are beginning to emerge for the different groups of mutualisms studied here. We reviewed the effect of climate change on ant-plant and plant-pollinator mutualisms. Ant-plant mutual-isms are likely to persist to face the increased herbivory and environmental stress expected under climate warming and drought. In contrast, plant-pollinator mutualisms are likely to be disrupted because of a temporal and spatial mismatch between plant flowering and pollinator activity. However, these outcomes are difficult to generalize be-cause of the complexity and variability of both mutual-isms. The response of mutualisms to climate change will depend on interaction characteristics like specificity, inti-macy (symbiotic or transitory) or the number of partici-pants in a given interaction.

On one hand, species interacting in symbiotic mutu-alisms are expected to evolve in the same direction and in

the case of ant-plant mutualism the tendency seems to be the maintenance of the interaction. The explosion of her-bivores attracted by the physicochemical modifications of the plants due to drought strengthens the mutualism ant-plant and hemiptera-ant-plant. All the actors of the mutu-alism maintain a cycle (protection, feeding) precious which allows them to survive the environmental changes.

On the other hand, species interacting in transitory mutualisms, like plants and their pollinators, risk disrup-tion because they react independently to environmental changes. The presence of generalist species in plant-pollinator networks may enhance the maintenance of pollination services at community levels. However, many specialists, equally important to the functioning of these networks, risk becoming extinct and should not be ne-glected. Increased efforts in modeling plant-pollination systems highlights the importance of data on life-history traits and population ecology to achieve a better under-standing of the future of biotic interactions.

Our review is limited to only two types of mutual-isms, but plants interact with many organisms that may influence plant responses to climate change and affect all inter-dependent trophic levels. Some interactions, such as plant-pollinator mutualisms, have received more attention, while some interactions remain poorly studied. However, in recent years progress has been made in understanding the effects of climate change and anthropogenic influ-ences on biotic interactions and on ecosystem responses.

Acknowledgements We thank Céline Leroy for the subject proposition

and for the guidance throughout the research. We equally thank Timothy Chubb for the English corrections and suggestions.

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The effect of climate change on plant mutualistic interactions · plant protection and nutrition,...

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