Plant–Animal Interactions: Exploring Costs and Benefits in Highly Conditional Relationships

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Protection and Biotic Interactions".

Deadline for manuscript submissions: 30 June 2024 | Viewed by 13036

Special Issue Editor

Laboratório de Ecologia Comportamental e de Interações, Instituto de Biologia, Universidade Federal de Uberlândia, Cx. P. 593, Uberlândia CEP 38400-920, MG, Brazil
Interests: animal behavior; arthropod–plant interactions; behavioral ecology; plant–animal interactions
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Whether or not they are mutually beneficial, plant–animal interactions are highly variable in their outcomes, depending on a variety or combination of abiotic and biotic factors. Depending on the biotic features of the associated species, a mutualistic interaction can be converted into a facilitative one, or even an exploitative one, such as parasitism. In this special volume, we intend to pay special attention to studies that explore how variation in environmental and biological aspects, which shape plant–animal systems, can directly influence the outcomes of these interactions.

Prof. Dr. Kleber Del-Claro
Guest Editor

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Keywords

  • mutualism
  • facilitation
  • herbivory
  • pollination

Published Papers (11 papers)

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Research

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12 pages, 5300 KiB  
Article
Effects of Florivory on Floral Visitors and Reproductive Success of Sagittaria lancifolia (Alismataceae) in a Mexican Wetland
Plants 2024, 13(4), 547; https://doi.org/10.3390/plants13040547 - 17 Feb 2024
Viewed by 329
Abstract
Florivores consume floral structures with negative effects on plant fitness and pollinator attraction. Several studies have evaluated these consequences in hermaphroditic plants, but little is known about the effects on monoecious and dioecious species. We characterize the florivory and its effects on floral [...] Read more.
Florivores consume floral structures with negative effects on plant fitness and pollinator attraction. Several studies have evaluated these consequences in hermaphroditic plants, but little is known about the effects on monoecious and dioecious species. We characterize the florivory and its effects on floral visitors and reproductive success in a monoecious population of Sagittaria lancifolia. Five categories of florivory were established according to the petal area consumed. Visits were recorded in male and female flowers within the different damage categories. Reproductive success was evaluated through fruit number and weight, as well as the number of seeds per fruit. Our results show that the weevil Tanysphyrus lemnae is the main florivore, and it mainly damages the female flowers. Hymenoptera were recorded as the most frequent visitors of both male and female flowers. Male and female flowers showed differences in visit frequency, which decreases as flower damage increases. Reproductive success was negatively related to the level of damage. We found that florivory is common in the population of S. lancifolia, which can exert a strong selective pressure by making the flowers less attractive and reducing the number of seeds per fruit. Future studies are needed to know how florivores affect plant male fitness. Full article
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10 pages, 1792 KiB  
Article
Plant Reproductive Success Mediated by Nectar Offered to Pollinators and Defensive Ants in Terrestrial Bromeliaceae
Plants 2024, 13(4), 493; https://doi.org/10.3390/plants13040493 - 08 Feb 2024
Viewed by 409
Abstract
Most plants produce floral nectar to attract pollinators that impact pollination and seed production; some of them also secrete extrafloral nectar harvested by insects that may influence the plant reproductive success. The aim of this study was to analyze the effects of excluding [...] Read more.
Most plants produce floral nectar to attract pollinators that impact pollination and seed production; some of them also secrete extrafloral nectar harvested by insects that may influence the plant reproductive success. The aim of this study was to analyze the effects of excluding pollinators and/or ants on the per-plant reproductive success in two species (Dyckia floribunda Griseb. and Dyckia longipetala Baker, Bromeliaceae) that produce floral and extrafloral nectar. The hypothesis states that both ecological processes (pollination and ant defense) involving nectar-mediated animal–plant interactions are beneficial for plant reproductive success. We expected the highest decrease in the plant fruit and seed sets when the pollinators and ants were excluded, and a moderate decrease when solely ants were excluded, compared to the control plants (those exposed to pollinators and ants). In addition, a lower natural reproductive success was also expected in the self-incompatible D. longipetala than in the self-compatible D. floribunda, as the former totally depends on animal pollination for seed production. D. floribunda and D. longipetala presented similar trends in the response variables, and the expected results for the experimental treatments were observed, with some variations between species and among populations. The ecological function of nectar is important because these two plant species depend on pollinators to produce seeds and on ants to defend flowers from the endophytic larvae of Lepidoptera. The study of multispecies interactions through mechanistic experiments could be necessary to clarify the specific effects of different animals on plant reproductive success. Full article
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12 pages, 1472 KiB  
Article
Spider–Plant Interaction: The Role of Extrafloral Nectaries in Spider Attraction and Their Influence on Plant Herbivory and Reproduction
Plants 2024, 13(3), 368; https://doi.org/10.3390/plants13030368 - 26 Jan 2024
Viewed by 553
Abstract
Spiders, abundant and diverse arthropods which occur in vegetation, have received little attention in studies investigating spider–plant interactions, especially in plants which have extrafloral nectaries (EFNs). This study examines whether spiders attracted to EFNs on the plant Heteropterys pteropetala (Malpighiaceae) function as biological [...] Read more.
Spiders, abundant and diverse arthropods which occur in vegetation, have received little attention in studies investigating spider–plant interactions, especially in plants which have extrafloral nectaries (EFNs). This study examines whether spiders attracted to EFNs on the plant Heteropterys pteropetala (Malpighiaceae) function as biological protectors, mitigating leaf herbivory and positively impacting plant fitness, through manipulative experiments. Spiders are attracted to EFNs because, in addition to consuming the resource offered by these structures, they also consume the herbivores that are attracted by the nectar. At the same time, we documented the reproductive phenology of the plant studied and the abundance of spiders over time. Our results revealed that the plant’s reproductive period begins in December with the emergence of flower buds and ends in April with the production of samarids, fruits which are morphologically adapted for wind dispersal, aligning with the peak abundance of spiders. Furthermore, our results demonstrated that spiders are attracted to plants that exude EFNs, resulting in a positive impact on reducing leaf area loss but with a neutral effect on protecting reproductive structures. By revealing the protective function of spiders’ vegetative structures on plants, this research highlights the ecological importance of elucidating the dynamics between spiders and plants, contributing to a deeper understanding of ecosystems. Full article
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12 pages, 1419 KiB  
Article
Chemical Camouflage Induced by Diet in a Pest Treehopper on Host Plants
Plants 2024, 13(2), 216; https://doi.org/10.3390/plants13020216 - 12 Jan 2024
Viewed by 594
Abstract
Ants patrol foliage and exert a strong selective pressure on herbivorous insects, being their primary predators. As ants are chemically oriented, some organisms that interact with them (myrmecophiles) use chemical strategies mediated by their cuticular hydrocarbons (CHCs) to deal with ants. Thus, a [...] Read more.
Ants patrol foliage and exert a strong selective pressure on herbivorous insects, being their primary predators. As ants are chemically oriented, some organisms that interact with them (myrmecophiles) use chemical strategies mediated by their cuticular hydrocarbons (CHCs) to deal with ants. Thus, a better understanding of the ecology and evolution of the mutualistic interactions between myrmecophiles and ants depends on the accurate recognition of these chemical strategies. Few studies have examined whether treehoppers may use an additional strategy called chemical camouflage to reduce ant aggression, and none considered highly polyphagous pest insects. We analyzed whether the chemical similarity of the CHC profiles of three host plants from three plant families (Fabaceae, Malvaceae, and Moraceae) and the facultative myrmecophilous honeydew-producing treehopper Aetalion reticulatum (Hemiptera: Aetalionidae), a pest of citrus plants, may play a role as a proximate mechanism serving as a protection against ant attacks on plants. We found a high similarity (>80%) between the CHCs of the treehoppers and two of their host plants. The treehoppers acquire CHCs through their diet, and the chemical similarity varies according to host plant. Chemical camouflage on host plants plays a role in the interaction of treehoppers with their ant mutualistic partners. Full article
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13 pages, 3698 KiB  
Article
Context-Dependent Ant-Pollinator Mutualism Impacts Fruit Set in a Hummingbird-Pollinated Plant
Plants 2023, 12(21), 3688; https://doi.org/10.3390/plants12213688 - 26 Oct 2023
Viewed by 2225
Abstract
Context-dependence in mutualisms is a fundamental aspect of ecological interactions. Within plant-ant mutualisms, particularly in terms of biotic protection and pollination, research has predominantly focused on elucidating the benefits while largely overlooking potential costs. This notable gap underscores the need for investigations into [...] Read more.
Context-dependence in mutualisms is a fundamental aspect of ecological interactions. Within plant-ant mutualisms, particularly in terms of biotic protection and pollination, research has predominantly focused on elucidating the benefits while largely overlooking potential costs. This notable gap underscores the need for investigations into the drawbacks and trade-offs associated with such mutualistic relationships. Here, we evaluated the role of pericarpial nectaries (PNs) in shaping the dynamics of ant-pollinator mutualisms. Specifically, we investigated whether ants visiting the PN of Palicourea rigida (Rubiaceae) could deter hummingbirds and disrupt pollination, ultimately influencing fruit production. Our research involved manipulative experiments and observation of ant-pollinator interactions on P. rigida plants in the Brazilian savannah. We found that visiting ants can deter hummingbirds and/or disrupt pollination in P. rigida, directly influencing fruit set. However, these results are species-specific. The presence of very aggressive, large predatory ants, such as E. tuberculatum, had a negative impact on hummingbird behavior, whereas aggressive mid-sized ants, such as C. crassus, showed no effects. Our study illuminates the multifaceted aspects of ant-plant mutualisms and underscores the importance of evaluating costs and unexpected outcomes within these ecological relationships. Full article
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16 pages, 2946 KiB  
Article
Extrafloral Nectary-Bearing Plants Recover Ant Association Benefits Faster and More Effectively after Frost-Fire Events Than Frost
Plants 2023, 12(20), 3592; https://doi.org/10.3390/plants12203592 - 17 Oct 2023
Viewed by 2182
Abstract
The Cerrado confronts threats such as fire and frost due to natural or human-induced factors. These disturbances trigger attribute changes that impact biodiversity. Given escalating climate extremes, understanding the effects of these phenomena on ecological relationships is crucial for biodiversity conservation. To understand [...] Read more.
The Cerrado confronts threats such as fire and frost due to natural or human-induced factors. These disturbances trigger attribute changes that impact biodiversity. Given escalating climate extremes, understanding the effects of these phenomena on ecological relationships is crucial for biodiversity conservation. To understand how fire and frost affect interactions and influence biological communities in the Cerrado, our study aimed to comprehend the effects of these two disturbances on extrafloral nectar (EFN)-bearing plants (Ouratea spectabilis, Ochnaceae) and their interactions. Our main hypothesis was that plants affected by fire would grow again more quickly than those affected only by frost due to the better adaptation of Cerrado flora to fire. The results showed that fire accelerated the regrowth of O. spectabilis. Regrowth in plants with EFNs attracted ants that proved to be efficient in removing herbivores, significantly reducing foliar herbivory rates in this species, when compared to the species without EFNs, or when ant access was prevented through experimental manipulation. Post-disturbance ant and herbivore populations were low, with frost leading to greater reductions. Ant richness and diversity are higher where frost precedes fire, suggesting that fire restores Cerrado ecological interactions better than frost, with less impact on plants, ants, and herbivores. Full article
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10 pages, 1416 KiB  
Article
Lutein and Zeaxanthin Content in 21 Plant Species from a Very Humid Premontane Forest in Colombia Palatable for Free-Range Laying Hens
Plants 2023, 12(19), 3484; https://doi.org/10.3390/plants12193484 - 05 Oct 2023
Viewed by 698
Abstract
Xanthophylls, such as lutein and zeaxanthin, have several functions in both plants and humans, including detoxification of oxidants (reactive oxygen species (ROS) and other radicals), maintenance of the structural and functional integrity of biological membranes, and photoprotection from intense light damage. The objective [...] Read more.
Xanthophylls, such as lutein and zeaxanthin, have several functions in both plants and humans, including detoxification of oxidants (reactive oxygen species (ROS) and other radicals), maintenance of the structural and functional integrity of biological membranes, and photoprotection from intense light damage. The objective of the present study was to investigate the lutein and zeaxanthin content of 21 species of plants from a very humid premontane forest in Colombia during both dry and rainy seasons. The plants were selected based on being voluntarily eaten by laying hens under free-range conditions. Lutein and zeaxanthin were identified and quantified by high-performance liquid chromatography (HPLC). The results showed that all plants tested contained lutein, at levels ranging from 65.7 to 350 µg/g. Zeaxanthin levels were much lower (2.2 to 26.2 µg/lg) and were detected in only 5 of the 21 plants analyzed. Given that the lutein content of the plants tested in the present study was found to be comparable to that reported in marigold flowers (4–800 µg/g), it is possible that these plants can be used as a source of lutein in free-range laying hen production systems. Full article
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17 pages, 2097 KiB  
Article
Flowering Time Variation in Two Sympatric Tree Species Contributes to Avoid Competition for Pollinator Services
Plants 2023, 12(19), 3347; https://doi.org/10.3390/plants12193347 - 22 Sep 2023
Viewed by 2416
Abstract
Competition is an important biological filter that can define crucial features of species’ natural history, like survival and reproduction success. We evaluated in the Brazilian tropical savanna whether two sympatric and congenereric species, Qualea multiflora Mart. and Q. parviflora Mart. (Vochysiaceae), compete for [...] Read more.
Competition is an important biological filter that can define crucial features of species’ natural history, like survival and reproduction success. We evaluated in the Brazilian tropical savanna whether two sympatric and congenereric species, Qualea multiflora Mart. and Q. parviflora Mart. (Vochysiaceae), compete for pollinator services, testing whether there is a better competitor or whether plants present any anti-competitive mechanism. Additionally, we investigated the breeding system, pollinators, and flowering phenology of both species. The results showed that Q. multiflora and Q. parviflora are dependent on pollinators for fruit formation, as they exhibited a self-incompatible and non-agamospermic breeding system. These plants shared the same guild of pollinators, which was formed by bees and hummingbirds, and an overlap in the flower visitation time was observed. Each plant species had different pollinator attraction strategies: Q. multiflora invested in floral resource quality, while Q. parviflora invested in resource quantity. The blooming time showed a temporal flowering partition, with highly sequential flowering and no overlap. Qualea parviflora bloomed intensely from September to October, while Q. multiflora bloomed from November to January, with the flowering peak occurring in December. The two Qualea species have morphologically similar flowers, are sympatric, and share the same pollinator community, with overlapping foraging activity during the day. However, they do not compete for pollinator services as they exhibit an anti-competitive mechanism mediated by temporal flowering partition. Full article
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16 pages, 1469 KiB  
Article
Floral Aroma and Pollinator Relationships in Two Sympatric Late-Summer-Flowering Mediterranean Asparagus Species
Plants 2023, 12(18), 3219; https://doi.org/10.3390/plants12183219 - 10 Sep 2023
Viewed by 725
Abstract
This research delves into plant–pollinator relationships within the Mediterranean region, focusing on two synchronous and sympatric asparagus species: A. acutifolius and A. albus. For the first time, the floral scents of the genus Asparagus are reported. We investigate the volatile organic compounds [...] Read more.
This research delves into plant–pollinator relationships within the Mediterranean region, focusing on two synchronous and sympatric asparagus species: A. acutifolius and A. albus. For the first time, the floral scents of the genus Asparagus are reported. We investigate the volatile organic compounds (VOCs) present in their floral scents and their impact on pollinator attraction. Captured flower-emitted VOCs underwent solid-phase microextraction of headspace (SPME-HS) and gas chromatography and mass spectrometry (GC-MS) analysis. The investigation confirms distinctive aroma profiles for each species. A. albus predominantly emits benzene derivatives and sesquiterpenes, while A. acutifolius is characterized by carotenoid derivatives, monoterpenes, and sesquiterpenes. The only shared compounds between the two species are the sesquiterpenes (Z,E)-α-farnesene and (E,E)-α-farnesene. A positive correlation links peak floral aroma intensity (benzenoids in A. albus and ionones in A. acutifolius) with a higher pollinator visit frequency, emphasizing the critical role of intense floral scents in pollinator attraction. The study of reproductive aspects reveals almost complete gynodioecy in A. acutifolius, influencing unique dynamics for the two species. These adaptations hold significant importance within the Mediterranean ecosystem, particularly during the late dry summer period, when a limited number of plant species vie for a shared primary pollinator. Full article
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10 pages, 276 KiB  
Article
Measuring Bee Effects on Seed Traits of Hybrid Sunflower
Plants 2023, 12(14), 2662; https://doi.org/10.3390/plants12142662 - 16 Jul 2023
Viewed by 924
Abstract
In hybrid sunflower, bee pollination can improve productivity, but the contribution of bees to productivity may be over or underestimated. To estimate bee effects (seed trait gains from exposure to bees during anthesis), single capitula are commonly covered with a porous material to [...] Read more.
In hybrid sunflower, bee pollination can improve productivity, but the contribution of bees to productivity may be over or underestimated. To estimate bee effects (seed trait gains from exposure to bees during anthesis), single capitula are commonly covered with a porous material to exclude bees. However, depending on the exclosure porosity, estimates of the magnitude of bee effects will vary. In two studies, porosity size and bee effect gains in two sunflower types were tested. In the exclosure study, Delnet exclosures severely reduced seed set and exclosures with larger porosities and had smaller and similar effects. However, since a few small bees penetrated the largest porosity size tested, exclosures with porosity sizes < 7 mm are recommended. With an exclosure porosity of 5 X 5 mm, the estimated bee effect contribution to the yield was 323 kg per hectare. Effects of exclosures on seed traits were similar in the oilseed and confectionary hybrids tested. Insecticide use did not affect seed traits but did lower insect damage to seeds. Bees from three families, mostly Apidae, were collected while foraging on sunflower. In summary, we recommend the use of exclosures with porosities of about 3 to 5 mm to avoid over or underestimating bee effects. And we recommend holistic insect management for sunflower cropping systems that balances the benefits of bee effects on seed traits with management of pest insects. Full article

Review

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24 pages, 5596 KiB  
Review
Visual-, Olfactory-, and Nectar-Taste-Based Flower Aposematism
Plants 2024, 13(3), 391; https://doi.org/10.3390/plants13030391 - 29 Jan 2024
Viewed by 640
Abstract
Florivory, i.e., flower herbivory, of various types is common and can strongly reduce plant fitness. Flowers suffer two very different types of herbivory: (1) the classic herbivory of consuming tissues and (2) nectar theft. Unlike the non-reversibility of consumed tissues, nectar theft, while [...] Read more.
Florivory, i.e., flower herbivory, of various types is common and can strongly reduce plant fitness. Flowers suffer two very different types of herbivory: (1) the classic herbivory of consuming tissues and (2) nectar theft. Unlike the non-reversibility of consumed tissues, nectar theft, while potentially reducing a plant’s fitness by lowering its attraction to pollinators, can, in various cases, be fixed quickly by the production of additional nectar. Therefore, various mechanisms to avoid or reduce florivory have evolved. Here, I focus on one of the flowers’ defensive mechanisms, aposematism, i.e., warning signaling to avoid or at least reduce herbivory via the repelling of herbivores. While plant aposematism of various types was almost ignored until the year 2000, it is a common anti-herbivory defense mechanism in many plant taxa, operating visually, olfactorily, and, in the case of nectar, via a bitter taste. Flower aposematism has received only very little focused attention as such, and many of the relevant publications that actually demonstrated herbivore repellence and avoidance learning following flower signaling did not refer to repellence as aposematism. Here, I review what is known concerning visual-, olfactory-, and nectar-taste-based flower aposematism, including some relevant cases of mimicry, and suggest some lines for future research. Full article
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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

Title: The Ecology of Cheating: Why Nectar-Rob a Flower More than Once?
Authors: J.L. Bronstein; E.M. Lichtenberg; R.E. Irwin
Affiliation: JLB- University of Arizona; EML - University of North Texas; REI - North Carolina State University
Abstract: Cheating is ubiquitous within mutualisms. Primary nectar-robbers, ubiquitous exploiters of pollination mutualisms, feed through holes they make in corollas. One commonly observed behavior is the addition of new holes to previously robbed flowers. Why flowers should be robbed repeatedly is difficult to understand: a hole signals that a nectar forager has already fed, perhaps very recently, likely reducing its value. Possibilities include: (1) Multiple holes appear only once every flower has been robbed; hence, they represent the only way to acquire nectar for robbers unwilling to re-use an existing hole and who cannot reach nectar by visiting flowers legitimately. (2) Individual foragers make multiple holes during single visits, perhaps as the most effective way to obtain the maximum amount of nectar. (3) previously robbed flowers contain more nectar than unrobbed ones, making them better choices for bees seeking high nectar rewards. During 2014-2016, inflorescences in a Colorado population of Corydalis caseana were tagged and flowers were marked with date-specific colors as they opened. Nectar volumes were recorded from flowers of known age that were protected and exposed to robbers. Holes were counted on exposed flowers as they aged. We also recorded population-wide rates of multiple robbing twice weekly. Multiple holes began appearing when >75% of flowers lacked a single hole, allowing us to reject Hypothesis 1. Hypothesis 2 cannot offer a full explanation because >50% of holes appeared in flowers one or more days after the first hole appeared. Repeated sampling of bagged and exposed inflorescences revealed that flowers fill at a constant rate for 5-7 days and refill after being drained (either by a robber or a pollinator). As a direct consequence, consistent with Hypothesis 3, young, unrobbed flowers are of relatively low value to primary robbers because they contain little nectar. Rather, it is more profitable in many cases for bees to rob older flowers, even if they have previously been robbed. These results cannot explain why bees choose to create new holes rather than reuse existing ones. However, they do offer a simple explanation for the paradoxical clustering of cheater activity. Research on cheating in mutualisms has focused to date on the consequences of being cheated. Conversely, little is known about the choices involved in adopting cheating behaviors. We argue that nectar-robbing can serve as an ideal model system for the broader study of cheating in mutualism.

Title: Plant performance depends to resistance phenotype to a gall-inducing insect
Authors: Jean C. Santos, Janete F. Andrade, Guilherme Ramos Demetrio Ferreira, Eduardo Soares Calixto, Pablo Cuevas-Reyes, Marcos Vinicius Meiado, Denise G. Santana & Wanessa Rejane de Almeida
Affiliation: Universidade Federal de Sergipe; Universidade Federal de Alagoas; University of Florida; Universidad Michoacana de San Nicolás de Hidalgo; Universidade Federal de Uberlândia
Abstract: Variations in plant genotypes and phenotypes are expressed in ways to develop defensive abilities against herbivory. Induced defenses are well-known mechanisms that affect herbivore insect performance and foraging behavior. We aimed to evaluate the performance of Bauhinia brevipes according to phenotype (resistant versus susceptible) against attacks by the gall-inducing insect Schizomyia macrocapillata. We hypothesized that there is a positive relationship between resistance to S. macrocapillata and host plant performance because resistance can have high adaptive value. We evaluated plant architecture, nutritional leaf quality (vegetative performance), and capacity to compound fruits and seeds (reproductive performance) between groups of plants. Offspring performance was also evaluated at three stages of development: seeds, seedlings, and juveniles. There were no differences in the vegetative and reproductive performance of resistant and susceptible mature plants. In addition, there was no relationship between nutritional leaf quality and resistance to S. macrocapillata. Offspring performance was equal for both phenotypes at all developmental stages. We believe that the low incidence of S. macrocapillata in the B. brevipes population contributed to the similar performance between phenotypes. In contrast, plant defenses are costly, and resistant genotypes are favored when the probability of damage to insects is high. However, these genotypes may be disfavored when the probability of herbivore attack is low. Susceptible individuals can overcompensate for the damage caused by S. macrocapillata by increasing the number of leaves and branches. Moreover, strategies such as tolerance to herbivory should be analyzed in this gall insect/plant host system.

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