An official website of the United States government
Phenological mismatch can occur when plants and herbivores differentially respond to changing phenological cues, such as temperature or snow melt date. This often shifts herbivore feeding to plant stages of lower quality. How herbivores respond to plant quality may be also mediated by temperature, which could lead to temperature-by-phenology interactions. We examined how aphid abundance and mutualism with ants were impacted by temperature and host plant phenology. In this study system, aphids Aphis asclepiadis colonize flowering stalks of the host plant, Ligusticum porteri. Like other aphids, abundance of this species is dependent on ant protection. To understand how host plant phenology and temperature affect aphid abundance, we used a multiyear observational study and a field experiment. We observed 20 host plant populations over five years (2017–2021), tracking temperature and snow melt date as well as host plant phenology and insect abundance. We found host plant and aphid phenology to differentially respond to temperature and snow melt timing. Early snow melt accelerated host plant phenology to a greater extent than aphid phenology, which was more responsive to temperature. Both the likelihood of aphid colony establishment and ant recruitment were reduced when aphids colonized host plants at post-flowering stages. In 2019, we experimentally accelerated host plant phenology by advancing snow melt date by two weeks. We factorially combined this treatment with open top warming chambers surrounding aphid colonies. Greatest growth occurred for colonies under ambient temperatures when they occurred on host plants at the flowering stage. Altogether, our results suggest that phenological mismatch with host plants can decrease aphid abundance, and this effect is exacerbated by temperature increases and changes to the ant–aphid mutualism.
more »
« less
Early snowmelt reduces aphid abundance (Aphis asclepiadis) by creating water-stressed host plants (Ligusticum porteri) and altering interactions with ants
Abstract Declining snow cover is reshaping ecological communities. Early loss of snow cover initiates changes in key interactions that mediate herbivore abundance, i.e., top-down and bottom-up effects. In this study, we used a field experiment to test the effects of host plant water stress and phenology on the multitrophic interactions that determine aphid abundance. The aphid, Aphis asclepiadis , in our study system colonizes the flowering stalks of the host plant Ligusticum porteri and relies on a protection mutualism with ants. We added snow and water to replicate host plants and tested for a variety of phenological and physiological responses to these treatments. Relative to host plants in ambient conditions, both water and snow addition reduced key signals of water stress (senescence and abscisic acid levels) and increased seed set. While aphid colonies were generally larger with reduced host plant water stress, the ant–aphid mutualism interacted with plant quality in complex ways. Without ant tending, we did not detect differences in aphid colony growth with host plant treatment. When tended by ants, aphid colony growth was greatest on host plants with snow addition. Host plant quality also altered the benefits exchanged in this mutualism. Ant-tended colonies hosted by plants with snow addition produced honeydew enriched in trehalose, which may have decreased both ant and natural enemy abundance. Our results suggest that early loss of snow reduces aphid abundance by creating low-quality, water-stressed host plants, and this effect may be exacerbated by natural enemies and the costs of ant attendance.
more »
« less
- Award ID(s):
- 1655914
- PAR ID:
- 10228065
- Date Published:
- Journal Name:
- Arthropod-Plant Interactions
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 1872-8855
- Page Range / eLocation ID:
- 33 to 46
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Cooperative interactions may frequently be reinforced by “partner fidelity feedback,” in which high‐ or low‐quality partners drive positive feedbacks with high or low benefits for the host, respectively. Benefits of plant–animal mutualisms for plants have been quantified almost universally in terms of growth or reproduction, but these are only two of many sinks to which a host‐plant allocates its resources. By investigating how partners to host‐plants impact two fundamental plant resources, carbon and water, we can better characterize plant–partner fidelity and understand how plant–partner mutualisms may be modulated by resource dynamics. In Laikipia, Kenya, four ant species compete forAcacia drepanolobiumhost‐plants. These ants differ in multiple traits, from nectar consumption to host‐plant protection. Using a 5‐year ant removal experiment, we compared carbon fixation, leaf water status, and stem non‐structural carbohydrate concentrations for adult ant–plants with and without ant partners. Removal treatments showed that the ants differentially mediate tree carbon and/or water resources. All three ant species known to be aggressive against herbivores were linked to benefits for host‐plant resources, but only the two species that defend but do not prune the host,Crematogaster mimosaeandTetraponera penzigi, increased tree carbon fixation. Of these two species, only the nectivoreC. mimosaeincreased tree simple sugars.Crematogaster nigriceps, which defends the tree but also castrates flowers and prunes meristems, was linked only to lower tree water stress approximated by pre‐dawn leaf water potential. In contrast to those defensive ants,Crematogaster sjostedti, a poor defender that displaces other ants, was linked to lower tree carbon fixation. Comparing the effects of the four ant species across control trees suggests that differential ant occupancy drives substantial differences in carbon and water supply among host trees. Our results highlight that ant partners can positively or negatively impact carbon and/or water relations for their host‐plant, and we discuss the likelihood that carbon‐ and water‐related partner fidelity feedback loops occur across ant–plant mutualisms.more » « less
-
Abstract Over 125 million years of ant-plant interactions have culminated in one of the most intriguing evolutionary outcomes in life history. The myrmecophyteDuroia hirsuta(Rubiaceae) is known for its mutualistic association with the antMyrmelachista schumanniand several other species, mainlyAzteca, in the north-western Amazon. While both ants provide indirect defences to plants, onlyM. schumanninests in plant domatia and has the unique behaviour of clearing the surroundings of its host tree from heterospecific plants, potentially increasing resource availability to its host. Using a 12-year survey, we asked how the continuous presence of either onlyM. schumannior onlyAztecaspp. benefits the growth and defence traits of host trees. We found that the continuous presence ofM. schumanniimproved relative growth rates and leaf shearing resistance ofDuroiabetter than trees withAzteca. However, leaf herbivory, dry matter content, trichome density, and secondary metabolite production were the same in all trees. Survival depended directly on ant association (> 94% of trees died when ants were absent). This study extends our understanding of the long-term effects of strict ant-plant mutualism on host plant traits in the field and reinforces the use ofD. hirsuta–M. schumannias a model system suitable for eco-co-evolutionary research on plant–animal interactions.more » « less
-
Imperiale, Michael J. (Ed.)ABSTRACT Within social insect colonies, microbiomes often differ between castes due to their different functional roles and between colony locations. Trachymyrmex septentrionalis fungus-growing ants form colonies throughout the eastern United States and northern Mexico that include workers, female and male alates (unmated reproductive castes), larvae, and pupae. How T. septentrionalis microbiomes vary across this geographic range and between castes is unknown. Our sampling of individual ants from colonies across the eastern United States revealed a conserved T. septentrionalis worker ant microbiome and revealed that worker ant microbiomes are more conserved within colonies than between them. A deeper sampling of individual ants from two colonies that included all available castes (pupae, larvae, workers, and female and male alates), from both before and after adaptation to controlled laboratory conditions, revealed that ant microbiomes from each colony, caste, and rearing condition were typically conserved within but not between each sampling category. Tenericute bacterial symbionts were especially abundant in these ant microbiomes and varied widely in abundance between sampling categories. This study demonstrates how individual insect colonies primarily drive the composition of their microbiomes and shows that these microbiomes are further modified by developmental differences between insect castes and the different environmental conditions experienced by each colony. IMPORTANCE This study investigates microbiome assembly in the fungus-growing ant Trachymyrmex septentrionalis , showing how colony, caste, and lab adaptation influence the microbiome and revealing unique patterns of mollicute symbiont abundance. We find that ant microbiomes differ strongly between colonies but less so within colonies. Microbiomes of different castes and following lab adaptation also differ in a colony-specific manner. This study advances our understanding of the nature of individuality in social insect microbiomes and cautions against the common practice of only sampling a limited number of populations to understand microbiome diversity and function.more » « less
-
ABSTRACT Successful plant growth requires plants to minimize harm from antagonists and maximize benefit from mutualists. However, these outcomes may be difficult to achieve simultaneously, since plant defenses activated in response to antagonists can compromise mutualism function, and plant resources allocated to defense may trade off with resources allocated to managing mutualists. Here, we investigate how antagonist attack affects plant ability to manage mutualists with sanctions, in which a plant rewards cooperative mutualists and/or punishes uncooperative mutualists. We studied interactions among wild and domesticated pea plants, pea aphids, an aphid‐vectored virus (Pea Enation Mosaic Virus, PEMV), and mutualistic rhizobial bacteria that fix nitrogen in root nodules. Using isogenic rhizobial strains that differ in their ability to fix nitrogen and express contrasting fluorescent proteins, we found that peas demonstrated sanctions in both singly‐infected nodules and mixed‐infection nodules containing both strains. However, the plant's ability to manage mutualists in mixed‐infection nodules traded off with its ability to defend against antagonists: when plants were attacked by aphids, they stopped sanctioning within mixed‐infection nodules, and plants that exerted stricter sanctions within nodules during aphid attack accumulated higher levels of the aphid‐vectored virus, PEMV. Our findings suggest that plants engaged in defense against antagonists suffer a reduced ability to select for the most beneficial symbionts in mixed‐infection tissues. Mixed‐infection tissues may be relatively common in this mutualism, and reduced plant sanctions in these tissues could provide a refuge for uncooperative mutualists and compromise the benefit that plants obtain from mutualistic symbionts during antagonist attack. Understanding the conflicting selective pressures plants face in complex biotic environments will be crucial for breeding crop varieties that can maximize benefits from mutualists even when they encounter antagonists.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1007/s11829-020-09793-2
