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Dynamics of the aphid-ant mutualism
Stockholm University, Faculty of Science, Department of Zoology.
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

An appreciation of the role of mutualism is essential when studying ecology and evolution in most ecosystems. Information covering aspects of mutualistic interactions can serve as a complement to the somewhat one-sided perspective from the 1950’s and 60’s that is used when teaching biology. In this thesis I applied an in-depth approach in which variation in the interspecific interaction between Aphis fabae aphids and Lasius niger ants was studied both in the field and in the laboratory. An emphasis was put on studies spanning several consecutive aphid generations. This approach revealed important differences between ant tended aphids and those without ants. In the lab, I found an initial decrease in aphid adult size and reproductive investment in the first generations after the start of ant tending, which was followed by a recovery to the pre-tending situation after about four generations. Another laboratory experiment showed an increase in alate (winged aphid) production from exposure to aphid alarm pheromones, and an even stronger decrease in alate production from ant attendance, suggesting that ants have gained the upper hand in an evolutionary conflict over aphid dispersal. Results from a field experiment further emphasized the possibility of negative effects of ants on aphids, showing that ant-tended aphid colonies experienced a higher rate of parasitoid attacks, produced fewer alates and embryos in adult aphids. The thesis highlights the scope for variation in the net effect of the interaction for aphids, and argues that, depending on the environmental circumstances, the interaction may sometimes and perhaps even often not really be a case of mutualism. 

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2015. , 24 p.
Keyword [en]
mutualism, transgenerational, aphids, aphid-ant, conflict of interest, (E)-β-farnesene, phenotypic plasticity, predation risk, wing induction, maternal effect, reproductive investment, embryo size
National Category
Behavioral Sciences Biology
Research subject
Ethology
Identifiers
URN: urn:nbn:se:su:diva-111301ISBN: 978-91-7649-076-1 (print)OAI: oai:DiVA.org:su-111301DiVA: diva2:775168
Public defence
2015-02-06, Ahlmannsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 4: Manuscript.

Available from: 2015-01-15 Created: 2014-12-30 Last updated: 2017-11-22Bibliographically approved
List of papers
1. Ant-aphid mutualism: the influence of ants on the aphid summer cycle
Open this publication in new window or tab >>Ant-aphid mutualism: the influence of ants on the aphid summer cycle
Show others...
2012 (English)In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 121, no 1, 61-66 p.Article in journal (Refereed) Published
Abstract [en]

There are few longtime studies on the effects on aphids of being tended by ants. The aim of this study is to investigate how the presence of ants influences settling decisions by colonizing aphids and the post-settlement growth and survival of aphid colonies. We conducted a field experiment using the facultative myrmecophile Aphis fabae and the ant Lasius niger. The experiment relied on natural aphid colonization of potted plants of scentless mayweed Tripleurospermum perforatum placed outdoors. Ants occurred naturally at the field site and had access to half of the pots and were prevented from accessing the remainder. The presence of winged, dispersing aphids, the growth and survival of establishing aphid colonies, and the presence of parasitoids were measured in relation to presence or absence of ants, over a period of five weeks. The presence of ants did not significantly influence the pattern of initial host plant colonization or the initial colony growth, but ant-tended aphids were subject to higher parasitism by hymenopteran parasitoids. The net result over the experimental period was that the presence of ants decreased aphid colony productivity, measured as the number of winged summer migrants produced from the colonized host plants. This implies that aphids do not always benefit from the presence of ants, but under some conditions rather pay a cost in the form of reduced dispersal.

National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-71655 (URN)10.1111/j.1600-0706.2011.19387.x (DOI)000298484200007 ()
Available from: 2012-01-29 Created: 2012-01-29 Last updated: 2017-12-08Bibliographically approved
2. Transgenerational effects and the cost of ant tending in aphids
Open this publication in new window or tab >>Transgenerational effects and the cost of ant tending in aphids
2013 (English)In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 173, no 3, 779-790 p.Article in journal (Refereed) Published
Abstract [en]

In mutualistic interactions, partners obtain a net benefit, but there may also be costs associated with the provision of benefits for a partner. The question of whether aphids suffer such costs when attended by ants has been raised in previous work. Transgenerational effects, where offspring phenotypes are adjusted based on maternal influences, could be important in the mutualistic interaction between aphids and ants, in particular because aphids have telescoping generations where two offspring generations can be present in a mature aphid. We investigated the immediate and transgenerational influence of ant tending on aphid life history and reproduction by observing the interaction between the facultative myrmecophile Aphis fabae and the ant Lasius niger over 13 aphid generations in the laboratory. We found that the effect of ant tending changes dynamically over successive aphid generations after the start of tending. Initially, total aphid colony weight, aphid adult weight and aphid embryo size decreased compared with untended aphids, consistent with a cost of ant association, but these differences disappeared within four generations of interaction. We conclude that transgenerational effects are important in the aphid-ant interactions and that the costs for aphids of being tended by ants can vary over generations.

Keyword
Aphid-ant mutualism, Maternal effects, Reproductive investment, Embryo size, Plasticity
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-96878 (URN)10.1007/s00442-013-2659-y (DOI)000325819700014 ()
Funder
Swedish Research Council, 621-2010-5437
Note

AuthorCount:4;

Available from: 2013-11-28 Created: 2013-11-28 Last updated: 2017-12-06Bibliographically approved
3. Alate production in an aphid in relation to ant tending and alarm pheromone
Open this publication in new window or tab >>Alate production in an aphid in relation to ant tending and alarm pheromone
2014 (English)In: Ecological Entomology, ISSN 0307-6946, E-ISSN 1365-2311, Vol. 39, no 5, 664-666 p.Article in journal (Refereed) Published
Abstract [en]

1. Winged dispersal is vital for aphids as predation pressure and host plant conditions fluctuate. 2. Ant-tended aphids also need to disperse, but this may represent a cost for the ants, resulting in an evolutionary conflict of interest over aphid dispersal. 3. The combined effects of aphid alarm pheromone, indicating predation risk, and ant attendance on the production of winged aphids were examined in an experiment with Aphis fabae (Homoptera: Aphididae) (Scopoli 1763) aphids and Lasius niger (Formicidae: Formicinae) (Linne, 1758) ants. 4. This study is the first to investigate the joint effects of alarm pheromone and ant attendance, and also the first to detect an influence of alarm pheromone on the production of winged morphs in A. fabae. 5. After a period of 2 weeks, it was found that aphid colonies exposed to intermittent doses of alarm pheromone produced more winged individuals, whereas ant tending had the opposite effect. The effects were additive on a log scale, and ant attendance had a greater proportional influence than exposure to alarm pheromone. A tentative conclusion is that ants have gained the upper hand in an evolutionary conflict about aphid dispersal.

Keyword
(E)--farnesene, alarm pheromone, aphid-ant mutualism, phenotypic plasticity, predation risk, wing induction
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-108997 (URN)10.1111/een.12130 (DOI)000342982000016 ()
Note

AuthorCount:2;

Available from: 2014-12-04 Created: 2014-11-10 Last updated: 2017-12-05Bibliographically approved
4. The influence of ants and parasitoids on aphid reproduction in the field
Open this publication in new window or tab >>The influence of ants and parasitoids on aphid reproduction in the field
(English)Manuscript (preprint) (Other academic)
Abstract [en]
  1. The aim of this study is to investigate how the availability of attending ants influences aphid reproductive investment and the rate of parasitoid attack.
  2. We conducted a field experiment involving the facultative myrmecophile Aphis fabae and the ant species Lasius niger. The experiment relied on natural aphid colonization of potted plants of scentless mayweed (Tripleurospermum perforatum) placed outdoors. Ants that were naturally present at the field site had access to half of the pots and were excluded from the remainder.
  3. Adults aphids were sampled from plotted plants during the 4th and 5th weeks of the study, preserved in ethanol and then dissected to reveal the numbers and sizes of aphid embryos and the presence of hymenopteran parasitoid larvae.
  4. Ant-tended aphids were more often parasitized and contained fewer embryos, but with a greater proportion of these embryos being large. In conjunction with previous analyses of this interaction, the results indicate that under the conditions of our field experiment the net effect of the presence of ants on aphids is negative, throwing doubt on the mutualistic nature of the interaction. 
Keyword
ant-aphid interactions, Aphis fabae, Lasius niger, mutualism, parasitism, reproductive investment, aphid embryo sizes
National Category
Behavioral Sciences Biology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-111217 (URN)
Funder
Swedish Research Council
Available from: 2014-12-29 Created: 2014-12-29 Last updated: 2016-01-29Bibliographically approved

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