Nutritional challenges of feeding a mutualist: Testing for a nutrient–toxin tradeoff in fungus-farming leafcutter ants
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Nutritional challenges of feeding a mutualist : Testing for a nutrient–toxin tradeoff in fungus-farming leafcutter ants. / Crumière, Antonin J. J.; Mallett, Sophie; Michelsen, Anders; Rinnan, Riikka; Shik, Jonathan Z.
I: Ecology, Bind 103, Nr. 6, e3684, 2022.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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TY - JOUR
T1 - Nutritional challenges of feeding a mutualist
T2 - Testing for a nutrient–toxin tradeoff in fungus-farming leafcutter ants
AU - Crumière, Antonin J. J.
AU - Mallett, Sophie
AU - Michelsen, Anders
AU - Rinnan, Riikka
AU - Shik, Jonathan Z.
N1 - Publisher Copyright: © 2022 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.
PY - 2022
Y1 - 2022
N2 - The biochemical heterogeneity of food items often yields tradeoffs as each bite of food tends to contain some nutrients in surplus and others in deficit, as well as other less palatable or even toxic compounds. These multidimensional nutritional challenges are likely to be compounded when foraged foods are used to provision others (e.g., offspring or symbionts) with different physiological needs and tolerances. We explored these challenges in free-ranging colonies of leafcutter ants that navigate a diverse tropical forest to collect plant fragments they use to provision a co-evolved fungal cultivar. We tested the prediction that leafcutter farmers face provisioning tradeoffs between the nutritional quality and concentration of toxic tannins in foraged plant fragments. Chemical analyses of plant fragments sampled from the mandibles of Panamanian Atta colombica leafcutter ants provided little support for a nutrient–tannin foraging tradeoff. First, colonies foraged for plant fragments that ranged widely in tannin concentration. Second, high tannin levels did not appear to restrict colonies from selecting plant fragments with blends of protein and carbohydrates that maximized cultivar performance when measured with in vitro experiments. We also tested whether tannins expand the realized nutritional niche selected by leafcutter ants into high-protein dimensions as: (1) tannins can bind proteins and reduce their accessibility during digestion, and (2) in vitro experiments have shown that excess protein provisioning reduces cultivar performance. Contrary to this hypothesis, the most protein-rich plant fragments did not have highest tannin levels. More generally, the approach developed here can be used to test how multidimensional interactions between nutrients and toxins shape the costs and benefits of providing care to offspring or symbionts.
AB - The biochemical heterogeneity of food items often yields tradeoffs as each bite of food tends to contain some nutrients in surplus and others in deficit, as well as other less palatable or even toxic compounds. These multidimensional nutritional challenges are likely to be compounded when foraged foods are used to provision others (e.g., offspring or symbionts) with different physiological needs and tolerances. We explored these challenges in free-ranging colonies of leafcutter ants that navigate a diverse tropical forest to collect plant fragments they use to provision a co-evolved fungal cultivar. We tested the prediction that leafcutter farmers face provisioning tradeoffs between the nutritional quality and concentration of toxic tannins in foraged plant fragments. Chemical analyses of plant fragments sampled from the mandibles of Panamanian Atta colombica leafcutter ants provided little support for a nutrient–tannin foraging tradeoff. First, colonies foraged for plant fragments that ranged widely in tannin concentration. Second, high tannin levels did not appear to restrict colonies from selecting plant fragments with blends of protein and carbohydrates that maximized cultivar performance when measured with in vitro experiments. We also tested whether tannins expand the realized nutritional niche selected by leafcutter ants into high-protein dimensions as: (1) tannins can bind proteins and reduce their accessibility during digestion, and (2) in vitro experiments have shown that excess protein provisioning reduces cultivar performance. Contrary to this hypothesis, the most protein-rich plant fragments did not have highest tannin levels. More generally, the approach developed here can be used to test how multidimensional interactions between nutrients and toxins shape the costs and benefits of providing care to offspring or symbionts.
KW - fungus
KW - herbivory
KW - leafcutter ants
KW - nutritional geometry
KW - plant secondary metabolites
KW - tannins
U2 - 10.1002/ecy.3684
DO - 10.1002/ecy.3684
M3 - Journal article
C2 - 35315052
AN - SCOPUS:85127935818
VL - 103
JO - Ecology
JF - Ecology
SN - 0012-9658
IS - 6
M1 - e3684
ER -
ID: 308900897