Abstract

The emerging field of nutritional geometry (NG) provides powerful new approaches to test whether and how organisms prioritize specific nutritional blends when consuming chemically complex foods. NG approaches can thus help move beyond food-level estimates of diet breadth to predict invasive success, for instance by revealing narrow nutritional niches if broad diets are actually composed of nutritionally similar foods. We used two NG paradigms to provide different, but complementary insights into nutrient regulation strategies and test a hypothesis of extreme nutritional generalism in colony propagules of the globally distributed invasive ant Monomorium pharaonis. First, in two dimensions (protein:carbohydrates; P:C), M. pharaonis colonies consistently defended a slightly carbohydrate-biased intake target, while using a generalist equal-distance strategy of collectively overharvesting both protein and carbohydrates to reach this target when confined to imbalanced P:C diets. Second, a recently developed right-angled mixture triangle method enabled us to define the fundamental niche breadth in three dimensions (protein:carbohydrates:lipid, P:C:L). We found that colonies navigated the P:C:L landscape, in part, to mediate a tradeoff between worker survival (maximized on high-carbohydrate diets) and brood production (maximized on high-protein diets). Colonies further appeared unable to avoid this tradeoff by consuming extra lipids when the other nutrients were limiting. Colonies also did not rely on nutrient regulation inside their nests, as they did not hoard or scatter fractions of harvested diets to adjust the nutritional blends they consumed. These complementary NG approaches highlight that even the most successful invasive species with broad fundamental macronutrient niches must navigate complex multidimensional nutritional landscapes to acquire limiting macronutrients and overcome developmental constraints as small propagules.

Highlights

  • The factors enabling a species to thrive outside its native range include propagule pressure [1], the absence of natural enemies [2], and the ecological match between its introduced and native habitat [3,4]

  • Using 2-D arrays, we show that M. pharaonis colonies exhibit a generalist equal-distance strategy of regulating total diet harvest and consumption levels even if this requires over-consuming both protein and carbohydrates relative to their respective intake targets

  • An important step will be to test whether and how the realized macronutrient niche of M. pharaonis approaches its fundamental macronutrient niche (FMN) over time during invasions as colony demographic demands change [5], and across invasive populations confined to different nutritional environments [43]

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Summary

Introduction

The factors enabling a species to thrive outside its native range include propagule pressure [1], the absence of natural enemies [2], and the ecological match between its introduced and native habitat [3,4]. Nutritional geometry (NG) has become a powerful hypothesis-driven approach for visualizing how taxa from slime molds [14] to gorillas [15] prioritize multiple competing nutritional requirements to maximize their fitness [7] Since these analyses explicitly define foods as mixtures of multiple covarying nutrients, it is possible to test the hypothesis that successful invaders have exceptionally wide physiological tolerances for nutritionally imbalanced foods, while describing an organism’s ‘fundamental macronutrient niche’ in several dimensions of co-varying nutritional availability [12]. We explore multidimensional nutritional requirements and strategies for meeting those requirements in the invasive ant Monomorium pharaonis We do this by employing two different, but complementary NG paradigms: 1) a 2-D protein:carbohydrate (P:C) approach to visualize how and why colonies prioritize specific nutrients when prevented from reaching their self-selected optimum, and 2) a 3-D protein:carbohydrate:lipid (P:C:L) approach to map the fundamental macronutrient niche of M. pharaonis

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