Eavesdropping Selects for Conspicuous Signals, Elinor M
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Current Biology Vol 24 No 13 R598 glands, and differentiates conspecific small numbers of marks (0.05 bee Eavesdropping from heterospecific pheromones equivalents, 2 marks). This strategy selects for [4,8]. Trigona hyalinata displaces of determining resource access T. spinipes from desirable food [7], costs by eavesdropping on foraging conspicuous signals but must recruit more nestmates to information may be common. do so when the contested resource is Diverse social insects show behavior Elinor M. Lichtenberg1,2,*, heavily occupied. consistent with assessing food Joshua Graff Zivin3, Michael Hrncir4, To test if more odor marks indicate accessibility via the resident’s size, and James C. Nieh1 a more visited, and therefore better group size, familiarity or aggression guarded, food source, we measured (Supplemental information). Animal communication signals T. spinipes pheromone deposition To examine this more general generally evolve to become and recruit arrival. We trained case, we developed a decision increasingly conspicuous for individual foragers to visit a rich analysis model (Supplemental intended receivers [1]. However, sucrose feeder 100 m from their nest information) that tests if more such conspicuous signals and then permitted them to freely conspicuous signals (increased are also more susceptible to recruit nestmates (Supplemental recruitment pheromone deposition) eavesdropping, i.e. exploitation information). The number of foragers lead to higher takeover costs by unintended receivers [2]. It is increased with the number of for eavesdroppers. This model typically thought that eavesdroppers recent odor marks, and continued determines the fight duration at harm signalers and select against to rise once pheromone intensity which individual eavesdroppers conspicuous signals [3]. But, if plateaued (Figure 1A). Forager should switch from approaching to signal conspicuousness deters abundance significantly correlated avoiding non-nestmate odor marks eavesdroppers by indicating a with the cumulative number of odor to maximize the colony’s energetic cost, all receivers benefit. This may marks in the current (r = 0.94) and yield (Figure 1D). It also calculates occur when eavesdroppers exploit preceding (r = 0.75) five-minute the relative cost of making sub- food recruitment signals but need periods (Supplemental information). optimal eavesdropping decisions to fight for food access [4]. Using Thus, the species-specific chemical (Figure 1E). eusocial insects, stingless bees, composition [4,5,8] and the We used our model to predict we show that conspicuous signals number of odor marks provide the eavesdropping behavior for three can indicate competitive costs information eavesdroppers need stingless bee species (T. hyalinata, and enable signalers to escape to infer costs of accessing an T. spinipes [4] and Melipona eavesdropper-imposed costs. The advertised resource. rufiventris [8]; Supplemental dominant eavesdropper, Triogona Next, we determined if T. hyalinata information), and compared hyalinata, avoided higher levels of matches its eavesdropping predicted with measured Trigona spinipes pheromone that responses to these inferred costs. patterns. When parameterized indicate a food source difficult to Individual T. hyalinata foragers were for experimental conditions, our win, and showed attraction to lower given a choice of two feeders, one model predicts well. Decisions pheromone levels that indicate a with no pheromone and one with a that maximize colony fitness (daily relatively undefended resource. Our specific number of T. spinipes odor energetic gain) agree with empirical decision-analysis model reveals that marks (Supplemental information). eavesdropping data (Figure 1D,E). eavesdropping individuals that can We presented pheromone from two Our model predicts that T. hyalinata assess takeover costs can benefit sources: labial glands dissected and M. rufiventris, but not their colony by recruiting to weakly from T. spinipes foragers’ heads, and T. spinipes, colonies benefit when defended resources and avoiding fresh odor marks deposited on filter individual eavesdroppers match costly takeover attempts. paper strips by nearby T. spinipes responses to perceived access costs Stingless bees are important colonies. Trigona hyalinata foragers (Figure S2C–E). Live T. hyalinata and tropical pollinators that live in diverse exhibited a similar non-linear M. rufiventris foragers show clear communities with high competition eavesdropping response to labial preferences for or against odor- for floral resources. Many deposit gland extract and to fresh odor marked feeders, but T. spinipes species-specific pheromones around marks (Figure 1B,C). The bees were foragers do not (Figure 1B,C). rich, persistent resources to recruit highly attracted to a low number Attraction to heterospecific odor nestmates [5]. Foragers deposit of marks (0.075 bee equivalents, marks is beneficial when takeover odor marks (pheromone droplets) 4 marks), indicating they recognize occurs within about one hour of with approximately equal intensity competitors’ pheromones as signals resource detection by a T. hyalinata at all food sources deemed worth of high-quality food sources. eavesdropper, and is never good recruiting to [6]. Many of these Attraction to few odor marks for a M. rufiventris eavesdropper. marking species intensely defend persisted for the full 15 minutes of a Model results further showed resources [7]. Thus, eavesdroppers trial despite pheromone volatilization that T. spinipes colony fitness is may have to fight for the advertised (Supplemental information). the same for all eavesdropping resource, recruiting nestmates and However, the bees strongly avoided decisions (Supplemental increasing the colony’s energetic a larger number of odor marks that information). However, T. hyalinata expenditure. Our focal Trigona correspond to significant fight effort and M. rufiventris incur significant species produce chemically distinct (0.1 and 0.2 bee equivalents, 9 costs from sub-optimal decisions recruitment pheromones in labial marks). Bees may not detect very (Figure 1E). Thus, strong energetic Magazine R599 A B C D E Bees ) 0 A 0 A/D ) Model results Recent odor marks that elicit approach 0.05 A 2 A/D Recent odor marks 60 that elicit avoidance 0.075 approach B 4 B hyalinata T. 69 min 0.1 avoid C 9 C/D 40 0.2 avoid C This study 20 0.1 0 Heterospecific pheromone Heterospecific pheromone concentration (# odor marks Cumulative count spinipes concentration (bee equivalents T. 0 0 min Many 0 avoid 0510 15 20 25 30 35 Time interval (min) M. rufiventris 0 0.5 1 0 0.5101014 Empirical preference/attraction probability Optimal Cost of sub- approach optimal decisions probability (hrs search effort) Current Biology Figure 1. Empirical and modeled stingless bee recruitment and eavesdropping behavior. Empirical data show attraction (light gray dots, bars and lines) or avoidance (black), and the corresponding number of marks eliciting each response. (A) Average buildup of T. spinipes odor marks and recruits over time. (B,C) Trigona hyalinata eavesdropping responses depend on the quantity of T. spinipes pheromone encountered (B: LG extract; C: fresh odor marks; ANOVA including both pheromone sources: F7,80 = 40.89, p < 0.0001). A bee equivalent is the total contents of labial glands from one bee. Bars show mean ± SEM proportion of bees in a trial that preferred the pheromone. Letters indicate statistically different groups. The box encloses data collected in this study. (D) Calculated fight efforts (times) at which the model predicts eavesdroppers will switch from attraction to avoidance. These values cannot be computed when the eavesdropper does not detect the recruitment pheromone (0, 0.05 bee equivalents), or when the relative cost of sub-optimal deci- sions is zero. (E) Modeled energetic benefit to the colony when the eavesdropper makes a fitness-maximizing decision relative to sub-opti- mal decisions, standardized to hours of search effort. constraints can select for Supplemental Information In Food Exploitation by Social Insects: Supplemental Information including exper- Ecological, Behavioral, and Theoretical eavesdroppers that assess the Approaches Contemporary Topics in accessibility of advertised resource, imental procedures and two figures can be Entomology., S. Jarau and M. Hrncir, eds. but not all species are subject to found with this article online at http://dx.doi. (Boca Raton, FL: CRC Press), pp. 223–249. org/10.1016/j.cub.2014.05.062. 6. Schmidt, V.M., Zucchi, R., and Barth, F.G. these constraints. (2006). Recruitment in a scent trail laying The current paradigm suggests stingless bee (Scaptotrigona aff. depilis): changes with reduction but not with increase that signalers should use less Acknowledgements V. Imperatriz-Fonseca, S. Mateus and of the energy gain. Apidologie 37, 487–500. conspicuous communication to 7. Lichtenberg, E. M., Imperatriz-Fonseca, V. R. Zucchi provided lab space and equipment; avoid eavesdropping [2,3]. However, L., and Nieh, J.C. (2010). Behavioral suites M.A. Eckles shared previously unpublished mediate group-level foraging dynamics in we show that there is not always a data; A. Forde, D.A. Holway, C. Johnston, communities of tropical stingless bees. conflict between optimizing a signal Insectes Sociaux 57, 105–113. P. Nonacs, K.A. Paczolt, G.S. Wilkinson and 8. Nieh, J.C., Barreto, L.S., Contrera, F.A.L., and to escape from eavesdropping and E.E. Wilson gave feedback. A NSF Doctoral Imperatriz-Fonseca, V.L. (2004). Olfactory to benefit the intended