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Effects of Protein-Constrained Brood Food on Honey Bee (Apis Mellifera L.) Pollen Foraging and Colony Growth

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Effects of Protein-Constrained Brood Food on Honey Bee (Apis Mellifera L.) Pollen Foraging and Colony Growth Behav Ecol Sociobiol (2007) 61:1471–1478 DOI 10.1007/s00265-007-0379-1 ORIGINAL PAPER Effects of protein-constrained brood food on honey bee (Apis mellifera L.) pollen foraging and colony growth Ramesh R. Sagili & Tanya Pankiw Received: 28 July 2006 /Revised: 14 February 2007 /Accepted: 18 February 2007 /Published online: 6 March 2007 # Springer-Verlag 2007 Abstract Pollen is the sole source of protein for honey Introduction bees, most importantly used to rear young. Honey bees are adept at regulating pollen stores in the colonies based For the nonreproducing worker caste of social insect on the needs of the colony. Mechanisms for regulation of colonies, colony growth and reproduction are the principal pollen foraging in honey bee are complex and remain sources of fitness. Honey bee colonies reproduce through a controversial. In this study, we used a novel approach to process of colony budding, commonly referred to as swarm- test the two competing hypothesis of pollen foraging ing (Winston 1987). In general, a larger adult population regulation. We manipulated nurse bee biosynthesis of results in increased probabilities for colonies to reproduce brood food using a protease inhibitor that interferes with and for swarms to survive; fitness traits (Cole 1984; Lee and midgut protein digestion, significantly decreasing the Winston 1987; Little 1979; Michener 1964; Pomeroy 1979; amount of protein extractable from hypopharyngeal Richards and Richards 1951; Seeley 1985a,b; Seeley and glands. Experimental colonies were given equal amounts Visscher 1985; Winston 1987). The mechanism for colony of protease inhibitor-treated and untreated pollen. Colo- growth is increased brood rearing. The honey bee (Apis nies receiving protease inhibitor treatment had signifi- mellifera L.), like most social insects, have a division of cantly lower hypopharyngeal gland protein content than labor whereby individuals perform different tasks as they controls. There was no significant difference in the ratio age. Brood rearing labor is divided among nurse bees and of pollen to nonpollen foragers between the treatments. foragers. Ordinarily, younger nurse bees work within the Pollen load weights were also not significantly different nest directly tending larvae. Older bees are more probably between treatments. Our results supported the pollen found foraging for nectar or pollen outside the nest. Nurse foraging effort predictions generated from the direct bees consume forager-collected pollen to biosynthesize a independent effects of pollen on the regulation of pollen proteinacious hypopharyngeal gland secretion called brood foraging and did not support the prediction that nurse food that is progressively provisioned to larvae. Pollen is the bees regulate pollen foraging through amount of hypo- only source of protein available to bees and it is through pharyngeal gland protein biosynthesis. nurse bees that larvae are the principal consumers of protein in a colony. Pollen foragers collect pollen from flowers, Keywords Honey bee . Pollen foraging . Protease inhibitor . carry it back to the colony on the outside of the body packed Brood food . Hypopharyngeal glands onto special structures of their hind legs called corbiculae, and directly deposit their loads into wax cells usually situated around brood rearing areas of the nest (Camazine Communicated by R.F.A. Moritz 1991). The allocation of the foraging force profoundly affects colony growth and development (Farrar 1944; * : R. R. Sagili ( ) T. Pankiw Moeller 1958, 1961; Free and Racey 1968; Nelson and Jay Department of Entomology, Texas A&M University, College Station, TX 77843-2475, USA 1972; Smirl and Jay 1972; Pankiw et al. 2004). As such, the e-mail: [email protected] mechanisms that regulate the allocation of the pollen 1472 Behav Ecol Sociobiol (2007) 61:1471–1478 foraging force are integral to an understanding of colony predict the same pollen foraging outcomes. But for the fitness. different mechanistic reasons, both hypotheses predict Two hypothetical mechanisms dominate studies of pollen pollen foraging decreases with additional quantities of foraging regulation. The first is an “information center” stored pollen and pollen foraging increases with additional model and subsequent modifications (Seeley 1985a,b, amounts of brood. Given a fixed amount of available 1995; Seeley et al. 1991) named in this study as the brood comb area, there is an interaction between amount of food hypothesis. The second is a “stimulus–response stored pollen, number of larvae, and empty space. threshold model”, referred to in this study as the direct Changing one necessarily changes the others. However, independent effects of stored pollen and brood (Page and manipulating amount of brood pheromone allows for a Mitchell 1998; Page and Erber 2002;Scheineretal.2004). change in the perceived number of larvae without The brood food hypothesis predicts that brood and changing the allocation of comb area for larvae, pollen, stored pollen indirectly affect the behavior of pollen and empty storage space (Pankiw et al. 1998;Pankiw foragers through a single inhibitory signal (Camazine 2004a–c;LeConteetal.2001; Pankiw and Rubink 2002). 1993;Seeley1995). Bees are activated to collect pollen, With brood pheromone added to colonies, the brood food thus regulation occurs through inhibition. With excess hypothesis predicts no change in pollen foraging due to no pollen stored in a colony there is also an excess of change in demand for brood food. The direct independent inhibitor that is presumably distributed to foragers by effect of amount of brood and pollen hypothesis predicts trophallaxis with nurse bees. If pollen is in surplus, it is an increase in amount of pollen foraging as a consequence hypothesized that nurse bees transfer more protein to of the increased pollen foraging stimulus of brood foragers and inhibit pollen foraging. Brood food is the pheromone. Colonies treated with supplemental amounts most likely inhibitor, thus the brood food hypothesis for of brood pheromone foraged more for pollen than did the regulation of pollen foraging. Some information center control colonies containing the same amount of brood and based studies have focused on trophallaxis as mechanism stored pollen (Pankiw et al. 1998, 2004;Pankiwand for the transmission of information that may regulate Rubink 2002; Schulz and Robinson 2002;Pankiw2004a–c). pollen foraging (Camazine et al. 1998; Weidenmüller and Results of these studies support the direct, independent Tautz 2002). effects hypothesis, such that colonies approximated amount A competing hypothesis is that stored pollen and brood of larvae from their chemicals and foraged for pollen have direct, independent effects on pollen foraging. Many accordingly. studies have demonstrated the effects of quantities of Direct experimental evidence of brood food protein as a brood and stored pollen. Increasing the amount of larvae in feedback mechanism inhibiting pollen foraging has yet to colonies, or the chemical cues derived from larvae called be demonstrated. In this study, we manipulated nurse bee brood pheromone, increases the number of pollen foragers biosynthesis of brood food using a protease inhibitor that and pollen load weights returned (Filmer 1932; Al-Tikrity interferes with midgut protein digestion in adults, signifi- et al. 1972;Free1979; Eckert et al. 1994;Pankiwetal. cantly decreasing the amount of protein extractable from 1998, 2004; Fewell and Bertram 1999;PankiwandPage hypopharyngeal glands (Sagili et al. 2005). Manipulating 2001; Pankiw and Rubink 2002; Pankiw 2004a–c.Pollen the amount of hypopharyngeal gland protein and control- foraging activity level decreases in response to the ling for amount of stored pollen resulted in the following addition of stored pollen (Free 1967;Barker1971; Moeller predictions tested here: (1) the direct, independent effects 1972; Danka et al. 1987; Fewell and Winston 1992; hypothesis predicts no difference in pollen foraging effort Camazine 1993;FewellandBertram1999) and increases because amount of stored pollen is the same in treated and in response to the removal of stored pollen (Free 1967; control colonies vs (2) the brood food hypothesis predicts Fewell and Winston 1992; Camazine 1993). Increasing the that protease inhibited colonies should allocate a greater amount of stored pollen in colonies concurrently increases pollen foraging effort due to a decreased amount of nurse brood rearing and decreases pollen foraging activity to a produced protein. The primary objective in this experiment homeostatic set point (Fewell and Winston 1992). Empty was to measure the effects of manipulating hypopharyngeal comb space near the brood also stimulates pollen foraging gland protein (brood food) content in nurse bees on pollen behavior, while stored pollen clearly inhibits. Dreller et al. foraging. (1999) demonstrated that pollen foraging decreases only when foragers have direct access to stored pollen, and direct access to brood is necessary for an increase in pollen Materials and methods foraging response to an increase in amount of brood. Using conventional colony-level manipulations is prob- This experiment was replicated four times and had two lematic because both the direct and indirect hypotheses treatments, 1% SBTI (soybean trypsin inhibitor) (Sigma- Behav Ecol Sociobiol (2007) 61:1471–1478 1473 Aldrich product T-9003, St. Louis, MO, USA) and control. further analyzed using analysis of variance (ANOVA) Micronucleus hives made of styrofoam (25×19×14
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