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1988

Do Brood Exist?

Laurence Morel USDA-ARS

Robert K. Vander Meer USDA-ARS

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Morel, Laurence and Vander Meer, Robert K., "Do Ant Brood Pheromones Exist?" (1988). Entomology Papers from Other Sources. 54. https://digitalcommons.unl.edu/entomologyother/54

This Article is brought to you for free and open access by the Entomology Collections, Miscellaneous at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Entomology Papers from Other Sources by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. FORUM

Do Ant Brood Pheromones Exist?

LAURENCE MOREL AND ROBERT K. V ANDER MEER

Insects Affecting Man and Animals Laboratory, USDA-ARS, Gainesville, Florida 32604

FORUM: Ann. Entomol. Soc. Am. 81(5): 705-710 (1988) ABSTRACT A brood is a chemical or mixture of chemicals released by im­ mature stages that elicits a behavioral response in conspecific adults. The current literature devoted to brood pheromones in several ant does not prove the existence of such a pheromone or even of brood-specific chemicals. The possibility of a food response or a nestmate recognition response, two of the most confounding factors, has not been eliminated. Two alternative hypotheses involving brood behavior, morphology, cuticular chemicals, and associative learning are proposed.

KEY WORDS Insecta, ant, brood, pheromones

THE DIFFERENTIAL TREATMENT received by brood Attraction: Suggests that brood releases a vola­ ~immature stages) in (Le Masne 1953), and tile pheromone that attracts adults. experimental evidence that workers of Neivamyr­ Aggregation: Involves clustering of ants on or mex opacithorax (Emery) show an aggregation re­ around a substance secreted by brood that elicits sponse to larval secretions (Watkins & Cole 1966), settling behavior in workers. led to the hypothesis that ant brood produces pher­ Brood-Tending: An all-encompassing term for omones that elicit specific adult behaviors. From several adult behaviors toward brood, which in­ the early 1970s to the present, several studies have clude feeding, grooming, and (under disrupted col­ attempted to document the existence of brood ony conditions) retrieval back to the nest. The only pheromones; most effort has been directed toward tending behavior used in brood pheromone bioas­ the fire ant, Solenopsis invicta Buren (Vander Meer says to date has been retrieval to the nest. Brood 1983). recognition is prerequisite to these worker re­ Several problems arise in demonstrating conclu­ sponses. sively that brood does produce pheromones. Most important are the species-specificity of a phero­ Problems in Demonstrating mone, the adequacy of bioassays, the existence of Brood Pheromones reliable controls (which include food and nestmate recognition controls), the quantity of material used Species-Specificity. The term "pheromone" is to obtain a positive response, and chemical tech­ defined as a substance released by an organism to niques. Here we review how these different prob­ the outside that causes a specific behavioral or phys­ lems have been addressed in the current literature iological reaction in a receiving organism of the and whether or not they have been solved. We same species (Nordlund & Lewis 1976). The spec­ then review the experimental support for the in­ ificity of pheromones contributes to the isolation volvement of nonchemical cues in the differential of sympatric species (Roelofs 1981). There are also treatment of ant brood and propose some alter­ examples of species with common pheromone com­ native hypotheses. ponents; however, it is not clear that the total blend of chemicals used by a species to attain the full behavioral repertoire is matched by any other Brood Pheromone Classifications species. In particular, it is unlikely that pheromones Brood pheromones can be classified in several responsible for the full range of ant worker be­ categories according to the behavioral reactions they haviors associated with rearing brood would be elicit. identical among several species. The chemical iso­ Brood Recognition: Suggests that the surface lation and identification of pheromone components chemistry of brood is recognized by adult ants as are limited by the bioassay, which usually breaks being different from that of adults. At a more re­ down a complex sequence of behaviors into a single fined level, each immature developmental stage measurable response. This limitation was illustrat­ may produce a specific pheromone that is distin­ ed by studies on trail pheromones in two species guished by adult workers, leading to segregation of fire ants. A trail-following (i.e., orientation) of immature stages in the nest (see Le Masne 1953). bioassay demonstrated the lack of species-specific- 706 FORUM: ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 81, no. 5

ity in So[enopsis richteri Forel and S. invicta (Bar­ & Dickens (1988) subsequently used this type of lin et al. 1976). However, subsequent research olfactometer to bioassay volatiles from larvae. They showed that species-specificity was achieved dur­ found that at least 30 live immatures were required ing recruitment, another element of the trail pher­ to elicit a significant response. LaMon & Topoff omone behavioral hierarchy (Vander Meer 1986, (1985) studied the involvement of pheromones in Vander Meer et al. 1988). social facilitation of eclosion in S. invicta. Workers The problem of species-specificity has not been are attracted to eclosing pupae and then avidly addressed in brood pheromone studies, although strip away the pupal . However, LaMon & Brian (1975) suggested a chemical is released by Topoff's bioassays measure only aggregation and queen-biased larvae of M yrmica rubra L. that elic­ retrieval, which appear to be inappropriate to its a worker response (, leading to the quantify attraction. A more appropriate bioassay loss of queen potentiality); this effect was trans­ may be to apply rinses of eclosing pupae to non­ specific between M. rubra and M. scabrinodis Ny­ eclosing pupae and monitor worker behavior. lander. The conceptual problem of the species­ Reliability of Controls. In each study, the reli­ specificity of brood pheromones is important, ability of controls used to differentiate food or nest­ because interspecific adoption of brood is widely mate recognition responses from brood pheromone reported (see Jaisson 1971). In addition, the dem­ responses is questionable. Several investigators have onstration of brood pheromone species-specificity attempted to deal with the food response problem would help to eliminate the confounding food re­ by requiring (for a positive result) that brood-treat­ sponse factor. ed particles be deposited in a brood chamber, or Adequacy of Bioassays. The adequacy of a comparing response to the test sample with that to bioassay to test an hypothesis becomes acute when food controls. However, with the first method, the test objects are not live animals. A widely used workers feed the larvae and therefore must bring bioassay consists of retrieval of inert objects treated food into the brood chamber. The type of food with brood extracts (Glancey et al. 1970, Robinson used as a control also presents problems. For ex­ & Cherrett 1974, Walsh & Tschinkel1974, Bigley ample, the food value of a soybean oil control & Vinson 1975, Brian 1975, LaMon & Topoff 1985, (Glancey et al. 1970, Bigley & Vinson 1975) is not Glancey & Dickens 1988). However, this bioassay similar to the food value of extracted brood. Ex­ can be confounded by food responses as discussed tracted brood contains a complex mixture of lipids, below. To overcome this problem, some experi­ proteins, carbohydrates, etc., whereas soybean oil menters (Walsh & Tschinkel 1974, Brian 1975, contains mostly triglycerides. The rinse LaMon & Topoff 1985) used a nest design that used as a food control by Glancey & Dickens (1988) incorporated a distinct brood chamber. Retrieval is not fully satisfactory either, because the weights of tested objects into the brood chamber was used of extracted material from and brood as the criterion for a brood-specific worker re­ were not matched, and the relative amounts of lipid sponse. However, because food must be brought to classes were not investigated in the two extracts. the larvae by workers, a food response cannot be Walsh & Tschinkel (1974) dampened out the food eliminated. response by overfeeding the colony with the food In some cases, bioassays designed to demonstrate used as a control. However, as demonstrated by the existence of attractant brood pheromones (Wat­ these authors, such dampening may only increase kins & Cole 1966, Glancey & Dickens 1988) ac­ the probability of workers responding to a novel tually measured aggregation. In these bioassays, the food source (i.e., brood extract). Ideally, one should cumulative number of ants was counted at various use a food control that consists of an equivalent times at a spot of test material. The difficulty with amount of extract, by weight, of a non-ant larval this kind of test is that during random searching, form not currently in the colony diet. worker ants could contact the spot and aggregate. Glancey & Dickens (1988) used an electroanten­ Therefore, it is not possible to associate attraction nogram (EAG) assay to test for a volatile compo­ with the test results. The only way to measure nent of the fire ant's brood pheromone. The mean attraction is via an olfactometer which, by defi­ EAG response to their control (hexanol, 100 /-Lg) nition, measures only the response to volatiles. Walsh was small (-0.38 m V), and the response to brood & Tschinkel (1974) used this technique to deter­ (100 larva-equivalent) was much smaller (-0.01 mine if fire ant brood produces a volatile attractant. m V). The authors argued that the low response to They allowed only one ant to make a choice before brood is significant because may have nu­ cleaning the apparatus, thus preventing subsequent merous receptors to hexanol (green volatile) workers from following the first ant's trail. Walsh but only a few highly specific brood pheromone & Tschinkel (1974) concluded that fire ant brood receptors. This is not a convincing argument, for does not produce a volatile pheromone. Vander Vander Meer (unpublished data) obtained a -0.5- Meer et al. (1988) designed a Y-tube olfactometer m V EAG response from fire ant workers to 0.2 that measured the initial choice of the first 20 ants. queen equivalents of the queen attractant phero­ Because fire ant trail-laying occurs on the return mone. For the EAG test of the brood volatile, it to the nest (Wilson 1962), it was assumed that trail would have been better to have used a solvent formation was not a complicating factor. Glancey control and to have tested a known fire ant pher- September 1988 MOREL & V ANDER MEER: ANT BROOD PHEROMONES 707

omone standard (e.g., queen attractant pheromone Glancey et al. 1970, Bigley & Vinson 1975, LaMon [Glancey 1986]) in sequence with unknowns. & Topoff 1985) is the lack of regarding None of the brood pheromone studies used work­ the brood equivalents of the extracts and amount er or sexual adult ants as controls, either intact or of the control substances used in bioassays. Without as extracts. Therefore, it is impossible to determine this information, it is impossible to determine if a if the behaviors elicited were general nestmate or pheromonal response is being tested. Glancey et al. species-specific responses obtainable from any col­ (1970) and Bigley & Vinson (1975) used extracts ony group. Walsh & Tschinkel (1974) used adult of crushed immatures; yet discrimination cues such male body contents as a colony response control; as a brood recognition pheromone are most likely however, this does not take into account that colony to be found on the cuticular surface rather than discrimination cues are probably located on· the within the body (Wilson 1971). Moreover, the use cuticle (Wilson 1971). Moreover, colony discrimi­ of whole-body extracts increases the food value of nation occurs principally among workers and may the test material, which may swamp out potential be applied in a different way, or not at all, to adult pheromonal responses. sexuals. Ant brood appears to be colony-specific to Chemical Techniques. Bigley & Vinson (1975) a certain extent in Lasius niger L. (Lenoir 1981) used inappropriate chemical techniques to mistak­ and in Cataglyphis cursor Fonscolombe (Lenoir enly identify triolein as the brood pheromone in 1984, Isingrini et al. 1985). Although initially there S. invicta (see Vander Meer [1983] and Vander is a differential treatment of alien brood, intercol­ Meer & Morel [1988] for details). ony adoption in these two species has always been successful. In S. invicta, no significant differences have been found between the worker response to Evidence for Involvement of nestmates and to alien brood (Glancey & Dickens Nonchemical Signals in Specific 1988). Results may vary among species, but at this Behaviors Directed to Brood point we cannot eliminate colony recognition as an explanation of the results obtained in brood pher­ Morphology. Immature stages obviously differ omone bioassays. morphologically from adults. Also, differences exist Quantitation. The wealth of pheromone re­ between the various brood stages (egg, larva, pupa) search on ants and other has shown that and even between the successive larval stages, as pheromones are present in minute quantities rel­ reported for S. invicta (Petralia & Vinson 1979). ative to the individual's biomass. For example, each Morphological properties of third instars and phar­ fire ant queen has only about 10 ng of attractant ate pupae of M. rubra were investigated for pos­ pheromone (Glancey 1986), and the trail orienta­ sible recognition cues by Brian (1975). In this case, tion and recruitment pheromones occur at only 6 flaccidity and hairiness playa significant role in and 0.075 ng per worker, respectively (Vander Meer eliciting retrieval to the brood chamber. Robinson et al. 1981, Vander Meer et al. 1988). Behavioral & Cherrett (1974) concluded that the diminished responses to these fire ant pheromones are obtained retrieval of freeze-killed Atta cephalotes L. larvae with one or fewer body-equivalents. Consequently, was caused by a deterioration of their physical serious questions arise when investigations of a brood properties. pheromone require w hole-bod y extracts or a large Behavior. Brood behavior is very different from number of brood or both to elicit worker responses adult behavior; however, it has not been investi­ (Glancey et al. 1970, Bigley & Vinson 1975, Glan­ gated as a possible cue inducing brood-directed cey & Dickens 1988). The last-named authors behavior. The most obvious larval behavior is the showed that 500 larva equivalents were required exchange of liquids with workers (); this for a positive worker response in a "spot" bioassay exchange is bidirectional and both individuals ben­ (aggregation), and 300 living larvae were required efit (Wilson 1971). Although pupae lack noticeable for a positive response in an olfactometer. The need behavior, investigators can recognize eclosing pu­ for so many immatures suggests that the results of pae by their gross uncoordinated movements (e.g., the rinse may be a response to food or contami­ LaMon & Topoff 1985). Worker ants may respond nation from pheromone released by nest mates (e.g., to eclosing pupae using these cues. trail and queen pheromopes). The olfactometer re­ sults could be caused by the asymmetry of the air Alternative Hypotheses streams created by the respiratory products of the large amount of brood used in the experiment. Adult ants distinguish brood from adults and These results represent an effect of the group (which different brood stages from each other. Some stud­ may, in fact, be real in a colony situation where ies suggest that chemical signals mediate these dis­ immature stages are concentrated). However, in tinct behaviors; e.g., loss of activity following sol­ retrieval experiments, workers do respond to in­ vent rinses (Robinson & Cherrett 1974, Brian 1975). dividualliving immatures (i.e., in a disrupted col­ However, none of the studies we reviewed dem­ ony). onstrated the unambiguous existence of a brood One of the most frustrating inadequacies in many pheromone in the strictest . If brood phero­ brood pheromone papers (Watkins & Cole 1966, mones do exist, technical difficulties in the devel- 708 FORUM: ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 81, no. 5 opment of bioassays or chemical methodologies so fication of any of the factors may affect the be­ far have precluded their clear demonstration. havior of workers toward brood. However, in our opinion, the current literature more The second hypothesis is an expansion of the first strongly supports the possibility that brood pher­ based on associative learning of a characteristic omones do not exist in ants. (morphological, behavioral, or chemical) of brood From the literature about adult/brood interac­ and a "reward" obtained by adult workers from tions in ants, we can conclude that an "I am brood" brood. Learning in ants and other social insects has signal is not located on a specific part of the body been known for a long time (Alloway 1972, Menzel of the immature form (Walsh & Tschinkel 1974, 1985). The concept of rewards moderating ant Brian 1975); body morphology can be a cue used behavior is well documented in studies on ants by adults to distinguish brood from adults (Rob­ tending (Way 1963), larvae inson & Cherrett 1974, Brian 1975); interspecific (Cottrell 1984, Maschwitz et al. 1986) and in troph­ adoptions of brood between related species have allactic appeasement among ants (Kloft 1983). If been known for a long time (see Jaisson 1971) chemicals alone were used as the identifying char­ and workers in the host colony display typical brood­ acter, they would have to be specific to the brood. tending behaviors toward the adoptees; and that The worker reward for tending brood may be re­ interspecific adoptions are also successful with new­ lated to the observed ingestion of oral secretions ly eclosed (callow) workers (see Jaisson 1971). and excretory products from larvae (see Le Masne It is possible, then, that adult behavior toward 1953). These products may have nutritive value for brood can be moderated by a combination of mor­ recipient workers (Wilson 1971). Queens of mature phological, behavioral, and cuticular chemical fac­ colonies of the primitive ant Amhlyopone silvestrii tors. We propose two alternative hypotheses that Wheeler feed entirely on the hemolymph of their involve these factors to explain the differential own larvae in nondestructive cannibalism (Masuko treatment of brood by adult ants. 1986). In addition, fourth-instar regurgitates of S. Under the first hypothesis, we define the brood invicta play an important role in colony nutrition cuticular chemicals involved in worker-brood in­ and, in particular, queen egg production (Tschin­ teractions as nestmate recognition cues. These cues kel in press). This learning hypothesis can account can be derived from any source-the individual directly for the behavior of workers toward larvae itself, nest mates, or the environment. In addition, and possibly eclosing pupae. Although eggs and these cues elicit different behaviors (acceptance or pupae do not offer workers a reward, the benefits rejection) in individuals of the same species under of the associative learning could be extended to all the same experimental conditions. For these rea­ stages. sons, they should not be considered pheromones The combination of multiple signals in brood (Vander Meer 1988). The cues, whatever their recognition has been demonstrated in honey source, are transferred between workers (Errard & and Vespa wasps. Although chemical signals from Jallon 1987; Vander Meer & Carlin, unpublished the brood have been found, mechanical and mor­ data) and are probably also transferred to brood. phological cues are also necessary to induce tending As shown in two species, Lasius niger L. (Lenoir in these social insects (Free & Winder 1983, Koe­ 1981) and C. cursor (Lenoir 1984, Isingrini et al. niger 1984). Invoking multiple factors in ant brood­ 1985), there is colony-brood recognition. However, worker interactions, based on either of the above colony discrimination of alien brood lasts only a hypotheses, offers an interesting explanation for the short time, and foreign brood is soon fully adopted. successful adoption of brood into alien colonies. These data suggest that time is required for the Aggressive behavior between two workers of two brood to acquire the host colony's (nestmate colonies of the same species, or two different species, recognition cues). Initially, alien brood of these two involves recognition and a hierarchy of agonistic species receive quantitatively less care than nest­ beha viors in both partners. Because brood lack the mate brood. Therefore, nestmate recognition cues ability for agonistic display, it would be predicted may be involved in quantitative differences in the that aggressive behavior toward them would be specific treatment of brood, whereas other cues moderated even if their nestmate recognition label (morphology and behavior) may be responsible for did not match that of the receiving colony (see the specific treatment itself. The combination of Breed & Bennett [1987] for a review of nestmate chemical recognition with morphological or be­ recognition). Once inside the foreign colony, the havioral cues or both could in fact be sufficient to successful adoptee can begin to acquire a new col­ account for the full differential treatment of brood ony odor through social interactions. This situation by adult ants. Brood-derived nest mate recognition may be analogous to the passive integration mech­ cues could account for all results obtained with anism used by a myrmecophilous (Vander bioassays in which brood rinses or extracts are tested Meer & Wojcik 1982). The limitation of interspe­ as baits (although results with brood extracts are cific adoption of brood to closely related species most likely food responses). The contribution of (Jaisson 1971) indicates that species differences in each factor (morphology, behavior, nestmate rec­ one or some combination of the three factors (most ognition cues) may vary from species to species. As likely morphology or cuticular chemistry or both) shown in the brood pheromone literature, modi- negatively influences interspecific brood-worker September 1988 MOREL & V ANDER MEER: ANT BROOD PHEROMONES 709 interactions. Similarly, the acceptance of callow ology, biochemistry and pharmacology, vol. 9. Per­ workers in alien colonies may be attributed to their gamon, Oxford. reduced behavioral repertoire and lack of acquired Kloft, W. J. 1983. Interspecific trophallactic relations nestmate recognition cues, as cited by Jaisson (1985). between ants of different species, genera and subfam­ ilies-an important strategy in population ecology. The hypotheses presented here are testable and Ann. Entomol. 1: 85-86. require supporting experimental evidence. We hope Koeniger, N. 1984. Brood care and recognition of this critical review of brood pheromone literature pupae in the honeybee (A pis mellifera) and the hor­ and the alternative propositions stimulate interest net (Vespa crabro), pp. 267-283. In T. Lewis [ed.), and research in this extremely complicated but communication. Academic, London. fascinating area. LaMon, B. & H. Topoff. 1985. Social facilitation of eclosion in the fire ant, Solenopsis invicta. Dev. Psy­ chobiol. 18: 367-374. Acknowledgment Le Masne, G. 1953. 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