Use of Chemosensors in Foraging Animals

Ella Gadoury, Emma Lee, Floriane Baudin, Tian Rui Wang

Abstract

All animals must search for and collect the substances they consume in order to survive. However, this foraging process is not as simple as it may seem, and this leads these various animals towards strategies which can maximize the efficiency of this essential task. Being that animals reside within chemically complex environments, they must navigate these conditions in such a way that can maintain their survival. This essay examines animals’ power to steer themselves through complex chemical environments and the repeated assistance of their sensory driven strategies to do so. Indeed, the chemical environment is used as a mode of communication; bees use chemical information as alerting signals of neighbouring food sources, roundworms create complex chemical vocabulary made up of amino acids and carbohydrates molecules, and termites using sophisticated chemical messages to communicate. Additionally, it can also be studied as a medium that needs to be navigated; phytophagous insects make selective foraging choices using their highly selective olfactory receptors, similarly to parasitoids that locate their hosts and food source through volatile mosaics composed of various chemicals, while ants operate their environment using two decision making systems for foraging, as well as fruit bats using olfaction to locate and quality check their food source. Lastly, reptiles use tongue-flicking to sample chemicals in the external environment. All in all, this paper concludes that chemoreception improves animals’ capacity to acquire their food and thus the fittest sensing organs establish whether an animal survives and reproduces, as natural selection goes.

Introduction

Animals live in a dynamic environment characterized by chemical complexity. In order to live and feed, animals have developed a variety of effective detection mechanisms in a way that makes foraging activities sustainable. Animals use sensory modalities such as olfaction, vision and taste to locate distant food sources, but also to communicate important information among individuals within the same species. In other words, chemical cues act as important messengers that mediate the interaction between the autotroph (food source) and the heterotroph (forager), but also that among individuals in the same group during group foraging. The chemical cues can be separated into different categories depending on its function. For instance, pheromones are chemicals that affect behavioural responses of the members within the same species (Wyatt, 2017). Kairomone, on the other hand, is a broader term designating chemicals that are emitted by an individual in a species but received by another species, in a way that greatly benefits the receiver (Klowden, 2013). The recognition of these chemical cues, despite its diversity in structure, is a task that requires an extensive repertoire of corresponding receptors. This essay examines a variety of animal species including reptiles, phytophagous insects and its parasitoids, bees, ants, roundworms, termite, as well as fruit bats. The focus of the essay is the interaction of these species with their chemically heterogeneous environment, more specifically the traffic of nutrients through chemoreception.

Tongue-Flicking Behaviour

Olfactory and vomeronasal systems enable reptiles to receive chemosensory information from the environment. The chemosensory information, in this case odorant chemical cues, enter the olfactory system through the olfactory epithelium that is located posterior to the nasal cavity. Vomeronasal epithelium, on the other hand, lies within the vomeronasal organ, which is located at the base of the nasal septum (Martinez-Marcos et al., 2002). Hence, unlike the olfactory system, the vomeronasal system requires a mechanism to deliver odorant molecules to the epithelia.

Tongue-flicking is a foraging tactic used by many reptiles such as lizards and snakes, to gather chemicals for the detection of food sources. Tongue-flicking consists of ingesting surrounding particles into the vomeronasal organ using the tongue. Volatile molecules in the external environment adhere to the tongue’s moist surface, and reach the vomeronasal epithelium where vomerolfactory receptor cells are located (Cooper & Alberts, 1991) (Figure 1).

Studies involving species of lizards have shown that in most cases, the species that are classified as active foragers heavily rely on tongue-flicking to detect food by chemosensory means, as opposed to the ambush foragers that are called ‘sit-and-wait’ foragers (Regal, 1978). The latter statement implies that the species of lizards that search for food sources that are hidden or distributed unevenly require ingestion of particles through tongue-flicking, compared to the ambush foragers that rely relatively more on visual cues to detect food (Cooper & Alberts, 1991).

Host Odor Recognition by Phytophagous Insects

Phytophagous insects are foragers whose host detection mechanism requires a sophisticated manipulation of host-produced volatile chemical cues called kairomones (Bruce et al., 2005). Among 1700 different plant volatile compounds that are produced by diverse plant species, many belong to the groups of terpenoids, phenylpropanoids or benzenoids, fatty acid derivatives, and amino acid derivatives (Beyaert & Hilker, 2013). These chemical compounds form different odour plumes, which is the blend of volatile compounds dispersed by the wind. Insects are therefore constantly exposed to a chemically heterogeneous environment, and their foraging activities involve the tedious task of tracking the relevant, resource-indicating odour plumes.

Plant host location by the phytophagous insects involves the integration of sensory inputs, perceived mostly by the olfactory receptor neurons located on the insect antennae (Hansson, 2002) (Figure 2). Insect antennae are important anatomical structures that convert chemical signals into electrical signals, which are subsequently analyzed in the insect’s central nervous system (CNS). The selectivity of the receptors depends largely on the reaction group the olfactory receptor cells belong to. In fact, the olfactory receptors are divided into two distinct reaction groups depending on their reactivity to the chemical cues: 1) the group that responds to one class of chemicals and 2) the group that responds to different odor components (Visser, 1986). The existence of different degrees of specialization of the peripheral receptor cells can be explained by the fact that different types of membrane receptors, each providing a binding site to a limited number of chemical compounds, are present within the same cell (Mustaparta, 1990).

The electrophysiological studies of various species of phytophagous insects have shown that the peripheral receptors of most phytophagous insects detect a complex mixture of ubiquitous compounds produced by a variety of plants in their habitat (Bruce et al., 2005). Phytophagous insects must therefore utilize ratios and blends of kairomones to identify and locate the correct host plant to feed on. Consequently, altered ratios of kairomones can significantly affect phytophagous insects’ foraging decisions. Plant odors are assessed by an array of olfactory receptor cells that, as mentioned previously, elicit different levels of responses depending on the encountered chemical component. Upon stimulation, these neurons increase or decrease the frequency of nerve impulses accordingly, hence varying the degrees of excitation and inhibition in response to a wide range of kairomones. The net effect of the nerve impulses determines the individual’s foraging decision by eliciting corresponding behavioural responses.

Inputs to the CNS originating from different chemical compounds are distinct from each other. Hence, behavioural responses to the kairomones, be it host attraction or non-host avoidance, depend largely on how the peripheral inputs are processed within the CNS (Bruce et al., 2005). Electrophysiological responses recorded by the antennae and the resulting behavioural responses are correlated in a way that allows phytophagous insects to forage optimally by maximizing nutrient intake.

Parasitoids of Phytophagous Insects

As previously discussed for phytophagous insects, volatiles are central elements of vegetation. Parasitoids are parasites that spend their larval stage living inside a host, once more mature, they then destroy them to live freely and navigate vegetation in order to find other hosts (Vinson, 1976). Surely, host selection is not a random process. In fact, parasitoids must locate their host, hence chemical and physical parameters guide them towards host habitats (Vinson, 1976). To in turn survive, parasitoids somewhat regulate the survival of their host. In order to locate the plants their hosts consume, parasitoids of phytophagous insects use the food plants’ emitted volatiles to distinguish them (Wäschke et al., 2013). More specifically, parasitoids make use of HIPVs, herbivore-induced plant volatiles (Aartsma et al., 2017). In fact, intake plants emit a very minor quantity of volatiles, it is upon plant consumption by the host that their food releases a volatile blend of different chemical classes, all synthesized through biosynthetic pathways (Aartsma et al., 2017). HIPVs are emitted in areas where there are diverse plant species, hence this heterogeneous distribution makes for a complex medley of volatile blends composed of various chemicals seen in Figure 3 (Aartsma et al., 2017).

Once again, these volatiles are produced by the consumed plants, making the assortment depend on herbivore species, density and herbivore development (Aartsma et al., 2017). Furthermore, emitted volatiles are transported over large environments and can simultaneously break down, posing a challenge for parasitoids to distinguish between different odor sources on larger spatial scales. Indeed, volatile compounds progressively decay when interacting with reactive chemicals found in the atmosphere, for instance, ozone (Aartsma et al., 2017). Therefore, this degradation can modify odors by changing the ratio of chemical compounds or even producing new breakdown products, thus hindering the parasitoids’ food source detection. Consequently, parasitoids maneuver these chemical complexities in one of three ways: ignoring, avoiding, or preferring them. They will choose to ignore by utilizing their other important senses when volatile mixtures become too distracting, they will avoid when the chemical complexities hinder their ability to detect their hosts, and lastly, they prefer these environments in the presence of flowers, seeing as flowers come to produce the most complex volatiles while also providing nectar (Wäschke et al., 2013). In sum, chemical cues highly support parasitoids in their foraging strategies and help them navigate chemical environments in order to better their host selection.

Chemical Communication by Pheromones of Bees

Bees forage by using their sense of smell and return to floral odours that can be associated with high-quality food rewards. Foraging bees communicate with other bees in the hive about food sources by exchanging chemical and locational information. Indeed, bees generate foraging alerts, in order to mobilise as many bees as possible, with pheromones such as eucalyptol (Granero et al., 2005). Pheromones can be defined as chemical stimuli evoking a stereotypical response in members of the same species (Orlova & Amsalem, 2021).

Bumblebee (Bombus terrestris) foragers, upon returning to their hives, are able to alert their nestmates to the presence of food sources thanks to the distribution of a pheromone. Bumblebees returning to the nest from a successful foraging mission release a pheromone by running excitedly around the nest which encourages their nestmates to go out and find food (Molet et al., 2009). In fact, bumble bees possess a pheromone-producing gland, named the tergal gland, which is located on their dorsal abdomen as discovered in experiments performed by Dornhaus et al. in 2003 (Figure 4).

The pheromones produced by the tergal gland include two monoterpenes and one sesquiterpene (eucalyptol, ocimene and farnesol) (Fig 5a). Among these sesquiterpene, one has a special effect on the bumblebees’ recruitment during foraging activities. Indeed, the experiment done by Granero in 2005 identified eucalyptol as the main active ingredient of the bumblebee foraging alert as they showed that this molecule can activate the entire foraging force of the colony, twice as fast as any other components (Fig 5b). 

Bumblebees are not the only ones to use pheromones as an alerting signal. Honeybees (Apis mellifera) also distribute pheromone produced by the Nasanov gland (Dornhaus et al., 2003). Similar to bumblebees, the pheromone is used for alerting nestmates to the presence of rewarding food resources but also for attraction or recruitment. The distribution of pheromones is done during the waggle dance (consisting of excited runs with bouts of wing-fanning) or during trophallaxis (transfer of fluids among members of a community through mouth-to-mouth or anus-to-mouth feeding).

Other sources of chemical information, such as the floral volatiles, can alert bees in the hive about neighboring food sources. Indeed, the floral volatiles carried by the returning foraging bees on their body, mainly on the cuticles, can stimulate recruiting (Mas et al., 2019), but the mobilization effect remains lower than eucalyptol.

Chemical information such as pheromone or floral volatiles is key for bees to determine their foraging behaviour. The information provided by these chemicals support the colony to identify high-quality food sources and to avoid needless energy expenditure, as well as the exposure to risk.

Foraging Systems of Ants

Similar to bees, ants are living in very large communities and the search for food relies on communication and mutual aid between each member. In many cases, ants discover food sources that are much larger than what they can handle on their own, thus the need to recruit and orientate workers. Some of the most important communication signals used by foraging ants are chemicals. Indeed, chemicals are used for two distinct functions: the recruitment and mobilisation of ants for food retrieval and the path indication towards the food source.

The chemicals used are pheromones mixed with a volatile or semi-volatile compound. The trail pheromones are synthesized in different glands depending on the ant species: either in the ventral venom gland, in the Dufour gland, in the pygidial gland, or in the Hint gut (Figure 6) (Morgan, 2009). When secreted, the pheromone is dropped in patches by the foraging ant. Each species of ant uses various mixtures of pheromone and components. For example, the M. pergandei ant uses the n-tridecane, produced by the pygidial gland, as a powerful alarm-recruitment pheromone.

There are multiple species of ants, but all operate using two decision making systems for foraging: the “Democratic” or the “Autocratic” chemical mass recruitment (Jaffe et al., 2012). The Democratic recruitment system is well adapted for fast mobilisation towards ephemeral food sources whereas the Autocratic is used when multiple sustainable food sources are available. In the Democratic system, all workers have the same responsibility and release a fixed amount of recruitment pheromone to the trail. A strong pheromone trail indicates a large food source which then attracts more workers to join the foraging opportunity. As a result, this leads to a significant mobilisation of the ant colony in the shortest possible time in order to collect the ephemeral food source. In the Autocratic system, workers are specialized either in identification and chemical communication on where the food sources are or in food retrieval. The first type of workers, the communication specialists, visit different food sources and signal the quantity and quality of their findings with variable levels of pheromones. Indeed, a very good food source will be signaled with a high amount of chemicals on the trail whereas a low quality will have a reduced deposit (Figure 7).

Ant species such as the Atta and the Acromyrmex are usually large colonies with sophisticated social structure using the Autocratic recruitment process. They use carboxylates and pyrazines to lay their pheromone trail which are semi volatile compounds that remain for several hours. These long-lasting chemicals allow ants to locate the food source after spots of inactivity due to rain, heat, cold, or other environmental interruption.

On the contrary, ant species of the subfamily Ponerinae, uses alcohols and acetate, which are much more volatile compounds that requires a fast Democratic recruitment process for a short-term food source. Indeed, the trail made with short lasting volatile can only last if it is reinforced by hundreds of workers.

Chemical Communication in Roundworms

The roundworms, Caenorhabditis elegans, use a highly sophisticated chemical language in order to control their social behaviour such as foraging (Srinivasan et al, 2012). In fact, they combine different chemical fragments to create a precise message telling their group to aggregate or to disperse (Figure 8C). These highly specific molecules are called the indole ascarosides, and they are built with carbohydrate and amino acid groups. In addition, we know that they have at least three functions: aggregation, male attraction and Dauer Formation, which allow the animal to enter a stress resistant stage in adverse situation (Figure 8B).

To perceive these external cues, C. elegans have a highly developed chemoreception system. Indeed, its nervous system is mainly composed of olfactory and gustatory neurons and more than 5% of its genome contains information about chemoreception (Bargmann, 2006). The amphid chemosensory system which is responsible for making decisions related to chemoreception is composed of 11 neurons, each of them expresses a specific set of genes and is sensitive to some molecules (Ludewig & Schroeder, 2018). Information captured by neurons is transmitted to the information processing system via two main transduction systems. The first one mostly relies on TRPV which is a set of ion channels located on the plasma membrane, and second one relies on CGMP which is another set of cation channels.

Ascaroside side chains, the molecules used by the worm, originate from peroxisomal β-oxidation. This reaction includes 4 steps that shorten the long chain fatty acid (von Reuss et al., 2012). First, the enzyme acyl-CoA oxidises the carbon chain and introduces an unsaturation at α,β (Figure 9). The following two steps which include the hydration of the double bond and dehydrogenation is catalyzed by a protein called MFE-2. Finally, the last step was completed by the protein C. elegans DHS-28.

The Evolution of Termite Pheromones

Termites, sometimes referred to as white ants, are a group of cellulose-eating insects. Even though they don’t belong to the same family as ants and bees, they share many common characteristics. For example, they are all composed of great numbers of siblings and live in a highly organized society (Krishna, 2020). Individuals living in these societies are able to communicate using chemical molecules to undertake everyday tasks such as foraging (Mitaka et al., 2021). Since termites often encounter large amounts of resources that are difficult to transport individually, it is especially important to communicate information between individuals within the same family. The molecules used by termites for communication, as seen with bees and ants, are pheromones. There are two distinct ways in which pheromones can evolve (Symonds & Elgar, 2008). First, evolution originates from the accumulation of small changes in components. For example, the quantity of a single component could vary, or the general proportion could change over time. As a result, species that are closely related to each other will share similar pheromone composition. For example, we can observe many similarities in the trail pheromones used by many types of harvester ant of species Pogonomyrmex (Baker, 2002). These changes deviate the pheromones from the normal chemical composition and make the individual less attractive. Thus, individuals will be in an unfavourable position. This is the reason why evolutions are mainly due to the second type, called saltational evolution. These are complete changes in pheromone’s chemical composition. It may happen when an inactive gene is suddenly expressed due to genetic mutation (Baker, 2002). For example, Roelofs et al. (2002, as cited in Baker, 2002) provided evidence that mutation in the genome of Ostrinia gave rise to a modification in the position of the double bond of its pheromone (Figure 10). As a result, a shift to the new pheromone was accomplished by the species.

Fruit Bats

Frugivorous bats, seen in Figure 11, are solitary foragers who pick fruits from plants (Bonaccorso & Gush, 1987). Being nocturnal mammals implies that the fruit bat has an acute sense of smell, therefore relying mainly on olfaction to locate their food source (Hodgkison et al., 2007). For instance, in Neo- and Paleotropical rain forests, there are fig species eaten and scattered by these nocturnal mammals (Kalko et al., 1996). Due to being foraged in the dark, these figs are characterized by specific odors, rather than visual cues that would favour them in the light (Hodgkison et al., 2007). These bats take in the fruits’ odors to differentiate between ripe and unripe fruits. This sensory sensitivity allows them to distinguish odor quality and quantity, hence the introduction of a chemical concentration gradient. The chemical gradient created by a fruit source has an odor structure depending on molecular masses, diffusion coefficients and emission rates as well as depending on the distance from the source itself (Brokaw & Smotherman, 2021). Further away from the fruit, bats move laterally to orient themselves towards that chemical origin, as they continuously sample the odors of the fruit (Brokaw & Smotherman, 2021). Once closer, at high gradient marks, the bat can compare odor intensities using separate receptors, a method also known as a tropotaxis (Brokaw & Smotherman, 2021). Moreover, to specifically localize fruit, bats depend on low volatility compounds (Hodgkison et al., 2007). For instance, sesquiterpenes, which compared to high-volatility compounds, such as ketones and alcohols, help bats distinguish between the ripe and unripe fruit in their proximity by producing more spatially condensed scents (Hodgkison et al., 2007).

Conclusion

Ultimately, the use of chemosensory information determines the animal’s foraging success. The animal’s capacity to detect and retrieve such crucial information affects fitness, given that animals devote a large part of their lifetime foraging. Since all living things are shaped by natural selection, only those with the most efficient sensing organs can survive and reproduce. The essay has demonstrated that kairomones are secreted by plants, allowing phytophagous insects and its parasitoids to effectively locate food sources. Communication between individuals is mediated by pheromones, as seen in ants, bees, roundworms, as well as termites that engage in foraging activities as a group. As for reptiles, some species have been observed using their unique anatomical structures to retrieve chemicals from the external environment. Among diverse senses that allow species to forage optimally, olfaction was seemingly the most prominent one. Although further research is needed to give more insights into how natural selection influenced chemosensory adaptations, the use of chemosensors in foraging animals, as we know now, is fascinating to watch.

References

Aartsma, Y., Bianchi, F. J. J. A., van der Werf, W., Poelman, E. H., & Dicke, M. (2017). Herbivore-induced plant volatiles and tritrophic interactions across spatial scales. New Phytologist, 216(4), 1054-1063. https://doi.org/https://doi.org/10.1111/nph.14475

Baker, T. C. (2002). Mechanism for saltational shifts in pheromone communication systems. Proceedings of the National Academy of Sciences, 99(21), 13368-13370. https://doi.org/doi:10.1073/pnas.222539799

Bargmann, C. I. (2006). Chemosensation in C. elegans. WormBook, 1-29. https://doi.org/10.1895/wormbook.1.123.1

Beyaert, I., & Hilker, M. (2013). Plant odour plumes as mediators of plant-insect interactions. Biological reviews of the Cambridge Philosophical Society, 89. https://doi.org/10.1111/brv.12043

Bonaccorso, F. J., & Gush, T. J. (1987). Feeding Behaviour and Foraging Strategies of Captive Phyllostomid Fruit Bats: An Experimental Study. Journal of Animal Ecology, 56(3), 907-920. https://doi.org/10.2307/4956

Brokaw, A. F., & Smotherman, M. (2021). Olfactory tracking strategies in a neotropical fruit bat. J Exp Biol, 224(Pt 4). https://doi.org/10.1242/jeb.231829

Bruce, T. J., Wadhams, L. J., & Woodcock, C. M. (2005). Insect host location: a volatile situation. Trends Plant Sci, 10(6), 269-274. https://doi.org/10.1016/j.tplants.2005.04.003

Cooper, W. E., Jr., & Alberts, A. C. (1991). Tongue-flicking and biting in response to chemical food stimuli by an iguanid lizard (Dipsosaurus dorsalis) having sealed vomeronasal ducts: Vomerolfaction may mediate these behavioral responses. J Chem Ecol, 17(1), 135-146. https://doi.org/10.1007/bf00994427

Dornhaus, A., Brockmann, A., & Chittka, L. (2003). Bumble bees alert to food with pheromone from tergal gland. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 189(1), 47-51. https://doi.org/10.1007/s00359-002-0374-y

Granero, A. M., Sanz, J. M., Gonzalez, F. J., Vidal, J. L., Dornhaus, A., Ghani, J., Serrano, A. R., & Chittka, L. (2005). Chemical compounds of the foraging recruitment pheromone in bumblebees. Naturwissenschaften, 92(8), 371-374. https://doi.org/10.1007/s00114-005-0002-0

Hansson, B. S. (2002). A bug’s smell–research into insect olfaction. Trends Neurosci, 25(5), 270-274. https://doi.org/10.1016/s0166-2236(02)02140-9

Hodgkison, R., Ayasse, M., Kalko, E. K., Häberlein, C., Schulz, S., Mustapha, W. A., Zubaid, A., & Kunz, T. H. (2007). Chemical ecology of fruit bat foraging behavior in relation to the fruit odors of two species of paleotropical bat-dispersed figs (Ficus hispida and Ficus scortechinii). J Chem Ecol, 33(11), 2097-2110. https://doi.org/10.1007/s10886-007-9367-1

Hölldobler, B., Plowes, N. J., Johnson, R. A., Nishshanka, U., Liu, C., & Attygalle, A. B. (2013). Pygidial gland chemistry and potential alarm-recruitment function in column foraging, but not solitary, Nearctic Messor harvesting ants (Hymenoptera: Formicidae: Myrmicinae). J Insect Physiol, 59(9), 863-869. https://doi.org/10.1016/j.jinsphys.2013.06.006

Hurd, H. (2019). Receptors that help mosquitoes smell us. BugBitten. https://blogs.biomedcentral.com/bugbitten/2019/04/19/receptors-help-mosquitoes-smell-us/

Jackson, B. D., & Morgan, E. D. (1993). Insect chemical communication: Pheromones and exocrine glands of ants. Chemoecology, 4(3-4), 125-144. https://doi.org/10.1007/bf01256548

Jaffe, K., Issa, S., & Sainz-Borgo, C. (2012). Chemical Recruitment for Foraging in Ants (Formicidae) and Termites (Isoptera): A Revealing Comparison. Psyche, 2012, 694910. https://doi.org/10.1155/2012/694910

Kalko, E. K. V., Herre, E. A., & Handley, C. O. (1996). Relation of Fig Fruit Characteristics to Fruit-Eating Bats in the New and Old World Tropics. Journal of Biogeography, 23(4), 565-576. http://www.jstor.org/stable/2845800

Klowden, M. J. (2013). Chapter 12 – Communication Systems. In M. J. Klowden (Ed.), Physiological Systems in Insects (Third Edition) (pp. 603-647). Academic Press. https://doi.org/https://doi.org/10.1016/B978-0-12-415819-1.00012-X

Krishna, K. (2020, April 8). termite. Encyclopaedia Britannica. Retrieved November 4, 2021, from https://www.britannica.com/animal/termite

Ludewig, A. H., & Schroeder, F. C. (2013). Ascaroside signaling in C. elegans. WormBook, 1-22. https://doi.org/10.1895/wormbook.1.155.1

Martinez-Marcos, A., Lanuza, E., & Halpern, M. (2002). Neural substrates for processing chemosensory information in snakes. Brain Research Bulletin, 57, 543-546. https://doi.org/10.1016/S0361-9230(01)00686-4

Mas, F., Horner, R., Brierley, S., Harper, A., & Suckling, D. M. (2020). The Scent of Individual Foraging Bees. J Chem Ecol, 46(5-6), 524-533. https://doi.org/10.1007/s10886-020-01181-7

Mitaka, Y., & Akino, T. (2021). A Review of Termite Pheromones: Multifaceted, Context-Dependent, and Rational Chemical Communications. Frontiers in Ecology and Evolution, 8, 595614. https://doi.org/10.3389/fevo.2020.595614

Molet, M., Chittka, L., & Raine, N. E. (2009). How floral odours are learned inside the bumblebee (Bombus terrestris) nest. Naturwissenschaften, 96(2), 213-219. https://doi.org/10.1007/s00114-008-0465-x

Morgan, E. D. (2009). Trail pheromones of ants. Physiological Entomology, 34(1), 1-17. https://doi.org/https://doi.org/10.1111/j.1365-3032.2008.00658.x

Mustaparta, H. (1990). Chemical information processing in the olfactory system of insects. Physiol Rev, 70(1), 199-245. https://doi.org/10.1152/physrev.1990.70.1.199

Orlova, M., & Amsalem, E. (2021). Bumble bee queen pheromones are context-dependent. Sci Rep, 11(1), 16931. https://doi.org/10.1038/s41598-021-96411-7

Pino, E., Zabala, N. A., Alvarez, M. I., Colmenares, O., Navarro, J. G., Puche, H., Jaffe, K., & Villegas, G. (1985). Two different decision-making systems in recruitment to food in ant societies. Behaviour, 92(1-2), 9-21.

Regal, P. J. (1978). Behavioral Differences Between Reptiles and mammals: An Analysis of Activity and Mental Capabilities. In N. Greenberg & P. D. MacLean (Eds.), Behavior and Neurology of Lizards: An Interdisciplinary Colloquium. U.S. Department of Health, Education, and Welfare, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute of Mental Health.

Roelofs, W. L., Liu, W., Hao, G., Jiao, H., Rooney, A. P., & Linn, C. E., Jr. (2002). Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci U S A, 99(21), 13621-13626. https://doi.org/10.1073/pnas.152445399

Schwenk, K. (2021, June 17). Smelling in stereo: The real reason snakes have flicking, forked tongues. Phys.org. https://phys.org/news/2021-06-stereo-real-snakes-flicking-forked.html

Srinivasan, J., von Reuss, S. H., Bose, N., Zaslaver, A., Mahanti, P., Ho, M. C., O’Doherty, O. G., Edison, A. S., Sternberg, P. W., & Schroeder, F. C. (2012). A modular library of small molecule signals regulates social behaviors in Caenorhabditis elegans. PLoS biology, 10(1), e1001237. https://doi.org/10.1371/journal.pbio.1001237

Sumpter, D., & Beekman, M. (2003). From nonlinearity to optimality: Pheromone trail foraging by ants. Animal Behaviour, 66, 273-280. https://doi.org/10.1006/anbe.2003.2224

Symonds, M. R., & Elgar, M. A. (2008). The evolution of pheromone diversity. Trends Ecol Evol, 23(4), 220-228. https://doi.org/10.1016/j.tree.2007.11.009

Vinson, S. B. (1976). Host Selection by Insect Parasitoids. Annual Review of Entomology, 21(1), 109-133. https://doi.org/10.1146/annurev.en.21.010176.000545

Visser, J. H. (1986). Host Odor Perception in Phytophagous Insects. Annual Review of Entomology, 31(1), 121-144. https://doi.org/10.1146/annurev.en.31.010186.001005

von Reuss, S. H., Bose, N., Srinivasan, J., Yim, J. J., Judkins, J. C., Sternberg, P. W., & Schroeder, F. C. (2012). Comparative metabolomics reveals biogenesis of ascarosides, a modular library of small-molecule signals in C. elegans. J Am Chem Soc, 134(3), 1817-1824. https://doi.org/10.1021/ja210202y

Wäschke, N., Meiners, T., & Rostàs, M. (2013). Foraging strategies of insect parasitoids in complex chemical environments. Recent Advances in Chemical Ecology of Insect Parasitoids, 193-224.

Wyatt, T. D. (2017). Pheromones. Curr Biol, 27(15), R739-r743. https://doi.org/10.1016/j.cub.2017.06.039