Animal Communication: A Chemical Review

Table of Contents

Abstract

Chemical reactions are the base of our universe. From the light of the sun to the function of our own brains, chemical reactions are behind it. It is therefore not unrealistic to imagine that communication can also be explained by chemical reactions. This paper examines the chemistry behind different forms of communication in plants and animals. First, the use of volatile organic compounds by plants is explored, looking specifically at the communication between the Rafflesia Cantelyi flowerand female carrion flies. Next, the use of sex pheromones by moths to communicate with members of the opposite sex to attract mates is investigated. Subsequently, pigments in chameleon skin used to communicate aggression and mood is inspected. Finally, bioluminescence in both dinoflagellates, who communicate their presence mistakenly and fatally to predators by lighting up, and anglerfish, who in the deep-sea use bioluminescence for courtship, is evaluated. With the incredible array of species on Earth, there is a stunning variety of unique forms of communication, and thus these examples are just a taste of the chemistry behind communication in the plant and animal kingdoms.

Introduction

Communication plays a key role in the plant and animal kingdom in a variety of important tasks, including courtship, informing other species of dangers such as predators and diseases, acquiring resources, and more. Most often, communication is specific to a given species and therefore is observed more frequently between conspecifics. Animals from different species may communicate but it is dependent on whether they can understand each other’s “language”.

Communication can vary immensely from one species to the other and the foundations on which these exchanges occur also differ. This paper will focus on the chemical aspects allowing for communication in the plant and animal kingdom. Volatile organic compounds will be explored as a means of communication between plants and insects, and amongst male and female silk moths during courtship. Pigment molecules and chromatophore cells will then be studied as they are crucial elements in a chameleon ability to change its color and thus, to communicate. Lastly, communication between aquatic animals will be explored through bioluminescence, a phenomenon by which chemical reactions occurring within the organism emit light.

Plant Communication through Volatile Organic Compounds (VOCs)

Volatile organic compounds are a multitude of signaling molecules that are primarily secreted by plants into their environment. Although these compounds are chemically disparate, they are all characterized by weak intermolecular attractions and high partial pressures. These characteristics allow VOCs to readily enter gaseous phase and diffuse through the air to the intended target (Bouwmeester et al., 2019). In nature, VOCs are used for all manner of functions. Specific volatile cocktails attract pollinators and mutualists, give flowers their scent, combat pathogens and alert neighboring plants of threats such as disease, drought, or herbivory (Farré-Armengol et al., 2016).

Though the discussion of plant volatiles presented in this section may appear unfamiliar to the reader, VOCs are ubiquitous in our everyday experience. For example, the compound ethylene is responsible for the ripening of fruit such as bananas and apples (Ehrenberg, 2018), while the smell of freshly cut grass is due to the release of the unstable green-leaf volatile (Z)-3-hexanal that typically isomerizes to form the ‘green-leaf aldehyde’ (E)-2-hexanal (Ameye et al., 2018).

In the coming subsections, the classification and biosynthesis of plant-emitted VOCs will be outlined. Thereafter, the specific role of oligosulfides in the mediating plant-pollinator interactions in the carrion-flower rafflesia cantleyi will be discussed as an example of cross-species communication using volatile compounds.  

Biosynthesis

VOCs belong to a variety of chemical classes, including terpenoids, phenylpropanoids, benzenoids/phenolics and fatty-acid derivatives as well as sulfides, aldoximes and nitriles albeit to a lesser extent. Terpenoids are compounds consisting of multiple 5-carbon isoprene subunits and they represent the largest class of volatiles by far (“27.5 Terpenoids,” 2020). Monoterpenoids, sesquiterpenoids and diterpenoids consist of two, three and four isoprene subunits respectively.

The biosynthetic pathways responsible for producing the four major classes of VOCs are outlined in Figure 1 (Bouwmeester et al., 2019).

Fig. 1 Schematic representation of the biosynthetic pathways producing the main classes of VOCs with the substrate and endpoint of each pathway indicated. Representative compounds are given for each chemical class (Bouwmeester et al., 2019).

Fatty acids are produced through the acetate pathway that begins with the substrate acetyl-coA originating from glycolysis. The pathway produces two C18 precursors, namely linoleic and linolenic acid that are successively oxidized and reduced to form aldehydes, alcohols and then acetates such as (Z)-3-hexanal that was briefly discussed in the introduction section (Bouwmeester et al., 2019).  

The MVA and MEP pathways also begin with substrates derived from glycolysis although the substrate of the MEP pathway is pyruvate rather than acetyl-coA. Regardless, both pathways produce the isomeric precursors methylallyl and isopentyl diphosphate that are condensed by the enzymes GDP synthase, GGDP synthase and farnesyl diphosphate synthase to produce the respective products GDP, GGDP and FDP. GDP from the MEP pathway goes on to produce carotenoids and monoterpenoids following a series of enzymatic steps while MVA-derived FDP leads to the formation of sesquiterpenoids (Bouwmeester et al., 2019). Table 1 has a more detailed description of the key compounds involved in the MVA and MEP pathways.

AbbreviationIUPAC NameChemical Formulae
MVA3,5-Dihydroxy-3-methylvaleric acidC6H12O4
MEP[(2R,3S)-2,3,4-trihydroxy-3-methylbutyl] dihydrogen phosphateC5H13O7P
GDP[(2E)-3,7-dimethylocta-2,6-dienyl] phosphono hydrogen phosphateC10H20O7P2
GGDPphosphono [(2E,6E,10E)-3,7,11,15-tetramethylhexadeca-2,6,10,14-tetraenyl] hydrogen phosphateC20H36O7P2
FDPphosphono [(2E,6E)-3,7,11-trimethyldodeca-2,6,10-trienyl] hydrogen phosphateC15H28O7P2
Table 1. The abbreviations, full IUPAC names and chemical formulae of key compounds involved in the MVA and MEP pathways (National Center for Biotechnology Information, 2021a, 2021b, 2021c, 2021d, 2021e).

The Shikimate pathway differs from the rest as it involves two substrates d-erythrose-4-phosphate from pentose phosphate cycle and phosphenylpyruvic acid from the glycolytic reactions. This pathway involves six enzymatic steps that culminate in the end-product chorismic acid, the precursor to the vast majority of benzenoid and phenylpropanoid volatiles (Bouwmeester et al., 2019).

VOC-mediated Plant-Pollinarot Interactions in Rafflesia Cantelyi

Rafflesia cantleyi is one of 36 members of the ‘monster flower’ genus Rafflesia that are endemic to the tropical and subtropical rainforests of Southeast Asia. Rafflesia species are obligate endoparasites that have lost all recognizable leaves, roots, and vegetative stems although some species retain scale-like structures that are the vestigial remnants of leaves. The plants themselves consist only of filamentous cellular threads resembling mycelial hyphae that penetrate and draw nutrients from the roots of Tetrastigma vines. Rafflesia boasts some of the largest inflorescences in the plant kingdom with flowers from the species R. Arnoldii surpassing 1 m in length and 24 lb in weight (The Editors of Encyclopaedia Britannica, 2017).

The flowers of R. cantleyi are pollinated almost exclusively by female carrion flies of the species Chyromya chani (C. chani). To attract these pollinators, the blooms of R. cantleyi have evolved to mimic rotting flesh, the oviposition substrate of C. chani, using visual, chemical, and morphological cues. Over long distances, carrion-flies are drawn to the flowers via olfaction of the emitted volatiles dimethyl disulfide (DMDS) and dimethyl trisulfide (DMTS) which are by-products of the bacterial decomposition of methionine and cysteine in rotting meat (Wee et al., 2018). Over short ranges, the flower’s gruesome reddish-brown, mottled pigmentation alerts the flies to the source of the odor. Once flies venture into the perigone tube, they are guided by hairs and grooves to the sexual organs (Fig. 2) (Beaman et al., 1988; Wee et al., 2018).

Fig. 2 Flower of the rafflesia species R. cantleyi (not to scale) with key morphological characteristics highlighted (Wee et al., 2018).

From the perspective of plant-pollinator communication, R. cantleyi’s is remarkable in its ability to attract a single pollinator species. In field studies, five different species of calliphorid flies were observed to visit R. cantleyi inflorescences although females of the species C. chani constituted 97% of visitors and were the sole flies observed to carry pollen. By contrast, rotting meat samples attracted 9 fly species of which C. chani represented only a quarter of visitors. Since the volatiles DMDS and DMTS are known to attract a plethora of carrion flies, the root cause of the pollinator-specificity of R. cantleyi is debated. In addition to oligosulfides, R. cantleyi emits small amounts of terpenoid and green-leaf volatiles that could potentially deter non-pollinating fly species and C. chani males. Alternatively, the 9:1 ratio of DMDS to DMTS could be specifically attractive to C. chani females. This last conjecture is supported by a study which observed strong attraction to a 9:1 ratio of synthetic DMDS/DMTS in C. chani females and no attraction in 1:1 blend (Wee et al., 2018).

Pheromones

There is a world of communication in the animal kingdom that utilizes what we might consider our weakest sense: smell. Mammals, insects, and reptiles communicate through semiochemicals (chemicals that participate in communication). Though semiochemicals include substances involved in both interspecific and intraspecific communication, pheromones, which is what will be discussed in this section, are limited to chemicals involved in intraspecific communication (i.e. communication between two mice and not between a mouse and a cat). Pheromones are not simply smells. In many ways pheromones are like hormones as when they are received by a conspecific it produces certain physiological responses (Fleischer & Krieger, 2018). There are many examples of pheromone use that are observed in our daily lives: dogs peeing on a fire hydrant, worker bees following their queen bee, and ants following a trail from their food source back to their anthill.

This section will explore the use of sex pheromones in moths for communication.

Sex Pheromones in Lepidoptera (Moths and Butterflies)

Adult moths have incredibly short life spans and thus exist to procreate. For this to be successful they must locate a member of the same species and of the opposite sex (Sandler et al., 2000). Female moths can attract males from many kilometers away by protruding their abdominal tip to release long range sex pheromones (Allison & Cardé, 2016). Female moth sex pheromones are species-specific blends of chemicals (often two to three components) (Kaissling, 2014) with a particular ratio. Different blends and ratios of chemicals will not have the desired effect on males of the same species (Ando et al., 2004). Most of female moth’s pheromone blends are composed of one of two types of compounds. Type I pheromones consist of straight carbon chains between 10 and 18 carbons long with a few double bonds interspersed throughout and an oxygenated functional group – either an alcohol, aldehyde, or acetate ester. Most lepidoptera sex pheromone mixtures are composed of Type I compounds. Type II pheromones are composed of biosynthesized chemicals using linoleic/linolenic acids (1-3 cis hydrocarbons and 0-2 epoxide functions) that are consumed through their diet (D.-S. Chen et al., 2017).

The first species to have its sex pheromone’s chemical profile identified is that of the silkworm moth (Bombyx mori) (Fig. 3) (Sandler et al., 2000). Its sex pheromone blend is composed of (E,Z)-10, 12-hexadecadiene-1-ol (bombykol) (Fig. 4) and small amounts of (E,E)-isomer of the alcohol and the analogous (E,Z)-aldehyde (bombykal) (Kaissling, 2014).

Fig. 3 Image of the Bombyx mori (Baum, 2017).
Fig. 4 Bond line diagram of Bombykol (the main chemical in the pheromone blend of the female silkworm moth).

In most female moths, the synthesis of sex pheromones begins with the synthesis of a long, saturated fatty acid chain: first, the carboxylation of Acetyl-CoA is catalyzed by the enzyme Acetyl-CoA carboxylase to form Malonyl-CoA; then, from Malonyl-CoA, fatty acid synthetase catalyzes an acyl chain; subsequently, double bonds between carbons are added to specific points along the carbon chain by desaturates; and finally fatty acid reductases synthesise the oxygenated functional groups which are added to the fatty acids. There are also enzymes that help transport the pheromones produced by the female moth to be released out of the abdominal tip (D.-S. Chen et al., 2017).

Once released into the air, female moth sex pheromones enter the antennal sensilla of male moths through pore tubules. The inside of the sensilla has an aqueous solution and as the pheromone molecules are hydrophobic (moth pheromones are mainly fatty acids and though they have a polar functional group, most of the molecule is a hydrocarbon chain which is hydrophobic), they are not soluble in this solution. Thus, pheromone-binding proteins bind to the pheromones to solubilize them into the solution by interacting with the pheromone molecule through Van der Waals interactions. A concentrated gradient of the pheromone within the sensilla leads to the pheromones diffusion away from the pore tubules and towards the olfactory receptor neurons (ORNs). From there, a series of signals is sent throughout the moth’s body which leads to a behavioural response. In male moths, the behavioural response to the reception of female moth sex pheromones is to follow the pheromone until the female moth is found (Leal, 2016).

And thus, female moths can successfully communicate their desire for a mate to conspecific males using species-specific blends of sex pheromones.

Chameleon Communication through Skin Color Variations

Chameleons (Fig. 5) rely on changing the color of their skin to communicate with conspecifics. They can do so as a result of the chromatophore and iridophore cells located in their skin tissues. Chromatophores contain pigment molecules that occupy varying amounts of space and iridophore cells can reflect light (Yu et al., 2020). These color variations serve as signals to communicate a readiness to mate, mood such as aggressiveness, and more.

Fig. 5 Chameleon expressing multiple skin colors (Ryan, 2016).

Chameleons have long been known to change their skin color; however, unlike commonly believed, they do so to regulate their body temperature and communicate, not necessarily to camouflage (Smith et al., 2016). Until 2015, it was believed that pigment molecules were solely responsible for a chameleon’s color; however, it was discovered that the spacing between nanocrystals in iridophore cells can be adjusted causing changes in the reflection of light, thereby inducing a change in color (Teyssier et al., 2015). This section of the paper will cover chameleon communication with a focus on the chemical foundations allowing for such changes in skin color.

Chameleon Skin Anatomy

A chameleon’s skin is composed of chromatophores, cells containing pigment molecules. Chromatophores can be further subdivided based on the color they produce under white light: Xanthophores are yellow, erythrophores are red, leucophores are white, melanophores are black/brown, cyanophores are blue, and iridophores produce iridescent colors (Cuervo et al., 2016).

A chameleon’s skin has an outermost transparent epidermis followed by the dermis which contains the chromatophores; namely, a layer of xanthophores and a layer of erthyrophores, below which can be found the iridophore layer containing guanine nanocrystals, followed by the melanophore layer (Fig. 6) (Taylor & Hadley, 1970) .

Fig. 6 Cross section of a bright-green chameleon’s skin. C is a layer of cornified cells. E is the epidermis. D is the dermis. M and PMA are the locations of the melanophore pigments. X and I are the location of the xanthophores and iridophores respectively (Taylor & Hadley, 1970).

How do Chromatophores Contribute to Color Change?

Chromatophore cells contain a pigment sac which can be expanded and contracted through muscle fibers (Ligon & McCartney, 2016). When the sac is expanded, the chromatocyte is filled with pigments and motor proteins that allow for uniform dispersal of the pigments. A study performed by Nery and Castrucci in 1997 suggests that the dispersal of pigment would be done via the following pathway: a signal molecule binds to the receptor located on the plasma membrane, which increases the concentration of cAMP (cyclic adenosine monophosphate), thereby triggering the activation of kinase A. The former phosphorylates the proteins attached to the pigment molecules, allowing for the motor proteins (kinesin, dynein, or myosin) to transport the pigments along microtubules within the chromatophore (Fig. 7). The opposite phenomenon may also occur when the pigment is contracted. In such a case, kinase A is inactivated and proteins are dephosphorylated, thereby allowing the motor proteins to transport the pigment back towards the center of the cell.

Fig. 7 The dispersion of melanin pigment along microtubules with the help of motor proteins (Ligon & McCartney, 2016).

Chameleons can control the contraction of pigment sacs via nerve endings. Chameleons only have three pigment colors: yellow, red, and black/ brown. The remaining colors are produced by reflective guanine nanocrystals located in the iridophore cells.

Pigment Metabolization

Xanthophore cells contain yellow pteridine pigments that are metabolized within the chromatophore from guanosine triphosphate and through biochemical pathways. Erythrophores contain carotenoids, which are metabolized outside of the chromatophore cell before they migrate to the chromatocyte. Unlike pteridine, carotenoids are not synthesized directly in the chromatophore and can only be metabolized through the chameleon’s diet. Although carotenoids and pteridine may both be present within a xanthophore or erythrophore cell, the overall coloration is determined by the relative amounts of each pigment. Melanophores contain melanin which is synthesized by the oxidation and polymerization of tyrosine with the help of the enzyme tyrosinase (Ligon & McCartney, 2016).

What does a Chameleon’s Color Signify?

In a resting state, a chameleon will exbibit a greenish brown color to help it blend into its environment (Fig. 8). The green color is produced by combination of the expanded yellow pigments within the chameleon’s skin and the blue light produced by the reflection of the nanocrystals (Smith et al., 2016).

Fig. 8 A chameleon in its resting state (Bradford, 2015).

To show aggression and dominance, male chameleons will become bright red, green, blue, or yellow (Fig. 9). Doing so allows them to protect their territory and attract females as they are more visible. The color of their skin is changed through pigment expansion or contraction and refraction of iridescent light. The colors produced may result from the interactions between the pigment and reflected light (as explained above for the case of a green chameleon) (Smith et al., 2016).

Fig. 9 A chameleon in an angry state (Melina, 2011).

A chameleon can also share its mood with conspecifics based on the color of its skin. For example, red chameleons are associated with anger while darker colors near the throat area signify illness, depression, or the need to attract more sunlight to regulate body temperature. Depression may occur if they are sick or lack food and result in the chameleon remaining stationary and showing very little excitation. Females may also take on brown or white colors (Fig. 10) when they are carrying children which signals to males that they are not actively searching for a mating partner (Smith et al., 2016).

Fig. 10 Female chameleon carrying children (Dan, 2019).

Bioluminescence in Deep Sea Benthos

In extensive pressure, cold waters, and below 1000 meters of depth, creatures living beyond the twilight zone (Fig. 11) spend their lives in an expanse of darkness. With no sunlight existing in the deep sea, many of these organisms have adapted advantageous attributes such as self-creation or aid of twinkling, flashing, pulsating lights to communicate with one another and other species. These adaptations are created by the process of bioluminescence, the result of a chemical reaction that produces light energy within the body of an organism. This single adaptation unites vastly different marine species, from miniscule marine plankton to enormous anglerfish.

Fig. 11 Classification of deep sea regions (Martini et al., 2019)

Prey Warning by Dinoflagellates

Dinoflagellates (Fig. 12) are motile unicellular eukaryotes, often classified as marine plankton. They only possess two flagella, lash-like appendage perturbing from the cell body used for locomotion. These simple structured organisms’ range in size from 30 µm to 1 mm and effectively exist in colonies, which line the ocean surface. Certain dinoflagellate species are photosynthetic, such as the Lingulodinium polyedra species (Fig. 13). This photosynthetic property allows the creation of bioluminescence and can cause the surface of the ocean to sparkle at night (Santhanam, 2015).

Fig. 12 Dinoflagellates (Dinoflagellates, 2011).
Fig. 13 A Lingulodinium polyedra colony off the coast of California (Olson, 2011).

Although certain dinoflagellates do have the ability to self-produce light, it is regulated by flow-agitation. This can be modelled by a shrimp travelling through water containing colonies of dinoflagellates.

To achieve bioluminescence, dinoflagellate self-synthesize a light-producing compound called luciferin and a rate-affecting catalyst called luciferase. These two chemicals remain inactive in the dinoflagellate’s scintillons, their luminant producing organelles, until there is motion or disturbance in the water. As a shrimp travels through dinoflagellate-filled waters, the shrimp creates motion in the water. This shrimp’s motion in water creates a mixing of the surface of water, which is oxygenated from diffusion of the surrounding atmosphere, with lower sublayers of water (Fig. 14). As oxygenated water is diffused to interact in the regions of dinoflagellates existence, oxygen component triggers the oxidation of luciferase with luciferin (Fig. 15). As the alcohol functional groups are clefted from the luciferin compound, energy is released and an oxyluciferin by-product is created. The energy is transmitted in form of light, which can be observed as bioluminescence (Wang, 2008).

In a social-organism context, the dinoflagellates use light creation to communicate visually to other marine species. When the light is created, it visually signals to predators that the shrimp is present in location, allowing the predator to catch their prey, the shrimp. This then, prevents the shrimp from eating the dinoflagellates.

Fig. 14 Diffusion and Circulation of Oxygen in Water (Fondriest Environmental, Inc, 2013).
Fig. 15 Oxidation of Luciferin (Man, 2019).

Anglerfish Courtship with aid of Photobacterium

The anglerfish (Fig. 16) inhabits the waters 4000 meters below sea level. In a region with no light or oxygen, species are required to adapt for survival. The anglerfish is prominently known for its use bioluminescence as a form of visual communication in courtship.

Fig. 16 Female anglerfish with male attached on anterior (Haddock et al., 2010).

The anglerfish’s light emanates from the esca, a fishing-rod-like extension on the forehead. In the esca and illicium structure are bioluminescent bacteria, photobacterium. Due to the lack of ability for the anglerfish to self-produce light, the bacteria live as a symbiont, obtaining minerals from the fish, while providing the anglerfish ability to produce light.

In the esca of the anglerfish, the photobacterium provides a bacterial luciferase to oxidize the FMNH2 molecule, a cofactor, which the anglerfish self-synthesises through coupling reactions (Fig. 17 Step 2). The bacterial luciferase is mobilized by the presence FMNH2 and can be immobilized by Sepharose, a signal peptide produced by the anglerfish (Y.-G. Chen et al., 1995)

Fig. 17 Coupling Reaction from a fatty acid reactant to produce light, occurring in esca of anglerfish (Kricka, 2005).

This controlled ability of anglerfish to activate the release of bacterial luciferase allows the female anglerfish to visually communicate to lure males for courtship.

With over 40% of all deep-sea organism possessing the capability of synthesizing light, the property of bioluminescence is regarded as an integral attribute of communication for sustaining life in the deep depths of the ocean.

Conclusion

Over the course of this review, communication methods spanning both the plant and animal kingdoms were analyzed from a chemical perspective. In the case of the carrion-mimicking flower Rafflesia cantleyi, DMDS and DMTS are the primary compounds responsible for pollinator attraction, a form of plant-insect communication. Similarly, communication between male and female silk moths during courtship can be primarily attributed to a handful of volatiles, the most prominent of which is bombykol. Chameleons, on the other hand, make use of both chemical and physical principles to communicate with conspecifics, as they communicate through skin color variation, which is dependent on pigment molecules in its chromatophore cells in addition tostructural coloration elements. Finally, the last section of this essay describes bioluminescent communication, a phenomenon that occurs due to the enzyme-catalyzed oxidation of luciferin. In summary, these findings indicate that seemingly disparate communication methods are unified by their exploitation of and reliance upon biochemical pathways and semiochemicals. Hence, communication and chemistry, are inextricably linked.

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