Earthworms produce a collagen-like substance detected by the garter snake vomeronasal system.

Abstract

Earthworms (Lumbricus terrestris) produce a chemical substance that is readily detected by and serves as an attractant for garter snakes (Thamnophis sirtalis). This chemoattractant is sensed by the vomeronasal system ofsnakes. Amino acid analysis of the chemoattractant revealed a high hydroxyproline/proline ratio and large amounts of serine and threonine. More than one-third of the residues were glycine. No hydroxylysine and no cysteine were present. Carbohydrate analyses revealed a high content of galactose (11% by weight) and smaller amounts of fucose, mannose, glucose, N-acetylglucosamine, and N-acetylgalactosamine. These results were very similar to results reported for the amino acid composition and carbohydrate content of earthworm cuticle collagen and gelatin. A preparation of purified earthworm cuticle collagen proved to be a potent source of chemoattractant for garter snakes. Further, it was not possible to prepare chemoattractant from decuticlized earthworms. These results strongly suggest that a component of the earthworm chemoattractant for snakes is structurally related to earthworm cuticle collagen.Earthworms (Lumbricus terrestris) are a favorite prey of garter snakes of the genus Thamnophis and form a major component of their natural diet (1, 2). Garter snakes respond to objects coated with warm-water washings from earthworms by rapid tongue-flicking and an attack (1-3), thus suggesting that these washings contain a chemoattractant for the snake. In addition, garter snakes can be trained to follow trails of earthworm washings to receive bits of worm as rewards (4,5). Garter snakes use their vomeronasal systems, but apparently do not require a functional olfactory system, to detect and appropriately respond to this chemoattractant contained in earthworm washings (3,(6)(7)(8). Substances that stimulate the vomeronasal organs are typically naturally occurring complex large molecules that have been difficult to characterize chemically (9)(10)(11)(12)(13)(14).Earthworm washings (EWW), prepared as described by Wilde (3) and Burghardt (1), have been found to contain a chemoattractant for garter snakes that is water-soluble, absorbs at 280 nm, contains carbohydrate, and gives a positive reaction with ninhydrin and positive Lowry and Bradford tests for protein (15)(16)(17).A solution of EWW that had been dialyzed, lyophilized, and reconstituted in 0.15 M NaCl to 5 times its original concentration was separated on various calibrated gel-exclusion columns (16). When 0.15 M NaCl was used as eluent, two peaks were detected by 280 nm absorption (16). The first peak, F2, comprising components of Mr > 65,000, contained all the chemoattractant. This peak also contained neutral carbohydrate and ninhydrin-positive material and gave positive tests for protein. The second peak, F4, comprising components of much lower molecular weight, contained neutral carbohydrate but was devoid of chemoattractant (16).Snakes were able to discriminate the chemoattractant in EWW (pH 5.8) from solvent after the EWW was heated f...

Differential distribution of olfactory receptor neurons in goldfish: Structural and molecular correlates

“…The segregation of the rodent olfactory system into two compartments, the VNO housing the microvillous receptor cells and the main OE housing the ciliated ORNs, led to the belief that ciliated ORNs mediate detection of general odorant cues, whereas microvillous ORNs are responsible for pheromone detection. This view is overly simplistic when applied to vertebrates in general; e.g., the VNO of snakes, which contains microvillous ORNs, is capable of detecting feeding cues (Burghardt, 1970; Kirschenbaum et al, 1986), and the main OE in rodents also responds to sex pheromones (Sipos et al, 1995; Navarro Becerra et al, 1996). For fish, in which the three types of ORNs are intermingled in a single OE, the results of various studies have been contradictory even for a single species.…”

“…Although many nonvolatile odorants are socially relevant signals in rodents, the commonly stated hypothesis that the VNO detects only pheromones is oversimplified and not generally applicable across all species (Johnston, 2000). For example, the VNO of snakes detects feeding‐related cues (Burghardt, 1970; Kirschenbaum et al, 1986; Halpern et al, 1997).…”

Of Pheromones and Kairomones: What Receptors Mediate Innate Emotional Responses?

“…The vomeronasal organ can also mediate the detection of and the innate response to chemical signals of individuals of species different from that of the receiver, the so‐called allomones. Among others, these include prey chemicals detected by their predators, as for the vomeronasal detection of an earthworm glycoprotein by snakes (Kirschenbaum et al, ). Conversely, some preys innately react with defensive (antipredatory) behaviors to the detection of predator allomones.…”

Glycosaminoglycans from earthworms (Eisenia andrei)

“…Comparative studies of two earthworms, Neris (a polychaete) and Lumbricus (an oligochaete) showed that Lumbricus earthworm did not contain the acidic disaccharides but had more galactose units [1, 2]. Interestingly, Lumbricus terrestris earthworm produces a collagen-like substance detected by the garter snake [3]. The carbohydrate content of this collagen-like substance, reveals a high content of galactose (11 wt%) with lesser amounts of fucose, mannose, glucose, N -acetylglucosamine (GlcNAc), and N -acetylgalactosamine (GalNAc) [3].…”

“…Interestingly, Lumbricus terrestris earthworm produces a collagen-like substance detected by the garter snake [3]. The carbohydrate content of this collagen-like substance, reveals a high content of galactose (11 wt%) with lesser amounts of fucose, mannose, glucose, N -acetylglucosamine (GlcNAc), and N -acetylgalactosamine (GalNAc) [3]. Glycosaminoglycans (GAGs) are composed of repeating uronic acid (glucuronic acid (GlcA) or iduronic acid (IdoA)) residues and either GlcNAc or GalNAc residues.…”