Characterization of vomeronasally-mediated response-eliciting components of earthworm wash-II

Halpern, Mimi; Schulman, Nancy; Scribani, L.; Kirschenbaum, Donald M.

doi:10.1016/s0091-3057(84)80053-2

Cited by 15 publications

(10 citation statements)

References 17 publications

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“…Earthworm mucus is known to affect insect behaviour, either as an attractant (Morris and Pivnick, 1991), or as a repellent (Laakso and Setailai, 1997). The earthworm Lumbricus terrestris has been shown to excrete a cutaneous snake-attracting compound that acts after contact through the vomeronasal system of the snake (Halpern et al, 1984;Kirschenbaum et al, 1985;Wang et al, 1988). Attraction could be mediated by various nitrogenous molecules which are contained in the epidermal earthworm mucus (glycoproteins, peptides, amino acids) and in urine (ammonia, urea) which mingles with mucus (El Duweini and Ghabbour, 1971;Cortez and Bouché, 1987).…”

Section: Direct Contact With Earthworm Excretamentioning

confidence: 99%

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Earthworm excreta attract soil springtails: laboratory experiments on Heteromurus Nitidus (Collembola: Entomobryidae)

Salmon¹,

Ponge²

2001

Soil Biology and Biochemistry

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Microarthropods are often found more abundantly in soils with earthworms than in soils without.Earthworms probably create a favourable environment for microarthropods but few studies have aimed to explain this earthworm effect. The soil collembolan (Hexapoda) Heteromurus nitidus, living in soils at pH > 5 only and thus rich in earthworms, is particularly attracted by earthworms in humus cores. The effect of earthworms on the distribution of H. nitidus can be mediated either by direct contact or by odour perception.Two experimental designs were used to determine the pathway of attraction. The first set of experiments studied the effect of direct contact with earthworm excreta on the distribution of H. nitidus. The mixture of urine and mucus of the lumbricid earthworms Aporrectodea giardi and Alollobophora chlorotica signifcantly attracted H.nitidus as compared to deionized water while fresh earthworm casts were not preferred to calcic mull made of older casts. The same experiment involving direct contact with mucus and methyl blue showed that Collembola sucked on mucus/urine, indicating that the interaction of Collembola and earthworms was at least partly trophic. The second experiment demonstrated that H. nitidus was attracted by the odour of Aporrectodea giardi at short distance. The odour of excreta (mucus, urine and casts) of Aporrectodea giardi also attracted H. nitidus but this attraction was weaker and did not occur constantly, possibly due to interactions with light and aggregation pheromones. We conclude that the prominent pathway by which earthworms could attract H. nitidus in the field is through direct contact with earthworm mucus and urine. The acid-intolerant distribution of this species in the field could be partly explained by a trophic interaction with some earthworm species.

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Section: Direct Contact With Earthworm Excretamentioning

confidence: 99%

“…Some Collembola were also attracted by a mite species (Huber, 1979). In addition, earthworms are known to attract other invertebrate species (Halpern et al, 1984;Morris and Pivnick, 1991).…”

Section: Introductionmentioning

confidence: 99%

Earthworm excreta attract soil springtails: laboratory experiments on Heteromurus Nitidus (Collembola: Entomobryidae)

Salmon¹,

Ponge²

2001

Soil Biology and Biochemistry

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“…It has been demonstrated that some Collembolan species are attracted by odours produced by fungal species on which they feed (Bengtson et al, 1988), which may support the idea of chemoattraction if such odours are produced by 17 earthworms. Furthermore, glycoproteins excreted by Lumbricus terrestris have been suspected to induce attack by its predators (Halpern et al, 1984).…”

Section: Consequently the Distribution Of H Nitidus In Relation To mentioning

confidence: 99%

Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil acidity: interactions with earthworms and predator pressure

Salmon¹

1999

Soil Biology and Biochemistry

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“…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).…”

mentioning

confidence: 99%

“…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).…”

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confidence: 99%

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

Kirschenbaum¹,

Schulman²,

Halpern³

1986

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Characterization of vomeronasally-mediated response-eliciting components of earthworm wash-II

Cited by 15 publications

References 17 publications

Earthworm excreta attract soil springtails: laboratory experiments on Heteromurus Nitidus (Collembola: Entomobryidae)

Earthworm excreta attract soil springtails: laboratory experiments on Heteromurus Nitidus (Collembola: Entomobryidae)

Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil acidity: interactions with earthworms and predator pressure

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

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