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Gnawing by small mammals
GNAWING BY SMALL MAMMALS on effused stromatic ascomycetes Brian Spooner* lichenised fungi, may also be important. Reindeer, in particular, feed regularly on lichens, especially Cetraria islandica (Iceland moss), as well as various Cladonia and Usnea species, and in Sweden voles and other small mammals may eat lichens when other food sources are scarce (Hansson & Larsson, 1978). Non-lichenised ascomycetes other than truffles and truffle-like species (Elaphomycetales, Tuberales) are evidently little used, though a few of the larger Pezizales may be taken (Fogel & Trappe, 1978). The purpose of this note is to report observations on the utilisation by small mammals of effused fungal stromata1, mostly on dead decorticated branches. This appears to be undocumented behaviour and yet can be commonly encountered, indicated by conspicuous toothmarks over areas of the branch where the fungus is present (Fig. 1). These toothmarks can be found most frequently on stromata of Eutypa maura (Diatrypaceae)(= E. acharii), a common species which occurs on dead branches of Acer pseudoplatanus. Toothmarks occur on attached branches to a height of at least 4m in the tree, and can also be found commonly on fallen branches. Similar toothmarks have also been found on stromata of two other fungi, though each only on one occasion: on basal stromatic tissue of Cryptostroma corticale (the cause of ‘sooty bark disease’) on dead trunks of young trees of Acer pseudoplatanus (West Molesey, Cow Common, 2006) and once on the stroma of Ascodichaena rugosa on living branches of Fagus sylvatica in the New Forest (Lyndhurst, Gritnam Wood, April 2005). The marks are always paired,
he importance of fungi as a food source for small mammals is well known. Fogel & Trappe (1978) compiled a detailed review of fungus consumption by small mammals and provided a comprehensive list of fungal species reported as food sources. The diversity of fungi involved is high, with no fewer than 89 species listed by these authors, as is the range of mammal families which include species known to eat fungi at least as an occasional part of their diet. For some mammals fungi form a major part of the diet, more than 50% yearly dietary volume for some chipmunks and squirrels (see Fogel & Trappe, 1978), and in some cases a remarkable symbiosis exists whereby hypogeous fungi, which have no active spore discharge, may rely on dispersal by mammals. Their tree hosts are equally reliant on this symbiosis, forming a significant three-way relationship which is important for forest management (Maser et al., 1978 a,b; Trappe, 1979). In other cases fungi are taken only occasionally to supplement the diet, though for rabbits and some squirrels fungus consumption may be a regular activity, especially during winter. Many British examples of this activity were reported by Hastings & Mottram (1917), and Turnbull (1995) reported various hypogeous species and boletes identified from gut contents of red squirrels in Scotland. Mice and voles also utilise fungi as food in varying amounts (e.g. Watts, 1968). In most cases it is the fruitbodies of larger fleshy fungi, especially agaricoid species, including boletes, and some polypores, which are utilised, though others, including some
T
Mycology Section, Royal Botanic Gardens, Kew, Surrey TW9 3AB
63
Fig. 1. Rodent toothmarks on stromata of Eutypa maura on dead branch of Acer pseudoplatanus ftom West Molesey, Surrey. Photograph © Royal Botanic Gardens, Kew.
with narrow central strip, and presumably are due to the lower incisors of a rodent. They are narrow, being individually no more than 0.5 - 0.7 mm across, and are surely due to either mice or voles (see Strachan, 1995). The occurrence on attached branches high in trees indicates a climbing mammal, most likely bank vole (Clethrionomys glareolus), which has been shown to regularly use fungi in the diet (Watts, 1968), or perhaps field mouse (Apodemus sylvaticus). The latter species, though well known to climb, appears to be less dependent on fungi as a food source. A detailed study of food eaten by these species at Wytham Woods in Berkshire (Watts, 1968) showed bank voles to regularly take fungi but makes no mention of stromatic ascomycetes, nor does it report any feeding by bank voles on dead wood, though dead leaves and dead bracken (Pteridium aquilinum) are noted as being eaten at times. Members of Diatrypaceae are not specifically known to provide a food source for small mammals and these fungi are not listed by Fogel & Trappe (1978) though spores of members of this family (which are allantoid, pigmented and quite characteristic) have
been reported from winter gut contents of flying squirrels (Currah et al., 2000). Most small mammals which occasionally take fungi rely on plant matter as the main part of their diet, and this will often include bark stripped from living trees, especially during winter months (Strachan, 1995). The inner layers of the bark are nutritious and, in some cases, damage to trees due to branches being completely stripped of bark can be severe and of commercial importance so that the mammals are regarded as pests. This applies especially to grey squirrels and rabbits, though voles are also culprits at times. Dead wood is evidently not taken and presumably would have little or no nutritional value to mammals. On dead branches where the fungus is not developed there is no feeding and no trace of toothmarks, which suggests that it is definitely the fungus that is being utilised. Furthermore, dead bark still covering fungal stromata developed in the wood beneath has at times been seen to be pulled back to gain access to the fungal tissue. These observations suggest the regular utilisation of carbonised fungal tissue by 64
rodents, which prompts the question as to what the animals gain from this behaviour. Close inspection of the branches involved shows that it is only the effused, carbonised stroma that is utilised. The perithecia, which in all material examined have been found to contain fertile hymenial tissue and spores which might be conceivably be of food value, lie more deeply sunken in the wood and remain untouched. The black, carbonised stromatal tissue seems unlikely to provide any nutritional value. It may be that this tissue has some function other than nutrition in the gut, or could it provide a useful toothsharpening tool?
References Currah, R.S., Smreciu, E.A., Lehesvirta, T.M., Niemi, M. & Larsen, K.W. (2000). Fungi in the winter diets of northern flying squirrels and red squirrels in the boreal mixed wood forest of northeastern Alberta. Can. J. Bot. 78: 1514 - 1520. Fogel, R & Trappe, J.M. (1978). Fungus Consumption (Mycophagy) by Small Animals. Northwest Science 52: 1 - 31. Hansson, L. & Larsson, T-B. (1978). Vole diet in experimentally managed reforestation areas in northern Sweden. Holarctic Ecology 1: 16 - 26. Hastings, S. & Mottram, J.C. (1917). Observations upon the edibility of fungi for rodents. Trans. Brit. Mycol. Soc. 5: 364 - 378. Maser, C., Trappe, J.M. & Nussbaum, R.A. (1978). Fungal-small mammal interrelationships with emphasis on Oregon coniferous forests. Ecology 59: 799 - 809. Maser, C., Trappe, J.M. & Ure, D.C. (1978). Implications of Small Mammal Mycophagy to the Management of Western Coniferous Forests. Trans. 43rd N. Am. Wildlife & Nat. Res. Conference: 78 - 88. Strachan, R. (1995). Mammal Detective. Whittet Books. London. Trappe, J. (1979). Small mammals traffic in truffles. Forestry Research West 1979(1): 1-4 Turnbull, E. (1995). Not only nuts in May.... Mycologist 9: 82-83. Watts, C.H.S. (1968). The foods eaten by wood mice and bank voles in Wytham Woods, Berkshire. J. Animal. Ecol. 37: 25 - 41.
Acknowledgements Thanks are due to Peter Gasson (RBG Kew) for general discussion and for contact information, to Dr Pat Morris for helpful comments, and to Mariko Parslow for taking the photograph.
1Stroma (plural stromata) A stroma comprises sterile or vegetative tissue of a fungus, sometimes intermixed with tissue of the host plant, in, on or beneath which the sporebearing structures of the fungus are developed. The structure and position of stromatic tissue varies greatly according to the type of fungus involved. In many ascomycetes the tissue commonly comprises cells with thickened, blackish, melanised ('carbonised') walls and reduced lumen, as is the case in many Diatrypaceae (including Eutypa), and other families, notably Xylariaceae. In Eutypa, the stroma usually develops in host wood beneath the bark and appears as an effused or widely-spreading blackened, crustlike surface to the wood, the spore-producing perithecia developing in the wood just beneath the blackened surface.
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he importance of fungi as a food source for small mammals is well known. Fogel & Trappe (1978) compiled a detailed review of fungus consumption by small mammals and provided a comprehensive list of fungal species reported as food sources. The diversity of fungi involved is high, with no fewer than 89 species listed by these authors, as is the range of mammal families which include species known to eat fungi at least as an occasional part of their diet. For some mammals fungi form a major part of the diet, more than 50% yearly dietary volume for some chipmunks and squirrels (see Fogel & Trappe, 1978), and in some cases a remarkable symbiosis exists whereby hypogeous fungi, which have no active spore discharge, may rely on dispersal by mammals. Their tree hosts are equally reliant on this symbiosis, forming a significant three-way relationship which is important for forest management (Maser et al., 1978 a,b; Trappe, 1979). In other cases fungi are taken only occasionally to supplement the diet, though for rabbits and some squirrels fungus consumption may be a regular activity, especially during winter. Many British examples of this activity were reported by Hastings & Mottram (1917), and Turnbull (1995) reported various hypogeous species and boletes identified from gut contents of red squirrels in Scotland. Mice and voles also utilise fungi as food in varying amounts (e.g. Watts, 1968). In most cases it is the fruitbodies of larger fleshy fungi, especially agaricoid species, including boletes, and some polypores, which are utilised, though others, including some
T
Mycology Section, Royal Botanic Gardens, Kew, Surrey TW9 3AB
63
Fig. 1. Rodent toothmarks on stromata of Eutypa maura on dead branch of Acer pseudoplatanus ftom West Molesey, Surrey. Photograph © Royal Botanic Gardens, Kew.
with narrow central strip, and presumably are due to the lower incisors of a rodent. They are narrow, being individually no more than 0.5 - 0.7 mm across, and are surely due to either mice or voles (see Strachan, 1995). The occurrence on attached branches high in trees indicates a climbing mammal, most likely bank vole (Clethrionomys glareolus), which has been shown to regularly use fungi in the diet (Watts, 1968), or perhaps field mouse (Apodemus sylvaticus). The latter species, though well known to climb, appears to be less dependent on fungi as a food source. A detailed study of food eaten by these species at Wytham Woods in Berkshire (Watts, 1968) showed bank voles to regularly take fungi but makes no mention of stromatic ascomycetes, nor does it report any feeding by bank voles on dead wood, though dead leaves and dead bracken (Pteridium aquilinum) are noted as being eaten at times. Members of Diatrypaceae are not specifically known to provide a food source for small mammals and these fungi are not listed by Fogel & Trappe (1978) though spores of members of this family (which are allantoid, pigmented and quite characteristic) have
been reported from winter gut contents of flying squirrels (Currah et al., 2000). Most small mammals which occasionally take fungi rely on plant matter as the main part of their diet, and this will often include bark stripped from living trees, especially during winter months (Strachan, 1995). The inner layers of the bark are nutritious and, in some cases, damage to trees due to branches being completely stripped of bark can be severe and of commercial importance so that the mammals are regarded as pests. This applies especially to grey squirrels and rabbits, though voles are also culprits at times. Dead wood is evidently not taken and presumably would have little or no nutritional value to mammals. On dead branches where the fungus is not developed there is no feeding and no trace of toothmarks, which suggests that it is definitely the fungus that is being utilised. Furthermore, dead bark still covering fungal stromata developed in the wood beneath has at times been seen to be pulled back to gain access to the fungal tissue. These observations suggest the regular utilisation of carbonised fungal tissue by 64
rodents, which prompts the question as to what the animals gain from this behaviour. Close inspection of the branches involved shows that it is only the effused, carbonised stroma that is utilised. The perithecia, which in all material examined have been found to contain fertile hymenial tissue and spores which might be conceivably be of food value, lie more deeply sunken in the wood and remain untouched. The black, carbonised stromatal tissue seems unlikely to provide any nutritional value. It may be that this tissue has some function other than nutrition in the gut, or could it provide a useful toothsharpening tool?
References Currah, R.S., Smreciu, E.A., Lehesvirta, T.M., Niemi, M. & Larsen, K.W. (2000). Fungi in the winter diets of northern flying squirrels and red squirrels in the boreal mixed wood forest of northeastern Alberta. Can. J. Bot. 78: 1514 - 1520. Fogel, R & Trappe, J.M. (1978). Fungus Consumption (Mycophagy) by Small Animals. Northwest Science 52: 1 - 31. Hansson, L. & Larsson, T-B. (1978). Vole diet in experimentally managed reforestation areas in northern Sweden. Holarctic Ecology 1: 16 - 26. Hastings, S. & Mottram, J.C. (1917). Observations upon the edibility of fungi for rodents. Trans. Brit. Mycol. Soc. 5: 364 - 378. Maser, C., Trappe, J.M. & Nussbaum, R.A. (1978). Fungal-small mammal interrelationships with emphasis on Oregon coniferous forests. Ecology 59: 799 - 809. Maser, C., Trappe, J.M. & Ure, D.C. (1978). Implications of Small Mammal Mycophagy to the Management of Western Coniferous Forests. Trans. 43rd N. Am. Wildlife & Nat. Res. Conference: 78 - 88. Strachan, R. (1995). Mammal Detective. Whittet Books. London. Trappe, J. (1979). Small mammals traffic in truffles. Forestry Research West 1979(1): 1-4 Turnbull, E. (1995). Not only nuts in May.... Mycologist 9: 82-83. Watts, C.H.S. (1968). The foods eaten by wood mice and bank voles in Wytham Woods, Berkshire. J. Animal. Ecol. 37: 25 - 41.
Acknowledgements Thanks are due to Peter Gasson (RBG Kew) for general discussion and for contact information, to Dr Pat Morris for helpful comments, and to Mariko Parslow for taking the photograph.
1Stroma (plural stromata) A stroma comprises sterile or vegetative tissue of a fungus, sometimes intermixed with tissue of the host plant, in, on or beneath which the sporebearing structures of the fungus are developed. The structure and position of stromatic tissue varies greatly according to the type of fungus involved. In many ascomycetes the tissue commonly comprises cells with thickened, blackish, melanised ('carbonised') walls and reduced lumen, as is the case in many Diatrypaceae (including Eutypa), and other families, notably Xylariaceae. In Eutypa, the stroma usually develops in host wood beneath the bark and appears as an effused or widely-spreading blackened, crustlike surface to the wood, the spore-producing perithecia developing in the wood just beneath the blackened surface.
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