Article

The Substrate Associations of Tetraplodon mnioides

rFig. 6. Tetraplodon mnioides on/inside sheep skull, on scree, Helvellyn. F. Cameron From dung to decaying carcases, Fiona Cameron presents the evidence for substrate preference in this charismatic moss with a taste for the macabre n his 2010 article for Field Bryology, John (Smith, 2004), and “found on dung in wet heath O’Reilly raised the issue of substrate-specificity and bog….also grows on animal remains, usually within the Splachnaceae and invited readers the decomposing bones of deer and sheep” Ito share their thoughts and observations on the (Porley & Hodgetts, 2005), and more recently; group. This prompted me to re-examine records “very habitat-specific, growing on the scats of from VC69 (Westmorland and Furness) and carnivores (usually fox), ...in scree and by paths,” subsequently for the UK as a whole, and the (Hodgetts: in Atherton et al. (eds.) 2010). This following represents the results of findings (much poses the question: Is T. mnioides exclusive or delayed!) with particular reference to Tetraplodon inclusive in its requirements? mnioides. Accounts of the substrate and habitat Evidence from the Records: Here and away associations of Tetraplodon mnioides vary widely Preliminary investigation of the total 846 in UK literature and range from “on decaying records held by the British Bryological Society bones, less frequently on dung in bogs, on for Tetraplodon mnioides, from 1773 to 2013 boggy ground, moorland, and in the mountains” (Blockeel et al. 2014), suggests that Tetraplodon

2 FieldBryology No113 | May 15 16 The substrate associations of Tetraplodon mnioides 14 12 10 8 6 4 Number of records of Number 2 0 No detail Scat (fox) Dung Dung Carcase Bone Old skull (unspec.) (cattle) (sheep) (sheep) (sheep)

Substrate Tetraplodon mnioides Splachnum ampullaceum Splachnum sphaericum Splachnum vasculosum rFig. 1. Substrate records of Splachnaceae from VC69 (Westmorland and Furness). can colonise both carrion and dung of various (half of which specify herbivore), with fox scat types, and within a range of macro-habitats. In identified just twice (Fig. 2). Any observations of VC69, all post-2000 records were derived from carrion representing a secondary substrate have my MSc study of Lake District scree vegetation, not been reported. Scree is classified as the single where I encountered T. mnioides apparently most frequent macro-habitat at 27%, followed on sheep remains on a quarter of the 25 screes by mires at 15%, with 14% each for tracks investigated. The single previous entry providing and semi-aquatic habitats, and 8% from mine substrate details in the county also refers to spoil records; the latter of which, all but two carrion (Fig. 1). Nationally, of the total 65 records represent lead, (Fig. 3). 90% and 56% of entries, that list substrate-type, the bones and carcases of respectively, lack any sort of substrate/macro- sheep, rabbits, hares, birds and a garden-shrew habitat information. (!) account for 62% of entries, dung: 31%

2 2 8 Bone (general) 6 Bone/skull (sheep)

Carcase (sheep)

Carcase (bird)

15 Carcase (rabbit/hare) 12 Bird pellets

Dung (general)

Dung (sheep) 3 Dung (deer) 2 3 12 Fox scat rFig. 2. Counts (>1) of substrate-type associated with Tetraplodon minioides, from UK records.

FieldBryology No113 | May15 3 52 53 Bog/mire

Heath 24 Stream/Flush/Lochside 44 12 Rock/Cliffs/Scree

Mine spoil (Lead) 28 Grassland 52 Woodland

Tracks 97 r Fig. 3. Counts (>2) of macro-habitat type associated with Tetraplodon mnioides from UK records

Discussion scat-matrix has been washed away, and some Interpreting the ecological niche of Tetraplodon believe that Tetraplodon can colonise dung mnioides from field records is known to be only when it contains such material (Koponen, problematical (Frisvoll, 1978). The micro- 1990). However, it remains difficult to state site conditions experienced by the moss can with certainty whether a population on bone did be very different from those associated with not first colonise a scat deposited upon it, and the broader macro-habitat recorded, and the conversely, if a population on scat did not first relationships between animal demographics and colonise some small fragment of bone within it. the preferences of T. mnioides are particularly The issue is further complicated by the challenging to define, especially when the source lack of studies examining possible changes in of the primary substrate cannot be identified the requirements of the relatively long-lived and a secondary one might be involved. Tetraplodon mnioides over time, which might Upland paths, for example, can serve as a M1 explain in part why a population can inexplicably for commuting foxes, but wildlife corridors disappear from one year to the next but also are frequented by a range of additional fauna persists for twelve years or more in a particular including predatory birds and their prey, and the spot. Is substrate-type important only during less sure-footed of sheep often meet their demise the colonisation and establishment stage, which beneath the steeper crags on scree, where foxes could account for populations on ephemeral find both accommodation and a ready meal scat? Or is persistence a function of substrate- when pickings are slim. longevity, which would tend to favour bone? Professor Stephen Harris, Head of the UK’s (Koponen, 1990). If the latter, then how do we Mammal Research Unit and fox-specialist, tells explain the records from herbivore dung, which us that foxes are known to mark linear features is usually substantial enough to be recognised and objects of interest including old bones, and with some confidence in the field? often visit repeatedly (pers. comm.), but fox-scat In the peatlands and forests of Alberta, – or the matrix at least - is relatively ephemeral, Canada, Splachnaceae researcher Paul Marino and can disappear within a couple of days during encountered Tetraplodon mnioides primarily in periods of heavy rain; leaching all nutrients association with the droppings of large mammals and rendering the primary substrate virtually during his study of co-existence mechanisms impossible to determine. Fragments of bone and within the group, with results confirming that hair do occasionally persist after the surrounding substrate longevity can play an important role in

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the distribution of this species. He demonstrated bare peat; providing an excellent example of that T. mnioides, T. angustatus, Splachnum these preferences (pers. comm.). ampullaceum and S. luteum all grow equally Interestingly, Marino has never encountered well on both moose and wolf dung in the field Tetraplodon mnioides on (visible) fox-scat during there (Marino, 1991a, 1991b), and found no his Alaskan/Canadian research, despite an evidence to suggest differential performance ofT. abundance of foxes (neither have I, or Harris), but mnioides on the basis of dung-type, i.e. herbivore, neither has he found it on bone, though he states omnivore, or carnivore. However, although that he “would not be at all surprised” to find all four species flourished in both wet and dry Tetraplodon on such substrates (pers. comm.), conditions in the absence of competition (i.e. and includes carrion in his forthcoming account in the laboratory), a significant correlation was of the Splachnaceae in the Bryophyte Flora of established 1) between the rapid decomposition North America (provisional publication online, of dung associated with wetter habitats and the accessed date 2014). Several other Splachnaceae absence of Tetraplodon spp in the wild, and 2) researchers working further south in North between drier habitats with more persistent America (where the species is less common), dung and the rapid disappearance of the short- report that bones and carcases represent an lived Splachnum spp; with the conclusion important substrate type for T. mnioides in their being that it is differences in habitat-moisture areas (Goffinet et al., 2004; Slack, 1990), and regime that shift competitive outcomes between a very convincing argument in support of its these species (Marino, 1991a). Botanist Paul ability to colonise such material directly comes Leadbitter’s photograph (Fig. 5) displays his from Webster’s 1987 study in Scandinavia. As unusual encounter with S. sphaericum and T. far as I am aware, the latter represents the only mnioides growing together, in wet versus dry research to involve mineral/chemical analysis microsites respectively, on a sheep carcase on of both field-collected Splachnaceae and their sFig. 4. Tetraplodon mnioides on scree, Great Gable. F. Cameron

FieldBryology No113 | May15 5 substrates. The Splachnaceae are the only mosses that rely The study, (reported in some detail by on flies for dispersal and there have been several Koponen (1990)), revealed that the tissues of studies investigating the specific range of visual Tetraplodon mnioides and Aplodon wormskioldii and olfactory cues that Tetraplodon mnioides has contained similarly high levels of nitrogen, evolved for attracting suitable fly-vectors. Some phosphorus and calcium, in comparison with of these adaptations appear to further underline those of control mosses and Splachnum spp the ability of this species to colonise carrion. more commonly associated with herbivore dung, Bequaert (1921) remarked that the cushions of and reflected the content of their respective T. mnioides were considerably larger and more substrata. In the case of T. mnioides, these colourful than those of Splachnum, and displayed included; skeletal remains, antlers, the pellets shorter, stiffer setae better able to support of predatory birds and carnivore dung (though larger insects such as blow flies. More recently, see the previous paragraphs). A similar range of Marino (1991b) investigated the fly species substrate types, including dung in general, have visiting Splachnum and Tetraplodon and found been noted by Frisvoll (1978) in Norway, where, that though each received a different mixture of interestingly, the common name for the species species in wet vs. dry locations, within-habitat is “the lemming moss”, due to close association visitor composition overlapped to a large degree. with carcases during “lemming years”. Frey et al. Although he concluded that most of these flies (2006) include carrion in their pan-European were therefore not moss-specific, Marino’s study account, and Goffinetet al. (2004), make further involved only dung substrates, and it remains reference to colonisation of blood-soaked soil. a possibility that populations on carrion might Collaborating frequently with Marino, Goffinet attract a characteristic fly fauna. What is widely places particular emphasis on the tolerance/ accepted is that species of the Splachnaceae requirement of all the Splachnaceae for substrates each emit volatile compounds associated with of high nitrogen-concentrations; an adaptation particular substrate types i.e. S. ampullaceum thought to confer a key competitive advantage and S. sphaericum emit odours resembling urine during the establishment stage in comparison to and faeces, while T. mnioides replicates those of non-coprophilous species. rotting flesh (Slack, 1990) (Fig. 7).

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vFig. 5 (left). Tetraplodon mnioides longevity might be of particular significance. in the upper, drier microsite, Tetraplodon mnioides is a Circumpolar Boreo- (right) and Splachnum arctic Montane moss, and over 60% of UK sphaericum closest to the wet observations are from the Scottish Highlands. All peat, (left) on sheep carcase, Harthope Head, (VC66). North the habitat categories associated with the species Pennines Area of Outstanding achieve their greatest frequency in Scotland, with Natural Beauty. P. Leadbitter the notable exception of two; those of lead mine vFig. 7 (right). Tetraplodon spoil and plantation forestry. Twenty one of the mnioides on sheep carcase, twenty eight records for lead mine spoil refer to on scree, Sprinkling tarn. sites on the orefields of Mid and North Wales F. Cameron (VC44, 46 & 47), with additional localities in Yorkshire, (VC64 & 65), Dumfriesshire, (VC72), and the Wicklow mountains in Ireland Regional variation in substrate/habitat (VC H20), and bryologist Sam Bosanquet association remarks that in parts of Wales this represents In comparison to wind-dispersed species, by far the most significant habitat-type forT. Tetraplodon mnioides is spatially constrained mnioides (pers. comm.). Heavy metal toxicity largely by fly activity, and such limitation is thought to significantly reduce competition is thought likely to result in distinct habitat and also the rate of decomposition of organic associations within the species (Marino, 1988; material, and numbers of UK records for dung Slack, 1990). Differences in the geographical indeed reach a peak on Welsh lead mine spoil. ranges and habitat preferences of the animals Recent research of fox distribution patterns involved in substrate-forming have also been based on faecal counts from field-sites across seen to result in regional resource segregation (or the country has established that densities are patterns of substrate/habitat association that vary positively correlated with coniferous woodland according to locality), within other members of and negatively with Rights of Way access in the the Splachnaceae. Nancy Slack cites the example UK (Webbon et al., 2004); habitats providing of S. rubrum, which became extinct in the ample cover for the small mammals favoured by NewYork/Adirondacks area at the same time foxes during times of plenty. Tetraplodon mnioides as moose in the 19th century, whereas the more has been recorded primarily in association with generalist S. ampullaceum that grows also on disused forestry tracks in Northumberland deer dung was able to persist. Similarly, whereas (VC67), with single records in Wales (VC46), S. luteum is associated with moose, wolf or bear and Caithness (VC108), and 12% of total UK dung in Canada, further south where these species records for T. mnioides were derived from animals do not occur it is found on the droppings repeat surveys of the Caledonian pinewoods of deer (Slack, 1990). Preliminary investigations and moorland of the Abernethy Forest reserve of T. mnioides substrate/habitat frequencies, (VC95 & 96), where the “general tracks” habitat including observations from bryologists working category for the species has also been the most particular areas of the country, suggest that frequently recorded. associations may vary also within the UK, and The majority of entries from Abernethy were factors including local substrate availability and collated by Stewart Taylor over the last decade,

FieldBryology No113 | May15 7 The substrate associations of Tetraplodon mnioides

and though largely unspecified in the BBS scat colonisation in certain areas of Scotland dataset, he communicates that most finds have and carrion really is more frequent in southern indeed been in association with fox or pine localities. marten scat on disused forest tracks (Fig. 8), There is certainly no shortage of carrion on with an additional record from a hare carcase, scree in England and Wales. Stocking rates of and a couple from summit viewpoints he (increasingly unhefted) sheep in England are attributes to possible bird of prey pellets (pers. known to be double or more per hectare than comm.). Significantly perhaps, sheep exclusion- those of Scotland, with 10.8 vs. 4.6 million management has always been in operation total head documented respectively in 2012. In within the woodland sites Taylor surveyed at northern Scotland (as at Abernethy), considerable Abernethy, and as large parts of the surrounding numbers of sheep have been removed or reduced upland moorland have been totally sheep-free in recent decades for local conservation purposes; since the ‘90s, scat is likely to represent the most including peat bog restoration, woodland frequently available substrate type in the locality. regeneration and deer management, and a The second and last remaining entry for fox decline in the raven (whose primary food-source scat substrates in the BBS dataset refers to scree is sheep carrion) was attributed to large-scale within the Cairngorms, and David Genney of afforestation of former sheepwalk in southern SNH has encountered Tetraplodon mnioides Scotland and the North-East in the 1970s, exclusively on scat within other montane habitats (Marquiss et al., 1978), whereas in the Lake in the region, (pers. comm.), but only sheep District the species has continued to flourish. carrion has been reported from scree further Colder temperatures could also prolong the south in the Lake District. Indeed, though 80% shelf-life of scat and dung to the extent that of specified UK scree records refer to carrion, such substrates are favoured at more northerly and despite the greater frequency of T. mnioides latitudes. Walkers in the Cairngorms are in Scotland, observations of this substrate type advised rather pointedly to take away ALL that appear to reach a peak in Westmorland (VC69), they bring when camping on the plateau, as North Wales (VC42) and the Peak District excretions persist and accumulate along popular (VC57), (Fig. 10). routes. Differences in regional climate and the The extent to which recorder activity way it affects substrate longevity might also contributes to this pattern remains unclear, and explain the similar contrasts that occur between there are a number of additional factors which Tetraplodon association patterns in Canada could be significant. Substrate information is versus North America. Additionally, the greater rarely collated during the large-scale surveys temporal/spatial separation between populations frequently undertaken in Scotland, where of T. mnioides in marginal areas where it is less carnivore scat is widely considered to represent common might be resulting in fewer instances of the only possible substrate, and BBS recording successful colonisation of ephemeral substrates, cards do not require detailed information for and a tendency of the species to favour more common species, whereas a rare one in England substantial and persistent ones in England and and Wales might be more fully described. But Wales? But this remains largely conjecture. perhaps higher numbers of unspecified records Perhaps more definitive evidence of regional could imply greater prevalence of ephemeral resource segregation within Tetraplodon

8 FieldBryology No113 | May 15 mnioides and indeed of the ecological amplitude of the species in relation to substrate association, comes from the frequency of records from the islands and archipelagos off Scotland’s northern coastline. The BBS dataset contains thirty records in total for T. mnioides on the islands of Arran, Mull, Rum, Raasay, Harris, Orkney, Shetland, and the sea-stack of the Old Man of Stoer, but foxes are known to be entirely absent from all these localities, and only on Mull has a population of (non-native) pine martens been recently documented. A small rFig. 8. top. Tetraplodon mnioides on fox/pine marten scat: number of stoats have been sighted on Mull, track sides within the Abernethy Forest Reserve. S. Taylor Shetland and Raasay, but the recent introduction NB: the maximum diameter of scats were 5 to 6cm vs. of the North American mink to Harris has been the 30cm+ of populations on carrion, recorded elsewhere, just as quickly eradicated. Arran, Rum, Orkney (e.g. Fig. 7). (where T. mnioides has been found sixteen times) rFig. 9. bottom. Tetraplodon mnioides on the carcase of a in addition to numerous other small islands are hare in the Abernethy Forest Reserve. S. Taylor. NB: No thought to be entirely free of these carnivores. trace of fox scat was detected and cover of T. mnioides was widespread, indicating multiple developmental stages. Birds of prey pellets would seem likely to represent a particularly frequent substrate-type of deer; the latter representing in fact, the only in such areas, but during surveys of the smaller terrestrial mammal of significant size in these Outer Hebridean islands, where sheep are absent localities (pers. comm.). or much reduced, bryologist Martin Godfrey The substrate associations of Tetraplodon has regularly encountered Tetraplodon mnioides mnioides could thus reflect the availability of exclusively in association with the droppings particular animals (or birds) within the wider

FieldBryology No113 | May15 9 rFig. 10. Tetraplodon mnioides: Counts of sheep carrion substrates according to Vice County, (mainland Britain).

landscape, with the implication that there is an the specific traits currently used to distinguish element of opportunism in relation to T. mnioides the species (Lewis et al. 2014). Frisvoll (1978) colonisation, and several of the more unusual describes three varieties within “the T. mnioides records might support this. There are a number complex”, a hybrid with T. angustatus and of entries for bird skeletons beneath pylons and considerable phenotypic and possible additional powerlines, one for sludge of indeterminate genotypic variation in his taxonomic revision organic origin at the bottom of a plastic bucket, from Norway, and a further six species within one report of human excrement from the scene of the genus are known to occur in Scandinavia and a former rave (!) in addition to a rather worrying the Alps (Frey et al. 2006). Endemics previously one from a cemetery... But another intriguing classified as T. mnioides have been described speculation, and one that might be implied by from both Scandinavia, (Frisvoll, 1978), and taxonomic research from other parts of Europe the Americas (Steere, 1977), but only one other and beyond, is the possibility that such regional species of Tetraplodon is known from the UK, variation could also indicate more substantial and as yet no varieties have been described. differences within the species. Present on all continents except Australia and Conclusion New Zealand, Tetraplodon mnioides exhibits A wide range of often interacting factors the most widespread distribution and most including substrate, habitat, dispersal ability/fly extreme disjunctions of all the Splachnaceae, vector activity and distance to source-population and considerable variation has been documented are thought to contribute to the distribution of within the species at a global scale. Recent research Tetraplodon mnioides, with one or more factors of the phylogenetic lineage of Tetraplodon has often varying in importance, and modelling revealed that it consists of three distinct clades such dynamics is currently the focus of that display broadly overlapping geographical Marino’s research team at Memorial University, distributions but that apparently do not match Newfoundland. T. mnioides would appear to be up with the taxa under our morphological generalist in its macro-habitat preferences (though species concept; highlighting the variability of this is clearly linked to animal demographics),

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but specific in the requirement for nitrogen-rich, British Bryological Society. dry microsites as a result of its physiology, life- Koponen, A. (1990). Entomophily in the Splachnaceae. cycle and adaptations for competitive survival. Botanical Journal of the Linnaean Society 104: 115-127. Fox scat and other comparatively ephemeral Lewis, L., Rozzi, R. & Goffinet, B. (2014). Direct long- substrates are undoubtedly under-represented distance dispersal shapes a new world amphitropical within our records, but additional surveys disjunction in the dispersal-limited dung-moss Tetraplodon (Bryopsida: Splachnaceae). Journal of Biogeography 41:2385- including chemical analyses are required if we are 2395 to determine the relative importance of carrion Marquiss, M., Newton, I. & Ratcliffe, D.A. (1978).The vs. dung and scat and its contents as primary decline of the Raven, Corvus corax, in relation to afforestation substrates for the species. There is considerable in Southern Scotland and Northern England. Journal of evidence both within the UK and further afield Applied Ecology 15: 129-144 to suggest the broad ecological amplitude of Marino, P.C. (1988). The North American distributions of Tetraplodon mnioides in relation to substrate the circumboreal species of Splachnum and Tetraplodon. The association, and preferences here could well be Bryologist 91: 161-166. regionally distinct. Marino, P.C. (1991a). Competition between mosses (Splachnaceae) in patchy habitats. Journal of Ecology 79: Acknowledgements 1031-1046. Thank you to Paul Marino, Stephen Harris and Stewart Taylor Marino, P.C. (1991b). Dispersal and coexistence of mosses for sharing their knowledge and experience, to Christopher (Splachnaceae) in patchy habitats. Journal of Ecology 79: Preston, Sam Bosanquet and John O’Reilly for proof-reading 1047-1060. the article and for their invaluable advice, and a special thank O’Reilly, J. (2010). Changing patterns in frequency of the you to Martin Godfrey for his help locating some of the more coprophilous/necrophilous mosses in Northern England obscure papers! and some notes on forestry tracks. Field Bryology 101: 5-7 Porley, R. & Hodgetts, N. (2005). Mosses and Liverworts (New References Naturalist Series No. 97) London: HarperCollins. Bequaert, J. (1921). On the dispersal by flies of the spores of Slack, N.G. (1990). Bryophytes and ecological niche theory. certain mosses of the family Splachnaceae. Bryologist 24: 1-4. Botanical Journal of the Linnean Society 104: 187-213. Blockeel, T.L., Bosanquet, S.D.S., Hill, M.O. & Preston, Smith, A.J.E. (2004). The moss flora of Britain and Ireland,nd 2 C. D. (eds.) (2014). Atlas of British and Irish Bryophytes. edn. Cambridge: Cambridge University Press. Newbury: Pisces Publications. Steere, W.C. (1977). Tetraplodon paradoxus and T. pallidus Frey, W. Frahm, J.-P., Fischer, E. & Lobin, W. (2006). (Musci: Splachnaceae) in North America. Brittonia 29: 353- The liverworts, mosses and ferns of Europe. Harley Books. 367. Colchester. Webbon, C., Baker, J. & Harris, S. (2004). Faecal density Frisvoll, A.A. (1978). The genus Tetraplodon in Norway. A counts for monitoring changes in red fox numbers in rural taxonomic revision. Lindbergia 4: 225-246. Britain. Journal of Applied Ecology 41: 718-779. Goffinet, B., Shaw, A.J. & Cox, C.J. (2004). Phylogenetic Webster, H.J. (1987). Elemental analysis of dung mosses inferences in the dung-moss family Splachnaceae from (Splachnaceae) and their substrates. Memoirs of the New York analysis of CPDNA sequence data and implications for the Botanical Garden 45: 171-178. evolution of entomophily. American Journal of Botany 91: 748-759. Atherton, I., Bosanquet, S. & Lawley, M. (eds.) (2010). Fiona Cameron 4 Yard 18, Kirkland, Kendal, LA95AD Mosses and Liverworts of Britain and Ireland: a field guide. e. [email protected]

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