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Sporophyte odours identified from Northern Hemisphere Splachnaceae. Numbers in parentheses are the number of distinct volatile compounds identified per species. A. 1-octene-3-ol and 3-octanone common to peat moss and mushrooms. B. 6-methyl-5-hepten-2- one and -ol, derived from carotenoids. C. Butanoic acid and other short-chain fermentation products. D. cyclohexane carboxylic acid esters and heptanal, both common to mammalian urine. E. Dimethyl disulfide and -trisulfide, common to rotting flesh. F. Indole, G. Phenol and cresol, all common to herbivore dung. H. 2-phenyl ethanol and benzyl alcohol; floral odours. Photos of S. sphaericum and T. mnioides ©B. Goffinet; others ©R.A. Raguso.
Source publication
The use of sensory attractants is central to most animal-mediated pollination and seed dispersal interactions. Approximately
half the 73 species of mosses’ in the family Splachnaceae are entomophilous (have their spores dispersed by flies) and are
coprophilous (grow on feces and carrion). When mature, entomophilous species often produce brightly co...
Contexts in source publication
Context 1
... ) only on Tetraplodon mnioides , which, unlike Splachnum species, typically colonize carnivore dung in dry habitats (Marino, 1988a; 1991a). Lucilia are attracted to dimethyl disulfide and similar sulfurous compounds emitted by rotting meat and by flowers that mimic carrion (Borg-Karlson et al., 1994; Patiño et al., 2000; Stensmyr et al., 2002). Thus, either the sporophytes of T. mnioides or their substrates should emit oligosulfides. In contrast, the brightly coloured, parasol-like sporophytes of S. ampullaceum and S. luteum attract more diverse fly spectra, including pollen and nectar-feeding anthomyiids (Marino, 1991b). Several lines of evidence reviewed above (see Fig. 4a) suggest that interspecific variation in sporophyte odour chemistry should be found in the Splachnaceae. Pyysalo et al. (1978) extracted sporophyte volatiles from several species of entomophilous Splachnaceae in Finland using pentane and diethyl ether solvents for analysis with gas chromatography-mass spectrometry (GC- MS). They identified a series of sour-smelling organic acids (in Splachnum vasculosum, Tetraplodon mnioides and Tayloria tenuis ) and mushroom-scented octane-derived alcohols and ketones (particularly in Splachnum luteum ), whereas no volatiles were detected from sporophytes of Tayloria lingulata , an anemophilous species collected from the same habitats as their target species. A follow up study by the same authors (Pyysalo et al., 1983), collected volatiles from intact and dissected sporophytes of three boreal species, Splachnum sphaericum, S. vasculosum and Aplodon wormskioldii . They localized octanol and octanone production to the setae of each species, with species- specific organic acids (e.g. benzoic acid) and alcohols (e.g. benzyl alcohol) present in the apophyses. Their studies confirmed that volatiles could be identified from sporophytes of entomophilous species, blend compositions probably are distinct enough to promote vector specialization, and scent emissions are localized to the part of the sporophyte most likely to affect spore transfer to the body of an insect visitor. However, solvent extraction of cut plant material frequently produces artifacts associated with plant wounding (Raguso and Pellmyr, 1998; Dobson et al., 2005), Thus, odour chemistry in the Splachnaceae must be studied using less invasive methods, in which odours emitted by live, intact plants equilibrate in small “headspace” chambers, adsorb onto the surface of solid phase microextraction (SPME) fibres, and are desorbed directly onto the GC column for GC-MS analysis (see Dafni et al., 2005 for details). To date, we have collected volatiles from several North American ( T. mnioides, S. ampullaceum, S. luteum, S. pensylvanicum, S. rubrum and S. sphaericum ), South American ( Tetraplodon fuegiensis, Tayloria dubyi and T. mirabilis ) and Australasian ( Tayloria gunnii and T. octablepharum ) species of Splachnaceae using living sporophytes and gametophytes growing on mammal dung and bone collected in the field and transported to analytical chemistry laboratories for analysis. First, we collected total volatiles from small populations (50–100) of living sporo- phytes placed within small headspace chambers as described by Raguso et al. (2003) (see also Dafni et al., 2005). Additional samples were collected simultaneously from moss substrates and non-Splachnaceae mosses that were present, to control for background odours. Second, we determined the sources of different volatiles by separating sporophytes from gametophytes (up to 50 per species whenever possible) and further dissecting sporophytes into setae and apophyses + capsules. Our analyses of scent chemistry identified informative patterns on several levels. Haploid and diploid generations of the moss differ in their odours with gametophytes were either unscented or weakly scented in most species. When odours were present in gametophyte tissue, they were chemically restricted to two classes: sesquiterpenoid hydrocarbons (ubiquitous in terrestrial plants) and the octane-derived odours identified by Pyysalo et al. (1978). The octanols and octanones also were present in gametophytes of Sphagnum and an outgroup, Pleurozium schreberi , and thus constitute background odours in the habitats we studied. In contrast, sporophyte odours were universally stronger per unit mass and more chemically complex. With the exception of T. mnioides , the apophyses + capsules were the primary sources of sporophytic odours, again consistent with the findings of Pyysalo et al. (1983). All substrates tested were scentless, as we would expect given that Splachnaceae sporulate during the second year after protonemal germination, by which time substrates are no longer in a state of decay. Sporophyte odours among North American species are complex and diverse, with an apparent inverse relationship between the size and showiness of the apophysis and its odour complexity (Fig. 5). For example, the small, brownish coloured apophyses of Splachnum sphaericum constitute one of the least visually conspicuous sporophytes in their genus, but emit over 50 volatiles from several biosynthetic classes (Fig. 5), with specific compounds indicative of fermenting sugar, floral odours, herbivore feces and, remarkably, moose urine (see Whittle et al., 2000). At the opposite extreme were the large, bright yellow sporophytes of S. luteum , whose odour consisted of little more than fungal octane-derivatives plus trace levels of butanoic acid and indole, a nitrogenous compound common to night-blooming flowers (Kaiser, 1993) and bacterial metabolism of feces (Jürgens et al., 2006). Sporophytes of the closely related S. rubrum are similar in size to those of S. luteum , but are almost iridescent ruby-red in colour (see Fig. 5) and emit a uniquely pungent blend of odours. These compounds, which include indole and phenol (herbivore feces), benzyl alcohol and 2-phenylethanol (flowers) and the alcohols and esters of propanoic and butanoic acids (fermenting sugar), seemingly represent a generalized strategy of targeting diverse spore vectors attracted to a broad spectrum of foods or hosts; however, all of these compounds can be found in cow dung (Kite, 1995). As predicted from fly visitation records, Tetraplodon mnioides was the only species found to emit dimethyl disulfide, a known indicator of carrion and carnivore dung, and a universal attractant of calliphorid flies (Stensmyr et al., 2002; Jürgens et al., 2006). Dissections consistently identified setae, rather than apophyses, as the source of sulphurous volatiles in Tetraplodon sporophytes. Another pattern emerging from our studies is that populations of related species sometimes grow intermixed on the same droppings where their geographic ranges are sympatric (Marino, 1988b). The frequent co-occurrence of S. luteum and S. sphaericum on individual droppings combined with the dramatic difference between the two species in visual vs. olfactory display, respectively, is suggestive of a mutually advantageous relationship with respect to spore dispersal. In contrast, in eastern Newfoundland, Canada S. ampullaceum with its large, yellowish sporophytes grows sympatrically and often in mixed populations on the same droppings with S. pensylvanicum which has relatively tiny reddish sporophytes yet both species produce strong, although very different, scents. Manipulative field experiments would elucidate the extent (if any) to which these related species- pairs benefit from each other’s presence in mixed populations. Sporophyte odours from a smaller sample of Southern Hemisphere species suggested similar themes of generational contrast and chemical mimicry through the emission of sporophyte-specific volatile compounds. Tayloria mirabilis was found growing on cow dung in the understory of Nothofagus forest on Isla Navarino, in Patagonian Chile. Its pearl-like greenish white apophyses emitted a simple, fetid blend of phenol, cresol and indole indicative of cow feces (Kite, 1995). The related but much less conspicuous T. dubyi was found growing on goose dung on hummocks of Sphagnum moss in exposed peat bogs. The spindle-shaped, burgundy coloured sporophytes of T. dubyi emitted a sharply unpleasant, fecal blend of phenol, cresols and methyl p-cresol with smaller amounts of indole. Populations of Tetraplodon fuegiensis were found in the same peat bogs as Tayloria dubyi but were restricted to fox feces and bone substrates. As was found for its relatives half a planet away, the sporophyte odour of T. fuegiensis was dominated by sulphurous volatiles (dimethyl disulfide and trisulfide) consistent with a strategy of carrion mimicry. All three taxa emitted octane-derived compounds from all parts and complex sesquiterpenoid blends from gametophytic tissues. The closest extant relatives of the Patagonian Taylorias are found in Tasmania and New Zealand (see below). Remarkably, two of these putatively entomophilous species, Tayloria gunnii and T. octablepharum , were found to emit different ratios of phenol, p-cresol and indole, as well as octane-derivatives and organic acids from their apophyses. Together, the findings described above, however preliminary, suggest that chemical mimicry of herbivore dung is a common strategy for spore dispersal within and between lineages of entomophilous Splachnaceae, effective at high latitudes of Northern and Southern Hemispheres, wherever large populations of herbivores and their attendant fly faunas flourish. Our data suggest that fly trapping experiments comparing synthetic blends of sporophyte odours with positive controls of closely related species in different microhabitats can help to determine the relative contribution of species-specific odour blends to substrate limitation and reduced competition among Splachnaceae. What we lack at present is a comparative study in which sporophyte architecture and chemistry are ...
Context 2
... disulfide and similar sulfurous compounds emitted by rotting meat and by flowers that mimic carrion (Borg-Karlson et al., 1994; Patiño et al., 2000; Stensmyr et al., 2002). Thus, either the sporophytes of T. mnioides or their substrates should emit oligosulfides. In contrast, the brightly coloured, parasol-like sporophytes of S. ampullaceum and S. luteum attract more diverse fly spectra, including pollen and nectar-feeding anthomyiids (Marino, 1991b). Several lines of evidence reviewed above (see Fig. 4a) suggest that interspecific variation in sporophyte odour chemistry should be found in the Splachnaceae. Pyysalo et al. (1978) extracted sporophyte volatiles from several species of entomophilous Splachnaceae in Finland using pentane and diethyl ether solvents for analysis with gas chromatography-mass spectrometry (GC- MS). They identified a series of sour-smelling organic acids (in Splachnum vasculosum, Tetraplodon mnioides and Tayloria tenuis ) and mushroom-scented octane-derived alcohols and ketones (particularly in Splachnum luteum ), whereas no volatiles were detected from sporophytes of Tayloria lingulata , an anemophilous species collected from the same habitats as their target species. A follow up study by the same authors (Pyysalo et al., 1983), collected volatiles from intact and dissected sporophytes of three boreal species, Splachnum sphaericum, S. vasculosum and Aplodon wormskioldii . They localized octanol and octanone production to the setae of each species, with species- specific organic acids (e.g. benzoic acid) and alcohols (e.g. benzyl alcohol) present in the apophyses. Their studies confirmed that volatiles could be identified from sporophytes of entomophilous species, blend compositions probably are distinct enough to promote vector specialization, and scent emissions are localized to the part of the sporophyte most likely to affect spore transfer to the body of an insect visitor. However, solvent extraction of cut plant material frequently produces artifacts associated with plant wounding (Raguso and Pellmyr, 1998; Dobson et al., 2005), Thus, odour chemistry in the Splachnaceae must be studied using less invasive methods, in which odours emitted by live, intact plants equilibrate in small “headspace” chambers, adsorb onto the surface of solid phase microextraction (SPME) fibres, and are desorbed directly onto the GC column for GC-MS analysis (see Dafni et al., 2005 for details). To date, we have collected volatiles from several North American ( T. mnioides, S. ampullaceum, S. luteum, S. pensylvanicum, S. rubrum and S. sphaericum ), South American ( Tetraplodon fuegiensis, Tayloria dubyi and T. mirabilis ) and Australasian ( Tayloria gunnii and T. octablepharum ) species of Splachnaceae using living sporophytes and gametophytes growing on mammal dung and bone collected in the field and transported to analytical chemistry laboratories for analysis. First, we collected total volatiles from small populations (50–100) of living sporo- phytes placed within small headspace chambers as described by Raguso et al. (2003) (see also Dafni et al., 2005). Additional samples were collected simultaneously from moss substrates and non-Splachnaceae mosses that were present, to control for background odours. Second, we determined the sources of different volatiles by separating sporophytes from gametophytes (up to 50 per species whenever possible) and further dissecting sporophytes into setae and apophyses + capsules. Our analyses of scent chemistry identified informative patterns on several levels. Haploid and diploid generations of the moss differ in their odours with gametophytes were either unscented or weakly scented in most species. When odours were present in gametophyte tissue, they were chemically restricted to two classes: sesquiterpenoid hydrocarbons (ubiquitous in terrestrial plants) and the octane-derived odours identified by Pyysalo et al. (1978). The octanols and octanones also were present in gametophytes of Sphagnum and an outgroup, Pleurozium schreberi , and thus constitute background odours in the habitats we studied. In contrast, sporophyte odours were universally stronger per unit mass and more chemically complex. With the exception of T. mnioides , the apophyses + capsules were the primary sources of sporophytic odours, again consistent with the findings of Pyysalo et al. (1983). All substrates tested were scentless, as we would expect given that Splachnaceae sporulate during the second year after protonemal germination, by which time substrates are no longer in a state of decay. Sporophyte odours among North American species are complex and diverse, with an apparent inverse relationship between the size and showiness of the apophysis and its odour complexity (Fig. 5). For example, the small, brownish coloured apophyses of Splachnum sphaericum constitute one of the least visually conspicuous sporophytes in their genus, but emit over 50 volatiles from several biosynthetic classes (Fig. 5), with specific compounds indicative of fermenting sugar, floral odours, herbivore feces and, remarkably, moose urine (see Whittle et al., 2000). At the opposite extreme were the large, bright yellow sporophytes of S. luteum , whose odour consisted of little more than fungal octane-derivatives plus trace levels of butanoic acid and indole, a nitrogenous compound common to night-blooming flowers (Kaiser, 1993) and bacterial metabolism of feces (Jürgens et al., 2006). Sporophytes of the closely related S. rubrum are similar in size to those of S. luteum , but are almost iridescent ruby-red in colour (see Fig. 5) and emit a uniquely pungent blend of odours. These compounds, which include indole and phenol (herbivore feces), benzyl alcohol and 2-phenylethanol (flowers) and the alcohols and esters of propanoic and butanoic acids (fermenting sugar), seemingly represent a generalized strategy of targeting diverse spore vectors attracted to a broad spectrum of foods or hosts; however, all of these compounds can be found in cow dung (Kite, 1995). As predicted from fly visitation records, Tetraplodon mnioides was the only species found to emit dimethyl disulfide, a known indicator of carrion and carnivore dung, and a universal attractant of calliphorid flies (Stensmyr et al., 2002; Jürgens et al., 2006). Dissections consistently identified setae, rather than apophyses, as the source of sulphurous volatiles in Tetraplodon sporophytes. Another pattern emerging from our studies is that populations of related species sometimes grow intermixed on the same droppings where their geographic ranges are sympatric (Marino, 1988b). The frequent co-occurrence of S. luteum and S. sphaericum on individual droppings combined with the dramatic difference between the two species in visual vs. olfactory display, respectively, is suggestive of a mutually advantageous relationship with respect to spore dispersal. In contrast, in eastern Newfoundland, Canada S. ampullaceum with its large, yellowish sporophytes grows sympatrically and often in mixed populations on the same droppings with S. pensylvanicum which has relatively tiny reddish sporophytes yet both species produce strong, although very different, scents. Manipulative field experiments would elucidate the extent (if any) to which these related species- pairs benefit from each other’s presence in mixed populations. Sporophyte odours from a smaller sample of Southern Hemisphere species suggested similar themes of generational contrast and chemical mimicry through the emission of sporophyte-specific volatile compounds. Tayloria mirabilis was found growing on cow dung in the understory of Nothofagus forest on Isla Navarino, in Patagonian Chile. Its pearl-like greenish white apophyses emitted a simple, fetid blend of phenol, cresol and indole indicative of cow feces (Kite, 1995). The related but much less conspicuous T. dubyi was found growing on goose dung on hummocks of Sphagnum moss in exposed peat bogs. The spindle-shaped, burgundy coloured sporophytes of T. dubyi emitted a sharply unpleasant, fecal blend of phenol, cresols and methyl p-cresol with smaller amounts of indole. Populations of Tetraplodon fuegiensis were found in the same peat bogs as Tayloria dubyi but were restricted to fox feces and bone substrates. As was found for its relatives half a planet away, the sporophyte odour of T. fuegiensis was dominated by sulphurous volatiles (dimethyl disulfide and trisulfide) consistent with a strategy of carrion mimicry. All three taxa emitted octane-derived compounds from all parts and complex sesquiterpenoid blends from gametophytic tissues. The closest extant relatives of the Patagonian Taylorias are found in Tasmania and New Zealand (see below). Remarkably, two of these putatively entomophilous species, Tayloria gunnii and T. octablepharum , were found to emit different ratios of phenol, p-cresol and indole, as well as octane-derivatives and organic acids from their apophyses. Together, the findings described above, however preliminary, suggest that chemical mimicry of herbivore dung is a common strategy for spore dispersal within and between lineages of entomophilous Splachnaceae, effective at high latitudes of Northern and Southern Hemispheres, wherever large populations of herbivores and their attendant fly faunas flourish. Our data suggest that fly trapping experiments comparing synthetic blends of sporophyte odours with positive controls of closely related species in different microhabitats can help to determine the relative contribution of species-specific odour blends to substrate limitation and reduced competition among Splachnaceae. What we lack at present is a comparative study in which sporophyte architecture and chemistry are characterized for key sister and outgroup species as well as members of the putatively anemophilous lineages of Splachnaceae. The classification and hence the intuitive phylogenetic relationships among mosses have historically been ...
Context 3
... et al. (1978) extracted sporophyte volatiles from several species of entomophilous Splachnaceae in Finland using pentane and diethyl ether solvents for analysis with gas chromatography-mass spectrometry (GC- MS). They identified a series of sour-smelling organic acids (in Splachnum vasculosum, Tetraplodon mnioides and Tayloria tenuis ) and mushroom-scented octane-derived alcohols and ketones (particularly in Splachnum luteum ), whereas no volatiles were detected from sporophytes of Tayloria lingulata , an anemophilous species collected from the same habitats as their target species. A follow up study by the same authors (Pyysalo et al., 1983), collected volatiles from intact and dissected sporophytes of three boreal species, Splachnum sphaericum, S. vasculosum and Aplodon wormskioldii . They localized octanol and octanone production to the setae of each species, with species- specific organic acids (e.g. benzoic acid) and alcohols (e.g. benzyl alcohol) present in the apophyses. Their studies confirmed that volatiles could be identified from sporophytes of entomophilous species, blend compositions probably are distinct enough to promote vector specialization, and scent emissions are localized to the part of the sporophyte most likely to affect spore transfer to the body of an insect visitor. However, solvent extraction of cut plant material frequently produces artifacts associated with plant wounding (Raguso and Pellmyr, 1998; Dobson et al., 2005), Thus, odour chemistry in the Splachnaceae must be studied using less invasive methods, in which odours emitted by live, intact plants equilibrate in small “headspace” chambers, adsorb onto the surface of solid phase microextraction (SPME) fibres, and are desorbed directly onto the GC column for GC-MS analysis (see Dafni et al., 2005 for details). To date, we have collected volatiles from several North American ( T. mnioides, S. ampullaceum, S. luteum, S. pensylvanicum, S. rubrum and S. sphaericum ), South American ( Tetraplodon fuegiensis, Tayloria dubyi and T. mirabilis ) and Australasian ( Tayloria gunnii and T. octablepharum ) species of Splachnaceae using living sporophytes and gametophytes growing on mammal dung and bone collected in the field and transported to analytical chemistry laboratories for analysis. First, we collected total volatiles from small populations (50–100) of living sporo- phytes placed within small headspace chambers as described by Raguso et al. (2003) (see also Dafni et al., 2005). Additional samples were collected simultaneously from moss substrates and non-Splachnaceae mosses that were present, to control for background odours. Second, we determined the sources of different volatiles by separating sporophytes from gametophytes (up to 50 per species whenever possible) and further dissecting sporophytes into setae and apophyses + capsules. Our analyses of scent chemistry identified informative patterns on several levels. Haploid and diploid generations of the moss differ in their odours with gametophytes were either unscented or weakly scented in most species. When odours were present in gametophyte tissue, they were chemically restricted to two classes: sesquiterpenoid hydrocarbons (ubiquitous in terrestrial plants) and the octane-derived odours identified by Pyysalo et al. (1978). The octanols and octanones also were present in gametophytes of Sphagnum and an outgroup, Pleurozium schreberi , and thus constitute background odours in the habitats we studied. In contrast, sporophyte odours were universally stronger per unit mass and more chemically complex. With the exception of T. mnioides , the apophyses + capsules were the primary sources of sporophytic odours, again consistent with the findings of Pyysalo et al. (1983). All substrates tested were scentless, as we would expect given that Splachnaceae sporulate during the second year after protonemal germination, by which time substrates are no longer in a state of decay. Sporophyte odours among North American species are complex and diverse, with an apparent inverse relationship between the size and showiness of the apophysis and its odour complexity (Fig. 5). For example, the small, brownish coloured apophyses of Splachnum sphaericum constitute one of the least visually conspicuous sporophytes in their genus, but emit over 50 volatiles from several biosynthetic classes (Fig. 5), with specific compounds indicative of fermenting sugar, floral odours, herbivore feces and, remarkably, moose urine (see Whittle et al., 2000). At the opposite extreme were the large, bright yellow sporophytes of S. luteum , whose odour consisted of little more than fungal octane-derivatives plus trace levels of butanoic acid and indole, a nitrogenous compound common to night-blooming flowers (Kaiser, 1993) and bacterial metabolism of feces (Jürgens et al., 2006). Sporophytes of the closely related S. rubrum are similar in size to those of S. luteum , but are almost iridescent ruby-red in colour (see Fig. 5) and emit a uniquely pungent blend of odours. These compounds, which include indole and phenol (herbivore feces), benzyl alcohol and 2-phenylethanol (flowers) and the alcohols and esters of propanoic and butanoic acids (fermenting sugar), seemingly represent a generalized strategy of targeting diverse spore vectors attracted to a broad spectrum of foods or hosts; however, all of these compounds can be found in cow dung (Kite, 1995). As predicted from fly visitation records, Tetraplodon mnioides was the only species found to emit dimethyl disulfide, a known indicator of carrion and carnivore dung, and a universal attractant of calliphorid flies (Stensmyr et al., 2002; Jürgens et al., 2006). Dissections consistently identified setae, rather than apophyses, as the source of sulphurous volatiles in Tetraplodon sporophytes. Another pattern emerging from our studies is that populations of related species sometimes grow intermixed on the same droppings where their geographic ranges are sympatric (Marino, 1988b). The frequent co-occurrence of S. luteum and S. sphaericum on individual droppings combined with the dramatic difference between the two species in visual vs. olfactory display, respectively, is suggestive of a mutually advantageous relationship with respect to spore dispersal. In contrast, in eastern Newfoundland, Canada S. ampullaceum with its large, yellowish sporophytes grows sympatrically and often in mixed populations on the same droppings with S. pensylvanicum which has relatively tiny reddish sporophytes yet both species produce strong, although very different, scents. Manipulative field experiments would elucidate the extent (if any) to which these related species- pairs benefit from each other’s presence in mixed populations. Sporophyte odours from a smaller sample of Southern Hemisphere species suggested similar themes of generational contrast and chemical mimicry through the emission of sporophyte-specific volatile compounds. Tayloria mirabilis was found growing on cow dung in the understory of Nothofagus forest on Isla Navarino, in Patagonian Chile. Its pearl-like greenish white apophyses emitted a simple, fetid blend of phenol, cresol and indole indicative of cow feces (Kite, 1995). The related but much less conspicuous T. dubyi was found growing on goose dung on hummocks of Sphagnum moss in exposed peat bogs. The spindle-shaped, burgundy coloured sporophytes of T. dubyi emitted a sharply unpleasant, fecal blend of phenol, cresols and methyl p-cresol with smaller amounts of indole. Populations of Tetraplodon fuegiensis were found in the same peat bogs as Tayloria dubyi but were restricted to fox feces and bone substrates. As was found for its relatives half a planet away, the sporophyte odour of T. fuegiensis was dominated by sulphurous volatiles (dimethyl disulfide and trisulfide) consistent with a strategy of carrion mimicry. All three taxa emitted octane-derived compounds from all parts and complex sesquiterpenoid blends from gametophytic tissues. The closest extant relatives of the Patagonian Taylorias are found in Tasmania and New Zealand (see below). Remarkably, two of these putatively entomophilous species, Tayloria gunnii and T. octablepharum , were found to emit different ratios of phenol, p-cresol and indole, as well as octane-derivatives and organic acids from their apophyses. Together, the findings described above, however preliminary, suggest that chemical mimicry of herbivore dung is a common strategy for spore dispersal within and between lineages of entomophilous Splachnaceae, effective at high latitudes of Northern and Southern Hemispheres, wherever large populations of herbivores and their attendant fly faunas flourish. Our data suggest that fly trapping experiments comparing synthetic blends of sporophyte odours with positive controls of closely related species in different microhabitats can help to determine the relative contribution of species-specific odour blends to substrate limitation and reduced competition among Splachnaceae. What we lack at present is a comparative study in which sporophyte architecture and chemistry are characterized for key sister and outgroup species as well as members of the putatively anemophilous lineages of Splachnaceae. The classification and hence the intuitive phylogenetic relationships among mosses have historically been drawn primarily from variation in the architecture of the sporophyte (e.g., Brotherus, 1924; Vitt, 1984). In essence, the moss capsule is to the bryologist what the flower is to the angiosperm systematist. Splachnaceae differ most conspicuously from one another in the aspects of their capsule. Their leafy stems are orthotropic, scarcely if at all branched and their leaves, which compose heteroblastic series along the stem, vary in their shape and ...
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... Nevertheless, all species grew well when grown alone from spores on droppings in wet habitats. Thus, although Splachnum spp. may be physiologically restricted from colonizing dung in dry habitats, Tetraplodon spp. were either excluded from dung in wet habitats by Splachnum spp. or were restricted from dung in wet habitats by dispersal constraints. As the chemistry of droppings also differs between dry and wet habitats, these habitat-sensitive growth differences between genera may result from differences in moisture availability and the chemistry of droppings (Marino, 1991a). Are different species of Splachnaceae associated with particular types of dung? There is observational evidence suggesting non-random substrate utilization in the field, although not in the laboratory (Marino, 1991a). For example in the field, T. mnioides (Alaska, Alberta and Labrador) has always been found growing on carnivore or omnivore droppings whereas S. ampullaceum (Alberta; Isle Royale, Michigan; Newfoundland, Labrador) has always been found growing on herbivore droppings (Marino, pers. obs.). In Chilean Patagonia, Tayloria mirabilis was found growing on cattle dung (Goffinet et al., 2006), Tayloria dubyi on goose droppings (Jofre, 2007) and Tetraplodon fuegiensis on carnivore droppings (Marino et al., pers. obs.; Fig. 2). Both spore germination and protonemal development appear to be influenced by pH (Armentano and Caponetti, 1972; Cameron and Wyatt, 1989) although this early growth stage sensitivity to pH does not result in substrate restriction (Marino, 1997). The fact that several species appear to be restricted to specific types of droppings in the wild, but are capable of initiating spore germination and gametophyte growth on various types of droppings and levels of pH suggests that directed spore dispersal by different flies may play a critical role in the observed patterns of substrate restriction. Several further observations suggest that directed spore dispersal may promote substrate restriction among entomophilous Splachnaceae. First, sympatric species of Splachnaceae vary greatly in the fly faunas that they attract (Marino, 1991b) (Table 2; Fig. 3). Second, the fragrances emitted by the mature sporophytes of Splachnaceae differ greatly in chemical composition with different species emitting odours characteristic of either carrion or dung (see below). Taken together these observations suggest that specific species of Splachnaceae and specific substrate types are likely attracting relatively distinct guilds of flies, which may in part explain the observed substrate restriction among various species of Splachnaceae. Koponen and Koponen (1977) trapped flies in Finland using traps baited with the sporophytes of S. ampullaceum and S. luteum, S. vasculosum and T. mnioides and using non-baited control traps. Traps baited with Splachnaceae captured 92 coprophilous flies (families Sepsidae, Scatophagidae, Muscidae and Sarcophagidae) whereas control traps captured only 8 such individuals from these families. The majority (77%) of flies trapped were Pyrellia and Orthellia spp. (Muscidae) and sepsid flies. The latter, in particular, were associated with mixed populations of S. ampullaceum and S. luteum . Marino (1991a) studied sympatric moss assemblages of S. ampullaceum , S. luteum , T. angustatus and T. mnioides in central Alberta, Canada and quantified the number of spores carried by individual flies. Consistent with the findings of Koponen and Koponen in Finland (1977), Marino (1991b) also found that most flies trapped on Splachnaceae with spores on their bodies were coprophilous species, and that Pyrellia spp. and sepsids were especially attracted to S. ampullaceum . However, few of the relatively small, hairless sepsid flies carried spores. Unlike the trapping results of Koponen and Koponen (1977), Marino (1991b) also trapped large numbers of spore carrying anthomyiid and calliphorid flies (e.g., Calliphora vomitoria ). The larvae of most anthomyiids are phytophagous but some are saprophagous, feeding on decaying material (McAlpine et al., 1981). Adults, however, feed on nectar and are important plant pollinators, particularly at high latitudes and altitudes (Kearns and Inouye, 1993; Larson et al., 2001; Zoller et al., 2002). Anthomyiids thus would appear to be ideal potential vectors for spores of Splachnaceae, as the adults are attracted by flower-like visual displays and odours but they also visit fresh dung or carrion on which to lay their eggs. Indeed, the showiest sporophytes of Splachnaceae (e.g. those of Splachnum luteum, S. rubrum ) approximate small flowers in colour display and physical dimensions (Fig. 5). However, an important departure from the pollination metaphor is that insect-mediated spore dispersal in the Splachnaceae requires that sporophytes attract flies only once, after which they fly to appropriate host sites, whereas successful cross-pollination requires flowers to attract pollen vectors at least twice. Marino (1991b) trapped flies visiting four sympatric moss species ( Tetraplodon angustatus, T. mnioides, Splachnum ampullaceum, S. luteum ) and identified overlapping but distinctive patterns of fly visitation per species. Fig. 3 shows his data in a bipartite interaction network, revealing that only one third of the possible moss- by-fly interactions actually were observed. When shown as a matrix (Table 2), the data reveal “modules” or distinctive visitor faunas for each moss. The visitor spectra differed among the four species by 77–92% between species (Table 2). For example, the carrion-scented sporophytes of Tetraplodon mnioides relied heavily upon calliphorid flies as spore vectors, of which only Calliphora vomitoria also was observed to visit Splachnum spp. (Fig. 3). In contrast, the bright yellow, weakly scented sporophytes of Splachnum luteum were visited by five families of flies, including anthomyiids (Fig. 3). Moreover, fly faunas captured on dung were more similar to each other than were those captured on Splachnaceae; all flies trapped on Splachnaceae were also trapped on dung (Marino, 1991b). Overall, there appear to be at least three niche dimensions that may be responsible for coexistence of regionally sympatric species: 1) habitat and substrate type (e.g., between spp. of Tetraplodon and Splachnum ), 2) fruiting phenology (e.g., between spp. of Tetraplodon ) and 3) the ‘potential’ for sensory filtering and targeted dispersal by different vectors, using colour-odour combinations (Marino, 1991a;b; 1997). Evolutionary modifications of visual and olfactory stimuli in different mosses may lead to diversification within the larger syndrome of fly-dispersed moss spores. Entomophilous Splachnaceae differ greatly in the size, shape and colour of the sporophytes as well as the height of the seta (Fig. 2). Cameron and Troilo (1982) assayed landing by Pyrellia cyanicolor on coloured disks placed among sporophytes of S. ampullaceum in Michigan; the flies showed a clear 20-fold preference for yellow over blue or red. More recently, Marino et al. (in prep.) experimentally decoupled olfactory and visual cues (e.g., Roy and Raguso, 1997) to explore their relative importance in fly attraction to S. ampullaceum in Newfoundland, Canada. In that study, flies were trapped on pure populations of: A) S. ampullaceum with mature sporophytes (olfactory + visual cues), B) S. ampullaceum with mature sporophytes covered with green dyed cheese cloth (olfactory cues only), C) scentless models of S. ampullaceum sporophytes placed adjacent to immature (gametophyte only) populations of S. ampullaceum (visual cue only), and D) scentless artificial models of S. ampullaceum placed adjacent to cheese cloth covered S. ampullaceum with mature sporophytes (model + odour, the reconstituted combination of cues). Of the approximately 1000 flies trapped, significantly more flies were trapped on the S. ampullaceum positive control (A) and the model + odour treatment (D) than either the model alone (C) or the odour alone (B; Fig. 4a), indicating that neither sporophyte odour nor colour are sufficient to attract the full spectrum of flies. However, the relative importance of olfactory and visual cues differed among the eight families of flies trapped. Nearly all taxa caught are commonly associated with dung or other decaying organic matter (McAlpine et al., 1981). The exceptions were the Dolichopodidae, whose adults are predacious (Ulrich, 2005) and whose larvae are thought to be predators or scavengers and the Sciomyzidae, whose larvae are parasitic on molluscs (Rozkosny, 1984). The most abundantly trapped flies were in the families Anisipodidae, Muscidae and Sepsidae. Anisipodids and sepsids were most attracted to the S. ampullaceum positive controls and to a lesser extent to the odour only and model + odour treatments, whereas muscids and anthomyiids were equally attracted to all three scented treatments (Fig. 4b). As the relatively large and hairy muscids and anthomyiids have been shown to carry many spores (Marino, 1991b), these results suggest that, for S. ampullaceum , odour is a key factor facilitating the dispersal of spores to fresh patches of dung by flies. Sporophyte odour in the Splachnaceae is, to our knowledge, novel among mosses and constitutes a key adaptation associated with entomophily in this family (Koponen, 1990). In angiosperm evolution, key adaptations such as floral oil (Anderson, 1979; Buchmann, 1988), nectar spurs (Hodges, 1997) and bilateral floral symmetry (Donoghue et al., 1998) are thought to have triggered evolutionary shifts to novel pollination strategies. When such shifts occur, ...
Citations
... Um Dungfliegen (Scatophagidae) anzulocken, bedienen sie sich einer Kadaver-Mimikri. Sie geben flüchtige organische Verbindungen wie Dimethyldisulfid DMDS, Buttersäure oder Essigsäure ab, um Fliegen anzulocken (STUDLAR 2007, MARINO 2009, BENBOW 2016. Diese Lockstoffe werden von der Apophyse abgegeben, dem unteren verdickten Teil der Sporenkapsel (KOPONEN 1990). ...
Only a few systematic investigations on mosses at carcasses have been performed until now. This article describes the bryophyte flora at two bait places in the Bavarian Forest National Park, Germany. At such bait places, carcasses are regularly exposed. Accordingly, the soil is characterized by an extraordinary high nutrient concentration. Typical identified substrates were soil, bones and deadwood. Both examined locations showed a different bryophyte vegetation. Overall, the examination revealed species that are prevalent in the study area, growing at typical substrates. Soil mosses as well as bone mosses are marked acidification indicators. Even in identical substrates, species with very different light requirements are growing very close together, indicating a clearly differing ecological situation within short distances. Year-round follow-up mappings of bryophytes are necessary to register potential Splachnaceae species.
... ott (1824:442) family or dung mosses. Around half the species in this unique moss family are adapted to utilize insects as dispersers, to transport the moss between its unusual habitat of animal dung or carcasses. The moss exploits insects that are themselves attracted to decaying carcasses or droppings, known as coprophilous insects (Koponen 1990;Marino et. al 2009). The spores of the entomophilous Splachnaceae mosses are generally characterized as thin walled and oblong in shape and are produced in association with a sticky mucilage (Koponen 1990). These characteristics are thought to aid the moss spore in sticking to insect visitors (Koponen 1990;Marino et. al 2009), but would make wind dispersal ...
... own as coprophilous insects (Koponen 1990;Marino et. al 2009). The spores of the entomophilous Splachnaceae mosses are generally characterized as thin walled and oblong in shape and are produced in association with a sticky mucilage (Koponen 1990). These characteristics are thought to aid the moss spore in sticking to insect visitors (Koponen 1990;Marino et. al 2009), but would make wind dispersal difficult. ...
... Additionally, we demonstrated that the droppings of birds fed an omnivorous diet provide suitable habitat for this species of dung moss to progress through its protonemal stage and on to producing buds which is the next stage in the progression towards fully mature gametophytes. This, combined with the plausibility of insectivorous birds consuming spore laden insects, could provide evidence for the dispersal of spores via endozoochory and explain dispersal events over medium distances such as between pockets of habitat within a region (Koponen 1990;Marino et al 2009) and long, intercontinental distances such as those seen in S. pensylvanicum (Lüth and Goffinet 2005). ...
The dispersal of reproductive material plays a key role in the ecology of plants. Dung mosses (Splachnaceae), have evolved to utilise insects to disperse spores to habitat sites consisting of dung or dead animals—a marked departure from the wind based spore dispersal seen in other mosses. However, adapting to insect dispersal likely precludes long distance airborne dispersal, and limits dispersal events to the movements of the spore bearing insect. However, there are several disjunct populations of these mosses, incompatible with insect dispersal, raising questions over the manner of their origin. Hypotheses put forward include the dispersal of the mosses to these sites by birds. Here, the possibility that insectivorous birds could internally transport spores is explored by feeding insects bearing spores to captive myna birds. We tested if the spores of the New Zealand dung moss, Tayloria callophylla, can survive gut passage. Ultimately 9 of 10 dung samples produced viable moss colonies after a period of 30 days, demonstrating the survival of the spores through an avian digestive tract. Our results provide evidence for a unique model of dispersal in dung mosses, where a spore bearing insect is eaten by a bird that eats insects transports the spores in its gut over a much greater distance than otherwise likely with the insect alone.
... In bryophytes, it has been shown that VOCs may play a role in spore and spermatozoid dispersal. For examples, several species from the moss family Splachnaceae use brightly colored, scented sporophytes to attract flies that facilitate spore dispersal [12]. Similarly, the moss Ceratodon purpureus utilizes volatile scents to manipulate microarthropod behavior, increasing moss fertilization [13]. ...
... Similarly, the moss Ceratodon purpureus utilizes volatile scents to manipulate microarthropod behavior, increasing moss fertilization [13]. It has also been found that odors of gametophytes and sporophytes of Splachnaceae species differed significantly, with gametophyte odors consisting of sesquiterpenoids and hydrocarbons, whereas sporophyte odors were much more pungent and chemically complex [12]. In some cases, VOCs may serve as chemotaxonomic markers and be used as characters in taxonomy, e.g., in recognition of cryptic species of Conocephalum conicum [14]. ...
... Splachnaceae Manipulation of insect behavior to facilitate spore dispersal Marino et al. [12] Ceratodon purpureus (Hedw.) Brid. ...
Volatile emissions from 22 bryophyte species from Peninsular Malaysia were collected using a dynamic headspace technique and analyzed by gas chromatography-mass spectrometry (GC-MS). Thirty organic compounds (VOCs) from eight different groups were detected in bryo-phytes from the montane forest in Cameron Highlands and the lowland dipterocarp forest in Lata Belatan. The headspace of bryophytes in Cameron Highlands was dominated by tetradecane, 2-ethyl-1-hexanol, decanal, pentanoic acid, 2,2,4-trimethyl-3-carboxyisopropyl, isobutyl ester, D-lim-onene and naphthalene. On the contrary, in the bryophyte headspace of Lata Belatan, naphthalene and tetradecane were dominant compounds. The elevational pattern detected in VOC composition of bryophytes appears to be an evolutionary feature at the family level that needs verification at other sites. The results also confirmed that the VOC composition of bryophytes is species-specific. The roles of VOCs in bryophytes are presented, including plant-plant communication and plant-insect interaction and as an additional taxonomic character in chemotaxonomy.
... Recently, a study confirmed the capacity of cattle dung VOCs to alter the composition of dung-inhabiting insect assemblages [22]. Further evidence for the roles played by VOCs in the behavior of dung-inhabiting insects comes from the coevolutionary phenomenon of deception of these species by dung-mimicking odoriferous plants to facilitate their seed dispersal [23,24]. However, studies to more fully characterize livestock dung volatilomes remain limited. ...
Volatile cues can play a significant role in the location and discrimination of food resources by insects. Dung beetles have been reported to discriminate among dung types produced by different species, thereby exhibiting behavioral preferences. However, the role of volatile organic compounds (VOCs) in dung localization and preference remains largely unexplored in dung beetles. Here we performed several studies: firstly, cage olfactometer bioassays were performed to evaluate the behavioral responses of Bubas bison (Coleoptera: Scarabaeidae) to VOCs emanating from fresh horse, sheep, and cattle dung; secondly, concurrent volatilome analysis was performed to characterize volatilomes of these dung types. Bubas bison adults exhibited greater attraction to horse dung and less attraction to cattle dung, and they preferred dung from horses fed a pasture-based diet over dung from those fed lucerne hay. Volatilomes of the corresponding dung samples from each livestock species contained a diverse group of alkanes, alkenes, alkynes, alcohols, aldehydes, ketones, esters, phenols, and sulfurous compounds, but the composition and abundance of annotated VOCs varied with dung type and livestock diet. The volatilome of horse dung was the most chemically diverse. Results from a third study evaluating electroantennogram response and supplementary olfactometry provided strong evidence that indole, butyric acid, butanone, p-cresol, skatole, and phenol, as well as toluene, are involved in the attraction of B. bison to dung, with a mixture of these components significantly more attractive than individual constituents.
... Besides wind, water in the form of rain or running water is an important vector, and rain ends dispersal events by washing out windblown diaspores from the air (Kimmerer 1991;Korpelainen et al. 2013). Animals serve as dispersal agents over short (Boch et al. 2013(Boch et al. , 2015, moderate (Marino et al. 2009;Barbé et al. 2016a), and even long distances (Lewis et al. 2014;Chmielewski and Eppley 2019). Additionally, spatial and temporal factors constrain diaspore production. ...
Introduction
Half a century since the creation of the International Association of Bryologists, we carried out a review to identify outstanding challenges and future perspectives in bryology. Specifically, we have identified 50 fundamental questions that are critical in advancing the discipline.
Methods
We have adapted a deep-rooted methodology of horizon scanning to identify key research foci. An initial pool of 258 questions was prepared by a multidisciplinary and international working group of 32 bryologists. A series of online surveys completed by a broader community of researchers in bryology, followed by quality-control steps implemented by the working group, were used to create a list of top-priority questions. This final list was restricted to 50 questions with a broad conceptual scope and answerable through realistic research approaches.
Key results
The top list of 50 fundamental questions was organised into four general topics: Bryophyte Biodiversity and Biogeography; Bryophyte Ecology, Physiology and Reproductive Biology; Bryophyte Conservation and Management; and Bryophyte Evolution and Systematics. These topics included 9, 19, 14 and 8 questions, respectively.
Conclusions
Although many of the research challenges identified are not newly conceived, our horizon-scanning exercise has established a significant foundation for future bryological research. We suggest analytical and conceptual strategies and novel developments for potential use in advancing the research agenda for bryology.
... In parallel, the four saprophilous fly-pollinated species (J. leucotricha, J. laciniata, J. rotacea and J. sativa) generally were characterized by the presence of universal volatile components (e.g., oligosulfides, cresol, indole) indicative of carrion-or dung-mimicking flowers, fungi and mosses [62][63][64]89]. Specifically, most of the Andean clade species emitted DMDS and DMTS, behaviorally active compounds that are common to rotting meat and carrion-mimicking flowers worldwide [26,59,60]. ...
Floral scent is a key communication channel between plants and pollinators. However, the contributions of environment and phylogeny to floral scent composition remain poorly understood. In this study, we characterized interspecific variation of floral scent composition in the genus Jaborosa Juss. (Solanaceae) and, using an ecological niche modelling approach (ENM), we assessed the environmental variables that exerted the strongest influence on floral scent variation, taking into account pollination mode and phylogenetic relationships. Our results indicate that two major evolutionary themes have emerged: (i) a ‘warm Lowland Subtropical nectar-rewarding clade’ with large white hawkmoth pollinated flowers that emit fragrances dominated by oxygenated aromatic or sesquiterpenoid volatiles, and (ii) a ‘cool-temperate brood-deceptive clade’ of largely fly-pollinated species found at high altitudes (Andes) or latitudes (Patagonian Steppe) that emit foul odors including cresol, indole and sulfuric volatiles. The joint consideration of floral scent profiles, pollination mode, and geoclimatic context helped us to disentangle the factors that shaped floral scent evolution across “pollinator climates” (geographic differences in pollinator abundance or preference). Our findings suggest that the ability of plants in the genus Jaborosa to colonize newly formed habitats during Andean orogeny was associated with striking transitions in flower scent composition that trigger specific odor-driven behaviors in nocturnal hawkmoths and saprophilous fly pollinators.
... The majority of flowering plants rely on animals for pollination; they attract pollinators by providing a food source (such as nectar), and their pollen is picked up or deposited by the pollinators as they feed (Abrol 2012). Pollinator/spore disperser attraction is also found in cycads (e.g., Terry et al. 2007, Marler 2010, mosses (Marino et al. 2009), sea grasses (van Tussenbroek et al. 2016), and fungi (e.g., Horton 2017, Elliot et al. 2019, Suetsugu et al. 2019. Similarly, over half of trees in both tropical and temperate forests produce fruit to attract consumers, which then can serve as seed dispersers (Howe and Smallwood 1982). ...
Movement is a widespread behavior across organisms and is driven in part by interspecific interactions. Generally, negative interspecific interactions (such as competition and natural enemies) are more often studied in the context of movement than positive interactions (mutualism). Mutualistic relationships are incredibly common, yet only a subset are studied in the context of movement (transportation mutualisms). Overall, the costs and benefits that an individual experiences are shaped both by their movement behavior and their mutualistic relationships, as well as the intersection between these. Here we argue that the intersection between movement behavior and mutualistic relationships is understudied, and we present a conceptual framework to synthesize the links between movement and mutualisms and give examples of species that exhibit each. Our framework serves both to highlight the ways that mutualism can shape movement (and vice versa) and to draw parallels across different organisms (enabling a more abstract perspective of these biological systems, complementing the system‐focused perspective). Finally, we show how considering movement in light of mutualisms (and vice versa) presents a number of new research questions to be answered by each empirical and theoretical approach going forward.
... Insect decomposers locate resources using volatile organic compounds (VOCs) (Frank et al. 2018;Wurmitzer et al. 2017) and can even be deceived by plants that mimic the scent of their natural food resources Jürgens et al. 2013;Marino et al. 2009;Midgley et al. 2015). Communities of insect decomposers inhabit decaying ephemeral resource patches, such as dung and carrion, that are temporally unstable, yet energy-rich (Finn 2001). ...
Chemical cues, such as volatile organic compounds (VOCs), are often essential for insects to locate food. Relative to the volume of studies on the role of VOCs in insect-plant relationships, the role of VOCs emitted by dung and carrion in mediating the behavior of insect decomposers is understudied. Such relationships may provide a mechanistic understanding of the temporal axis of community assembly processes in decomposing insect communities. We focused on the temporal succession of volatiles released by cow dung pats and the potential influence on dung-inhabiting insects. Using gas chromatography/mass spectrometry we identified and quantified VOCs released from dung 1-h, and 1, 2 3, 5, and 7 d-old. We then related changes in VOCs to successional patterns of dung-inhabiting beetles and flies. We detected 54 VOCs which could be assigned to two successional groups, with chemical turnover in dung changing around day 2. The early successional group consisted primarily of aliphatic alcohols and phenols, and the late one of aliphatic esters, nitrogen- and sulfur-bearing compounds. Flies were predominately associated with the early successional group, mainly with 1-butanol. Beetles were associated predominately with the late-successional group, mainly with dimethyl trisulfide. This association between insect and chemical successional patterns supports the idea that habitat filtering drives the community assembly of dung-inhabiting insects on an aging resource. Moreover, the affinity of both insect groups to specific VOC groups provides a mechanistic explanation for the predictability of successional patterns found in dung-inhabiting insect communities.
... relationship between animals and spore plants in future studies, as well as the formation, maintenance mechanism and future evolutionary trends of spore plant-animal relationships. Key words: spore plants; zoochorous dispersal; mutualistic relationship; vegetation regeneration; biodiversity conservation 孢子植物旧称隐花植物, 不产生种子, 生活史 中通过产生孢子的方式完成后代繁殖。生物群落中 的藻类、菌类、地衣、苔藓和蕨类均属于孢子植物 (罗健馨, 1977)。孢子植物是许多陆生动物的重要食 源 (Bråthen et al, 2007;Boch et al, 2011)。 虽然孢子植 物不像被子植物那样有着鲜艳的花、果实、种子来 吸引动物, 但是某些孢子植物(如菌类、 苔藓)能够产 生特殊的气味 (Tuno, 1998;Fischer & Vicha, 2003;Marino et al, 2009;Chen et al, 2014) ...
Background & Aims: Spore plants, as an important food source for terrestrial animal, play a vital role in maintaining the subtle balance of the earth’s ecological system. Animals and spore plants may also together form an interaction system similar to the network of zoochorous seed dispersal. Therefore, the effect of animals on spore plant propagules dispersal has been receiving increasing attention. Here, we summarize that (1) the adaptation of spore plants to dispersal by animals. On the one hand, spore plants can provide food, shelters and breeding sites for animals; on the other hand, spore plants can also produce visual and/or olfactory cues and so on to attract animals in order to increase their propagule dispersal. (2) the two zoochorous dispersal patterns of spore plants that can effectively disperse propagules of spore plants, namely endozoochory (through the digestive tract and parasitism) and epizoochory. Due to the different morphological characteristics and life habits between animals, the distance of dispersal is also different, with the shortest distance of 0.1 cm and the longest distance from the northern hemisphere to the southern hemisphere. (3) The ecological and evolutionary meanings of zoochorous dispersal of spore plants. For some spore plant propagules, due to their special structural characteristics or particular need for germination, the propagules can only be dispersed by specific animals, which leads to an inseparable relationship between such animals and spore plants. At present, few studies in this field have been conducted in China. The researches on spore plant dispersal in other countries are mainly descriptive, most of which are independent pattern on spore plant dispersal. Prospects: We propose that more consideration should be given to the multi-pattern dispersal and mutualisticrelationship between animals and spore plants in future studies, as well as the formation, maintenance mechanism and future evolutionary trends of spore plant-animal relationships.
... Beaman et al., 1988;J€ urgens et al., 2006;Kowalkowska and Margo nska 2009;Kowalkowska et al., 2010;Van der Niet et al., 2011;Wi sniewska et al., 2015;Naczk et al., 2018). Conversely, animal visitors have developed morphological and behavioural features that facilitate their interactions with flowers (Marino et al., 2009;Johnson and J€ urgens 2010). ...
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This micromorphological, chemical and ultrastructural study is a continuation of research conducted on fly-pollinated species. The aim of proposed project is to examine the features of floral secretory tissue of stapeliads (Eudicots, Apocynaceae, Asclepiadoideae) and compare them with previously published Bulbophyllum species (Monocots, Orchidaceae, Epidendroideae). The Echidnopsis cereiformis and Stapelia scitula flowers comprised features that characterize a fly-pollinated syndrome. Secretory activity was observed on the adaxial (upper) surface of flowers of both species, however, the chemical composition of secretion differs between species. In S. scitula it is lipid-rich material, whereas in E. cereiformis it is protein-rich. The ultrastructural studies revealed dense cytoplasm in the epidermis and subepidermal tissue with large nuclei and numerous mitochondria, the profiles of SER and RER, and dictyosomes. Large amounts of secreted material were present on the cuticle surface, similar to the unusual prominent periplasmic space with flocculent secretory material. The most remarkable feature was the presence of a prominent periplasmic space in the epidermal cells of S. scitula. Interestingly, subcuticular spaces have been noted only in a few other species, including three orchids from the section Lepidorhiza. Since Asclepiadaceae and Orchidaceae share other features which developed independently, such as pollen mass coherent in pollinia, presence of a periplasmic space could have also developed as a consequence of pollinators pressure and could be a feature important taxonomically.
