Fungal succession and wood decay in living trees – a seminar report (Part II)

See Part I here.

The second part of this cluster of blog posts is one the first of the duo of talks presented by Lynne Boddy. Lynne is a well-known mycologist and researcher and thus, as regards wood-decay fungi, is a good authority from which we can all learn a substantial amount. For a fungi enthusiast such as myself, learning about fungi from one of the best is, in and of itself, very exciting. However, the information presented was equally as exciting, which I shall run through below.

As a slight aside, please watch out for her new book, which is currently being written and should be finished later this year, currently entitled Fungi in Trees. This book will be aimed at the arboriculturist. Lynne is also planning to re-write Fungal Decomposition of Wood, which was a magnum opus co-authored with Alan Rayner.

Fungi invading trees

Primarily, we must accept one core tenet of wood decay: the anatomy of wood has a massive impact upon mycelial networks that sojourn through the wood substrate and selectively metabolise woody cells and their deposits as they go. Indeed, in an ideal world, fungi would gun right for the ray parenchyma, which are incredibly nutritious living cells. However, these cells are very challenging to get to, by virtue of their ‘aliveness’ – living cells in good condition are not easily devoured. Further to this, the sapwood also offers a great for invading fungi, though again – because of the high moisture condition meaning the environment is largely anaerobic (fungi are aerobes and require oxygen to metabolise) – this part of the wood structure is not easily accessed. Of course, the vascular wilts have a better time invading sapwood that is functional, though many fungi will have to bide their time or arrive opportunistically onto and into dysfunctional sapwood if they are to have any means of success in acquiring the treasures within. Thus, is recognising that such living (i.e. conductive and functional) areas of wood are likely just beyond the reach of many fungi, wood-decayers will typically resort to the back-up food source: non-functional xylem vessels within the heartwood or ripewood.

The heart rotters

Now, in accepting this, we come on to perhaps the broadest cohort of wood-decay fungi in living and standing trees (fallen trees have their dysfunctional sapwood metabolised like ravens engulfing a fresh meal) we know of: the heart rotters. These fungi will enter the central wood (i.e. ‘the heart’) through exposed areas of this central column by either sufficiently deep root, stem or branch injury – ultimately, there generally needs to be a continuity of viable ‘heart’ substrate, if any significant degree of colonisation is to take place. Where continuity doesn’t exist, or the fungus finds itself limited to only a certain area, the only manner in which is will typically be able to continue existing is by (1) exiting and finding another host or (2) biding its time and waiting for currently functional sapwood to become incorporated into the heartwood or ripewood, in which it can then spread into – assuming the tree doesn’t lay down defensive barriers that cannot be breached, in order to protect its sapwood, which is in itself a pursuit undertaken to safeguard and hence sustain the high-moisture content of its sapwood (contrary to Shigo’s model, which infers compartmentalisation is largely there with the end in mind of prohibiting fungal succession into the wood). When we look at the ripewood of beech (Fagus sylvatica), we can observe this phenomenon very well – a rosy-coloured ripewood (red heart) with lots of separation lines between instances of decay successions. Ganoderma australe, Ganoderma pfeifferi and Ganoderma resinaceum will afford the most acutely observable examples of this, given their ability to breach such zones by metabolising the phenolic deposits laid down by the tree (this touches upon the idea of a fifth wall in the CODIT model, which will be discussed more later on).

laetiporus-taxus-baccata-yew-3
An old Laetiporus sp. on yew (Taxus baccata).

By virtue of the heartwood or ripewood being the least inhospitable (heartwood, in particular, is still often disgustingly harsh, as regards its environment), we can observe immediately some species-specific associations. For instance, the dyer’s mazegill (Phaeolus schweinitzii) will frequent gymnospermous hosts, such as the cedars (Cedrus spp.) and pines (Pinus spp.), whilst chicken of the woods (Laetiporus spp. – often L. sulphureus, though by all means not always, as we will see) will be found often on oak (Quercus spp.), sweet chestnut (Castanea sativa) and yew (Taxus baccata) – it can, indeed, be found on other hosts, as well. On the face value of things, these three tree species have seemingly little in common, though all three have extractive-rich heartwood that this genus can metabolise effectively. In terms of why the genus is referred to and not the exact species, Lynne is of the stance that what we term ‘chicken of the woods’ and default to as L. sulphureus is actually a variety of different species each with their own specialisations – perhaps even down to a specific host tree species (notably for yew, where the chicken species is most pertinently viewed as being a different one).

From a tree management perspective, Lynne then addressed the importance of the heart rotters – what is their impact? Put simply, they change the way in which we view the tree from a safety perspective; as in, when fruiting bodies of heart rotters are identified, if the tree is standing and there exists a target, management considerations are routinely entertained and sometimes the tree is felled. Additionally to this, however, we have other things to appreciate:

  • heart rotters do a great job at recycling nutrients, which can then be re-assimilated by the tree when they are uptaken back through its roots (including adventitious aerial roots) or the mycorrhizal fungi the roots associate with
  • the wood qualities produced by heart rotters are ideal as habitat for saproxylic insects and nesting birds
phlebia-tremellosa-fagus-sylvatica-pollard-2
The heart of this beech has been hollowed-out by decay fungi. In the process, before its failure, what conditions did this decay provide for insects and, crucially, what habitat does it provide now?

Latent colonisers

Considered the specialised opportunists, such fungi are present within the sapwood or bark, as propagules (thick-walled resting spores known as chlamydospores). Biding their time until conditions are right, wherein the sapwood becomes dysfunctional through means such as wounding or drought (causing embolism), they are perhaps most acutely observed in the years after drought years where they can trigger the formation of strip cankers and resultant reaction growth by the tree (see the below photo). Thus, this year, in the UK, is one to watch out for, as regards such fungi (it might also explain why Kretzschmaria deusta was so abundant this year, given Ascomycetes love dry conditions, which prevailed last summer).

B nummularia Eutypa spinosa beech canker strip
A strip canker in beech caused by the latent fungus Biscogniauxia nummularia that has induced reaction growth, which can be seen cross-sectionally in the bottom right image).

At this point, a delegate enquired as to whether Massaria disease of plane (Splanchnonema platani), as an Ascomycete, could be prevailing in urban conditions recently, because of dry conditions (such as London, where it was been very severe these past few years but prior to that un-noticed). Discussions continued and Frank Rinn interjected to add his thoughts:

  • massaria progresses quickly in dry conditions
  • recent dry summers have allowed for massaria to thus progress very rapidly (killing branches in as little as three months)
  • the lowering of water tables in cities for the construction of basement levels of buildings has meant that plane trees can no longer tap into groundwater supplies
  • mature plane trees afford the best conditions for massaria; notably lower lateral branches, which are shaded from the rest of the crown and thus may be most prone to stress
  • there have been reports since 1903 from Croatia where large plane trees have shed branches and the massaria fungus was termed the “branch-cleaning fungus”
  • conditions are collectively ideal for massaria to become prevalent, as they stand

Reverting back to latent fungi, Lynne then mentioned that she considers fungi to be latent across a broad variety of trees. For example, the coal fungus (Daldinia concentrica), whilst found most often on ash (Fraxinus excelsior) can be isolated from the sapwood of a great range of different broadleaved tree species in the UK. It is, indeed, only when specific conditions arise that are preferable for this fungus that it begins to create mycelial networks – such conditions might not arise in particular trees, or may arise only after conditions suitable for other fungi have arisen and thus D. concentrica then has no capacity to colonise the substrate. Hence, ash remains the core host of this species, in the current climate. However, for the jelly ear fungus (Auricularia auricula-judae), which is also a latent fungus within the vascular system, having been found largely solely on elder (Sambucus nigra) in the 1950s, it is now found on over 20 host species – this marks a huge increase in host range, prompted perhaps by changing climatic conditions.

Wall V

The CODIT model, offered to us by Shigo, details four walls – as can be seen here. As mentioned by Frank Rinn, Shigo himself was considering the possibility of a fifth wall, though this never ‘made it into’ the model. However, Lynne argues that there is the potential for a fifth one, which hearkens back to what was discussed above, as regards rot within the heart of beech wood).

Specifically, whilst the barrier zone (fourth wall) is a zone laid down at the time of wounding by the vascular cambium, the dynamic responses by the tree that occur in real-time as fungal decay advances constitutes a distinction from this initial barrier. Indeed, as decay advances, living cells within the heartwood or ripewood (they do exist; though through mechanisms not fully appreciated, but thought to be associated with the rays running radially through the wood), in addition to the functional sapwood, will, in order to protect the sapwood and keeps its high-moisture quality intact, will plug woody cells beyond the current zone of decay with extractives and phenolic compounds – this will occur within the sapwood most often, though may also be able to occur in the heartwood around the regions where pockets of living cells exist. This response resultantly produces incredibly dense zones of wood that afford the tree’s sapwood a means of protection, which it would otherwise lack, assuming the barrier zone (Wall IV) failed to contain fungal decay. Of course, if this fifth wall fails, another will form, and so on and so forth.

Ganoderma pfeifferi beeswax beech failure 3
See the myriad of demarcations across this cross-section of a beech that failed from decay by Ganoderma pfeifferi, which suggest a dynamic fifth wall being effective.

Perhaps we will see this idea discussed more in Lynne’s re-write of Fungal Decomposition of Wood.

Fungal succession

When a tree decays, the fungi that initiated the decay process will not end it. This is because, much like all other ecosystems, as an environment changes those organisms that are best-placed to utilise it change as well. In this sense, fungi are no different – they succeed into a dynamic and ever-altering substrate (wood). Such a phenomenon can be so readily observed when walking into any woodland, when comparing the fungi on standing trees and those in early stages of decay and those much more heavily decomposed. In instances where an entire tree falls and stays largely intact, succession can be most acutely observed, as Lynne detailed with a little help from Ted Green and some research students.

The tree in question, a mature beech, failed and was left, in sections, for ease of its movement into an accessible place, to decay. Along the beech, it was found, through analysis of the wood in the laboratory and by presence of fruiting bodies, different fungi were observed colonising different parts at different stages of decay (as shown below). Such an observation does seem readily apparent, though to have it confirmed through scientific means affords us with an understanding that is more concrete than merely the anecdotal. Indeed, whilst Trametes gibbosa was not isolated from this beech, the presence of Bjerkandera adusta infers that, at some point in the future, T. gibbosa will be found – it parasitises upon the mycelium B. adusta, before then colonising the wood substrate itself. We are, in a sense, therefore, witnessing fungal warfare.

beech fungi succession analysis
The different fungi found at different parts of the beech at different stages of the decay process (open in a new tab to see this in a slightly larger size).

Delving further into the notion of fungal warfare, what is essentially meant is chemical warfare. Fungi synthesise and secrete enzymes, which they use principally to degrade wood, though that can also be used to defend territory or attack other fungi. The result of any fungal battle can be one of four things:

  • deadlock, whereby neither fungi gains any ground against the competing fungus
  • replacement, whereby one fungus loses its territory entirely by the other
  • partial replacement, whereby one fungus loses of some its territory to the other
  • mutual replacement, whereby the fungi essentially ‘trade’ places with one another and neither gains any net ground

So how does one determine the outcome of any such skirmish, you ask? Unfortunately, there are so many variables in play that even pitting two fungi against one another in a laboratory is only going to give a slight allusion to what really occurs, though there does nonetheless exist a limited hierarchy of combativeness from which we can assume who the victor will be, under most circumstances (see here at 25:09 timestamp).

Of course, even in assessing this we still have so many caveats to throw in. For example, where moisture conditions are drier because the wood is more exposed, Ascomycetes (i.e. Hypoxylon spp.) will have a better time in securing more wood substrate, as they operate effectively under dry conditions. Indeed, the wood qualities of the substrate itself will even play a role – did the tree uptake pollutants during its life or is it exposed to such pollutants currently, for example. More crucially, if a dead piece of wood (or entire tree) is standing and has thus been subject to relatively dry and exposed conditions suddenly falls to the woodland floor, those fungi reigning when the tree was standing will likely succumb to wood-decay fungi adapted to higher moisture levels and cooler more stable conditions.

The next part of this series will be a brief one on bacteria in wood, as discussed again by Lynne Boddy. I hope to have that written up in the coming few days.

Advertisements
Fungal succession and wood decay in living trees – a seminar report (Part II)

Wood-decay fungi in the Antarctic Peninsula

No, this title is not a click-baiting one – it’s wholly serious!

Courtesy of some recent research undertaken by scientists on Deception Island, which is an actively volcanic island in the archipelago that forms the South Shetland Islands, we now have a fascinating glimpse of the fungal activity that can be found upon the abanonded 19th and early to middle 20th century timber-framed buildings found upon the island’s shores. Indeed, with 57% of the island being covered by glaciers, these buildings were built along the coastline and were used for research and European whaling purposes (Whalers Bay), up until the Chileans departed from Pendulum Cove in 1967. Nowadays, it’s a tourist area for those that quite fancy spending large sums exploring such a desolate island, as well as a research base for Spanish and Argentinian scientists.

antarctica-deception-island-3-xl
Decaying timbers on the island. Source: The Planet D.

As regards to prior research on the historic timber buildings upon the island, research has uncovered fungal decomposition of the timber by Ascomycete fungi, thereby inferring some timber has begun to degrade via a soft rot. However, brown and whit rot fungi had not previously been identified on the island to any marked degree (one fruiting Pholiota sp. sample was found on the wood of a buried whaling vessel in 1967), and thus this research sought to ascertain whether fungal diversity was more appreciable than previously understood. At this point, it is also worth noting that some Asocmycetous fungi are indigenous to the island (such as Cadophora spp.), being found as saprotrophs on the plants growing freely on the island. Moreover, the research enabled for an insightful look into fungal ecology in a location where soil temperature range from below freezing to as high as 90°C.

Using two sites on the island where such timber-framed buildings could be found, which were Whalers Bay and Pendulum Cove (see the below image for rather precise locations), very small wood fragments from the timber-framed buildings (largerly made of Pinus spp. and Picea spp. timbers, though also Betula spp.) were sampled (188 from Whalers Bay and 30 from Pendulum Cove) and taken back to the laboratory under sterile conditions for assessment in a growth medium comprised principally of malt extract agar. Following the placement of the samples within the agar for a few weeks and the subsequent transfer of growing mycelium into pure cultures, genetic analysis was undertaken to ascertain what fungi were present within the wood samples.

Fungi on Antarctica
The two research locations used for the study (as denoted by the red arrows).

In total, 326 isolates were found from the total 218 sampled wood fragments. Indeed, as was probably expected, the large majority (79%) of the isolated were of Ascomycete fungi from 53 different taxa that were causing a soft rot. However, quite interestingly, 15% of samples (equating to 11 different taxa) were from the Basidiomycetes division and a few (6%) also belonged to the Zygomycota.

From the Basidiomycetes, which are probably more well-known to those who read this blog, 18% of isolates were from the genus Pholiota. Indeed, this genus is a frequently identified one in the UK and further afield, and the genetic analysis revealed that one particular clade of the genus was of the species Pholiota multicingulata, which was found exclusively at the Pendulum Cove site where the Chilean undertook their scientific research up until the late 1960s. Found across the South Pacific and notably in New Zealand, its presence in the Antarctic Peninsula is considered to be as a consequence of infected timbers brought over by the Chileans.

Other common wood-decay Basidiomycetes known to arboriculturists included Coprinellus micaceus and Coniophora puteana, though only one sample of each was identified from genetic analysis – both considered to have been introduced by the Europeans during whaling escapades. Postia pelliculosa, a brown rot fungus of gymnospermous wood, was also identified – as was Jaapia argillacea, which is a rare fungus within Europe and thus its finding at Whalers Bay presented the authors with some surprise.

440224
A group of caps of the fungus Pholiota multicingulata growing on deadwood. Source: Mushroom Observer.

With reference to the other fungal genera and species found, species from the genus Cadophora wthe most abundant and amounted to 20% of all identified fungal samples. Furthermore, Hypochniciellium species accounted for 13% of the total sample count and Phialocephala 7%. Pholiota, as a genus, contributed only to 4% of the total number of records. Importantly, it was also found that many of the historic timbers were extensively decayed by the same fungi at both sites, inferring potentially a long-standing decay arising from a fungal metapopulation on the island. Decayed timbers were found most observably around the locations where the timber was in contact with the soil, perhaps due to a higher moiture content within the wood facilitating for more effective hyphal ingression into the timbers and the localised warming of soils because of volcanic activity. At the Chilean base, white rots of the sampled timbers were found only just beneath the soil surface, with brown and soft rots being identified on timber from both sites in wood exposed to ambient conditions.

As alluded to within the preceding text, it is highly probable that the fungal isolates from the two sites were introduced alongside human migration to Deception Island. Certainly, there have been plenty of opportunities for spores to be deposited on the island, given the whaling and research activities over the past two centuries. Importantly, the current phenomenon of tourism to the island will facilitate potentially in the emergence of new fungal species, which makes future research prospects exciting as the inherent isolation of the site would have rendered it almost impossible for exotic fungi to have otherwise arrived on site and – assuming they had – there would have been no timber for them to colonise. In this respect, the research undertaken on this island outlines a very critical biosecurity risk: human migration.

A further aspect of interest from the results is that native Ascomycetous fungi to the island, which were found to be acting saprotrophically on native plants, broadened their host range to that of the exotic timbers introduced. Thus, the notion of fungal adaptation alongside a change in the potential inoculum base is given credence, which can again be related to current issues with fungal pathogens of trees within Europe and further afield.

Source: Held, B. & Blanchette, R. (2017) Deception Island, Antarctica, harbors a diverse assemblage of wood decay fungi. Fungal Biology. 121 (2). p145-157.

Wood-decay fungi in the Antarctic Peninsula

Some fungal finds from the week

Some say it’s written in the stars, though the only experience I have had with braille is from select old Nintendo games from the 1990s and early 2000s (revealing my age a little here!). Others say it’s just annoying. I’d probably agree with the latter! Regardless, here we have it: more pictures of fungi on trees.

As always, I keep my eye out for some interesting finds. This week has been pretty decent on the fungal side of things, though given the time of year only the perennial polypores are really observable – asides from the odd Flammulina velutipes / elastica and some enterprising Pleurotus species. Nonetheless, for the sake of showcasing unique finds and for educational purposes, here are a few species of polypore and some common agarics.

Firstly, we have a rather cool deck of Ganoderma resinaceum brackets around a rather pronounced buttress on an oak (Quercus robur). The fruiting between the two buttress roots is likely indicative of good reaction growth that is well-compartmentalised, which in turn infers respectable and probably sound (i.e. free of appreciable decay) buttressing from which the oak is supporting itself. We then have some shots of a rather aberrant duo of Trametes gibbosa on what is probably an old sycamore (Acer pseudoplatanus) stump, some Kretzschmaria deusta on (again!) sycamore, Ganoderma australe on a fallen ash (Fraxinus excelsior) and finally some Flammulina sp. and Pleutorus ostreatus on a very decayed stump of an unknown deciduous broadleaved species.

ganoderma-resinaceum-quercus-robur-buttress-1ganoderma-resinaceum-quercus-robur-buttress-2ganoderma-resinaceum-quercus-robur-buttress-3

trametes-gibbosa-stump-acer-2trametes-gibbosa-stump-acer-3trametes-gibbosa-stump-acer-4

acer-pseudoplatanus-kretzschmaria-deusta-monolith-1acer-pseudoplatanus-kretzschmaria-deusta-monolith-2acer-pseudoplatanus-kretzschmaria-deusta-monolith-3

fraxinus-excelsior-ganoderma-australe-fallen-1fraxinus-excelsior-ganoderma-australe-fallen-2fraxinus-excelsior-ganoderma-australe-fallen-3fraxinus-excelsior-ganoderma-australe-fallen-4

flammulina-velutipes-pleutorus-ostreatus-stump-1flammulina-velutipes-pleutorus-ostreatus-stump-2flammulina-velutipes-pleutorus-ostreatus-stump-3

Some fungal finds from the week

Trees in the ecosystem pt IV: Trees & arthropods

The arthropods are vast in terms of species, and include ants, beetles, butterflies, mites, moths, spiders, and so on. Therefore, covering the entire spectrum of arthropods in this section is impractical, though the general provisioning by trees will be outlined and species will be used to illustrate given examples.

Many arthropods are considered to be saproxylic in nature – they principally utilise dead woody material (both standing and fallen, in both dead and living trees) as habitat, for at least part of their life cycle, though they may also rely upon fungal sporophores associated with the presence of deadwood, as is to be detailed below (Gibb et al., 2006; Harding & Rose, 1986; Komonen et al., 2000). Of all the saproxylic arthropods, beetles are perhaps the most significant in terms of the proportion occupied of total saproxylic species worldwide (Müller et al., 2010), though saproxylic flies also feature in great numerical abundance (Falk, 2014; Harding & Rose, 1986).

Beetles may be either generalist or specialist in nature (on either broadleaved or coniferous hosts), and they will normally require a host with an abundance of deadwood (or large sections of coarse woody debris) usually over 7.5cm in diameter that resides within an area typically not heavily shaded (Müller et al., 2010; Siitonen & Ranius, 2015). This may be, in part, due to many beetle species (in their adult stage) requiring nectar from herbaceous plants, which would be lacking in woodland with significant canopy closure (Falk, 2014; Siitonen & Ranius, 2015). This means that veteran trees amongst wood pasture and parklands (including in urban areas) may be particularly suitable (Bergmeier & Roellig, 2014; Harding & Rose, 1986; Ramírez-Hernández et al., 2014; Jonsell, 2012; Jørgensen & Quelch, 2014), though this is not at all a steadfast rule as species may also be found abundantly in (perhaps more open) woodland, and particularly where there are large amounts of veteran trees and deadwood – around 60 cubic metres per hectare, according to Müller et al. (2010). Granted, they are found particularly in older (mature to veteran) trees, including within cavities that possess wood mould, water-filled rot holes, dead bark, exposed wood, sap flows, fruiting bodies (of fungi and slime moulds), mycelia of fungi, dead branches, and dead roots (Carpaneto et al., 2010; Falk, 2014; Harding & Rose, 1986; Siitonen & Ranius, 2015; Stokland et al., 2012). Beetle species may also not necessarily associate preferentially with a species (or group of species), but with the conditions aforementioned that are present within a tree (Harding & Rose, 1986; Jonsell, 2012). At times, preferable conditions may be an infrequent as one veteran tree in every hundred (Harding & Rose, 1986).

veteran-oak-tree
A veteran oak tree that is of prime habitat for a variety of organisms.

Despite this, species preference is observed. For broadleaved obligates, heavier shade may be more necessary, and in such instances there is a closer affinity of the beetles with fungal mycelium. Because fungi tend to produce more mycelium in cooler and more humid conditions (though this does, of course, vary with the species), the broadleaved obligates may therefore be found normally in greater abundance where conditions are more suited to fungal growth, and their presence may thus be associated with a canopy openness of as little as 20% (Bässler et al., 2010; Müller et al., 2010). This is, of course, not a steadfast rule, and many open wood pastures may support a great abundance of saproxylic beetles (Harding & Rose, 1986).

It is also important to recognise that many species of saproxylic beetle are reliant upon particular stages of the wood decay process. For instance, species that require fresh phloem tissue will only be able to colonise briefly in the first few summers following on from the death of the phloem tissue (Falk, 2014). Other species require significantly-decayed wood in a particular micro-climate, and even of a particular tree species (Harding & Rose, 1986). There also exist intricate associations between species of fungi and saproxylic insects. Inonotus hispidus, which is usually found upon ash, is the habitat for Triplax russica and Orchesia micans, whilst the coal fungus (Daldinia concentrica), also oft found upon the deadwood of ash (Fraxinus excelsior), is the main provider of habitat for Platyrhinus resinosus (Falk, 2014). The birch polypore (Fomitopsis betulina) is also host to numerous species of Coleoptera (Harding & Rose, 1986); as is the polypore Fomitopsis pinicola (Jonsson & Nordlander, 2006; Komonen, 2003; Komonen et al., 2000). This means that these species may be found where there is a suitable population of the fungus’ host species, where sporophores are present and will likely fruit again in the future, across numerous trees, and for many years. Most beetle species rely on oak more so than other tree species however, as oak generally lives for much longer and thus provides a wider array of different micro-habitats, and possesses increased compositional complexity as a result (Harding & Rose, 1986; Siitonen & Ranius, 2015).

ancient_orchard_malus_inonotus_hispidus4
A fruiting body of Inonotus hispidus on apple (Malus sp.). This fungus not only creates habitat in the wood that it degrades but also is a direct habitat through its sporophore.

Therefore, the loss of suitable habitat through active management programmes (including logging, and felling trees for safety reasons in urban areas) will have a very adverse impact upon saproxylic beetles, though also certain species of moth, and even species associated with saproxylic insects, including parasitic wasps, solitary wasps (which use beetle bore holes for habitat), and predatory Coleoptera (Harding & Rose, 1986; Komonen et al., 2000). Curiously, research by Carpaneto et al. (2010) concluded that trees that were ranked as the most evidently ‘hazardous’ were host to the most saproxylic beetle species, and their removal would therefore have a drastic impact upon local populations. Similarly, fragmentation of woodland patches suitable for saproxylic populations has led to a decline in the meta-populations (Grove, 2002; Komonen et al., 2000), as has deadwood removal in a managed site itself (Gibb et al., 2006). Interestingly, though not surprisingly, ‘deadwood fragmentation’ also has an adverse impact upon saproxylic insect populations (Schiegg, 2000).

Both ants and termites also benefit from the presence of deadwood. With regards to both, nests will usually form at the base of a tree or at an area where there is at least moderate decay – enough to support a viable population (Jones et al., 2003; Shigo, 1986; Stokland et al., 2012). Ants and termites both follow CODIT (compartmentalisation of damage in trees) patterns in relation to how their nests progress, and thus their territory will increase as fungal decay propagates further into the host. Ants will not feed on the decaying wood of the host however, and will simply use the decaying site as a nesting area. Conversely, termites will feast upon decayed wood and essentially control (perhaps by slowing down) the spread of fungal decay in a manner that provides as much longevity of the host as possible for a viable nesting site (Shigo, 1986). In tropical rainforests, termites are in fact considered to be one of the principal means of wood decomposition (Mori et al., 2014), and thus the provisioning of deadwood habitat is absolutely critical. Without decaying wood within trees therefore, ants and particularly termites will lack a potential habitat, and thus where a stand is actively managed populations may be markedly reduced (Donovan et al., 2007; Eggleton et al., 1995). Of course, termites are not necessarily to be desired when they are invading the wood structure of a property, and therefore deadwood is not universally beneficial (Esenther & Beal, 1979; Morales-Ramos & Rojas, 2001) – at least, when human properties are involved.

termites_1_007
Ecologically beneficial? Yes. Economically beneficial? No. Termites can – and do – damage timber-frames buildings, as is the case here. Source: Pestec.

The presence of deadwood may also be beneficial for ground-nesting and leaf-litter dwelling spiders, which can utilise downed woody debris (particularly pieces with only slight decay) for both nesting and foraging (Varady-Szabo & Buddle, 2006). In fact, research by Buddle (2001) suggested that such spiders may more routinely utilise downed woody material when compared to elevated woody material (dead branches and telephone poles) because of the greater array of associated micro-habitats, and particularly at certain life stages – such as during egg-laying, for females (Koch et al., 2010). Furthermore, as fallen woody debris can help to retain leaf litter (or even facilitate in the build-up leaf litter), spider populations are more abundant and more diverse in sites where such woody debris is present (Castro & Wise, 2010). Therefore, where woodlands are managed and areas are clear-cut, spider populations may be markedly reduced in terms of the diversity of species. However, generalist species may benefit from the amount of cut stumps (Pearce et al., 2004). Curiously, Koch et al. (2010) suggest that spiders may perhaps benefit from woodland clearance, because the vigorous re-growth of trees and the higher light availability to the woodland floor (promoting herbaceous plant growth) increases the abundance of potential prey. Despite this, old-growth species will suffer (Buddle & Shorthouse, 2008), and thus the population structure of spider populations may dramatically change.

Soil mites are a further group that benefit from coarse woody debris, though also from hollows and holes throughout the basal region of a tree (including water-filled cavities), and from fungal sporophores and hyphae associated with wood decay (Fashing, 1998; Johnston & Crossley, 1993). Typically, termites will use fungi and insects found within the wood as a food source, and the wood structure itself will provide for an array of niche micro-habitats that are critical at different life stages of a mite. Certain mite species are obligates that associate with coarse woody debris exclusively, and may in fact only be associated with certain species’ woody debris. Additionally, mites may utilise woody debris and hollows within trees to parasitise upon other species using the ‘resource’, with both lizards and snakes being parasitised by mites following their frequenting of such resources. Beetles may also be parasitised, though the mite in such an instance may use the beetle as a means of entry into woody debris (Norton, 1980).

It is not just deadwood that arthropods will utilise, however. Foliage, both alive and abscised, is also of use (Falk, 2014). For example, the ermine moth (Yponomeutidae) will rely upon the living foliage of a host tree as a food source, and the bird cherry ermine moth (Yponomeuta evonymella) is one example of this. During late spring, larvae will fully defoliate their host Prunus padus, before pupating, emerging, and then laying eggs upon the shoots ready for the following year (Leather & Bland, 1999). Many other moth species will, during their larval stage, also behave in such a manner and thus defoliate their host – either entirely, or in part (Herrick & Gansner, 1987). Other species may alternatively have larvae mine into the leaf and feed upon the tissues within (Thalmann et al., 2003), such as horse chestnut leaf miner (Cameraria ohridella). Flies, including the holly leaf-miner (Phytomyza ilicis), will also mine leaves in a similar fashion (Owen, 1978). Ultimately however, the same purpose is served – the insect uses the living tissues of a leaf to complete its life cycle, and fuel further generations.

1280px-yponomeuta_evonymella_on_prunus_padus
Bird cherry ermine moth having defoliated an entire tree. Source: Wikimedia.

Fallen leaf litter, as briefly touched upon earlier when discussing spiders, may also be of marked benefit to many arthropods. Ants, beetles, and spiders are but three examples of groups that will utilise leaf litter as a means of habitat (Apigian et al., 2006). Beetles will, for instance, rely upon leaf litter to attract potential prey, though also to provide niche micro-climates that remain relatively stable in terms of humidity, light availability, and temperature (Haila & Niemelä, 1999). Their abundance may, according to Molnár et al., (2001) be greatest at forest edges, perhaps because prey is most abundant at these edge sites (Magura, 2002). Of course, this does not mean that edges created through artificial means will necessarily improve beetle populations, as research has shown that there are few ‘edge specialists’ and therefore populations usually will go into decline where there has been significant disturbance. Unless management mimics natural mortality events of forest trees, then constituent beetle populations may thus suffer adversely (Niemelä et al., 2007).

With regards to ants, Belshaw & Bolton (1993) suggest that management practices may not necessarily impact upon ant populations, though if there is a decline in leaf litter cover then ants associated with leaf litter presence may go into – perhaps only temporary (until leaf litter accumulations once again reach desirable levels) – decline (Woodcock et al., 2011). For example, logging within a stand may reduce leaf litter abundance for some years (Vasconcelos et al., 2000), as may (to a much lesser extent) controlled burning (Apigian et al., 2006; Vasconcelos et al., 2009), though in time (up to 10 years) leaf litter may once again reach a depth suitable to support a wide variety of ant species. However, the conversion of forest stands into plantations may be one driver behind more permanently falling ant populations (Fayle et al., 2010), as may habitat fragmentation (Carvalho & Vasconcelos, 1999) – particularly when forest patches are fragmented by vast monoculture plantations of tree or crop (Brühl et al., 2003). The conversion of Iberian wood pastures to eucalyptus plantations is one real world example of such a practice (Bergmeier & Roellig, 2014).

Also of benefit to many arthropods are nectar and pollen. Bees, beetles, butterflies, and hoverflies will, for instance, use nectar from flowers as a food source (Dick et al., 2003; Kay et al., 1984), and generally (but not always) a nectar source will lack significant specificity in terms of the insect species attracted (Karban, 2015). Despite this, different chemicals secreted by different flowers, and the toxicity of certain nectar sources to particular insects, means certain tree species may only be visited by certain insect species (Adler, 2000; Rasmont et al., 2005). Tree diversity may therefore be key to sustaining healthy insect populations (Holl, 1995), and where species may prefer to frequent herbaceous plant species the presence of a diverse woodland canopy above may still be very influential (Kitahara et al., 2008). This may be because a diverse array of woody plant species increases the diversity of herbaceous species. At times, pollen may also be a reward, as may (more rarely) a flower’s scent. Karban (2015) remarks that all are collectively dubbed as ‘floral rewards’.

References

Adler, L. (2000) The ecological significance of toxic nectar. Oikos. 91 (3). p409-420.

Apigian, K., Dahlsten, D., & Stephens, S. (2006) Fire and fire surrogate treatment effects on leaf litter arthropods in a western Sierra Nevada mixed-conifer forest. Forest Ecology and Management. 221 (1). p110-122.

Bässler, C., Müller, J., Dziock, F., & Brandl, R. (2010) Effects of resource availability and climate on the diversity of wood‐decaying fungi. Journal of Ecology. 98 (4). p822-832.

Belshaw, R. & Bolton, B. (1993) The effect of forest disturbance on the leaf litter ant fauna in Ghana. Biodiversity & Conservation. 2 (6). p656-666.

Bergmeier, E. & Roellig, M. (2014) Diversity, threats, and conservation of European wood-pastures. In Hartel, T. & Plieninger, T. (eds.) European wood-pastures in transition: A social-ecological approach. UK: Earthscan.

Brühl, C., Eltz, T., & Linsenmair, K. (2003) Size does matter–effects of tropical rainforest fragmentation on the leaf litter ant community in Sabah, Malaysia. Biodiversity & Conservation. 12 (7). p1371-1389.

Buddle, C. (2001) Spiders (Araneae) associated with downed woody material in a deciduous forest in central Alberta, Canada. Agricultural and Forest Entomology. 3 (4). p241-251.

Buddle, C. & Shorthouse, D. (2008) Effects of experimental harvesting on spider (Araneae) assemblages in boreal deciduous forests. The Canadian Entomologist. 140 (4). p437-452.

Carpaneto, G., Mazziotta, A., Coletti, G., Luiselli, L., & Audisio, P. (2010) Conflict between insect conservation and public safety: the case study of a saproxylic beetle (Osmoderma eremita) in urban parks. Journal of Insect Conservation. 14 (5). p555-565.

Carvalho, K. & Vasconcelos, H. (1999) Forest fragmentation in central Amazonia and its effects on litter-dwelling ants. Biological Conservation. 91 (2). p151-157.

Castro, A. & Wise, D. (2010) Influence of fallen coarse woody debris on the diversity and community structure of forest-floor spiders (Arachnida: Araneae). Forest Ecology and Management. 260 (12). p2088-2101.

Dick, C., Etchelecu, G., & Austerlitz, F. (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology. 12 (3). p753-764.

Donovan, S., Griffiths, G., Homathevi, R., & Winder, L. (2007) The spatial pattern of soil‐dwelling termites in primary and logged forest in Sabah, Malaysia. Ecological Entomology. 32 (1). p1-10.

Eggleton, P., Bignell, D., Sands, W., Waite, B., Wood, T., & Lawton, J. (1995) The species richness of termites (Isoptera) under differing levels of forest disturbance in the Mbalmayo Forest Reserve, southern Cameroon. Journal of Tropical Ecology. 11 (1). p85-98.

Esenther, G. & Beal, R. (1979) Termite control: decayed wood bait. Sociobiology. 4 (2). p215-222.

Falk, S. (2014) Wood-pastures as reservoirs for invertebrates. In Hartel, T. & Plieninger, T. (eds.) European wood-pastures in transition: A social-ecological approach. UK:     Earthscan.

Fashing, N. (1998) Functional morphology as an aid in determining trophic behaviour: the placement of astigmatic mites in food webs of water-filled tree-hole communities. Experimental & Applied Acarology. 22 (8). p435-453.

Fayle, T., Turner, E., Snaddon, J., Chey, V., Chung, A., Eggleton, P., & Foster, W. (2010) Oil palm expansion into rain forest greatly reduces ant biodiversity in canopy, epiphytes and leaf-litter. Basic and Applied Ecology. 11 (4). p337-345.

Gibb, H., Pettersson, R., Hjältén, J., Hilszczański, J., Ball, J., Johansson, T., Atlegrim, O., & Danell, K. (2006) Conservation-oriented forestry and early successional saproxylic beetles: responses of functional groups to manipulated dead wood substrates. Biological Conservation. 129 (4). p437-450.

Grove, S. (2002) Saproxylic insect ecology and the sustainable management of forests. Annual Review of Ecology and Systematics. 33 (1). p1-23.

Haila, Y. & Niemelä, J. (1999) Leaf litter and the small‐scale distribution of carabid beetles (Coleoptera, Carabidae) in the boreal forest. Ecography. 22 (4). p424-435.

Harding, P. & Rose, F. (1986) Pasture-Woodlands in Lowland Britain: A review of their importance for wildlife conservation. UK: NERC.

Herrick, O. & Gansner, D. (1987) Gypsy moth on a new frontier: forest tree defoliation and mortality. Northern Journal of Applied Forestry. 4 (3). p128-133.

Holl, K. (1995) Nectar resources and their influence on butterfly communities on reclaimed coal surface mines. Restoration Ecology. 3 (2). p76-85.

Jones, D., Susilo, F., Bignell, D., Hardiwinoto, S., Gillison, A., & Eggleton, P. (2003) Termite assemblage collapse along a land‐use intensification gradient in lowland central Sumatra, Indonesia. Journal of Applied Ecology. 40 (2). p380-391.

Jonsell, M. (2012) Old park trees as habitat for saproxylic beetle species. Biodiversity and Conservation. 21 (3). p619-642.

Jonsell, M. & Nordlander, G. (2004) Host selection patterns in insects breeding in bracket fungi. Ecological Entomology. 29 (6), p697-705.

Johnston, J. & Crossley, D. (1993) The significance of coarse woody debris for the diversity of soil mites. In McMinn, J. & Crossley, D. (eds.) Proceedings of the Workshop on Coarse Woody Debris in Southern Forests: Effects on Biodiversity. General Technical Report SE-94.

Jørgensen, D. & Quelch, P. (2014) The origins and history of medieval wood-pastures. In Hartel, T. & Plieninger, T. (eds.) European wood-pastures in transition: A social-ecological approach. UK: Earthscan.

Karban, R. (2015) Plant Sensing & Communication. USA: University of Chicago Press.

Kay, Q., Lack, A., Bamber, F., & Davies, C. (1984) Differences between sexes in floral morphology, nectar production and insect visits in a dioecious species, Silene dioica. New Phytologist. 98 (3). p515-529.

Kitahara, M., Yumoto, M., & Kobayashi, T. (2008) Relationship of butterfly diversity with nectar plant species richness in and around the Aokigahara primary woodland of Mount Fuji, central Japan. Biodiversity and Conservation. 17 (11). p2713-2734.

Koch, J., Grigg, A., Gordon, R., & Majer, J. (2010) Arthropods in coarse woody debris in jarrah forest and rehabilitated bauxite mines in Western Australia. Annals of Forest Science. 67 (1). p106-115.

Komonen, A. (2003) Distribution and abundance of insect fungivores in the fruiting bodies of Fomitopsis pinicola. Annales Zoologici Fennici. 40 (6). p495-504.

Komonen, A., Penttilä, R., Lindgren, M., & Hanski, I. (2000) Forest fragmentation truncates a food chain based on an old-growth forest bracket fungus. Oikos. 90 (1). p119-126.

Leather, S. & Bland, K. (1999) Naturalists’ Handbook 27: Insects on cherry trees. UK: The Richmond Publishing Co. Ltd.

Magura, T. (2002) Carabids and forest edge: spatial pattern and edge effect. Forest Ecology and Management. 157 (1). p23-37.

Molnár, T., Magura, T., Tóthmérész, B., & Elek, Z. (2001) Ground beetles (Carabidae) and edge effect in oak-hornbeam forest and grassland transects. European Journal of Soil Biology. 37 (4). p297-300.

Morales-Ramos, J. & Rojas, M. (2001) Nutritional Ecology of the Formosan Subterranean Termite (Isoptera: Rhinotermitidae) – Feeding Response to Commercial Wood Species. Journal of Economic Entomology. 94 (2). p516-523.

Mori, S., Itoh, A., Nanami, S., Tan, S., Chong, L., & Yamakura, T. (2014) Effect of wood density and water permeability on wood decomposition rates of 32 Bornean rainforest trees. Journal of Plant Ecology. 7 (4). p356-363.

Müller, J., Noss, R., Bussler, H., & Brandl, R. (2010) Learning from a “benign neglect strategy” in a national park: Response of saproxylic beetles to dead wood accumulation. Biological Conservation. 143 (11). p2559-2569.

Norton, R. (1980) Observations on phoresy by oribatid mites (Acari: Oribatei). International Journal of Acarology. 6 (2). p121-130.

Niemelä, J., Koivula, M., & Kotze, D. (2007) The effects of forestry on carabid beetles (Coleoptera: Carabidae) in boreal forests. Journal of Insect Conservation. 11 (1). p5-18.

Owen, D. (1978) The effect of a consumer, Phytomyza ilicis, on seasonal leaf-fall in the holly, Ilex aquifolium. Oikos. 31 (2). p268-271.

Pearce, J., Venier, L., Eccles, G., Pedlar, J., & McKenney, D. (2004) Influence of habitat and microhabitat on epigeal spider (Araneae) assemblages in four stand types. Biodiversity & Conservation. 13 (7). p1305-1334.

Ramírez-Hernández, A., Micó, E., de los Ángeles Marcos-García, M., Brustel, H., & Galante, E. (2014) The “dehesa”, a key ecosystem in maintaining the diversity of Mediterranean saproxylic insects (Coleoptera and Diptera: Syrphidae). Biodiversity and Conservation. 23 (8). p2069-2086.

Rasmont, P., Regali, A., Ings, T., Lognay, G., Baudart, E., Marlier, M., Delcarte, E., Viville, P., Marot, C., Falmagne, P., & Verhaeghe, J. (2005) Analysis of pollen and nectar of Arbutus unedo as a food source for Bombus terrestris (Hymenoptera: Apidae). Journal of Economic Entomology. 98 (3). p656-663.

Schiegg, K. (2000) Are there saproxylic beetle species characteristic of high dead wood connectivity?. Ecography. 23 (5). p579-587.

Shigo, A. (1986) A New Tree Biology. USA: Shigo and Trees Associates.

Siitonen, J. & Ranius, T. (2015) The Importance of Veteran Trees for Saproxylic Insects. In Kirby, K. & Watkins, C. (eds.) Europe’s Changing Woods and Forests: From Wildwood to Managed Landscapes. UK: CABI.

Stokland, J., Siitonen, J., & Jonsson, B. (2012) Biodiversity in Dead Wood. UK: Cambridge University Press.

Thalmann, C., Freise, J., Heitland, W., & Bacher, S. (2003) Effects of defoliation by horse chestnut leafminer (Cameraria ohridella) on reproduction in Aesculus hippocastanum. Trees. 17 (5). p383-388.

Varady-Szabo, H. & Buddle, C. (2006) On the relationships between ground-dwelling spider (Araneae) assemblages and dead wood in a northern sugar maple forest. Biodiversity & Conservation. 15 (13). p4119-4141.

Vasconcelos, H., Pacheco, R., Silva, R., Vasconcelos, P., Lopes, C., Costa, A., & Bruna, E. (2009) Dynamics of the leaf-litter arthropod fauna following fire in a neotropical woodland savanna. PLoS One. 4 (11). p1-9.

Vasconcelos, H., Vilhena, J., & Caliri, G. (2000) Responses of ants to selective logging of a central Amazonian forest. Journal of Applied Ecology. 37 (3). p508-514.

Woodcock, P., Edwards, D., Fayle, T., Newton, R., Khen, C., Bottrell, S., & Hamer, K. (2011) The conservation value of South East Asia’s highly degraded forests: evidence from leaf-litter ants. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 366 (1582). p3256-3264.

Trees in the ecosystem pt IV: Trees & arthropods