Lunch in the tree-tops for the birds and the bugs

A few weeks ago, our laboratory published a paper in PeerJ (an open-access journal) titled “Vertical heterogeneity in predation pressure in a temperate forest canopy“. This work resulted from a project by former Master’s student Kathleen Aikens. She graduated a little while ago, and although we published one of her thesis chapters in 2012, it took another year to get this paper out, in part because Kathleen and I both become too busy.  Thankfully, post-doc Dr. Laura Timms agreed to help us finish up the paper, and she worked with me and Kathleen to re-analyze the data, re-write some sections, and whip it into shape.

As is now traditional for my laboratory, here’s a plain-language summary of the paper:

Tree canopies, including those in deciduous forests in southern Quebec, are important for many different animals, including insects and spiders. These small, marvelous creatures crawl up and down trees with regularity, feed upon the leaves of trees, feed upon each other, and are food for animals such as birds and bats. Past research has shown that many species of insects and spiders live in tree canopies, and in general, more insects and spiders are found closer to the ground compared to the very tops of the trees. This makes sense, since deciduous tree canopies often need to be recolonized each spring, and tree canopies are relatively harsh environments – they are windy, hot, and often-dry places as compared to the forest floor.  What we don’t know, however, is whether the insects and spiders avoid the tree canopies because they may be eaten more frequently in the canopy as compared to the understory. The objective of this research was to test this question directly, and find out whether insects and spiders are arranging themselves, vertically, because predators may be preferentially feeding on them along this vertical gradient. This is a very important area of study since biodiversity is highly valued and important in forests, but we cannot fully appreciate the status of this diversity without discovering what controls it.

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Our mobile aerial lift platform. TO THE CANOPY!

We did this work by using two experiments that involved manipulating different factors so we could get at our question in the most direct way possible. In the first experiment, we made ‘cages’ out of chicken wire and enclosed branches of sugar maple trees in the cages. We did this at the ground level all the way to the tops of trees, using a ‘mobile aerial lift platform’. These cages acted to keep out large predators, such as birds, but allowed insects and spiders to live normally on the vegetation. We counted, identified, and tracked the insects and spiders both within these cages, and in adjacent branches that did not have cages (the ‘control’). By comparing the control to the cage, we could find out whether feeding activity by larger vertebrate predators affected insects and spiders, and whether this differed when comparing the ground to the top of the trees. In the second experiment, we used small pins and attached live mealy worms (larvae of beetles) to the trunks of trees, and we did this in the understory all the way up to the canopy. We watched what happened to these mealy worms, and compared what happened during the day and overnight. This is called a ‘bait trial’, and let us figure out what sort of predators are out there in the environment, and in our case, whether they fed more often in the canopy compared to the ground-level. This second experiment was designed for seeing the effects of insect and spider predators along a vertical gradient whereas the first experiment was focused more on vertebrate predators (e.g., birds).

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Munch munch. Carpenter ants feeding on mealworms.

Our results from the first experiment showed that the cages had an effect: more insects and spiders were found when they were protected from predation by birds. Birds are playing a big role in forest canopies: they are feeding on insects and spiders, and in the absence of vertebrate predators, you might speculate more insects and spiders would occupy trees. Our second experiment showed that ants were important predators along the tree trunks, and overall, the most invertebrate predators were found in the lower canopy. Both experiments, together, confirmed that the understory contained the most insects and spiders, and was also the place with the highest amount of predation pressure.  The take-home message is that there is an effect of predation on insects and spiders in deciduous forests, and this effect changes if you are in the understory as compared to the top of the canopy. We also learned and confirmed that insects and spiders remain a key element of a ‘whole tree’ food web that includes vertebrates such as birds, and that predators in trees tend to feed on insects and spiders along a gradient. Where there is more food, there is more predation pressure! Our work was unique and novel because this is the first time a study of predation pressure was done along a vertical gradient in deciduous forests. It will help better guide our understanding of forest biodiversity, and the processes that govern this diversity.

A more detailed discussion of this work is posted on the PeerJ blog.

Spiders as catalysts for ecosystem development

It is well known that spiders are effective at dispersal and colonization, in part because of their ability to ‘balloon‘ – small spiders (i.e., immature specimens, or adults of species that are small) will release a strand of silk and let the wind pick them up and carry them far distances.  This passive ability to disperse has served spiders well, and enabled them to be among the first animals to colonize new habitats.  For example, after the eruption of Mount St Helens, the depopulated Pumice Plain was re-colonized over time, and biologists kept an eye on what was dropping from the skies.  Not surprising (to me!) was that spiders represented a lot of this ‘aerial plankton‘ – Crawford et al. (1995) reported that spiders represented “23% of windblown arthropod fallout and contributed 105 individuals per square meter“.

A spider about to launch!  Photo by Bryan Reynolds, reproduced here with permission. Please visit his work!

A spider about to launch! Photo by Bryan Reynolds, reproduced here with permission.

Many, many people have recognized this amazing ability of spiders to get to places effectively and quickly.  During his voyages on the HMS Beagle, Darwin observed and commented on this. He noticed spiders landing on the ship when they were far offshore.  Here’s a lovely quote:

      These, glittering in the sunshine, might be compared to diverging rays of light; they were not, however, straight, but in undulations like films of silk blown by the wind.

-Charles Darwin, Voyage of the Beagle, 1832

A wonderful paper titled “Distribution of Insects, Spiders, and Mites in the Air” (Glick 1939) also discusses aerial plankton. In this work, Glick reports on how a plane was used to collect arthropods in the skies – this was done by modifying the plane so it had a collection net attached to it.  Spiders were among the most commonly collected taxa, and were found up to 15,000 ft in altitude.   Glick followed this up with work published in 1957, and spiders were again reported as common aerial plankton.

Convinced?  Spiders really are everywhere and can get anywhere – from dominating the tundra, to floating far above as tiny eight-legged aeronauts.

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This takes me (finally) to the point of this post, and some reflection about a paper by Hodkinson et al. (2001), titled “What a wonderful web they weave: spiders, nutrient capture and early ecosystem development in the high Arctic – some counter-intuitive ideas on community assembly”.  In this work, the authors provide some data about aerial plankton in a series of sites representing different stages of succession in Midtre Lovénbreen – a ‘small valley’ glacier in Spitsbergen (a Norwegian high Arctic Island).   This forum paper was meant to present an idea about ecosystem development in the Arctic, with a focus on spiders and other aerial plankton and their relationship to nutrients.

  • Spiders are among the first to arrive due to their amazing abilities at dispersal and colonization.
  • Many spiders will just die, and their sad, little bodies will decompose and leave behind nutrients.
  • Many of the spider species that arrive will build webs, and the silk contains many nutrients. Regardless of whether the silk successfully captures prey, the silk will eventually be a hot-spot of nutrients.
  • A lot of other aerial plankton will hit these webs – this will include other arthropods (Hodkinson et al. rightfully point out the importance of Chironomids, or midges, as key prey for spiders in the north) and these prey may or may not be eaten by spiders.  The aerial plankton also includes other ‘debris’ that would be floating around (fungal spores, dirt, etc).  The webs capture all these goodies, and act as a concentrated area for a growing soup of nutrients.
  • The spider webs will collect moisture.  In Arctic systems, dry polar-deserts, and many other newly created habitats, the accumulation of moisture is rather essential for continued ecosystem development.

Taken together, Hodkinson et al. (2001) argue that spiders and their webs represent little pockets of concentrated nutrients in landscapes that are void of much other life.  These hotspots could be catalysts for ecosystem development in systems that are starting from scratch.  I really like this idea – not only does is stir up the imagination (little spiders gently falling from the sky, landing on habitat never before touched by animals, and providing the start of an ecosystem…), it really makes some biological sense.  Ecosystem development requires nutrients and substrates – of course, these would both be available without spiders, but our eight-legged friends are helping move things a long a little more quickly.

The paper by Hodkinson et al. has been cited less than I would have expected.   Although they don’t provide any experimental data, their ideas are interesting and relevant and should be studied in detail. Recently, a few papers have come out that are taking the ideas to the next level.  Konig et al. (2011) studied arthropods of glacier foregrounds in the Alps. They found that although Collembola and other ‘decomposers’ are quite important in early successional stages, overall, generalist predators (including spiders) were dominant and using stable isotope analyses, they showed that these generalist predators often ate each other – an interaction known as intraguild predation.

I often discuss Hodkinson et al.’s (2001) paper in lectures, and invariably I get the question “If spiders are first to arrive, what do they eat?“. I typically answer that spiders eat other spiders, and it’s reassuring to see literature that supports this claim.  In turn, intraguild predation itself contributes further to the accumulation of nutrients (more sad, little spider bodies littering the landscape…).

Placing this work in a more general framework, these ideas are pointing to the increased importance of predators in overall nutrient dynamics in ecosystems. I was thrilled to see a paper by Schmitz et al. (2010) that argues “predators can create heterogeneous or homogeneous nutrient distributions across natural landscapes“. Bingo. This is exactly what Hodkinson et al. were arguing – predators, such as spiders, can arrive quickly to an area, and in the context of newly formed ecosystems, may provide a hotspot for nutrients in an otherwise desolate landscape.

Although the Hodkinson et al. paper is over a decade old, it’s still relevant, and quite important. I suspect that if more newly created habitats are studied in detail, spiders will indeed prove to be catalysts for ecosystem development.

References:

Crawford, R., Sugg, P., & Edwards, J. (1995). Spider Arrival and Primary Establishment on Terrain Depopulated by Volcanic Eruption at Mount St. Helens, Washington American Midland Naturalist, 133 (1) DOI: 10.2307/2426348

Hodkinson, I., Coulson, S., Harrison, J., & Webb, N. (2001). What a wonderful web they weave: spiders, nutrient capture and early ecosystem development in the high Arctic – some counter-intuitive ideas on community assembly Oikos, 95 (2), 349-352 DOI: 10.1034/j.1600-0706.2001.950217.x

König, T., Kaufmann, R., & Scheu, S. (2011). The formation of terrestrial food webs in glacier foreland: Evidence for the pivotal role of decomposer prey and intraguild predation Pedobiologia, 54 (2), 147-152 DOI: 10.1016/j.pedobi.2010.12.004

Schmitz, O., Hawlena, D., & Trussell, G. (2010). Predator control of ecosystem nutrient dynamics Ecology Letters, 13 (10), 1199-1209 DOI: 10.1111/j.1461-0248.2010.01511.x

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A special thanks to Bryan Reynolds for permission to use his photograph of the dispersing Pisaurid spider.  Please visit his work here.

Assessing five decades of change in a high Arctic parasitoid community

As my colleague Terry Wheeler mentioned on his blog, our Northern Biodiversity Program team is thrilled to see post-doc Laura Timms‘s paper about Arctic parasitoid wasps published in Ecography!  Our team worked on Ellesmere Island, Nunavut, in 2010, and compared parasitoid wasps to historical collections from the same site that were made in 1961-65, 1980-82, and 1989-92. Parasitoid wasps are at the top of the insect food chain: they lay eggs inside or on top of other arthropods and the wasp larvae emerge after consuming their hosts – a gruesome but very common lifestyle for many types of wasps.  Species at higher trophic levels, such as these parasitoid wasps, are often the first to respond to new environmental pressures, including the climate change that is occurring rapidly in Arctic systems.

Laura identified a LOT of wasps, recorded the type of host attacked (e.g. plant-feeding hosts versus hosts that are predators), and the body size of two species of wasps that were commonly collected in all time periods.  We found no clear pattern of change in most aspects of the parasitoid wasp community on Ellesmere Island over past 50 years, even though temperature and precipitation have increased significantly during the same period. However, there were some signs that parasitoids of plant-feeding insects may be more affected more than other groups: one common parasitoid species that was abundant in 1960s hasn’t been collected since then, and the community in the 2010 study contained fewer parasitoids of plant-feeding insects than previous studies.

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Some members of the Northern Biodiversity Program working in the Yukon in 2012. (l-r, Chris Buddle, Laura Timms, Crystal Ernst and Katie Sim)

Laura takes it as a good sign that no major changes in the ecology of the high Arctic parasitoid community have been observed, but isn’t taking it for granted that the community will remain unaffected for long.  At 82°N, Ellesmere Island is relatively isolated, but other research has found that parasitoid communities further south are changing dramatically (Fernandez-Triana et al 2011).

Laura has the following comment about our work: “We hope that our findings will be used as baseline data for ongoing monitoring on Ellesmere Island”, said Timms.  “We know so little about these high Arctic insect communities, we should learn as much as possible about them while they are still intact.

References

Timms, L., Bennett, A., Buddle, C., & Wheeler, T. (2013). Assessing five decades of change in a high Arctic parasitoid community Ecography DOI: 10.1111/j.1600-0587.2012.00278.x

Fernandez-Triana, J., Smith, M., Boudreault, C., Goulet, H., Hebert, P., Smith, A., & Roughley, R. (2011). A Poorly Known High-Latitude Parasitoid Wasp Community: Unexpected Diversity and Dramatic Changes through Time PLoS ONE, 6 (8) DOI: 10.1371/journal.pone.0023719

Arthropods in the tree-tops: Canopy ecology in Quebec (Part 3)

This is the final post in a three part series about studying canopy arthropods in Quebec.  Part 1 was about canopy access and Part 2 was about patterns of diversity.  This post is about ecological interactions in the canopy. 

I had the pleasure of supervising a M.Sc. student, Kathleen Aikens, who was keen to work on a canopy project that looked deeper into some of the ecological interactions occurring in our deciduous forest canopies.  This was possible since we had, by this time, acquired a lot of base-line data on arthropods in many strata of the forest.  Kathleen’s work included using exclosure cages to see whether or not bird predation might affect arthropods in the Canopy differently than in the understorey.   This was exciting work, as it took our laboratory in a new direction, and lets us start to unravel some of the complexities of the food-webs in the tree-tops.  Her main result was that birds did have a strong top-down effect on arthropods, and that effect did differ as a function of height.  Using some bait trials, we also found that predation by arthropods on arthropods was also stratified.   This research suggests that arthropods living in trees in our region of the world are always under significant predation pressure, from both vertebrate and invertebrate predators.

A cage experiment, to assess the effect of predators on insects living in the forest canopy.

More recently, my laboratory has started to collaborate closely with another group at McGill studying “ecosystem services” – this is work done with Elena Bennett, another colleague at McGill University.  The research framework with this project is about how different ecosystem services are affected by the fragmented landscape that occurs in a large region just south of Montreal.  Elena and I co-supervise a PhD student Dorothy Maguire, who is looking at the ecosystem function of insect herbivory, and studying how herbivory varies as a function of forest size and degree of isolation (i.e., from a large contiguous forest), and she is studying herbivory in the understorey as well as the canopy.  Herbivory is closely linked to ecosystem services because of its effect on nutrient cycling, forest aesthetics, and more.  Although this project is currently underway, Dorothy is uncovering some interesting results, already.  For example, she is finding that levels of insect herbivory differ between the understorey and the canopy, and that forest fragmentation is affecting insect herbivory.

Summary

I have provided some highlights of some of the work that our laboratory has done in Quebec’s deciduous forests (and my apologies to the students who I didn’t mention!).  Although we have come a long way, and uncovered some interesting research results, I still feel that the work is just beginning.  For example, the bulk of our work has been on only two tree species (Sugar Maple and American Beech), and we have only studied a fraction of the arthropods that exist in the canopies of our forests.  I would like to expand the research to include other plant-feeding guilds, bees and wasps.  I’m also always curious about the piles of dead and decaying leaves that we find nestled between the crotches of high branches – these micro-habitats surely contain suspended soil (e.g., see Lindo & Winchester 2007), and within those “islands” there should be a host of arthropods.   Not surprisingly, the forest canopies in southern Quebec are home to a marvelous diversity of arthropods.  It’s a scientist’s model system, and a delightful system in which to work and play.

Me (Chris Buddle) above the canopy at Mont St Hilaire!

A few reasons to study Arctic entomology

I’m a big fan of the Arctic, and I am on a mission to get more people interested in studying northern ecosystems.  In this post, I wanted to share some of the reasons why:

Poorly understood food-web

Arthropod-based food-webs in the Arctic are largely unknown.  This is a great research opportunity – our laboratory is working on this, and I am trying to put together an Arctic food-web from an arthropod perspective.    My PhD student Crystal Ernst is also thinking a lot about how high Arctic food webs are structured, and has some interesting ideas and thoughts in one of her previous posts.

Some of Crystal’s thinking about high arctic food-webs (reproduced here, with permission)

Look at all those spiders!

As most terrestrial Arctic biologists know, spiders are among the most common of the Arctic animals.  Our lab has documented that wolf spiders on the tundra occur at a high density, and the biology of Arctic wolf spiders is amazing.

An Arctic wolf spider (Lycosidae) female with egg sac, living on scree slopes of high elevation slopes, Bylot Island (Nunavut)

So, if you are an aspiring Arachnologist…head north!

Excellent base-line dat

Arctic Entomology has a long history of excellence.  Canada has been sending entomologist up to the Arctic for decades, perhaps most notably the Northern Insect Survey of the 1940s, 50s and 60s  – some information on that survey can be found here .  There has also been a lot of research at Lake Hazen, at the tip of Ellesmere Island (above 81 degrees N)  – earlier work reports over 200 species of Arthropods up at Hazen and a recent article in the Biological Survey of Canada’s newsletter, found here, does a nice job of summarizing the insect studies at Hazen (including our own work with the Northern Biodiversity Program).  These past studies provide an excellent baseline for current and future projects related to Arctic entomology – and you need a baseline to move forward.

The Arctic is changing

The Arctic is a very fragile and special environment, and one that is changing rapidly, in part because of climate change.  Permafrost is melting, tree-line is changing, glaciers are melting, and plant and animal assemblages are facing dramatic changes to their environments.  We must strive to document, quantify, and study the biology of life in the Arctic, and given the dominance of arthropods (i.e, diversity and abundance) in the north, they are a priority.  The time is NOW for Arctic entomology.

Biting flies:

If you have an interest in biting flies (and many people do, believe it or not!), the Arctic is the place for you.  Emerging from the tundra are thousands of flies, per hectare.  Many of them want your blood, and if they don’t get you during the day, they will be there at the end of the day, in your tent.

A host of biting flies, sitting between my tent and the tent fly. Just waiting for me to exit the tent and have a feast.

…and a couple of other reasons that have less to do with entomology:

Canada = Arctic 

We are a northern country, eh?  However, few of us spend much time in the “REAL” north.  From a biogeographic standpoint, we are a country without roads and people, but with a lot of boreal forest, tundra, and high arctic landscapes.

It is beautiful

The north is stunning; awesome landscapes, vistas that never end, big sky, large rivers, glaciers and mountains.

The stunning landscape of the Yukon Territory (Tombstone range)

Help Build an Arctic Food Web

A couple of weeks ago I was fortunate to be able to attend a workshop about monitoring terrestrial arthropod biodiversity in the Arctic. In advance of that workshop, I offered to prepare a draft of a food-web that was ‘Arthropod-centric’.  There are many ways to build a food-web, and my first draft was focused on who eats whom.  In other words, an arrow depicting interactions would indicate predation (loosely defined).  An alternative would be to focus on energy moving through the system (i.e., the arrow would move ‘up’ from trophic level to trophic level, to indicate a transfer of energy).

Putting this together is a challenging, yet rewarding process.   I consulted with many of my colleagues with expertise in Arctic systems (including the folks involved with our Northern Biodiversity Program), and I am struggling to find the right balance between generality and specificity.  Here’s a portion of the (draft) food-web, showing some of the interactions:

Part of an Arctic Food Web, with an Arthropod Focus

When working on this food web, some interesting generalities are emerging: First, the overall dominance of Diptera (flies).  This is certainly because they do everything (e.g., decomposers, pollinators, blood-feeders) and they are very diverse.   Second,  arthropods are integrators - meaning they connect different processes, and they bridge different systems (aquatic/terrestrial).  Third,  highly valued vertebrates  (and humans!) depend on arthropods (and/or are affected by them).

Does all of this pique your interest?  Want to help? Together with colleagues, I am seeking help as this food-web develops.  Send me an e-mail or drop a comment on this post and think about some of these questions and provide some feedback if you are so inclined:

….what interactions do you think are important in the Arctic, from an arthropod perspective?

….how can the interactions between vertebrates and invertebrates best be depicted?

….what interactions between humans and arthropods need to be included? (other than biting flies – that one is pretty obvious!)

….what ecological processes should be included in an Arctic food-web? 

There are other Arctic food-webs out there.   The Bear Island food-web is probably the best one that focuses on Arctic arthropods.  If you’ve not seen it, the paper by Ian Hodkinson and Stephen Coulson (2004) is worth a look.   That food-web is more specific than the one I am working on (it should be since it’s focused on a specific location and it can be because a lot of research has occurred there!).   I really like one of the last sentences in their paper: ...the Svalbard high Arctic terrestrial food web is far more complex than has previously been appreciated but further sections remain to be resolved.  Indeed!  I would argue that we need to develop these kind of specific food-webs from other locations in the Arctic, but to get there, we also need a general, broad overview that encapsulates the overall role and importance of Arthropods to the Arctic.  Hence the development of a general food web.

I’ll finish with some thoughts about using this blog as a platform for generating and refining ideas about this food web.  Last year I had a long discussion with my PhD student Crystal Ernst (aka the Bug Geek) about the use of social media in the creative thinking process.   Some parts of the discussion we had showed up in one of her posts about the role of social media in science.  There’s a nice quote in that post that really hits the nail on the head:

Social media is just another kind of “hallway talk…in a really, really, long hallway”. (Crystal attributes part of that quote to another fine blogger, Bug Girl)

Social media can be used effectively as a platform for soliciting feedback and generating ideas about science, including specific projects such as building a food-web diagram.   At this stage, I admit that I’m not ready to put the entire draft food-web in this post – it’s far too incomplete.  However, it is the perfect time to ask for help, and solicit ideas.

….I welcome your feedback.

Reference

D. Hodkinson, I., & J. Coulson, S. (2004). Are high Arctic terrestrial food chains really that simple? – The Bear Island food web revisited Oikos, 106 (2), 427-431 DOI: 10.1111/j.0030-1299.2004.13091.x

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Opening an ecological black box: entomopathogenic fungi in the Arctic

While visiting Alaska last week, I had the pleasure of meeting Niels M. Schmidt.  He is a community ecologist (from Aarhus University, Denmark), who studies Arctic sytems and he is one of the key people behind the Zackenberg Research Station in Greenland.   He told me about one of his recently published papers (authored by Nicolai V. Meyling, Niels M. Schmidt, and Jørgen Eilenberg) titled “Occurrence and diversity of fungal entomopathogens in soils of low and high Arctic Greenland” (published in Polar Biology).

An ecological black box: the tundra

By definition (from Wikipediaentomopathogenic fungi act as parasites of insects – these fungi can kill, or seriously disable insects.  I was amazed at this paper because I have never given much thought to fungal entomopathogens in the Arctic (despite knowing their prevalence in other ecosystems).    Could these fungi be ecologically important in Arctic?  I think Arctic community ecology has been seriously understudied, and we know little about what drives the relative abundance of species.  From an arthropod perspective, we know that some birds depend  on Arthropods for food (e.g. see Holmes 1966), and that flies are important nuisance pests to large mammals (e.g., Witter et al. 2012), but I would argue that most ecological interactions in the Arctic involving arthropods (and their relative importance) remain a mystery.   I could not even speculate on the role of fungal entomopathogens in the Arctic.  This is one of those feared ‘black boxes in ecology':  probably there, possibly important, likely complex, but knowledge is seriously lacking. 

So along comes this paper: Meyling et al.  took soil samples from locations in the high and low Arctic (i.e., including Zackenberg, at about 74.5 degrees N), and they returned the samples to their laboratory in Denmark.   In their lab, the authors allowed live insects (using Lepidoptera [Pyralidae)] and Coleoptera [Tenebrionidae]) to be exposed to their samples, and they checked regularly for mortality: “...cadavers were rinsed in water, incubated in moist containers and monitored for the emergence of fungi“.  Any fungi that emerged from the (dead) host were identified.

The results: they identified five species of fungal entomopathogens (all in the division Ascomycota).  As the authors state in the start of their discussion “This study is the first to document fungal entomopathogens in soils from Greenland at both low and high Arctic sites. Furthermore, the use of in vivo isolation with living insect baits explicitly documented pathogenicity to these insects.”

Could this Arctic Weevil die from a fungal infection?

The black box has been opened:  indeed, fungal entomopathogens are in the high and low Arctic of Greenland, and are therefore likely in the high and low Arctic around the globe.  These fungi probably play a role in arthropod mortality in these systems, but this remains completely understudied.  As the authors point out, given the tight relationship between fungi and temperature, what effect could a changing climate have on these fungal entomopathogens?   This is potentially very important, as increased mortality of insects by fungi could trickle all the way up the food web…  I think we need to get more mycologists into the Arctic, and we must work to properly articulate high Arctic food webs with all the black boxes opened wide. 

References:

Holmes, R. (1966). Feeding Ecology of the Red-Backed Sandpiper (Calidris Alpina) in Arctic Alaska Ecology, 47 (1) DOI: 10.2307/1935742

Meyling, N., Schmidt, N., & Eilenberg, J. (2012). Occurrence and diversity of fungal entomopathogens in soils of low and high Arctic Greenland Polar Biology DOI: 10.1007/s00300-012-1183-6

Witter, L., Johnson, C., Croft, B., Gunn, A., & Gillingham, M. (2012). Behavioural trade-offs in response to external stimuli: time allocation of an Arctic ungulate during varying intensities of harassment by parasitic flies Journal of Animal Ecology, 81 (1), 284-295 DOI: 10.1111/j.1365-2656.2011.01905.x

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