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.

Screen Shot 2013-04-08 at 11.06.08 PM

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.

The Value of Field Courses

Part 1 – Why Include Field Courses in Undergraduate University Curriculum?

Taking students outside the classroom, and into streams, forests, or fields, can be a rewarding experience for both the instructor and the student.  I am reminded of this every autumn when I teach an introductory field ecology course as part of McGill University’s Major in Environmental Biology.  In this class, we visit many ecosystems, and the hope is that students, through learning outdoors, gain additional insights, and exposure to a suite of experiences they would otherwise not get in a classroom.

That being said, what is the real pedagogical value of field courses?  Or, why do we bother with field courses?  Sure, it’s fun to be outside, and for those students who like wearing rubber boots and ‘toughing it’ outdoors, it’s much more interesting than a lecture hall.  However, is there real value in terms of how content might be delivered or retained?  Are field courses just a feel-good ‘gimmick’?

Undergraduate students doing field work in an undergraduate course: hands-on experience

These questions were at the forefront of a teaching workshop we had in May of 2012 (I wrote about this previously) – as part of that workshop, Graham Scott (from University of Hull in the UK), highlighted some of his research about the value of field courses, and this work resonated with a lot of us who teach field courses at McGill.  I was particularly interested in reading his paper titled ‘The Value of Fieldwork in Life and Environmental Sciences in the Context of Higher Education: A Case Study in Learning About Biodiversity.  In this work, there is a nice introduction that states how many people believe and assume fieldwork is valuable because (and I am paraphrasing here):

Field trips are rewarding and satisfying (i.e., FUN) for the instructor and student

Field courses will improve recruitment and retention (i.e., used as a tool to draw students into an academic program at University, and keep them in the program once they arrive)

Field courses enable students to gain key skills, and transferable skills

The mushroom collecting laboratory as part of an undergraduate University course about field biology

This has certainly been my (informal) assessment about the value of field courses.  Students demonstrate (through enthusiasm, passion, motivation, and conversation) that they appreciate seeing and doing things outside of the classroom.  Earlier this term, when walking around the Morgan Arboretum with my class, we stopped and looked at invasive Noway Maple trees, and my Teaching Assistant was able to show them how to identify the species. Many of the students were able to grab a leaf, right there and at that time, and look at the key characteristics.  I like to think this visual and hands-on approach will help the content sink in, long-term, and that students will be able to remember the biology and natural history of Norway maples months or years after the course finishes.  I also think they will look at all maple tress a little differently, and think about similarities and differences, and about introduced (or alien/exotic) species.  These are big topics, of significance to conservation of biodiversity and environmental science at large.  Or, in other words, I think this experience will lead to life-long learning.

Just last week we had a field trip devoted to collections and identification of mushrooms.  The students split into groups and collected a diversity of fruiting bodies over the course of the three-hour laboratory.  They seemed genuinely enthusiastic and in awe of the diversity of shapes, sizes, colours and smells of the mushrooms. I don’t think this experience could ever be replicated in a classroom setting, or even in an indoor laboratory.  Being out in the woods, crouching down beside rotten logs, and learning how to watch for and collect mushrooms is something many of the students had never done before, and I like to think that this kind of experiential learning will stick.  Life-long learning again!  As I’ve mentioned in a previous post, I attribute my love of natural history to my exposure to nature as a child, through field guides and hands-on learning (although in this case the instructor was my father).  Field-courses, at a University level, can inspire people the very same way!

In fairness, I have only presented anecdotes and it would be nice to look to the scientific literature for proper studies that test for the pedagogical value of field courses for undergraduate students.  This takes us back to the work of Graham Scott and colleagues.  Graham et al. worked with undergraduate students and separated them into two groups: one group received instructions and then did a hands-on (in the stream) collection of aquatic invertebrates, and the second group received the same instruction in an indoor laboratory setting (i.e., as a laboratory demonstration) but did not actually do the sampling in a stream. It’s also important to note that the students did not know, ahead of time, whether they were going to participate in a laboratory or field-based activity (there were told to expect ‘practical work’ and be potentially prepared for outdoor activities). In a laboratory, after a short break, from the field/lab work, the students were asked to separate and characterize (draw, label) the biodiversity of the aquatic invertebrates.  These specific samples were collected separately (by the instructors) so there was no potential bias associated regarding who collected what samples.

Undergraduate students sampling aquatic invertebrates in an undergraduate course at McGill University

The result?  The authors document that the actual hands-on experiences had a real effect on students.  Students that had the field component to the activity enjoyed and valued the experience, felt that they learned more effectively, and ‘…were better able to construct a taxonomic list of organisms that they had collected themselves’.   Although more research on this topic is required (their sample size was relatively low), this paper does help provide some solid evidence that field courses are, from a pedagogical perspective, valuable.

Field courses are much more than a teaching gimmick:  field course benefit a student’s academic experience.  Field courses are an effective way to teach and learn course material. Of course, field courses are not relevant to all disciplines, but for students in biology or environmental science programs, field courses often appear in the curriculum, and I would argue they are en essential part of these programs.  Universities ought to support and promote their field courses.  When developing curriculum for an undergraduate program, field course should be as essential as a microbiology lab.  We live in a world that requires people to have experience in all facets of their environment, from shopping malls and urban centres, to corn-fields, marshes, and forests.   We are doing a disservice to undergraduate students if our teaching does not venture into the field.   That is the “why”.

To finish, I really appreciate a quote from the Discussion of Graham et al.’s paper: ‘Learning is enhanced in the field’.   Indeed – this is exactly my perception, and my experiences with field courses suggest this is true.  Feedback on my course evaluations speaks to this, also.  In my area of teaching, field courses will remain central to the academic program of Environmental Biology, and I encourage others to consider adding field courses to their own program.

Naysayers:  We often hear that field courses are too expensive, too difficult, too logistically complicated, and can be done only with small groups of studentsThese are not valid arguments and in a future post, I will discuss these issues in detail.  Part 2 will, therefore, deal with the “how“.  Stay tuned.

Reference:
Scott, G.W., et al. (2012). The Value of Fieldwork in Life and Environmental Sciences in the Context of Higher Education: A Case Study in Learning About Biodiversity Journal of Science Education and Technology, 21, 11-21 DOI: 10.1007/s10956-010-9276-x

Seven-legged spiders walking on water

Many spiders are known to ‘walk on water‘ (including dock spiders): spiders are small enough that many species and life stages can be held by the meniscus of water.  Spiders also have eight legs but they often lose one or more of their legs (in the scientific jargon, this is ‘leg autotomy‘).   In general, this is often part of defensive behaviour, and is common in many animals.  Sacrificing an appendage is a better idea than being eaten by a predator.

So… let’s link these thoughts together- spiders run on land as well as water, and they are often missing a leg.

A wolf spider (Pardoa mackenziana). In this photo, a leg that was previously lost has been ‘re-grown’ (4th leg on right side). The cost of this spider’s lost leg must have been minimal, since it survived and moulted again!

So, next comes the research question:   what is the ‘cost’ of leg autotomy and does this cost vary depending on whether the spider is traveling on the land or on water.  This is an interesting question, and one that was addressed directly by Christopher Brown and Daniel Formanowicz Jr in a recent research paper in the Journal of Arachnology.   These authors used the wolf spider Pardosa valens as their model species, and conducted ‘speed trials’ for male and female spiders on a terrestrial track as well as an aquatic track (i.e., these were constructed in a laboratory setting).  After doing the trials with intact spiders, the authors ‘induced autotomy’ (yes, this sounds somewhat horrific, but autotomy is very common with wolf spiders, and although they lose a little of their hemolymph, they heal quickly) and ran the trials again, with the same spiders (sans legs).

Results?  Well, perhaps not surprisingly, in the first year of their study, the species ran more slowly when they were missing a leg, but in the second year of the study, this affect varied by sex (males were slower, and autotomy only affected the females).   They report some rather complicated results when comparing terrestrial to aquatic trials, but in general, the spiders tended to run more slowly on the aquatic tracks when they were missing legs.  Again, this is perhaps not a surprising result, since having seven instead of eight legs will certainly change the biomechanics when considering how the spiders interacts with the meniscus of water.

Clearly, there are some costs associated with missing legs, but it is important to note that even without legs, these wolf spiders were able to run effectively on land and water, and even if their speed was slower than when they had all eight legs, they can still move an impressive speeds.  The range of speeds in some of the trials was between  20 cm/s and 50 cm/s – this translates to  running speeds between 0.72 and 1.8 km per hour!

Leg autotomy in wolf spiders in natural habitats range from between 8% and 32% as reported by Brueseke et al. in 2001 and by Apontes & Brown in 2005.  In the present study, the authors state that natural populations of P. valens exhibit between 25% and 45% autotomy.    These numbers are in line what what I have observed, as well.  This is pretty amazing – wolf spiders exhibit leg autotomy at a very high frequency, and in some cases, half the spiders in a population are missing a leg.  What can we infer from this?   Although there are some costs associated with leg autotomy (as reported by Brown and Formanowicz), they must not be that high – otherwise, natural selection certainly wouldn’t have favoured autotomy as a means to escape predation.  Brueseke et al., research supports this as they found very few costs associated with autotomy in Pardosa milvina.  In their work, Brueseke et al. studied locomotory behaviour as well as prey capture, and found overall support for the ‘spare leg hypothesis’ (i.e., look at all of my legs!  I can manage without one!).

So, here are the take-home messages:

Wolf spiders can run quite quickly, some species can run across water and land, and they can do so with missing legs.  Although they may be a little slower without their full complement of legs, the costs must be relatively minor given the frequency of leg autotomy in wolf spiders. 

This gives you more reasons to watch spiders – count some legs and see how many individuals are without their full complement of legs.

References:

Apontes, P., & Brown, C.A. (2005). Between-set variation in running speed and a potential cost of leg autotomy in the wolf spider Pirata sedentarius. American Midland Naturalist, 154, 115-125 DOI: 10.1674/0003-0031(2005)154[0115:BVIRSA]2.0.CO;2

Brown, C.M., & Formanowicz Jr, D.R. (2012). The effect of leg autotomy on terrestrial and aquatic locomation in the wolf spider Pardosa valens (Araneae: Lycosidae). Journal of Arachnology, 40, 234-239 DOI: 10.1636/Hill-59.1

Brueseke, M.A., Rypstra, A.L., Walker, S.E., & Persons M.H. (2001). Leg autotomy in the wolf spider Pardosa milvina: a common phenomenon with few apparent costs. America Midland Naturalist, 146, 153-160 DOI: 10.1674/0003-0031(2001)146[0153:LAITWS]2.0.CO;2

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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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Rethinking guild classifications for insect herbivores

This is the start a (somewhat) regular series of blog posts highlighting some of my favourite research papers in the discipline of Arthropod ecology – I’ll call this category “must-read research papers”.  These posts will force me to look critically at some of the great research papers I have read in the past little while, figure out the ‘take home messages’ from these papers, and articulate this message.  I also hope these posts can inspire others to think about the best papers within their discipline and to share their opinions and ideas to a broad audience.  That is what science communication is all about! 

Typical herbivory by a “leaf chewing” insect

For the first in this series, I wanted to highlight a paper by Novotny (and fifteen other co-authors) published in 2010 in the Journal of Animal Ecology.  This work is titled “Guild-specific patterns of species richness and host specialization in plant–herbivore food webs from a tropical forest.”   This paper was discussed in my Insect Diversity class last autumn (co-taught with Terry Wheeler), and was used as an example of assumptions we make when considering what it means to be a herbivore.    From my biassed perspective (working mostly in north-eastern deciduous forests and the Arctic), when I think about herbivores, I automatically classify herbivores into a few pretty obvious categories: leaf chewers, leaf miners, gall-makers, and a suite of ‘piercing-sucking’-type herbivores.  My off-the-cuff estimate of the number of herbivore guilds would be much less than a dozen.

Novotny et al.’s paper really shook up my view of what it means to be a herbivore.  Using their considerable data and expertise from work in Papua New Guinea, the authors refine plant-herbivore food webs and, quite simply, explode the concept.    The authors classified insect herbivores by their main mode of feeding (chewing, sucking), developmental stages (larvae, adult), where they feed (internally, externally), and by the plant part which is fed upon (leaves, flowers, fruits, xylem, phloem, etc).    Their system resulted in 72 classifications – which they reduced down to more manageable 24 – still over double what my initial estimate was.  Their system certainly includes the classic guilds (e.g., leaf chewers) but also included some wonderfully detailed interactions that are easily overlooked (especially by someone who studies spiders…).  For example, fruit chewers, flower chewers, and xylem suckers.   As an aside, and for some eye candy, here’s a nice photo of a caterpillar from The Bug Geek (reproduced here, with permission)

A cryptic caterpillar, (c) C. Ernst

The authors then took their new and detailed classification system and completed a food web analysis for their tropical system in Papua New Guinea, focusing on 11 main guilds.  Their resulting 11 food-web diagrams are a lovely depiction of multivariate data in 2-dimensions, as they show the frequency with which each host plant is consumed by herbivores, the herbivore abundance and the frequency of each interaction – and they present this for 9 standardized plant species, for each of the 11 guilds.   Their research depicts “6818 feeding links between 224 plant species and 1490 herbivore species drawn from 11 distinct feeding guilds”. WOW!  They also show that 251 species of herbivores are associated with each tree species within their study system.  There are clearly a lot of different ways for herbivores to make a living.

This paper represents a major undertaking, and it is a bit sobering to see the results and see that despite the efforts, relatively few ‘generalities’ exist – that is to say, there are examples of extreme host specificity, extreme generalist feeding, and everything in between.   Here’s a quote from that paper to illustrate that point:

“We documented a wide range of host specificity patterns among herbivorous guilds: host specificity measures spanned almost the full range of theoretically possible values from extreme trophic generalization to monophagy. These results demonstrate the importance of taxonomically and ecologically comprehensive studies, as no single guild can be designated as ecologically representative of all herbivores.”

Mealybugs: another type of herbivore. (c) C. Ernst, reproduced with permission

What’s the take-home message?  

For me, this is a strong paper that depicts effectively the complexity of plant-herbivore food-webs and illustrates (once again!) that diversity in tropical forests is stunning. More than that, the work shows this diversity from a functional, food-web perspective, and illustrates how guilds behave differently.   From a more practical perspective, this paper is forcing me to rethink how I view herbivores – i.e., they are more than leaf-chewing caterpillars and aphids.  They are also root-feeders, fruit chewers, flower chewers, and specialized xylem suckers.  Novotny et al. suggest researchers use their 24 guild system for classifying insect herbivores, and I agree – their classification system is still manageable, yet much more comprehensive than what many researchers use.

If the topic of food-webs, plant-insect interactions, and the biodiversity & ecology of tropical forests interests you, this is a must-read paper.

Reference:

Novotny, V., Miller, S., Baje, L., Balagawi, S., Basset, Y., Cizek, L., Craft, K., Dem, F., Drew, R., Hulcr, J., Leps, J., Lewis, O., Pokon, R., Stewart, A., Allan Samuelson, G., & Weiblen, G. (2010). Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest Journal of Animal Ecology, 79 (6), 1193-1203 DOI: 10.1111/j.1365-2656.2010.01728.x