Under the influence: how insecticides affect jumping spider personalities (Part 2)

This post is written by former PhD student Raphaël Royauté, and is a plain-language summary for our most recent article titled: Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider

It’s well known that personalities can shift and change when we are ‘under the influence’ of chemicals, be it drugs or alcohol. As entomologists, we also consider this question for the insects and spiders that live among us: although we assume arthropods can similarly be affected by chemicals in their environment, it’s less clear how these chemicals may affect the personalities of these arthropods. We tested the effects of insecticide residues on the personalities of a jumping spider known to live in apple orchards. We found that individual-based personality shifts occurred when spiders were exposed to sub-lethal doses of an insecticide. This mean that even before we might see ‘population-level’ effects of insecticides on an important predator in agro-ecosystems, individual spiders themselves get, um, sort of messed up when under the influence.

How is this cute jumping sipder affected by insecticides? (photo by C. Ernst, reproduced here with permission)

How is this cute jumping sipder affected by insecticides? (photo by C. Ernst, reproduced here with permission)

Insecticides are often used in agriculture for various reasons, but can have negative effects on the ‘non-target’ fauna living in our agricultural fields. One of the most important challenges in evaluating their toxicity is that these chemicals can persist at low concentration in the environment. These concentrations are unlikely to kill exposed organisms but may substantially alter behaviours. Most of our evidence of the toxicity of insecticides on behaviours comes from studies on pollinators and research has shown decreases in spatial memory and learning capacities.

There remain gaps in our knowledge about how other types of organisms respond to these compounds. Studies on insecticide toxicity may be also limited because they tend to ignore how insecticides shape variation in behaviour. This is important because individuals differ in their behavioural tendencies and may not have the same weight in ecological processes: some individuals are more active, show more aggressiveness or consume more food. Personality traits can also be inter-related and form “behavioural syndromes”: clusters of behavioural traits that are correlated and evolve as a package. If personality traits are interconnected, any insecticide modifying one trait is likely to alter the whole syndrome. We’ve shown previously that behavioural syndromes differed between populations exposed and unexposed to insecticides in the Bronze Jumping Spider, a species common in apple orchards and known to prey on several economically important pests. But those populations could be different for a variety of reasons: for example, perhaps the insecticides affect spider behaviours because there is simply less food available in insecticide-exposed areas for example.

We wanted to test if insecticides could be directly responsible for the shifts in personality and behavioural syndromes we noticed. In other words, when a spider is “under the influence” of insecticides, is it still behaving according to its personality type?

The similarities between insecticides and drugs is fascinating: Both types of compounds target the nervous system, both can affect behaviours and both can kill above a certain lethal dose. In fact caffeine and nicotine evolved as natural plant defenses against insect herbivory and the latter was one of the first insecticides ever used. As crazy as it sounds, the effect of psychoactive drugs has been investigated in spiders in the past! The legend goes that, back in 1948, zoologist H. M. Peters was annoyed by his garden spiders spinning webs at “such ungodly hours” (2 am-5am). He wanted to found a compound that would shift the spinning behaviour to more a “decent” schedule, and he asked pharmacologist Peter N. Witt for help. Witt tried different psychoactive compounds on the spiders, including caffeine, LSD and marijuana but couldn’t produce the desired effect. What he found was in fact much more interesting: each compounds produced a distinct type of “drug web”, altering its shape, size or regularity ! (from Foelix’s “Biology of Spiders”) More recent research has shown that some commonly used insecticides affect web building in the same way drugs do.

We focused on how activity and prey capture capacities were affected by exposure to a widely used insecticide (phosmet) in the Bronze Jumping Spider. We tested activity and prey capture before and after exposure the insecticide and compared the amount of behavioural variation with that of a control group. Doing research in ecology sometimes requires using original equipment. In our case we found that the best way to expose our spiders to the insecticide was to use a hotdog warmer! We applied the insecticide solution on test tubes and used the rotation of the hotdog machine to get a homogeneous surface coated with dry insecticide residues. This allowed us to have a more precise control of the dose that each spider received while simulating field exposure conditions.

Unusual research equipment: hot-dog warmer.

Unusual research equipment: hot-dog warmer. (photo by R. Royaute)

One of our study spiders, in its tube. (Photo by R. Royaute)

One of our study spiders, in its tube. (Photo by R. Royaute)

We did not found any effect of the insecticide on average behaviour between treatments but the ranking of individuals was strongly affected after insecticide exposure. In general spiders exposed to the insecticide were more variable in their behavioural tendencies. This suggests that the effects of insecticides on personality differences may manifest before any effects on the population as a whole are detected, in which case scientists may be frequently underestimating the toxicity of insecticides. Another puzzling result was that males and females did not respond in the same way to insecticide exposure. Males were most affected in the way they explored their environment but their capacity to capture prey remained intact. Females instead showed a decrease in the strength of the activity-prey capture syndrome.

Spiders play an important role in agricultural fields as they help regulate pest outbreaks. By altering personality differences and their syndromes, insecticides may limit spiders’ capacity to provide this important ecosystem service in subtle ways. As usual, this research leads to more questions than answers. At the organism’s level, it is important to understand how long these personality shifts last for. Do these shifts vary depending on how frequently spiders get exposed to insecticide or to what types of insecticides they are exposed to? How do they ultimately affect a spider’s capacity to escape predators, capture prey or reproduce depending on the individual’s personality? At the ecosystem level, prey get exposed to insecticides too, what happens to the predator-prey dynamics when the personality of both prey and predator is affected? How does that translate into biocontrol services? These are all important questions that I hope to contribute to in the future. Stay tuned!

A male bronze jumper (Eris militaris). Photo by C. Ernst, reproduced here with permission.

A male bronze jumper (Eris militaris). Photo by C. Ernst, reproduced here with permission.

References:

Royauté, R., CM Buddle & C. Vincent: Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Functional Ecology. . http://dx.doi.org/10.1111/1365-2435.12413

Godfray, H.C.J., T. Blacquiere, L.M. Field, R.S.Hails, G. Petrokofsky, S.G. Potts, N.E. Raine, A.J. Vanbergen & A.R. McLean. 2014. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. B 281: 40558 http://dx.doi.org/10.1098/rspb.2014.0558

Royaute, R., C.M. Buddle & C. Vincent. 2014. Interpopulation Variations in Behavioral Syndromes of a Jumping Spider from Insecticide-Treated and Insecticide-Free Orchards. Ethology. 120, 127-139. http://dx.doi.org/10.1111/eth.12185

Nathanson, J.A. 1984. Caffeine and related methylxanthines: possible naturally occurring pesticides. Science. 226, 184-187. http://dx.doi.org/10.1126/science.6207592

Rainer F. Foelix (2010). Biology of spiders. Oxford University Press. p. 179.

Samu & Vollrath. 1992. Spider orb web as bioassay for pesticide side effects. Entomologia Experimentalis et Applicata. 62, 117-124. http://dx.doi.org/10.1111/j.1570-7458.1992.tb00650.x

Spider Book!

WE are excited. The “We” is me and Eleanor Spicer Rice, of Buzz Hoot Roar fame, and author of the incredible e-books about ants.

Here’s the really big news…

We are teaming up with The University of Chicago Press, and writing a book about spiders!

Lynx spider! Photo by Sean McCann, reproduced here with permission

Lynx spider! Photo by Sean McCann, reproduced here with permission

There are already some really amazing spider books out there – one of our favourites is Rich Bradley’s gem, Common Spiders of North America: it’s beautifully illustrated, rich and in-depth. For those looking to cuddle up with a microscope, there is “Spiders of North America: an identification manual“: that book can unleash your inner taxonomist and help you identify (to genus) most spiders of the region. There are also some regional field guides about spiders, photography books, and detailed books about spider silk, or about general spider biology.

However, more books about spiders are needed! There is so much to say! These amazing arachnids are one of the most diverse groups of animals on the planet, with about 40,000 known species. They have the most unusual courtship and mating behaviours, and are often misunderstood, eliciting fear and loathing due to unwarranted fears about spider bites. Fundamentally, spiders are our friends and our goal with this project is to help share a fascination and love of these eight-legged marvels. We want all people to be familiar with the spiders they most commonly encounter, and when they bump into spiders as they move about the world, they’ll see friends and familiar faces instead of fangs. We want our book to be a non-technical primer of spiders and our goal is to bring awe and wonder, dispel myths, and help create an entire generation of arachnophiles. We hope to reach as broad an audience as possible, and teaming with University of Chicago Press will certainly help with this.

Our project will share stories about some of the most common spiders you will find in North America. Much like Eleanor’s ant books, we will research (using the primary literature) the life history and biology of common spiders in North America, and weave the science into a narrative about the species. We will unpack their biology, and write about spiders using accessible language. We’ll team up with our favourite photographers, and stunning images will accompany the text. Our hopes are that this book will complement the other books out there, and provide readers an accessible and fun-filled glimpse into the fascinating world of spiders.

An awesome Phidippus spider. Photo by Sean McCann, reproduced here with permission

An awesome Phidippus spider. Photo by Sean McCann, reproduced here with permission

Calling all Arachnologists!

We can’t do this project alone and WE WANT YOU! This project will be bigger and better with your help. Although we would love to include ALL the common spiders in our backyards, local forests and fields, this would make the project a little too big… so we need to narrow down to a reasonable number of species. So, we would like to know what species you want to read about.

Do you want a chapter about the glorious Black-and-yellow garden spiders?

What about the Zebra spiders?

Surely you would like to hear more about black widows?

Please provide us some feedback in the comment section, below. Tell us what you want to read about, and what aspects of spider biology must be included in our book. We will take your feedback seriously and try to include your suggestions.

Surely you want to know more about these lovely Black Widow spiders? Photo by Sean McCann, reproduced here with permission

Surely you want to know more about these lovely Black Widow spiders? Photo by Sean McCann, reproduced here with permission

Needless to say, we are SUPER excited about this project, and those of you that know us are already aware that we super-enthusiastic people to begin with, so this project has taken things to a WHOLE NEW LEVEL OF EXCITEMENT!!! We are so thankful for University of Chicago Press for the opportunity to tackle this project, and are already quick out of the starting gate: we have an upcoming writing retreat planned in March, and have already drafted some chapters. And in the coming months, we will certainly keep you updated on progress. We do hope you are as eager as us to see the finished project hit the bookshelves.

Spiderly, yours,

Chris & Eleanor

/\/\o00o/\/\

The effect of insecticides on jumping spider personalities

This post was written by C. Buddle and R. Royaute (a PhD student in the Arthropod Ecology lab).

We are pleased to announce a recent publication from our lab, titled Interpopulation variations in behavioral syndromes of a jumping spider from insecticide-treated and insecticide-free Orchards.  As is traditional in the lab, here’s a plain language summary of the work:

Agriculture has strongly intensified in the last 60 years, causing major concerns the sustainability of biodiversity. Agricultural practices can reduce habitats available for wildlife and also release toxins in the environment through the use of pesticides. Not all organisms living in agricultural fields are harmful, and many predators, including spiders, can help to reduce pest density. We have a relatively good knowledge that the diversity of spider species in agriculture, especially under our temperate latitudes, can help reduce pest damage. However, many of the factors that influence spider predation on pests depend on the outcome of behavioural interactions and we don’t know much about that topic. Spiders are often cannibalistic and aggressive with one another and these types of behaviours may limit their efficiency for pest control. We also need to understand if these aggressive tendencies vary depending on the type of agricultural field considered, a pesticide treated field may favour very different behaviours than one that is managed organically. Another important point is that populations are composed by a multitude of individuals, each with its own behavioural tendencies. Some individuals take more risks when confronted with predators (i.e. they are more bold), others are more active and explore larger areas or consume more prey. These tendencies – often referred to as personality traits – may also be correlated with one another.

In the context of agriculture, this may mean that certain individual spiders may contribute more to biocontrol because they consume more prey, or that certain individuals are more at risk of being in contact with pesticides because they are more active. To understand, how agricultural practices, and particularly insecticidal applications, affects personality and behavioural syndromes in spiders, we focused on the jumping spider Eris militaris, an abundant and charming jumping spider occurring in apple orchards in Quebec. Here’s a lovely photo from Crystal Ernst to illustrate how attractive they are: (thanks, Crystal, for permission to post the photo here!)

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We collected spiders from pesticide-treated and pesticide-free orchards, brought them back to the laboratory, and did a number of behavioural tests on the individuals from the two populations. Compared to the insecticide-free populations, we document that individuals from orchards that did receive insecticides experienced a shift in their behaviours syndromes. The overall shape of this syndrome is multidimensional, but it suffices to say that the correlations among different behaviours (the ‘syndromes’, otherwise known as the ‘personality’) differed depending on where the population came from.

A 'mirror test' - used to study behaviour in E. militaris (photo by R. Royaute)

A ‘mirror test’ – used to study behaviour in E. militaris (photo by R. Royaute)

In sum, the personality shifts that we documented for E. militaris are potentially quite important since the relationships between different behaviours may affect a spider’s ability to be an effective generalist predator in apple orchards. We need to consider how management  (including use of insecticides) may affect specific behaviours, and more importantly, the relationships between the different behaviours.

Reference

Royaute, R., C.M. Buddle & C. Vincent. 2013.  Interpopulation Variations in Behavioral Syndromes of a Jumping Spider from Insecticide-Treated and Insecticide-Free Orchards. Ethology. doi: 10.1111/eth.12185

Expiscor (21 October 2013)

Good Monday morning to all! I’m excited to be attending the Entomological Society of Canada’s annual meeting (you can follow along on twitter using the hashtag #ESCJAM2013).  Hope you have a good week ahead, and to help you start it right, here are some discoveries from the past while.

  • Poor spiders. So much bad press. Time for a lovely photo, perhaps? This one is a lynx spider from Crystal Ernst (Thanks, Crystal, for letting me post it here)

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  • Death of an order. (insect order, that is). An intriguing paper about Termites and their relatives (thanks to students in my introductory Entomology class for pointing out this paper, and the associated controversy)
  • Ever feel like your social calendar looks like this? (from “Wrong Hands“)

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  • To finish… an Icelandic Hymn – in a train station. Wow (thanks Jamin!)

Expiscor (7 October 2013)

Another week has passed… here are some discoveries!

  • Speaking of bugshot, here’s one of Nash Turley‘s pics from that adventure (Thanks, Nash, for letting me post it here!)

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  • Students in my intro Entomology class are teaching me a lot (they are lecturing on the Insect Orders). Last week, I learned of Desert Locusts that can swim, underwater. (note: they ‘can’ but they don’t necessarily ‘do’ the swimming.)
  • My students also told me of the hip, cool family of Orthoptera called…. Cooloolidae. Yeah, that’s awesome.
  • You like ants?  What about a jumping spider that looks like an ant? Here you go:
A species of jumping spider in the genus Peckhamia (photo by Alex Wild, reproduced here with permission)

A species of jumping spider in the genus Peckhamia (photo by Alex Wild, reproduced here with permission)

  • Tweet of the week goes to …  Erin McKiernan. This is awesome. Don’t worry: My neighbours think I’m crazy too. I’ve been caught running up and down the street with a sweep net.

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  • On robots: here’s a Wild Cat: This is both terrifying and amazing:

My favourite spider species: a natural history story 120 years in the making

A little while ago my nephew asked me what my favourite spider was. I quickly answered “Peckhamia picata“, in part because I had recently returned from a field trip in which that species was collected (a trip to one of my favourite places in Quebec), but also because the species has the most amazing habitus: is a myrmecomorph – a species that looks a heck of a lot like an ant. Here’s a photo to illustrate this:

A species of jumping spider in the genus Peckhamia (photo by Alex Wild, reproduced here with permission)

A species of jumping spider in the genus Peckhamia (photo by Alex Wild, reproduced here with permission)

So, what does this species do? What are its behaviours? Where does it live?

I started digging around to see what literature exist on this species. There are certainly many publications that discuss its distribution – it is on many checklists (see here for a relatively complete list), and I was aware that it was originally described as Synemosyna picata (by Hentz, in 1846).

I did a search of Web of Science for publications with the species name, and came up with two hits. One was a systematics papers on a related genus of jumping spider, and the second was a paper by Durkee et al. in 2011*.  They did some laboratory studies of the species, to assess whether or not its ant-like appearance helped it avoid being eaten by predators (spoiler: the answer is yes). A little more digging on-line took me to various sites, and in some cases, I came across this statement:  “almost no information on them

What?  Really?

A Peckhamia picata, from Quebec (Photo by J. Brodeur, reproduced here with permission)

A Peckhamia picata, from Quebec (Photo by J. Brodeur, reproduced here with permission)

Peckhamia picata is a widespread species, with an incredible appearance, and it’s a jumping spider!  Salticids are the darling of the arthropod world –> the panda bears of the invertebrates: big eyes, furry, fascinating courtship behaviours, and truckloads of ‘personality’.  Surely we know SOMETHING about what I declared as my favourite species.

Thankfully, in a filing cabinet in my laboratory, I have a series of older publications on the Salticidae, including “A Revision of the Attidae of North America” by Peckham & Peckham (1909) [available here as a PDF download – note: big file!]. The George and Elizabeth Peckham did an incredible amount of work on the Salticidae (called Attidae, previously). The Peckhams are themselves a fascinating story – some details are on their Wikipedia page  and I’ll summarize briefly: they were teachers (in Wisconsin), natural historians, behavioural ecologists and taxonomists, notably with jumping spiders.  The bulk of their work was done in the late 1800s, and they often cited and discussed Darwinian concepts. They were awesome and I would have liked to meet them.

Another stunning Peckhamia species, this one from Thomas Shahan.

Another stunning Peckhamia species, this one from Thomas Shahan.

So, back to Peckamia picata: Their 1909 tome states the following about the species “We have described in detail its mating and general habits in Vol. II, Part 1 of the Occ. Pap. Nat. Hist. Soc. Wis. pp. 4-7)”.

So, apparently 1909 does not take us far enough back in history to learn about Peckhamia picata. Their paper from 1892 had all the details, and thankfully was fully accessible on the biodiversity heritage library.

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Here is some of the lovely writings about Peckhamia picata, from the Peckhams, in 1892 (transcribed from their papers):

About appearance:

While picata is ant-like in form and colour, by far the most deceptive thing about it is the way it which it moves. It does not jump like the other Attidae [Salticidae], nor does it walk in a straight line, but zig-zags continually from side to side, exactly like an ant which is out in search of booty. This is another illustration of which Wallace has shown in relation to butterflies ...”

(note: The Peckhams give a node to that Wallace guy….)

About feeding behaviour:

Spiders commonly remain nearly motionless while they are eating; picata, on the other hand, acts liks an ant which is engaged in pulling some treasure-trove into pieces convenient for carrying I have noticed a female picata which, after getting possession of a gnat, kept beating it with her front legs as she ate, pulling it about in different directions, and all the time twitching her ant-like abdomen

Regarding courtship:

From the Peckham's 1892 publication.

From the Peckham’s 1892 publication.

His abdomen is lifted vertically so that it is at right angle to the plane of the cephalothorax. in this position he sways from side to side. After a moment he drops the abdomen, runs a few steps nearer the female, then then tips his body and begins to sway again. Now he runs in one direction, now in another, pausing every few moments to rock from side to side and to bend his brilliant legs so that she may look full at them.”

In sum, this journey of discovery has made me fall in love with Peckhamia picata even more. It’s also reminded me that OLD literature is essential to our current understanding of the species we identify. There is a wealth of information in these “natural history” papers – although the writing is in a different style, it is scientific, it is the foundation of current biodiversity science.  We cannot ignore these older books and “Occasional papers”. We can’t rely on quick internet searches and we certainly can’t rely on literature indexed on Web of Science.

We must dig deep and far into the past. There are ‘treasure-troves’ aplenty.

—————–

*The oldest paper cited in Durkee et al. is from 1960. They did not cite the Peckhams.

Another Peckhamia species, courtesy of Matt Bertone (reproduced here, with permission)

Another Peckhamia species, courtesy of Matt Bertone (reproduced here, with permission)

References:

Durkee, C. A. et al. 2011. Ant Mimicry Lessens Predation on a North American Jumping Spider by Larger Salticid Spiders. Environmental Entomology 40(5): 1223-1231

Peckham, G.W., and E.G. Peckham. 1892. Ant like spiders of the family Attidae Occ. Pap. Nat. Hist. Soc. Wis. II, 1 .

Peckham, G.W., and E.G. Peckham. 1909. Revision of the Attidae of North America. Trans. Wis. Academy of Sci., Arts & Letters. Vol. XVI, 1(5), 355-646.

Expiscor (30 September 2013)

Expiscor – your voyage of discovery: bugs, biology and beyond!

Here’s what I stumbled across this week:

  • Ah, Botflies. Gross or cool? For entomologists, this is some pretty amazing stuff.
  • The amazing Ainsley Seago knows how to draw spiders. Here is one of her pieces; perfect for Archnophiles:
A male peacock spider (Maratus amabiis), doing his dance. [by A. Seago, reproduced here with permission]

A male peacock spider (Maratus amabiis), doing his dance. [by A. Seago, reproduced here with permission]

  • Better beetle news: here’s a nice wood-boring beetle, and one that is sexual dimorphic.
  • A lovely image from Sean McCann, showing a moulting Opiliones. (Thanks, Sean, for allowing me to share it here)

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  • To finish, more on the peacock spiders (last week I was teaching about courtship behaviours in arthropods, and that discussion is not complete without viewing this video!):