Effects of Symbionts on Host Population Dynamics

Sometimes it can be really difficult to determine whether a symbiont is a mutualist, a commensal, or a parasite of its host. The context-dependent nature of these relationships is partially to blame for our inability to stick a label on any given symbiosis, because the net outcome of the relationship might vary every time we try to measure it! But even if we limit our focus to just one set of conditions, it can be difficult to say for sure what net impact the symbiont has on host fitness, because we may not be able to simultaneously quantify all of the ways that the symbiont might affect the host. For instance, we might find that the symbiont does not affect host survival, and then we might be tempted to call the symbiont a commensal. But if we didn’t measure host reproductive output as well as survival, how do we know that the symbiont didn’t affect that particular host vital rate? And to make things more confusing, how long-term must our measurements be? Do we need to record every detail from the second the host is born until the second it dies? And then do we need to do the same for each of the host’s offspring?

In this post, I’m not going to answer any of those questions. (GOTCHA!) Instead, let’s talk about a beautifully written and relevant paper about ants on cacti (Ford et al. 2015). If you need a refresher on the incredibly cool ecological relationships between ants and myrmecophytic plants (and/or you want to see some sweet photography by Alex Wild), check out this post. Otherwise, I’ll assume you’re on board with the terminology that I’m using.

The fishhook barrel cactus sports a bunch of extrafloral nectaries that are visited by ants. If insects visit the plant’s fruits or flowers when there are ants on guard, those insects might get attacked by the ants. If the ants are deterring herbivorous insects, they might be positively affecting host fitness. To determine whether that was the case, Ford et al. (2015) quantified the effects that ants had on three host vital rates: number of fruits, plant growth rate, and plant survival. Ants increased the number of fruits produced by the plants, but ants did not affect plant growth rates or survival.

If ants are increasing fruit output, that should have important implications for cactus population dynamics, right? Actually…maybe not! Ford et al. (2015) used some integral projection models to show that cactus population dynamics were really sensitive to cactus growth rates and survival probabilities, but cactus population dynamics weren’t affected by the number of fruits produced per plant – the one vital rate that ants affected.

So, Ford et al. (2015) used three years of very detailed survey data to show that ants don’t seem to be having any affect on cactus population dynamics. But what if they were to follow these populations for a longer period? What if ants don’t really affect the cactus population most years, but they have a big effect during the rare years where there are “catastrophes” (i.e., outbreaks of herbivorous insects) or “bonanzas” (i.e., relatively wet years)? Ford et al. (2015) used some simulations to show that ants could potentially have positive effects on host population dynamics in the long-tem, especially when there were high frequencies or intensities of certain catastrophes or bonanzas. Neat!

Reference:

Ford, K.R., J.H. Ness, J.L. Bronstein, and W.F. Morris. 2015. The demographic consequences of mutualism: ants increase host‑plant fruit production but not population growth. Oecologia.

Cheaters in Mutualisms

Ants are involved in an astounding diversity of symbiotic relationships: they pollinate flowers, they disperse seeds, they farm fungi, they defend trees and insects from natural enemies, etc. Those are some very diverse services! But of course, even when the ants are dutifully performing those services, the ants don’t necessarily benefit their partners. For instance, ants may also sterilize their host plants or eat some of the aphids that they are tending for honeydew. Furthermore, the net outcome for the ants’ partners may be context specific, where the costs and benefits of interacting with ants vary with ecological and environmental conditions. For instance, if you’re an Acacia tree, having ants around to protect you from elephants may be very beneficial, but only if you live in an area that actually has elephants.

Here’s a different question: do ants always benefit from their relationships with their partners? Ants appear to be the decision makers in many of these relationships, where trees and aphids and scale insects and fungi seem less capable of making active decisions to participate (or not) in the relationship. But it turns out that ant partners aren’t as passive as they seem, because they can often use “rewards” and/or “sanctions” to control ants. For example, trees can ‘decide’ how many domatia to produce or whether to produce extrafloral nectar, which in turn determines whether ants will be attracted to the tree. (For an example of a cool sanction, check out this system, where hosts eat their symbionts when the symbionts aren’t beneficial!)

Ants can also experience negative effects of symbiotic interactions when they are tricked by mimic species or individuals called “cheaters.” In fact, there are many neat insect species that trick ants. I really want to go crazy and devote a six page blog post to all of my favorite ones, but here are just two:

1) The lacewing larva that wears aphids: Yes, for real. Lacewing larvae eat aphids, but that can be hard to do when the aphids are protected by ants. So, these lacewing larvae have evolved to wear aphid carcasses (or the cottony-fluff that aphids create) like the proverbial sheep suit worn by the wolf. The ant defenders can’t detect the difference between the aphids and the lacewings in aphid clothing, so the lacewings get to sneak onto the aphid farm to feast without being chased off.

2) Aphids that aggressively mimic ants: A single species of aphid can often have several distinct phenotypes. For instance, there are phenotypes with wings that disperse across relatively long distances and wingless phenotypes that don’t disperse very far. In some aphid species, there are phenotypes that reproduce, and other soldier phenotypes that never reproduce and protect the colony from natural enemies. Finally, in the species Paracletus cimiciformis, there is a green, pot-bellied aphid phenotype that has a typical symbiotic relationship with ants, where the ants protect and clean the root-dwelling aphids in return for honeydew. There is also a second phenotype that is flatter and yellow-ish, with hydrocarbons in the cuticle that are similar to the hydrocarbons in ant larvae (Salazar et al. 2015). When adult ants find aphids with the flat phenotype, the ants carry the aphids back to the ant nest, and plop the aphids onto the piles of ant larvae. From there, the aphids feed on the hemolymph of the ant larvae using their piercing/sucking mouthparts! So, the aphids get to hang out in the protective environment provided by the ant nest while sucking on baby ant juices, and they don’t have to do anything in return. Awesome.

References:

Salazar, A., B. Furstenaub, C. Quero, N. Perez-Hidalgo, P. Carazo, E. Font, D. Mantinez-Torres. 2015. Aggressive mimicry coexists with mutualism in an aphid. PNAS 112(4): 1101-1106.

Spartants on Epiphytes: Species Assembly Rules

On Monday night, I read an amazing paper. It was so amazing that I knew I’d need to save it for my post on Parasite Ecology’s second birthday…which I then realized was less than two days away. So, in the past 24 hours, I have fallen hopelessly in love with ants (again!), reorganized two months worth of queued posts, and made a symbiont cartoon incorporating the phrase, “This is Sparta!” – something that I’ve been waiting for the right moment to do for TWO YEARS. The moment has arrived. Happy Birthday, Parasite Ecology! 

As we’ve talked about previously, some ants live on plants in special hollow chambers that the plants provide called domatia. But ants can also live on plants that don’t provide domatia, such as the epiphytic birds’ nest ferns that trap leaf litter in the canopies of tropical forests. Amazingly, up to 12 ant species can be found living together on just one of these epiphytes! But what determines exactly which species can be found living together?

Ant competition might be a major structuring force that determines which ant species live together in a given epiphyte community, and ant species that are most similar in size may be more likely to compete. And in fact, in a survey of 86 epiphytes, ant species that were similar in size were less likely to co-occur than one would predict based on a null model (Fayle et al. 2015). But that doesn’t prove that competition is driving the observed pattern, so Fayle et al. (2015) conducted an experiment where they inoculated epiphytes with single or multi-host communities of ants, and then two days later, they inoculated the same epiphytes with an “invader” species. There was strong competition between similarly sized ants, but not between ants of disparate sizes. Furthermore, the threshold size ratio between the invading and resident ants that determined whether there was strong competition or not was roughly the same in both the observational study and the invasion experiments.  And get this:

“In each replicate, an invading colony was introduced into a fern, which was supported on a fluon-coated cylinder above a fluon- coated container, and left for 24 h with ants ejected from the fern falling into the container. Competition manifested as direct attacks between workers of different colonies, with ants sometimes being thrown from the edge of the fern (Appendix S3).”  

Ok, but we’re not done! Fayle et al. (2015) took things a step further and ran simulations with different sets of species assembly rules to see which set of rules, if any, could re-create the community diversity patterns that they observed in the field. Their null model was that size-based competition didn’t matter, so that every species had the same probability of invading a community, regardless of the sizes of the resident species. They compared this to four other sets of rules (1a, 1b, 2a, 2b), where the relationship between the invader-resident size difference and the strength of competition was described as a (1) threshold assembly rule or a (2) saturating assembly rule and competition between ants was assumed to be (a) between the invader and the resident of the most similar size (nearest neighbor competition) or (b) between the invader and all resident species (diffuse competition).  The rules that resulted in the best fit to the observed diversity patterns were the combination of the saturating relationship between the invader-resident size difference and the strength of competition and nearest neighbor competition (2a). SO. COOL.

Go check out the paper! It’s open access.

Reference:

Fayle, TM, P Eggleton, A Manica, KM Yusah, and WA Foster. 2015. Experimentally testing and assessing the predictive power of species assembly rules for tropical canopy ants. Ecology Letters 18: 254–262.

Bears Indirectly Affect Plant Fitness

If you haven’t seen it yet, there’s a really cool paper in Ecology Letters about the indirect effects of bears on ecological communities (Grinath et al. 2015). Did you know that bears will eat ants? Well, they will! Especially during periods when they are food limited. And when bears disturb ant nests, the ants stop tending the leaf and tree hoppers (=herbivorous insects) that they farm for honeydew. Without ants patrolling nearby, tree hoppers experience higher predation pressures from other arthropod predators, like lady beetles and spiders. And when the densities of herbivorous insects decline, plant fitness increases. So, by eating ants, bears can increase plant fitness! Nuts!

I glossed over some of the details of this story, such as variation in the effects of bears across years. To get all of the details and to see some cool structural equation modeling, go check out the paper!

Reference:

Grinath, J.B., B.D. Inouye, and N. Underwood. 2015. Bears benefit plants via a cascade with both antagonistic and mutualistic interactions. Ecology Letters 18(2): 164-173.

The benefits of attracting many symbiont species

Textbook examples of mutualisms usually involve two interacting species; for instance, honey bees and clover. But of course, one host may have many mutualists (e.g., bees, butterflies) and one mutualist may have many hosts (e.g., clover, blueberries). In many cases, the benefits of having multiple possible host species are obvious. For instance, for ants that eat tasty elaiosomes and disperse plant seeds, it would be hard to get by while specializing on the seeds of only one plant species, because those seeds would only be available for part of the year. But how does the host benefit from having many symbiont species?

In ant-plant interactions, one plant species may have individual visitors from many ant species. For instance, the shrub Urera baccifera receives visitors from 22 facultative ant species, which visit to harvest food bodies and/or fruits (Dutra et al. 2006). Similarly, the yellow alder (Turnera ulmifolia) receives visitors from 24 facultative ant species, which visit to harvest seeds with elaisomes and/or to feed at extrafloral nectaries (Cuautle et al. 2005). While they’re on the plant, these ants can protect the plant from herbivores, like caterpillars. And finally, there may be multiple ant species visitors to a given plant species even when the associations are obligate: for instance, Acacia drepanolobium may be inhabitated by one of four ant species at any given time (Palmer et al. 2010).

Ok, but why so many species of ant visitors? Why shouldn’t the plant sanction any partners except the most beneficial species? This is still an active area of research, but at least part of the answer is that different ant species vary in the services that they provide to the plant. For instance, ant species may be more of less aggressive defenders, more or less likely to disperse seeds, more or less likely to farm scale insects, etc. (You might remember that this is true for guard crabs, too, where big crab species are good at protecting corals against starfish, while small crab species are good at protecting against vermetid snails.) Ant species also vary in how costly they are to harbor. For instance, one species may be a good defender, but it may also sterilize the host plant (e.g., Stanton 1999). So, a plant’s lifetime fitness may be determined not only by the guild of ant species that visits the plant during its life, but also on the timing and order in which those species visit the plant (Palmer et al. 2010). For instance, having sterilizing symbionts when you’re young can actually increase lifetime plant fitness. Isn’t that wild?

References:

Cuautle M, Rico-Gray V, Diaz-Castelazo C (2005) Effects of ant behaviour and presence of extrafloral nectaries on seed dispersal of the Neotropical myrmecochore Turnera ulmifolia L. (Turneraceae). Biological journal of the Linnean Society 86: 67-77.

Dutra HP, Freitas VL, Oliveira PS (2006) Dual Ant Attraction in the Neotropical Shrub Urera baccifera (Urticaceae): The Role of Ant Visitation to Pearl Bodies and Fruits in Herbivore Deterrence and Leaf Longevity. Functional Ecology 20(2): 252-260.

Palmera TM, Doak DF, Stanton ML, Bronstein JL, Kiers T (2010) Synergy of multiple partners, including freeloaders,increases host fitness in a multispecies mutualism. PNAS 107(40): 17234–17239.

Stanton ML, Palmer TM, Young TP, Evans A, Turner ML (1999) Sterilization and canopy modification of a swollen thorn acacia tree by a plant-ant. Nature 401:578–581.

Elepunts

Are elephants afraid of mice? Well, maybe. There isn’t much evidence, unless you like sample sizes of 1 individual. However, elephants are definitely afraid of ants, and that is a much more interesting ecological story.

Last week, I posted an introduction to the symbiosis between ants and plants. One of the services provided by ants is protection from herbivores. Those herbivores may be insects, like caterpillars and grasshoppers, but they may also be megafauna, like elephants.

Elephants love munching on Acacia trees, but some Acacia species are protected by ants. With the ants removed, elephants will gladly eat species that typically have ants. But when the ants are present, the elephants avoid defended trees (Goheen and Palmer 2010). This decision to avoid getting viciously stung by hordes of ants may have far-reaching consequences in savanna ecosystems: tree community composition is affected, because defended tree species are more likely to survive in areas with many elephants (Goheen and Palmer 2010).  Tiny symbionts can play big roles in ecological communities!

References:

Goheen JR, Palmer TM (2010) Defensive plant-ants stabilize megaherbivore-driven landscape change in an African savanna. Curr Biol 20:1768–72.

Myrmecophytic Plants and Their Ants

You can find ants and plants in almost every terrestrial habitat on the planet. Both groups can be incredibly abundant, so it isn’t surprising that ants and plants interact a lot. But some plants and ants have intimate symbiotic relationships that go far beyond the occasional interaction. Some of my favorite ecological stories involve these symbioses, and I’m going to post those stories in the coming weeks. But this week, I just want to introduce you to the system and let the insane photography skills of Alex Wild bring these organisms into your life.

Myrmecophytic plants: Who are they, and what do they provide their ant symbionts?

There are many genera of myrmecophytic plants, including flowers, shrubs, trees, and even ferns. These plants vary widely in the degree to which they invest in their ant symbionts. Below is a list of the structures that plants have evolved to provide their ants with resources, but not all ant-plants have all of these structures.

Domatia: Domatia are hollow structures that the ants can use for nests. Depending on the plant species, these domatia may be hollow stems or spines. For instance, check out this hollow thorn on an Acacia tree and the hollow base of this epiphytic plant. Both are homes for ants!

Extrafloral nectaries: Many plants provide nectar rewards in their flowers in order to attract pollinators. Ant-plants may also have extrafloral nectaries – structures that provide nectar but that are not associated with flowers. On ant-plants with domatia and active ant colonies, these extrafloral nectaries can feed resident ants. On ant-plants without domatia, these nectaries can attract ant visitors. Here are two gorgeous ants feeding at an extrafloral nectary.

Food Bodies: Ants can’t just survive on nectar; they need resources other than sugar, too. Some ant-plants have evolved to produce food bodies that contain proteins or lipids that ants can harvest for those vital nutrients. Here’s an ant harvesting one such food body.

Plant-ants: Who are they, and what do they provide their plants?

There are also many genera of ants that have symbiotic relationships with their plants. These ants can be facultative or obligate symbionts (meaning that they are only found living on plants), depending on the species. In the coming weeks, I’ll talk a lot more about the services that ants do (and do not) provide to plants, but here are the main points:

Defense: Plant-ants are feisty plant protectors! They can bite and sting herbivores or even throw the herbivores off the plant. Plant-ants will also attack competing plants. For instance, they will bite encroaching vines or inject neighboring plants with formic acid. (Yeah. For real. Look up Devil’s Garden.) Here are some ants getting rid of a vine, and some different ants hauling away an intruder ant.

Nutrients: When ants die and defecate, they fertilize their plants. (I bet you can imagine this one without a photo. Also, arboreal earthworms are a thing, and plants eat their poop, too. You’re welcome.)

Seed Dispersal: Some plants produce seeds with tasty exterior food bodies called elaiosomes. The ants collect these seeds and eat off the elaisomes, then put the seeds in their waste piles. During this process, the seeds are dispersed, and they’re also protected from predators while they’re in the ant nests.

Aren’t plant-ants and ant-plants cool?! You should check out Alex Wild’s website for more awesome photos. Stay tuned for more on plant-ant ecology next week!

The Last of Us

I thought that we’d do a quick, just-for-fun post today.  ABOUT ZOMBIES.  Now, I like me some zombie movies.  Sometimes their plots even have cool disease ecology components, like competition between the “zombie virus” and other host pathogens.  On the other hand, there are many, many biological inaccuracies involved in the popular zombie idea, as Neil deGrasse Tyson explains.  

But if you’ve been following this blog or popular science for any length of time, you know that in a way, Neil deGrasse Tyson is wrong in saying that if zombies exist, they only exist on other planets.  There are “zombies” on Earth: parasite zombies!  That is, some parasites can dramatically alter their host’s behavior, so that the host is effectively just a vehicle for the parasite.  The point of this manipulation is to get the host to behave in such a way as to increase the parasite’s probability of transmission to the next host.  Usually, this involves the host getting eaten by the next host, like when infected ants hang out at the top of blades of grass, where they are likely to be eaten by cows or sheep.  But that’s not always the case.  For instance, with rabies – the pathogen most similar to the classic idea of a zombie virus –  the virus makes (some) animals behave aggressively, and this increases the probability that the virus will be transmitted to new hosts via bites.  

Now, thankfully, there aren’t any parasites that re-animate dead corpses…yet.  But there are parasites that use corpses as points of transmission.  For instance, Cordyceps fungus makes ants leave their normal routines to go bite onto leaves above major areas of ant traffic.  Then the fungus sprouts a fruiting body out of the ant’s corpse and rains spores of death down on the ant’s extended family.  

Don’t you think that a Coryceps fungus apocalypse would be a cool video game plot?  Well, actually, it already is a cool video game plot!  The Last of Us has been out for a while on PS3, and a remastered version was just released on PS4.  From Wiki:

“In 2013, Joel (Troy Baker) is a single father living near Austin, Texas with his twelve-year-old daughter Sarah (Hana Hayes). One night, an outbreak of a mutant Cordyceps fungus ravages the United States, which transforms its human hosts into cannibalistic monsters…”

Now, real Cordyceps doesn’t turn insects into cannibals, but I’m willing to overlook this error in biology because – WAIT FOR IT – they’re going to make The Last of Us into a movie, too!  That’s right.  Cordyceps is coming to the big screen.  Awwyisss.     

The Oatmeal – Parasite Zombies

Are you getting tired of parasite zombie posts yet?  I hope not, because I’ve got a lot more where these have come from!  Starting with this really awesome (I mean, REALLY AWESOME) cartoon by The Oatmeal.   

Dicrocoelium dendriticum, the lancet liver fluke, is a parasite of livestock (e.g., cows, sheep).  Of course, Parasite of the Day has written about this awesome parasite before.  I highly recommend popping over there for more details.  And of course, check out the full cartoon from The Oatmeal!

A taste of The Oatmeal‘s brilliant cartoon about the lancet fluke.

Zombie Ants

Instead of talking about a specific paper today, I’m going to talk about ZOMBIE ANTS <cue horror music>.  Parts of this will count as self-plagiarism, because I’ve blogged about this in other places.  Let the post cannibalism begin!

I attended the annual meeting of the American Society of Parasitologists last summer, and it was awesome.  David Hughes gave a really awesome talk called “Zombie Ants: The Precise Manipulation of Social Insect Behavior by a Fungal Parasite.”  I’m sure you’re totally hooked already, but just in case you’re not seeing how cool this is, let me reel you in with some photos.  (These aren’t ants, but you’ll see those later.)

Photo from here.

Photo from here.   For more cool fungus pics, just google “Cordyceps fungus.”

Parasites often manipulate their host’s behavior in order to increase the probability that they (the parasites) will be successfully transmitted to their next host.  In the case of the parasitic fungus of these ants, the fungus wants the ant to go hang out somewhere that will result in the fungus being able to rain spores down on other ants.  It does this by making the ants climb up to a leaf above an area of a high ant traffic (areas that Hughes calls “killing fields”). The ant is then “forced” to bite down on the main vein of that leaf, and then its mandibles get stuck that way, so that the ant is attached to the underside of the leaf forever.  Then the fungus sprouts out of the ant’s head and does its whole raining spores of death thing.

Since David Attenborough explains things better than I do, I’m going to link you to David Hughes’ website, where he has more info and some sexy videos (including Attenborough).

As a final note, Hughes is looking into using this parasitic fungus as a form of biocontrol for pest ants, like on farms.  In other words, YOU TOO could have your very own ZOMBIE ANTS.

How do you feel about using parasites as biocontrols?  That’s a huge can of worms, I know, but I’d like to hear your opinions.