I can’t believe that I only just learned about the glorious symbiosis between boxer crabs and anemones. The crabs hold one tiny anemone in each claw, and they use the anemones to defend themselves from predators. The anemones benefit from increased access to food because they’re constantly being waved about.
LOOK AT THIS FACE!
And look at these dance moves!
That tiny cheerleader’s got game.
I’m in love.
Ecologists sometimes use the terms “mutualism” and “symbiosis” interchangeably, and I wish that they would not do so! I recently bought a copy of Judie Bronstein’s new book about mutualism, and the first two chapters are devoted to defining the terms mutualism and symbiosis, and distinguishing between the two. Here, I’ll outline the main points. For a longer treatment of this topic, check out the book!
Mutualism is an ecological interaction between at least two species (=partners) where both partners benefit from the relationship.
Symbiosis is an ecological interaction between at least two species (=partners) where there is persistent contact between the partners.
In symbioses, one partner is often smaller, lives on or in the larger partner, and has a shorter lifespan that the larger partner. The smaller partner is a symbiont, and the larger partner is a host.
Not all mutualisms are symbioses. Some mutualisms are non-persistent, like when a pollinator very briefly visits a flower and then never returns to that flower again. Additionally, not all symbiosis are mutualistic. For instance, parasites are also symbionts.
A few months ago, I posted this useful classification scheme for thinking about different types of ecological interactions. The two axes are the “relative duration of association” and “net effect of the relationship on the ‘host.’” Mutualisms are any relationships on the right-hand/positive side of the net effect of the relationship on the ‘host’ axis, regardless of where the relationship falls on the vertical axis. Symbioses are relationships at the ‘top’ of the relative duration of association axis – where much of the symbiont’s lifespan is spent in association with the same host – regardless of where the relationship falls on the horizontal axis.
By definition, mutualists, commensals, and parasites (hereafter “affiliates” in this post) depend on their hosts for resources or services. Therefore, if a host species goes extinct, the affiliates associated with that host may go extinct, too. And in fact, coextinction events like this should be as common as – or even more common than – extinctions of hosts, because we know that every host species has many mutualists, commensals, and parasites. Just think about the mites living in your eyebrows, the bacteria living in your intestines, and that one time that you had lice in third grade. If humans disappeared, all of those affiliate species might also go extinct!
Of course, you might not believe in the intrinsic value of all species; you might be wondering why you should care if some tiny species that you’ve never heard of goes extinct. Extinctions of mutualistic species – such as the gut microbes that help you digest food and the pollinators that keep our agricultural systems running – have obvious implications for our economy and health. But parasites, too, play important roles in our lives. For instance, they regulate populations of wildlife host species, and they may prevent you from having allergic reactions to things that you shouldn’t be allergic to. And of course, species exist in intricate webs of interactions, and by accidentally (or purposely!) adding or removing species from ecosystems, we have often learned that one species can have huge impacts on ecological communities.
So, coextinctions of affiliates are important, and these coextinctions should be common. That means that we have documented tons of these coextinction events, right? Actually, we haven’t! There are very few examples of documented coextinctions (Dunn 2009, Colwell et al. 2012), and some of those are not entirely open and shut cases. But why?
Say that you document the extinction of a particular host species: Host A. Should every affiliate associated with Host A also go extinct? Because some affiliates likely use multiple host species, some of the affiliates of Host A probably survived on other host species. Also, even an affiliate that historically only used Host A might be able to continue existing if it can switch to a new host species. For instance, maybe Host B, a close relative of Host A, is a suitable alternative host.
Now imagine that you’re trying to document affiliate coextinctions as Host A disappears. What evidence might you use to figure out which affiliates have also disappeared? There might be published accounts of some of the affiliates of Host A, but there are very few host species (if any) for which every affiliate species has been documented. Therefore, the loss of one host species means that several unnamed and undescribed invertebrate species will be lost before ever being documented by humans. Even if you had a perfect list of every affiliate species, it might be really difficult to confirm whether each affiliate was now extinct. That’s because we rarely (if ever) have perfect lists of every host species used by a given affiliate species. So, if one affiliate species frequently uses three host species, but you think it is a specialist on Host A, you might think the affiliate has gone extinct, only to find it happily hanging out on Hosts B and C when you survey those species three decades later.
To summarize, we predict many coextinctions of affiliates to occur as hosts go extinct, but we have hardly documented any such coextinctions. It may be that that affiliate species are much less vulnerable than we expect due to the use of multiple host species or host species switching as a primary host goes extinct, and/or it may be that we are just very poorly equipped to observe and document these coexinctions. Clearly, if we’re going to get better estimates of affiliate coextinction rates, we need more data! Specifically, we need:
(It’s been too long since my last pirate worm cartoon….)
Some related reading:
Conservation – save the parasites along with the hosts?
References:
Colwell, R.K., R.R. Dunn, N.C. Harris, and D.J. Futuyme. 2012. Coextinction and Persistence of Dependent Species in a Changing World. Annual Review of Ecology Evolution and Systematics 43: 183-203.
Dunn, R.R., N.C. Harris, R.K. Colwell, L.P. Koh, and N.S. Sodhi. 2009. The sixth mass coextinction: are most endangered species parasites and mutualists? Proc. R. Soc. B 276: 3037–3045.
Kiers, E.T., T.M. Palmer, A.R. Ives, J.F. Bruno, and J.L. Bronstein. 2010. Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13(12): 1459-1474.
Lots of plants eat poop (via roots), but pitcher plants acquire their fertilizer in a bizarre way: by becoming toilets. Check out these sweet examples:
Pitcher plants are well known for their carnivory: they live in soils with low nitrogen content, and they have spectacular adaptations for catching and digesting arthropods as an alternative means of nitrogen acquisition. But in Borneo, there are some pitchers that aren’t so great at catching arthropods. For instance, the Nepenthes lowii pitcher plant produces two kinds of pitchers: when the plants are immature, their pitchers are close to the ground, and they are proficient at catching and digesting arthropods. But when the plants are mature, they produce aerial pitchers with different shapes, open lids, no slippery wax, and rough inner surfaces. In other words, the aerial pitchers are missing many of the important adaptations for trapping arthropods. The aerial pitchers also have specialized nectar glands on the underside of the lid, and a super cute mammal called a tree shrew visits those nectar glands. And get this: the nectar glands are positioned in such a way that the tree shrew sits in the mouth of the pitcher plant while feeding, and that ensures that if the tree shrew defecates, it will fall into the pitcher plant. (You might need a visual of how shrews loo by sitting on the toilet backwards.) Clarke et al. (2009) estimated that 57-100% of the adult pitcher plants’ foliar nitrogen comes from tree shrew poo. Isn’t that wild?!
So, are tree shrews the only mammals that use pitchers as toilets? Nope. A different species of pitcher plant in the same genus (Nepenthes rafflesiana elongata) is also quite bad at catching arthropods. That was puzzling until Ulmar Grafe et al. (2011) found Hardwicke’s woolly bats (Kerivoula hardwickii hardwickii) roosting inside the pitcher plants during the day. In fact, the Hardwicke’s woolly bats that Ulmar Grafe et al. (2011) followed during their study roosted exclusively in pitcher plants! And the plants with bat visitors received ~34% of their foliar nitrogen from the bats. So, yeah, this interaction is kind of like paying for your room at a motel by leaving the toilet unflushed.
References:
Clarke, CM, U Bauer, CC Lee, AA Tuen, K Rembold, and JA Moran. 2009. Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5: 632–635.
Ulmar Grafe, T, CR Schoner, G Kerth, A Junaidi, and MG Schoner. 2011. A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7: 436–439.
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.
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.
Besides my typical holiday posts, this is going to be the last post of 2014. Where did the time go?! To celebrate the end of another awesome year of parasite ecology, I’m going to finish with one of my favorite symbiont stories of the year: sloth, their moths, algae, and poo.
I bet you guys have heard about this one, because it was in the mainstream news a bunch when the paper came out. Therefore, instead of summarizing the paper for you, I’m just going to say that it’s awesome, and you can read a summary here. You can also see a cute cartoon version of the story here. And of course, the citation for the paper is below.
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.
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!
Continuing my theme of Odes to Awesome systems, I want to tell you guys about one of my favorite animals: guard crabs. These crabs live on corals and deter starfish predators from attacking the corals by pinching the starfish. The guard crab cute factor is out of this world:
Photo credit: Bryan Mayes
I’ve been fascinated by guard crabs ever since I read the really thorough studies of Peter Glynn from the 1970’s and 1980’s. He did all kinds of work showing that guard crabs protect corals from predation by Ancanthaster starfish. Not all coral species have guard crabs, and Peter Glynn showed that populations of unprotected coral species are decimated during Ancanthaster outbreaks, while protected species suffer few losses. Furthermore, protected corals sometimes indirectly defend unprotected corals, because starfish won’t cross barriers of protected corals.
Previously, it seemed like some guard crab species were a lot better at protecting corals than others. This is true in other defensive symbiont systems, too (e.g., ants that protect Acacia trees). But I just read a really cool study by McKeon and Moore (2014) that shows that the slacker symbionts may not be as lazy as we thought! Specifically, small guard crabs aren’t very good at protecting corals from starfish predation. However, small guard crabs are good at protecting corals from smaller corallivores, like predatory snails. Furthermore, big crabs are no good at protecting against those smaller corallivores. (This is a cool parallel to the paper I talked about last week, where hydroids protect hermit crabs from limpets but not blue crabs.)
So, corals need functionally diverse guard crab communities – communities with large and small guard crabs – to be protected from multiple corallivore species. Awwwwesome!
Reference:
McKeon CS, Moore JM (2014) Species and size diversity in protective services offered by coral guard-crabs. PeerJ 2:e574.
Parasite Ecology 