Part Three: Untangling the Mystery of Red Gaster Ants
By Dr. Kyle Lesack
The ability of certain parasites to modify the appearance or behaviour of their host to increase the likelihood of transmission to another is among the most impressive evolutionary achievements. The roundworm Myrmeconema neotropicum is particularly noteworthy, being a rare example of a parasite that causes dramatic changes in both the appearance and defences of a host species. These small worms infect the ant species Cephalotes atratus whose gaster they turn bright red. This transformation of the ant shows a striking similarity to ripe berries and is believed to facilitate the parasite’s transmission to a bird host species. Importantly, the gaster transformation is accompanied by behavioural changes, including decreased defence responses that could otherwise deter bird predation. This parasitic relationship was first described in a 2005 paper by Dr. Yanoviak and colleagues (1), who hypothesized that the red gaster plays an adaptive role that facilitates the parasite’s transmission to a fruit eating bird host, where it completes its life cycle. The work described in this paper provides an excellent overview of parasitology field work and valuable insights into how scientists design their experiments to test their hypotheses. [kl1]
Differences Between Infected and Uninfected Ants[CL2]
To quantify the impact of M. neotropicum on the ants, they characterized the physical differences between infected and uninfected ants collected from colonies located in Panama and Peru. Unsurprisingly, the most conspicuous difference was the bright red gaster of the infected ants. They also noted that infected ants frequently held their gasters in a raised position, a behaviour known as gaster flagging. Surprisingly, the infected ants were found to be both 10% and 40% heavier[CL3] [CL4] . While this may seem to be a contradiction, it is consistent with parasites being able to both impair host growth and contribute extra weight.
Figure 1: Normal (right) and infected (left) ants.
Why turning ant hosts gaster to a berry color? [and the lifecycle]
“Based on the behaviours of rainforest birds and how conspicuous red things are in a mostly green environment, putting all pieces together it seems like this parasite is causing the ant to resemble a red fruit.” Said by Dr. Yanoviak. The red gasters are full of nematode eggs, being predated by birds, they would being deposit somewhere else in bird feces. “This particular species of ant is quite found of bird feces, as they are really good source of nutrients and salts.” Ants likely pick up the eggs through bird feces and fed the eggs to the larvae in the colony. This is the part we are currently unknown about the lifecycle of this parasite - how the eggs transmitted into larvae ants. It’s presumably through forager ants fed the egg to the larvae ants, or the forager ants brought them back to the nest, and the nematode burrowing through larvae ants body wall. Then these eggs develop inside the ant larvae and become adult nematodes. At the pupil ant stage, the nematode migrate to the gaster of the ants. Before ants emerge as adult ant, the nematode mate and male die inside the gaster. The new adult ants are initially black, and they spends most of time tending brood inside the colony. As the workers age, they started foraging. At this time the nematode eggs are developing inside the gaster of the ants, it’s becoming increasingly red. And they become more sluggish, with the constant gaster flagging behaviour, they are very conspicuous. “When you see them in the field it’s like oh yeah, that’s really a bright red ball on the end of that ant.” Presumably birds like Red Cap Mannequins that eat red fruit would bite off the gaster from an ant, and disperse it somewhere else.
Is the Red Gaster an Adaptive Trait?
Science has provided countless benefits, which, in large part, can be attributed to how the scientific method compensates for many of our biases and flawed thinking. It is common for people—and many biologists—to assume, rather than demonstrate, that a given trait is adaptive, having been selected for by natural selection. Due to its striking resemblance to a berry, it is hard to doubt that the parasite-induced gaster change is an adaptive trait, selected to facilitate transmission to a bird host. Nonetheless, it is important to demonstrate that this resemblance is not coincidental, but a true adaptation evolved that provides an advantage to the parasite. Several experiments were included to test this hypothesis and the results provided further evidence that supported this view. For example, the colour properties of the red gasters and a local fruit Hyeronima alchorneoides were quantified. Both the red gasters and fruit had similar properties, consistent with the gasters being a mock food source.
After noticing that the red gasters easily detached when handled in the lab, the researchers decided to quantify the force required to detach the gaster from infected and uninfected ants. The force required to detach the gaster was significantly lower in the infected ants, indicating that it could be easily plucked by a predator.
The researchers also observed the ants’ behaviour and identified several key changes that occurred in the infected ants. Those related to defence responses were of particular importance, as insect eating birds typically avoid this ant species[CL6] . For example, infected ants were described as being lethargic and less inclined to bite when handled. Furthermore, they produced fewer alarm pheromones that are associated with the C. atratus defence responses. [placeholder for behaviour quote][kl7] [CL8] . The timing of parasite-induced changes is often informative. If the gaster plays an adaptive role in attracting a host, the colour changes should coincide with the onset of the parasite infectivity. This is exactly what was observed in the infected ants, as both the peak gaster redness and parasite infectivity occurred at the same time. Furthermore, the magnitude of the gaster reddening was associated with the severity of the behavioural changes. Together these findings suggest a synchronization between the parasite’s development and the changes it induces in the host.
Mechanisms underlying the parasite caused fruit mimicry
Dissection revealed that the colour change was not a product of red pigment; rather, thinning of the ants’ exoskeletons accounted for the reddening. “When the Myrmeconema neotropicum larva are developing inside the eggs inside the ant gaster they are slowly thinning that exoskeleton and it is the combination of the amber color of the exoskeleton and the yellowish color of the eggs inside it plus a little bit of sunlight that creates this red appearance in the field.”, said by Dr. Yanoviak. The thinning of the exoskeleton might also be the reason for the weakening of the post patio connection to make the gaster fall off easily.
For the gaster flagging behaviour, Dr. Yanoviak said, “We don't know what biochemical changes are happening within the ants; we do know that the ventral nerve cord of the ants so the main nerve chord of the of the insect is modified by the parasite and it appears to be atrophied.” “We believe that's probably what's causing the ants to have the gaster flagging behavior so consistently. As far as we know the ants have no sense of that the gaster even being present at that point.”
Evidence of Bird Predation
The researchers included several experiments aimed at characterizing predation by fruit eating birds. Although they did not observe any bird predation on either infected or uninfected C. atratus ants, their results provide indirect support for a fruit eating bird being a host. In the first experiment, infected and uninfected ants were attached to fishing line and suspended side-by-side from branches in the forest canopy. The proportion of missing gasters was higher in the infected ants compared to the uninfected group. In most cases, the missing gaster was not found in a colander they had placed underneath the ants to collect any fallen body parts.
In another experiment, clay balls of various colours were placed on pins and suspended from branches in the forest canopy. These included multiple colours, including red and pink, which approximated the size and appearance of an ant gaster. An analysis of the clay balls revealed that a higher proportion of red and pink balls were either missing or showed signs of bird attack, results consistent with the red gasters being associated with bird predation.
Lastly, they fed an infected and uninfected ant to a chicken and analyzed the feces afterwards. Hundreds of intact parasite eggs were observed in the chicken feces within several hours of being fed the infected the infected ant. The researchers also noted that 68% of the solid material collected by foraging ants was comprised of bird feces. These results provide a plausible mechanism for the dispersal and transmission of the parasite. According to Dr. Yanoviak "This particular species of ant really um is quite fond of bird feces. Birds don't digest everything that they eat and so the ants will scavenge up the rest of that including the seeds or dead insect parts that are in the fecal material."
Putting the Pieces Together
These experiments allowed Dr. Yanoviak and colleagues to piece together the different parts of the puzzle. They describe how Myrmeconema neotropicum, a tiny worm, transforms its ant host into a strikingly different creature to infect the next host. Once infected, the ants gradually develop a bright red gaster and exhibit reduced defence responses. In doing so, fruit eating birds are fooled into thinking it is a delicious berry, ripe for the picking. The gaster is then digested and the parasite eggs are passed in the bird feces. The cycle is completed once the parasite-infested feces are collected by ants and fed to developing larvae.
This research provides and excellent example of parasitology field-work and how to test scientific hypotheses. Due to its resemblance to a berry, the researchers hypothesized that the red gaster was, in actuality, a parasite-induced change that facilitates transmission to a fruit eating bird host. The experiments that they performed to test this hypothesis are notable for their simplicity and creativity. To collect evidence in support of bird predation, they used fishing line to suspend infected and uninfected ants from branches, as well coloured clay balls that approximated the appearance of the ant gaster. To see if the parasite eggs could spread through bird feces, they fed an infected ant to a chicken. Although many parasitology studies would not have been possible without complex and expensive laboratory methods, these experiments show meaningful insights can be gained using items available at a sporting goods or craft store.
" I think this is a good example of how much we still need to learn about the biology of tropical rainforest. There's so much diversity. There's not only actual biodiversity in terms of genetic and species diversity that exists out there, is also a diversity of interactions, diversity of behaviors. There's just a lot going on out there, and it's a question of being in the field and keeping your eyes open and exploring things that that you're curious about. and for me that's one of the more fulfilling or perhaps the most fulfilling aspect of this job is out there discovering new patterns and um new phenomena in nature.“ Said Dr. Yanoviak.
Why would a worm turn an ant into a berry? In short, to infect a bird host.
References
1. Price PW. General Concepts on the Evolutionary Biology of Parasites Author ( s ): Peter W . Price Published by : Society for the Study of Evolution Stable URL : http://www.jstor.org/stable/2407761 . Evolution (N Y). 1977;31(2):405–20.
2. Kaya H, K. Horsehair worms, Hairworms [Internet]. 2013. Available from: https://ipm.ucanr.edu/PMG/PESTNOTES/pn7471.html
3. DeLaCruz D. Leucochloridium paradoxum. 2003; Available from: https://animaldiversity.org/accounts/Leucochloridium_paradoxum/
4. Yanoviak SP, Kaspari M, Dudley R, Poinar G. Parasite-induced fruit mimicry in a tropical canopy ant. Am Nat. 2008;171(4):536–44.
Comments