Thursday, August 25, 2016

A story on competition. Competition and parasites, sort of.

I was recently talking about my PhD work with some new colleagues in the Department, when I realized I was getting a little bit nostalgic. Working in Trinidad was a great experience, and I had a lot of fun doing all the small and large experiments, but in reality one of the things I missed the most was one little fish – and no, it was not the Trinidadina guppy.

Fig. 1. I guess that they do look like they are smiling...

During one of my first trips to the island, I got to familiarize myself with the very charismatic jumping wabeen, or more formally Rivulus hartii. It is hard to explain why I got so fond of this little guy, but many people that have worked with Rivulus share the same feeling – although many others don't even want to hear about them, and you will know why soon. My love for Rivulus, like any other love relationship, went through ups and downs. Rivulus tend to jump (a lot!), and that is why their local name is jumping wabeen. You cannot leave one inch of the aquaria uncovered because one by one they will jump out, and you will end up with a parade of jumping little blobs on your lab floor. Those were the days I hated working with Rivulus. Then were the days that they were sitting quietly in their aquaria, looking straight at me with their huge, baby eyes and big smile (or at least that is how their mouth looks to me, see for yourself in Fig. 1). Those were the days when I loved working with Rivulus. But then again were the days where you needed to transfer two of them to a new facility, and make the mistake to put different sizes together. You still arrive to your destination with the two fish, but one will definitely be inside the other – in a way, it was similar to  the painting " Big fish eat small fish" by Pieter Bruegel the Elder (Fig. 2), where pretty much every fish is munching on a smaller one, which is munching on a yet smaller one. Those were also the days I hated working with Rivulus.

Fig. 2. Big fish eat small fish by Pieter Bruegel the Elder. I really like the walking fish munching on a smaller one.

The fact that Rivulus are relatively small and voracious, and coexist with the Trinidadian guppy has been of great interest to many ecologists and evolutionary biologists – among which I can certainly include myself. In particular, I was very interested in how the interaction between guppies and Rivulus could be affected by a guppy specific parasite, Gyrodactylus (you can see some of my previous blogs about guppies and Gyros). But before I go into the details of that experiment let me talk a little bit more about Rivulus' ecology. Adult Rivulus  are much  larger  than  adult  guppies (the largest Rivulus are almost three times larger than the largest guppies!) and  are  strict  predators,  foraging  mainly  on everything that fits in their mouth, like invertebrates  and  small  fish,  including  juvenile  guppies. Juvenile  Rivulus,  on  the  other  hand,  are  of  similar size as guppies, and directly compete with guppies for shelter and food (i.e. aquatic invertebrates). Previous studies have also shown that the  presence of guppies  decreases the  growth  rate  of  size-mathced juvenile  Rivulus   – through resource competition – but dramatically increases the growth rate of adult Rivulus, through guppy predation on Rivulus young, and the release of adult Rivulus from intra-specific competition. Given these strong interactions between the various classes of Rivulus and guppies, it was very conceivable that a guppy-specific parasite could tip the balance in Rivulus' favor. Or at least that was my initial hypothesis.

I designed an experiment that would allow me to break down the different effects of Rivulus, guppies and the guppy-specific ectoparasite, Gyrodactylus, could have on both fish species' growth. The experiment  consisted  of five  experimental  treatments:  guppies  only  (GO);  guppies and Gyrodactylus (GG); guppies,  Gyrodactylus, and Rivulus (GGR); guppies and Rivulus (GR); and Rivulus only (RO). I made sure that the total biomass was, if not equal, very similar among the different replicates, and put the sized-matched fish in mesocosms that replicate natural streams (i.e. lots of gravel with invertebrates and algae, flowing water, etc.), and came back 20 days later to see how much guppies and Rivulus had grown in the presence of each other and/or the parasite. (if you want to check out the full article with the detailed methods you can do it here).

 The results were somehow surprising. Remember that I said that my hypothesis was that Gyrodactylus was going to tip the balance in favor of Rivulus. I found that the presence of  Gyrodactylus  parasites  decreased  female  guppy  growth, and this effect was much stronger than the effect of Rivulus  (Fig.  3), but more intriguingly I found a very  strong  antagonistic  interaction:  Gyrodactylus  reduced   guppy  growth  in the  absence but  not the  presence  of Rivulus.  In  short, the  relative  effect  of  Gyrodactylus  on  the  growth  of  guppies  was  much  greater  than  that  of  the  competitor  (and potential predator), but the two effects were strongly interactive. In other words, Gyrodactylus did not significantly affect the interaction between Rivulus and guppies!!!

Fig. 3. Gyrodactylus did not influence Rivulus-guppy competition, but certainly had an effect on its own!

 In the paper, my co-authors and I suggest  two  potential  mechanisms that may have prevented Gyrodactylus from influencing the guppy-Rivulus interaction. First, the coexistence  between  guppies  and  Rivulus  has  been commonly viewed as a balance between predation and competition, with guppies being the better competitors, but large adult Rivulus actively preying upon juvenile guppies. So, although we did find a trend for a decrease in growth of Rivulus in the presence of size-matched guppies, this was not significantly different from the Rivulus-only control. It is possible that under these experimental conditions competition is lessened due to relatively low fish density per mesocosms; however, an alternative possibility is that Rivulus grow larger than guppies and shift their diet towards terrestrial prey that are too large for guppies to eat, releasing them from  resource  competition. Indeed, at the end of the experiment Rivulus in the mixed-species treatment were almost three times larger than female guppies, despite being of similar size as the largest female guppies in the mesocosms at the beginning of the experiment. Second, as  an  apparently  adaptive response  to reduce  Rivulus  predation on juvenile guppies, these increase their growth rate when exposed to chemical cues from adult Rivulus.  Guppies  might  thus  show  a  phenotypic response  to  Rivulus  as  a  potential  predator, and not a competitor.  Even  though the Rivulus in our experiment were not large enough to eat the guppies, the presence of small Rivulus is presumably a  reliable cue of the likely presence of larger Rivulus. If guppies increased their growth in response to chemical cues signaling the presence of Rivulus, this would have partially counteracted the negative effects of parasitism on guppy growth, consistent with our observation that female  guppy in the presence of Gyrodactylus and Rivulus was intermediate between guppy-only and guppy–Gyrodactylus treatments.

 I certainly think that these results generate several important insights into the nature of guppy–GyrodactylusRivulus interactions and, more generally, food web interactions. But these results have also helped me better understand what is going on in the small and shallow tributaries of Trinidad, where I spent several nights and days exploring and collecting fish.

Rivulus are more easily collected at night, so Pierson Hill had this great picture of one of those days I helped them collect Rivs for David Reznick's FIBR project.

Our paper:  Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. and Scott, M. E. (2016), An experimental test of antagonistic effects of competition and parasitism on host performance in semi-natural mesocosms. Oikos, 125: 790–796. doi:10.1111/oik.02499.

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