Biotropica 46(1) Editor’s Choice: Hurricanes & Risk of Exposure to Parasites

Dr. Alison Behie in the field (photo: Dr. Ben Rawson)

Dr. Alison Behie in the field (photo: Dr. Ben Rawson)

I’m pleased to announce the January 2014 Editor’s Choice article: Alison M. Behie, Susan Kutz, and Mary S. Pavelka. 2014. Cascading Effects of Climate Change: Do Hurricane-damaged Forests Increase Risk of Exposure to Parasites? Biotropica 46(1): 25-31.

One of the most important consequences of climate change is the potential for altered frequency and intensity of storms such as hurricanes. Alison Behie and colleagues have taken advantage of a hurricane win Belize to study the susceptibility and exposure of black howler monkeys (Alouatta pigra) to parasites; their fascinating study yields insights into the potential for climate-related changes in diet, behavior, and forest structure to alter the risk of exposure to parasites. Below she describes the motivation for her study and its implications. Congratulations to Dr. Behie and colleagues!  EB

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It is well documented that when wild primates are found in disturbed forests they tend to have higher levels of parasitism. This is generally thought to be due to the fact that in such forests food is less available and often of lower quality, which can lead to nutritional stress. This sort of stress can have negative implications for many body systems including the immune system, potentially making animals more susceptible to contracting diseases, including parasites. This synergism between nutrition, stress and parasites was the topic of my PhD research, which documented the impact of a major hurricane on a wild howler monkey population in Belize. As co-author, Dr. Mary Pavelka, had been running the monkey River study site prior to the hurricane, I was able to use this natural experiment as a means to investigate how changes in diet and activity following severe habitat alteration affect the nutritional intake, stress levels and parasite load of the population and in turn how that related to patterns of population recovery.

 

Collecting ants from Cecropia for molecular analysis. Clockwise from top: Co-author Dr. Mary Pavelka, Barbara Kowalzik, Co-author  Dr. Susan Kutz, Tracy Wymam (photo credit: Megan Blades)

Collecting ants from Cecropia for molecular analysis. Clockwise from top: Co-author Dr. Mary Pavelka, Barbara Kowalzik, Co-author Dr. Susan Kutz, Tracy Wymam (photo credit: Megan Blades)

Our specific interest in the issue of the relationship between indirectly transmitted parasites and the types of trees that grow in disturbed areas arose with the Master’s thesis results of Barb Kowalzik. Working closely with co-author and parasitologist, Dr. Susan Kutz, this project was designed to profile and describe the parasites that could be retrieved in the feces of the howler study population over a 6 month period in 2007, and explore how parasites were affected by what food items the animals were eating. In her short study, Controrchis, an indirectly transmitted trematode that is contracted via the consumption of ants, was found to be the only parasite with a high prevalence.   This was initially puzzling to us as in 10 years of feeding data we have no records of the howlers intentionally ingesting ants, or insects of any kind.   This problem was fairly quickly solved by tests that showed that levels of Controrchis infection were significantly correlated with the time that both individuals and groups spent feeding on Cecropia, a pioneer species that is a known myrmecophyte, defended by ants.  This result provided the first circumstantial evidence to support an earlier speculation that black howlers might contract Controrchis by the accidental consumption of ants while feeding on Cecropia. It also provided us with a potentially significant ecological relationship that needed further probing.

 

Adult male black howling monkey ingesting Cecropia leaves (photo credit: Travis Steffens)

Adult male black howling monkey ingesting Cecropia leaves (photo credit: Travis Steffens)

As part of my own PhD research I had collected a larger parasite data set that spanned 18 months (2005 – 2006) and coincided with the collection of nutritional data from all ingested food items and fecal cortisol levels. My nutritional data revealed that Cecropia leaves are high in sugar and protein and low in fibre in relation to other trees in the forest. In addition Cecropia stems are the only items that meet sodium requirements. Couple this with the fact that Cecropia was significantly more abundant after the hurricane (relative abundance increased 40 fold by 2006) and it all started to make sense :  as a pioneer tree, Cecropia is abundant in disturbed areas, invests in rapid growth rather than in chemical or constituative defenses and is, as a result, a high quality food resource for the monkeys.   It is not limited by light so can easily produce sugar to inexpensively feed ants in exchange for defense.  Maybe the tiny ants that pour out onto the leaves in response to disturbance make it even more nutritious, but they also expose the monkeys to a parasite they would not be exposed to in an undisturbed forest where the pioneer Cecropia is much less common.

Despite this, we still wanted to show that exposure was the real mechanism responsible for the increased parasitism we saw post hurricane, and that it wasn’t just an artefact of potential malnutrition or dietary stress resulting from the altered food supply. As the fecal samples I collected were analyzed both for parasites and fecal cortisol we were able to use it as a proxy for stress and test it against the prevalence and intensity of all parasites discovered at high enough levels for further analysis (Controrchis, Trichuris, strongyle type eggs). Finding no relationship between any measure of susceptibility and any parasite variable we were confident that our proposed mechanism – that the increased consumption of highly nutritious myrmecophytic pioneer species following the hurricane increased exposure to the parasites.

Adult male black howling monkey ingesting the Cecropica stems, which are the only food items that meet sodium requirements (Photo credit: Dr. Lisa Corewyn).

Adult male black howling monkey ingesting the Cecropica stems, which are the only food items that meet sodium requirements (Photo credit: Dr. Lisa Corewyn).

This then led us to question if this pattern might be true of disturbance and primates in general, and if so, does this imply that increased exposure plays a bigger role in increased parasitism post-disturbance that it has been previously recognized? We know that as a direct result of disturbance, there is an increased abundance of many species of these nutritious pioneer trees, which can introduce ants into the diet of primates, possibly exposing them to a range of new indirectly transmitted parasites.     Proposing this idea to Dr. Steven Brewer, a botanist living and working part time in Belize, we were relieved that he encouraged and supported our suggestion that Cecropia may be an example of what is generally true of first and even second wave plant species that are committed to rapid growth, making them a high quality food source and reliant on external defenses as a result.   It is certainly true that the Pipers, the various genera of Acacia, and many of the legumes are fast growing and have symbiotic relationships with ants, suggesting that first wave species have stronger and longer lasting ant associations.  We hope that this paper will inspire other researchers to look at their own data to find evidence of a relationship between consumption of pioneer species and fecal parasites.

Juvenile black howling monkey resting in a Cecropia tree (photo credit: Meagan Ody)

Juvenile black howling monkey resting in a Cecropia tree (photo credit: Meagan Ody)

The next step of the puzzle for us will be to find the actual parasite in the Cecropia ants. We spent some time last May collecting ants from various Cecropia trees in Belize and can attest to their painful biting defense!  We are currently conducting molecular analysis in Dr. Kutz’s lab to positively identify Controrchis metacecarae in these ants.

Ants covering the stem and leaves of Cecropia (photo credit: Meagan Ody).

Ants covering the stem and leaves of Cecropia (photo credit: Meagan Ody).