The impact of parasites can often reach beyond their individual hosts, shaping populations and communities in their ecosystems. Parasites often control the behaviour of their hosts, leading to their role as “ecosystem engineers,” changing the ways in which the hosts physically shape their environments.
In lakes
and rivers, gammarid amphipods, small shrimp-like crustaceans, are known to act
as ecosystem engineers by digging into the sand, in a process called
bioturbation. Bioturbation is a major process in the ecosystem, as this digging
alters the concentration of oxygen in the sand, the concentration of nutrients
in the water, and the biological communities living in and on the sand. We
wanted to know whether the amphipods would dig into the sand more or less when
infected with behaviour-changing parasites, like Polymorphus minutus, and whether the temperature of the ecosystem
influenced the rate of digging.
Every year, the Trinity College Dublin Zoology, Botany, and Environmental Science moderatorship students (final year undergraduates) complete their own research projects related to their course. It has been my absolute privilege to spend time with these talented students and to watch their projects take shape. I am blown away by the dedication they show, the incredible topics they cover, and the way in which they approach their investigations. After their theses are submitted, the students hold a poster session where they present their work. From beetles to beer and back again, this year’s students have done impressive and solid work. I hope all our readers enjoy learning about these projects as much as I did! If you’d like to contact any of these students to congratulate them, offer them prizes/jobs, or learn more about their projects, most of them have included contact information. Without further ado, I’ll let them take it away! -Maureen Williams, PhD Student, Zoology
Last month, the Zoology Department’s Dr. David Kelly launched his first book of Japanese short form poetry, Hammerscale from the Thrush’s Anvil. At the launch of the book, David invited us in the audience to try our hand at writing our own haikus.
Taking him up on his challenge, and taking inspiration from his book, a few of us in the School of Natural Sciences have penned our own poems based on our areas of study. We even have a contribution from David Kelly himself!
Trying not to sacrifice coherency at the alter of syllable number was a rather new struggle for most of us, but we managed and, I’d like to think, emerged with a greater appreciation for the poets in our midst. Read on for our science-y foray into the arts!
Splitting the atom, unlocking the secrets of radiation, or even leading a peaceful civil rights movement.
I grew up knowing that these were the sorts of achievements that earn you a gold medal and an invitation to Sweden in mid-December. I have since learned that the annual ceremony held in honour of Alfred Nobel hasn’t always been awarded to the most deserving candidate, and that sometimes the winners simply stumbled upon a discovery that changed the world. This was not the case with the 2015 Nobel prize for Physiology and Medicine. Continue reading “A Nobel Pursuit”
As mentioned previously on the blog, Andrew Jackson and I started a new module this year called “Research Comprehension”. The module revolves around our Evolutionary Biology and Ecology seminar series and the continuous assessment for the module is in the form of blog posts discussing these seminars. We posted a selection of these earlier in the term, but now that the students have had their final degree marks we wanted to post the blogs with the best marks. This means there are more blog posts for some seminars than for others, though we’ve avoided reposting anything we’ve posted previously. We hope you enjoy reading them, and of course congratulations to all the students of the class of 2014! – Natalie
Here’s views from Sharon Matthews on Dr. Amy Pedersen‘s seminar, “A systems ecology approach to infection and immunity in the wild” and Dermot McMorrough’s take on Professor Christine Maggs‘ seminar, “Invasive seaweeds and other marine organisms”.
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It’s a ‘wormy’ world we live
Sharon Matthews
We all walk around thinking I will never have parasites but apparently our chances of becoming infected are high because there are around 1,400 species of parasite that can infect humans. If this news wasn’t bad enough, Dr. Amy Pederson informed us at her seminar that our chances of becoming infected with two or more parasites at the same time, is also very high. Dr. Pederson explained that through her work, she hopes to understand the phenomenon of co-infection and the interactions between these parasites in a host that drive this trend.
Dr. Pederson and colleagues showed through a meta-analysis of studies that co-infection is often associated with higher parasite abundance and a negative effect on human health. The interspecific interactions between parasites in a host can influence disease severity and transmission through the immunological responses of the host, making an environment more accessible for another species.
To investigate this phenomenon, Dr. Pederson chose to do a perturbation study using the wild species of wood mouse, Apodemus sylvaticus as a host system. A lot of past studies on parasitism have used a laboratory mouse model because of accessibility to the subject and ease of manipulation and control of confounding factors. I think it is very important to also have wild animal model systems because they strongly represent the variation and dynamics that would be seen in a real-life infection scenario. Also the wood mouse can be parasitised by 30 different species (both micro and macro parasites) and up to 70% of them can be co-infected which resembles the situation in humans.
Dr. Pederson wanted to determine the nature of the interactions among the parasite community in the woodmouse and to assess the stability of the community so she used the anthelminthic drug ivermectin to perturb the system. This drug targets nematodes, the most abundant member of this community so interactions between these and other groups should be apparent from perturbing their numbers. I liked the fact there was a longitudinal aspect to the experimental design as it allowed the effects on the parasite community to be analysed over time. All of the wood mice were tagged at the beginning and there were 3 different treatment groups: controls that received water at every monthly capture, a single treatment group and a group that received treatment of ivermectin at every capture. Faecal and blood samples were taken at each capture to check for levels of infection through egg counts and blood smears.
The results showed that treated mice had a 71% lower probability of infection 3 weeks after treatment than control mice but no difference was seen after one to two months because nematode numbers increased. This suggests that the effect on nematodes was short-lived and the community of parasites was resilient, returning to the original state before perturbation. This pattern for reduction and then returning to normal levels of infection was seen in Heligmosomoides polygyrus, the most abundant nematode in the community. This parasite shares an infection site with the protist, Eimeria hungaryensis. As the numbers of H. polygyrus reduced, the numbers of E. hungayensis increased and then returned to original levels once H. polygyrus recovered. This effect on a non-target species suggests that there may be a competitive interaction between the two species. They both occupy the same niche in the gastrointestinal tract of the wood mouse and reduction of numbers of the more dominant nematode may have given the protozoan a chance to use resources not normally available to it to colonise. No treatment effect was seen on any of the other parasite species.
The work of Dr. Pederson is very interesting and it gives us a window into the dynamics underlying co-infection. This work will broaden our understanding of the world of parasites and how they interact and will help inform us in our choice of treatment and which species may be effected by it. The one thing I was happy about coming out of the seminar was the fact that Dr. Pederson said, “those who are wormy usually remain wormy”. In other words, individuals with high burdens of nematodes (worms) show a tendency for reinfection over time. That leaves me with some hope that for at least now, I remain wormless and if the stats are anything to go by, I have a chance at remaining wormless for the forseeable future.
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Review of Christine Maggs’ seminar
Dermott McMorrough
The effect of invasive species is, by now, well documented and is often brought to light when species’ such as grey squirrels, American crayfish, zebra mussels, and Japanese knotweed turn up in a new environment; an event all to familiar to ecologists. Those listed above are just some of the examples of ‘alien’ species known to kill off native creatures and plants when they become established in new habitats. In Ireland, for example, the role of the North American Grey Squirrel has been well studied due to the effect they have had on our native Red Squirrel since their introduction into Co. Longford in 1911.
Invasive species have an incredible ability to migrate and establish themselves thousands of miles from their origin, either organically, or often with a helping hand from humans for example by hitching a ride as stowaways on trade ships or in ballast tanks, as has been the case with Zebra Mussels. The shared ability of the aforementioned species to colonise vast areas is no mere coincidence. Several species are introduced to new ecosystems, accidentally or otherwise, but relatively few have enjoyed such enduring success. Aside from threatening native species of plants and wildlife, the incredible growth of these species can lead to them negatively impacting on anthropogenic activities, whether it be fouling mooring lines or clogging water intake pipes as has been the case at the Guinness brewery at St. James’ Gate.
Professor Maggs’ seminar began with an explanation of how an invasive species can colonise an area. While her background was evidently in Botany, she made a particular effort to appeal to the zoologists in the audience with numerous references to the role of oysters in the spread of macro algae. Her research covers a fairly broad area, and pinpointing an exact research question has eluded many in the room. We were, however, treated to a synopsis of how invasives go about establishing themselves, and the methods often employed to prevent this process or eradicate it if it has already taken place. For example, methods such as immersing oysters in concentrated brine or flash boiling them have proven effective in fighting the spread of invasive algae, which use the oysters as a vector.
The spread of an invasive alga would not seem like an immediately worrying problem to those untrained in ecology. As with many problems in science, it is not until the issue directly affects the people in charge of policy making that anything is done to rectify it. This unfortunate criterion was evident in one of the examples used by Professor Maggs. In 2008, the city of Qingdao was due to host the Sailing event of the 29th Olympic games, but just weeks before racing was due to start, an algal bloom covered Qingdao bay in a thick layer of Enteromorpha algae. The presence and strength of the bloom was largely accredited to the high levels of nitrates in the water as a result of farmland runoff, coupled with higher than average temperatures and rainfall. During the seminar, the use of giant plastic sheets in San Diego Bay was seen as an American answer to an ecological problem, but it worked. Credit where credit is due. The imminent deadline of the Olympiad prompted the Chinese authorities to tackle this ecological disaster with what has to be the most wonderfully Chinese way possible: by ordering 20,000 locals to line the beaches, and man over 1,000 fishing boats to rake in the bloom manually. Sure enough, within a few days over 100,000 tonnes of the algae had been shipped out of the bay.
Increases in the amount of travelling done by humans and more importantly freight over the past century has led to an explosion in the ranges of successful invasive species, to the point at which one must wonder how endemic species can survive at all? The increased efficiency of our transit routes has also meant that invasives no longer rely on miracle migrations, such as that likely undertaken by the Iguana of the Galapagos. With the ever-increasing demand for fresh exotic produce in the developed world, the ships are getting faster, the coolers are getting colder, and the chances of an invasive species making it’s way around the world in less than 24 hours, perfectly preserved in Tesco wrapping and ready to colonise a new ecosystem have been made just that much easier. It seems that when it comes to being an invasive species, every little helps.
It has been estimated that less than 10% of global spending on health research is devoted to diseases or conditions that account for 90% of the global disease burden. These are mostly diseases of the world’s poorest people. The general public, and funding agencies, often equate third world diseases with the big three killers; HIV/Aids, tuberculosis and malaria. There is, however, a group of conditions known as neglected tropical diseases (NTDs) which have an even wider impact. They include some of the most common helminth parasites that, while don’t often kill, result in morbidity and debilitation. One of these, the large human roundworm Ascaris lumbricoides, is the focus of research by Professor Celia Holland at Trinity College Dublin.
A. lumbricoides infects over a billion people globally, mainly in tropical and sub-tropical regions. Infection occurs through the faecal-oral route. Poor sanitation results in soil becoming a reservoir for infectious eggs and ascarisis included within the group known as soil-transmitted helminths or geohelminths. This is why, sometimes, the salad is not the safest bet. Once swallowed the infective ova hatch in the small intestine. From the small intestine they migrate to the proximal colon, through the mucosa and onto the liver and eventually the lungs. In the lungs they penetrate the alveolar space, move into the pharynx where they are swallowed and returned back to the small intestine. The migratory route of ascaris and other related helminths may be an evolutionary holdover from a skin penetrating ancestor.
The discovery of the ascaris life cycle in humans is one of those great anecdotes that pepper medical history. In 1922 Japanese paediatrician, Shimesu Koino, infected both a volunteer and himself with ascaris eggs. He realised the larvae were migrating when he found large numbers of larvae in his sputum. Put plainly, he coughed up baby nematodes that had penetrated his lungs. Not a methodology likely to get past ethics committees today.
Worldwide, severe ascaris infections cause approximately 60,000 deaths per year, with serious health consequences observed in a further 122 million people. Children from preschool age to adolescents carry the greatest worm burdens. Ascariasis is the disease associated with ascaris infection and symptoms include appetite loss, lactose maldigestion and impaired weight gain. As children are at vulnerable stages of growth and development, these nutritional deficits lead to stunted growth, diminished physical fitness and impaired memory and cognition. Other symptoms of adult worms include abdominal distension and pain, nausea and diarrhoea. In heavy infections entangled worms have been known to cause intestinal blockages. The migrating larvae cause their own set of problems which include acute lung inflammation, difficulty in breathing and fever.
Ascariasis and other neglected infectious diseases are diseases that result from poverty but also help to perpetuate it. Children cannot develop to their full potential, and infected adults are not as productive as they could be. The good news is that there is a renewed momentum in combating these diseases. The World Health Organization (WHO), and public-private partnerships are linking their efforts to combat NTDs in a more coordinated and systematic way. The Bill and Melinda Gates Foundation have to date committed more than US$1.02 billion in grants to organizations working to address NTDs and have named ascaris as one of their newly targeted diseases. The WHO has set out a strategy for eliminating morbidity from soil transmitted helminths in children by 2020.
This makes Professor Holland’s new book “Ascaris: The Neglected Parasite”, a timely and important contribution to the fight against NTDs. The book is the first on ascaris in over 20 years and presents a wealth of new insights. The 16 chapters from top authors from around the world include detailed information on the biology, epidemiology, host and parasite genetics and public health and clinical aspects of A. lumbricoides and the closely related A. sum, an economically important parasite of pigs. As any researcher new to a field knows, having up to date research collected and summarised in an assessable format, with lists of lovely, lovely references, is a gift. This is the third book Professor Holland is senior editor on, the others being “Toxocara the enigmatic parasite” and “The Geohelminths: Ascaris, Trichuris and Hookworm”.
*by parasites here I am referring to all kinds of infectious disease causing agents including bacteria, viruses, fungi, protozoa, helminths and arthropods.
Why do we care about primate parasites?
Many of the most devastating infectious diseases in humans have origins in wildlife. For example, the global AIDS pandemic originated through human contact with wild African primates and influenza viruses circulate among wild bird populations. These are not only historical occurrences. Recently, for example, rodents were identified as the source of a Hantavirus outbreak in Yosemite National Park, USA . As human populations continue to expand into new areas and global changes in temperature and habitat alter the distributions of wild animals, humans around the world will have greater contact with wildlife. Thus, understanding which infectious agents have the potential to spread from animals to humans is crucial for preventing future human disease outbreaks.
Many efforts are being made to collate information on wildlife and human diseases. Much of my research (which I will blog about when I get chance!) uses an amazing database known as the Global Mammal Parasite Database or GMPD for short. Every time a paper is published which contains details of parasites found in either primates, carnivores or ungulates, the information is added to the database. As much data as possible is recorded, including the species infected, the type of parasite, the prevalence of the parasite, and the geographic location of the study. Prof. Charles Nunn and his colleagues have been collecting data for the GMPD since around 2005 and it currently contains around 6000 records for primates alone. This definitely makes it the most comprehensive dataset of primate parasites in existence.
The GMPD sounds amazing…so what’s the problem?
The problem with the GMPD (and this is a feature of virtually all datasets) is that there is sampling bias. Certain primates are sampled for parasites much more frequently than others. Chimpanzees, for example, are sampled for parasites all the time, whereas species such as tarsiers are sampled much less often. This has the effect of making it look like chimpanzees have far more parasites than tarsiers, simply because they have been sampled more often. In analyses using the database we usually deal with this problem by adding sampling effort into our models, so we give less emphasis to high numbers of parasites in primates we have lots of samples for. Unfortunately this problem is also evident when we look at parasites (things like malarial parasites are often sampled because of their importance to human health) and geographic regions (areas with primate research stations are sampled far more regularly than more remote regions). If we hope to use the GMPD data to make reliable predictions about future risks to humans, we need to identify gaps in our knowledge of primate parasites.
So what did you do?
Without going into the technical details, we looked across the primate phylogeny and primate geographic ranges to identify gaps in our knowledge, and used statistical models to investigate what factors led to primates and geographic areas being relatively well- or relatively poorly-sampled. We also used species accumulation curves to extrapolate parasite species richness for primates.
Where are the gaps in our knowledge?
We found that apes (chimpanzees, gorillas and orangutans) were generally better-sampled than other primates, but there was incredible variation in sampling among all other major primate groups. Apart from apes, the primates that researchers appear to sample most are the species they encounter most often, i.e., widespread, terrestrial, diurnal species. However, some primates were sampled more often because they are already intensively studied for other research, because they live in frequently visited field sites, or because of their importance in medical research. Across countries, we found that in general, parasite sampling is highest in countries with more primates to sample. We expected that the GDP of the countries would also affect sampling effort, with wealthier countries having more money for disease monitoring. However, we found no evidence for this in our analyses, probably because most research on primate diseases is not funded by the country in which the research takes place.
Sampling effort for primate parasites across the world. Poorly-sampled countries are in red, and better sampled countries are in yellow.
When we extrapolated parasite species richness values we found that even within our best-sampled primates and countries, we are missing a lot of parasites. On average we predicted that 38-79% more parasite species than currently reported in the GMPD should be found in our best sampled primate species, and 29-40% more parasite species than currently reported in the GMPD should be found in our best sampled countries. This emphasizes exactly how poor our sampling is across all primates and countries. Another concern is that although viruses make up only 12% of the parasites in our dataset, viruses arguably present the greatest zoonotic disease threat to humans because their fast rates of evolution should allow them to easily adapt to new hosts.
What next?
Identifying parasite sampling gaps across primate species and geographic regions is only the first step; we need to find strategies to minimize these sampling gaps if we are to predict which primate diseases may emerge in humans. One solution is to set research priorities based on the sampling gaps, for example, by focusing effort and funding on relatively poorly-sampled primate species, arboreal primates, those with small geographic ranges, or those found in relatively poorly-sampled regions of South East Asia, Central and Western Africa, and South America.
Focusing on relatively poorly-sampled primate species and areas may improve our general understanding of primate parasites, but it is only one factor in predicting risk to humans. For example, hosts are more likely to share parasites with their close relatives than with more distant relatives. Thus, continuing to focus our sampling efforts on parasites of our closest relatives (chimpanzees, gorillas and orangutans) may provide the greatest return in the case of risks to humans. This is particularly important because we found that chimpanzees are expected to have 33-50% more parasites than currently found in the GMPD. In addition, ecological similarities also influence parasite sharing among primates, and humans share more parasites with terrestrial than arboreal primate species. As with sampling effort, this probably reflects higher contact rates among humans and terrestrial primates compared to arboreal primates. As a related issue, a host living at higher density is expected to have higher prevalence of parasites and may have more contact with human populations or our domesticated animals, thus increasing opportunities for host shifts to humans. The large numbers of zoonotic emerging infectious diseases with rodent or domesticated animal sources also highlight the importance of rates of contact and host density for disease emergence in humans.
In conclusion Sampling effort for primate parasites is uneven and low. The sobering message is that we know little about even the best studied primates, and even less regarding the spatial and temporal distribution of parasitism within species. Much more sampling is needed if we hope to predict or prevent future emerging infectious diseases outbreaks.
The media is all abuzz about the Carter Centre’s recent announcement that 542 cases of guinea worm infection were reported in 2012. That is a remarkable achievement, considering that 3.5million cases where the reported when the Carter Centre began their eradication programme in 1986. The guinea worm (Dracunculus medinensis) is a particularly gruesome parasitic nematode that causes painful and debilitating disease. It is one species no one will be too sorry to see go. Well no one except the folks at the (tongue in cheek) Save the Guinea worm Foundation.
Perversely, considering our track record of causing extinctions, actually trying to get rid of a species can be extremely difficult. Targeted eradication of disease in humans has been successful only once before, with small pox. That required a massive and expensive vaccination programme and it is unlikely that the mandatory aspect of the vaccines would be tolerated today. However, helminths are a different beastie altogether. Helminths (parasitic worms) differ from pathogens in that, with a few exceptions, they don’t multiply within human hosts or have direct transmission. Helminths require a period of passage through the environment, either as infectious eggs or through other intermediate hosts. The guinea worm life cycle involves water fleas (Cyclopidae) as intermediate hosts. Water containing infected water fleas is drunk and the parasites are released. After about a year of maturation, females emerge via a painful skin blister, which erupts on contact with water, releasing thousands of larvae ready to continue the cycle.
The peculiarities of the life cycle meant the eradication programme was successful, not though vaccination or medication, but through changing people’s behaviour in the key areas of transmission and infection. To prevent infection people were taught about the need to filter drinking water, particularly standing water where cyclops abound. The burning sensation caused by the female worm emerging meant people often cooled the blister in a nearby pond, usually the same the one that supplied drinking water. By educating about the link between this behaviour and infected ponds, transmission of the larval stages was successfully reduced.
Of course, various other aspects of the guinea worm life cycle played a part. Cyclops is a relative large (1mm) so filtering material could be made and supplied cheaply. They are also immobile; once an infection is eradicated from an area it is easier to keep it out than in diseases like malaria. Unlike helminths that release eggs and larvae through the intestinal tract, people shedding guinea worm infectious stages are much more likely to be identified quickly.
One important factor influencing the success of small pox eradication was that the virus had no hosts other than humans. There is no wildlife reservoir from which the disease may re-emerge. Guinea worms on the other hand have been found in cats, dogs and cattle, though none appear to act as a reservoir for human infection. It may, therefore, be more correct to speak of elimination of human guinea worm infections rather than total eradication of the species. Save The Guinea Worm Foundation will be pleased.
No man is an island; the same could be said for the millions of life forms that populate our planet. Think of all the ways in which organisms interact with each other through predation, parasitism and the countless symbioses. Sometimes a pair of interacting partners can become inextricably linked such is their mutual dependence. Each one may provide the other with a resource it’s unable to obtain on its own.
A recent collaboration explored instances when these interactions lead to the loss of a trait and showed the fragility of this situation. One of the examples the authors use is an ant species that farms fungus. The fungus provides the ants with all the arginine (an amino acid) they need so they have lost the ability to synthesise it themselves. Thus anytime an ecological interaction involves some provision of a resource by one partner to another the evolutionary pressure is removed and the trait can be lost in the species receiving the goods. In other words we end up getting ‘compensated trait loss’ due to the ecological interaction. This can tighten a symbiosis from a facultative to an obligatory one.
But the fragility of compensated trait loss should be obvious now. In the ant example, were the fungus to go extinct the ant would disappear along with it. It’s like the ecological interaction is undermining all the good work done by natural selection in providing the ancestral ants with all the traits they need. The authors reckon that trait loss is “grossly underestimated” which puts many species in a precarious position in this age of mass extinction. Although there have been some instances where the trait was recovered, in flagrant disregard for Dollo’s law. Some of these law breakers include parasitic insects who regained their ability to synthesise lipids once the provision was lost.
A difficulty in studying these systems is how to detect when trait loss is taking place. A decreased expression of some gene in some members of a population would probably be reported as natural variation. But with ever improving molecular techniques we will be able to get a better estimate of the number of compensated trait loss interactions.
