March 20th, 2016
The Arctic Ocean
Interestingly and coincidentally, “Arctic” comes from the Greek word αρκτος -arctos-, which means “bear” and is a reference to the constellation Ursa Minor, where is the North Star, which indicates the geographic North Pole .
The Arctic constitutes a unique ecosystem of the Earth, consisting of a large ice field, or ice-covered ocean, sometimes regarded as the northern part of the Atlantic Ocean, and it is surrounded by land, which is permafrost, with complete absence of trees. Life in the Arctic consists of organisms adapted to ice, including zooplankton and phytoplankton, fish, marine mammals, birds, land animals, plants and human societies fully adapted to the extreme conditions of the environment.
Due to global warming, isotherms are moving northward at a rate exceeding 50 km per decade over the past 30 years, so if we define the Arctic from a defined temperature or the tree line, its size is diminishing, being the reduction of sea ice the most visible effect.
Anthropogenic climate change: global warming, especially in the Arctic
Yes: climate change is here and it is generated by human activities, that is, it is anthropogenic. Previously there have been on Earth fluctuations in global temperature caused by natural phenomena, usually long-term and cyclical variations. For example, glaciations since about 2 million years are repeated every 100,000 years, and last ice age ended 15,000 years ago. So we are living now in an interglacial period and the next ice age could become not before 50,000 years. The cause of this cycle of glaciations seems to be orbital variations of the Earth, resulting in a lower insolation in high latitudes of the northern hemisphere during glacial periods.
Solar activity, like other stars, has cycles and roughly every 600 years there are periods of little activity (absence of very few solar spots and auroras), with lower energy output, which corresponds to cold periods in the Earth’s climate. The last minimal was in the period 1645-1715, and therefore from the middle of the eighteenth century we enjoy a maximum solar activity, with small cycles of minimum and maximum every 11 years.
Discounting these natural variations, it is clear that throughout the 20th century and especially since the 1960s there has been a steady increase in global average temperature (Figure 1), reaching almost 1ºC more than the beginning of the 20th century. In the early years of the current century the trend is worsening. The last 10 years have been the warmest since there are records, and the forecast is to continue increasing. Most experts agree that humans exert a direct impact on the heating process known as the greenhouse effect. The causes of this effect are some of gaseous components of the atmosphere, especially CO2, which has grown in parallel with rising temperatures, from about 300 ppm at the beginning of 20th century to nearly 400 ppm today. This CO2 and other gases as water vapour, methane and other exclusively anthropogenic absorb radiation and the result is that the atmosphere warms further.
Figure 1. Increase in average global temperature compared to the beginning of 20th century (from GISTEMP).
This global warming is particularly evident in the Arctic. The temperature increases are higher in northern latitudes, especially 60-70º N, where this past December 2015 (Figure 2) have raised to 9ºC above average in large areas of North America and Eurasia. This is called Polar Warming Amplification (PWA). The cause of this overheating in the Arctic respect of the rest of Earth is partly due to the loss of snow and ice (retroactive effect) because the largest area of land and water absorbs more solar energy than white ice (albedo effect), but also the PWA is partly due to the dynamic atmospheric transport, which transports heat energy from the clouds and subtropical regions to the north (Taylor et al 2013).
Figure 2. Thermal anomaly registered in December 2015 with respect to the average 1951-1980 (from GISTEMP).
Besides the consequences of this warming on the Arctic ice that we will comment below, another serious problem is the melting of permafrost, since then methane gas trapped under the frozen ground is released. This way, vast quantities of methane are released, and this greenhouse gas is contributing further to accelerate the global warming.
Less and less ice in the Arctic
Linear trends of sea ice extent and sea ice in the Arctic from 1979 to date are negative year after year, for any month is considered, but it is more clear by comparing Septembers, at the end of the summer when the ice is melting (Figure 3). Of the approximately 7 million km2 minimum in September (the maximum in March is about 16 million), about 100,000 km2 are melt per year, almost 9% every 10 years (Serreze et al 2007), so that there is now almost half ice than in 1979 (Figure 4).
Figure 3. Comparison of the extent of sea ice (in red): September 1979 and 2012 (from The Cryosphere Today).
Figure 4. Average monthly extension of Arctic sea ice since 1979 (Reeves et al 2013).
In addition to the reduction in surface ice, keep in mind the reduction in volume, representing now a third of what it was in September 1979.
There is a big difference between the different models for predicting the disappearance of Arctic sea ice. Half of them expect the total disappearance by September 2100. Predictions move since September 2040 the less optimistic until well past 2100 for the other (Serreze et al 2007).
Other problems resulting from the disappearance of sea ice are the ship traffic, which could shorten distances trips between the ports of northern countries, and on the other hand the exploitation of oilfields and other fossil fuels and minerals, since there is a large part of global reserves in the Arctic (Figure 5).
Figure 5. Left: forecast paths for open sea ships (blue) and for icebreakers (red) for 2040-2059. Right: Distribution of the potential major reserves of oil and gas (yellow) and licenses (red) and wells in operation or to operate (black). The dashed line indicates the limit of Conservation of Arctic Flora and Fauna (CAFF) declared by the Working Group of the Arctic Council (www.arctic-council.org). Figures from Reeves et al (2013).
Ecological consequences of the disappearance of the Arctic ice pack
There are many living beings linked to the ice. The polar bears roam on the Arctic ice, so we are feared for his fate. Many fish, seals and crustaceans (krill) form a food chain that starts from the algae that grow under the ice in a very consistent environment, rich in nutrients, especially favourable for marine life (Figure 6 A). Moreover, floating sea ice in summer is a good corridor for dispersion of terrestrial vertebrates (for instance arctic foxes) and plants.
The gradual disappearance of sea ice and warming in the Arctic coast involves a series of ecological imbalances (Figure 6 B). We see for example how walruses forced to remain grouped on the ground are more predisposed to disease transmission. The loss of sea ice diminishes dispersion by ice corridors and then the land populations are most isolated, thus gene flow is restricted. Polar bears and other predators that hunt on the sea ice have it much harder and their populations are at risk. Phytoplankton productivity decreases significantly, thereby reducing zooplankton, and then the whole food chain (fish, seals, etc.) is affected (Post et al 2013).
Figure 6. Ecological interactions influenced by sea ice. A: The distribution and seasonality of sea ice affects the abundance, distribution and interactions of the entire ecosystem in balance. B: The longest period without ice and less sea ice extent have disastrous consequences on the balance of the ecosystem (Post et al 2013).
The polar bear tries to survive
The polar bear (Ursus maritimus) is considered an endangered animal. There are only about 25,000 worldwide. The impact of climate change affects the exclusive habitat of polar regions and forecasts suggest that in a few years from now the ice of the Arctic will melt permanently and polar bears may become extinct because of warming area.
The polar bear is basically carnivorous, unlike others such as brown bears, and remains above the ice hunting seals. With the gradual disappearance of the ice it has more trouble finding preys, and some have begun to learn how to catch salmon rivers, as we see in the images (Figure 7).
Figure 7. White Bear dedicated to fishing salmons in order to survive (www.youtube.com/watch?v=9m_Q9Ojbcmw).
We have also seen groups of polar bears at sea fishing (see video) and dive emerging alternately as if they were dolphins or porpoises. Despite these small adaptations, the food is very low and it is clear that their populations are declining rapidly.
Orcas thrive north
The disappearance of the northern ice is a dramatic ecological change that is causing the disappearance of some species like the polar bear, but interestingly these imbalances benefit some other emerging species. This is the case of the killer whale (Orcinus orca), which is thriving more and more to the north (Figure 8).
Figure 8. Places (marked with numbers) of the Canadian Arctic where groups of orcas were repeatedly photographed between 2004 and 2009 (Young et al 2011).
Eskimo Inuit people live around the American Arctic (from Quebec to Alaska including Hudson Bay and adjacent islands) and the west coast of Greenland, and they are the first witnesses since the mid-twentieth century observing whales in their waters, unknown before. Moreover, in recent years scientists have made numerous orca’ sightings, they have been photographed individually (Young et al 2011), and their travels have been followed through bioacoustics (Ferguson et al 2010) and other techniques.
Figure 9. (Top): Narwhals with the characteristic great tusk, which gave rise to the myth of the unicorn. (Low): Group of orcas attacking narwhals cornered on the beach. Watch the video of PBS Nature.
For some years attacks by orcas on narwhals (as in Figure 9) have been observed repeatedly by Inuit Eskimos and studied in detail by several scientists. Laidre et al (2006) observed that before approaching whales, the narwhals tend to group, are more quiet and swim closer to the beach in shallow waters. During the attack, the narwhals disperse significantly but nevertheless mortality is very high. After predation, which can last several hours, oily stains are observed in sea surface, which come from fat of depredated narwhals (Figure 10).
Figure 10. Group of orcas surrounded by patches of oil on the sea surface from the fat of attacked narwhals (Laidre et al 2006).
Orcas’ attacks on narwhals are so common and effective that are beginning to affect the population. The effects are even worse in other cetaceans with smaller population such as whales of Greenland or bowhead (Balena mysticetus), which are now virtually extinct (Figure 11).
Figure 11. Scheme of preys’ proportions by a group of orcas from Hudson Bay (Ferguson et al 2010).
In conclusion, anthropogenic climate change is affecting the Arctic ecosystem severely (and all the other ecosystems), and although this problem is becoming known, effective policy measures to reduce emissions of CO2 and other greenhouse gases are so scarce that hardly will arrive in time. We are leading the planet Earth to a massive extinction of species and ecological changes ever seen in the history of humans.
The picture says it all: polar bear habitat is running out.
Arctic Council: http://www.arctic-council.org
Ferguson S.H., Higdon J.W. & Chmelnitsky E.G. (2010) The rise of killer whales as a major Arctic predator. In S.H. Ferguson, et al. (eds.): A little less Arctic: top predators in the world’s largest northern inland sea, Hudson Bay. Pp. 117–136. New York: Springer
GISTEMP, Goddard Institute for Space Studies Surface Temperature Analysis (NASA-GISS): http://data.giss.nasa.gov/gistemp/
Hawkings E (2014) nov 28: http://www.climate-lab-book.ac.uk/2014/hiatuses-in-the-rise-of-temperature/
Laidre KL, Heide-Jørgensen MP, Orr J (2006) Reactions of narwhals, Monodon monoceros, to killer whale, Orcinus orca, attacks in the Eastern Canadian Arctic. Can. Field Nat., 120, 457–465
Morell V (2012) Killer whale menu finally revealed. http://www.sciencemag.org/news/2012/01/killer-whale-menu-finally-revealed
Post et al. (2013) Ecological Consequences of Sea-Ice Decline. Science. DOI: 10.1126/science.1235225: http://www.carbonbrief.org/knock-on-effects-for-wildlife-as-the-arctic-loses-ice
Reeves RR et al (2014) Distribution of endemic cetaceans in relation to hydrocarbon development and commercial shipping in a warming arctic. Marine Policy 44, 375-389
Serreze MC, Holland MM, Stroeve J (2007) Perspectives on the Arctic’s shrinking sea-ice cover. Science 315, 5818, 1533–6.
Taylor PC, Cai M, Hu A, Meehl J, Washington W, Zhang GJ (2013) Decomposition of feedback contributions to Polar Warming Amplification. J Climate 26, 7023-43
The Cryosphere Today: http://arctic.atmos.uiuc.edu/cryosphere/
Young BG, Jeff W. Higdon JW, Steven H. Ferguson SH (2011) Killer whale (Orcinus orca) photo-identification in the eastern Canadian Arctic. Polar Research Vol 30
21st March 2015
Clostridia: who are they ?
The clostridia or Clostridiales, with Clostridium and other related genera, are Gram-positive sporulating bacteria. They are obligate anaerobes, and belong to the taxonomic phylum Firmicutes. This phylum includes clostridia, the aerobic sporulating Bacillales (Bacillus, Listeria, Staphylococcus and others) and also the anaerobic aero-tolerant Lactobacillales (id est, lactic acid bacteria: Lactobacillus, Leuconostoc, Oenococcus, Pediococcus, Lactococcus, Streptococcus, etc.). All Firmicutes have regular shapes of rod or coccus, and they are the evolutionary branch of gram-positive bacteria with low G + C content in their DNA. The other branch of evolutionary bacteria are gram-positive Actinobacteria, of high G + C and irregular shapes, which include Streptomyces, Corynebacterium, Propionibacterium, and Bifidobacterium, among others.
Being anaerobes, the clostridia have a fermentative metabolism of both carbohydrates and amino acids, being primarily responsible for the anaerobic decomposition of proteins, known as putrefaction. They can live in many different habitats, but especially in soil and on decaying plant and animal material. As we will see below, they are also part of the human intestinal microbiota and of other vertebrates.
The best known clostridia are the bad ones (Figure 1): a) C. botulinum, which produces botulin, the botulism toxin, although nowadays has medical and cosmetic applications (Botox); b) C. perfringens, the agent of gangrene; c) C. tetani, which causes tetanus; and d) C. difficile, which is the cause of hospital diarrhea and some postantibiotics colitis.
Figure 1. The four more pathogen species of Clostridium. Image from http://www.tabletsmanual.com/wiki/read/botulism
Clostridia in gut microbiota
As I mentioned in a previous post (Bacteria in the gut …..) of this blog, we have a complex ecosystem in our gastrointestinal tract, and diverse depending on each person and age, with a total of 1014 microorganisms. Most of these are bacteria, besides some archaea methanogens (0.1%) and some eukaryotic (yeasts and filamentous fungi). When classical microbiological methods were carried out from samples of colon, isolates from some 400 microbial species were obtained, belonging especially to proteobacteria (including Enterobacteriaceae, such as E. coli), Firmicutes as Lactobacillus and some Clostridium, some Actinobacteria as Bifidobacterium, and also some Bacteroides. Among all these isolates, some have been recognized with positive effect on health and are used as probiotics, such as Lactobacillus and Bifidobacterium, which are considered GRAS (Generally Recognized As Safe).
But 10 years ago culture-independent molecular tools began to be used, by sequencing of ribosomal RNA genes, and they have revealed many more gut microorganisms, around 1000 species. As shown in Figure 2, taken from the good review of Rajilic-Stojanovic et al (2007), there are clearly two groups that have many more representatives than thought before: Bacteroides and Clostridiales.
Figure 2. Phylogenetic tree based on 16S rRNA gene sequences of various phylotypes found in the human gastrointestinal tract. The proportion of cultured or uncultured phylotypes for each group is represented by the colour from white (cultured) passing through grey to black (uncultured). For each phylogenetic group the number of different phylotypes is indicated (Rajilic-Stojanovic et al 2007)
In more recent studies related to diet such as Walker et al (2011) — a work done with faecal samples from volunteers –, population numbers of the various groups were estimated by quantitative PCR of 16S rRNA gene. The largest groups, with 30% each, were Bacteroides and clostridia. Among Clostridiales were included: Faecalibacterium prausnitzii (11%), Eubacterium rectale (7%) and Ruminococcus (6%). As we see the clostridial group includes many different genera besides the known Clostridium.
In fact, if we consider the population of each species present in the human gastrointestinal tract, the most abundant seems to be a clostridial: F. prausnitzii (Duncan et al 2013).
Benefits of some clostridia
These last years it has been discovered that clostridial genera of Faecalibacterium, Eubacterium, Roseburia and Anaerostipes (Duncan et al 2013) are those which contribute most to the production of short chain fatty acids (SCFA) in the colon. Clostridia ferment dietary carbohydrate that escape digestion producing SCFA, mainly acetate, propionate and butyrate, which are found in the stool (50-100 mM) and are absorbed in the intestine. Acetate is metabolized primarily by the peripheral tissues, propionate is gluconeogenic, and butyrate is the main energy source for the colonic epithelium. The SCFA become in total 10% of the energy obtained by the human host. Some of these clostridia as Eubacterium and Anaerostipes also use as a substrate the lactate produced by other bacteria such as Bifidobacterium and lactic acid bacteria, producing finally also the SCFA (Tiihonen et al 2010).
Clostridia of microbiota protect us against food allergen sensitization
This is the last found positive aspect of clostridia microbiota, that Stefka et al (2014) have shown in a recent excellent work. In administering allergens (“Ara h”) of peanut (Arachis hypogaea) to mice that had been treated with antibiotics or to mice without microbiota (Germ-free, sterile environment bred), these authors observed that there was a systemic allergic hyper reactivity with induction of specific immunoglobulins, id est., a sensitization.
In mice treated with antibiotics they observed a significant reduction in the number of bacterial microbiota (analysing the 16S rRNA gene) in the ileum and faeces, and also biodiversity was altered, so that the predominant Bacteroides and clostridia in normal conditions almost disappeared and instead lactobacilli were increased.
To view the role of these predominant groups in the microbiota, Stefka et al. colonized with Bacteroides and clostridia the gut of mice previously absent of microbiota. These animals are known as gnotobiotic, meaning animals where it is known exactly which types of microorganisms contain.
In this way, Stefka et al. have shown that selective colonization of gnotobiotic mice with clostridia confers protection against peanut allergens, which does not happen with Bacteroides. For colonization with clostridia, the authors used a spore suspension extracted from faecal samples of healthy mice and confirmed that the gene sequences of the extract corresponded to clostridial species.
So in effect, the mice colonized with clostridia had lower levels of allergen in the blood serum (Figure 3), had a lower content of immunoglobulins, there was no caecum inflammation, and body temperature was maintained. The mice treated with antibiotics which had presented the hyper allergic reaction when administered with antigens, also had a lower reaction when they were colonized with clostridia.
Figure 3. Levels of “Ara h” peanut allergen in serum after ingestion of peanuts in mice without microbiota (Germ-free), colonized with Bacteroides (B. uniformis) and colonized with clostridia. From Stefka et al (2014).
In addition, in this work, Stefka et al. have conducted a transcriptomic analysis with microarrays of the intestinal epithelium cells of mice and they have found that the genes producing the cytokine IL-22 are induced in animals colonized with clostridia, and that this cytokine reduces the allergen uptake by the epithelium and thus prevents its entry into the systemic circulation, contributing to the protection against hypersensitivity. All these mechanisms, reviewed by Cao et al (2014), can be seen in the diagram of Figure 4.
In conclusion, this study opens new perspectives to prevent food allergies by modulating the composition of the intestinal microbiota. So, adding these anti-inflammatory qualities to the production of butyrate and other SCFA, and the lactate consumption, we must start thinking about the use of clostridia for candidates as probiotics, in addition to the known Lactobacillus and Bifidobacterium.
Figure 4. Induction of clostridia on cytokine production by epithelial cells of the intestine, as well as the production of short chain fatty acids (SCFA) by clostridia (Cao et al 2014).
Cao S, Feehley TJ, Nagler CR (2014) The role of commensal bacteria in the regulation of sensitization to food allergens. FEBS Lett 588, 4258-4266
Duncan SH, Flint HJ (2013) Probiotics and prebiotics and health in ageing populations. Maturitas 75, 44-50
Rajilic-Stojanovic M, Smidt H, de Vos WM (2007) Diversity of the human gastrointestinal tract microbiota revisited. Environ Microbiol 9, 2125-2136
Rosen M (2014) Gut bacteria may prevent food allergies. Science News 186, 7, 4 oct 2014
Russell SL, et al. (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13(5):440–447
Stefka AT et al (2014) Commensal bacteria protect against food allergen sensitization. Proc Nat Acad Sci 111, 13145-13150
Tiihonen K, Ouwehand AC, Rautonen N (2010) Human intestinal microbiota and healthy aging. Ageing Research Reviews 9:107–16
Walker AW et al (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. The ISME J 5, 220-230
It seems to be so: the microbes in our gastrointestinal tract (GIT) influence our choice of food. No wonder: microbes, primarily bacteria, are present in significant amounts in GIT, more than 10 bacterial cells for each of our cells, a total of 1014 (The human body has about 1013 cells). This amounts to about 1-1.5 kg. And these bacteria have lived with us always, since all mammals have them. So, they have evolved with our ancestors and therefore they are well suited to our internal environment. Being our bodies their habitat, much the better if they can control what reaches the intestine. And how can they do? Then giving orders to the brain to eat such a thing or that other, appropriate for them, the microbes.
Well, gone seriously, there is some previous work in this direction. It seems there is a relationship between preferences for a particular diet and microbial composition of GIT (Norris et al 2013). In fact, it is a two-way interaction, one of the many aspects of symbiotic mutualism between us and our microbiota (Dethlefsen et al 2007).
There is much evidence that diet influences the microbiota. One of the most striking examples is that African children fed almost exclusively in sorghum have more cellulolytic microbes than other children (De Filippo et al 2010).
The brain can also indirectly influence the gut microbiota by changes in intestinal motility, secretion and permeability, or directly releasing specific molecules to the gut digestive lumen from the sub epithelial cells (neurons or from the immune system) (Rhee et al 2009).
The GIT is a complex ecosystem where different species of bacteria and other microorganisms must compete and cooperate among themselves and with the host cells. The food ingested by the host (human or other mammal) is an important factor in the continuous selection of these microbes and the nature of food is often determined by the preferences of the host. Those bacteria that are able to manipulate these preferences will have advantages over those that are not (Norris et al 2013).
Recently Alcock et al (2014) have reviewed the evidences of all this. Microbes can manipulate the feeding behaviour of the host in their own benefit through various possible strategies. We’ll see some examples in relation to the scheme of Figure 2.
Figure 2. As if microbes were puppeteers and we humans were the puppets, microbes can control what we eat by a number of marked mechanisms. Adapted from Alcock et al 2014.
People who have “desires” of chocolate have different microbial metabolites in urine from people indifferent to chocolate, despite having the same diet.
Dysphoria, id est, human discomfort until we eat food which improve microbial “welfare”, may be due to the expression of bacterial virulence genes and perception of pain by the host. This is because the production of toxins is often triggered by a low concentration of nutrients limiting growth. The detection of sugars and other nutrients regulates virulence and growth of various microbes. These directly injure the intestinal epithelium when nutrients are absent. According to this hypothesis, it has been shown that bacterial virulence proteins activate pain receptors. It has been shown that fasting in mice increases the perception of pain by a mechanism of vagal nerve.
Microbes can also alter food preferences of guests changing the expression of taste receptors on the host. In this sense, for instance germ-free mice prefer more sweet food and have a greater number of sweet receptors on the tongue and intestine that mice with a normal microbiota.
The feeding behaviour of the host can also be manipulated by microbes through the nervous system, through the vagus nerve, which connects the 100 million neurons of the enteric nervous system from the gut to the brain via the medulla. Enteric nerves have receptors that react to the presence of certain bacteria and bacterial metabolites such as short chain fatty acids. The vagus nerve regulates eating behaviour and body weight. It has been seen that the activity of the vagus nerve of rats stimulated with norepinephrine causes that they keep eating despite being satiated. This suggests that GIT microbes produce neurotransmitters that can contribute to overeating.
Neurotransmitters produced by microbes are analogue compounds to mammalian hormones related to mood and behaviour. More than 50% of dopamine and most of serotonin in the body have an intestinal origin. Many persistent and transient inhabitants of the gut, including E. coli, several Bacillus, Staphylococcus and Proteus secrete dopamine. In Table 1 we can see the various neurotransmitters produced by GIT microbes. At the same time, it is known that host enzymes such as amine oxidase can degrade neurotransmitters produced by microorganisms, which demonstrates the evolutionary interactions between microbes and hosts.
Table 1. Diversity of neurotransmitters isolated from several microbial species (Roschchina 2010)
|GABA (gamma-amino-butyric acid)||Lactobacillus, Bifidobacterium|
|Norepinephrine||Escherichia, Bacillus, Saccharomyces|
|Serotonin||Candida, Streptococcus, Escherichia, Enterococcus|
Some bacteria induce hosts to provide their favourite nutrients. For example, Bacteroides thetaiotaomicron inhabits the intestinal mucus, where it feeds on oligosaccharides secreted by goblet cells of the intestine, and this bacterium induces its host mammal to increase the secretion of these oligosaccharides. Instead, Faecalibacterium prausnitzii, a not degrading mucus, which is associated with B. thetaiotaomicron, inhibits the mucus production. Therefore, this is an ecosystem with multiple agents that interact with each other and with the host.
As microbiota is easily manipulated by prebiotics, probiotics, antibiotics, faecal transplants, and changes in diet, controlling and altering our microbiota provides a viable method to the otherwise insoluble problems of obesity and poor diet.
Alcock J, Maley CC, Aktipis CA (2014) Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms. BioEssays 36, DOI: 10.1002/bies.201400071
De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107:14691–6
Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811-818
Lyte M (2011) Probiotics function mechanistically as delivery for neuroactive compounds: Microbial endocrinology in teh design and use of probiotics. BioEssays 33:574-581
Norris V, Molina F, Gewirtz AT (2013) Hypothesis: bacteria control host appetites. J Bacteriol 195:411–416
Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain–gut–enteric microbiota axis. Nature Reviews Gastroenterology and Hepatology 6:306-314
Roschchina VV (2010) Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells. In Lyte M, Freestone PPE, eds; Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health. New York: Springer. pp. 17–52
The spotted hyena (Crocuta crocuta), also known as laughing hyena, is the best known and greatest species of hyena, living in Sub-Saharan Africa. Although not considered in immediate danger of extinction, their numbers have been increasingly shrinking, like all other large African mammals and their total number is estimated at about 40,000. Most of them live in national parks of the East Africa, especially in the Serengeti in Tanzania. In the rest of western and southern Africa, populations in many cases are lower than 1000 individuals in each country, and isolated from each other, so in real danger of extinction.
The spotted hyena (Crocuta crocuta). Photo: Tophat21 (animalswikia.com)
It is the carnivorous mammal with more complexity of social behaviour, similar to the cercopithecine primates (baboons and macaques), and because of this, his intelligence is comparable to those primates and in some respects even to the chimpanzees.
They live in communities, clans, of about 40 to 80 individuals and these societies are matriarchal: females, larger than males, are dominant, with even the lowest ranking females being dominant over the highest ranking males. Maybe they could be caught by the radical feminists as a symbol, right?
Social relationships among hyenas may have to do with maintaining the hierarchy, or to find food (hunting or scavenging), or reproduce, or control of the territory against other clans, and are based on communication systems that manifest with multiple sensory modalities, both body language and vocalizations. Of these, a wide range of sounds (about 12 different) have been registered, the best known of which are a howl and a kind of laughing where the nickname comes from. Body language is also quite complex, with different attitudes and positions of the ears, tail, etc., sometimes similar to wolves.
Like primates, spotted hyenas recognize individual conspecifics, are conscious that some clan-mates may be more reliable than others, recognize foreign family groups and rank relationships among clan-mates, and adaptively use this knowledge during social decision making.
Creamy secretion of anal scent glands, and olfactory communication
The title of this blog post refers to a particular form of communication, but very common among these hyenas: a chemical signal, olfactively detectable. It is an odorous marking, with a smelly white creamy secretion, called paste, produced by a pair of anal sebaceous glands. This secretion is composed of lipid-rich sebum and desquamated epithelial cells. The paste is deposited on grass stalks, and produces a powerful soapy odour, which even humans can detect. They do it on several occasions, as when lions are present, or the males do it near the dens, and most often in their territory limits. Often, after the pasting, they scratch the ground with their front legs, which adds even more flavours that come from the secretions of their interdigital glands. Clans mark their territories by either pasting or pawing in special latrines located on clan range boundaries.
In addition, this odorous secretion is also part of usual greetings among members of the clan. So, two of the individuals are placed in parallel and in opposite directions from one another, lifting one leg back and smelling each other anogenital areas .
Spotted hyenas greeting one another. Photo: Tony Camacho, Science Photo Library
The scent of paste secretion
The major volatile constituents of paste are fatty acids, esters, hydrocarbons, alcohols and aldehydes. Collectively, they give paste a pungent, sour mulch odour that persists, detectable by the human nose, for more than a month after paste is deposited on grass stalks.
It has been shown that odour of spotted hyena paste varies based on the individual identity, sex and group membership of the scent donor. Hyenas’ group-specific odours, in particular, are due to underlying variation in the structure of short-chain fatty acid (mainly acetic, propionic and butyric acids) and ester profiles of paste.
These odorants are well-documented products of bacterial fermentation. These scent glands are warm, moist, organic-rich and largely anaerobic, and thus appear highly conducive to the proliferation of fermentative symbiotic bacteria.
Symbiotic bacterial communities that produce social odour of hyenas
The bacteria use protein and lipid of glands as substrates, producing odoriferous metabolites, which are used by their mammal guests as chemical signals. The bacterial communities differ according to the hyena individuals and especially to the clans, according to symbiotic microbial communities are slightly different among clans, they are group-specific. Bacterial communities arise from the contact between the hyenas of the same clan, as they share the same space and common areas where they deposit the paste secretion. Spotted hyenas frequently scent mark the same grass stalks as their clan-mates (i.e. overmarking), and they often do so in rapid succession to one another. Therefore, overmarking appears to be a viable pathway for the transmission of bacterial communities among members of hyena clans. Although average genetic relatedness within hyena clans is low, it is higher within than among clans.
This mechanism to explain the social scent specific for group has also been proposed for some other mammals such as bats (Eptesicus fuscus, Myotis bechsteinii) and badger (Meles meles), but precisely in the spotted hyena it has been well demonstrated recently in an article published by scientists from Michigan (USA) .
These authors have worked with anal scent secretions of female hyenas from Masai Mara reserve in Kenya. They have shown by electron microscopy the presence of bacteria in the paste.
Bacilli- and cocci-shaped bacteria surrounded by the paste secretion, with lipid droplets (asterisk) .
Bacterial DNA was extracted from samples of paste secretion and 16S rRNA genes were amplified and sequenced. Comparing the obtained sequences with data from GenBank ® (public database of genetic sequences, http://www.ncbi.nlm.nih.gov), different bacteria were identified. The genera found were some of the groups of gram-positive Actinobacteria (Corynebacterium and Propionibacterium) and Firmicutes (Anaerococcus and others), and some of the gram-negative group of bacteroides. While the types found were more or less the same in the different clans of hyenas, the proportions of bacterial types were significantly different according to the clan.
Propionibacterium, coloured electron microscopy image: Dennis Kunkel Microscopy, Inc./Visuals Unlimited, Inc. Other species of this bacterial genus producing propionic acid are involved in the production of Emmental cheese types.
So, using the latest molecular techniques, culture independent techniques and sequencing, this work  shows that symbiotic bacteria may be helpful to their animal guests, by increasing diversity of odoriferous signals available, with variability among hyenas’ clans.
Importance of symbiosis
This is a quite peculiar symbiosis of bacteria with mammals. But, as you know, most mammals, including us the humans, live with millions of bacteria inside, many of which are beneficial, like most that inhabit the digestive tract or other body parts, which constitute the so-called “microbiome”. The probiotics we eat with some fermented dairy products contribute to maintaining populations of these symbiotic bacteria.
More and more data on the importance of symbiosis in multiple aspects of living beings is being known, as well as symbiosis is a key factor in evolution. Just remember that the most likely hypothesis for the origin of the first eukaryotic cells (about 2000 million years), is that it was due to a combination of the two types of prokaryotes, bacteria and archaea. Some millions of years later, the two well known endosymbiosis took place in the eukaryotic cell: bacteria carrying aerobic respiration that gave rise to mitochondria, and photosynthetic oxygenogenic cyanobacteria that were the origin of chloroplasts in algae and plants.
Other important evolutionary symbiosis were the establishment of mycorrhizae between fungi and plants, which led to the colonization of land by these, or nitrogen-fixing bacteria (Rhizobium) with legume plants, or a group of organisms, lichens, which are symbiosis of fungi with some algae or cyanobacteria, and live in many very different and hostile environments. And many other cases of symbiosis between distinct species getting benefits because live together.
So, symbiosis is a good lesson from biological evolution: by cooperation, benefits for both participants are always obtained.
 Mills, G., H. Hofer (1998). Hyaenas: status survey and conservation action plan. IUCN/SSC Hyena Specialist Group.
 Theis, K.R., T.M. Schmidt, K.E. Holekamp (2012) Evidence for a bacterial mechanism for group-specific social odors among hyenas. Nature Scientific Reports 2, 615
It is the “pearl of Siberia”, so named for its beauty and nature. As shown on the map below, it is located in the south of central Siberia, in the Russian Federation, quite near of Mongolia and China. Historically, the chinese called it as the North Sea. The Russians do not began to explore the lake until the end of 17th century. Although today most of the population is of russian origin, the south of the lake is inhabited by buryats, of Mongolian origin. They are the largest ethnic minority group in Siberia, with their own language. They are about 400,000 and their principal city is Ulan-Ude.
The famous Trans-Siberian railway passes beside the lake, bordering it by the southwest corner, with stops in the cities of Irkutsk and Ulan-Ude. This section is spectacular, with 200 bridges and 33 tunnels. This area is “only” about 5000 km far from Moscow (3 days) and 4000 km of Vladivostok (3 days) in the Pacific.
As you can see in this map, the lake is shaped like a crescent. It is the largest freshwater lake in the world (31,000 km2, like Catalonia or Belgium) and the deepest (1600 m maximum depth), and the world’s oldest (about 25-30 million years ago). The lake is in a rift, where tectonic plates are separating, and so it widens gradually.
It has an enormous biodiversity, with over 1700 species of plants and animals, 2/3 of which are endemic, and in 1996 UNESCO declared it a World Heritage Site. With minimum temperatures of -20°C most of the winter, lake Baikal is frozen for half the year.
The Baikal seal
The Baikal seal or “nerpa” is Pusa sibirica (formerly classified as Phoca sibirina), which is across all the lake, but nowhere else. The lake is 2400 km far from the Arctic ocean where the lake waters flow through the siberian river Yenissei.
The nerpa is one of the few species of freshwater seals. It is relatively small, measuring just over 1 meter and weighs about 60-70 kg. It eats several species of fish, but especially a so-called “golomyanka”, which is endemic of lake Baikal. This fish is very abundant in the lake, it is translucent, very fat (it is known as “oilfish”) and lives at depths of 200-500 meters. Seals dive down to eat them, they can resist up to 40 minutes underwater.
Well relaxed Baikal seals. Picture from Uryah. http://diertjevandedag.classy.be/zoogdieren/roofdieren/zeehond/baikalrob.htm
Well, and how this seal came to lake Baikal ?
Well, it is not very clear, it is almost a mystery, since the seal lives far from the open seas, where all other species of seals live. But anyway, as for everything, we can look for the more reliable scientific hypothesis. Let’s see what we can found ….
This species is most similar to the Arctic seal or ringed seal, Pusa hispida, which lives in the Arctic. Like this and other of the family of Phocids (such as the common seal, Phoca vitulina), it is earless, unlike other Pinnipedia (sea lions and fur seals). Another species quite similar is the Caspian seal, Pusa caspica, which is also a curious case, because the Caspian is also an isolated sea. But the Caspian is almost a real sea, with a salinity of 1.2% (the third of the others seas and oceans), and therefore the Caspian seal, such as the Arctic, is not a freshwater seal.
However, there are two subspecies of the arctic seal, with few numbers, which are freshwater, like that of Baikal lake: they are the seals of lakes Saimaa (Finland) and Ladoga (Russia, near Finland), which are relatively near of the Arctic ocean. These two subspecies probably came from the Arctic, after the last glaciation, and they remained confined to these lakes. Probably, to change from salt water to freshwater is a relatively easy adaptation for mammals like these.
Another common feature of the Baikal seal and these of the same genus Pusa (the arctic and the Caspian ones), and others, is that their pups have white fur, changing it shortly after to the grey fur typical of adults. This suggests the origin of the common ancestor in a icy place, the arctic or a related environment.
Therefore, the prevailing scientific theory by 1960  was that the origin of Baikal and Caspian seals from the Arctic would have been during one of the glacial periods of the Pleistocene, perhaps around 90,000 years ago, that is relatively recent in terms of evolution. As shown in the map below, during this period, north ice of the arctic covered part of Siberia (red line) and functioned as a barrier to all waters coming from the south, which currently drain to the Arctic ocean (by the rivers Ob and Yenissei, and others). Thus, a large lake was formed, which communicated probably with the Baikal and the Caspian, and all water flowed westward towards the Black Sea, as shown. Geologically, these connections of the Aral and Caspian to the Black Sea seem demonstrated [3, 4]. With this, the seals of the Arctic would have migrated south and led to the Caspian, and the Baikal perhaps.
Map collage of this from Mangerud  (left) with the one of freeworldmaps.net (right). The area in white until the red line was covered by north ice sheet, by 90,000 years ago.
But, as I mentioned, 90,000 years is a very short evolutionary time to explain the differences between these species, although they are closely related.
Therefore, it seems likely a previous common origin, and to prove it, molecular tools have been used the recent years. In this way, specific gene sequences of 12 mitochondrial proteins from different species have been compared. This study has been done including all pinnipeds .
Thus, in developing the corresponding dendrogram, as we see below, it can be observed that the evolutionary separation of the Baikal seal from the Arctic (ringed seal), and the Caspian, and the grey seal, occurred about 5 million years ago, at the beginning of the Pliocene. Therefore, these species of seals must have a common geographical origin, relating to these arctic lakes or internal seas. Molecular similarities have been also found between arctic amphipods (small crustaceans) and those of the Caspian Sea.
Furthermore, at the period when this seal speciation took place, and from the Oligocene (20 million years) to the Pliocene, the sea Paratethys (see diagram below) was extending from central Europe to this part Asia, over the Alps, Carpathians and other mountain ranges separating Paratethys from the Tethys sea. In fact, the current Black, Caspian and Aral seas, and other lakes in central Asia, are relics of what was the Paratethys. This great sea had connections with the Arctic during different periods.
Diagram from Woudloper: http://commons.wikimedia.org/wiki/User:Woudloper
Therefore, it is likely that the Caspian seal was originated from the Arctic ones or backwards, through these geographical connections of the Paratethys until the Pliocene. However, for our protagonist, the Baikal seal, there is not enough evidence to say that the Baikal was connected to the other seas of Paratethys because it is quite to the east. So, either Pusa sibirica came across this alleged connection with Paratethys, or maybe there was a separate settlement from the Arctic across the river Yenissei, also at this period. Nothing is discarded. Therefore, the Baikal seal will keep some mystery ……
 Arnason U. et al (2006) Pinniped phylogeny and a new hypothesis for their origin and dispersal. Molecular Phylogenetics and Evolution 41, 345-354
 McLaren I.A. (1960) On the origin of the Caspian and Baikal seals and the paleoclimatological implication. American Journal of Science 258, 47-64
 Mangerud J. et al. (2004) Ice-dammed lakes and rerouting of the drainage of northern Eurasia during the Last Glaciation. Quaternary Science Reviews 23, 1313-1332
 Mangerud J. et al. (2001) Huge ice-age lakes in Russia. Journal of Quaternary Science 16, 773-777
 ……. and Wikipedia, of course !!