Hyenas communicate by scent through symbiotic bacteria

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 [1].

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) [2].

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) [2].

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 [2] 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.

References

[1] Mills, G., H. Hofer (1998). Hyaenas: status survey and conservation action plan. IUCN/SSC Hyena Specialist Group.

[2] 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

Theis et al. (2013) Symbiotic bacteria appear to mediate hyena social odors, Proc. Natl. Acad. Sci., 110, 19.832-19.837

http://en.wikipedia.org/wiki/Spotted_hyena