Latrine behaviour as a multimodal communicatory signal station in wild lemurs: the case of Hapalemur meridionalis

1. What they did

Many mammals, from carnivores to antelopes and rodents, use latrines: the same spots, used again and again for dung and urine. This is rare in primates, but some lemurs do it. The authors made the first systematic study of latrine use by a group-living lemur, the southern bamboo lemur, in the littoral forest of Mandena in southeast Madagascar.

They tested four ideas about what latrines are for:

• Hiding: concealing dung from predators, or protecting it from sun and rain.
• Territorial defence: if so, latrines should be placed more towards the edges of the home range than in the core.
• Advertising that females are ready to mate: if so, females should use latrines and scent mark more in the mating season (June and July).
• Mate guarding: if so, males should mark over females’ scent marks during the mating season.

Ten adults in four neighbouring groups were darted and fitted with radio collars, which made these shy, hard-to-find lemurs easier to locate. Through 2013 the team followed three groups from sunrise to sunset, about 5 days a month each. They flagged and mapped every latrine visited, noted who used it, whether old dung was already there, and the tree or structure it was under. From June to December they also recorded scent marking at latrines, and they noted all fights between groups. Latrine trees were compared with trees in 20 botanical plots.

2. What they found

General latrine use

• In 1762 hours of observation, the lemurs used latrines 429 times at 282 sites. Old dung was already present at 92.55% of uses.
• Females started latrine use 52.45% of the time, males 25.87% and juveniles 21.68%.
• Most visits (73.43%) involved more than one animal. About 30% of sites were used more than once, and these accounted for 53.85% of defecations.
• The lemurs defecated on average 0.41 m above the ground, nearly always within 1 m; 6.10% of the time they came right down to the ground.

Where latrines were

• 86.62% of latrines were at visually conspicuous places: the stilt roots of Uapaca trees, large liana tangles on the ground, and fallen trees. The lemurs clearly favoured these over ordinary-looking spots.
• Uapaca trees used as latrines were larger (trunk diameter, height and crown volume) than Uapaca trees in the plots, and Uapaca made up only 1.51% of trees in the plots.
• Home ranges were 6.60 to 18.39 hectares, with very little overlap between groups. Every overlap zone held latrines, and some latrines were used by two groups.
• Latrines were denser in the core areas (8.54 per hectare) than elsewhere in the home range (3.98 per hectare).
• Only 13 fights between groups were seen in the whole year.

Returning to the same latrines

Both males and females were more likely to return to latrines in the core of the home range. Males also returned more often to nondescript sites. Season made no difference.

Scent marking

• Males scrape the bark (for example, a Uapaca stilt root) with their lower front teeth, rub their forearm glands against their upper arm glands, then smear the scrape. Females rub their anogenital area along the wood, rarely adding urine.
• Scent marking happened at 71.53% of 281 latrine uses from June to December. More adults marked in the nonmating season, and marking was driven mostly by males.
• Males marked over females’ scent marks at 40.79% of female-marked sites. Females were never seen marking over males. Overmarking was more common outside the mating season (about 0.39 versus 0.15 per visit).

3. What they concluded

• Hiding: most latrines were under low horizontal structures, which might hide dung from predators, or protect the scent from sun and rain. The study cannot tell these apart.
• Territorial defence: not supported, because latrines were concentrated in the core of the home range rather than at the edges.
• Advertising mating condition: not supported. Females scent marked at steady rates from June to December.
• Mate guarding: plausibly supported. Males covered females’ marks mainly outside the mating season, but this is when animals were seen dispersing between groups (September to December). Overmarking may hide the females’ presence from newcomer males.
• A multimodal signal post: latrines combine smell (dung, urine and gland secretions) with sight (the distinctive structure, the scrapes on the wood and the piles of dung). Because these lemurs are active by day and by night, using both senses would be efficient. This low-cost signal fits the energy frugality hypothesis, which suggests lemur societies evolved low aggression because Madagascar’s forests are poor in resources. It may help explain why the groups kept separate ranges with so little fighting.
• The authors caution that scent marking also happens away from latrines, which they did not record, so the results should be treated with care.

4. How tracking was or was not used

No trailing was reported; the lemurs were located with radio telemetry and followed directly. Signs were used in two ways. Accumulated dung at latrines (from two to more than 50 droppings) was identified as bamboo lemur dung by its typically green colour and fibrous content, from a diet of grasses and lianas; the only similar-sized lemur in the forest does not use latrines, and similar-sized carnivores are very rare there. The paper also describes the scrapes and notches males make with their teeth on bark before scent marking, as a visual part of the signal.

5. Tracker or observer certification

Not reported. The lemurs were captured by “an experienced Malagasy technician”, and the tree measurements at latrines were made by the first author. Nothing is said about who identified the accumulated dung.

6. Other technologies, skills or innovations

• External radio transmitters with data-logging ability (ARC400, Advanced Telemetry Systems) on neoprene collars, plus colour-coded pendants to tell individuals apart.
• A handheld Garmin GPSMAP 62S recording the group’s position every 15 minutes, analysed in ArcGIS with kernel density estimates.
• Flagging and coding of every latrine site.

7. Implications for conservation (from the paper)

• Southern bamboo lemurs also used conspicuous Uapaca trees as latrines at Ampasy, about 50 km away, so this habit may be widespread across the species’ range.
• Because bamboo lemurs are cryptic, searching these conspicuous sites for accumulated dung could give conservationists a nontraditional way to detect the species.
• Lemur dung may fertilise the Uapaca trees, and the lemurs eat Uapaca fruit and swallow the seeds, which hints at a possible mutual relationship between lemur and tree.