Scent-Marking by Male Mammals: Cheat-Proof Signals to Competitors and Mates

1. What they did

Scent marks are an odd way to send a message. They are left on objects in the environment, often when no one is there to receive them, and may be found much later, when the animal that left them has gone. Yet most male mammals scent-mark, and most, perhaps all, territories defended for their resources are scent-marked.

The authors reviewed the field and laboratory evidence for one explanation: that scent marks let rivals judge the strength of the animal that left them. They asked:

• How do signalers make sure their marks are found? How long marks last, how far away they can be smelled, and where animals place them.
• How do receivers use marks to judge the signaler? With or without meeting the signaler.
• What do marks cost and what do they gain? Including whether marks are honest signals.
• Who else reads the marks? Rivals, females, predators and parasites (“eavesdropping”).
• How do females use male scent marks to choose mates?

They added their own theoretical models and some unpublished laboratory results on mice.

2. What they found

Scent-marking and competition between males

• Males often scent-mark during contests, such as the “stink fights” of sifakas and the boundary meetings of wildebeest, where males take turns marking and trying to remove each other’s marks.
• Territory owners and dominant males generally mark more than other males. Marks are denser where the threat of intrusion is greatest.
• Male hartebeest trying to take over a territory mark the owner’s dung piles rather than confronting the owner. The owner follows, paws the new marks away and replaces them before chasing the intruder. Marking seems to come before aggression.

How long marks last and how far they reach

• Studies suggest marks stay active for 48 to 72 hours in mouse urine, about 7 days in klipspringer, 10 days in dwarf mongooses and 100 days in hamsters. Odour from hyena anal gland marks can be detected even by humans after 1 to 6 months.
• Brown hyenas leave two pastes each time they mark. A longer-lasting part may carry the identity of the marker, and a shorter-lived part may tell receivers how old the mark is, and so how recently the owner passed.
• Large molecules make marks last longer but limit how far they can be smelled. One study estimated a detection distance of about 2 to 5 m in black-tailed deer. In larger mammals, detection distances are probably measured in meters, not tens of meters.

Where marks are placed

• Marks are usually clustered either along the territory boundary or towards the centre. Dung middens are often on the boundary.
• In hyenas, small territories are marked along the edge, and very large territories towards the centre. One model found that a ring of marks at about 0.8 of the territory radius best limits intrusions.
• Marks are often placed along trails and paths, in boundary areas frequented by rivals, next to more threatening neighbours, and around burrows. Some animals go on boundary patrols to mark, especially after a recent intrusion.
• Marks are often made easy to find: klipspringers mark dead twigs on slightly raised ground above a break in slope, and some animals mark as high as possible. Many add visual signs: pawing, scraping, antler thrashing, or tearing bark off trees.
• Receivers seek out marks. Black-tailed deer search for marks after entering a new area, and ring-tailed lemurs investigated 62% of new marks within 10 minutes.

How receivers judge signalers

The authors describe three ways:

• The mark itself. Marks of dominant male mice put off other males more than those of subordinates or castrated males, because of hormone-dependent chemicals. Small male mice avoid marked areas more than large ones.
• Memory of past fights. Many species can tell individuals apart by smell and remember them for days to weeks; genets remembered males’ marks for 9 to 12 weeks.
• Scent-matching. A receiver remembers the smell of the marks in an area and compares it with any male it meets. If they match, the male is the owner. Territory owners often rub marking substances onto their own bodies and let rivals sniff them; hartebeest lie in their own dung. Intruding mice fought less hard when the ground smelled of the resident male.

House mice use all three. A game theory model suggested intruders usually do best by scent-matching. Owners do best by letting themselves be assessed when marks are likely to be found (usually in small territories), and by attacking straight away when they are not.

Costs and benefits

• A pattern of marks cannot be faked: the owner has to hold the area, or its rank, for as long as it takes to mark it. Owners quickly overmark marks left by intruders.
• In mice, males that marked more grew more slowly. Small dominant males marked more, had larger scent glands and lost their dominance more often.
• Fallow deer stags that marked at high rates were involved in fewer fights. A model of wolves suggests territories cannot form without scent-marking.

Eavesdropping

• Kestrels can see vole scent marks in ultraviolet light and hunt over areas with many marks; rough-legged buzzards do too, but Tengmalm’s owls did not.
• Male mice that mark a lot approached a stranger’s marks faster, but investigated them for less time, when ferret urine was present.
• White-tailed deer are densest in the buffer zones between wolf territories, which are outlined by wolf scent marks; whether the deer read the marks is unknown.
• Ticks gather on klipspringer marks on branch tips, waiting for the antelope to return.

Mate choice

• Female white-tailed deer visit and mark at male marking sites when in heat.
• Female rabbits, hamsters and mice prefer males whose smell matches the marks they found, and female mice prefer males that countermark intruders’ scent.
• Female mice prefer the urine of dominant and healthy males, and choose mates partly by MHC odours that reveal how closely related they are.

3. What they concluded

• Much evidence supports the idea that male scent marks let rivals judge the strength of the marker. Few studies were designed to test this, and more experiments are needed in the laboratory and the field.
• Scent marks may be cheat-proof signals of status, because males must defend their territory or rank for as long as it takes to mark it. Marks also appear costly, in energy and in attracting predators.
• Because most intruders are weaker than territory owners and leave after reading the marks, scent-marking may greatly lower the cost of defending a territory. Resource-defence mating systems in mammals may not be workable without it.
• Animals are unlikely to rely on only one way of reading marks. Which one they use probably depends on the costs and benefits at the time.
• Females do use information in scent marks to choose mates, but it is not known whether males signal to females directly or females eavesdrop on signals meant for rivals. Data on how females respond to male scent marks in the wild are strikingly lacking.

6. Other technologies, skills or innovations

• A simple cost and benefit rule for when a receiver should leave a marked area, weighing the chance of meeting the owner, the cost of a fight, the strength of each animal and the value of the area to each.
• A game theory model of owners and intruders, showing when intruders should fight, withdraw or scent-match.