Perspectives on over-marking: is it good to be on top?

1. What they did

Imagine a small mammal, such as a rodent, moving through its home range. It is surrounded by scent marks, some its own and some left by others of its kind. Some of these marks are placed well apart, but others are placed on top of, touching, or right next to an earlier mark. The authors call this over-marking, and they note that it seems to happen in almost all land mammals, especially those that share paths, trails and runways.

In this review the authors bring together what was known about:

• How common over-marking is. Reports cover rodents, insectivores, ungulates, carnivores and primates.
• Why animals over-mark. From the literature they set out ten hypotheses, which are not mutually exclusive.
• How animals respond to an over-mark. Can they tell the top mark from the bottom one, and which do they pay more attention to? This work comes almost entirely from laboratory studies on golden hamsters and voles.
• The costs and benefits for the animal whose mark ends up on top.

2. What they found

Ten hypotheses on why animals over-mark

• Competition (counter-marking). The over-marker gains an advantage, for example by masking the other mark, showing social rank, or making a threat. Support comes from many species, including voles, hamsters, house mice, gerbils, tamarins, lemurs, wolves, honey badgers and African antelopes.
• Bulletin board. Animals leave marks along shared paths or on features such as rocks, trees or mounds to show they are present; top and bottom marks are treated much the same. Some support from prairie voles, tamarins and marmosets.
• Territory. Like competition, but applied to one’s own territory: residents over-mark intruders’ marks, inside the territory or along its borders. Support from hyenas, Eurasian beavers, Ethiopian wolves, rabbits, Alpine marmots, aardwolves and klipspringers.
• Mate attraction. Animals over-mark the marks of the opposite sex more than those of their own sex, especially of sexually receptive animals, before mating. Some support from zebras, hyenas, wolves, meadow voles, lemurs, tamarins and mice.
• Mate guarding. After mating, over-marking a partner’s mark may tell others that the two are associated. Support from hyenas, prairie voles, wolves, klipspringers, antelope, tamarins and lemurs.
• Navigation. Over-marking may help animals find their way in unfamiliar areas and back to familiar ones. Not tested directly.
• Foraging efficiency. Over-marking may build a scent path to food, perhaps like trail marking in ants. Indirect support from honey badgers and otters.
• Group scent. In group-living mammals, mixed marks may make a shared group scent. Indirect support from marmosets and Ethiopian wolves.
• No function. Some species rarely over-mark, and some researchers argue it is an artifact of captivity and small test areas. The authors reply that little evidence shows it has no function, and that animals reported not to over-mark do so under other test conditions.
• Multiple functions. Over-marking may serve different purposes depending on who is on top, who is underneath, and who is investigating, and may change with season, breeding condition, social status and age.

How animals respond to an over-mark

• After investigating an over-mark, golden hamsters and voles later responded more to the top-scent donor than to the bottom-scent donor. They behaved as if they had a better memory for, and preference for, the top mark.
• Meadow voles still preferred the top mark when it overlapped only about 5% of the bottom mark. In meadow voles the two marks had to overlap for this effect; in golden hamsters they did not.
• With mixed-sex over-marks, meadow voles were drawn to the opposite-sex mark even when it was underneath, while prairie voles preferred the opposite-sex donor only when it was on top. The authors suggest the “modified bulletin board” idea (both marks stay distinct, but the investigator values each one for itself) best fits meadow voles, and the competition idea best fits prairie voles.
• Male meadow voles preferred the mark of a female with higher estradiol, whatever its position. Female meadow voles preferred a male who was both on top and had higher testosterone.
• Voles can tell which donor was on top more often than underneath across many over-marks (relative numerosity).

Is it good to be on top?

• The animal on top is likely the most recent visitor, so its mark may carry more weight with those investigating it.
• Over-marking other males’ marks is generally done by dominant males in rodents, ungulates and primates, and female mice respond selectively to males that over-mark other males.
• Prairie voles, which can be socially monogamous and share a nest and territory, remember the top-scent donor for less than 12 hours, and residents over-mark most of a same-sex intruder’s marks. Meadow voles are promiscuous and do not pair bond.
• Whether over-marking improves fitness is untested. Female golden hamsters mated more often with males that left more scent marks, but two studies found that female prairie voles did not favour top-scent males. The authors give four reasons to treat those prairie vole results with caution, including that reproductive success was not measured and that tethering males may have affected their behaviour.

3. What they concluded

• Several of the ten hypotheses are plausible, but most of the literature fits the view that over-marking plays a role in scent communication between animals of the same sex and of the opposite sex.
• Over-marking is likely a specialized form of scent communication, not an artifact of experiments or two animals happening to mark the same spot.
• Animals may pay selective attention to, and selectively remember, the top mark. If scent marks are “read” selectively, ideas about scent communication need to include selective detection and perception.
• For over-marking to be worthwhile, the benefits to the top-scent donor must outweigh the costs of announcing its presence. Animals should therefore check areas holding their own marks and keep at least some of their marks on top.
• Open questions: whether species differences are linked to social and mating systems, how life history, ecology and habitat affect over-marking, and whether over-marking affects reproductive success.

6. Other technologies, skills or innovations

• The paper reviews laboratory scent-preference tests in which animals investigate an over-mark and then, in a test phase, are offered the top and bottom donors’ marks separately, with time spent investigating each one as the measure.