Food-plant preferences in the Arctic: a report from the lemming cafeteria
Interactions between herbivores and their food-plants play a very important role in shaping ecosystems. This may be especially true for low productive areas, where ecosystems are usually less complex and characterized by a relatively low diversity of both plants and herbivores. A typical example of such an ecosystem is the Arctic tundra. Here plant communities are almost two-dimensional, and in general dominated by a few species, e.g. willows (Salix spp) and mountain avens (Dryas spp) in dry areas, and sedges (Carex spp) and cotton grass (Eriophorum spp) in mesic habitats. The herbivore community primarily consists of musk-oxen, caribou, geese, hares and lemmings (and of course insects). Lemmings in particular have been interesting ecologists a great deal for a long time. This is because they show great fluctuations in numbers, with peak numbers every 3-5 years, and also because they play a central role in the trophic dynamics of the Arctic ecosystem. Lemmings may determine predator numbers because they are the most important prey for many species, and they are also likely to have a pronounced impact on the plant community. In particular, lemmings may have a strong impact on the interactions between plant species or between individuals within plant species if they feed selectively on certain plant species, on certain individuals, or on certain parts of individuals. For example, less preferred plant species may gain a competitive advantage over more preferred ones, or less preferred individuals may increase in frequency compared to more preferred ones. In addition, certain parts/shoots of the plant may be preferred within individuals, which could affect plant reproduction. Although these questions are often raised by animal as well as plant ecologists, lemming food preferences are still poorly understood. The aim of this project was to examine lemming preferences for some of their more important food plants. Here we present some of the specific questions investigated.
A. Do lemmings distinguish between coexisting species of willows?
This was a comparison between species in order to determine if lemming food preferences have the potential to alter the competitive balance between similar plant species.
B. Do lemmings prefer some individuals over others with in a willow species?
Here we examined food preference for males versus females within the most common and widespread Arctic willow species, Salix Arctica. This was of particular interest because the sex ratio is generally skewed towards females in many willow species, and herbivores feeding selectively on male willows could be one explanation for this pattern.
C. Do lemmings feed selectively on certain sedge shoots?
Sedges have clonal growth as well as sexual reproduction and each individual plant has three different shoot types (flowering, old non-flowering, and young non-flowering). If lemmings prefer to feed on e.g. flowering shoots within an individual, this would promote clonal growth, whereas if the plant individual is more likely to lose its nonflowering shoots it should invest more in flowers (i.e. sexual reproduction). We examined these aspects in one of the dominant Arctic sedges, Carex bigelowii.
Methods
There are two species of lemmings in Arctic Canada: the collared lemming (Dierostonyx groenlandicus), which is present in most of the Arctic, and the brown lemming (Lemmus trimucronatus), which is found in the southern and western parts. The collared lemming is believed to feed primarily on willows and herbs (diocotyledons), whereas the brown lemming should feed mainly on sedges and grasses (monocotyledons). During the ship-bound Tundra Northwest 1999 expedition we trapped for lemmings at 17 different sites on the mainland and in the archipelago of the Canadian Arctic. We primarily used Sherman live-traps placed selectively around seemingly active burrow-systems, but, to boost numbers, employed whatever methods necessary, e.g. catching by hand and digging up burrows with spades or spoons. Although lemming densities were in general low, in all we caught 18 collared lemmings (at eight different sites) and 8 brown lemmings (all at one site) which were included in the food preference tests. After capture, the animals were housed and fed in large aluminium boxes in the field until being transported by helicopter to the laboratory on board the ship. In the laboratory, animals were placed in individual cages with free access to apple, mouse-chew and water. Each individual was allowed a minimum of 48 hours before testing, in order to adjust to laboratory conditions. Plants used in the food preference trials were dug up with roots and soil and brought to the ship on plastic trays, on which they were kept and watered until the onset of the trial (usually within 24 hours).
Food preference tests were performed as ”cafeteria”-trials, a classic way of examining food preferences. When tested, the animal was moved to a clean cage and presented with a choice between two or more different food types. It was then allowed to move around and feed freely for 30 minutes, during which we recorded the number of seconds it spent feeding on each food type. In tests with willows, each collared lemming was given the choice between two different plant individuals (of different species or sex) rooted in soil, which were placed one in each far corner of the cage. We focused on Salix Arctica and examined the preference for this dominant willow species in relation to two other willows, Salix polaris and Salix reticulata. To check for differences between sexes only female plants were used in these trials. Using the same method we also specifically examined potential differences in lemming preference for male and female Salix Arctica. In tests with sedges we examined brown lemming preferences for three shoot types (flowering, old, and young) growing on the same block of soil (approximately 3 dm3). Prior to the onset of the trial we removed all vegetation from the block of soil, except for 2-3 sedge-shoots of each type (here by ensuring that similar amounts were available of each shoot-type).
Results and discussion
Collared lemmings showed a pronounced preference for both Salix polaris and Salix reticulata over Salix Arctica. Lemmings obviously feed selectively among co-existing willows, and our results suggest that lemming herbivory can benefit Salix Arctica in competition with other willow species. Whether this is one explanation for the relatively dominant role of Salix Arctica in the Arctic ecosystems is hard to know, but at least during times of high lemming density (peak years) the impact on the plant community is likely to be substantial. Plants with a chemical composition and/or morphology less preferred by herbivores (e.g. Salix Arctica in this case) should during such times sustain less damage, and consequently gain a competitive advantage over more preferred species.
Regarding lemming preferences for individuals within a willow species, it was obvious that males were much preferred to females. Although this pattern was surprisingly pronounced, a general bias towards more herbivore feeding on males could be expected. The suggested rationale for this is that female willows produce more herbivore deterring compounds than do males in order to defend their reproductive investment. The sex ratio among willows is generally female biased (i.e. more females than males are found), and although selective feeding by lemmings may not be the only explanation for this pattern, it may well contribute to the female dominance in these species.
Willows are well-known for their chemical substances which in part function to deter herbivores (e.g. several phenolic compounds), and it will be extremely interesting to compare our findings on lemming food preferences with a thorough chemical analysis of these willow species (to be performed in ca-operation with the specific Salix-project).
A preliminary study has indicated that young sedge shoots have comparatively high concentrations of substances that inhibit the uptake of protein by herbivores. We therefore expected brown lemmings to avoid young shoots, and to feed primarily on flowering and old ones. Our food preference trials revealed that lemmings fed primarily on flowering shoots when given sedges in earlier phenological stages, but that this pattern gradually disappeared later during the growing season. Young shoots were, however, in general avoided except during the last phenological stage. It is possible that chemical compounds which deter herbivores have a more pronounced role in the beginning of the growing season, but that ”defence-investment” gradually decreases, and other aspects, e.g. fibre content, become more important for the herbivores. Detailed data on the temporal variation of proteinase inhibiting substances as well as other potentially important compounds in this sedge will consequently be of great interest (to be performed by the specific Carex-project). The fact that lemmings primarily seem to prefer flowering shoots has some interesting implications for the reproduction of sedges. During high lemming density, flowering shoots should suffer more damage than vegetative ones, and sexual reproduction (flowering) should become less important. In years when lemmings are few, on the other hand, sexual reproduction in sedges should be promoted.
To conclude, lemmings are very selective feeders, and show pronounced preferences for certain plant species, certain individual plants within species, and certain plant parts within individuals. This behavioural interaction between lemmings and their food-plants has therefore the potential to influence both species’ composition and reproduction in Arctic plant communities.
Dates
June–September 1999
Participants
Principal investigator
Jep Agrell
Department of Animal Ecology, Lund University
Sweden
Principal investigator
Dominique Berteaux
Department of Natural Resources and Sciences, McGill University
Sainte-Anne-de-Bellevue, Canada