Are trampling effects by wild tundra reindeer understudied ?

Grazing and trampling by the wide-ranging wild tundra reindeer may have major top down landscape effects by causing vegetation changes. Grazing, as the collective effect of eating, trampling, defecation, and urination, has been studied extensively. In contrast, trampling effects per se are rarely studied, and almost never quantified, even though considered very important. The main reason appears to be methodological; effects of trampling imprints are difficult to measure and quantify systematically. In particular, in winter reindeer may largely subsist on slow-growing ground lichens. They grow in habitats with little snow cover and extensive soil frost, and dry lichen may be particularly susceptible to trampling, generating a likely substantial forage loss.


Introduction
Grazing and trampling by large herbivores like northern reindeer (Rangifer tarandus L.) can have extensive top down landscape effects on tundra and alpine vegetation through generating vegetation changes (e.g.Suominen & Olofsson, 2000;Austrheim & Eriksson, 2001;Cairns & Moen, 2004;Wehn et al., 2011;Holtmeier, 2015).Thus, herbivores can be ecosystem keystone species (e.g.Naiman & Rogers, 1997;Suominen & Olofsson, 2000;Eby et al., 2014).This type of ecological changes are often referred to as generated by a single process, 'grazing' or 'browsing' (e.g.Olff et al., 1999;Albon et al., 2007;Tremblay et al., 2007;Mysterud & Austrheim, 2008).However, this is meant to collectively cover the two concomitants but different processes of eating and trampling of vegetation (e.g.Pellerin et al., 2006).The directed and selective eating of plants, including effects of defecation and urination, and to some extent also spill (material not eaten, but spilled) on soil, has been studied extensively in herbivores, with several different and well developed methods both in the field and the laboratory (e.g.Stewart, 1967;Holechek et al., 1982;Dove & Mayes, 1991), and including reindeer (Skogland, 1984;Sormo et al., 1999;Stark et al., 2000;Stark et al., 2007;Finstad & Kielland, 2011;Ophof et al., 2013;Zielinska et al., 2016).However, the necessarily associated but undirected trampling of vegetation may be as important in generating vegetation changes, but is an additional eco-logical mechanism that likely depends on different ecological factors, e.g.reindeer hoofs and movement behaviours and ambient climatic conditions like air humidity.For example, in 1911 the Norwegian High Mountain Grazing Commission (Hardangervidda) (Hirsch et al., 1911) stated.'In summer, the reindeer herders are afraid of letting the herds onto areas where there is lush winter forage, that is where the ground is covered by lichen.In summer when the lichens are dry and brittle, it is devastating when a herd tramples back and forth over it'.Although perceived to be of such major importance, it appears to us that one hundred years later trampling remains a challenge to study and quantify, and is still understudied.Open alpine grazing systems is a particularly good model for studying trampling effects, because chionofobic oligotrophic vegetation, like lichen, may be exposed to trampling year round (e. g.Skogland, 1984).More forested grazing systems, e.g.northern pine Pinus sylvestris and birch Betula pubescens forests, may also be used as reindeer pasture in summer or year-round, but is often more snow-covered in winter, and therefore more susceptible to trampling during the summer season (e. g.Kumpula et al., 2011;Pekkarinen et al., 2015).

Methodological challenges in the study of trampling
Thus, in a recent review of low-intensity grazing, Rosenthal et al. (2012) concluded that the impact of trampling even by domestic herbivores on plant species composition and richness, is underestimated.The direct and easily observable mechanical disruption of vegetation cover and soil, including soil compaction, infiltration of water, and nutrient cycling, have to some extent been studied and quantified in some herbivores (Stark et al., 2000;Pellerin et al., 2006;Schrama et al., 2013;Xu et al., 2013;Ludvikova et al., 2014) (but for different results see Plumptre, 1994;Cumming & Cumming, 2003;Van Uytvanck & Hoffmann, 2009).However, the more subtle preceding effects on the vegetation appear to be rather understudied.This is likely due to methodological difficulties: how can we quantify trampling effects on not eaten (not removed), but still trampled vegetation?Although trampling is frequently referred to as important in studies of interactive herbivore-vegetation effects, it is still stated in a non-quantitative and often rather anecdotal way (Persson et al., 2000;Austrheim et al., 2008;Suominen et al., 2008), including for the northern reindeer living in fragile and vulnerable cold high-latitude alpine and Arctic ecosystems (Skogland, 1983;Skogland, 1984;Körner, 2003).During the critical winter, reindeer may eat substantial amounts of lichen (Skogland, 1984;Kumpula, 2001;Storeheier et al., 2002;Vistnes & Nellemann, 2008;Hansen et al., 2010) which may be the most important and easily available forage.Slow-growing ground lichens are weak competitors, mainly found on sites where the environmental conditions are challenging to most vascular plants.Alpine lichen heaths are dominated by chionofobic species growing mainly on exposed, nutrient poor habitats where wind blows the snow away, resulting in extensive frost (Dahl, 1956;Odland & Munkejord, 2008).Dry, brittle lichen in exposed habitats will likely be subject to trampling, and, importantly, maintain hoof footprints.Combined with their ecological significance, lichen may present a model more suitable for quantitative trampling studies than the more pliable, and therefore resilient, vascular plants.Total lichen cover and biomass vary greatly, from a total dry biomass of 2 kg m -2 in undisturbed Pine forests and 1.2 kg m -2 in undisturbed exposed alpine heaths (e.g.Kumpula, 2001), to less than 0.1 kg m -2 in heavily grazed, and necessarily also trampled alpine heaths (Odland et al., 2014).Desiccated and brittle lichen will be particularly susceptible to trampling (Holtmeier et al., 2003;Kumpula et al., 2011).New high-resolution 3D laser technology may prove helpful to quantify lichen loss in experimental studies (Heggenes et al., 2017).
Reindeer, with their large body, graze extensively, live in herds, are nearly always on the move, with some of the longest ungulate migrations known, are known to take a toll on the typically low production and patchy distribution of high quality vegetation resources in the Alpine and Arctic landscapes.Thus, vegetation eating and trampling are major ecological processes affecting these fragile ecosystems.But how well studied is reindeer trampling per se?

Qualitative and understudied reindeer trampling relative to eating of vegetation
During the long northern winters, reindeer often depend on lichen forage (Skogland, 1989;Ferguson et al., 2001;Vikhamar-Schuler et al., 2013).As for other ungulate-grazing ecosystems, it is common knowledge that the two main factors plant eating and trampling dictate the quantity and quality of the vegetation grazing resource (Gaare & Skogland, 1975;Gaare & Skogland, 1980;Koster et al., 2013;Holtmeier, 2015).Unfortunately, also for reindeer this is conveniently often seen as a single process (e.g.den Herder et al., 2003;Boudreau & Payette, 2004;Kumpula et al., 2014), likely because they are difficult to separate (Olofsson et al., 2001).In reported studies, the negative effects of trampling on fruticose lichens may qualitatively be stated as substantial and important (Pegau, 1970;Suominen & Olofsson, 2000;Cooper & Wookey, 2001;Moen & Danell, 2003;Cairns & Moen, 2004;Olofsson et al., 2004;Cooper, 2006;Moen & Lagerstrom, 2008;Kitti et al., 2009;Olofsson, 2009;Kumpula et al., 2011;Koster et al., 2013).Trampling has even recently been speculated to be more important than grazing (Vistnes & Nellemann, 2008;Kumpula et al., 2011), and especially for lichen winter forage.The effects of trampling on lichen have been suggested to depend on abiotic and biotic ecological factors (Sorensen et al., 2009), in particular humidity (Cooper et al., 2001;Moen et al., 2009;Kumpula et al., 2011) and species (Bayfield et al., 1981;Sorensen et al., 2009).However, few studies try to estimate such trampling effects per se.Thus, for example Vistnes & Nellemann (2008) in a recent study on reindeer winter grazing suggest an estimated "spillage" factor of 10 ('times consumption'), not based on presenting any original data, but with reference to a study by Gaare & Skogland (1975)."Spillage" is not specified, but likely includes trampling as a major factor, but also additional waste that may be associated with plant eating, e.g.selective feeding and dislodged vegetation, and spill during winter crater digging and feeding.During the summer season, trampling will by far be more important, whereas in winter, when snow cover partly protects ground lichen, trampling will be less, and spill may be relatively more important.If a spillage factor of 10 was the case, i.e. trampling is even more important than plant eating (Kumpula et al., 2011), would not the ecological effects of how reindeer behave and move (causing spill and trampling), and vegetation sensitivity to trampling, be far more important than how and how much reindeer eat?If so, the widespread focus on grazing as a collective effect of reindeer on vegetation in relevant literature (e.g.Moen & Danell, 2003;Olofsson, 2006;Olofsson et al., 2010;Kumpula et al., 2014) may benefit from a separation and better understanding of the effects of different activities by reindeer.A conceptual model of vegetation loss due to plant eating and trampling versus reindeer density (Fig. 1) is necessarily speculative and bold, because data are so few or lacking.However, we suggest a linear relationship when forage is abundant and reindeer forage at maximum level, but with decreasing removal of vegetation per head as higher reindeer density increases food compe-tition.Trampling effects may be relatively low for more pliable, i.e. resilient vascular plants.This relationship is likely more linear in particular in dry, brittle lichen, but will decrease when increased reindeer density results in more repeat footprints.Loss will increase sharply when vegetation cover approaches mechanical disruption (Fig. 1) with additional loads of water and soil erosion.Once the vegetation cover disrupts, vegetation loss will obviously drop sharply (not included in the figure).

Understudied and overrated reindeer trampling: gossip snowballing?
The food requirements and diet of reindeer are extensively studied and research methods well established (e.g.Gaare & Skogland, 1975;Holleman et al., 1979;Skogland, 1980;Adamczewski et al., 1988;Ferguson et al., 2001;Storeheier et al., 2003;Ophof et al., 2013).Similarly, the extent and consequences of active grazing by reindeer are well documented (e.g.Gaio-Oliveira et al., 2006;Moen et al., 2009;Kumpula et al., 2011;Tommervik et al., 2012;Thompson & Barboza, 2013;Turunen et al., 2013).However, trampling is not, in spite of being considered so important (Kumpula et al., 2011), with a potential "spillage" factor of up to 10 (Gaare & Skogland, 1975;Vistnes & Nellemann, 2008).We are only aware of one relatively old quantitative report on this, which is also the basis for the suggested (summer trampling) factor of 10.From measurements of trampling and material removed, but A near linear relationship may exist for plant eating (black line) and reindeer density when forage is abundant, but decreasing as competition for food increases, and depending on annual production of forage.Trampling loss may be low at low reindeer densities for pliable vascular plants (light grey darted line), but likely more linear in lichen (dark grey darted line), in particular in dry lichen, and considerably more than vegetation eaten.Step overlap may perhaps initially decrease loss rate of lichen as reindeer density increases.Loss will increase until vegetation cover is reduced, and eventually approaches mechanical disruption, when loss will obviously drop sharply (not modelled here).
not eaten by six domestic reindeer on relatively thick lichen mats, Gaare & Skogland (1975) estimated a loss factor of 10, relative to what the animals actually consumed during the snow season (103 g ±SD 71 DM m -2 versus 10 g DM m -2 ).Clearly, this factor will depend on season, and when, how, and how much reindeer graze on lichen ranges.In Alpine habitats this may be year round (e. g.Skogland, 1980;Skogland, 1984), in forested habitats variable, but often more in summer (Stark et al., 2000;Stark et al., 2007;Kumpula et al., 2011).In a later publication (Gaare & Skogland, 1980) this is restated as a 'wastage' factor varying positively with available lichen biomass, of '10 times intake at available biomass near the K-value' that 'declines to a factor of 2 at a biomass of 0.09 K' (K=maximum lichen biomass, with reference to Alpine habitats with lichen as primary winter forage).Here 'wastage' is attributed to reindeer selective feeding, which vary, for example with biomass, plant composition, and the degree of snow cover, and results in 'spillage of rejected lichen species dismantled from the mat in the process of digging and extracting'.Trampling per se was apparently not included here.Consequently, in addition to trampling, there may be substantial spill, i.e. reindeer appear to be not very efficient winter foragers.Already more than thirty years ago, Gaare & Skogland (1980) also stated that "The wastage factor appeared the most uncertain and critical value…".The substantial scale of such a 'wastage' factor is supported by a recent experimental study of reindeer trampling effects in dry, brittle lichen, i.e. a worst case scenario (Heggenes et al., 2017).Indeed, with reference to Gaare & Skogland (1980) recent attempts to build population models for reindeer (e. g.Moxnes et al., 2001;Tahvonen et al., 2014;Pekkarinen et al., 2015) have included "…removal is increased by wastage of lichen caused by grazing reindeer.….the fraction of lichen that is really lost to grazing, for instance by ending up in lakes and rivers.It does not include lichen, which fastens in a new location and continues to grow there" (Moxnes et al., 2001).Estimated loss factor was set to vary from 0.5 to 4.5 (times intake) depending on density of lichen.Again, type of grazing system may be important, likely with the highest loss factor in open alpine areas.Tahvonen et al. (2014) modelled lower, forested grazing systems with considerable snow depth, and modified the loss factor, taken from Moxnes et al. (2001), to 1.3 lichen removed (intake plus loss).Recently, Pekkarinen et al. (2015), again with reference to Moxnes et al. (2001), used seasonal wastage factors for lower, forested grazing systems, lowest (=1.3; intake plus loss in all factors) in winter due to snow cover, increasing during spring (=1.6) to a maximum in summer (=3.0), and then decreasing again in the fall (=1.6).Since all factors are more than one, the assumption is again that reindeer in summer waste considerably more lichen than they eat.
In an early observational field study, Pegau (1970) herded approximately 500 reindeer over a non-utilized portion of a large dwarf shrub meadow during moist and dry conditions, i.e. a rainy and foggy day and a dry, warm day after 24 hours without rain.The amount of dislodged and shattered lichens roughly doubled.After one summer, 68 % of the lichens were dislodged and 16 % were shattered into segments less than ½ inch.It was concluded that 'on summer ranges where lichens comprise at least 30 % of available forage, at least 15 % of the lichens should be considered as unavailable because of trampling by reindeer".To the best of our knowledge, this paper is the only one that describes the damage of trampling in more detail, suggesting that trampling may cause substantial loss of lichen, but depending on moisture.Observed differences of lichen biomass between different seasonal forested grazing areas (Kumpula et al., 2011, Kumpula et al., 2014) suggest major lichen waste, depending on season, weather conditions and moisture.It is, however, important to note that whereas shattered lichen may be unavailable as food for reindeer, this lichen is not necessarily lost or dead to the ecosystem.Such disturbance may also facilitate lichen spreading.

Conclusion
The common idea that reindeer trampling may be a major cause of lichen forage losses appears to be based on anecdotal observations, and does not seem well substantiated or quantified scientifically.However, vegetation loss due to 'wastage' appears to be much more important than vegetation eaten by reindeer, at least during certain ecological conditions, i.e. dry weather, in summer.Therefore, more studies and experiments are required that disentangle the important 'wastage' effects of different activities of reindeer.It appears difficult to state on a general basis that the 'wastage' of forage is 2-10 times the consumed forage, at least when it comes to trampling.The additional spill associated with selective vegetation eating, also remains to be studied in more detail.

Figure 1 .
Figure 1.A conceptual model of vegetation loss due to eating and trampling by reindeer.Trampling generates more vegetation loss than eating, but the relationship is likely underestimated in the figure (illustration purposes).A near linear relationship may exist for plant eating (black line) and reindeer density when forage is abundant, but decreasing as competition for food increases, and depending on annual production of forage.Trampling loss may be low at low reindeer densities for pliable vascular plants (light grey darted line), but likely more linear in lichen (dark grey darted line), in particular in dry lichen, and considerably more than vegetation eaten.Step overlap may perhaps initially decrease loss rate of lichen as reindeer density increases.Loss will increase until vegetation cover is reduced, and eventually approaches mechanical disruption, when loss will obviously drop sharply (not modelled here).