Fifty Years of Food and Foraging in Moose: Lessons in Ecology from a Model Herbivore

ALCES VOL. 46, 2010 SHIPLEY - MOOSE AS A MODEL HERBIVORE

FIFTY YEARS OF FOOD AND FORAGING IN MOOSE: LESSONS IN ECOLOGY FROM A MODEL HERBIVORE

Lisa A. Shipley

Department of Natural Resource Sciences, Washington State University, Pullman, Washington 99164-6410, USA

ABSTRACT: For more than half a century, biologists have intensively studied food habits and foraging behavior of moose (Alces alces) across their circumpolar range. This focus stems, in part, from the economic, recreational, and ecosystem values of moose, and because they are relatively easy to observe. As a result of this research effort and the relatively simple and intact ecosystems in which they often reside, moose have emerged as a model herbivore through which many key ecological questions have been examined. First, dietary specialization has traditionally been defined solely based on a narrow, realized diet (e.g., obtaining >60% of its diet from 1 plant genus). This definition has not been particularly useful in understanding herbivore adaptations because >99% of mammalian herbivores are thus classified as generalists. Although moose consume a variety of browses across their range, many populations consume 50-99% of their diets from 1 genus (e.g., Salix). Like obligatory herbivores, moose have demonstrated adaptations to the chemistry and morphology of their nearly monospecific diets, which precludes them from eating large amounts of grass and many forbs. New classifications for dietary niche suggest that moose fit on the continuum between facultative specialists and facultative generalists. Second, moose have been the subject of early and influential models predicting foraging behavior based on the tradeoffs between quality and quantity in plants. Subsequent models have predicted the size of stems selected by moose based on the tradeoffs between fast harvesting (large twigs) and quick digestion (small twigs). Because of their size, moose require many hours to harvest food, often selecting large bites as browse density declines. Finally, long-term monitoring of moose populations has provided evidence of how populations and communities are regulated. Low reproductive rates and long-term population trends shaped by moose density and forage availability on Isle Royale suggest a strong bottom-up effect on moose populations. Empirical data and simulation models suggest that moose may shape their own forage supply, influencing their community and their own populations, especially when large predators are scarce. Likewise, predation is the primary fac- tor affecting calf survival and thus moose populations in Alaska, demonstrating the important role of top-down factors. Moose will continue to provide a model for examining ecological questions such as tolerances for plant chemistry, what governs animal movements over landscapes, and reciprocal interactions between predation and reproduction.

ALCES VOL. 46: 1-13 (2010)

Key words: Alces alces, diet selection, foraging behavior, moose, niche breadth, specialization, population regulation.

For more than half a century, biologists America, Europe, and Asia, and their large size, have intensively studied food habits, foraging magnificent antlers, and fascinating behavior behavior, and nutrition of moose (Alces alces) make them valuable for consumptive and (Table 1, Fig. 1-3, reviews by Gasaway and non-consumptive recreation and subsistence Coady 1974 and Schwartz 1992). This large (Storaas et al. 2001, Timmerman and Rod- body of research has arisen both because moose gers 2005.) For example, a recent economic are of global interest occupying a circumpo- analysis estimated the annual harvest value of lar range spanning northern parts of North moose in Alaska alone at nearly $364 million

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Table 1. Time spent foraging and ruminating by moose. Location Season Feeding (hr) Ruminating (hr) Reference Central Alberta Winter 9.8 11 Renecker and Hudson 1989 Centra Alberta Summer 10.3 6.5 Renecker and Hudson 1989 Denali National Park, Alaska Winter 4.8 9.6 Risenhoover 1986 Denali National Park, Alaska Summer 7.2 7.2 Van Ballenberghe and Miquelle 1990 Rocky Mountain National Summer 8.9 9.1 Dungan et al. 2010 Park, Colorado and viewing value at $62 million (Northern herbivores, thus Dearing et al. (2000) relaxed Economics, Inc. 2006). Besides research the definition of a specialist for herbivores to aimed directly at better management of wild include animals consuming at least 60% of and captive populations of moose, moose have their diet from 1 plant genus. Regardless, <1% emerged in the ecological literature as a model of mammalian herbivores can be classified as herbivore through which many key broad eco- a specialist using this definition (Dearing et logical processes have been examined. Here, al. 2000, Shipley et al. 2009), which limits its I will review examples from the past 50 years usefulness for understanding dietary strategies of how and why moose have been used to test in most herbivores. and demonstrate ecological theory related to Moose provide a good example of the food and foraging. Specifically I will highlight difficulties in assigning herbivores to a how research with moose has contributed to 3 specialist-generalist category. In the literature dichotomies in herbivore ecology: 1) how to they have been referred to as both a “generalist define niche breadth relative to specialist and herbivore” (Belovsky 1978) and a “special- generalist herbivores, 2) how herbivores trade ist browser” (Hagerman and Robbins 1993). off food quality and quantity when selecting Across much of the moose’s range in western diets, and 3) the roles of top-down and bottom- North America, summer and winter diets up processes in regulating populations. consist of 75-91% willow (Salix spp., Fig. 1a- e). Likewise, diets in parts of eastern North Dietary niche: America and Sweden consist of primarily of 1 specialist OR generalist? species/genus specific to location (Fig. 2a-d). The question of what governs the dietary In contrast, in other areas moose consume a niche has been the focus of community ecology more diverse diet in which no single genus for decades (e.g., Hutchinson 1957, Levins comprises >60% of their diet (Fig. 3a-c). 1962, Futuyma and Moreno 1988, Kawechi Therefore, how moose are classified according 1994, Julliard et al. 2006). Many articles to the traditional definition of specialization have examined the question of why some depends on the location and scale that their herbivores consume a diverse diet consisting diet is measured. of many plant species, whereas others consume Because assigning herbivores like moose a very narrow diet (e.g., Freeland and Janzen to a specialization category based on their 1974, Westoby 1978, Sorensen and Dearing realized diet alone can be problematic, many 2003). Because dietary specialization is so have suggested characteristics of food plants common in herbivorous insects, specialists and the forager that are consistent with dietary have been traditionally been defined as an specialization. Specialist herbivores are ex- animal consuming only 1 plant species (i.e., pected to compete well in habitats where large, monophagous, Crawley 1983). However, predictable, mono-specific patches of chemi- dietary specialization is rare in vertebrate cally or physically defended foods occur that

2 ALCES VOL. 46, 2010 SHIPLEY - MOOSE AS A MODEL HERBIVORE are avoided by other animals (Freeland and al. 2000, Sorensen et al. 2005a). However, Janzen 1974, Westoby 1978, Crawley 1983, these adaptations reduce the range of plants, Lawler et al. 1998, Dearing et al. 2000, Moore especially novel plants, that they can consume et al. 2004). Because this food is normally less (Futuyma and Moreno 1988, Berenbaum and nutritious, these animals tend to be small with Zangerl 1994, Sorensen et al. 2005b). As a lower absolute energy requirements, or have result, specialists are difficult to feed in captiv- relatively low mass-specific metabolic rates. ity (Pahl and Hume 1991), respond poorly to The food often offers conspicuous stimuli for a changing environment, and are most likely easy detection, which requires lower neural to become vulnerable to extinction (Fisher et sophistication when selecting a diet, thus less al. 2003, Smith 2008.) energy invested towards brain tissue (Smith Moose generally conform with many, but 1979, Bernays and Funk 1999, Martin and not all of these criteria. In particular, moose Handasyde 1999). Specialists are expected are adapted to foods that form the bulk of to have specialized anatomical, physiologi- their diet. Willow and certain other hardwood cal, or behavioral adaptations for consuming browse species contain linear condensed tan- their primary food, especially advanced and nins that reduce protein digestibility (Hager- less expensive detoxification systems for a narrow range of plant chemicals (Freeland and Janzen 1974, Crawley 1983, Dearing et

Fig. 2. Examples of moose consuming a “specialist” diet of > 60% of a plant genus on a variety of Fig. 1. Examples of moose consuming a “spe- browse species in winter across its range, includ- cialist” diet of > 60% willow (Salix spp.) in the ing a) Scots pine (Pinus sylvestris, Shipley et al. summer in a) Wyoming (McMillan 1953), b) 1998), b) balsam fir (Abies balsamea, Ludewig Colorado (Dungan and Wright 2005), c) Alaska and Bowyer 1985), c) 3 species of maple (Acer (Van Ballenberghe et al. 1989), and during winter spp., Routledge and Roese 2004), and d) birch in Alaska (Risenhoover 1987) and British Co- (Betula spp., especially B. papyrifera, Thomas lumbia (Poole and Stuart Smith 2005). 1990). 3 MOOSE AS A MODEL HERBIVORE - SHIPLEY ALCES VOL. 46, 2010

al. 1999, Sorensen et al. 2005a). Moose have a relatively large liver for their size (Hofmann and Nygren 1992), thus an increased capacity to detoxify conifer browse with cytochrome P-450 enzymes (MacArthur et al. 1991). The moose has adapted an unusually large amount of room between the nasals and premaxillae which has allowed the development of a long, muscular, prehensile nose with widely spaced nostrils (Bubenik 2007). Presumably this anatomy aids stripping of willow leaves to increase bite size and harvest rate. However, this long nose is a liability when consuming small bites of forbs. Shipley et al. (1994) found that moose have the longest cropping time (min/bite) of 13 herbivores ranging from 0.01-500 kg. The anatomy of their nose allows moose to swallow underwater, enabling Fig. 3. Examples of moose consuming a “generalist” diet where no plant genus constitutes > 60% efficient consumption of aquatic plants that of the winter diet in Alaska (Wixelman et al. are avoided by most North American cervids 1998), b) Ontario (Cummings 1987), and British (Geist 1999). Columbia (Poole and Stuart Smith 2005). Moose also resemble specialist herbivores because they are difficult to feed in captivity. man and Robbins 1993). Moose produce The typical herbivore diet consisting of grain- specific salivary binding proteins particularly based pellets supplemented with alfalfa or efficient at binding linear condensed tannins, grass hay causes diarrhea, enteritis, and wast- whereas herbivores like mule deer (Odocoileus ing in moose (Schwartz et al. 1985, Shochat et hemionus) that consume a more diverse diet al. 1997). Although general diets of herbivores produce salivary binding proteins aimed at are much higher in starch than a typical moose both branched and linear tannins (Hagerman diet dominated by browse, moose do not and Robbins 1993). Willows also produce lack enzymes (e.g., pancreatic alpha amylase salicylates, a bitter phenolic glycoside, that and intestinal maltase) for digesting starch deters feeding by some herbivores, for example (Schwartz et al. 1996, Shochat et al. 1997). brushtail possums (Trichosurus vulpecula) However, moose only thrive in captivity when (Markham 1971, Edwards 1978, DeGabriel fed large amounts of supplemental browse et al. 2010). Likewise, conifers consumed and aspen-based herbivore pellets (Schwartz in large amounts contain monoterpenes and et al. 1985, Shochat et al. 1997). Therefore, other plant secondary metabolites that deter other components of browse diets such as feeding by herbivores such as snowshoe hares lignin, tannins, and salicin may contribute to (Lepus americanus; Rodgers et al. 1993) and the digestive health of moose. rodents (Murphy and Linhart 1999) Although Because many other herbivores fall in the little is known about how moose deal with gray area between a specialist and generalist, large amounts of these plant chemicals, other Shipley et al. (2009) developed a specializa- animals that specialize on terpenes such as tion key designed to more accurately place woodrats (Neotoma spp.) and arboreal marsu- a herbivore along the specialist-generalist pials have adapted efficient and less expensive continuum, thus accounting for a variety of detoxification enzymes in the liver (Boyle et 4 ALCES VOL. 46, 2010 SHIPLEY - MOOSE AS A MODEL HERBIVORE dietary strategies and forming a framework or change across their range. for comparative studies. The key assigns the modifiers “obligatory” and “facultative” to Diet selection: the terms “specialist” and “generalist” based quality OR quantity? on 1) relative breadth of the animal’s realized The fibrous cell walls of plants are niche and diet (what it eats), 2) relative breadth difficult for herbivores to digest, thus the of the fundamental niche and available diet nutritional quality and biomass of plants are (what it could eat), 3) the extent of chemical usually inversely related (Van Soest 1984). or physical characteristics, termed “difficulty”, Therefore, herbivores must make tradeoffs that make food items either low in value or when selecting diets, a process which forms unpalatable to most herbivores, and 4) relevant the backbone of most models predicting diet temporal and spatial scales at which diets and selection for herbivores. Many innovations in niche breadth are measured. optimal foraging models have been designed Obligatory specialists always consume for and tested with moose. One of the first a narrow diet of a difficult plant. They have and best-known optimal foraging models for unique adaptations that allow them to con- mammalian herbivores was Belovsky’s linear sume this plant that is generally abundant in programming model (Belovsky 1978). This their habitat, but these adaptations also tend model was based on the simple tradeoffs to prevent them from expanding their diet as moose in northeastern USA make when choos- environmental conditions change. Like the ing whether to consume deciduous leaves or obligatory specialist, facultative specialists al- aquatic plants. Deciduous leaves are less ways have a consistently narrow, realized niche fibrous and easier to harvest and digest than for difficult foods during at least 1 spatial or aquatic plants, but because many boreal for- temporal scale such as winter, but because their ests are depauperate in sodium (Belovsky and fundamental niche is broader, they can expand Jordan 1981), forest plants typically have less their diet to include less difficult foods when sodium than aquatic plants. To effectively meet environmental conditions allow, such as sum- their daily sodium requirement, moose need to mer. Like facultative specialists, the realized consume a minimal amount of aquatic plants. niche of the facultative generalist can change Based on simple intake and digestion models, depending on the local conditions. However, Belovsky (1978) suggested that moose needed they differ from facultative specialists in that to consume either a large amount of aquatic their diet is more commonly broad, they focus plants or a moderate amount of deciduous on different plant species in different seasons plants to meet their energy requirements, but or locations, and when their diet becomes because of digestion limitations, could only narrow, they tend to focus on less difficult consume a moderate amount of aquatic plants plants that are also consumed readily by other or a large amount of deciduous plants. His herbivores. Finally, obligatory generalists model, therefore, predicted that moose must always consume a mixed diet because they consume a mixture of aquatic and terrestrial have a a low tolerance for difficult foods that plants within a narrow range of possibilities. precludes them from eating much of any dif- He suggested that the exact mixture a moose ficult plant. Therefore, based on these criteria, should consume depends on its goal – whether moose would fall on the continuum between to maximize energy by consuming the minimal the facultative specialist and the facultative amount of aquatic plants possible with the generalist, because their diets consist of only maximum amount of deciduous plants subject 1 species and genus of moderately difficult to digestion limitations, or to minimize time plants in many areas, but their diet can expand spent feeding by consuming the minimum of

5 MOOSE AS A MODEL HERBIVORE - SHIPLEY ALCES VOL. 46, 2010 both types of plants to provide more time for sity changes. For example, moose consumed other life requisites. His data on diet composi- larger stem diameters as the size of patches tion of moose from Isle Royale National Park of red maple (Acer glabrum) stems declined in Michigan fit most closely with the energy and the distance between patches increased maximizing strategy. (Shipley and Spalinger 1995), and consumed Two decades later, moose were also the proportionately more birch as density declined subject of several models designed to exam- (Vivås and Sæther 1987). Fast harvesting and ine diet selection on a finer scale – what twig digestion is particularly important for large diameter a moose should select when foraging herbivores like moose that spend on average on deciduous browse in winter (Vivås et al. >8 h/d each feeding and ruminating throughout 1991, Kielland and Osborne 1998, Shipley et the year (Table 1). Therefore diet choices that al. 1999). These models incorporated more reduce the time spent in these activities allow mechanistic intake and digestion models to moose more time for other life requisites such examine tradeoffs between consuming bites as raising young, avoiding predators, and of a larger or smaller stem diameter. Crop- thermoregulation. ping stems at larger diameters allows moose Finally, many of the first spatially explicit to take larger bites (Vivås et al. 1991, Shipley individual-based foraging models (IBM) for et al. 1998, 1999), and in turn, taking larger large herbivores were built for moose (Roese bites allows moose to harvest food faster et al. 1991, Moen et al. 1997, 1998). For ex- (Risenhoover 1987, Shipley and Spalinger ample, Moen et al. (1997) used IBM to examine 1992, Gross et al. 1993). However, smaller how foraging rules affect emergent properties stem diameters have less fiber making them such as body mass and movement pathways of easier to crop, chew, and digest (Shipley and moose foraging across patchy and seasonally Spalinger 1992, Kielland and Osborne 1998, changing landscapes. Landscapes consisted Shipley et al. 1998). Keilland and Osborne of grids with 1 m2 feeding stations contain- (1998) and Shipley et al. (1999) predicted ing bites of deciduous browse. Quantity and the twig size that herbivores should select quality of browse was updated seasonally and to maximize digestible energy/d based on with herbivory, and animals moved in nested mass-specific constraints on consumption time steps according to foraging rules. Moen and digestion based on specific architecture et al. (1997) validated the emergent properties and chemistry of browse species. In Sweden, of their model with field and pen data, and moose selected twig diameters very consistent found that simulated moose using optimal with the predictions of the optimal bite size rules based, in part, on quantity and quality model when fed 5 deciduous browse species of forage had higher body mass and survival varying in structure and chemistry in concen- at the end of the year than moose foraging trated patches (Shipley et al. 1999). Likewise, randomly. Although different in approach, the twig diameters that moose selected from these linear programming, optimal bite size, feltleaf willow (Salix alaxensis) in Alaska and IBM models indicate that when choosing (Keilland and Osborne 1998) and pubescent diets, moose seem to weigh the value of fast birch (Betula pubescens) in Norway (Vivås harvesting and fast digesting and select the et al. 1991) were predictable from tradeoffs diet that gives them the highest digestible in quality and quantity. energy per day, and in many cases are more Further experiments also showed that sensitive to the effects of plant morphology on moose perceive these tradeoffs between intake rate than plant chemistry on digestion harvesting and digesting plants quickly, and (Keilland and Osborne 1998). modify their harvesting behavior as plant den-

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Population regulation: ecosystems are limited from the top down or top-down or bottom-up? bottom up depends on the productivity of the Moose populations provide excellent case ecosystem. They argued that extremely unpro- studies for investigating the classic question in ductive systems like deserts and tundra do not population ecology of whether populations are produce enough forage to support herbivores, regulated top-down by predators or bottom-up let alone carnivores. In moderately productive by food. The theoretical implications of this ecosystems, plants are limited by herbivores, question have been recognized and debated for but plants support insufficient herbivore popu- at least 100 years since the beginning of the lations to support large numbers of predators. field of ecology (Pimm 1991); however, the In very productive systems, such as rainforests, practical implications have become increas- herbivores are limited by predators, but plants ingly important as many large carnivores are are not limited by herbivores as Hairston et either disappearing [e.g., lynx (Lynx canaden- al. (1960) proposed originally. sis) in northwestern USA; Koehler et al. 2008] Moose are considered a “classic textbook or reappearing [e.g., successful recolonization case” by ecologists for examining this debate of wolves (Canis lupus) in the northern Rocky (Peckarsky et al. 2008), both because many Mountains of the USA; Oakleaf et al. 2006] moose populations live in remote areas with on the landscape. relatively intact ecosystems in which their Almost 50 years ago, Hairston et al. (1960) large predators are still present, and because argued that “the world is green” because plants of the availability of unique long-term datasets are more abundant than animals, thus herbivore such as that collected in Isle Royale National populations must be controlled top-down by Park for the last 50 years. On Isle Royale, carnivores. They suggested that carnivores bottom-up effects seem to predominate in the should compete for food because they lack unique ecosystem of single plant (balsam fir, predators to limit their populations, whereas Abies balsamea), large herbivore (moose), and because herbivore populations are limited by large predator (gray wolves) largely unaltered predators, they should not compete for food. by humans. Vucetich and Peterson (2004) Assuming that herbivore populations are found that annual production of balsam fir was limited by predators, they should be unable 3 times more important in models predicting to limit plant populations that in turn would moose density over the last 50 years than compete for resources. Therefore, removing was wolf density. In turn, wolf density was carnivores should have a strong effect on predicted both by moose density and balsam herbivores, but removing herbivores should fir production. In areas with more diverse have little effect on plant densities. Murdoch plants, herbivores, and predators and those (1966) later suggested that the world is not that have been modified by humans through green – instead plants are mostly “prickly harvest, both bottom-up and top-down effects and taste bad” – arguing that ecosystems are have been observed. For example, moose regulated bottom-up because physical and range in south-central Alaska contains wil- chemical defenses make plants largely ined- low and other forage plants, an alternative ible. Therefore, herbivores are scarce and large herbivore, and at least two abundant compete intensely for limited nutrients avail- large carnivores [bears (Ursus americanus, U. able in plants. As a consequence, predators are arctos) and wolves; Testa 2004]. In a 4-year limited by competing for scarce herbivores. study, Testa (2004) found female moose in Thus, removing either predators or herbivores poor body condition, with low twinning rates has little effect on their food supply. Finally, and delayed age of first reproduction, and a Oksanen et al. (1981) suggested that whether negative relationship between raising a calf

7 MOOSE AS A MODEL HERBIVORE - SHIPLEY ALCES VOL. 46, 2010 successfully and producing twins the following and even a dedicated scientific journal (Alces). year. These characteristics suggest that food Additional characteristics of moose and the (willow) plays a role in limiting the moose habitats in which they reside have caused population. However, in the same study, Testa moose to emerge as a model herbivore for (2004) found high calf and adult mortality from testing broad ecological principles. First, predation, resulting in low recruitment indicat- moose often reside in simple and/or intact ing that predation had a greater influence on ecosystems that facilitate basic research. For population dynamics than nutrition. example, in many boreal systems moose select Whether a large herbivore might control an from fewer than 10 species of available plants ecosystem as a top-down influence may depend during winter (Shipley et al. 1998, Vucetich on its ability to escape higher top-down control and Peterson 2004). In addition, many habitats by carnivore populations through large size, moose occupy have been protected by parks migration, or availability of alternative prey and reserves (e.g., Yellowstone National Park, or predators (Sinclair 2003). A vast body of Rocky Mountain National Park, Isle Royale, literature (e.g., Bergström and Danell 1987, Denali National Park), or are protected de Lozinov and Kuznetsov 2002, Morris 2002, facto by their remoteness. Therefore, much Persson et al. 2005, Siipilento and Heikkilä of moose range still contains large carnivores 2005, Stolter 2008) suggests that in areas where and natural vegetation. Second, compared populations of large carnivores are naturally or with many small and wary herbivores, moose artificially low, moose can control their food have proven to be surprisingly easy to observe sources from the top-down. A review (Pastor both in the field and captivity. For example, and Danell 2003) of moose across their cir- Risenhoover (1987), Van Ballenberghe and cumpolar range concluded that as moose select Miquelle (1990), and Dungan and Wright the most nutritious parts of hardwood browse, (2005) were able to count bites from wild they damage or remove the photosynthetic and moose that tolerated their presence, and meristematic tissues. Many species of browse researchers such as Renecker and Hudson respond by growing more quickly and with less (1986) and Shipley and Spalinger (1992, fiber and plant secondary metabolites. This, in 1995) hand-reared moose for foraging studies turn, provides more high quality moose forage in semi-natural conditions. Moose also leave and an incentive for moose to re-browse the conspicuous remnants of their foraging activity same plant. However, over the long term these such as easy-to-see browsed twigs and fecal plants grow more slowly, have lower survival, pellets. Finally, insights into food and foraging and are less competitive. Furthermore, Stolter are often most lucrative when studying large (2008) found that browsed willows had fewer herbivores like moose that must spend most catkins and reduced reproductive output. It of their time foraging to satisfy their high follows that in situations of overpopulation, forage requirements. With these desirable preferred moose forages could be replaced characteristics, moose will continue to provide with less nutritious plants, such as conifers, a model for examining ecological questions that grow and decompose more slowly and such as tolerances for plant chemistry, what ultimately change the composition and reduce governs animal movements over landscapes, productivity of an ecosystem. and reciprocal interactions between predation and reproduction. overview Moose are widespread, charismatic, and Acknowledgments popular for recreation and subsistence, and Thanks to T. Bowyer, K. Danell, N. T. thus have been the subject of much research Hobbs, J. Forbey, B. Moore, and D. E. Spal-

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