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Roles for the Canidae in food webs reviewed: Where do they fit?

Peter J.S. Fleming, Huw Nolan, Stephen M. Jackson, Guy-Anthony Ballard, Andrew Bengsen, Wendy Y. Brown, Paul D. Meek, Gregory Mifsud, Sunil K. Pal, Jessica Sparkes

PII: S2352-2496(16)30011-8 DOI: doi:10.1016/j.fooweb.2017.03.001 Reference: FOOWEB 55

To appear in:

Received date: 8 June 2016 Revised date: 9 March 2017 Accepted date: 10 March 2017

Please cite this article as: Fleming, Peter J.S., Nolan, Huw, Jackson, Stephen M., Ballard, Guy-Anthony, Bengsen, Andrew, Brown, Wendy Y., Meek, Paul D., Mifsud, Gregory, Pal, Sunil K., Sparkes, Jessica, Roles for the Canidae in food webs reviewed: Where do they fit?, (2017), doi:10.1016/j.fooweb.2017.03.001

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs

Roles for the Canidae in food webs reviewed: where do they fit?

Peter J. S. Fleminga,b, Huw Nolanb, Stephen M. Jacksond,e,f, Guy-Anthony Ballardb,g, Andrew Bengsena, Wendy Y. Brownb, Paul D. Meekb,h, Gregory Mifsudi, Sunil K. Palj, and Jessica Sparkesa,b a Vertebrate Pest Research Unit, New South Wales Department of Primary Industries, 1447 Forest Road, Orange, New South Wales 2800, Australia. Corresponding author: [email protected] b School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2351, Australia. d Animal Biosecurity and Welfare, New South Wales Department of Primary Industries, 161 Kite Street, Orange, New South Wales 2800, Australia. e School of Biological, Earth and Environmental Sciences, University of New South Wales, UNSW Sydney, NSW 2052, Australia. f Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, United States of America. g Vertebrate Pest Research Unit, New South Wales Department of Primary Industries, Allingham Street, Armidale, New South Wales 2350, Australia. h Vertebrate PestACCEPTED Research Unit, New South MANUSCRIPT Wales Department of Primary Industries, 76 Harbour Drive, Coffs Harbour, New South Wales 2450, Australia. i Invasive Animals Cooperative Research Centre, 203 Tor St, Toowoomba, Queensland 4352, Australia. j Katwa Bharati Bhaban, Post Office Katwa, Burdwan District, Pin-713130, West Bengal, India .

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Abstract

The roles of the 37 species in the family Canidae (the dog family), are of great current interest. The Gray Wolf is the largest canid and their roles in food webs are much researched, as are those of Domestic Dogs, Coyotes and Red Foxes. Much less is known about the other canid species and their ecological roles.

Here we describe general food web theory and the potential application of network theory to it; summarise the possible roles of predators in food webs; document the occurrence, diet and presumed functions that canids play in food webs throughout the world; give case studies of four threatened canid species of top, middle and basal trophic positions and six anthropogenically affected species; and identify knowledge limitations and propose research frameworks necessary to establish the roles of canids in food webs.

Canids can be top-down drivers of systems or responsive to the availability of resources including suitable prey. They can be affected anthropogenically by habitat change, lethal control and changes to basic resource availability. They can be sustainable yield harvesters of their indigenous prey or passengers in complex ecosystems, and some are prey of larger canids and of other predators. Nevertheless, the roles of most canids are generally poorly studied and described, and some, e.g. Gray Wolves, Coyotes and Australian dingoes, are controversial. We advocate mensurative and experimental research into communities and ecosystems containing canids for a quantitativeACCEPTED understanding ofMANUSCRIPT their roles in food webs and consequent development of better management strategies for ecosystems.

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Graphical Abstract

A continental schematic showing relative trophic positions (top, middle, bottom) of the 37 species of the family Canidae. Numbers are canid species in alphabetical order from Table 1 and their IUCN status is shown by coloured shading, with white being of “least concern” and darkest being “critically endangered” (after Woodroffe & Sillero- Zubiri, 2012). Non-canid predators, including humans, are excluded for simplicity and some species, e.g. 5, 6, 36 and 37, occupy two or three trophic positions. The green & brown arrows at left (Interaction vector) represent the non-scalar, strength and directions of networkACCEPTED interactions between MANUSCRIPT canids at the three trophic levels, which are presently unquantified (?).

Keywords

Allometry; anthropogenic; basal predator; bottom-up; endangered fauna; invasive animal; mesopredator; network theory; top-down; top-predator; trophic position

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1. Introduction

The concept of food webs (sensu MacArthur 1955; MacArthur & Levins 1964), while seemingly intuitive, is a relatively recent theoretical development, deriving from contributions in the early- to mid-twentieth century. Andrewartha and Birch (1954; 1986) described a precursor concept to a food web, the “ecological web”. Central to an ecological web is the “average” organism of interest, the population in which it occurs and its influencing factors such as resource availability, mates and predators. This is the “centrum” (Andrewartha & Birch 1986) around which is a branching web of indirectly acting organic and inorganic components. The ecological web is a useful environmental theory to conceptualise the interactions of biotic and abiotic factors in “average” environments, but falls short for quantifying the relationships among animals in communities or whole ecosystems.

Food webs provide capacity to conceptualise and quantify the size and net direction of ecological interactions. They are networks of interactions between and within populations of consumer organisms and the organisms they consume, encapsulating and describing trophic interactions within ecological communities (Dunne et al., 2002; MacArthur & Levins, 1964). The simplest food webs are linear food chains with one primary producer (usually a plant or fungi species), one first level consumer (usually a herbivore), and one or two levels of upper consumers (i.e. a predatory species and its predator/s) (e.g. Paine 1980). Reticulate food webs are more complex in that the lowest or first ACCEPTEDconsumer levels have two speciesMANUSCRIPT (Fox & Olsen, 2000; Teng & McCann 2004). These systems have been useful in artificial laboratory constructs (e.g. Fox & Olsen 2000) and framing more complex topological food webs, which are qualitative (Rossberg, 2012).

Of critical importance to food web theory is that the relative magnitude and directions of interactions between populations of organisms and trophic levels can be quantified as vectors and used to model system dynamics in response to trophic interactions (Rossberg, 2012; Williams & Martinez, 2000). The calculated variables that are useful measures of interrelationships between species and complexity in ecosystems are: 1) connectance, which is the number of links between trophic species divided by the

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ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs maximum possible number of species squared (Martinez 1991; Montoya & Solé 2001) and a measure of the overall connectedness of the system; 2) links per species, which is a simple averaging measure of the interrelationship between species (Dunne et al., 2002); 3) degree distribution, which is a frequency distribution of species with links from 1 to the maximum number for the system (Montoya & Solé, 2001); and 4) generality, the mean number of prey per predator, which is a simple measure of the foraging relationships between predators and prey (Strong & Leroux, 2014) or relative biomass (Hatton et al. 2015). The objective of these measures is to provide both descriptive and predictive models of ecosystem function and the likely effects of natural and anthropogenic perturbations.

Dunne et al. (2002) discuss the application of network theory to food webs because previous models implied symmetry of link strength between trophic levels (see Williams & Martinez, 2000), whereas asymmetry prevails (Abrams & Cortez, 2015; Schoener, 1983). Network theory incorporates clustering around nodes of different strength linkages relating to distance from the node, with neighbours much more likely to be connected to each other (see Strogatz, 2001 for a review of network theory applications and development).

With asymmetric link strengths, system responses to perturbations are potentially more accurately described in a network-modelled food web (Dunne et al., 2002). Running the models with empirical or simulated values of the strength and clustering of relationshipsACCEPTED within and between trophic MANUSCRIPT species could predict the stability of a food web and the consequences of removing or adding species. This approach has potential application to food webs where predators are suspected to regulate prey abundance and drive or shape ecosystem structure and function.

There are usually few carnivores in food webs but they can play the important roles in ecosystem function (e.g. Hauffaker, 1958; Mninshall, 1967; Murdoch, 1969; Paine, 1966). Members of the family Canidae are mostly predators, potentially fulfilling a variety of roles in the food webs where they occur, but their ecological roles and relative importance in shaping ecosystems and the development of subsequent ecological theory have been the topic of much recent debate (e.g., Abrams & Cortez,

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2015; Allen, 2015b; Allen et al., 2014; Estes et al., 2011; Mech, 2012; Ripple et al., 2014; White, 2013).

Despite the active debate about canid roles and function, our literature searches have revealed little application of food web theory to canid-topped systems: WEB OF SCIENCE searches on combinations of “food web”, “ecological role”, “apex predator”, “top predator”, “wolf” and “dingo” yielded just two references (Eisenberg et al., 2013; Glen et al., 2007). Although Colman et al. (2014; 2015) and Hunter et al. (2015) used analogous methods to describe Australian ecosystems, we could find no literature that directly applied network theory to systems with canid predators. With this in mind, we here review the possible roles of canids as a commencement point for future application of food web and network theory to describe ecosystems in which they occur. We have chosen to return to first principles so that research questions about the functional roles of canids in ecosystems can be multidirectional and therefore more likely to progress theory.

2. Possible roles of predators in food webs

As May (1986) pointed out, populations without limitation (i.e. with density- independent vital rates) would increase without bound, which is impossible. Therefore, some density-dependent limiters prevail in order to keep the food web balanced with approximately stable or cyclical populations of organisms. Population and community dynamics are subject to both resource-mediated (bottom-up) and predator-mediatedACCEPTED (top-down) processes MANUSCRIPT (Andrewartha & Birch, 1954, 1986; Hairston et al., 1960; Krebs, 2014; Slobodkin, 1980). Early laboratory experiments by Connell (1961) and Slobodkin (1964) demonstrated the beneficial influence of predators on prey diversity, but also showed that ultimately all members of the artificial communities were dependent on available resources, i.e. water, nutrients and cover. More recent laboratory experiments with perturbed simple linear and reticulate food webs of unicellular organisms (Fox & Olsen 2000) indicated that increasing the complexity of the system by addition of bottom prey species enhanced the numerical response at the top trophic level, i.e. a bottom-up system. But, what roles do predators, specifically canids, play in real food webs?

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Real food webs are usually more complex than artificial or laboratory systems. When food webs exhibit greater complexity, predators are predicted to be less crucial for system dynamics, and, conversely, to be more important in less complex networks. This is because the fewer the nodes and links, the more crucial each species is in the structure of the web (Dunne et al., 2002). Predator roles and ecosystem complexity will therefore be context-specific. The roles that animals, producers and consumers, play in food webs have interrelated impacts, including regulation of populations. It is traditional and convenient to view food webs as networks of trophic species with different levels from primary producers at the bottom up to tertiary consumers at the top.

2.1 Trophic position and allometry Functionally, predators are usually categorised into three trophic positions: 1) top (or apex) predators that are denominated by their presumed or known top trophic position; 2) the mesopredators, or middle predators, which can be functional prey of top predators but prey upon smaller herbivores and predators; and 3) bottom, or basal, predators, which are sometimes prey of all those co-occurring predators in higher trophic levels (Krebs, 2014). The term “mesopredator” (deriving from the Greek μέσος, and transliterated, “mésos”) means middle or average predator. This terminology allows for flexibility of roles according to the scale of the system, so that a mesopredator in one system can be top or bottom predators in others (Fleming et al., 2013; Johnson& Ritchie, 2013). However, this terminology can be confusing. For example, bothACCEPTED Gray Wolves (Canis lupus ) MANUSCRIPTand Australian dingoes (C. familiaris) can be top predators in systems without humans (Estes et al., 2013; Fleming & Ballard, In press 2015); the former is a large predator, and the latter, although the largest of Australia’s non-human predators, is middle-sized in relation to other canids and mammalian predators.

Perhaps we should simplify and standardise the language used to describe trophic position and body size because these do not always align in the family Canidae. For example, if we used English consistently, we would have large, medium and small sized predators, occupying top, middle and basal trophic positions. “Apex” is intrinsically problematic in that it implies singularity at the peak of a trophic pyramid, when

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Form and function are sometimes conflated in the nomenclature canid ecologists use. The confusion occurs when the functional role in the food web is assumed from the form, usually from absolute body size (e.g. see discussion in Johnson & Ritchie, 2013 and Fleming et al., 2013), rather than size relative to other animals and the energetic flux in the system (Rossberg, 2012). Despite this, trophic roles do partially depend on absolute body size, which effects behaviour through energetic constraints on movements and diet (Rossberg, 2012), and on the interactions of food capture, handling time, relative prey size and foraging frequency (Stephens & Krebs, 1986). Predation rates and predatory impacts on subordinate predators and consumed prey are expected to comply with allometric relationships under optimal foraging theory (Sinervo, 1997). Allometric scaling is usually described by a power function of body mass or weight with the exponent affected by trophic relationships (e.g. Harestad & Bunnell, 1979; Lindstedt et al., 1986). From allometric calculations, it is expected that smaller canids can capture and handle prey that is a greater proportion of their body weight than can larger canids. However, by changing their foraging tactics and hunting as a group, someACCEPTED canids (particularly the topMANUSCRIPT predators) can capture and kill prey much larger than would be predicted from allometry: effectively they act as a single, larger predator (see below examples and Fig 2.).

2.2 Possible ecosystem functions of predators

The functional roles of predators vary greatly as they can be population regulators, population limiters, harvesters, prey for other predators, facilitators, catastrophic agents or carriers of pathogens affecting population dynamics of themselves and ecosystems. In some ecosystems, the suite of eutherian predators is diverse (e.g. the Little Karoo in South Africa, which has sympatric Leopards (Panthera pardus), Black- backed Jackals (Canis mesomelas), Caracals (Caracal caracal), African Wild Cats (Felis 8

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs sylvestris lybica) and several smaller species of mustelid: Mann et al., 2015), leading to complex food webs and interspecific roles and dynamics. Others, such as most Australian ecosystems, are simpler with two to three eutherian predators (Domestic Dogs, Red Foxes, Vulpes vulpes, and feral Domestic Cats, Felis catus), which are all introduced and have as-yet unconfirmed ecological roles (Allen et al., 2013a;b; 2014; Newsome et al., 2015a). Some might be keystone species (e.g. Ripple et al., 2014, consider the Gray Wolf a keystone in Yellowstone National Park: Letnic et al., 2009, consider the Australian dingo a keystone in parts of Australia). They can have more than one role simultaneously and can change roles depending on context.

Predators as population regulators: Diversity of lower trophic levels can benefit from greater diversity of predators (e.g. Estes et al., 2011; Paine, 1966; 1980) and suffer from predator removal (Estes et al., 2011; Ripple et al., 2014), i.e., top-down systems. For this to occur, the predators must act as regulators. Population regulation is a density-dependent process whereby a population of consumer organisms (in upper trophic levels, either predators or herbivores), controls the abundance and distribution of a population of producer organisms (either prey or herbage) (see Krebs 2014 for a good discussion). In this case, the regulating factor is the population density of the higher trophic organism, which increases the per capita mortality rate, or decreases the per capita reproductive rate, of the lower trophic organism with its increased density. Conversely, declines in consumer density will feed back to an increased producer density through decreases in its per capita mortality or increases in its fecundity. ThisACCEPTED is a top-down process and MANUSCRIPT the consumer has essential function in population dynamics of the consumed: when predators are regulators, they are essential strands in the food web, which increase complexity and biodiversity of the system (Corbett, 2001; Krebs, 2014). Regulation is a necessary function of a keystone species.

Predators as population limiters: Population limiters stop the food web getting too big. Limitation occurs when the presence of predators reduces the equilibrium density of prey such that prey abundance is higher if the predator is absent. Hence, the predator has a function but is not essential for prey because the abundance of both predator and prey is food limited. In such systems, the food web is driven by primary production 9

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs with predators modulating abundances of prey, and is a predator-modulated bottom- up system (Kay, 1998).

Predators as sustainable yield harvesters: Sustainable yield harvesting occurs when the ratio between the harvested biomass (i.e. prey or forage) and the productivity of the system is retained at a fluctuating equilibrium through time (Caughley, 1980). Predator abundance is responsive to the abundance of the prey and continues to sustainably harvest a doomed surplus without affecting overall mortality rates. In the theoretical extreme of this case, the maximum sustained yield, predators increase the equilibrium density of prey such that prey abundance is lower if the predator is absent (Caughley & Sinclair, 1994). Hence, the predator has a function but is not essential for prey dynamics, which fluctuate according to availability of forage (i.e. food-limited) and other resources. We suggest that such systems are bottom-up ecosystems, which would be predator-modulated in cases of maximum sustained yield.

Predators as supernumerary harvesters: A possible less-functional role for predators is that of supernumerary harvesters or passengers in the system. In such cases, predators would have no effect on equilibrium density of prey, prey dynamics would be unaffected if the predator were present or absent and the predator is non-essential. In such systems, abundances of all species would be food-limited (White, 2013) and predators would be redundant strands in the web.

Predators as prey: Smaller predators can also be the prey of larger predators, or functionally soACCEPTED (e.g. Chamberlain & Leopold, MANUSCRIPT 2005; Lourenço et al., 2014; Pils & Martin 1974). Some authors (e.g. Newsome & Ripple 2015) separate consumptive predation from interspecific competitive and intraguild killing with no associated consumption, but the population effects will be the same regardless of consumption. For many species, the young are vulnerable to predation until a threshold size (e.g. Artic Fox (Alopex lagopus) and Red Fox interspecific predation on cubs, Frafjord et al., 1989), at which the ratio of energy gained by the consumer to its capture effort expended switches in their favour. Basal predators such as these have no effect on equilibrium density of other prey except as part of a guild of prey whose relative availability to the predator changes with abundance or cover. Overall predator-prey dynamics and

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ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs measures of food web complexity are unaffected if the basal predator is present or absent. As prey, the small predator is non-essential and can be substituted by organisms of similar energy and nutritive value. Abundance of such predators could be bottom-up and producer-limited, top-down or a combination system with some modulation or regulation by larger predators.

Predators as trophic structural imperatives: There are two ways that a predator can be imperative to an ecosystem, as facilitator or keystone. Facilitation of subordinate predators occurs when, in a system with surplus resources, its abundance is exaggerated through subsidies of food types beyond their normal hunting strategies (e.g. Gray Wolves facilitating Coyotes, Canis latrans, through the provision of large herbivore carcasses; Switalski, 2003; Wilmers & Getz, 2004). Scavengers are able to feed upon prey that would otherwise be too large for them to capture and handling energy is saved because the hard work of capture has been done by the top predator. In these cases, the abundance and diversity of subordinate predators and some prey would be higher when the top predator is present.

For a top predator to be keystone in a food web (see also above), the abundance of subordinate predators and their preferred prey would be higher when the top predator is absent and removed (Paine 1966). There, without the keystone species, the system diversity declines though a trophic cascade to a lower state. Such systems are classic top-down system exemplified by mesopredator release-led trophic cascades (Estes et al., 2011ACCEPTED; 2013; Ripple et al., 2014; MANUSCRIPT Newsome & Ripple, 2015). Predators as pathogen carriers: The abundance of animals can be driven by pathogens of which predators are common vectors in complex, often multispecies disease life cycles (e.g. hydatidosis, Jenkins & Morris, 2003). Intra-specifically, the introduction of a virulent pathogen can drive the density of a predator lower causing a local rapid population decline (e.g. canine distemper in African Wild Dogs (Lycaon pictus), Marco et al., 2002), which can create mosaics of different densities into which prey and subordinate predators can leak and multiply if they are below the carrying capacity of the forage. Density-dependent disease transmission may be triggered at a threshold density of predators. Naïve and susceptible predator populations can rapidly decline

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(e.g. canine parvovirus in Gray Wolves; Mech & Goyal, 1993) or be driven functionally extinct (e.g. rabies in Kenyan African Wild Dog packs; Kat et al., 1995). Disease dynamics that depend on social interaction among predators, e.g. those spread by direct contact such as rabies, can be independent of density (e.g. Sparkes et al., 2014). Loss of predators from disease could potentially be the driver of increased prey populations and stimulus for cycles if the underlying food web is top-down mediated. Of particular association with canids is rabies, which is a rhabdovirus infection that irrupts in endemic regions, reducing populations of carnivores substantially (Tenzin & Ward, 2012; Sparkes et al., 2014).

Predator-borne pathogens can have population effects for predators (e.g. sarcoptic mange in Red Foxes; Bates, 2003) and prey through some predator/ herbivore disease cycles (e.g. canid-borne hydatid disease in Brush-tailed Rock-wallabies, Petrogale penicillata; Barnes et al., 2008: Gray Wolf-borne hydatids infecting moose, Alces alces and increasing their risk of predation by wolves; Joly & Messier, 2004). This effect on food webs is indirect and may operate in top-down or bottom-up systems. Predator- borne zoonoses sometimes affect human-dominated ecosystems (e.g. Echinococcus granulosus and E. multilocularis affecting humans in Africa and Asia; Jenkins et al., 2005).

Predators as catastrophic agents: Population, and indeed community, catastrophes can be caused by predators, usually those anthropogenically introduced (e.g. Red Foxes: Risbey etACCEPTED al., 2000; Lapidge & Henshall, MANUSCRIPT 2001; Abbott, 2011). In this scenario, the introduction of a novel predator drives the equilibrium rate of increase of the prey population below zero, which leads to their extinction. The predator then either switches to alternative prey or becomes locally extinct itself. This is initially a top-down system, which can change to a bottom-up system when the predator switches to alternative prey. In such cases, the predator is a threatening process and naïve and vulnerable prey populations can be rapidly driven extinct, which may be independent of density of predator.

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3. Canidae: phylogeny, occurrence, trophic position and sympatric interactions

3.1 Phylogeny and distribution of the Canidae

The Canidae is a widely distributed family of eutherian predators, that are thought to have evolved in North America about 40 Mya (Wang et al., 2004), and is divided into three subfamilies; the extant Caninae; the Hesperocyoninae, which became extinct about 15 Mya; and the Borophaginae, the last of which date back approximately 2 Mya (Wang et al., 2004). The Caninae comprise approximately 37 species that are dispersed naturally and anthropogenically across all continents except Antarctica (Table 1). There are 13 living genera of canid, nine of which have only one extant species and the most diverse being Canis, the South American Pseudalopex and Vulpes.

Insert Table 1 hereabouts

The Domestic Dog was the first species to be domesticated, deriving from the Gray Wolf or a common ancestor at least 27,000 years ago (Skoglund et al., 2015), although the exact date and location are conjectural (Freedman et al., 2014; Pang et al., 2009; Savolainen et al., 2002; Skoglund et al., 2015; Thalmann et al., 2013). Phylogenetic studies in the Domestic Dog have been assisted by the early sequencing of its genome (Lindblad-Toh et al., 2005), predating that of the human genome. Domestic Dogs have undergone selective pressures applied from their environment and by humans, resulting in great phenotypic diversity (Larson et al., 2012; Lindblad-Toh et al., 2005). They vary in shape and modernity from ancient breeds that have become feral (e.g. Australian dingoesACCEPTED and New Guinea singing MANUSCRIPT dogs) to modern types that require human intervention to give birth (e.g. pugs and bulldogs). Apart from the Red Fox, which has been experimentally domesticated in the 20th century with domesticates showing substantial genetic, morphological and behavioural changes (Kukekova et al., 2008), and possible domestication of the extinct Fuegian dog from the Culpeo (Pseudalopex culpaeus) (Petrigh & Fugassa, 2013), no other canid has been domesticated.

There is some hybridisation and admixing among canid species in the wild (e.g. Coyotes and Domestic Dogs, Leonard et al., 2014: Gray Wolves and Domestic Dogs, Klütsch et al., 2011). Animal hybridisation and genetic introgression can be a conservation risk, by combining genetics and homogenising populations and reducing 13

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs genetic diversity, or can drive speciation by increasing evolutionary novelty and adaptation (Rhymer & Simberloff , 1996; Seehausen, 2004). Prior to advances in genetic technology, recognising hybrids was often difficult or impossible (Benson & Patterson, 2013; Koepfli et al., 2015). Furthermore, the multiplicity of species concepts (Agapow et al. 2004; de Queiroz, 2005) makes it nearly impossible to elucidate the effects of hybridisation on the ecology of canids. For example, , the Red wolf (Canis rufus) in Northern America has previously been the subject of much debate regarding its classification as a separate species (e.g. Nowak, 1992) or the result of hybridisation between C. lupus and C. latrans (e.g. Roy et al., 1994). Another wolf, the Eastern Wolf (Canis lycaon), is recognised by some as a distinct species based on dissimilar genetic analyses (Rutledge, 2010). However, it remains largely unrecognised as a species: it co- occurs and hybridises both with C. lupus and C. latrans, and all three Canis types, including their known hybrids, have morphological and ecological similarities (Benson & Patterson, 2013).

Hybridisation between Australian dingoes and more modern Domestic Dogs is often cited as a major threat to “species” survival (e.g. Corbett, 2008; Smith, 2015b), yet the taxonomic status and nomenclature of Australian dingoes is controversial. Corbett (2008) categorised the dingo as a sub-species of Gray Wolf, i.e. Canis lupus dingo (while using the synonym Canis familiaris dingo) and others (e.g. Crowther et al. 2014; Smith, 2015a) have called for the dingo to be classified as its own species, Canis dingo. However, the ancient breeds of Domestic Dog, such as the Indian pariah dog, basenjis, the New GuineaACCEPTED singing dog and the Australian MANUSCRIPT dingo, all interbreed with more modern Domestic Dog breeds, producing reproductively viable hybrid swarms (Koler-Matznick et al. 2007; Stephens et al., 2015), and Jackson and Groves (2015) have argued that C. familiaris best applies to Australian dingoes and all other Domestic Dogs. Regardless, the effect of hybridisation and introgression on food web function and whether canid hybrids confer negative or positive impacts upon ecosystems and trophic structure is debated (Claridge et al., 2014; Grant et al., 2005; Stronen et al., 2012).

3.2 Positions in food webs

Canids range in size from 0.8 kg to 60 kg (Table 1) and occur in a diverse range of habitats, from deserts and rainforests to mountains and wetlands, and from extremely 14

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs hot to extremely cold environments (Macdonald & Sillero-Zubiri, 2004; Rosenblatt et al., 2013; Sillero-Zubiri et al., 2004). Such a diversely adapted family occupies a range of roles in natural and human-manipulated food webs.

The position of each canid species within its respective food web is driven by its absolute and relative size, the presence and nature of competitor species, availability of food and the associated foraging strategy required to acquire it. The diets of the Canidae vary widely as some are hyper-carnivorous and specialists (e.g. see Gray Wolves: Table 2), while others, such as Domestic Dogs and Red Foxes, are more opportunistic generalists but predominately carnivorous. Other species, such as the Side-striped Jackal (Canis adustus) and Maned Wolf (Chrysocyon brachyurus), are primarily omnivorous generalists, favouring frugivory (Table 2).

Insert Table 2 hereabouts

The positions and roles of predators in food webs also depend on their foraging strategies. These strategies vary substantially amongst the Canidae, irrespective of their social structure and the relative size between predator and prey. Some canids, notably Gray Wolves, African Wild Dogs and Asiatic Dholes (C. alpinus), hunt cooperatively in large groups, which allows them to kill ungulate prey much larger than the individual canids. A foraging group can be a pack (which describes the social grouping), a number of packs, part of a pack, a dyad (usually a breeding pair) or unitary. Side-striped Jackals will hunt small prey cooperatively (Macdonald et al. 2004) whereas the KitACCEPTED Fox (Vulpes macrotis) is aMANUSCRIPT solitary hunter preying upon rabbits that can be twice its size. The Bat-eared Fox (Otocyon megalotis) forages for small invertebrates in family groups, whilst the Ethiopian Wolf (Canis simensis) lives in a social group, but is a solitary hunter. Some canids exhibit flexibility in their foraging strategies, such as the Coyote and Australian dingoes, which hunt solitarily, as dyads or in groups when tackling large prey (Gese & Grothe, 1995; Thomson 1992; Fleming et al., 2001). Other species, such as the Red Fox, while mostly solitary, sometimes forage as dyads (Gosselink et al., 2010) and most of the smaller species usually forage individually and feed on invertebrates and small vertebrates (Table 2).

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3.3 Sympatric interactions among predators

The nature of interactions among co-occurring canids is often allometrically determined, with larger canids dominating smaller ones. Co-occurrence among predators is likely facilitated by spatial or temporal niche separation, and interesting co-relationships such as mutualism, kleptoparasitism and amensalism can occur (e.g. Saggiomo et al. 2017). However, interspecific deadly interactions are also common. Such intraguild predation and interspecific killing may be ecological forces involved in the evolution and structuring of communities (Polis et al., 1989; Polis &Holt, 1992; de Oliveira & Pereira 2014). Both processes are reported across taxa (Polis et al., 1989; Arim & Marquet, 2004; Gagnon et al., 2011), and the behavioural attributes in mammalian carnivores are well defined (Arim & Marquet,2004). Intraguild predation and killing are often asymmetrical (Palomares & Caro, 1999), occurring most frequently when there is a measure of niche overlap (Rosenzweig, 1966, Creel & Creel 1996). The intensity and frequency of predation reaches a maximum when the larger species is 2-5.4 times the mass of the victim (Donadio & Buskirk 2006). In general, the larger, higher trophic order species can restrict the population sizes and distribution of subordinate species by predation, competitive displacement or exclusion (Creel et al., 2001; Gause, 1934; Kamler et al., 2003; Lindström et al., 1995; Mills & Gorman 1997; Volterra, 1926).

Behavioural adaptations by numerically superior smaller canids can facilitate sympatry between species of canids (Atwood & Gese, 2010). Vigorous displays of aggression sometimes allowACCEPTED smaller canid species to MANUSCRIPT gain access to resources that might otherwise be dominated by larger predator species. Maynard and Smith (1976) termed this successful aggressive behaviour by an asymmetrically subordinate competitor “resource holding potential”. Condition-dependent superior vigour by a smaller, more aggressive species is not without precedent among canids. For example, Loveridge and Macdonald (2002) observed smaller Black-backed Jackal displace the larger Side- striped Jackal from prime foraging habitat. When numerically superior, Coyotes can supplant Gray Wolves at carcasses through aggressive behaviour (Atwood & Gese, 2007; 2010; Creel & Crabtree, 1999). In such cases, Coyotes likely do not perceive Gray Wolves as a threat requiring generalized spatial avoidance; rather, the threat of

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Lethal interpredator interactions also vary between species and localities. Upward of 65% of Kit Fox mortalities can be caused by Coyotes and > 50% of their carcases can be fed upon (Ralls & White, 1995; Cypher & Spencer, 1998). Disney and Spiegel (1992) also found Domestic Dogs and Bobcats (Lynx rufus) were major predators of Kit Foxes but rarely ate them. Conversely, in a Canadian study, no Swift Foxes (V. Velox) and Kit Foxes were killed by Coyotes (Moehrenschlager et al., 2007). Variations in canid home range size associated with prey density and ecosystem productivity could affect the probability of intraguild predator encounters (Moehrenschlager et al., 2007).

The social behaviour of predators also appears to be important in interguild relationships, with social carnivores killing larger species than solitary ones (Palomares & Caro 1999). This might explain why Dholes, which although usually communal hunters often hunt solitarily for small prey (Cohen, 1977), can live sympatrically with Tigers (Panthera tigris) and Leopards (Durbin et al., 2008). Ecological similarities and taxonomic relatedness also increase the probability of lethal interactions (Donadio & Buskirk 2006): the Asian distributional separation of Dholes and Gray Wolves could be caused by either or both behaviour and phylogenetic relatedness.

Intraguild predation and killing can be avoided through isolation mechanisms that partition common resources and reduce niche overlap (Hardin, 1960; Schoener, 1974). The partitioningACCEPTED of resources and the use MANUSCRIPT of competition refuges, maximises habitat availability to multiple species, and help facilitate co-existence (Durant, 1998). Temporal partitioning might not decrease dietary overlap but could reduce agonistic interactions with the dominant competitor (Dekker, 1989; Tannerfeldt et al., 2002). Canid sympatry can be enabled by dietary (e.g. Arjo et al.,2002; Zapata et al., 2005), spatial (e.g. Johnson & Franklin, 1994), and temporal (e.g. Fuller et al., 1989) niche separation. Sympatric canids may use secondary predator avoidance strategies, such as tree climbing in Gray Foxes (Urocyon cinereoargenteus) (Cypher, 1993) and year- round den use (e.g. Swift Fox: Kilgore, 1969), in combination with other isolation mechanisms.

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4. Case studies: diets, roles, food web complexity, evidence and research needs

In this section, we use some case studies to illustrate the possible ecological roles of canids. These are: the Gray Wolf, the largest canid and a top-predator; a middle-sized predator that has undergone very recent taxonomic reassignment due to genetic studies (Eurasian Golden Jackal / African Golden Wolf: C. aureus/C. anthus); two of the smallest canids, the Fennec Fox (Vulpes zerda) and Sechuran Fox (Pseudalopex sechurae), and one of the predominately frugivorous canids, the Side-striped Jackal.

4.1 Gray Wolf, the largest top canid

Gray Wolves are one of the most extensively studied canids (e.g. Fox-Dobbs et al., 2007; Gude et al., 2012; Mech, 1995; Nelson & Mech, 2006; Vucetich et al., 2011) and are top predators (Ripple et al., 2014). They are usually hyper-carnivorous that rely on the vulnerability and availability of wild ungulates (Paquet & Carbyn, 2003) but can survive on a wide array of other foodstuffs including anthropogenically-derived food including livestock and garbage (Peterson & Ciucci, 2003; Newsome et al., 2016 In Press). Most literature (e.g. Laundré et al., 2001; Ripple et al., 2014; Peterson et al., 2014) assigns Gray Wolves to apex status, having only top-down and often regulatory impacts, but they can also be sustainable yield harvesters (e.g. Peterson et al., 2014) and are often part of a suite of sympatric top predators (e.g. with Cougars, Puma concolor, and bears).

As top predators, Gray Wolves could affect food webs by suppressing the abundance or by altering theACCEPTED dispersion and temporal MANUSCRIPT activity of their main prey, such as Elk (Cervas canadensis), and lower order competitors such as Coyotes. Where this occurs, indirect effects on stream morphology (Beschta & Ripple 2012), woody plants (Painter et al., 2014) and berry production (Ripple et al. 2014b) have been observed as well as for a suite of animals including medium-sized ungulates (e.g. White-tailed Deer, Odocoileus virginianus, and Pronghorn, Antilocapra americana: Berger et al., 2008), small mammals (Miller et al., 2012), Beavers (Castor canadensis: Smith & Tyers 2012), songbirds (Baril et al., 2011), and Grizzly Bears (Ursus arctos: Ripple et al., 2014b). Alternatively, some authors (e.g. Creel & Christianson,2009; Kauffman et al.,2010;

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Marshall et al., 2013) suggest that these observations of reintroduced Gray Wolves could be explained by bottom-up processes.

Wolves also provide carcases for scavengers to feed on (Wilmers & Getz, 2005), which could facilitate co-existence with and between other carnivores (Paquet, 1992). For example, carcases provided by Gray Wolves have been associated with increased coyote litter size and pup survival (Crabtree & Sheldon 1999). The carcasses are also food for decomposing insects and microorganisms, adding a variety of nutrients such as carbon, nitrogen and calcium to the soil (Doughty et al., 2013; Melis et al., 2007).

The extent to which Gray Wolves can suppress or alter the foraging behaviour of their ungulate prey is also the subject of debate (e.g. Peterson et al., 2014; Muhly et al., 2013; Winnie 2012). A key issue is determining the relative importance of all the factors that could potentially influence ungulate abundance and behaviour. A recent study concluded that juvenile Elk recruitment declined by 35% in the presence of Gray Wolves, and that predation could explain about half of the observed declines in Elk counts in areas where Gray Wolves were reintroduced in southwestern Montana and northwestern Wyoming, U.S.A. (Christianson & Creel, 2014). Several other studies (e.g. Eberhardt et al., 2007; Evans et al., 2006; Wright et al., 2006) support that conclusion, but drought, recreational harvests and predation by Grizzly Bears and Cougars were sometimes responsible for more Elk mortality than Gray Wolves in Yellowstone National Park (Peterson et al., 2014; Middleton et al., 2013). This suggests that it is necessary to considerACCEPTED the relative importance MANUSCRIPT of predation rates by multiple carnivores, as well as other external factors, when assessing the causes of ungulate population fluctuations.

Gray Wolves can suppress lower-order competitors such as Coyotes: Prugh et al. (2009) and Ripple et al. (2013) argue that the range expansion of Coyotes in North America into areas where Gray Wolves were extirpated by humans is one of the best examples of mammalian mesopredator release. As evidence of this process, Coyote populations naïve to the presence of Wolves, after their 70 year absence from the Greater Yellowstone Environment, suffered >50% declines following Gray Wolf reintroduction in 1996 (Crabtree & Sheldon, 1999; Peterson et al., 2014). However,

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Coyotes remain the most numerous predators in the Greater Yellowstone Environment (Arjo et al., 2002; Atwood & Gese, 2010) and Berger and Gese (2007) ascribe human alteration of landscapes through agriculture, logging, livestock grazing, and development as a more parsimonious explanation for the increase in Coyotes’ North American distribution.

The complexity of relationships among canids is highlighted by studies showing that Gray Wolves might benefit Red Foxes by suppressing Coyotes (Levi &Wilmers, 2012; Newsome & Ripple, 2015). That Gray Wolves kill Coyotes (Carbyn, 1982; Merkle et al., 2009; Stenlund, 1955) and, less so, Red Foxes at local scales (Mech, 1966; Peterson, 1977; Stenlund, 1955), and inverse correlations between the densities of both Gray Wolves and Coyotes (Berger & Gese, 2007), and of Coyotes and Red Foxes (Fedriani et al., 2000; Levi & Wilmers, 2012), support the contention of indirect effects of Gray Wolves suppressing Coyotes. Spatial and temporal separation among the three predators also occurs (Arjo & Pletscher, 1999; Gosselink et al., 2003; Sargeant et al., 1987), which could be a response to top-down suppression or explain how co- occurrence and facilitation is enabled.

It remains unresolved whether reintroduced or recolonising Gray Wolves can suppress overabundant mesopredator and large herbivore populations over large areas in North America and Europe, especially in human-modified systems (Bergerud et al., 2007; Ripple et al., 2014a; Peterson et al., 2014). Top-down control exerted by Gray Wolves might not be theACCEPTED same in all ecosystems (ElmhagenMANUSCRIPT & Rushton, 2007). Anthropogenic habitat changes could moderate top-down forces from Gray Wolves (Muhly et al., 2009; Muhly et al., 2011) such that they perform different ecological functions in human-modified systems than in National Parks, where the majority of studies have been undertaken (Mech, 2012). Ultimately, though, the impact of top predators on middle-ranked predators and herbivores will likely depend on their relative densities and absolute densities of top predators and all herbivores (Bergerud et al., 2007; Hervieux et al., 2014). A greater understanding of what those densities are and interactive population dynamics are therefore required.

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4.2 A middle-sized canid undergoing taxonomic review, the Golden Jackal

The Golden Jackal is a medium-sized canid with a wide distribution, occurring in northern and eastern Africa, across Asia Minor, Middle East, and Caucasus to the west, Thailand to the East and south-eastern Europe (Table 1; Ćirović et al., 2014).

The Golden Jackal is an opportunistic generalist that exploits a broad spectrum of food items (Macdonald, 1979; Yom-Tov et al., 1995). Golden Jackals often live around human habitations and garbage dumps (Macdonald, 1979; Giannatos et al., 2005; Rotem et al., 2011) and consequently their diet often tracks human-influenced seasonal events. Large game species were present in stomach contents during restricted hunting seasons (Bošković et al., 2013; Lanszki et al., 2015), livestock becomes more prevalent during slaughtering seasons in rural households (Bošković et al., 2013), and the occurrence of plant materials increases during harvest and periods of ripened fruits (Bošković et al., 2013). In the absence of anthropogenic resource subsidies, major food items are principally small mammals, largely voles (Cricetidae spp.), and Wild Boar (Sus scrofa) piglets. Birds, snakes, lizards, fish, invertebrates and plant materials are also eaten, but rarely (Lanszki et al., 2006). There is no seasonality in natural diet (Lanszki & Heltai, 2002) except that during cub dependency, waterfowl become important (Lanszki et al., 2009) and there is an increase in the consumption, and importance of, anthropogenic resources during winter months (Ćirović et al., 2014, Hayward et al. 2017).

A dietary nicheACCEPTED overlap exists between the MANUSCRIPT Golden Jackal and Red Fox (Lanszki et al., 2006), the most common sympatric competitor (Giannatos et al., 2005; Scheinin et al., 2006). Gray Wolves are also sympatric, but less numerous across their shared range (Yumnam et al., 2015). The broad Golden Jackal diet supports the hypothesis that, in addition to possible top-down pressures from Gray Wolves, increases in food abundance (bottom-up pressures) likely determine Golden Jackal densities (Macdonald, 1979; Elmhagen & Rushton 2007). Habitat generalism and flexibility in diet and social structure are facilitating the expansion of Golden Jackals across Europe and Asia (Macdonald, 1979; Brooks et al., 1993; Arnold et al., 2012). We could find no experiments to determine density dependence (top-down or bottom-up) nor regulation of the mesopredator by the Gray Wolf on Golden Jackals, but the historic 21

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs anthropogenic extirpation of Gray Wolves across Europe and Asia likely assisted Golden Jackal range expansion.

It has recently been suggested that the Golden Jackal be reclassified into two species differentiated by both genetics and distribution (Rueness et al., 2011). The northern component, named the Eurasian Golden Jackal, is restricted to Eurasia while the newly recognised African Golden Wolf is restricted to northern Africa (Koepfli et al., 2015). Although the genetic ancestries of these two species reveal their distinctiveness, they have strikingly similar morphologies, including cranio-dental anatomy, and body size (Koepfli et al., 2015). Koepfli et al. (2015) suggest that natural selection has driven the parallel evolution of the two species, but speciation due to geographical separation is also plausible. Taking this logic one step further, we suggest that the similarities between these species may also relate to similarities in niches. The majority of the literature on Golden Jackal diets is from Europe and Asia so potentially reflects the diet of Eurasian Golden Jackals but not the African Golden Wolf. Hybridisation between the Eurasian Golden Jackal and the African Golden Wolf has been recorded in Israel (Koepfli et al., 2015), demonstrating the two populations do overlap. Eurasian Golden Jackals in Israel also show signs of hybridisation with Domestic Dogs and Gray Wolves (Koepfli et al., 2015). The Eurasian Golden Jackal and African Golden Wolf are classical mesopredators, but their roles in their respective ecosystems require further study.

4.3 Analogous small canids from two continents, the Fennec and Sechuran foxes Very little is knownACCEPTED about the feeding ecology MANUSCRIPT of the smallest canid, the Fennec Fox (Table 1), but they appear to be generalist omnivores (Gauthier-Pilters, 1962; Stevens & Hume, 1995). Native to the arid desert regions of northern Africa and the Sinai Peninsula, their diet includes small rodents, birds, small reptiles, insects and plant matter (Gauthier-Pilters, 1962). Fennec Foxes are nocturnal or crepuscular (Gauthier- Pilters, 1962; Ortolani & Caro, 1996) and can take animals larger than themselves, such as rabbits (Gauthier-Pilters, 1962). There is very little dietary information on wild-living Fennecs; however, the morphology of their digestive system is similar to that of other carnivores (Stevens & Hume, 2004). They are likely basal or mesopredators, when in sympatry with larger canids, but their specialisation for sandy desert habitats (Saleh &

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Basuony, 1998) means that they are often the largest canid present, and could then be top predators.

The small desert Sechuran Fox of South America (Table 1) has a similar ecology to its African analogue, the Fennec Fox, including year-round denning and nocturnal activity patterns (Asa & Wallace 1990). Asa and Wallace (1990) examined scats of Sechuran Foxes before and after an El Niño event. Before El Niño the fox scats contained >99% seed and seed pods (by weight) and <1% beetles, lizards, birds and crabs (Decapoda). The inclusion of shorebirds and Humboldt Penguins (Spheniscus humboldti) led the authors to conclude they may have been consumed as carrion. After the El Niño event the diet changed to grasshoppers (Acrididae: 42%), seed pods (39%) and mice (Phyllotis gerbillus : 20%) (Asa & Wallace, 1990). In other regions of Peru, primary food items include fruit of wild papaya (Carica candicans), Muridae, insects, and scorpions (Cossíos, 2010). Other anthropogenic food sources include goats (Capra hircus), poultry, rodents of the family Caviidae, eggs and cultivated vegetables (Aguilar et al., 1977; Landeo Sanchez, 1992; Cossíos Meza, 2004). Sechuran Foxes are also likely important as seed dispersers (Cossíos, 2005).

These two small species are little studied and their roles and interguild interactions in their respective continents require further study. Similarly, the strength and direction of interactions within their food webs are undetermined.

4.4 Omnivore or Frugivore?: the Side-striped Jackal

The Side-stripedACCEPTED Jackal is a middle-sized , generalistMANUSCRIPT omnivorore (Table 1), occupying a wide range of habitats in the mesic areas of Africa, particularly fruit-rich grasslands (Atkinson et al., 2002). It has strong ecological similarities to the Red Fox; the diet varies seasonally (Loveridge & Macdonald, 2003), tracking the abundance of fruit species rather than the abundance of small mammals (Atkinson et al., 2002). Its diet is broad, including small to medium sized mammals (e.g. Rodentia: Muroidea, Pedetidae; Lagomorpha and young ungulates), birds and birds’ eggs, fruit, invertebrates such as insects, carrion, plant matter and human refuse (Stuart & Stuart, 2001; Atkinson, et al. 2002; Kingdon et al., 2013). When sympatric with other jackal species, Side-striped

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Jackals often shift their range to include more densely vegetated habitats (e.g. Pienaar, 1969; Fuller et al., 1989; Kingdon et al., 2013).

The importance of anthropogenic resources to the Side-striped Jackal can be inferred from data on rabies transmission. From 1950–1996, 89% of rabies cases in the Side- striped Jackal occurred in commercial farmland (Bingham et al., 1999) where jackal densities were high enough to allow disease outbreaks: conversely, jackal rabies is very rare outside of farming lands (Bingham et al., 1999; Butler et al., 2004). However, there is little evidence that Side-striped Jackals prey upon livestock (Van der Merwe, 1953; Loveridge & Macdonald, 2003). Based on the size of prey species, most ungulates found in Side-striped Jackal scats were probably scavenged rather than hunted, particularly as this species does not generally hunt co-operatively (Loveridge & Macdonald, 2003).

The Side-striped Jackal is sympatric with other nocturnal predators including canids, mustelids, viverrids, felids and owls (e.g. Atkinson et al., 2002) and hyaenas (Butler et al., 2004), most of which potentially compete for food but probably do not prey upon Jackals. Dietary overlap between sympatric Side-striped Jackal and the Black-backed Jackal varies seasonally, with the greatest overlap in diet occurring in the hot dry season (Loveridge & Macdonald, 2003). However, niche overlap remains relatively high even when resources are abundant (Loveridge & Macdonald, 2003). There is some evidence to suggest exclusion of the Side-striped Jackal by the larger Black-backed Jackal. LoveridgeACCEPTED and Macdonald (2003) foundMANUSCRIPT a greater biomass of Springhares (Pedetes capensis) in Black-backed Jackal scats than in those of Side-striped Jackals. Likewise, the territories of open grasslands preferred by the hares are more aggressively defended by Black-backed Jackal than the neighbouring woodlands. Side- striped Jackals fit below hyaenas, Ethiopian Wolves and African Wild Dogs, but would be higher on a trophic pyramid than potentially sympatric smaller canids (Table 2).

5. Anthropogenically influenced canids

Humans have advertently and inadvertently changed the distribution and abundance of some members of the Canidae. Some species have benefited from anthropogenic movements and supplementations, whereas others have suffered drastic declines and 24

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs are listed on the IUCN Red list as species at risk of extinction, yet most canids fall into the least concern category (Table 1).

The expansion of some canids both within their native distributions and abroad is often facilitated by direct and indirect human actions. An example of direct action is purposeful release, either for sport hunting, e.g. Coyotes (Hill et al., 1987) and Red Foxes (Abbott, 2011), or for the fur trade, e.g. Raccoon Dogs (Nyctereutes procyonoides: Nowak, 1984) and Arctic Foxes (Alopex lagopus: Ashbrook & Walker, 1925). Indirect actions include: the release of invasive herbivores that are then exploited as prey, e.g. European Rabbit (Oryctolagus cuniculus) facilitating Culpeos (Rubio et al., 2013), European Rabbits benefiting free-ranging Domestic Dogs and Red Foxes in Australia (Jarman, 1986; Marsack & Campbell, 1990) and European Brown Hare (Lepus capensis) possibly increasing Chilla (Pseudalopex griseus) abundance (Johnson& Franklin, 1994); expansion of agriculture (e.g. Coyotes northward expansion), both from direct predation on livestock, e.g. African Wild Dogs (Woodroffe et al., 2005); and less obvious effects such as increases in herbivore abundance and distribution in response to greater permanency and wider distribution of water (Allen & West, 2013; Fleming & Ballard, 2015), predation on dung beetles by Hoary Foxes (Pseudalopex vetulus)(Courtenay et al., 2006), urbanisation, e.g. Golden Jackals (Macdonald, 1979), Red Foxes (Bino et al., 2010; Baker & Harris, 2007), and extirpation of top predators (Roemer et al., 2009; Estes et al., 2011).

Conversely, humansACCEPTED have negatively impacted MANUSCRIPT upon many canid populations through one or a combination of habitat destruction, hunting, predation by Domestic Dogs, and facilitation of hybridisation and disease spread. The ICUN Red List currently has two species listed as critically endangered and four as endangered due to these factors (Table 1). Further, humans were a causal factor in the only modern extinction of a canid, the Falkland Islands Wolf (Dusicyon australis)(Austin et al., 2013). Here we list six case studies, three being species that have benefited from anthropogenic influence and three that are examples of three levels of endangerment from the five IUCN categories.

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5.1 Invasive canids: responding positively to people

As opportunistic predators, canids frequently take advantage of human-provided foods when available: Newsome et al. (2014) found that, across the globe, canids consume crops, garbage (waste), and livestock (including carcasses) at relatively high proportions (Figure 1). Of all the terrestrial mammalian predators >1kg bodyweight, canids of all categories (top–basal predators and domesticates) are the most frequently documented group that accesses human-provided foods (Figure 1). When canids utilise human-provided foods, it can alter their abundance and dietary ecology. For example, Fedriani et al. (2001) found an eight-fold increase in Coyote densities in areas where use of human-provided foods was greatest. For species such as Golden Jackals in Israel (Macdonald, 1979) and Iberian Wolves (Canis lupus signatus) in north Portugal (Vos, 2000), > 90% of the diet can comprise anthropogenically-sourced foods. Human-provided foods are often utilised when wild prey are depleted. For instance, in central Iran where there is low abundance of wild prey, Gray Wolves fed almost exclusively on farmed chicken, domestic goats and garbage (Tourani et al., 2014). Prey switching to domestic species by Gray Wolves has also been demonstrated in Belarus, where a six-fold increase in livestock consumption was recorded when wild ungulate densities were at a low level (Sidorovich et al., 2003). Use of human-provided foods can also directly alter canid life history and sociality, with studies showing changes to group sizes (Newsome et al., 2013) and home-ranges (Hidalgo-Mihart et al., 2004), and increased tolerance of conspecifics (Shivik et al., 1996). Free-roaming Domestic Dogs are often keptACCEPTED for security, especially during MANUSCRIPT the night, in rural India (Pal, 1999) and industrial sites in Singapore and Malaysia, and their foraging on refuse is often regarded as a service.

Given that many canids have adaptable foraging strategies and flexible social systems, their documented use of human-provided foods is not surprising. However, there are broader implications to consider with respect to the ecological relationship between canids, humans and their environment. Specifically, co-occurring species can be affected when canids utilise human-provided foods, especially if canid densities increase and predation pressure leads to lower abundances of prey (Shapira et al., 2008) or outcompeting of other scavengers (Butler & du Toit, 2002). Conversely,

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5.1.1 Domestic Dogs; made and spread by humans

Domestic Dogs were likely the first taxon derived by domestication and now their global population, excluding free-roaming Australian dingoes, Indian pariah dogs, New Guinea singing dogs, other native dogs and hybrids, has been estimated at >700 million (Hughes & Macdonald, 2013). They are distributed across all areas where there is human habitation and the ancient breeds have a broader range, including most of Australia (Fleming et al., 2014). Domestic Dogs are considered to be one of the four most pervasive and damaging invasive vertebrate species globally (Doherty et al. 2016). Despite this and an association with humans that is > 10,000–12,000 years old (Fox & Bekoff, 1975), and possibly much longer (27,000 – 40,000 years: Skoglund et al., 2015), the ecology of free-ranging Domestic Dogs in many parts of the world is poorly understood (Gompper, 2014).

Free-ranging Domestic Dogs occur in many urban, agricultural and wild areas throughout the world and are the most widely distributed of the Canidae (Table 1; Gompper, 2014). They include ancient Domestic Dog breeds such as the Australian dingo, the NewACCEPTED Guinea singing dog, the IndianMANUSCRIPT pariah dog and the basenji, all of which have wild populations and are often deemed native (e.g. the Indian pariah dog is usually referred to as “Indian Native Dog” in India, Pal 1999) or legislated native (e.g. Australian dingoes under the Australia Government Environmental Protection and Biodiversity Act 1999). Free-roaming Domestic Dogs often occur at high densities, particularly when reliant on human subsidised food resources (Butler et al. 2004; Newsome et al. 2014; Vanak & Gompper 2009).

Although ubiquitous, here we concentrate on free-ranging Domestic Dogs in India and Australia, which have abundant and widespread populations of them (Fleming et al., 2014; Pal, 1999; 2008; West, 2008). The Indian pariah dog is sometimes referred to as 27

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Nedi Kukur, Deshi Kukur, and Deshi Kutta on the Indian sub-continent. Dingoes are similarly referred to by many indigenous names (e.g. Warrigal and Tingo; Tench, 1793: Wingkiwarnu; Reece, 1986), few of which are known by most Australians. Like other primitive Domestic Dogs, Indian pariah dogs are medium-sized canids, commonly have yellow to rust-coloured coats, are very social and territorial, and often associate with human habitation (Bonanni et al., 2010; Fox et al., 1975; Pal, 2003: 2008).

Since its introduction to Australia from South East Asia about 4,500 years ago (Corbett, 2001; Oskarsson et al. 2012; Savolainen et al., 2004), the dingo has adapted to a wide range of environments, from alpine south-eastern Australia to the hottest and driest parts of central Australia (Corbett, 2001; Fleming et al., 2001; 2014). The Australian dingo is a classic feralised domesticate of long standing that has adapted and re- adapted to different human- dominated landscapes, particularly in the recent past (e.g. Allen et al., 2016; Newsome et al., 2014). Primitive Domestic Dog breeds like the Australian dingo and Indian pariah dog have a single and seasonal annual oestrus (Jones & Stevens, 1988; Thomson, 1992; Pal et al., 1998). The Australian dingo has hybridised with other breeds of Domestic Dog introduced since 1788, and most (>90%) of the population in south-eastern Australia is hybrid (Stephens et al., 2015; 2016). Although many Domestic Dogs of similar size have two oestrus cycles, the hybrids appear to only have one oestrus (Jones & Stevens 1988).

The Australian dingo is one of the few canids to have network-style models of trophic interactions amongACCEPTED predators and herbivores MANUSCRIPT fitted (Colman et al., 2014; Hunter et al., 2015). In these papers, the strength and direction of interactions between dingoes, Red Foxes, feral Domestic Cats and prey were modelled using structural equation models. Modelling indicated that lethal control of dingoes induced trophic cascades, consistent with the mesopredator release hypothesis. While conceptually progressive, some of the top-down interactions were unidirectional by way of assumption, rather than by experimentation, or lethal control of Australian dingoes was assumed to be complete (e.g. Hunter et al., 2015), an effect size that has not been demonstrated (Fleming 1996; Thomson 1992; Fleming et al., 2014) and is improbable (Bomford and O’Brien 1995). Bottom-up forces White, 2013), which have been shown to affect interactions among Australian dingoes, Red Foxes and feral Domestic Cats in Australian 28

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs resource-pulse environments (Allen, 2015a;b) and mixed top-down/ bottom-up models (e.g. Greenville et al., 2014), provide alternative explanations of equal merit.

The roles of free-ranging Domestic Dogs in human-dominated ecosystems are variable. In some urban and rural ecosystems in India, Indian pariah dogs play a positive role. In almost all the towns of West Bengal, the municipal sanitation arrangement is gradually developing but people living in the slum areas defecate on open ground. Likewise, it is common for children under ten years of age and belonging to the lower castes to defecate beside open drains. In these areas, free-ranging Domestic Dogs consume most of the faeces as food, thereby reducing disease risk to humans (Pal 1999).

When allowed to wander, owned Domestic Dogs sometimes harass and kill wildlife (Meek, 1999; Daniels & Kirkpatrick, 2011; Hughes & Macdonald, 2013: Plate 1). Free- ranging Domestic Dogs have been observed chasing and killing wildlife, including Mongolian Saiga (Saiga tatarica mongolica), Pudu (Pudu pudu), Coati (Nasua nasua) (Campos et al., 2007; Silva-Rodriguez et al., 2010a; 2010b; Young et al., 2011), possums (Phalangeridae), macropods (Macropodidae: Meek, 1999; Daniels & Kirkpatrick, 2011: Plate 1), and sympatric canids, the Gray Fox and Darwin’s Fox (Pseudalopex fulvipes; Jiminez et al. 2004), and Red Foxes (Moseby et al., 2012). The consequences of those interactions for native prey populations (e.g. Koler-Matznick et al. 2007; Allen et al. 2014) require further study.

Insert Plate 1 hereabouts ACCEPTED MANUSCRIPT The ecological niche of free-ranging Domestic Dogs may overlap with native canids and other predators, creating potential competition for resources (Young et al., 2011). This is particularly relevant for threatened species in Australia such as the Spotted-tail Quoll (Dasyurus maculatus), where high dietary niche overlap has been observed (Glen & Dickman, 2008; Myer-Gleaves, 2008). In some circumstances, free-ranging Domestic Dogs, including Australian dingoes, could benefit native wildlife, particularly critical weight range prey species (500g–5,000g liveweight: Burbidge & McKenzie, 1989), through suppression of other introduced mesopredators such as the Red Fox and feral Domestic Cat (Glen et al., 2011; Krauze-Gryz et al., 2012; Wang & Fisher, 2012). However, the experimental evidence for these potential benefits for native wildlife and 29

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs a causal relationship between dingoes and the abundance of associated mesopredators has not been demonstrated (Fleming et al. 2012; Allen et al. 2013a; Allen 2015b) or has been shown to be absent (e.g. between arid- zone dingoes and feral Domestic Cats: Allen et al. 2015; Allen 2015b). Large-scale manipulative experiments are required to quantify the strength and direction of trophic interactions between free-roaming Domestic Dogs and co-occurring larger and smaller predators (Allen et al. 2017), particularly in Australia (Ritchie et al. 2012; Allen et al. 2014; Newsome et al. 2015a).

In some ecosystems, free-ranging Domestic Dogs are prey for larger carnivores, with possible benefit for local wildlife populations (Hughes & Macdonald, 2013). In north- west Zimbabwe, Butler et al. (2004) found more than 6% of a Domestic Dog population was removed by predation from Leopards, Lions (P. leo) and Spotted Hyaenas. Similarly, Coyotes were reported to attack pet dogs in Tucson, USA (Grinder & Krausman, 1998). However, these negative interactions can increase human-wildlife conflict, which may be detrimental to conservation efforts for wild canids and other predators.

Free-ranging Domestic Dogs can act upon food webs indirectly as reservoirs for pathogens (Butler et al., 2004; Jackson, 2003; Woodroffe et al., 2012), which can affect population dynamics and trophic interactions (e.g. Barnes et al., 2008; Jenkins et al., 2008; Otranto et al., 2015). These pathogens include ectoparasites (e.g. fleas, lice, mites and ticksACCEPTED: Corbett, 2001), endoparasitic MANUSCRIPT worms that can affect fitness and susceptibility of individual prey to predation (Barnes et al., 2008; Jenkins et al., 2008), protozoans affecting ungulates (e.g. neosporosis, causative agent Neospora caninum: King et al., 2010), bacteria, fungus and viruses (including canine distemper, canine parvovirus and rabies, which affect wild canid populations). The population effects that the above pathogens and parasites have on free-ranging Domestic Dogs or their prey require quantification.

Spill-over of diseases from Domestic Dogs to wildlife populations can pose significant conservation challenges (e.g. Barnes et al., 2008). Domestic Dogs in Africa were thought to be the reservoirs for the rabies and canine distemper viruses, which

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ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs resulted in substantial declines of Lions, Ethiopian Wolves and African Wild Dog populations (Cleaveland et al., 2000; Prager et al., 2012; Randall et al., 2006). Although canine rabies is a potential threat to the Dhole (Durbin et al., 2004), the impacts of rabies among Indian pariah dogs on Indian wildlife, including sympatric canids, are yet to be fully investigated. While affecting prey and sympatric predator populations, some of Domestic Dog-borne pathogens also cause zoonoses, e.g. hydatidosis, causative agents Echinococcus granulosus (Jenkins & Morris, 2003; Jenkins et al., 2008) and E. multilocularis (Jenkins et al., 2005; Raoul et al., 2015), and rabies, which annually accounts for 50,000 human deaths globally (Tenzin & Ward, 2012) and is a major cause of dog-related human mortality in India (Pal, 1999). In India, apart from rabies, the most serious hazards to humans from free-ranging Domestic Dogs are bites and infections from their skin, faeces and urine, including 65 recorded zoonoses (including viruses, bacteria, fungi, protozoa, nematoda, cestoda and arthropods: Pal 1999).

5.1.2 Coyotes: anthropogenic range expansion without introduction

Predation by Coyotes can have detrimental effects on a wide range of fauna, including mammals, birds and reptiles (Ripple et al., 2013), and Coyote abundance is limited by Gray Wolves, likely through negative interactions between Wolves and dispersing or transient Coyotes (Berger & Gese, 2007). Coyotes were historically mostly located in central United States of America (Gompper, 2002), but by the early 1900’s they expanded theirACCEPTED distribution to as far north MANUSCRIPT as Alaska (Peterson, 1995). Coyotes also dispersed as far east as Nova Scotia by the 1980’s and they are now ubiquitous throughout north-eastern North America, with dramatic increases in the number of sightings in urban areas such as New York since the 1940’s (Fener et al., 2005) and Chicago since the 1990’s (Gehrt et al., 2011). Several reasons for this dramatic range expansion have been proposed including the eradication of the Gray Wolf (see above), and logging and agricultural development which changed landscapes and opened additional habitat to Coyotes and prey species such as White-tailed Deer (Gompper, 2002).

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The rapidity with which Coyotes dispersed and their ability to thrive in urban regions highlights the opportunistic and flexible nature of the species’ ecology. Indeed, Coyotes are one of the few mammalian carnivores that occur in urban areas, and they have been described as behaviourally misanthropic and demographically synanthropic because they display strong spatial and temporal avoidance of people, but have elevated survival, density and possibly reproduction in urban areas (Gehrt et al., 2011). As Coyotes continue to expand into urban areas, more research will be needed in order to predict their ecological impacts in peri-urban and urban environments.

As a mid-sized predator, Coyotes have a diverse diet so they are potential competitors with, and predators of, other species. Indeed, the observed release of feral Domestic Cats from the suppressive effect of Coyotes and subsequent decline in bird abundance was the source of mesopredator release hypothesis for terrestrial systems (Crooks & Soulé 1999). Levi and Wilmers (2012) and Newsome and Ripple (2015) suggest that Coyotes could limit other introduced carnivores in North America, such as the Red Fox by interference competition and/or intraguild predation. In such cases, a resultant cascade of ecosystem effects could occur, although such studies are currently unavailable in north-eastern North America. Coyotes might also perform ecosystem services in suburban and urban areas by suppressing feral Domestic Cat populations and possibly other small carnivores that would otherwise be at high densities because of anthropogenic food subsidies (Ripple et al., 2013), but this idea requires testing. However, in the absence of wolves, Coyotes can exert intense predation pressure on their typical preyACCEPTED including threatened rodents, MANUSCRIPT ungulates, carnivores, leporids, and birds (Ripple et al., 2013), although the relationship between density and kill-rates and hence the functional responses of the systems require quantification for inclusion in network and other models.

5.1.3 European Red Fox, ubiquitous invader

The Red Fox is predominantly a solitary, opportunistic predator and scavenger (Saunders et al., 2010). It is the world’s most widely distributed canid, other than the Domestic Dog, and an archetypal generalist mesopredator. At least 34 subspecies have been recognised, inhabiting environments ranging from alpine and arctic tundra to

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ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs deserts and cities (Larivière & Pasitschniak-Arts 1996). The use of such a wide range of biomes requires a high degree of adaptability and ecological flexibility. These are provided by a suite of morphological, reproductive and behavioural traits that facilitate efficient temperature regulation, an extremely broad dietary range and a high tolerance for persecution (Devenish-Nelson et al., 2012; Larivière & Pasitschniak-Arts, 1996).

The Red Fox occurs in Pleistecene (10,000 to 1 MYa) fossil records in Europe (Zeuner, 1963) and its natural distribution is throughout Europe, North America and Eurasia. Much of the species’ current distribution can be attributed to human-assisted dispersal, usually for fur harvesting or recreational hunting (Long, 2003; Saunders et al., 2010). Where it has been introduced (e.g. Australia and North America), it has had a devastating effect on biodiversity and agriculture, and has been implicated in widespread mammal declines and extinctions (Burbidge & McKenzie, 1989; Lewis et al., 1999; Saunders et al., 2010). Likewise, in its putative native range the Red Fox is implicated in agricultural damage (Moberly et al., 2004) and bird predation (Seymour et al., 2003). Interference competition from, or predation by, Red Foxes could be limiting factors on populations of smaller predators, such as the Arctic Fox and Pine Marten (Martes martes), although other factors, including abiotic bottom-up forces, may be more important (Elmhagen & Rushton, 2007; Linnell et al., 1999).

Red Fox dietary samples are typically dominated by small, terrestrial vertebrates, such as rodents, lagomorphs,ACCEPTED sciurids and ground MANUSCRIPT nesting birds (e.g. White et al., 2006; Helldin & Danielsson, 2007) that can be hunted and killed by a solitary predator. There are many examples of Red Foxes suppressing prey populations, within both their native and introduced ranges (e.g. Banks et al., 2000; Harding et al., 2001; Jarnemo & Liberg, 2005). However, Red Foxes occur in such a wide range of communities that it is difficult to make generalisations, even with apparently simple two-species relationships. For example, in Australia, introduced Red Foxes can suppress European Rabbit populations that have been depleted by disease or drought (Newsome et al., 1989; Pech et al., 1992), but they are generally unable to prevent rapid population recovery when conditions improve (Pech et al., 1992; Norbury & Jones, 2015). They might also have become ‘super predators’ because the presence of European Rabbits 33

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs has artificially elevated and maintained Red Fox numbers (e.g. Cooke & Soriguer 2016), and thereby increased their impact on native fauna (i.e. ‘hyperpredation’: Williams et al., 1995; Smith & Quin, 1996; Jackson & Vernes, 2010).

Vegetation, invertebrates and carrion are also often important components of the Red Fox diet (e.g. Helldin & Danielsson, 2007). Opportunistic scavenging habits have pre- adapted foxes to exploit anthropogenic food sources such as refuse, garden produce, poultry and small ruminants. Thus, foxes can benefit from anthropogenic conversion of relatively homogeneous vegetation communities into fragmented, heterogeneous landscapes that provide a greater diversity of foraging and shelter opportunities (Panek & Bresiński, 2002; White et al., 2006). Rural, peri-urban and urban environments often support high Red Fox densities (e.g. Bino et al., 2010; Contesse et al., 2004; Panek & Bresiński, 2002).

Human land use change could further benefit foxes by reducing densities or activity of some higher order predators, either directly through deliberate persecution or indirectly by reducing habitat quality. A meta-analysis concluded that Red Fox populations across their native distribution, Eurasia, were limited by Eurasian Lynx (Lynx lynx); where Lynx were absent, Red Fox density appeared to be driven by bottom-up factors, being positively related to annual productivity, summer temperature and human density (Pasanen‐Mortensen et al., 2013). In North America, Coyotes can limit Red Fox populations (Harrison et al., 1989), with Red Fox populations appearing to haveACCEPTED benefited from the suppression MANUSCRIPT of Coyotes by Gray Wolves (Levi & Wilmers, 2012; Newsome & Ripple, 2015). Letnic et al. (2011; 2012) and others (e.g. Johnson et al. 2007; Colman et al., 2014; Hunter et al., 2015) identify human suppression of Australian dingo populations as a possible contributor to the establishment and spread of Red Fox populations in Australia, but the evidence to support this conclusion has been contested (see 5.1.1 above). In such cases, the Red Fox would be regulated by the top- and larger middle-order predators, conforming to mesopredator release mediated trophic cascade theory. Nonetheless, the value of Australian dingoes as Red Fox control agents remains unclear (Allen et al. 2013b) and is likely context specific (Haswell et al. 2016), and requires experimental investigation (Allen et al., 2014; Fleming et al., 2012; Newsome et al., 2015a). 34

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Alternatively, the distribution and abundance of introduced Red Foxes in Australia has been facilitated by absence of ecological equivalent mesopredators and by the presence of co-released food species (e.g. rabbits, sheep and goats) or extant equivalent or substitute prey, many of which were behaviourally unprepared for the incursion (e.g. Anson et al., 2015): the extant marsupial carnivores, quolls (Dasuyurus spp.), are all smaller than Red Foxes, which are smaller than Australian dingoes (Table 1). The range of Red Foxes in Australia approximately correlates with that of European Rabbits and their temporal spread throughout the continent from introductions in Geelong, Victoria, followed the spread of rabbits (Jarman, 1986; Coman 1999; Abbott 2011). Such roles are bottom-up and result in greater abundances than are evident in their native distributions.

The roles of the Red Fox in food webs are highly context-specific, and can be determined by a range of interacting top-down and bottom-up factors, often complicated by human intervention. Where foxes are the apex predator, typically where they have been introduced by humans, they can have profound effects on lower trophic levels. More commonly, Red Foxes occur as a mesopredator. Even then, their role is often complicated by the presence of higher- and lower-order predators including other canids, felids, mustelids, viverrids and dasyurids (Elmhagen & Rushton, 2007; Glen& Dickman, 2005).

5.2 Endangered canids: Canids responding negatively to people The IUCN red listACCEPTED categorises threatened MANUSCRIPTfauna into increasing risk of extinction. Canids and other carnivores are over-represented in the list, particularly the larger species that often come into conflict with humans, and are usually in lower abundance than those of least concern. We present examples of critically endangered, endangered and near threatened canids to demonstrate the lack of knowledge, not only of their roles but also of their basic biology, behaviour and ecology. They all require mensurative study, which will be difficult for the rarer species, conducted in conjunction with manipulative, experimental studies, most preferably with population additions, to determine their functional roles.

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5.2.1 Critically endangered Red Wolf

The Red Wolf was an important part of the culture of the Native Americans and appeared to have been sacred to at least some tribes (e.g. Panther-Yates, 2011). It was broadly distributed throughout south- eastern United States of America (Paradiso & Nowak, 1972) before its decline and extinction and its broad distribution suggests that they utilised a large suite of habitat types (Kelly et al., 2008). Red Wolves were believed to be major killers of livestock and were actively trapped and poisoned in campaigns that expanded in the early 1900s (Paradiso & Nowak, 1972). In Texas, about 12,600 Red Wolves were taken by State and Federal authorities between 1915 and 1939 and a further 419 wolves were trapped in Missouri between 1916 and 1939 (Young, 1940). In North Dakota, the decline has been due to Government poisoning drives against predators from as early as 1913 (Young, 1940). Other factors that could have contributed to its decline include habitat modification and endoparasites such as hookworm (unidentified nematode species) and heartworm (Dirofilaria immitis) and distemper (Paramyxovirus) (Paradiso & Nowak, 1972). Consequently, the Red Wolf population had dramatically declined by the early 1960s and was extinct in the wild by 1980. It was subsequently reintroduced into North Carolina in 1987 from captive populations (Kelly et al., 2004, 2008; Sillero-Zubiri, 2009).

The limited historic information suggests that Red Wolves were not a major predator of big game, especially in comparison with the Gray Wolf (Paradiso & Nowak, 1972). It appears they primarilyACCEPTED hunted smaller prey MANUSCRIPT including rabbits (Sylvilagus spp.), Coypu (Myocaster coypus) and small rodents including those of the genera Sigmodon, Oryzomys and Ondatra (Sillero-Zubiri, 2009), though other studies suggest that it preyed upon sub-adult domestic calves (Howell, 1921). In Alabama, records suggest that in 1912 Red Wolves were responsible livestock losses including sheep, goats and calves, making it difficult to raise these animals (Howell, 1921). Other studies suggested that Red Wolves hunted deer in the Carolinas and Wild Boar in Louisiana (Young, 1946). Since they have been reintroduced into North Carolina, their primary food items include White-tailed Deer, Northern Racoons (Procyon lotor) and rabbits (Sillero-Zubiri, 2009).

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5.2.2 African Wild Dog, endangered hypercarnivore

African Wild Dogs historically had a wide distribution throughout sub-Saharan Africa that included 34 countries, and excluding lowland rainforests and the driest deserts (Lindsey et al., 2004; Woodroffe et al., 2004). However, by the 1990s their distribution had dramatically contracted so that it was almost completely extinct in west Africa and greatly reduced in the rest of its range, being limited to isolated and highly fragmented populations (Fanshawe et al., 1997; Woodroffe et al., 2004a; Sillero-Zubiri, 2009). Now endangered, the largest populations occur in Botswana, Tanzania and Zimbabwe, which are estimated to contain approximately half the remaining wild population. Smaller populations can be found in the Central African Republic, Ethiopia, Kenya, Mozambique, Namibia, South Africa, Sudan and Zambia; while very small populations (with < 100 individuals) could exist in Cameroon, Chad, Senegal and Somalia (Sillero- Zubiri, 2009). In 2004, the estimated total population size was only 5750 individuals (Woodroffe et al., 2004a).

The main reasons for the dramatic decline in African Wild Dogs include possible competition with co-occurring top predators and intraguild predation, suppression through active hunting (Woodroffe et al., 2004b), resulting from conflict with the expanding human population, vehicle impacts and from disease (Woodroffe & Ginsberg, 1997; Ginsberg & Woodroffe, 1997). Diseases introduced from Domestic Dogs, including canine distemper, have caused great declines and endemic rabies has caused local extinctionACCEPTEDs of African Wild DogMANUSCRIPT packs (Creel et al., 1997; Sillero-Zubiri, 2009). The African Wild Dog hunts cooperatively in groups, usually packs, with as few as 3 individuals up to 20 or more adults. This foraging strategy allows them to successfully hunt small to medium-sized antelope that weigh 15–200 kg (average 50 kg: Creel & Creel 1995; Woodroffe & Sillero-Zubiri, 2012). Impala (Aepyceros melampus), Duikers (tribe Cephalophini), Common Wildebeest (Connochaetes taurinus), Thomson's Gazelle (Eudorcas thomsonii), Dik-dik (Madoqua spp.), warthogs (Phacochoerus spp.), Steenbok (Raphicerus campestris) and Greater Kudu (Tragelaphus strepsiceros) predominate in their diet. In addition, hares, reptiles such as lizards and eggs comprise

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ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs a relatively small component of the diet (Estes & Goddard, 1967; Woodroffe & Sillero- Zubiri, 2012). A minimum of 4-6 dogs is needed to hunt effectively as a group (Estes & Goddard 1967) and, as the number of adults in a group increases, the hunt success increases, the chase distance decreases and competition with the larger Spotted Hyaena decreases (Fanshawe & Fitzgibbon, 1993; Fuller & Kat, 1993; Creel & Creel, 1995).

5.2.3 Near threatened hypercarnivore, the Bush Dog

The Bush Dog (Speothos venaticus) is a near threatened canid from South America, impacted upon by habitat destruction, prey depletion from poaching, and diseases spread from Domestic Dogs (Zuercher et al., 2004). Although the Bush Dog is considered one of the four hypercarnivorous canids (Van Valkenburgh, 1991; Zuercher et al., 2005), their diets and foraging behaviours are little studied and reliant on few observational reports (e.g. Peres, 1991). Paca (Cuniculus paca) and Agoutis (Dasyprocta spp.) are likely preferred prey (Zuercher et al., 2005). Bush Dogs are highly social animals that hunt in groups of up to 12 individuals (mostly whole pack), which allows Bush Dogs to take Capybaras (Hydrochaeris hydrochaeris), Rheas (Rhea americana), and Brocket Deer (Mazama spp.) (Peres, 1991; Zuercher et al., 2005), suggesting that Bush Dogs are ecologically intermediate between large sympatric felids (Jaguar Panthera onca, Puma) and smaller mesopredators (Zuercher et al., 2005). Zuercher (2001) found no strong dietary overlap between Paraguayan Bush Dogs and any of the otherACCEPTED 15 sympatric mammalian MANUSCRIPT carnivores, indicating that competition is limited or unlikely and limiting the likelihood of top-down regulation or mesopredator suppression in these ecosystems.

6. Discussion and conclusions

Canids can be predators, prey or both. They can be regulators of their prey, limiters of their prey abundance, sustainable yield harvesters, beneficiaries or sufferers of human impacts or passengers in the system. They can be the glue that adheres the strands of a food web or they can be just part of the bigger picture.

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Humans aside (Fleming & Ballard, 2015; Gude et al., 2012; Lewis et al. 2017), three species (Gray Wolf, Red Wolf, and the mono-generic Dhole) are usually top predators (Mech, 2012; Estes et al., 2013; Newsome & Ripple, 2015; Ripple et al., 2014), two (free-ranging Domestic Dogs and African Wild Dogs) are facultative top or middle ranked predators depending on situation, eleven are either bottom or middle predators and the remainder are middle predators co-occurring with larger canids or other larger predators. The largest canid, the Gray Wolf, is always a top predator but may share that position with other large predators such as Cougars, Lynx and bears. Gray and Red Wolves are potentially keystone species in food webs if their omission or removal from the trophic structure cannot be substituted by a predator of similar role and subsequently web complexity declines through a trophic cascade (Estes et al., 2011; Winnie & Creel 2017). The Tibetan Fox and Ethiopian Wolf are likely examples of canid species in simple linear or reticulate food webs, but studies about the dynamics of their ecosystems are lacking.

There have been numerous studies of Red Foxes in native and exotic environments (e.g. Banks et al., 2000; Devenish-Nelson et al., 2013; Elmhagen et al., 2002; Saunders et al., 1995; 2010). Coyotes have also been subject to extensive study in relation to resource use and interactions with other canid species but often from an impact viewpoint (e.g. Arjo et al., 2002; Berger & Gese, 2007; Crabtree & Sheldon 1999). Ethological processes (e.g. temporal niche separation; Atwood & Gese 2010; Atwood et al. 2009; 2011: behavioural flexibility; Atwood & Gese, 2010: and facilitation among Gray Wolf andACCEPTED Coyotes; Switalski, 2003) canMANUSCRIPT mitigate risk of adverse interactions among sympatric canids of different trophic positions, e.g. Gray Wolves and Coyotes (Atwood & Gese, 2008; 2010), which reduces the likelihood of suppression of smaller species and hence top-down regulation.

There is much qualitative and correlative evidence, and theory supporting canid- dominated top-down systems (e.g. Estes et al., 2011; Letnic et al., 2009; Ritchie et al., 2012) but little modelling of interactions at trophic levels to support the theory (exceptions Choquenot & Forsyth, 2014; Colman et al., 2014; Greenville et al. 2014; Hunter et al., 2015). However, White (2013), Fleming et al. (2012; 2013) and Kaufmann et al. (2010) have argued that bottom-up systems are more likely, with the abundance 39

ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs of predators and their prey being ultimately food-limited, and in particular nitrogen- limited (White 1993). Observed regulation by predators (i.e. top-down processes) could be an artefact of an “over-run” of predators after the peak in a pulse of prey, which then exaggerates the food-limited decline/crash in prey populations, which conceal underlying bottom-up forces (White, 2013). In such bottom-up systems, all trophic functional roles will depend on abiotic limitations, such as soil structure and fertility, latitudinally and elevationally-determined temperature, daylight and rainfall patterns, biotic resource availability (food and water), structural complexity (cover and foraging spaces) and an allometry-constrained energy space (sensu Kelt & Van Vuren, 1999). The meta-analysis of Cusens et al. (2012) showed positive relationships between system productivity and species richness predominated across diverse animal taxa (primary productivity being abiotically constrained and predetermined), which also supports bottom-up driving of systems. If this assertion holds, then we should abandon attempts to find regulation by top canids and, assuming bottom-up drivers prevail, go about determining which of the bottom-up drivers are missing or suppressed in food webs at risk. Only then could recovery strategies for species and food webs be expected to be successful.

Here we have concentrated on canid species that are endangered, invasive or about which most is published. The roles of other canids are less well studied and described (Hayward et al. 2015; Allen et al. 2017; Meadows 2017), and for many species, basic biology and ecology are insufficiently quantified. Some canids, such as Australian dingoes and GrayACCEPTED Wolves, are subject to muchMANUSCRIPT controversy about their roles and impacts on agriculture, environment and humans (e.g. Allen et al., 2013c; Letnic et al., 2012; Newsome et al., 2015a; Ripple et al., 2013). The discourse is restricted because of a tendency for work to focus on individual predator species or simpler systems (as in Australia with only two canids; see Graphical abstract), or to be unidirectional in hypothesis setting. This latter trend, which fits data into theory rather than testing multiple hypotheses, is unfortunate because alternative functions and explanations are not countenanced or accommodated, which can lead to erroneous conclusions and management proposals.

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Few works, for example Colman et al. (2014; but see Allen, 2015a comment); and Hunter et al. (2015; but see Baker et al., 2016, and Fancourt & Mooney 2016, comments), have attempted what were effectively network analyses of the trophic roles of canids and then only for the comparatively simple Australian systems (see Graphical Abstract). Concerted research effort is required to measure and describe the food webs canids occupy and to understand canid function in those ecosystems (Allen et al. 2017; Haswell et al. 2017; Meadows et al. 2017). Interactions between predators co-occurring with canids also require further investigation (Winnie & Creel 2017), particularly in an experimental setting.

Quantification of connectance, links per species and degree distributions among canids, their trophic level confamilials and subordinates and prey are required to fit vectors to canid-topped networks and determine the strength of interrelationships. Importantly, we require measures of predation/ foraging rates, an essential parameter when determining functional responses that underlie the transfer of energy and nutrients from lower to higher trophic levels (Holling, 1959). These rates are difficult to measure, which could account for the paucity of such data. Therefore, we advocate both mensurative and experimental research for better understanding of the roles of Canidae in food webs and consequent better management strategies. This is particularly important for the conservation of endangered canids and the management of those that sometimes interact adversely with humans and their values.

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8. Tables & Figures

Table 1. Taxonomy, body size, distribution and IUCN conservation status of the Canidae (adapted from Sillero-Zubiri et al. 2004).

Canid Scientific name Common name Continental distribution Weight IUCN conservation No. (kg) status

1 Alopex lagopus Arctic Fox Europe, North America, Asia 3.6-4.2 Least concern

2 Atelocynus microtis Short-eared Dog South America 9.0-10.0 Near threatened

3 Canis adustus Side-striped Jackal Africa 7.3-12.0 Least concern

4* Canis anthus African Golden Wolf Africa 6.5-9.8 Least concern

ACCEPTED MANUSCRIPT 5* Canis aureus Eurasian Golden Jackal Europe, Asia 6.5-9.8 Least concern

6 Canis familiaris Domestic Dog (includes Ubiquitous 9-60 (푥̅≈ Least concern ancient , e.g. Australian 15.0) dingo and Indian pariah

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dog, and modern breeds, e.g. great Dane, collies and Chihuahua, and hybrids between them)

7 Canis latrans Coyote North America 7.7-15.8 Least concern (푥̅≈10.3)

8 Canis lupus Gray Wolf Europe, North America, Asia 36-60 Least concern

9 Canis mesomelas Black-backed Jackal Africa 5.9-12.0 Least concern

10 Canis rufus Red Wolf North America 22-34 Critically endangered

ACCEPTED MANUSCRIPT 11 Canis simensis Ethiopian Wolf Africa 11.2-19.3 Endangered

12 Cerdocyon thous Crab-eating Fox South America 4.5-8.5 Least concern

13 Chrysocyon brachyurus Maned Wolf South America 20.5-30 Near threatened

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14 Cuon alpinus Dhole Asia 10.0-13.0 Endangered

15 Lycaon pictus African Wild Dog Africa 21.0-34.5 Endangered

16 Nyctereutes Raccoon Dog Asia 2.9-12.4 Least concern procyonoides

17 Otocyon megalotis Bat-eared Fox Africa 3.4-4.9 Least concern

18 Pseudalopex culpaeus Culpeo South America 3.4-13.8 Least concern

19 Pseudalopex fulvipes Darwin's Fox South America 1.9-4.0 Critically endangered

20 Pseudalopex griseus Chilla ACCEPTEDSouth MANUSCRIPT America 2.5-5.0 Least concern

21 Pseudalopex Pampas Fox South America 4.0-8.0 Least concern gymnocercus

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22 Pseudalopex sechurae Sechuran Fox South America 2.6-4.2 Near threatened

23 Pseudalopex vetulus Hoary Fox South America 2.5-4.0 Least concern

24 Speothos venaticus Bush Dog South America 5.0-8.0 Near threatened

25 Urocyon Gray Fox North America, South 2.0-5.5 Least concern cinereoargenteus America

26 Urocyon littoralis Island Fox North America 1.4-2.5 Critically endangered

27 Vulpes bengalensis Indian Fox Asia 1.8-3.2 Least concern

28 Vulpes cana Blanford's FoxACCEPTED Africa, MANUSCRIPT Asia 0.8-1.4 Least concern

29 Vulpes chama Cape Fox Africa 2.0-4.2 Least concern

30 Vulpes corsac Corsac Fox Asia 1.6-3.2 Least concern

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31 Vulpes ferrilata Tibetan Fox Asia 3.2-4.6 Least concern

32 Vulpes macrotis Kit Fox North America 1.7-2.7 Vulnerable

33 Vulpes pallida Pale Fox Africa 2.0-3.6 Least concern

34 Vulpes rueppellii Rüppell’s Fox Africa 1.1-2.3 Least concern

35 Vulpes velox Swift Fox North America 2.0-2.5 Least concern

36 Vulpes vulpes Red Fox Europe, North America, Asia, 3-14 (푥̅≈ Least concern Australia 5.2)

37 Vulpes zerda Fennec Fox ACCEPTEDAfrica MANUSCRIPT 0.8-1.9 Least concern

* The taxonomy of Golden Jackals (Canis aureus) is under review, so both proposed new species (C. aureus and C. anthus) are presented here and in the text above.

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Table 2. The predominant dietary type, food items and foraging strategies of the Canidae, and their likely trophic role among potential sympatric canids. Canid numbering corresponds with Table 1.

Canid Dietary type Primary Food Items * Foraging strategy** Trophic role Potential sympatric canids No. 1 Omnivore Small mammals, birds, carrion Individual Mesopredator Gray Wolf, Red Fox 2 Omnivore Fish, insects, small mammals, Individual and dyad Mesopredator Bush Dog, Culpeo, Crab-eating Fox, Maned frogs, crabs, birds, fruit Wolf 3 Omnivore Fruit, small to medium Individual and small Mesopredator African Wild Dog, Bat-eared Fox, Fennec mammals,, insects, birds, grass group Fox, Ethiopian Wolf, Pale Fox, Cape Fox, Bat-eared Fox, Black-backed Jackal, Rüppells Fox 4 Omnivore Small vertebrates, Individual and small Mesopredator Ethiopian Wolf, African Wild Dog, Bat-eared invertebrates, fruit group Fox, Red Fox, Pale Fox, Fennec Fox, Raccoon Dog 5 Omnivore Birds, fruit, small vertebrates, Individual and small Mesopredator Dhole, Red Fox invertebrates group 6 Carnivore/ Medium-large mammals, small Individual, dyad and Mesopredator/ Top Red Fox, Coyote, Black-backed Jackal, Gray omnivore mammals, reptiles, birds, group predator Wolf refuse, carrion, grass, 7 Carnivore/ Fruit, insects, small mammals Individual and group Mesopredator Red Wolf, Gray Fox, Swift Fox, Kit Fox, Red Omnivore ACCEPTED MANUSCRIPT Fox, Bush Dog 8 Hyper- Ungulates, large vertebrates, Group Top predator Coyote, Red Fox, Arctic Fox, Tibetan Fox, carnivore carrion Indian Fox, Dhole, Fennec Fox, Blanford’s Fox, Rüppells Fox, Corsac Fox, Raccoon Dog, Grey Fox 9 Carnivore Small-medium mammals Dyad and small group Mesopredator Ethiopian Wolf, African Wild Dog, Bat-eared including rodents, young Fox, Cape Fox, Side-Striped Jackal, Pale Fox, ungulates, insects Rüppell’s Fox

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10 Obligate Coypu, rabbits, White-tailed Individual and group Top predator Coyote, Gray Fox, Red Fox carnivore Deer, Raccoons, rodents 11 Carnivore Rodents, hares, Hyrax Individual Mesopredator African Golden Wolf, Black-backed Jackal, Rüppell’s Fox, African Wild Dog, Side- striped Jackal, Bat-eared Fox, Pale Fox

12 Omnivore Fruit, vertebrates, insects, Individual, dyad and Mesopredator Maned Wolf, Hoary Fox, Bush Dog, Short- amphibians, crustaceans, birds, pack eared Dog, Chilla, Pampas, Culpeo, Gray Fox carrion 13 Omnivore Fruits, small to medium Individual Mesopredator Bush Dog, Crab-eating Fox, Hoary Fox, vertebrates Pampas Fox, Short-eared Dog, Culpeo, Chilla 14 Carnivore/ Insects, small mammals, birds, Group Top predator Eurasian Golden Jackal, Red Fox, Corsac omnivore grass, medium-large ungulates Fox, Tibetan Fox, Indian Fox, Grey Wolf, Corsac Fox, Raccoon Dog 15 Carnivore Small to medium sized Group Mesopredator/ Top Side-striped Jackal, Black-backed Jackal, mammals predator African Golden Wolf, Bat-eared Fox, Cape Fox, Rüppell’s Fox, Pale Fox, 16 Omnivore Frogs, lizards, invertebrates, Pairs Mesopredator Red Fox, Grey Wolf, Corsac Fox, Tibetan insects, birds, eggs Fox, Dhole, Golden Jackal 17 Omnivore Insects, spiders, fruit, small Small groups Mesopredator African Golden Wolf, Side-striped Jackal, mammals, birds, eggs, reptiles ACCEPTED MANUSCRIPT Black-backed Jackal, African Wild Dog, Cape Fox, Rüppell’s Fox, Ethiopian Wolf 18 Omnivore Small to medium mammals, Individual Mesopredator Bush dog, Pampas, Short-eared dog, Grey fruit Fox, Chilla, Darwin's Fox, Sechuran Fox 19 Omnivore Small mammals, reptiles, Individual? Mesopredator Culpeo, Chilla insects, birds, spiders, fruit 20 Omnivore Small mammals, arthropods, Individual Mesopredator Culpeo, Bush dog, Crab-eating Fox, Short- birds, reptiles, fruit, carrion eared Dog, Maned Wolf, Grey Fox, Pampas Fox, Darwin's Fox

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21 Omnivore Small mammals, birds, fruit, Individual Mesopredator Bush dog, Crab-eating Fox, Culpeo, Chilla insects, carrion 22 Omnivore Small mammals, insects, Individual? Mesopredator Culpeo scorpions, fruit 23 Omnivore Insects, small mammals, birds, Individual / small family Mesopredator Maned Wolf, Bush Dog, Crab-eating Fox, reptiles groups 24 Carnivore Small mammals, lizards, snakes, Groups Mesopredator Maned Wolf, Hoary Fox, Short-eared Dog, birds. Some larger prey Crab-eating Fox, Culpeo, Pampas Fox, Coyote, Gray Fox 25 Omnivore Rabbits and rodents, insects, Individual? / small Mesopredator Coyote, Red Wolf, Swift Fox, Kit Fox, Red carrion, fruit, nuts family groups? Fox, Bush dog, Crab-eating Fox, Grey Wolf

26 Omnivore Insects, small vertebrates, fruit, Individual Mesopredator/ molluscs, shore invertebrates basal predator 27 Omnivore Insects, small mammals, birds, Individual Mesopredator Gray Wolf, Dhole, Red Fox, Blanford’s Fox eggs 28 Omnivore Insects, fruit Individual Mesopredator Gray Wolf, Eurasian Golden Jackal, Red Fox, Corsac Fox, Rüppell’s Fox, Fennec Fox, Indian Fox 29 Omnivore Small mammals, reptiles, birds, Individual Mesopredator Black-backed Jackal, African Wild Dog, Bat- invertebrates, fruit eared Fox, Side-striped Jackal 30 Omnivore Small mammals, birds, reptiles,ACCEPTED Individual MANUSCRIPTMesopredator Dhole, Red Fox, Raccoon Dog, Blanford’s insects, carrion Fox, Gray Wolf, Tibetan Fox 31 Omnivore Small rodents, carrion, insects, Individual Mesopredator Gray Wolf, Dhole, Red Fox, Corsac Fox, birds, fruit, lizards Raccoon Dog, Dhole 32 Omnivore Small mammals, insects, birds, Individual Mesopredator Coyote, Gray Fox, Grey Wolf, Red Fox, Swift reptiles, carrion, fruits Fox

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33 Omnivore Fruit, small mammals, Unknown Mesopredator Fennec Fox, Black-backed Jackal, Ethiopian birdsreptiles, invertebrates Wolf, Rüppell’s Fox, African Wild Dog, Side- striped Jackal, African Golden Wolf

34 Omnivore Small mammals, reptiles, birds, Individual Mesopredator Red Fox, Pale Fox, Fennec Fox, Ethiopian fruit Wolf, Side-striped Jackal, Grey Wolf, Blanford's Fox, Bat-eared Fox 35 Omnivore Small mammals, birds, insects, Individual Mesopredator Coyote, Gray Fox, Grey Wolf, Red Fox, Kit fruit, carrion, seeds Fox 36 Omnivore Small mammals, birds, reptiles Individual Mesopredator/top Gray Wolf, Arctic Fox, Swift Fox, Coyote, Kit amphibians, fruit, predator Fox, Raccoon dog, Corsac Fox, Bengal Fox, invertebrates, carrion Tibetan Fox, Dhole, Fennec Fox, Rüppell’s Fox, Blanford’s Fox, Gray Fox, Arctic Fox, Red Wolf, African Golden Wolf, Eurasian Golden Jackal

37 Omnivore Insects, small mammals, small Individual? Top/mesopredator/ African Golden Wolf, Rüppell’s Fox, Grey reptiles, small birds, eggs, fruits basal predator Wolf, Blanford’s Fox, Pale Fox, Side-striped Jackal, African Wild Dog

* All species opportunistically scavenge

** Predominant foraging strategies listed. ForagingACCEPTED strategies differ MANUSCRIPT from social groupings because canids do not always forage as a full social group. Therefore, “individual” describes foraging as a single animal, “dyad” describes two individuals foraging cooperatively and "group" describes cooperative foraging parties >2 individuals. “Pack”, “pair” and “solitary” describe social groupings.

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Figure 1. a) Average occurrence of four main human-provided food groups in the diet of canids across the globe (n= number of studies; after Newsome et al. 2015b). b) The number of studies assessing use of human-provided foods by all terrestrial mammals across the globe with a body size of over 1 kg (from Newsome et al. 2015b, which details of data collection, species groups and prey categories). In b) species groups are split into three categories: T = top predator, M = mesopredator, and D = domestic species.

a) 60 Canidae

50

n=11 40

30 n=15

n=37 20

10 Average occurrence in diet in (%)occurrence Average n=1

0 Crop Waste Carcass Livestock

b) 60 Ursidae Hyaenidae 50 Felidae Canidae 40 Other

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20 ACCEPTED MANUSCRIPT Number of studies studies of Number 10

0 D M T D M T D M T D M T D M T D M T Food Township Crop Waste Carcass Livestock supply

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Plate 1. Unrestrained Domestic Dogs harass native wildlife in Australia (Meek 1999): two free-ranging Domestic Dogs (Canis familiaris) pursue a female Common Wallaroo (Osphranter robustus robustus) with pouch young, in an agri-ecosystem near Armidale, New South Wales, Australia. A young male Common Wallaroo, circled at left, is also disturbed, while Sheep graze in the background. Plate: J. Sparkes.

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Acknowledgements

Peter Fleming, Guy Ballard, Paul Meek and Greg Mifsud receive funds and inkind contributions from the Invasive Animals Cooperative Research Centre, NSW National Parks and Wildlife Service and Local Land Services. Thomas Newsome provided valuable comments and permission to use the data in Figure 1.

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