ÔØ ÅÒÙ×Ö ÔØ 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 . 1 ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs 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. 2 ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs 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 3 ACCEPTED MANUSCRIPT Fleming et al. Canids in food webs 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 4 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