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Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes)夽 Simon Gadbois a,∗ , Olivia Sievert a , Catherine Reeve a , F.H. Harrington b , J.C. Fentress c a

Department of Psychology & Neuroscience, Dalhousie University, 1355 Oxford Street, PO BOX 15000, Halifax, Nova Scotia, Canada B3H 4R2 Department of Psychology, Mount Saint Vincent University, Halifax, Nova Scotia, Canada B3M 2J6 c 30312 Fox Hollow Road, Eugene, OR 97405, United States b

a r t i c l e

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Article history: Available online xxx Keywords: Action sequence Fixed action pattern Food caching sequences Red foxes Coyotes Wolves

a b s t r a c t We discuss the history, conceptualization, and relevance of behavior patterns in modern ethology by explaining the evolution of the concepts of fixed action patterns and modal action patterns. We present the movement toward a more flexible concept of natural action sequences with significant degrees of (production and expressive) freedom. An example is presented with the food caching behavior of three Canidae species: red fox (Vulpes vulpes), coyote (Canis latrans) and gray wolf (Canis lupus). Evolutionary, ecological, and neuroecological/neuroethological arguments are presented to explain the difference in levels of complexity and stereotypy between Canis and Vulpes. This article is part of a Special Issue entitled: Canine Behavior. © 2014 Elsevier B.V. All rights reserved.

Traditional ethology has always had a focus on structure and form. It was concerned with behavior patterns that were given a number of names over the years: instinctive behavior patterns (Lorenz, 1953), inherited coordination (Erbkoordination; Tinbergen, 1951), inborn skills (Eibl-Eibesfeldt, 1970), speciestypical or species-specific behavior patterns (Beach, 1960; Beer, 1973), innate or instinctive behaviors, grammar (Fentress and Stillwell, 1973), syntax (Berridge et al., 1987), action or motor patterns, motor programs (Fentress, 1991), movement or action sequences (Fentress, 1972; Fentress and Gadbois, 2001), etc. All these terms convey the idea of a structure governed by some rules. Similar ideas have been adopted in other areas, including with

humans, starting with language (Chomsky, 1957; Jackendoff, 1994; MacNeilage, 2011; Pinker, 1994), music (Jackendoff, 1994), and social behavior (Fentress, 1983; Jackendoff, 1994; de Waal, 1996; de Waal and Tyack, 2003). In ethology, the concept of predictable, genetically predetermined and rigid sequences of behavior became popular under the labels of “fixed action patterns” or FAPs (Lorenz, 1950; Tinbergen, 1951, 1963) and later, “modal action patterns” or MAPs (Barlow, 1977). In the field of comparative ethology, the study of the structure of behavior became as important as the study of the structure of more traditional phenotypical features such as morphology and anatomy. Lorenz, in particular, made some very convincing arguments for the observational analysis of behavior patterns (Lorenz, 1982). In fact, in his last book, “The Foundations of Ethology”, Lorenz describes the following scenario (Lorenz, 1982; p. 48–49; emphasis added):

夽 This paper follows the first of three presentations at SPARCS 2014 given by the first author, Simon Gadbois. The talk was broadly about the influence of rule-based systems in neuroethology (explaining neural networks), and ethology (explaining behavior patterns and sequences, social dynamics and networks). The focus of this paper will on behavior patterns, presenting food caching sequences in canids as an example. ∗ Corresponding author at: Canid Behaviour Research Team, Department of Psychology & Neuroscience, Dalhousie University, 1355 Oxford Street, PO BOX 15000, Halifax, Nova Scotia, Canada B3H 4R2. Tel.: +1 902 494 8848; fax: +1 902 494 6585. E-mail addresses: [email protected] (S. Gadbois), [email protected] (O. Sievert), [email protected] (C. Reeve), [email protected] (F.H. Harrington), [email protected] (J.C. Fentress).

“If, for example, a researcher is able to observe the way in which a wolf in the wild carries the remains of a kill to a covert place, digs a hole in the earth there, pushes the piece of plunder in with his nose, shovels the excavated earth back – still using his nose – and then levels the site through shoves with the nose, the teleonomic question concerning this behavior sequence is easy to answer, but the question concerning the causal origin of this behavior pattern remains completely unanswered. If, in contrast to this, the observer of captive animals sees the way in which a young wolf or dog carries a bone to behind the dining

1. General introduction

http://dx.doi.org/10.1016/j.beproc.2014.10.001 0376-6357/© 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Gadbois, S., et al., Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes). Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.10.001

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room drapes, lays it down there, scrapes violently for a while next to the bone, pushes the bone with his nose to the place where all the scraping was done and then, again with his nose and now squeaking along the surface of the parquetry flooring, shoves the nonexistent earth back into the hole that has not been dug and goes away satisfied, the observer knows quite a lot about the phylogenetic program of the behavior pattern.” Although clearly Lorenz evokes phylogeny in this quote, one very contemporary issue in animal behavior is expressed here: The cognitive control of the behavior. The quotation indeed illustrates how observing animals in captivity can lead to the identification of “performance failures” that are more likely to be noticed by the observer. These disturbances of behavior can be created by a new environment or an unusual incident and question the role of conscious processing and execution of the behavior. There is another interesting dimension to this example: It is a fairly complex and long sequence of behavior. We are quite removed here from the more classical stimulus–response model that early ethologists envisioned: a sign stimulus triggers a neurophysiological process (the innate releasing mechanism, often described in the neuroethology literature as involving central pattern generators or neural networks) that in turn triggers the FAP or MAP mentioned above.

words, the animal may seem to be stuck in a loop. Regardless, the stereotypy (rigidity) of the behavior is remarkable, in some instances, the pattern may even qualify as deterministic, in other words, the occurrence, form, duration, etc. of the behavior pattern (FAP) is 100% determined by the sign stimulus, its context, etc. (points 2 and 3). This set of principles satisfied early 20th century ethologists. Subsequent ethologists and neuroethologists (e.g., Barlow, 1977; Schleidt, 1974) were starting to see the limitations of such a conceptualization. Although Barlow’s MAP loosened some if not most of the points above, the MAP concept did not go far enough. A more systematic and broader view of behavior patterns began to emerge in the 60s and solidified itself in the 70s (e.g., Bekoff, 1977; Dawkins, 1976; Fentress, 1972, 1976; Fentress and Stillwell, 1973). Fentress (1987, 1991, 1992, 1993) discussed at length the complexity of the concept, including its modern relevance to neuroethology, developmental ethology and behavioral neuroscience as a whole. There were a few more problems, not necessarily addressed by the principles outlined above, or a loosening of those principles: 1. The length of the behavior pattern. 2. The simplicity of the original FAP concept and its historical evolution. Here, questions of rigidity (stereotypy) and degrees of freedom are front and center.

1.1. The evolution of FAPs into MAPs But what led to the creation of the MAP concept? Some ethologists and neuroethologists were starting to get uncomfortable with the “rigidity” of the whole FAP concept and felt as though it was necessary to loosen-up the FAP definition and expand on its basic assumptions. There are nine basic principles, at least implicit, surrounding the original concept of FAP: 1. The behavior pattern is genetically encoded. Therefore, it tends to be highly species-specific or species-typical. 2. The behavior pattern is very stimulus specific. 3. The behavior pattern is context- or situation-specific. 4. The behavior pattern is obligatory (in the presence of the appropriate stimulus, see point #2), “automatic”, and, although not a reflex, very reflex-like in appearance. 5. The behavior pattern is independent of immediate control, including explicit, conscious, or “cognitive” control. Some behavior patterns can even be described as “ballistic”, in other words, when the behavior is started, it cannot be interrupted. This is likely related, at least partially, to the next point. 6. The behavior pattern is immune to sensory feedback, i.e., the process is independent of afferent input. The “egg rolling” behavior of the graylag goose is a classic example of this point (see Lorenz and Tinbergen, 1970, pp. 328–342). Sensory-motor integration links points 4 and 5, but this will not be discussed here. 7. Individual differences (temperament or personality) are not relevant. All individuals of the species typically respond the same way to the sign stimulus. 8. Learning (and to some extent maturation) or any other dimension of “experience” are not factors in the expression of the behavior patterns. The behavior patterns are developmentally fixed, pre-determined. This ties back to point #1. Note that by “learning” we include here both simple or non-associative learning (habituation and sensitization) and associative learning (classical and instrumental conditioning). 9. For all those reasons, the behavior patterns are highly predictable, with little if any expressive freedom (no or few degrees of freedom). The only possible variation may be (especially in social communication) in the redundancy of the response, expressed in often rhythmic and repetitive behaviors, in other

Those two issues are intertwined. It is important to remember that the original concept was used for relatively simple patterns. Those patterns were short in terms of total duration (milliseconds, or seconds) and in terms of the number of events (actions, behaviors) involved. Schleidt (1974) reminds us that the average MAP (already more complex by definition than FAPs) lasts 1 s, and typically ranges from 0.1 to 10 s. The short length of those patterns (FAPs and MAPs) necessarily restrains the “degrees of freedom” or “expressive freedom” of those behaviors, especially in terms of any possible sequencing. Barlow (1977) summarizes a few typical MAPs (Table 2, pp. 104–105). In his summary, only one MAP exceeds 5 s in duration. Again, a typical FAP or MAP is triggered by a relatively simple stimulus (the sign stimulus) and results in a relatively simple response (e.g., a tongue flick in Ewert’s toads, sometimes, if necessary, preceded by a head turn, or orientation to the moving sign stimulus, the potential prey; Ewert, 1987). But what about grooming sequences in rodents (Fentress, 1972; Fentress and Stillwell, 1973) comprised of many changes of postures and paw strokes? Or the hunting sequence in a canid (Coppinger and Coppinger, 2001)? The hunting sequence of carnivores and more specifically canids is discussed elegantly by Coppinger and Coppinger (2001), including in the context of the domesticated border collie and the ensuing modified sequence. A general hunting-stalking sequence looks like this: orient > eyestalk > grab-bite > kill-bite > dissect > consume. Coppinger and Coppinger (2001) point out that the mouse-jump behavior in foxes and coyotes during the winter months (when snow covers the ground) is a modification of the previous sequence adapted to the context (see also Henry, 1986). Interestingly, the border collie is discussed in the book as an example of how the sequence can be modified through artificial selection (selective breeding) to truncate the original sequence, keeping (in principle) only the “orient” and “eye-stalk” behaviors. Those two examples (grooming and hunting sequences) are different from FAPs and MAPs in two respects mentioned above: They are long (in duration) sequences of many events or behaviors, and although recognizable, a significant level of complexity is present. Grooming sequences are fast, and require filming at high speed and the ability to replay in slow motion in order to analyze them. Hunting sequences, although recognizable, have many degrees of freedom in constant

Please cite this article in press as: Gadbois, S., et al., Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes). Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.10.001

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adaptation to the immediate movement of the prey (violating assumption # 6 of the principles). Note that we have started to use the word “sequence”. This is key here to the rest of this discussion. Many behaviors do not fall into the traditional FAP definition simply because of the length (in duration and/or number of events) and complexity of the serial configuration. In other words, from deterministic behavior patterns (100% predictable), to random behavior sequences (0% predictability), there is a large realm of behaviors with significant variation (we called them stochastic, or having a probability of occurrence). The behavior or behaviors following the sign stimulus can be short, simple and very deterministic, or long, complex, or quasi random (at least in appearance, but we can argue this is rarely the case, Fentress and Gadbois, 2001). Although some textbooks in biology or psychology may suggest that the concept of FAP is passé, it is unclear what that assertion means. If it is a suggestion that the original FAP concept was too rigid, yes, we can agree and the recent history of the concept would support that idea. If it is suggested that the FAP does not exist, this is clearly wrong. We can certainly make the argument that many behaviors fall into the nine principles presented above. Others fit better the loosened criteria of the MAP. But many cannot be described with the conservative or liberal version of the previously outlined nine principles. They go beyond and above the Stimulus–Response-like simple configuration of the FAP/MAP into a complex arrangement of coordinated movements that are still identifiable and recognizable. In other words, a pattern is still present, but their analysis is challenging. 1.2. Action sequences: structure and analysis So if complex behavior sequences follow some rules for their motor and spatio-temporal expression, can we still talk about “pattern” and “structure”? Again, if the behavior is recognizable as a “hunting” sequence, we can certainly argue that there is a program, or grammar or syntax to direct the expression of the behavior sequence. This is the modern perspective on what we will now call “action sequences”, or behavior patterns than can be described probabilistically, with temporal (including serial) and spatial degrees of freedom, from close to fully deterministic, to close to fully random. The concept of a behavior syntax or grammar emerges: The idea that a rule-based system could be used to conceptualize, describe, analyze, and model behavior is intriguing. One potential objection would be to point out that any rule can have an exception or exceptions. That may actually be the strength of a rule-based model. Chomsky (1957) is known for suggesting a Universal Grammar for human languages, but linguistics is not the only discipline that uses the concept of rules. Mathematics comes to the rescue. Ian Stewart (1998) wrote a great piece on the importance of rules in biology in his book “Life’s other secret: The New Mathematics of the Living World”. He identifies four reasons why rules are useful: 1. Efficiency: as he asserts “Rules are simpler than the behavior they generate”. 2. Consistency: Rules guarantee consistency, but behavior can evolve quickly while keeping internal consistency. 3. Adaptability: Adaptations (to immediate constraints, or more distal constraints) occur by modifying the rules (including the insertion of exceptions, if necessary). 4. Individuality and proximity: Rules concern individuals, or “involve only what an individual can reasonably be expected to perceive”. This is the concept of “local rules”. In the context of modern ethology, the conceptualization of behavior as a system of rules gives flexibility within a framework.

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Instead of talking about instincts and innate behaviors, behaviors that seem to be strongly genetically determined can be discussed as a system of rules or “syntax” or “grammar”. This was a point made by the semiotician Charles Morris (1946, 1938/1970) that distinguished three components to the study of signs in animals (a field labeled as zoosemiotics): Zoosemantics, dealing with the meaning behind the signs and behaviors, zoopragmatics, addressing the use of signs and behaviors in context (including in social communication) and finally the one that we want to focus on, zoosyntactics. For instance Sebeok (1990) states that zoosyntactics “deals with combinations of signs abstracted from their specific signification or their ecological setting” (p. 43) and Nöth (1990) writes that zoosyntactics “determines the sign repertoires of animals, investigates their temporal and spatial elements, and studies the rules of their combination into messages” (p. 148). Gadbois (2013) gives a short history of the zoosemiotic movement in ethology and how that influence opened the door to the study of the structure of complex behaviors in ethology. Fentress and Gadbois (2001) and Gadbois (2013) go further by adding prosody (we could label this fourth area “zooprosodics”), making the point that the musical expressiveness of a behavior is relevant and may hide some patterns otherwise undetectable (to continue the use of the linguistic or semiotic analogy: prosody). In summary, behavior can be defined essentially as an observable change in time and space. Early models were simplistic, although they described the reality of structurally simple, short, and highly predicable behaviors (FAPs, MAPs). Ethologists quickly became interested in longer, more complex, and less predictable sequences of behaviors. This led to a few fundamental conceptual changes and considerations: 1. A relaxation of the constraints contained in the principles presented earlier 2. Consideration of behavior sequences of increased length in both duration and number of events 3. Consideration of behavior sequences of increased combinatorial complexity (syntax) 4. Consideration of behavior sequences of increased spatial–temporal freedom and expression (prosody) From a behavior structure analysis perspective, two elements are essential to the understanding of behavior: syntax and prosody. Beyond syntax (combinatorial structure) behavior can be analyzed based on its prosodic characteristics or musicality: Rhythm (e.g., frequency and rate changes), melody (e.g., amplitude modulation) and harmony (subtle but non-random coordination of movements). See Fentress and Gadbois (2001) for an extensive review of the idea of syntactic and prosodic analysis of behavior. We will now examine an example of a behavior sequence already mentioned above. The food caching example given by Lorenz was systematically investigated by the Fentress group at the Canadian Centre for Wolf Research and Dalhousie University in the early 90s (Phillips et al., 1990, 1991) with wolves and coyotes respectively, and with red foxes in the mid 90s (Fentress and Gadbois, 2001). We will take a new look at the work done with those three species by looking specifically at species differences in perseverations (repetitions) of elements of the caching sequence. Food caching, also labeled food storing or food hoarding (Vander Wall, 1990), is a common behavior in many species of birds and mammals, with the general purpose of concealment and protection of food. Among mammals, rodents and carnivores seem to be the leading cachers (Vander Wall, 1990). Food caching sequences may vary in stereotypy. For example, Muul (1970) reported extreme stereotypy in female flying squirrels (Glaucomys volans). While in peak caching season, when presented with a stimulus (hickory nuts), and their pups at the same time, the squirrels would begin

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“storing” their pups. In this instance, the females were unable to alter or discontinue this natural action sequence regardless of the distress calls emitted from their pups during the sequence. We already presented Lorenz’ scenario involving a canine cacher not aware of the immediate environment. It is generally accepted that food hoarding is described as the act of storing available food supplies for the purpose of later access (Vander Wall, 1990) and it is understood that food caching gives animals a biological advantage over non-cachers as it allows for the control over the availability of food in harsh or changing environments. Furthermore, food hoarders may not need to migrate, hibernate or suffer weight loss during food shortages (Vander Wall, 1990). There are two different types of food cachers: larder hoarders and scatter hoarders. Larder hoarders, such as those within the family Mustelidae, utilize a single cache site. Scatter hoarders by contrast, distribute food to multiple sites, as is common in rodents and the family Canidae (Vander Wall, 1990). Caching in canids is well documented, at least in the three species that will be of interest to us here (Dekker, 1983; Fisher, 1951; Henry, 1977, 1980, 1986, 1993; Harrington, 1981, 1982; Jeselnik and Brisbin, 1980; Macdonald, 1976, 1987; Montevecchi and Sklepkovych, 1985; Phillips et al., 1990, 1991). Despite this handful of studies on food caching behaviors in canids, little is known about the proximate mechanisms involved, likely because of the difficulty in experimenting with this type of behavior. Vander Wall (1990) mentions a number of internal and external regulatory mechanisms relevant to food caching: physiological (neural and hormonal control, e.g., hunger, sexual differences), light (photoperiod, intensity), temperature, and social regulation. Other factors can be considered such as the substrate (the digging environment such as earth, sand and snow), the food item to be cached (type of food to be cached) and amount of food already cached as well as familiarity with the environment (Vander Wall, 1990). It is important to note here that the substrate and its conditions did not seem to influence wolves (Phillips et al., 1990) or coyotes (Phillips et al., 1991) in any significant way during the caching process. This does suggest the presence of a set of rules governing the flow and expression of the behavior. 1.3. The form, flow and expression of food caching in canids Canids adopt a caching style that requires extensive temporal and sequential expression. In other words, reasonably well defined steps are needed to complete the sequence. Each step has its own purpose, and often, the sequence has a “logical” flow and pattern (in terms of the functional value of each element of the sequence): the order of events in the sequence is not random, but rather predictable (e.g., Fentress and Gadbois, 2001; Phillips et al., 1990, 1991). Canids are scatter hoarders, spreading their caches or storage sites over fairly large areas (Foxes – Dekker, 1983; Fisher, 1951; Henry, 1977, 1980, 1986, 1993; Jeselnik and Brisbin, 1980; Macdonald, 1976, 1987; Montevecchi and Sklepkovych, 1985; Tinbergen, 1972; wolves – Harrington, 1981; Phillips et al., 1990 and coyotes – Harrington, 1982; Mech, 1970; Phillips et al., 1991). This is one of the factors that explains the variable length of the caching sequence in canids. Indeed, the early stages include two behaviors that we label “food carrying” (FC) and “site inspection” (SI) respectively. Although food carrying is mandatory, site inspection is facultative. Both behaviors are of very variable length, and seem to have little stereotypy. Following the choice of the site, pawing (P) or a series of strokes with the left or right forepaw on the inspected or chosen site may occur. This step may be skipped in some cases but when produced, it is always of a very short duration (a few strokes). The substrate is typically scratched by the same paw more than once: L–L–L.

In some instances, more than one pawing is done using different limbs: L–L–L then R–R–R–R. The pawing is usually followed by digging. Digging (D) is done with the forepaws that are used alternatively to displace the substrate. Digging can, on occasion, look like it is a succession of pawing segments (e.g., 3 left strokes, 10 right strokes, 2 left strokes, etc.) instead of pure alternating forepaw strokes. What follows is by far the most interesting and distinctive part of the caching sequence in canids. It typically consists of a clear alternation of Tamps (T) and Scoops (S), usually beginning with Tamps. Tamps are head motions resulting in a muzzle stroke of the soil at the caching site. A segment of Tamps (more than two in succession) is similar to a woodpecker’s head motion when digging holes in trees, although not as rapid and assertive. Phillips et al. (1991) describe Tamps as: “vertical motion of the snout which pressed the food into the depression in the substrate”. Scoops (S) are head motions resulting in a sweep with the muzzle in order to push soil, leaves, etc. over the site. Phillips et al. (1991) describe Scoops as: “horizontal motion of the snout directed away from the [subject]’s body along the substrate surface”. Scoops often end in Tamp-like actions: the subject Scoops the dirt over the site and without the “wood pecking” motion typical of pure Tamps, finishes the Scoop by pressing the dirt with its muzzle. In summary, a food caching sequence in red foxes, coyotes and wolves is comprised of the following three phases. Phase 1: Food carrying (mandatory) and site inspection (facultative): Very variable Phase 2: Pawing (facultative) and digging (mandatory, or very high occurrence): Variable Phase 3: Tamping and scooping (in principle and most instances, both mandatory), some exceptions: Variable but potential for pattern emergence. Phase 3 will be our focus for the rest of this paper. As mentioned above, Phase 3 is characterized by an alternation of Tamp and Scoop “segments”. These segments are a crucial unit for our descriptive analysis of the sequences. Each segment (of Tamps or Scoops) contains one or more occurrence of Tamps or Scoops. A Tamp–Scoop sequence (Phase 3) could look like the following: TTTSSSSTTTTTST, in which case a segment is either a single Tamp or Scoop or a perseveration of either (see Berridge et al., 1987). The example TTTSSSSTTTTTST has 5 segments – three T segments and two S segments. 2. Method 2.1. Subjects All of the data were collected in rural Nova Scotia, Canada, and animals were cared for in accordance with the guidelines and principles of the Canadian Council of Animal Care. Data from Coyotes (Canis latrans) and Wolves (Canis lupus) was collected in previous studies (see Phillips et al., 1990, 1991 for details) at the Canadian Centre for Wolf Research, in Shubenacadie, Nova Scotia. Hand-raised wolves in enclosures of 0.2 hectare (half acre) were part of this study. Further details for the coyotes and gray wolves can be found in Phillips et al. (1990, 1991). Three yearling foxes, Vulpes vulpes (A, B, and C) were observed at the Shubenacadie Wildlife Park Zoo (Nova Scotia) in 1993 and five yearling foxes (D, E, F, G, and H) were observed at Hope for Wildlife in Seaforth, Nova Scotia in 2013. The sex of all individual foxes was undetermined. Foxes C, D, G and H never cached, or at least non-consistently and were not included in the analyses. Foxes were in enclosures under 0.1 hectare (quarter of an acre). Fights for cache sites and

Please cite this article in press as: Gadbois, S., et al., Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes). Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.10.001

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site defense post-caching were commonly observed amongst all individuals, with the exception of fox C and fox H, who avoided confrontation and rarely left the back of the enclosures. 2.2. Material and observation environments For all three species, the substrates consisted mostly of earth and loose stones, with sporadic patches of grass. Animals could therefore easily dig in the ground. For each filming session, the observer provided the subjects with 20–60 deceased, 2–3 day-old chicks. Details concerning observations on wolves and coyotes can be found in Phillips et al. (1990) and Phillips et al. (1991), respectively. Foxes in 1993 were filmed using an 8 mm/HI-8 video camera (Canon A-1 digital recorder – Canovision 8). The HI-8 tapes were dubbed on S-VHF videocassettes to be viewed and scored on an S-VHF tape deck (Panasonic S-VHS AG-5710) and a high resolution monitor (Sony Trinitron Color Video Monitor model PVM-1341), allowing frame by frame scoring and/or slow motion. Filming conducted in 2013 was done with a Sony Handycam Mega Pixel DCR-HC40 NSTC digital video camera recorder. Recordings were saved on a memory card and uploaded onto a LaCie external hard drive. Videos were analyzed on Windows Media Player. CaniSequence (programmed by S. Gadbois) was used to enter and analyze the data. It is a standalone relational database management system with a data analysis module for the sequential analysis of caching. CaniSequence was initially programmed in FileMaker Pro 2 (FileMaker Inc.) in 1993 and updated through the years to the current version (FileMaker Pro Advanced 13).

Fig. 1. A typical fox tamping–scooping phase: this Tamp/Scoop sequence has 12 segments.

available for a species), it was repeated to ensure reliability (i.e., all sequences were fully analyzed twice, in two distinct passes). For example, the first fox cohort sequences were analyzed in October of 1993, and again in April of 1994 by the same scorer. Other scorers analyzed the same sequences later that year (see next point). 12. Inter-rater reliability was very strict for both fox groups and we explicitly sought consensus. For the 1993 group, there was an initial score by the main investigator followed by four independent re-scorings. Only the sequences with full agreement were kept. For the 2013 group, two scorers were working simultaneously and both investigators had to agree on the sequences observed. Sequences were disregarded if a consensus among raters could not be obtained. 3. Results

2.3. Procedure Again, details for the wolves and coyotes can be found in Phillips et al. (1990) and Phillips et al. (1991), respectively. The information below is based on the trials (1993 and 2013) with the foxes, but for all three species and locations, the procedures are very similar: 1. The main observer is trained to identify all individuals with a high degree of certainty. 2. Observations are made by a single individual recording the caching sequence. 3. Feeding schedules were as prescribed by the facilities in most cases. 4. For the foxes that were observed in facilities that are typically visited by the public, observations were made either before the facility would open to the public, or on days when the facilities were not opened to the public. 5. Rainy and/or windy days were avoided to optimize filming conditions. 6. None of the foxes, coyotes, or wolves were handled or hand-fed by the observer. 7. Observations were typically done in the morning, at the time of feeding. 8. Food items (e.g., dead chicks for the red foxes) were brought in by the observer and dumped in the center of the enclosure. 9. Depending on the enclosure, the observer would retreat and begin filming, either outside or inside (at the periphery) the enclosure. In order to analyze with precision the sequences, most recordings had to be done within 20 m (66 feet) of the caching individual. 10. Length of recordings varied from day to day, and concluded when all individuals completed caching (when all the individuals began to rest and no longer visited the feeding area, or all the food items were gone, consumed, or cached). 11. When filming was completed, the observer conducted tape scoring. After the initial scoring was completed (of all the tapes

Data presented here are based on animals that were consistently caching and were not just occasional/rare cachers. Four red foxes, five wolves, and four coyotes contributed to this dataset. A main objective here is to present and compare caching sequences among three species of canids. We know from previous work (Phillips et al., 1990, 1991; Fentress and Gadbois, 2001) that a significant level of degrees of freedom can be found in the tamping and scooping phase with a potentially high rate of perseveration (or repetition of actions within a sequence), yet, the tamping–scooping phase is highly recognizable. Therefore this part of the sequence is the focus of our analysis. The structure of a typical canid caching sequence was described in our introduction, and Fig. 1 illustrates further the general structure of the tamping and scooping phase with an example. We will first present data on the durations of the full caching sequences for foxes and then, comparatively among the three species. The same format will be used for the subsequent sections. Our observations were made on a limited number of animals, although we have many observations per animal for which we provide descriptive summaries. All averages presented below are followed by standard deviations unless otherwise specified. As mentioned earlier, further details on the wolves and coyotes studies are provided in Phillips et al. (1990, 1991, respectively). About 340 fox caching sequences were filmed but only 323 were visible or complete enough to be scored and recorded. As mentioned earlier, only half the foxes cached. 3.1. Data on the durations of the full caching sequences in foxes The average duration of sequences (from picking up the food to completion of the Tamp/Scoop phase) was 28.39 ± 16.89 s (range: 8–154 s). Henry (1986) reports 90 s as an average for free-ranging foxes. Note that this is significantly higher than what is expected from a FAP or MAP, as reported by Barlow (1977). The state of the ground (e.g., wet or dry) and type of substrate (e.g., sand,

Please cite this article in press as: Gadbois, S., et al., Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes). Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.10.001

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Table 1 Comparative table of basic sequence parameters for red foxes, coyotes and wolves. Wolves (n = 5) Phillips et al. (1990) Number of observations (full sequences) Length of sequence in number of segments Length of sequence in number of elements Duration of caching sequence in seconds Sequences with pawing (count) Sequences with site inspections Sequences with digging omissions

Coyotes (n = 4) Phillips et al. (1991)

124 9.08 ± 5.48 (1–28) 31.97 ± 20.21 (2–113) 66.37 ± 41.19 (8–331) 72% 100% (average per sequence 1.40) 53%

snow) must certainly be taken into account although Phillips et al. (1990,1991) did not find that the substrate or state of the ground influenced the flow and pattern of the sequences significantly. Longer and presumably more variable sequences could be expected in natural settings because of the presence of roots, rocks, grass and therefore harder ground to excavate. 3.2. Comparative data on the durations of the full caching sequences in foxes, coyotes and wolves 3.2.1. Caching duration in seconds Table 1 synthesizes data from the present study and the two studies by Phillips et al. (1990, 1991) on wolves and coyotes. Note the similarity between coyotes and wolves in Table 1; the average duration and the maxima for these two species are very similar. Foxes have both an average and a maximal duration at less than half those of coyotes and wolves. The caching duration difference between the three species (in seconds) is significant (Kruskall–Wallis [non-parametric] comparison = 157.7, p < 0.0001). Foxes clearly take less time than coyotes or wolves to complete the caching process. A Dunn multiple comparison test shows that the difference in caching duration is significant between foxes and wolves, and foxes and coyotes, but not within Canis (coyotes and wolves). 3.2.2. Site inspections, pawing and digging Site inspections and pawing (Table 1) seem also to distinguish Canis from Vulpes: Canis rarely omits site inspections before starting

92 6.34 ± 4.01 (1–17) 20.89 ± 9.60 (3–49) 82.48 ± 56.41 (27–243) 78% 99% (average per sequence 1.23) 4.3%

Red foxes (n = 4)

323 6.01 ± 3.84 (2–27) 17.32 ± 8.63 (3–82) 28.39 ± 16.89 (8–154) 20% 14.3% (average per sequence 1.33) 15.17%

the digging process, while foxes will inspect sites only 14.3% of the time. Since the enclosures for foxes, coyotes, and wolves were different in appearance, size, and landscape configuration, it could be attributed to a spatial difference, e.g., a larger area would require more site inspection (keeping in mind that size is relative – for a 45 kg wolf, 0.2 hectare might seem smaller than 0.1 hectare feels to a 4.5 kg fox). Foxes had the smallest available area, followed by wolves and coyotes in half acre enclosures. Another similarity is found within Canis: Wolves and coyotes will paw 72 and 78% of the time respectively, while foxes paw only 20% of the time. Digging patterns are not clear, and seem to be associated with the presence of already made holes in the enclosures. This pattern would vary daily with all three species, so we are not putting too much significance in those numbers. Foxes rarely pawed the ground but began to dig almost immediately in most cases. Wolves, who paw a lot and rarely dig, may be able to excavate a reasonable hole for their food item without digging. Coyotes paw more often than all the others and dig nearly as often as foxes.

3.3. Data on the Tamp/Scoop phase in foxes This phase of the caching sequence was the most “stereotyped” phase of caching found by Phillips et al. (1990, 1991) and Fentress and Gadbois (2001) with coyotes and wolves. As mentioned earlier, because of the highly predictable sequential organization of the first part of the food caching sequence, we were mostly interested in

Fig. 2. Comparative length of sequences (in number of segments). The numbers on the x axis represent the length of the sequence in segments, and the y axis indicates the number of sequences with that length.

Please cite this article in press as: Gadbois, S., et al., Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in Wolves (Canis lupus), Coyotes (Canis latrans), and Red Foxes (Vulpes vulpes). Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.10.001

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Table 2 Parameters illustrating the unequal distribution of Tamps and Scoops and digrams (T–T, T–S, S–S, S–T) in a first order Markov model.

Overall % of Tamps (T) Overall % of Scoops (S) T–T probabilities T–S probabilities S–T probabilities S–S probabilities Chi-square

Wolves

Coyotes

Foxes

36% 64% 25% 21% 16% 38% 125.1 (1),

Revisiting the concept of behavior patterns in animal behavior with an example from food-caching sequences in wolves (Canis lupus), coyotes (Canis latrans), and red foxes (Vulpes vulpes).

We discuss the history, conceptualization, and relevance of behavior patterns in modern ethology by explaining the evolution of the concepts of fixed ...
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