TEMPLE GRANDIN

Department of Animal Science, Colorado State University, Ft. Collins, Colorado, USA

At the time of my contribution to the first edition of this book in 2005 my research group had conducted some of the early research that showed that cattle temperament had an effect on weight gain. Beef cattle that struggled or moved more while loosely held in a squeeze chute (chute test) had lower weight gains (Voisinet et al., 1997). Other studies have replicated this result in cattle and pigs (Benhajali et al., 2010; Holl et al., 2010). Studies using another type of temperament testing, termed exit speed scoring, found that beef cattle that run out of a squeeze chute quickly have lower weight gain, poorer reproductive performance, and higher physiological measures of stress (Burrows and Dillon, 1997; Vetters et al., 2013; Kasimanickam et al., 2014).

The above studies served as motivation for the US beef cattle industry to include both chute scoring and exit scoring in their criteria for selecting breeding animals. Twenty years later, I have observed that this has resulted in improved mental well-being in herds of beef cattle: the animals are much less reactive and calmer when they are handled. In the United States, today’s extensively raised beef cattle are very different – in emotionality and temperament – than the beef cattle that were raised before chute scoring and exit speed scoring became a regular industry practice.

16.2 When Fearfulness is Reduced, Other Personality Traits Become Evident

Twenty years of temperament selection has reduced fearfulness in beef cattle. This may be similar to the reduction in fearfulness in domestic dogs. Zapata et al. (2016) found genetic variations that reduce fear that may have contributed to dog domestication. Recent studies are showing that temperament or personality in farm animals cannot be completely explained by determining an animal’s overall fear level. For example, whereas the exit speed test would measure fear, the chute test measures fear combined with another trait (Bruno et al., 2016). In addition, Brazilian researchers evaluated the influence of different genes while using an electronic chute test to measure struggling while held in a squeeze chute (dos Santos et al., 2017). They concluded that temperament is a complex trait that incorporates a variety of different behavioral phenotypes. I hypothesize that standard industry temperament tests mainly measure fear, but in some cases they may also be measuring other emotional traits such as aggression or separation distress (Grandin and Deesing, 2014), which likely differ from fear.

16.3 Panksepp Emotional System

After reading many papers in the farm animal, pet and wildlife literature I came to the conclusion that the Panksepp (1998, 2011; Montag and Panksepp, 2017) basic emotional systems would be the best way to explain many conflicting results in scientific studies of farm animal temperament. Different researchers use different terms and the trait of fearfulness is often confused with other behavioral traits. What follows is an outline of the Panksepp emotional system – with my added explanations – which may provide a good framework for animal personality traits.

Panksepp (2011) and a review by Morris et al. (2011) have explained the brain systems that underlie these seven emotional systems. While many of these older studies were done with invasive procedures that would never be approved today due to animal welfare concerns, the findings of those studies are still valid today. One of the advantages of using an electrode penetrating the brain to study emotional circuits is that it can definitively determine which node on a network activates an entire network, something functional magnetic resonance imaging (fMRI) cannot do. The early studies with electrical stimulation clearly show that subcortical brain structures activate the emotional networks.

Social behavior has a strong emotional basis, with some animals being more social than others. For example, chimpanzees and lions are more social whereas orangutans, panthers and tigers are more solitary. Some recent research has indicated that social behaviors of solitary-living and nonmonogamous mammals, which do not form strong social bonds, resemble behaviors in humans with autism, a neurodevelopmental disorder connected with impairment in social interactions and communication (Reser, 2014; Persson et al. 2016). For example, Reser (2014) reports that solitary mammals exhibit certain biomarkers that are characteristic of autism, such as reduced oxytocin and vasopressin signaling during social interactions as well as reduced hypothalamic–pituitary–adrenal activity when they are separated or isolated from other animals. Another study by Persson et al. (2016) found common genes for social contact in dogs and in humans with autism spectrum disorder. I hypothesize that the solitary animals have lower levels of Panksepp’s Nurture and Panic (separation distress) traits. Within the nurture system there are subsystems for different aspects of nurturing behavior, each of which may also be affected by genetics. The nurture system appears to underlie parenting behavior, and a study by Bendesky et al. (2017) identified four parenting behaviors in mice: pup retrieval, huddling, licking the pups, and nest building.

16.4 Music Mixing Board of the Seven Panksepp Emotional Traits

A music mixing board consists of separate volume control for many different soundtracks. Now imagine that each emotional trait has a separate sliding volume control knob. Each of the seven Panksepp emotional traits can be viewed as a separate channel on a music mixing board, where the ‘volume’ or intensity of each trait is determined by an interaction of inherited genetic factors, learning from previous experience and direct effects of experiences on nervous system reactivity (Fig. 16.1). An example of a genetic influence would be temperament in cattle (Voisinet et al., 1997). An example of a learned influence would be the benefits of low-stress cattle handling (Ligon, 2015). The probable effects of these two influences are either an inherited or learned reduction in fear. Neonatal handling experiments reviewed by Raineki et al. (2014) show that handling may have direct effects on the development of the nervous system by either deregulating or down-regulating different emotional traits. Recent work by Montag et al. (2017) supports the idea that the primary emotional systems may work as a continuum with variable strengths, providing support for the music mixing board as a model.

Recent studies in beef cattle that have been selected for ease of handling clearly show that cattle behavioral traits, like temperament and personality mentioned earlier, cannot be fully explained by fear levels. Wesley et al. (2012) recently demonstrated that when cattle were handled and restrained their cortisol levels were very low – between 5.5 ng/ml and 8.8 ng/ml. In contrast, older studies of beef cattle handling (reviewed by Grandin, 1997) found much higher levels of cortisol during restraint – ranging from 20 ng/ml to 60 ng/ml. This difference is likely due to the herd of the more recent study having been selected for calmness by using standard industry temperament tests. In an even more recent study, Reeves and Derner (2015) found that in cattle raised extensively on rangeland flight speed score had no effect on average daily gain – seeming to confirm the reduced fear over the past two decades of culling the most fearful animals. Reeves and Derner (2015) concluded that ranchers on extensive rangeland can now be less selective on temperament. Scoring beef cattle for temperament is now a common industry practice (Northcutt and Bowman, 2010).

Ranchers who operate in areas with lots of predators have used a simple but effective set of criteria for selecting range cows.

At the Lasater Ranch in Colorado, they used similar criteria with one added test: replacement heifers had to be willing to approach people and eat treats off the end of a stick. This resulted in a herd that would approach people and would seek out stroking (Grandin and Deesing, 2014). Using the Panksepp model, I hypothesize that they had selected for an increase of the Nurture and Seek traits.

Wesley et al. (2012) and Goodman et al. (2016) divided cattle into two behavior groups by using GPS tracking devices to monitor grazing behavior (see Table 16.1). I hypothesize that on the Seek trait the go getters are high and the laid-back cattle are low. A study with wild boars (Vetter et al., 2016) shows how differences in these personality traits may have a positive effect on the number of young raised to full independence. Mothers that had a greater exploratory drive (Seek) had more juvenile mortality when food was abundant, but not when food availability was reduced. It is likely that when food is scarce, greater exploratory behavior may help prevent starvation. However, when food is abundant, greater exploratory behavior may increase exposure to predators.

16.5 The Fear Factor

Veterinarians, animal scientists, and industry people often use the vague word ‘stress’ but the word ‘fear’ is often avoided. In the 10 years that has elapsed since the first edition of this text was published the word fear is more widely accepted, yet there remains some resistance to its use. The steer in a slaughter plant that refuses to move forward when it sees a shiny reflection is likely experiencing the emotion of fear. Numerous studies by Paul Hemsworth and his colleagues have shown that pigs and dairy cattle that fear people are less productive (Hemsworth and Coleman, 1998; Rushen and dePassille, 2015). Pigs and cattle that have been treated in an aversive manner, such as being slapped or shocked, will have lower productivity (Hemsworth and Barnett, 1991). Dairy cows that had been treated harshly also had larger flight zones and lower milk production (Breuer et al., 2000; Hemsworth et al., 2002). A newer study showed that animals will be more productive if they are cared for by stock people who have a positive attitude toward them (Kauppinen et al., 2012).

Reducing an animal’s fearfulness during handling and transport is an easy thing to do and requires no expensive equipment. During a 40-year career as a designer of livestock handling equipment, I have observed that people are often much more willing to make an expensive investment in equipment rather than learning behaviorally based, low-stress animal handling methods. Cattle handling has improved greatly in recent years (Woiwode et al., 2016) but there are still some people who continue to yell at animals and frequently use electric prods. Why do they continue to do this? Both research and practical experience shows that it costs money. It is difficult for some people to comprehend that what the animal experiences is important. I have observed that highly verbal people who have poor visual skills are often the ones who have the most difficulty understanding how an animal may think or feel. Since animals do not have verbal language, it is hard for these people to imagine that the animal feels fear in a manner comparable to humans (this concept is discussed in greater detail in Grandin and Johnson [2005]). However, research shows very clearly that the brain circuits that control fear are very similar in people and animals (LeDoux, 1996; Rogan and LeDoux, 1996). In some of his later papers, LeDoux questions animal emotions and calls them ‘survival circuits’, based on the hypothesis that verbal language is required to fully experience emotions (LeDoux and Brown, 2017). I disagree with this hypothesis and reasoning.

16.6 Fear Circuits in the Brain

Fear is a primary emotion in all animals and promotes survival by motivating animals to avoid predators and other threatening circumstances in the wild (Boissy, 1995; LeDoux, 1996; Boissy and Lee, 2014). All mammals and birds can be conditioned to fear things that are perceived as dangerous. The amygdala is the location of the central fear system involved in both fear behavior and learning to fear certain things or people (Davis, 1992). In humans, electrical stimulation of the amygdala elicits feelings of fear (Gloor et al., 1981). Stimulating the amygdala in the animal brain elicits nervous system responses similar to fear responses in humans (Redgate and Fahringer, 1973). Conversely, destroying the amygdala will block both unconditioned (unlearned) and conditioned (learned) fear responses (LeDoux, 1996; Rogan and LeDoux, 1996). Lesioning of the amygdala also had a taming effect on wild rats (Kemble et al., 1984). An example of an unlearned fear response would be a horse being spooked at the sound of a firecracker. A learned fear response has occurred if the horse refuses to enter the place where the firecracker went off. Fear learning takes place in a subcortical pathway; extinguishing a learned fear response is difficult because it requires the animal to suppress the fear memory via an active learning process. A single, very frightening or painful event can produce a strong learned fear response (see also Chapter 14, this volume), but eliminating this fear response is much more difficult (LeDoux, 1996). Accordingly, animals may develop fear memories that are difficult to eliminate.

The most recent research shows that the amygdala has separate circuits for a freezing fear response and an active flight response (Fadok et al., 2017). In some situations, a freezing response may be more adaptive than a flight response. There may also be genetic differences in how fearful cattle react. The author has observed that Bos indicus cattle are more likely to become tonic and immobile when restrained and certain genetic lines of Saler cattle have such an active response they may injure themselves when they are restrained.

16.7 Good First Experiences are Important

First experiences with new things make major and lasting impressions on animals, and it is important that an animal’s first experience with such things as a new corral, trailer, or restraining chute be pleasant in nature. My observations on cattle ranches have shown that to prevent cattle and sheep from becoming averse to and fearful of a new squeeze chute or corral system, painful or frightening procedures that cause visible signs of agitation should be avoided the first time the animals enter the facility (Grandin, 1997, 1998; Grandin and Shivley, 2015). In addition, practical experience has shown that if a horse has a frightening or painful experience the first time it goes into a trailer, teaching the animal to get in a trailer may be difficult. This happens because the horse has developed a fear memory.

When an animal is first brought into a new farm or laboratory, its first experiences should be made pleasant by feeding it and giving it time to settle down. Nonslip flooring is essential because slipping and falling in the new facility may create a fear memory. Locking head stanchions are often used for dairy cows because they make it easy to restrain the animals for vaccinations or artificial insemination. I have observed that they also work well for Angus beef cows on grass-fed beef farms in Ireland. To create a positive association with the stanchions, the animals are fed in the stanchions for 2 weeks before experiencing having their heads locked in. Separating the calves for vaccinations is then easy when the mothers are eating in the stanchions; the calves are vaccinated and returned before the cows realize they are gone.

16.8 Sensory Basis and Specificity of Fear Memories in Animals

Because I think in pictures rather than language, my autism allows me to closely relate to how an animal may think or feel (Grandin, 1995, 1997; Grandin and Johnson, 2005). Many practical experiences with animals indicate that fear memories are stored as pictures or sounds. Fear memories are often very specific. I observed a horse that was afraid of black cowboy hats because it had been abused by a person wearing such a hat (Grandin and Johnson, 2005), whereas white cowboy hats and baseball caps had no effect on this horse. The black hat was most threatening when it was on a person’s head and somewhat less threatening when it was on the ground. At a zoo, an elephant with a fear of bearded men became aggressive toward a new keeper who had a beard. The new keeper was accepted after he shaved off the beard.

Research published since the first edition continues to substantiate this specificity of animal learning. To horses, umbrellas and flapping tarps look totally different, and if a horse is carefully habituated to a suddenly opening umbrella this does not transfer to a flapping tarp (Leiner and Fendt, 2011). I have observed that cattle differentiate between a person on a horse and a person walking on the ground. Cattle that have been handled exclusively by people on horseback may panic if they are suddenly confronted with a person on the ground. It is important to train cattle that both people walking on the ground and people on horses are safe. Because cattle are visual thinkers, people on horses and people on the ground are perceived as different things.

The human voice can be a very specific stimulus for animals, and animals have the ability to distinguish between the voices of individual people. Animals that had been darted by the zoo veterinarian were able to recognize his voice, and they would run and hide. The opposite emotional effect has been seen by ranchers, who report that fearful cattle will often quiet down when they hear the voice of a familiar person who is associated with previous positive experiences. The auditory memories of animals are hyperspecific.

Research on animal perception indicates that cattle are able to differentiate between ‘good’ and ‘bad’ people. Animals have a tendency to associate bad experiences with prominent visual features on people such as beards (mentioned above) or lab coats, or they may associate a scary or painful experience with a specific place. For instance, pigs and cattle can recognize a person by the color of their clothing (Koba and Tanida, 1999; Rybarczyk et al., 2003) and can also learn that some places are safe and others are scary and bad. Cattle can learn that a certain person is scary or dangerous in a specific context (Rushen and dePassille, 2015). For example, the animal may see the person as bad only when that person is in the milking parlor because he gave injections there. Cooke et al. (2009) found that beef cattle that became acclimated to people being close to them while feeding did not display a reduction in agitated responses to handling in the corrals.

It is also possible for an animal to associate a painful or scary experience with a prominent feature in the environment. In one case, a young stallion fell down and was whipped during his first attempt to mount a dummy for semen collection. He developed a fear of overhead garage doors because he had been looking at one when he fell. A future collection was done easily when it was done outdoors away from buildings and garage doors. Unfortunately, a fear of something as common and unavoidable as garage doors can create problems when a horse is ridden.

Sometimes, problems with bucking or rearing in horses can be stopped by changing the type of bridle or saddle because the horse has a fear memory associated with the feeling of certain equipment. A different bridle or saddle feels different. In this case, the fear memory may be a ‘touch’ picture. For example, a horse that was abused with a jointed snaffle bit may tolerate a hackamore or a standard one-piece western bit. One horse had a sound fear memory because it had a bad experience with a canvas tarp; horse blankets that sounded like a tarp were scary, but a wool blanket that made little sound was well tolerated.

Animal fears may be very specific, but they also can generalize. One common generalization is that men are a threat to be avoided and women are safe. Fear of a man in blue coveralls can generalize to other people wearing blue coveralls. I was once asked how a fear memory can be a specific visual image if it can spread and generalize. I observed an example of both generalization and specificity in a dog named Red Dog. This dog developed a fear of hot air balloons after one flew over the house and its burner roared. Red Dog’s fear then spread to round plastic balls on electric lines. A few months later when she was riding in a car, she became afraid of the round rear end of a tanker truck and a round streetlight. I was puzzled why other round objects such as traffic lights and round globe lights on a building were tolerated. I finally figured out that the dog had made a very specific generalization. Round objects with the sky as a background had become feared because the original hot air balloon was a round object against the sky. The globe lights on the building had a brown brick background, and the traffic lights were mounted on a black metal rectangle; therefore, they were not round objects with a sky background.

16.9 Handling Training

Training animals to handling procedures and using feed rewards can greatly reduce agitation and make animal handling easier (Hutson, 1985). When an animal becomes accustomed to a procedure, fear will be reduced. Pigs will become easier to handle and transport if they become accustomed to people walking through their pens (Grandin, 1993). In my work, I have found that getting pigs accustomed to people walking among them makes it possible to greatly reduce electric prod use, which is highly detrimental to pig welfare (Benjamin et al., 2001) (Fig. 16.2). Pigs that have been walked in the aisles during finishing are easier to handle (Geverink et al., 1998; Goumon et al., 2013). Moving pigs a month prior to slaughter improved their willingness to move (Abbott et al., 1997).

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