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Is there any relationship between heartbeat rate and life span of an animal?

Is there any relationship between heartbeat rate and life span of an animal?


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Is there any relationship between heartbeat rate and life span of an animal?

Do they belong to a cause-and-effect relationship or are they both caused by some phenomenons or a common cause?


Interestingly there is a inverse negative correlation between heart rate and life span, meaning the faster your heart rate is, the shorter is your lifespan. See this figure (from the paper 2 cited below):

When the authors plotted the approximately total heartbeats vs. the lifespan, the amount of total heartbeats was in a pretty narrow corridor:

So it seems that at least the hearts in mammals have a maximum number of strokes they could do. The obvious question what causes this phenomenon is not really answered. Since the metabolism of small animals is (compared to their weight) higher and also their oxygen consumption is higher because of that, it is hypothesized that this causes more reactive oxygen species and related damage which subsequently leads to an earlier death.

See the references for more details:


There is a relationship: they are negatively correlated. Shorter-lived animals tend to have faster heartbeats, and longer-lived animals tend to have slower heartbeats. It gets more striking than that, however: they aren't just negatively correlated, they're approximately inversely proportional. A mouse, and an elephant, will both have around 1.5 billion heart beats before they die.

Poetic as this is, the relationship probably isn't causal. It's not that you have a given number of heartbeats, and when you use up your last one your heart dies of exhaustion. That would be silly.

It is illuminating to view the invariance as emerging from how both heart rate and lifespan scale allometrically with body size ($mass=W$).$^1$ Larger animals tend to have slower heart rates, and also tend to live longer; both relationships are in the form of power functions, whose exponents are multiples of $1/4$.

  • Heart rate ($R$) scales with a negative quarter power exponent: $R propto W^{-1/4}$
  • Lifespan ($E$) scales with a positive quarter power exponent: $E propto W^{1/4}$

"Total number of heartbeats in a lifetime" is just the product of heart rate and lifespan. As such, it should scale as

$R cdot E propto W^{-1/4} cdot W^{1/4}$

$R cdot E propto W^{-1/4+1/4}$

$R cdot E propto W^0$

$R cdot E propto 1$

That is: if $R$ and $E$ scale in these ways - which they do, approximately, within many taxa - then their product $R cdot E$, the total number of heartbeats in a lifetime, will be approximately invariant.

The question is why they scale in this way; and, beyond that, why the exponents in rate and time allometries are so ubiquitously multiples of $1/4$.

  • Does lifespan scale with $M^{1/4}$ because (for whatever reason) heart rate scales with $M^{-1/4}$; and your heart dies of exhaustion after a billion beats? (Call this the Heartbeat hypothesis.)
  • Does heart rate scale with $M^{-1/4}$ because (for whatever reason) lifespan scales with $M^{1/4}$; and, at the pearly gates, if the ledger says your heart beat 1.5 billion times before dying, you get a free t-shirt; and the heart likes t-shirts, but is also economical, beating as fast as necessary but no faster? (Call this the T-Shirt hypothesis; in my opinion it's barely sillier than the Heartbeat hypothesis.)
  • Does lifespan scale with $M^{1/4}$ because (for whatever reason) something else, like mass-specific metabolic rate, also scales with $M^{-1/4}$; and that something has damaging and life-shortening effects? (This was the once-popular Rate of Living theory.$^2$)
  • Does lifespan scale with $M^{1/4}$ because longer life causes selection for larger body size, in such a way that gets you the appropriate scaling? (Long-lived animals can afford to sexually mature later; maturing later means they have more time to grow, and will be bigger when they finally do mature. Apparently this can get you $M^{1/4}$ lifespan allometry if you combine it with certain assumptions about growth and fecundity, you model selection as happening in a stationary population, etc. This is sometimes called the Charnov model.$^3$)
  • Does heart rate scale with $M^{-1/4}$ because mass-specific metabolic rate does? Does mass-specific metabolic rate scale with $M^{-1/4}$ because heart rate does? (I dunno, these sound plausible? A cell's metabolism is fueled by stuff delivered to it by the blood stream, so it'd make sense for them to be proportional, right?)
  • Does mass-specific metabolic rate scale with $M^{-1/4}$ because that's how the optimum scales for efficient resource delivery through fractally branching networks like the bloodstream? (The proof is too math-y for me. This idea is the current mainstream explanation for why biological times and rates ubiquitously scale with exponents that are multiples of $1/4$, instead of eg. $1/3$ as you might expect if it were just to do with surface area / volume ratios. This is called the West, Brown & Enquist model.$^{1,4,5}$)

tl;dr: There is a striking negative correlation - specifically, an inverse proportionality - between heart rate and lifespan. But there's no particular reason to think it's causal, and both also correlate strikingly with a million other things. A lot of this has to do with how things scale with body size. Such scaling is called allometry; allometries are often power functions; for biological rates and times, the exponents of these power functions are often multiples of $1/4$ (as opposed to eg. $1/3$ or $1$). This quarter-power ubiquity in biology used to be mysterious, but now has been given an explanation (at least for the scaling of metabolic rate, which intuitively could do part of the explaining for other rates) by the West, Brown & Enquist model as being the result of optimally efficient resource delivery in fractally branching transportation networks.$^1$

The Heartbeat hypothesis is silly; presumably the approximate invariance of "1.5 billion heartbeats in a lifetime" comes from the $M^{-1/4}$ and $M^{1/4}$ scaling of heart rate and lifespan, themselves occurring for some other reason. I don't know but I assume the fractally-branching bloodstream explains the heart rate allometry. The lifespan allometry is more mysterious. It was once commonly thought to follow directly from the mass-specific metabolic rate allometry (Rate of Living theory), but that theory has fallen on hard times.$^2$ It has been given other potential explanations, notably the Charnov model which suggests that low mortality rates result in selection for a later age of maturity, giving animals more time to grow large.$^3$


  1. West, G. B. "The Origin of Universal Scaling Laws in Biology". Physica A, 1999.
  2. Austad, S. N. "Cats, 'Rats,' and Bats: The Comparative Biology of Aging in the 21st Century". Integrative and Comparative Biology, 2010.
  3. Charnov, E. L. "Evolution of Life History Variation Among Female Mammals". Proceedings of the National Academy of Sciences, 1991.
  4. West, G. B., Brown, J. H. and Enquist, B. J. "A General Model for the Origin of Allometric Scaling Laws in Biology". Science, 1997.
  5. Dawkins, R. and Wong, Y. "The Cauliflower's Tale" in The Ancestor's Tale, 2004.

Mechanisms of Premature Aging in Diabetes

The clinical and phenotypic similarities between aging and diabetes suggest that there may be shared biochemical pathways leading to the tissue changes. Glucose is the principal metabolic fuel for many animal species. In general, with few exceptions, the plasma glucose level in various animals is maintained within a narrow range (60-140 mg/dl). It is possible that the lower limit of blood glucose levels is determined by the minimum tissue requirements of metabolic fuel, and the upper limit defines the threshold beyond which glucotoxicity limits survival of the species (Mooradian and Thurman, 1999b). Avian species, especially owls and parrots, are the exception to this generalization. These animals have high blood glucose levels in the range of 250 to 350 mg/dl and yet have a relatively long life expectancy and show no signs of classical diabetic complications. The overall constancy of blood glucose levels across a wide range of animal species suggests that hyperglycemia, except in rare exceptions, is not compatible with healthy living. However, the lack of correlation between the maximum life span of species and the blood glucose levels raises doubts as to the fundamental role of glucose in the rate of aging. Nevertheless, it can be argued that interspecies comparisons are not necessarily relevant to the role of glucotoxicity. In addition, recent clinical studies indicate that there is a continuum in the relationship between tissue toxicity and serum glucose levels rather than there being a threshold of a glucose level beyond which diabetes complications emerge. Such data underscore the fundamental nature of glucotoxicity in animal biology.

The multiplicity of theories of aging makes it difficult to determine with any degree of certainty, the precise mechanism of premature aging in diabetes. However, several sentinel discoveries within the last three decades have shed light on the potential mechanisms of glucose-related toxicity and its effect on degenerative changes of aging. There are several biochemical mechanisms of glucotoxicity (Brownlee, 2001) (see Figure 56.1).

These include the polyol pathway, protein kinase C pathway, glycosylation pathway, and the oxidative pathway. These pathways, although conceptually separate, are interlinked biochemically (Brownlee, 2001). It has been suggested that a unifying hypothesis that incorporates these different pathways of glucotoxicity is hinged upon the mitochondrial generation of free radicals (Brownlee, 2001). According to this hypothesis, excess superoxide (oxidation pathway) partially inhibits the glycolytic enzyme GAPDH, thereby diverting upstream metabolites from glycolysis into pathways of glucose over utilization. This increases the flux of dihydroxyacetone phosphate (DHAP) to DAG, an activator of PKC (PKC activation pathway), and of triose phosphates to methyl-glyoxal, the main intracellular AGE precursor (glycation pathway). Increased flux of fructose-6-phosphate to UDP-N-acetylglucosamine increases modification of proteins by O-linked N-acetylglucosamine (GlcNAc) (hexosamine pathway), and increased glucose flux through the polyol pathway consumes NADPH and depletes GSH, thereby further aggravating the increased oxidative stress (Brownlee, 2001).

Some of the key mechanisms that may contribute to tissue changes in diabetes, and may also be involved in the aging, will be discussed. The relevance of polyol pathway in human disease has been controversial. The hexosamine pathway is an important pathway contributing to the pathogenesis of insulin resistance and diabetes complications. The glycolytic intermediate fructose-6-phosphate (Fruc-6-P) is converted to glucosamine-6-phosphate by the enzyme glutamine:fructose-6-phosphate amido-transferase (GFAT). Intracellular glycosylation of key transcription factors, such as Sp1, by the addition of N-acetylglucosamine (GlcNAc) to serine and threonine, is catalyzed by the enzyme O-GlcNAc transferase (OGT). These changes result in profound alterations in the expression of genes, such as plasminogen activator inhibitor-1 (PAI-1) and transforming growth factor beta-1 (TGF-^1) that are implicated in the emergence of some diabetic complications (Brownlee, 2001). The age-related changes in Sp1 are not concordant with the changes seen in diabetes. Thus, the polyol pathway and hexosamine pathway will not be discussed any further as they appear to be, at the present time, more uniquely related to diabetes rather than to aging.


The biggest hearts on Earth

Blue whales are the largest animals ever known to have lived on Earth. As full-grown adults, blue whales can measure more than 100 feet (30 meters) long, or roughly the size of two school buses parked bumper-to-bumper. It takes a big heart to power a creature that size while not actually large enough for a human to swim through, as an urban myth claims, one beached blue whale's heart weighed in at 400 pounds (180 kilograms) in 2015 and looked to be about the size of a golf cart.

Scientists already knew that a blue whale's pulse must slow down at depth. When air-breathing mammals dive underwater, their bodies automatically start redistributing oxygen hearts and brains get more O2, while muscles, skin and other organs get less. This allows animals to stay underwater longer on a single breath, and it results in a significantly lower heart rate than normal. This is as true for human landlubbers as it is for blue whales — however, given the whale's gargantuan size and proficiency at diving more than 1,000 feet (300 m) below the surface, their hearts are pushed to limits far beyond ours.

To find out exactly how much a blue whale's heart rate changes during a dive, the study authors followed a group of whales they'd previously studied in Monterey Bay, California, and tagged one with a special sensor mounted on the end of a 20-foot-long pole (6 m). The whale was a male first sighted 15 years ago. The sensor was a plastic, lunchbox-size shell equipped with four suction cups, two of which contained electrodes for measuring the whale's heartbeat.

The researchers tagged the whale with the sensor on their first attempt, and there it remained for the next 8.5 hours as the whale dove down and resurfaced on dozens of food-foraging missions. Most of this time was spent underwater: The whale's longest dive lasted 16.5 minutes and reached a maximum depth of 600 feet (184 m), while the whale never spent more than 4 minutes at the surface to refill its lungs.

The sensor showed that, at the lowest depths of each dive, the whale's heart was beating an average of four to eight times a minute, with a low of just two beats per minute. Between these low-tempo beats, the whale's stretchy aortic artery slowly contracted to keep oxygenated blood slowly moving through the animal's body, the researchers wrote.

Back at the surface, the whale's heart rate accelerated to a blistering 25 to 37 beats per minute, rapidly charging the animal's bloodstream with enough oxygen to support the next deep dive. During these rapid refueling stops, the whale's heart was working close to its physical limits, the study authors wrote — it's unlikely a whale's heart could beat any faster than that.

This natural cardiac limit may explain why blue whales max out at a certain size, and why there have never been any known animals on Earth any larger. Because a bigger creature would require even more oxygen to sustain its long, deep dives for sustenance, its heart would need to beat even faster than a blue whale's to refuel its body with oxygen at the surface.

According to the study authors, that doesn't seem possible based on the current data blue whales may have — now and forever — the hardest-working hearts on Earth.


Introduction

Social grooming is a widespread behavior among mammals, birds, and arthropods. Self-grooming is directed toward the individual’s own body, while allogrooming is carried out on others’ body parts, inaccessible or invisible to self-grooming. Although the primary biological function of allogrooming is to take care of the body surface of others, many studies demonstrated its social function in many animals (1𠄸) and especially in non-human primates [see Ref. (9) for a review].

The grooming among non-human primates is characterized by bimanual actions with rhythmic sweeps and plucking movements of the fingernails in precision grip, while being directed at addressing skin debris, spots, blemishes, ectoparasites, or vegetation trapped in the fur (10). Allogrooming is primary carried out to clean others’ body parts, inaccessible or invisible to self-grooming (11), and for the control of lice infection (12). Nevertheless, all non-human primates devote a significant amount of time grooming other individuals, suggesting that there is a reason behind this phenomenon, besides merely the hygiene function (13�). It has been hypothesized that the allogrooming is the most common affiliative relationship and social strategy to create and maintain relationships and reliable alliances in order to respond collectively to whatever environmental, physical, social, or predatory challenges they may face (18, 22�). Moreover, it was reported that allogrooming enhance relaxation and feelings of security (18), while simultaneously reducing anxiety levels (14, 25). These effects were supported by the investigation of physiological parameters, such as heart rate (HR) and cortisol levels. In particular, a decrement of the HR when receiving grooming (26, 27), and a reduction of the cortisol levels during both passive grooming (28) and active grooming (29) was demonstrated.

In addition to the numerous studies related to allogrooming, also the behavioral and physiological impact of grooming conducted by humans on monkeys or other animals has been explored. For example, the effect of human contact in horses (30), cats (31), dogs (32�), and in farm animals such as dairy cows (36), cattle, and lambs (37�) was investigated. These studies underlined that human grooming determined a positive effect in terms of autonomic responses (30, 33, 34, 39) but also in terms of behavior of the animals, for example, the interaction and the approach to humans (31, 33, 35, 37, 38).

Concerning non-human primates, Taira and Rolls (40) demonstrated that receiving grooming from humans is a positive reinforcement in operant conditioning for rhesus monkeys. However, there is no evidence regarding the psychophysiological consequences of human grooming on monkeys at the autonomous system level. Moreover, there is currently no evidence regarding the modulation of the heart rate variability (HRV) during either allogrooming or grooming by humans. Many human studies suggested that the HRV is an important indicator for the non-invasive assessment of autonomous nervous system activity in healthy people (41�), in patients with mental diseases (45, 46), cardiac dysfunction (47, 48), and stress (49). It was also demonstrated that HRV analysis provides a useful index for emotional states (50�). Analyzing HRV is also important in the veterinary field, as recently reviewed by von Borell (55), to assess the autonomous changes associated with pathological situation (56�), during stress and anxiety (60�), training situations (63, 64), and to detect emotional states (65�). In fact, pathological and psychological states may have an impact on the sympathovagal balance, detectable through HRV analysis and in the absence of any palpable changes in the mean of HR and/or respiration rates (41). Concerning non-human primates, HRV has only been used in pharmacological studies (44, 68), or to evaluate autonomic activations during task learning (69).

The aim of the present study was to investigate the physiological effect of human grooming to experimental non-human primates. We investigated the modulation of the HR and HRV of two experimental male rhesus monkeys receiving grooming by a familiar human (the experimenter) in relation to three different body parts (the chest, the mouth, and the arm).


Results

The inhibitory effects of wild-type and RGD-deficient IGFBP-2 on somatic growth observed at 10 weeks of age were also persistent in 30-week-old female mice (Fig. 1). In both age groups, the weight reductions of D-mice and E-mice in comparison with C-mice ranged between 8% and 13%. On a tissue level (Fig. 2), overexpression of wild-type IGFBP-2 in female D-mice resulted in stronger weight reductions in skeletal muscles than in the liver, heart, or brain, which is in accordance with previous results (Hoeflich et al., 1999 ). At 10 weeks of age, the effects of RGD-deficient IGFBP-2 in E-mice were comparable to those in D-mice for body weight and weights of isolated muscle, liver, heart, perinephric, brown fat, and gonadal fat. At 10 weeks of age, the negative effect of IGFBP-2 on the brain weight observed in D-mice was not reproduced in E-mice. Perinephric fat mass was particularly sensitive to the inhibitory effects of wild-type IGFBP-2 overexpression. At an age of 30 weeks, the effects of wild-type and mutant IGFBP-2 overexpression were significantly different. The absolute weight data and pairwise comparisons for both age groups are provided as Tables S1–S4. As identified by three independent studies in three different mouse facilities including 78 transgenic mice and 63 controls (Fig. 3A), overexpression of wild-type IGFBP-2 resulted in a significant increase of long-term survival in female D-mice (P < 0.05). The beneficial effects of elevated IGFBP-2 expression for maximal life length were observed in C57BL/6 (study I and III) and in mice of a mixed genetic background (50% C57BL/6, 50% NMRI study II). Consequently, this increase is not restricted to one defined inbred strain but is also present in a more complex genetic background. While growth restrictions were also present in male mice, ranging between 9% and 11% (Tables S2 and S4), in contrast to their female counterparts, male D-mice and E-mice had no increase in lifespan compared to sex-matched C-mice (Fig. 3B). In addition, progressive survival was higher (P = 0.002) in female but not in male D-mice (Fig. 4). While at an age of 831 days, 31% of all female D-mice were still alive, less than 6% of nontransgenic littermates had survived. However, the effects of IGFBP-2 on lifespan were dependent on the presence of the RGD-sequence in IGFBP-2 because in E-mice, no life-prolonging effect was observed (study IV lifespan E-mice: 765 ± 34 days, n = 19 lifespan C-mice: 750 ± 37 days, n = 33). It was next considered if reproductive development was altered in D- or E-mice. In fact, female D- but not E-mice were characterized by significantly delayed sexual maturity (Fig. 5). While in control mice, age at first estrus was 36.1 ± 1.1 days, D-mice reached an age of 42.9 ± 1.8 days before they came into their first estrus. By contrast, a delay of reproductive development was not found in E-mice (E-mice 37.0 ± 1.7 days). Age at vaginal opening was unaffected by the genotype. At an age of 10 weeks phosphorylation of Ser473 present in AKT was specifically increased in female brain lysates (Fig. 6) but not in liver, fat, or muscle tissues (data not shown) from D-mice compared to E-mice and controls.


  • Publisher &rlm : &lrm Joseph Henry Press (August 24, 2006)
  • Language &rlm : &lrm English
  • Hardcover &rlm : &lrm 278 pages
  • ISBN-10 &rlm : &lrm 0309096812
  • ISBN-13 &rlm : &lrm 978-0309096812
  • Item Weight &rlm : &lrm 1.29 pounds
  • Dimensions &rlm : &lrm 6.25 x 1.25 x 9.25 inches

Top reviews from the United States

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This book is all about the contributions of physics to biological systems. It take on from where
D'Arcy Thompson's "On Growth and Form" left off. It looks for the laws that govern biology - focusing on the laws not discovered by Darwin. It explores the causes of metabolic scaling laws, considers the relationship between the sizes of ecosystems and their diversity - and many similar topics. The book goes into the history of the topic in some detail.

The author subsequently went on to develop an interest in maximum entropy thermodynamics - and I was curious to see if there was any content relating to that in this book. There isn't really, and it's a pretty big omission - this is a big and important area where physics has something important and useful to say about biological systems.

The author is a great science writer. I'm sure he could make practically anything sound interesting. However, his topic here is fairly esoteric and technical - not all readers will be interested in the content. If you want to understand why metabolic rate scales with size to the power of 3/4 - and not the 2/3 you might naively expect - this book will tell you all about that in great detail. However, if this question merely evokes a "meh" from you, then you might be one of the yawning readers.

If you're interested in how physics applies to biology, you should read this - and something that covers maximum entropy thermodynamics.

The central question of this fascinating book is the precise role of energy in the living world.

Biology is in an interesting state of flux, with some visionary scientists believing that all biological processes are explainable by the laws of physics and mathematics. Meanwhile another group believes that quantum mechanics provides the best explanation for life process and a minority who think that we need to look elsewhere for an explanation of biological organization and function. In the middle is a very large group of teachers are researchers who are unfamiliar with the debates that are raging at scientific conferences and in the scholarly journals.

This is far from being an idle discussion: it has enormous implications for our understanding not only of biology, but also of health and disease. Wherever your sympathies lie in this ongoing debate, it is useful and important to know the current state of play in each of these different camps.

This book is an extremely well written and enthralling account of scientific discovery, that focuses on the efforts of a determined band of investigators who believe that they can - simply by using the currently known laws of physics and mathematics - build a unified theory of how living organisms function.

The idea that energy might be a unifying concept is not new. One of the first to discuss it was D'Arcy Wentworth Thompson who published a classic book on the topic - On Growth and Form - in 1917. In that book Thompson explored the effects of body size on life. Since larger animals need to expend more energy to do their day-to-day jobs, he began the study of metabolic rate and the way in which it sets the tempo for life processes. If metabolism slows, then so do all the processes in cells and organs. There is an almost linear relationship between metabolic rate and animal size: unicellular organs produce and require little energy a leopard or elephant requires an enormous amount. That much is obvious. But what is less obvious is that there is a precise mathematical formula, first discovered in the 1930s, that relates body mass and energy use.

This initial observation has been expanded over the years and some theorists now consider that metabolic energy is the common denominator in determining animal form and biodiversity.

For example, larger animal species require more food and land, and are therefore more vulnerable to extinction than smaller creatures. An argument that has been applied to the extinction of the dinosaurs and the eventual emergence of small, mobile proto-mammalian species. I was interested to learn that some biologists working in animal conservation have discovered a mathematical law linking the specific area within a region and the number of species that it can sustain. On the other hand, the simple formula linking body mass and metabolic rate is the most parsimonious explanation for the quickest way for an organism to keep its cells supplied with energy, given the way in which the geometry of transportation systems change with size.

Although this a book about biology, it is easy to see that many of the same principles apply in countless other situations, including supply lines for an army, or the provision of men and materials in a game of chess or soccer.

This book explores a number of important idea, though I remain doubtful that all biological phenomena can be explained so neatly. I still tend to favor the group of biologists who think that the ultimate solution to biological form and function requires a new - and a yet poorly defined - organizing principle.

This is science writing at its best, and I highly recommend the book to anyone interested in human and animal biology.


RESULTS AND DISCUSSION

Mass measurements

There was no significant change in X. gideon body mass during the experiments (F2,24=0.196 P=0.824 Njam=11, NK=9, NRb=4). The mean (±s.e.) body mass was 3.84±0.43 g for the jam diet, 4.15±0.43 g for the K + diet and 4.47±0.4 3g for the Rb + diet.

The effect of dietary K + and Rb + on 86 Rb washout

The rapid biological decay of 86 Rb in X. gideon on all three diets indicates that 86 Rb was being excreted, possibly through the same excretory processes as K + . The elimination of K + is a well-described aspect of insect iono-regulation (Schweikl et al., 1989 Wieczorek et al., 1989 Klein et al., 1991 Wieczorek et al., 1991 Maddrell and O'Donnell, 1992 Wieczorek, 1992 Zeiske, 1992 O'Donnell, 2008), and K + and Rb + are excreted through the same homeostatic processes (Ringer, 1884 Shoemaker et al., 1972 Lehninger, 1975 Metzler, 1977). The increased 86 Rb kb in beetles on both the K + and Rb + experimental diets compared with the jam diet suggests that increases in K + intake increase the 86 Rb kb. Furthermore, the turnover rates of both the K + and Rb + diet groups were the same, consistent with data reported by Fairbanks and Burch (Fairbanks and Burch, 1968), implying that, although 86 Rb is obviously analogous to Rb + , it is also an analogue of K + .

There was some variability around the general exponential decline (Fig. 1), where from day to day some measures tended to occasionally plateau, or sometimes increase at low levels of enrichment. This was probably a result of measurement variability, as small shifts in the posture of the beetles have higher proportional impacts on activity counts at low levels of enrichment. It is, however, also possible that the beetles managed to re-ingest some excreted 86 Rb isotope, and that their enrichment genuinely rose. Although this is a difficulty of using radioisotopes in contained and contaminated environments, it is unlikely to be a problem in the field, where excreted isotope should dissipate rapidly.

86 Rb washout curves of the Xylotrupes gideon control, K + and Rb + diet groups and the physical decay of 86 Rb over 25 days. Data are mean (±s.e.) percentage of initial enrichment, uncorrected for physical decay lines are non-linear least squares models of exponential decay for each diet.

86 Rb washout curves of the Xylotrupes gideon control, K + and Rb + diet groups and the physical decay of 86 Rb over 25 days. Data are mean (±s.e.) percentage of initial enrichment, uncorrected for physical decay lines are non-linear least squares models of exponential decay for each diet.

86 Rb kb, temperature and metabolic rate

The rate of CO2 production increased significantly with increasing ambient temperature (Ta) (F1,19=30.1, P=2.71×10 −5 Njam=5, NK=4), and there was no effect of diet (F1,19=0.031 P=0.862 Fig. 2A). At Ta=20°C the was 0.11±0.01 l day −1 , which increased to 0.15±0.01 l day −1 at 25°C and 0.18±0.01 l day −1 at 30°C on the jam diet. At Ta=20°C the was 0.11±5.0×10 −4 l day −1 , which increased to 0.16±0.005 l day −1 at 25°C and 0.18±0.02 l day −1 at 30°C on the K + diet.

The 86 Rb kb increased significantly with increasing Ta (F1,19=19.4, P=3.03×10 −4 Njam=5, NK=4), and was significantly higher on the K + -supplemented diet than on the jam diet at each Ta (F1,19=73.2 P=6.10×10 −8 Fig. 2B). At Ta=20°C the 86 Rb kb was 0.536±0.098 kb g, which increased to 0.656±0.119 kb g at 25°C and 0.964±0.078 kb g at 30°C on the jam diet. At Ta=20°C the 86 Rb kb was 1.22±0.108 kb g, which increased to 2.14±0.129 kb g at 25°C and 2.24±0.276 kb g at 30°C on the K + diet.

Although the washout trials established a link between K + excretion and 86 Rb kb, this is not informative of DEE, nor of any association between DEE and 86 Rb kb. Consistent with our expectations for an ectotherm (Lighton, 1996 Komai, 1998 Zhou et al., 2000 Acar et al., 2001 Woodman et al., 2007 Gibbs and Hoshizaki, 2008), DEE increased with increasing Ta. Furthermore, consistent with the expectation that 86 Rb kb should increase similarly to (A), and 86 Rb kb g (B). (C) The relationship between and 86 Rb kb g for K + and control diet. Linear trendlines are shown.

Interrelationships of isotopic and indirect calorimetric measures of metabolic rate. The effect of ambient temperature (Ta) on (A), and 86 Rb kb g (B). (C) The relationship between and 86 Rb kb g for K + and control diet. Linear trendlines are shown.

As there was no difference in the of the beetles on the control diet and the K + experimental diet, it is apparent that additional K + intake had no effect on DEE. However, consistent with the washout trials, the relationship of 86 Rb kb to Ta had a higher slope in the beetles receiving the K + diet to that in those receiving the jam diet. A more intuitive way of interpreting these data is that at the same Ta there was a higher 86 Rb kb in the K + experimental diet group than in the jam diet group. As was not different between the two groups, presumably the effect was related to K + elimination, independent of the role of K + in what we measured as the metabolic rate ( and 86 Rb kb for both the jam (F1,11=35.00 P=1.0×10 −3 ) and the K + diets (F1,8=64.33 P=4.3×10 −5 ). The relationship had a significantly higher slope, resulting in higher 86 Rb kb for a given , on the K + -enriched diet compared with the jam diet (F1,19=215.8 P=7.95×10 −12 Fig. 2C).

We have shown that 86 Rb kb is related to metabolic rate in an insect, and that the measure is changed when dietary [K + ] intake is altered. Buscarlet et al. (Buscarlet et al., 1974) stated that the biological half-life of radioisotopes in insects obeys the same laws as those regulating metabolism, and good correlations between metabolic rate and 86 Rb kb have been reported in vertebrates (Peters et al., 1995 Peters, 1996 Bradshaw and Bradshaw, 2007 Tomlinson et al., 2013). The results for the control jam diet were not congruent with a previous meta-analysis of 86 Rb kb for ectotherms (Tomlinson et al., 2013) (Fig. 3), registering at a lower elevation, with lower 86 Rb kb at a given . The data for X. gideon on the K + experimental diet, however, were congruent with those previous findings (Fig. 3). Deviations from the established pattern could be an artefact of elevated K + elimination to maintain ionic balance on the higher [K + ] diet, but this interpretation was not supported by the meta-analysis, where the K + -enriched diet group conformed to expectations. This raises two possibilities: either our jam diet had a lower [K + ] than is normal in the natural diet of X.gideon, or the previous published literature was based on animals receiving K + -enriched diets. While the [K + ] of our K + experimental diet was similar to the 1.81±0.14 mg g −1 reported by the USDA (USDA, 2004) for naturally occurring levels of K + in fruit, the [K + ] of jam was substantially lower (0.75 mg g −1 ). This suggests that our jam diet provided less than the normal dietary K + for the beetles, while our K + experimental diet in fact represents a more accurate control. Under such a scenario our data would be consistent with previous findings (Fig. 3). The dietary K + has not previously been controlled or reported in other studies. Such a confounding of comparative interpretation strengthens our recommendation that, although 86 Rb kb can be used to infer FMR in a broad range of taxa, dietary K + should be carefully controlled in any laboratory validations of the technique to mimic the [K + ] that a species will be consuming in the wild.

Results of a meta-analysis of 86 Rb biological turnover versus CO2 production in a range of ectothermic species. See Tomlinson et al. (Tomlinson et al., 2013) and references therein. The results for X. gideon on the jam diet (filled circles) were not consistent with the established relationship the results for those beetles on the K + diet (open circles) were consistent with these relationships.

Results of a meta-analysis of 86 Rb biological turnover versus CO2 production in a range of ectothermic species. See Tomlinson et al. (Tomlinson et al., 2013) and references therein. The results for X. gideon on the jam diet (filled circles) were not consistent with the established relationship the results for those beetles on the K + diet (open circles) were consistent with these relationships.

The mechanism of association between 86 Rb kb and DEE has been speculated to be the substitution of 86 Rb + for K + by the Na + /K + -ATPase that transports K + into, and Na + out of, cells in an active process that consumes ATP (Peters et al., 1995 Peters, 1996 Bradshaw and Bradshaw, 2007 Tomlinson et al., 2013). Peters et al. (Peters et al., 1995) extensively explored the possibilities that 86 Rb kb and 22 Na kb were co-correlated with both the metabolic rate and the dietary intake of the ions, and managed to separate the effectors for each isotope using statistical methods. While 22 Na kb was mostly influenced by food intake, 86 Rb kb was most strongly associated with DEE (Peters et al., 1995). Following the conclusions of Peters et al. (Peters et al., 1995), with some inferences from our data presented here, we speculate that, after the bolus of initial enrichment, the Na + /K + -ATPase transports most of the injected 86 Rb + into cells, thus entering an intracellular pool. The movement of K + (and 86 Rb + ) out of the cell should be directly proportional to the activity of the Na + /K + -ATPase, as intracellular K + is regulated. As the activity of the Na + /K + -ATPase comprises a large component of DEE (Withers, 1992), the rate of this exchange should increase or decrease proportionally with metabolic rate. An increase in dietary K + will result in an increase in the excretion of K + (and 86 Rb + ), and it is the extracellular fluid that is filtered by the Malpighian tubule system to produce excreta. The mechanism suggested is that 86 Rb + is released from the cell at a rate that is proportional to metabolic rate, and the rate of excretion of K + (and 86 Rb + ) from the extracellular fluid is proportional to K + intake. When 86 Rb + leaves the cell, some of it will be excreted, while some will return to the intracellular fluid via the Na + /K + -ATPase. If the rate of excretion of K + (and 86 Rb + ) from the extracellular fluid increases when K + intake increases, then the balance of 86 Rb + exchange between the intracellular and extracellular pools is altered. While the transfer of 86 Rb + from the intracellular to the extracellular pool remains constant, more of that 86 Rb + will be excreted from the extracellular pool, reducing the probability of a given molecule of 86 Rb + being transported back to the intracellular pool via Na + /K + -ATPase, and increasing its probability of being excreted. While there is a constant movement of 86 Rb from the intracellular to the extracellular fluid in proportion to metabolic rate, the excretion of 86 Rb from the extracellular fluid increases when K + intake increases. The association of 22 Na with food intake probably results from 22 Na being maintained mostly in the extracellular body pool that is regulated in response to ionic intake with food, and is only tangentially influenced by the Na + /K + -ATPase and metabolic rate.

Conclusion

FMR is a useful ecological measurement because it quantifies the energetic link between a species and its environment. It can be used to understand the impacts of temperature and climate (Anderson and Jetz, 2005), reproduction (Fyhn et al., 2001 Bevan et al., 2002 Jodice et al., 2003), ecosystem productivity (Bradshaw and Bradshaw, 1999 Bradshaw and Bradshaw, 2007 Bradshaw et al., 2007), dispersal (Clusella Trullas et al., 2006) and anthropogenic disturbance upon a species of interest. Although the DLW method has broad support and application for measuring FMR, the technique has theoretical and practical limits, where some species and habitats are not suitable for the technique (for review, see Tomlinson et al., 2013). The biological turnover of radioactive 86 Rb has been proposed as an alternative that avoids some of the limitations of DLW, and may be applicable to taxa that are unsuitable for DLW (Peters et al., 1995 Peters, 1996 Bradshaw and Bradshaw, 2007 Tomlinson et al., 2013). A problem with using 86 Rb kb as a measure of an animal's metabolism is a lack of understanding of the mechanistic link between metabolism and the turnover of 86 Rb (Bradshaw and Bradshaw, 2007 Tomlinson et al., 2013). One suggested mechanistic pathway is that Rb + turnover is related to K + turnover, and we here provide some evidence to support that contention.

Measurement of 86 Rb kb is a cheap, non-invasive and practical technique to measure DEE and FMR in small vertebrates and insects. We found that the 86 Rb kb was influenced by dietary levels of K + and Rb + , but that changes in the intake of these ions did not affect . Although there were significant relationships between and 86 Rb kb, the relationship was different in beetles on the different diets, presumably as a result of the influence of K + elimination upon 86 Rb kb. These data support the likelihood that 86 Rb kb is related to DEE and FMR via the action of the ubiquitous Na + /K + -ATPase. Future calibrations of 86 Rb kb with will need to control [K + ] intake to natural levels in order to maximise the accuracy of the relationship between 86 Rb kb and DEE to make it ecologically relevant as a measure of FMR.


Contents

The English "wolf" stems from the Old English wulf, which is itself thought to be derived from the Proto-Germanic *wulfaz. The Proto-Indo-European root * wĺ̥kʷos may also be the source of the Latin word for the animal lupus (* lúkʷos ). [4] [5] The name "gray wolf" refers to the grayish colour of the species. [6]

Since pre-Christian times, Germanic peoples such as the Anglo-Saxons took on wulf as a prefix or suffix in their names. Examples include Wulfhere ("Wolf Army"), Cynewulf ("Royal Wolf"), Cēnwulf ("Bold Wolf"), Wulfheard ("Wolf-hard"), Earnwulf ("Eagle Wolf"), Wulfstān ("Wolf Stone") Æðelwulf ("Noble Wolf"), Wolfhroc ("Wolf-Frock"), Wolfhetan ("Wolf Hide"), Isangrim ("Gray Mask"), Scrutolf ("Garb Wolf"), Wolfgang ("Wolf Gait") and Wolfdregil ("Wolf Runner"). [7]

In 1758, the Swedish botanist and zoologist Carl Linnaeus published in his Systema Naturae the binomial nomenclature. [3] Canis is the Latin word meaning "dog", [9] and under this genus he listed the doglike carnivores including domestic dogs, wolves, and jackals. He classified the domestic dog as Canis familiaris, and the wolf as Canis lupus. [3] Linnaeus considered the dog to be a separate species from the wolf because of its "cauda recurvata" (upturning tail) which is not found in any other canid. [10]

Subspecies

In the third edition of Mammal Species of the World published in 2005, the mammalogist W. Christopher Wozencraft listed under C. lupus 36 wild subspecies, and proposed two additional subspecies: familiaris (Linnaeus, 1758) and dingo (Meyer, 1793). Wozencraft included hallstromi—the New Guinea singing dog—as a taxonomic synonym for the dingo. Wozencraft referred to a 1999 mitochondrial DNA study as one of the guides in forming his decision, and listed the 38 subspecies of C. lupus under the biological common name of "wolf", the nominate subspecies being the Eurasian wolf (C. l. lupus) based on the type specimen that Linnaeus studied in Sweden. [11] Studies using paleogenomic techniques reveal that the modern wolf and the dog are sister taxa, as modern wolves are not closely related to the population of wolves that was first domesticated. [12] In 2019, a workshop hosted by the IUCN/Species Survival Commission's Canid Specialist Group considered the New Guinea singing dog and the dingo to be feral dogs Canis familiaris, and therefore should not be assessed for the IUCN Red List. [13]

Evolution

The phylogenetic descent of the extant wolf C. lupus from C. etruscus through C. mosbachensis is widely accepted. [14] The earliest fossils of C. lupus were found in what was once eastern Beringia at Old Crow, Yukon, Canada, and at Cripple Creek Sump, Fairbanks, Alaska. The age is not agreed upon but could date to one million years ago. Considerable morphological diversity existed among wolves by the Late Pleistocene. They had more robust skulls and teeth than modern wolves, often with a shortened snout, a pronounced development of the temporalis muscle, and robust premolars. It is proposed that these features were specialized adaptations for the processing of carcass and bone associated with the hunting and scavenging of Pleistocene megafauna. Compared with modern wolves, some Pleistocene wolves showed an increase in tooth breakage similar to that seen in the extinct dire wolf. This suggests they either often processed carcasses, or that they competed with other carnivores and needed to consume their prey quickly. Compared with those found in the modern spotted hyena, the frequency and location of tooth fractures in these wolves indicates they were habitual bone crackers. [15] In June 2019, the severed yet preserved head of a Pleistocene wolf, dated to over 40,000 years ago, was found close to the Tirekhtyakh River in Yakutia, Russia, near the Arctic Circle. The head was about 16 in (41 cm) long, much bigger than a modern wolf's head.

Genomic studies suggest modern wolves and dogs descend from a common ancestral wolf population [16] [17] [18] that existed 20,000 years ago. [16] Studies in 2017 and 2018 found that the Himalayan wolf is part of a lineage that is basal to other wolves and split from them 691,000–740,000 years ago. [19] [20] Other wolves appear to have originated in Beringia in an expansion that was driven by the huge ecological changes during the close of the Late Pleistocene. [20] A study in 2016 indicates that a population bottleneck was followed by a rapid radiation from an ancestral population at a time during, or just after, the Last Glacial Maximum. This implies the original morphologically diverse wolf populations were out-competed and replaced by more modern wolves. [21]

A 2016 genomic study suggests that Old World and New World wolves split around 12,500 years ago followed by the divergence of the lineage that led to dogs from other Old World wolves around 11,100–12,300 years ago. [18] An extinct Late Pleistocene wolf may have been the ancestor of the dog, [22] [15] with the dog's similarity to the extant wolf being the result of genetic admixture between the two. [15] The dingo, Basenji, Tibetan Mastiff and Chinese indigenous breeds are basal members of the domestic dog clade. The divergence time for wolves in Europe, the Middle East, and Asia is estimated to be fairly recent at around 1,600 years ago. Among New World wolves, the Mexican wolf diverged around 5,400 years ago. [18]

Admixture with other canids

In the distant past, there has been gene flow between African golden wolves, golden jackals, and gray wolves. The African golden wolf is a descendant of a genetically admixed canid of 72% wolf and 28% Ethiopian wolf ancestry. One African golden wolf from the Egyptian Sinai Peninsula shows admixture with Middle Eastern wolves and dogs. [23] There is evidence of gene flow between golden jackals and Middle Eastern wolves, less so with European and Asian wolves, and least with North American wolves. This indicates the golden jackal ancestry found in North American wolves may have occurred before the divergence of the Eurasian and North American wolves. [24]

The common ancestor of the coyote and the wolf has admixed with a ghost population of an extinct unidentified canid. This canid is genetically close to the dhole and evolved after the divergence of the African hunting dog from the other canid species. The basal position of the coyote compared to the wolf is proposed to be due to the coyote retaining more of the mitochondrial genome of this unidentified canid. [23] Similarly, a museum specimen of a wolf from southern China collected in 1963 showed a genome that was 12–14% admixed from this unknown canid. [25] In North America, most coyotes and wolves show varying degrees of past genetic admixture. The red wolf of the southeastern United States is a hybrid animal with 40%:60% wolf to coyote ancestry. In addition, there was found to be 60%:40% wolf to coyote genetics in Eastern timber wolves, and 75%:25% in the Great Lakes region wolves. [24]

In more recent times, some male Italian wolves originated from dog ancestry, which indicates female wolves will breed with male dogs in the wild. [26] In the Caucasus Mountains, ten percent of dogs including livestock guardian dogs, are first generation hybrids. [27] Although mating between golden jackals and wolves has never been observed, evidence of jackal-wolf hybridization was discovered through mitochondrial DNA analysis of jackals living in the Caucasus Mountains [27] and in Bulgaria. [28]

In 2021, a genetic study found that the dog's similarity to the extant gray wolf was the result of substantial dog-into-wolf gene flow, with almost negligible wolf-into-dog gene flow since the dog's domestication. Some gray wolves were related to all ancient and modern dogs. [29]

The wolf is the largest extant member of the Canidae family, [30] and is further distinguished from coyotes and jackals by a broader snout, shorter ears, a shorter torso and a longer tail. [31] [30] It is slender and powerfully built, with a large, deeply descending rib cage, a sloping back, and a heavily muscled neck. [32] The wolf's legs are moderately longer than those of other canids, which enables the animal to move swiftly, and to overcome the deep snow that covers most of its geographical range in winter. [33] The ears are relatively small and triangular. [32] The wolf's head is large and heavy, with a wide forehead, strong jaws and a long, blunt muzzle. [34] The skull is 230–280 mm (9–11 in) in length and 130–150 mm (5–6 in) in width. [35] The teeth are heavy and large, making them better suited to crushing bone than those of other canids. They are not as specialized as those found in hyenas though. [36] [37] Its molars have a flat chewing surface, but not to the same extent as the coyote, whose diet contains more vegetable matter. [38] Females tend to have narrower muzzles and foreheads, thinner necks, slightly shorter legs, and less massive shoulders than males. [39]

Pelage

The wolf has very dense and fluffy winter fur, with a short undercoat and long, coarse guard hairs. [34] Most of the undercoat and some guard hairs are shed in spring and grow back in autumn. [43] The longest hairs occur on the back, particularly on the front quarters and neck. Especially long hairs grow on the shoulders and almost form a crest on the upper part of the neck. The hairs on the cheeks are elongated and form tufts. The ears are covered in short hairs and project from the fur. Short, elastic and closely adjacent hairs are present on the limbs from the elbows down to the calcaneal tendons. [34] The winter fur is highly resistant to the cold. Wolves in northern climates can rest comfortably in open areas at −40 °C (−40 °F) by placing their muzzles between the rear legs and covering their faces with their tail. Wolf fur provides better insulation than dog fur and does not collect ice when warm breath is condensed against it. [43]

A wolf's coat colour is determined by its guard hairs. Wolves usually have some hairs that are white, brown, gray and black. [46] The coat of the Eurasian wolf is a mixture of ochreous (yellow to orange) and rusty ochreous (orange/red/brown) colours with light gray. The muzzle is pale ochreous gray, and the area of the lips, cheeks, chin, and throat is white. The top of the head, forehead, under and between the eyes, and between the eyes and ears is gray with a reddish film. The neck is ochreous. Long, black tips on the hairs along the back form a broad stripe, with black hair tips on the shoulders, upper chest and rear of the body. The sides of the body, tail, and outer limbs are a pale dirty ochreous colour, while the inner sides of the limbs, belly, and groin are white. Apart from those wolves which are pure white or black, these tones vary little across geographical areas, although the patterns of these colours vary between individuals. [47]

In North America, the coat colours of wolves follow Gloger's rule, wolves in the Canadian arctic being white and those in southern Canada, the U.S., and Mexico being predominantly gray. In some areas of the Rocky Mountains of Alberta and British Columbia, the coat colour is predominantly black, some being blue-gray and some with silver and black. [46] Differences in coat colour between sexes is absent in Eurasia [48] females tend to have redder tones in North America. [49] Black-coloured wolves in North America acquired their colour from wolf-dog admixture after the first arrival of dogs across the Bering Strait 12,000 to 14,000 years ago. [50] Research into the inheritance of white colour from dogs into wolves has yet to be undertaken. [51]

Distribution and habitat

Wolves occurred originally across Eurasia and North America. Deliberate human persecution because of livestock predation and fear of attacks on humans has reduced the wolf's range to about one-third of what it once was. The wolf is now extirpated (locally extinct) in much of Western Europe, the United States and Mexico, and in Japan. In modern times, the wolf occurs mostly in wilderness and remote areas. The wolf can be found between sea level and 3,000 m (9,800 ft). Wolves live in forests, inland wetlands, shrublands, grasslands (including Arctic tundra), pastures, deserts, and rocky peaks on mountains. [2] Habitat use by wolves depends on the abundance of prey, snow conditions, livestock densities, road densities, human presence and topography. [38]

Like all land mammals that are pack hunters, the wolf feeds predominantly on wild herbivorous hoofed mammals that can be divided into large size 240–650 kg (530–1,430 lb) and medium size 23–130 kg (51–287 lb), and have a body mass similar to that of the combined mass of the pack members. [52] [53] The wolf specializes in preying on the vulnerable individuals of large prey, [38] with a pack of 15 able to bring down an adult moose. [54] The variation in diet between wolves living on different continents is based on the variety of hoofed mammals and of available smaller and domesticated prey. [55]

In North America, the wolf's diet is dominated by wild large hoofed mammals (ungulates) and medium-sized mammals. In Asia and Europe, their diet is dominated by wild medium-sized hoofed mammals and domestic species. The wolf depends on wild species, and if these are not readily available, as in Asia, the wolf is more reliant on domestic species. [55] Across Eurasia, wolves prey mostly on moose, red deer, roe deer and wild boar. [56] In North America, important range-wide prey are elk, moose, caribou, white-tailed deer and mule deer. [57] Wolves can digest their meal in a few hours and can feed several times in one day, making quick use of large quantities of meat. [58] A well-fed wolf stores fat under the skin, around the heart, intestines, kidneys, and bone marrow, particularly during the autumn and winter. [59]

Nonetheless, wolves are not fussy eaters. Smaller-sized animals that may supplement their diet include rodents, hares, insectivores and smaller carnivores. They frequently eat waterfowl and their eggs. When such foods are insufficient, they prey on lizards, snakes, frogs, and large insects when available. [60] Wolves in northern Minnesota prey on northern pike in freshwater streams. [61] The diet of coastal wolves in Alaska includes 20% salmon, [62] while those of coastal wolves in British Columbia includes 25% marine sources, and those on the nearby islands 75%. [63]

In Europe, wolves eat apples, pears, figs, melons, berries and cherries. In North America, wolves eat blueberries and raspberries. Wolves also eat grass, which may provide some vitamins, but is most likely used mainly to induce vomiting to rid themselves of intestinal parasites or long guard hairs. [64] They are known to eat the berries of mountain-ash, lily of the valley, bilberries, cowberries, European black nightshade, grain crops, and the shoots of reeds. [60]

In times of scarcity, wolves will readily eat carrion. [60] In Eurasian areas with dense human activity, many wolf populations are forced to subsist largely on livestock and garbage. [56] Prey in North America continue to occupy suitable habitats with low human density, the wolves eating livestock and garbage only in dire circumstances. [65] Cannibalism is not uncommon in wolves during harsh winters, when packs often attack weak or injured wolves and may eat the bodies of dead pack members. [60] [66] [67]

Interactions with other predators

Wolves typically dominate other canid species in areas where they both occur. In North America, incidents of wolves killing coyotes are common, particularly in winter, when coyotes feed on wolf kills. Wolves may attack coyote den sites, digging out and killing their pups, though rarely eating them. There are no records of coyotes killing wolves, though coyotes may chase wolves if they outnumber them. [68] According to a press release by the U.S. Department of Agriculture in 1921, the infamous Custer Wolf relied on coyotes to accompany him and warn him of danger. Though they fed from his kills, he never allowed them to approach him. [69] Interactions have been observed in Eurasia between wolves and golden jackals, the latter's numbers being comparatively small in areas with high wolf densities. [34] [68] [70] Wolves also kill red, Arctic and corsac foxes, usually in disputes over carcasses, sometimes eating them. [34] [71]

Brown bears typically dominate wolf packs in disputes over carcasses, while wolf packs mostly prevail against bears when defending their den sites. Both species kill each other's young. Wolves eat the brown bears they kill, while brown bears seem to eat only young wolves. [72] Wolf interactions with American black bears are much rarer because of differences in habitat preferences. Wolves have been recorded on numerous occasions actively seeking out American black bears in their dens and killing them without eating them. Unlike brown bears, American black bears frequently lose against wolves in disputes over kills. [73] Wolves also dominate and sometimes kill wolverines, and will chase off those that attempt to scavenge from their kills. Wolverines escape from wolves in caves or up trees. [74]

Wolves may interact and compete with felids, such as the Eurasian lynx, which may feed on smaller prey where wolves are present [75] and may be suppressed by large wolf populations. [76] Wolves encounter cougars along portions of the Rocky Mountains and adjacent mountain ranges. Wolves and cougars typically avoid encountering each other by hunting at different elevations for different prey (niche partitioning). In winter, when snow accumulation forces their prey into valleys, interactions between the two species become more likely. Wolves in packs usually dominate cougars and can steal their kills or even kill them, [77] while one-to-one encounters tend to be dominated by the cat. There are several documented cases of cougars killing wolves. [78] Wolves more broadly affect cougar population dynamics and distribution by dominating territory and prey opportunities and disrupting the feline's behaviour. [79] Wolf and Siberian tiger interactions are well-documented in the Russian Far East, where tigers significantly depress wolf numbers, sometimes to the point of localized extinction. Only human depletion of tiger numbers appears to protect wolves from competitive exclusion from them. With perhaps only four proven records of tigers killing wolves, these cases are rare attacks appear to be competitive rather than predatory in nature. [80] [75]

In Israel, Central Asia and India wolves may encounter striped hyenas, usually in disputes over carcasses. Striped hyenas feed extensively on wolf-killed carcasses in areas where the two species interact. One-to-one, hyenas dominate wolves, and may prey on them, [81] but wolf packs can drive off single or outnumbered hyenas. [82] [83] There is at least one case in Israel of a hyena associating and cooperating with a wolf pack. It is proposed that the hyena could benefit from the wolves' superior ability to hunt large, agile prey. The wolves could benefit from the hyena's superior sense of smell, to locate and dig out tortoises, to crack open large bones, and to tear open discarded food containers like tin cans. [84]

Social structure

The wolf is a social animal. [34] Its populations consist of packs and lone wolves, most lone wolves being temporarily alone while they disperse from packs to form their own or join another one. [85] The wolf's basic social unit is the nuclear family consisting of a mated pair accompanied by their offspring. [34] The average pack size in North America is eight wolves and in Europe 5.5 wolves. [41] The average pack across Eurasia consists of a family of eight wolves (two adults, juveniles, and yearlings), [34] or sometimes two or three such families, [38] with examples of exceptionally large packs consisting of up to 42 wolves being known. [86] Cortisol levels in wolves rise significantly when a pack member dies, indicating the presence of stress. [87] During times of prey abundance caused by calving or migration, different wolf packs may join together temporarily. [34]

Offspring typically stay in the pack for 10–54 months before dispersing. [88] Triggers for dispersal include the onset of sexual maturity and competition within the pack for food. [89] The distance travelled by dispersing wolves varies widely some stay in the vicinity of the parental group, while other individuals may travel great distances of upwards of 206 km (128 mi), 390 km (240 mi), and 670 km (420 mi) from their natal (birth) packs. [90] A new pack is usually founded by an unrelated dispersing male and female, travelling together in search of an area devoid of other hostile packs. [91] Wolf packs rarely adopt other wolves into their fold and typically kill them. In the rare cases where other wolves are adopted, the adoptee is almost invariably an immature animal of one to three years old, and unlikely to compete for breeding rights with the mated pair. This usually occurs between the months of February and May. Adoptee males may mate with an available pack female and then form their own pack. In some cases, a lone wolf is adopted into a pack to replace a deceased breeder. [86]

Wolves are territorial and generally establish territories far larger than they require to survive assuring a steady supply of prey. Territory size depends largely on the amount of prey available and the age of the pack's pups. They tend to increase in size in areas with low prey populations, [92] or when the pups reach the age of six months when they have the same nutritional needs as adults. [93] Wolf packs travel constantly in search of prey, covering roughly 9% of their territory per day, on average 25 km/d (16 mi/d). The core of their territory is on average 35 km 2 (14 sq mi) where they spend 50% of their time. [92] Prey density tends to be much higher on the territory's periphery. Except out of desperation, wolves tend to avoid hunting on the fringes of their range to avoid fatal confrontations with neighbouring packs. [94] The smallest territory on record was held by a pack of six wolves in northeastern Minnesota, which occupied an estimated 33 km 2 (13 sq mi), while the largest was held by an Alaskan pack of ten wolves encompassing 6,272 km 2 (2,422 sq mi). [93] Wolf packs are typically settled, and usually leave their accustomed ranges only during severe food shortages. [34]

Wolves advertise their territories to other packs through howling and scent marking. Scent marking involves urine, feces, and anal gland scents. This is more effective at advertising territory than howling and is often used in combination with scratch marks. Wolves increase their rate of scent marking when they encounter the marks of wolves from other packs. Lone wolves will rarely mark, but newly bonded pairs will scent mark the most. [38] These marks are generally left every 240 m (260 yd) throughout the territory on regular travelways and junctions. Such markers can last for two to three weeks, [93] and are typically placed near rocks, boulders, trees, or the skeletons of large animals. [34] Territorial fights are among the principal causes of wolf mortality, one study concluding that 14–65% of wolf deaths in Minnesota and the Denali National Park and Preserve were due to other wolves. [95]

Wolves communicate to anticipate what their pack mates or other wolves might do next. [96] This includes the use of vocalization, body posture, scent, touch, and taste. [97] The phases of the moon have no effect on wolf vocalization, and despite popular belief, wolves do not howl at the moon. [98] Wolves howl to assemble the pack usually before and after hunts, to pass on an alarm particularly at a den site, to locate each other during a storm, while crossing unfamiliar territory, and to communicate across great distances. [99] Wolf howls can under certain conditions be heard over areas of up to 130 km 2 (50 sq mi). [38] Other vocalizations include growls, barks and whines. Wolves do not bark as loudly or continuously as dogs do in confrontations, rather barking a few times and then retreating from a perceived danger. [100] Aggressive or self-assertive wolves are characterized by their slow and deliberate movements, high body posture and raised hackles, while submissive ones carry their bodies low, flatten their fur, and lower their ears and tail. [101] Raised leg urination is considered to be one of the most important forms of scent communication in the wolf, making up 60–80% of all scent marks observed. [102]

Reproduction

Wolves are monogamous, mated pairs usually remaining together for life. Should one of the pair die, another mate is found quickly. [103] With wolves in the wild, inbreeding does not occur where outbreeding is possible. [104] Wolves become mature at the age of two years and sexually mature from the age of three years. [103] The age of first breeding in wolves depends largely on environmental factors: when food is plentiful, or when wolf populations are heavily managed, wolves can rear pups at younger ages to better exploit abundant resources. Females are capable of producing pups every year, one litter annually being the average. [105] Oestrus and rut begin in the second half of winter and lasts for two weeks. [103]

Dens are usually constructed for pups during the summer period. When building dens, females make use of natural shelters like fissures in rocks, cliffs overhanging riverbanks and holes thickly covered by vegetation. Sometimes, the den is the appropriated burrow of smaller animals such as foxes, badgers or marmots. An appropriated den is often widened and partly remade. On rare occasions, female wolves dig burrows themselves, which are usually small and short with one to three openings. The den is usually constructed not more than 500 m (550 yd) away from a water source. It typically faces southwards where it can be better warmed by sunlight exposure, and the snow can thaw more quickly. Resting places, play areas for the pups, and food remains are commonly found around wolf dens. The odor of urine and rotting food emanating from the denning area often attracts scavenging birds like magpies and ravens. Though they mostly avoid areas within human sight, wolves have been known to nest near domiciles, paved roads and railways. [106] During pregnancy, female wolves remain in a den located away from the peripheral zone of their territories, where violent encounters with other packs are less likely to occur. [107]

Hunting and feeding

Single wolves or mated pairs typically have higher success rates in hunting than do large packs single wolves have occasionally been observed to kill large prey such as moose, bison and muskoxen unaided. [112] [113] This contrasts with the commonly held belief that larger packs benefit from cooperative hunting to bring down large game. [113] The size of a wolf hunting pack is related to the number of pups that survived the previous winter, adult survival, and the rate of dispersing wolves leaving the pack. The optimal pack size for hunting elk is four wolves, and for bison a large pack size is more successful. [114]

Wolves move around their territory when hunting, using the same trails for extended periods. After snowfalls, wolves find their old trails and continue using them. These follow the banks of rivers, the shorelines of lakes, ravines overgrown with shrubs, plantations, or roads and human paths. [115] Wolves are nocturnal predators. During the winter, a pack will commence hunting in the twilight of early evening and will hunt all night, traveling tens of kilometres. Sometimes hunting large prey occurs during the day. During the summer, wolves generally tend to hunt individually, ambushing their prey and rarely giving pursuit. [116]

When hunting large gregarious prey, wolves will try to isolate an individual from its group. [117] If successful, a wolf pack can bring down game that will feed it for days, but one error in judgement can lead to serious injury or death. Most large prey have developed defensive adaptations and behaviours. Wolves have been killed while attempting to bring down bison, elk, moose, muskoxen, and even by one of their smallest hoofed prey, the white-tailed deer. With smaller prey like beaver, geese, and hares, there is no risk to the wolf. [118] Although people often believe wolves can easily overcome any of their prey, their success rate in hunting hoofed prey is usually low. [119]

Once prey is brought down, wolves begin to feed excitedly, ripping and tugging at the carcass in all directions, and bolting down large chunks of it. [122] The breeding pair typically monopolizes food to continue producing pups. When food is scarce, this is done at the expense of other family members, especially non-pups. [123] The breeding pair typically eats first. They usually work the hardest at killing prey, and may rest after a long hunt and allow the rest of the family to eat undisturbed. Once the breeding pair has finished eating, the rest of the family tears off pieces of the carcass and transports them to secluded areas where they can eat in peace. Wolves typically commence feeding by consuming the larger internal organs, like the heart, liver, lungs, and stomach lining. The kidneys and spleen are eaten once they are exposed, followed by the muscles. [124] A wolf can eat 15–19% of its body weight in a single feeding. [59]

Viral and bacterial

Viral diseases carried by wolves include: rabies, canine distemper, canine parvovirus, infectious canine hepatitis, papillomatosis, and canine coronavirus. [125] Wolves are a major host for rabies in Russia, Iran, Afghanistan, Iraq and India. [126] In wolves, the incubation period is eight to 21 days, and results in the host becoming agitated, deserting its pack, and travelling up to 80 km (50 mi) a day, thus increasing the risk of infecting other wolves. Infected wolves do not show any fear of humans, most documented wolf attacks on people being attributed to rabid animals. Although canine distemper is lethal in dogs, it has not been recorded to kill wolves, except in Canada and Alaska. The canine parvovirus, which causes death by dehydration, electrolyte imbalance, and endotoxic shock or sepsis, is largely survivable in wolves, but can be lethal to pups. Wolves may catch infectious canine hepatitis from dogs, though there are no records of wolves dying from it. Papillomatosis has been recorded only once in wolves, and likely does not cause serious illness or death, though it may alter feeding behaviours. The canine coronavirus has been recorded in Alaskan wolves, infections being most prevalent in winter months. [125]

Bacterial diseases carried by wolves include: brucellosis, Lyme disease, leptospirosis, tularemia, bovine tuberculosis, [127] listeriosis and anthrax. [126] Wolves can catch Brucella suis from wild and domestic reindeer. While adult wolves tend not to show any clinical signs, it can severely weaken the pups of infected females. Although lyme disease can debilitate individual wolves, it does not appear to significantly affect wolf populations. Leptospirosis can be contracted through contact with infected prey or urine, and can cause fever, anorexia, vomiting, anemia, hematuria, icterus, and death. Wolves living near farms are more vulnerable to the disease than those living in the wilderness, probably because of prolonged contact with infected domestic animal waste. Wolves may catch tularemia from lagomorph prey, though its effect on wolves is unknown. Although bovine tuberculosis is not considered a major threat to wolves, it has been recorded to have killed two wolf pups in Canada. [127]

Parasitic

Wolves carry ectoparasites and endoparasites those in the former Soviet Union have been recorded to carry at least 50 species. [126] Most of these parasites infect wolves without adverse effects, though the effects may become more serious in sick or malnourished specimens. [128] Parasitic infection in wolves is of particular concern to people. Wolves can spread them to dogs, which in turn can carry the parasites to humans. In areas where wolves inhabit pastoral areas, the parasites can be spread to livestock. [126]

Wolves are often infested with a variety of arthropod exoparasites, including fleas, ticks, lice, and mites. The most harmful to wolves, particularly pups, is the mange mite (Sarcoptes scabiei), [128] though they rarely develop full-blown mange, unlike foxes. [34] Lice, such as Trichodectes canis, may cause sickness in wolves, but rarely death. Ticks of the genus Ixodes can infect wolves with Lyme disease and Rocky Mountain spotted fever. [128] The tick Dermacentor pictus also infests wolves. Other ectoparasites include chewing lice, sucking lice and the fleas Pulex irritans and Ctenocephalides canis. [34]

Endoparasites known to infect wolves include: protozoans and helminths (flukes, tapeworms, roundworms and thorny-headed worms). Of 30,000 protozoan species, only a few have been recorded to infect wolves: Isospora, Toxoplasma, Sarcocystis, Babesia, and Giardia. [128] Some wolves carry Neospora caninum, which can be spread to cattle and is correlated with bovine miscarriages. [129] Among flukes, the most common in North American wolves is Alaria, which infects small rodents and amphibians which are eaten by wolves. Upon reaching maturity, Alaria migrates to the wolf's intestine, but does little harm. Metorchis conjunctus, which enters wolves through eating fish, infects the wolf's liver or gall bladder, causing liver disease, inflammation of the pancreas, and emaciation. Most other fluke species reside in the wolf's intestine, though Paragonimus westermani lives in the lungs. Tapeworms are commonly found in wolves, as their primary hosts are ungulates, small mammals, and fish, which wolves feed upon. Tapeworms generally cause little harm in wolves, though this depends on the number and size of the parasites, and the sensitivity of the host. Symptoms often include constipation, toxic and allergic reactions, irritation of the intestinal mucosa, and malnutrition. Infections by the tapeworm Echinococcus granulosus in ungulate populations tend to increase in areas with high wolf densities, as wolves can shed Echinoccocus eggs in their feces onto grazing areas. [128]

Wolves can carry over 30 roundworm species, though most roundworm infections appear benign, depending on the number of worms and the age of the host. Ancylostoma caninum attaches itself on the intestinal wall to feed on the host's blood, and can cause hyperchromic anemia, emaciation, diarrhea, and possibly death. Toxocara canis, a hookworm known to infect wolf pups in the uterus, can cause intestinal irritation, bloating, vomiting, and diarrhea. Wolves may catch Dioctophyma renale from minks, which infects the kidneys, and can grow to lengths of 100 cm (40 in). D. renale causes the complete destruction of the kidney's functional tissue and can be fatal if both kidneys are infected. Wolves can tolerate low levels of Dirofilaria immitis for many years without showing any ill effects, though high levels can kill wolves through cardiac enlargement and congestive hepatopathy. Wolves probably become infected with Trichinella spiralis by eating infected ungulates. Although T. spiralis is not known to produce clinical signs in wolves, it can cause emaciation, salivation, and crippling muscle pains in dogs. Thorny-headed worms rarely infect wolves, though three species have been identified in Russian wolves: Nicolla skrjabini, Macracanthorhynchus catulinus, and Moniliformis moniliformis. [128]

The global wild wolf population in 2003 was estimated at 300,000. [130] Wolf population declines have been arrested since the 1970s. This has fostered recolonization and reintroduction in parts of its former range as a result of legal protection, changes in land use, and rural human population shifts to cities. Competition with humans for livestock and game species, concerns over the danger posed by wolves to people, and habitat fragmentation pose a continued threat to the wolf. Despite these threats, the IUCN classifies the wolf as Least Concern on its Red List due to its relatively widespread range and stable population. The species is listed by the Convention on International Trade in Endangered Species of Wild Fauna and Flora in its Appendix II, indicating that it is not threatened with extinction. However, those wolf populations living in Bhutan, India, Nepal and Pakistan are listed in its Appendix I, indicating that these may become extinct without restrictions on their trade. [2]

North America

In Canada, 50,000–60,000 wolves live in 80% of their historical range, making Canada an important stronghold for the species. [38] Under Canadian law, First Nations people can hunt wolves without restrictions, but others must acquire licenses for the hunting and trapping seasons. As many as 4,000 wolves may be harvested in Canada each year. [131] The wolf is a protected species in national parks under the Canada National Parks Act. [132] In Alaska, 7,000–11,000 wolves are found on 85% of the state's 1,517,733 km 2 (586,000 sq mi). Wolves may be hunted or trapped with a license around 1,200 wolves are harvested annually. [133]

In the contiguous United States, wolf declines were caused by the expansion of agriculture, the decimation of the wolf's main prey species like the American bison, and extermination campaigns. [38] Wolves were given protection under the Endangered Species Act (ESA) of 1973, and have since returned to parts of their former range thanks to both natural recolonizations and reintroductions in Yellowstone and Idaho. [134] The repopulation of wolves in Midwestern United States has been concentrated in the Great Lakes states of Minnesota, Wisconsin and Michigan where wolves number over 4,000 as of 2018. [135] Wolves also occupy much of the northern Rocky Mountains region, with at least 1,704 wolves in Montana, Idaho and Wyoming as of 2015. They have also established populations in Washington and Oregon. [136] [137] In Mexico and parts of the southwestern United States, the Mexican and U.S. governments collaborated from 1977 to 1980 in capturing all Mexican wolves remaining in the wild to prevent their extinction and established captive breeding programs for reintroduction. [138]

Eurasia

Europe, excluding Russia, Belarus and Ukraine, has 17,000 wolves in more than 28 countries. [139] In many countries of the European Union, the wolf is strictly protected under the 1979 Berne Convention on the Conservation of European Wildlife and Natural Habitats (Appendix II) and the 1992 Council Directive 92/43/EEC on the Conservation of Natural Habitats and of Wild Fauna and Flora (Annex II and IV). There is extensive legal protection in many European countries, although there are national exceptions. [2] [140]

Wolves have been persecuted in Europe for centuries, having been exterminated in Great Britain by 1684, in Ireland by 1770, in Central Europe by 1899, in France by the 1930s, and in much of Scandinavia by the early 1970s. They continued to survive in parts of Finland, Eastern Europe and Southern Europe. [141] Since 1980, European wolves have rebounded and expanded into parts of their former range. The decline of the traditional pastoral and rural economies seems to have ended the need to exterminate the wolf in parts of Europe. [131] As of 2016, estimates of wolf numbers include: 4,000 in the Balkans, 3,460–3,849 in the Carpathian Mountains, 1,700–2,240 in the Baltic states, 1,100–2,400 in the Italian peninsula, and around 2,500 in the northwest Iberian peninsula as of 2007. [139]

In the former Soviet Union, wolf populations have retained much of their historical range despite Soviet-era large scale extermination campaigns. Their numbers range from 1,500 in Georgia, to 20,000 in Kazakhstan and up to 45,000 in Russia. [142] In Russia, the wolf is regarded as a pest because of its attacks on livestock, and wolf management means controlling their numbers by destroying them throughout the year. Russian history over the past century shows that reduced hunting leads to an abundance of wolves. [143] The Russian government has continued to pay bounties for wolves and annual harvests of 20–30% do not appear to significantly affect their numbers. [144]

In the Middle East, only Israel and Oman give wolves explicit legal protection. [145] Israel has protected its wolves since 1954 and has maintained a moderately sized population of 150 through effective enforcement of conservation policies. These wolves have moved into neighboring countries. Approximately 300–600 wolves inhabit the Arabian Peninsula. [146] The wolf also appears to be widespread in Iran. [147] Turkey has an estimated population of about 7,000 wolves. [148] Outside of Turkey, wolf populations in the Middle East may total 1,000–2,000. [145]

In southern Asia, the northern regions of Afghanistan and Pakistan are important strongholds for wolves. The wolf has been protected in India since 1972. [149] The Indian wolf is distributed across the states of Gujarat, Rajasthan, Haryana, Uttar Pradesh, Madhya Pradesh, Maharashtra, Karnataka and Andhra Pradesh. [150] As of 2019, it is estimated that there are around 2,000–3,000 Indian wolves in the country. [151] In East Asia, Mongolia's population numbers 10,000–20,000. In China, Heilongjiang has roughly 650 wolves, Xinjiang has 10,000 and Tibet has 2,000. [152] 2017 evidence suggests that wolves range across all of mainland China. [153] Wolves have been historically persecuted in China [154] but have been legally protected since 1998. [155] The last Japanese wolf was captured and killed in 1905. [156]

In culture

In folklore, religion and mythology

The wolf is a common motif in the mythologies and cosmologies of peoples throughout its historical range. The Ancient Greeks associated wolves with Apollo, the god of light and order. [157] The Ancient Romans connected the wolf with their god of war and agriculture Mars, [158] and believed their city's founders, Romulus and Remus, were suckled by a she-wolf. [159] Norse mythology includes the feared giant wolf Fenrir, [160] and Geri and Freki, Odin's faithful pets. [161]

In Chinese astronomy, the wolf represents Sirius and guards the heavenly gate. In China, the wolf was traditionally associated with greed and cruelty and wolf epithets were used to describe negative behaviours such as cruelty ("wolf's heart"), mistrust ("wolf's look") and lechery ("wolf-sex"). In both Hinduism and Buddhism, the wolf is ridden by gods of protection. In Vedic Hinduism, the wolf is a symbol of the night and the daytime quail must escape from its jaws. In Tantric Buddhism, wolves are depicted as inhabitants of graveyards and destroyers of corpses. [160]

In the Pawnee creation myth, the wolf was the first animal brought to Earth. When humans killed it, they were punished with death, destruction and the loss of immortality. [162] For the Pawnee, Sirius is the "wolf star" and its disappearance and reappearance signified the wolf moving to and from the spirit world. Both Pawnee and Blackfoot call the Milky Way the "wolf trail". [163] The wolf is also an important crest symbol for clans of the Pacific Northwest like the Kwakwakaʼwakw. [160]

The concept of people turning into wolves, and the inverse, has been present in many cultures. One Greek myth tells of Lycaon of Arcadia being transformed into a wolf by Zeus as punishment for his evil deeds. [164] The legend of the werewolf has been widespread in European folklore and involves people willingly turning into wolves to attack and kill others. [165] The Navajo have traditionally believed that witches would turn into wolves by donning wolf skins and would kill people and raid graveyards. [166] The Dena'ina believed wolves were once men and viewed them as brothers. [157]

In fable and literature

Aesop featured wolves in several of his fables, playing on the concerns of Ancient Greece's settled, sheep-herding world. His most famous is the fable of "The Boy Who Cried Wolf", which is directed at those who knowingly raise false alarms, and from which the idiomatic phrase "to cry wolf" is derived. Some of his other fables concentrate on maintaining the trust between shepherds and guard dogs in their vigilance against wolves, as well as anxieties over the close relationship between wolves and dogs. Although Aesop used wolves to warn, criticize and moralize about human behaviour, his portrayals added to the wolf's image as a deceitful and dangerous animal. The Bible uses an image of a wolf lying with a lamb in a utopian vision of the future. In the New Testament, Jesus is said to have used wolves as illustrations of the dangers his followers, whom he represents as sheep, would face should they follow him. [167]

Isengrim the wolf, a character first appearing in the 12th-century Latin poem Ysengrimus, is a major character in the Reynard Cycle, where he stands for the low nobility, whilst his adversary, Reynard the fox, represents the peasant hero. Isengrim is forever the victim of Reynard's wit and cruelty, often dying at the end of each story. [168] The tale of "Little Red Riding Hood", first written in 1697 by Charles Perrault, is considered to have further contributed to the wolf's negative reputation in the Western world. The Big Bad Wolf is portrayed as a villain capable of imitating human speech and disguising itself with human clothing. The character has been interpreted as an allegorical sexual predator. [169] Villainous wolf characters also appear in The Three Little Pigs and "The Wolf and the Seven Young Goats". [170] The hunting of wolves, and their attacks on humans and livestock, feature prominently in Russian literature, and are included in the works of Leo Tolstoy, Anton Chekhov, Nikolay Nekrasov, Ivan Bunin, Leonid Pavlovich Sabaneyev, and others. Tolstoy's War and Peace and Chekhov's Peasants both feature scenes in which wolves are hunted with hounds and Borzois. [171] The musical Peter and the Wolf involves a wolf being captured for eating a duck, but is spared and sent to a zoo. [172]

Wolves are among the central characters of Rudyard Kipling's The Jungle Book. His portrayal of wolves has been praised posthumously by wolf biologists for his depiction of them: rather than being villainous or gluttonous, as was common in wolf portrayals at the time of the book's publication, they are shown as living in amiable family groups and drawing on the experience of infirm but experienced elder pack members. [173] Farley Mowat's largely fictional 1963 memoir Never Cry Wolf is widely considered to be the most popular book on wolves, having been adapted into a Hollywood film and taught in several schools decades after its publication. Although credited with having changed popular perceptions on wolves by portraying them as loving, cooperative and noble, it has been criticized for its idealization of wolves and its factual inaccuracies. [174] [175] [176]

Conflicts

Human presence appears to stress wolves, as seen by increased cortisol levels in instances such as snowmobiling near their territory. [177]

Predation on livestock

Livestock depredation has been one of the primary reasons for hunting wolves and can pose a severe problem for wolf conservation. As well as causing economic losses, the threat of wolf predation causes great stress on livestock producers, and no foolproof solution of preventing such attacks short of exterminating wolves has been found. [178] Some nations help offset economic losses to wolves through compensation programs or state insurance. [179] Domesticated animals are easy prey for wolves, as they have been bred under constant human protection, and are thus unable to defend themselves very well. [180] Wolves typically resort to attacking livestock when wild prey is depleted. [181] In Eurasia, a large part of the diet of some wolf populations consists of livestock, while such incidents are rare in North America, where healthy populations of wild prey have been largely restored. [178]

The majority of losses occur during the summer grazing period, untended livestock in remote pastures being the most vulnerable to wolf predation. [182] The most frequently targeted livestock species are sheep (Europe), domestic reindeer (northern Scandinavia), goats (India), horses (Mongolia), cattle and turkeys (North America). [178] The number of animals killed in single attacks varies according to species: most attacks on cattle and horses result in one death, while turkeys, sheep and domestic reindeer may be killed in surplus. [183] Wolves mainly attack livestock when the animals are grazing, though they occasionally break into fenced enclosures. [184]

Competition with dogs

A review of the studies on the competitive effects of dogs on sympatric carnivores did not mention any research on competition between dogs and wolves. [185] [186] Competition would favour the wolf, which is known to kill dogs however wolves usually live in pairs or in small packs in areas with high human persecution, giving them a disadvantage when facing large groups of dogs. [186] [187]

Wolves kill dogs on occasion, and some wolf populations rely on dogs as an important food source. In Croatia, wolves kill more dogs than sheep, and wolves in Russia appear to limit stray dog populations. Wolves may display unusually bold behaviour when attacking dogs accompanied by people, sometimes ignoring nearby humans. Wolf attacks on dogs may occur both in house yards and in forests. Wolf attacks on hunting dogs are considered a major problem in Scandinavia and Wisconsin. [178] [188] The most frequently killed hunting breeds in Scandinavia are Harriers, older animals being most at risk, likely because they are less timid than younger animals, and react to the presence of wolves differently. Large hunting dogs such as Swedish Elkhounds are more likely to survive wolf attacks because of their better ability to defend themselves. [188]

Although the number of dogs killed each year by wolves is relatively low, it induces a fear of wolves' entering villages and farmyards to prey on them. In many cultures, dogs are seen as family members, or at least working team members, and losing one can lead to strong emotional responses such as demanding more liberal hunting regulations. [186]

Dogs that are employed to guard sheep help to mitigate human–wolf conflicts, and are often proposed as one of the non-lethal tools in the conservation of wolves. [186] [189] Shepherd dogs are not particularly aggressive, but they can disrupt potential wolf predation by displaying what is to the wolf ambiguous behaviours, such as barking, social greeting, invitation to play or aggression. The historical use of shepherd dogs across Eurasia has been effective against wolf predation, [186] [190] especially when confining sheep in the presence of several livestock guardian dogs. [186] [191] Shepherd dogs are sometimes killed by wolves. [186]

Attacks on humans

The fear of wolves has been pervasive in many societies, though humans are not part of the wolf's natural prey. [192] How wolves react to humans depends largely on their prior experience with people: wolves lacking any negative experience of humans, or which are food-conditioned, may show little fear of people. [193] Although wolves may react aggressively when provoked, such attacks are mostly limited to quick bites on extremities, and the attacks are not pressed. [192]

Predatory attacks may be preceded by a long period of habituation, in which wolves gradually lose their fear of humans. The victims are repeatedly bitten on the head and face, and are then dragged off and consumed unless the wolves are driven off. Such attacks typically occur only locally and do not stop until the wolves involved are eliminated. Predatory attacks can occur at any time of the year, with a peak in the June–August period, when the chances of people entering forested areas (for livestock grazing or berry and mushroom picking) increase. [192] Cases of non-rabid wolf attacks in winter have been recorded in Belarus, Kirov and Irkutsk oblasts, Karelia and Ukraine. Also, wolves with pups experience greater food stresses during this period. [34] The majority of victims of predatory wolf attacks are children under the age of 18 and, in the rare cases where adults are killed, the victims are almost always women. [192] Indian wolves have a history of preying on children, a phenomenon called "child-lifting". They may be taken primarily in the summer period in the evening hours, and often within human settlements. [194]

Cases of rabid wolves are low when compared to other species, as wolves do not serve as primary reservoirs of the disease, but can be infected by animals such as dogs, jackals and foxes. Incidents of rabies in wolves are very rare in North America, though numerous in the eastern Mediterranean, the Middle East and Central Asia. Wolves apparently develop the "furious" phase of rabies to a very high degree. This, coupled with their size and strength, makes rabid wolves perhaps the most dangerous of rabid animals. [192] Bites from rabid wolves are 15 times more dangerous than those of rabid dogs. [195] Rabid wolves usually act alone, travelling large distances and often biting large numbers of people and domestic animals. Most rabid wolf attacks occur in the spring and autumn periods. Unlike with predatory attacks, the victims of rabid wolves are not eaten, and the attacks generally occur only on a single day. The victims are chosen at random, though most cases involve adult men. During the fifty years up to 2002, there were eight fatal attacks in Europe and Russia, and more than two hundred in southern Asia. [192]

Human hunting of wolves

Theodore Roosevelt said wolves are difficult to hunt because of their elusiveness, sharp senses, high endurance, and ability to quickly incapacitate and kill a dog. [196] Historic methods included killing of spring-born litters in their dens, coursing with dogs (usually combinations of sighthounds, Bloodhounds and Fox Terriers), poisoning with strychnine, and trapping. [197] [198]

A popular method of wolf hunting in Russia involves trapping a pack within a small area by encircling it with fladry poles carrying a human scent. This method relies heavily on the wolf's fear of human scents, though it can lose its effectiveness when wolves become accustomed to the odor. Some hunters can lure wolves by imitating their calls. In Kazakhstan and Mongolia, wolves are traditionally hunted with eagles and falcons, though this practice is declining, as experienced falconers are becoming few in number. Shooting wolves from aircraft is highly effective, due to increased visibility and direct lines of fire. [198] Several types of dog, including the Borzoi and Kyrgyz Tajgan, have been specifically bred for wolf hunting. [186]

As pets and working animals

Wolves and wolf-dog hybrids are sometimes kept as exotic pets. Although closely related to domestic dogs, wolves do not show the same tractability as dogs in living alongside humans, being generally less responsive to human commands and more likely to act aggressively. A person is more likely to be fatally mauled by a pet wolf or wolf-dog hybrid than by a dog. [199]

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RESULTS

Traces of body acceleration during different behaviours

When the birds undertook `active' behaviours (walking and eating food pellets), distinctive patterns were observed in the raw acceleration traces in both the x and z axes(Fig. 1). Traces for different behaviours were distinguishable from each other and also from periods when the chickens were `inactive' (digesting a meal or thermoregulating outside their TNZ). However, the raw acceleration traces associated with these two inactive behaviours were not easily distinguishable from each other(Fig. 1).

Mean (±s.e.m.) values of (A) partial dynamic body acceleration in the x and z axes (PDBAxz) and (B) heart rate (white bars, all ±s.e.m.) measured in bantam chickens(N=8) while they digested a meal of food pellets or rested while post-absorptive at the same constant temperature (18°C) as a control. Concurrently made measurements of the rate of oxygen consumption (black bars,±s.e.m.) are also shown. Significant differences between control and digesting states are indicated by the following symbols: * and#.

Mean (±s.e.m.) values of (A) partial dynamic body acceleration in the x and z axes (PDBAxz) and (B) heart rate (white bars, all ±s.e.m.) measured in bantam chickens(N=8) while they digested a meal of food pellets or rested while post-absorptive at the same constant temperature (18°C) as a control. Concurrently made measurements of the rate of oxygen consumption (black bars,±s.e.m.) are also shown. Significant differences between control and digesting states are indicated by the following symbols: * and#.

Mean (±s.e.m.) values of (A) partial dynamic body acceleration in the x and z axes (PDBAxz) and (B) heart rate (white symbols) measured in bantam chickens (N=8) at a range of ambient temperature along with concurrent measurements of mean(±s.e.m.) rate of oxygen consumption (black symbols).

Mean (±s.e.m.) values of (A) partial dynamic body acceleration in the x and z axes (PDBAxz) and (B) heart rate (white symbols) measured in bantam chickens (N=8) at a range of ambient temperature along with concurrent measurements of mean(±s.e.m.) rate of oxygen consumption (black symbols).

Body acceleration during eating and digestion

While instrumented with an accelerometer and eating a meal of food pellets placed into the respirometer, the chickens showed a significant increase in both PDBAxz (paired t-test t(7)=3.88, P<0.01) and O2 (paired t-test t(7)=2.98, P<0.05) when compared with resting quietly at the same temperature (18°C)(Fig. 2). Similarly, when fH was recorded, both fH (paired t-test t(7)=7.27, P<0.01) and O2 (paired t-test t(7)=5.28, P<0.01) were significantly greater during eating. After eating, the magnitude of SDA during digestion was evaluated (Fig. 3). When PDBAxz was recorded, O2 was significantly higher during digestion (paired t-test t(7)=3.24, P<0.05), but there was no difference in PDBAxz (paired t-test t(7)=1.28, P=0.24). When fHwas recorded, both O2 (paired t-test t(7)=3.78, P<0.01) and fH (paired t-test t(7)=3.66, P<0.01) were significantly higher during digestion than while the chickens rested at the same temperature.

Body acceleration during thermoregulation

When exposed to a range of different temperatures, the chickens showed changes in metabolism, suggesting a TNZ with an upper critical temperature around 30°C and a lower critical temperature as low as 20°C(Fig. 4). When instrumented with an accelerometer, the rate of oxygen consumption(O2) was at a minimum at 30°C and was significantly elevated at 1°C and 11°C(two-way ANOVA, with Tukey multiple comparisons F(4,28)=7.29, P<0.001). There were no significant differences in PDBAxz between the different temperatures (two-way ANOVA F(4,28)=0.32, P=0.86). When O2 and heart rate (fH) were recorded simultaneously, both O2 and fH were again at a minimum at 30°C, and both were significantly elevated at 1°C and 11°C (two-way ANOVA, with Tukey multiple comparisons F(4,28)=44.3 and 22.7, P<0.001).

Body acceleration during locomotion

The chickens exhibited a range of behaviours as well as walking while undertaking the treadmill experiments. They also pecked the ground, jumped and flapped their wings. During these trials, there was a positive, linear relationship between O2 and walking speed in bantam chickens instrumented with an accelerometer (weighted regression P<0.05, R 2 =0.80)(Fig. 5). This was matched by a linear increase in PDBAxz with walking speed (weighted regression P<0.001, R 2 =0.96). Similarly when O2 and fH were recorded simultaneously, there was a linear relationship between walking speed and both O2 (weighted regression P<0.01, R 2 =0.90) and fH (weighted regression P<0.001, R 2 =0.97) (Fig. 5).

Mean (±s.e.m.) values of (A) partial dynamic body acceleration in the x and z axes (PDBAxz) and (B) heart rate (white symbols) measured in bantam chickens (N=8) while walking on a treadmill at different speeds along with concurrent measurements of mean(±s.e.m.) rate of oxygen consumption (black symbols). Weighted regression relationships are also shown for heart rate and PDBAxz (solid lines) and rate of oxygen consumption(broken lines).

Mean (±s.e.m.) values of (A) partial dynamic body acceleration in the x and z axes (PDBAxz) and (B) heart rate (white symbols) measured in bantam chickens (N=8) while walking on a treadmill at different speeds along with concurrent measurements of mean(±s.e.m.) rate of oxygen consumption (black symbols). Weighted regression relationships are also shown for heart rate and PDBAxz (solid lines) and rate of oxygen consumption(broken lines).

Predicting the rate of oxygen consumption as a function of body acceleration

The behaviour-specific tests described above suggested that, although PDBAxz might be an effective predictor of O2 during active behaviours such as locomotion or eating, it was likely to be less effective while the chickens were inactive, either thermoregulating or digesting a meal. To investigate this further, O2 was plotted as a function of PDBAxz for each animal (see Fig. 6A for example). Visual inspection confirmed this initial suspicion that PDBAxzwas likely to be an accurate predictor of O2 during walking but was unlikely to be so accurate while the chickens were inactive. However, although there was a lot scatter in PDBAxz and O2 during inactivity, these data rarely overlapped with data recorded during activity. Converting PDBAxz to a logarithmic scale suggested that,with a single curvilinear model, it might be possible to predict O2 from PDBAxz across all behaviours(Fig. 6C). An analysis of covariance was conducted to investigate this further.

Analysis of covariance indicated no significant interaction between behaviour and log(PDBAxz)(F(3,688)=1.69, P=0.17) and thus the slope of the relationship between log(PDBAxz) and O2 did not differ between behaviours. Therefore, a single function was used to predict O2 from PDBAxz across all behaviours(Table 1). As both behaviour and individual identity were significant factors in the model, two extra error terms would need to be introduced when calculating s.e.e. values made using this single model. Fig. 7illustrates this effect and shows how using a single relationship might not be the best approach. Calculation of 95% confidence intervals and 95% prediction intervals shows that using this one-model approach will tend to underestimate O2 during walking. Even if O2 were predicted for a large sample of animals, the error of the estimate would be considerable for estimates made during walking, despite the relatively close relationship during this behaviour.

Analysis of variance (ANOVA) of a GLM model to estimate rate of oxygen consumption from partial dynamic body acceleration in the x and z axes (PDBAxz) during all activities

Factor . d.f. . Seq SS . F . P .
Individual 7 893.9 6.15 <0.001
log(PDBAxz) 1 10413.1 143.85 <0.001
Behaviour 3 314.5 14.50 <0.001
Error 719 5196.8
Total 730 16818.3
Factor . d.f. . Seq SS . F . P .
Individual 7 893.9 6.15 <0.001
log(PDBAxz) 1 10413.1 143.85 <0.001
Behaviour 3 314.5 14.50 <0.001
Error 719 5196.8
Total 730 16818.3

Data were collected while eight bantam hens undertook four behaviours(eating, digesting, thermoregulating, walking). The model selected was: O2=[8.51 ×log(PDBAxz)]+23.84, R 2 =0.69. The significant effects of individual identity and behaviour were incorporated into the standard error of the estimate (s.e.e.) calculated when using the selected model

Rate of oxygen consumption as a function of (A) partial dynamic body acceleration in the x and z axes(PDBAxz) and (B) heart rate across a range of behaviours in a single bantam chicken (ID 73C5). In each case, data were recorded while the chicken walked on a treadmill (filled squares), ate a meal of food pellets(filled triangles), digested the meal of food pellets (open triangles) or thermoregulated (open squares). Data shown in (C) and (D) are the same as in(A) and (B), respectively, but with the x-axis displayed as a logarithmic scale.

Rate of oxygen consumption as a function of (A) partial dynamic body acceleration in the x and z axes(PDBAxz) and (B) heart rate across a range of behaviours in a single bantam chicken (ID 73C5). In each case, data were recorded while the chicken walked on a treadmill (filled squares), ate a meal of food pellets(filled triangles), digested the meal of food pellets (open triangles) or thermoregulated (open squares). Data shown in (C) and (D) are the same as in(A) and (B), respectively, but with the x-axis displayed as a logarithmic scale.

Further investigation was undertaken with analyses of covariance comparing digestion with thermoregulation (`inactive' states), and walking with eating(`active' states), to investigate the creation of two models. In the case of thermoregulation and digestion, there was again no significant interaction between behaviour and log(PDBAxz)(F(1,588)=2.44, P=0.12) and a significant model for inactivity was created (Table 2). While the model was relatively inaccurate(R 2 =0.21), the relationship between PDBAxz and O2 during inactivity was statistically significant. Similarly, there was no significant interaction between behaviour and log(PDBAxz) when eating and walking were compared (F(1,93)=0.22, P=0.64). Furthermore, there was no significant effect of behaviour in this model(F(1,108)=1.95, P=0.17), and so a model with only one additional error term was created(Table 3). Plotting predictions made with this two-model approach (Fig. 8) shows that, although the 95% prediction intervals are still relatively large during inactivity, they are substantially smaller during activity than they are in the one-model approach. Furthermore, there is no longer a systematic underestimation of O2 during walking, as in the one-model approach.

Analysis of variance (ANOVA) of a GLM model to estimate rate of oxygen consumption from partial dynamic body acceleration in the x and z axes (PDBAxz) while inactive

Factor . d.f. . Seq SS . F . P .
Individual 7 500.8 5.77 <0.001
log(PDBAxz) 1 549.8 84.69 <0.001
Behaviour 1 161.0 21.52 <0.001
Error 603 4510.8
Total 612 5722.4
Factor . d.f. . Seq SS . F . P .
Individual 7 500.8 5.77 <0.001
log(PDBAxz) 1 549.8 84.69 <0.001
Behaviour 1 161.0 21.52 <0.001
Error 603 4510.8
Total 612 5722.4

Data were collected while eight bantam hens undertook two inactive behaviours (digesting, thermoregulating). The model selected was: O2=[8.29 ×log(PDBAxz)]+22.75, R 2 =0.21. The significant effects of individual identity and behaviour were incorporated into the standard error of the estimate (s.e.e.) calculated when using the selected model

Analysis of variance (ANOVA) of a GLM model to estimate rate of oxygen consumption from partial dynamic body acceleration in the x and z axes (PDBAxz) while active

Factor . d.f. . Seq SS . F . P .
Individual 1 309.4 14.46 <0.001
log(PDBAxz) 7 931.2 279.78 <0.001
Error 109 362.8
Total 117 1603.3
Factor . d.f. . Seq SS . F . P .
Individual 1 309.4 14.46 <0.001
log(PDBAxz) 7 931.2 279.78 <0.001
Error 109 362.8
Total 117 1603.3

Data were collected while eight bantam hens undertook two active behaviours(eating, walking). The model selected was: O2=[10.79× log(PDBAxz)]+27.03, R 2 =0.77. The significant effects of individual identity were incorporated into the standard error of the estimate (s.e.e.) calculated when using the selected model

Predicting the rate of oxygen consumption as a function of heart rate

Heart rate appeared to be an effective predictor of O2 during all behaviours. To investigate this further, O2 was plotted as a function of fH during all behaviours for each animal(see Fig. 6B for example). Again, a logarithmic relationship appeared to best fit the data across all behaviours. However, analysis of covariance indicated a significant interaction between behaviour and log(fH)(F(3,699)=5.23, P<0.001). Eliminating each of the behaviours in turn and repeating this analysis revealed that the relationship between fH and O2 during digestion was significantly different to the relationship between the other three (Fig. 9). Thus, two models were created: one during SDA and the other for all other behaviours. In this two-model approach, there was a considerable overlap between the two relationships (Fig. 9), and so a one-model approach was also investigated. In this case, a single relationship was constructed to enable prediction where behaviour was not known, with behaviour included as an additional error term in the calculation of the s.e.e. (Table 4 Fig. 10). Despite adding this potential for increased uncertainty, there was very little difference in the 95% prediction intervals when comparing the one-model and two-model approaches(Figs 9 and 10).

Analysis of variance (ANOVA) of a GLM model to estimate rate of oxygen consumption from heart rate (fH)

Factor . d.f. . Seq SS . F . P .
Individual 7 979.6 37.54 <0.001
log(fH) 1 13001.3 1423.30 <0.001
Behaviour 3 60.3 5.35 <0.001
Error 730 2741.9
Total 741 16783.1
Factor . d.f. . Seq SS . F . P .
Individual 7 979.6 37.54 <0.001
log(fH) 1 13001.3 1423.30 <0.001
Behaviour 3 60.3 5.35 <0.001
Error 730 2741.9
Total 741 16783.1

Data were collected while eight bantam hens undertook two inactive behaviours (digesting, thermoregulating). The model selected was: O2=[37.39× log(fH)]–64.55, R 2 =0.84. The significant effects of individual identity and behaviour were incorporated into the standard error of the estimate (s.e.e.) calculated when using the selected model

Rate of oxygen consumption as a function of partial dynamic body acceleration in the x and z axes(PDBAxz) in eight bantam chickens. Data were recorded while the chickens walked on a treadmill (filled squares), ate a meal of food pellets (filled triangles), digested the meal of food pellets (open triangles)or thermoregulated (open squares). Also plotted is a best-fit regression line(solid line) and 95% confidence intervals (black broken lines) and 95%prediction intervals (grey broken lines). 95% confidence intervals were calculated as if s O2 was estimated from one measurement of PDBAxz during one additional behaviour by one additional chicken. 95% prediction intervals were calculated as if s O2 was estimated from 10,000 measurements of PDBAxz of four additional behaviours by 100 additional chickens, effectively the smallest possible prediction interval for this model.

Rate of oxygen consumption as a function of partial dynamic body acceleration in the x and z axes(PDBAxz) in eight bantam chickens. Data were recorded while the chickens walked on a treadmill (filled squares), ate a meal of food pellets (filled triangles), digested the meal of food pellets (open triangles)or thermoregulated (open squares). Also plotted is a best-fit regression line(solid line) and 95% confidence intervals (black broken lines) and 95%prediction intervals (grey broken lines). 95% confidence intervals were calculated as if s O2 was estimated from one measurement of PDBAxz during one additional behaviour by one additional chicken. 95% prediction intervals were calculated as if s O2 was estimated from 10,000 measurements of PDBAxz of four additional behaviours by 100 additional chickens, effectively the smallest possible prediction interval for this model.


Universitat de Barcelona

The southern giant petrel, a frequent victim of accidental capture by trawlers, is included on the Red List of Threatened Species maintained by the International Union for Conservation of Nature (IUCN).

The length of telomeres, the DNA fragments that protect the ends of chromosomes from deterioration, could be an indicator of life expectancy in the southern giant petrel (Macronectes giganteus), an emblematic species of the Antarctic and sub-Antarctic regions, according to an article published in the journal Behavioral Ecology by an international group of researchers including Dr. Jacob González-Solís, from the UB&rsquos Department of Animal Biology and the Institute of Research of the Biodiversity (IRBio) at the University of Barcelona, . The project on which the article is based, which is directed by the expert Pat Monhagan (University of Glasgow, UK), also reveals that adult male giant petrels have shorter telomere lengths than females, a genetic difference that had not been documented until now in a scientific study of a bird species.