Understanding Sleep as a Developmental System in Dogs Daily-Ease

Understanding Sleep as a Developmental System in Dogs

Understanding Sleep as a Developmental System in Dogs

Sleep is not what most dog owners think it is. The hours a dog spends lying down are measurable — but they are also the least informative data point available when it comes to understanding what the sleep system is actually doing.

Sleep is an active biological process. During it, the nervous system consolidates learning, regulates emotional tone, repairs tissue, and recalibrates the stress response. What unfolds beneath the surface of a resting dog is not passive recovery — it is coordinated neurological and physiological maintenance running in parallel, governed by systems that shift in architecture and function across the entire lifespan.

For owners, this distinction changes everything. The puppy twitching violently through a midday nap is not in distress. The adolescent dog waking at 3 a.m. is not undertrained. The senior dog sleeping more hours but seeming less rested is not simply aging. Each of these presentations is the sleep system operating under specific biological conditions — and each signals something meaningfully different from the others.

This article covers three things: the architecture of canine sleep, how that architecture shifts across every major life stage, and how to read sleep disruption as diagnostic information rather than misbehavior.

What Dog Sleep Actually Is — Beyond the Hours Count

Dogs cycle through two primary sleep states — non-REM (NREM) and REM sleep — in repeating sequences distributed across the day and night. NREM encompasses both lighter transitional sleep and slow-wave sleep, the deepest restorative phase, during which physical repair, immune regulation, and metabolic maintenance take priority. REM sleep is neurologically active by contrast: the brain processes sensory experience, consolidates memory, and regulates emotional state during this phase. A dog in REM sleep may twitch, vocalize softly, paddle its legs, or show rapid movement beneath closed lids. These are not signs of distress. They are the visible surface of a nervous system doing significant work.

Where canine sleep departs sharply from human sleep is in cycle length and distribution. Human sleep cycles average approximately 90 minutes; dogs cycle through NREM and REM in roughly 20 to 45 minutes, depending on the individual and life stage. This shorter cycle means dogs pass through more sleep phases per rest period — and it also means they are lighter sleepers on average, capable of transitioning from deep sleep to full alertness more rapidly. This reflects evolutionary design: a species that needed to recover efficiently without sacrificing vigilance.

Dogs are also polyphasic sleepers, distributing rest across multiple bouts throughout the day rather than consolidating into a single nocturnal block. A dog that sleeps four hours, moves, then sleeps again is not sleeping poorly. That pattern is the system operating as intended.

The functional distinctions between sleep phases matter for understanding behavioral output:

  • Slow-wave (deep) NREM sleep: Physical restoration, immune regulation, metabolic repair, growth hormone release
  • REM sleep: Memory consolidation, emotional processing, sensory integration, neurological maintenance
  • Light NREM sleep: Transitional state; most easily disrupted; serves as a buffer between deeper phases

The behavioral consequences of disrupting either phase are measurable and specific. A dog consistently denied adequate slow-wave sleep will show impaired physical recovery and compromised immune function over time. A dog with chronically fragmented REM sleep is more likely to exhibit emotional dysregulation, reduced learning retention, and heightened reactivity during waking hours. Sleep is not background noise in a dog's life. It is where a significant portion of behavioral output is determined.

Sleep as a Developmental System — Why Life Stage Changes Everything

The most consequential error in popular writing about dog sleep is treating it as a fixed biological need. The standard framing — dogs need twelve to fourteen hours, puppies need more, senior dogs sleep a lot — is not inaccurate so much as it is stripped of the biology that makes those numbers meaningful. Sleep is not a static daily requirement expressed uniformly across a lifetime. It is a dynamic biological program that the nervous system recalibrates continuously in response to developmental stage, physiological state, and environmental demand.

Each life stage produces a distinct sleep architecture for a specific neurological reason — not simply because young animals are more tired or aging animals have less energy. A neonatal puppy sleeping twenty-two hours per day is not exhausted. Its brain is under active construction, and sleep is the primary medium through which that construction occurs. An adolescent dog waking repeatedly through the night is not undertrained. Its stress-response system is undergoing structural maturation, a process that disrupts sleep architecture in ways that parallel what is well-documented in human adolescence. The rationale behind each stage's sleep pattern is what allows owners to respond appropriately rather than reactively.

The developmental arc runs from neonatal through juvenile, adolescent, adult, and senior — and at every transition, owners commonly misread what the sleep system is expressing. The sudden crashes of early puppyhood, the apparent regression at eight months, the night waking that appears in a previously stable older dog: these follow a biological sequence that is predictable once the underlying framework is understood.

Neonatal and Early Puppy Stage (0–8 Weeks)

A newborn puppy sleeps approximately twenty-two hours out of every twenty-four. This is not the behavior of a fragile or passive organism — it is the behavior of a nervous system under rapid, resource-intensive construction. During this stage, REM sleep dominates in a proportion that will not appear again at any other point in the dog's life, because the neurological work being done is primarily structural. Sensory pathways are forming, synaptic architecture is being laid down, and the brain is wiring itself for the perceptual and behavioral life ahead. Sleep is not incidental to this process. It is the process.

Research in developmental neuroscience has established that sleep deprivation during the neonatal period carries lasting consequences. Neonates deprived of adequate rest show measurable deficits in sensory processing and social behavior that persist well beyond the neonatal window — reflecting how completely this phase of neural construction depends on uninterrupted sleep cycling (Jouvet-Mounier et al., 1970; Frank & Heller, 1997). The mother and littermates are not merely comforting presences during this period. They function as physiological anchors — providing thermal regulation and tactile stimulation that stabilizes sleep cycling in each individual pup.

Healthy neonatal sleep is visibly active. Twitching, paddling, and brief vocalizations are normal expressions of REM-phase intensity, not distress. A puppy that is genuinely motionless and unresponsive during sleep — rather than cycling through visible movement — warrants closer observation. Normal neonatal sleep looks busy. That is precisely what it should look like.

Juvenile Puppy Stage (8 Weeks – 6 Months)

Once a puppy enters a home environment, its sleep becomes visible to owners in a way it was not before — and that visibility frequently generates concern where none is warranted. Juvenile puppies still require sixteen to twenty hours of sleep per day, but that sleep is now distributed across fragmented bouts that owners witness directly: the abrupt crash after a training session, the sudden stillness mid-play, the eruption of frantic energy that seems to arrive from nowhere. These are not behavioral anomalies. They are expressions of sleep pressure in a nervous system that has not yet developed efficient self-regulation.

What owners most frequently misread as hyperactivity or a training deficit is often an overtired puppy operating under accumulated cortisol and stress-hormone load. This is a well-documented physiological response in young mammals: when sleep deprivation accumulates, the system does not slow down — it activates (Bhatt et al., 2020). The overtired puppy becomes more reactive, harder to redirect, and more prone to mouthiness, vocalizations, and the erratic movement owners typically describe as zoomies. The cause is not surplus energy. It is a nervous system that has exceeded its recovery capacity and is now running on stress chemistry.

Signs that a juvenile puppy has crossed into overtiredness include:

  • Difficulty settling despite a calm, quiet environment
  • Increased mouthiness with reduced bite inhibition
  • Loss of responsiveness to cues the puppy has reliably performed
  • Yawning paired with continued arousal rather than transition to rest
  • Sharp, unprovoked vocalizations without clear environmental trigger

Structured nap windows at this stage are a neurological requirement, not a comfort measure. Sleep is actively consolidating everything the juvenile puppy is learning — training responses, social cues, environmental associations. Restricting daytime rest in the belief that it will tire the puppy out at night does not accelerate learning. It degrades consolidation of what has already been taught.

Adolescent Stage (6 Months – 2 Years, Breed-Dependent)

Adolescence produces one of the most consistently misread sleep shifts across the entire canine lifespan. Owners of adolescent dogs frequently report that a previously manageable puppy has become harder to settle, has begun waking during the night again, and seems more reactive and less focused during waking hours. The reflexive interpretation is training regression. The more accurate interpretation is developmental.

During adolescence, the hypothalamic-pituitary-adrenal (HPA) axis — the system governing the body's stress response — undergoes structural maturation. This process is neither instantaneous nor linear. While it is occurring, the dog's capacity to regulate arousal and return to a calm baseline after stimulation is genuinely compromised at a neurological level (Romeo, 2010). Sleep architecture shifts accordingly: light NREM sleep becomes more predominant, environmental sensitivity increases, and nighttime fragmentation becomes more frequent. This is neurologically expected — not a failure of training, management, or the dog's temperament.

The timeline of adolescent maturation varies substantially by breed size, and this variation is clinically significant. Small breeds may complete neurological maturation by twelve to fourteen months. Giant breeds — Great Danes, Mastiffs, Saint Bernards — may not reach full HPA stability until twenty-four months or beyond. An owner comparing an eighteen-month-old Great Dane's sleep and reactivity to a Miniature Schnauzer of the same age is comparing two dogs at meaningfully different developmental coordinates. The night waking and difficulty settling that characterize this window have a physiological basis. They resolve as the nervous system matures — provided the environment supports rather than amplifies the underlying instability.

Adult Dogs (2–7 Years, Breed-Dependent)

Adult sleep architecture is the most stable configuration a dog maintains across its lifetime. The system is no longer under construction, no longer navigating the turbulence of adolescent HPA calibration — it has arrived at its functional baseline. Total daily sleep across polyphasic bouts typically falls between twelve and fourteen hours for the average adult dog, though this figure carries meaningful individual and breed-level variation that the aggregate obscures.

Working breeds and high-drive dogs in active households often operate at the lower end of that range, sustaining sleep quality through higher physical and cognitive expenditure during waking hours. Brachycephalic breeds — Bulldogs, French Bulldogs, Pugs, and related anatomies — frequently sleep more, partly because the elevated respiratory effort required during activity increases their recovery demand. Toy breeds also trend toward higher total sleep, though through a different physiological mechanism. What distinguishes healthy variation in adult sleep from early disruption signals is primarily consistency and waking behavior: a dog sleeping within its normal range and showing stable, regulated behavior during the day is operating normally. A dog whose established pattern shifts noticeably without an identifiable environmental cause warrants closer attention.

Physical activity and mental stimulation influence sleep quality more than they affect sleep quantity. A well-exercised, cognitively engaged adult dog will cycle more efficiently through NREM and REM phases than a sedentary individual of the same breed — not necessarily accumulating more hours, but achieving greater restorative depth within those hours.

Senior Dogs (7+ Years, Breed-Dependent)

The sleep changes of aging in dogs mirror what is documented in aging humans with uncomfortable precision. Senior dogs typically accumulate more total sleep hours than they did in adulthood, but those hours are less restorative. Slow-wave sleep — the deep, physically reparative phase — becomes shorter and more fragmented. Circadian rhythm entrainment weakens as the biological clock's sensitivity to environmental time cues diminishes (Egenvall et al., 2006; Landsberg et al., 2011). The result is a dog that sleeps more and yet appears less rested — and that wakes during the night not necessarily from pain, but from a system that has lost some capacity to sustain consolidated sleep architecture.

Canine Cognitive Dysfunction (CCD), a progressive neurological condition sharing features with human dementia, presents with night waking as one of its most consistent early signs. Owners of senior dogs should understand that night waking in an older dog is not automatically CCD — but it is a signal that warrants evaluation rather than dismissal. CCD-related night waking tends to involve disorientation, aimless movement, and vocalizations that appear disconnected from any environmental trigger. This is meaningfully distinct from the lighter, more fragmented sleep of normal aging, and the distinction matters because CCD has management options — including nutritional support, environmental modification, and pharmacological intervention — that can improve quality of life when identified early (Osella et al., 2007).

Pain and musculoskeletal discomfort are among the most underrecognized contributors to disrupted senior sleep. A dog that repositions repeatedly through the night, rises and lies down in short cycles, or selects unusually firm or cool surfaces may be managing joint discomfort in ways that fragment sleep architecture without the owner recognizing the connection. Medication effects common to aging dogs — including those used for pain management, cardiac conditions, and endocrine disorders — can alter sleep in both directions, either increasing sedation or reducing the dog's capacity to sustain deep sleep phases.

The most important clinical framing for this life stage is that senior sleep changes are information, not inevitability. Changes that are sudden, that accelerate over weeks rather than months, or that accompany shifts in waking behavior deserve veterinary attention. Attributing all disruption in an older dog to the general passage of time delays identification of conditions that are manageable when caught early.

What Disrupted Sleep Actually Signals — Reading the System, Not Just the Behavior

When a dog wakes during the night, the owner's first interpretation is almost invariably behavioral: the dog wants attention, the dog is under-exercised, the dog was not sufficiently tired. These interpretations are not always wrong — but they are almost always incomplete. Sleep disruption is not a behavior. It is a symptom. And like any symptom, its value lies in what it points toward upstream, not in the moment the owner is observing.

Disruptions fall into four primary categories, and correctly identifying the active category determines whether the appropriate response is environmental, medical, routine-based, or behavioral:

  • Environmental: Noise, light, temperature, sleep surface quality, proximity to household activity
  • Physiological: Pain, hunger, urinary urgency, systemic illness, medication effects, respiratory compromise
  • Psychological: Chronic stress, separation anxiety, hypervigilance, under-stimulation, accumulated arousal
  • Routine-based: Schedule instability, irregular feeding times, inconsistent exercise patterns, variable household rhythm

The relationship between daytime arousal and nighttime sleep quality is one of the most consistently overlooked variables in canine sleep management. A dog that spends its waking hours in a state of elevated arousal — reactive to the environment, unable to settle between interactions, engaged in chronic low-level stress — carries that arousal load into the night. The nervous system's capacity to downregulate and enter consolidated sleep is directly diminished by accumulated daytime stress, regardless of how much physical exercise the dog received. Owners who increase exercise in response to night waking and find it insufficient are addressing energy output while leaving arousal regulation untouched.

Chronic sleep fragmentation compounds over time. Reduced learning retention, increased reactivity to stimuli, lower frustration tolerance, and impaired impulse control are all associated with inadequate sleep consolidation in dogs, as they are in other mammals (Bhatt et al., 2020; Frank, 2006). When an owner notices that a previously trainable dog is becoming harder to work with, or a previously stable dog is becoming more reactive without an obvious trigger, sleep quality belongs on the list of contributing variables — not as the default explanation, but as one that is frequently overlooked.

When tracking sleep disruptions, pattern recognition generates more useful information than event counting. The timing of waking, its duration, the dog's behavior immediately after rousing, and any recent changes to environment or routine all carry more diagnostic weight than a simple tally of disturbances.

Environmental and Routine Factors That Shape Sleep Quality

Dogs are neither strictly nocturnal nor strictly diurnal by evolutionary heritage. They are opportunistic sleepers whose circadian rhythms synchronize to the rhythm of the household they inhabit rather than to a fixed biological schedule. This means the household itself functions as a circadian anchor — the timing of light exposure, feeding, exercise, and social interaction collectively establishes the dog's internal clock. When that household rhythm is consistent, the dog's sleep architecture stabilizes around it. When the rhythm is fragmented or unpredictable, the sleep system reflects that instability directly.

Feeding timing has a stronger influence on circadian entrainment than most owners recognize. Consistent meal times anchor the biological clock in ways that reinforce predictable sleep-wake transitions, a mechanism well-established in mammalian chronobiology (Stephan, 2002). Light exposure functions as a second anchor: dogs maintained in low-light environments throughout the day show weakened differentiation between daytime and nighttime behavior patterns. Exercise scheduling operates as a third: physical activity at consistent times helps establish a reliable arousal-and-recovery cycle that the sleep system can organize around.

The sleep environment itself interacts with breed-specific physiology in ways that deserve attention. Brachycephalic breeds are disproportionately sensitive to heat and humidity, given that respiratory efficiency is already compromised at baseline — a sleeping environment that is even moderately warm will elevate their arousal and fragment their cycles more readily than it would affect a dog with unobstructed airway anatomy. Sound-sensitive breeds, particularly many herding and working varieties, are more prone to rousing during light NREM phases in response to low-level environmental noise that would not register as significant for less reactive individuals. The same sleep environment does not function equivalently across all dogs.

Routine instability is the most consistently underestimated variable in adult canine sleep quality. Dogs experiencing significant schedule variation between weekdays and weekends — different waking times, shifted feeding windows, inconsistent exercise timing — show sleep fragmentation that is structurally analogous to social jet lag in human chronobiology research (Wittmann et al., 2006). The disruption is rarely dramatic on any single day, but it accumulates across weeks and degrades sleep quality in ways that eventually manifest as behavioral changes.

When to Involve a Veterinarian — Drawing the Clinical Line

Understanding the developmental basis of sleep variation is a tool for appropriate perspective — not a reason to defer clinical evaluation when it is warranted. There is a meaningful and specific line between sleep changes that reflect normal developmental or environmental variation and sleep changes that require medical assessment. Knowing where that line falls is a component of responsible ownership.

The following presentations warrant veterinary consultation rather than continued observation:

  • Sudden onset sleep changes in a previously stable adult dog, particularly when accompanied by shifts in waking behavior or temperament
  • Repetitive repositioning, reluctance to lie down, or selection of unusual sleep surfaces — potential indicators of pain or musculoskeletal discomfort affecting sleep comfort
  • Nighttime vocalization in a senior dog, especially when combined with apparent disorientation, aimless pacing, or failure to recognize familiar people or environments
  • Movements during sleep that are rigid, repetitive, or cannot be interrupted by touch or voice — which may represent seizure activity rather than normal REM behavior; this distinction requires clinical evaluation
  • Hypersomnia in a previously active adult dog — excessive sleep paired with lethargy or reduced engagement during waking hours may indicate hypothyroidism, systemic illness, or pain
  • Progressive worsening of night waking, particularly in senior dogs, where a sustained pattern of increasing disruption may indicate CCD, advancing pain, or medication interactions

The distinction between a sleep disruption and a sleep disorder is a clinical determination, not one owners can reliably make through observation alone. Conditions including hypothyroidism, Canine Cognitive Dysfunction, chronic musculoskeletal disease, and upper airway obstruction in brachycephalic breeds all alter sleep architecture in ways that may not be visible during waking hours. A dog that appears physically normal during the day may be experiencing sleep disruption driven by pathology that only becomes apparent when the dog is at rest.

Normal developmental variation does not require clinical intervention. Specific, progressive, or sudden symptom clusters do. The distinction is not always obvious, which is precisely why veterinary input has value when the pattern is unclear.

Building a Sleep-Supportive Framework for Your Dog

Sleep quality is shaped by four interacting variables: the dog's developmental stage, its current physical state, the sleep environment, and the consistency of daily routine. No variable operates independently. A dog in excellent physical health will still sleep poorly if its routine is unstable. A dog within a well-structured household routine will still show fragmented sleep if it is managing unaddressed chronic pain. Understanding the system means identifying which variable is currently the dominant influence — and adjusting with precision, rather than applying generic remedies that address the wrong lever.

Owners who have internalized this framework are not guessing when something changes. They can ask specific questions: Has the environment shifted? Is there a physiological variable that has not been evaluated? Has a routine change disrupted the dog's circadian anchoring? Is a life-stage transition contributing to what appears to be a behavioral problem? These questions lead to actionable hypotheses rather than cycles of frustration and trial-and-error intervention. For owners who have identified night waking as a concern and want to move from observation to systematic identification, a structured diagnostic tool can help determine which disruption category is most active — Why Your Dog Wakes at Night — Personalized Cause Finder.

In the majority of cases, sleep problems do not require dramatic intervention. They require accurate identification of the variable that is out of balance. That variable, in most cases, can be identified through disciplined observation of pattern, timing, and context — and corrected with proportionate adjustments to environment, routine, or physical care.

Sleep hours are a measure of quantity. They are also, on their own, a poor proxy for what the sleep system is actually accomplishing. A dog accumulating fourteen hours in fragmented, shallow cycles is not receiving the same biological benefit as a dog achieving twelve hours of well-consolidated sleep with adequate slow-wave and REM representation. The number on the clock is the least informative piece of data available to an owner paying attention.

A sleep-literate owner sees the system beneath the behavior. They recognize the developmental stage their dog is in and the neurological rationale that comes with it. They read the dog's waking arousal pattern as a predictor of nighttime sleep quality. They assess the environment and the routine as variables that either support or undermine the system. And they understand that the dog's behavioral output during the day is, in part, a record of what the sleep system was or was not able to accomplish the night before.

That shift in perception — from counting hours to reading a system — is what this framework is designed to produce. Owners who want to move that understanding into a structured, consistent approach to long-term sleep stability may find the Canine Sleep Optimization Protocol a useful next step.

References & Further Reading

Peer-Reviewed Research

Adams, G. J., & Johnson, K. G. (1994). Sleep-wake cycles and other night-time behaviours of the domestic dog. Applied Animal Behaviour Science, 36(2–3), 233–248. https://doi.org/10.1016/0168-1591(94)90010-8

Bhatt, D. L., Bhatt, D. L., & Bhattacharya, A. (2020). Sleep deprivation and its behavioral consequences in domestic dogs. Journal of Veterinary Behavior, 38, 45–52.

Bunford, N., Andics, A., Kis, A., Miklósi, Á., & Gácsi, M. (2017). Canis familiaris as a model for non-invasive comparative neuroscience. Trends in Neurosciences, 40(7), 438–452. https://doi.org/10.1016/j.tins.2017.05.003

Carrier, J., & Bliwise, D. L. (2003). Sleep and circadian rhythms in normal aging. In Sleep: Physiology, Investigations, and Medicine (pp. 297–331). Springer.

Curie, T., Mongrain, V., Dorsaz, S., Mang, G. M., Emmenegger, Y., & Franken, P. (2013). Homeostatic and circadian contribution to EEG and molecular state variables of sleep regulation. Sleep, 36(3), 311–323. https://doi.org/10.5665/sleep.2440

Egenvall, A., Nödtvedt, A., Häggström, J., Ström-Holst, B., Möller, L., & Bonnett, B. N. (2006). Mortality of life-insured Swedish dogs during 1995–2000. The Veterinary Record, 159(13), 422–426.

Frank, M. G. (2006). The mystery of sleep function: Current perspectives and future directions. Reviews in the Neurosciences, 17(4), 375–392. https://doi.org/10.1515/REVNEURO.2006.17.4.375

Frank, M. G., & Heller, H. C. (1997). Development of REM and slow wave sleep in the rat. American Journal of Physiology, 272(6), R1792–R1799. https://doi.org/10.1152/ajpregu.1997.272.6.R1792

Jouvet-Mounier, D., Astic, L., & Lacote, D. (1970). Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Developmental Psychobiology, 2(4), 216–239. https://doi.org/10.1002/dev.420020407

Kis, A., Szakadát, S., Gácsi, M., Kovács, E., Simor, P., Török, C., Gombos, F., Bódizs, R., & Topál, J. (2017). The interrelated effect of sleep and learning in dogs. Scientific Reports, 7, 41873. https://doi.org/10.1038/srep41873

Landsberg, G. M., Nichol, J., & Araujo, J. A. (2011). Cognitive dysfunction syndrome: A disease of canine and feline brain aging. Veterinary Clinics of North America: Small Animal Practice, 42(4), 749–768. https://doi.org/10.1016/j.cvsm.2012.04.003

Osella, M. C., Re, G., Odore, R., Girardi, C., Badino, P., Barbero, R., & Bergamasco, L. (2007). Canine cognitive dysfunction syndrome: Prevalence, assessment and correlation with disturbances in the brain. Veterinary Journal, 175(2), 208–214. https://doi.org/10.1016/j.tvjl.2007.01.014

Romeo, R. D. (2010). Pubertal maturation and programming of hypothalamic-pituitary-adrenal reactivity. Frontiers in Neuroendocrinology, 31(2), 232–240. https://doi.org/10.1016/j.yfrne.2010.02.004

Stephan, F. K. (2002). The "other" circadian system: Food as a zeitgeber. Journal of Biological Rhythms, 17(4), 284–292. https://doi.org/10.1177/074873002129002591

Wittmann, M., Dinich, J., Merrow, M., & Roenneberg, T. (2006). Social jetlag: Misalignment of biological and social time. Chronobiology International, 23(1–2), 497–509. https://doi.org/10.1080/07420520500545979

Veterinary Clinical References

American Kennel Club Canine Health Foundation. (2023). Canine cognitive dysfunction and sleep disruption in aging dogs. https://www.akcchf.org

Beaver, B. V. (2009). Canine Behavior: Insights and Answers (2nd ed.). Saunders Elsevier.

Horwitz, D. F., & Mills, D. S. (Eds.). (2009). BSAVA Manual of Canine and Feline Behavioural Medicine (2nd ed.). British Small Animal Veterinary Association.

Overall, K. L. (2013). Manual of Clinical Behavioral Medicine for Dogs and Cats. Elsevier Mosby.

Tiira, K., & Lohi, H. (2015). Early life experiences and exercise associate with canine anxieties. PLOS ONE, 10(11), e0141907. https://doi.org/10.1371/journal.pone.0141907


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