Evaluating the effects of giraffe skin disease and wire snare wounds on the gaits of free-ranging nubian giraffe

ABSTRACT Giraffe skin disease (GSD), a condition that results in superficial lesions in certain giraffe (_Giraffa_ spp.) populations, has emerged as a potential conservation threat.

Preliminary findings suggested that individuals with GSD lesions move with greater difficulty which may in turn reduce their foraging efficiency or make them more vulnerable to predation. A

current known threat to some giraffe populations is their mortality associated with entrapment in wire snares, and the morbidity and potential locomotor deficiencies associated with wounds

acquired from snares. The goal of our study was to quantify the locomotor kinematics of free-ranging Nubian giraffe (_G. camelopardalis camelopardalis_) in Murchison Falls National Park

(MFNP), Uganda, and compare spatiotemporal limb and neck angle kinematics of healthy giraffe to those of giraffe with GSD lesions, snare wounds, and both GSD lesions and snare wounds. The

presence of GSD lesions did not significantly affect spatiotemporal limb kinematic parameters. This finding is potentially because lesions were located primarily on the necks of Nubian

giraffe in MFNP. The kinematic parameters of individuals with snare wounds differed from those of healthy individuals, resulting in significantly shorter stride lengths, reduced speed, lower

limb phase values, and increased gait asymmetry. Neck angle kinematic parameters did not differ among giraffe categories, which suggests that GSD neck lesions do not impair normal neck

movements and range of motion during walking. Overall, MFNP giraffe locomotor patterns are largely conservative between healthy individuals and those with GSD, while individuals with snare

wounds showed more discernible kinematic adjustments consistent with unilateral limb injuries. Additional studies are recommended to assess spatiotemporal limb kinematics of giraffe at sites

where lesions are found predominantly on the limbs to better assess the potential significance of GSD on their locomotion. SIMILAR CONTENT BEING VIEWED BY OTHERS RAPID RECOVERY OF LOCOMOTOR

PERFORMANCE AFTER LEG LOSS IN HARVESTMEN Article Open access 13 August 2020 MALLARD HINDLIMBS LOCOMOTION SYSTEM RESPOND TO CHANGES IN SANDY GROUND HARDNESS AND SLOPE Article Open access 05

July 2024 THE DIFFERENTIATED IMPACTS AND CONSTRAINTS OF ALLOMETRY, PHYLOGENY, AND ENVIRONMENT ON THE RUMINANTS’ ANKLE BONE Article Open access 18 March 2025 INTRODUCTION Once widely

distributed across the continent of Africa, giraffe (_Giraffa_ spp.) have declined in both distribution and abundance over the last century due to habitat loss and fragmentation, civil

unrest, poaching (i.e., illegal hunting), and ecological change1,2,3,4. Giraffe populations experienced an overall ~ 30% decline in the last three and a half decades, and today there are an

estimated 117,000 giraffe in the wild3. In 2016, the International Union for Conservation of Nature (IUCN) up-listed giraffe as a single species (i.e., _Giraffa camelopardalis_) from “Least

Concern” to “Vulnerable” on the Red List, emphasizing the population declines and severity of threats facing them. The taxonomic classification of giraffe is a topic of

debate5,6,7,8,9,10,11,12; however, here we utilize the classification that recognizes four taxonomically distinct species: Masai giraffe (_G. tippelskirchi_), reticulated giraffe (_G.

reticulata_), northern giraffe (_G. camelopardalis_), and southern giraffe (_G. giraffa_)7,8,12. The conservation status of three species (_G. tippelskirchi_, _G. camelopardalis_, and _G.

reticulata)_ are of great concern, with their numbers all declining by > 50% and absent from much of their estimated historic geographical ranges3,13. Giraffe play a key role in shaping

the ecology of savannah and woodland ecosystems, and their loss across the continent could have far-reaching long-term ecological consequences14,15. In the mid-1990’s, giraffe skin disease

(GSD) emerged as a new potential threat to giraffe conservation. GSD was first described in a population of Nubian giraffe (_G. c. camelopardalis_) in Uganda16. Since then, GSD has been

detected in at least 13 parks and reserves across seven countries in Africa, including South Africa, Botswana, Namibia, Zimbabwe, Kenya, Tanzania, and Uganda17. Prevalence of GSD has been

reported to be as high as 86% in Masai giraffe inhabiting Ruaha National Park (NP), Tanzania18,19,20, and at a given time, as many as 51% of giraffe in Murchison Falls NP (MFNP) in Uganda

may be afflicted with visible signs of GSD (M. Brown, pers. comm., May 2021). Furthermore, skin conditions resembling GSD have been reported in 11 zoos in six countries, including Belgium,

England, France, Italy, the Netherlands, and the United States17. We now know that GSD manifests as different skin conditions; however, all GSDs generally manifest as large, crusted,

scab-like wounds, sometimes with accompanying cracks in the skin, appearing mainly on the limbs, chest, and neck, though location of lesions differs by geographical location17,18,21,22,23

(Fig. 1A). Several etiological agents have been suggested in the pathogenesis of different GSDs, including bacterial, fungal, and protozoal organisms, although current research suggests a

nematode origin, with possible accompanying fungal infection18,23,24. Further, the mode of transmission of GSDs remains unknown. In some populations, severe forms of infection could make

afflicted individuals more prone to predation because it may affect locomotion. Researchers have noted that infected animals seem to move with difficulty or suffer from lameness18; however,

no studies to date have systematically studied the effects of GSDs on giraffe locomotion. As MFNP giraffe travel an average of ~ 14 km per day (M. Brown, pers. comm., May 2021), a disease

that affects locomotor mechanics and efficiency could have serious consequences for an individual’s ability to seek resources25 and evade predators26,27. Another threat to some giraffe

populations is morbidity associated with snare-related injuries and potential mortality caused by entrapment in wire snares (Fig. 1B). The increasing illegal harvesting of bushmeat is a

significant cause of population declines for many wildlife species across sub-Saharan Africa, and the use of wire snares is a common technique28. The relatively indiscriminate nature of

snares results in a considerable amount of unintended bycatch29,30, which includes giraffe4,31. In addition to the mortality associated with poaching, injuries associated with escaping from

snares have been shown to affect locomotion and behavior in other taxa32 and have been linked to increased parasite load33. In giraffe, modified locomotion and behavior could potentially

increase predation risk and decrease foraging efficiency. In this way, evaluating the effects of snare wounds on giraffe locomotion could lead to a deeper mechanistic understanding of

snare-related mortality and morbidity. A handful of studies have examined the locomotion and gait of giraffes34,35,36,37,38,39. These important studies provide the groundwork for our

investigation. Recently, Basu et al.39 quantified spatiotemporal limb kinematics, kinetics (i.e., ground reaction forces), and neck angle kinematics of walking gaits in three adult

zoo-housed reticulated giraffe. They found that giraffe walking gaits can be classified as lateral sequence, lateral couplets (LSLC, i.e., a gait in which the touchdown of a hindlimb is

followed shortly thereafter by a touchdown of the ipsilateral forelimb). This gait type helps to avoid limb interference in which limbs contact one another during the stride but differs from

a true “pace” gait where the touchdowns and liftoffs of ipsilateral limbs is simultaneous or approximately simultaneous40. The movement of the neck is functionally linked to the giraffe

walking gait, with horizontal acceleration of the neck out of phase with the horizontal acceleration of the trunk39. The goal of our study was to quantify the spatiotemporal limb kinematics

and neck angle kinematics in free-ranging Nubian giraffe in MFNP. In doing so, we compared kinematic parameters of healthy free-ranging giraffe (i.e., no visible GSD nor visible snare

wounds) to those of free-ranging giraffe with GSD, snare wounds, and both GSD and snare wounds. Based on field observations that some giraffe with GSD were found to walk with greater

difficulty18, we predicted that the spatiotemporal limb kinematics and neck angle kinematics of individuals with GSD would differ from those of healthy individuals. We also examined the

mechanisms through which snare wounds impacted giraffe locomotion and predicted that, compared to healthy giraffe, individuals with snare wounds would exhibit slower walking speeds and

kinematic adjustments consistent with reduced loading on the injured limb41. To our knowledge, our study is the first to quantify walking gait kinematics in free-ranging giraffe and the

first to test whether and how GSD and snare wounds affect giraffe locomotion. Given the prevalence of GSD and intense wire snaring pressure on giraffe in MFNP, gaining a better understanding

of how GSD and snare wounds impact locomotor capabilities of afflicted giraffe will provide important context for assessing broader health and fitness. METHODS SUBJECTS AND VIDEO RECORDINGS

PRELIMINARY DATA COLLECTION AT CLEVELAND METROPARKS ZOO We first developed and piloted our methods in a zoo setting at Cleveland Metroparks Zoo, Ohio, USA, before applying them to videos of

free-ranging Nubian giraffe from MFNP. We analyzed the gait of four Masai giraffe at Cleveland Metroparks Zoo including: one adult male (aged eight) and three adult females (aged seven,

nine, and ten). The subjects were known to be in good health during the time of observation. We filmed giraffe at 30 frames per second walking over flat ground using a Casio EX-FC150 camera.

Thirteen video clips containing 31 strides were suitable for spatiotemporal limb kinematic analyses (i.e., all footfalls visible), and seven strides were suitable for neck angle kinematic

analyses (i.e., giraffe moving approximately perpendicular to the camera). MURCHISON FALLS NATIONAL PARK (MFNP) We collected data on 52 adult male giraffe in MFNP (2.1458° N, 31.8069° E)

from July 2015–August 2016. In association with a long-term study designed to evaluate the demography and spatial ecology of male giraffe in MFNP, a series of fixed route individual based

photographic surveys were conducted over the entire extent of the park42. We identified each individual using their unique pelage patterns43. Videos were recorded opportunistically during

ongoing conservation science research, which included assessing the etiology of GSD locally23. All videos were recorded at ~ 75–100 m from the focal animal. Individuals were recorded on flat

ground to control for gait adjustments driven by changes in terrain and inclination/declination. Each giraffe was assigned to one of four condition categories: (1) healthy (i.e., no visible

GSD lesions nor snare wounds), (2) GSD (presence of GSD lesions), (3) snare (presence of snare wound), or (4) GSD and snare (presence of both GSD lesion(s) and snare wound). We acknowledge

that giraffe assigned to our healthy category may have underlying health issues other than GSD, and some historical snare wounds are not easily observable; however, we assumed these

potential factors did not significantly impact the kinematic variables examined in our study. Additionally, we recognize that researchers have categorized the severity of GSD18,22; however,

due to limitations with our sample size, we opted to report presence vs. absence of GSD as other studies have done19,44. Giraffe locomotion at MFNP was filmed at 30 frames per second using

either a Nikon CoolPix AW110 or a Canon 7D Mark II digital camera. We selected only videos with clear, unobstructed views of limb touchdowns (n = 32 videos). The videos included in the

spatiotemporal gait analyses ranged from eight to 49 s and contained between one and eight strides per individual (n = 115 strides). We attempted to film perpendicular to the line of travel

when possible; however, parallax is not an issue for timing and digitizing limb touchdown and liftoff events. Furthermore, our spatial points (i.e., stride length and shoulder height) were

all digitized in the same video frame for a given video clip, eliminating potential distortion due to parallax issues. That is, all in-plane linear distance metrics would suffer a similar

degree of distortion, allowing ratios of these distances to be unbiased45. Because angular measurements are susceptible to parallax issues, only strides in which giraffe were moving

approximately perpendicular to the camera were used to quantify neck angle measurements (n = 71 strides) (Table 1). DIGITIZING METHODS We used GaitKeeper, an open-source MATLAB package, to

digitize limb liftoff and touchdown events, stride length, and shoulder height45 (Fig. 2; http://www.younglaboratory.org/GaitKeeper). We recorded neck angle measurements for individual

videoframes using the angle tool in ImageJ46. KINEMATIC VARIABLES SPATIOTEMPORAL LIMB KINEMATICS We quantified giraffe shoulder height (in pixels) by digitizing a point at roughly the height

of the glenohumeral joint and another point at ground level directly below the shoulder. We quantified stride length (in pixels) by digitizing the initial touchdown of a reference limb

(e.g., left hindlimb) and the subsequent reference limb touchdown. Relative stride length was calculated by dividing stride length in pixels by shoulder height in pixels. Relative (i.e.,

dimensionless) stride length was reported to account for differences in body size among giraffe. We predicted that giraffe with GSD and/or snare wounds would have shorter relative stride

lengths than healthy individuals41. Stride duration was recorded as the amount of time (in seconds) between the initial and subsequent touchdown of a reference limb. We used stride durations

for each limb to generate mean stride duration. We predicted that giraffe with GSD and/or snare wounds would have greater mean stride durations than healthy individuals41. We calculated

relative speed by dividing relative stride length by mean stride duration, resulting in values with units of % of shoulder height per second. Relative speed was reported to control for

potential speed differences due to differences in body size among giraffe. We predicted that giraffe with GSD and/or snare wounds would move at slower relative speeds compared to healthy

individuals41. We quantified footfall patterns according to limb phase which is defined as the proportion of stride duration separating hindlimb touchdown from ipsilateral forelimb touchdown

during symmetrical gaits. Limb phase patterns are associated with stability during movement47 and vary among species due to differences in anatomy and habitats and can vary within a species

or individuals depending on the speed of movement and the substrate or terrain in which the animal is moving. These limb phase values are often used to classify symmetrical gaits such that

limb phase values between 0 and 25% are designated as LSLC gaits, values between 25 and 50% are lateral sequence, diagonal couplet (LSDC) gaits, values between 50 and 75% are diagonal

sequence, diagonal couplet (DSDC) gaits, and values between 75 and 100% are diagonal sequence, lateral couplets (DSLC) gaits. While researchers utilize different thresholds for named gait

types, limb phase values equal to or approximately equal to 0%, 25%, 50%, and 75% are classified as pace, lateral sequence singlefoot, trot, and diagonal sequence singlefoot gaits,

respectively40,47,48. Our preliminary data revealed that Masai giraffe housed at Cleveland Metroparks Zoo exclusively used LSLC walking gaits—a pattern consistent with another recent study

of zoo-housed reticulated giraffe39. We predicted that free-ranging Nubian giraffe would also use LSLC gaits and tested whether limb phase values for giraffe with GSD and/or snare wounds

deviated from the limb phase values of healthy giraffe. The mean number of supporting limbs (NSL) can theoretically vary between zero (i.e., aerial phase) and four (i.e., stationary animal)

throughout different portions of a stride. We quantified the portion of stride duration in which individuals were supported by zero, one, two, three or four limbs, to generate mean NSL

throughout the stride49,50,51. Controlling for speed, we predicted that giraffe with snare wounds would have greater mean NSL compared to healthy individuals as a strategy to reduce loading

on the affected limb41. We quantified duty factor (i.e., the amount of time a limb is in contact with the ground divided by stride duration) for each of the four limbs. We then calculated an

asymmetry index for ipsilateral duty factors (ipsilateral DFAI) modified from Robinson et al.52 and Vanden Hole et al.53 such that: ((Ldf − Rdf)/(0.5 (Ldf + Rdf)) × 100, where Ldf = mean of

left forelimb and left hindlimb duty factors and Rdf = mean of right forelimb and right hindlimb duty factors. Values can theoretically range from − 100 to 100% with 0% indicating perfect

contralateral symmetry. More negative values indicate lower duty factors on the left limbs compared to the right limbs. More positive values indicate lower duty factors on the right limbs

compared to the left limbs. For animals with unilateral snare injuries, we modified the equation such that the injured/affected limb would be considered first. That is, for animals with

right limb snare wounds, we used ((Rdf − Ldf)/(0.5 (Rdf + Ldf)) × 100. Thus, more negative values indicate lower duty factor on the side of the injured limb and more positive values indicate

greater duty factors on the side of the injured limb. Because giraffe are typically supported by ipsilateral limb couplets for long periods of stride duration39, we predicted that

individuals with unilateral snare injuries would have more negative ipsilateral DFAI values due to reduced contact time on the side of the injured limb as part of a pattern to reduce loading

on that limb41,54. In contrast, we predicted healthy individual would have ipsilateral DFAI values equal to or close to zero (i.e., consistent with contralateral symmetry). NECK ANGLE

KINEMATICS A giraffe’s neck oscillates twice during a typical walking stride with peak dorsal extension (i.e., neck more vertical) occurring during early stance phase of each forelimb and

peak ventral flexion (i.e., neck more horizontal) occurring at roughly midstance of each forelimb35,39. Basu et al.39 found that the horizontal acceleration of the neck was largely out of

phase with the acceleration with the trunk which likely allows giraffe to move more efficiently (i.e., similar to how a crouched jockey can horizontally oscillate their body out of phase

with a race horse’s body thereby reducing the mass the horse has to accelerate and decelerate in the horizontal plane). This ultimately improves the horse’s locomotor performance55. Given

the importance of the neck during giraffe locomotion, we quantified neck angle during peak dorsal extension and peak ventral flexion for each stride. Points located at the base of the tail,

apex of the dorsal spinous processes of the thoracic vertebrae (i.e., “withers”), and apex of the occipital bone posterior to the ossicones were used to generate the neck angle. These

landmarks were chosen because they were easily observable on the giraffe from our video sample (Fig. 3) and are similar to those used previously35,39. We digitized neck angle in each video

frame using ImageJ46 and identified the minimum and maximum values as peak dorsal extension and peak ventral flexion, respectively. We then calculated neck range of motion (ROM) as the

difference between peak ventral flexion and peak dorsal extension following Basu et al.39. STATISTICAL ANALYSES We used linear mixed models to examine the effect of giraffe condition on

spatiotemporal limb kinematics variables, including relative stride length, mean stride duration, relative speed, limb phase, mean NSL, and ipsilateral DFAI. Similarly, we used linear mixed

models to assess the effect of giraffe condition on neck angle kinematics, including peak dorsal extension, peak ventral flexion, and neck ROM. For all statistical models, we included GSD

(presence vs. absence) and snare wound (presence vs. absence) as fixed factors. Individual giraffe were nested within video clip as a random factor (intercept) in each model to control for

random variation between individuals, providing greater power to detect meaningful variation associated with the fixed factors of interest (i.e., presence vs. absence of GSD and snare

wound). Satterthwaite approximations were used to adjust degrees of freedom in cases of heteroscedasticity for all models relating giraffe condition to spatiotemporal limb kinematics and

neck angle kinematics. Analyses were conducted in R statistical software56, including add-on packages: lme4 and lmerTest57. We used the emmeans package58 to generate estimated marginal mean

values for each dependent variable listed above. Post hoc pairwise comparisons of mixed models were conducted using the emmeans package, with multiple pairwise comparisons corrected using

the false discovery rate method59. Relative speed was included as a covariate in the mean NSL and neck ROM models because speed has been shown to negatively correlate with mean NSL in other

taxa51 and positively correlate with neck ROM in zoo-housed giraffe39. RESULTS ZOO VS. FIELD DATA We found that the spatiotemporal limb kinematics and neck angle kinematics of the zoo-housed

Masai giraffe were generally similar to those recorded in healthy free-ranging Nubian giraffe (Table 2). Given the two datasets were collected on different giraffe species occupying

different environments, and the fact that the zoo sample contained both an adult male and three adult female giraffe and the free-ranging samples contained only adult male giraffe, we did

not statistically compare the two datasets. Nonetheless, the similar results suggest that our methods developed at Cleveland Metroparks Zoo were transferrable to field conditions. EFFECTS OF

GIRAFFE CONDITION ON SPATIOTEMPORAL LIMB KINEMATICS We found that GSD lesions were primarily located on the necks of giraffe in our sample (Table 3). Snare wounds were observed more

frequently on one of the hindlimbs (n = 9) compared to one of the forelimbs (n = 4) (Table 3). The presence of snare wounds affected multiple aspects of spatiotemporal limb kinematics while,

contrary to our predictions, the presence of GSD did not significantly affect any of the spatiotemporal limb kinematic variables investigated (Table 4). When examining post hoc multiple

pairwise comparisons of estimated marginal means, individuals with only snare wounds had significantly shorter relative stride lengths (p = 0.006), slower relative speeds (p = 0.009), lower

limb phase values (p = 0.01), and more negative ipsilateral DFAI (p = 0.02) compared to healthy giraffe. Similarly, individuals with both GSD and snare wounds had lower limb phase values (p 

= 0.04), and more negative ipsilateral DFAI (p = 0.02) compared to healthy individuals (Table 5; Fig. 4). EFFECT OF GIRAFFE CONDITION ON NECK ANGLE KINEMATICS The presence of GSD had a

significant effect on peak ventral flexion (Table 6); however, posthoc tests revealed no significant differences among groups after controlling for multiple pairwise comparisons (Table 7;

Fig. 5). DISCUSSION We undertook the first in-depth investigation of the spatiotemporal limb kinematics and neck angle kinematics of walking gaits in free-ranging Nubian giraffe. We found

that the spatiotemporal limb kinematics of healthy free-ranging giraffe from our sample were generally comparable to those of healthy zoo-housed Masai giraffe both from our preliminary

analyses at Cleveland Metroparks Zoo and those reported in Basu et al.39. In general, all giraffe used LSLC walking gaits. The average gait cycle of the healthy Nubian giraffe recorded can

be described as 66:13 in Hildebrand40 terms (i.e., mean duty factor %: limb phase %), which is similar to the 64:15 average gait recorded in our Cleveland Metroparks Zoo sample and the 70:14

average gait recorded by Basu et al.39. This suggests that basic kinematic parameters of giraffe walking gaits are conservative across environments and among healthy individuals of

different giraffe taxa. Contrary to our predictions from the knowledge that some Masai giraffe with GSD were found to walk with greater difficulty18, the spatiotemporal limb kinematics of

Nubian giraffe with only GSD did not differ from those of healthy giraffe. This result is potentially attributable to the fact that GSD lesions were predominantly found on the necks in our

sample. GSD primarily affects the necks of the MFNP’s Nubian giraffe population21, while GSD lesions are more commonly found on the limbs of giraffe taxa at other sites surveyed to date:

e.g., Tanzania (Masai giraffe—Manyara Ranch Conservancy, Selous Game Reserve, Ruaha NP, Serengeti NP, and Tarangire NP) and Namibia (Angolan giraffe—Etosha NP and Puros Conservancy)17. It is

not yet clear why the population in MFNP is affected primarily on the neck as opposed to the limbs, although ongoing studies by Giraffe Conservation Foundation and partners are being

undertaken to evaluate etiology and vector dynamics. We found that giraffe with snare wounds had shorter stride lengths, slower walking speeds, reduced limb phase values, and more negative

ipsilateral DFAI compared to healthy giraffe. Similarly, giraffe with both GSD and snare wounds had reduced limb phase values, and more negative ipsilateral DFAI compared to healthy giraffe.

In their study of zoo-housed giraffe, Basu et al.39 found that stride frequency (i.e., inverse of stride duration) was consistent across walking speeds and that giraffe increased walking

speed by taking longer strides. Our results support this pattern, as giraffe with snare wounds had shorter stride lengths (but consistent stride durations) resulting in slower relative

speeds. These kinematic compensations are common in animals with limb or hoof pathologies, and increased ipsilateral asymmetry, in particular, is consistent with a strategy to reduce loading

on the injured limb41,54. The more negative ipsilateral DFAI values for giraffe with snare wounds indicate shorter contact durations, and potentially reduced peak ground reaction forces

and/or impulse, on the side of the injured limb. Recording the ground reaction forces of different limbs throughout stride sequences via force plates could be used to test this assumption—a

technique commonly employed to detect lameness in domestic and laboratory animals60,61,62. The decreased mobility and locomotor efficiency of individuals with snare wounds could have

important ramifications for giraffe health and fitness. Giraffe in MFNP travel ~ 14 km per day (M. Brown, pers. comm., May 2021), whilst some individuals, especially subadult and adult

males, embark on seasonal migrations related to changes in food availability in the park. As part of these seasonal migrations, individuals may travel up to 30 km between acacia savanna in

the wet seasons and broadleaf savanna in the dry seasons63. Reduced mobility in affected giraffe may reduce foraging efficiency, limit the extent of seasonal movements, and/or reduce the

amount of time giraffe can spend engaging in other behaviors (e.g., resting, breeding, etc.) due to increased time spent locomoting. Impaired mobility may also have negative consequences on

important social behaviors. For example, adult males compete for access to females with larger bulls typically out-competing other males64,65. Subordinate males may travel in search of other

locations where female density is too high for bulls to effectively monopolize63. Locomotor deficiencies related to snare wounds and/or GSD may limit dominant males’ ability to mate guard

and limit more subordinate males’ ability to travel in search of other breeding opportunities. Finally, although giraffe predation is rare in MFNP21, reduced mobility and potential flight

ability may make affected individuals more vulnerable to predators. Muneza et al.27 examined relationships between GSD and lion predation in Ruaha NP—a site where giraffe are commonly preyed

upon by lions. The study documented a positive relationship between severe GSD lesions and signs of attempted lion predation (i.e., bite marks, claw marks, and amputated tails). This

suggests lions may preferentially target individuals with severe GSD; however, the authors found no evidence that GSD lesions impacted the likelihood of surviving a lion attack and were not

able to record GSD presence or severity on giraffe killed by lions. Walking gaits were characterized by two oscillations of the neck (one for the left limbs and one for the right limbs).

Peak dorsal extension of the neck was consistent with early stance phase of each forelimb and peak ventral flexion occurred at roughly midstance of each forelimb as other have

described35,39. Basu et al.39 modelled neck accelerations and mean ground reaction forces to assess the relationship between the accelerations of the trunk and neck. They found that the

horizontal acceleration of neck was largely out of phase (i.e., phase relationship of 23%) with the horizontal acceleration of the trunk, essentially decoupling neck movement from the rest

of the body which likely results in significant energy savings. We did not find any significant differences in peak dorsal extension or peak ventral flexion of the neck when comparing

animals with GSD and/or snare wounds to healthy individuals. Controlling for speed, neck ROM did not differ among the different condition categories. This is noteworthy given the prevalence

of GSD lesions on the neck of giraffe in our sample and suggests that normal neck ROM during walking gaits is attainable despite GSD lesions on the neck. Future research examining the

spatiotemporal gait kinematics of the various giraffe taxa at locations where GSD is common on the limbs is required to better determine the extent to which GSD may affect locomotion. Muneza

et al.22 found that GSD was especially common on the forelimbs (including cases of unilateral and bilateral lesions) but less common on the hindlimbs of Masai giraffe in Ruaha and Serengeti

NPs. This provides an opportunity to examine how forelimb vs. hindlimb, and unilateral vs. bilateral limb lesions impact gait kinematics. Researchers have previously categorized the

severity of GSD by estimating lesion sizes18 or quantifying lesion sizes via photogrammetry techniques22, rather than report presence vs. absence19,44 as we have done here due to limitations

in our sample size. Another recommended line of research would be to test whether severity of GSD (e.g., mild vs. severe forms) differentially impacts giraffe locomotion. Overall, we found

that MFNP’s Nubian giraffe spatiotemporal limb kinematics and neck angle kinematics were largely conservative between healthy individuals and those with GSD. Our results are consistent with

the idea that GSD does not appear to increase mortality of affected giraffe and does not warrant veterinary intervention44; however, future study is required to examine locomotor kinematics

of giraffe at sites where lesions are found predominantly on the limbs to better assess the potential significance of GSD on giraffe locomotion and associated morbidity and mortality. We

found that individuals with snare wounds showed more discernible kinematic compensations consistent with reduced speed and minimized contact on the injured limb. It is likely that some

severe snare wounds impact locomotor efficiency and flight capability to the extent that they increase mortality in affected individuals. Furthermore, many animals, including giraffe, do not

escape from snare entrapments30. In long-term surveys of MFNP, Mudumba et al.30 observed the highest density of wire snares recorded to date in sub-Saharan Africa and recorded the remains

of fifteen giraffe caught in wire snares. Targeted veterinary de-snaring efforts in MFNP from February 2019 to December 2021 effectively removed snares from 257 live giraffe, emphasizing the

severity and scope of this threat (S. Ferguson, pers. comm., April 2021). Ongoing studies in MFNP seek to evaluate the potential fitness costs and impacts of GSD and snare wounds on

survival. Locomotor kinematic studies like ours can provide crucial mechanistic perspectives on emergent patterns of larger scale movements and demographic consequences. MFNP supports the

largest known population of the critically endangered Nubian giraffe remaining in the world, so identifying and quantifying potential threats to this population is of global consequence for

their conservation42. DATA AVAILABILITY All data generated or analyzed during this study are included in this published article as a Supplementary Information file. REFERENCES * Muller, Z.

_et al_. _Giraffa camelopardalis_. The IUCN red list of threatened species 2016:e.T9194A109326950 (2018). * Oconnor, D. _et al._ Updated geographic range maps for giraffe, _Giraffa_ spp.,

throughout sub-Saharan Africa, and implications of changing distributions for conservation. _Mamm. Rev._ 49, 285–299. https://doi.org/10.1111/mam.12165 (2019). Article  Google Scholar  *

Brown, M. B. _et al._ Conservation status of giraffe: Evaluating contemporary distribution and abundance with evolving taxonomic perspectives. _Ref. Module Earth Syst. Environ. Sci._

https://doi.org/10.1016/B978-0-12-821139-7.00139-2 (2021). Article  Google Scholar  * Dunn, M. E. _et al._ Investigating the international and pan-African trade in giraffe parts and

derivatives. _Conserv. Sci. Pract._ 3, e390. https://doi.org/10.1111/csp2.390 (2021). Article  Google Scholar  * Hassanin, A. _et al._ Mitochondrial DNA variability in _Giraffa

camelopardalis_: Consequences for taxonomy, phylogeography and conservation of giraffes in West and Central Africa. _C.R. Biol._ 330, 265–274. https://doi.org/10.1016/j.crvi.2007.02.008

(2007). Article  CAS  Google Scholar  * Groves, C. & Grubb, P. _Ungulate Taxonomy_ (Johns Hopkins University Press, 2011). Book  Google Scholar  * Fennessy, J. _et al._ Multi-locus

analyses reveal four giraffe species instead of one. _Curr. Biol._ 26, 1–7. https://doi.org/10.1016/j.cub.2016.07.036 (2016). Article  CAS  Google Scholar  * Winter, S., Fennessy, J. &

Janke, A. Limited introgression supports division of giraffe into four species. _Ecol. Evol._ 8, 10156–10165. https://doi.org/10.1002/ece3.4490 (2018). Article  Google Scholar  * Bercovitch,

F. B. Giraffe taxonomy, geographic distribution, and conservation. _Afr. J. Ecol._ 58, 150–158. https://doi.org/10.1111/aje.12741 (2020). Article  Google Scholar  * Petzold, A. &

Hassanin, A. A comparative approach for species delimitation based on multiple methods of multi-locus DNA sequence analysis: A case study of the genus _Giraffa_ (Mammalia, Cetartiodactyla).

_PLoS ONE_ 15, e0217956. https://doi.org/10.1371/journal.pone.0217956 (2020). Article  CAS  Google Scholar  * Petzold, A. _et al._ First insights into past biodiversity of giraffes based on

mitochondrial sequences from museum specimens. _Eur. J. Taxon._ 703, L57-63. https://doi.org/10.1371/journal.pone.0217956 (2020). Article  CAS  Google Scholar  * Coimbra, R. T. F. _et al._

Whole-genome analysis of giraffe supports four distinct species. _Curr. Biol._ 31, 2929-2938.e5. https://doi.org/10.1016/j.cub.2021.04.033 (2021). Article  CAS  Google Scholar  * Muneza, A.

B. _et al_. _Giraffa camelopardalis_ ssp._ reticulata_. The IUCN Red List of Threatened Species 2018:e.T88420717A88420720 (2018). * Miller, M. F. Dispersal of _Acacia_ seeds by ungulates and

ostriches in an African Savanna. _J. Trop. Ecol._ 12, 345–356. https://doi.org/10.1017/S0266467400009548 (1996). Article  Google Scholar  * Palmer, T. M. _et al._ Breakdown of an ant-plant

mutualism follows the loss of large herbivores from an African savanna. _Science_ 319, 192–195. https://doi.org/10.1126/science.1151579 (2008). Article  ADS  CAS  Google Scholar  * Kalema,

G. Investigation of a skin disease in giraffe in Murchison Falls National Park. _Report Submitted to Uganda National Park._ Uganda National Parks. Kampala, Uganda (1996). * Muneza, A. B. _et

al._ Regional variation of the manifestation, prevalence, and severity of giraffe skin disease: A review of an emerging disease in wild and captive giraffe populations. _Biol. Conserv._

198, 145–156. https://doi.org/10.1016/j.biocon.2016.04.014 (2016). Article  Google Scholar  * Epaphras, A. M., Karimuribo, E. D., Mpanduji, D. G. & Meing’ataki, G. E. Prevalence, disease

description and epidemiological factors of a novel skin disease in giraffes (_Giraffa camelopardalis_) in Ruaha National Park, Tanzania. _Res. Opin. Anim. Vet. Sci._ 2, 60–65 (2012). Google

Scholar  * Lee, D. E. & Bond, M. L. The occurrence and prevalence of giraffe skin disease in protected areas of northern Tanzania. _J. Wildl. Dis._ 52, 753–755.

https://doi.org/10.7589/2015-09-24 (2016). Article  Google Scholar  * Muneza, A. B. _et al._ Examining disease prevalence for species of conservation concern using non-invasive spatial

capture–recapture techniques. _J. Appl. Ecol._ 54, 709–717. https://doi.org/10.1111/1365-2664.12796 (2017). Article  Google Scholar  * Brown, M. Murchison falls giraffe project: Field

report. _Giraffid_ 9, 5–10 (2015). Google Scholar  * Muneza, A. B. _et al._ Quantifying the severity of an emerging skin disease affecting giraffe populations using photogrammetry analysis

of camera trap data. _J. Wildl. Dis._ 55, 770–781. https://doi.org/10.7589/2018-06-149 (2019). Article  Google Scholar  * Han, S. _et al._ Giraffe skin disease: Clinicopathologic

characterization of cutaneous filariasis in the critically endangered Nubian giraffe (_Giraffa camelopardalis camelopardalis_). _Vet. Pathol._ https://doi.org/10.1177/03009858221082606

(2022). Article  Google Scholar  * Whittier, C. A. _et al._ Cutaneous filariasis in free-ranging Rothschild’s giraffes (_Giraffa Camelopardalis rothschildi_) in Uganda. _J. Wildl. Dis._ 56,

1–5. https://doi.org/10.7589/2018-09-212 (2020). Article  Google Scholar  * Pellew, R. Food consumption and energy budgets of the giraffe. _J. Appl. Ecol._ 21, 141–159.

https://doi.org/10.2307/2403043 (1984). Article  Google Scholar  * Strauss, M. K. L. & Packer, C. Using claw marks to study lion predation on giraffes of the Serengeti. _J. Zool._ 289,

134–142. https://doi.org/10.1111/j.1469-7998.2012.00972.x (2013). Article  Google Scholar  * Muneza, A. B. _et al._ Exploring the connections between giraffe skin disease and lion predation.

_J. Zool._ https://doi.org/10.1111/jzo.12930 (2021). Article  Google Scholar  * Lindsey, P. A. _et al._ The bushmeat trade in African savannas: Impacts, drivers, and possible solutions.

_Biol. Conserv._ 160, 80–96. https://doi.org/10.1016/j.biocon.2012.12.020 (2013). Article  Google Scholar  * Becker, M. _et al._ Evaluating wire-snare poaching trends and the impacts of

by-catch on elephants and large carnivores. _Biol. Conserv._ 158, 26–36. https://doi.org/10.1016/j.biocon.2012.08.017 (2013). Article  Google Scholar  * Mudumba, T., Jingo, S., Heit, D.

& Montgomery, R. A. The landscape configuration and lethality of snare poaching of sympatric guilds of large carnivores and ungulates. _Afr. J. Ecol._ 59, 51–62.

https://doi.org/10.1111/aje.12781 (2020). Article  Google Scholar  * Strauss, M. K. L., Kilewo, M., Rentsch, D. & Packer, C. Food supply and poaching limit giraffe abundance in the

Serengeti. _Popul. Ecol._ 57, 505–516. https://doi.org/10.1007/s10144-015-0499-9 (2015). Article  Google Scholar  * Munn, J. Effects of injury on the locomotion of free-ranging chimpanzees

in the Budongo Forest Reserve, Uganda. In _Primates of Western Uganda: Developments in Primatology: Progress and Prospects_ (eds. Newton-Fisher, N. E., Notman, H., Paterson, J. D., &

Reynolds, V.) 259–280 (Springer, 2006). * Yersin, H., Asiimwe, C., Voordouw, M. J. & Zuberbühler, K. Impact of snare injuries on parasite prevalence in wild chimpanzees (_Pan

troglodytes_). _Int. J. Primatol._ 38, 21–30. https://doi.org/10.1007/s10764-016-9941-x (2017). Article  Google Scholar  * Dagg, A. I. Gaits of the giraffe and okapi. _J. Mammal._ 41,

282–282. https://doi.org/10.2307/1376381 (1960). Article  Google Scholar  * Dagg, A. I. The role of the neck in the movements of the giraffe. _J. Mammal._ 43, 88–97.

https://doi.org/10.2307/1376883 (1962). Article  Google Scholar  * Dagg, A. I. & Vos, A. D. The walking gaits of some species of Pecora. _J. Zool._ 155, 103–110.

https://doi.org/10.1111/j.1469-7998.1968.tb03031.x (1968). Article  Google Scholar  * Alexander, R. M. N., Langman, V. A. & Jayes, A. S. Fast locomotion of some African ungulates. _J.

Zool._ 183, 291–300. https://doi.org/10.1111/j.1469-7998.1977.tb04188.x (1977). Article  Google Scholar  * Basu, C., Deacon, F., Hutchinson, J. R. & Wilson, A. M. The running kinematics

of free-roaming giraffes, measured using a low cost unmanned aerial vehicle (UAV). _PeerJ_ 7, e6312. https://doi.org/10.7717/peerj.6312 (2019). Article  Google Scholar  * Basu, C., Wilson,

A. M. & Hutchinson, J. R. The locomotor kinematics and ground reaction forces of walking giraffes. _J. Exp. Biol._ 222, jeb159277. https://doi.org/10.1242/jeb.159277 (2019). Article 

Google Scholar  * Hildebrand, M. The adaptive significance of tetrapod gait selection. _Am. Zool._ 20, 255–267. https://doi.org/10.1093/icb/20.1.255 (1980). Article  Google Scholar  *

Flower, F. C., Sanderson, D. J. & Weary, D. M. Hoof pathologies influence kinematic measures of dairy cow gait. _J. Dairy Sci._ 88, 3166–3173.

https://doi.org/10.3168/jds.s0022-0302(05)73000-9 (2005). Article  CAS  Google Scholar  * Brown, M. B., Bolger, D. T. & Fennessy, J. All the eggs in one basket: A countrywide assessment

of current and historical giraffe population distribution in Uganda. _Glob. Ecol. Conserv._ 19, e00612. https://doi.org/10.1016/j.gecco.2019.e00612 (2019). Article  Google Scholar  * Foster,

J. B. The giraffe of Nairobi National Park: Home range, sex ratios, the herd, and food. _Afr. J. Ecol._ 4, 139–148. https://doi.org/10.1111/j.1365-2028.1966.tb00889.x (1966). Article 

Google Scholar  * Bond, M. L., Strauss, M. K. L. & Lee, D. E. Soil correlates and mortality from giraffe skin disease in Tanzania. _J. Wildl. Dis._ 52, 953–958.

https://doi.org/10.7589/2016-02-047 (2016). Article  Google Scholar  * Dunham, N. T., McNamara, A., Shapiro, L., Hieronymus, T. & Young, J. W. A user’s guide for the quantitative

analysis of substrate characteristics and locomotor kinematics in free-ranging primates. _Am. J. Phys. Anthropol._ 167, 569–584. https://doi.org/10.1002/ajpa.23686 (2018). Article  Google

Scholar  * Rueden, C. T. _et al._ Imagej 2: Imagej for the next generation of scientific image data. _BMC Bioinform._ 18, 529. https://doi.org/10.1186/s12859-017-1934-z (2017). Article 

Google Scholar  * Cartmill, M., Lemelin, P. & Schmitt, D. Support polygons and symmetrical gaits in mammals. _Zool. J. Linn. Soc._ 136, 401–420.

https://doi.org/10.1046/j.1096-3642.2002.00038.x (2002). Article  Google Scholar  * Hildebrand, M. Analysis of the symmetrical gaits of tetrapods. _Folia Biotheoretica_ 6, 1–22.

https://doi.org/10.2307/1379571 (1966). Article  Google Scholar  * Shapiro, L. J. & Young, J. W. Kinematics of quadrupedal locomotion in sugar gliders (_Petaurus breviceps_): Effects of

age and substrate size. _J. Exp. Biol._ 215, 480–496. https://doi.org/10.1242/jeb.062588 (2012). Article  Google Scholar  * Shapiro, L. J., Young, J. W. & VandeBerg, J. L. Body size and

the small branch niche: Using marsupial ontogeny to model primate locomotor evolution. _J. Hum. Evol._ 68, 14–31. https://doi.org/10.1016/j.jhevol.2013.12.006 (2014). Article  Google Scholar

  * Dunham, N. T., McNamara, A., Shapiro, L., Phelps, T. & Young, J. W. Asymmetrical gait kinematics of free-ranging callitrichines in response to changes in substrate diameter,

orientation, and displacement. _J. Exp. Biol._ 223, jeb217562. https://doi.org/10.1242/jeb.217562 (2020). Article  Google Scholar  * Robinson, R., Herzog, W. & Nigg, B. Use of force

platform variables to quantify the effects of chiropractic manipulation on gait symmetry. _J. Manipulative Physiol. Ther._ 10, 172–176 (1987). CAS  Google Scholar  * Vanden Hole, C. _et al._

How innate is locomotion in precocial animals? A study on the early development of spatiotemporal gait variables and gait symmetry in piglets. _J. Exp. Biol._ 220, 2706–2716.

https://doi.org/10.1242/jeb.157693 (2017). Article  Google Scholar  * Jacobs, B. Y., Kloefkorn, H. E. & Allen, K. D. Gait analysis methods for rodent models of osteoarthritis. _Curr.

Pain Headache Rep._ 18, 456–475. https://doi.org/10.1007/s11916-014-0456-x (2014). Article  Google Scholar  * Pfau, T., Spence, A., Starke, S., Ferrari, M. & Wilson, A. Modern riding

style improves horse racing times. _Science_ 325, 289–289. https://doi.org/10.1126/science.1174605 (2009). Article  ADS  CAS  Google Scholar  * R Core Team. _R: A Language and Environment

for Statistical Computing_. (R Foundation for Statistical Computing, 2019). http://www.R-project.org/. * Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. LmerTest package: Tests

in linear mixed effects models. _J. Stat. Softw._ https://doi.org/10.18637/jss.v082.i13 (2017). Article  Google Scholar  * Length, R. emmeans: Estimated marginal means, aka least‐squares

means. R package version 0.9. https://CRAN.R-project.org/package=emmeans (2017). * Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to

multiple testing. _J. R. Stat. Soc. Ser. B (Methodol.)_ 57, 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x (1995). Article  MathSciNet  MATH  Google Scholar  * Merkens, H. W.

& Schamhardt, H. C. Evaluation of equine locomotion during different degrees of experimentally induced lameness I: Lameness model and quantification of ground reaction force patterns of

the limbs. _Equine Vet. J._ 20, 99–106. https://doi.org/10.1111/j.2042-3306.1988.tb04655.x (1988). Article  Google Scholar  * Fanchon, L. & Grandjean, D. Accuracy of asymmetry indices of

ground reaction forces for diagnosis of hind limb lameness in dogs. _Am. J. Vet. Res._ 68, 1089–1094. https://doi.org/10.2460/ajvr.68.10.1089 (2007). Article  Google Scholar  * Bragança, F.

M. S., Rhodin, M. & van Weeren, P. R. On the brink of daily clinical application of objective gait analysis: What evidence do we have so far from studies using an induced lameness

model?. _Vet. J._ 234, 11–23. https://doi.org/10.1016/j.tvjl.2018.01.006 (2018). Article  Google Scholar  * Brown, M. B. & Bolger, D. T. Male-biased partial migration in a giraffe

population. _Front. Ecol. Evol._ 7, 524. https://doi.org/10.3389/fevo.2019.00524 (2020). Article  Google Scholar  * Dagg, A. I. _Giraffe: Biology, Behaviour and Conservation_ (Cambridge

University Press, 2014). Book  Google Scholar  * Castles, M. P. _et al._ Relationships between male giraffes’ colour, age and sociability. _Anim. Behav._ 157, 13–25.

https://doi.org/10.1016/j.anbehav.2019.08.003 (2019). Article  Google Scholar  Download references ACKNOWLEDGEMENTS Funding for the fieldwork component of this study was made possible by

Cleveland Zoological Society, Giraffe Conservation Foundation and its partners, and Dartmouth College Cramer/RPD Funds. Thanks to the Uganda Wildlife Authority and the rangers/administration

of Murchison Falls National Park for logistical support. Data were collected under Ugandan Wildlife Authority Permit UWA/TDO/33/02, Uganda National Council of Science and Technology Permit

ADM 154/212/03, and Dartmouth College IACUC A3259-01. We thank Roy Ritzmann and Jesse Young for advice on methodology and statistical analyses used in this study. Thanks to Christopher Basu,

John Hutchinson, the editor, and two anonymous reviewers for their comments that improved this manuscript. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Division of Conservation and

Science, Cleveland Metroparks Zoo, 4200 Wildlife Way, Cleveland, OH, 44109, USA L. M. Bernstein-Kurtycz, N. T. Dunham, P. M. Dennis & K. E. Lukas * Department of Biology, Case Western

Reserve University, Cleveland, OH, USA L. M. Bernstein-Kurtycz, N. T. Dunham, J. Evenhuis, P. M. Dennis & K. E. Lukas * Little Rock Zoo, Little Rock, AR, USA L. M. Bernstein-Kurtycz *

College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA J. Evenhuis * Giraffe Conservation Foundation, P.O. Box 86099, Eros, Namibia M. B.

Brown, A. B. Muneza & J. Fennessy * Smithsonian National Zoo and Conservation Biology Institute, Front Royal, VA, 22630, USA M. B. Brown * Department of Biological Sciences Program in

Ecology, Evolution, Ecosystems, and Society, Dartmouth College, Hanover, NH, USA M. B. Brown * Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH, USA P.

M. Dennis Authors * L. M. Bernstein-Kurtycz View author publications You can also search for this author inPubMed Google Scholar * N. T. Dunham View author publications You can also search

for this author inPubMed Google Scholar * J. Evenhuis View author publications You can also search for this author inPubMed Google Scholar * M. B. Brown View author publications You can also

search for this author inPubMed Google Scholar * A. B. Muneza View author publications You can also search for this author inPubMed Google Scholar * J. Fennessy View author publications You

can also search for this author inPubMed Google Scholar * P. M. Dennis View author publications You can also search for this author inPubMed Google Scholar * K. E. Lukas View author

publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS L.M.B.K., N.T.D., J.E., P.M.D., and K.E.L. conceptualized the study. M.B. and J.F. secured funding for

the study and conducted fieldwork in Uganda. L.M.B.K., N.T.D., and J.E. processed videos and extracted data. L.M.B.K. and N.T.D. conducted statistical analyses and drafted the manuscript.

L.M.B.K., N.T.D., J.E., M.B., A.B.M., J.F., P.D., and K.E.L. contributed critically to drafts and gave final approval for publication. CORRESPONDING AUTHOR Correspondence to N. T. Dunham.

ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing interests. ADDITIONAL INFORMATION PUBLISHER'S NOTE Springer Nature remains neutral with regard to jurisdictional

claims in published maps and institutional affiliations. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION. RIGHTS AND PERMISSIONS OPEN ACCESS This article is licensed under a Creative

Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the

original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in

the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your

intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence,

visit http://creativecommons.org/licenses/by/4.0/. Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Bernstein-Kurtycz, L.M., Dunham, N.T., Evenhuis, J. _et al._ Evaluating the

effects of giraffe skin disease and wire snare wounds on the gaits of free-ranging Nubian giraffe. _Sci Rep_ 13, 1959 (2023). https://doi.org/10.1038/s41598-023-28677-y Download citation *

Received: 15 February 2022 * Accepted: 23 January 2023 * Published: 03 February 2023 * DOI: https://doi.org/10.1038/s41598-023-28677-y SHARE THIS ARTICLE Anyone you share the following link

with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt

content-sharing initiative