Skeletal Dysplasia-Like Syndromes in Wild Giraffe

Brown and Wells BMC Res Notes (2020) 13:569 https://doi.org/10.1186/s13104-020-05403-9 BMC Research Notes RESEARCH NOTE Open Access Skeletal dysplasia-like syndromes in wild girafe Michael Butler Brown1,2,3* and Emma Wells1 Abstract Objective: Skeletal dysplasias, cartilaginous or skeletal disorders that sometimes result in abnormal bone development, are seldom reported in free-ranging wild animals. Here, we use photogrammetry and comparative morphometric analyses to describe cases of abnormal appendicular skeletal proportions of free-ranging girafe in two geographically distinct taxa: a Nubian girafe (Girafa camelopardalis camelopardalis) in Murchison Falls National Park, Uganda and an Angolan girafe (Girafa girafa angolensis) on a private farm in central Namibia. Results: These girafe exhibited extremely shortened radius and metacarpal bones relative to other similarly aged girafe. Both girafe survived to at least subadult life stage. This report documents rare occurrences of these apparent skeletal dysplasias in free-ranging wild animals and the frst records in girafe. Keywords: Girafe, Skeletal dysplasia, Disproportionate dwarfsm Introduction dwarfsm in Uda Walwe National Park (NP) in southern Skeletal dysplasias broadly refer to cartilaginous or skel- Sri Lanka [7, 19]. Here, we used digital photogramme- etal disorders that may result in abnormalities in bone try to characterize skeletal dysplasia-like syndromes in development. Tese developmental aberrations are two wild girafe observed during population surveys of sometimes characterized by shortened and irregularly geographically distinct taxa—a Nubian girafe (Girafa proportioned appendicular skeletal anatomy, resulting in camelopardalis camelopardalis) in Murchison Falls NP, what is vernacularly described as disproportionate dwarf- Uganda and an Angolan girafe (Girafa girafa ango- ism [10]. Skeletal dysplasias can be caused by a diverse lensis) on a private farm in central Namibia. We applied suite of molecular etiologies and can manifest in difer- morphometric analyses to compare cervical vertebrae ent forms including micromelia (shortening of the entire and appendicular skeletal measurements of these two limb), rhizomelia (shortening of the femur), mesomelia cases to the dimensions of girafe of diferent age/sex (shortening of the radius, ulna, tibia, and fbula) [14]. classes in the Murchison Falls NP population. Forms of skeletal dysplasias have been described in a wide range of captive and domestic taxa, including dogs Main text [13], cows [1], pigs [9], rats [18], and common marmo- Methods sets [3]. However, observations of wild animals with We conducted standard photographic surveys of the forms of skeletal dysplasia are rare, with notable records girafe population in Murchison Falls NP, Uganda in of a red deer in Scotland with chondrydysplasia [16] and association with ongoing research and monitoring pro- a male Asian elephant with described disproportionate grammes developed to examine population dynamics [5]. From July 2014 until March 2019, we regularly sur- *Correspondence: [email protected]; [email protected] veyed the park at four-month intervals corresponding 1 Girafe Conservation Foundation, Eros, PO Box 86099, Windhoek, approximately with seasonal transition periods (March, Namibia July, December). During these surveys, we systemati- Full list of author information is available at the end of the article cally drove a series of fxed routes comprising the road © The Author(s) 2020. 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The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Brown and Wells BMC Res Notes (2020) 13:569 Page 2 of 6 network over the entire extent of the park where girafe • Phalanx from the end of the distal phalanx to the are known to exist. When girafe were encountered, we approximate end of the lateral proximal sesamoid photographed the perpendicular lateral view of each (Fig. 1a) individual’s right side and identifed every individual • Metacarpal (canon) bone as the lateral proximal sesa- girafe using their unique, unchanging coat patterns in moid to the ulnar carpal bone (Fig. 1b). association with WILDID, a specialized pattern rec- • Radius as the ulnar carpal bone to the lateral epicon- ognition software package [2, 8]. In addition to photo- dyle (Fig. 1c). graphing all encountered girafe, we recorded the spatial • Neck from approximately the C7/T1 vertebrae to the coordinates of each observation, sexed each individual, atlanto-occipital joint (Fig. 1d). and estimated its age class (calf: 0–12 months; subadult female: 1–3 years; subadult male: 1–6 years; adult Using the derived camera body specifc linear rela- female: > 3 years; adult male > 6 years) based on a suite tionships between distance to the girafe and the asso- of diagnostic features including body size, limb propor- ciated pixel size at a given focal length extracted from tions and secondary sex characteristics (see [17]. In embedded Exif fles of the digital image, we calculated Namibia, we conducted targeted surveys of individual the estimated dimensions to the nearest centimeter for properties using similar survey techniques to establish each of the featured morphological traits. baseline girafe population estimates for these areas. To compare morphometric data across age classes, we Photographic survey methods were strictly non-invasive, created a reference morphometric database from the were approved by an Institutional Animal Care and Use central survey database of all recorded girafe observa- Committee (IACUC). tions. All encounters from the database were fltered To better assess age classes and to noninvasively col- to include only images with the recorded distance data lect morphometric data, we also employed a photogram- and focal length associated with our pre-calculated cal- metry technique initially designed for measuring African ibration curves (100 mm, 200 mm, 300 mm, 400 mm). elephant [15] and subsequently adopted for girafe [11]. We then visually inspected the remaining photographs Tis technique uses a laser range fnder to measure the to exclude images in which vegetation and body posi- distance to features of interest, forming a relationship tion obscured potential leg and neck measurements. All with digital pixels in the image and actual size of the focal feature thereby allowing for the accurate measurement of girafe morphological characteristics. To ensure precise relationships between digital pixel size and actual metric units, we frst created reference curves for each desig- nated lens focal length by photographing an object of a known size with a digital camera (Canon 7D Mark II body with Canon Ultrasonic IS 100–400 mm lens and Canon 5D Mark II body with a Canon ef 100–400 mm 1:4.5–5.6 L IS lens. Canon U.S.A., Inc., Melville, New York) at 10 m intervals from 10 to 150 m. Since the pixel to centimeter ratio increases linearly with distance to the photographed object, we determined the linear relationship of the number of pixels in a digital image per centimeter of the object photographed over the range of distances photographed using linear regressions for each specifc focal length (Fig. in Appendix 1). In the feld, when each girafe was photographed, we used a laser rangefnder (Bushnell Scout Arc 1000, Bushnell Outdoor Products, 8500 Mar- shall Drive, Lenexa Kansas 66214) to measure the distance of the camera to the girafe to the nearest 0.1 m. For the corresponding image, we then measured the length in pixels of each of the focal morphological features in the image editing software GIMPv2.8 (GNU Image Manipu- lation Program, GIMP Development Team, http://www. gimp.org). When possible, we measured the following Fig. 1 Diagram of diagnostic morphometrics for digital features: photogrammetry Brown and Wells BMC Res Notes (2020) 13:569 Page 3 of 6 reference anatomical measurements were conducted on measurements (Fig. 2c). According to the landowner, these resulting images. this girafe was born in 2014. We observed the Namibian Since girafe exhibit considerable sexual dimorphism girafe again on 29 July 2020. No other girafe were noted as adults, we grouped the measurements of all girafe with similar morphological abnormalities in either popu- according to age classes (adult, subadult, and calf) and lation surveyed. partitioned adult girafe measurements by sex. To evalu- Morphometric comparisons from photogrammetry ate morphological diferences of the observed dysplastic measurements indicated that both girafe with abnor- girafe from recorded girafe of known age classes, we malities had skeletal proportions that difered signif- calculated the 95% confdence interval for each meas- cantly from population level measurements of subadults urement for each age/sex class and compared to the (Fig. 3). Te Ugandan girafe exhibited a phalanx length observed measurements of each focal dysplastic girafe (21.2 cm) consistent with the reference measurements of to population-level subadult means using one -sample subadult girafe at the population level (20.0 cm, 3.30 SD) t-tests. (t18 = − 1.63, p = 0.12), but the Namibian girafe exhibited a relatively shortened phalanx measurement (15.8 cm) Results for a subadult girafe (t18 = 5.54, p < 0.01) (Fig.

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