Ectoparasitic Skin Diseases of Two-toed and Three-toed Sloths in Costa Rica

Stephanie Dewell

Faculty Sponsor: Dr. Clay Britton epartent of iology

Abstract

total of sloths in the wil an in captiity eight ariegats an eight C hoffanni were ealate for eratitis oer a twowee perio in anel ntonio Costa ica ngal cltre sin ipression an sin scrapings were concte on each iniial case in orer to follow the ifferential iagnostic ini ataase of sall anial eratology Captie poplation saples were taen fro a willife sanctary an he loth nstitte Costa ica rehailitation facility efinitie iagnosis was not possile in fie of the cases n the captie poplation si ariegats an fie C hoffanni eratophytosis y icrospor gypse was etecte in three C hoffanni alts sarcoptic ange in three prritic ariegats infants an pyotraatic eratitis in one alt C hoffanni oonotic ectoparasites were fon eclsiely in the captie sloth poplations at the willife sanctary ie sloths fro the wil presente with sin lesions electric shoc traa fro telephone wires was the priary case of of these lesions an seconary alasseia eratitis an pyotraatic eratitis were confire with sin ipression he general trens of the trial inicate that the ost prealent case of eratitis was oonotic ectoparasites roper anageent an increase iological secrity in captie poplations ay contrite to the preention of isease transission

Introduction

rayps ariegats an Choloeps hoffanni respectiely nown as the threetoe an twotoe sloths are inhaitants of tropical rainforests of the Cariean an acific regions of Central an oth erica cCarthy et al loths are priarily aroreal aals an elong to the taonoic orer ilosa ccoring to the e ist of hreatene pecies plishe y the nternational nion for Conseration of Natre an Natral esorces NC nearly half of the genera elonging to the faily raypoiae are recognie as critically enangere with ecreasing poplation trens C hoffanni shares the phylogenic faily egalonychiae with one other sloth species Choloeps iactyls hogh C hoffanni an ariegats are crrently liste as two species of least concern NC their ftre srial is threatene y trens of

65 rapi eforestation an han encroachent on their natral haitat arence et al iaaorales et al ering as a pilot sty for eelopent of a recor of ectoparasitic infections aong Costa ican sloths the crrent research ses the eratologic testing ini ataase to enale ientification of specific ectoparasitic organiss in the sect poplation of sloths soe captie an soe wil he reslts spport the proposition that oonotic ectoparasites—parasites that can e transitte fro anials to hans— are the ost coon case of eratitis in captie sloths an ths that proper anageent an increase iological secrity in captie poplations are esirale to preent isease transission in oth han an anial poplations

Habitat Loss & Fragmentation ring the s an s Costa ica eperience soe of the highest rates of poplation growth an of eforestation in the worl iy an alloni aer an oyce aitat loss an fragentation threaten sloth srial as they not only isplace the sloths fro their appropriate niche t also sect the species to a ast array of physiological stressors they wol not eperience in the wil he Costa ican goernent has proote ecotoris to presere the eteriorating tropical lanscape of Costa ica t its policy has seeral liitations anghol et al y efinition ecotoris enales traelers fro aron the worl to eperience the natral forest an willife while inflicting inial han ipact on the natie ecosystes et sties analying the echaniss y which toris of the tropics is eelope operate an organie inicate that crrent practices allow for negatie ipact on the aintenance of oerall healthy ecosystes saacs er the last two ecaes sloths hae ecoe an increasingly poplar attraction to traelers in Central erica ong sloths are often captre an taen fro their others in the wil an hel captie in iproise shelters here they are sol to international traelers oreno an lese oth yers an sellers of the sloths are often naware of the specific ietary nees of the anial reslting in the srrener of etreely alnorishe iniials to rehailitation facilities f the sloths intercepte y officials fro trafficers in only sloths were ale to srie rehailitation— of the ariegats species an of the C hoffanni species oreno an lese

Clinical Disorders loths are ecoing increasingly lnerale to isease as raniation an ecotoris introce irect pathways for infectios organiss that are ncoon in the wil s wil haitats shrin an wil sloths are captre not only are sloths epose to nfailiar parasites an other organiss carrie y oestic anials t also their inocopetency is coproise y the stresses of ran haars an inappropriate iets realent clinical isorers recore aong oth species are ntritional isorers igestie alaies respiratory coplications an inries ini an liiera ne case of haitat estrction reslte in the isplaceent of nearly sloths to grasslans an eaches where they sffere fro staration ehyration an parasite infection oreno an lese Coon physical inries reporte after the haitat istrance incle ehicleince

66 which increased the sloths’ susceptibility to secondary bacterial infect

Dermatitis: Transmission and Manifestations fungal skin diseases that ultimately hinder the sloth’s mobility and ability to feed (Diniz

67 because the species of mite that infects animals is only able to reproduce on its specific host (andi and aikumar alton scabiei infestation on both the animal host and human reseroir presents as lesions including papules alopecia erythema crusts and ecoriations (lack Diaz nilica esions formed by hypersensitiities to the byproducts of the animal mange mite lead to secondary bacterial infection therefore differential diagnosis is crucial to the oerall health of the animal host Dermatophytosis (ringworm is a zoonotic fungal infection of the hair shafts caused by keratinophilic fungi from the genera icrosporum richophyton and pidermophyton (aier et al nlike yeast dermatitis dermatophyte organisms are transmitted through direct contact with fur and dandruff that contain fungal particles originating from an infected animal or enironment kin inolement in both humans and animals may be localized or generalized with areas of circular irregular or diffuse alopecia with scaling ther symptoms include erythema papules crusts seborrhea and onychodystrophy of the digits (nilica

Differential Diagnosis he dermatologic diagnostic minimum database includes skin scrapes cutaneous skin cytologyimpression and fungal cultures (nilica Differential diagnosis is crucial to determine the primary cause of a skin disease since lesions appear similar howeer these diseases can also cooccur and reuire different methods of treatment s discussed in detail below published research has not applied these differential diagnostic standards possibly resulting in the publication of falsenegatie findings er a oneyear period osta ican sloth species from au aulo oo were eamined for gastrointestinal parasites and ectoparasites he study concluded that sloths presented with pruritic lesions erythema and hair loss and were positie for scabiei itch no eidence of fungal infection was found (ibaaorales et al hough ibaaMorales and colleagues’ study was the first to discover that captie sloths can be infected with sarcoptic mange it is of concern that no diagnostic test other than skin scraping was documented he diagnosis was further supported when four researchers deeloped rashes after handling infected sloths (ibaaorales et al onetheless this method raises seeral uestions for concern as the accuracy of skin scrapings is less than percent when no other diagnostic test is performed (nilica alter n additional study in outh merica discoered that of fungal cultures taken from sloths that presented with skin lesions tested positie for dermatophytosis from the genera icrosporum (aier et al he researchers in this study did not perform additional skin impression and skin scraping tests which fails the standard of differential diagnosis in small animal dermatology uch incomplete protocols can lead to ineffectie treatments with hazardous effects not just on the animal’s health but also on the alidity of statistics for future research esearch pertaining to ariegatus and hoffmanni ectoparasitic diseases is a relatiely new field hile a few studies hae inestigated the presence of clinical diseases in sloths—and incorporate a brief synopsis of dermatological illnesses—the researchers hae not conducted differential diagnosis of skin diseases whether in wild or captie

68 animals ini and liviera Moreno and lese ibajaMorales et al avier et al he objective of the resent research is to serve as a ilot study to aid in establishing a recorded foundation of ectoarasitic infection incidence in sloths across various environments in osta ica by utiliing the dermatologic testing minimum database he hyothesis of this study is that oonotic ectoarasites are the rimary cause of dermatitis in both cative and wild sloth oulations in osta ica he data collected throughout this eeriment can be utilied in future longterm studies investigating the rimary cause of sin diseases urthermore an increased freuency of oonotic arasite infection would indicate the need for establishing reventive measures to avoid further transmission in both the human and animal oulations

Materials and Methods

Location ifferential diagnostics were conducted on sloth secies hoffmanni and variegatus residing in the wild and in cativity over a twowee eriod in Manuel ntonio osta ica amles from cative secimens were obtained from two searate facilities he first facility a wildlife sanctuary is located m outside ueos entral he sanctuary is oen three hours daily to the general ublic for wildlife tours loths are searated by age and laced in either the nursery or ehibition enclosure he nursery is a solid studio structure that serves as housing for infant and juvenile sloths of both secies he adult hoffmanni sloths are held in a steel wire ehibition enclosure m as there are no adult variegatus individuals he second samling site the loth nstitute osta ica located in Manuel ntonio is a research facility that rehabilitates and reintroduces sloths into the wild houses variegatus and hoffmanni adult individuals that are held in enclosures m divided by steel fencing for searation of the secies loths are in direct contact with trained research rofessionals for aroimately one to two hours daily and the enclosures are not accessible to the general ublic

Skin Scraping: Technique and Interpretation uerficial sin scraes of the sloth lesions were taen by alying moderate ressure with a dulled o sterile scalel blade in the direction of hair growth on the affected area air and debris collected on the blade were then transferred to a standard microscoe slide reared with three dros of veterinary grade mineral oil at the surface lides were eamined microscoically under total magnification to visualie suerficial ectoarasitic mites scabiei can be identified based on the resence of a long unjointed edicel with a sucer on the end of the etremities endri he ideal deths for sin scraes deend on the organism in uestion endri nilica therefore secondary sin scraes were reuired econdary samles were taen in order to eel mites from dee within the hair follicles Mineral oil was alied to the affected area which was then scraed reeatedly in the direction of hair growth until the sin aeared in with the caillaries visible and ooing blood endri alton alsenegative findings can result if the dee sin scraing fails to rovide a small amount of blood due to an increased otential for mites to be left

69 within the follicle he dee sin scrae samles were eamined under total magnification for hair follicle mites emode s

Skin Impression: Technique and Interpretation econdary bacterial infection and Malasseia dermatitis revalence or absence were evaluated utiliing acetate tae rearations of suerficial samles he acetate tae rearation techniue involves the use of transarent adhesive tae to collect a samle of hair or suerficial sin debris he adhesive side of the tae was alied reeatedly to the lichenified lesions and rocessed with etne aid ifferential tain methylene blue hoshate salts for seconds he tae was rinsed for five seconds with deionied water laced on a microscoe slide and eamined under total magnification to visualie the resence or absence of bacteria and yeast Malasseia outgrowth he cytology of sin taen from sloth individuals with yotraumatic dermatitis revealed the resence of mied bacteria whereas Malasseiasis was confirmed by the finding of several round to budding yeasts nilica he bacteria in this techniue are described based on morhology and not identified to secies level

Fungal Culture: Inoculation, Incubation, and Examination ardy iagnostics ermuetM MMM ilate mlml individually wraed actiab ulture ystemM was used to isolate and identify dermatohyte organisms his culture late has two sections M and M ermatohyte fungal contaminant growing on M lates forms alaline roducts that change indicators in the medium from yellow to dee red he M roduces a blue color change in resonse to a dermatohyte organism and also eedites the sorulation of macroconidia he twosection late is euied with an antibacterial and antifungal comound that rohibits the growth of sarohytic fungi and bacteria contaminants however bacteria are not comletely suressed and some nondermatohytic fungi can cause a falseositive red M or falseositive bluegreen M color change esions were scraed with a o sterile scalel blade and transferred by rubbing the broad side of the scalel blade directly onto the agar surface of the late lucs of hair were taen from the diseased area with a hemostat and the resulting secimen was taed gently into the surface of the media ultures were stored away from light lidside down at for days he media were eamined every hours during the incubation eriod for characteristic color change and colony aearance ultures that ehibited color change on the M or M on the th day of incubation were eamined microscoically microscoe slide was reared with one dro of etne aid ifferential tain methylene blue hoshate salts cetate tae rearation was then used to collect conidia from the M segment and laced adhesive side down on the reared slide he slide was eamined for sores under total magnification ermatohytes and sarohytes were identified down to secies level with identification charts rovided by actiab in ulture ystemsM Microscoic eamination of fungal contaminants eliminated falsenegativefalseositive results based solely on color change and colony morhology

70 Results

General Overview total of sloths were evaluated for dermatitis over a twowee eriod leven sloths in cativity resented with dermal illness of which was attributed to oonotic ectoarasite infection able oonotic ectoarasites were found eclusively in the nursery and adult ehibition oulations at the wildlife sanctuary ive sloths from the wild resented with sin lesions of these lesions were attributed to electric shoc trauma three of the lesions had evidence of secondary bacterial infection and Malasseia overgrowth

Figure 1. scabiei infection A, ruritic ariegatus with mange B, resence of scabiei mite under total magnification after suerficial sin scraing hotograhs by author

71 Captive Juveniles hree variegatus juveniles from the wildlife sanctuary resented with ruritic lesions and scabiei mites were confirmed ost sin scraing igure in imressions of the three individuals were negative for secondary bacterial infection and Malasseia overgrowth ac of blue color change on M agar indicated the absence of dermatohyte growth which was confirmed with microscoic eamination of fungal conidia on the th day of incubation

Captive Exhibition Adults hree hoffmanni ehibition adults resented with lesions at the wildlife sanctuary he first case involved a male sloth estimated to be one year old with lesions resent on four limbs measuring cm on left lateral metacaral cm on the ventral asect of the metatarsal and cm the right rear carus igure monthold female resented secondarily with bisymmetrical aloecia measuring cm on the right and left metacarals he third and most severe of the cases was an aroimately oneyearold male with lesions on stifle joint elbow lateral asect of the antebrachium and both cari Measurements of lesions were not obtained in this case due to the individual’s aggressive behavior. Lesions were flaky, erythematous, and non eudative and had no callouses formed

Figure 2. esions caused by dermatohyte infection ote the multifocal scaling erythema and onychodystrohy of the digits hotograhs by author

lue color change on the M lates igure left half and red color change on the M lates igure right half indicated dermatohytosis olony to view aearance was cinnamonmauve in color and reverse colony coloration was darly

72 igmented. irosoi eamination of onidia revealed ovoidshaed maroonidia with three to si ells, whih onfirmed irosorum gyseum dermatohytosis igure . kin imressions for seondary baterial infetion of the skin and skin sraings for suerfiial and dee mites were negative for all three ehibition ases.

Figure 3. ermatohytosis in three ative . hoffmanni individuals. A, o view of fungal ontaminant growing on fungal ulture agar at day of inubation. B, irosoi eamination of dermatohyte irosorum gyseum maroonidia under total magnifiation. ote the maroonidia ovoid shae with si or fewer ell divisions. hotograhs by author.

Captive Non-Exhibition Adults wo . variegatus and one . hoffmanni were evaluated for skin illness. three yearold male . hoffmanni resented for etoarasite removal. n engorged non pathogenic tick was found on the ventral aspect of the individual’s neck near the trachea igure and a m lesion was observed at the attahment site ost removal

Figure 4. eondary baterial infetion. A, ik attahment site on ventral nek of . offmanni. B, esidual wound from tik attahment. C, onathogeni tik. hotograhs by author.

73 igure icroscopic interpretation of skin ipression taken of tick attachent site on the individual’s neck wound was consistent for pyotraumatic dermatitis due to high levels of cocci acteria aaoto ollege of eterinar edicine eratolog elephone onsultation personal counication ct kin ipression skin scraping and fungal culture results were negative for a twoandahalfearold feale variegatus and a oneandahalfearold ale variegatus that oth presented with flak skin ausation for the skin conditions in these two cases was inconclusive

Free-Living Population ive sloths fro the wild presented with severe deral lesions ungal cultures and skin scrapings fro all five individuals were negative for ite infection and deratophtosis otrauatic deratitis was diagnosed in three of the five cases fro the wild that presented with skin lesions n the first case a feale variegatus was found with nails that were anorall dark hair thinning on the left forear and skin on the carpus that was easil reoved and oist he second and third cases were hoffanni individuals that presented with urns on forears that etended to the adoen kin ipression results fro the three individuals were positive for cocci acterial infection

Figure 5. east deratitis A, entral neck seconddegree urn fro electric shock traua on an adult C. hoffmanni sloth found in the wild B, icroscopic iage of Malassezia east organis overgrowth under total agnification fro acetate tape preparation hotographs author

single hoffanni adult ale presented with ultiple areas of hair loss and seconddegree urns after accidental electric shock traua fro telephone wires igure kin ipression revealed ore than alasseia organiss per field of view igure he coination of clinical signs and high levels of organiss present on skin ipression confired east deratitis in this case aaoto ollege of eterinar edicineeratolog elephone onsultation personal counication ct

74 Atypical Findings ungal culture results for the captive nonehiition sloths had red color change on the side igure icroscopic eamination of the fungal contaminant revealed the presence of conidiophores that resemled paintrushes with conidia emanating from the top and conidiospores in fingerlike chains on phialides proecting from vesicles igure which confirmed the presence of saprophyte enicillium spp

Figure 6. aprophytic fungi growth A, ed color change on plate with asence of lue color change on plate B, icroscopic eamination of fungal contaminant ote the conidiophores that resemle paintrushes with conidia emanating from the top hotographs y author ne adult hoffmanni female from the wild presented with etremely flaky skin and no apparent lesions or ectoparasites n the th day of incuation the fungal culture had oth lue and red color change rom the top view multiple fungal colonies appeared uffpowdery with reverse dark rown colony coloration on oth and segments icroscopic eamination of fungal contaminant revealed curled hyphae consistent with richophyton mentagrophtes ut results were inconclusive due to the asence of macroconidia

Discussion

he purpose of this study was to differentiate among skin diseases of osta ican sloth populations y utiliing the dermatologic diagnostic minimum dataase isease freuencies were then compared in order to estalish which was the most prevalent ue to pseudoreplications in the sampling procedure chisuare analysis was not conducted on the data in this eperiment therefore there is no significant statistical evidence to suggest that oonotic ectoparasites are the primary cause of dermatitis in oast ican sloth populations evertheless the general trends of the trial indicate that the highest freuency of dermatitis was induced y oonotic ectoparasites

75 he presence of scaiei mites on the sloths in this study confirmed the previous report y iaaorales et al which recorded the first case of this parasite affecting oth hoffmanni and variegatus individuals in osta ica t is noteworthy that during this study two of the volunteer staff at the wildlife sanctuary developed pruritic rashes that resolved without any medical therapy hese rashes can possily e attriuted to oonosis caused y the animal species scaiei as human infestation is generally selflimiting dditional evidence of oonotic disease was found in the ehiition population of hoffmanni individuals he clinical presentations of the dermatophyte lesions and the microiological findings oserved in the present study are supported y previous reports from avier et al which descried dermatophytes in freeliving variegatus individuals of rail his is the first study to document dermatophytosis caused y the keratinophilic fungi icrosporum gypseum in captive osta ican hoffmanni populations ll of the sloths that presented with oonotic ectoparasite infection were residents at the wildlife sanctuary lthough it is not possile to confirm the origin of the infections at the wildlife sanctuary several husandry factors might have contriuted to the increased rate of oonotic parasitism oserved in its populations he nursery not only functioned as housing for infant sloths ut also as a living space for volunteer staff and uarantined animals hough uarantined animals were separated to prevent direct contact with the nursery sloth population the personnel involved in the care of the nursery wildlife were a possile source for transmission of parasites as they come in direct prolonged contact with oth the uarantined individuals and the nursery sloths throughout the day n addition inspection of the ehiition cage revealed a suspended kennel containing stagnant water and numerous piles of moldy ecrement on the cage floor loths must travel to the ground to urinate and defecate making them more at risk of fungal contraction since gypseum is considered to e a geophilic dermatophyte found in the soil owever transmission from direct contact with fur and dandruff that contain fungal particles must also e considered econdary pyotraumatic dermatitis and alasseia dermatitis from electric shock traumas were the most common skin ailments of sloths that presented from the wild he four cases with shock wounds were found on the ground after heavy storms anuel ntonio eperiences increased rates of rainfall from ay to ovemer therefore the freuency of shock traumas should e statistically analyed in future studies to correlate seasonal variations with disease patterns ommon wounds of sloths in captivity such as wireinduced inuries and fight wounds reported y ini and liviera were not oserved in this study deuate enclosure sie for the sloth populations at and the ehiition population at the wildlife sanctuary enaled each sloth to estalish its own territory therefore the risk for aggression etween individuals was decreased leven fungal cultures in this study were positive for the saprophytic fungi enicillium spp aprophytes live primarily on decaying vegetation and are commonly oserved in human and animal clinical practices hough the presence of the fungus does not generally indicate disease penicilliosis can e pathogenic and fatal in immunocompromised individuals ok et al s previously reported y iaa orales et al sloths are at a higher risk of contracting disease due to the stress

76 factors associated with captivity mmunosuppression from stress and constant eposure to materials haroring the enicillium spp fungus in sloth enclosures puts captive sloth individuals in danger of contracting nephrotoic and carcinogenic mycotoins produced y enicillium spp uring this study two variegatus individuals that were not evaluated for skin disease presented with sudden onset of upper respiratory distress neumonia was confirmed in oth cases at necropsy his is important to note as enicillium spp has een isolated from patients with pneumonia and respiratory disorders are the second most common organic disorder of sloths in captivity as reported y ini and liviera uture studies investigating the pathogenicity of enicillium spp in captive sloths should e conducted to aid wildlife rehailitators in maintaining the upper respiratory health of the species

Conclusion

ncreased iological security must e considered in order to eliminate further transmission of oonotic diseases to wildlife staff the general pulic and other captive species he wildlife sanctuary should estalish preventive measures such as volunteer dormitories and a separate isolation ward for uarantined animals agespecific clothing such as coveralls and disposale shoe covers should e worn y staff at the wildlife sanctuary and at whenever they are handling wildlife and entering enclosures in order to avoid crosscontamination in their wildlife populations he practice of responsile ecotourism y persons traveling to osta ica is also essential for the success of oth species in captivity and in the wild ractices such as touching holding and taking photographs that physically disrupt the sloth should e eliminated as this contriutes to increased stress levels disruption of the symiotic algal communities on the sloth fur and risk of oonosis

Acknowledgements: would like first to thank oth the enter for esearch and reativity and the iology epartment at ethodist niversity for making this proect financially possile econdly to am rull the director of the loth nstitute of osta ica who trusted me to work with her sloth population and to r arie urris for her continuous support and technical assistance etend my deep appreciation

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