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First case of lordosis in a wild- caught European pond turtle (Emys orbicularis)

Abstract

Even though osteological abnormalities are very rare in wild reptiles (Telemaco et al. 2013, Löwenborg & Hagman 2017), they are more frequent in captivity as a consequence of a deficient care, especially related to nutrition and UV deficiencies (Mendyk 2008). In chelonians, in some cases, it is also related to soft shell and pyramidism (Museti et al. 2014). Kyphosis and lordosis are problems related to the vertebral column, namely kyphosis when the column is extruded and lordosis when the column is intruded. There are several cases of both anomalies described in lacertids (Garin-Barrio et al. 2011), skinks (Arrivillaga & Brown 2019) and sea turtles (Drenen 1990). Nevertheless, in freshwater turtles only kyphosis is relatively common (Saumure 2001, Trembath 2009, Moldowan et al. 2015), with few documented lordosis cases (Mitchell 2014; Selman 2019). In wild Emys orbicularis several deformities have been described such as microophtalmia (Escoriza 2012), axanthism (Cavalcante & Bruni 2018), pholydosis abnormalities as accessory scutes (Cordero et al. 2008) or accessory and absent scutes (Lada & Voldireva 2018). Here, we report the first case of lordosis in a European freshwater turtle (Emys orbicularis), being the first reported case of a lordotic wild turtle in Europe. The turtle was captured on the 22th July 2011 in “Río Areta”, which is a Special Area of Conservation (ES2200013), in Navarre (Spain), in a little cattle pond (42º42’N; -1º16’E), where the majority of turtles were juveniles (Table 1), including the lordotic turtle, showing a differential habitat selection among juveniles and adults ... Valdeon, A.; Ayres, C.; Rada, V.; Baneres, A.; Martinez-Silvestre, A.

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First case of lordosis in a wild- caught European pond turtle (Emys orbicularis)

Author: Valdeon, A.; Baneres, A.; Martinez-Silvestre, A.; Ayres, C.; Rada, V.
Year: 2020
Source: https://zaguan.unizar.es/record/99224/files/texto_completo.pdf
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Key wo ds: Apa hya yassujica, In aspeci ic a iabili y, I an, m DNA
Cy b.
A icle No: e207502
Recei ed: 10. May 2020 / Accep ed: 31. July 2020
A ailable online: 03. Augus 2020 / P in ed: Decembe 2020
Hamzeh ORAIE1,2,* and Aza KHOSRAVANI3
1. Depa men o Zoology, Facul y o Science, Shah eko d Uni e si y,
Shah eko d, I an.
2. Depa men o Biodi e si y, Ins i u e o Bio echnology, Shah eko d Uni e si-
y, Shah eko d, I an.
3. I anian Pla eau He pe ology Resea ch G oup (IPHRG), Facul y o Science,
Razi Uni e si y, 6714967346 Ke manshah, I an.
*Co esponding au ho , H. O aie, E-mail: [email p o ec ed]
Fi s case o lo dosis in a wild- caugh Eu ope-
an pond u le (Emys o bicula is)
E en hough os eological abno mali ies a e e y a e in wild
ep iles (Telemaco e al. 2013, Löwenbo g & Hagman 2017),
hey a e mo e equen in cap i i y as a consequence o a de-
icien ca e, especially ela ed o nu i ion and UV de icien-
cies (Mendyk 2008). In chelonians, in some cases, i is also e-
la ed o so shell and py amidism (Muse i e al. 2014).
Kyphosis and lo dosis a e p oblems ela ed o he e e-
b al column, namely kyphosis when he column is ex uded
and lo dosis when he column is in uded. The e a e se e al
cases o bo h anomalies desc ibed in lace ids (Ga in-Ba io
e al. 2011), skinks (A i illaga & B own 2019) and sea u les
(D enen 1990). Ne e heless, in eshwa e u les only ky-
phosis is ela i ely common (Saumu e 2001, T emba h 2009,
Moldowan e al. 2015), wi h ew documen ed lo dosis cases
(Mi chell 2014; Selman 2019).
In wild Emys o bicula is se e al de o mi ies ha e been
desc ibed such as mic ooph almia (Esco iza 2012), axan h-
ism (Ca alcan e & B uni 2018), pholydosis abno mali ies as
accesso y scu es (Co de o e al. 2008) o accesso y and ab-
sen scu es (Lada & Voldi e a 2018). He e, we epo he i s
case o lo dosis in a Eu opean eshwa e u le (Emys o bicu-
la is), being he i s epo ed case o a lo do ic wild u le in
Eu ope.
The u le was cap u ed on he 22 h July 2011 in “Río A e a”, which
is a Special A ea o Conse a ion (ES2200013), in Na a e (Spain), in
a li le ca le pond (42º42’N; -1º16’E), whe e he majo i y o u les
we e ju eniles (Table 1), including he lo do ic u le, showing a di -
e en ial habi a selec ion among ju eniles and adul s (Ay es &
Co de o 2007). I was a h ee-yea -old u le (CL = 46,6 mm, weigh =
21 g) wi h algae enc us ed on he ca apace, and a conca e de o mi y
in he middle o he ca apace (Fig.1). Howe e , he e was appa en ly
no lack o mobili y.
The pond had a maximum dep h o less han 1 me e , wi h
Figu e 1. Lo do ic ju enile E.o bicula is wi h wo no mal shaped ju-
eniles.
Table 1. Measu emen s o he specimens cap u ed in he pond whe e
he lo do ic u le (in bold) was ound. Sex was classi ied as M
(male), F ( emale) o J (Ju enile wi h no ex e nal sexual cha ac e s).
Weigh was measu ed in g ams and he ca apace leng h (CL) in mil-
lime e s.
ID
Sex
Weigh (g)
CL (mm)
Neo10_04
J
12
38.49
Neo10_08
J
13
40.28
Neo10_02
J
13
40.38
Neo10_09
J
17
43.6
Neo10_05
J
17
45.16
Neo10_03
J
18
45.98
Neo09_04
J
21
46.63
Neo10_07
J
21
49.08
Neo10_06
J
22
49.49
Neo10_10
J
26
51.79
2454
J
72
73.28
2463
J
67
74.58
2450
F
141
92.26
2462
F
136
94.22
2446
F
152
97.76
2460
M
169
104.14
2465
M
207
111.7
2461
M
222
112.08
2457
F
260
112.76
2449
M
224
113.57
2455
M
234
118.79
2447
F
416
131.46
abundan wa e plan s, mac oin e eb a es and ogs. Nei he ishes
no c ay ishes we e p esen in he pond, al hough hey a e p esen in
he A e a Ri e , whe e adul u les commonly li e. In addi ion, i is
possible o conside he popula ion and hei indi iduals comple ely
wild since he loca ion was e y a om ci ies, illages o ou is ic
o ec ea ional a eas. Hence, i is e y imp obable ha he animal
could be main ained in cap i i y and eleased la e in he wild.
The u le was ca ied o CRFS Ilundáin, whe e i was adi-
og aphed, and i was eleased again he ollowing day in he pond
whe e i was cap u ed.
In adiog aphs aken in do so- en al (Fig. 2A) and la e o-
la e al (Fig. 2B) p ojec ion, he angle be ween he las ce i-
cal and i s ho acic e eb ae as well as he op o lumba
e eb ae and he op o he sac um e eb ae a e clea ly
acu e and no conca ous. Nei he usion, demi-ne aliza ion
No h-Wes e n Jou nal o Zoology 2020, ol.16 (2) - Co espondence: No es
243
Figu e 2. Radiog aphs aken in do so- en al (A) and la e o-la e al
(B) p ojec ion wi h 1cm whi e ba as scale, showing lo dosis.
no in ec ious signs (local de o mi ies o os eolysis) a e ob-
se ed in any a ec ed e eb ae (Ro schild e al. 2013).
Howe e , Figu e 2B shows ha abno mal cu a u e a ec ed
no only he e eb al column bu also he plas al bones.
Ven al bones had a ligh lo do ic cu a u e bu wi h a less
acu e angle han he one obse ed in e eb al spine. Despi e
a common belie ha lo dosis could be a isk ac o o back
pain, beha iou al e idences in his u le e ealed ha he e
was no back pain symp oms du ing locomo ion. Rega ding
he de mal scales, nei he duplica ion o usion, no e e-
b al o cos al scu es we e obse ed.
In ep iles, spinal mal o ma ions o spinal e a ology can
be due o inco ec condi ions du ing he incuba ion o eggs,
i.e. excessi ely low o high empe a u es and low ela i e
humidi y; hough no ably, oxics and pollu an s (e.g. insec i-
cides) migh also be esponsible o mal o ma ions obse ed
in wild ep iles (Bellai s 1981). Se e al hypo heses ha e been
p oposed o explain he o igin o shell abno mali ies in che-
lonians. Mos o hem a e ela ed o p oblems du ing em-
b yonic o ea ly ju enile de elopmen (Ro hschild e al.
2013, Ca acappa e al. 2016, Nagle e al. 2018, Zimm e al.
2018, Lange e al. 2020). The e is e idence ha polychlo in-
a ed biphenyls (PCBs), a azine and glyphosa e ha e a nega-
i e e ec on bone de elopmen du ing incuba ion on
eshwa e u les (Adams e al. 2016; Mendoçal e al. 2016).
Addi ional s udies ha e also shown ha inb eeding o ep-
ile popula ions wi h low gene ic di e si y can cause mal-
o ma ions (Madsen e al. 1992; Olsson e al. 1996). In cap i e
u les, spinal mal o ma ions can also be caused by me abol-
ic bone diseases (F ye 1991, Muse i e al. 2014).
In u les, he ho acic and lumba e eb ae canno
mo e in he join due o he ac ha hey me ge o ming
acon ex column in he ea ly s ages o de elopmen
(P i cha d 2008). In ou case, he shell conca i y and he ab-
sence o up igh pos u e could ha e been de eloped since
he i s de elopmen s ages o he u le. Mine al de icien-
cies we e disca ded by adiog aphic analyses, and he u le
seemed o ha e g own no mally as well as he o he u les
ound in he pond, so ha nu i ional p oblems should no
be he cause o he lo dosis. En i onmen al pollu an s a e al-
so a highly unlikely cause, as indica ed by he absence o
o he a ec ed animals such as u les o o he aqua ic o gan-
isms a ound he a ea. As he e was no shield usion, he
cause o he abno mali y could be congeni al.
Acknowledgemen s. Eu opean pond u les we e cap u ed unde
licence o he Na a e Regional Go e nmen Numbe 581/2011. The
CRFS Ilundáin, depending on he Go e nmen o Na a e and
managed by he public en e p ise ‘Ges ión Ambien al de Na a a’,
assumed he cos s o he adiog aphs.
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A icle No: e207503
Recei ed: 23. June 2020 / Accep ed: 19. Augus 2020
A ailable online: 23. Augus 2020 / P in ed: Decembe 2020
Ai o VALDEÓN1,2,*, Césa AYRES3, Vi ginia RADA4,
Al onso BAÑERES5 and Albe MARTÍNEZ-SILVESTRE6
1. G upo de in es igación Clima, Agua, Cambio Global y Sis emas Na u ales-
IUCA-Depa amen o de Geog a ía-Uni e sidad de Za agoza. C/Ped o Ce -
buna, 12. 50009 Za agoza. Spain.
2. Dp o. He pe ología. Sociedad de Ciencias A anzadi. Zo oagagaina 11. 20014
Donos ia-San Sebas ián. Spain
3. AHE-Galicia. Ba celona, 86, 6C. 36211, Vigo (Pon e ed a). Spain.
4. Ta alla, Spain, E-mail: [email p o ec ed]
5. BASATI Ve e ina y N.G.O. Na a a egion, Spain, E-mail: [email p o ec ed]
6. Ca alonian Rep ile and Amphibian Rehabili a ion Cen e (CRARC) 08783,
Masque a, Spain.
* Co espponding au ho , A. Valdeón, E-mail: [email p o ec ed]
Unsuccess ul p eda ion a emp o
Lep odac ylus syphax (Anu a:
Lep odac ylidae) on Acan hoscu ia sp.
(A aneae: The aphosidae)
Anu ans a e conside ed gene alis and oppo unis ic p eda-
o s, hei gape and head size being he main cons ain s o
he maximum p ey size hey can seize and inges (Duellman
& T ueb 1994, Ce on e al. 2018, Ma ques-Pin o e al. 2019).
F ogs a e impo an elemen s in he complex ene gy ne -
wo ks a opical egions, since hey eed on a wide a ie y
o ood i ems, such as insec s and a h opods, and a e
p eyed upon by a a ie y o animals such as snakes and
small and medium mammals (Ma ques-Pin o e al. 2019,
Zipkin e al. 2020).
Spide s a e commonly ea en by anu ans (Solé e al. 2005,
Sugai e al. 2012, Came a e al. 2014), mainly because hey
co-occu in en i onmen s used by ogs (Schalk & Sezano
2014). Con e sely, spide s o he amilies Psau idae, C e-
nidae, and The aphosidae o en eed on amphibians (Menin
e al. 2005, Meneses e al. 2020). Howe e , p eda ion e en s
o ogs consuming a an ulas a e a e in na u e, since hese
gene ally la ge spide s p esen a po en ial dange o hei
p eda o s by wounding hem wi h hei se ae and en en-
oma ing hem using he chelice ae (Rosa e al. 2012, Be ani
& Guadanucci 2013, Bogan & Eppehime 2017, Valencia-
Valdez e al. 2019).
He e we p esen a p eda ion a emp on an Acan ho-
scu ia sp. (The aphosidae) by a Lep odac ylus syphax Boke -
mann 1969. The e en was obse ed on Oc obe 15, 2018,
du ing nigh ieldwo k o a emnan o na i e ege a ion,
nea he Roncado Ecological S a ion, B asília, Dis i o Fed-
e al, B azil (15°56'S, 47°48 'W, 1095 m a.s.l.). The og was in
an open ocky a ea (sensu Ribei o & Wal e 2008), holding
he spide in i s mou h when we loca ed hem. One o he
spide 's chelice a was pene a ing he lowe lip o he og
(Fig. 1). A e 5 min he og eleased he spide , bu i was
al eady dead. The og le he a ea, no showing any ob i-
ous sign o dis ess. The obse a ion was du ing he ainy
season o he Ce ado, a a ime ha he males o bo h spe-
cies a e in hei ep oduc i e pe iods and ac i ely sea ching
o emales (Sil a & Gia e a 2009, Mo a 2014), which could
inc ease he chance o he wo species encoun e ing.
Figu e 1. An adul male Lep odac ylus syphax a emp ing p eda ion on
an adul male Acan hoscu ia sp. No e ha a leas one o he spi-
de ’s chelice ae is pe o a ing he og’s uppe lip.
Lep odac ylus ogs use he “si and wai ” o aging s a e-
gy (Sugai e al. 2012, Ganci e al. 2018, Solé e al. 2019) ha is
ypical o species wi h a gene alis die , la gely based on in-
e eb a es such as Bla a ia, Coleop e a, Dip e a, Hemip-
e a, Hymenop e a, O hop e a, and A aneae (including
The aphosidae spide s; see Solé e al. 2005, Sugai e al. 2012,
Teles e al. 2018). Lep odac ylus syphax is a mid-sized og be-
longing o he L. uscus g oup (Sá e al. 2014), widely dis ib-
u ed in B azil (especially in he Ce ado, Caa inga and Chaco
biomes), wi h eco ds in Boli ia and Pa aguay (And ade e
al. 2011). I is commonly associa ed wi h open a eas wi h
ocky ou c ops, using ock ca i ies and e mi e bu ows
close o c eeks as e ea si es (Heye e al. 2010).
Acan hoscu ia is a The aphosid genus o la ge Mygalo-
mo ph spide s, wi h species in he Ce ado eaching up o 80
mm in body leng h (cephalo ho ax + abdomen; Mo a 2014).
These spide s can be iden i ied by hei dis inc s idula o y
se ae on he e ola e al ace o he palpal ochan e and by
he p esence o one ibial apophysis on he male’s leg I (Pé-
ez-Miles e al. 1996). Se en species we e eco ded o he