Basic and Applied Herpetology 31 (2017) 69-75

Helminth parasitizing cyreni (Müller et Hellmich, 1937) from Gredos Mountains, Iberian Peninsula

Vicente Roca*

Departament de Zoologia, Facultat de Ciències Biològiques, Universitat de València. C/Dr. Moliner, 50, 46100 Burjassot (Spain).

*Correspondence: Phone: +34 963544606, Fax: +34 963543049, E-mail: [email protected]

Received: 19 September 2017; returned for review: 16 October 2017; accepted 3 November 2017.

A survey of the helminth communities of a population of (MÜller et Hellmich, 1937), a small endemic to Sistema Central (Iberian Peninsula), was conducted to determine the prevalence, abundance and diversity of parasites of these . Four species of hel- minths were found, one trematode, Plagiorchis molini Lent et Freitas, 1940, one cestode, Nemato- taenia tarentolae LÓpez-Neyra, 1944, and two nematodes, Skrjabinelazia sp. and Spauligodon car- bonelli Roca García-Adell, 1988. Helminth infracommunities of I. cireny showed very low values of abundance and species richness and diversity, being similar to other European . The para- sites found seem to have no influence on the conservation status of the host species in its natural .

Key words: conservation; helminths; Iberian Peninsula; lizards.

Iberolacerta cyreni (Müller et Hellmich, These lizards are typically linked to 1937) is an endemic lacertid lizard from high mountain rocks. They are generalist Gredos and Guadarrama Mountains in feeders eating many and other ar- Central-West and Central Iberian Peninsu- thropods. They use both sit-and-wait, and la (Carretero et al., 2014). Morphological active foraging strategies (Martín Sal- characteristics, structure of chromosomes, vador, 1993). and electrophoretic data (Arribas, 1996), Iberolacerta cyreni is considered as a as well as recent data from mitochondrial threatened species (Pérez-Mellado et al., and nuclear DNA confirm the specific sta- 2009). The destruction of its high mountain tus of the lizard populations from this geo- , and the vulnerable nature of cer- graphical area (Martín, 2009). It seems tain populations derived from the isola- that the origin of this lizard (prior to the tion regime among each other, are the Pleistocene glacial oscillation) was fa- main threats (Martín, 2009). voured by the complex orography of these Concerning parasites, haemogregarines mountains, acting as speciation cores and have been found infecting erythrocytes refuge of the species (Crochet et al., 2004). from lizard populations in Guadarrama

DOI: http://dx.doi.org/10.11160/bah.89 Supplementary material available online ROCA

(Amo et al., 2004; Jovani et al., 2004), but the conservation of the host species. there is no data on parasitic helminths of Materials and Methods any population of this species. As lizards living in high-altitude habi- Study Area tats, we would expect a poor helminth The area of the study, Sierra de Gredos community for I. cyreni. However, there (40° 15’ N, 5° 13’ O), are a group of moun- are not conclusive results regarding the tains belonging to the Sistema Central, influence of altitude in relation to the para- located at the West-Centre of the Iberian site infection in reptiles. For instance, Ma- Peninsula. It consists of granitic rocks and ia et al. (2016) found a negative correlation a variety of vegetation cover, changing between prevalence and altitude in according to the altitude, with a typical Pristurus rupestris (Gekkonidae) from Oman, high mountain climate (Delgado-Sánchez, Arabia. Low richness of the helminth com- 1996). munity has also been recorded from a population of Mabuya dorsivittata Host samples (Scincidae) in Itatiaia, a high-altitude habi- Samples correspond to 23 specimens of tat in Rio de Janeiro State (Rocha et al., I. cyreni stored in the collection of the Labora- 2003). Nevertheless, populations of Scelo- tory of Parasitology of the Depart- porus occidentalis (Iguanidae) from San Gabri- ment of Zoology, University of Valencia el Mountains (montane, ca. 1584 m eleva- (Spain) (see collection numbers in the Sup- tion, Los Angeles, California) showed plementary Material, Section S1). The greater prevalence of infection of gastroin- specimens were caught in the Sierra de testinal nematodes than populations from Gredos in the years 1985 (four hosts), 1986 Puente Hills (lowland, ca. 150 m elevation) (six hosts), 1987 (six hosts) and 1988 (seven (Goldberg et al., 1998). Additionally, it hosts), and the samples were sent to our seems that digestive parasite nematodes laboratory, following the necropsy of dead do not play a major role in setting altitudi- hosts. The digestive tract, heart, lungs, and nal distribution limits for Liolaemus liz- liver were removed, opened, and placed in ards in the central Chilean cordillera Ringer solution for examination. (Carothers Jaksic, 2001). Analysis of parasites Hence, the objective of this study was to investigate for the first time the hel- The parasites were preserved in 70% minth fauna of the host species I. cyreni. alcohol and are deposited in the collection More specifically, this study aimed: (1) to of the Laboratory of Animal Parasitology, know what kind of helminths parasitize Department of Zoology of the University this lizard; (2) to determine the patterns of of Valencia (Spain) (see collection numbers helminth community richness and diversi- in the Supplementary Material, Section ty; (3) to compare these patterns with S2). Now they have been studied accord- those already described for other allied ing to standard techniques (Hornero, lizards; (4) to take into account the para- 1991). Parasites were identified, when pos- sites among the issues to be considered for sible, to the species level and the number

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Table 1: Parameters Helminth species Prevalence Intensity of Abundance of infection of hel- (%) infection (range) (range) minths in Iberolacerta Trematoda cyreni. Plagiorchis molini 9 1.5 ± 0.7 (1 – 2) 0.1 ± 0.5 (0 – 2)

Cestoda

Nematotaenia tarentolae 13 1 ± 0 (1 – 1) 0.1 ± 0.3 (0 – 1)

Nematoda

Skrjabinelazia sp. 9 1 ± 0 (1 – 1) 0.1 ± 0.3 (0 – 1)

Spauligodon carbonelli 52 3.3 ± 6.9 (1 – 25) 1.7 ± 5.1 (0 – 25) and location of individual parasites of are given in Table 1. The average number each species per host were recorded. Di- of parasite species per lizard was 0.8 ± 0.6 versity and infection parameters described (0 – 2) and the maximum number of para- in Bush et al. (1997) were used to define the site taxa found in any individual lizard ecology of the parasites. Thus, prevalence never exceeded two. The helminths en- is defined as the number of hosts parasi- countered had a global prevalence (all tized divided by the total number of hosts taxa) of 74% (17/23). While the mean inten- sampled; mean intensity, as the total num- sity of infection (all taxa) was 2.8 ± 6.2 (1 – ber of helminths divided by the number of 27), the mean abundance (all taxa) was 2.1 infected hosts; mean abundance, as the ± 5.5 (0 – 27). The value of Brillouin’s index total number of worms divided by the to- diversity was 0.03 ± 0.08 (0 – 0.35). Propor- tal number of hosts sampled. Brillouin’s tion of hosts with 0 or 1 helminth species index was used for calculating diversity, was 91%. according to Magurran (2004). Discussion Results The trematode P. molini, which is mainly The host I. cyreni was infected with four characterized by the extension of the vitel- species of helminths (one trematode, one laria (Roca Navarro, 1983), was previ- cestode and two nematodes, see Table 1). ously found in Iberian Peninsula parasitiz- All the helminths were found in the diges- ing different species of lizards, such as tive tract; the nematode Skrjabinelazia sp. Podarcis muralis, Lacerta schreiberi or Zootoca in the stomach, the trematode Plagiorchis vivipara, all of them living in high mountains molini and the cestode Nematotaenia taren- and linked to humid environments tolae in the small intestine and the nematode (García-Adell Roca, 1988; Roca Fer- Spauligodon carbonelli (but see discussion) in ragut, 1989; Sanchis et al., 2000), which are the large intestine. Of the species found, S. adequate for the development of the life carbonelli was the most common, with 52% of cycle of this parasite. So, it is not surpris- all hosts infected. Detailed infection pa- ing the finding of this trematode in the rameters for individual species of parasite lizard I. cireny, as this host shares the ecologi-

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Geographical Brillouin’s Table 2: Compari- Host species Reference distribution index son of values of Iberian Peninsula Brillouin’s index of diversity of several Iberolacerta cyreni Gredos 0.03 Present study continental Europe- an lacertid lizards. Podarcis bocagei NW Portugal 0 GaldÓn et al., 2006

Podarcis carbonelli NW Portugal 0.001 GaldÓn et al., 2006

Zootoca vivipara Pyrenees 0.003 Sanchis et al., 2000

Caucasian

Darevskia rudis NE Anatolia 0.01 Roca et al., 2016a

Darevskia parvula NE Anatolia 0.01 Roca et al., 2016b

Other Darevskia spp. NE Anatolia 0 Roca et al., 2016b cal characteristics with those other hosts morph” with reduced morphological traits quoted (Martín, 2009). resembling more closely the males of the The cestode N. tarentolae is a species with sister Skrjabinodon than Spauligo- a wider range of distribution, which has don maj or males. Spauligodon carbonelli is one been previously found in several lizard of the species with “major” and “minor” hosts in different ecological conditions, forms (Jorge et al., 2014). It usually infects including habitats of high mountains lacertid lizards sympatric with I. cyreni, (García-Adell Roca, 1988; Roca Fer- such as Podarcis hispanica, P. bocagei and P. ragut, 1989). carbonelli (GaldÓn et al., 2006). So, it is prob- As only females were found, the speci- able that males found here belong to the mens of Sk rjabinelazia were not exactly species S. carbonelli. identified to the species level. They proba- The most common helminth in the bly belong to S. hoffmanni, a species usually community of I. cyreni is the pharyngodonid found parasitizing other lizards in this nematode S. carbonelli, which should be con- area (Roca et al., 1990). sidered as a rock lizard specialist (Roca The other nematode found was firstly Hornero, 1994), since it has been recorded identified as Skrjabinodon medinae, accord- for this group of lizards (GaldÓn et al., ing to the morphological characteristics of 2006). The remaining helminth species males and females (Hornero Roca, have been recorded from several other 1992). Nevertheless, recently Jorge et al. lizard genera, so they appear to be gener- (2014) suggested that in parasitic nema- alists. todes of the genus Spauligodon there is a Most helminth species found in I. cyreni “major male form”, which exhibits the tra- occurred at low prevalence and intensity. ditional male morphological traits report- Only S. carbonelli can be considered as a core ed for this taxon, coexisting with a “minor species (Roca Hornero, 1992); N. taren-

72 PARASITES OF IBEROLACERTA CYRENI tolae is a secondary species and S. hoffmanni (Roca et al., 1999; Roca, 2002) have evi- and P. molini are satellite species at the com- denced that these hosts coexist in equilibri- ponent community level. um with their parasitic helminths (Roca The low average number of parasite Carbonell, 1993), and that these parasites species per lizard, as well as the low val- are not a potential cause of a decline or ues of Brillouin’s index, emphasizes the eventual extinction of any population of very low diversity of the helminth in- those lizards (Roca et al., 1999). The pattern fracommunities of I. cyrreni. This agrees of the helminth community of I. cyreni with the typical pattern of helminth infec- (helminth species and low parameters of tion in many lizards (Roca et al., 2016a). infection) suggest that, as in the cases Nevertheless, the helminth community of mentioned above, parasites should not be I. cyreni seems less depauperate than helminth a problem for the survival of the host spe- communities found in other continental cies in its current habitats and environ- carnivorous lizards in Iberian Peninsula, mental conditions. or in the Caucasus (Table 2). Probably Bioethical Considerations some ecological factors (i.e. high number of interactions with other species) The author has followed the corre- occurring in the habitats occupied by I. sponding legislation on animal care. cyreni, allow major opportunities for parasite References recruitment. Rocha et al. (2003) and Maia et al. (2016) Amo, L.; LÓpez, P. Martín, J. (2004). found a negative correlation between par- Prevalence and intensity of asite infection and altitude. Rocha et al. Haemogregarinid blood parasites in a (2003) suggested that depauperate hel- population of the , minth communities in M. dorsivittata may Lacerta monticola. Parasitology Research be a result of the relative isolation 94: 290-293. (insularity effect) of the study area. Our Arribas, O. (1996). Taxonomic revision of results, not only corroborate a possible the Iberian ʹArchaeolacertaeʹ 1: a new negative correlation between parasite in- interpretation of the geographical vari- fection and altitude, but also suggest that ation of ʹLacertaʹ monticola Boulenger, the habitats occupied by I. cyreni in Sierra 1905 and ʹLacertaʹ cyreni MÜller de Gredos are also useful for many other Hellmich, 1937 (: Sauria: Lac- species which can act as intermediate ertidae). Herpetozoa 9: 31-56. hosts in the life cycle of its parasites, and Bush, A.O.; Laferty, K.D.; Loft, J.M. also let the development of the parasites Shostak, A.W. (1997). Parasitology with direct life cycles. meets ecology on its own terms: Mar- Although parasites can affect the health golis et al. revisited. Journal of Parasito- of the host, thereby undermining the bal- logy 83: 575–583. ance of the host-parasite relationship Carothers, J.H. Jaksic, F.M. (2001). Para- (Marcogliese, 2004), studies on the con- site loads and altitudinal distribution of servation of various species of lizards Liolaemus lizards in the central Chilean

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