Parasites in Spanish Populations Of

Basic and Applied Herpetology 33 (2019) 53-67

Parasites in Spanish populations of Psammodromus algirus (Algerian sand lizard, lagartija colilarga) and Psam- modromus occidentalis (Western sand lizard, lagarto de arena occidental) (Squamata, Lacertidae, Gallotiinae)

Stephen D. Busack1,2,*, Charles R. Bursey3, Lance A. Durden4

1 Director Emeritus, Research and Collections, North Carolina Museum of Natural Sciences, Raleigh, North Carolina, U.S.A. 2 Research Associate, Section of Amphibians and Reptiles, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, U.S.A. 3 Department of Biology, Pennsylvania State University, Sharon, Pennsylvania, U.S.A. 4 Department of Biology, Georgia Southern University, 4324 Old Register Road, Statesboro, Georgia, U.S.A.

*Correspondence: E-mail: [email protected]

Received: 05 June 2019; returned for review: 02 July 2019; accepted 04 July 2019.

Psammodromus algirus from Madrid, Ávila, and Cádiz provinces, Spain, and P. occidentalis from Cádiz province were examined for the presence of external and internal parasites. Among those parasites represented were: Ixodes inopinatus (Arthropoda, Arachnida, Acari, Ixodidae); Haemaphysa- lis punctata (Arthropoda, Arachnida, Acari, Ixodidae); Skrjabinelazia cf. taurica (Nematoda, Secernentea, Ascaridida, Seuratidae); Spauligodon carbonelli (Nematoda: Secernentea, Oxyurida, Pharyngo- donidae); Parapharyngodon psammodromi (Nematoda, Secernentea, Oxyurida, Pharyngodoni- dae); Abbreviata abbreviata (Nematoda, Secernentea, Physalopteroidea, Physalopteridae); Meso- cestoides sp. (Platyhelminthes, Cestoda, Cyclophyllidea, Mesocestoididae); and Oochoristica cf. tuberculata (Platyhelminthes, Cestoda, Cyclophyllidea, Davaineidae). Details regarding localities from which host species were collected, number of parasites and sites of attachment, and estimates of prevalence and intensities of infection are presented. Nematode diversity, along with parasite prevalence, parasitaemia, and relationship to elevation are also discussed. A table of Psammodromus parasites in Spain is also included.

Key words: cestodes; Iberolacerta; nematodes; Psammodromus; Spain; ticks.

Distributional data regarding para- ples of museum specimens from well- sites, when coupled with habitat infor- referenced localities can be difficult to lo- mation regarding vertebrate hosts, can be cate and access. instructive with respect to ecological con- Although nematode and cestode para- ditions experienced by both parasites and sites of Spanish Psammodromus algirus their hosts. External parasites may not be and P. occidentalis have been subjects of retained or identified, and internal para- previous studies (Roca et al., 1986; Roca sites are rarely discovered, during field Lluch, 1986, 1988; Busack Bursey, surveys of living individuals; large sam- 2016), and known parasites were summa-

DOI: http://dx.doi.org/10.11160/bah.167 Supplementary material available online BUSACK ET AL.

Figure 1: Psammodromus algirus, Cádiz, vicinity of Facinas (note tick scar, axil area), (left); P. occidentalis (CM 54808), Cádiz; Facinas, 7.3 km (airline) NE (N36.14809 W5.62074, 174m), (right). rized in Salvador (2014), detailed distri- of P. algirus and P. occidentalis housed at butional data, useful to parasitologists, Carnegie Museum of Natural History herpetologists, ecologists, and conserva- (CM), Pittsburgh, PA, and the U.S. Nation- tionists remain difficult to locate and ac- al Museum of Natural History (USNM), cess. Our limited data from Ávila Prov- Washington D.C., parasites were removed ince, considered along with recent data and identified. Internal parasites are de- for Iberolacerta cyreni provided by Roca posited in the H. W. Manter Laboratory of (2017a), provide an enhanced picture of Parasitology (HWML), Lincoln, Nebraska, nematode infection in lacertid lizards U.S.A., and ticks are deposited at the U.S. from the Sierra de Gredos. Previously National Tick Collection (USNM ENT), unpublished data regarding identification located and curated at Georgia Southern and distribution of internal and external University, Statesboro, GA, U.S.A. parasites from three populations of Psam- Data analysis modromus algirus, and one population of P. Snout-vent length (SVL in mm) of liz- occidentalis, (Fig. 1), based on museum speci- ard specimens were recorded after several mens from Cádiz Province, Spain, are years of storage in 70% ethanol. Helminth presented below; prevalence, intensity of identification was facilitated by utilizing infection or infestation, and abundance descriptions and illustrations in Anderson data are considered in the discussion. A et al. (2009) for genera, and Bursey Gold- summary of parasites known to be hosted berg (2015), Lhermitte et al. (2008), and by lizards of the genus Psammodromus Morgan (1945) for species; cestode identi- from the Iberian Peninsula is provided in fication was confirmed following Rausch Supplementary Material S1. (1994), McAllister Bursey (2017), and Materials and Methods McAllister et al. (2013); Estrada-PeÑa et al. (2014, 2017) were consulted for tick identi- Specimens examined fication. Identification guides generally While examining historical (Cádiz, 1969 illustrate only male Skrjabinelazia and we -1971, Madrid and Ávila, 1975) collections found only females in our samples; those

54 PARASITES OF SPANISH PSAMMODROMUS females, however, most closely resembled (CM 60959, SVL 57.1), not otherwise para- illustrations of S. taurica. In Parapharyngo- sitized during late August, 1975, was don, females in our samples most closely re- found heavily infected with Mesocestoides sembled illustrations of P. psammodromi. sp. (Platyhelminthes, Cestoda, Cyclophyl- To ensure accuracy of species identifi- lidea, Mesocestoididae; HWML 96281). cation from scar tissue resulting from pre- In the vicinity of Nogal del Barranco vious tick infestations in specimens no (N40.23145, W5.15995, elev. ~1102 m, Ávi- longer carrying representative adults, we la Province), also during late August, 1975, compared previously-infested tissue with 10 of 12 P. algirus (CM 60953-60956, tissue from specimens continuing to carry USNM 199215 & 199217-199219) bore scar larval Ixodes inopinatus (Arthropoda, Ac- tissue consistent with prior tick infesta- ari, Ixodidae) at the same locality (see Es- tion, and two (USNM 199216 & 199221; trada-PeÑa et al., 2014 for developmental USNM ENT 00862246 & 00862247) carried data regarding Ixodes inopinatus). H. punctata larvae, in axillary regions. Three Original locality data were transcribed of these 10 (USNM 199216-199218) indi- from field notes (SDB, unpubl.) and pre- viduals also carried five, three, and two sented as modern locality data using Trip Skrjabinelazia cf. taurica (Secernentea, Asca- and Waypoint Manager v 5 and the City Navi- ridida, Seuratidae; HWML 96279) in the gator Europe NT 2014.4 update in Map posterior stomach and/or anterior small Source version 6.16.3 (https:// intestine, and one (USNM 199219), in ad- www.garmin.com/en-US/maps/outdoor); dition to several axillary H. punctata scars, airline distances and elevations are from was host to one male and 8 female Spauli- Google Earth™, Spearmanʹs Rank Correla- godon carbonelli (HWML 96280; Secernentea, tion (Rho) was calculated using the on-line Oxyurida, Pharyngodonidae) in her anteri- program provided by Social Science Statis- or small intestine. Two P. algirus, appar- tics (https://www.socscistatistics.com/ ently not parasitized by ticks (CM 60957, tests/spearman/default2.aspx). USNM 199221), carried one and two S. cf. taurica in the anterior small intestine or pos- Results terior stomach. From Manzanares el Real (Madrid Haemaphysalis punctata prevalence at the Province; ~N40.73728 W3.85772, elev. ~982 Nogal del Barranco locality was 83% (95% m), one male Psammodromus algirus confidence limits [CL]: 59% - 100%; see (USNM 199213), of two sampled during also Bush et al, 1997). For internal parasites late August, carried scar tissue and one the nematode S. cf. taurica was found to larva (left axil; USNM ENT 00862246) indi- be most prevalent (42%; CL: 9% - 74%), cating prior and current tick infestation with an estimated mean intensity of 2.6 ± (Haemaphysalis punctata; Arachnida, Acari, 0.8 for the number of parasites expected Ixodidae). per individual; the prevalence of S. car- Close to Guisando (Ávila Province; 2.7 bonelli was 8% (CL: 0% - 27%), and its esti- km NE [airline, 244.9° true] ~ N40.23294 mated mean intensity was 0.8 ± 0.8 at this W5.11034, elev. 824 m), one male P. algirus locality. Nematode diversity (Brillouinʹs

55 BUSACK ET AL.

Table 1: Estimates for nematode intensities of infection arranged by elevation within Spain.

Host species Elevation (m) Helminth species Intensity Authority

Iberolacerta cyreni 1780 Spauligodon carbonelli 3.3 ± 6.9 Roca (2017a)

Skrjabinelazia cf. hoﬀmanni 1.0 ± 0 Roca (2017a)

Psammodromus algirus ~1102 Spauligodon carbonelli 0.8 ± 0.8 This study

Skrjabinelazia cf. taurica 2.6 ± 0.8 This study

80-440 Skrjabinelazia cf. taurica 4.2 ± 1.3 This study

Abbreviata abbreviata 1.1 ± 0.2 This study

Index, H = 0.369; Poole, 1974) at this local- 1.a. La Algaida (N36.85791 W6.30826, elev. 2 ity, based on 22 worms supported by six of m). 12 P. algirus, is apparently the highest diversi- Three male P. algirus (CM 54874 [no ty yet reported from the Iberian Peninsula letter], SVL 67.1 [June]; CM 54874I, SVL (ﬁde Roca 2017a: Table 2). 49.5 [June]; and CM 53403, SVL 61.2 Of 198 P. algirus examined from locali- [August]) each carried one P. psammo- ties within Cádiz Province (Fig. 2a, cir- dromi (HWML 64802 & 94159) involving cles), 85 (43%) were female and 113 (57%) stomach, small intestine, or body wall as were male, suggesting that the sex ratio in infection sites (see also Busack Bursey, the population may be narrowly skewed 2016). toward males (p = 0.05); some specimens Two female P. algirus (CM 53247, SVL at these localities were unsuitable for in- 54.1 [May] and CM 54677G, SVL 63.6 clusion in our analysis, however, and the [April]) were each parasitized by a single precise degree of parasite representation P. psammodromi (HWML 64802 & 94159). across the province cannot be determined In one specimen, the nematode was using these data. Six P. occidentalis (Fig. attached to the body wall, in the other it 2a, triangles) were also examined. was found in the lower portion of the large Number and precise geographical lo- intestine. calities (Fig. 2b) for lizard hosts, their SVL, 2. Skrjabinelazia cf. taurica (Nematoda, sex, and month of discovery; the number, Ascaridida, Secernentea, Seuratidae; lot sex, and developmental stage of individu- catalogued as HWML 64803 & 94157). al parasites encountered; and the hostʹs 2.a. La Barca de la Florida, ~3.8 km E. site of infection/infestation are provided on CA-503 (N36.62981 W5.86369, elev. 80 below. Museum catalogue numbers for m). hosts and parasites are also provided: Four male P. algirus (CM 53139, SVL 1. Parapharyngodon psammodromi 59.5 [April]; CM 51934, SVL 61.6 (Nematoda, Secernentea, Oxyurida, [September]; CM 53306, SVL 63.5 [June]; Pharyngodonidae). and CM 51977, SVL 68.4 [September]) car-

56 PARASITES OF SPANISH PSAMMODROMUS

Figure 2: Psammodromus specimens examined (a)  Psammodromus algirus,  P. occidentalis; (b)  Skrjabinelazia cf. taurica,  Parapharyngodon psammodromi,  Abbreviata abbreviata,  Oochoristica cf. tuberculata,  Ixodes inopinatus (P. algirus), and  Ixodes inopinatus (P. occidentalis). Agricultural areas indicated are defined in Mapas provinciales de suelos. Cádiz (Instituto Nacional de investigaciones AgronÓmicas, 1971). ried one, 10, 12, and two female S. cf. tau- (73° true, N36.5768 W5.5314, elev. 594 m) rica, respectively, within the rear intestinal during August, carried two female S. cf. tract and bladder. taurica (HWML 94157), one within the poste- Four female P. algirus (CM 51333, SVL rior large intestine, the other within the 55.9 [August]; CM 51332, SVL 56.0 anterior stomach. [August]; CM 53140, SVL 57.8 [April]; and 3. Abbreviata abbreviata (Nematoda, Secernen- CM 51089, SVL 59.0 [July]) carried five, tea, Physalopteroidea, Physalopteridae; lot catalo- one, one, and six female S. cf. taurica re- gued as HWML 64801 or 94158). spectively within the caecum, small intes- 3.a. La Algaida. tine, or attached to the ventral body wall. During June two male P. algirus (CM 2.b. Montes Propios de Jerez, various 53291, SVL 54.2; CM 53353, SVL 65.9) were sites along logging roads in the vicinity of found hosting A. abbreviata; one male par- Galis (N36.55958 W5.60101, elev. 440 m). asite was attached to the ventral ab- One male P. algirus (CM 54687F, SVL dominal wall of CM 53291, and a female 70.2) collected ~9.7 km WNW of Galis parasite was found in testicular tissue of (277° true, N36.5706 W5.7080, elev. 244 m) CM 53353. During August another male during May, carried two female S. cf. tau- (CM 53426D, SVL 64.8) was host to an im- rica (HWML 94157) within its intestinal mature A. abbreviata found unattached within tract, and one female P. algirus (CM 55442, the anterior abdomen, and during October SVL 72.4) collected ~6.4 km ENE of Galis a female P. algirus (CM 55662, SVL 59.8) 57 BUSACK ET AL. was discovered with a female A. abbrevi- dactylus erythrurus at La Algaida have been ata attached to the external wall of her stom- deposited in the U.S. National Helmintho- ach. logical Collection [USNM 74378], and with 3.b. La Barca de la Florida. the Laboratoire de Zoologie (Vers), Muséum During March, two female A. abbreviata National dʹHistoire Naturelle, Paris [MNHN were found on the anterior stomach wall of a 153 Hb-164 Hb, Bocal C91] (Busack Jaksić, 56.4 mm male P. algirus (CM 53092); during 1982). April, two male P. algirus (CM 53139, SVL 5. Ixodes inopinatus (Arachnida, Acari, 59.5; CM 53045D, SVL 61.0) hosted one and Ixodidae). two female A. abbreviata, respectively, in 5.a. Alcalá de los Gazules, 8.7 km W on the abdominal cavity. CM 53045D also car- ʺoldʺ C-440 (N36.46835 W5.84245, 62 m). ried one unidentified parasite (HWML A female P. algirus (CM 51084, SVL 62) 64801). During July a female P. algirus (CM collected in July was parasitized in the right 51106, SVL 59) carried a female A. abbrevi- axil by one nymph and one larva (USNM ata in its small intestine, and in September one ENT 00862190). female P. algirus (CM 51935, SVL 60.1) was 5.b. Facinas, 7.3 km (airline) NE discovered with an immature A. abbreviata (N36.14809 W5.62074, 174 m). in its stomach. One female P. occidentalis (CM 54808, 3.c. Benamahoma, 1.6 km N on A-372 SVL 41.7) hosted a nymph (USNM ENT (N36.7558 W5.4548, 636 m) or Ubrique, 8.4 00862245) in the right axil during May. km SE (airline, 208° true; N36.6114 W5.4911, 5.c. Los Barrios (benchmark), ca. 8.2 km 579 m). SW (230° true), (N36.13894 W5.56441, 259 Assignment to the original locality for m). each of these four P. algirus (one male, three A male P. algirus (CM 53197, SVL 43.4) females; CM 55456 - CM 55459) collected in was found with two larvae attached in the September is not possible, and the following right axil, and one larva was found data are included here and within composite attached directly over the heart (USNM analyses for the province. The only parasi- ENT 00862191) during May. tized specimen within the series (a male, CM 5.d. Algodonales, 3.2 km W on N-342, 55456, SVL 69.6) carried two female A. abbre- then 6.1 km N on C-339, (N36.91652 viata at the junction of his stomach with the in- W5.42705, 549 m). testine. Two nymphs and one larva (USNM 4. Oochoristica cf. tuberculata ENT 00862192) were found in the right axil (Platyhelminthes, Cestoda, Cyclophyllidea, of a male P. algirus (CM 53311, SVL 63.3) Davaineidae) . during June. 4.a. La Barca de la Florida. 5.e. Montes Propios de Jerez, various Six pieces conforming to the remains of a sites along logging roads in the vicinity of cestode (cf. Oochoristica) were found in the Galis (N36.55958 W5.60101, 440 m). intestinal tract of CM 53045B, a 40.1 mm SVL Psammodromus algirus were collected and male P. algirus collected during April. Oo- ʺlot cataloguedʺ from five sites (N36.59800 choristica cf. tuberculata parasitizing Acantho- W5.61980 [226 m], N36.58187 W5.64094

58 PARASITES OF SPANISH PSAMMODROMUS

[130 m], N36.57800 W5.66500 [517 m], et al., 2017). Although immature stages N36.57738 W5.66582 [474 m], and (larvae and nymphs) parasitize several N36.57060 W5.70800 [238 m]) during May lizard species, adults parasitize mammals in what is now the Parque Natural de Los (especially red fox [Vulpes vulpes]; Estra- Alcornocales. Ixodes inopinatus was en- da-PeÑa et al., 2017), but this tick is not rec- countered on three individuals from these ognized as a vector of any pathogen five sites, but cannot be associated with any (Estrada-PeÑa et al., 2017). Immature stag- specific site. Two male P. algirus (CM es of Haemaphysalis punctata parasitize a 54687B and CM 54687C, SVL 72.6 and 76.6, wide variety of lizards, birds, and small respectively) hosted a total of seven mammals, whereas adults parasitize main- nymphs (USNM ENT 00862193-00862194) ly ungulates across much of the Southern in right and left axillae. The left axil of a Palearctic region (Barandika et al., 2011; female (CM 54687D, SVL 67.4) carried three Estrada-PeÑa et al., 2017). In contrast with nymphs and one larva, the right axil carried I. inopinatus, H. punctata serves as a vector two nymphs, and one larva was recovered for several pathogens, including arbo- from the mid-lateral portion of the abdo- viruses, rickettsial bacteria and protozoa men (USNM ENT 00862221). (including Babesia spp., an apicomplexan 6. Ixodes inopinatus (Arthropoda, Arachni- parasite that infects red blood cells) da, Acari, Ixodidae). (Estrada-PeÑa et al., 2017). 6.a. Facinas, 7.3 km (airline) NE (266.2°; Tapeworms in the genus Mesoces- N36.14809 W5.62074, 71 m). toides have a complex three stage life cycle One female P. occidentalis (CM 54808, that apparently includes Psammodromus SVL 41) hosted a nymph (USNM ENT among its secondary hosts. Literák et al. 00862245) in the right axil during May. (2006) discuss morphometric and riboso- Considering only nematode diversity mal DNA in isolates of M. litteratus from from within provincial borders of Cádiz, red fox (Vulpes vulpes) originating in the only one specimen (CM 53139), a male from Czech Republic, Slovakia, and Spain La Barca de la Florida, carried more than (Solsona, Lleida Province). Their results one nematode species (S. cf. taurica and A. suggest that 18S rNA sequences can be abbreviata). Brillouin’s Diversity index for used to differentiate between M. litteratus this P. algirus sample (H = 0.1104) is also and M. lineatus that, along with M. am- higher than those summarized by ROCA biguus, have been reported from Spain and are (2017a: Table 2) for the Iberian Peninsula. known to parasitize humans (Fuentes et al., 2003; Iberfauna, 2005; & Bowman, Discussion 2014). The tick Ixodes inopinatus has been The correlations between estimates of recorded in Austria, Germany, Romania, prevalence (52% vs 8%), and intensity of Portugal, Spain, Morocco, and Tunisia in infection (3.3 ± 6.9 vs 0.8 ± 0.75), regarding the Western Palearctic region, largely from Spauligodon carbonelli parasitism of Iberol- regions not inhabited by the morphologi- acerta cyreni at ~1780 m and Psammodromus cally similar Ixodes ricinus, (Estrada-PeÑa algirus at ~1102 m of elevation are positive (I.

59 BUSACK ET AL.

bled available illustrations of male mor- phology; Roca (2017a) considered a sample he examined from a nearby locality to represent S. cf. hoffmanni because this was ʺthe species usually found parasitizing other lizards in this area (Roca et al., 1990)ʺ. We have redrawn the map referenced in ROCA et al. (1990), and on it we have placed a symbol locating our joint area of investigation (Fig. 3). There are two refuges in the area, the Refugio de Reguero Llano (closest for ve- hicle access [40°16.550ʹN, 5°14.225ʹW, 1907 m]), and the Refugio Laguna Grande de Gredos (40°15.040ʹN, 5°16.791ʹW, 1950 m), whose locations can be used to create a Figure 3.: Map redrawn from Roca et al. (1990) triangle that likely includes the general providing comparison among survey locali- area from which Rocaʹs specimens were ties. collected (ʺ40°15’N, 5°13’Wʺ). Elevations cyreni data from Roca, 2017a: Table 1). between ~1780 meters and ~1950 meters, Whether these results are best explained coupled with the terrain and its general by a paucity of suitable hosts at higher difficulty of access, make it reasonable to elevations, a seasonally-reduced develop- assume that previous investigators were mental period, by unrecognized issues operating within this triangle, and that precipitated by physiogeographic evolu- Iberolacerta cyreni samples were collected in tion of the Sistema Central of Spain, or proximity to one, or both, of these refuges. simply demonstrate that these two data Skrjabinelazia hoffmanni has recently sets alone cannot provide a sufficient basis (Roca, 2017b) been reported parasitizing for an appropriate generalization of corre- P. algirus in the area of La Alberca (Salamanca lations between parasite populations and Province, 40°29.350ʹN 6°6.667ʹW, 1050 m), elevations (see discussion in Roca [2017a]) approximately 86 km northwest from cannot, as yet, be determined. Rocaʹs (2017a) Sierra de Gredos locality, Positive identification of female nema- and on the western side of the Sierra de todes in the genus Skrjabinelazia requires Gredos. Elevations within a circular area access to male specimens, and no males of 6 km diameter centered on La Alberca were represented in our sample, or in the range between 980 m and 1350 m, placing sample examined by Roca (2017a); conse- it within the elevational range (824 m - quently, the tentative species assignments 1100 m) for the S. cf. taurica samples we differ between samples. We considered sampled from the eastern side of the Sierra our specimens to represent S. cf. taurica de Gredos, rather than in the much higher because the females most closely resem- elevational range (1780 m - 1950 m) for the

60 PARASITES OF SPANISH PSAMMODROMUS

Iberolacerta cyreni reported by Roca (2017a). end. Roca (2017b) further states ʺ…se confirma Iberolacerta cyreni, a lizard inhabiting la gran variabililidad intraespecifica de rocky areas of limited vegetative diversity esta especie de nematodo en la peninsula at relatively high elevations (1700 m - 2500 ibérica….ʺ, a point made previously in m [with occasional variation at the lower Roca et al. (1990), as he explains why assign- end] in the Gredos Mountains), is active ment to subspecies is not advisable for the from late March until early October as La Alberca specimens. temperatures and weather conditions al- Skrjabinelazia hoffmanni is diheterox- low maintenance of suitable body temper- enic and poecilogynous; its life cycle in- atures (18.4°C - 37.5°C,  = 29.4; Arribas, cludes two intermediate hosts, one of 2014). At these high elevations population which is a coprophagous insect, and fe- densities of poikilothermic species poten- males are of two types. Few third stage tially acting as intermediate parasite hosts larvae develop in the uterus of viviparous generally occur in lower densities, and young females, providing for parasite may be active at lower body temperatures, multiplication directly inside the host, and than suitable hosts at lower elevations old females are oviparous, their eggs con- (SDB, pers. obs.), and nematodes with life taining a third stage infective larva that histories tolerating lower-density hosts or requires ʺsecondary ingestionʺ. ʺThese lower developmental temperatures will eggs, after being ingested by field-crickets, likely benefit from less competition from hatch and without further development nematode species not well adapted to con- remain as larvae in the insect. An… ditions at these high elevations. entomophagus lizard host, which… has no The landscape separating our Psammo- opportunity to ingest the eggs, is infested dromus algirus from Rocaʹs Iberolacerta cyre- by eating insects…, and lizard parasitism ni presents a rugged topography of varying ele- remains lowʺ (Chabaud et al., 1988). vations. Crossing the approximately 5.2 Intermediate hosts may differ among km (airline) distance from our site at ~1100 Skrjabinelazia species, and may include arthro- m to Rocaʹs site will traverse rugged terrain pods and gastropods among Podarcis spe- at 1597 m, then 1955 m, and then 1657 m cies studied by Roca (2006). Citing Orte- before reaching the approximately 1780 m ga-Mora Rojo-Vázquez (2007), Roca locality supporting I. cyreni. That the lacer- (2015) infers that ecological factors may tid lizard species representing this lower favor encounters between insect hosts and elevation is generally active at body tem- the lizards that feed upon them, thereby peratures between 32.0°C and 38.6°C ( = facilitating completion of the parasite life 35.2 ± [SE] 0.5°C, n = 15; see also Busack, cycle. As neither low host specificity 1976), suggests that different species of (eurixeny), nor high host specificity Skrjabinelazia, along with differing species of (estenoxeny) require ʺlong contact time in invertebrate carriers, may be represented in the [co-evolution] of parasite and hostʺ, if each of these areas in the Sierra de Gredos. placed on a continuum S. ho ffmanni falls Booth-Rea et al. (2018) present a scenario close to the low end, and far from the high explaining geological and biological obser-

61 BUSACK ET AL. vations regarding the exchange of terrestri- of the three localities, provided any male al biota between Iberia and Africa before parasite specimens required for positive (~7 Ma – 3 Ma), during (10 Ma – 6.2 Ma), species identification, thereby reducing and after the Mediterranean Salinity Crisis experienced parasitologists to providing (MSC). Figs. 1 and 2 in Booth-Rea et al. provisional identifications of species in- (2018) illustrate how the eastern Alboran volved. Basinʹs well-differentiated (14 km–17 km What we now understand regarding thick) volcanic arc, with sufficient buoy- physiogeographic changes in Iberia ancy to create an archipelago and support throughout the phylogenetic, and natural a filter bridge, may serve to explain these history of the genus Psammodromus, pro- phenomena. Progressive build-up and vides at least a theoretical pathway to un- later subsidence of that filter bridge can derstanding why P. algirus may host explain the extended exchange of terres- different species of the nematode genus trial biota between Iberia and Africa, and Skrjabinelazia within similar elevation agrees with patterns of biota speciation ranges on each side of this mountain and terrestrial fossil distribution before range. The Pleistocene ʺsplitʺ referenced the MSC. by Carranza et al. (2006) may have been Extensive morphological and phyloge- precipitated, and later facilitated, by netic analyses provide confirmation of northward expansion within the western eastern and western clade development clade of P. algirus. This, and the fact that within Psammodromus algirus (Busack et representatives of western and eastern al., 2006; Carranza et al., 2006: Fig. 2; clades of P. algirus may be represented VerdÚ-Ricoy et al., 2010: Fig. 1) during the on lower elevation areas of the western Pliocene (approximately 3.6 Ma). Between and eastern slopes of the Sierra de Gre- western assemblages, Iberian and North dos, suggests that different species of African specimens represent two, weakly- Skrjabinelazia may also be represented on supported, monophyletic groups that ap- these lower and higher elevation areas of pear to have developed approximately 1.9 the Sierra de Gredos. Is the Sk rjabine- Ma, around the beginning of the Pleisto- lazia species discovered at the highest eleva- cene (see Fig. 1 in Carranza et al., 2006). tion likely to represent S. hoffmanni? Or Two of three localities supporting both does it, too, represent yet a separate spe- P. algirus and nematode species in the genus cies? As there are considerable intraspe- Skrjabinelazia under consideration are cific differences found among popula- positioned, respectively, at similar elevations representing several areas of Spain tional ranges on eastern and western sides (Roca et al., 1990; Roca, 2017b; Fig. 3), it of the Sierra de Gredos. The third locality is our opinion that additional research is is at a considerably higher elevation, and necessary before defensible generaliza- supports both a different lacertid lizard tions regarding parasitization by species (I. cyreni), and representatives of Skrjabinelazia species within the Iberian the nematode genus Skrjabinelazia. Un- Peninsula may be presented. fortunately, only La Alberca, western-most In Cádiz Province, at elevations vary-

62 PARASITES OF SPANISH PSAMMODROMUS ing between 80 m and 440 m, 15 representative of a 50:50 relationship (p = Skrjabinelazia cf. taurica were found dis- 0.78). When considering abundance data tributed as five, one, one, six, and two from three different localities within the nematodes within five female P. algirus, province to be representative of the prov- and 27 S. cf. taurica were found distrib- ince as a whole, 100% of males carried uted as one, 10, 12, two, and two nema- these parasites, but only 50% of females todes within five male P. algirus. Mean did. Mean helminth-to-host intensity esti- parasite abundance and intensity was 3.0 mates for infection, however, overlap ± 1.1 nematodes per female host, and 5.4 broadly between females (1.1 ± 0.2) and ± 2.3 nematodes per male host. When sex males (1.4 ± 0.2). Only during August and of the host is not considered, mean abun- September were immature parasites dance and intensity for S. cf. taurica in- found, but insufficient sample sizes pre- fection was 4.2 ± 1.3 nematodes per indi- clude any meaningful comparison be- vidual P. algirus. tween parasite abundance and SVL for Prevalence of S. cf. taurica infection either sex; neither is there sufficient varia- in male P. algirus may be significantly bility in this relationship when sex is not greater than that in females (p = 0.03), considered a variable. but further analysis suggests no associa- An on-going discussion regarding the tion between number of parasites and relationship between parasitism and eleva- SVL for either males (n = 5, Spearman tion has offered both negative and positive rank [rs] = 0.15; p = 0.80), or females (n = 5, correlations regarding this relationship; rs = 0.15; p = 0.80); neither is there a statistical Rocha et al. (2003) attributed low helminth association between parasite load and in- diversity within Aspronema dorsivittatum dividual SVL, when sex is not considered (Scincidae; see Hedges Conn (2012) re- as a variable (n = 10, rs = 0.19; p = 0.59). If, garding this taxonomic change) not to an however, we consider cumulative body elevation-diversity effect, but to the size and parasite number within sexes to ʺrelative isolation (insularity effect)ʺ of be the more important comparison, in this their study area at 2460 m in Brazil’s Man- particular population sample a total of 27 tiqueira Mountains. Van Sluys et al. (1997) S. cf. taurica were identified within 323.2 mm similarly suggested habitat isolation as an of cumulative male body length and a to- explanation for low nematode diversity in tal of 15 S. cf. taurica were identified “restinga” habitat within southeastern within 301.1 mm of cumulative female Brazil. body length. Viewed from this perspecti- Dobson et al. (1992) found no relationship ve, infected males carry a parasite load between elevation and parasite density or ~1.6 times that of infected females (0.08 abundance for Anolis in the northern Less- parasites/mm versus 0.05 parasites/mm of er Antilles; Maia et al. (2016) did not detect a SVL). correlation between parasitaemia and ele- Proportions of female (0.46) and male vation but found individual Pristrurus (0.54) Psammodromus algirus hosting A. ab- rupestris (Gekkota, Sphaerodactylidae) to be breviata (n = 13) within Cádiz Province were less-infected with haplotype 5 haemogreg-

63 BUSACK ET AL. arines at higher elevations than at lower tion intensity for Spauligodon carbonelli elevations in Oman. Carbayo et al. (2019), decreases greatly between 1780 m (3.3 ± working in Madrid Province, Spain, found 6.9) and 1102 meters (0.8 ± 0.8). Overall the prevalence of infection by intra- helminth species diversity, on the other erythrocytic parasites (haemococcidia) hand, appears highest (H = 0.369) at locali- assigned to Schellack ia sp. (Conoidasida: ties around 1102 m and lowest (0.110) at Eucoccidiorida; Lankesterellidae) signifi- localities between 80 m and 440 m in Cá- cantly lower at a higher elevation (48.3% at diz Province. 1200 m; Navacerrada, 40°44′N, 4°02′W) Larger samples are necessary before a than at a lower elevation (90.3% at 850 m; generalized relationship between elevation Colmenar Viejo, 40°41’N, 3°49’W), but in- and parasite intensities of infection can be festation by tick nymphs tentatively as- supported (see Table 1), at least for these signed to Ixodes sp. was significantly low- nematodes in Spain. er at Colmenar than at Navacerrada (1.6% Acknowledgement infected vs 91.6% infected). Data for the relationship between Stephen P. Rogers, Collections Manager, Skrjabinelazia prevalence and parasitaemia, Section of Amphibians and Reptiles, Carne- and elevation within Spain, for example, gie Museum of Natural History, Jeremy F. are not easily generalized. At higher ele- Jacobs at USNM, graciously provided assis- vations in the Sierra de Gredos (ca. 1780 tance and access to specimens in their care; m) Iberolacerta cyreni was found to host S. Janet Edgerton, Head Librarian at the Brim- cf. hoffmanni at a lower level (one para- ley Library, North Carolina Museum of site/individual) than a sample of Psammo- Natural Sciences (NCSM), provided invalu- dromus algirus was found to host S. cf. taurica able bibliographic assistance in an efficient in the same general geographical area but and timely manner; Liz Bradford, formerly at a lower elevation (ca. 873 m - 1098 m; of Raleigh, North Carolina, executed the one-five parasites/individual). At a signifi- parasite map (Fig. 2); and Lisa Yow- cantly lower elevation in Cádiz Province Ferguson, Art Director, NCSM, edited Fig. 1 (ca. 440 m), one male and one female P. and produced Fig. 3. Busackʹs wife (Gin) algirus each carried few (two) S. cf. taurica, endured alcoholic specimens in the base- but at an even lower (76 m) elevation four ment during completion of the laboratory males and four females hosted between 1- work, and provided sustinence and com- 12 and one-six S. cf. taurica, respectively panionship during the execution and com- (see Results - Cádiz, Section 2). pletion of this project. Production is always In summary, we note that infection in- a joint effort, and we thank all who assisted. tensity for Skrjabinelazia sp. at 1780 me- This project was self-funded by Busack. ters (1.0 ± 0) increases to 2.6 ± 0.8 as you descend to 1102 m, and increases further References to 4.2 ± 1.3 as sea level is approached Anderson, R.C.; Chabaud, A.G. Willmott, S. (between 440 m and 80 m). In the same (2009). Keys to the nematode parasites of relatively-high-elevation localities, infec- vertebrates. Archival volume, CABI Pub-

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