Gallotia Galloti Palmae, Fam

CITE THIS ARTCILE AS “IN PRESS” Basic and Applied Herpetology 00 (0000) 000-000

Chemical discrimination of pesticide-treated grapes by lizards (Gallotia galloti palmae, Fam. Lacertidae)

Nieves Rosa Yanes-Marichal1, Angel Fermín Francisco-Sánchez1, Miguel Molina-Borja2*

1 Laboratorio de Agrobiología, Cabildo Insular de La Palma.

2 Grupo Etología y Ecología del Comportamiento, Departamento de Biología Animal, Facultad de Biología, Universidad de La Laguna, 38206 La Laguna, Tenerife, Canary Islands.

* Correspondence: Phone: +34 922318341, Fax: +34 922318311, Email: [email protected]

Received: 14 November 2016; returned for review: 1 December 2016; accepted 3 January 2017

Lizards from the Canary Islands may act as pests of several cultivated plants. As a case in point, vineyard farmers often complain about the lizards’ impact on grapes. Though no specific pesticide is used for lizards, several pesticides are used in vineyards to control for insects, fungi, etc. We therefore tested whether lizards (Gallotia galloti palmae) could detect and discriminate pesticide- treated from untreated grapes. To answer this question, we performed experiments with adults of both sexes obtained from three localities in La Palma Island. Two of them were a vineyard and a banana plantation that had been treated with pesticides and the other one was in a natural (untreated) site. In the laboratory, lizards were offered simultaneously one untreated (water sprayed) and one treated (with Folithion 50 LE, diluted to 0.1%) grape placed on small plates. The behaviour of the lizards towards the fruits was filmed and subsequently quantified by means of their tongue-flick, licks or bite rates to each of the grapes. Results showed that only lizards from the natural (untreated) site clearly differentiated the two types of grapes, performing significantly more tongue-flicks, licks and bites to the untreated than to the pesticide-treated grapes. Lizards captured at the other two sites (cultivated fields with pesticide treatment), did not show a significantly different response to the two types of grapes. These results suggest that lizards living in or near cultivated fields may be habituated to pesticide-treated food and, therefore, do not clearly discriminate treated from untreated food items. However, another possibility is that natural selection (or maybe resistance) could be responsible by these individuals in the populations showing this kind of pesticide insensitiveness.

Key words: chemical detection; Gallotia; grapes; lizards; pesticide.

Impact of wild fauna on crops is a arachnids), but also by several vertebrates problem documented worldwide such as rats, mice, birds and lizards (Dolbeer, 1990; Dolbeer et al., 1994; Hill, (Rodríguez-López, 1996). While there is 1997; Brittingham et al., 2000; Tillman et some information on the effects of insects al., 2000; Avery, 2002; Witmer et al., 2007 ). on Canary vineyards (Pérez-Padrón & In the Canary Islands, cultivated plants are Rodríguez-López, 1987; Lorenzo Bethen- affected by a wide variety of animal spe- court et al., 2004), nothing is known on the cies, mainly invertebrates (insects and quantitative effect of vertebrate species

DOI: http://dx.doi.org/10.11160/bah.63 YANES-MARICHAL ET AL.

(indirect estimations appeared in Marqui- “ahulaga” (Launaea arborescens, Fam. na, 1977). However, farmers have tradi- Asteraceae), and petals and fruits of tionally complained about damage con- “tunera” (Opuntia dilenii, Fam. Cactaceae) ducted by several vertebrates, mainly (Molina-Borja, 1981, 1986, 1991; Molina- blackbirds and lizards, to several crops Borja & Barquín, 1986; Molina-Borja & including vineyard fields. Bischoff, 1998). As far as animal prey, Invertebrate pests are usually treated these lizards eat beetles, ants, cochineals by applying different kinds of pesticides. (Dactylopius coccus), and small Cepaea Folithion 50 LE (the organophosphate snails (Molina-Borja & Bischoff, 1998; Fenitrothion 50%) is the acaricide- Valido et al. 2003). fungicide most commonly used for differ- Gallotia galloti palmae is a medium sized ent plant pests, including those found in lizard (mean adult male snout-vent length vineyards. This pesticide may help to con- = 102 mm and body mass = 44 g). It has a trol some insect-arachnid pests, but almost striking sexual dimorphism with large and no data exist on its effect on any lizard robust males with a conspicuous blue- species (but see Bain et al., 2004). Howev- coloured gular skin, and smaller and cryp- er, other cholinesterase-inhibiting pesti- tically coloured females (see Bischoff, 1998 cides have been shown to affect physiolog- for a detailed description of the species). ical/performance traits in some reptiles According to farmers’ oral tradition the (Pauli & Money, 2000; Hopkins et al., 2005; lizards consume, in addition to grapes, the Hopkins & Winne, 2006); on the other leaves, flowers or fruits of other cultivated hand, while pesticide treatment was sown plants such as pumpkins, peppers, and to affect presence of reptiles in natural are- tomatoes. as (Lambert, 2005), few significant differ- Squamata typically use their tongue to ences were found in populations of Po- collect chemicals from the environment, darcis bocagei living in agricultural habitats and transfer them to the paired vomerona- which were either regularly exposed or sal organs located in the roof of the buccal not to pesticides (Amaral et al., 2012). cavity (Burghardt, 1970, 1980; Graves & La Palma Island has many vineyards Halpern, 1989, 1990). Numerous publica- with different types of pest treatments. tions have documented the lizards’ capaci- Gallotia galloti palmae lizards are found ty to detect chemical products produced throughout the island and are, like other by plants and other animals (conspecifics Gallotia species, omnivorous (Roca et al. or predators) (Cooper, 1989, 1994a,b; Font, 2005). They consume several wild plant 1996; Cooper & Pérez-Mellado, 2001a; species, including fruits of “balo” (Plocama Cooper et al., 2002; Font & Desfilis, 2002). pendula, Fam. Rubiaceae), leaves and inflo- Therefore, lizards have the ability to detect rescences of “verode” (Senecio kleinia, Fam. (sense) chemical products from several Asteraceae), leaves and flowers of origins, both natural and artificial. As “salado” (Schizogine sericea, Fam. Composi- vineyards are commonly treated with pes- tae), flowers of “lavandula” (Lavandula ticides, we therefore hypothesized that canariensis, Fam. Lamiaceae), lizards could detect and differentiate pesti-

2 DISCRIMINATION PESTICIDE-TREATED GRAPES IN GALLOTIA cide-treated from untreated grapes. Lizard maintenance The specific objectives of the present The animals were transported to the paper are: 1) to determine experimentally laboratory were they were housed individ- if lizards of both sexes of G. g. palmae are ually in plastic cages with a 12L-12D light- capable of discriminating between untreat- dark cycle provided by daylight fluores- ed and pesticide-treated grapes by com- cent lamps (including the near ultraviolet paring the behaviour patterns directed spectrum; Sylvania Reptistar 18W – towards both types of grapes; 2) Compare Havells-Sylvannia, Erlangen, Germany), the rates of behaviour patterns directed to and room/ambient temperature of 28 + the grapes by lizards coming from sites 1ºC. Our previous long experience with with pesticide-treated crops with those of lizards kept in captivity, has shown that individuals coming from a natural site individuals only eat at most two times a without any pesticide treatment. week, even when continuously provided MATERIALS AND METHODS with food. Therefore, in order to ensure adequate feeding motivation during the Study zones and capturing method experimental trials, lizards were kept We selected three sites to collect lizards without food for 7 days before beginning for the experiments. One was very close (< the experiments. Immediately after the 10 m) to a banana plantation in Tazacorte trials, all lizards were allowed to eat pieces (28º37’36.42”N, 17º55’06.08”W; altitude: of banana or tomato placed in their indi- 184.9 m), another was inside a vineyard at vidual cages. Fuencaliente (28º30’26.98”N, Experimental procedure 17º491’23.66”W; altitude: 639.5 m) with volcanic lapilli as substrate, and the third Experiments were conducted in an ex- was a natural site at Tigalate perimental cage (100 x 100 x 80 cm, with a (28º32’59.01”N, 17º48’10.19”W; altitude: cork plate as substrate) with the same 608.7 m). The first two sites were inside or lighting and temperature regime as the in the vicinity of cultivated fields (where maintenance cages, and two small glass pesticides are commonly applied), while dishes placed near one of the cage walls, the third locality was far away from any 30 cm apart. We put a single untreated pesticide-treated crop. The main vegeta- grape in one dish and a grape treated with tion of the last site was composed of: a solution of Folithion 50 LE® (Bayer Crop- “cerrillo” (Hyparrhenia hirta), science, Ltd., Spain; composition: Fenitro- “higuerilla” (Euphorbia obtusifolia), and thion 50% p/v) in the other. We could not “verode” (Klenia neriifolia). Lizards were access to data on usual pesticide concen- collected during June and July of 2002. trations for treating crops; moreover, as Adult individuals of both sexes of G. g. we tried to avoid causing any harm to the palmae were captured with 5 l can traps experimental lizards, and as our aim for baited with pieces of banana and tomato this work was to determine if lizards could that were washed with running water be- respond even to very low levels of pesti- fore putting them into the cans. cide, we diluted Folithion with distilled

3 YANES-MARICHAL ET AL. water to 0.1%. Both grapes had been previ- vent length (SVL) and took their body ously washed in running water and then mass (BM) after the trials. All animals dried. The pesticide was applied to one were adults as their SVL was similar to or grape of every pair with a small brush im- larger than size at sexual maturity mersed once in the Folithion solution (Molina-Borja & Rodríguez-Domínguez, (while the control grape was similarly 2004). Only in very few cases some experi- brushed with distilled water). We used mental animals ate only a piece of a Foli- two different grapes of similar size/weight thion-treated grape. In these cases we for each experimental trial and we decided checked if the animals did not show any by flipping a coin which dish (right or left) symptoms of illness during the following would have the treated grape. days. After finishing the experiments, all Each experimental lizard was placed at lizards were released at their capture sites. the end of the cage opposite that holding Data and Statistics the grapes and we filmed its behaviour during at least 20 min after it resumed From the recorded videos we quanti- spontaneous activity. Filming was per- fied three behaviour patterns performed formed with a video camera Panasonic NV by the lizards towards the grapes: tongue- -DS15, mini DV (Panasonic, Kadoma, Osa- flicks, licks and bites (full descriptions in ka, Japan) placed outside the transparent Molina-Borja, 1981, 1987 ). As the dura- plastic wall of the cage that was closer to tion of trials was around 20 min, we calcu- the dishes with the grapes. The whole set lated the relative frequency (rate) of each up was visually isolated from the rest of behaviour pattern dividing the number of the room by a movable screen. Tempera- times it occurred by the exact duration of ture inside the cage (1 cm above substrate) each trial. In some trials, individuals did was measured with a digital thermometer not direct at least one tongue-flick, lick or (0.1ºC precision) at the beginning of each bite to one of the two grapes and were not experimental session. After each trial, the included in the analyses; this resulted in a bottom and walls of the cage were thor- smaller sample size for the corresponding oughly cleaned with alcohol (70%) and statistical comparisons. allowed to dry for 10 min. The minimum Data were analysed with the SPSS 20.0® interval between successive trials was 15 statistical package (Armonk, New York, min and all trials were performed between USA). As variable distributions did not 11:00 and 13:00; each lizard was tested on- fulfil normality and homoscedasticity re- ly once. quirements, we used Wilcoxon and Krus- We set up three experimental groups: kal-Wallis tests (Siegel & Castellan, 1988) 1) lizards that were captured very close to to compare the rates of behaviour patterns the banana plantation of Tazacorte (N = directed to the two types of grapes within 36); 2) those from the vineyard of Fuen- and between populations, respectively. caliente (N = 33); 3) animals captured at We verified that small differences in cage the natural site of Tigalate (N = 29). For all temperature among trials did not affect individuals we measured their snout-to- rates of the selected behaviour patterns

4 DISCRIMINATION PESTICIDE-TREATED GRAPES IN GALLOTIA

Table 1: Mean (+ SE) values, range (minimum, maximum) and sample size (N) for male (m) and female (f) Snout-to-vent length (SVL) and Body mass (BM) of the three populations sampled.

Fuencaliente Tazacorte Tigalate

m f m f m f

SVL Mean 100.30 80.98 104.97 87.65 96.31 83.15

S.E. 6.26 5.60 7.99 8.22 7.32 5.91

Minimum 87.99 68.65 90.23 69.75 85.67 72.53

Maximum 108.94 93.34 120.38 100.04 105.40 92.44

N 16 17 18 18 15 14

BM Mean 54.50 54.50 42.27 23.0 33.06 22.92

S.E. 5.79 4.17 11.75 6.25 5.81 3.81

Minimum 43.0 36.0 19.0 13.0 24.0 17.0

Maximum 61.0 51.0 67.0 37.0 41.0 30.0

N 16 17 18 18 15 14 and compared relative frequencies of multiple tests when appropriate (Wright those performed by the lizards towards 1992). the untreated and Folithion-treated RESULTS grapes. We also tested for differences in Mean (+ SE, range and sample size) of body size (SVL) of lizards from the three SVL and BM for males and females used populations and did not detect any signifi- in the experiments are shown in Table 1. cant difference (Bonferroni and Tukey post There was no significant relationship -hoc pair-wise comparisons; P > 0.05 in all between substrate temperatures inside the cases). Rates of the three selected behav- experimental cage and the rates at which iour patterns were not significantly differ- the lizards performed the three behaviour ent (Mann-Whitney U test) for males and patterns (rho = 0.20, P = 0.28; rho = - 0.27, P females from any site (P > 0.01 in all cases); = 0.20; and rho = 0.22, P = 0.39; for tongue- therefore, we pooled data from both sexes flicks, licks and bites, respectively, N = 29 of each site in order to make the statistical in all cases). comparisons of behaviour patterns di- Lizards captured at Fuencaliente per- rected towards each type of grape. We set formed significantly more tongue-flicks to alpha = 0.05, significance tests were two- the untreated than to the treated grapes tailed and we applied Sidak correction for (Wilcoxon tests, Z = - 2.189, N = 31, P =

5 YANES-MARICHAL ET AL.

Figure 1: Mean (+ 95% CI) relative frequencies of tongue-flicks (Tf), licks (L) and bites (B) of experimental lizards from Tazacorte, Fuencaliente and Tigalate towards untreated (U) and pesticide -treated (P) grapes.

0.029), but there was no difference in their differed (alpha = 0.025 after Sidak correc- licks (Z = - 0.731, N = 19, P = 0.46), or bites tion) among lizards from the three sites. (Z = - 1.364, N = 7, P = 0.174) (Fig. 1). Thus, lizards from Tigalate performed On the other hand, lizards captured at more tongue-flicks than those of Fuen- Tazacorte did not show any significant caliente and Tazacorte (Kruskal-Wallis difference in their rates of behaviour to- test, chi-square = 50.66, d.f. = 2, P < 0.0001). ward the treated and untreated grapes However, there was no significant differ- (tongue-flicks, Z = - 0.778, N = 32, P = 0.437; ence in the frequencies of licks or bites to licks, Z = - 1.178, N = 25, P = 0.239; bites, Z the untreated grapes by lizards from the = - 1.50, N = 21, P = 0.33, Fig. 1). three sites. In the case of pesticide-treated Lizards captured at Tigalate directed grapes, lizards from Tigalate again tongue significantly more tongue-flicks (Z = - -flicked significantly more often than those 4.371, N = 29, P = 0.0001), licks (Z = - 2.574, from Fuencaliente and Tazacorte (Kruskal- N = 24, P = 0.01), and bites (Z = - 2.255, N = Wallis test, chi-square = 22.83, d.f. = 2, P < 17, P = 0.02), at the untreated than at the 0.0001) while those from Fuencaliente bit treated grapes (Fig. 1). significantly more than those of Tazacorte On the other hand, rates of behaviour and Tigalate (Kruskal-Wallis test, chi- patterns directed at untreated grapes square = 8.30, d.f. = 2, P = 0.016); there was

6 DISCRIMINATION PESTICIDE-TREATED GRAPES IN GALLOTIA no significant difference in the rates of lick- from Fuencaliente could have been more ing among lizards from the three sites. water-deprived than those of Tazacorte The number of lizards that actually bit and then be more prone to consume the pesticide-treated grapes or the untreated grapes. ones were, respectively, five and two On the other hand, lizards from the (Fuencaliente), four and 15 (Tigalate) and untreated site tongue-flicked, licked and 10 and 14 (Tazacorte). bit untreated grapes more often than treated grapes. These results seem to indicate DISCUSSION that lizards that inhabit natural areas, It has been noted that while differential without previous contact with pesticide- tongue-flick rates may indicate discrimina- treated crops, have the ability to discrimi- tion, their absence does not necessarily nate between pesticide-treated and un- indicate lack of discriminatory ability (see treated fruits. Cooper 1998). However, the number of Several lizard species, including the bites in each of our experimental condi- Canarian lizards of the genus Gallotia, have tions seems to support a lack of discrimi- been shown to respond with tongue-flicks nation by G. g. palmae lizards from pesti- to sugar, fat and also to toxins of several cide-treated areas. On the contrary, lizards plants (Cooper, 1994a,b; Cooper & Pérez- from the untreated site had the ability to Mellado, 2001a,b,c; Cooper et al., 2002), discriminate Folithion-treated from un- but this is the first time a lizard is shown to treated grapes. Specifically, lizards from chemically discriminate the presence of sites were pesticides are used did not sig- pesticide on a fruit. nificantly differ in their behaviour towards Does this imply that the application of untreated and treated grapes, the only ex- non-specific pesticides could contribute to ception being the larger number of tongue- reduce the rate of consumption of pesti- flicks directed by lizards from Fuen- cide-treated fruits by lizards? We cannot caliente to untreated than to treated currently answer this question as field be- grapes. There is no clear explanation for havioural analyses are needed to compare this difference (though the statistic value rates of tongue-flicks, licks or bites to pesti- found, P = 0.029, could well be a false posi- cide-treated and untreated grapes (or other tive) nor for the higher frequency of biting fruits or plant items). Our results suggest treated grapes by lizards from Fuen- that, after continuous pesticide treatment caliente in comparison with those of Taza- on crops, the surviving lizards could be- corte; a potential explanation could be re- come habituated or somehow handi- lated with a difference in water supply in capped in their chemosensory abilities, these two sites. In the second location and therefore not be able to discriminate there were some open sewage pipes and pesticide-treated from untreated fruits or water leaks from some pipes while in the consume them differentially. Alternatively, first site there was a complete absence of lizards could have been selected for pesti- water sources. This last fact would imply cide resistance. However, to disentangle that, previously to their capture, lizards between acclimation and selection, a com-

7 YANES-MARICHAL ET AL. mon garden experiment would be needed. ards from pesticide-treated areas did in In fact, lizards from one of the pesticide- fact lick or bite pesticide-treated grapes. treated sites (Fuencaliente) significantly bit This result poses two suggestions: 1) that more pesticide-treated grapes than indi- vineyards treated with Fenitrothion might viduals from the other two sites. not have an effect on consumption of It is possible that lizards from pesticide grapes by lizards; 2) the consumption of -treated crops could have some of its sen- pesticide-treated grapes could induce sory/brain functions affected from previ- some organism dysfunction in lizards (see ous ingestion of pesticide-treated fruit above); this last effect could then affect and, therefore, would not be able to differ- conservation of populations living in or entiate treated from untreated grapes. near crops and their predators. There are data on several possible contam- On the other hand, most individuals inants for reptiles (Campbell & Campbell, from the natural zone (Tigalate) avoided 2000, 2002; Pauli & Money, 2000) and Car- consuming pesticide-treated grapes: 15 bamate and other organophosphate-based lizards from that location bit the untreated pesticides are known to inhibit brain ace- grape compared to only four that bit the tylcholinesterase activity (Hall & Clark, pesticide-treated grape. This suggests that 1982; Russell & Overstreet, 1987). For lizards not previously having experience example, a reduction in swimming perfor- of pesticide-treated foods could avoid eat- mance was detected in cholinesterase- ing them; only after reiterated pesticide inhibiting pesticide treated natricine treatments of a zone, they could become snakes (Hopkins & Winne, 2006). Howev- habituated. er, low doses of Fenitrothion did not have Acknowledgements any significant effect on several physiolog- ical and behavioural parameters of the We thank Enrique Font for a detailed agamid Pogona vitticeps (Bain et al., 2004), revision of an earlier version of the manu- nor were these traits affected by low doses script. To Consejería de Agricultura, Ga- of carbaryl (a carbamate pesticide) in Scelo- nadería y Pesca from Cabildo Insular de porus occidentalis (DuRant, 2006). La Palma (island institution) that funded Another possibility is that lizards may the study; we are especially indebted to learn to avoid the consumption of certain the deceased Margarita Castro, former foods if associated with illness. Thus, for director of that Consejería. We also thank example, Burghardt et al. (1973) could the staff of Laboratorio de Agrobiología induce aversion to palatable prey by de- for their support during the experimental layed illness in garter snakes, and Paradis work. To the offices of Extensión Agraria & Cabanac (2004) found flavour aversion in La Palma for their cooperation provid- learning in several basilisks and skink spe- ing information on common pests and pes- cies when injected with lithium chloride ticides in the Island. Consejería de Medio (an illness inducer) after consuming novel Ambiente of Cabildo de La Palma provid- food. However our data do not support ed the permissions to capture the lizards this hypothesis as some experimental liz- (given by a decree of Cabildo de La Palma,

8 DISCRIMINATION PESTICIDE-TREATED GRAPES IN GALLOTIA dated 22nd February 2000). For the experi- stein (eds.) Chemical signals, vertebrates and mental work, we followed the correspond- aquatic invertebrates. Plenum Press, New ing regulation and legislation on animal York, London, pp. 275-301. care. Burghardt, G.M.; Wilcoxon, H.C. & Czaplicki, J.A. (1973). Conditioning in garter snakes: REFERENCES Aversion to palatable prey induced by de- Amaral, M.J.; Carretero, M.A.; Bicho, R.C.; layed illness. Animal Learning and Behavior 1: Soares, A.M.V.M. & Mann, R.M. (2012). The 317-320. use of a lacertid lizard as a model for reptile Campbell, K.R. & Campbell, T.S. (2000). Lizard ecotoxicology studies: Part 1 – Field de- contaminant data for ecological risk assess- mographics and morphology. Chemosphere, ment. Reviews of Environmental Contamina- 87: 757-764. tion and Toxicology 165: 39–116. Avery, M.L. (2002). Behavioral and Ecological Campbell, K.R. & Campbell, T.S. (2002). A logi- Considerations for Managing Bird Damage cal starting point for developing priorities to Cultivated Fruit, In D.J Levey; W.R. Silva for lizard and snake ecotoxicology: a review & M. Galetti (eds.) Seed Dispersal and Fru- of available data. Environmental Toxicology givory: Ecology. Evolution and Conservation. and Chemistry 21: 894–898. CABI Publishing, New York, USA, pp. 467- Cooper, W.E.Jr. (1989). Prey odor discrimina- 477. tion in the varanoid lizards Heloderma sus- Bain, D.; Buttemer, W.A.; Astheimer, L.; Fil- pectum and Varanus exanthematicus. Ethology des, K. & Hooper M.J. (2004). Effects of sub- 81: 250-258. lethal fenitrothion ingestion on cholinester- Cooper, W.E.Jr. (1994a). Chemical discrimina- ase inhibition, standard metabolism, ther- tion by tongue-flicking in lizards: a review mal preference, and prey-capture ability in with hypotheses on its origin and its ecolog- the Australian central bearded dragon ical and phylogenetic relationships. Journal (Pogona vitticeps, Agamidae). Environmental of Chemical Ecology 20: 439-487. Toxicology & Chemistry 23: 109-116. Cooper, W.E.Jr. (1994b). Multiple functions of Bischoff, W. (1998). Handbuch der reptilien und extraoral lingual behaviour in iguanian amphibien Europas. Band 6: Die reptilien der lizards: prey capture, grooming and swal- Kanarischen inseln, der Selvagens-Inseln und lowing, but not prey detection. Animal Be- des Madeira-Archipels. Wiesbaden:AULA- haviour 47: 765-775. Verlag, Berlin, Germany. Cooper, W.E.Jr. (1998). Evaluation of swab and Brittingham, M.C.; Kays, J. & McPeake, R. related tests for responses by squamates to (2000). Proceedings of the Ninth Wildlife chemical stimuli. Journal of Chemical Ecology Damage Management Conference. State 24: 841-866. College, PA, USA. Cooper, W.E.Jr. & Pérez-Mellado, V. (2001a). Burghardt, G.M. (1970). Chemical perception Food chemical cues elicit general and popu- in reptiles, In J.W. Johnston; D.G. Moulton lation-specific effects on lingual and biting & A. Turk (eds.) Advances in Chemoreception, behaviors in the lacertid lizard Podarcis lil- Vol. 1, Communication by Chemical Signals. fordi. Journal of Experimental Zoology 290: 207 Appleton-Century-Crofts, New York, pp. –217. 241-308. Cooper, W.E.Jr. & Pérez-Mellado, V. (2001b). Burghardt, G.M. (1980). Behavioral and stimu- Location of fruit using only airborne odor lus correlates of vomeronasal functioning in cues by a lizard. Physiology & Behavior 74: reptiles: feeding, grouping, sex, and tongue 339-342. use, In D. Müller-Schwarze & R.M. Silver- Cooper, W.E.Jr. & Pérez-Mellado, V. (2001c).

9 YANES-MARICHAL ET AL.

Chemosensory responses to sugar and fat organophosphorus pesticides. Environmen- by the omnivorous lizard Gallotia caesaris tal Pollution 28: 45-52. with behavioral evidence suggesting a role Hill, C.M. (1997). Crop-raiding by wild verte- for gustation. Physiology & Behavior 73: 509- brates: the farmer’s perspective in an agri- 516. cultural community in western Uganda. Cooper, W.E.Jr.; Pérez-Mellado, V.; Vitt, L.J. International Journal of Pest Management 43: & Budzinsky, B. (2002). Behavioral responses 77-84. to plant toxins by two omnivorous lizard Hopkins, W.A.; Winne, C.T. & DuRant, S.E. species. Physiology & Behavior 76: 297-303. (2005). Differential swimming performance Dolbeer, R.A. (1990) Ornithology and integrat- of two natricine snakes exposed to a cholin- ed pest management: red- winged black- esterase-inhibiting pesticide. Environmental birds Agelaius phoeniceus and corn. Ibis 132: Pollution 133: 531–540. 309–322. Hopkins, W.A., & Winne, C.T. (2006). Influence Dolbeer, R.A.; Holler, N.R. & Hawthorne, of body size on swimming performance of D.W. (1994). Identification and assessment four species of neonatal natricine snakes of wildlife damage: an overview, In S.E. acutely exposed to a cholinesterase- Hygnstrom; R.M. Timm & G.E. Larson inhibiting pesticide. Environmental Toxicolo- (eds.) Prevention and Control of Wildlife Dam- gy & Chemistry 25: 1208-1213. age. University of Nebraska-Lincoln, USA, Lambert, M.R.K. (2005). Lizards used as bioin- pp. A1-A18. dicators to monitor pesticide contamination DuRant, S.E. (2006). Sublethal effects of an acetyl- in sub-Saharan Africa: A review. Applied cholinesterase-inhibiting pesticide on fitness- Herpetology 2: 99-107. related traits in the western fence lizard Lorenzo Bethencourt, C.D.; Prendes Ayala, (Sceloporous occidentalis). Ph.D. Dissertation. C.; Alvarez de la Paz, F.J.; Cabrera Pérez, University of Virginia, USA. R. & Prendes Lorenzo, C.D. (2004). Distri- Font, E. (1996). Los sentidos químicos de los bución y daños producidos por Stenidea reptiles. Un enfoque etológico, In F. Colme- annulicornis (Brullé 1838) (Coleoptera: Ce- nares (ed.) Etología, psicología comparada y rambycidae) en los viñedos de Tacoronte. comportamiento animal. Editorial Síntesis, Tenerife. Canarias, In XI Congreso Ibérico de Madrid, pp. 196-288. Entomología (Funchal (Madeira), - Portugal, Font, E. & Desfilis, E. (2002). Chemosensory Septiembre 2004. recognition of familiar and unfamiliar con- Marquina, T. (1977). Los lagartos (Lacerta sp.), specifics by juveniles of the Iberian wall una plaga de algunos cultivos de las Islas lizard Podarcis hispanica. Ethology 108: 319- Canarias. Anales del Instituto Nacional de 330. Investigaciones Agrarias. Serie Proteccion Vege- Graves, B. & Halpern, M. (1989). Chemical tal: 1-3. access to the vomeronasal organs of the Molina-Borja, M. (1981). Etograma del lagarto lizard Chalcides ocellatus. Journal of Experi- de Tenerife, Gallotia galloti galloti (Sauria- mental Zoology 249: 150-157. Lacertidae). Doñana Acta Vertebrata 8: 43-78. Graves, B. & Halpern, M. (1990). Roles of vo- Molina-Borja, M. (1986). Notes on the diet of meronasal organ chemoreception in tongue Gallotia stehlini as obtained from behaviour flicking, exploratory and feeding behaviour observations. Vieraea 16: 23-26. of the lizard Chalcides ocellatus. Animal Be- Molina-Borja, M. (1987). Additions to the haviour 39: 692-698. ethogram of the lizard Gallotia galloti from Hall, R.J. & Clark, D.R. Jr. (1982). Response of Tenerife, Canary Islands. Vieraea 17: 171- the iguanid lizard Anolis carolinensis to four 178.

10 DISCRIMINATION PESTICIDE-TREATED GRAPES IN GALLOTIA

Molina-Borja, M. (1991). Notes on alimentary McGraw-Hill, New York, USA. habits and spatial-temporal distribution of Tillman, E.A.; Van Doom, A. & Avery, M.L. eating behaviour patterns in a natural pop- (2000). Bird damage to tropical fruit in ulation of lizards (Gallotia galloti). Vieraea 20: South Florida, In M.C. Brittingham; J. Kays 1-9. & R. McPeake (eds.) The Ninth Wildlife Dam- Molina-Borja, M. & Barquín, E. (1986). On the age Management Conference Proceedings. consumption of Launaea arborescens flowers Pennsylvania State College, Pennsylvania, by the lizard Gallotia atlantica. Vieraea 16: 233 USA, pp. 47-49. -236. Valido, A.; Nogales, M. & Medina, F.M. (2003). Molina-Borja, M. & Bischoff, W. (1998). Gallo- Fleshy fruits in the diet of Canarian lizards tia galloti, (Oudart, 1839) Kanareneidechse, Gallotia galloti (Lacertidae) in a xeric habitat In W. Bischoff (ed.). Handbuch der Reptilien of the Island of Tenerife. Journal of Herpetolo- und Amphibien Europas, Band 6, Aula-Verlag, gy 37: 741-747. Wiesbaden, Germany, pp. 287-339. Wittner, G. (2007). The ecology of vertebrate Molina-Borja, M. & Rodríguez-Domínguez, pests and integrated pest management M.A. (2004). Evolution of biometric and life- (IPM), In M. Kogan & P. Jepson (eds) Per- history traits in lizards (Gallotia) from the spectives in Ecological Theory and Integrated Canary Islands. Journal of Zoological System- Pest Management. Cambridge University atics and Evolutionary Research 42: 44-53. Press, Cambridge, UK, pp. 393-410. Pauli, B.D. & Money, S. (2000). Ecotoxicology Wright, S.P. (1992). Adjusted P-values and of pesticides in reptiles, In D.W. Sparling; simultaneous inference. Biometrics 48: 1005- G. Linder & C.A. Bishop (eds.) Ecotoxicology 1013. of Amphibians and Reptiles, SETAC Press, Pensacola (FL), USA, pp. 269–324. Pérez-Padrón, F. & Rodríguez-López, P. (1987). Observaciones sobre la biología, fenología y daños en la vid de dos especies de curcu- liónidos del género Laparocerus en la isla de Tenerife. Boletín de Sanidad Vegetal 13: 361- 364. Roca, V.; Carretero, M.A.; Llorente, G.A.; Montori, A. & Martin, J.E. (2005): Hel- minth communities of two lizard populations (Lacertidae) from Canary Islands (Spain). Host diet-parasite relationships. Amphibia-Reptilia, 26: 535-542. Rodríguez-López, P. (1996). Plagas y enfermeda- des de la vid en Canarias. Gobierno de Cana- rias, Consejería de Agricultura, Ganadería, Pesca y Alimentación, Spain. Russell, R.W. & Overstreet, D.H. (1987). Mechanisms underlying sensitivity to organophosphorus anticholinesterase com- pounds. Progress in Neurobiology 28: 97-129. Siegel, S. & Castellan, N.J. (1988). Nonparamet- ric Statistics for the Behavioral Sciences, 2nd ed.