Interpopulation variation in kairomone use by Cyrba ... - Springer Link

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Ana M. Cerveira • Robert R. Jackson. Received: 30 November 2009 / Accepted: 7 July 2010 / Published online: 10 August 2010. Ó Japan Ethological Society ...
J Ethol (2011) 29:121–129 DOI 10.1007/s10164-010-0233-1

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Interpopulation variation in kairomone use by Cyrba algerina, an araneophagic jumping spider from Portugal Ana M. Cerveira • Robert R. Jackson

Received: 30 November 2009 / Accepted: 7 July 2010 / Published online: 10 August 2010 Ó Japan Ethological Society and Springer 2010

Abstract Geographic variation in a predator’s reliance on kairomones from prey was investigated. The predator studied, Cyrba algerina, is an araneophagic (spider-eating) jumping spider (Salticidae) and the prey were oecobiid spiders (Oecobiidae). There were two study sites (Sintra and Tavira), both in Portugal. Oecobius machadoi was a common oecobiid in Sintra, but no oecobiids were found in Tavira. Staged encounters showed that oecobiid-specific prey-capture behaviour was adopted by the C. algerina in Sintra but not in Tavira. In experiments using a Y-shaped olfactometer, significantly more Sintra C. algerina individuals chose the side with oecobiid odour instead of the blank side when the odour came from females of a sympatric species (O. machadoi), but not when the odour came from O. machadoi males or from females of an allopatric species (O. amboseli). Regardless of whether the odour came from O. machadoi or O. amboseli, the Tavira C. algerina did not choose the odour side significantly more often than the blank side. These findings suggest that, in Sintra, C. algerina is locally adapted to a locally A. M. Cerveira (&)  R. R. Jackson School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand e-mail: [email protected] R. R. Jackson e-mail: [email protected] Present Address: A. M. Cerveira CESAM, Departamento de Biologia Animal, Faculdade de Cieˆncias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal R. R. Jackson International Centre of Insect Physiology and Ecology (ICIPE), Thomas Odhiambo Campus, P.O. Box 30, Mbita Point, Kenya

abundant oecobiid species. Whether this example of geographic variation in kairomone use is a behavioural ecotype or instead an instance of phenotypic plasticity is currently unknown. Keywords Predation  Specialisation  Geographic variation  Chemical cues  Salticid  Spartaeinae  Oecobiidae

Introduction To understand predatory specialisation, examples of within-species geographic variation in behaviour are particularly important because they often suggest specific hypotheses concerning local adaptation (specialisation) to local prey. However, owing to an unfortunate habit of using the term ‘specialised’ when referring to a predator’s natural diet (e.g. Berenbaum 1996), the literature on predatory specialisation is often confusing. The correct terms for natural diet are ‘stenophagic’ for a predator with narrow range of prey types in its natural diet and ‘euryphagic’ for a predator with a wide range of prey types (Huseynov et al. 2008). Determining where a predator lies along a stenophagy–euryphagy continuum is distinctively different from determining whether a predator adopts specialised predatory tactics, with versatile predators (Curio 1976) illustrating this especially clearly. A versatile predator is euryphagic and also highly specialised, each individual having a conditional strategy (Dawkins 1980) based on a repertoire of different prey-specific (specialised) tactics (i.e. a versatile predator is a poly-specialist; WestEberhard 2003). Pronounced predatory versatility and distinctive geographic variation in behaviour may often occur in the same species, with the predator’s conditional strategy

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being locally adapted to the local assortment of available prey (Jackson 1992a, b). Some of the most distinctive examples known of predatory versatility have come from jumping spiders (Salticidae) (Jackson and Pollard 1996), predatory arthropods that are renowned for their unique, complex eyes (Land and Nilsson 2002) and for eyesight based on spatial acuity exceeding that known for any other animals of comparable size (Land 1969; Williams and McIntyre 1980). The evolution of exceptional eyesight has not, however, precluded salticids from being proficient at using other sensory modalities, including chemoreception. In fact, some of the most striking examples of spiders using chemical cues during predatory encounters come from salticids (e.g, Jackson et al. 2005). Here, our objective is to investigate a novel example of distinct geographical variation in a predator’s use of foraging kairomones (see Ruther et al. 2002). ‘Kairomone’ is a term for chemical signals exchanged between members of different species which elicit responses that are beneficial to the receiver and detrimental to the sender (Brown et al. 1970; Dicke and Sabelis 1988). Cyrba algerina, the species we consider here, belongs to the salticid subfamily Spartaeinae. This subfamily is unusual because, although most salticids may prey primarily on insects (Richman and Jackson 1992), specialised araneophagy (i.e. exploiting spiders as prey by using specialised tactics) is prevalent in the Spartaeinae (Su et al. 2007). Although araneophagy has evolved independently in many spider families (Jackson 1992a), the most intricate strategies known by which spiders target other spiders as prey are found in the Spartaeinae (Jackson and Wilcox 1998). As another spider is, for an araneophagic spider, not only potential prey but also a potential predator, the fine tuning of strategies that can be achieved by local adaptation to local prey may also be especially advantageous for spartaeines (Jackson et al. 2002b). Especially distinctive examples of intraspecific geographic variation in predatory strategies, including geographic variation in reliance on foraging kairomones, are known from a particular spartaeine genus, Portia (Jackson and Hallas 1986a; Jackson et al. 2002a). Although we might predict the finding of more examples among the Spartaeinae, no species from other genera have been considered in previous work. While spartaeines are found primarily in the tropics (Wanless 1984a), C. algerina is a species from higher latitudes (Wanless 1984b). With its distribution stretching from the Canary Islands through the Mediterranean Region and into Central Asia, C. algerina also has the distinction of having the widest geographic range known for any spartaeine (Wanless 1984b). This wide geographic range suggests that local adaptation in kairomone-use strategies might be especially well developed in this species.

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In this initial study, we focus specifically on kairomone use in the context of predation by C. algerina on spiders from a particular spider genus, Oecobius (Oecobiidae). The rationale for considering oecobiids in particular is an earlier study in which it was shown that C. algerina from a population in Baku (Azerbaijan) uses specialised preycapture behaviour during encounters with Oecobius maculatus, this being an especially common prey species in Baku (Guseinov et al. 2004). Preliminary field work in Portugal revealed a striking difference between two sites. There was a common oecobiid (O. machadoi) in one site (Sintra), but we failed to find any oecobiids in another site (Tavira). This was the rationale for a specific prediction: that the predatory strategy of the Sintra population, but not that of the Tavira population, includes oecobiid-specific predatory tactics. First, we provide a synopsis of the prey-capture behaviour adopted by the Sintra and the Tavira C. algerina during encounters with oecobiids. This synopsis is qualitative, as our primary objective is to compare how individuals from the two Portugal populations respond to olfactory cues from oecobiids. In the earlier research on the Baku C. algerina, olfaction was not considered. However, field observations suggest that C. algerina forages especially under or on the sides of stones on the ground (Jackson and Hallas 1986b; Jackson 1990; Jackson and Li 1998; Guseinov et al. 2004), this being a microhabitat where ambient light levels are probably low in comparison to the sunlit habitats most often associated with salticids (Richman and Jackson 1992). Predation under dim light suggests that C. algerina may be a salticid for which reliance on olfactory cues from prey is especially important. Secondly, we investigate the role of oecobiid olfactory cues in the predatory strategies of the two C. algerina populations from Portugal. Our hypothesis is that C. algerina’s responsiveness to species-specific oecobiid odour (i.e. volatile compounds derived from oecobids) is subject to within-species geographic variation. In particular, we predict that the C. algerina from Sintra, but not the C. algerina from Tavira, responds to the odour of the sympatric oecobiid species, O. machadoi.

Materials and methods Our two study sites (Sintra and Tavira) have a Mediterranean climate (summer hot and dry, winter cool and wet). The Tavira site is located in southeast Portugal (37°80 N, 7°410 W; 107 m above sea level) and the Sintra site is located in west central Portugal (38°510 N, 9°200 W; 60 m above sea level). Typical habitats in both sites were clearings with rocky ground and low vegetation. C. algerina was usually found

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Table 1 Elements of behaviour seen when Cyrba algerina encounters prey (for details, see Jackson and Hallas 1986b; Jackson 1990) Element of behaviour

Description

Crouch

Body lowered, with ventral surface almost touching the substrate

Forward-hunched legs

Legs I–III highly flexed, with femora extended ca. 90° to side (patella and tibia held straight forward, parallel to longitudinal axis of cephalothorax). Legs IV extended and angled straight back. Posture usually adopted when crouching

Leap Palp flutter

Sudden forward movement of body while rapidly extending legs IV (all legs leave substrate) Palps waved very rapidly up and down at low amplitude

Palp pluck

Three modal forms (up-and-down, forward-and-backward, rotary forward-and-backward), with amplitude and speed of each varying considerably and with frequent changes from one modal form to another

Probe

Backward and forward movement of palps while in contact with silk

Swim wave

Legs I and II move together up and to the side and then, without pausing, more slowly down and inward (tarsi of both legs usually contacting substrate at end of downward motion

under or on the sides of stones (10–60 cm long) that were lying loose on the ground or partly embedded in soil. Individuals of C. algerina were collected in the field from the two study sites. The prey we used in experiments was Oecobius machadoi [sympatric with C. algerina in Sintra, but never found over three consecutive field seasons (spring) in Tavira], and O. amboseli (an East African species not known to be sympatric with any natural population of C. algerina). Although it may be exceedingly difficult to determine that a spider species is absolutely absent in a field site, our experience in the field suggests at least that oecobiids in Tavira, compared with Sintra, are rare in the microhabitat where we found C. algerina. Individuals of O. machadoi were collected from the field (Sintra), and O. amboseli came from a laboratory culture established from specimens collected in western Kenya. In the laboratory, we adopted the standard maintenance procedures, rearing-cage design and terminology that have been used in numerous earlier salticid studies (e.g. Jackson and Hallas 1986a; Guseinov et al. 2004). All testing was carried between 0900 and 1800 hours. All test spiders used were adult C. algerina females and no individual test spider was used more than once in the same experiment. Each individual of C. algerina was kept individually in an enriched environment (see Carducci and Jakob 2000), a spacious cage with a cardboard harmonium placed inside for nest building, under a 12–12 h dark–light regime (lights on at 0700 hours). C. algerina was maintained on a mixed diet of spiders (juvenile Dolomedes minor and Pardosa sp.) and insects (fruit flies, Drosophila melanogaster). Oecobiids were kept in communal cages (mating status unknown) and were fed insects alone (fruit flies). Humidity and drinking water was provided through water-logged cotton rolls. For standardising hunger level before the beginning of experiments, each individual of C. algerina was subjected to a 5-day fast. All field collected spiders used were tested after a minimum acclimation 30-day period.

Staged predator–prey encounters in the laboratory Here, our goal was simply a qualitative characterisation of prey-capture behaviour by which we made broad comparisons between the two Portugal populations and with the previously studied Baku C. algerina (see Table 1 for definitions of elements of behaviour; for details, see Jackson 1990). We staged two types of encounters between C. algerina and oecobiids: away-from-nest and in-nest encounters. For away-from-nest encounters, one oecobiid was put in a transparent plastic Petri dish (diameter 85 mm, height 12.5 mm) and then, 30 min later, a test spider (C. algerina) was introduced. This corresponded to the way encounters with oecobiids outside nests were staged in the earlier study of the Baku C. algerina (Guseinov et al. 2004). However, for staging encounters at nests, we particularly wanted to observe C. algerina’s initial reaction upon detecting an oecobiid inside a nest. Preliminary observations showed that, when housed in Petri dishes, the oecobiid usually built its nest along the side of the dish. This was problematic because C. algerina, being predisposed to walk or run rapidly along the sides of the Petri dish, often found the oecobiid’s nest almost immediately, and apparently by chance, after entering the Petri dish. To avoid having this happening, we used a specially designed testing arena for staging in-nest encounters. This testing arena forced the oecobiid to build its nest away from the side of the Petri dish. The arena was made of acrylic plastic and consisted on a circular base (diameter 85 mm) with a small disc (diameter 20 mm, height 5 mm) affixed to the top. We created a crevice in the disc by removing a slice equal to about 25% of the disc’s area. We sanded the perimeter of the disc, leaving the crevice as the only space where the oecobiid would be inclined to build a nest (Fig. 1). The disc was positioned with its closest side 15 mm away from the edge of the base and with the crevice being oriented inward (towards the centre of the arena).

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Fig. 1 Arena to test Cyrba algerina with oecobiids. Oecobiids were induced to build a nest against the crevice by surrounding the experimental arena with water. Before encounters, the base was covered with the lid of a Petri dish

An oecobiid was placed in the arena 1 week before testing began, during which time it built a nest in the crevice (no food provided). Preliminary observations showed that oecobiids were averse to contacting water and this aversion gave us a method for confining oecobiids to the arena (i.e. the arena was placed in the centre of a wider dish and surrounded by water). Before staging an encounter, the base was removed from the water and covered by the lid of a Petri dish (diameter 85 mm, height 12.5 mm). The test spider (C. algerina) was introduced 30 min later. Before staging an encounter, the test spider was taken into a transfer tube (transparent plastic, diameter 8 mm, length 20 mm, two ends plugged with corks). After a 5-min acclimation period, the cork was removed from one of the tube’s ends and this end was positioned tightly in a hole on the side of the Petri dish lid. The hole was oriented toward the crevice (i.e. the test spider faced directly toward the oecobiid nest as it entered the arena). The test spider usually walked spontaneously out of the tube and into the arena. However, on the rare occasions when a test spider did not enter the arena within 10 min, the other cork was removed and a soft brush was slowly inserted, prodding the test spider into the arena. Testing began when the test spider entered the arena and ended when either the test spider captured the oecobiid or, if the oecobiid was not captured, when 90 min had elapsed. About equal numbers of encounters were staged between the two C. algerina’s populations and O. machadoi and O. amboseli (Sintra: n = 19; n = 20, respectively; Algarve: n = 21; n = 20, respectively). Olfactometer testing As in numerous earlier salticid studies (e.g. Jackson et al. 2005), we used a Y-shape olfactometer (Fig. 2) with airflow adjusted to 1500 ml/min (Matheson FM-1000 flowmeter). There was no evidence that this airflow setting impaired locomotion or had any adverse effects on the test spider’s behaviour. Air was pushed by a pump from a tap

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Fig. 2 Y-shape olfactometer (from Jackson et al. 2002a) (not drawn to scale). f Flowmeters, sc stimulus chamber, cc control chamber, b opaque barrier to preclude Cyrba algerina seeing prey (i.e. odour source), sa stimulus arm, ca control arm, ta test arm, n metal grill to block C. algerina’s access to test arm during acclimation period, hc holding chamber

through two separate flowmeters into two chambers (control and experimental) and from each chamber into two choice arms (i.e. the arms of the Y). Air from each choice arm then converged and moved into the test arm (i.e. the stem of the Y). There were two types of olfactometer tests. Both chambers were empty in blank tests, the objective of these tests being to determine whether there was a left–right bias when C. algerina was in the olfactometer. In prey tests, six adult oecobiids of the same sex and species (O. machadoi or O. amboseli) were placed in one chamber (the stimulus chamber) while the other chamber (the control chamber) was left empty. The oecobiids were placed in the stimulus chamber 30 min before testing began. There were no problems with keeping more than one oecobiid together in the experimental chamber, as individuals of both oecobiid species are often found aggregated in nature and preliminary work showed that they were not prone to cannibalism or aggression. For each trial, we decided at random whether the stimulus chamber that contained the odour source would be on the left or the right.

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The test spider could not see the oecobiids in the stimulus chamber as there was an opaque barrier between the choice arms and the chambers. Test spiders were placed in a holding chamber (connected to the test arm) and kept there for 2 min (acclimation period). A removable metal grill, positioned in a slit in the chamber roof, blocked the test spider’s access to the test arm. After the 2-min acclimation period, the grill was gently lifted, allowing the test spider to initiate the test by entering the test arm. Whenever a test spider rushed out of the holding chamber and immediately entered one of the choice arms, testing was aborted and the test spider was not used again until the following day. The olfactometer was cleaned between tests with 80% ethanol, followed by distilled water, and then dried. When using other salticid species in olfactometer experiments (e.g. Jackson et al. 2005), the criterion for recording that a test spider had made a choice was seeing it enter one of the choice arms and remain there for 30 s. However, C. algerina’s demeanor in the olfactometer was strikingly different from that of the salticids used in earlier studies. C. algerina was disinclined to remain in the first choice arm it entered and, unlike other salticids that have been studied, often entered and left both arms repeatedly before eventually settling. Taking this into consideration, we defined test spider choice in the present study as the arm in which the test spider spent the most time during a 20-min period. A score was obtained for each individual by subtracting the time spent in the stimulus arm from the time spent in the control arm. The spider’s choice was analysed using chi-square tests for goodness of fit (null hypothesis: no tendency to choose one arm more often than the other). Scores were analysed using Wilcoxon signed-rank tests (null hypothesis: time spent in one choice arm equal to time spent in the other arm; i.e. scores were zero). For between-prey and betweenpopulation comparisons on the spider’s choice, we used chi-square tests for independence (see Sokal and Rohlf 1995). Score differences were analysed using two-way independent Student’s t tests. Bonferroni adjustments (table-wide) for repeated analysis of datasets did not change any conclusions concerning significant differences between datasets.

Results Predator–prey encounters In the absence of nests, the prey-capture sequences observed were similar to those described in earlier studies in which encounters were staged between C. algerina and small cursorial spiders (Jackson and Hallas 1986b; Jackson

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1990; Jackson and Li 1998; Guseinov et al. 2004). Both the Sintra and the Tavira C. algerina stalked stationary oecobiids and chased after moving oecobiids. When close, C. algerina lunged at and captured the oecobiid. No conspicuous differences between the Sintra and the Tavira C. algerina were evident during encounters with either oecobiid species outside nests. However, our qualitative synopsis suggests that the Sintra differs from the Tavira C. algerina when oecobiids are inside nests. While swim waving and fluttering its palps (Table 1), the Sintra C. algerina typically approached the oecobiid nest slowly and then, when only a few body lengths away, stopped and crouched directly in front of the nest. After a variable interval, the Sintra C. algerina, while remaining in the crouched posture, resumed slowly approaching the nest, all the while slowly swim waving and fluttering its palps. Sometimes, the Sintra C. algerina slowly moved sideways so that it approached the oecobiid head on. When the nest was only a few millimetres away, the Sintra C. algerina stopped and remained quiescent for a highly variable interval. Next the Sintra C. algerina either: (1) turned and walked slowly away from the nest; (2) walked on the nest or moved its legs into the forwardhunched posture; or (3) contacted the nest by softly plucking on the silk and then lunged at the oecobiid’s nest. After lunging, the Sintra C. algerina often resumed probing or softly plucking on the silk. Subsequently, in highly variable sequences, the test spider repeatedly plucked, probed and lunged at the nest. When the oecobiid eventually responded by leaving the nest, the Sintra C. algerina used one of the following capture methods: (1) lunged at the oecobiid and captured it as it left the nest; (2) after remaining quiescent at the nest, captured the oecobiid upon its return; (3) chased after, overtook and captured the fleeing oecobiid; or (4) watched the fleeing oecobiid, and then stalked and captured it. The predatory sequences typical of the Sintra C. algerina were not often observed when encounters were staged between Tavira C. algerina and either species of oeobiid. Usually the Tavira C. algerina showed no overt response to oecobiids in nests and capturing an oecobiid was rare. Olfactometer testing No left–right bias was evident for either the Tavira (v2 = 0.73, df = 1, P = 0.39, n = 22; Fig. 3) or the Sintra (v2 = 1.09, df = 1, P = 0.30, n = 23; Fig. 4) C. algerina, nor did the spiders from Tavira or Sintra spend significantly more time in either arm in the blank tests (Fig. 5). Additionally, no significant differences were found between the Tavira and the Sintra C. algerina concerning the spider’s choice (test of independence v2 = 1.79, df = 1, P = 0.18, n = 45) or the time spent in either arm

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Fig. 3 Choice in olfactometer tests using Tavira Cyrba algerina. Blank tests: no odour present. Prey tests: odour from Oecobius machadoi in stimulus arm. F Female, M male. Data compared using chi square tests for goodness of fit. NS P [ 0.05

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Fig. 6 Scores from testing Tavira and Sintra Cyrba algerina in olfactometer tests using odour from female Oecobius machadoi. Each individual provided a score (time spent on left arm minus time spent on right arm). Sintra, but not Tavira C. algerina, spent significantly more time on the stimulus arm than on the control arm (Wilcoxon signed-rank tests: Tavira, P = 0.28, n = 28; Sintra, P \ 0.01, n = 28)

** Stimulus Control NS

NS

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NS

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Fig. 4 Choice in olfactometer tests using Sintra Cyrba algerina. Blank tests: no odour present. Prey tests: odour from Oecobius machadoi and O. amboseli in stimulus arm. F Female, M male. Data compared using chi square tests for goodness of fit. NS P [ 0.05, **P \ 0.05 5 Sintra Tavira

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Fig. 5 Scores from testing Tavira and Sintra Cyrba algerina in blank olfactometer tests (no odour source present). Each individual provided a score (time spent on left arm minus time spent on right arm). C. algerina did not spend significantly more time on either of the two choice arms (Wilcoxon signed-rank tests: Tavira, P = 0.24, n = 22; Sintra, P = 0.26, n = 22)

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(two-sample Student’s t test, t = 0.20, df = 43, P = 0.85) in the blank tests. The number of Sintra C. algerina females that chose the stimulus arm was significantly higher than the number that chose the control arm when tested with sympatric (Sintra) oecobiid females (test of goodness of fit, O. machadoi, v2 = 9.14, df = 1, P = 0.002, n = 28, Fig. 4), but not when tested with allopatric (Kenya) oecobiid females (O. amboseli, v2 = 0.39, df = 1, P = 0.53, n = 23), or with sympatric (Sintra) oecobiid males (O. machadoi, v2 = 0.04, df = 1, P = 0.84, n = 25). Similarly, Sintra C. algerina also spent significantly more time in the stimulus arm than in the control arm (i.e. they had higher scores) when tested with sympatric (Sintra) oecobiid females (Fig. 6), but not when tested with allopatric (Kenya) oecobiid females (Fig. 7), or with sympatric (Sintra) oecobiid males (Fig. 8). The Sintra C. algerina chose the odour of O. machadoi females significantly more often than the odour of O. machadoi males (test of independence, v2 = 4.16, df = 1, P = 0.04, n = 53). However, when C. algerina’s scores were analysed, no significant differences were found for the odour of female versus male O. machadoi (twosample Student’s t test, t = 1.78, df = 51, P = 0.08). The number of Tavira C. algerina that chose the arm of the olfactometer containing odour from either of the oecobiid species (both allopatric) was not significantly different from the number that chose the control arm (test of goodness of fit, O. machadoi females: v2 = 1.29, df = 1, P = 0.26, n = 28; O. amboseli females: v2 = 0.80, df = 1, P = 0.37, n = 20; Fig. 3). Similarly, time spent in the stimulus arm when using either O. machadoi or O. amboseli females was also not significantly different

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Fig. 7 Scores from testing Tavira and Sintra Cyrba algerina in olfactometer tests using odour from female Oecobius amboseli. Each individual provided a score (time spent on left arm minus time spent on right arm). Both Sintra and Tavira C. algerina, did not spend significantly more time on either of the choice arms (Wilcoxon signed-rank tests: Tavira, P = 0.72, n = 20; Sintra, P = 0.75, n = 28)

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Fig. 8 Scores from testing Sintra Cyrba algerina in olfactometer tests using odour from male Oecobius machadoi. Each individual provided a score (time spent on left arm minus time spent on right arm). Sintra C. algerina, did not spend significantly more time on either of the choice arms (Wilcoxon signed-rank tests, P = 0.84, n = 25)

from time spent in the control arm (i.e. scores were not significantly different; Figs. 6 and 7). When O. machadoi females (common in Sintra but not found in Tavira) were the odour source, the Sintra C. algerina chose the stimulus arm significantly more often and spent significantly more time in the stimulus arm (i.e. had higher scores) than the Tavira C. algerina (test of independence, v2 = 8.93, df = 1, P = 0.003, n = 56; twosample Student’s t test, t = 2.56, df = 54, P = 0.01). However, when O. amboseli females (i.e. the oecobiid species allopatric to both C. algerina populations) were the odour source, the choice made and the time spent in either arm (i.e. scores) by the Sintra C. algerina were not significantly different from Tavira C. algerina (test of independence, v2 = 1.17, df = 1, P = 0.28, n = 43; twosample Student’s t test, t = 0.27, df = 41, P = 0.98).

Despite this initial study being limited to only a qualitative synopsis of prey-capture behaviour, our observations suggest that local prey diversity has led to interpopulation variation in prey-capture behaviour (i.e. the Sintra C. algerina behaved in a way that is strikingly different from how the Tavira C. algerina behaved during encounters with oecobiids in nests). On the whole, the prey-capture behaviour adopted by the Sintra C. algerina was similar to that described earlier for the Baku C. algerina (Guseinov et al. 2004). The Sintra C. algerina approached the oecobiid nest slowly and then, by making signals on the nest silk, enticed the oecobiid out of the nest. Using this basic tactic, individuals from the Sintra population, like individuals from the Baku population, were highly effective at capturing oecobiids either as or after they fled from the nest. Remarkably, the Tavira C. algerina showed little in the way of a response to oecobiid’s nests. There was nothing to suggest that the Sintra C. algerina adopted different prey-capture behaviour depending on whether the oecobiid species encountered was the sympatric or the allopatric species, but distinctive specificity was revealed by the findings from the olfactometer experiment. Regardless of which of the two oecobiid species (sympatric vs. allopatric) provided the odour, the number of Tavira C. algerina individuals that chose the side with oecobiid odour was not significantly different from the number that chose the blank. However, there was evidence that the Sintra C. algerina was attracted to the oecobiid odour, but only when the oecobiids were females of the sympatric species (O. machadoi). The two oecobiid species are similar in appearance and, using vision alone, the Sintra C. algerina may categorise these two species as belonging to a single prey type, ‘‘oecobiid’’. However, for the Sintra C. algerina, the distinction between O. machadoi and O. amboseli seems to be important when relying on odour cues alone. The sympatric, but not the allopatric, oecobiid seems to be categorised by odour as prey. As we did not control for potential effects of the oecobiid’s field diet, we cannot rule out the possibility that diet-induced odour, instead of oecobiid species-specific odour, accounts for our findings when using the olfactometer. However, as we standardised the feeding regime in the laboratory, any such effect of diet on odour would only be evident if it persisted after spiders were taken into captivity and put on the standardised diet. Therefore, although persisting effects from the field are conceivable, they seem unlikely. The odour that affects Sintra C. algerina appears to be very specific. Only the odour from O. machadoi females seems to affect the behaviour of the Sintra C. algerina;

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odour from O. machadoi males had no significant effect on the Sintra C. algerina during the olfactometer experiment. This is of interest because, in other research (unpublished), we found that the odour of O. machadoi females attracts O. machadoi males, but neither the males nor the females of O. machadoi appear to be influenced by the odour of conspecific males. This suggests that, by eavesdropping on a pheromonal communication system used for mate attraction by O. machadoi females, the Sintra C. algerina exploits its prey’s sex pheromones to its own advantage. In other words, a blend of volatile compounds that normally functions as pheromones for O. machadoi appears to function as a foraging kairomone for the Sintra C. algerina. Other spiders are known to use foraging kairomones, with one of the best-known examples coming from a lycosid species, Schizocosa ocreata. Females of this species detect the presence versus absence of substratumborne chemical cues (silk and faeces) left by prey and adjust the time they spend in a foraging patch accordingly (Persons and Uetz 1996). Among salticids, Habrocestum pulex, an ant-eating salticid, has been shown to detect antderived chemical traces on the soil (Clark et al. 2000b). However, as a guide for future research on C. algerina, previous research on the Queensland population of Portia fimbriata might be particularly instructive. For individuals from this population, but not for individuals from any other population of this or any other Portia species that has been studied, other salticids are a category of prey against which a particular tactic (called ‘‘cryptic stalking’’) is deployed (Jackson and Blest 1982; Harland and Jackson 2004). Salticids are a special prey category because of their exceptional eyesight and cryptic stalking (approaching from behind, freezing when faced and the adoption of a special posture that masks the outlines of P. fimbriata’s legs and palps) is a tactic by which the Queensland P. fimbriata seems to compensate for the acuity of salticid vision. Although the Queensland P. fimbriata deploys cryptic stalking against salticids in general, there is more specificity in the use of foraging kairomones. Jacksonoides queenslandicus is the most abundant salticid species in the Queensland habitat (Jackson 1988) and the Queensland P. fimbriata responds to silk-associated and olfactory kairomones uniquely from J. queenslandicus (Jackson et al. 2002a). In the presence of foraging kairomones from J. queenslandicus, the Queensland P. fimbriata adopts the posture specific to cryptic stalking and shifts selective visual attention to the optical cues by which it identifies J. queenslandicus (Jackson et al. 2002a). These kairomones also stimulate the Queensland P. fimbriata to perform undirected leaps (erratic leaping with no particular target being evident), behaviour that has been

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shown experimentally to trigger an orientation response by J. queenslandicus, with this response revealing J. queenslandicus’ location to P. fimbriata (Clark et al. 2000a). Foraging kairomones, by providing forewarning of the other spider’s presence, might be especially advantageous for spiders that prey on other spiders. Often, kairomones may ensure that the araneophagic species can prepare for an eminent encounter with dangerous prey. With C. algerina, an additional advantage may apply. The microhabitat in which C. algerina normally encounters oecobiids (undersides of stones) may often preclude rapid, accurate prey identification by sight alone. For C. algerina, preying on spiders under dim ambient light conditions may make reliance on foraging kairomones from common prey an especially important complement to optical prey-identification cues. Our findings suggest that, for C. algerina, as for P. fimbriata, foraging-kairomone use is subject to geographic variation. By using F2 and F3 generation individuals in the laboratory, with none of these individuals or their parents having experienced prior exposure to the prey with which they were tested, research on Portia (Jackson and Carter 2001; Jackson et al. 1998, 2002a, b; Jackson and Wilcox 1990; Li and Jackson 2003) has ruled out maternal effects and previous experience with the prey as likely factors accounting for the observed interpopulation variation in prey-specific tactics and foraging kairomone use. This implied that the divergent strategies of the different populations are behavioural ecotypes based on adaptive fine tuning to local prey (i.e. each population has a different genotype adapted to particular local conditions; see Turesson 1922; Foster 1999). Using laboratory-reared test spiders was not practicable in this initial study of C. algerina from Portugal and, as the individuals of C. algerina that we used in experiments were collected from the field, we cannot rule out maternal effects or the possibility that prey-capture behaviour and response to odour had been shaped by the test spider’s previous experience with oecobiids (i.e. we cannot rule out the possibility that, for C. algerina, geographic variation is the result of phenotypic plasticity instead of ecotypic variation). Distinguishing between ecotypic variation and phenotypic plasticity (West-Eberhard 2003) as potential explanations for the interpopulation variation is a priority for future research on C. algerina in Portugal. Acknowledgments For a Doctoral Scholarship (SFRH/BD/8311/ 2002) to A.M.C. through the European Regional Development Fund, we thank the Fundac¸a˜o para a Cieˆncia e a Tecnologia. We also thank the Royal Society of New Zealand for funding to R.R.J. (a grant from the Marsden Fund and a James Cook Fellowship) and three anonymous reviewers for comments on the manuscript.

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