ASIAN J. EXP. BIOL. SCI. VOL 3 (1) 2012: 105 - 109
© Society of Applied Sciences
ORIGINAL ARTICLE
Prey Preferences of Evarcha Flavocincta and Plexippus Petersi (Araneae: Salticidae) from Malaysia Maimusa A. H., Rabiu S., Inusa M. N. and Grandawa M. M. Department of Science Laboratory Technology, Mai Idriss Alooma Polytechnic P. M. B. 1020, Geidam, Yobe State, Nigeria.. ABSTRACT Two jumping spiders, Plexippus petersi and Evarcha flavocincta (Araneae: Salticidae) were chosen for a test of prey preference from several species of spiders commonly found in University Putra Malaysia (UPM) Serdang, Malaysia campus. Test spiders were maintained in captivity on diet of early stage larvae of Tenebrio molitor (mealworm beetle) and midges, Chironomus sp. For testing, adult mosquito, Aedes albopictus (Skuse), fruit flies (Drosophila melanogaster) and rice weevil (Sitophilus oryzae) were used. Two types of tests using living prey were employed, i.e. simultaneous-presentation tests (two types of prey provided at the same time) and alternate-day tests (different types of prey provided on successive days). All level of significance was determined at = 0.05 using a statistical program with Chi-square t-Test Goodness of Fit and Mc Nemar test. The results shows that, well-fed (last meal 7 days before testing) and starved (last meal 14 days before testing) test spiders of each species took Ae. albopictus mosquito more often than other insects in both alternate-day and simultaneouspresentation tests using living prey (P < 0.05). It was also revealed that the preference of P. petersi for Ae. Albopictus mosquito over other insects offered is weaker than that of E. flavocincta. Larger salticids showed quick response; while attack was quite delayed by the smaller ones and with some difficulties. There was similar preference by both test spiders when well-fed and starved. Keywords: Aede albopictus, jumping spiders, prey, preference.
INTRODUCTION Jumping spiders belonging to the Family Salticidae has worldwide distribution. About 5,000 species (roughly 7% of the total number of spider species in the world) are known throughout the globe, mostly in the tropical regions. When viewed from above, the eyes of the jumping spiders are arranged in three pairs of row: two in the front, tiny ones in the middle and another pair further back. This arrangement of eyes allows jumping spiders to enjoy almost 360° field of vision [1]. Jumping spiders possess highly elaborate vision-guided predatory strategies ever observed in any animal of equal size [2]. Preference does not simply mean knowing predator's natural diet, or the use of prey-specific preycapture behaviour. Instead, it requires evidence that the predator can distinguish between different types of prey and choose to take one rather than the other [3]. East African jumping spider, Evarcha culicivora had chosen, as preferred prey, female mosquitoes that have had recent blood meals [4]. In a laboratory experiments [5 and 6], Cyrba algerina and four species of Portia (P. africana, P. fimbriata, P. labiata and P. schultzi) have shown preference to web-building spiders over insects. [7] Reported that, Phaeacius malayensis, a spartaeine jumping spider took other spiders (salticids or hunting spiders) more often than insects. In a study in rubber estate [8] found Heteropoda venatoria (Sparassidae) playing the role of predator of Aedes albopictus. Five species of spider (Passiena sp., Leucauge grata, Heteropoda venatoria, Cyclosa insulana and
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Nephila maculata) were also serologically identified and found to be acting as predators of dengue fever vector, Ae. albopictus [9]. It was suggested in an optimal foraging theory that, when well fed (i.e. when prey are abundant), predators will primarily exercise preference [10]. A study indicates that, eight species of myrmecophagic salticids showed preference for ants on 14-day fasts [11]. For Cyrba algerina and Portia spp. and for another 12 myrmecophagic species, prey preferences appeared to be unaltered by 14-day fasts [6]. However, after 21-day fasts these species no longer shows preferences. The objectives of this study were, firstly, to investigate whether Evarcha flavocincta and Plexippus petersi prefer Aedes albopictus or other insects with which it was paired as prey. Secondly, whether or not hunger state influences the preference for the prey.
MATERIALSAND METHODS Collection and maintaining spiders Spiders were collected from non-residential areas of the University Putra Malaysia, UPM that include; the Agricultural Conservatory Park (ACP), Rubber Plantation, Pine Plantation and some areas of the Faculty of Design and Architecture. Two species of spiders, Evarcha flavocincta commonly known as horned grass jumper and Plexippus petersi or larger housefly catcher were used for this study and kept in captivity. The rearing environments were similar to those described by [1 and12]. These were plastic containers (14cm height x 8cm diameter) stopped with ball of cotton wool and has been wetted daily. The spiders were maintained by feeding each to satiation twice a week on young larvae of Tenebrio molitor (mealworm beetle) and adult midges, Chironomus sp. Rearing and maintaining of test insects Ae. albopictus mosquitoes cultures were initiated from larvae collected from the same sites with spiders. The first two and the last two instars were fed with ox-liver powder and TetrababyR commercial fish feeds respectively. The surface of the water was skimmed off occasionally with a piece of paper to remove the surface scum formed. The pupae were then transferred into metal trays (800cm3) containing aged tap water and placed in cages (40cm x 35cm x35cn). After emergence, the adults were maintained with glucose (10%) solution (added with little vitamin B) provided on wick. Rats (in a small restraining cage) were occasionally introduced into the mosquito cages as blood source for the female mosquitoes. Small ceramic bowls (250cm3) containing aged tap water with filter paper cones were used for oviposition. Eggs on the filter papers were collected after three to five days intervals and hung to dry and then hatched when needed. Fruit flies (Drosophila melanogaster) were laboratory cultured and maintained in agar media containing meshed ripe banana and yeast. Sitophilus oryzae were laboratory maintained in rice grain in a container.All rearing and subsequent preference test were carried out in laboratory condition with temperature 26.5o C, relative humidity 67% and light intensity 165 Lux. Prey preference tests Simultaneous-presentation tests This involves presentation of two types of prey at a time. A test began when a salticid was put into a test box containing two prey items (one of each of the two types) and ended when the spider took one of the two (i.e. it was not allowed to take both). Alternate-day tests This involves presentation of one individual of one prey type at a time. An individual of one type of prey was provided to test spider on one day, then an individual of the other type provided on the following day. Each salticid was used in a pair of tests. Half of test spiders of each species were tested first with one of the three types of prey; while the other half was tested first with the other type of prey. Each salticid was assigned to one of the two groups randomly. Laboratory procedures A total of 40 spiders, 20 each of P. petersi and E. flavocincta were used as sample size. Body length and weight for the large, medium and small sized Plexippus petersi (measured from head's anterior end to the abdomen's posterior end) was 8-9mm, 5-6mm, 3-4mm and about 0.89mg, 0.29mg 0.13mg respectively. Body length and weight for E. flavocincta (as categorized above for P. petersi) was 8-10mm 6-7mm, 4-5mm and about 0.92mg, 0.33mg, 0.16mg respectively. All testing were carried out between 0900h and 1700h in laboratory. For testing, adult mosquito, A. albopictus (Skuse), fruit flies (D. melanogaster) and rice weevil (S. oryzae) were used. Body length of all fruit flies, rice weevil and mosquitoes used for testing (measured from the head's anterior end to the abdomen's posterior end) was 2-3 mm, 3-4 mm, 3-5 mm and body weight about 0.03 mg, 0.09 mg and 0.04 mg respectively. Simultaneouspresentation tests (i.e. two types of prey provided at the same time) and alternate-day tests (different types of prey provided on successive days) were carried out. Different individual test spider was used in each test of any one type. 106
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Species used as prey in preference testing were representative of natural prey of the test spiders and for any individual salticid, the species of prey used for maintaining were always different from the species used in preference testing. Both spiders were tested when 'well fed' (last meal 7 days before testing) and when starved (last meal 14 days before testing) as recommended [13]. All spiders tested were adults (body length 3 - 9mm). All preys were between 20% and 30% of the body size of the spider with which they were tested. Tests of prey preference As in earlier study [13], simultaneous-presentation test and alternate-day test were carried out using living preys. Well-fed and starved adults of P. petersi and E. flavocincta were tested. Ten testing boxes made from plastic (9cm x 6cm) similar in size to individual cell in testing box [14] were used. Using these apparatuses, 10 salticids could be tested at a time. The top of the apparatuses was opaque, but the sides were transparent. However, a salticid in one test box could not see into neighbouring boxes as they were screened and not closely placed. During simultaneous presentation test, a test spider (an individual of one of the two species) was put in the test box. The preys were already in the box 5-10 minutes before a test spider was allowed to enter and no prey was observed attacking one another, else the test was aborted. To begin testing, once the test spider was in the box, the plugging cotton ball was replaced. Tests ended when the test spider had captured either of the two preys or the 15 minutes dateline is due. However, if the 15 minutes dateline elapsed and a test spider was still pursuing a prey, the observation continued until end of the sequence. Unless 4 days of unsuccessful testing elapsed, a spider from aborted test was retested up to 3 times a day and on subsequent days until completion of successful test. The criterion for recording 'choice' was met when a spider stalk a prey or else leapt on to it. During alternate-day tests, preys were in the test box 5 10 minutes before a test spider was allowed to enter. Each individual test spider was given access to one type of prey on one day and that of the other type on the following day. Each salticid was assigned to one of the two groups in a randomized design. Data analysis Data were analysed with Chi-square Tests of Goodness of Fit for simultaneous presentation tests in which one type of prey was consistently taken and Mc Nemar for significance of changes in the alternate day tests [15]. All levels of significance were determined at a = 0.05.
RESULTS In both simultaneous-presentation and alternate-day tests using living prey, both well-fed and starved of each species of test spiders (P. petersi and E. flavocincta) attacked mosquitoes (Ae. albopictus) more often than either fruit flies or 2 rice weevils (χ = 11.4; P = 0.003). The attack was also higher on fruit flies than rice weevils (Table 1 and 2). Table 1: Prey preference of test spiders (Well fed & starved) when two living prey are presented simultaneously. Test spider ? P. petersi E. flavocincta P. petersi E. flavocincta
Hunger state (Well-fed1) (Well-fed1) (Starved2) (Starved2)
Ae. albopictus (Prey1) versus fruit fly (prey2)
15 12 16 17
P. petersi E. flavocincta P. petersi E. flavocincta
(Well-fed1) (Well-fed1) (Starved2) (Starved2)
fruit fly (Prey1) versus rice weevil (prey2)
14 15 19 16
2 3 1 3
4 2 0 1
Ae. albopictus (Prey1) versus rice weevil (prey2)
17 14 18 18
1 4 1 2
2 2 1 0
P. petersi (Well-fed1) E. flavocincta (Well-fed1) P. petersi (Starved2) E. flavocincta (Starved2)
Prey used
Chose Prey 1
Chose Chose Test of Prey 2 Neither goodness of f t 4 1 P < 0.05 8 0 NS 4 0 3 0 P < 0.05
P < 0.05
P < 0.05
1
Well-fed = Last fed 7 days before testing 2 Starved = Last fed 14 days before testing nd rd Data in 2 and 3 columns used in these tests
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The rate at which test spiders ate each type of prey was not affected by the ability of the spiders to capture different types of prey as almost always the attacked prey was also eaten. The first prey eaten or attacked was considered spider's 'live-prey choice'. As for the effect of hunger on preference, both well-fed and starved test spiders had almost similar preference in all types of test. However, E. flavocincta was more aggressive, quicker in stalking prey and select more mosquito than P. petersi. Larger salticids showed quick response; while attack was quite delayed by the smaller ones and with some difficulties. In both tests, preference for size was not investigated and tests spiders were not distinguished into male and female. Table 2: Test spiders tested with living prey on alternate days est spider
Hunger state
Well-fed1 Starved2 Well-fed1 Starved2 E. flavocincta Well-fed1 Starved2 Well-fed1 Starved2
P. petersi.
Mosquito
Other insect
Ae. albopictus
Fruit fly Rice weevil Fruit fly Rice weevil
Ate Ate other mosquito insect only only 11 4 13 3 17 1 16 1 13 1 15 0 16 1 17 1
Ate both 5 4 2 2 5 5 2 2
Ate McNemar neither test3 0 0 0 1 1 0 1 0
P < 0.05
1
Well-fed = Last fed 7 days before testing 2 Starved = Last fed 14 days before testing 3 Data in column 5 & 6 only used in these tests
DISCUSSION The choice of species of spider for the preference tests was based on its commonness and abundance during the collection of spider in the areas. Both E. flavocincta and P. petersi chose Ae. albopictus significantly more often than either of the prey with which it was paired. It was found in Kenya (East Africa) that, another salticid, E. Culicivora, not only preferred mosquito but uniquely chose engorged female Anopheles mosquitoes [13]. However, in this study, both test spiders of all sizes (large, medium and small) selected Ae. albopictus more often regardless of sex, size and gut contents. Infrequent in choosing rice weevil (S. oryzae) could have been due to the characteristic hard exoskeleton of the organism which sometimes appeared difficult for the spider to pierce. On the other hand, mosquitoes and fruit flies appear to have no comparable hard skins which make it difficult for the salticids to attack. Similarly, most salticids are polyphagic predators feeding on soft-bodied arthropods [16]; while avoiding ants [17]. However, it was also found in an experiment that, myrmecophagic (ant-eating) salticids prefer ants to other prey, and distinguish ants from other prey when relying on optical cues alone and in the absence of prey movement [18]. In this study, test spiders orient toward and continue to pursue mosquito while flying but attack was always achieved when the mosquito was in resting position. It was also reported that movement tends to stimulate salticid to align toward and persuade prey [19]; and to distinguish between different types of prey that salticids sometimes rely on cues from different style of movement [20]. However, many species of salticid occasionally stalk and attack motionless prey [21]. It appears that the preference of P. petersi for Ae. albopictus over the two other preys is weaker than that of E. flavocincta. Although this is the second time of reporting this genus (Evarcha) to show preference for mosquito after the study by [4], it is worth concluding that the genus have high preference for mosquitoes. It was also found that five species of Natta and 2 other species of Silver, both genera of salticids, when well fed prefer ants to other insects as prey, but when starved for 14 days prior to testing, appear to take prey indiscriminately [11] . Another study shows no evidence that 14 days fasting affect prey choice in araneophagic Cyrba algerina and Portia spp [5]. This study also indicates that preference of mosquito over fruit flies and rice weevil remain intact after both 7 and 14 day fasts, hence E. flavocincta and P. petersi resembles those araneophagic observed [5]. Present study had shown that attack was quite quick after 14 days fasts compare to 7 days fast, but in both cases mosquito was still chosen. Effect of fast longer than 14 days on prey choice was not investigated as the test spiders in the current holding could not withstood starvation longer than 14 days. The significant impact of spiders on the population of mosquitoes has never been thoroughly studied even though Heteropoda venatoria (Sparassidae) was found playing the role of predator of A. albopictus [8]; 108
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five species of spider (Passiena sp., Leucauge grata, Heteropoda venatoria, Cyclosa insulana and Nephila maculata) were also serologically identified as predators of Ae. albopictus [9]; The preference of E. flavocincta and P. petersi to Ae. Albopictus in the current study and that of E. culicivora over engorged female Anopheles mosquitoes [4] merit further investigation on the potential use of spiders as a biological control agent for mosquitoes.
ACKNOWLEDGMENT The authors wish to thank the Director of the Institute Bioscience (IBS), University Putra Malaysia UPM, for allowing access to the research areas. REFERENCES [1]. Koh, J. K. H. (1990). A Guide to Common Singapore Spiders, B. P. Guides, Science Centre. 49-51pp. [2]. Su, K. F., Meier, R., Jackson, R. R., Harland, D. P. and. Li, D. Q. (2007) Convergent evolution of eye ultrastructure and divergent evolution of vision-mediated predatorybehaviour in jumping spiders. European Society for Evolutionary Biology 20: 1478-1489. [3]. Fox, L. R., and P.A. Morrow. (1981). Specialization: Species property or local phenomenon? Science. 211: 887-893. [4]. Jackson, R. R., Nelson, X. J. and Sune, G. O. (2005).Aspider that feeds indirectly on vertebrate blood by choosing female mosquitoes as prey. Proc. Natl. Acad. Sci. USA.102: 15155-15160. [5]. Li, D. Q., Jackson, R. R. and Barrion,A. (1997). Prey preferences of Portialabiata,P. africana & P. schultzi, araneophagic jumping spiders (Araneae: Salticidae) from the Philippines, Sri Lanka, Kenya, & Uganda. N. Z. J. 24: 33-349. [6]. Jackson, R. R. and Li, D. (1998). Prey preferences and visual discrimination ability of Cyrba algerina, an araneophagic jumping spiders (Araneae: Salticidae) with primitive retinae. Isrl J.l Zool. 44: 227- 242. [7]. Li, Daiqin (2000). Prey preferences of Phaeacius malayensis, a spartaeine jumping spider (Araneae: Salticidae) from Singapore. Can. J. Zool. 78: 2218-2226. [8]. Sulaiman, S., Baharudin O., Sulaiman O., Ismail G. and Jeffery, J. (1990). Detection of Aedes aegypti (L) (Diptera: Culicidae) Predators in urban Slums in Malaysia using the precipitin test. Mosq-Borne Dis Bull.7 (4): 123-126. [9]. Sulaiman, S., Pawanchee Z.A., Karim, M. A., Jeffery, J., Busparani, V. and. Wahab,A. (1996). Serological identification of the predators of adults Aedes albopictus (Skuse) (Diptera: Culicidae) in rubber plantations and a cemetery in Malaysia. J. Vec. Ecol. 21: 22-25. [10]. Pyke, G. H. (1984). Optimal foraging theory: A critical review. Annual Review of Ecology and Systematic 15: 523-575. [11]. Jackson, R. R. and van Olphen, A. (1992). Prey-capture techniques and prey preferences of Chrysilla, Natta, and Silver, ant-eating jumping spiders (Araneae: Salticidae) from Kenya and Sri Lanka. J. Zool London 227: 163-170. [12]. Miyashita, K. (1969) . Seasonal changes of population density and some characteristics of overwintering nymphs of Lycosa tinsignita Boes et Str. (Araneae: Lycosidae). Appl. Entomol. Zool. 4; 1-8. Inst Oswaldo Cruz 98: 659-663. [13]. Jackson R. R.(2000) . Prey preferences and visual discrimination ability of Brettus,Cocalus & Cyrba, araneophagic jumping spiders (Araneae: Salticidae) fromAustralia, Kenya & Sri Lanka. N. Z. J. 27: 29-39. [14]. Li, D. Q. and Jackson, R. R. (1996a). Prey-specific capture behaviour and prey preferences of myrmecophagic and araneophagic jumping spiders (Araneae: Salticidae). Rev. Suisse Zool. 423-436. [15]. Sokal, R. R., and Rohlf, F. J. (1981). Biometry; the principles of statistics in biological research. W. H. Freeman and Co., San Francisco. [16]. Huseynov, E. F. (2005). Natural prey of the jumping spider Menemerus taeniatus (Araneae: Saticidae). Eur. J. Entomol. 102: 797-799. [17]. Nelson, X. J., and Jackson, R. R.( 2007). Vision-based ability of an ant-mimicking jumping spider to discriminate models, conspecific individuals and prey. Insectes Soc. 54: 1- 4. [18]. Li, D. Q., Jackson, R. R. and Cutler, B. (1996). Prey-capture techniques & prey preferences of Habrocestum pulex, an ant-eating jumping spiders (Araneae: Salticidae) from NorthAmerica. J. Zool London. 240: 551-562. [19]. Dill, L. M. (1975). Predatory behaviour of the zebra spider, Salticus scenicus ((Araneae: Salticidae). Can. J. Zool. 53: 1284-1289. [20]. Freed,A. N. (1984). Foraging behaviour in the jumping spider Phidippus audax: bases for selectivity. J. Zool. London. 203: 49-61. [21]. Tarsitano, M., Jackson, R. R. and Kirchner, W. H. (2000). Signal and signal choices made by the araneophagic jumping spider Portia fimbriata while hunting the orb- weaving web spiders Zygiella x-notata and Zosis geniculatus. Ethology. 106: 595-615.
Corresponding Author : Maimusa A. H . Department of Science Laboratory Technology , Mai Idriss Alooma Polytechnic P. M. B. 1020, Geidam, Yobe State, Nigeria. Email:
[email protected]
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