1015 Comparison of Foraging Ability Between Solenopsis invicta and Tapinoma melanocephalum (Hymenoptera: Formicidae) by Lu Yong-Yue*, Wu Bi-Qiu, Zeng Ling & Xu Yi-Juan ABstrAct In this study, we investigated the foraging ability of the invasive ant So- lenopsis invicta and native ant Tapinoma melanocephalum (Hymenoptera: Formicidae) by measuring their searching and recruitment time for 5 types of food (sausage, sausage & honey, honey, mealworm and peanut oil) in infested wasteland and litchi orchards in south china. The searching time was determined by measuring the time required for the first ant to find the food. The recruitment time was determined by measuring the time to recruit 10 ants to the food which was placed on petri dish 30 cm away from nest entrances. 30 colonies each of T. melanocephalum and S. invicta were tested. In the infested wasteland, the searching time of S. invicta for sausage & honey, sausage, mealworm and honey and the recruitment time of S. invicta for sausage & honey, mealworm and honey were significantly longer than those of T. melanocephalum, but the searching time of these two species of ants for peanut oil was not significantly different. In the infested litchi orchard, the recruitment time of S. invicta for sausage was significantly longer than that of T. melanocephalum, while the recruitment time for the other four types of food was not significantly different between the two species of ants. The searching time for all the five types of food was not significantly different between the two species of ants in the infested litchi orchard. Key words: Solenopsis invicta, Tapinoma melanocephalum, searching time, recruitment time INtrODUctION Interspecific competition refers to interference or suppression between two or more species. The consequences of interspecific competition are often red Imported Fire Ant research center, south china Agricultural University, Guangzhou 510642, P.r.china *corresponding author, email:luyong yue@scau.edu.cn, insectlu@163.com 1016 sociobiolog y Vol. 59, No. 3, 2012 a reduction of efficiency in reproduction, growth and survival of one species due to the utilization or interference of common resources by another species. competition for scarce resources by two species leads to an adverse effect on both species. resource competition can be divided into exploitation competi- tion and interference competition (reitz & trumble 2002). In exploitation competition, the ability of acquiring resources in one species is greater than that in another species. The mechanisms of exploitation competition include differential resource acquisition, differential female fecundity, differential searching ability, resource preemption, differential strategies and reactions to bad resources (reitz & trumble 2002, Xu & cheng 2005). Solenopsis invicta Buren is a dangerous pest originally discovered in south America, Brazil, Argentina, Paraguay and the Panama canal (Vinson 1997). It is currently distributed all over the 19 southern states and regions of the Us, an area of 128 million hectares (callott & collin 1996, callott 2002, Alfredo & Jim 2004). On sep., 28, 2004, S. invicta was first identified in Wuchuan, Guangdong in china, and subsequently it was found in other areas of Guangdong, Guangxi, Fujian, Hunan, and Hongkong (Zeng et al. 2005a). This alien ant can reduce the diversity of the native ants and cause effects on other organisms directly or indirectly (Holway et al. 2002). During the competition with native ants, the invasive ants can extend their search- ing and recruitment time due to their large popualtions, which enhances the exploitation competition ( Johnson et al. 1987). In invaded areas, compared to the native ants, S. invicta normally has stronger exploitation competition, which allows them to rapidly find food, discover more food resources, recruit more ants and extend the recruitment time ( Jones & Phillips 1990, Porter & saignano 1990, Morrison 1999, calcaterra et al. 2008). Previous studies have shown that invasion by S. invicta has already reduced the diversity and abundance of native ants in south china (sheng et al. 2007, Wu et al. 2008, Lu et al. 2012). However, further studies on the exploitation competition between S. invicta and native ants in south china are needed. While investigating the ant diversity in the areas with S. invicta in south china, we found that a small and fast-moving native ant (Tapinoma melano- cephalum Fabricius) can co-exist with S. invicta, and is still the one of dominant species in the areas infected by S. invicta (Lu et al. 2012). T. melanocephalum and S. invicta have similar reactions to the soil surface temperature: with 1017 Yu, Y-L. et al. —comparison of Foraging Ability of two Ant species the increases of soil surface temperature, the percentage of ants appearing and controlling the food was decreased (Zheng et al. 2007). However, the heat resistance of T. melanocephalum is slightly higher than that of S. invicta (Zheng et al. 2007). How about the competition between these two species of ants? Which is stronger? These questions need to be answered. to avoid the interference of other species of ants and reveal the foraging ability of T. melanocephalum and S. invicta, we investigated the foraging capabilities and recruitment dynamics of both ants at a short distance (30 cm to the ant nest) in different habitats. By comparing the exploitation competition between T. melanocephalum and S. invicta, we expected to provide potential mechanisms by which T. melanocephalum co-exists with S. invicta and remains a dominant species in the areas with S. invicta in south china. MAtErIALs AND MEtHODs Experimental environment This study was conducted in Longgang, shenzhen in 2007. S. invicta colonies in this district were polyg yne. Based on the density and distribution of active S. invicta colonies (Zeng et al. 2005b), S. invicta was considered to be introduced for more than two years at the infested wasteland and litchi orchard. The general information of the two regions is summarized in table 1. table.1 General information of infested wasteland and litchi orchard areas Area type Infested wasteland Infested litchi orchard Altitude(m) 46.5 40.7 Longitude and latitude N22°44".260" E114°22'.340" N22°44'.227" E114°22'.303" Area (m2) 1826 2241 Agrotype yellow-red soil yellow lato soil Grass coverage degree(%) 90 60 Defoliation thickness (cm) - 2-3cm shade density(%) - 92 Active S. invicta nests/100m2 0.93 0.18 1018 sociobiolog y Vol. 59, No. 3, 2012 Experimental design Three fan-shaped side wall with equal areas (≈ 0.023 cm2) were removed from the bottom side of plastic petri dishes (diameter = 9 cm) and then wet filter paper (diameter = 9 cm) was placed on the bottom of the petri dishes. subsequently, five types of food including sausage (representing artificial food with abundant protein), sausage & three drops of honey (representing artificial food with abundant protein and carbohydrates), mealworms (representing natural food with abundant protein), peanut oil (representing artificial food with abundant oils) and honey (representing artificial food with abundant carbohydrates) were placed on the center of the petri dishes as baits. Peanut oil and honey were dropped in the cotton wool at the center of the petri dishes with a plastic head dropper. Five types of baits were placed (at a distance of 30 cm) around the nest of T. melanocephalum and S. invicta. The time from food placement in petri dishes to the first ant appearing on the food was the searching time, and the time required to recruit 10 ants to the food was recruitment time, and both of them were recorded by stopwatch. A total of 30 nests for T. melanocephalum and S. invicta respectively were tested in the wasteland and litchi orchard. Because of the hot weather in August in shenzhen, we performed the experiments at the time of the relatively low temperature, from 8 AM to 10 AM in the morning or from3 PM to 6 PM. in the afternoon. During the experiment, the soil surface temperature in the wasteland was between 30.0°c and 42.4°c, and the relative atmospheric humidity was between 49% and 81%. The soil surface temperature in the litchi orchard was between 30.8°c and 36.9°c, and the relative atmospheric humidity was between 61% and 92%. Statistical analysis Each nest in wasteland and litchi orchard was regarded as one replicate and Duncan's new multiple range method was used to compare the foraging ability between different types of food. Non-paired student t test was used to compare the foraging ability between T. melanocephalum and S. invicta. All statistical analyses were conducted using sPss, version 14.0 (sPss Inc., chicago, IL, UsA). 1019 Yu, Y-L. et al. —comparison of Foraging Ability of two Ant species rEsULts Foraging ability of S. invicta for different types of food In the wasteland, the shortest searching time (2.98 min) for S. invicta was observed for peanut oil, which was significantly shorter than the longest searching time (7.84 min) for sausage (n=30, P<0.05). searching time of S. invicta for sausage & honey, honey and mealworms was not significantly dif- ferent. The longest recruitment time for S. invicta was 9.87 min, recorded for honey, which was significantly longer than that for sausage & honey, sausage and mealworms (n=30, P<0.05). S. invicta’s recruitment time for honey and peanut oil was not significantly different. In the litchi orchard, S. invicta’s shortest searching time was observed for peanut oil (2.1 min), while the longest searching time was observed for sau- sage (3.5 min) (n=30, P<0.05). The longest recruitment time was observed for honey (12 min), which was significantly longer than that for sausage & honey, sausage and peanut oil (n=30, P<0.05). The recruitment time for honey and mealworms was not significantly different (table 2). Foraging ability of T. melanocephalum for different types of food In the wasteland, the longest searching time of T. melanocephalum was observed for peanut oil (3.02 min), while the shortest searching time was observed for honey (1.07 min). The searching time for peanut oil was sig- nificantly longer than that for sausage & honey (1.37 min) and honey (1.07 min) (n=30, P<0.05), but was not significantly different from that for sausage and mealworms. The longest recruitment time was observed for peanut oil (12.55 min), which was significantly longer than that for the other four types of food (n=30, P<0.05). In the litchi orchard, the longest searching time of T. melanocephalum was observed for mealworms (2.84 min), while the shortest searching time was observed for peanut oil (1.54 min). The searching time for mealworms was significantly longer than that for sausage & honey (1.85 min), honey (1.82 min) and peanut oil (2.84 min) (n=30, P<0.05), but was not significantly different from that for sausage. The longest recruitment time for peanut oil was observed for peanut oil (8.42 min), which was significantly longer than that for the other four types of food (n=30, P<0.05, table 2) . 1020 sociobiolog y Vol. 59, No. 3, 2012 Comparison of foraging ability between T. melanocephalum and S. invicta The results for the comparison of the foraging ability between T. mel- anocephalum and S. invicta are summarized in table 2. In the wasteland, the searching time of S. invicta for sausage & honey, sausage, honey and mealworms was significantly longer than that of T. melanocephalum (n=30, P<0.05). The searching time of S. invicta for peanut oil was not significantly different from that of T. melanocephalum. The recruitment time of S. invicta for sausage & honey, sausage, honey and mealworms was longer than that of T. melanocephalum (n=30, P<0.05). In the litchi orchard, all searching timse for five types of food between S. invicta and T. melanocephalum were not significantly different. The recruit- ment time of S. invicta for sausage, honey and mealworms was significantly longer than that of T. melanocephalum. DIscUssION In the wasteland and litchi orchard, the shortest searching time of S. invicta was observed for peanut oil, while the longest searching time was observed for sausage. This is possibly due to the rapid attraction of S. invicta to the food by the evaporated peanut smell. When they discover food, S. invicta can recruit their companions rapidly to the sausage or sausage & honey, then cut and move the sausage back to the nests. The longest recruitment time of S. invicta was observed for the honey. These results suggest that S. invicta favors high-protein food, while high-carbohydrate food is least attractive for S. invicta, which is in agreement with previous studies (Xu et al. 2006). T. melanocephalum prefers honey to the other food sources according to the shortest searching and recruitment time both in the wasteland and lithci or- chard. In contrast, in the litchi orchard, the smell of the peanut oil attracts T. melanocephalum early, but the recruitment time of sausage & honey, sausage, honey and mealworms was significantly shorter than that of the peanut oil, suggesting that T. melanocephalum favors artificial or natural food with high levels of carbohydrate and protein. The litchi orchard has higher diversity of vegetation and provides more honey than wasteland. This may explain why T. melanocephalum in the litchi orchard does not search for honey or recruit as rapidly as in the wasteland. The results suggest that T. melanocephalum 1021 Yu, Y-L. et al. —comparison of Foraging Ability of two Ant species ta bl e 2. s ea rc hi ng ti m e an d re cr ui tm en t t im e of s . i nv ic ta a nd t . m el an oc ep ha lu m fo r 5 fo od s i n in fe st ed a re as (m in ). Fo od ty pe se ar ch in g tim e r ec ru itm en t t im e W as te la nd L it ch i o rc ha rd W as te la nd L ic hi o rc ha rd S. in vi ct a T. m el an oc ep ha lu m S. in vi ct a T. m el an oc ep ha lu m S. in vi ct a T. m el an oc ep ha lu m S. in vi ct a T. m el an oc ep ha lu m sa us ag e & h on ey 4. 61 ± 0. 68 bc 1. 37 ± 0. 23 bc ** 3. 13 ± 0. 66 ab 1. 85 ± 0. 37 b 4. 86 ± 0. 96 b 1. 87 ± 0. 40 b* * 3. 69 ± 0. 54 b 2. 42 ± 0. 24 b sa us ag e 7. 84 ± 1. 10 a 2. 44 ± 0. 83 ab ** 3. 50 ± 0. 57 a 2. 18 ± 0. 49 ab 4. 88 ± 0. 70 b 2. 76 ± 0. 85 b 4. 86 ± 0. 70 b 2. 07 ± 0. 33 b* * H on ey 5. 09 ± 1. 27 bc 1. 07 ± 0. 09 c* * 2. 41 ± 0. 33 ab 1. 82 ± 0. 37 b 9. 87 ± 2. 82 a 1. 85 ± 0. 57 b* * 12 .0 0± 3. 17 a 4. 09 ± 0. 82 b* * M ea lw or m 5. 99 ± 1. 01 ab 2. 11 ± 0. 45 ab c* * 2. 48 ± 0. 40 ab 2. 84 ± 0. 57 a 5. 02 ± 1. 02 b 1. 92 ± 0. 33 b* * 9. 24 ± 3. 30 ab 3. 21 ± 1. 11 b* * Pe an ut o il 2. 98 ± 0. 34 c 3. 02 ± 0. 72 a 2. 10 ± 0. 28 b 1. 54 ± 0. 33 b 8. 09 ± 2. 11 ab 12 .5 5± 2. 74 a 5. 75 ± 1. 92 b 8. 42 ± 2. 34 a M ea ns w ith in a co lu m n fo llo w ed b y t he sa m e l et te r a re n ot si gn ifi ca nt ly d iff er en t ( P＞ 0. 05 ) u si ng th e D un ca n m et ho d of m ul tip le co m pa ri so ns , f ol lo w in g a on e- w ay A N O VA . “ *”, “ ** ” re pr es en t s ig ni fic an t d iff er en ce s a t P ＜ 0. 05 a nd P ＜ 0. 01 re sp ec tiv el y, be tw ee n m ea ns u si ng th e un pa ir ed sm al l s w at ch es t- te st . 1022 sociobiolog y Vol. 59, No. 3, 2012 searches for high-carbohydrate or high-protein food more rapidly than S. invicta. In addition, the recruitment of T. melanocephalum is faster than that of S. invicta. Ants belonging to Dolichoderinae and Formicinae favor sweet foods (Li et al. 2000). The honeydew secreted by aphids, scale insects, and angle cicadas, etc. is the favorite food of ants belonging to Formicinae (Wu & Wang 1995). In this study, we found that T. melanocephalum favors high-carbohydrate foods, e.g., honey. We also found that food proficient in protein is the favorite food of both T. melanocephalum and S. invicta, which is one of the reasons leading to the competition between these two species of ants. However, T. melanocephalum also favors high-carbohydrate foods, but S. invicta does not, which provides a good condition for the survival and proliferation of T. mel- anocephalum when it lives in the areas with S. invicta. Furthermore, for the high-carbohydrate food and high-protein food, the searching and recruitment ability of T. melanocephalum is stronger than that of S. invicta, indicating that the exploitation competition of T. melanocephalum is stronger than that of S. invicta. In addition, T. melanocephalum has a smaller size and moves more rapidly than S. invicta (Li et al. 2008). Therefore, T. melanocephalum can find and transport sufficient food before S. invicta arrives. We also found that T. melanocephalum lived in many S. invicta-abandoned nests (naturally abandoned or abandoned due to human activities), and sometimes the nests of these two speices were very close. The exploitative nesting habit and wide range of favorite food allows T. melanocephalum to survive in various areas (smith 1965). rapid food searching and recruitment of T. melanocephalum can explain why T. melanocephalum can co-exist with the alien ant S. invicta and continue to be one of the dominant species in areas invaded by S. invicta. This is also in agreement with the hypothesis that resource division (e.g., food, time and space) can result in ecological segregation between species. The areas with long-term (several years) invasion of S. invicta were chosen as experimental sites in this study. Therefore, the effect of short-term inva- sion of S. invicta on the foraging ability of T. melanocephalum needs to be further studied. AcKNOWLEDGMENts We would like to thank Zhendong song and Haiquan Wu for their observa- tions and records. Our study was supported by the National Basic research 1023 Yu, Y-L. et al. —comparison of Foraging Ability of two Ant species Program of china (Award# 2009cB119200) and National Natural science Foundation of china (Award# 305712427). rEFErENcEs Alfredo, F., c. Jim. 2004. Putting out the fire. Agri. res. 52(12):12-14. calcaterra, L.A., J.P. Livore, A. Delgado & J.A. Briano. 2008. Ecological dominance of the red imported fire ant, Solenopsis invicta, in its native range. Oecol. 152(2): 411-421. callcott, A.M., H.L. collins. 1996. Invasion and range expansion of imported fire ant (Hymenoptera: Formicidae) in North America from 1918-1995. Flor. Entomol. (79):240-251. callott, A.M. 2002. range expansion of the imported fire ant 1918-2001. In Diffie, s.K.(ed) 2002 Annual Imported fire ant research conference, Athens, Georgia. Holway, D.A., L. Lach, A.V. suarez, N.D. tsutsui & t.J. case. 2002. The cause and consequences of ant invasions. Ann. rev. Ecol. and syst. (33):181-233. Johnson, L.K., s.P. Hubbell & D.H. Feener. 1987. Defense of food supply by eusocial colonies. Am. Zool. (27):347-358. Jones, s.r., s.A. Philips. 1990. resource collecting abilities of Solenopsis invicta (Hymenoptera: Formicidae) compared with those of three sympatric texas ants. south-west. Nat. (35):416-422. Li, J., s.c.Han,Z.G. Li, & B.s. Zhang. 2008. The behavior observe of Tapinoma melanocephalum native competitive species of Solenopsis invicta. Plant Quarantine, 22(1):19-21. Li, Q.X., D.H. He, Y.D. chang, & L.D. Liu. 2000. Overview of ants foraging. J. Ningxia Agri. Uni. 21(2):94-97. Lu, Y.Y., B.Q. Wu, Y.J. Xu, & L. Zeng. 2012. Effects of red imported fire ants (Solenopsis invicta) on the species strcuture of several ant communities in south china. sociobio. 59(1) Morrison, L.W. 1999. Indirect effects of phorid fly parasitoids on the mechanisms of interspecific competition among ants. Oecol., (121):113-122. Porter, s.D., D.A. savignano. 1990. Invasion of polyg yne fire ants decimates native ants and disrupts arthropod community. Ecol. (71):2095-2106. Porter, s.D.1992. Frequency and distribution of polygyne fire ant (Hymenoptera: Formicidae) in Florida. Fla. Entomol. (75):248-257. reitz, s.r., J.t. trumble. 2002. competitive displacement among insects and arachnids. Annu. rev. Entomol. (47): 435-465. schoener, t.W. 1974. resource portioning in ecological communities. science,185:27-39. shen, P., X.L. Zhao, D.F. cheng, Y.Q. Zheng & F.r . Lin. Impacts of the imported fire ant Solenopsis invicta invasion on the diversity of native ants.J. southwest Nor.Uni. 32 (4):93-97. smith, M.r. 1965. House-infesting ants of the eastern United states: Their recognition biolog y and economic importance. U.s.D.A. tech. Bull. 1326. Vinson, s.B. 1997. Invasion of the red imported fire ant (Hymenoptera: Formicidae): spread, biolog y and impact. Am. Entomol. 43(1):23-29. 1024 sociobiolog y Vol. 59, No. 3, 2012 Wu, B.Q., Y.Y. Lu, L. Zeng, & G.W Liang. 2008. Influences of Solenopsis invicta Buren invasion on the native ant communities in different habitats in Guangdong. chin. J. Appl. Ecol. 19(1):151-156. Wu, J., c.L. Wang.1995. chinese ants.Beijing :chin. Forestry Pr. Xu, r.M., X.Y. cheng. 2005. Insect population ecolog y-foundation and frontier. Beijing : sci. and tch. Press, 326. Xu, Y.J., Y.Y. Lu, L. Zeng, & N.D. Li.2006.Attraction of several baits to workers of red imported fire ant, solenopsis invicta.chin. B. Entomol.43(6):856-857. Zeng, L., Y.Y. Lu & Z.N. chen 2005. Management and surveillance of red imported fire ant. Guangdong science & technique Press, Guangzhou, china, 106pp. Zeng , L., Y.Y. Lu, X.F. He, W.Q. Zhang & G.W. Liang. 2005. Identification of red imported fire ant solenopsis invicta to invade mainland china and infestation in Wuchuan，Guangdong. chin. Bul. Entomol. 42:144-148. Zheng,J.H., Mao r.Q., & r.J. Zhang. 2007. comparisons of foraging activities and competitive interactions between the red imported fire ant (Hymenoptera: Formicidae) and two native ants under high soil-surface temperatures. sociobio. 50(3):1165-1175.