POPULATION ECOLOGY

On the Competition Occurring Between Aedes albopictus and Culex pipiens (Diptera: Culicidae) in Italy MARCO CARRIERI, MARTA BACCHI, ROMEO BELLINI,1

AND

STEFANO MAINI2

Centro Agricoltura Ambiente, Crevalcore 40014, Italy

Environ. Entomol. 32(6): 1313Ð1321 (2003)

KEY WORDS Aedes albopictus, Culex pipiens, larval competition, exotic species, ecological niche

OVER THE LAST FEW DECADES, the intensiÞcation of the international used tire trade has caused the passive spread of a number of insect species, some of which have a signiÞcant impact on public health. Aedes albopictus (Skuse) was discovered in Italy in 1990 (Sabatini et al. 1990), having been introduced through the tire trade (Dalla Pozza and Majori 1992). Because of its high biological adaptability (Hawley 1988) and its ability to overwinter in embryonic diapause, it spread rapidly to colonize various areas in the central and northern regions of Italy (Romi 2001). The species tends to colonize mainly urban and suburban environments, occupying a habitat already exploited by Culex pipiens L. Ae. albopictus is more anthropophilic than Cx. pipiens and is a highly efÞcient vector for a number of arboviruses (Schroyer 1986, Mitchell 1991). Therefore, the introduction of this new species may represent a serious nuisance for the resident population and could play a signiÞcant role in the transmission cycle of arboviruses in the Mediterranean basin (Mitchell 1995). In general, the likelihood that exotic species will colonize new regions depends on their capacity to E-mail: [email protected]. Dip. Scienze e Tecnologie Agroambientali, Universita` di Bologna, V. Ce G. Fanin 44, Bologna 40127, Italy. 1 2

adapt to the new environmental conditions and to compete with the pre-existing species. Some studies conducted in the United States have already demonstrated the ability of Ae. albopictus to compete with other species such as Ae. aegypti (L.) and Ochlerotatus triseriatus (Say) (Livdahl and Willey 1991, Novak et al. 1993). The introduction and spread of Ae. albopictus has been associated with the decline in Ae. aegypti populations (Hobbs et al. 1991, McHugh 1991, 1992; Hornby et al. 1994, OÕMeara et al. 1992, 1995), and a number of hypotheses have been advanced to account for this trend. Attention has been focused, above all, on larval competition (Juliano 1998, Black et al. 1989, Daugherty et al. 2000), reproductive and metabolic differences (Ho et al. 1992, Klowden and Chambers 1992), interference in mating (Nasci et al. 1989, Brogdon 1994, Harper and Paulson 1994), inßuence of pre-existing eggs and larvae on ovideposition (Allan and Kline 1998), and interspeciÞc differences in the vulnerability to Ascogregarina spp. (Blackmore et al. 1995, Juliano 1998). This study aims to analyze the ecological niche that Ae. albopictus is colonizing in Italy and its possible interactions with the indigenous species Cx. pipiens. The ability of this species to adapt to Italian urban environments was assessed through Þeld surveys, whereas the differences in preimaginal development

0046-225X/03/1313Ð1321$04.00/0 䉷 2003 Entomological Society of America

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ABSTRACT Aedes albopictus (Skuse) was detected for the Þrst time in Italy in 1990. Thanks to its high biological adaptability, it spread rapidly to colonize various urban areas in central and northern Italy. The purpose of this study was to examine the ecological niche occupied by Ae. albopictus and the role of competition with Culex pipiens L., which is a widespread indigenous species, in urban areas. The larval development cycle and competition for food between the two species was also studied under laboratory conditions. The study showed that both species can colonize any type of artiÞcial water container. Ae. albopictus mainly occupies saucers under ßower pots and other, usually smallersized, containers, whereas Cx. pipiens tends to develop more in large tanks (100 Ð200 liters) used in residential gardens and other larger-sized containers. It would seem that the two species interact mainly in medium-sized containers (10 Ð50 liters) such as manholes and tires. Laboratory studies showed that, at 25⬚C, the food-biomass conversion coefÞcient is signiÞcantly higher in Ae. albopictus than in Cx. pipiens, indicating that the new established species is more efÞcient in transforming food into biomass. As a consequence, it has a greater capacity to exploit food resources and therefore grow more rapidly than Cx. pipiens. In larval association where food was scarce, it was noted that competition between the two species takes place and is inßuenced by temperature: at 25 ⫾ 2⬚C, Ae. albopictus prevails but is much less likely to do so at 20⬚C.

1314 Table 1.

ENVIRONMENTAL ENTOMOLOGY

Vol. 32, no. 6

Larval number and water volume (liters) for the breeding sites detected Cx. pipiens N

Larvae (mean ⫾ SD)

N

Larvae (mean ⫾ SD)

Volume (mean ⫾ SD)

Cx. pipiens ⫹ Ae. albopictus N

Larvae (mean ⫾ SD)

Volume (mean ⫾ SD)

95.3 ⫾ 77.6 1.3 ⫾ 1.4 25.5 ⫾ 24.4 1.5 ⫾ 0.7 1.8 ⫾ 1.6 63.4 ⫾ 64.8 575.4 ⫾ 848.4 17.8 ⫾ 37.8 54.5 ⫾ 162.5

15 1621.7 ⫾ 3087.4 36 78.6 ⫾ 116.4 31 106.1 ⫾ 121.0 72 55.4 ⫾ 80.6 7 19.7 ⫾ 20.5 9 142.7 ⫾ 240.7 3 99.9 ⫾ 86.7 83 106.5 ⫾ 336.2 256 175.8 ⫾ 835.6

89.3 ⫾ 80.3 1.3 ⫾ 1.1 6.4 ⫾ 11.1 0.7 ⫾ 0.9 0.7 ⫾ 0.4 29.9 ⫾ 54.0 3.0 ⫾ 2.0 7.0 ⫾ 26.3 9.8 ⫾ 33.3

10 11490.1 ⫾ 16340.5 18 54.8 ⫾ 32.9 10 903.3 ⫾ 2017.4 4 72.2 ⫾ 46.6 2 70.0 ⫾ 70.7 3 76.7 ⫾ 42.5 7 6638.0 ⫾ 17114.6 17 678.8 ⫾ 2209.2 71 2585.7 ⫾ 8819.9

92.0 ⫾ 81.2 1.2 ⫾ 0.7 14.9 ⫾ 30.2 0.5 ⫾ 0.0 1.3 ⫾ 1.0 2.2 ⫾ 0.3 39.9 ⫾ 82.2 8.3 ⫾ 26.3 21.4 ⫾ 51.5

148.3 ⫾ 73.9 1.8 ⫾ 0.4 13.5 ⫾ 7.2 0.8 ⫾ 0.6 8.7 ⫾ 10.0 202.7 ⫾ 507.1 158.1 ⫾ 365.2 173.0 ⫾ 877.4 119.3 ⫾ 448.5

4 19 4 45 10 24 1 37 145

58.5 ⫾ 95.2 1.0 ⫾ 0.0 6.0 ⫾ 9.3 0.5 ⫾ 0.4 0.6 ⫾ 0.2 8.6 ⫾ 5.8 4.0 ⫾ 0.0 2.1 ⫾ 3.7 4.1 ⫾ 17.1

2 0 5 9 4 34 0 10 64

377.5 ⫾ 385.4

25.5 ⫾ 34.6

760.0 ⫾ 673.9 238.9 ⫾ 476.4 45.2 ⫾ 44.1 6636.5 ⫾ 4306.3

14.0 ⫾ 10.2 2.2 ⫾ 3.0 0.9 ⫾ 0.2 94.0 ⫾ 48.8

281.4 ⫾ 544.9 3677.0 ⫾ 4463.2

6.3 ⫾ 10.2 53.2 ⫾ 56.79

and competition for food with Cx. pipiens in the larval stage were examined under laboratory conditions. Materials and Methods Field Study. The Þeld study was conducted in Desenzano del Garda (longitude 10⬚32⬘48⬙ E and latitude 45⬚27⬘51⬙ N), where the presence of Ae. albopictus was Þrst detected in 1993 (Celli et al. 1994). Subsequent surveys have provided evidence that the species has reached a capillary distribution over the territory despite the fact that mosquito control programs have reduced adult density to a level below the public nuisance threshold (Bellini et al. 1994 Ð1997). A mosquito control program, which included larvicide treatments on public and private catch basins and other permanent breeding sites, source reduction campaigns, and public education initiatives aimed at stimulating community participation were also conducted in the area during the study period. An investigation on breeding sites within the urban area of Desenzano del Garda was conducted with weekly surveys from April to October 1996 and 1997. The urban surface area monitored over the 2 yr was ⬇250 ha (⬇25% of the total infested area). The volume, the quantity of water present, the degree of exposure to the sun, the species, and larval density were determined for each breeding site detected. Laboratory Study. Aedes albopictus larvae obtained from eggs collected with ovitraps in Desenzano del Garda and Cx. pipiens larvae reared from an autogenous strain colonized starting from Northern Italy populations were used in our laboratory experiments. Trials were carried out in a climate-controlled chamber set at 90% RH; 16:8 L:D. The eggs of both species were placed in separate containers with dechlorinated water and cat biscuits (Friskies adult, Friskies Italia Spa, Mantova, Italy).

70.5 ⫾ 89.7 17.4 ⫾ 6.5 70.8 ⫾ 88.3 17.9 ⫾ 20.5 53.7 ⫾ 58.73 371.7 ⫾ 224.2 50.0 ⫾ 0.0 19.7 ⫾ 36.2 82.9 ⫾ 161.6

Twenty-four hours later, pools of 30 Þrst-instar larvae were separated and placed in 390-ml plastic glasses containing 300 ml dechlorinated water. Three food doses (cat biscuits) were used: 2.83, 1.9, and 0.95 mg/larva at 25 ⫾ 2⬚C. The inßuence of temperature was studied by comparing larval competition at 20 ⫾ 2⬚C and 25 ⫾ 2⬚C using the intermediate food dose of 1.9 mg/larva, which had been previously identiÞed as being the most appropriate dosage for showing competition between the two species. The development time, body weight, and adult production rate corresponding to each temperature and food dose were studied, as was the effect of competition between the two species at the following ratios of Ae. albopictus/Cx. pipiens larvae: 1:0; 2:1; 1:1; 1:2, and 0:1. To prevent the formation of a Þlm on the water surface that could be dangerous to the larvae, during each of the Þrst 6 d of larval development, the food was supplied in doses proportional to age, i.e., 10% on the Þrst and second day, 15% on the third, 21% on the fourth, and 22% on the Þfth and sixth day.

Fig. 1. Climatic trend during the 2-yr study period.

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1996 Drums 54 5448.7 ⫾ 6677.3 Tyres 47 44.0 ⫾ 35.7 Buckets 27 1103.7 ⫾ 1047.4 Flower saucers 2 101.5 ⫾ 139.3 Tarpaulins 2 199.7 ⫾ 141.8 Manholes 14 3497.5 ⫾ 5018.0 Bathtubs 5 28191.8 ⫾ 41539.2 Others 39 1012.0 ⫾ 3306.3 Average 190 2927.0 ⫾ 8677.1 1997 Drums 127 8860.3 ⫾ 14910.7 Tyres 22 52.4 ⫾ 40.7 Buckets 98 694.7 ⫾ 1111.1 Flower saucers 21 47.6 ⫾ 48.1 Tarpaulins 3 183.3 ⫾ 189.3 Manholes 84 12750.2 ⫾ 32753.6 Bathtubs 14 7228.7 ⫾ 18457.6 Others 85 1959.4 ⫾ 5301.9 Average 454 5583.3 ⫾ 17233.9

Ae. albopictus Volume (mean ⫾ SD)

December 2003

CARRIERI ET AL.: COMPETITION BETWEEN Ae. albopictus AND Cx. pipiens

Fig. 2. Seasonal trend of active breeding sites recovered.

RCCs ⫽ {[1/2 * (Ae2:1/Cx2:1) ⫹ (Ae1:1/Cx1:1) ⫹ 2*(Ae1:2/Cx1:2)]/3}/{Ae0:1/Cx1:0}. When RCC ⬎ 1, competition favors Ae. albopictus, and vice versa, if RCC ⬍ 1, Cx. pipiens prevails. The MacArthur and Levins (1967) index was used to show the overlapping of Ae. albopictus and Cx. pipiens niches:

␣j,i ⫽

冋冘

册冒冋冘 册

(Uih * Ujh)

h

Uih2

h

This index measures the probability that the two species (i and j) will use the same resources and thus enter into competition. This probability is proportional to the product of the utilization (U) of each breeding site for each species (Uih ⫻ Ujh) where Uih and Ujh are the proportions of each species in the hth Table 2. Monthly competition (Loubinos index [L]) during the study period Month

1996

1997

May June July August September October

0 0 0.149 0.380 0.344 0.439

0 0.137 0.222 0.601 0.964 0.010

unit of the resource set (type of breeding site, volume, sun exposure). To obtain a signiÞcant estimate of ␣, it is necessary to compare interspeciÞc competition with the competition between individuals of the same species exploiting the same resources 1/⌺Uih2 (niche breadth of species i), where Uih is the proportion of a species found in the ith unit of the resource set. Low values indicate a low amount of ecological similarity and a lack of competition, whereas high values indicate high ecological similarity, low resource partitions, and the occurrence of competition. Values above 1 indicate that the speciesÕ ideal habitat is not included in the types of habitat considered (Ricklefs 1987, Schreiber et al. 1988, Service 1993). Another niche overlap index, which takes into account the abundance of the resources being exploited, is recommended by Hurlbert (1978) and used by Lounibos (1980): L ⫽ [V/(Ae * Cx)]*

冘

[(Aei * Cxi)/vi]

h

where Aei and Cxi represent the abundance of the two species in the ith microhabitat, and vi is the resource abundance, which Lounibos considered as the ßuid volume of the hth microhabitat. Ae and Cx are the total number of each species, and V is the total volume in all microhabitats considered. A value of L ⫽ 1 indicates that each species uses each microhabitat in proportion to its relative abundance, L ⬍ 1 indicates nonoverlap, and L ⬎ 1 indicates overlap. Results Field Study. Overall, 1,194 artiÞcial breeding sites were detected and removed using similar methods during the two seasons studied: 526 in 1996 and 668 in 1997. Of these, 33.6% contained Ae. albopictus larvae only, 52.3% contained Cx. pipiens larvae only, 0.4% contained Cx. hortensis Ficalbi larvae only, 0.2% contained Anopheles larvae only (An. maculipennis Meigen and An. plumbeus Stephens), 0.2% contained Culiseta annulata Schrank larvae only; 11.3% hosted a mixed population of Ae. albopictus and Cx. pipiens, 1.3% contained Cx. pipiens and Anopheles spp., 0.2% contained Cx. pipiens and Cs. annulata, 0.4% contained Cx. pipiens, Ae. albopictus, and Anopheles spp., and 0.1% contained Cx. pipiens, Cs. annulata, and Anopheles spp. During the study, 3,597,026 larvae were found; 3,392,892 (94.3%) were Cx. pipiens, 173,912 (4.8%) were Ae. albopictus, 25,800 (0.7%) were Cs. annulata, 2,972 (0.08%) were Anopheles spp, and 1,450 (0.04%) were Cx. hortensis. Sixty-seven percent of the Ae. albopictus larvae were found in association with Cx. pipiens. Aedes albopictus larvae found in the Þrst half of the season (9,936 larvae collected during MayÐJuly) mainly originated from single species breeding sites (91.6%), whereas during the second half (164,576 larvae collected during AugustÐOctober), they originated mainly from mixed species sites (70.7%). The mean volume of water in single species sites was 100.2 ⫾ 387.8 liters for Cx. pipiens and 7.7 ⫾ 28.6 liters

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Four glasses were used for each food dose and each Ae. albopictus/Cx. pipiens ratio. Pupae were collected daily, placed in separate glasses with 50 ml dechlorinated water, and wrapped in a tulle bag. Every day, adults were aspirated and placed in a freezer at ⫺20⬚C, dried in an oven, and weighed on precision scales (Nasci 1990). Statistical Analysis. The data were analyzed by means of analysis of variance (ANOVA) after the percentages had undergone angular transformation; this was followed by the Newman-Keuls test to separate averages. Competition between the two species was measured using the relative crowding coefÞcient (RCC) as described by Harper (1977) and modiÞed by Novak et al. (1993) and Oberg et al. (1996):

1315

1316 Table 3.

ENVIRONMENTAL ENTOMOLOGY Breeding site typology and relative overlap index for Ae. albopictus and Cx. pipiens Ae. albopictus

Saucers Tarpaulins Bathtubs Tyres Manholes Buckets Drums Others

N

Larvae (mean ⫾ SD)

N

Larvae (mean ⫾ SD)

␣AeCx

␣CxAe

130 23 11 73 70 50 31 147

37.8 ⫾ 64.1 31.8 ⫾ 44.0 4135.0 ⫾ 13553.4 47.8 ⫾ 87.0 349.0 ⫾ 264.7 104.2 ⫾ 129.4 2530.5 ⫾ 7569.8 76.0 ⫾ 258.9

36 11 26 87 135 140 193 151

97.5 ⫾ 245.6 110.3 ⫾ 126.4 9365.0 ⫾ 23457.5 45.0 ⫾ 35.5 9863.8 ⫾ 26190.4 779.1 ⫾ 1150.9 7675.1 ⫾ 12966.8 1448.7 ⫾ 4401.7

0.01 0.01 0.06 0.15 0.32 0.66 1.03 0.13

27.96 19.33 0.15 1.32 0.36 0.39 0.25 0.69

Distribution of breeding sites divided according to volume (liter’s) and relative overlap index Niche overlap index

Cx. pipiens

N

Larvae (mean ⫾ SD)

N

Larvae (mean ⫾ SD)

␣AeCx

␣CxAe

46 173 102 99 35 33 47

13.9 ⫾ 16.6 28.4 ⫾ 48.5 38.1 ⫾ 66.0 70.1 ⫾ 98.9 276.8 ⫾ 212.2 177.8 ⫾ 375.6 3020.0 ⫾ 8758.1

7 68 75 154 52 167 256

57.2 ⫾ 66.6 50.7 ⫾ 74.5 72.9 ⫾ 104.0 144.0 ⫾ 288.0 480.7 ⫾ 1385.9 1113.0 ⫾ 1421.8 12306.6 ⫾ 22473.7

0.00 0.00 0.02 0.02 0.08 0.39 1.05

1.52 6.21 2.91 3.61 0.15 0.71 0.44

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only enter into contact slightly in the second part of the season (in August and September 1997, the Lounibos index resulted higher than in the same period in 1996 and close to 1). The high temperature registered in August and September 1997 (the mean temperature of the period of August and September was 4⬚C higher in 1997 than in 1996) and lower monthly rainfall (in August and September 1997 it was about one-half that recorded in the same period of the previous year; Fig. 1) may have reduced the availability of larval development sites thus causing an increase in niche overlap. All breeding sites detected were artiÞcial containers. A typological analysis shows that both species can colonize any kind of water container. Ae. albopictus alone occupies mostly saucers under ßower-pots (76.4% of total active saucers with ␣Ae:Cx ⫽ 0.01) and other small containers (discarded sheets of plastic and tires), whereas Cx. pipiens mainly develops in the 100to 200-liter tanks used in domestic vegetable gardens (86.2% of total active tanks with ␣Cx:Ae ⫽ 0.25) and larger-sized containers such as bathtubs (Table 3). However, the two species seem to overlap in medium-sized containers such as manholes and buckets (␣Cx:Ae ⫽ 0.36 and 0.39 and ␣Ae:Cx ⫽ 0.32 and 0.66, respectively; Table 3). This difference between the two species becomes clearer when the overlap index is analyzed in relation to the volume of water present in breeding containers (Table 4). High niche overlap indexes between the two species were observed in containers holding a quantity of water in the range of 10 Ð50 liters. Aedes albopictus tend to colonize small containers, even those holding just a few milliliters of water (78.5% of the containers colonized had a volume of ⬍5

Ae. albopictus

V ⱕ 0.1 0.1 ⬍ V ⱕ 0.5 0.5 ⬍ V ⱕ 1 1⬍Vⱕ5 5 ⬍ V ⱕ 10 10 ⬍ V ⱕ 50 V ⬎ 50

Niche overlap index

Cx. pipiens

for Ae. albopictus, whereas in the breeding sites hosting the two species, the mean quantity of water was 36.5 ⫾ 56.2 liters (Table 1) Niche overlap was analyzed by means of the L coefÞcient, which revealed that the two species are ecologically separate (Ltot ⫽ 0.26). Different values were obtained for the 2 yr of the study (1996, L ⫽ 0.17; 1997, L ⫽ 0.82). This disparity may be ascribed to different climatic trends during the period of MayÐ October: a higher average temperature was recorded in 1997 (21.4⬚C in 1996 and 22.1⬚C in 1997), accompanied by less rainfall (508.5 mm in 1996 and 306 mm in 1997; Fig. 1). The dry second half of the summer of 1997 is likely to have brought the two niches close together, thus reducing Ae. albopictus development possibilities in small rain-Þlled sites and allowing the accumulation of water in large containers only (drums, buckets, and manholes) as shown also by the mean water volume in containers found in 1996 (28 liters) compared with 1997 (87 liters). The investigation conducted showed that the Þrst species to become active was Cx. pipiens, with overwintering females beginning egglaying around the middle of April. The Cx. pipiens population reached a peak in July with 197 breeding sites discovered (Fig. 2). Aedes albopictus larval development started at the beginning of May with the hatching of diapausing eggs. Subsequently, the breeding sites colonized by Ae albopictus increased progressively until reaching a peak of 188 in September (Fig. 2). The mixed breeding sites were found mainly (88.9%) in the months of August and September. On the basis of the monthly competition Loubinos indexes (Table 2), it may be argued that the two species Table 4.

Vol. 32, no. 6

December 2003

CARRIERI ET AL.: COMPETITION BETWEEN Ae. albopictus AND Cx. pipiens

1317

larvae and 59.9% of the breeding sites were located in sunny areas; Table 5). In the mixed breeding sites found in shady areas, Ae. albopictus prevailed (the density ratio Ae/Cx resulted equal to 1.7), whereas in sunny areas, Cx. pipiens predominated (Ae/Cx ⫽ 0.07). Larval Competition for Food. Data obtained in single species development condition experiments showed signiÞcant differences in the adult production rates of

liters), whereas Cx. pipiens tends to occupy containers with a water volume of ⬎5 liters (61% of the breeding sites had a volume ⬎5 liters; Table 4). Considering the exposure of the breeding sites to the sun (Fig. 3), it was observed that Ae. albopictus tends to colonize sites that are located in shady areas for most of the day (71.2% of the larvae sampled and 57.7% of the breeding sites discovered), whereas Cx. pipiens seems to prefer sunny habitats (68.4% of the Table 5.

Exposure of breeding sites to sun and overlap index Ae. albopictus

Shady Sunny Intermediate

Niche overlap index

Cx. pipiens

N

Larvae (mean ⫾ SD)

N

Larvae (mean ⫾ SD)

␣AeCx

␣CxAe

308 163 64

402.07 ⫾ 3486.34 168.88 ⫾ 331.82 352.30 ⫾ 1582.78

271 467 41

3837.27 ⫾ 12797.82 4971.31 ⫾ 15248.69 765.66 ⫾ 1595.58

0.46 1.23 0.33

0.88 0.38 1.46

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Fig. 3. Exposure of breeding sites to sun: (a) typological analysis, (b) seasonal trend, and (c) breeding sites volume (liters).

1318

ENVIRONMENTAL ENTOMOLOGY

Table 6.

Vol. 32, no. 6

Comparison between some biological parameters (ⴞSD) of Ae. albopictus and Cx. pipiens at different food doses

Percent adult emergence Ae. albopictus Cx. pipiens Days from egg immersion to adult emergence Ae. albopictus Cx. pipiens Mean adult weight (mg) Ae. albopictus Cx. pipiens

Dose A25⬚C

Dose B25⬚C

Dose C25⬚C

Dose B20⬚C

0.60 (⫾0.10)a 0.73 (⫾0.08)a

0.77 (⫾0.06)a 0.50 (⫾0.12)b

0.60 (⫾0.07)a 0.09 (⫾0.04)b

0.68 (⫾0.11)a 0.27 (⫾0.09)b

8.77 (⫾0.49)a 9.29 (⫾1.09)a

9.45 (⫾0.72)a 10.69 (⫾0.57)b

0.63 (⫾0.10)a 0.43 (⫾0.03)b

0.41 (⫾0.03)a 0.35 (⫾0.05)a

10.96 (⫾1.33) Ð 0.23 (0.02)a 0.14 (⫾0.10)a

17.26 (⫾1.14)a 14.68 (⫾0.67)b 0.32 (⫾0.03)a 0.42 (⫾0.03)b

Means within a column followed by the same letter are not signiÞcantly different according to Student t-test.

Table 7. N Dose A25⬚C 4 Dose B25⬚C 4 Dose C25⬚C 4 Dose B20⬚C 3

either species (F ⫽ 2.39, P ⫽ 0.16 for Ae. albopictus and F ⫽ 0.85, P ⫽ 0.39 for Cx. pipiens for which doses A and B only were considered), therefore implying that biomass is directly proportional to diet. As the temperature decreases from 25 to 20⬚C, the efÞciency in converting food into biomass declines by 35% in Ae. albopictus and by 33% in Cx. pipiens (Table 7). Based on the data regarding larval competition at 25⬚C and with different food ratios, it was observed that, with dose A (2.83 mg/larva), no competition occurs (RCCbiomass ⫽ 0.65); thus, the quantity of food seems sufÞcient for the regular development of both species (Fig. 4a; Table 8). An analysis of the average

Efficiency in converting food into biomass Ae. albopictus Cx. pipiens (Biomass/diet ratio ⫾ SD) (Biomass/diet ratio ⫾ SD) 0.13 (⫾0.01)ab 0.17 (⫾0.03)a 0.15 (⫾0.03)ab 0.11 (⫾0.02)b

0.11 (⫾0.01)a 0.09 (⫾0.03)a 0.017 (⫾0.01)b 0.06 (⫾0.02)c

Means within a column followed by the same letter are not significantly different according to Newman-Keuls test.

Fig. 4. Record of cumulative adults biomass produced in relation to the following competition ratios: (a) 2.83 mg/larva and T ⫽ 25⬚C; (b) 1.9 mg/larva and T ⫽ 25⬚C; (c) 0.83 mg/larva and T ⫽ 25⬚C; and (d) 1.9 mg/larva and T ⫽ 20⬚C. Parameter by linear regression between biomass produced and competition ratio.

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the two species at food doses B (both at 20 and 25⬚C) and C (Table 6). In Cx. pipiens, with dose C, only males emerged, indicating that food was insufÞcient to achieve the full development of females. An increase in the adult emergence rate of Cx. pipiens was observed from 9% at dose C to 73% at dose A; whereas Ae. albopictus at dose C was able to achieve 60% of adult emergence. The maximum adult emergence rate in Ae. albopictus was recorded at the intermediate dose B25⬚C (77%). Both species showed a decrease in the adult emergence ratio at 20⬚C compared with 25⬚C. In regard to larval development time, at dose A25⬚C, no signiÞcant differences were noted between the two species, whereas with dose B25⬚C, it was noted that Ae. albopictus developed more rapidly than Cx. pipiens by ⬇1 d. On the contrary, with dose B20⬚C, Ae. albopictus developed considerably slower than Cx. pipiens and took ⬇2.5 d longer (Table 6). With dose C, only malesÑwhose development is quicker than that of femalesÑ emerged for Cx. pipiens; it was not possible to make a complete comparison between the two species, but it seems clear that in conditions of extreme food paucity, Ae. albopictus show better performances. Regarding adult weight, Ae. albopictus tend to produce bigger adults at the three food doses tested at 25⬚C, whereas the opposite was the case for dose B20⬚C (Table 6). At a temperature of 25⬚C, the relationship between adult weight and food dose, which shows the foodbiomass conversion coefÞcient, is signiÞcantly higher in Ae. albopictus (F ⫽ 18.81, P ⫽ 0.0002), indicating that this species is more efÞcient in transforming food into biomass and consequently is better able to exploit food resources and to grow more rapidly (Table 7). Furthermore, it was noted that, at 25⬚C, the adult weight/food ratio had no correlation with dosage in

December 2003 Table 8.

CARRIERI ET AL.: COMPETITION BETWEEN Ae. albopictus AND Cx. pipiens

1319

Effect of competition on the adult weight means (mg)

Ae. albopictus/Cx. pipiens ratio

Cx. pipiens (adult weight ⫾ SD)

Male

Female

Total

4 4 4 4 4

0.48 ⫾ 0.04 0.44 ⫾ 0.07 0.50 ⫾ 0.03 0.53 ⫾ 0.10

0.81 ⫾ 0.08 0.76 ⫾ 0.17 0.70 ⫾ 0.33 0.86 ⫾ 0.03

0.63 ⫾ 0.10 0.58 ⫾ 0.07 0.54 ⫾ 0.03 0.63 ⫾ 0.12

4 3 4 4 4

0.35 ⫾ 0.04a 0.38 ⫾ 0.03a 0.43 ⫾ 0.02a 0.50 ⫾ 0.06b

0.51 ⫾ 0.06 0.53 ⫾ 0.12 0.61 ⫾ 0.05 0.65 ⫾ 0.05

0.41 ⫾ 0.04a 0.43 ⫾ 0.07a 0.52 ⫾ 0.02ab 0.56 ⫾ 0.07b

4 4 4 3 4

0.21 ⫾ 0.02a 0.26 ⫾ 0.04b 0.28 ⫾ 0.02b 0.34 ⫾ 0.04c

0.28 ⫾ 0.01a 0.35 ⫾ 0.08b 0.37 ⫾ 0.04b 0.47 ⫾ 0.03b

0.23 ⫾ 0.02a 0.30 ⫾ 0.05b 0.33 ⫾ 0.02b 0.39 ⫾ 0.03c

3 3 3 3 4

0.29 ⫾ 0.07 0.30 ⫾ 0.04 0.25 ⫾ 0.03 0.35 ⫾ 0.05

0.36 ⫾ 0.04 0.39 ⫾ 0.05 0.32 ⫾ 0.12 0.44 ⫾ 0.10

0.32 ⫾ 0.03 0.35 ⫾ 0.05 0.28 ⫾ 0.05 0.39 ⫾ 0.06

Male

Female

Total

0.51 ⫾ 0.06 0.45 ⫾ 0.09 0.43 ⫾ 0.10 0.42 ⫾ 0.04

0.63 ⫾ 0.16 0.53 ⫾ 0.10 0.45 ⫾ 0.18 0.44 ⫾ 0.01

0.58 ⫾ 0.12 0.49 ⫾ 0.09 0.44 ⫾ 0.13 0.43 ⫾ 0.03

0.30 ⫾ 0.06 0.44 ⫾ 0.09

0.24 ⫾ 0.02a 0.25 ⫾ 0.06a 0.26 ⫾ 0.02a 0.35 ⫾ 0.05b

0.24 ⫾ 0.04 0.25 ⫾ 0.06 0.25 ⫾ 0.02 0.30 ⫾ 0.03

0.14 ⫾ 0.10 0.41 ⫾ 0.09 0.34 ⫾ 0.08 0.36 ⫾ 0.10 0.35 ⫾ 0.10

0.14 ⫾ 0.10 0.33 ⫾ 0.18 0.39 ⫾ 0.24 0.23 ⫾ 0.13 0.47 ⫾ 0.15

0.39 ⫾ 0.11 0.38 ⫾ 0.16 0.33 ⫾ 0.09 0.42 ⫾ 0.03

Means within a column followed by the same letter are not signiÞcantly different according to Newman-Keuls test.

weight of emerging adults reveals no signiÞcant differences in relation to the competition ratio (F ⫽ 0.94 and P ⫽ 0.45 in Ae. albopictus; F ⫽ 2.1 and P ⫽ 0.15 in Cx. pipiens). In Cx. pipiens, however, it is possible to observe a progressive increase in weight as the Cx. pipiens/Ae. albopictus ratio diminishes. It could be presumed that the quantity of food administered exceeded the actual requirements of Ae. albopictus larvae; thus, as the ratio decreased, the quantity of food available to Cx. pipiens increased (Table 8). A high level of competition RCCb ⫽ 2.5 was observed at dose B (1.9 mg/larva; Fig. 4b). Moreover, signiÞcant differences were found in the average weight of adults at different competition ratios (Ae. albopictus, F ⫽ 6.85 and P ⫽ 0.007; Cx. pipiens, F ⫽ 5.72 and P ⫽ 0.013; Table 8). The weight of Ae. albopictus adults increases as the Cx. pipiens/Ae. albopictus ratio increases, whereas the weight of Cx. pipiens adults declines as the ratio decreases. This seems to suggest that Ae. albopictus larvae are better at taking food than Cx. pipiens larvae. When food is scarce (dose C, 0.95 mg/larva), there is a signiÞcant reduction in the average weight of Ae. albopictus but not in the percentage of emergence (Table 6). At the same food dose and conditions of competition, Cx. pipiens is not capable of reaching the adult stage. Even when isolated from Ae. albopictus, only few males developed (Fig. 4c). Aedes albopictus is thus capable of depriving Cx. pipiens of the food it needs to develop; in fact, even at this dose, a signiÞcant increase in weight may be observed as the Cx. pipiens/Ae. albopictus ratio increases (F ⫽ 13.5 and P ⫽ 0.0005).

At a temperature of 20⬚C and with the intermediate dose of 1.9 mg/larva, low competition was observed (RCC ⫽ 1.4; Fig. 4d). Moreover, at different competition ratios, no signiÞcant differences were found in the weight of emerging adults (F ⫽ 2.47, P ⫽ 0.14 for Ae. albopictus and F ⫽ 0.33, P ⫽ 0.80 for Cx. pipiens). Discussion InterspeciÞc competition occurs when individuals of different species coexist in an ecological niche and rely on the same resources, which are limited compared with their capability of exploiting them. In our particular case, where mosquito breeding places may be found almost exclusively in artiÞcial containers, the introduction of Ae. albopictus may result in forms of competition with Cx. pipiens that do not necessarily bring on the displacement of one of the two. In Northern Italy, the two species seem to show preferences for containers of different volumes and position with regard to their exposure to the sun. From our observations, it seems unlikely that the introduction of Ae. albopictus could bring about the exclusion of the indigenous species Cx. pipiens in a similar way to the case in North and Central Florida, where Ae. aegypti disappeared after the arrival of Ae. albopictus (OÕMeara et al. 1995, Juliano 1998). Under laboratory conditions, at 25⬚C, we observed that Ae. albopictus is more successful than Cx. pipiens in exploiting artiÞcial microhabitats when food is scarce, thanks to its greater efÞciency in converting food into biomass and rapidity in larval development. Thus, in conditions of food paucity, the two species are brought into competition, and Ae. albopictus prevail.

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A25⬚C 1:0 2:1 1:1 1:2 0:1 B25⬚C 1:0 2:1 1:1 1:2 0:1 C25⬚C 1:0 2:1 1:1 1:2 0:1 B20⬚C 1:0 2:1 1:1 1:2 0:1

Ae. albopictus (adult weight ⫾ SD)

N

1320

ENVIRONMENTAL ENTOMOLOGY Acknowledgments

The work was partially funded by the AUSSL 17 of Salo` and the Municipalities of Desenzano del Garda, Sirmione e Lonato.

References Cited Allan, S. A., and D. L. Kline. 1998. Larval rearing water and preexisting eggs inßuence oviposition by Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 35: 943Ð947. Alto, B. W., and S. A. Juliano. 2001a. Temperature effect on the dynamics of Aedes albopictus (Diptera: Culicidae) populations in the laboratory. J. Med. Entomol. 38: 548 Ð 556. Alto, B. W., and S. A. Juliano. 2001b. Precipitation and temperature effects on populations of Aedes albopictus (Diptera: Culicidae): implications for range expansion. J. Med. Entomol. 38: 646 Ð 656. Bellini, R., M. Carrieri, and A. Benedetti. 1994. Aedes albopictus a Desenzano del Garda: avvio di un programma di eradicazione. Disinfestazione. 11: 19 Ð23. Bellini, R., M. Carrieri, and A. Benedetti. 1995. Primo anno di attivita` del programma di lotta a Aedes albopictus a Desenzano del Garda. Disinfestazione. 12: 29 Ð34. Bellini, R., M. Carrieri, M. Bacchi, and A. Benedetti. 1996. Secondo anno di attivita` del programma di lotta ad Aedes albopictus a Desenzano del Garda, Sirmione e Lonato. Disinfestazione. 13: 55Ð 61. Bellini, R., M. Carrieri, M. Bacchi, and A. Benedetti. 1997. Terzo anno di attivita` del programma di lotta ad Aedes albopictus a Desenzano del Garda, Sirmione e Lonato. Disinfestazione. 14: 51Ð56. Black, W.C.I.V., K. S. Rai, B. J. Turco, and D. C. Arroyo. 1989. Laboratory study of competition between United States strains of Aedes albopictus and Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 26: 260 Ð271. Blackmore, M. S., G. A. Scoles, and G. B. Craig Jr. 1995. Parasitism of Aedes aegypti and Ae. albopictus (Diptera: Culicidae) by Ascogregarina spp. (Apicomplex: Lecudinidae) in Florida. J. Med. Entomol. 32: 847Ð 852. Briegel, H., and S. E. Timermann. 2001. Aedes albopictus (Diptera: Culicidae): physiological aspects of development and reproduction. J. Med. Entomol. 38: 566 Ð571. Brogdon, W. G. 1994. Measurement of ßight tone difference between female Aedes aegypti and Ae. albopictus (Diptera: Culicidae). J. Med. Entomol. 31: 700 Ð703. Celli, G., R. Bellini, and M. Carrieri. 1994. Survey on Aedes albopictus (Skuse) (Diptera: Culicidae) infestation in Desenzano del Garda (Brescia province-Italy). Boll. Ist. Entomol. “G. Grandi” Univ. Bologna. 48: 211Ð217. Dalla Pozza, G., and G. Majori. 1992. First record of Aedes albopictus establishment in Italy. J. Am. Mosq. Control Assoc. 8: 318 Ð320. Daugherty, M. P., B. W. Alto, and S. A. Juliano. 2000. Invertebrate carcasses as a resource for competing Aedes albopictus and Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 37: 364 Ð372. Harper, J. L. 1977. Population biology of plants. Academic Press, New York. Harper, J. P., and S. L. Paulson. 1994. Reproductive isolation between Florida strains of Aedes aegypti and Aedes albopictus. J. Am. Mosq. Control Assoc. 10: 88 Ð92. Hawley, W. A. 1988. The biology of Aedes albopictus. J. Am. Mosq. Control Assoc. 4(suppl 1): 1Ð 40. Ho, B. C., G. N. Khoo, L. M. Chew, K. P. Wong, and A. Ewert. 1992. Food ingestion and digestive enzymes in larval

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However, Ae. albopictus were observed to be more sensitive to low temperatures (the food-biomass conversion coefÞcient dropped signiÞcantly as the temperature was lowered from 25 to 20⬚C) than Cx. pipiens, and at 20⬚C, in conditions of food scarcity, the two species apparently manage to coexist with apparent low competition. While inßuencing the larval trophic activity (Briegel and Timermann 2001, Alto and Juliano 2001a, b), temperature could play an important role in the capacity of competition for food (Teng and Apperson 2000). Field observations seem to indicate that Ae. albopictus have colonized an habitat in the urban environment of Northern Italy that only partially overlaps with that occupied by Cx. pipiens. There is a good correlation between the volume of water in breeding sites and the overlap coefÞcient of the two species. Ae. albopictus seems to prevail in small-sized habitats, which, being more subject to the alternation between periods in which they contain water and others in which they are dry (related to climate conditions and/or to human activities), are better exploited by an Aedes ßood water species originally adapted to natural small water deposits. Culex pipiens, on the other hand, mainly colonize large containers where water stays for longer periods and is often permanent throughout the season, food resources are usually available in abundance, microorganism activity is very high, and oviposition can take place continuously. The two species seem to coexist successfully in medium-size containers (10 Ð50 liters). This study has also revealed substantial differences between the population trends of the two species during the breeding season. The Þrst species to start larval development in the springtime is Cx. pipiens, which predominates in larval habitats until July, whereas Ae. albopictus larvae appear some weeks later and progressively increase in number until they reach a seasonal peak in September. In conclusion, Ae. albopictus seems to have carved out its own ecological niche that only partly overlaps with that of Cx. pipiens, and within this habitat, in the case of food paucity, it is capable of competing successfully with the indigenous species. The two species are most likely to come into contact late in the season, during the months of August and September, in medium-sized containers (10 Ð50 liters), where the food resources are sufÞcient to allow the development of both. Therefore at present there seem to be no obstacles to the spread of Ae. albopictus deriving from competition with the indigenous species Cx. pipiens. Unless other factors intervene to limit its development or speciÞc preventive and pest-control strategies are adopted, it is reasonable to expect that Ae. albopictus will shortly becomeÑalso in view of its high anthropophily and vectorial capacityÑthe most important mosquito species in the urban areas of Italy.

Vol. 32, no. 6

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CARRIERI ET AL.: COMPETITION BETWEEN Ae. albopictus AND Cx. pipiens

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