Popul Ecol (2006) 48:59–70 DOI 10.1007/s10144-005-0243-y
O R I GI N A L A R T IC L E
Special feature: Global climate change and the dynamics of biological communities
Midori Tuda Æ Takashi Matsumoto Æ Takao Itioka Norio Ishida Æ Masaaki Takanashi Æ Wataru Ashihara Mitsuko Kohyama Æ Masami Takagi
Climatic and intertrophic effects detected in 10-year population dynamics of biological control of the arrowhead scale by two parasitoids in southwestern Japan Received: 18 May 2005 / Accepted: 1 October 2005 / Published online: 9 December 2005 The Society of Population Ecology and Springer-Verlag Tokyo 2005
Abstract Relative effects of weather and three-trophic interactions were studied for a classical biological control system consisting of the arrowhead scale Unaspis yanonensis, known formerly as a serious pest of the Satsuma mandarin orange Citrus unshiu, and its two introduced parasitoids, Coccobius fulvus and Aphytis yanonensis. Yearly population responses of the three insect species on a per-tree basis for up to 10 years at two orange groves were analyzed by general linear models, with a backward stepwise procedure, to select M. Tuda (&) Æ M. Takagi Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan E-mail:
[email protected] Tel.: +81-92-6423038 Fax: +81-92-6423040 M. Kohyama Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka, Japan T. Matsumoto Æ T. Itioka Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
among abiotic (summer/winter temperature and rainfall) and biotic (densities of the three insect species and orange bearing in the previous years) independent variables. Temperature positively affected the arrowhead scale and the two parasitoids. A negative correlation of rainfall was detected for all three insect species. Mandarin fruiting showed negative delayed density dependence, thereby supporting the observed alternate bearing phenomenon in mandarins, presumably due to physiological imbalance triggered by climatic factors. The arrowhead scale was negatively correlated with fruit production in the preceding years, possibly due to reduced resistance in subsequent years of mast fruiting. We found a negative correlation of the arrowhead scale with Coccobius only in a single grove and none with Aphytis. Thus, it appears that bottom-up forces may be more important than top-down control by the parasitoids in the post-transient phase of this system. Keywords Time series data Æ Endogenous versus exogenous factors Æ Diaspididae Æ Global warming Æ Spatial heterogeneity Æ Host-density dependence in parasitism
N. Ishida People’s Institute of Environment, Kyoto, Japan M. Takanashi Æ W. Ashihara Department of Citrus Research, National Institute of Fruit Tree Science, National Agriculture and Bio-oriented Research Organization, Nagasaki, Japan Present addresses: M. Takanashi Department of Integrated Research for Agriculture, National Agriculture Research Center for Tohoku Region, National Agriculture and Bio-oriented Research Organization, Morioka, Japan W. Ashihara Department of Plant Protection, National Institute of Fruit Tree Science, National Agriculture and Bio-oriented Research Organization, Tsukuba, Japan
Introduction The relative contribution of climatic factors and interacting species as regulating factors in population dynamics has been one of the recurring central themes in basic and applied ecology (Nicholson 1933; Andrewartha and Birch 1948; Milne 1957; DeBach 1958). Insects have been observed to respond to long-term environmental trends such as global warming. For single-species populations, a number of changes have been predicted – and observed – in response to global warming; these include latitudinal (poleward) and altitudinal (to higher elevation) shifts in distribution (Parmesan 1996; Parmesan et al. 1999), an increased number of generations
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for multivoltine species (Pollard and Yates 1993; Yamamura and Kiritani 1998), increased survival during winter (Bale et al. 1988) and prolonged diapause (Tauber et al. 1986). A consideration of interspecific interactions is inevitable in applying these single-species responses to the community level. As the number of interacting species increases with increasing number of trophic levels, it becomes more difficult to predict the response of these species because insect species, as other invertebrates, are conservative in their temperature requirement for development, survival and reproduction, which in turn will lead to differential responses to temperature rise (Bale et al 2002; Walther et al. 2002). This might cause phenological asynchrony between insect species, including hosts and their parasitoids, or between insect herbivores and plants (Bale et al. 2002). Laboratory experiments on biological assemblages have demonstrated complex outcomes of temperature increases on population dynamics of interacting species (Tuda and Fujii 1993; Tuda and Shimada 1995; Davis et al. 1998; Fox and Morin 2001). In addition to controlled laboratory experiments, numerous empirical approaches have been applied to estimate the response of biological assemblages to temperature increase; these include cross-geographical and cross-periodical comparisons and the detection of responses under extreme warming (Parmesan et al. 2000; Bale et al. 2002 and references therein; Kiritani 2006; Koike et al. 2006; Kudo and Hirao 2006; Yukawa and Akimoto 2006). Multivariate analysis should also serve as a useful tool to estimate the relative effect of changing temperature among other climatic factors and ecological interactions (Redfern and Hunter 2005; Yamamura et al. 2006). Exotic species tend to have simpler trophic interactions with fewer species of long-standing ecological and evolutionary association than do native species. This property is ideal for studying the impact of abiotic factors. Biological control systems, often with introduced pests and natural enemies, should serve as models to study the impact of climate change. By means of a crossgeographical comparison, DeBach (1958) first ascribed the different control effects of introduced natural enemies on a citrus pest scale to climatic factors. The arrowhead scale Unaspis yanonensis (Kuwana) (Hemiptera: Diaspididae) has been a serious pest of the Satsuma mandarin orange Citrus unshiu Marc. (Rutaceae) in southwestern Japan throughout most of the 20th century. It was first found in 1907 in the Nagasaki Prefecture, which is located in the western-end of Japan. By 1930, the domestic transportation of infested young trees had enabled this pest to spread over citrus-producing areas in Kyushu and the Pacific side of southwestern Japan (Okudai and Korenaga 1966; Okudai et al. 1968; Furuhashi and Ohkubo 1990). In 1980, two parasitoid species of the arrowhead scale were imported to Japan from China where the scale originated. Since then, the arrowhead scale has been controlled at lowdensity levels (Itioka et al. 1997; T. Ujiye, unpublished
data). A multivariate model has been applied to the population data collected on the arrowhead scale during the 1960s and 1970s for predicting scale population density and elucidated temperature and rainfall as commonly significant explanatory variables for the scale in the absence of specialized parasitoids (Korenaga et al. 1978, 1981). Our goal is to predict the future influence of global warming on the arrowhead scale population dynamics in association with its host plant and two introduced parasitoids. General linear models are applied to the population responses of the three species of insects and reproduction of the orange trees at two locations in Japan to elucidate the relative effects of weather and intertrophic interactions on the species studied. This study is also the first to consider possible effects of plant characteristics on the biological control system of the arrowhead scale.
Materials and methods Insects and plant Females of the arrowhead scale Unaspis yanonensis are sessile; after dispersal from maternal scales as the first instar larvae, called crawlers, they settle down on nearby leaves of citrus plants for development and reproduction for the rest of their life. The primary host plant of U. yanonensis is the Satsuma mandarin orange, Citrus unshiu, which is grown throughout the southwestern part of Japan. The two parasitoids imported to Japan as control agents were an endoparasitic specialist Coccobius fulvus (Compere et Annecke) (Hymenoptera: Aphelinidae) and an ectoparasitic generalist Aphytis yanonensis DeBach et Rosen (Hymenoptera: Aphelinidae). The yearly number of generations is two to three for the arrowhead scale (Ohgushi 1969), four to six for Coccobius and 10–12 for Aphytis (Takagi 1983; Ogata 1987; Takagi and Ogata 1990; Furuhashi and Ohkubo 1990). The arrowhead scale reproduces in May, August and, depending on the temperature during late summer (Okudai et al. 1974), partially in October in western through central Japan. A. yanonensis is thelytokous, reproducing asexually. Mandarins and mandarin hybrids are known for their alternate bearing, which is due to nutritional and hormonal imbalance triggered by climatic factors (Monseliese and Goldschmidt 1982; Spiegel-Roy and Goldschmidt 1996), such as heat spells during flower bud formation in the spring and cold weather during the winter (Spiegel-Roy and Goldschmidt 1996; Kihara and Konakahara 2000). The mandarin orange trees bloom in the spring to produce fruits that mature in the fall. The yearly production of the Satsuma mandarin orange is variable, with an approximately biennial cycle that is geographically in synchrony, especially over prefectures in southwestern Japan (Kihara and Konakahara 2000).
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Orange groves Population densities of the insects were monitored at two sites (Fig. 1). The first is an experimental grove of the Department of Citrus Research, National Institute of Fruit Tree Science in Kuchinotsu Town, Nagasaki Prefecture in western Japan (3236¢N, 13011¢E), where one of the first releases of the two parasitoids was practiced. The grove is 1400 m2 in size and is situated on the south side of a hill on a cliff by the sea. The two parasitoids (50 females of Coccobius with males and 1,000 females of Aphytis) were first released in 1981; since then, the density of the arrowhead scale has shown cyclic changes at lower levels (T. Ujiye, unpublished data). The populations of the two parasitoids at this grove have shown oscillatory fluctuations out-of-phase with each other. Neither insecticides nor fertilizer were used during the census period. The second grove is approximately 5,000 m2 in size and is situated in Shimotsu Town, Wakayama Prefecture (3406¢N, 13512¢E) in the eastern part of southwestern Japan (Itioka et al. 1997). The two parasitoids (175 females of Coccobius with males and 175 females of Aphytis) were first released here in 1987, and the arrowhead scale has been maintained at low-density levels since about 1993 (Itioka et al. 1997; Matsumoto et al. 2003b). Neither insecticides nor fertilizer were used during the census period (Itioka et al. 1997; Matsumoto et al. 2004c). Data In Nagasaki, 50 leaves from individual mandarin trees were sampled in late December of each year from 1995 to 2003 and examined for the non-reproductive and reproductive (or mature) adult stages of the arrowhead
Fig. 1 Geographical location of the two groves. The dotted lines indicate the boundaries of prefectures
scale. A maximum of 57 trees of the 65 fully grown trees that were planted at a between-tree spacing of 2.8±1.0 m (mean ± SD, n=20) were monitored. In Wakayama, up to 600 leaves from each of a maximum of 16 trees of the approximately 500 fully grown trees planted at a between-tree spacing of 2.7±0.2 m (mean ± SD, n=37) were sampled in November of each year from 1993 to 2002. Adult scales were classified as: 1, live; 2, dead from unknown cause; 3, preyed upon (with damaged scale covers); 4, parasitized (with live/ dead larvae/pupae or with emergence holes). Live hosts were dissected to detect larvae of Coccobius. We disregarded adults that had been predated or that had a parasitoid emergence hole in order to minimize overestimation of scale cover remains that might have been attached to leaves for 1 year or more. Loge-transformed per-leaf densities of adult scales (H), Coccobius (C) and Aphytis (A) in year t were calculated for tree i, following Yamamura (1999)’s transformation: Ht; i = ln hsum; t; i + 0.5 /nt; i ; ð1Þ Ct; i = ln hC; t; i + 0.5 /nt; i ; At; i = ln hA; t; i + 0.5 /nt; i ; where hsum, t, i is the summed number of live and dead (from unknown cause) adult hosts on tree i, hC, t, i is the number of adult hosts with larvae and pupae of Coccobius on tree i, hA, t, i, the number of adult hosts with larvae and pupae of Aphytis on tree i and nt, i the number of leaves sampled from tree i, in year t. For an estimation of the yearly production of oranges, we calculated the number of fruits per tree at the study grove for Wakayama. For Nagasaki, because of a lack of data from the study grove, we used the prefectural agricultural statistics of mandarin orange bearing and area of reproducing trees, based on the strong synchrony of bearing over groves (Nagasaki Prefecture 2001, 2004). Therefore, the definition of mean production of fruits is slightly different between the groves: Ot = ln otot; t /ht ; ð2Þ where otot, t is either the total weight of fruit bearing (for Nagasaki) or the total number of fruits (for Wakayama), and ht is either the area of reproducing trees (for Nagasaki) or the number of trees (for Wakayama), in year t. There were no significant correlations in intraspecific density between the two groves for years that overlapped (the orange, r=0.214, df=6, P>0.6; the scale, r=0.398, df=6, P>0.3; Coccobius, r=0.207, df=6, P>0.6; Aphytis, r=0.0909, df=6, P>0.8). Monthly weather data were retrieved from the AMeDAS database (Japan Meteorological Agency; http://www.data.kishou.go.jp/etrn/index.html) for those monitored at the observatories in Kuchinotsu, Nagasaki (3236¢N, 13011¢E) and Wakayama City, Wakayama (3413¢N, 13509¢E), which are the two meteorological stations closest to each of the respective study grove. The mean monthly temperatures and total rainfall were
62 Fig. 2 a Temperature in Nagasaki, b temperature in Wakayama, c rainfall in Nagasaki, d rainfall in Wakayama. Circle Winter, square summer
a
b
c
d
calculated for the winter (January through May for Nagasaki; December through May for Wakayama; these months correspond to the season during which the overwintered generation of the scale – i.e. the second and third generations of the previous years – develops and reproduces) and the summer (June through December for Nagasaki; June through November for Wakayama; these months correspond to the season in which the first and second generations of the scale develop and reproduce and the third generation develops). The winter and summer temperatures were 12.3±0.7C (mean ± SD, n=8) and 20.9±0.3C in Nagasaki and 11.0±0.7C (n=9) and 22.8±0.5C in Wakayama. The winter and summer rainfall was 502±143 and 1,247±197 mm in Nagasaki and 500±188 and 753±248 mm in Wakayama. The climate at the two locations was significantly correlated with each other for temperature over the 7 years that overlapped between the two sites (winter, r=0.955, P0.3; summer, t=0.607, P>0.5) or rainfall (Nagasaki, winter, t=0.0135, P>0.9; summer, t=1.04, P>0.3; Wakayama, winter, t=0.306, P>0.7; summer, t=0.211, P>0.8) over the census period. Statistical analyses were performed using JMP 4.0 (SAS Institute 2000).
30
Orange bearing (t/ha)
PC; t; j
Abiotic factors
25
20
1996
1998
2000
2002
2004
2000
2002
2004
2000
2002
2004
Year
b 0.4
0.2
1994
Prediction under future climate change
1996
1998 Year
Density of parasitoids
For future change in climate at the two locations, we used 10·10-km mesh monthly weather data for the yearly periods 1981–2000 (current) and 2031–2050 (future) (Nishimori et al. 2005). The data for 1981–2000 are based on AMeDAS, while the prediction for 2031–2050 is derived based on 20·20-km resolution data predicted by Meteorological Research Institute (Nishimori et al. 2005). These researchers employed an A2 family scenario, assuming heterogeneous population growth without sustainability (IPCC 2000).
a
15 1994
Density of arrowhead scale
PC; t; i ¼ arcsinf½hC; t; i =ðhsum; t; i þ hC; t; i þ hA; t; i Þ2 g; 1 PA; t; i ¼ arcsinf½hA; t; i =ðhsum; t; i þ hC; t; i þ hA; t; i Þ2 g ;
Nagasaki grove) and Fig. 4 (for the Wakayama grove). Analyses of population responses using Eq. 4 detected both abiotic and biotic effects on all four species, a large proportion of which were in congruence at the two study groves (Tables 1, 2).
0.20
c 0.15 0.10 0.05 0.00 1994
1996
1998 Year
Results Population dynamics of the arrowhead scale and the two introduced parasitoids are shown in Fig. 3 (for the
Fig. 3 a Mean production (t/ha) of the Satsuma mandarin orange Citrus unshiu in Nagasaki Prefecture. b Per-leaf density of female adults of the arrowhead scale Unaspis yanonensis and c Per-leaf density of the larvae and pupae of the two parasitoids, Coccobius fulvus (solid line) and Aphytis yanonensis (dashed line), at the Nagasaki grove. Tree-wise mean ± standard error (SE)
64
Orange bearing (/tree)
300
a 200
100
0 1990
1995
2000
2005
Year
Density of arrowhead scale
0.10
b
of the previous years and negatively with orange bearing and Coccobius density of the previous years (Table 1). Population responses of all three insect species were negatively correlated with conspecific densities (Tables 1, 2). Interactions between any two significant biotic main effects (i.e. preceding densities) on population responses of the three insect species were tested further but none of them were significant. The population response of orange bearing was also negatively related with the bearing of the previous years (Tables 1, 2). Host-density dependence in parasitism
0.05
No host-density dependence in parasitism rate was found in either species of parasitoid at either the tree level or the grove level (Table 3). The lack of host-density dependence was observed at all spatial scales (Table 3).
0.00
-0.05 1990
1995
2000
2005
Year
Prediction under future climate change
Density of parasitoids
0.015
c 0.010
0.005
0.000
-0.005 1990
1995
2000
2005
Predicted temperature and rainfall changes at the two locations for the years 2031–2050 compared to those for 1981–2000 are shown in Table 4. Both temperature and rainfall are predicted to increase irrespective of seasons, and the trend is in common to both groves. Based on these predictions, changes in the population densities of the organisms studied were further estimated with the model selected earlier in the present study (Tables 1, 2): for Nagasaki, future densities are predicted by the equations
Year
Fig. 4 a Mean bearing (number of fruits/tree) of the Satsuma mandarin orange at the Wakayama grove. b Per-leaf density of female adults of the arrowhead scale and c per-leaf density of the two parasitoids, C. fulvus (solid line) and A. yanonensis (dashed line), at the Wakayama grove. Tree-wise mean ± SE
for the Coccobius population response at both groves (Tables 1, 2). Correlations with summer rainfall were negative with the population responses of the arrowhead scale and Aphytis and either positive or negative with that of Coccobius (Tables 1, 2). Biotic factors The population response of the arrowhead scale was negatively related with orange production at both groves and with Coccobius density of the previous year at the Nagasaki grove (Tables 1, 2). In contrast, no negative delay effect of Aphytis density on the arrowhead scale was found (Table 1). For the population response of Coccobius, a decreasing trend was detected at the two groves (Tables 1, 2). There were no interspecific correlations in congruence at both sites (Tables 1, 2). For Aphytis at the Nagasaki grove, the population response was correlated positively with the scale density
Otþ1 ¼ Ot 1:91 Ot þ 0:0569 T wt ; Ytþ1 ¼ Yt 0:600 Ot 1:02 Yt 0:703 Ct þ 0:0705 T wt 0:000487 Rst ; Ctþ1 ¼ Ct þ 0:0665 Yt 1:42 Ct þ 0:0505 T wt 0:0640 T st þ 0:000157 Rst 0:0332; Atþ1 ¼ At 0:262 Ot þ 0:0732 Yt 0:218 Ct 1:57 At þ 0:0921 T st 0:000196 Rst ; ð6Þ where Twt and Tst are the monthly mean temperatures for the winter and summer, respectively, and Rwt and Rst are the total rainfall for winter and summer, respectively, all of the year t. For Wakayama, population densities are predicted by the equations Otþ1 ¼ Ot 1:31 Ot ; Ytþ1 ¼ Yt 0:672 Ot 0:712 Yt þ 1:07 T wt 0:00271 Rwt 0:160; Ctþ1 ¼ Ct 0:835 Ct þ 0:484 T wt 0:00198 Rwt 0:172:
ð7Þ
For the initial densities for the simulation, the density data of the final year were applied. Temperature and rainfall are assumed to rise gradually to reach the final
65 a
Table 1 Result of the general linear model analysis on yearly (cross-generation) population responses of orange bearing, the arrowhead scale (Unaspis yanonensis) and its two parasitoids Coccobius and Aphytis at the grove in Nagasaki Independent variable
Population response (dependent variable)
Previous-year density (loge-transformed) Orange F
Orange
Arrowhead scale
512.6 (1)*** 1.91 –b
17.6 (1)*** 0.600 96.8 (1)*** 1.02 7.42 (1)** 0.703 ns
Arrowhead scale
F
Coccobius
F
–
Aphytis
F
–
Temperature (C) Winter
F
7.59 (1)* 0.0569 ns
Rainfall (mm) Summer
F
ns
Time (year)
F
ns
Summer
Tree Constant R2 n Model
F
F
F (df)
6.06 (1)* 0.0705 ns 11.0 (1)** 0.000487 ns
– 5.19*** 0.988 9 256.4 (2)***
1.44 (56)* ns 0.701 183 4.66 (61)***
Coccobius
ns 2.57 (1) ns 0.0665 162.6 (1)*** 1.42 ns
Aphytis 33.5 (1)*** 0.262 6.87 (1)** 0.0732 13.3 (1)*** 0.218 145 (1)*** 1.57
15.5 (1)*** 0.0505 6.13 (1)* 0.0640
ns
14.6 (1)*** 0.000157 16.5 (1)*** 0.0332 1.29 ns 66.1*** 0.755 183 5.97 (62)***
23.2 (1)*** 0.000196 ns
14.7 (1)*** 0.0921
1.81 (56)** 1.99*** 0.756 183 6.00 (62)***
*P
