RESOURCE DEPENDENT STABILITY IN AN EXPERIMENTAL LABORATORY RESOURCE-HERBIVORE-CARNIVORE SYSTEM

Transcription

1 Res. Popul. Ecol. (1983) Suppl. 3, RESOURCE DEPENDENT STABLTY N AN EXPERMENTAL LABORATORY RESOURCE-HERBVORE-CARNVORE SYSTEM Koichi Fuj nstitute of Biological Sciences, Univei-sity of Tsukuba, Sakura-Mura, baraki~305 Japan NTRODUCTON Predation and interspecific competition are probably the two most important biotic interactions among species that maintain the dynamics and structure of a community. There are, however, arguments against the relative importance of interspecific com- petition (e.g., CONNELL, 1980). Many predictive mathematical models describe predation Systems (e.g., LOTKA, 1925; VOLTERRA, 1926; NCHOLSON and BALEY, 1935; HASSELL, 1978). But in spite of considerable work on them, most of the experimentation to test the results predicted by these models have failed'to establish coexisting predation systems for Continuous study in a homogeneous environment. At present, mathematical models on predation have advanced far beyond empirical validation. A solid experimental basis must be established not only to test the existing and forthcoming mathematical models, but also to advance the theory of community ecology which relies on a firm understanding of each of the component systems of a community. HUFFAKER (1958), using two species of mites, one a predator, prolonged per- sistence in a predator-prey system. However, this was achieved by artificially alternat- ing the dispersal abilities of both species. The system persisted as a whole, with local extinctions here and there. These systems, therefore, can be interpreted as mimicing the complexity and heterogeneity found in nature. GAUSE (1934) tested the Lotka-Volterra predation model with Paramecium cau- datum (prey) and Didinium nasulum. Coexistence was achieved only by periodic addition of P. caudatum just before the extinction of Didinium. LUCKNBLL (1973) obtained a coexisting predation system with Paramecium aurelia (prey) and D. nasutum by adding methyl cellulose into the medium to reduce the rate of movement of both predator and prey, making the contact between them less frequent. UTDA (1953, 1955, 1956, 1957) has reported the only empirical results Of persistent predation without excessive artifcial manipulation. He studied predation on the azuki bean weevil, Callosobruchus chinensis by its parasitic wasps, Heterospilus prosopidis and Anisopteromalus calandrae.* n this report, would like to discuss the results of laboratory investigations on * nitially identified as Neocatolaccus mamezophagus, but later confirmed to be A. calandrae (TAcnmAWA, 1966).

2 16 the effects of types of resources (beans) and kinds of parasitic wasps on the bean-bean weevil-parasitic wasp system with regard to the current theories of predation and community dynamics. MATERALS AND METHODS Experimental systems consisting of a resource (bean), a herbivore (bean weevil), and a carnivore (parasitic wasp) were established. Three different species of beans, the azuki bean (Vigna angularis), the blackeye bean (V. u guiculata), and the Red Kidney bean (Phaseolus vulgaris), were selected as resources. The herbivore, the Mexican bean weevil, Zabroles subfascialus (KS) has been maintained for years in our aboratory on azuki beans under the constant environmental condition of 30~ and 70% r.h. One of the carnivore species (the parasitic wasps), Anisopteromalus calandrae (ja), has also been maintained for years in our laboratory on the larvae of the azuki bean weevil, C. chinensis, which feeds on the azuki bean. Another species of parasitic wasp, tteterospilus prosopidis (hp), was introduced into our laboratory from Hawaii in 1975 and has been maintained in the same way as A. calandrae. KS completes its development from egg to adult emergence in ca. 4 weeks, continues to lay eggs for about one week after emergence. On the other hand, ja and hp complete their development in less than 2 weeks. This asynchrony of prey and predator metamorphosis prevented establishment of a discrete-generation system. The following new procedure made the persistent predation system as well as a nearly continuous system possible. The experimental universe was maintained in a 4-compartment Petri dish (Falcon ~1009), at the top of which a l era diameter hole was drilled and covered with cheese cloth. A experiments were run at 30~ and both 70% r.h. with constant illumination. Five g of fresh beans and 8 pairs of KS adults emerged within 24hrs from the stock culture were placed in compartment. Ten days later, 5g of beans, 8 pairs of KS adults, and 4 pairs of fresh wasps from stock culture, when two wasp species were employed simultaneously, or 2 pairs of each species were introduced into com- partment. On day 20, the same procedure as on day 10 was followed in compart- ment. On day 30, only 5g of fresh beans were added to compartment V. Subsequently, on every 10th day, the compartment with the oldest beans was replaced with 5g of fresh beans. A population census was made each time when beans were replaced. ndividuals were anesthetized, removed from the Petri dish, sorted, and counted according to species and, dead and living within species. The live individuals were then returned to the Petri dish after counting. Each system was usually maintained until one of the component species was eliminated. Sometimes the system was restarted after the elimination of wasp species by reintroduction of the same wasp species (usually 4 pairs).

3 17 Resource-herbivore systems were also established to control for the absence of herbivore-carnivore interaction. Three replicates of each of the 12 possible resource- herbivore-carnivore combinations (Fig. 1) were assessed except in the case of the P. vulgaris experiment for which there were only two. RESULTS n most systems, the species which were eliminated and the patterns of popu- lation dynamics of each species were not significantly different among the replicates. The results of one replicate from each combination are presented here as typical, and the results of other replicates are mentioned only when they show a meaningful difference. Figure 2 shows the typical system dynamics of 4 combinations when the azuki hp ja hp ja \/ KS KS KS KS AZUK AZUK AZUK AZUK KS BLACKEYE hp ja hp ja \/ KS KS KS ) BLACKEYE BLACKEYE BLACKEYE KS RED KDNEY hp ja hp ja 1 1 \/ KS KS KS RED KDNEY RED KDNEY RED KDNEY Fig resource-herbivore-carnivore-combinations studied. KS; Mexican bean weevil, hp; parasitic wasp, t. prosopidis, and ja; parasitic wasp, A. calamtrae.

4 18 A?. -- ~zoo ~ t ~_ 1oo Z 84 l 9 ~J... ~ - f 1~ 200 3OO 4OO 500 6~ :SOO L-.- K2 KS hp 7 Azukl in,\ ',Jl "i o O OO k~o0 Ks o---o ts ~ i= C Azu~i -- z ~oo ~o / ~ ~.,/ '%. ~ ~..,,., - ~,.~,7 -. ~ ' ~,,, _..,.,..... o"%~ 40 "s- 4~ 40 4; o'o KS (hp 9 j~ ~7...,. ~( o.s-- + \ / y ,oo f '~176! ~~176 '~ soo t.oot t,oo 8~176 TME (DAYS] Fig. 2. Numbers of ]Jve adu ts at each census time with azuki beans. Arrow shows the time of extinction. Double arrow shows the time of reintroduction. O--Q; KS weevil, []... []; lap wasp, ; ja wasp.

5 19 bean was used as the resource. When there was no wasp (Fig. 2A), the number of live adults at each census time was between 100 and 300 with a mean of 176. The coefficient of variation through the entire period was 35%. When hp was added (Fig. 2B), it was eliminated from the system on day 680 in this replicate. During this period the adult population sizes of the coexisting herbivore and carnivore fluctuated markedly. The mean adult weevil population size was 70 with a coefficient of variation of 110%. This figure is more than 3 times that of the control population. The mean adult wasp population size was 36, with a 100% coefficient of variation. n this particular system, another replicate showed a similar pattern to that shown in Fig. 2 but hp was eliminated by day 590. n the third replicate, however, hp was extinct by day 160, a result still consistent with other replicates, considering the divergent population numbers of both KS and hp (Fig. 2B). When ja was introduced, the numbers of herbivores and carnivores were significantly different from the hp system (Fig. 2C). The herbivore and carnivore coexisted during the entire experimental period with minor population fluctuations in all three replicates. n the particular replicate shown in the Fig. 2(2, the mean population size of KS was 103 adults with a 24% coefficient of variation, smaller than the control. The mean population size of ja was 41 with a 34% coefficient of variation. When hp and ja were introduced simultaneously, the system dynamics were more stochastic, i.e., replicate dependent. n one replicate (Fig. 2D), both wasp species were extinct early, ]a by day 150 and hp by day 210. Thereafter the system only contained the resource and herbivore. On day 250, 4 ja pairs were introduced. The new system stayed relatively stable as in other azuki bean-ks-ja experiment until hp was introduced into the system on day 530. Then, as previously observed, ja was extinct by day 620, followed by hp by day 670, and the system was reduced to resource-herbivore again. Another replicate followed a similar pattern as both wasp species were not present by day 170. However, in the third replicate hp was eliminated by day 190, resulting in the azuki bean-ks-is system. After this replicate was simplified, it developed into the same pattern of coexistence of herbivore and carnivore as exhibited by the three replicates of the azuki bean-ks-ja combination. The typical system dynamics when blackeye beans were used at resource level are shown in Figure 3. The population size of live bean weevil adults in the control system was 175 with a coefficient of variation of 23%. The mean adult population size was almost identical to that of the azuki beans experiment, with a similar coefficient of variation. However, when the carnivores were introduced, the destinies of the systems were very different from those with azuki beans. When hp was introduced (Fig. 3B) it lasted only 80 days and although the KS population was close to extinction, a small number of weevils apparently escaped predation and recovered to a level comparable to the control. When hp was introduced on day 190 again, all the bean weevils were parasitized and extinct by day 250 and hp subsequently were not present

6 ~+~ 0 o~ ~o (0,~+ o~ +.~ ~e 8 m S7VN(]AON -O ~3BV~AN 0,.a o~ ~0 7 o $7vJTOJAJON! 40 ~138~17N

7 21 in the system by day 260. When ja was introduced into the blackeye-ks system, KS was gone by day 50, followed by ja by day 70 (Fig. 3C). When both hp and ja wasps were introduced simultaneously, KS was eliminated by day 50, followed by hp by day 60 and ja by day 70 (Fig. 3D). Figure 4 shows the typical system dynamics when Red Kidney beans were the resource. n the replicate illustrated (Fig. 4A), the mean population size of live adult weevils at each census time was 114, with a coefficient of variation of 36% without any wasp. The number of live adults at each census time seemed to be cyclic with a period of about 50 days. The cause of the cyclic fluctuations is not understood. 300 A 300 B 01 KS+ Q2 hp+ t c ~ KS Red Kidney oio KS KS m---u hp + Red Kidney J O0 300 TME (DAYS) 03 C jo 9 o--o KS n o o ja KS + Red Kidney 0 - ~"t:l *'~i ~hi'~l~"t 1 "r l"a" 0 f,oo t 200 t 300 TME (DAYS) 300 Q4 KS D----o hp o-...4 jo D,.~176 Red ~+Sflney loo 100 O'~D. ~A.._ -X'~-'@"d"~"t"av~.- t - i *oo r 200 '~ 300 TME (DAYS) 9 9 ~ "~d~, t f,oo t2~176 Cf 300 TME (DAYS) Fig. 4. Numbers of live adults at each census time with Red Kidney beans. legend, see Fig. 2. For

8 22 They were not observed in either the azuki or blackeye beans experiments. When either hp or ja or both simultaneously were introduced, they could not parasitize enough bean weevils to replace their numbers and in a short period of time dwindled to nothing. n these experiments the herbivore population was not affected significanty by the presence of wasp species. DSCUSSON Several striking generalizations can be made about the resource-herbivore-carnivore system of this study'. Figure 5 illustrates the transitions of the systems for each combination and the duration of each stage for all replicates. Clearly there is little variation among the replicates within each system. Also the times required for transition are very similar among replicates. Most of the systems become simplified into either the resource-herbivore or resource-only fate. The general view that the more complex system (with predator or predators) promotes the stability as defined by the coexistence of more species can clearly be dismissed in the present systems. The characteristic fate of a system with two cointroduced predators will be the same as that of a system having the single more unstable predator in it. Blackeye beans apparently made the bean weevils easily detected and thereby overexploited by the predator. On the other hand, Red Kidney beans made it difficult for the predator to find the prey and unable to survive. Therefore, further experiment is necessary to observe the destinies of the systems with two resources, blackeye and Red Kidney beans. Such experiments will test the stabilizing effect of diversity at the lowest level in the predation system. Although the weevils at the herbivore level are different, the biology of the organisms and procedures of our experiments are similar to UTDA's (1953, 1955, 1956, 1957) and the results are comparable when azuki bean is the resource. The ja wasp in combination with either species of weevil keeps the systems more stable than hp does. All of the replicates (UTDA, 1956) using ja maintained a complete set of the component species of all trophic levels through ca. 20 generations over 400 days. n his hp experiments (UTDA, 1953) 3 remained complete (25 generations over 500 days) and 3 degenerated to one of the two simpler forms. Our results confirm those of UTDA although the population numbers of Mexican weevils and wasps fluctuated more. Minor differences between UTDA's and our systems, however, cause quite different consequences when two wasp species are introduced simultaneously. n the azuki bean-azuki bean weevil-(hp+ja) combination (UTDA, 1955), the two wasp species coexisted for more than 1300 days. Coexistence lasted for about 200 days in our azuki bean-ks- (hp+ja) regimes (Figs. 2 and 5). Although UTDA has mentioned (personal communication) that coexistence was maintained in only one replicate of several and that the populations of the wasps were not always stable, it is unlikely that our combination would have remained stable for a long period of time. The reason for these differences may lie in the hp's more efficient foraging behavior. Details of the biological mecha-

9 23 A B C %~4 P4 (70) (190) P8 (=80) P12 ('-80) 1 Ks. hp.jo f"... ] L ~ M2(590) ~ K4 {o260] K3 (>700) P2 (110)~ t K2(690) ~ M4(~q70) M5(>700) P6(80) ~. P5(70) N2(160) "~ '~ N3(>450) P10(110) ~ P7(80) [ - ~ Pli(70) KS hp jo i Q4 (4100) Q8 (~00) o2(so,'b.. /o3,7o) Y iblaoke E E0 K'O"EYJ o KS : Mexican Bean Weevil (Zabrotes subfasciatus) hp : Parasitic Wasp 1 (Heterospilus prosopidis) ja : Parasitic Wasp 2 (Anisopteromalus calandrae) Fig. 5. Summary diagramm showing the system transition with time. Arrow shows the direction of change. The figure next to the arrow shows the code name of the replicate, with time required (days) for transition in parenthesis. nisms require further investigation. t is often argued that the prudent predator can bring the predation system to stability (e.g., SLOBODK[N, 1961). What is the exact biological characteristic of a predator to make it prudent? The two species of parasitic wasps, especially ja, could be said to be prudent predators when the prey lives in azuki bean. However, they easily overexploit, exterminate or nearly exterminate the prey when they live in blackeye. On the other hand, when the prey live in Red Kidney, they cannot exploit the prey even to the point of replacing their own numbers for a long period of time. Stability depends primarily on the predator's ability to seek out prey living in the resource. The primary characteristic for a prudent predator may be the modest searching ability. t is also clear that searching ability is not species specific, resource dependent. The beans in which the herbivore lives has a physiological effect on the carnivore. n the azuki bean both hp and ja adults live for about one week, but during which time females lay eggs on host larvae. However, when the host lives in the blackeye bean, ja females live for over 4 weeks and continue laying eggs during this period (Fuj, in manuscript). Apparently ja females use the host larvae not only for an oviposition site but also as a source of nutrition. This prolongation of female longevity and the accompanying increase in fecundity are other reasons why both of the blackeye bean

10 24 experimental systems with ja always crashed into a bean-only system in a relatively short period of time (Fig. 5). HUFFAKER's (1958) elegant experiments with two species of mites gave evidence in support of the prey-predator coexistence idea. Although both species of mites coexisted in the experimental universe, in the individual subareas in the universe the prey either increased in the absence of the predator or rapidly decreased with the predator present. This experiment is often cited to show the importance of the spatial heterogeneity in stabilizing and maintaining stability in communities. Spatial heterogeneity supplies a refuge for prey species. n our experiments no comparable spatial heterogeneity provided refuge for the prey. The experimental universe is small enough that each predator can seek out all available prey. There may be a temporal refuge when prey cannot be exploited for any reason. For example, the parasitic wasp can exploit the prey only at late larval (occasionally early pupal) stages. Consequently, the prey at other developmental stages can escape predation. Since bean weevils pupate near the surface of the bean, every prey is susceptible to predation during this period irrespective of the size of the bean. Further evidence that there is no spatial refuge for the prey is shown by the fact that the azuki bean system was the most stable even though Red Kidney and blackeye beans are both larger. The temporal refuge can be effective for the prey when its susceptible stage coincides with a period of low predator population density. This is apparently the reason for the wide fluctuation of the KS population size in the azuki-ks-hp system during day 200 and 350 (Fig. 2B). During this period, in spite of the fact that beans were supplied at 10 day intervals, the adult herbivore population showed peaks every 30 days, which roughly corresponds to one-generation period. As a consequence the system operated freely, nearly corresponding to the discrete generation time. The wasp species develop much faster and cannot synchronize well if the prey exists in a discrete generation. Consequently, during time interval of "discrete generations" the predator population remained very low. Once the discrete generation period is finished (around day 400), the predator began exploiting prey more efficiently, bringing the prey population to near extinction. Eventually the predator population would go extinct, unable to find enough prey to lay eggs. The temporal refuge can be effective for prolonging the time of coexistence of prey and predator in relatively discrete generation systems if their life cycles are asynchronous. However, temporal refuge cannot work as the stabilizing factor of the predation system. SUMMARY Long term predation systems were studied in the laboratory. Three species of beans (azuki bean, blackeye bean, and Red Kidney bean) were the resources, one species of bean weevil (Mexican bean weevil (KS)) the herbivore, and two species

11 25 of parasitic wasps (Anisopteromalus calandrae (ja), and Heterospilus prosopidis (hp)) the carnivores. Several combinations of the three components were maintained for up to 770 days. System persistence was dependent on the combination of species. The azuki bean-ks-ja system was the most stable; the herbivore and carnivore coexisted during the entire period of time (over 700 days). The azuki-ks-hp system was less stable, and hp wasp was eventually eliminated. Stability was primarily dependent on the species of carnivore due to differences in their searching ability. The blackeye-ks-ja system always ended with the extinction of both herbivore and carnivore in a short period of time, although the blackeye-ks-hp system termina- ted with blackeye-ks. The stability of predation system is also heavily dependent on the kind of resources on which prey lives. When the two species of wasps were introduced simultaneously, the unstable one (hp with azuki, and ja with blackeye) characterized the system dynamics. The effect of stabilizing species was minimal. Thus random introduction of more predator species did not make the system more stable. ACKNOWLEDGEMENTS: benefited a lot from discussions with Professor Emeritus Syunro UTVA. thank Professor Larry B. LxvvLs of Long sland University for his reading and corrections of the earlier manuscript. This work was supported in part by grant from National Science Foun- dation of U.S.A. (DEB ) and by Grant-in-Aid (No and ) from Ministry of Education, Science and Culture of Japan. REFERENCES CONNBLL, J.H. (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos, 35: GAusE, G.F. (1934) The struggle for existence. Williams and Wilkins. Baltimore. HASSELL, M.P. (1978) The dynamics of arthropod predator-prey systems. Princeton Univ. Press, Princeton, N.J. HUFFAKER, C.B. (1958) Experimental studies on predation: dispersion factors and predator-prey oscillations. Hilgardia 27: LOTKA, A.J. (1925) Elements of physical biology. Williams and Wilkins, Baltimore. LUCXmBLL, L.S. (1973) Coexistence in laboratory populations of Paramecium aurelia and its predator Didinium nasutum. Ecology 54: Nic~oLsot~, A.J. and BALBY, V.A. (1935) The balance of animal populations. Part. 19roc. Zool. Soc. London (3): SLOBODKN, L.B. (1961) Growth and regulation of animal populations. Holt, Rinehart and Winston, N.Y. TACHKAWA, T. (1966) On the identity of Neoeatolaccus mamezophagus shii et Nagasawa (Hy- menoptera: Pteromalidae). Jap. J. appl. Ent. Zool., 10:99 summary) (in Japanese with English UTDA, S. (1953) Population fluctuation in the system of host-parasite interaction. Res. Popul. Ecol., 2:22-46 (in Japanese with English summary)

12 26 UTwA, S. (1955) Population fluctuation in the system of interaction between a host and its two species parasite. Oy6-Konlya 11:43-48 (in Japanese with English summary) UTmA, S. (1956) Population fluctuation in the system of host-parasite interaction in different size of their environment. Res. Popul. Ecol., 3: UTWA, S. (1957) Population fluctuation, an experimental and theoretical approach. Cold Spring Harbor Syrup. Quant. Biol., 22: VOLT~RR*, V. (1926) Variazioni e fluttuazioni del numero d'individui in specie conviventi. Mere. Acad. Lincei Roma 2: (KS), 2~@~. (Anisopteromalus calandrae (ja), Heterospilus prosopidis ~=1=~ ~.~.Jt.J~]~@~_L,-C~~L,~':o 77~'@-KS-hp ~:, jeo~j: t) ~7i7~)~-~, ~!~]t~l~ " hp ;~ a~f_5~5o