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Incorporating physiological realism into models of parasitoid feeding behaviour
NEWS
&
COMMENT
Roger K. Butlin Ecology and Evolution Programme, Dept of Genetics, The University of Leeds, Leeds. UK LS2 9JT
References 1 Wallace, A.R. (1889) Darwinism: 2
An Exposition of the Theory of Natural Selection with some of its Applications, Macmillan Butlin, R.K. (1987) Trends Ecol. Evol. 2,8-13
3 Howard, D.J. (1993) in Hybrid Zones and the Euolutionary Process(Harrison, R.G., ed.), pp. 46-69, Oxford University Press 4 Littlejohn, M.J. (1993) Oxf Sum. Evol. Biol. 9, 135-165 5 Liou, L.W. and Price, T.D. (1994) Evolution 48, 1451-1459 6 Noor, M.A. (1995) Nature 375,674-675 7 Johannesson, K., Rot&r-Alvarez, E. and Ekendahl, A. Evolution (in press) 8 Guldemond, J.A. and Dixon, A.F.G.(1994) Biol. J. Linn. Sot. 52,287-303
Incorporating physiological realism into models of parasitoid feeding behaviour esearchers of parasitoids have long R been aware that such insects [whose females lay their eggs on or in other invertebrates (mainly insects) and whose larvae feed on the host and eventually kill it] habitually feed on hosts, nectar, pollen or honeydew in the field, but they have been slow to apply this knowledge to ecological studies. Awareness of the potential importance of adult feeding is, however, gaining momentum among behavioural ecologistslJ and theoretical population biologist+. New papers by Collier-1and Briggs et cd.6 are the latest milestones in the modelling of this biologically complex phenomenon, as they highlight the importance of physic+ logical correlates of feeding behaviour.
Modelling feeding behaviour So far as theoretical modelling of feeding behaviour is concerned, the most convenient starting point is ‘host feeding’ the consumption of host blood or tissues. The widespread occurrence of host feeding can be explained by the benefits it confers over the consumption of other food types. Compared with carbohydrate-based ‘nonhost foods’, such as nectar and honeydew, host blood is superior as a source of egg production materials, For many parasitoids, non-host foods tend to be spatially separated from hosts in the field, so searching for them will incur losses in energy and time-two potentially important resources for foraging parasitoids. Host feeding may incur costs, however. In particular, it may bring about a reduction in quality of the host as an oviposition resource, either by causing the host to die, or by significantly reducing the amount of resource available (through non-destructive host feeding, in which the same host individuals are used for the two activities). This cost may be lessened by the use of lower quality hosts for host feeding and higher quality hosts for ovipositionr. 434
0 1995, Elsevier
Science
Ltd
For non-concurrent destructive host feeders, the decision of whether to feed on or oviposit in a host is an example of the classical trade-off between current reproduction (oviposition) and investment in future reproduction (feeding)lJ. The main problem faced by theoreticians has been to achieve a sufficient degree of biological realism in models, given the (I priori expectation that the decision by a female to host feed will depend dynamically on factors such as the internal state of the parasitoid, for example, the number of mature eggs it has available for oviposition (‘egg load’), the level of its nutrient reserves, the amount of host blood in its gut, and the female’s age, and also any external mortality risk. Collier’ constructed his models within the framework of dynamic state variable modellinga. The models include a number of physiological state variables - such as the quantity of the parasitoid’s nutrient reserves, and/or its egg load - that are altered when feeding or oviposition occur. Using this technique, the parasitoid’s life time is divided into numerous time-steps within each of which there is a probability of an encounter with a host. The optimal decision by the female maximizes the sum of current fitness gains from oviposition and future fitness gains, the latter depending both on alterations in the state variable(s) and on the probability of surviving the time-step. Between time-steps, the female ages and eventually approaches a ‘time horizon’ representing either its maximum longevity or the end of the season. Collier’s are among the more biologically realistic models of host-feeding behaviour in assuming that nutrients can be used for egg production and for maintenance metabolism. They predict that host feeding can occur at egg loads greater than zero, and that it is more likely at low egg loads. Critical egg loads at and below which
9 Gerhardt, H.C. (1994) Anim. Eehav. 47, 959-969
10 Spencer, H.G., McArdle, B.H. and Lambert, D.M. (1986)Am. Nat. 128,241-262 11 Maynard Smith, .I. (1991) Trends Ecol. Evol. 6, 146-151 12 Sanderson, N. (1989) Evolution 43,1223-1235 13 Wu, C-l. and Palopoli, M.F. (1994) Annu. Rev. Cenet. 27,283-308
14 Mallet, J. (1995) Trends Ecol. Evol. 10,294-299 15 Johannesson, K., Johannesson, B. and Rolarr-Alvarez, E. (1993) Evolution 47,1770-1787
host feeding occurs depend on the parasitoid’s age or closeness of the time horizon. The tendency to host feed declines as the insect approaches the end of its reproductive life, gaining little in terms of future survival or egg production. A problem faced by Collier and previous modellers has been the realistic rep resentation of the time delay between the act of host feeding and the appearance of mature eggs in the ovaries. In simpler models, host feeding leads to the formation of new eggs in the time-step immediately following feeding (e.g. the next day). Modellers have rightly suspected there to be an egg maturation delay, but some have avoided incorporating this into models, one reason being the need to involve a large number of state variables that alter over different time scales. This difficulty was resolved by Collier using the technique of ‘sequential coupling’, which involves dividing the different processes on each time scale into a number of sequentially linked or ‘coupled’ submodels*. Collier shows that the incorporation of a realistically long egg-maturation delay generally raises the critical egg load at which host feeding is predicted to occur. The functional explanation for this is that without a delay, the female can delay host-feeding until she has no eggs. With a delay, however, there is a risk of her being without any eggs to lay for an extended period of time. Collier also examined in one model the effect of resorption of mature eggs. Egg re sorption is viewed as a physiological lastresort survival tactic of parasitoidsg; if there are insufficient nutrients in the gut at the end of the daily foraging period to meet the metabolic demand, the nutrients within mature eggs are used. The model assumes, realistically, that egg resorption incurs a metabolic cost, and it predicts that host feeding should occur at higher critical egg loads when resorption occurs. What is so remarkable about Collier’s models is that (1) they incorporate physic logical features hitherto overlooked by modellers, and (2) for the first time realistic, empirically obtained values are used for a wide range of parameters, including, importantly, the egg maturation TREE
vol.
IO,
no.
II
Nooember
199.5
NEWS delay. Furthermore, the models predict a range of critical egg loads that agrees well with the range at which Aphytis wasps have been observed to host feed in laboratory experiments2J.
Incorporating feeding behaviour into population models Host feeding needs to be investigated at the population level for two main reasons: l It affects parasitoid fecundity and survival, and destructive host feeding can result in very high mortality of hosts. It is therefore a potentially important component in parasitoid-host population dynamics.
l In the literature on biological pest control, destructively host-feeding parasitoids are purported by some authors to be superior to other parasitoids as pest control agents, based on the observation that host feeding is an additional source of host mortality to parasitism. Population biologists have, over the past decade, recognized the need to incorporate host feeding together with its physiological correlates into parasitoidhost population models3.6.Briggs etal.6 take account of the fact that real populations of parasitoids comprise a physiological mix of individuals owing to their different histo ries of encountering hosts. In their models,
(4
&
COMMENT
the physiological variability within the parasitoid population is expressed in terms of egg load, and egg load controls the decision whether to host feed or oviposit. Briggs et al. found that host feeding by itself does not affect stability. Instead, host and parasitoid equilibria are shown to be stabilized by a parasitoid mortality rate that is a decreasing function of egg load (Fig. la). Destabilization of equilibria occurs, however (Fig. lb), if there is a drain of nutrients, obtained through host feeding, towards maintenance, coupled with a dependence of either parasitoid death rate or birth rate on egg load. An input of nutrients from a source other than the host population has a stabilizing effect (Fig. lc). This last finding is highly significant. First, alternative food sources act in a manner analogous to refuges or other stabilizing mechanisms that provide an uncoupled recruitment rate. Second, it adds weight to the long-held view of biological control practitioners that the provision of non-host food sources may help to conserve parasitoids and enhance their impact on pests.
Future developments?
(b)
0
40
20
60
100
80
120
140
(c) 65-
40
60
80
100
Time Fig. 1. Brig@ et a/.‘s simulations of one of their population models, in which parasitoid death rate decreasing function of egg load. (a) If there is no drain on materials towards somatic maintenance, equilibrium is stable; (b) if there is a continuous drain, the equilibrium is unstable; (c) if the parasitoids also on a non-host food source the equilibrium is stable. Hosts: thick solid line. Parasitoids: thin solid Reproduced, with permission, from Ref. 6.
TREE
vol.
IO,
no.
II
November
199.5
is a the feed line.
Even greater physiological and ecological realism needs to be incorporated in models of parasitoid feeding behaviour and population dynamics, if they are ultimately to be of practical significance. So far as physiological realism is concerned, Collier points out that whereas in his and previous models, all nutrients in excess of metabolic demand are directed towards egg production, in reality some are likely to be allocated to storage, in the female’s fat body. A more detailed understanding of nutrient allocation in parasitoids is therefore likely to be critical to future developments in this area. So far as ecological realism is concerned, behavioural modellers using the dynamic state variable approach have been quick to examine the effects of variation in host quality and of host spatial distributionlo. Variation in host quality has also been examined by population modeller.9. Avaluable step in the development of foraging models and of population models would be also to take account of the quality and spatial distribution of non-host food sources. There will, of course, be the added complication of incorporating the relative costs and benefits of searching for host and non-host food sources, but at least models explicitly incorporating nonhost foods are likely to approximate more closely the natural situation in which parasitoids live. Acknowledgements We are very grateful to George Heimpel and an anonymous reviewer for their comments on our manuscript.
435
NEWS
&
COMMENT
Mark Jervis Neil Kidd School of Pure and Applied Biology, University of Wales, Cardie UK CFl3TL
References 1 Collier, T.R. (1995) Euol. Ecol. 9,217-235 2 Heimpel, GE. and Rosenheim, J.A. (1995)
J. Anim. Ecol. 64,153-167 3 Kidd, N.A.C. and Jervis, M.A. (1989) Res. PopuI. Ecol. 31.235-274 4 Murdoch, W.W., Nisbet, R.M., Luck, R.F., Godfray, H.C.J.and Gurney, W.S.C.(1992) J. Anim. Ecol. 61,533-541 5 Collier, T.R., Murdoch, W.W. and Nisbet, R.M. (1994) J. Anim. Eco/. 63,299-306 6 Briggs, C.J.,Nisbet, R.M., Murdoch, W.W., Collier, T.R. and Metz, J.A.J. (1995)J. Anim.
Cuckoo-host coevolution: from snapshots of an arms race to the documentation of microevolution t is not often that a notable study in Ihasevolutionary biology published in nearly all of its assumptions and con-
inferred during a short-term comparative study. The relationships between parasitic clusions challenged by a second paper. cuckoos and their hosts are thought But that is precisely what happened when to represent clear cases of coevolution4. Zuniga and Redondol questioned Soler The cost of being parasitized selects for and Moller’s2 work on coevolution between the evolution of host defenses against the the brood parasitic great spotted cuckoo parasite, which in turn, select for counter(Clamatorglandarius) and its magpie (Pica adaptations in the parasite. Several experipica) host. These authors reported that mental and comparative studies strongly support this coevolutionary scenarios-s. varying degrees of egg discrimination shown by three magpie populations corre- For example, actual and potential cuckoo late with the duration of sympatry between hosts exhibit higher rejection rates of nonthe host and its parasite. They found that mimetic eggs than do species unsuitable magpies never reject even strongly non- as hosts5.6.Although convincing, such evimimetic eggs in Uppsala, Sweden, where dence does not involve a direct observation of evolutionary change because inferences cuckoos are absent. But most importantly, they argued that significant differences in regarding evolutionary change in the past behavior between two magpie populations are based only upon patterns and seleconly 60 km apart in Spain exist because tive pressures observed in the present. But magpies at one site, Guadix, have been sym- now, depending on which side of the great patric with cuckoos only since the 196Os, spotted cuckoo controversy one chooses while those at Santa Fe have experienced to believe, the study of avian brood parasitcuckoos for much longer. Thus, the data ism may finally have its own case of ‘industrial melanism’ in which microevolutionary obtained from the two sites appeared tore fleet different stages in a continuing evolu- changes have actually been observed. One tionary arms race between the cuckoo and thing that is clear is that the great spotted its host. Soler and Moller also argued that cuckoo is potentially a very strong seleccuckoos at Guadix area show other charac- tive pressure on magpies. Although other teristics expected of a new parasite-host corvids are occasionally parasitized at ~5% association, for example, many cuckoo of their nests, European populations of this eggs per magpie nest, cuckoo parasitism cuckoo specialize on the magpie, with local of additional host species, and an overall parasitism rates sometimes exceeding 50% high reproductive success in the parasite and parasitized magpies often failing to owing to weak host defenses. raise any of their own young3,g. Zuniga and Redondo’sl challenge of Zuniga and Redondo’s doubts about these findings have recently been re- Soler and Mprller’s original paper made three fundamental assertions. (1) There is butted by Soler et ~1.3,who also present new evidence for coevolutionary changes no reliable evidence for differences in the in the past lo-15 years. So, what started duration of sympatry between Guadix and as a controversy over the correct facts Santa Fe. (2) The characteristics of a new and the sorts of evolutionary inferences parasite-host association that Soler and one can make from them may lead the Moller claimed for Guadix apply just as well research on avian brood parasitism into a to Santa Fe. (3) Any differences between new phase in which microevolutionary magpie responses to foreign eggs at these change is observed during the course of two sites could be due to a conditional a long-term study, rather than simply response, with higher cuckoo populations Nature
436
o 1995, Elsevier
Science
Ltd
Ecol. 64,403-416 7 Kidd, N.A.C. and Jervis, M.A. (1991) Rex fopul. Ecol. 33,13-28 8 Mangel, M. and Clark, C.W. (1988) Dynamic Modekng in Behaoioural Ecology, Princeton University Press 9 Jet%, M.A. and Kidd, M.A. (1986) Biol. Reu. 61,395-434 10 Houston, A., McNamara, J.M. and Godfray, H.C.J. (1992) Bull. Math. Biol. 54,465-476
at one site stimulating magpies to inspect their eggs more thoroughly or more often, thereby leading to higher rejection rates. Only the third criticism is of general importance and also totally testable; thus, it should be the target of future efforts. While the duration of sympatry at Guadix is an essential point, no clear resolution of this particular argument seems possible. Soler and Moller’s evidence for recent sympatry at Guadix is based on local hunters who shot a great spotted cuckoo there in 1962 and claimed never to have seen such a bird before. While this cuckoo is a large, and at times, noisy bird, this whole issue depends on how much faith one places in the observational skills of nonbiologists. We have both known nonbiologists who were remarkably attentive observers of natural history and others who were unaware of common birds they have lived among all their lives. So this issue is simply not resolvable, especially since cuckoo presence may be episodic as they have died out in much of North Africa during this centurylo. Also, cuckoos could have been at Guadix long ago because they were wide spread in Spain over 120 years ago. Saunders (in Ref. 11) noted that this primarily African species was very common at Aranjuez, 300 km north of the Guadix area before 1870 and that multiple parasitized magpie nests occurred frequently. Although Soler and Mollerz supported their claim of recent sympatry at Guadix by suggesting that cuckoos rarely occur in such mountainous areas, Wadleylz found them to be ‘well distributed’ parasites of magpies throughout Anatolia, Turkey, at high elevations (900-1050 m versus 900-l 100 m at Guadix). In arguing that Guadix does not show the characteristics putatively associated with the recent arrival of a parasite, Zuniga and Redondo pointed out that the claim for an expanded host niche at Guadix is weak because of the simple fact that several corvid species breed there but only the magpie occurs at Santa Fe. However, their argument that Santa Fe and not Guadix shows such characteristics as frequent multiple parasitism, and high overall cuckoo breeding success is weakened by Soler and Moller’s new analyses. The latter demonstrate that various breeding parameters show temporal variation that could have confounded TREE
vol.
IO,
no.
II
November
199.5
&
COMMENT
Roger K. Butlin Ecology and Evolution Programme, Dept of Genetics, The University of Leeds, Leeds. UK LS2 9JT
References 1 Wallace, A.R. (1889) Darwinism: 2
An Exposition of the Theory of Natural Selection with some of its Applications, Macmillan Butlin, R.K. (1987) Trends Ecol. Evol. 2,8-13
3 Howard, D.J. (1993) in Hybrid Zones and the Euolutionary Process(Harrison, R.G., ed.), pp. 46-69, Oxford University Press 4 Littlejohn, M.J. (1993) Oxf Sum. Evol. Biol. 9, 135-165 5 Liou, L.W. and Price, T.D. (1994) Evolution 48, 1451-1459 6 Noor, M.A. (1995) Nature 375,674-675 7 Johannesson, K., Rot&r-Alvarez, E. and Ekendahl, A. Evolution (in press) 8 Guldemond, J.A. and Dixon, A.F.G.(1994) Biol. J. Linn. Sot. 52,287-303
Incorporating physiological realism into models of parasitoid feeding behaviour esearchers of parasitoids have long R been aware that such insects [whose females lay their eggs on or in other invertebrates (mainly insects) and whose larvae feed on the host and eventually kill it] habitually feed on hosts, nectar, pollen or honeydew in the field, but they have been slow to apply this knowledge to ecological studies. Awareness of the potential importance of adult feeding is, however, gaining momentum among behavioural ecologistslJ and theoretical population biologist+. New papers by Collier-1and Briggs et cd.6 are the latest milestones in the modelling of this biologically complex phenomenon, as they highlight the importance of physic+ logical correlates of feeding behaviour.
Modelling feeding behaviour So far as theoretical modelling of feeding behaviour is concerned, the most convenient starting point is ‘host feeding’ the consumption of host blood or tissues. The widespread occurrence of host feeding can be explained by the benefits it confers over the consumption of other food types. Compared with carbohydrate-based ‘nonhost foods’, such as nectar and honeydew, host blood is superior as a source of egg production materials, For many parasitoids, non-host foods tend to be spatially separated from hosts in the field, so searching for them will incur losses in energy and time-two potentially important resources for foraging parasitoids. Host feeding may incur costs, however. In particular, it may bring about a reduction in quality of the host as an oviposition resource, either by causing the host to die, or by significantly reducing the amount of resource available (through non-destructive host feeding, in which the same host individuals are used for the two activities). This cost may be lessened by the use of lower quality hosts for host feeding and higher quality hosts for ovipositionr. 434
0 1995, Elsevier
Science
Ltd
For non-concurrent destructive host feeders, the decision of whether to feed on or oviposit in a host is an example of the classical trade-off between current reproduction (oviposition) and investment in future reproduction (feeding)lJ. The main problem faced by theoreticians has been to achieve a sufficient degree of biological realism in models, given the (I priori expectation that the decision by a female to host feed will depend dynamically on factors such as the internal state of the parasitoid, for example, the number of mature eggs it has available for oviposition (‘egg load’), the level of its nutrient reserves, the amount of host blood in its gut, and the female’s age, and also any external mortality risk. Collier’ constructed his models within the framework of dynamic state variable modellinga. The models include a number of physiological state variables - such as the quantity of the parasitoid’s nutrient reserves, and/or its egg load - that are altered when feeding or oviposition occur. Using this technique, the parasitoid’s life time is divided into numerous time-steps within each of which there is a probability of an encounter with a host. The optimal decision by the female maximizes the sum of current fitness gains from oviposition and future fitness gains, the latter depending both on alterations in the state variable(s) and on the probability of surviving the time-step. Between time-steps, the female ages and eventually approaches a ‘time horizon’ representing either its maximum longevity or the end of the season. Collier’s are among the more biologically realistic models of host-feeding behaviour in assuming that nutrients can be used for egg production and for maintenance metabolism. They predict that host feeding can occur at egg loads greater than zero, and that it is more likely at low egg loads. Critical egg loads at and below which
9 Gerhardt, H.C. (1994) Anim. Eehav. 47, 959-969
10 Spencer, H.G., McArdle, B.H. and Lambert, D.M. (1986)Am. Nat. 128,241-262 11 Maynard Smith, .I. (1991) Trends Ecol. Evol. 6, 146-151 12 Sanderson, N. (1989) Evolution 43,1223-1235 13 Wu, C-l. and Palopoli, M.F. (1994) Annu. Rev. Cenet. 27,283-308
14 Mallet, J. (1995) Trends Ecol. Evol. 10,294-299 15 Johannesson, K., Johannesson, B. and Rolarr-Alvarez, E. (1993) Evolution 47,1770-1787
host feeding occurs depend on the parasitoid’s age or closeness of the time horizon. The tendency to host feed declines as the insect approaches the end of its reproductive life, gaining little in terms of future survival or egg production. A problem faced by Collier and previous modellers has been the realistic rep resentation of the time delay between the act of host feeding and the appearance of mature eggs in the ovaries. In simpler models, host feeding leads to the formation of new eggs in the time-step immediately following feeding (e.g. the next day). Modellers have rightly suspected there to be an egg maturation delay, but some have avoided incorporating this into models, one reason being the need to involve a large number of state variables that alter over different time scales. This difficulty was resolved by Collier using the technique of ‘sequential coupling’, which involves dividing the different processes on each time scale into a number of sequentially linked or ‘coupled’ submodels*. Collier shows that the incorporation of a realistically long egg-maturation delay generally raises the critical egg load at which host feeding is predicted to occur. The functional explanation for this is that without a delay, the female can delay host-feeding until she has no eggs. With a delay, however, there is a risk of her being without any eggs to lay for an extended period of time. Collier also examined in one model the effect of resorption of mature eggs. Egg re sorption is viewed as a physiological lastresort survival tactic of parasitoidsg; if there are insufficient nutrients in the gut at the end of the daily foraging period to meet the metabolic demand, the nutrients within mature eggs are used. The model assumes, realistically, that egg resorption incurs a metabolic cost, and it predicts that host feeding should occur at higher critical egg loads when resorption occurs. What is so remarkable about Collier’s models is that (1) they incorporate physic logical features hitherto overlooked by modellers, and (2) for the first time realistic, empirically obtained values are used for a wide range of parameters, including, importantly, the egg maturation TREE
vol.
IO,
no.
II
Nooember
199.5
NEWS delay. Furthermore, the models predict a range of critical egg loads that agrees well with the range at which Aphytis wasps have been observed to host feed in laboratory experiments2J.
Incorporating feeding behaviour into population models Host feeding needs to be investigated at the population level for two main reasons: l It affects parasitoid fecundity and survival, and destructive host feeding can result in very high mortality of hosts. It is therefore a potentially important component in parasitoid-host population dynamics.
l In the literature on biological pest control, destructively host-feeding parasitoids are purported by some authors to be superior to other parasitoids as pest control agents, based on the observation that host feeding is an additional source of host mortality to parasitism. Population biologists have, over the past decade, recognized the need to incorporate host feeding together with its physiological correlates into parasitoidhost population models3.6.Briggs etal.6 take account of the fact that real populations of parasitoids comprise a physiological mix of individuals owing to their different histo ries of encountering hosts. In their models,
(4
&
COMMENT
the physiological variability within the parasitoid population is expressed in terms of egg load, and egg load controls the decision whether to host feed or oviposit. Briggs et al. found that host feeding by itself does not affect stability. Instead, host and parasitoid equilibria are shown to be stabilized by a parasitoid mortality rate that is a decreasing function of egg load (Fig. la). Destabilization of equilibria occurs, however (Fig. lb), if there is a drain of nutrients, obtained through host feeding, towards maintenance, coupled with a dependence of either parasitoid death rate or birth rate on egg load. An input of nutrients from a source other than the host population has a stabilizing effect (Fig. lc). This last finding is highly significant. First, alternative food sources act in a manner analogous to refuges or other stabilizing mechanisms that provide an uncoupled recruitment rate. Second, it adds weight to the long-held view of biological control practitioners that the provision of non-host food sources may help to conserve parasitoids and enhance their impact on pests.
Future developments?
(b)
0
40
20
60
100
80
120
140
(c) 65-
40
60
80
100
Time Fig. 1. Brig@ et a/.‘s simulations of one of their population models, in which parasitoid death rate decreasing function of egg load. (a) If there is no drain on materials towards somatic maintenance, equilibrium is stable; (b) if there is a continuous drain, the equilibrium is unstable; (c) if the parasitoids also on a non-host food source the equilibrium is stable. Hosts: thick solid line. Parasitoids: thin solid Reproduced, with permission, from Ref. 6.
TREE
vol.
IO,
no.
II
November
199.5
is a the feed line.
Even greater physiological and ecological realism needs to be incorporated in models of parasitoid feeding behaviour and population dynamics, if they are ultimately to be of practical significance. So far as physiological realism is concerned, Collier points out that whereas in his and previous models, all nutrients in excess of metabolic demand are directed towards egg production, in reality some are likely to be allocated to storage, in the female’s fat body. A more detailed understanding of nutrient allocation in parasitoids is therefore likely to be critical to future developments in this area. So far as ecological realism is concerned, behavioural modellers using the dynamic state variable approach have been quick to examine the effects of variation in host quality and of host spatial distributionlo. Variation in host quality has also been examined by population modeller.9. Avaluable step in the development of foraging models and of population models would be also to take account of the quality and spatial distribution of non-host food sources. There will, of course, be the added complication of incorporating the relative costs and benefits of searching for host and non-host food sources, but at least models explicitly incorporating nonhost foods are likely to approximate more closely the natural situation in which parasitoids live. Acknowledgements We are very grateful to George Heimpel and an anonymous reviewer for their comments on our manuscript.
435
NEWS
&
COMMENT
Mark Jervis Neil Kidd School of Pure and Applied Biology, University of Wales, Cardie UK CFl3TL
References 1 Collier, T.R. (1995) Euol. Ecol. 9,217-235 2 Heimpel, GE. and Rosenheim, J.A. (1995)
J. Anim. Ecol. 64,153-167 3 Kidd, N.A.C. and Jervis, M.A. (1989) Res. PopuI. Ecol. 31.235-274 4 Murdoch, W.W., Nisbet, R.M., Luck, R.F., Godfray, H.C.J.and Gurney, W.S.C.(1992) J. Anim. Ecol. 61,533-541 5 Collier, T.R., Murdoch, W.W. and Nisbet, R.M. (1994) J. Anim. Eco/. 63,299-306 6 Briggs, C.J.,Nisbet, R.M., Murdoch, W.W., Collier, T.R. and Metz, J.A.J. (1995)J. Anim.
Cuckoo-host coevolution: from snapshots of an arms race to the documentation of microevolution t is not often that a notable study in Ihasevolutionary biology published in nearly all of its assumptions and con-
inferred during a short-term comparative study. The relationships between parasitic clusions challenged by a second paper. cuckoos and their hosts are thought But that is precisely what happened when to represent clear cases of coevolution4. Zuniga and Redondol questioned Soler The cost of being parasitized selects for and Moller’s2 work on coevolution between the evolution of host defenses against the the brood parasitic great spotted cuckoo parasite, which in turn, select for counter(Clamatorglandarius) and its magpie (Pica adaptations in the parasite. Several experipica) host. These authors reported that mental and comparative studies strongly support this coevolutionary scenarios-s. varying degrees of egg discrimination shown by three magpie populations corre- For example, actual and potential cuckoo late with the duration of sympatry between hosts exhibit higher rejection rates of nonthe host and its parasite. They found that mimetic eggs than do species unsuitable magpies never reject even strongly non- as hosts5.6.Although convincing, such evimimetic eggs in Uppsala, Sweden, where dence does not involve a direct observation of evolutionary change because inferences cuckoos are absent. But most importantly, they argued that significant differences in regarding evolutionary change in the past behavior between two magpie populations are based only upon patterns and seleconly 60 km apart in Spain exist because tive pressures observed in the present. But magpies at one site, Guadix, have been sym- now, depending on which side of the great patric with cuckoos only since the 196Os, spotted cuckoo controversy one chooses while those at Santa Fe have experienced to believe, the study of avian brood parasitcuckoos for much longer. Thus, the data ism may finally have its own case of ‘industrial melanism’ in which microevolutionary obtained from the two sites appeared tore fleet different stages in a continuing evolu- changes have actually been observed. One tionary arms race between the cuckoo and thing that is clear is that the great spotted its host. Soler and Moller also argued that cuckoo is potentially a very strong seleccuckoos at Guadix area show other charac- tive pressure on magpies. Although other teristics expected of a new parasite-host corvids are occasionally parasitized at ~5% association, for example, many cuckoo of their nests, European populations of this eggs per magpie nest, cuckoo parasitism cuckoo specialize on the magpie, with local of additional host species, and an overall parasitism rates sometimes exceeding 50% high reproductive success in the parasite and parasitized magpies often failing to owing to weak host defenses. raise any of their own young3,g. Zuniga and Redondo’sl challenge of Zuniga and Redondo’s doubts about these findings have recently been re- Soler and Mprller’s original paper made three fundamental assertions. (1) There is butted by Soler et ~1.3,who also present new evidence for coevolutionary changes no reliable evidence for differences in the in the past lo-15 years. So, what started duration of sympatry between Guadix and as a controversy over the correct facts Santa Fe. (2) The characteristics of a new and the sorts of evolutionary inferences parasite-host association that Soler and one can make from them may lead the Moller claimed for Guadix apply just as well research on avian brood parasitism into a to Santa Fe. (3) Any differences between new phase in which microevolutionary magpie responses to foreign eggs at these change is observed during the course of two sites could be due to a conditional a long-term study, rather than simply response, with higher cuckoo populations Nature
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Ecol. 64,403-416 7 Kidd, N.A.C. and Jervis, M.A. (1991) Rex fopul. Ecol. 33,13-28 8 Mangel, M. and Clark, C.W. (1988) Dynamic Modekng in Behaoioural Ecology, Princeton University Press 9 Jet%, M.A. and Kidd, M.A. (1986) Biol. Reu. 61,395-434 10 Houston, A., McNamara, J.M. and Godfray, H.C.J. (1992) Bull. Math. Biol. 54,465-476
at one site stimulating magpies to inspect their eggs more thoroughly or more often, thereby leading to higher rejection rates. Only the third criticism is of general importance and also totally testable; thus, it should be the target of future efforts. While the duration of sympatry at Guadix is an essential point, no clear resolution of this particular argument seems possible. Soler and Moller’s evidence for recent sympatry at Guadix is based on local hunters who shot a great spotted cuckoo there in 1962 and claimed never to have seen such a bird before. While this cuckoo is a large, and at times, noisy bird, this whole issue depends on how much faith one places in the observational skills of nonbiologists. We have both known nonbiologists who were remarkably attentive observers of natural history and others who were unaware of common birds they have lived among all their lives. So this issue is simply not resolvable, especially since cuckoo presence may be episodic as they have died out in much of North Africa during this centurylo. Also, cuckoos could have been at Guadix long ago because they were wide spread in Spain over 120 years ago. Saunders (in Ref. 11) noted that this primarily African species was very common at Aranjuez, 300 km north of the Guadix area before 1870 and that multiple parasitized magpie nests occurred frequently. Although Soler and Mollerz supported their claim of recent sympatry at Guadix by suggesting that cuckoos rarely occur in such mountainous areas, Wadleylz found them to be ‘well distributed’ parasites of magpies throughout Anatolia, Turkey, at high elevations (900-1050 m versus 900-l 100 m at Guadix). In arguing that Guadix does not show the characteristics putatively associated with the recent arrival of a parasite, Zuniga and Redondo pointed out that the claim for an expanded host niche at Guadix is weak because of the simple fact that several corvid species breed there but only the magpie occurs at Santa Fe. However, their argument that Santa Fe and not Guadix shows such characteristics as frequent multiple parasitism, and high overall cuckoo breeding success is weakened by Soler and Moller’s new analyses. The latter demonstrate that various breeding parameters show temporal variation that could have confounded TREE
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