- Email: [email protected]
Death and reproduction in mantids
$ECOLOGYc 8EVOLUTION DeathandReproduction inMantids C. P. Kyriacou Like many people, I have always considered the praying mantis to be a good example of an organism with unpleasant sexual habits. The usual scenario envisaged is of a male copulating with a female, then having his head bitten off, and finally being totally consumed by his predatory mate. The removal of the male head is cited in the literature as a key factor in stimulating the male’s sexual movements, suggesting that the cephalic ganglion, when intact, normally inhibits the male’s copulatory behaviourl,*. This physiological view of the mantis’ sexual behaviour has recently been contradicted by Liske and Daviss. They had already noted that in previous reports, this type of violent sexual assault had been absent. Indeed, Roederl suggested over 50 years ago that sexual cannibalism was induced either by the effects of captivity or more directly by the nutritional state of the female. Liske and Davis have investigated Roeder’s early suggestion, and have also provided a detailed ethological study of the behaviour of rL._ PI_:____ -.._.__:__ Lilt: Llllllese prciy,r,g mantis, Tenodera aridifolia sinensis. Theyvideotaped ,,#’
encounters between pairs of mantids in order to gain insight into the functions of the male and female sexual displays. The courtship is not to be hurried: the male approaches the female slowly, taking l-2 h to get within a
few centimetres of her. His approach is cautious, and involves several specific behavioural elements, including antenna1 oscillations, abdominal movements and foot-stamping. The authors speculate that the male displays somehow serve to inhibit female aggression, as they are performed only when the female visually fixates the male. The closer he gets to the ‘danger zone’ the more intense the display becomes. Finally he takes a flying leap at her and attempts to copulate. The duration of copulation can be between 1 and 3 h and usually a single spermatophore is transferred. The development of the male’s sexual behaviour was also studied by placing an immature male on a female’s
December 1987 Volume 2, No. 12 1181
had been fedadlibitum on a diet of crickets, and no instances of sexual cannibalism were observed. However, when the amount of food given to the female was varied so as to produce ‘moderately hungry’ or ‘starved’ females, the picture changed dramatically. Most of the females that were
‘moderately hungry’ ate the male at some
sexual behaviour can be elicited. Also, removing the male’s head results in rhythmic sexual movethe earlier report ments, confirming by Roeder. Headless males, however, were not observed to mount the female, which is hardly surprising given the visual component in this behaviour. However, headless males were able to achieve intromission, even when extremely young, if the experimenter placed the headless insect on the female. Females also participate actively in the courtship by displaying various and abdominal movepostures ments. Sometimes females even stroke their partners before the flying leap - a touching display that does not conform to our usual stereotyped view of this insect. These ethological experiments were initially performed using females that
the males
with the females continuously. Of the males eaten in a sexual context during the daytime, only one was eaten after mounting; he was devoured head first but still succeeded in subsequent intromission and spermatophore transfer. This represents the only example of what the authors term ‘true sexual cannibalism’. Other males were eaten before mounting, or after mounting but before intromission. The majority of ‘starved’ females attacked their partner, but males that survived the initial onslaught mounted the females and copulated. The experiment was terminated at intromission so the authors were unable to see whether the contmued
on p. 350
TREE vol. 2, no. 12, December
escapees ultimately met their doom. Therefore, there seems little doubt that in this mantid species there is a strong relationship between female aggression and food deprivation. Courtship and mating can proceed perfectly amicably if the females are satiated, and decapitation of the male is not necessary for successful copulation. However, if females are hungry in the wild, one might expect to observe sexual cannibalism. The literature is rather obscure on this point, although the reports that do exist do not appear to support the view of frequent cannibalism in nature*. In a recent news article in TREE, I used the praying mantis as an extreme example of sexual feeding in insects5. Sexual feeding occurs when males offer females nutrients as an inducement for mating. In the mantis, therefore, the male himself becomes the nutrient. Sexual feeding can, of course, be studied in terms of the costs and benefits to each partner of this kind of ‘food for sex’ exchange. It is clear that ecological conditions are extremely important in determining the type of exchange that occurs, with available food resources being a critical factorsG7. Can we obtain any insight into the mantid’s behaviour within the context of sexual selection?
A simple view might be that the self-sacrifice of a male may ultimately result in an increase in the number of his offspring because the female could use the nutrients (i.e. the male) in her egg production, leading to better survival of fertilized eggs. A complicating factor here would perhaps be that only a small proportion of males succeed in mating in the wild. Possibly, they obtain several mates. If this is the case, then by definition they must have genes for ‘not getting eaten’, which will be passed on to their male progeny. Other males attempting to mate may get eaten before intromission. Such a situation would result in strong selection for males that do not get eaten. A study that might shed light on this general evolutionary theme would be an examination of who gets eaten and who does not. Perhaps eating a male before he can copulate, which evidently occurred in Liske and Davis’ study, is a rather extreme form of female rejection; perhaps she selects a mate based on a certain stimulus (e.g. male size or aspects of his display) and if the male fails to provide the correct stimulation and she is hungry, she attacks him. In the absence of any hard evidence on the frequency of sexual cannibalism in the wild, it is prema-
1987
ture to speculate too much along these lines. More work is required on the population density, age structure, food availability and mating dynamics of these insects before a clearer picture emerges. The role of sexual cannibalism may reveal some subtle insights into sexual selection in mantids. On the other hand, cannibalism may be so rare in the wild that it is not worth the effort of advancing evolutionary hypotheses to explain it. Nevertheless, the work of Liske and Davis has clarified some previous misconceptions about the sexual behaviour of this species. References 1 Roeder, K.D. (1935) Biol. Bull. 69, 203-220 2 Alcock, J. (1979) Animal Behaviour (2nd edn), Sinauer 3 Liske, E. and Davis, W.J. (1987) Anim. Behav. 35,1524-l 537 4 Bartley, T.A. (1982) Ann. Entomol. Sot.
Am. 75,484 5 Kyriacou, C.P. (1987) Trends Ecol. Evol. 2,85-86 6 Steele, R.H. (1986) Aim. Behav. 34, 1087-1098 7 Gwynne, D.T. (1981) Science 213, 779-780
C. P. Kyriacou is at the Dept of Genetics, University of Leicester, University Road, Leicester LE17RH,UK.
Plankton thatDon’Obey t theRules Ilkka Hanski versus-diversity problem (population-community approach) and in the ecosystem studies conducted during the International Biological Program (the process-functional approach). A well-known limitation of the population-community approach is the considerable redundancy of function often observed among species populations. For instance, in phytoplankton studies it is frequently found that factors other than the species composition of phytoplankton largely determine primary production. Recent studies have demonstrated the opposite redundancy, that is, species populations with radically alternative positions in their food webs. Stoecker et al.3 (see also Refs 4 and 5) show that some abundant marine planktonic ciliates consume unicellular algae without destroying their chloroplasts, which llkka Hanski is at the Dept of Zoology, Univer- continue to function and use light sity of Helsinki, P. Rautatiekatu 13, SF-00100 energy for photosynthesis inside ciliate. Helsinki, Finland. the Several common
The ecosystem concept has its roots in the study of small lakes and ponds. In a pioneering work, Lindemanl described the ‘trophic dynamics’ in lakes as the transfer of energy between the components of the ‘classic’ aquatic food chain, the producers (autotrophic algae), the consumers (zooplankton and fishes) and the decomposers (bacteria and other saprophages). Ecosystem ecology has remained a controversial and difficult subject. A recent exposition2 of hierarchy theory in ecosystem studies finds that both of the current approaches the population-community paradigm and the process-functional paradigm-unduly emphasize one of the many possible ‘observation sets’. Both approaches are commonly (though not universally) seen as having failed in solving the stability-
350
chloroplast-retaining species are mixotrophic, in other words, able to function both as grazers on phytoplankton and as autotrophs with their sequestered chloroplasts3. This phenomenon falls within a wider range of relationships between algae spanning from and protozoa, straightforward predator-prey interactions to endosymbiosis”. If these marine ciliates survive and reproduce in light with a minimum density of autotrophic algae (some are needed to provide the chloroplasts), other ‘heterotrophic’ zooplankton can do just the opposite, that is, grow and reproduce without light and phytoplankton. Salonen and Hammar studied macrozooplankton growth and reproduction in filtered water from small, humic lakes, using a radiotracer technique. They found that under low light intensity a mere 5%, and under high light intensity only 30-40%, of the carbon in zooplankton (Bosmina, Ceriodaphnia, Daphnia, Eudiaptomus, Scapholeberis) was of photosynthetic origin. In these experiments the zooplankton were not grazing on the food chain based on
lllk) ‘a, !, . 5’::0’ cc !$,, , ii‘“8t.II’,,rllird,,(“,i!‘.ilrillrld;~i~
encounters between pairs of mantids in order to gain insight into the functions of the male and female sexual displays. The courtship is not to be hurried: the male approaches the female slowly, taking l-2 h to get within a
few centimetres of her. His approach is cautious, and involves several specific behavioural elements, including antenna1 oscillations, abdominal movements and foot-stamping. The authors speculate that the male displays somehow serve to inhibit female aggression, as they are performed only when the female visually fixates the male. The closer he gets to the ‘danger zone’ the more intense the display becomes. Finally he takes a flying leap at her and attempts to copulate. The duration of copulation can be between 1 and 3 h and usually a single spermatophore is transferred. The development of the male’s sexual behaviour was also studied by placing an immature male on a female’s
December 1987 Volume 2, No. 12 1181
had been fedadlibitum on a diet of crickets, and no instances of sexual cannibalism were observed. However, when the amount of food given to the female was varied so as to produce ‘moderately hungry’ or ‘starved’ females, the picture changed dramatically. Most of the females that were
‘moderately hungry’ ate the male at some
sexual behaviour can be elicited. Also, removing the male’s head results in rhythmic sexual movethe earlier report ments, confirming by Roeder. Headless males, however, were not observed to mount the female, which is hardly surprising given the visual component in this behaviour. However, headless males were able to achieve intromission, even when extremely young, if the experimenter placed the headless insect on the female. Females also participate actively in the courtship by displaying various and abdominal movepostures ments. Sometimes females even stroke their partners before the flying leap - a touching display that does not conform to our usual stereotyped view of this insect. These ethological experiments were initially performed using females that
the males
with the females continuously. Of the males eaten in a sexual context during the daytime, only one was eaten after mounting; he was devoured head first but still succeeded in subsequent intromission and spermatophore transfer. This represents the only example of what the authors term ‘true sexual cannibalism’. Other males were eaten before mounting, or after mounting but before intromission. The majority of ‘starved’ females attacked their partner, but males that survived the initial onslaught mounted the females and copulated. The experiment was terminated at intromission so the authors were unable to see whether the contmued
on p. 350
TREE vol. 2, no. 12, December
escapees ultimately met their doom. Therefore, there seems little doubt that in this mantid species there is a strong relationship between female aggression and food deprivation. Courtship and mating can proceed perfectly amicably if the females are satiated, and decapitation of the male is not necessary for successful copulation. However, if females are hungry in the wild, one might expect to observe sexual cannibalism. The literature is rather obscure on this point, although the reports that do exist do not appear to support the view of frequent cannibalism in nature*. In a recent news article in TREE, I used the praying mantis as an extreme example of sexual feeding in insects5. Sexual feeding occurs when males offer females nutrients as an inducement for mating. In the mantis, therefore, the male himself becomes the nutrient. Sexual feeding can, of course, be studied in terms of the costs and benefits to each partner of this kind of ‘food for sex’ exchange. It is clear that ecological conditions are extremely important in determining the type of exchange that occurs, with available food resources being a critical factorsG7. Can we obtain any insight into the mantid’s behaviour within the context of sexual selection?
A simple view might be that the self-sacrifice of a male may ultimately result in an increase in the number of his offspring because the female could use the nutrients (i.e. the male) in her egg production, leading to better survival of fertilized eggs. A complicating factor here would perhaps be that only a small proportion of males succeed in mating in the wild. Possibly, they obtain several mates. If this is the case, then by definition they must have genes for ‘not getting eaten’, which will be passed on to their male progeny. Other males attempting to mate may get eaten before intromission. Such a situation would result in strong selection for males that do not get eaten. A study that might shed light on this general evolutionary theme would be an examination of who gets eaten and who does not. Perhaps eating a male before he can copulate, which evidently occurred in Liske and Davis’ study, is a rather extreme form of female rejection; perhaps she selects a mate based on a certain stimulus (e.g. male size or aspects of his display) and if the male fails to provide the correct stimulation and she is hungry, she attacks him. In the absence of any hard evidence on the frequency of sexual cannibalism in the wild, it is prema-
1987
ture to speculate too much along these lines. More work is required on the population density, age structure, food availability and mating dynamics of these insects before a clearer picture emerges. The role of sexual cannibalism may reveal some subtle insights into sexual selection in mantids. On the other hand, cannibalism may be so rare in the wild that it is not worth the effort of advancing evolutionary hypotheses to explain it. Nevertheless, the work of Liske and Davis has clarified some previous misconceptions about the sexual behaviour of this species. References 1 Roeder, K.D. (1935) Biol. Bull. 69, 203-220 2 Alcock, J. (1979) Animal Behaviour (2nd edn), Sinauer 3 Liske, E. and Davis, W.J. (1987) Anim. Behav. 35,1524-l 537 4 Bartley, T.A. (1982) Ann. Entomol. Sot.
Am. 75,484 5 Kyriacou, C.P. (1987) Trends Ecol. Evol. 2,85-86 6 Steele, R.H. (1986) Aim. Behav. 34, 1087-1098 7 Gwynne, D.T. (1981) Science 213, 779-780
C. P. Kyriacou is at the Dept of Genetics, University of Leicester, University Road, Leicester LE17RH,UK.
Plankton thatDon’Obey t theRules Ilkka Hanski versus-diversity problem (population-community approach) and in the ecosystem studies conducted during the International Biological Program (the process-functional approach). A well-known limitation of the population-community approach is the considerable redundancy of function often observed among species populations. For instance, in phytoplankton studies it is frequently found that factors other than the species composition of phytoplankton largely determine primary production. Recent studies have demonstrated the opposite redundancy, that is, species populations with radically alternative positions in their food webs. Stoecker et al.3 (see also Refs 4 and 5) show that some abundant marine planktonic ciliates consume unicellular algae without destroying their chloroplasts, which llkka Hanski is at the Dept of Zoology, Univer- continue to function and use light sity of Helsinki, P. Rautatiekatu 13, SF-00100 energy for photosynthesis inside ciliate. Helsinki, Finland. the Several common
The ecosystem concept has its roots in the study of small lakes and ponds. In a pioneering work, Lindemanl described the ‘trophic dynamics’ in lakes as the transfer of energy between the components of the ‘classic’ aquatic food chain, the producers (autotrophic algae), the consumers (zooplankton and fishes) and the decomposers (bacteria and other saprophages). Ecosystem ecology has remained a controversial and difficult subject. A recent exposition2 of hierarchy theory in ecosystem studies finds that both of the current approaches the population-community paradigm and the process-functional paradigm-unduly emphasize one of the many possible ‘observation sets’. Both approaches are commonly (though not universally) seen as having failed in solving the stability-
350
chloroplast-retaining species are mixotrophic, in other words, able to function both as grazers on phytoplankton and as autotrophs with their sequestered chloroplasts3. This phenomenon falls within a wider range of relationships between algae spanning from and protozoa, straightforward predator-prey interactions to endosymbiosis”. If these marine ciliates survive and reproduce in light with a minimum density of autotrophic algae (some are needed to provide the chloroplasts), other ‘heterotrophic’ zooplankton can do just the opposite, that is, grow and reproduce without light and phytoplankton. Salonen and Hammar studied macrozooplankton growth and reproduction in filtered water from small, humic lakes, using a radiotracer technique. They found that under low light intensity a mere 5%, and under high light intensity only 30-40%, of the carbon in zooplankton (Bosmina, Ceriodaphnia, Daphnia, Eudiaptomus, Scapholeberis) was of photosynthetic origin. In these experiments the zooplankton were not grazing on the food chain based on
lllk) ‘a, !, . 5’::0’ cc !$,, , ii‘“8t.II’,,rllird,,(“,i!‘.ilrillrld;~i~