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The part played by two species of pompilid wasp in population changes of P. antipodiana was investigated. A correlation of r = 0.7 between the body length of the wasp and the captured spider was found. The wasps tended to be selective, mainly capturing medium sized spiders. The two wasp species showed some niche differentiation, with the large black hunting wasp (Salius monachus) particularly favouring P. antipodiana as prey. Young spiders were generally safe from attack as their tunnels were too small for most wasps to enter. Spider mortality rates due to wasp attack varied from 12-30%. Wasp mortality rates directly attributable to spider bite was as high as 11%. Spider survival was found to be attributable to six tactics of behaviour of which the most significant was the spider failing to respond to web stimuli. The hypothesis is advanced that the main ecological impact of the wasp is to reduce intraspecific competition among spiders. The long term implication of some spiders surviving to breed for six or more years is also considered.
In part I of this study (Laing, 1978) on populations of the tunnel web spider A taxonomic revision of the New Zealand Pompilidae being prepared by Mr A. C. Harris of the Otago Museum will show that the generic name Porrhothele antipodiana, several features were described. Among them was the decline in numbers evident in most populations over the summer period. These declines coincided with the activities of pompilid wasps of the genus Salius.* A hypothesis suggesting thatPriocnemus should be used for these species, now placed in Salius.
Because the summer population declines shown by the spider populations could be as high as 30-40%. it was considered that the activities of the wasps were worthy of closer study as an aid in understanding the population dynamics of P. antipodiana.
Two wasp species were active around This wasp has been incorrectly referred to as P. antipodiana webs over the summer months in Wellington. Both were members of the family Pompilidae (Psammocharidae). The large black hunting wasp, Salius monachus (plate 1), is heavily built and gives the impression
Salius monachus. This individual of 18 mm body length was captured on Johnson's Hill, Karori, Wellington. The burrow shown in plate 2 was the work of this particular wasp. Even though the red hunting wasp Salius wakefieldi may also capture tunnel web spiders, the black wasp is normally responsible for most captures of these spiders.
Salius wakefieldi, is a somewhat more lightly built wasp than the black species. Measurements of the thorax of 20 black wasps and 20 red wasps gave the following figures:Salius fugax in previous papers the author. (Laing, 1973, 1975, 1978.)
The ratios of thorax length : thorax depth; and of thorax length : thorax width calculated from the above measurements were as follows:
It is apparent from these ratios that S. monachus is definitely a stouter wasp than S. wakefieldi. This fact may have some bearing on the types of spiders which are captured by each wasp, and reference to this is made in the later section on the partial niche separation of the two species. Individuals of both species may grow to a body length in excess of 20 mm, but the majority of those in the 20-25 mm range are black wasps.
In the Wellington areas studied, the wasps usually made their appearance in mid-October, though for those years when cool springs were experienced, early November was the time of appearance. Capture of tunnel-web spiders was seen between mid-November and February as shown below for 24 observations in Wellington (1974-77):
Adult pompilid wasps are nectar feeders. The spiders that they capture are sealed in burrows along with the wasp's egg in order to provide food for the developing wasp larva. It is because of this behaviour that the exact ecological status of the Pompilidae is not clear. Their relatives, the ichneumon wasps, have been called parasitoids due to their habit of laying eggs in the living tissues of host. The ichneumon larvae destroy their host, and so are not true
When the spider has been captured by the wasp. one or more of its legs may be chewed off, possibly to make transport to a prepared burrow easier. It is at this stage that the wasp may be observed
Salius monachus, Johnson's Hill, Karori, Wellington. Location was on a low clay bank. Burrow diameter was 12mm. The crumbled clay below the entrance is characteristic of burrows dug by this species.
The fact that hunting wasps often capture spiders far larger than themselves has been noted by most writers on the subject. Rau and Rau (1918) describe seeing a wasp dragging a spider at least five times its own weight; Petrunkevitch (1926) found that Pepsis marginata was paralysing Cyrtopholis portoricae individuals which were eight times heavier than itself. Andrewes (1969) writes of the spider being up to ten times the weight of the wasp in these associations.
In New Zealand, Quail (1903), who appears to have been the first to publish material on the Porrhothele/Salius association, described an example where the spider was grossly larger than the wasp. Miller (1971) mentions very much the same point in connection with these two species. There can be no doubt that these events do occur, and that they are quite striking visually. However, it is more usual in the New Zealand species for the wasp body length and the body length of the captured spider to be similar. To illustrate this point, a scatter diagram (Fig. 1) was drawn up from measurements of 24 wasp/captured spider pairs. These 24 sets of figures were obtained in Wellington between 1974-77, and in each case both the wasp and the spider were accurately measured. The correlation of 0.7 between wasp body length and captured spider body length is rather high for biological data, but is probably accounted for by the small sample size. For a sample of 24, the correlation of 0.7 is significant at the 1% level, and so it would be justifiable to claim a definite relationship between wasp body length and spider body length for the S. monachus/P. antipodiana association.
In terms of body weight, the New Zealand species are similar to the examples quoted earlier. An 18 mm S. monachus weighs around 0.2 g whereas an 18 mm P. antipodiana weighs around 1.0g. The weight of the spider is commonly five times that of the wasp in this association. In the case of an 18 mm S. monachus capturing a 23 mm P. antipodiana, the spider may be as much as ten times the weight of the wasp.
In this sample of 24 captures it was found that the spiders most often taken by the wasps were those in the 15-19 mm body length range:
It was felt that some confirmation of prey size favoured by the wasps was called for. The above figures were derived from observed captures only and hence represent only a small proportion of the captures that take place, most captures not being observed. Figures for the numbers of spiders missing from their webs over the summer period, and assumed to have been captured by wasps, are shown below. They were obtained from three different sites near Wellington.
From the size distribution of spiders at these sites in late October (prior to hunting wasp activity), the expected size distribution has been calculated, assuming that wasps had been unselective in their choice of spiders. Comparison of these expected values with the number of empty webs observed, shows that the wasps were clearly selective, again preferring spiders in the medium size range (Chi-square = 24.3; P < .001).
When both species of Salius were found active in the same area, direct comparisons of their hunting behaviour could be made. The first difference to strike the author was that the black wasp was a vigorous explorer of sheet webs and tunnel entrances, and would often disappear into the tunnel for up to ten seconds. The red wasp, on the other hand, paid more attention to gaps such as those between stones, under wood, and in crevices. It certainly walked over the sheet webs of P. antipodiana but did not spend as much time investigating the tunnel entrance or its interior as the black wasp.
The significance of these broad behavioural observations shows up when the types of spiders they capture are compared. When both wasp species were present in the one locality. and when both P. antipodiana and the brown grass spider Miturga were also present then the following pattern occurred regarding spider captures:
Salius monachus and body length of P. antipodiana captured by these wasps. N = 24 and correlation coefficient = 0.7.
It is clear that at this particular site we can accept the hypothesis that there is a genuine difference between the two wasp species in their choice of spiders (Chi-square = 25.9; P < .001). Ecologically this means there is at least a partial niche separation which reduces interspecific competition to a minimum when both wasps and both spiders are found in the same locality. However, when Porrhothele is not present, S. monachus mainly captures Miturga, while S. wakefieldi will take Dolomedes and lycosid spiders in the absence of Miturga. Thus generalisations on the food selection by these two wasp species cannot be made with much confidence.
The importance of the foraging behaviour in bringing about the partial niche separation must be recognised. Behaviour which leads
Miturga captures. On the other hand, behaviour which leads to much investigation of webs is likely to lead to Porrhothele captures. The origin of these behavioural differences can only be postulated, but two suggestions can be put forward: (i) that each wasp species learns where to look for the type of spider it fed on during the larval stage. Thorpe (1963) thought it probable that the early olfactory cueing at the larval stage could be what directed the adult to the appropriate host in some Hymenoptera. (ii) That each wasp species inherits a slightly different combination of kinesis or taxis components and this directs their foraging in slightly different directions.
These figures on prey differences can be related to the information on the wasp characteristics presented earlier in the article. The stouter bodied S. monachus specialises in hunting P. antipodiana; it needs the stouter body to withstand this spider's long, powerful fangs which have more penetrating power than the small fangs of Miturga and similar spiders.
What determines the size of spider that any given wasp is able to capture? The author is of the view that the diameter of the spider's tunnel places the lower limit on how small a spider can be taken, due to the restriction placed on larger wasps entering the tunnel. The upper limit is likely to be due to how readily the wasp is able to subdue a spider much larger than itself. Alternatively, there is some evidence (dealt with in the section on spider survival tactics) that very large spiders may be avoided because of the problems they cause the wasp in dragging them to a burrow, and then in fitting them into the burrow.
Using information gathered mainly during the study on a crib wall population at Johnsonville, figure 2 was drawn up to show the relationship between wasp body-length and size of spider which was likely to form the prey. The red wasps at that locality had a range of from 10-17 mm body-length with a mean body-length of 13 mm. The black wasps there had a range of 13-21 mm with a mean body-length of 16 mm. The smallest red wasps were able to enter the tunnels of spiders of approximately their own body-length. However, as only a few of the wasps were this small, the young spiders (being one year old at this time) were not under much hunting pressure. The tunnels of the second and third year spiders (spiders mainly in the 15-20 mm range) were able to be entered by most of the red wasps and all but the very large black wasps.
The outcome of these size relationships was that in most cases the first year spiders were safe from attack, as the capture statistics presented earlier have shown. The second year spiders, because they
In part I of this study several populations were described and the mortality rates due to factors operating over the summer period were
The author's estimate was that these three factors could account for up to 25% of those spiders which were missing over summer. Accordingly, the summer mortality due to wasps could be three-quarters of the 17-40% figures quoted earlier. This would give a wasp-induced mortality rate of between 12% and 30%, depending on the population being considered.
Entomologists who have written on the topic of hunting wasps and their spider prey have usually emphasised the ease with which the wasp subdues the spider. Rarely has any consideration been given to any mortality suffered by the wasp in these encounters. One could be forgiven for thinking that entomologists feel obliged to champion the cause of their wasps. There can be no doubting that the Pompilid wasp is a difficult insect for most spiders to subdue. Ambrose Quail, writing in 1903, put it very succinctly when he described S. monachus as a ‘regular Ned Kelly’, pointing out how impregnable the armoured body of the wasp must be to the spider's fangs. The body of the Salius wasps is not only very tough, but it is also shiny. This makes it doubly difficult for the spider's fangs to grip and pierce the wasp. During encounters between P. antipodiana and S. monachus which were observed at close quarters, the spider's fangs could be heard scratching over the wasp's body, unable to grip or penetrate. There is, however, at least one point in the wasp's body where it is vulnerable—and that is the junction between the head and the thorax. It must occasionally happen that the spider's fangs do slip into this joint, and in plate 3, an example of this is shown. The venom of P. antipodiana is certainly powerful enough to kill the Salius wasps. In experiments conducted on the German wasp V. germanica, a P. antipodiana bite lasting for two seconds immobilised the wasp in a little over five
P. antipodiana, body length 22 mm, was found feeding on the headless body of an S. monachus female, body length 17 mm. It is most likely that the spider's fangs penetrated between the head and the thorax of the wasp in this encounter, for this was the area the spider was found feeding from.
P. antipodiana is often fatal to an animal as large as a mouse.
The question of how many wasps are killed by spiders during the summer months is difficult to determine with any great accuracy, for if the wasp does lose an encounter, its body will most likely remain out of sight, deep within the spider's tunnel. Analysis of prey remains in tunnels has given some pointers to the wasp mortality rate though. Over the five years 1972-76, approximately 300 wasp sightings were recorded by the author. Over the same period, 8 dead wasps were found in P. antipodiana tunnels in the same locality as the sightings were made. This gave an estimate of a 2.6% mortality rate. This must be viewed as a highly conservative estimate. The real figure, for the reason already given, is likely to be much higher. The tunnels which were opened for inspection were a small proportion of the total population, and the main reason for sampling them was to gain general information on the prey taken by P. antipodiana.
Additional evidence for wasp mortality came from detailed studies
These values suggest a possible wasp mortality of 11%. Of the wasps killed. 3 were S. monachus and 3 were S. wakefieldi, which in itself is interesting, for even though the red wasp mainly hunts Miturga, sufficient numbers of them must enter P. antipodiana tunnels for such encounters to occur.
It is worth comparing these results with the results of laboratory investigations in which the wasp is rarely troubled by the spider's defence. For example. Petrunkevitch (1926), in an extensive examination of the wasp Pepsis and its attack pattern, found that the wasp was successful in the 200 or more encounters he observed. The problem with this type of study is that taking the spider out of its natural habitat considerably reduces its ability to defend itself The spider in a dark tunnel or burrow is far better equipped to defend itself than when it is brought out into an open, well lit environment. The latter conditions favour a quick moving, highly visual animal such as a wasp. The following section on spider tactics investigates how the spider does have some protection in its natural habitat.
The spider is faced with a formidable hunter. possesing an armoured body which largely renders the spider's weapons ineffective. In addition the sting of the wasp is powerful enough to immobilise even the largest P. antipodiana individuals. Along with these features. the wasp is an assiduous and persistent hunter; it is unlikely to miss out on investigating many of the webs in its search area. for by its very nature as a prey-capture device, the sheet web of Porrhothele must be located in the open.
Considering these facts, it seems surprising that there is not an almost 100% mortality rate among the spiders in areas where wasps are active. The question that poses itself is: what factors operate to ensure the survival of 70-90% of the spiders in a population which is facing wasp activity?
The following are some of the factors which are likely to be responsible for spider survival (see Fig. 3):
Non-response to stimuli from the sheet web during daylight may seem to be stating the obvious; however, when examined in detail, like any other biological variable it turns out to be complex. Mygalomorph spiders generally tend to be photo-negative and avoid exposure to light. They are reluctant to venture out of their tunnels in periods of bright light. There is a conflict of behaviour here, for it is one of the spider's most natural responses to react to web stimuli, for this is how they obtain their food. This conflict of drives can be demonstrated by dropping a slater into a sheet web and watching. Often the spider will appear at its tunnel entrance and then come no further. The author's interpretation of this behaviour is that at first the spider responded to the web stimuli, but on moving along its tunnel the light became progressively brighter until it inhibited the approach response to the prey in the web.
Not all individuals in a P. antipodiana population respond in the same way to web stimuli during the day; some appear readily at the tunnel entrance whereas others can never be enticed out of their tunnels. To illustrate this point, the response times of 42 spiders in one population are given in Figure 4. All of the spiders were second year or older and the test was performed with slaters; the slater was dropped on its back into the sheet web and left to entice the spider out. Times were recorded from when the slater was dropped in until the spider made its appearance at the edge of the sheet web. The P. antipodiana individuals which responded rapidly were described as ‘reactors’, while those individuals taking 60 seconds or longer to appear were described as ‘non-reactors’.
The reactors are the individuals which will be most at risk from the wasps, for they would be vulnerable, being out in the open and in strong light. These are most likely to be the spiders that Miller (1971) had in mind when he wrote of the wasp being naturally cautious and waiting until the spider had been enticed out of its tunnel before delivering the paralysing sting.
Evidence for the significance of this survival factor was obtained from the Johnsonville crib wall population. Here it was the
P. antipodiana populations.
‘reactors’ which disappeared from their webs very early on in the wasp season. Fig. 5 shows the results from one summer investigation on reaction times and survival.
Results such as this confirm that a slow reaction time is likely to be important for the survival of P. antipodiana in the face of hunting wasp predation.
The work by Coville (1976) on the wasp Chalybion contains a similar inference; that the reactor spiders are those most likely to be captured by the wasp. This variable may well be of widespread importance in spider-wasp relationships.
During the summer months it was common to see the openings of P. antipodiana tunnels covered by layers of silk, the thickness of which varied from tunnel to tunnel. Why this was done is not clear, but it may have been a sign of temporary inactivity by the spider. Whatever the case, the cover certainly does act as a partial deterrent to hunting wasps intent on entering the tunnel. It did not represent a complete barrier, for a determined wasp could force its way through. Often, though, the wasps moved off to investigate other areas after some entanglement with the silken barrier. When the number of wasps seen entering covered tunnels was compared with those entering open tunnels, it was found that the silk provided a significant degree of protection (Chi-square = 8.8; P < .01).
On a number of occasions, wasps were seen to enter and then remain within a tunnel for ten seconds or longer before reappearing. Several of these tunnels were opened up to see if a spider was resident there. In some of these instances, the spider was found sheltering at one end of a divided tunnel. Side tunnels of this type (see Fig. 3, d) are not found in all P. antipodiana webs, but where conditions permit
One of the surprising features of P. antipodiana was the discovery that during the dry months of summer, that is any time from December onward, up to 20% of a population was likely to be aestivating. Aestivation over summer may be common in Mygalomorphs, for Forster and Forster (1975) have noted that the trap door spiders of the genus Cantuaria also aestivate over summer until autumn. Aestivation introduces a difficulty in assessing the numbers of spiders that have been captured by wasps, for during this phase the sheet web becomes broken and weathered, in the same fashion as when a spider is no longer resident. Counts made later in the summer or early autumn usually reveal which spiders have been aestivating and which have gone from their webs. The effects of aestivation, apart from conservation of body fluids and food reserves, are that wasps do not usually waste time investigating old webs; thus aestivation may protect a spider from wasp attack.
Experiments carried out by the author on spiders and wasps in captivity showed that the larger spiders could sustain several quick stings from a Salius wasp and yet continue to run, even if a little unsteadily. The effect of the first sting was usually to make the spider take evasive action. Observations under natural conditions have been similar; with spiders observed escaping from their webs and running fast enough to escape the wasp, which is usually left running excitedly in circles in search of the spider. Leaving the web at speed after the initial contact with the wasp must enable a number of spiders to survive.
It has already been pointed out that the mortality rate of the wasps that can be attributed to the bite of the spider is at least 2.6% and may be as high as 11%. Active defence on the part of the spider is certainly a survival factor. Often the combat does not proceed to the point where one party is overcome; the wasp has been observed leaving the tunnel entrance where it could be seen wrestling with the spider. These cases always involved large spiders, and it would seem that the wasp was often reluctant to proceed against spiders with a
The reasons why wasps may not persist against large spiders are most likely to be or a combination of the following:
The second reason is certainly a practical one, for the diameter of the burrows dug by S. monachus ranged from 10-14 mm in the localities studied. A burrow of this size would not accommodate the very large spiders.
An attempt has been made to rank these factors in order to compare their effects on the survival of P. antipodiana. All of the information was taken from actual field observations. In some cases assumptions had to be made as to the effectiveness of a factor and these are noted on the chart:
These observations certainly support the non-response category as the most significant factor in the survival of the spider during the wasp season.
The selective action of the wasps in removing mainly the young-to-recently-mature members of a Porrhothele population must have some effect on the population structure of the spiders. Reduction of the number of spiders would certainly lower the pressure on food
P. antipodiana population in Palmerston North, where intermittent observation over several years had failed to show the presence of Salius wasps, revealed large numbers of spiders in the 13-18 mm body length range. This is the type of observation that could be expected if the hypothesis that the wasps' activities reduce intraspecific competition among the spiders is a valid one. However, it is obvious that a more detailed investigation of growth rates and age structures would be necessary before this hypothesis could be confirmed.
Continuing the theme of the selective behaviour of the wasps, it does seem necessary to assume learning behaviour on the part of the wasp. The avoidance of large spiders, and the prevalence of medium sized spiders as prey indicate to the author that the wasps may learn preferences for certain sized spiders. Such learning ability would be of no great surprise to those familiar with the work of Tinbergen on the bee-wasp Philanthus; or that of Baerends on the sand wasp Ammophila. For a discussion of the learning abilities of these and other Hymenoptera, Thorpe (1963) should be consulted. Another source of information on the intricacies of hunting-wasp behaviour is the very readable work by Rau and Rau (1918).
Relating the selection theme to Part I of this study, it can be seen as a partial explanation for the reduction of the Johnsonville crib-wall population almost to zero. This particular population was a young one with few large spiders; as such it was particularly susceptible to wasp activity, and the results of several years predation by the wasps proved this to be the case.
It has already been mentioned that certain individuals in a Porrhothele population survive year after year despite the activities of Salius wasps. There may well be long-term genetic implications arising from this; for the individuals surviving and breeding for many years are contributing large numbers of their genes to the gene pool. If they survive longer because of certain characteristics they possess then it is likely these characteristics will be spread through the gene pool. It is known that any one mature P. antipodiana female can produce up to 300 offspring in one year. A spider which survives to breed for six years could contribute her genetic material to 1800 offspring; whereas those individuals that are captured by wasps at the end of their first breeding season will have contributed to a maximum of 300 offspring each.
While it is relatively easy to discover the number of offspring produced by the spider, it is more difficult to say with any certainty how many offspring each wasp is likely to leave each season. From a knowledge of the number of wasps active in a given area, and utilising information on how many spiders have been captured in that area, it was possible to give an estimation of the number of wasp offspring
P. antipodiana populations are unlikely to be seriously threatened by wasp activity in the long term.
If a broader perspective is taken and the Pompilidae are considered in terms of trophic levels, then the fact that they procure food for their larvae from the third trophic level would mean that they must always be relatively insignificant in terms of biomass. This is characteristic of a predator which preys on other predators.
I would like to thank Dr Salius.
Published by the Entomological Society of New Zealand. Bulletin 4. 42 pp. 1977. Price $2.00. Available from Mrs B. M. May, c/o. Entomology Division, D.S.I.R., Private Bag, Auckland, New Zealand.
This list replaces an earlier ‘interim list’ issued in 1967 by the Society. It has been considerably expanded and now has about 860 entries, most of which are insects although mites, spiders, harvestmen, slugs, snails, and nematodes of economic importance are included. Standardisation of common names is, of course, the main objective of this bulletin, so that there will be no excuse for ambiguous communication between scientists and laymen where insect names are concerned. But there is more to it than that, for it provides a useful checklist of up-to-date nomenclature for the scientist and teacher. Each scientific name entry gives genus and species, author, family and order. Cross-referencing is employed for those species with recent name changes or where more than one name has been in common usage. A commendable effort has also been made to bring in Maori names where applicable — these are placed in parenthesis after the common name. Like the previous list, it is arranged in two parts, a scientific names index and a common names index.
The list is recommended to all who need to write or talk about common insects and terrestrial invertebrates and that must include a pretty wide range of New Zealand biologists.
Published by Heinemann Educational Books (N.Z.) Ltd. 230 pp. 1978. $24.75.
It is a difficult task to write for both the scientist and the interested layman within the confines of a single book but it is one that has been squarely tackled by Dr Bob McDowall in this much-needed reference work on the New Zealand freshwater fish fauna. To the freshwater biologist, the book is a mine of authoritative information on many aspects of our river and lake fishes, written by an expert who has spent his life catching and studying these species. To the fisherman or keen layman it may appear at first sight to be frighteningly scientific but it is certainly not incomprehensible. Although it contains many scientific terms (all explained), the text presents a wealth of easily readable natural history information.
The major part of the book comprises descriptive sections which treat each species of fish, family by family. An introductory chapter outlines morphological features of value for classifying and identifying fishes and explains the terms and measurements used in the descriptive sections. Field techniques are discussed and a key to all families of fishes found in fresh water is given. Incidentally, the definition of ‘freshwater fishes’ extends from wholly freshwater species to those that are basically marine but regularly enter estuaries and lowland rivers, so that fishes like kahawai, the mullets and a stargazer fall within the scope of this book.
Beautifully clear drawings by the author, as well as colour and monochrome photographs, illustrate each fish — its habitats and its diagnostic features. In most cases identification should be possible from the illustrations alone. However, all aids are provided with considerable emphasis on keys for family and species identification. The reference list with over 250 entries should be a valuable source of material for future workers.
Although the descriptive chapters concentrate on reference material, presented in a carefully standardised format which does not lend itself to casual reading, there is some scope for the latter in the chapters on New Zealand fisheries, the diseases and parasites of fishes and the distribution and relationships of our fish fauna. Here we find summaries of fish introductions, historical comments on fisheries (i.e. the days when West-Coasters used whitebait as garden fertiliser) and an expression of concern for the lack of consideration given to wetlands and freshwater fishes in the hurly-burly of ‘progress’.
There are many biologists who will find this book indispensable, others who will want to have it amongst their ‘answers to queries’ books and a still larger number of fishermen and naturalists who will enjoy its information and appreciate its clear guide to the fishes. All these readers should be well pleased and particularly grateful to Dr McDowall for presenting it so clearly and accurately.
The need to understand ecological processes and the dynamics of natural populations becomes more urgent as our utilisation of natural animal and plant resources becomes more intensive. During the last decade there has been reluctant recognition of the limitations inherent in the use of deterministic models to describe population functions of single species. While deterministic models have found wide acceptance in fisheries and game management, few take account of the complex relationships which any species has with its environment, and with other living components of an ecosystem. Consequently the limited success of such models in accurately predicting population changes is hardly surprising. The result has been renewed interest in ecosystem unit modelling and some of the problems we face with respect to aquatic ecosystems have been ably summarised by Mann (1972).
At first sight it might appear illogical to attempt to analyse ecosystem units before situations involving only single species can be resolved satisfactorily, but this is not so. Such analyses focus on the hierarchial structures of ecosystems, the flow of energy within them, the nature and patterns of primary productivity in a given system, the efficiency of energy transfer from one trophic level to the next, and the relative importance of horizontal links for degradation of energy within a trophic level. Rather than just considering numbers of animals or plants such studies can help us assess the nature and magnitude of the extrinsic and stochastic factors which so strongly influence the structure and relative sizes of populations in the real world. They permit us to quantify and evaluate some of the complexities of community structure, and to begin to perceive the mechanisms governing ecosystem stability. They may aid in the detection of quantitative changes in numbers and relationships of ecosystem components, and perhaps enable us to forecast the onset of those long term regular and irregular fluctuations in conditions, which so frequently confound predictions based on relatively simple deterministic population models. Acquisition of such knowledge cannot help but improve our understanding of the ecology and population dynamics of single populations.
The fundamental nature of the differences in the structures of terrestrial and marine ecosystems is still not generally appreciated, partly because experimental and simulation studies of system stability have usually involved terrestrial situations. Stability in marine environments is a concept which has received relatively little attention (Steele, 1974, p. 29), and in any case ‘stability’ is a word used with varying meaning by different authors. By some it has been used to imply equilibrium within an ecosystem, with only minor population size fluctuations among its components; for example, a tropical rain forest climax. Others use the same word but imply persistence of the ecosystem despite large fluctuations in the numerical values of components. Recently Holling (1973) applied the useful and descriptive term resilient to ecosystems which survive despite such large component fluctuations, and this is used here in preference to the term ‘stability’ coined by Smith (1972). Unless otherwise specified, discussion in this paper is concerned with resilience.
The purpose of the present paper is to draw together a number of ideas and findings from several independent lines of research, and to discuss a number of factors with possible bearing on the resilience of those pelagic marine ecosystems which characteristically have large component fluctuations. Before this is done, it is pertinent to consider briefly some modern ideas which relate to natural system stability.
May (1972), Smith (1972), Holling (1973) and Poole (1974) have reviewed the theories which attempt to describe in quantitative terms the interactions — either through predation or competition — of two or more natural animal populations. Most ecologists will be quite familiar with the Lotka-Volterra equations (Lotka 1925. Volterra 1928), and the numerous modifications and elaborations of these paired differential equations. The validity of the Lotka-Volterra equations has long been challenged, since the constraints implied in their application are quite unrealistic, and while they generate fairly regular oscillations in purely deterministic simulations, the prey species invariably oscillates to extinction under application of realistic stochastic influences (Bartlett 1957). The model of host-parasitic interactions proposed by Nicholson and Bailey (1935) suffers from similar deficiencies (Poole 1974).
Leslie and Gower (1960) experimented with modified forms of Lotka-type equations in stochastic simulations; their results paralleled in a general way some of the earlier experimental studies by Gause (1934) with Paramecium and the protozoan predator Didinium, and Utida (1957) with the bean weevil Callosobruchus and its parasite Heterospilus prosopidis, in that unprotected prey invariably became extinct, followed by the extinction of the predator. Leslie and Gower (1960) then attempted to simulate that section of Gause's study in
Protection of a significant fraction of any prey population from predation at any given time, whether through heterogeneous spatial distribution (Smith 1972), defence mechanisms, superior mobility of some prey, or differing predator responses to changing prey densities as considered by Holling (1959), and Griffiths and Holling (1969), appears to be essential for the survival of systems with components with large numerical fluctuations. A second factor which may be of great importance in system persistence is the time lag implicit in predator responses to build-up of prey. The existence of such time lags is implicit in a number of studies, and the concept was explored in quantitative terms by Wangersky and Cunningham (1957). Holling and Ewing (1971) combined the features of both explicit time lags and prey protection into a theoretical model in which prey protection counteracted the destabilising effects of time lag in predator response. The idea of a fraction of the prey population being particularly susceptible to ‘contagious attack’, was developed earlier by Griffiths and Holling (1969).
One of our major problems is that there is still no common philosophical approach to formulation of such hypotheses. Many of the models include the implication that population fluctuations are taking place around some kind of mean value; others (Milne 1957a, 1957b, 1962, and Holling 1973) have suggested that such equilibria may not in fact exist but are the result of the influence of statistical theory on much of our thought. Milne concluded that the upper limit of fluctuations was controlled by the carrying capacity of the environment, and the lower level by simple extinction. There is also a growing belief that the search for models which lead to conditions of neutral stability — as with Leslie and Gower's model — should be abandoned, since such neutral stability seems to occur very rarely in nature (Holling 1973).
Bulmer (1975) investigated phase difference in predator-prey relationships and established a model for the inter-relationships of the ten-year population cycles recognisable in some boreal mammals and ground-nesting birds in Canada. He concluded that, in general, the cycle of a species which fluctuated in such a manner appeared to be driven by another cyclic species which was either the prey or predator of the first species. He also calculated that if there was no density
Implicit in all these studies is the idea that if we can satisfactorily understand which factors are most important in population interactions between two or more species, we will ultimately be able to expand this knowledge to interactions between whole trophic levels. For example, Dempster (1971, 1975) determined that starvation was the major factor in prey population control in the case of the cinnabar moth Tyria jacobaeae, with predators of the larvae exercising only an incidental effect. Limited mobility of the ‘predators’ (i.e. = herbivorous caterpillars) and spatial heterogeneity in ‘prey’ (i.e. = food plants) distribution appear to provide some degree of protection to the vegetation. Such protection of vegetation is particularly evident in forest ecosystems, where most cycling of elements takes place following leaf fall, through the detritus route (Odum 1971), and totally defoliating attacks by consumers, e.g. migratory locust, are the exception rather than the rule. Crisp (1964) in the section of his book dealing with the nature of grazing in terrestrial ecosystems, estimated that barely 15% of the total standing crop of vegetation was eaten by herbivores in a given growing season, and that most terrestrial vegetation was protected by hard tissues, underground root systems, periodic leaf-fall, and so forth.
In pelagic marine ecosystems, however, although time lag phenomena are readily recognised, for example in patterns of grazing by herbivorous zooplankton, protection of a substantial fraction of the pelagic vegetation seems to be nearly non-existent. The significance of this seems to have escaped the attention of most workers. There is ready agreement that phytoplankton seems to be consumed about as fast as it is produced, but in the literature there is relatively little appreciation of the implications of this in terms of system stability and resilience discussed in the first part of this paper.
The evidence that such protection is lacking, is formidable.
et al. (1935), Wimpenney (1946) and others discussed the inverse relationship between distribution of phytoplankton and distribution of zooplankton. They concluded that this patchiness was caused primarily by intensive grazing, and was not just heterogeneous distribution resulting entirely from current movements and other physical effects. Studies by Menzel (1967), among others, have indicated that grazing by herbivorous copepods is in fact so intense that very little fallout of phytoplankton from upper waters seems to occur in most open oceanic areas. Estimates of sinking rates measured in mixed coastal waters are therefore suspect for application to general open ocean situations. Indeed, Riley (1963) doubted our ability to estimate sinking rates even to the nearest order of magnitude, and suggested that relative comparisons were the best we could hope for. These at least indicated that seasonal changes in sinking rates could occur. Animals of the lower trophic levels in most intermediate waters probably have to rely almost exclusively on detritus in the form of zooplankton faeces and colloidal aggregations if epipelagic autotrophs are eaten about as fast as they are produced. Furthermore the efficiency of energy transfer from one trophic level to the next in the sea, particularly from autotroph to herbivore, seems to be far above the 10% level generally accepted as a working value in terrestrial systems. Data for this conclusion were provided by Petipa et al. (1970), who found that transfer efficiency (measured as ratio of growth to ingestion) of herbivorous copepods in the Black Sea, was as high as 71%. The implications of the earlier discussion now become clear — if protection of a significant fraction of the epipelagic diatom vegetation of the sea does exist, it is far from obvious.
The phytoplankton populations appear to establish numerical ‘capital’ during the spring bloom, and this, together with the ‘interest’ accrued through subsequent reproduction, is steadily eroded through the season by zooplankton grazing until the populations are at a rather low level in middle to late summer. In most areas the pattern is generally repeated with a secondary autumnal bloom; after this numbers dwindle to minimal winter levels again.
Steele (1974) argued that heterogeneous spatial distribution of phytoplankton could not alone provide any kind of sufficient protection from grazing, especially since the distributions themselves seem largely to be effect rather than cause. Some have suggested that species diversity and predator switching responses may function together as protection in these systems. MacArthur (1955) argued elegantly that diversity can enhance stability in ecosystems, although he was really only considering the influence of diversity within essentially stable systems, rather than oscillating systems such as the pelagic north temperate marine environment. Smith (1972) developed an argument that both system stability and species diversity were primarily products of spatial heterogeneity, as shown in fig. 1. But more recently Goodman (1975) has concluded that no simple relationship
In his simulation of phytoplankton-zooplankton interactions in a marine system Steele (1974) was able to obtain persistence of the system for a 360-day period. He admitted, nevertheless, that this could only be done by assuming some generally not well-validated threshold responses at the herbivore level, and by incorporating some unrealistic parameters such as long-lived components and relatively low food chain efficiencies. In addition, Smith (1972) had already pointed out that translating a realistic approximation of spatial heterogeneity into a program to support such simulations is a most formidable task.
Steele concluded that unlike the situation in terrestrial ecosystems (Hairston et al. 1960), herbivores in pelagic marine systems are resource-limited. The available evidence strongly supports this view. Neglecting for the moment the influence of zooplankton, after the phytoplankton population reaches a certain level, the limiting factors will come into play. Probably the most important of these is the exhaustion of available nutrients in the immediate vicinity of the cells, or a change subsequent to this in the level of available nutrient for such processes within the cell (Laws 1975). Riley (1963) argued strongly that in his view this interplay between nutrients and phytoplankton
The balance of evidence suggests that grazing pressure in the pelagic marine system exerts a much more significant effect on the vegetation than in an analogous terrestrial situation. While grazing by zooplankters begins (or increases) immediately, it is unlikely that the density of overwintering zooplankters in temperate surface waters will be high (Raymont 1963). Nevertheless these populations increase rapidly after a measurable time lag. The decrease in phytoplankton concentration some weeks after the spring bloom is, at least in British waters, almost certainly associated with grazing by this increased population and not with an immediate reduction of light intensity or of available nutrients (Cushing 1958, Steele 1958). Steele found that the decrease in phytoplankton abundance occurred significantly earlier than any reduction in phosphate levels, and in a later paper (Steele 1961), he determined that quite large fluctuations in incident light levels in the North Sea had little effect on the populations of phytoplankton. It has also been suggested that there might be an adjustment by such populations to any particular light intensity, so that the rate of productivity and the nutrient supply are in balance (Ryther and Yentsch 1958). This seems somewhat less likely in view of Steele's findings concerning the lack of influence of variation in light levels. Both Steele and these workers found that production was limited by nutrient supply, but appeared to be independent of the concentration above a certain level (0.4 μg atoms P/litre according to Steele, 1958).
Riley (1963) was unable to accept the conclusion that the concentration of nutrients, and in particular phosphate, was not an important factor. If this was the case, he argued, then there would be no theoretical reason for the system to achieve a steady state; there would only be a maximum determined by the total carrying capacity. Yet the very essence of the arguments put forward by Milne (1957a, 1957b, 1962). Dempster (1975), and Holling (1973), seems to be that the idea of a ‘steady state’ is probably illusory. Nevertheless the emphatic expression of belief by Riley that nutrient concentrations are important determinative factors, is almost certainly justified. In practice the viewpoints are probably not irreconcilable, and for concentrations of phosphate below 0.4 μg, the findings of Riley and Steele are in agreement.
There remains, however, a basic conflict in the data obtained by Riley for George's Bank, and Steele, Cushing and others for European waters with respect to the relative importance of grazing by zooplankton in reducing phytoplankton numbers. Riley maintained that
While the proportion of diatoms to other phytoplanktonic organisms of similar size may vary from place to place — for example, in tropical Atlantic samples dinoflagellates may predominate — they usually form by far the largest fraction of the ‘phytomass’ of 5 μ and above in northern temperate surface waters.
That diatoms possess a rather unique pectin-silica test is well known, although all functions of this structure are not understood. Streaming of cytoplasm through a complex and elaborate system of pores, for example, appears to aid in locomotion (Fritsch 1965). Porter (1976) found that colonies of the green alga Sphaerocystis schroeteri were sometimes only damaged by passage through the gut of zooplankters, and the colonies were repaired by rapid cell replacement. In fact growth appeared to be enhanced by nutrients taken up during passage of the gut. The test of diatoms might give protection against digestion under some circumstances. To the best of my knowledge this has never been tested experimentally, but if this did occur it would have to be taken into account in estimates of grazing, and might even account for certain anomalous observations in the literature which need not be pursued here.
One view of the unique mode of division by diatoms into pairs of daughter cells, one of which is smaller than its kin, is that it is imposed on them by their morphology, i.e. that it is the price they pay for having the rigid pectin-silica test. I wish to propose an entirely different view, namely that reduction in size plays an important role in the basic reproduction and survival strategy of these species.
Diatom cells vary within the size range of 2 X 10-2 mm3 to 2 X 10-8 mm3 (Harvey 1950). There are size differences within populations and, more often, between populations of the same species. The typical asexual reproduction of diatoms by paired daughter cell formation with consequent reduction in modal size at each stage, was amply documented by Wimpenny (1936, 1946). Harvey (1950) noted that the reduction in cell volume in Didylum after a series of divisions could be as much as thirty fold. At any given time there seems to be a recognisable modal size in any specific population of diatoms (Wimpenny 1946; Lucas and Stubbings 1948). The approximate synchrony in such populations permitted Cushing (1953)
Navicula occurred when a critical minimum size of 8.5 μ was attained. It is fair to point out that reduction in size with division is a general rule, but that exceptions have been documented. In particular maintenance of daughter cell size in some culture strains of Nitzschia by enlargement through rapid intussusception has been observed (Fritsch 1965). This author noted that auxospores were actually quite rare in natural samples of phytoplankton, and cited other earlier workers' estimates of the relatively slow rate at which minimum size might usually be reached by diatoms; it seemed that auxospore formation would not be expected to occur more frequently than about once every two years in any particular individual lineage. Other workers (summarised by Raymont 1963), on the other hand, have found quite rapid reduction in modal size of populations within a single season.
Reproductive rates in diatom species vary considerably, but in Phaeodactylum they may be as high as one division every 24-36 hours under favourable natural conditions. Under less favourable circumstances the division rate can fall as low as one division every 18+ days (Raymont and Adams 1958). Even if grazing success can approach 100% in localised areas, it is obviously of vital importance to a diatom species that its reproductive rate be sufficient to cope with the worst possible combination of grazing pressure and unfavourable environmental conditions.
Since they have contagious distribution patterns, lack any significant form of habitat protection, and are subjected to progressively more intensive grazing by copepods through the summer, diatom species evolving under such feeding pressures might be expected to respond through increasing productivity. Since the supply of nutrients becomes limiting with respect to increase in biomass after a relatively
The rapid rate of division of most species under normal conditions will result in a significant reduction in mean particle size of the population in a relativel yshort time. The possible importance of this has not yet been fully explored, and it may well confer an important additional benefit. Brooks and Dodson (1965), and Kerr (1974), among others, have pointed out that relative size can be an important determinant in predator efficiency, and that observed size relationships are the result of size-dependent feedback between predator and prey.
Brooks and Dodson (1965) carried out a detailed study of feeding relationships between alewives (Alosa), zooplankton, and phytoplankton, in Crystal Lake, northern Connecticut. Their findings concerning the influence of size selectivity by predators can be briefly summarised as follows. When predation by alewives was moderate, both small and large zooplankters were common in their samples. When such predation was light, small plankters were competitively eliminated by large forms. The latter were presumed to be more efficient through possession of larger filtering surfaces because of a more favourable surface to volume ratio, giving reduced metabolic demands. The former were thought to have to work proportionately harder to resist sinking. When predation by alewives was intense, on the other hand, large zooplankters were selectively eliminated, and the smaller species, less attractive to fish because of their small particle size, predominated in samples.
From the energetic standpoint these authors believed that, all other things being equal, selection should tend to favour the predator with a feeding strategy that operated to take small numbers of larger particles rather than a large number of small particles. They suggested that whether or not a population was being eliminated depended on the average size of the smallest female instar which could produce viable eggs being below the particle size range exploited by the alewives. At this critical level they thought that not only particle size, but spatial distribution and escape movements might be of crucial marginal significance.
They also concluded that selection probably would not favour rigorous apportioning of food to body size, and pointed out that many congeneric zooplankters were of roughly similar size and were presumably of similar efficiency in food collecting. They suggested that all planktonic herbivores utilised small particles in the 1-15 μ range.
I believe, however, that where feeding of zooplankton on phytoplankton is concerned the specific range of particle size is far more
Kerr (1974) published a theoretical model based on trophic processes, and using the K-line concept developed by Paloheimo and Dickie (1966), concluded that prey and predator sizes are rather simply related, and that in living systems particle size was a far more important factor in predator grazing than particle density. Some important experimental studies giving insight into gain from grazing under different particle size regimes were carried out by Beamish and Dickie (1967) and Parsons and LeBrasseur (1970). When herbivorous pelagic crustaceans (copepods and euphausid furcilia) were fed with algae with individual size ranges having a modal value of 32 μ a weight gain of only 2% per day was noted; however, when the modal size of algae was in the 57-90 μ range the weight gain rose to 16-8%. It would seem, therefore, that successful utilisation of a prey species by a predator may be limited by a relatively small range of particle size. At one end of the scale the prey will be too large for the predator to easily manipulate it (Mann 1972), and at the other end of the scale be so small that not only might there be manipulation problems, but the predator's energy gain for energy cost through foraging and collection will become progressively smaller. Rapport and Turner (1975) recently published a theoretical consideration of feeding strategies; they concluded that as resources became limiting, different types of feeding strategy converged, as did respective consumption rates. Nevertheless, the available range of particles of a size which can be consumed with net energy gain must surely place constraints on just how far such convergence could go. Smith (1972) also considered the impact of relative catchability; the feeding efforts of a predator locally reducing prey numbers to a low level could well reduce the average catchability of the remaining prey, with profound effects not only on its own feeding strategy, but also on those of other predators seeking the same prey.
With respect to a specific predator or consumer, relatively rapid reduction of the individual particle size of a significant fraction of a food species population will affect first the feeding success, then shortly the feeding strategy of the consumer. A number of workers (as summarised by Steele 1974) have searched for switching responses among herbivorous zooplankton, to see if some kind of threshold was involved. The present author suggests that there may be no complex mechanism involved at all, and that simple reduction of availability of a favoured diatom species by a statistical shift of its population out of the optimal feeding particle size range characteristic of the consumer in question, will force upon the latter a change to alternative prey within that same optimal particle size range. While size is probably the most important single factor, it is clearly unlikely to be the only one involved; metabolite production by certain phytoplankton could deter zooplankters from feeding on them, and shape is probably also very important (Harvey 1937). The various larval and adult stages of zooplankters will all have different optimal particle size requirements. Marshall and Orr (1955) showed that Calanus finmarchicus will take a wide variety of diatom species if these are offered experimentally, but because of the effect of extra foraging time or handling time under limiting circumstances, a copepod is likely to optimalise its feeding strategy by taking food particles within a relatively narrow size and shape range. The successful exception to this might occur when small particles were locally dense enough that economical capture could take place. The catholic diet of Calanus finmarchicus is probably a factor in its success, since it certainly seems to be far more abundant in the boreal-temperate North Atlantic than many rather similar species. Ability to exploit a wide range of food species surely must statistically increase the chances of a predator finding food particles of optimum size.
Reduction of the modal value of particle size in the diatom population will, of course, not only function to remove it from the optimal feeding strategy zone of the first consumer, but also to expose the population sequentially to smaller consumers. Short generation time and consequent rapid reduction in size are likely to be strongly selected for, since this would reduce the time period of such exposures, and take advantage of any time lag in feeding reaction by the consumer to the newly available food source. While Hutchinson (1961) pointed out that few opportunities exist for simple physical niche diversification in turbulent open water, the concept of niche response surface, as examined by such authors as Makarewicz and Likens (1975), gives us a different view of the situation. By their definition, ‘niche’ variables may be considered as axes of an n-dimensional coordinate system defining the niche hyperspace. That part of the hyperspace occupied by or affected by a given species represents that species' niche hypervolume. Time, or duration, is certainly one of these axes, and by looking at the different particle
Even if the auxospore sometimes functions as an over-wintering stage as some authors believe, and is often involved in the onset of sexual reproduction (Chadefaud and Emberger 1960), it also serves the purpose of a kind of ‘quantum jump’ in size to somethi