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LIMNOLOGY

AND

September 1974 Volume Number 19 5

OCEANOGRAPHY
Adaptive change in plankton predation: A new hypothesis
Stanley I. Do&on
Department of Zoology, University of Wisconsin, Madison 53706

morphology in response to size-selective of cyclomorphosis

Abstract The literature of cyclomorphosis, the seasonal change in morphology within populations, is reviewed and a general theory concerning its adaptive significance is proposed. Several recent studies of cyclomorphic populations suggest that cyclomorphosis may be a means of reducing mortality due to size-selective predation. Various appurtenances (helmets, horns, or spines ) are grown by some prey species as an antilock and key mechanism to foil invertebrate predators. The larger prey species reduce the visible parts of their body to reduce vertebrate predation and elaborate hyaline appurtenances to foil invertebrates. Temporally, maximum development of appurtenances is best correlated with the presence of predator species. The appurtenances are not generally maintained in the absence of predators, presumably because of energy requirements for swimming and reproduction.

Cyclomorphosis involves the alternation of different morphs in time. Forms with elongate spines or body parts alternate, usually annually, with forms lacking these exuberances. Cyclomorphosis has been reported for some planktonic algae, rotifers, and crustaceans ( Hutchinson 1967). The most bizarre forms are usually found during the warmer part of the year. Total body size may increase, decrease, or remain the same throughout the cycle, depending on the species. The following discussion deals only with the gross features of cyclomorphosis; similar changes in small features such as the anal spines and antennal setae studied by Egloff ( 1968) are ignored. The proximal causes inducing cyclomorphosis are generally not well understood. A relatively warm, or warming, temperature is often contributory. Turbulence in the presence of light is required by DaphLIMNOLOGY AND OCEANOGRAPHY

nia ( Hazelwood 1966) although temperature is also involved (Egloff 1968). The effect of photoperiod has not been studied. Exuberant forms of rotifers have been correlated with starvation for Brachionus (Buchner et al. 1957) or with dense food ( Green 1963) or cold water ( Gallagher 1957). In the case of Brachionus and Asplanchna, concentrations of specific organic substances influence cyclomorphosis ( Gilbert 1973). Until recently, the adaptive significance of cyclomorphosis in all groups was thought to be related to buoyancy. Since warm water is less dense and less viscous than cold water, the exuberances were interpreted as brakes or parachutes to slow sinking in the summer. An experiment with preserved cyclomorphic forms of the dinoflagellate Ceratium ( Fritz 1935) supports this hypothesis, but these results are based on preserved plants which may have
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Dodson the size and shape of their prey. The specificity of the relationship between predator and prey suggests the lock and key rclationship of insect genitalia. Pejler (1957) and Edmondson ( 1965) found a relationship between the size of rotifers and of their food. Herbivorous rotifers ate particles on the order of 10 ,X or less, with larger rotifers eating larger particles. Even within one genus, such as Hexarthra, differcnccs in -the mastax (the jawlike structure) suggest different feeding specificities ( Hutchinson 1967). Asplanchna, a predaceous rotifer, cats particles between about 50 and 250 p long. Asplanchna sieboldi (850 p long) eats nonspined Brachionus calciflorus ( 150-220 p long) much more readily than spined ones of the same core body length ( Gilbert 1966). Pelagic filter-feeding copepods (0.5-3 mm) are to some degree able to control the sizes of particles they filter within the range of 7 to 70 p (Wilson 1973) : the various copepodid stages of Acartia tonsa ate the same minimum particle size (betwecn 10 and 15 E,L), but the upper size limit varied (about 30-60 p) depending on the size of the copepod (0.50-1.05 mm). Similarly, Hargrave and Gecn (1970) found four Calanoid copepod species to prefer Flagcllatcs 5 to 15 p long, a rather narrow range considering the total sizes of available phytoplankton. Cells with long spines (Ceratium and Chaetoceros) were not eaten. Adult Diaptomus oregonensis prcferred phytoplankton in the range of about 5 to 9 p ( 100-800 $) although particles LIP to 14.4 p were eaten ( McQucen 1969). Predaccous copepods in general prefer particles < 1 mm long. Adult Mesocyclops eclax prcfcrrcd immature to adult Diaptomw floridanus ( Confer 1971). Adult female AcanthocycZops viridus ate about ten times as many small (0.75-0.99 mm) Simocephalus vetulus per week as large ones (1.20-1.55 mm) (Smyly 1970). The two size classes were provided separately, but in excess. No mixed feeding trials wcrc ncrformcd. , but nreference is indicated ~

had altered densities through the leaching of their oil droplets. Exuberant forms of Daphnia, in fact, sink faster than the winter forms (Jacobs 1967). In contrast to the usual pattern of rotifer cyclomorphosis, Keratella cochlearis in large European lakes has its longest spine in the winter or early spring, the shortest spinc in August. Carlin ( 1943) suggested that the sclective mechanism involved was the dccreasc in buoyancy due to a decrease in turbulence with decreasing temperature, Green (1960) concluded that for a number of tropical rotifers, cyclomorphic development of spines was not correlated with cnvironmental parameters such as tempcraturc, which are rclatcd to buoyancy. The buoyancy hypothesis is clearly not universally applicable to cyclomorphosis, The buoyancy hypothesis has recently given way, at least for some crustaceans and rotifers, to hypotheses of predator avoidance. Jacobs (1967) found that exuberant Daphnia galeata mendota were better able to escape guppy predation than short-helmeted forms of the same core body size. Some rotifers grow spines to cscapc being eaten by other rotifers (Gilbcrt 1966 ). I would like to expand this idea and to propose that cyclomorphosis may be an adaptation to escape invertebrate predntion in many classes 0E organisms, First, it is necessary to show that invcrtcbrates prey in such a way as to invite a cyclomorphic response in their prey, and that invertebrate predation is generally intense enough to make cyclomorphosis a worthwhile adaptation. Drafts of this manuscript have profited from discussions with V. Dodson, W. T. Edmondson, C. Goulden, E. G. Leigh, L. B. Slobodkin, R. Smith, and F. Wiman. Sincere thanks are also due J. L. Brooks and 1~. T. Paine, whose ideas wcrc intellectual grandfathers of this paper. Mechanisms of invertebrate predation

Several studies have shown that invcrtcbrate predators have strict limitations on

Preclation and cyclomorphosis since the difference in number of small forms eaten (about 10x) is more than enough to offset the lesser volume of the smaller class (about a fourth that of the large animals). The predaccous stages of Cyclops bicuspidatus thomasi prcfcrrcd nauplii, rotifers, and their own copepodids to larger diaptomid copepodids and cladoccrans ( McQueen 1969). For a number of predaceous Calanoid copepods, Anderson (1970) found predation rates were invcrsely proportional to prey size over the range 0.4 to 2.2 mm. Dodson (1974) found adult Diaptomus shoshorw to prefer daphnids ( Daphnia and Ceriodaphnia) betwecn 0.5 and 0.9 mm; electivity coefficients for animals longer or smaller were lower than for those in the preferred range. Herbivorous filter-feeding Cladocera (0.5-2 mm long) prefer food particles from about 5 to 70 p (Burns 1968), with the larger animals eating larger items. Mordukhay-Boltovskaya (1958) found that the prcdaceous cladocerans Leptodora and Bythotrepes (l-10 mm long) preferred prey between 0.3 and 0.7 mm long, although larger animals were occasionally taken. Copepods, because of their agility, wcrc not eaten. Third and fourth instar Chaoborus larvae (lo-15 mm long) prefer prey in the size range of 0.7 to 1.2 mm (Dodson 1974). Allan (1973) found Chaoborus punctipennis to prefer food in the order Bosmina > Daphnia parvula > Cyclops sp. > Holopedium; he belicvcd that Bosmina was prcferred because of its small average size (0.33 mm) relative to the daphnia (0.79 mm). The Cyclops was of a preferred size (0.4 mm) but better able to cscapc being caught. The Holopedium, with its gclatinous case, was generally too large for the Chaoborus to grasp, Similarly Chydorus bicornutus was not found in midge guts, even though other species of Chydorus were ( C. Goulden personal communication); C. bicornutus differs chicfly from the other rclatcd spccics in having two long lateral spines. Vertebrate predators generally prefer prey larger than about 1 mm (Brooks 1968),

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with a maximum size of several centimeters, depending on the mouth size (Dodson and Dodson 1971). Thus, it is impossible for planktonic organisms to grow spines long enough to avoid being eaten by vertebratcs except for the very smallest ones. For cxamplc, small (1.9 cm) salamander larvae preferred Daphnia rosea from about 0.9 mm to not much larger than 1.6 mm ( Dodson 1972); these small vertebrates have the typically invertebrate pattern of a narrow size range of preferred food. In general then, predators prefer some size range of food particles, and for each trophic level and class, larger predators prefer larger prey. Each predator is also adapted to catch certain prey within its preferred size range: rotifers prcfcr rotifcrs, copepods eat other copepods, prcdaccous cladocerans eat cladocerans, and midge larvae prefer cladocerans. These size and spccics prefcrcnces arc a result of the trophic apparatus of the various predators. The malleatc or malleoramate mastax of herbivorous rotifers is spccialized to capture nannoplankton, while the incudatc trophi of Asplanchna arc spccializcd for catching small rotifers. The long but weak thoracic legs of Leptodora are spccializcd to catch cladocerans but not agile copepods, and so on. The raptorial organs of all these invertebrate predators are brought into play in response to a tactile stimulus. The eyes of rotifers and crustaceans, and most insects, arc useful in detecting light intensity and movcmcnt, but not for forming images. The specificity of prey for each predator can bc seen in the characteristic appearances of corpses after predation. Figure 1 shows a typical victim of D. shoshone: the top of the head, the tail spine, and the second antcnnac have been chewed off. Since most daphnids eaten were damaged in this way, the copepod must have a prcferred way of holding the prey. This suggests that a prey of the right size, but wrong shape, might bc rejected after being caught. For example, the prcscnce of long spines on B. calciflorus does not affect the rate of collision with Asplanchna, but de-

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Dodson Zooplankton consumed 100% of the average daily production in Bras dOr Lake and 66% in Morrisons Pond (Hargravc and Gecn 1970). Porters ( 1973) experiments suggcs t that zooplankton grazing determines the relative abundances and densities of phytoplankton species. Similarly, significant mortalitics in natural populations of small zooplankton spctics due to invertebrate predation have been reported. A population of Leptodora accounted for 33% of the daily net production of two Daphnia spccics (Wright 1965). Copcpodids IV, V, and VI of C. bicuspidatus thumasi ate about 31% of their own nauplius standing stock and 30.2% of the diaptomid nauplius standing stock in a year ( McQuecn 1969). About 90% of the total daphnid mortality was estimated to be due to Chaoborus americanus predation by Dodson ( 1972). During June and July between 20 and 40% of a D. parvula population was removed per day by Chaoborus nyblaei and C. punctipennis (Allan 1973). Discussion and conclusion9

I mm

Fig. 1. A Daphnia galeata mendotae that has been caten by 8 Diaptomus shoshone. Note the typical damage to the tail spine, helmet, and swimming antennae. Most of the Daphnia and Ceriodaphnia killed in feeding experiments with D. &o&one show this sort of damage (Dodson 1974).

creases the probability of being eaten once caught (Halbach 1971). Any factor which changes the prey shape, thcrcforc, might be of use in decreasing mortality. Given the apparently specialized nature of the predatory feeding apparatus, an energctitally unimportant appurtenance such as a spinc at the right place could make the prey unsuitable to its predator. The intensity of invertebrate predation If a connection exists between invertebrate predation (or grazing) and cyclomorphosis, then the predation rate must be a significant fraction of the preys total mortality. Several workers have found the herbivorous zooplankton able to limit or change the phytoplankton ( Cushing 1957). In Canyon Ferry Reservoir, zooplankton consumed as much as 85% of the daily net primary production (Wright 1.965).

The new hypothesis states that cyclomorphosis is largely a response to predation by invertebrates, vertcbratcs, or both. Prey populations may rcducc their mortality when invertebrate predators are abundant by a sort of antilock and key change in morphology that foils the tactile mode of feeding. Mortality due to vertebrate predators may be reduced by a change in morphology that reduces the core size of the prey spccics, making them less visible. There are several well documented examples of a cyclomorphic response to both invertebrate and vertebrate predation. 1~. Carlson (personal communication) fed Staurastrum pinque to D. galeata mendotae and followed the change in the sizefrequency distribution of the dcsmid. The Daphnia fed on the smaller individuals with short spines (about 44-p mean length), thus leaving the larger dcsmids (about 62 p) with long spines. The long spines prcsumably make the dcsmid larger than the largest size that the Daphnia can ingest.

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doubles its size. Keratellu cochlearis is Porter ( 1973) divided phytoplankton into an outstanding exception to the predator three functional groups: large, often filamentous, species that are rarely foulid in model of cyclomorphosis; it products the the guts of zooplankton cithcr because longest spines in late winter or early spring in large European lakes, when no prcdathey arc not catcn or actively rcjectcd; species cncascd in thick gelatinous sheaths ceous spccics arc abundant ( Carlin 1943). As in the other groups, cyclomorphosis that pass through grazers, frequently intact in Cladocera may easily be described as a and viable; and small edible spccics that In the Cladocera arc eaten and digested by grazers. Of rcsponsc to predation. a new phenomenon appears : the average thcsc three classes, populations of the first are unaffected by zooplankton grazing, adult body length (measured to exclude those of the second may be stimulated by spines, horns, or elongated helmets) may grazing, and the third suppressed. It is in decrease as the cxubcrances increase. In the smaller organisms-rotifers and algacthe third group that many cyclomorphic species are found, such as Staurastrum, Ce- the core body remains constant or inrat&m, and Asterionella. Thcrc is as yet crcascs as exuberances arc elaborated. This little direct evidence that grazing occurs is also true for the smaller cladocerans, such as some spccics of Bosmina (Wescnat the right time, and is intense enough, berg-Lund 1908; C. Goulden personal comto select for the appearance of cxubcrant prey forms, However, these forms do oc- munica tion ) . IIowcver, the cladocerans cur in summer, when invertebrate grazers bctwccn about I- and 2-mm adult length arc most active. ( interprctcd broadly) show a marked reduction in average core size as helmets or At least in some rotifers, cyclomorphosis spines lcngthcn. Dctailcd descriptions exis understood to be a response to invcrteBeauchamp ( 1952) and ist for SO~IWspecies of Daphnia (Brooks bratc predation. 1946), ScaphoZeberis ( Green 1963)) and Gilbert (1966, 1973) have shown that prc(Hartmann 1915). In some dnccous rotifers ( Asplanchnn) release a Ceriodaphnia protein into the water, to which prey rotispecies of these genera, the net effect of cyclomorphosis is to reduce the core of the fers (Brachionus) respond by growing long anterior and posterior spines. The forms body to a length of less than 1 mm, but with long spines occur only when As- to maintain a total size, at least in one planchna is abundant. Two common cy- dimension, of more than 1 .mm. Brooks clomorphic rotifers in the River Sokoto (1965) suggcstcd that the decrease in core (northern Nigeria) produced their longest size is a response to intensive size-selective spines in March and April (KerateZZa troppredation by fish. It occurs during the ica ) and June ( Brachionus caudatus) warmer part of the year. The seasonal as(Green 1960). Each spccics was dccreas- pcct is due to an increase in the number ing in number during the period of spinc of fish, via the hatching of a new year elongation; K. tropicu disappcarcd about class of many species in spring, and an a month before B. caudatus. At this time incrcasc in planktivore feeding rate due to of population decrease and spinc clongaincreasing or high water tempcraturc. Nution, the predaceous rotifer Aspknnchnn merous other studies bear out this hypothbrightwe& was most abundant. The cla- esis ( c.g. Wright 1965; Galbraith 1967). doceran Ilolopedium is not cyclomorphic, The mechanism for the production of but it uses tactics similar to those of some smaller core body size is that many fish, rotifers. Allan (1973) showed that IIoZo- during the warmer part of the year, feed pediums body is small enough to cscapc intensively on. zooplankton larger than vertebrate predation, but of a size prcabout 1 mm; limitations of the vertebrate fcrred by Chaoborus larvae. It cscapcs cyc probably preclude intense predation predation by Chaoborus by having, a clear, on particles smaller than about 1 mm. Howcvcr, Brooks ( 1965) also suggested gelatinous covering (or capsule) that nearly

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Dodson logical change with dcvelopmcnt during a lifetime is similar to changes seen in smaller spccics during an animal cycle of several generations. Adults of D. similis, longer than 2 mm, are longer than most invertebrate predators can handle; the young, as small as 0.9 mm, have high recurved helmets that increase their length by about 10%. Dodson (1974) suggested that the larger species arc probably an adap tntion to size-selective predation. In situations where vertebrate predation is absent ( such as small ponds) cladocerans can reduce their mortality greatly by being larger than the maximum size prcferrcd by the ubiquitous invertebrate predators. Daphniu gihba ( D. carinatu) and Daphnia barb&z of Africa are highly cyclomorphic as adults (Wagler 1936) and by far the largest cyclomorphic cladocerans (about 4 mm for D. gihha and 2 mm for D. barhata ) . Species of comparable size in North America (Daphnia magna and D. similis) and elsewhere (Daphnia atkinsoni, Daphniu dolichocep halu, and Dap hnin tias adults. hetana) are not cyclomorphic The fact that D. &ha and D. barbata ocCLU, respectively, with the unusually large and predaccous copepods Lover&z excellens (3-3.5 mm) and Lover&z f&fern (35 mm) (Hutchinson et al. 1932) suggests that they arc responding to invertebrate predators the same way daphnids respond to smaller invertebrate predators in North America and Europe. That is, although the young but not the adults of D. similis arc small enough (less helmets, etc.) to be eaten by size-selective invertebrate preda tars, both the young and adults of the two large cyclomorphic tropical daphnids arc of a size preferred by the large copepods. Since these spccics cxpericncc little or no visually directed predation, but perhaps significm t invertebrate tactile predation, their functional anatomy is analogous to that of the small cyclomorphic organisms that also cxpcriencc little vcrtcbratc but much invcrtcbratc predation. However, sadly little is known of the biology of thcsc tropical Duphnia; cnrcful mcasurcments of size and predator-specific death rates in these pop-

that elongated helmets (and in some spcties, tail spines) are associated with the small average ( summer ) size to maintain a certain critical biomass ncccssary for rapid reproduction but arc hyalinc to escape notice by the planktivorous fish. This second hypothesis has not generally been accepted. Jacobs ( 1967) presented several arguments that make it stem unlikely. A long helmet would increase the volume of a daphnid 1 mm long by only about 1.1% (the long tail spine by 0.01% ), and the short-helmeted forms are more massive than long-helmeted forms of the same length, in direct opposition to Brooks prcdiction. These objections do not contradict the invertebrate predation hypothesis: the long helmet is interpreted as a response to size-selective invertcbratc predation occurring at the same time as vertebrate predation. The predation hypothesis might also cxplain the curious example of cyclomorphosis in Scapholeberis (Green 1963). In S. mucronatcc the posterior spine and anterior horn Lmdergo cyclomorphic changes, but not in phase. The spine reaches its maximum length in the population as the horn is shortening. Attempts to explain this phenomenon as a result of some environmcntal factor were not satisfactory. However, the pattern of invertebrate predation for thcsc animals might be predicted to show a change with time: perhaps two populations of invertebrate predators (possibly different stages of one species) arc significant at different times, one being foiled by the horn, the other by the spine. Cyclomorphosis is seen only in animals that arc exposed to size-selective predation as a result of being smaller than or equal to the largest size preferred by invcrtcbrates (about 1.5-2 mm for most pelagic predators), Although the adults of intcrmediate-sized spccics arc strongly cyclomorphic, immature forms of the large Daphniu simiZis, not the adults, show a development similar to cyclomorphosis. This is not true cyclomorphosis, since the nconates always have high helmets and the adults ncvcr do. However, the morpho-

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ulations would provide a good test of the predation hypothesis of cyclomorphosis. Earlier workers looked at the proximal causes of cyclomorphosis, such as tempcrature or food density. These factors may act as environmental cuts to a prey spctics if they arc sufficiently well correlated with the advent of intense invertebrate predation. IIowevcr, there is no reason for different spccics, or cvcn widely separated populations, to USC the same cues. Pelagic invertcbratc predators are generally common only for a short period ( a few gcnerations ) each year, usually when their prey arc most common (cf. Wright 1965; Green 1960 ) . Cyclomorphosis should therefore bc corrclatcd with fluctuations in predator density, but not ncccssarily with any spccific set of environmental parameters. In a small geographic area, the intensity of invertebrate predation will Inc similar in similar nearby lakes and well corrclatcd with environmental conditions; predation patterns of widely separated lakes arc less likely to be similar and less likely to bc corrcla ted with the same environmental factors. Hence, the confusion about the cause of cyclomorphosis. Curiously little attention has been given previously to the noncxubcrant side of cyclomorphosis, nor has this work illuminated the problem. Apparently, the widely held but seldom stated hypothesis is that the production of exuberances costs energy that could othcrwisc be used to increase the growth rate or to product more eggs, Jacobs (1967) showed that the cncrgy contained in a high hchnet and long tail spinc in D. gulenta mendotae is worth only about a seventh of a resting egg. He also found that Daphnia with high helmets sank faster than nonhchnctcd Daphnia. This suggests that the hchnet also costs the extra energy used to maintain position in the water column, IIowcver, such speculation is science fiction; further rcscarch is nccdcd to show why organisms produce exuberances that arent rctaincd in all gcncrations. Cyclomorphic organisms can be divided into two groups on the basis of functional morphology ( Fig. 2) :

LENGTH A. 9. C. D.

OF PREY

WlICRONSI

Filter-feeding Zooplonkton Predaceous Rotifers Predaceous Crustaceans and Insects Planktivorous Vertebrates

Idealized relationship between prey Fig. 2. body size and tl re relative feeding intensity of predation on that prey. The three arrows mark the approximate sizes of cyclomorphic organisms. The left arrow refers to algae such as Cerutium, the center arrow to rotifers such as Brachionus, and the right arrow to cladocerans such as Bosminn or Daphnia. In each predator-prey relationship, cyclomorphosis is found in prey species that approach the maximum size caten by their respective invcrtcbrate predators.

1. Those organisms that are too small to experience vertebrate (visual.) predation. This class includes some of the larger planktonic algae (about 50 p long), rotifcrs ( about 250 p long), and cladocerans smaller than about 1 mm. These species are cyclomorphic in response to invertebratc predation alone, and their core body size does not dccrensc as spines or horns clongatc. Because of the very specific (tactilt) feeding methods of their predators, thcsc organisms can probably escape predation by elongating relatively small horns or spines at appropriate parts of the body. 2. Intcrmediatc-sized cladocerans (bc-. twccn 1 and 2 mm), which often face predation from both vertebrates and invertcbrates. Therefore, they reduce the visible parts of their body to escape vertebrate ( visual ) predators, and elaborate hyalinc spines, horns, or hchncts to foil invertcbrate (tactile) predators. Thus, they seem too small as prey to visually oriented prcdators and too large to tactile predators. Many large cladocerans (longer than about 2 mm) that can live only in the abscncc of intense vertebrate predation

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Dodson
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can outgrow the size-sclcctivc prcfcrcnccs of invertebrate predators. These species, not truly cyclomorphic, may resemble cyclomorphic species in imma turc, rclativcly small stages. A few Ixge species of Daphnia that occur with very large prcdaceous copepods may bc truly cyclomorphic. References
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Preclution und cyclomorphosis


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Submitted: 1 March 1974 Accepted: 3 June 1974