Freshwater Biology (1993) 30, 35-45

Juvenile survival of a planktonic insect: effects of foodlimitation and predation

JANET M. FISCHER* AND MARIANNE V. MOORE*Department of Biological Sciences. Wellesley College, Wellesley, MA 02181-8283. U.S.A.

•* Present address: Center for Limnology, University of Wisconsin, 680 N. Park Street, Madison, Wl 53706, U.S.A.* Author to whom correspondence should be addressed

SUMMARY

1. An experiment was conducted to investigate potential impacts of food limitation andcopepod predation on juvenile survival of Chaoborus punctipennis. We tested the hypo-theses that: (i) juvenile survival of Chaoborus is influenced more by copepod predationthan by starvation in a productive environment, and (ii) food limitation and predationinteract to affect survival.2. Effects of food concentration (approximately 800, 1400 and 2300 microzooplankton 1~')and predator density (0, 1 and 2 Mesocyclops edax 1"̂ ) on Chaoborus development andsurvival were evaluated using a 3 x 3 factorial design. Jars containing lake water, the

, appropriate food and predator treatments, and two Chaoborus (<12 h old) were rotated ona plankton wheel at 25°C. Survival and developmental stage were monitored daily untilall individuals had either died or moulted to instar II.3. Predation by Mesocyclops was the major source of mortality, causing 87.5% of Chaoborusdeaths over all treatments. Chaoborus mortality was significantly higher in treatmentswith Mesocyclops (67-100%) than in predator-free treatment (0-13%).4. Development time was sigruficantly longer in the low-density food treatment thanin the highest food treatment.5. No significant interaction between food limitation and predation was detected.6. These results suggest that predation by copepods may limit recruitment of juvenileChaoborus in productive lakes.

Introduction

In many invertebrate and fish populations, juvenilemortality is severe while adult mortality is relativelylow. For populations experiencing this type of mor-tality regime, investigation of processes influencingjuvenile mortality is fundamental to understandingabundance and distribution of adults (Neill, 1988;Olson & Olson, 1989; Sale, 1990). Food limitation andpredation influence juvenile survivorship in a widerange of aquatic spedes, including salamanders(Petranka, 1984), fish (Anderson, 1988; Leggett &Frank, 1990; Purcell & Grover, 1990), marine invert-ebrates (Olson, 1987; Daan, 1989; Petraitis, 1990;Stoner, 1990), and freshwater invertebrates (Neill &Peacock, 1980; Vanni, 1987; Baker, 1989; Osenberg,

1989; Spence, 1986). In many of these studies a singleprocess, either food limitation or predation, is ident-ified as the major constraint on juvenile survivorship(Daan, 1989; Osenberg, 1989; Purceli & Grover,1990; Stoner, 1990). Few studies, however, haveexamined experimentally the interactive effects offood linutation and predation on juvenile survivor-ship; two notable exceptions include Spence (1986)and Vanni (1987). Experiments investigating both therelative and interactive effects of food and predatorson juvenile survivorship are essential to improveour understanding of juvenile recruitment.

Chaoborus, a dipteran whose larvae inhabit thepelagic zone of freshwater lakes throughout theworld, lends itself particularly well to this t>^e ofinvestigation. As Chaoborus develops, individuals

35

36 }M. Fischer and M.V. Moore

pass through four distinct larval stages during whichtheir average body length increases approximatelyfour times (LaRow & Marzolf, 1970). Mortality ofearly instars (I and II) is often severe and can largelydetermine densities of later instars (III and IV) andadults (Neill & Peacock, 1980; Neill, 1988). Previousstudies suggest that juvenile mortality is influencedby food limitation {Neill & Peacock, 1980; Neill,1988). In a series of nutrient enrichment experimentsconducted in a Canadian montane lake, Neill &Peacock (1980) and Neill (1988) demonstrated thatthe survivorship bottleneck of early instar Chaoborustrhritattus (Loew) is removed when abundance of theirrotifer prey is enhanced. In this ultraoligotrophic fish-less lake, food limitation of early instars seems to bethe major constraint limiting Chaoborus abundance.

Other studies, however, suggest that predation bycopepods may affect survival of early instars. Intensepredation by the copepod, Diaptomus shoshone S.A.Forbes on juvenile Chaoborus has been proposed asa mechanism for the exclusion of Chaoborus fromfishless ponds in the Rocky Mountains (Sprules, 1972;Dodson, 1974; Williams, 1980). However, distributionof Diaptomus shoshone is limited to small lakes andponds in the Rocky and Sierra Nevada Mountains(Wilson, 1959). Very little is known about the poten-tial impact of predation by more common and widelydistributed cop>epod spedes on juvenile survival.Both large predatory copepods (e.g. Mesocyclopsand Epischura), and rotifer prey are abundant inmany productive lakes (Carter el al., 1980; Orcutt &Pace, 1984). Thus, predation may play a larger rolethan starvation in limiting population density ofChaoborus in more productive lakes.

Furthermore, food limitation and predation mayinteract to affect juvenile recruitment of Chaoborus,because predatory copepods and Chaoborus instar Iconsume similar prey (Williamson, 1983; Moore,1988). The degree of food limitation may enhance orreduce the effect of predation by altering the devel-opment time and/or escape response of juveniles.Thus, for spedes whose vulnerability to predation isgreatest at smaller body sizes or earlier stages ofdevelopment, loss of individuals due to predationmay be enhanced in environments with httle food.

Conversely, the intensity of predation may influ-ence the degree of food limitation if the predator alsocompetes with its prey for a common food source(Frank, 1986; Purcell & Grover, 1990). Predators may

reduce food densities to a level at which prey starve.Since the impact of predation is usually greaterat higher predator densities, enhanced starvationis most likely to occur in environments with highpredator densities.

The purpose of this study was to examine thepotential impacts of food limitation and copepod pre-dation on juvenile survival of Chaoborus punctipennis(Say) in a productive lake. The following hypotheseswere tested: (1) juvenile survival of Chaoborus isinfluenced more by copepod predation than bystarvation in a productive environment, and (2) foodlimitation and predation interact to affect survival.

Methods

Site description

Lake Waban is a 40-ha mesotrophic (Zmax = ^mean Secchi depth = 2.1m, total phosphorus = 40Hg y^) lake that borders the Wellesley College campusin Norfolk County, MA (Massachusetts Departmentof Environmental Engineering, Division of WaterPollution Control, 1981). This kettle lake is dimicticand during the summer it exhibits low hypolimneticoxygen concentrations (<lmgr*). The lake con-tains a small population of Chaoborus punctipennis(approximately 0.3 ± 0.11"^).

Field—laboratory experiment

Effects of predation and food limitation on juvenilesurvival of Chaoborus punctipennis were evaluatedin an experiment, conducted 17-25 July 1990, usinga 3 x 3 factorial design. Predator treatments in-duded three densities (0, 1 and 2 T^) of the predatorycopepod Mesocyclops edax (S.A. Forbes) (Fig. 1). Foodtreatments included ambient (natural lake water),one-half ambient and twice-ambient density ofplankton ranging in size (greatest axis of lineardimension) from 20 to 150 |im. This size class ofplankton represents the size range of prey consumedby Chaoborus punctipennis instar I (Moore, 1988).

Food treatments were prepared daily by sievingfreshly collected water from Lake Waban. Water wascollected using a bilge pump at a sampling stationnear the deepest point of the lake. Water was collectedfrom 3 m depth because Chaoborus first instars usuallyoccupy the lower epilimnion and upper metalimnion

Juvenile survival of Chaoborus 37

Fig. 1 Relative sizes of adult femaleMesoa/clops edax (left) and newly hatchedOtaoborus punctipennis instar I (right)used in the experiment. Drawing ofM. edax from Balcer, Korda & Dodson(1984).

500/im

(Moore, 1988). Mean temperature at 3 m in LakeWaban during the experiment was 25.2°C. In thelaboratory, adult females and late copepodid stagesof large predatory copepods {Mesocyclops edax andEpischura lacustris Forbes) were removed from thewater by hand. Predator-free water was well mixedand used to prepare food treatments that were addedto thirty-six (nine treatments, four replicates pertreatment) 1-1 clear glass bottles.

In both one-half and twice-ambient food treatments,picoplankton (<2 fim), nanoplankton (2-20 nm)and macroplankton (>150nm) were maintained atambient density while microplankton (20-150nm)were manipulated by sieving. In one-half ambienttreatments, microplankton were removed from halfof the water in each bottle. Twice-ambient bottlesreceived microplankton from an additional 11 of water.

Three replicate samples of each of the three freshlyprepared food treatments were preserved with Lugol'siodine on Day 0 and Day 4 of the experiment. Countsconducted on a compound microscope at 40x verifiedthat microzooplankton (plus the dinoflageilate, Cera-tium hirundella (O.F.M.) Schrank, and the chrysophyte,Dinobryon sp.) were successfully manipulated bysieving while macrozooplankton were maintained atambient density (Fig. 2). Hereafter, the term micro-zooplankton will also include Ceratium hirundella and

Dindjryon sp., because these taxa are ingested by earlyinstar Chaoborus (Moore, 1988). Microzooplanktonwere numerically dominated by Ceratium hirundella,Synchaeta kitina Rousselet, Keratella cochlearis (Gosse)and Kellicottia longispina (Kellicott) (Fig. 3). BetweenDay 0 and Day 4, a dramatic change in the density

4000

Ambient

Food treotment

2x ombien!

Fig. 2 Mean density (±SD) of microzooplankton plusCeratiutJi hirundella and Dinobryon sp. in exp»erimentalbotties on Day 0 (•) and Day 4 {•) of the experiment.Microzooplankton densities differed significantly amongfood treatments (F2,6 = 50.8, P< 0.001) and between Day 0and Day 4 (r,t, = 112.4; P<0.001) using two-way ANOVA.Hereafter, SD represents one standard deviation.

38 ].M. Fischer and M.V. Moore

Doy 0

5.4 4.14.2 9.0

22.3

21.6

55.7 69.4

Ceratium hirundella

Dinobryon sp.

Keratella cochlearis

Kellicottia longispina

Synchaeta kitina

Other

Fig. 3 Mean per cent numericalcomposition of the microzooplanktoncommunity (plus Ceratium hirundellaand Dinobryon sp.) in newly preparedambient food treatments on Day 0 andDay 4 of the experiment. Asterisksindicate per cent numerical comf>ositionis ^2.0%. The category 'other'includes Pompholyx sulcala Hudson andPolyarthra sp.

emd composition of the microzooplankton com-munity occurred in the lake. Mean microzooplanktondensity was significantly greater near the end of theexperiment (Day 4) than at the beginning (Day 0)(Fig. 2). Ambient S. kitina densities increased from1721"^ on Day 0 to 13981"' on Day 4, and Synchaetareplaced Ceratium hirundella as the dominant memberof the microzooplankton community.

Mean macrozooplankton density was similaramong all food treatments (two-way ANOVA,2̂,6 = 0-8, P = 0.46). Mean densities of macrozoo-

plankton on Day 0 and Day 4 were 23.4 ± 4.81"^ and24.8±4.9r \ respectively, and did not differ sig-nificantly (two-way ANOVA, Fi,6 = 0.4, P=0.54).Numerically dominant macrozooplankton includedDaphnia longiremis Sars, Daphnia retrocurva Forbes,Diaphanosoma birgei Korinek, Diaptomus minutus(Lilljeborg), Mesocyclops edax (males and early cope-podids only) and Tropocyclops prasinus mexicanusKiefer.

Plankton remaining in experimental bottles after24 h exposure to two Chaoborus instar I and 0, 1 or 2Mesocyclops were preserved on Day 5 to evaluateeffects of Chaoborus and Mesocyclops predation onmicrozooplankton densities. Mean microzooplanktondensity did not differ significantly before and after24h exposure to these predators ((-test, P=0.07).Soft-bodied rotifers lacking an escape response, suchas S. kitina, are the preferred prey of cyclopoid cope-pods (Stemberger, 1985) and juvenile Chaoborus(Moore & Gilbert, 1987). Nevertheless, counts ofS. kitina remaining in bottles on Day 5 indicated that

densities of S. kitina were not depleted significantlyover a 24-h period (f-test, P > 0.10). It is possible thatprey depletion occurred earlier in the experimentwhen Synchaeta densifies were much lower. How-ever, per cent depletion, estimated using literaturevalues for Chaoborus (Moore & Gilbert, 1987) andMesocyclops (Williamson, 1983) predation rates, wasprobably not greater than 50%, even in the one-halfambient food treatment.

On Day 1 of the experiment, two Chaoborus (<12hold; mean length = 1.16 ± 0.04mm) and either 0,1, or 2 acclimated adult female Mesocyclops (meanlength= 1.16±0.03mm) were added to each bottlecontaining the appropriate food treatment. Chaoboruswere cultured in the laboratory according to Moore(1986) and all individuals used in the experimentwere obtained from the same egg raft. Mesocyclopscollected from Lake Waban were acclimated on aplankton wheel in treatment bottles without Chao-borus for 24 h prior to the experiment. We chose to useadult female Mesocyclops as our experimental pre-dator because previous studies have demonstratedthat adult females are more voradous predators thanadult males and copepodites (Williamson & Magnien,1982). Hereafter, discussion oi Mesocyclops predationon Chaoborus wdU refer specifically to an interactionbetween adult female Mesocyclops and first instarChaoborus.

Bottles were sealed with caps containing plasticconical inserts to prevent formation of air bubbles.Bottles were mounted on a plankton wheel androtated for the duration of the experiment at 1 rpm

every 3min in a growth chamber at 25°C with an8:16 Ught:dark cycle. The chamber was lit with acool-white fluorescent light covered with a blackcloth to simulate light intensities at 3 m depth inLake Waban. Light intensity was 200 lux. Meanconcentration of dissolved oxygen in experimentalbottles containing freshly prepared food treatmentswas 8.1mgl~'. Dissolved oxygen in bottles con-taining two Chaoborus instar I and two Mesocyclopsdeclined to 7.4 ± 0.1 mgl"^ after 24h on the planktonwheel.

Chaoborus and Mesocyclops were transferred dailyto bottles containing freshly prepared food treatments.Survival and developmental stage of Chaoborus weremonitored during transfer. Transfers were executedcarefully using a wide-bore pipette (6 mm diam.)which did not alter the behaviour of the animals.In predator treatments, missing individuals wererecorded as predation-related mortalities. Recovereddead individuals were recorded as non-predahon-related mortalities. Mortality of Chaoborus due toexperimental error (i.e. individuals lost in transfer)was estimated from the number of unrecoveredindividuals in control (predator-free) treatments.Our dedsion to conduct this experiment in 1-1 bottleswas a compromise between the need to choose acontainer small enough to permit careful searchesfor dead and missing Chaoborus and the need toperform the experiment in a container that did notsignificantly alter the behaviour of the animals. Theexperiment was terminated when all Chaoborushad moulted to the second instar stage, becausevulnerability of Chaoborus instar 11 to Mesocyclopspredation is negligible (Moore Rodenhouse, 1986).

Mean per cent mortality and development time(days from hatching to instar 11) were calculated toevaluate the effects of food abundance and predatordensity on survival and development of juvenileChaoborus, Mean development Hme was calculatedonly for food treatments without predators becausemortality in treatments with predators was severe.Mean development time and per cent mortality werecalculated for each treatment using means frombottles (n = 4 per treatment). Contents of one bottlewere lost during the experiment due to an error intransfer and another bottle was excluded from theanalysis because Mesocyclops became covered withepiphytes.

The relative and interactive effects of food abun-

Juvenile survival of Chaoborus 39

dance and predator density on per cent mortalitywere examined using two-way ANOVA. Per centmortality data in this analysis were normalizedusing an arcsin transformation (Sokal & Rohlf, 1969).Development times of Chaoborus in predator-freefood treatments were compared using one-way nestedANOVA (bottles nested within treatments) andTukey's studentized range test.

Diel sampling

Day and night plankton samples were collected fromLake Waban on 25 July 1990 to monitor the spahaland temporal overlap of Chaoborus punctipennisinstar I and Mesocyclops edax adult females. It waspossible that predation-related mortalities in thelaboratory experiment were overestimated if Mesocy-clops exhibits pronounced diet vertical migrationsrelative to Chaoborus. Quantitative samples werecollected with a 102-|im mesh closing net by towingthrough each 2-m stratum from the bottom to thesurface. Samples were preserved with Lugol's iodineand counted with a dissecting microscope at 7 x .

Results

Field—laboratory experiment

Survival of juvenile Chaoborus was influenced moreby copepod predation than starvation (Table 1).Predation caused 87.5% of Chaoborus mortality overall treatments (Fig. 4). Per cent mortality of Chaoboruswas more than five times greater in treatments withMesocyclops (66.7—100%) than in predator-freetreatments (0-12.5%). Per cent mortality due topredation ranged from 50% to 100% in treatmentswith one predator. In treatments with two predators.

Table 1 Two-way ANOVA evaluating effects of food andpredator treatments on per cent mortality of C/iaof'orws instarI. Percentages were arcsin transformed before analysis

SourceSum of

df squares F

Food treatment 2 0.6 3.1 0.06Predator treatment 2 13.2 68.1 <0.001Interaction (food x predator) 4 0.1 0.3 0.87Error 25 2.4

(a)

40 J.M. Fischer and M. V, Moore

100-1

80-

60-

40-

20-

0

0 Predotors

Mortality source

Predation

Other

I Predator

l /2x ombient Ambient

Food treatment

ombient

Fig. 4 Per cent mortality of Chaoborus instar I in treatmentswith (a) zero, (b) one, (c) and two Mesocyclops predators. Thecategory 'other' represents non-predation-related mortalities(i.e. per cent dead Chaoborus recovered f>er treatment).Asterisks indicate treatmenls with zero mortality.

per cent predation-related mortality was 87.5%in each of the food treatments. Mortality due toexperimental error (i.e. individuals lost or injured intransfer) was estimated to be less than 4.2% and was,therefore, discounted in treatments with predators.Mortality due to factors other than predation andexperimental error (e.g. starvation) was relatively low(0-16.7%) and was not associated with a particularfood treatment. Neither food treatment alone, nor theinteraction of food and predator treatments, had asignificant effect on Chaoborus mortality (Table 1).

Food density influenced development time ofChaoborus instar I to instar 11 in predator-free treat-ments (Fig. 5). Mean development time was sig-

l/2x ambient Ambient

RxxJ treatment

2x ambient

Fig. 5 Mean development time (±SD) of Chaohorus instar Ito instar 11 for each food treatment lacking predators. Samplesizes ranged from 3 lo 4 per treatment. Means sharing acommon letter are not significantly different {P>0.05) asanalysed by one-way nested ANOVA and Tukey's studentizedrange test.

nificantly longer in the one-half ambient treatmentthan in the twice-ambient food treatment (nestedANOVA, f2,io = 8.61, P<0.01; Tukey's studentizedrange test). Mean development time in the ambientfood treatment, however, did not differ significantlyfrom that in either the one-half ambient or twice-ambient food treatments.

Diel sampling

Chaoborus instar 1 and Mesocyclops adult femalesoverlapped spatially and temporally in Lake Waban(Fig. 6). Maximum densities of both Chaoborus instarI (0.21"^) and Mesocyclops (l.OP^) in day and nightsamples occurred in the 4-6 m depth stratum.

Discussion

Predation

This study suggests that predation by copepods maycreate a juvenile bottleneck for Chaoborus populationsin productive lakes. Chaoborus mortality was so severein treatments with only one copepod predator (mor-tality ranged from 60% to 100%) that the presenceof an additional predator in the highest predatortreatment did not result in a corresponding increasein mortality. Therefore, juvenile recruitment may belimited by copepod predation at densities of onlyone adult female Mesocyclops \~^.

Juvenile survival of Chaoborus 41

Density {number I"')

0.4 0.6 0.8 1.0 1.2 1.4

8-10

Fig. 6 Vertical distributions of Oiaoborus punctipennis instar I(•) and Mesoci/chps edax adult females (a) at (a) 1500 and (b)2300 h, 25 July 1990, in Lake Waban, Massachusetts. Meandensities (±SD) of Cliaoborus and Mesocifclops were calculatedfrom three replicate closing net samples.

Although our experiments were conducted in smallenclosures, several lines of evidence suggest that ourfindings were not the result of forced interactionsin bottles. First, densities of predator and prey werewithin the range reported for eutrophic systems.Chaoborus instar 1 densities greater than 41"^ werereported by Yan, Lafrance & Hitchin (1982) and den-sities exceeding 21"^ have been observed by W.M.Lewis, Jr, J.F. Saunders and C. Cressa (pers. comm.).Mesocyclops edax adult female densities exceeding71"^ have also been documented (e.g. Williamson &Magnien, 1982). Second, containers of similar size orsmaller have been used in numerous studies of cope-pod and juvenile Chaoborus predation (Stemberger,1985; Williamson & Butler, 1986; Moore & Gilbert,1987; Schultze & Folt, 1990; Swift, 1992). Third, it isunlikely that the behaviour of Chaoborus was alteredsignificantly in the bottles used in this experiment.Early instar Chaoborus do not migrate (LaRow &Marzolf, 1970; Moore, 1988) and thus their die! move-ments were not constrained. Furthermore, Chaoborus

are sit-and-wait foragers. When they move, either tochange foraging position or to evade a predator, theytypically move one to three body lengths (1-3 mm)before assuming a stationary position (MooreRodenhouse, 1986). Thus, there should have beenspace in the experimental bottles for the escaperesponses of Chaoborus. Finally, similar predationrates were observed in containers whose volumeswere three times greater than those used in thisexperiment (M.V. Moore, unpublished). Furthermore,highly preferred alternative prey (i.e. Synchaeta) ofMesocyclops (Karabin, 1978; Williamson, 1983) were50-125 times more abundant than Chaoborus on thefirst day of the experiment and their abundanceincreased 10-fold by the end of the experiment. Thus,it is highly unlikely that Mesocyclops was forced toconsume Chaoborus because alternative prey werescarce (see also Methods).

Interestingly, Mesocyclops and Chaoborus are re-ciprocal predators (Williams, 1980), and it is possiblethat such predators exert strong prey selection fortheir future predator. Reciprocal predators are thosethat eat each other at different stages of their lifecycles (Williams, 1980; Polis, Myers & Holt, 1989).For example, adult predatory copepods consumejuvenile Chaoborus (Li, Jacobs & Colwell, 1979; MooreRodenhouse, 1986), whereas instar IV Chaoborus eatadult and copepodite stages of predatory copepods(Fedorenko, 1975; Pastorok, 1980). Pastorok (1980)demonstrated that Chaoborus instar IV prefer cope-pods over cladoceran prey and results of our exper-iment indicate that adult predatory copepods eatjuvenile Chaoborus in the presence of abundantalternative prey like Synchaeta (Karabin, 1978;Williamson, 1983).

In nature, the impact of copepod predation onjuvenile Chaoborus. and hence the coexistence of thesetwo invertebrate predators, is probably affected bydensities of juvenile Chaoborus experienced by thecopepod, by aggregations of juvenile Chaoborus, andby the extent of seasonal overlap between predatorand prey. Prey density experienced by copepods isinfluenced both by the absolute density and detect-ability of prey. At low densities of Chaoborus, thecryptic movement of this sit-and-wait forager mayrender it unapparent to tactile invertebrate predatorssuch as copepods. We chose, however, to conductour experiment at a relatively high Chaoborus density(21~') within the natural range to maximize the

42 J.M. Fischer and M.V. Moore

probability of an encounter between predator andprey. Such high encounter rates are likely to occurin lakes containing large Chaoborus populations oraggregations. Such lakes include hypereutrophicsystems, where Chaoborus densities greater than 41"^occur (Sehgal & Jyoti, 1984), and meromictic lakes,where Chaoborus aggregate in narrow depth layersat concentrations as high as 42 T ' (Baker, Baker &Tyler, 1985). Densities of Chaoborus Instar I may alsobe high near hatching egg masses which float onthe water surface. Near such egg masses, effects ofcopepod predation may be as severe as that observedin this study. Some instar I Chaoborus. however,are likely to survive due to predator swamping.

The impact of copepod predation on juvenileChaoborus will also be influenced by the extent ofseasonal overlap between the appropriate life stagesof these two taxa. In north temperate lakes, Chaoborusemergence and oviposition often occur synchron-ously during short (2—3 weeks) periods of thesummer (von Ende, 1982), such that high densitiesof first instars suddenly enter the water column.Abundance of adult Mesocyclops often peaks in mid-summer (Balcer et al.. 1984; C.E. Williamson, pers.comm.) when first instars of Chaoborus punctipennisare present. The extent of seasonal overlap betweencopepod predators and Chaoborus prey may varyamong years and lakes with different abiotic con-difions (e.g. temperature), but how such differencesinfiuence phenologies and seasonal overlap is un-known. The combined effects of seasonal overlapof predator and prey, as well as prey density andaggregation wUl determine if the number of sur-viving Chaoborus is sufficient to maintain a viablepopulation.

Food limitation

Food abtmdance did not strongly affect juvenile sur-vival of Chaoborus in the three food treatments lackingpredators. Per cent mortality of Chaoborus was onlyslightly higher in the one-half ambient food treatment(12.5%) than in the ambient and twice-ambient foodtreatments (both 0%). Mean development time wasaffected by food abundance such that developmenttime decreased with increasing food density; how-ever, the difference between development time inthe one-half ambient and the twice-ambient foodtreatments was less than 1 day.

Our results are consistent with findings of previousstudies of food requirements of first instar Chaoboruspunctipennis and other Chaoborus spedes. A 2-foldincrease in microzooplankton density occurred inthe lake between Day 0 and Day 4 and, consequently,influenced our laboratory experiment. It is likely,however, that the prey density at which Chaoborusare no longer vulnerable to starvation lies somewherebetween the approximate mean density of prey inthe one-half ambient (800 microzooplankton 1~' or500 rotifers 1"') and ambient (1400 microzooplanktonr ' or 900 rotifers 1~̂ ) food treatments. In Michiganbog lakes, Chaoborus punctipennis are released froma survivorship bottleneck at rotifer densities ofapproximately 1000r^(C.N. vonEnde, pers. comm.).Other Chaoborus species appear to have similar foodrequirements. In a series of nutrient enrichmentexperiments, Neill & Peacock (1980) and Neill (1988)demonstrated that the survivorship bottleneck ofearly instar Chaoborus trivittatus is removed at rotiferdensities in the range 200-1000r\

In this experiment, the relatively weak effect offood limitation in comparison to predation supportsthe idea that the productivity of the system mayinfiuence the relative importance of food limitationand predation (Gliwicz, Ghilarov & Pijanowska,1981; Huntley & Boyd, 1984; Olson & Olson, 1989).Specifically, individuals in less productive environ-ments may be more vulnerable to food limitationthan those in more productive environments. Inproductive systems, where food limitation is rare,the importance of predation generally increases(Gbwicz et al., 1981). In ultraproductive systems,however, food may actually become less availablebecause of changes in spedes composition (Gliwiczet al,. 1981) or severe oscillations in food density(DeMott, 1989). For example, food (i.e. rotifers andmicroplankton) may become temporarily very scarcewhen Daphnia are abundant (Gilbert, 1988). However,food did not become scarce during this study, ratherabundance of the rotifer, Synchaeta. which is readilyconsumed by juvenile Chaoborus and predatorycopepods, increased 10-foId.

Interaction of food limitation and predation

The hypothesis that food limitation and predationinteract to jointly affect juvenile survival of Chaoboruswas not supported (Table 1). Predation-related mor-

tality was expected to increase in low-density foodtreatments due to lengthened development timesand thus increased exposure of Chaoborus instarI to Mesocyclops. Lack of a statistically significantinteraction was not surprising because (1) meandevelopment time was less than 1 day longer in one-half ambient food treatments than in twice-ambientfood treatments, and (2) predation-related mortalitywas severe even at the maximum development rates.

Predation by Mesocyclops was predicted to influencefood limitation for Chaoborus instar I because bothof these predators feed on microzooplankton. Wepredicted that, in treatments containing Mesocyclops,starvation of Chaoborus instar I would increase dueto depletion of available food by Mesocyclops. Sincemean microzooplankton density was not significantlydifferent before and after 24 h exposure to Mesocyclopsand Chaoborus instar I, predation by Mesocyclops didnot deplete the total amount of food available toChaoborus. Furthermore, high predation-relatedmortality which occurred during the first 2 daysof the experiment essentially precluded starvationbecause Chaoborus were eaten before they had timeto starve. According to Moore (1986), median timeto starvation for Chaoborus punctipennis instar I is4.9 days at 20°C.

Lack of interaction of food limitation and predationmay be common in productive pelagic systemswhere (1) predators and food are abundant, (2) refugefrom predation is essentially non-existent, and (3)predators are often highly mobile. Under theseconditions, juveniles may exhibit maximum devel-opment rates yet experience severe mortality due topredation. In contrast, in unproductive waters whereboth food and predators are rare, mortality due topredation may be reduced and juveniles may bemore vulnerable to starvation.

To make predictions about population dynamics oforganisms with complex life cycles hke Chaoborus,we must understand the processes which affectsurvival at critical life stages. We focused on ident-ifying processes that influence survival of juvenilesbecause Chaoborus are known to experience massivemortality during these life stages. Although recruit-ment of later Chaoborus instars (e.g. HI and TV) andadults may be limited by this juvenile bottleneck,the abundance of these later stages may also beinfluenced by factors such as fish predation on instarIV and bat or bird predation on adults.' This study

Juvenile survival of Chaoborus 43

lays the groundwork for larger-scale experimentsinvestigating the impact of copepod predation onChaoborus population dynamics by demonstratingthat predation by a widely distributed and commoncopepod spedes can cause severe mortality of juvenileChaoborus.

Acknowledgments

This research was supported by funds from theNSF-Research Experiences for Undergraduates Sitegrant DIR 8900754. We are grateful to Diane Krauseand Macduff Sheehy for field and laboratory assist-ance, and to W.M. Lewis, Jr, J.F. Saunders andC. Cressa, for the use of unpublished data. JohnRichardson designed and built the plankton wheeland Richard Stemberger assisted with rotifer tax-onomy. Comments by Bill DeMott, Tom Frost andNick Rodenhouse improved the manuscript.

References

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{Manuscript accepted 13 January 1993)