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COMPLEMENTARY FEEDING BY SIZE-SELECTIVE NICHES SUSTAINED PREDATION1 Stanley I. Dodson Department of Zoology, University of Washington, Seattle 98105 ABSTRACI’ A study of the planktonic communities of 24 similar ponds in the mountains of Colorado supports the hypothesis that one predator population can sustain another as a result of sizeselective predation on the prey of both predators. A highly selective predator excludes its preferred (large) food items and thus favors the presence of suboptimal (smaller-sized) prey populations which are the preferred food of the second, dependent, predator. The suboptimal prey species are found only with size-selective predators, and it is probable that these are the only suitable prey species for the dependent predator. This interaction can occur in simple communities but also appears to be common in more diverse, complex communities. To support the discussion of this interaction, the electivity coefficients and predation pressures of three freshwater planktivores were estimated. INTRODUCKCON Major characteristics of a community are the number, identity, and density of the various species; these are affected through the interaction of predation, competition, and chance processes against the background of the physical environment. Predation acts through its intensity and selectivity. HrbiEek (1962) reviewed evidencc of the effect of fish predation on zooplankton species composition and presented observations supporting the effect. Brooks and Dodson (1965) showed a relationship between the size-selective predation pattern and the specific zooplanktonic composition in aquatic communities, and Brooks (1968) measured experimentally the relative size-selective feeding pattern of the fish Alma pseudohmangus. This predator-prey relationship based on predation patterns can be extended to include interactions between predator species; Paine ( 1966) showed that the removal of a “keystone” predator species from a marine intertidal community resulted in a reduction of the number of herbivore and carnivore species in the community. I hypothesize that size-selective predation affects the diversity of predator as well as prey species in freshwater planktonic communities. This effect can be demonstrated in very simple communities consisting of four or fewer major animal species on the herbivore and primary carnivore trophic levels. It has been observed in planktonic co8mmunities of a series of small ponds at high altitudes in the mountains of western Colorado, in which some combination of the three most common herbivores and the three common predators makes up the simple zooplanktonic community of each pond. Fieldwork was done from the Rocky Mountain Biological Laboratory ( Gunnison Co.), Colorado. An important study area containing several ponds was the laboratory’s newly acquired Mexican Cut (the Nature Conservancy’s “Galena Mountain Project”) biological preserve. MATEXIALS AND METHODS More than 50 small ponds in the mountains around the Gunnison River Basin and l This research, was supported by National Scion Grand Mesa, Colorado, were sampled ence Foundation Undergraduate Research Program from 1965 to 1969. Of these, 24 were quangrants from Yale University during the summers of 1965 and 1966, and by a N.D.E.A. Title IV Feltitatively sampled several times during one lowship and an N.S.F. Ecology Training Grant to three summers. The ponds are all seep(both from the University of Washington) from age ponds above 2,700-m elevation, have 1966 to 1969. This paper is condensed from a large areas of open water (relative to Ph.D. thesis to be submitted to the Department of Zoology of the University of Washington. emergent vegetation), and lack fish. 131 132 STANLEY Qualitative samples were taken by repeatedly towing a No. 20 plankton net through all depths of these generally shallow ponds. Series of quantitative samples were collected by pumping 8 or 12 liters of middepth water through a No. 20 plankton net at evenly spaced intervals along the ponds longest axis. The major zooplankters were identified, and size ranges were measured to the nearest 0.033 mm with an eyepiece micrometer in a binocular dissecting microscope. The population size distributions for the Daphnia species were estimated by measuring the total length (to the nearest 0.033 mm) of about 200 haphazardly selected individuals from each set of samples. Bailey’s triple catch method (Bailey 1952) for small samples was used to estimate the size of larval salamander (Ambystoma tigrinum) populations. Clipped toes marked the larvae for recapture. Three ponds containing salamander populations were carefully surveyed and their volumes estimated. Thus, the salamander predation pressure could be calculated on a per liter bmasis. Estimates of the larval salamander predation pattern were made from the analysis of stomach contents. On each sampling date, three or more larvae were killed, their stomachs opened, and the species therein identified and counted. Any Daphnk-z present were also measured. Field observations and feeding experiments show that the salamander larvae feed only during the day and mostly during the morning hours. They were therefore collected in the early afternoon when their stomachs still contained the entire day’s meal, permitting a direct estimate of feeding rate. Feeding experiments provided estimates of the predation pattern of two species of the larval midge Chaoborus. These experiments were done at the University of Washington, where the Colorado Chaolborz~s is not available. However, there is no reason to suspect that these laboratory observations depart qualitatively from the Colorado midge’s natural predation pattern. A single well-fed fourth instar larva of I. DODSON Chaoborus nyblaei or C. fluvicans was placed in a glass vessel with a culture of reproducing Daphnia pulex. After 24 l-n- at 2OC, and 12 hr of light, the animals were killed and measured. The Daphnia which had been eaten by the Chuoborus were reduced to balls of chitin, so the original total length of these animals was estimated by measuring the length of the postabdominal claw. (There was a linear correlation between the claw length and total length with a correlation coefficient greater than 0.95.) The experiments were done first in vessels of 30 ml, then 200 ml, with average Daphniu densities of 57 to I70 per liter. The statistic used to measure the predators’ selectivity is described but not recommended by Ivlev ( 1901). It is calculated by dividing the available and eaten size distributions into corresponding size classes, which in this case correspond to daphnid instars. For the ith size class, the percentage of individuals taken by the predator (r$) is divided by the percentage of all individuals (~4) available to the predator: E = ri/pu. E is equal to unity if the predator is acting nonselectively by taking food in the same proportion as it is available. Values of 0 to +l indicate avoidance ( taking food in lesser proportion than available ) , and values of +1 to + a indicate preference (taking food in greater propor tion than available). Preference is synonymous with the “positive selectivity” or “electivity” of Ivlev ( 1961) and “predator interest” of Brooks ( lQ68), avoidance with lack of selectivity or electivity and lack of predator interest. Ivlev prefers a different coefficient, E’, calculated as E’ = (rt - pi)/ ( r4 + pi), because it is finitely bounded and evenly distributed about zero. Zero indicates nonselective feeding; values from -1 to 0 indicate avoidance, and values from 0 to +I indicate preference. For general use, E is more versatile than E’. Ratios of the E coefficients for different predators ( with the same available prey) are equivalent to ratios of the relative selectivity of the predators, although the E’ coefficients are not related in any simple way. Also, for purposes of graphic representation of , SIZE-SELEC’ITVE TABLE 1. Dominant zooplanktonic species in 24 Colorado ponds Size range (mm) Species 1911; larvae (snout-vent) Chaoborus americanus (Johannsen, 1903); instars III & IV i larval 6-11 (total length) Diaptomus shoshone S. A. Forbes, 0.2-3.0 1893 Herbivores Branchinecta coloradensis 0.2-12 Packard, 1874 Daphnia pulex Leydig, Emend. 1860” Richard, 1896 Daphnia rosea Saw, 1862” Emend, Richard, 1896 0.7-3.0 0.4-1.5 Diaptomus coloradensis Marsh, 0.1-1.2 1911 * As Brooks (1957) also found, many Daphnin pogulations in western North America closely resemble D. pulex Leydig, but are yet distinctly different. Some populations in my study ponds resembled D. minnehaha Herrick 1884, a species not accepted by Brooks ( 1957), who considered it a form of D. pulex Leydig. I also found undescribed populations with morphological variations from the typical D. rosen Sars. However, since the variations are very small, all daphnid populations in this study are referred to as either D. pulex or D. rosea. E coefficients, log E has the range of avoidance equal to that of preference ( as does E’). Therefore, I have chosen to use the E coefficient. An electivity function is a set of coefficients for the size classes of a population size distribution. RESULTS The major species and their size ranges are listed in Table 1. These species are found in two general community types, represented as A and B, depending on the presence or absence of actively feeding salamander larvae (Table 2). The major differences between the two, communities are that the herbivorous species of A are smaller than those of B and that A .contains two predators, while B contains one. Rotifers, (represented by 5 major ubiquitous species in the 24 ponds) were about 10 times as dense in the type A ponds as in type B ponds. Populations of Sida crystallina (0. F. Muller, 1875), The two zooplanktonic communities found in 24 Colorado ponds No. onds containing alB these species Species Chaoborus americanus Ambystoma tigrinum Daphnia rosea Diaptomus coloradensis Daphnia pulex Diaptomus shoshone Branchinecta coloradensis A 6-75 only 2, TABLE Community Predators Ambystoma tigrinum Gary, 133 PREDATION B r I l2 1 3 ubiquitous 8 I ’ 1 Ceriodaphnia, Holopedium, and other small cladoceran species are occasionally common in type A communities, but never in type B communities. Of the 15 type A communities, 13 are preceded by type B communities when there are no active salamander larvae in the pond. Depending on their life cycle in each pond, salamander larvae are usually absent or at low densities between the time of the spring thaw and the early summer months. In all 13 ponds, the type A community replaces type B during the first few weeks of larval salamander development (beginning in early summer). During the period of increasing salamander predation, type B species form resting eggs at the same time that resting eggs of the type A ( crustacean) species are hatching. Chaoborus larvae are present all year, but recruitment occurs only when type A species are present. Table 3 shows the relative frequency of the large D. pulex (D. mlinnehctb-like form) in Leechmere ( Gunnison Co., Colorado) and in the larval salamanders’ diet during the time of transition from the type B to type A community, In the 9 ponds which do not contain larval salamanders, type B communities persist TABLE 3. The relative frequency of Daphnia pulex as per cent of the total Daphnia, Leechmere, 1968 Date 9 Jul” 19 Jul 29 Jul 8 Aug * The salamander In plankton (%I In salamander diet (%) 38 35 38 11 11 0.5 eggs hatched 19 5 on about this date. 134 STANLEY TABLE The feeding rate of salamanders in 4. Leechmere, 1968 Old generation --- 25 9 19 29 13 28 12 I* Jun Jul Jul Jul Aug Aug Sep 4 4 4 3 1 11-k 4 65 45 102 10 IrI* -. 1,275 1,250 1,217 1,209 1,179 0 0 5 ~- 3 2 3 11t The feeding rate of two species of Species 111s 50 est. 11,420 75 est. 10,290 110 9,370 101 7,910 34 6,445 5,388 34 all summer. Only one species (Diaptomus coloradensis) occurs in both communities, and except during a short transition period, only one or the other of these two sets of spccics will be present. Stomach analyses showed plankton to be the major food of salamanders only during the first few weeks of development. After this, plankton makes up less than lo;/, of the diet; the larger part is composed of insect larvae and amphipods. Chaobor~ larvae and pupae are a significant component of the diet, and most midge mor- I* C. flavicans C. f lavicans C. nybluei * I: t II: j: III: 0 IV: oborus. per day III* w- 170 2.4 44 3:9 _~ 11-t 30 200 200 7 13 z7” Number of trials. Size of the experimental vessel in milliliters. Effective daphnid concentration (per liter). Number of Daphnia pulex eaten per day per ChaNote that an average of 3.2 Daphnia were eaten by C. flnvicnns. tality is due to salamander predation. Copepods are seldom eaten. Although larval salamander feeding rates and elcctivity coefficients were gathered over four summers from 3 ponds, only a representative set from the 1968 Leechmere samples is given (Tables 4 and 5). The electivity coefficients in Table 5 are for the average salamander stomach content on each date. In this pond, the salamander larvae develop from egg to adult in 1 yr, with the transformation occurring in the end of July or early August. The fourth and probably the third larval instars of Chaoborus spp. feed exclusively on zooplankton (Berg 1937). ChaoboYmCs americanus feeds about equally on the larger developmental stages of D. colora- Representative electivity coefficients of salamander larvae from Leechmere, 1968 __~ p_p_p.-.--L. Date Avg snout-vent salamander length (cm) 9 Jul 6.8 19 Jul 6. Chaoborus New generation 1* * I: Number of salamander larvae examined. t II: Average number of Daphnin eaten per salamander per day. 4: III: Estimated number of salamanders in the pond. Censuses were taken on two dates in 1967 and on 8 July and 30 August in 1968. The other values are interpolated. TABLE 5. TABLE - _Date I. DODSON 7.0 Electivity coefficient, above the weighted mean of the prey size class (mm) 0.09 0.18 0.57 0.70 0.50 0.94 1.32 1.14 5.85 1.51 10.4 1.88 31.0 2.14 0.00 0.00 0.57 0.67 0.42 0.80 0.96 1.04 3.18 1.27 3.86 1.51 13.3 1.81 29 Jul 7.3 0.06 0.50 0.15 0.67 0.25 0.80 1.64 1.01 2.23 1.24 2.05 1.37 2.07 1.61 29 Jul 1.9 0.07 0.50 0.28 0.67 0.71 0.80 1.97 1.01 2.49 1.24 2.33 1.37 1.87 1.61 13 Aug 3.2 0.03 0.50 0.14 0.64 0.78 0.77 2.03 0.97 5.61 1.27 2.90 1.51 0.93 1.71 28 Aug 3.9 0.00 0.54 0.23 0.64 0.34 0.77 0.85 1.01 1.72 1.21 3.26 1.44 3.27 1.44 12 Sep 4.6 0.00 0.50 0.00 0.64 0.50 0.84 1.49 0.97 _----_-.- 3.03 1.17 2.23 1.44 -- SIZE-SEL~ECTIVE TABLE 7. Electivity 135 PREDATION coefficients of the fourth instars of two species of Chaoborus Electivity coefficient, above the weighted mean of the prey size class (mm) Species Avg total length (mm) C. f lavicans 12.0 1.74 0.67 0.98 0.84 2.81 1.04 1.26 1.31 0.18 1.61 0.00 1.98 0.00 2.24 C. nyblaei 14.5 0.88 0.67 1.19 0.84 2.18 1.04 1.31 0.61 1.61 0.00 1.98 Elii den&s and most instars of Daphnia rosea. As stated above, no feeding experiments were done with C. americanus. However, the two species which were used arc similar to C. americanus, and they have elcctivity functions that are similar to each other. The feeding rate ( Table *6) and electivity coefficients (Table 7) obtained for C. flavicans are substituted for C. americaws, since thcsc species are most similar in size. The density of fourth instar C. amSericanus larvae on representative dates in 1968 can be found in Table 8. The volume of Leechmere is about 1.36 X lo7 liters. Thus, with the data from Tables 4, 6, and 8, we can estimate the Daphnia per liter per day removed by the two predators from the type A planktonic community of Leechmere (Table 9). DISCUSSION The distributions of salamander and midge larvae are strongly restricted by winter conditions. Both live in ponds that probably do not freeze solid in winter. When a healthy population of salamanders is feeding in such ponds that lack fish, one finds a zooplankton community characterized by Chaobow and a small species of Daphnia, and no large Daphniu, large copepods, or fairy shrimp. Furthermore, the midge and small daphnid are only found in ponds suppoarting either a salamander population or planktivorous fish. Because there is no evidence that the TABLE 8. The density of fourth instar Chaoborus Date Density crustaceans are environmentally limited in their distribution in these alpine ponds, the strong correlation of the distribution of the various crustacean species with the prcsence of salamanders and midges suggests a strong biological interaction. The larval salamanders’ type of electivity function favors the presence of the smaller components of the zooplankton. For example, during the transition from type B to type A communities and early salamander larva dcvelopmcnt in Lcechmere, the larger daphnid is proportionally 2 to 10 times as abundant in the salamanders’ diet as in the plankton (Table 3). Brooks ( 1968) reviewed evidence that this type of size-selcctivc predation on the larger planktonic prey is the general vertebrate planktivore pattern, The salamander is thus responsible for the specific prey composition of the type A community. It is just these species that the midge may best USC for food. Although the correlation betwcen midge and salamander distribution is largely due to environmental factors, suitable midge food is scarcer in type B communities, and therefore midge distribution may also be restricted by food requirements. More than half the size range of each type B species (except D. cooiradensis) is greater than the largest food preferred by the midge, Therefore, in the simple type A community, one predator (the salamander) produces and maintains a suitable feeding niche, via size-selective ( per liter ) americanus larvae in Leechmere, 1968 25 Jun 9 Jul 19 Jul 29 Jul 13 Aug 28 Aug 12 Sep 0.06 0.01 0.01 0.27 0.45 0.65 0.27 136 STANLEY TABLE 9. Comparative removal rates due to salamander and midge larvae predation, 1968 Daphnia Date 25 Jun 9 Jul 19 Jul 29 Jul 13 Aug 28 Rug 12 Sep _-._. liter-l day-l removed by ___-______ salamander Chaoborus 0.00038 0.048 0.061 0.085 0.060 0.016 0.014 0.19 0.03 0.03 0.86 1.44 2.08 0.87 Tota! Da;~&-/ 2.4 17.6 27.7 14.9 11.2 9.0 4.9 predation, for a second predator (the midge larva ) . A priori, other dependent predators, such as Diaptomus shoshone ( Anderson 1967)) could co-octiur with the salamander larvae. However, competition between midge larvae and D. shoshone for the few prey species is implied by similar electivity functions (unpublished data), and salamander predation on the bright red copepod must be relatively greater than on the transparent midge larva. In more complex systems in large lakes, two or more invertebrate dependent predators do cooccur with size-selective vertebrate predators ( Tonolli 1962). The electivity functions of the midge and salamander larvae are complementary. From the electivity functions (Tables 5 and 7) we see that the midge specializes on daphnids (and copepods) between the lengths of 0.7 and 1.5 mm. Plankters above about 1.7 mm are not caten. Conversely, the salamander avoids plankters smaller than about 1.0 mm and strongly selects those over this length. Major food items in the salamanders diet are planktonic amphipods 1,45 to 4.35 mm long and dipteran larvae up to 12 mm long. The midge is thus able to make use of a large portion of the size distribution of the small zooplankters that are avoided by the salamander larva. The midge’s preferred food size range corresponds to the type A species size ranges, while the salamander’s preferred food is mo,re the size of type B plankters or larger. The two electivity functions are not complementary in the sense of shoting equally strong food preferences. The salamanders may concentrate large zooplankters as much as 31 times over what is I. DODSON available; the midges concentrate smaller ones only as much as 2.8 times. The salamander’s predation pattern determines the prey species with which it coexists, but the salamander is not responsible for the major part of the mortality in type A communities ( Table 9). In Leechmere, the total take of daphnids by salamander larvae was estimated to be about a tenth that of the rather nonselective midge larvae. (The salamander values may be somewhat higher, since the estimates did not include the average of 0.5 to 11 eggs per female carried by the larger, adult daphnids-the size preferred by salamandcrs. ) Thus, the salamander larvae act as a keystone species. Zooplankters are not a major component of its diet, and salamanders prey relatively lightly on the zooplankton species. The few animals they do take result in selection for the presence of small species, and these are harvested by the midge (for whom they arc a major part of the diet), There is much anecdotal evidence for the widespread occurrence of complementary feeding niches in aquatic communities. Galbraith’s (1967) study of the effect of rainbow trout predation on lake zooplankton populations supports the complementary niche hypothesis. After rainbow trout were added to Sporely Lake ( Michigan), the relatively large D. pulex was replaced by two smaller daphnid species and the average daphnid size decreased from 1.4 to 0.8 mm. The standing crop of daphnids decreased (but not the number of individuals) while that of other small cladoceran species (Bosmina longirostris, Chydorus sphuericus, and Diaptomus minutes) increased. Also Galbraith (personal communication) found that the percentage of daphnids between 0.4 and 0.7 mm increased from an average of 6% to 52% and the daphnid predator Leptodora kindtii appeared after the addition of trout. Mordukhai-Boltovskaya ( 1958) showed that L. kindtii does not eat cladocerans larger than about 0.7 mm. Thus Leptodora appeared in Sporely Lake only after the addition of the size-selective predator, as if in response SIZE-SELECTIVE PREDATION to the increased food supply maintained by the increased size-selective predation. Along with the cladoceran predator Leptodora, species of Bythotrephes and Polypherr~u.s,the several species of large predatory Calanoid copepods such as Limnocalunus, Heterocope, and Epischura, and the numerous Chaoborus species all occur typically in the planktonic communities of large lakes that generally contain one or more strong size-selective predators (usually various species of planktivorous fish). [E.g., see the habitat preferences of these species in Edmondson ( 1959 ) and Illics ( 1967). ] Since these are all prey of size-selective predators that feed using visual clues, it is not surprising that they are morphologically similar. They are often quite attcnuate, about the same size (on the order of 0.5 to 1.5 cm long), and transparent or only faintly colored. Where their food preferences have been investigated, they are known to prefer rotifers, the smaller spcties of Calanoid copepods, and clado&ra less than 1.5 mm long, such as Ceriodaphnia spp. and Bosmina spp. (Berg 1937; Mordukhai-Boltovskaya 1958). Thus, they depend on the prey species whose presence is favored by the highly selective feeding behavior of the co-occurring predators. REFERENCES ANDERSON, R. S. 1967. Diaptomid copepods from two mountain ponds in Alberta. Can. J. Zool. 45: 1043-1047. 137 1952. Improvements in the interpretation of recapture data. J. Animal Ecol. 21: 120-127. to the biology of BERG, K. 1937. Contributions Corethra Meigen ( Chaoborus Lichtenstein) . Biol. Medd. Danske Videnskab. Selskab 13 (11): l-101. BROOKS,J. L. 1957. The systematics of North Mem. Conn. Acad. Sci. American Daphnia. 13. 180 p, 1968. The effects of prey size selcc-. Syst. Zool. 17: tion by lake planktivores. 272-291. Predation, AND S. I. DODSON. 1985. Scibody size, and composition of plankton, ence 150 : 28-35. EDMONDSON, W. T. [ED.]. 1959. Fresh-water biology, 2nd ed. Wiley. 1248 p. GALDRAITH, M. G., JR. 1967. Size-selective predation on Daphnia by rainbow trout and yellow perch. Trans. Am. Fisheries Sot. 96: l-10. HRBBEEK, J. 1962 Species composition and the amount of the zooplankton in relation to the fish stock. Rozpravy Cesk. Akad. Ved 10 ( 72 ) : l-116. ILLIES, J. 1967. Limnofauna Europaca. Fischer. 474 p. ecology of the IVLEV, v. s. 1961. Experimental Yale Univ. Press, New feeding of fishes. IIaven, Conn. 302 p. MORDUKHAI-BOLTOVSKAYA,E. D. 1958. Preliminary notes on the feeding of the carnivorous cladocerans Leptodora and Bythotrephes. Dokl.-Biol. Sci. Sect. (English Transl. ) 122 : BAILEY, N. T. J. 828-830. PAINE, R. T. 1966. Food web complexity and species diversity. Am. Naturalist 100: 65-75. TONOLLI, V. 1962. L’attuale situazione de1 popolamento planctonico de1 Lago Maggiorc. Mem. 1st. Ital. Idrobiol. 15: 81-134.