Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans WILLIAM M. BETHEL'AND JOHNC. HOLMES
Can. J. Zool. Downloaded from www.nrcresearchpress.com by EAST CAROLINA UNIVERSITY on 10/26/14 For personal use only.
Department ofzoology, University ofAlberta, Edmonton, Alta., Canada T6G2EI Received June 11,1976
BETHEL,W. M., and J. C. HOLMES.1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Can. J. Zool. 55: 110-115. The amphipods Gammarus lacustris and Hyalella azteca, when infected with the acanthocephalan larvae Polymorphus paradoxus, P . marilis, or Corynosoma constrictum, show altered evasive behavior and (or) responses to light. We propose that the behavioral alterations are manifestations of an evolutionary strategy adopted by the parasites for enhancing transmission to their respective definitive hosts, and that the differences in behavior, and consequent microdistributions of infected amphipods, are tactical and specific to the different feeding habits of the definitive hosts. This hypothesis was tested, in part, by exposing equal numbers of infected and uninfected amphipods to two of the definitive hosts of P . paradoxus: mallard ducks and muskrats. Gammarids infected with cystacanths of P. paradoxus were significantly more vulnerable to predation by mallards and to accidental ingestion by muskrats. Hyalellids harboring cystacanths of C . constrictum, which use several species of waterfowl, including mallards, for definitive hosts, were more vulnerable than uninfected hyalellids, but less vulnerable than gammarids infected with P . paradoxus. No gammarids infected with cystacanths of P. marilis were eaten by mallards or muskrats; P . marilis is not infective to either of these hosts. BETHEL,W. M., et J. C. HOLMES.1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Can. J. Zool. 55: 110-115. Les amphipodes Gammarus lacustris et Hyalella azteca ont des comportements Cvasifs modifies ou des reactions a la lumitre, ou les deux a la fois, lorsqu'ils sont parasitts par les lames d'acanthocephales Polymorphus paradoxus, P . marilis ou ~ o ~ n o s o m a c o n s t r i c t u m On. croit que les modifications du comDortement sont des manifestations de la strategic evolutive adoptke par les parasites dans le but he favoriser leur passage vers leurs hBtes terminaux respectif;; de mkme, les differences de comportement, et par consequent les microdistributions des amphipodes infectts, sont strategiques et specifiques aux diverses habitudes predatrices des hBtes terminaux. Cette hypothese a ete partiellement verifiee par une experience mettant en presence des nombres egaux d'amphipodes infect& et d'amphipodes temoins et deux des hates terminaux d e P . paradoxus, soient des canards malards et des rats musques. Les gammares infectes par des cystacanthes de P . paradoxus sont significativement plus vulnerables a la prkdation par les malards et B I'ingestion accidentelle par des rats musquts. Les hyalellides infectes par des cystacanthes de C. constrictum, esptce qui parasite plusieurs esptces d'oiseaux aquatiques dont le malard, sont plus vulnerables B la predation mais moins vulntrables que les gammares infectts par P. paradoxus. Les gammares infectes par des cystacanthes d e P . marilis ne subissent aucune predation de la part des malards ou des rats musques; P . marilis ne parasite aucun de ces h6tes. [Traduit par le journal]
Introduction Parasitic helminths may be considered to occupy short-lived habitat 'islands' (=hosts). Unlike other island dwellers, their populations cannot be established by a small 'colonizing unit;' each individual must itself invade the host. In such a system, rates of invasion (= transmission) are important and evolution should select for adaptations that increase the probability of transmission. One general adaptation, possessed 'Present address: Department of Biology, Saint Louis University, Saint Louis, MO, U.S.A. 63103.
by many parasitic helminths, including those in this study, is the use of a resting stage in an intermediate host, transferred passively to the final host through a predator-prey system. In a previous paper (Holmes and Bethel 1972) we reviewed some characteristics of predatorprey relationships important to parasite transmission, deduced some evolutionary strategies that may increase the probability of that transmission, and reviewed evidence indicating that some parasites have evolved mechanisms appropriate to those strategies. One strategy, appropriate to situations in which the feeding niche of
11 1
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BETHEL A.ND HOLMES
the definitive host (predator) incompletely overlaps the habitat of the intermediate host (prey), i3 to alter some response of the infected intermediate host so as to move it into the area of overlap. We have shown also that the amphipods Gammarus lacustris and Hyalella azteca, infected with cystacanths of Polymorphus paradoxus, P. marilis, and Corynosoma constrictum (Acanthocephala: Polymorphidae), display altered photic and (or) evasive behavior (Bethel and Holmes 1973). In our study lakes and in the laboratory, uninfected amphipods were strongly photophobic and negatively phototactic, selecting benthic or heavily vegetated areas where light intensities are low; their evasive responses were directed away from light. Conversely, G. Iacustris harboring cystacanths of P. paradoxus selected areas of most intense light (photophilic) and 80% were positively phototactic when undisturbed. Their evasive behavior is markedly altered; after disturbance, almost all were positively phototactic, and skimmed along the water surface and (or) clung to surface material with their gnathopods. H. azteca harboring cystacanths of C. constrictum were also strongly photophilic; about 60% were positively phototactic when undisturbed, but after disturbance about 60% were negatively phototactic. Gammarids harboring cystacanths of P. marilis selected lighted areas (without showing a differential response to different intensities of light), but were negatively phototactic; their evasive responses were normal. These behavioral alterations have the overall effect of placing the infected amphipods in microdistributionsdifferent from those of each other and from those of uninfected amphipods. Mallards (Anas platyrhynchos), the avian definitive hosts for P. paradoxus, are dabblers that feed chiefly at the surface, at the edges of shores and banks, or by 'tipping' and searching randomly in shallow areas where they can reach the bottom (Kortright 1943;Perret 1962). The mammalian hosts for P. paradoxus, muskrats (Ondatra zibethica) and beavers (Castor canaden~is) (Connell and Corner 1957), are herbivores (Brandt 1938; Errington 1963) and, although muskrats have been known to feed on large arthropods and molluscs (Errington 1963), the probability of either animal intentionally feeding on an arthropod the size of G. lacustris is very low. Lesser scaup (Aythya afinis), the major
local definitive hosts for P. marilis (Graham 1966; Denny 1969), are divers and obtain most of their food by diving in open water or near submerged plants (Sugden 1973). Locally, C. constrictum uses both mallards and scaup, as well as other diving and dabbling ducks, as definitive hosts (Graham 1966; Podesta and Holmes 1970). The differences in the microdistributions of the amphipods and in the feeding behavior of the definitive hosts of the parasites suggest that the different behavioral alterations and corresponding differences in microdistributions are manifestations of a common evolutionary strategy (i.e., to move infected intermediate hosts into the zone of overlap with the feeding niche of the definitive host), and that the differences are specific strategic adaptations to the different predatory behavior patterns of the definitive hosts. Preliminary tests have shown an increased vulnerability of P. paradoxus-infected gammarids to predation by mallards (Holmes and Bethel 1972). The present study was designed to test whether the induced behavioral alterations render infected amphipods vulnerable to the proper definitive hosts.
Materials and Methods Infected and uninfected amphipods were collected and kept in the laboratory as described in Bethel and Holmes (1973). The ducks used in the study were raised in the laboratory from eggs collected from nests on the islands of Hastings Lake, Alberta. The ducks were kept in large pens provided with small water troughs. They were fed ad libitum on a mash diet, and were never starved before a test. New, naive ducks were used in each test. Predation tests were performed in a tank 1.2 x 0.7 x 0.6 m deep. The tank was lined with a fine-mesh net to enable recovery of the surviving amphipods at the end of each test. A mud bottom and about the same amount of floatage (one 15 x 4 cm wooden stick or two equal to the same area, two 10-cm pieces of reeds, and two 15-cm strands of Potamageton sp., Ceratophyllum sp., or Myriophyllum sp.) were provided for each test. The tank was filled to within a few centimetres of the top with dechlorinated water and lake water. The temperature, turbidity, and pH of the water were kept as consistent with the conditions in the study lakes as possible. The amphipods were allowed at least 10-15 min to settle in the tank before the predators were allowed to enter the water. Muskrats, live-trapped from Hastings and Wabamun Lakes, Alberta, were kept in large cages, with access to water, and were fed ad libitum on a combination of oatmeal, lettuce, carrots, and apples. The tank described above was modified for tests with
.
112
CAN. J. ZOOL. VOL. 55. 1977
TABLE1. Comparative vulnerability of uninfected Gammarus lacustris and ones infected with the cystacanths of two acanthocephalans to predation by mallards and muskrats Gammarids eaten / No. available
Can. J. Zool. Downloaded from www.nrcresearchpress.com by EAST CAROLINA UNIVERSITY on 10/26/14 For personal use only.
Test No. 1 2 3 4 5 6 Total 1 2 Total
2 3 Total 1 2 Total
No. Duration, predators min (ducks)
Uninfected
Infected with Polymorphus oaradoxus
Infected with Polymorphus marilis
P*
7 5 5 5 10 15 10 10
24 24
(Muskrats) 1 1 1
24 24
*P = probability, by chi-square contingency tests. tcomparison of numbers o f P. paradoxus-infected gammarids eaten with those of uninfected and P. morilisinfected gammarrds eaten.
muskrats. A wooden box, 28.7 x 48 x 33 crn deep, with a two-level interior, accessible by entrances at the bottom, front, back, and one side, was mounted at one end of the tank, about 3 cm above water level. The box and open area of the tank were enclosed by chicken wire. The muskrats were placed in the tank for at least 24 h before the tests began and observed frequently during this period. An ample supply of their normal laboratory food was available in a pan at the side of the box before and during the tests. The usual floatage was also provided, and the vegetation replenished at the beginning of the test period if necessary. At the end of tests, the interior of the box, as well as the net, was checked for gammarids.
Results The mallards and muskrats readily adjusted to experimental conditions. Some of the mallards were more at ease and performed better when used in pairs. They appeared to feed normally, and were remarkably easy to observe from relatively short distances. Preliminary experiments indicated that infected or uninfected gammarids readily survived 24 h in the testing tank. Vulnerability to Mallards The results of predation tests indicated that mallards ate a significantly greater number of gammarids infected with P. paradoxus than uninfected controls (Table 1).
When the mallards entered the water, they were first attracted to the floating material. Even at the beginning of the test, there were always some infected gammarids clinging to or otherwise associated with .the floating material. When the material was disturbed, most of the infected gammarids remained clinging onto it, although a few skimmed away along the water surface. (These clinging and skimming responses of P. paradoxus-infected gammarids are typical manifestations of their altered evasive behavior as described in Bethel and Holmes (1973).) Mallards fed first on the clinging gammarids, then on any skimming in the immediate vicinity. The skimming, which creates an obvious surface disturbance, appeared to be very attractive to the mallards, and they rarely missed skimming gammarids. They also struck at any small objects on the water surface. The mallards repeatedly returned to the floatage, turned it over, and fed on any gammarids present. Later, after several apparently unsuccessful attempts to feed around the floatage, they began dabbling or tipping. The mallards often were allowed to reenter the tanks after the completion of the test and removal of the surviving gammarids. During these periods, and at the ends of some of the tests, they repeatedly inspected the floatage and
BETHEL AND HOLMES
TABLE 2. Vulnerability of marked and unmarked Gammarus lacustris to predation by mallard ducks Gammarids eaten / No. available Test No.
Duration, min
No. ducks
1 2
10 10 10 10
1 2 1 1
3 4
Can. J. Zool. Downloaded from www.nrcresearchpress.com by EAST CAROLINA UNIVERSITY on 10/26/14 For personal use only.
Total
Marked
Unmarked
P*
3/50 5/50 0150 0150 81200
2/50 1/50 0150 0150 31200
>0.99 >0.1 +
-
>0.1
*P = probability, by chi-square contingerICY tests.
consumed many of the water plants and reeds on the dorsal-lateral aspect of the carapaces of that had been used. a group of uninfected gammarids. The paint was In a second experiment, three groups of gam- fast drying and did not appear to affect the marids (50 uninfected, 50 infected with P. para- health, behavior, or swimming ability of the doxus, and 50 infected with P. marilis) were gammarids, as determined by preliminary obplaced in the tank with a mallard. The behavior servations. In each of four 10-min tests, 50 unof the mallard was identical to that in the pre- infected, marked gammarids and 50 without the vious experiment; about 40% of the P. para- marks were placed in the tank, along with one doxus-infected gammarids, but not a single P. mallard. The mallard's behavior was identical to marilis-infected or uninfected gammarid, were that of the mallards in the tests with C. coneaten (Table 1). strictum-infected. hyalellids. They did not appear In a third experiment, 50 C. constrictum-in- to feed actively on the gammarids; very few were fected and 50 uninfected hyalellids were placed eaten (Table 2), and the proportions of marked in the tank, along with one mallard. Two such and unmarked gammarids that were eaten were tests were run, one lasting 15 min, the other not significantly different. 30 min. The behavior of the mallards in these tests was considerably different from that of the Vulnerabilitv to Muskrats The following series of experiments was demallards in the first two experiments. They signed to determine the susceptibility of infected promptly inspected the floating objects, but did and uninfected gammarids to ingestion by musknot return to them. They seldom dabbled or rats, and to determine if the gammarids were tipped and generally did not appear to be stimulated to search for food. The mallards engaged ingested by active predation and (or) accidental in other, casual activities, such as bathing, for a ingestion. In each of three tests. 75 uninfected and 75 P. much greater proportion of these tests. The only paradoxus-infected gammarids were exposed to hyalellids eaten by mallards were ones infected with C . constrictum, and, although significant, one muskrat for 24 h. Although no uninfected the numbers of those that were consumed were gammarids were eaten, significant numbers of relatively low, 6 in the first and 10 in the second infected gammarids were eaten in each of the three tests (Table 1). test (P =
Can. J. Zool. Downloaded from www.nrcresearchpress.com by EAST CAROLINA UNIVERSITY on 10/26/14 For personal use only.
Department ofzoology, University ofAlberta, Edmonton, Alta., Canada T6G2EI Received June 11,1976
BETHEL,W. M., and J. C. HOLMES.1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Can. J. Zool. 55: 110-115. The amphipods Gammarus lacustris and Hyalella azteca, when infected with the acanthocephalan larvae Polymorphus paradoxus, P . marilis, or Corynosoma constrictum, show altered evasive behavior and (or) responses to light. We propose that the behavioral alterations are manifestations of an evolutionary strategy adopted by the parasites for enhancing transmission to their respective definitive hosts, and that the differences in behavior, and consequent microdistributions of infected amphipods, are tactical and specific to the different feeding habits of the definitive hosts. This hypothesis was tested, in part, by exposing equal numbers of infected and uninfected amphipods to two of the definitive hosts of P . paradoxus: mallard ducks and muskrats. Gammarids infected with cystacanths of P. paradoxus were significantly more vulnerable to predation by mallards and to accidental ingestion by muskrats. Hyalellids harboring cystacanths of C . constrictum, which use several species of waterfowl, including mallards, for definitive hosts, were more vulnerable than uninfected hyalellids, but less vulnerable than gammarids infected with P . paradoxus. No gammarids infected with cystacanths of P. marilis were eaten by mallards or muskrats; P . marilis is not infective to either of these hosts. BETHEL,W. M., et J. C. HOLMES.1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Can. J. Zool. 55: 110-115. Les amphipodes Gammarus lacustris et Hyalella azteca ont des comportements Cvasifs modifies ou des reactions a la lumitre, ou les deux a la fois, lorsqu'ils sont parasitts par les lames d'acanthocephales Polymorphus paradoxus, P . marilis ou ~ o ~ n o s o m a c o n s t r i c t u m On. croit que les modifications du comDortement sont des manifestations de la strategic evolutive adoptke par les parasites dans le but he favoriser leur passage vers leurs hBtes terminaux respectif;; de mkme, les differences de comportement, et par consequent les microdistributions des amphipodes infectts, sont strategiques et specifiques aux diverses habitudes predatrices des hBtes terminaux. Cette hypothese a ete partiellement verifiee par une experience mettant en presence des nombres egaux d'amphipodes infect& et d'amphipodes temoins et deux des hates terminaux d e P . paradoxus, soient des canards malards et des rats musques. Les gammares infectes par des cystacanthes de P . paradoxus sont significativement plus vulnerables a la prkdation par les malards et B I'ingestion accidentelle par des rats musquts. Les hyalellides infectes par des cystacanthes de C. constrictum, esptce qui parasite plusieurs esptces d'oiseaux aquatiques dont le malard, sont plus vulnerables B la predation mais moins vulntrables que les gammares infectts par P. paradoxus. Les gammares infectes par des cystacanthes d e P . marilis ne subissent aucune predation de la part des malards ou des rats musques; P . marilis ne parasite aucun de ces h6tes. [Traduit par le journal]
Introduction Parasitic helminths may be considered to occupy short-lived habitat 'islands' (=hosts). Unlike other island dwellers, their populations cannot be established by a small 'colonizing unit;' each individual must itself invade the host. In such a system, rates of invasion (= transmission) are important and evolution should select for adaptations that increase the probability of transmission. One general adaptation, possessed 'Present address: Department of Biology, Saint Louis University, Saint Louis, MO, U.S.A. 63103.
by many parasitic helminths, including those in this study, is the use of a resting stage in an intermediate host, transferred passively to the final host through a predator-prey system. In a previous paper (Holmes and Bethel 1972) we reviewed some characteristics of predatorprey relationships important to parasite transmission, deduced some evolutionary strategies that may increase the probability of that transmission, and reviewed evidence indicating that some parasites have evolved mechanisms appropriate to those strategies. One strategy, appropriate to situations in which the feeding niche of
11 1
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BETHEL A.ND HOLMES
the definitive host (predator) incompletely overlaps the habitat of the intermediate host (prey), i3 to alter some response of the infected intermediate host so as to move it into the area of overlap. We have shown also that the amphipods Gammarus lacustris and Hyalella azteca, infected with cystacanths of Polymorphus paradoxus, P. marilis, and Corynosoma constrictum (Acanthocephala: Polymorphidae), display altered photic and (or) evasive behavior (Bethel and Holmes 1973). In our study lakes and in the laboratory, uninfected amphipods were strongly photophobic and negatively phototactic, selecting benthic or heavily vegetated areas where light intensities are low; their evasive responses were directed away from light. Conversely, G. Iacustris harboring cystacanths of P. paradoxus selected areas of most intense light (photophilic) and 80% were positively phototactic when undisturbed. Their evasive behavior is markedly altered; after disturbance, almost all were positively phototactic, and skimmed along the water surface and (or) clung to surface material with their gnathopods. H. azteca harboring cystacanths of C. constrictum were also strongly photophilic; about 60% were positively phototactic when undisturbed, but after disturbance about 60% were negatively phototactic. Gammarids harboring cystacanths of P. marilis selected lighted areas (without showing a differential response to different intensities of light), but were negatively phototactic; their evasive responses were normal. These behavioral alterations have the overall effect of placing the infected amphipods in microdistributionsdifferent from those of each other and from those of uninfected amphipods. Mallards (Anas platyrhynchos), the avian definitive hosts for P. paradoxus, are dabblers that feed chiefly at the surface, at the edges of shores and banks, or by 'tipping' and searching randomly in shallow areas where they can reach the bottom (Kortright 1943;Perret 1962). The mammalian hosts for P. paradoxus, muskrats (Ondatra zibethica) and beavers (Castor canaden~is) (Connell and Corner 1957), are herbivores (Brandt 1938; Errington 1963) and, although muskrats have been known to feed on large arthropods and molluscs (Errington 1963), the probability of either animal intentionally feeding on an arthropod the size of G. lacustris is very low. Lesser scaup (Aythya afinis), the major
local definitive hosts for P. marilis (Graham 1966; Denny 1969), are divers and obtain most of their food by diving in open water or near submerged plants (Sugden 1973). Locally, C. constrictum uses both mallards and scaup, as well as other diving and dabbling ducks, as definitive hosts (Graham 1966; Podesta and Holmes 1970). The differences in the microdistributions of the amphipods and in the feeding behavior of the definitive hosts of the parasites suggest that the different behavioral alterations and corresponding differences in microdistributions are manifestations of a common evolutionary strategy (i.e., to move infected intermediate hosts into the zone of overlap with the feeding niche of the definitive host), and that the differences are specific strategic adaptations to the different predatory behavior patterns of the definitive hosts. Preliminary tests have shown an increased vulnerability of P. paradoxus-infected gammarids to predation by mallards (Holmes and Bethel 1972). The present study was designed to test whether the induced behavioral alterations render infected amphipods vulnerable to the proper definitive hosts.
Materials and Methods Infected and uninfected amphipods were collected and kept in the laboratory as described in Bethel and Holmes (1973). The ducks used in the study were raised in the laboratory from eggs collected from nests on the islands of Hastings Lake, Alberta. The ducks were kept in large pens provided with small water troughs. They were fed ad libitum on a mash diet, and were never starved before a test. New, naive ducks were used in each test. Predation tests were performed in a tank 1.2 x 0.7 x 0.6 m deep. The tank was lined with a fine-mesh net to enable recovery of the surviving amphipods at the end of each test. A mud bottom and about the same amount of floatage (one 15 x 4 cm wooden stick or two equal to the same area, two 10-cm pieces of reeds, and two 15-cm strands of Potamageton sp., Ceratophyllum sp., or Myriophyllum sp.) were provided for each test. The tank was filled to within a few centimetres of the top with dechlorinated water and lake water. The temperature, turbidity, and pH of the water were kept as consistent with the conditions in the study lakes as possible. The amphipods were allowed at least 10-15 min to settle in the tank before the predators were allowed to enter the water. Muskrats, live-trapped from Hastings and Wabamun Lakes, Alberta, were kept in large cages, with access to water, and were fed ad libitum on a combination of oatmeal, lettuce, carrots, and apples. The tank described above was modified for tests with
.
112
CAN. J. ZOOL. VOL. 55. 1977
TABLE1. Comparative vulnerability of uninfected Gammarus lacustris and ones infected with the cystacanths of two acanthocephalans to predation by mallards and muskrats Gammarids eaten / No. available
Can. J. Zool. Downloaded from www.nrcresearchpress.com by EAST CAROLINA UNIVERSITY on 10/26/14 For personal use only.
Test No. 1 2 3 4 5 6 Total 1 2 Total
2 3 Total 1 2 Total
No. Duration, predators min (ducks)
Uninfected
Infected with Polymorphus oaradoxus
Infected with Polymorphus marilis
P*
7 5 5 5 10 15 10 10
24 24
(Muskrats) 1 1 1
24 24
*P = probability, by chi-square contingency tests. tcomparison of numbers o f P. paradoxus-infected gammarids eaten with those of uninfected and P. morilisinfected gammarrds eaten.
muskrats. A wooden box, 28.7 x 48 x 33 crn deep, with a two-level interior, accessible by entrances at the bottom, front, back, and one side, was mounted at one end of the tank, about 3 cm above water level. The box and open area of the tank were enclosed by chicken wire. The muskrats were placed in the tank for at least 24 h before the tests began and observed frequently during this period. An ample supply of their normal laboratory food was available in a pan at the side of the box before and during the tests. The usual floatage was also provided, and the vegetation replenished at the beginning of the test period if necessary. At the end of tests, the interior of the box, as well as the net, was checked for gammarids.
Results The mallards and muskrats readily adjusted to experimental conditions. Some of the mallards were more at ease and performed better when used in pairs. They appeared to feed normally, and were remarkably easy to observe from relatively short distances. Preliminary experiments indicated that infected or uninfected gammarids readily survived 24 h in the testing tank. Vulnerability to Mallards The results of predation tests indicated that mallards ate a significantly greater number of gammarids infected with P. paradoxus than uninfected controls (Table 1).
When the mallards entered the water, they were first attracted to the floating material. Even at the beginning of the test, there were always some infected gammarids clinging to or otherwise associated with .the floating material. When the material was disturbed, most of the infected gammarids remained clinging onto it, although a few skimmed away along the water surface. (These clinging and skimming responses of P. paradoxus-infected gammarids are typical manifestations of their altered evasive behavior as described in Bethel and Holmes (1973).) Mallards fed first on the clinging gammarids, then on any skimming in the immediate vicinity. The skimming, which creates an obvious surface disturbance, appeared to be very attractive to the mallards, and they rarely missed skimming gammarids. They also struck at any small objects on the water surface. The mallards repeatedly returned to the floatage, turned it over, and fed on any gammarids present. Later, after several apparently unsuccessful attempts to feed around the floatage, they began dabbling or tipping. The mallards often were allowed to reenter the tanks after the completion of the test and removal of the surviving gammarids. During these periods, and at the ends of some of the tests, they repeatedly inspected the floatage and
BETHEL AND HOLMES
TABLE 2. Vulnerability of marked and unmarked Gammarus lacustris to predation by mallard ducks Gammarids eaten / No. available Test No.
Duration, min
No. ducks
1 2
10 10 10 10
1 2 1 1
3 4
Can. J. Zool. Downloaded from www.nrcresearchpress.com by EAST CAROLINA UNIVERSITY on 10/26/14 For personal use only.
Total
Marked
Unmarked
P*
3/50 5/50 0150 0150 81200
2/50 1/50 0150 0150 31200
>0.99 >0.1 +
-
>0.1
*P = probability, by chi-square contingerICY tests.
consumed many of the water plants and reeds on the dorsal-lateral aspect of the carapaces of that had been used. a group of uninfected gammarids. The paint was In a second experiment, three groups of gam- fast drying and did not appear to affect the marids (50 uninfected, 50 infected with P. para- health, behavior, or swimming ability of the doxus, and 50 infected with P. marilis) were gammarids, as determined by preliminary obplaced in the tank with a mallard. The behavior servations. In each of four 10-min tests, 50 unof the mallard was identical to that in the pre- infected, marked gammarids and 50 without the vious experiment; about 40% of the P. para- marks were placed in the tank, along with one doxus-infected gammarids, but not a single P. mallard. The mallard's behavior was identical to marilis-infected or uninfected gammarid, were that of the mallards in the tests with C. coneaten (Table 1). strictum-infected. hyalellids. They did not appear In a third experiment, 50 C. constrictum-in- to feed actively on the gammarids; very few were fected and 50 uninfected hyalellids were placed eaten (Table 2), and the proportions of marked in the tank, along with one mallard. Two such and unmarked gammarids that were eaten were tests were run, one lasting 15 min, the other not significantly different. 30 min. The behavior of the mallards in these tests was considerably different from that of the Vulnerabilitv to Muskrats The following series of experiments was demallards in the first two experiments. They signed to determine the susceptibility of infected promptly inspected the floating objects, but did and uninfected gammarids to ingestion by musknot return to them. They seldom dabbled or rats, and to determine if the gammarids were tipped and generally did not appear to be stimulated to search for food. The mallards engaged ingested by active predation and (or) accidental in other, casual activities, such as bathing, for a ingestion. In each of three tests. 75 uninfected and 75 P. much greater proportion of these tests. The only paradoxus-infected gammarids were exposed to hyalellids eaten by mallards were ones infected with C . constrictum, and, although significant, one muskrat for 24 h. Although no uninfected the numbers of those that were consumed were gammarids were eaten, significant numbers of relatively low, 6 in the first and 10 in the second infected gammarids were eaten in each of the three tests (Table 1). test (P =
