Influence of social status on the helminth community of late-winter mallards

CAROL A. GRAY Department of Pathology, Texas Tech University Health Sciences Center, Lubbock, TX 79430, U.S.A.

PAUL N. GRAY' Department of Range and Wildlife Management, Texas Tech University, Lubbock, TX 79409, U. S.A.

AND

DANNY B. PENCE^ Department of Pathology, Texas Tech University Health Sciences Center, Lubbock, TX 79430, U. S.A.

Received June 27, 1986

GRAY, C. A., GRAY, P. N., and PENCE, D. B. 1989. Influence of social status on the helminth community of late-winter mal- lards. Can. J. Zool. 67: 1937-1944.

The influence of body condition, molting status, sex, and pairing status on the helminth community at the component com- munity level (all parasites in all individuals of a given host species in a defined geographic region) of an infrapopulation of mallards (Anas platyrhynchos) wintering on the Southern High Plains of Texas was examined. From a data matrix of 45 mal- lards (15 pairs and 15 unpaired males), pairing status was the most important variable that accounted for significant differ- ences in helminth abundances. In six of 15 common helminth species (Sobolevicanthus gracilis, Microsomacanthus hopkinsi, Amidostomum acutum, Capillaria anatis, Capillaria contorta, and Epomidiostomum uncinatum), abundances were signifi- cantly higher in unpaired males than in paired birds. Abundance of only one of 15 helminth species (E. uncinatum) differed significantly between paired males and females. The significantly higher helminth abundances of unpaired males may be due to their potentially more gregarious and mobile behavior, which increases their exposure to certain helminth species. This study emphasizes the importance of incorporating social status in experimental designs involving waterfowl.

GRAY, C. A., GRAY, P. N., et PENCE, D. B. 1989. Influence of social status on the helminth community of late-winter mal- lards. Can. J. Zool. 67 : 1937-1944.

On trouvera ici les rCsultats d'une Ctude sur l'influence de la condition physique, du stade de la mue, du sexe et du statut social sur la communautC d'helminthes (dCfinie c o m e l'ensemble de tous les parasites de tous les individus d'une espkce dans une rCgion gCographique donnCe) d'une sous-population de Canards colverts (Anas platyrhynchos) dans son territoire d'hiver dans les hautes plaines meridionales du Texas. D'aprks la matrice des donnCes obtenues chez 45 canards (15 couples et 15 mlles seuls), le statut social est la variable la plus dkterminante des diffkrences significatives entre les fardeaux d'hel- minthes. L'abondance des helminthes Ctait significativement plus ClevCe chez les mlles seuls que chez les oiseaux en couples dans le cas de six des 15 espkces rencontrkes (Sobolevicanthus gracilis, Microsomacanthus hopkinsi, Amidostomum acutum, Capillaria anatis, Capillaria contorta et Epomidiostomum uncinatum). L'abondance d'une seule des 15 espkces (E. uncina- tum) diffkrait significativement chez les mlles et chez les femelles en couple. L'abondance significativement plus ClevCe des helminthes chez les mlles seuls est probablement attribuable h leurs habitudes plus grCgaires et h leur mobilitC plus grande, ce qui les expose davantage h certaines espkces d'helminthes. Cette Ctude souligne l'importance de tenir compte du statut social lors de la mise au point de protocoles expkrimentaux destines h 1'Ctude d'oiseaux aquatiques.

[Traduit par la revue]

Introduction Waterfowl breeding success may be affected by preceding

events in the wintering areas because wintering waterfowl which attain a high level of fitness are probably better pre- pared for the subsequent breeding season (Heitmeyer and Fredrickson 198 1). Theoretically, the healthiest birds are the first to initiate prebreeding activities. In wintering areas, a female's mate can protect her from harassing males. Both members of the pair accumulate fat and protein reserves and the female initiates her prebasic molt. Ultimately, the pair will be among the first northward migrants to select a breeding spot in the most preferred habitat and nest more successfully than later arriving birds. Also, early breeders have a renesting advantage if their first attempt fails.

The occurrence of the above events in the annual cycle of

meyer and Vohs 1984; Jorde et al. 1984; Heitmeyer 1985), food habit shifts during the winter and prebreeding seasons (Drobney et al. 1983; Heitmeyer 1985), and seasonal changes in daily activity patterns (Lee 1985; Miller 1985).

Considering the physiological and behavioral changes that occur over the winter, this study was initiated to determine the influence of certain physical (body condition and molting status) and social (pairing status and sex) factors on the hel- minth community at the component community level (all para- sites in all individuals of a given host species from a defined geographic locality) of an infrapopulation of late-winter mal- lards (Anus platyrhynchos) from the Southern High Plains of Texas. Additionally, this study represents the first characteri- zation of the helminth community of any waterfowl species wintering in this region.

waterfowl is indicated in social dominance of paired birds over unpaired birds (Wishart 1979; Paulus 1983; Jorde et al. 1984; Materials and methods

Heitmeyer 1985), habitat shifts by birds after pairing (Heit- Study area Mallards were collected near Hart, Castro County, Texas

'Present address: Cooperative Fish and Wildlife Research Unit, (34 "20 I- 34 "60 IN, 10 1 "05 ' - 102 " 30 'W) on the Southern High University of Florida, Gainesville, FL 3261 1, U.S.A. Plains. This semiarid region (annual precipitation < 50 cm) is inten-

'Author to whom correspondence and reprint requests should be sively cultivated, with irrigated row crops of corn, grain sorghum, addressed. cotton, and vegetables. The only prominent hydrographical features Printed in Canada 1 Imprime au Canada

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1938 CAN. J. ZOOL. VOL. 67, 1989

of the region are the 17 000 - 18 000 playa lakes distributed through- out the Texas Panhandle and adjacent areas of New Mexico (Bolen and Guthery 1982). Playas are round to oval drainage basins with nearly impermeable Randall clay bottoms that permit the accumula- tion of surface water produced by sporadic thunderstorms and (or) groundwater used for irrigation. Playa lakes are ephemeral unless their basins have been "modified" to provide more permanent water- holding capacities (Dvoracek 198 1 ; Bolen and Guthery 1982; Gray 1986). Together, grain fields and playa lakes are attractive to water- fowl, and the region is rated as the second most important waterfowl wintering area in the Central Flyway (Buller 1954). About 1 x lo6 waterfowl (300 000 mallards) overwinter annually in the playa lakes region of the Southern High Plains (Bellrose 1976; Curtis and Beier- man 1980).

Mallard data base Forty-five mallards were collected by shooting in a 43-day period

(January 28 to March 11, 1984). The sample included 30 paired mal- lards (15 pairs) and 15 unpaired males. Pairing status was assessed during 10- to 30-min observation periods, using the criteria of Paulus (1983). The paired category was limited to mallards that (i) mutually avoided or threatened other ducks; (ii) demonstrated consistent syn- chronization of activities, especially locomotion; and (iii) remained within 2 m of each other during the observation period (Paulus 1983). Because mallard sex ratios are biased toward males (Bellrose 1976), unpaired females were rare in the population and were not collected.

Molting status was quantified by counting feathers along line tran- sects from 2 1 body regions. Fifty feathers were counted along a tran- sect and the percentage of new feathers (identified by blood in the quills) was recorded. In areas such as the tail and tertials where < 50 feathers were present, a percentage of feathers was calculated. Feather areas surveyed were crown, cheek, chin -throat, neck, upper back (center), scapulars, lower back, rump, upper tail coverts, tail, lower tail coverts, belly, chest center, chest side, side, flank, primaries, secondaries, tertials, wing coverts, and leg (Heitmeyer 1985).

Primary and secondary feathers were not molting and were not quantified. The percentage of molting feathers from all other feather areas was averaged to obtain a single value for molting status. Percent molt values from crown, cheek, and chin-throat areas were aver- aged together before they were included in the overall molting status percentage, because they represented a small biomass compared with other feather areas.

Wing length was used as a determinant of structural size. The right wing was measured from the proximal end of the carpometacarpus to the tip of the flattened ninth primary feather (Ringleman and Szymc- zak 1985). Mallards were aged using the criteria of Krapu et al. ( 1979).

Eviscerated mallard carcasses were sheared to remove feathers and ground four times through a 9-mm sieve plate in a commercial meat grinder. Ground ducks were air-dried for 2 weeks at 70°C (until they lost < 1 g waterlday) and then reground twice through a 4.5-mm sieve plate. Fat was extracted from the ground duck homogenate with cellulose extraction thimbles in a Soxhlet ether (petroleum) extraction apparatus for 36 h (Dobush et al. 1985). Two (5.6 g) samples were extracted for each bird and averaged for percent fat. Total fat (g) was calculated for each bird as percent fat x dry carcass weight (Ringle- man and Szymczak 1985).

Helminth data base Ducks were eviscerated within 10 min of collection. Viscera were

quick-frozen in a mixture of methanol and dry ice (Bush 1980; Bush and Holmes 1983). The body cavity was examined for helminths dur- ing evisceration. Viscera were stored at - 5 OC until necropsy .

Collection of helminths was facilitated by washing the respective visceral organs followed by examination of the sediment collected in conical glasses. Small cestodes were collected by scraping the intesti- nal mucosa, followed by sedimentation. Recovery of all individuals was attempted, but because of the excessive time required to examine the large volume of mucinous intestinal contents, absolute counts of

some small species were not possible. Therefore, small intestinal hel- minths were subsampled and the values were extrapolated to estimate for total abundance values. Contents of the small intestine and mucosal scrapings were brought to a volume of 500 mL and thoroughly mixed, and a 100-mL aliquot was removed for examina- tion under a dissecting microscope. We initially tested the accuracy of this procedure by comparing the actual counts versus extrapolated counts from three representative mallards. There were no significant differences in these counts. Also, the entire intestinal contents from the 500-mL sample of each bird were scanned visually, the larger hel- minth species were counted, and the actual versus extrapolated data were compared to further verify the accuracy of the aliquoting pro- cedure. Thus, considering the above and because all subsampling was conducted by the same individual, we assumed that any errors were distributed across all samples and, therefore, the differences were real and not due to a sampling artifact.

Nematodes were fixed briefly in glacial acetic acid, stored in a mix- ture of 70% ethyl alcohol with 5 % glycerine, and examined in glycer- ine wet mounts. Cestodes and digeneans were fixed in an acetic acid - formalin - ethyl alcohol mixture, and mounted in Canada balsam. Representative specimens of helminths recovered in this study were deposited in the U.S. National Parasite Collection, Belts- ville, MD 20705, U.S.A. (Nos. 79629 -79653).

Definitions The terms prevalence, abundance, intensity, and mean intensity

follow the definitions of Margolis et al. (1982). Total helminths refers to all individuals of all helminth species occurring in the host population or in host subpopulations as defined in the text. The hel- minth community (at the component community level) is defined as that assemblage of helminth species represented in all infracom- munities occurring in all host individuals sampled from the host infra- population. Use of significant and significantly refer to statistical significance at P I 0.05.

Condition is defined as the amount of lipid in the mallard. Body size is defined as a function of wing length. The amount of body fat and wing length are treated as autocorrelated variables where pos- sible, with wing length as a covariate of condition. Social class refers to the combination of pairing status, age, and sex of the birds. Differ- ences were not detected between age-groups, so the three social classes were defined as paired males, paired females, and unpaired males.

Overdispersion is defined by Bliss and Fisher (1953), and in the present study it refers to a frequency distribution of a helminth spe- cies in which a few hosts harbor many individuals and many hosts have few or no individuals of a particular helminth species.

Experimental design and analysis The influence of physical factors (molting status, condition, and

body size) on social factors (age, sex, and pairing status) of this mal- lard population was examined. The relationships of molting status and age to social status were examined by one-way ANOVA with a pro- tected least significant difference (LSD) test (Carmer and Swanson 1973) (PROC GLM; SAS Institute Inc. 1982). Linear regression (PROC REG; SAS Institute Inc. 1982) was used to test the relation- ship of body condition (g fat) with body size (wing length). There was not a significant relationship with abundance of total helminths and condition (or body size), and in only 2 of the 15 common helminth species were there significant increases in abundances of individuals with increased condition (PROC REG; SAS Institute Inc. 1982). ANCOVA (PROC GLM; SAS Institute Inc. 1982) was used to test for differences in condition of the three social classes using wing length as a covariate of body size. As a result of heteroscedasticity in the data set, a Wilcoxon two-sample test was used to test for differences in condition and molting status between ages within the three social classes. Birds were not stratified based on condition in subsequent analyses because there were no significant differences between social classes. Condition and (or) body size was not further considered in subsequent analyses of the helminth community structure in this host population. Molting rates were significantly different between, but

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GRAY ET AL. 1939

similar within, social classes; therefore, tests between social classes were reflective of molting rate categories. In only 1 of 15 common helminth species was there a significant difference in abundance between juveniles and adults for any of the three social classes; there- fore, further analysis did not stratify mallards by age.

The remaining analyses examined the effects of the social status components of sex and pairing status on the helminth communities of this mallard population. This also allowed us to test the hypothesis that molting paired females which require additional dietary protein may eat more invertebrates and thus acquire greater helminth abun- dances. The following analyses are based on the 15 common ( > 20% prevalence) helminth species.

Overdispersion was indicated when the variance was significantly larger than the mean based on X2 analysis of the frequency distribu- tions for the respective helminth species. Overdispersion was mea- sured by the negative binomial parameter, k, which is an inverse measure of the degree of overdispersion (Bliss and Fisher 1953). A test for homogeneity of k across the three social classes of the host population was modified from Bliss and Fisher (1953), using total X2

analysis where the value of k for each helminth species generated across the collective host population was treated as the expected value (Wallace and Pence 1986). A value of P I 0.05 for the sum of values from X2 analysis generated across the three social classes was con- sidered to represent significant heterogeneity in the distribution pat- tern of the respective helminth species.

Because the preceding analysis indicated an other than normal dis- tribution of individuals for most of the helminth species, subsequent analysis required either use of nonparametric tests or transformation of the data set prior to analysis with parametric statistical methods. The rank transformation procedure of Conover and Iman (1981) provided a useful technique for application in a unified manner of the usual parametric statistical methods by replacing abundance values in the contagiously distributed data set with their ranks (RT-2 of Conover and Iman 1981, PROC RANK; SAS Institute Inc. 1982). Abundance values of each helminth species were ranked indepen- dently because of potential differences in distribution patterns (J. Conover, personal communication).

Diversity in the helminth communities of each mallard from the 45-sample data set of 26 helminth species was calculated using Bril- louin's index for completely censused communities (Pielou 1975). Diversity values were compared across the three social classes.

Stepwise multiple discriminant analysis of the 45-sample data matrix of ranked abundances of the 15 common helminth species across three social classes indicated (i) those helrninth species that were significant discriminators between all possible combinations of category variables and (ii) the number of cases (samples) classified correctly into all possible groups of interactive category variables (BMD P7M; Dixon 1981). One-way ANOVA with a protected LSD (PROC GLM; SAS Institute Inc. 1982) compared the three social classes across the ranked abundances of the 15 common helminth species.

Overlap of helminth species in individual pairs of mallards was examined using Jaccard's coefficients (Jaccard 1912). This is a qualitative index of overlap calculated as J = 100 cl(a + b - c), where a is the number of taxa in the paired male, b is the number in the paired female, and c is the number common to both members of the pair.

Paired rank correlations (Kendall's 7; PROC CORR; SAS Institute Inc. 1982) compared individuals of each pair of mallards based on abundances of the 15 common helrninth species. These determined if individuals of the pair varied in concert (significant positive correla- tion), oppositely (significant negative correlation), or independently.

Results Helminth communities

Twenty -six helminth species (1 0 trematodes, 8 cestodes, and 8 nematodes) were found. Prevalence, intensity, and abundance data are presented in Table 1. The 15 common

( > 20 % prevalence) helminth species included Apatemon gracilis, Echinostoma revolutum, Echinoparyphium recurva- tum, Trichobilharzia physellae, Zygocotyle lunata , Cloacotae- nia megalops, Microsomacanthus hopkinsi, Sobolevicanthus filumferens , Sobolevicanthus gracilis , Amidostomum acutum, Capillaria anatis, C. contorta , Epomidiostomum uncinatum , Streptocara crassicauda, and Tetrameres ryjikovi. These accounted for 93% of the total number of helminth indi- viduals.

All mallards were infected with 3 - 14 (X = 8.1) helminth species. There were 1 (2%), 2 (4%), 4 (9%), 5 (11 %), 8 (18%), 7 (16%), 1 (2%), 11 (24%), 3 (7%), 1 (2%), and 2 (4%) hosts infected with 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, and 14 helminth species, respectively. Helminth intensities were 1 -279 (X = 75.2). A total of 3385 helminth individuals was estimated, based on actual counts plus extrapolated counts from the aliquots.

Digeneans represented 3 1 % of the total helminths collected. Ninety-eight percent of the hosts had digenean infections (X = 2.5 species; range, 1 - 6). Mean intensity was 24 (1 - 132). Echinoparyphium recurvatum and A. gracilis were the most abundant species, representing 35 and 3 1 % , respectively, of total digeneans recovered.

Ninety-six percent of the mallards were infected with cestodes (X = 2.6 species; range, 1 - 5). Mean intensity was 4 1 (1 - 279). Fifty-two percent of the total helminth individ- uals were cestodes, and M. hopkinsi was the most abundant species (68 % of all cestodes).

Nematodes represented 17% of the total helminth indi- viduals, with 98 % of the mallards infected (X = 3.2 species; range, 1 - 6). Mean intensity was 13 (1 -49). Capillaria con- torts and T. ryjikovi represented 44 and 22 % of the nematode individuals, respectively.

The mallard population As the body size of mallards increased there was a signifi-

cant increase in condition (r = 0.3960; df = 1,44; P = 0.007). The abundances of total helminths did not increase sig- nificantly with increased body 'size (r = 0.0245; df = 1,44; P = 0.872) or condition (r = 0.2069; df = 1,44; P = 0.173). Abundances of individuals in only 2 of 15 common helminth species increased significantly with increased condition. These were Epomidiostomum uncinatum (r = 0.3464; df = 1,44; P = 0.025) and Gastrotaenia cygni (r = 0.353 1 ; df = 1,44; P = 0.043); however, only in E. uncinatum did the abun- dances increase with increased body size (r = 0.1308; df = 1,44; P = 0.016).

Body size was not significantly different between paired and unpaired males, but males were significantly larger than females (Table 2). There were no significant differences in condition across the three social classes, although females had less fat than paired (P = 0.07) or unpaired (P = 0.23) males. The lower fat levels probably were associated with the pre- basic molt in females (Heitmeyer 1985).

Seven of 45 mallards collected were classified as juveniles based on the criteria of Krapu et al. (1979). We detected no significant differences from adults in condition, body size, or pairing status (four of seven juveniles were paired), although the low number of juveniles collected may have made differ- ences difficult to detect. Comparison of abundances for the 15 common helminth species and total helminths in the three social classes indicated that the abundance of Streptocara cras- sicauda was significantly higher in unpaired juvenile males

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TABLE 1 . Prevalences, intensities, and abundances of helminth species from late-winter mallards collected on the Southern High Plains of Texas

Prevalence Intensity Abundance

No. examinedl Total Helminth species no. infected % x f SE Range x f SE individuals

Digenea Apatemon gracilis (SI, LI) Dendritobilharzia pulverulenta (H , S , MV) Diplostomulum sp. (SI) Echinoparyphium recurvatum (SI, C, LI) Echinostomu revolutum (C , LI) Eucotyle zakharowi (K) Orchipedum tracheicola (T) Trichobilharzia physellae (L, MV, K, S, H, Typhlocoelum sisowi (T, BC, E) Zygocotyle lunata (C)

Cestoda Anomotaenia ciliata (SI) Cloacotaenia megalops (CL) Fimbriaria fasciolaris (SI, C, LI) Gastrotaenia cygni (G) Microsomucanthus hopkinsi (C, LI) Sobolevicanthus filumferens (SI, C, LI) Sobolevicanthus gracilis (SI) Sobolevicanthus sp. (BC)

Nematoda Amidostomum acutum (G) Capillaria anatis (C) Capillaria contorta (E) Epomidiostomum uncinutum (G) Streptocara crassicauda (G) Strongyloides sp. (LI, C) Tetrameres ryjikovi (P) Tetrameres striata (P)

NOTE: BC, body cavity; C, caecum; CL, cloaca; E, esophagus; G, gizzard; H, heart; K, kidney; L, liver; LU, lungs; LI, large intestine; MV, mesentric vein; P, proventriculus; S, spleen; SI, small intestine; T, trachea.

TABLE 2. Physical data for three social classes of late-winter mallards from the Southern High Plains of Texas

Total body Fat . Wing length Social class N weight (g) (g) (mm)

- -

Pairedmale 15 1306f21 275f13 289f3 Pairedfemale 15 1101f24 205f13 271f2 Unpaired male 15 1251 f 33 257 f 18 289 f 2

NOTE: Values are means f SE.

not within, classes. Abundqnces of total helminths and of only one and two individual species differed across age-classes or varied with body size and condition, respectively.

Helminth dispersion patterns In each of the 15 common helminth species, the variance

was significantly larger than the mean as determined from the frequency distributions of numbers of helminth individuals in the 45-sample data set (Table 3). This is characteristic of an overdispersed distribution as defined by Bliss and Fisher (1953) and discussed by Wallace and Pence (1986). The values of the negative bionokial parameter, k, were low (Wallace than in unpaired adult males. Because there was a significant and Pence 1986) in all 15 helminth species, indicating a high

difference in of the 48 possible across degree of aggregation of individuals from the collective host social classes, subsequent analyses did not treat juveniles population .(Table 3). separately from adults. The degree of overdispersion, based on the relative values

Molting rate was significantly different between social of k, in all helmin* species across the three social with at a rate of 24'0%, paired males classes of hosts was not significantly different from that calcu-

at OV9%, and at O' % ' We < % lated for the collective host population (Table 3). Thus, over- molt rate in paired and unpaired males as biologically insig- dispersion was homogeneous across social classes. nificant. All females were molting at a similar rate; ,they con- stituted a distinct molting and social class. Host social classes and helminth communities

Subsequent analyses of the mallard helminth community Mean diversity values of helminth communities were involved comparisons only of social classes (sex and pairing 0.49 f 0.04,0.54 f 0.03, and 0.56 + 0.04 for paired males, status). Physical factors were not included because body size paired females, and unpaired males, respectively. This indi- and condition were not significantly different between sex and cated similar patterns of diversity in the helminth community pairing status classes and molting rates differed between, but at the component community level.

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TABLE 3. Determination of overdispersion and measure of the degree of aggregation in helrninth species based on the frequency distribution of numbers of individuals of each helminth species from the 45-sample data set of late-winter

mallards collected from the Southern High Plains of Texas

Total sample, Paired males, Paired females, Unpaired males, Homogeneity Helminth species k k k k P

Apatemon gracilis Echinoparyphium recurvatum Echinostomu revolutum Trichobilharzia physellae Zygocotyle lunata Cloacotaenia megalops Microsomucanthus hopkinsi Sobolevicanthus gracilis Sobolevicanthus filumferens Amidostomum acutum Capillaria anatis Capillaria contorta Epomidiostomum uncinatum Streptocara crassicauda Tetrameres ryjikovi

'Variance significantly larger than mean, P s 0.05, x2 analysis.

There was one significant discriminating variable (helminth species) across the three social classes; this was C. anatis. The number of cases (samples from the 45-mallard data matrix) classified correctly into social classes were 80, 73, and 100% for paired males, paired females, and unpaired males, respec- tively.

Pairing was the most important independent social class variable that accounted for significant differences in rank abundances of the collective common helminth species (N = 15) of mallards (Table 4). Unpaired males had significantly higher helminth abundances than paired birds (Table 5).

Epomidiostomum uncinatum was the only common helminth species that had significantly different rank abundances between paired male and female mallards (Tables 4, 5). However, this species occurred in only 4 of 15 paired males and was absent from paired females (prevalences were 53 and 27 % for unpaired and paired males, respectively). Abun- dances of the remaining 14 common helrninth species did not differ significantly between sexes in paired birds.

Rank abundances of five helminth species (M. hopkinsi, A. acutum, C. anatis, C. contorta, and E. uncinatum) were significantly greater in unpaired males than in paired females, and S. gracilis approached significance (P = 0.07). Similarly, rank abundances of four helminth species (S. gracilis, M. hop- kinsi, C. anatis, and C. contorta) were significantly greater in unpaired males than in paired males, and A. acutum approached significant (P = 0.10; Tables 4, 5).

There were appreciable differences also in prevalences of these helminth species in paired mallards versus unpaired males. Prevalences in paired males, paired females, and unpaired males, respectively, were 53, 67, and 80% for S. gracilis; 53, 53, and 100% for M. hopkinsi; 47, 40, and 67% for A. acutum; 40, 33, and 80% for C. anatis; and 60, 80, and 93 % for C. contorta.

Jaccard's coefficients of overlap for helminth species (N = 26) were low ( s 67) between respective individuals of all 15 pairs of mallards. Eleven of 15 pairs had values < 50 (E = 39 f 4).

Pairwise comparisons using Kendall's 7 for the abundances of the 15 common helminth species for each pair of mallards

indicated a significant correlation in 3 of 15 pairs. Thus, in only 20% of the pairs did the abundances of common helminth species vary in concert (significant positive correlation) between cohorts of a mallard pair. The abundance of helminth species in cohorts of the remainder of the mallard pairs varied independently.

Discussion Mallards undergo distributional changes in habitat during

winter in response to disturbance, climate, physiological, and behavioral changes, and habitat quality availability (Nichols et al. 1983; Heitmeyer and Vohs 1984; Jorde et al. 1984; Heitmeyer 1985). Although mallards have the most balanced sex ratios of all the common game ducks (Bellrose 1976), esti- mates indicate that from 51 to33 % of the population is com- posed of males in the spring and on the breeding grounds (Bellrose et al. 1961 ; Bellrose 1976). Thus, there is always a surplus of males. Paired birds are socially dominant, and they occupy and defend the most favorable winter habitats (Jorde et al. 1983, 1984; Heitmeyer and Vohs 1984; Heitmeyer 1985). As winter progresses, paired mallards tend to segregate themselves from unpaired birds by moving to smaller, secluded wetlands or to microhabitats within a particular wet- land (Heitmeyer and Vohs 1984; Jorde et al. 1984; Heitmeyer 1985). In contrast, unpaired males tend to be gregarious on larger and more marginal wetlands (Heitmeyer and Vohs 1984; Jorde et al. 1984) and possibly are more explorative than paired birds (Jorde et al. 1984).

We propose that intraspecific differences in behavior and habitat utilization by paired and unpaired mallards contributed to the differences observed in helminth abundances. Intersex- ual habitat and foraging differences cause significant varia- tions in the helminth communities of males and females in certain waterfowl species (Bourgeois and Threlfall 1982; Drobney et al. 1983; Thul et al. 1985).

Species similarity in the helminth communities representing the three social classes of mallards in the present study could result from loss of residual helminths acquired on the breeding grounds or limited acquisiton of helminths on the wintering

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TABLE 4. Values of the F-statistic and significance for one-way ANOVA across three independent social classes for the 45-sample data matrix of 15 common helminth species from late-winter mal-

lards collected from the Southern High Plains of Texas

Paired males vs. Unpaired males vs. Unpaired males vs. Helminth species paired females paired males paired females

Apatemon gracilis Echinoparyphium recurvatum Echinostoma revolutum Trichobilharzia physellae Zygocotyle lunata Cloacotaenia megalops Microsomacanthus hopkinsi Sobolevicanthus filumferens Sobolevicanthus gracilis Amidostomum acutum Capillaria anatis Capillaria contorta Epomidiostomum uncinatum Streptocara crassicauda Tetrameres ryjikovi

Total

'Denotes significance at P s 0.05.

TABLE 5. Comparison of abundances of 15 common species of helminths in paired and unpaired late-winter mallards from the Southern High Plains of Texas

Helminth species Paired males Unpaired males Unpaired males

Apatemon gracilis Echinoparyphium recurvatum Echinostoma revolutum Trichobilharzia physellae Zygocotyle lunata Cloacotaenia megalops Microsomacanthus hopkinsi Sobolevicanthus filumferens Sobolevicanthus gracilis Amidostomum acutum Capillaria anatis Capillaria contorta Epomidiostomum uncinatum Streptocara crassicauda .

Tetrameres ryjikovi Total

NOTE: Values are means f SE.

grounds. Although there were no important differences in mean diversity values between social classes of mallards on wintering grounds, unpaired males retained and (or) acquired significantly greater abundances of some helminth species.

Direct life-cycle helminths from this mallard population (A. acutum, C. anatis, C. contorta, and E. uncinatum) were more prevalent and significantly more abundant in unpaired than in paired birds. High host densities enhance the transmis- sion potentials of directly transmitted nematodes (Thul et al. 1985). The higher prevalences and abundances in unpaired males could be attributed to host gregariousness and (or) utili- zation of environments having higher densities of infective larvae. However, nematode abundances in winter-collected waterfowl may not reflect winter acquisiton alone, since they can include individuals acquired before reaching the wintering area (Buscher 1965; Thul et al. 1985).

Sobolevicanthus gracilis and M. hopkinsi had appreciably

higher prevalences and were the only indirect life-cycle hel- rninths that were significantly more abundant in unpaired males than in paired birds. Sobolevicanthus gracilis utilizes ostracods and copepods as intermediate hosts (Grytner-Ziecina 1984) and remains infective over the winter (Czaplinski and Szelenbaum 1974; Mineev 1980; Grytner-Ziecina 1980, 1984). Although retardation of strobila growth during autumn and winter can occur (Kharchenko 1960; Egizbaeva and Akaev 1978), we found both strobilated and destrobilated scolices. Thus, the higher abundance of S. gracilis could result from the more frequent and (or) prolonged contact of unpaired males with wetlands containing higher densities of infected intermediate hosts. We cannot explain the significantly differ- ent abundances of M. hopkinsi in unpaired versus paired mal- lards. It is unlikely that this cestode is transmitted on the Southern High Plains because its only known intermediate host is the amphipod Hyalella azteca (McLaughlin and Burt

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GRAY ET AL. 1943

1970; Podesta and Holmes 1970), and amphipods are uncom- mon in the playa lakes (Sublette and Sublette 1967; Thompson 1985; Gray 1986).

Unfortunately, transmission of helminth species in water- fowl on the Southern High Plains is poorly understood. Also, there is little information concerning waterfowl movements out of the area which may occur during periods of prolonged freezing temperatures. Presently, it is possible to report only the apparent differences in helminth abundances between waterfowl subpopulations. Additional studies are necessary to delineate the dynamics of transmission of helminths in this region.

Female mallards undergoing their prebasic molt in spring have an increased protein demand for feather replacement, and this additional requirement may be fulfilled by supplementing their diet with a higher proportion of invertebrates (Heitmeyer 1985). Thus, we speculated that molting females on the Southern High Plains of Texas would acquire higher helminth abundances than males, but this was not apparent in the present study.

Anderson (1982) regarded the observed patterns of distribu- tion in helminth populations as dynamic and controlled by two opposing sets of forces, one acting to increase overdispersion and the other acting to reduce it. He emphasized that as a result of changes in the relative magnitude of these opposing forces, the observed distribution patterns may change seasonally or in different host age strata. The predominant factor causing over- dispersion was believed to be heterogeneity in rates of estab- lishment, survival, and reproduction of parasites within the individuals of a host population (Anderson 1982). Factors that contribute to this heterogeneity include genetic variability, behavioral and social traits, innate susceptibility to infection, and random chance of encountering intermediate hosts con- taining aggregated distributions of larval helminths (Anderson 1982; Wallace and Pence 1986). The dispersion pattern of hel- minths in this wintering mallard population was unaffected by social status because overdispersion was homogeneous across all three social classes.

There were low overlap index values for helminth species between cohorts of 11 of 15 mallard pairs. These results coin- cide with the paired rank correlations in which only 3 of 15 individual pairs of birds linked together based on helminth abundances. Thus, whereas abundances of certain helminth species were sufficiently different to distinguish the broad categories based on pairing status, individual pairs usually could not be differentiated.

Heitmeyer (1985) suggested that phenology is more impor- tant than chronology in understanding the biological rela- tionships of wintering mallards. Our results support this hypothesis. Paired and unpaired birds may represent unique subpopulations based on their helminth abundances. These significant variations in helminth abundances may be reflec- tive of differences in physiological requirements, behavioral responses, and habitat utilization. Therefore, it is important for waterfowl specialists to recognize these apparent differ- ences and to incorporate social status into their waterfowl experimental designs.

Acknowledgements The authors appreciate the assistance of Albert 0. Bush,

Dan Combs, and Don McKenzie who critically reviewed an earlier draft of this manuscript. This project was supported in

part by the Department of Pathology, Texas Tech University Health Sciences Center, and the Institute for Museum Research, The Museum of Texas Tech University.

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