Seed dispersers as disease vectors: bird transmission of mistletoes seeds to plant hosts (original) (raw)

Abstract

The relationship between mistletoes and birds has been studied from the perspectives of mutualism and seed dispersal. Here, we emphasize the role that avian dispersers play as agents of mistletoe seed transmission to plant hosts. We describe the patterns of transmission of the seeds of Tristerix aphyllus, an endophytic Chilean mistletoe, on two of its columnar cacti hosts (Eulychnia acida and Echinopsis skottsbergii) by the Chilean Mockingbird Mimus thenca. In north-central Chile, these cacti grow in relatively discrete subpopulations on north-facing slopes. We measured variation in seed transmission within 10 subpopulations varying in species composition, host density, parasite density, parasite prevalence (defined as the percentage of hosts infested in a given population), and disperser abundance. Seed transmission was independent of species, but was strongly de- pendent on prior parasitism. Parasitized individuals received seeds much more frequently than expected from their relative abundance. We found no correlation between the density of hosts and seed transmission. We found strong positive correlations, however, between parasite prevalence and seed transmission to both parasitized and nonparasitized hosts. Seed transmission of T. aphyllus seeds by M. thenca appeared to be frequency- rather than density- dependent. Seed transmission was also tightly and positively correlated with the abundance of seed-dispersing birds at each site. Because bird abundance and parasite prevalence were correlated, we conducted path analysis to disentangle their relative effect on seed trans- mission. A model including only the direct effect of bird abundance and the indirect effect of parasite prevalence through bird abundance explained roughly the same variance as a full model including both the direct and indirect effects of bird abundance and prevalence on seed transmission. Apparently, variation in bird abundance was the main determinant of variation in transmission. We suggest that mistletoes, host plants, and the birds that disperse mistletoe seeds are systems well suited for studies of the ecological and evolu- tionary dynamics of disease transmission.

Figures (9)

Fic. 1. Mean cactus height in 10 different subpopulations (sites) at Parque Nacional Fray Jorge. Open bars, parasitized cacti; closed bars, nonparasitized cacti. Errors are standard deviations. Sample sizes per species are given in Table 1. The prevalence of T. aphyllus on E. skottsbergii and E. acida was not significantly different from that ex-

Fic. 1. Mean cactus height in 10 different subpopulations (sites) at Parque Nacional Fray Jorge. Open bars, parasitized cacti; closed bars, nonparasitized cacti. Errors are standard deviations. Sample sizes per species are given in Table 1. The prevalence of T. aphyllus on E. skottsbergii and E. acida was not significantly different from that ex-

* Estimated from nearest neighbor distances based on Krebs (1989:95). + Percent of individual cacti infected by Tristerix. TABLE 1. Characteristics of 10 north-facing subpopulations of Echinopisis skottsbergii and Eulychnia acida at Parque Nacional Fray Jorge, Chile.

* Estimated from nearest neighbor distances based on Krebs (1989:95). + Percent of individual cacti infected by Tristerix. TABLE 1. Characteristics of 10 north-facing subpopulations of Echinopisis skottsbergii and Eulychnia acida at Parque Nacional Fray Jorge, Chile.

Fic. 2. Observed vs. expected number of E. skottsbergii and E. acida parasitized by T. aphyllus in 10 subpopulations. The frequency of seed deposition on cacti was independent of species at all sites. The number of parasitized cacti of each species was not significantly different from that expected based on the specific relative abundances at each subpopu- lation.

Fic. 2. Observed vs. expected number of E. skottsbergii and E. acida parasitized by T. aphyllus in 10 subpopulations. The frequency of seed deposition on cacti was independent of species at all sites. The number of parasitized cacti of each species was not significantly different from that expected based on the specific relative abundances at each subpopu- lation.

Soar We used the percentage of cacti receiving seeds and the mean number of seeds received per cactus as es- timators of seed transmission. Seed deposition on non- parasitized cacti estimates new infections, whereas seed deposition on parasitized cacti estimates reinfec- tions. In order to distinguish between these two pro- cesses, we analyzed seed rain on parasitized and non- parasitized cacti separately. The percentage of non- parasitized cacti receiving seeds increased significantly with T. aphyllus prevalence (r = 0.75, P < 0.03; Fig. 4c). Surprisingly, we found no significant correlation between the percentage of nonparasitized cacti receiv- ing seeds and parasitized cactus density or total cactus density (r = 0.31, P > 0.3; and r = —0.09, P > 0.5, respectively). The pattern of transmission from para- sitized to parasitized cacti followed a similar pattern: The percentage of parasitized individuals receiving seeds increased significantly with increasing T. aphyl- lus prevalence (r = 0.58, P > 0.05; Fig. 4b) but was not significantly correlated with parasitized cactus den- sity or total cactus density (r = —0.41, P > 0.5; r= —0.01, P > 0.1, respectively). The mean number of seeds received by parasitized and nonparasitized cacti followed trends similar to those for the percentage of cacti receiving seeds. The mean number of seeds re- ceived by parasitized and nonparasitized cacti in- creased significantly with T. aphyllus prevalence (r = 0.59 and r = 0.81, P < 0.05, respectively). The mean

Soar We used the percentage of cacti receiving seeds and the mean number of seeds received per cactus as es- timators of seed transmission. Seed deposition on non- parasitized cacti estimates new infections, whereas seed deposition on parasitized cacti estimates reinfec- tions. In order to distinguish between these two pro- cesses, we analyzed seed rain on parasitized and non- parasitized cacti separately. The percentage of non- parasitized cacti receiving seeds increased significantly with T. aphyllus prevalence (r = 0.75, P < 0.03; Fig. 4c). Surprisingly, we found no significant correlation between the percentage of nonparasitized cacti receiv- ing seeds and parasitized cactus density or total cactus density (r = 0.31, P > 0.3; and r = —0.09, P > 0.5, respectively). The pattern of transmission from para- sitized to parasitized cacti followed a similar pattern: The percentage of parasitized individuals receiving seeds increased significantly with increasing T. aphyl- lus prevalence (r = 0.58, P > 0.05; Fig. 4b) but was not significantly correlated with parasitized cactus den- sity or total cactus density (r = —0.41, P > 0.5; r= —0.01, P > 0.1, respectively). The mean number of seeds received by parasitized and nonparasitized cacti followed trends similar to those for the percentage of cacti receiving seeds. The mean number of seeds re- ceived by parasitized and nonparasitized cacti in- creased significantly with T. aphyllus prevalence (r = 0.59 and r = 0.81, P < 0.05, respectively). The mean

Fic. 4. (a) Density of Chilean Mockingbirds, M. thenca, and seed deposition frequency of T. aphyllus on (b) parasit- ized and (c) nonparasitized cacti, as a function of T. aphyllus prevalence (percent of 100 cacti individuals infected).

Fic. 4. (a) Density of Chilean Mockingbirds, M. thenca, and seed deposition frequency of T. aphyllus on (b) parasit- ized and (c) nonparasitized cacti, as a function of T. aphyllus prevalence (percent of 100 cacti individuals infected).

Fic. 5. Seed deposition frequency on parasitized (a) and nonparasitized cacti (b) as a function of M. thenca density at each subpopulation. Note that the correlation between de- position frequency and bird density is higher than that be- tween deposition frequency and prevalence of T. aphyllus (see Fig. 4).

Fic. 5. Seed deposition frequency on parasitized (a) and nonparasitized cacti (b) as a function of M. thenca density at each subpopulation. Note that the correlation between de- position frequency and bird density is higher than that be- tween deposition frequency and prevalence of T. aphyllus (see Fig. 4).

Fic. 6. Two alternative structural models illustrating the possible causal relationships between seed transmission and seed disperser abundance and mistletoe prevalence. In model (A), both bird abundance and T. aphyllus prevalence have direct and indirect effects on transmission. Thus, the coeffi- cient of correlation (r) for model (A) includes terms for both direct and indirect effects. In model (B), only bird abundance has a direct effect on seed transmission; mistletoe prevalence influences transmission only indirectly through its effect on bird abundance. Thus, the coefficient of correlation (r,,) for model (B) includes only the direct effect of bird abundance (Po) 2

Fic. 6. Two alternative structural models illustrating the possible causal relationships between seed transmission and seed disperser abundance and mistletoe prevalence. In model (A), both bird abundance and T. aphyllus prevalence have direct and indirect effects on transmission. Thus, the coeffi- cient of correlation (r) for model (A) includes terms for both direct and indirect effects. In model (B), only bird abundance has a direct effect on seed transmission; mistletoe prevalence influences transmission only indirectly through its effect on bird abundance. Thus, the coefficient of correlation (r,,) for model (B) includes only the direct effect of bird abundance (Po) 2

Fic. 7. Comparison of the performance of two structural models relating bird abundance and T. aphyllus prevalence with several estimators of seed transmission to parasitized and nonparasitized cacti. In each panel, the values contiguous to straight arrows connecting the independent variables (bird abundance and T. aphyllus prevalence) with the dependent variable (seed transmission) are path coefficients. The value contiguous to the curved arrow connecting the two independent variables is the correlation coefficient between them. Each panel contains the coefficient of correlation (r) for model (A), which includes the direct and indirect effects of both independent variables on seed transmission (see Fig. 6). Each panel also includes the correlation coefficient (r) for model (B). Significance levels of each path coefficient are indicated with asterisks (*, P < 0.05; **, P < 0.005; Ns, not significantly different from 0).

Fic. 7. Comparison of the performance of two structural models relating bird abundance and T. aphyllus prevalence with several estimators of seed transmission to parasitized and nonparasitized cacti. In each panel, the values contiguous to straight arrows connecting the independent variables (bird abundance and T. aphyllus prevalence) with the dependent variable (seed transmission) are path coefficients. The value contiguous to the curved arrow connecting the two independent variables is the correlation coefficient between them. Each panel contains the coefficient of correlation (r) for model (A), which includes the direct and indirect effects of both independent variables on seed transmission (see Fig. 6). Each panel also includes the correlation coefficient (r) for model (B). Significance levels of each path coefficient are indicated with asterisks (*, P < 0.05; **, P < 0.005; Ns, not significantly different from 0).

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