Springer-VerlagTokyohttp://www.springer.de101640289-07711439-5444Journal
of EthologyJ
EtholLifeSciences17410.1007/s10164-005-0174-2
J Ethol (2006) 24:147–153 DOI 10.1007/s10164-005-0174-2
© Japan Ethological Society and Springer-Verlag Tokyo 2005
ARTICLE
David M. Powell • David E. Danze • Michael A. Gwinn
Predictors of biting fly harassment and its impact on habitat use by feral horses (Equus caballus) on a barrier island
Received: April 12, 2005 / Accepted: July 29, 2005 / Published online: October 22, 2005 Japan Ethological Society and Springer-Verlag 2005
Abstract Feral horses on Assateague Island, Maryland, were observed in June and August 2000 to determine what behavioral and ecological factors affect the intensity of biting fly harassment and whether habitat use by horses was influenced by biting flies. Fly counts and frequencies of comfort movements (i.e., movements designed to dislodge insects) were recorded during focal animal samples, as well as data on sex, group size, habitat type, temperature, humidity, wind speed, and behavior. Seasonal habitat use patterns were assessed using 7 years of monthly census data on the horses. The number of biting flies on the horse was affected by horse sex, habitat, temperature, and group size. The number of comfort movements a horse showed was affected by habitat, temperature, wind speed, group size, and number of horses within one body length of the focal. The number of comfort movements made by a horse was found to be highly correlated with fly numbers. Though marshes were used most throughout the year, the pattern of use of dune, scrub, and human-altered habitats reflects a pattern of biting fly avoidance and refuge-seeking by the horses. Key words Horses · Fly · Barrier Island · Habitat use · Harassment
D.M. Powell (*) Department of Mammalogy, Wildlife Conservation Society, Bronx Zoo, 2300 Southern Blvd, Bronx, NY, 10460, USA Tel. +1-718-2205162; Fax +1-718-3650307 e-mail:
[email protected] D.E. Danze Administrative Management Systems Support Branch, Office of the Chief Technology Officer, Smithsonian Institution, Washington DC, 20013, USA M.A. Gwinn Department of Biology, Georgetown University, Washington DC, 20057, USA
Introduction Hamilton’s (1971) “selfish herd” model of how spatial relationships among individuals can reduce predation may also apply to animals subjected to ectoparasitism by biting flies (Mooring and Hart 1992). Encounter-dilution effects (Mooring and Hart 1992) assume that in order for an increase in the number of potential hosts (group size) to dilute the risk of ectoparasitism on any one of them, the increase in number of hosts cannot result in an equal or larger increase in parasite numbers. Three studies of feral horse populations have found that per capita fly numbers decreased with increasing social group size (Duncan and Vigne 1979; Rutberg 1987; Rubenstein and Hohmann 1989). In addition to aggregating into groups, animals may take other measures to lessen the degree of biting fly harassment. These measures include body movements designed to remove or flush flies from the body, lying down to reduce exposed surface area, increasing physical activity, and moving to different habitat types (Hart 1990; Mooring and Hart 1992). Attacks by biting flies can have serious consequences for ungulate hosts, including decreases in resting or feeding behavior, failure to nurse offspring, growth deficits, disease transmission, blood loss, and death (reviewed by Hart 1990, 1994). A study in New York found that a horse may receive as many as 4,000 fly bites per day, resulting in a loss of as much as 0.5 l of blood (Tashiro and Schwardt 1953). In this study we sought to determine (1) what behavioral and ecological factors predict biting fly intensity and (2) whether use of different habitat types by feral horses reflects a pattern of fly avoidance and refuge-seeking. We hypothesized that per capita biting fly intensity would be lower in larger groups of horses and on horses standing in tightly clumped groups, as measured by the number of horses within one body length of a focal animal. Biting fly intensity was hypothesized to be higher when temperature and humidity were high and wind speed was low (Tashiro and Schwardt 1949; Rockel and Hansens 1970a). We also predicted that biting fly harassment would be more
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intense on stationary as opposed to moving animals. Finally, we hypothesized that biting fly intensity would be higher in habitats with more vegetation (marshes and scrub/forest areas) than in areas with less vegetation, such as dunes and beaches (Keiper and Berger 1982; Mooring et al. 2003). With respect to habitat use, our general hypothesis was that horses would be less likely to be found in habitats where fly activity is likely to be high and that habitat use would fluctuate seasonally. We predicted that fly activity would be highest during the summer in scrub/forest habitats followed by marshes and dunes. Therefore, the horses’ use of scrub/forest habitats should be higher in fall and winter compared to spring and summer.
Materials and methods Our study was conducted on Assateague Island, a 56-kmlong barrier island running along the coasts of Maryland and Virginia, USA. Observations were made on the Maryland portion of the island, an area of about 35.5 km2. There are five common species of tabanid flies on Assateague: green-headed horse flies (Tabanus nigrovittatus and Tabanus lineloa), deer flies (Chrysops fuliginosus and Chrysops atlanticus) and a stable fly, Stomoxys calcitrans (Rockel and Hansens 1970b). Females of these species lay eggs in wet areas, and the larvae develop in the soil. On Assateague, this primarily takes place in the marshes where the adults emerge and reach maximum numbers in late July through mid-August (Morgan and Lee 1977). Female flies seek hosts and engorge themselves with the host’s blood in order to produce eggs (Hughes et al. 1981). The third author observed feral ponies at Assateague Island National Seashore on a total of 15 days from 8–16 June and 14–28 August 2000. We conducted the study on an approximately 18-km portion of the island that had been developed for both a national and state park. This portion of the island contains beaches and dunes, bayberry-scrub (Myrica spp., Rubus argutus) and pine (Pinus taeda, Pinus virginiana) forests, salt marshes, and human-altered habitats (e.g., roads, parking lots, mowed areas around buildings). The Maryland portion of the island supports a population of approximately 170 feral horses, approximately 140 of which inhabited the study area during the sampling period. Our analyses of factors affecting biting fly harassment are based on 93 focal observations on a sample of 55 horses. Analyses of habitat use by horses are based on a sample of 83 horses. We sampled all possible individuals in the study area. Horses were identified using drawings provided by the National Parks Service. Horses were never sampled more than once per day. In most cases, groups of horses could be approached to within 5–10 m; otherwise, binoculars were used to conduct observations. Focal sampling of horses within a group was done in random order. The horse’s color pattern (bay, sorrel, or pinto), habitat type (dune/beach, scrub/forest, marsh, other), group size, number of horses
within one body length of the focal’s head, behavior, and any important weather data (e.g., wind gusts or rain) were recorded. Pintos are multi-colored with patches of white, brown, or black. Sorrels are mostly light brown with brownish-red manes and tails. Bay horses are dark brown with black manes and tails. Marshes were defined as moist areas dominated by short grass (Spartina spp.). Scrub habitats included areas of vegetation > 0.5 m in height, including pine forest. Dunes included open beach areas and sparsely vegetated dunes with a sand substrate. Other areas included paved roads, parking lots, and areas of mowed grass. Behavior was classified as grazing (head lowered to ground, mouth biting or chewing, animal moving or stationary), standing (head not lowered to ground, animal stationary), or “other.” The only “other” behavior observed was locomotor play (running) in a young male. On each side of the horse, three counts of flies on the horse were taken at 20-s intervals during a 1-min sample. We did not make attempts to count mosquitoes in this study due to their small size and our inability to approach the horses close enough to get reliable counts of mosquitoes. We acknowledge that mosquitoes may also represent significant sources of blood loss and vectors for disease. During the next minute, all comfort movements (snorts, foot stomps, head sways to flanks, bites, muscle twitches) intended to dislodge flies were counted and totaled. We did not tally tail movements of the horses for two reasons. First, tail movements to dislodge flies were sometimes rendered ineffective in thick vegetation, and second, tail movements occurred so frequently that they and other comfort movements could not be reliably tallied. During the third minute, three additional fly counts were taken as described previously. This procedure was repeated for the other side of the horse. Data from both sides of the animal were averaged to produce one fly count and one value for the number of comfort movements per minute per horse sampled. All samples were collected between 1030 and 1930 hours. Weather data were obtained for sampling periods from the National Parks Service weather station on Assateague. Temperature, humidity, and wind speed data were recorded every hour by the station. Proc Mixed (SAS Stat module, SAS Stat User’s Guide Version 8, SAS Institute, Cary, NC) was used to perform a repeated-measures general linear model predicting mean number of comfort movements and the mean number of flies on the horse during the sample based on the following. Fixed effects included wind speed, temperature, humidity, group size, number of horses within one body length of the focal horse, habitat type, behavior (play, graze, or stand), color, and sex. Horse identification was included to control for repeated measures but was never found to be a significant factor (P > 0.05). Mean numbers of flies on the horses were square-root transformed to achieve normality. Tukey tests were performed when habitat type, behavior, and sex were found to have significant effects. Tukey tests were not performed when group size and number of horses within one body length of the focal were found to be significant effects because the number of tests was too large relative to the number of degrees of freedom. Means were
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inspected visually to identify these effects. Means are presented ± SE. Comfort movements as indicators of flies We calculated the Pearson correlation between comfort movements and fly numbers in order to determine whether comfort movements could be used as reliable indicators of fly numbers. We also included fly numbers in the mixed model with the other factors that were found to have significant effects on comfort movements in order to determine how much impact those factors had when the effect of fly numbers was controlled for. Habitat use by horses We first determined the availability of the four habitat types (dunes, scrub/forest, marsh, and other) using transects drawn at 10-m intervals along a GIS vegetation map of the Maryland portion of Assateague Island. The linear distance of the transect line falling within each of the vegetation types was determined and converted to a percentage of each transect. These percentages were averaged across all transects to determine the overall percent cover of each vegetation type on the island. We used monthly census data of the horses to assess how their use of habitat types changes during the year. Each month, every horse on the island is located, and the habitat type in which each is found is recorded. Habitat categories were dunes/beaches, scrub/forest, marsh, and other (see definitions above). We selected the months of January, April, July, and October to represent winter, spring, summer, and fall. These months were chosen because they represented the mid-points of each season and were not characterized as transitional periods between seasons. We generated a new sample of 83 horses that were found in each census from 1995 to 2002. We calculated the percentage of horses in the sample found in each habitat type in each census. Because these percentages sum to 100, we were unable to test for an interaction between habitat type and season. We ran separate repeated measures ANOVAs for each habitat type with season as the main effect and year as the repeated measure in order to determine if use of a particular habitat type changed during the year. We used Tukey tests to compare seasonal means to one another when significant main effects were found. Results were considered significant when P < 0.05, but some non-significant trends are also reported. Analyses were run using SigmaStat software (v. 3.0, SPSS). We also compared habitat use to habitat availability overall and within each season using the technique described by Neu et al. (1974). For these analyses, the overall P value was kept at .05 for each set of comparisons (all year, within winter, spring, summer, and fall). Each set of comparisons involved four two-tailed tests so the experimentwise error level was 0.0062.
Results The sample included 93 focal observations collected from 31 males (mean age 9.2 years, range 0–21 years) and 24 females (mean age 8.9 years, range 0–21 years), including four males and one female aged 0–1 year. In the majority of the observations (82%, n = 93), the focal animal was grazing. The focal animal was standing (17%) or playing (1%) in the rest of the samples. Because only one sample included an animal that was playing, only the effects of standing vs. grazing were tested in the behavior analysis. The horses were in the marsh in 37.5% of the samples, the scrub/pine forest in 38.5% of the samples, and in the dunes/ beach area in 24% of the samples. Relative humidity averaged 78.6% (range: 57–100%); the average temperature was 23.9°C (range: 17.2–29.4°C). Wind speed averaged 15.4 km/h (6.4–22.5 km/h).
Fly counts Male horses had more flies on them than female horses (males: 3.88 ± 0.48, females: 1.94 ± 0.25; F1,53 = 11.30, P = 0.001). Behavior also had a significant effect on fly counts (F1,12 = 5.96, P = 0.031). Grazing horses (3.30 ± 0.36) had more flies on them than standing horses (1.76 ± 0.49). Fly numbers were highest in the scrub habitat followed by the dunes and marshes (F2,13 = 8.79, P = 0.004, Fig. 1). The difference in fly counts between marsh and scrub habitats was significant (P = 0.002). There was no significant difference in fly numbers between marsh and dune habitats (P = 0.498). The difference in fly numbers between scrub and dune habitats approached significance (P = 0.088). Fly numbers increased with increasing temperature (F1,33 = 8.54, P = 0.006, Fig. 2; β = 0.048, intercept = −2.083) and decreased with increasing group size (F1,33 = 15.24, P = < 0.001, Fig. 3; β = −0.152, intercept = −2.083). Horse color was not a significant predictor of fly numbers (F2,0 = 2.20, P = 1.0).
Comfort movements As with fly numbers, comfort movements were highest in scrub habitat, followed by marsh and dunes (F2,13 = 5.05, P = 0.024, Fig. 1); however, only scrub and dune habitats differed significantly (P = 0.019). Comfort movements increased with increasing temperature (F1,32 = 15.80, P < 0.001; β = 1.289, intercept = −51.911) and decreased with increasing wind speed (F1,32 = 14.01, P = < 0.001, Fig. 4; β = −2.081, intercept = −51.911). Comfort movements decreased with increasing numbers of horses within one body length (F1,32 = 4.69, P = 0.038, Fig. 5; β = −2.466, intercept = −51.911) as well as with group size. The effect of group size on comfort movements approached significance as well (F1,32 = 2.95, P = 0.095). Horse color was not a significant predictor of comfort movements (F2,0 = 0.04, P = 1.0).
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Fig. 3. Mean number (± SE) of flies/horse as a function of group size
Fig. 1. Least-squares mean number (± SE) of flies/horse (A) and comfort moves/min (B) in different habitat types. Bars with different superscripts are significantly different
Fig. 4. Mean number of comfort movements/minute as a function of temperature (A) and wind speed (B)
mixed model with habitat type, temperature, wind speed, and number of horses within one body length. Fig. 2. Mean number of flies/horse as a function of temperature. A simple linear regression line is presented
Comfort movements as indicators of flies Fly count was significantly correlated with comfort movements (ρ = 0.46, P < 0.001). Fly count was also a significant predictor of comfort movements when included in the
Habitat use by horses throughout the year There was a significant main effect of season on the percentage of horses found during the censuses in each habitat type examined (see Fig. 6 for ANOVA results). Most horses were found in the marsh regardless of season. The only significant difference in percentage of horses seen in the marsh was between spring and summer (P = 0.035), and the difference
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between spring and fall approached significance (P = 0.085). The smallest percentage of horses sighted in marshes occurred in summer. Dunes were used most in summer and were used significantly more often in summer compared to winter (P = 0.004). The difference in use of dunes between fall and winter approached significance (P = 0.066). Scrub areas were used most in fall and winter. Significantly more horses were found in the scrub in winter compared to spring (P = 0.028) and summer (P = 0.001). The difference
between fall and summer was significant (P = 0.003), while the difference between fall and spring approached significance (P = 0.077). Summer was when most horses were found in the other habitats, and summer use of other habitats was significantly greater than for other seasons (winter, P < 0.001; fall, P = 0.002; spring, P = 0.003). Throughout the year, forest/scrub habitat was used less than expected, based on availability (44.9% cover), whereas marsh habitat (40.6% cover) was used more than expected. Dunes (9.0%) and other habitats (5.5%) were utilized in proportion to availability. During the fall, scrub habitats were used less than expected whereas all other habitat types were used in proportion to availability. In winter, dunes were used less and marshes were used more than expected. Scrub/forest and marshes were used more than expected in spring. During summer, dunes and other habitats were used more than expected whereas scrub/forest was used less than expected.
Discussion Our first objective was to identify factors that predict levels of biting fly harassment of feral horses. Male horses had Fig. 5. Mean number (± SE) of comfort movements/min as a function more flies on them than females, consistent with previous studies of barrier island horses (Rubenstein and Hohmann of the number of horses within one body length of the focal horse
Fig. 6. Mean percentage of horses in the study sample that were found in each habitat category across different seasons of the year. There is a significant effect of season in each habitat. Bars with different superscripts are significantly different
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1989; Rutberg 1987). In general, metabolic rates of males are higher than those of females (Altmann and Dittmer 1968), and metabolic rate may be linked to carbon dioxide (CO2) emission (Smythe and Goody 1972). Biting flies are drawn to baits with a carbon dioxide source (Knox and Hays 1972); therefore, more CO2 production by males may attract more flies to them. However, a number of chemicals appear to be involved in the attraction of biting insects (i.e., Hargrove et al. 1995), so we cannot say for certain that CO2 is the only relevant chemical factor distinguishing males and females. We found support for our hypothesis that per capita fly harassment would decrease with increasing group size and increasing numbers of close (i.e., within one body length) neighbors. Similar results have been found in other studies (Hart 1990; Mooring and Hart 1992; Duncan and Vigne 1979; Rutberg 1987; Rubenstein and Hohmann 1989). Because the observational study was conducted during the summer when biting flies are generally most numerous, we were unable to demonstrate that the horses in our sample reduced their inter-personal distances in response to flies (but see Rutberg 1987), but we did observe that the horses formed tightly clumped groups, often standing with their flanks touching one another. Very commonly groups of horses would stand side by side in opposite orientations, such that one horse’s face was flanked by a neighbor’s tail. In this position the tail movements of one horse would help flush flies off the face of its neighbor (see Tyler 1972). Movement in these groups was fluid, with animals continuously trying to occupy positions in the middle, where both of their sides would be protected. Fly numbers and comfort movements increased with increasing temperature as predicted. We did not find a significant effect of wind speed on fly numbers, but comfort movements did decrease with increasing wind speed. We found no significant effect of humidity on either measure of fly harassment. Keiper and Berger (1982) found that tail swishes by horses were less frequent on rainy days compared to cloudy and sunny days, whereas Tashiro and Schwardt (1949) found that fly activity increased with humidity. Fly numbers and comfort movements show a slight decrease with increasing humidity (data not shown); however, this effect may be due in part to the effect of rain. Samples were not collected during heavy rain, but some were collected during light rain. It is impossible to distinguish rainy periods from very high humidity periods in the meteorological data from the weather station, so some of the high humidity readings might actually reflect rain. If we exclude samples when humidity readings exceeded 80%, then both measures of fly intensity show a general increase with increasing humidity. It may be that fly activity increases with humidity until rain falls. We hypothesized that fly harassment would be greater for animals that were standing still as opposed to those that were moving. In fact we found that the opposite was true. Horses that were grazing (and thus moving) had more flies on them than horses that were standing still resting. We believe that this is because grazing horses flushed flies from surrounding vegetation through the movements of their
limbs and snouts, whereas resting horses were not disturbing the surrounding vegetation. Findings from studies of red deer (Cervus elaphus) support this hypothesis (Espmank and Langvatn 1979). Similarly, we found that flies and mosquitoes bothered the observers less when they were sitting or standing still as opposed to walking through the marshes. We expected that fly harassment would be greatest in marshes and scrub/forest habitats because these areas are where adults emerge and lay eggs, and they provide more shelter from winds. Fly counts were significantly higher in scrub habitat than in marshes and dunes/beaches. Comfort movements did not differ between marsh and scrub habitats, but movements were significantly more frequent in scrub compared to dunes and beaches. Marshes did not differ from dunes and beaches in comfort movements. These findings support the hypothesis that vegetation provides “cover” for flying insects to rest in during periods of high wind or rain. Dunes and beaches likely have fewer flies because they provide the least amount of cover for insects because vegetation or other features are very sparse, and wind speed is generally higher on the beach than inland (see also Rubenstein and Hohmann 1989; Mooring et al. 2003). Previous work also indicates that vegetation can be an effective barrier to fly movement (Morgan and Lee 1977). The taller scrub/forest zone in the middle of Assateague likely acts in conjunction with higher wind speeds on beaches to reduce biting fly harassment in dune and beach areas. In a previous study on Assateague, Keiper and Berger (1982) reported lower rates of tail swishing by horses when in bays, beaches, and mudflats compared to when the horses occupied marshes, dunes, and inner dunes. In our study, we combined dunes and beaches into one category, and the inner dune areas described by Keiper and Berger would fall into our scrub/forest category. Our results therefore agree with previous studies on Assateague. One of our goals was to assess the validity of using comfort movements as a proxy measure of fly harassment, given that fly counts are generally more difficult to do for a number of reasons. Using comfort movements as indicators would also reflect harassment by mosquitoes, which are difficult to quantify visually in the field. Our analyses indicate that comfort movements are a useful and reliable indicator of biting fly intensity (see also Keiper and Berger 1982; Mooring et al. 2003). When we analyzed habitat use by the horses over a 7year period, we found significant seasonal variation in the proportion of horses found in dunes/beaches, scrub/forest, marsh, and altered habitats. Our hypothesis was that habitat use by horses would be influenced by biting flies. Marshes and scrub/forest areas should be the habitats with the most fly activity given that this is where adults emerge in the summer and where most vegetative cover occurs. We would predict that horses should avoid marshes and scrub areas during summer. Marshes were where most horses were found, regardless of season, likely because this is where the majority of their food is found. Marshes were used more than expected based on availability during the spring and winter. However, we did see a significant decrease in the number of horses found in the marsh in summer.
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Fewer horses were found in the scrub habitats in the warmer months compared to the fall and winter. The increase in scrub use in the fall and winter possibly reflects foraging on alternative food sources and seeking of shelter from cold winds; however, this habitat was used less than expected during fall, based on availability. Scrub was used more than expected in spring though still not at the level seen during the cooler months. During summer, scrub was used less than expected based on availability, and in fact this was the season when scrub was used least by the horses. Dune and beach areas have the least amount of vegetative cover, so they don’t offer much in terms of food for horses, but the winds present in this habitat make it a refuge from biting insects. Therefore we would not expect to find many horses in this habitat throughout the year, but we should see an increase in horse numbers here during the warmer months. In fact we did find that more horses were found in the dunes in summer relative to other seasons, though only the difference between summer and winter was statistically significant. Dunes were used less than expected during winter and more than expected during summer, based on availability. This provides further support for our hypothesis that dunes provide a seasonal refuge during periods of high insect activity. Finally, our “other” habitat category mainly included human-altered areas (e.g., parking lots, roads, and some mowed areas) that are in the developed area of the island. This is also an area that is sprayed in the summer to provide relief for tourists from biting insects. We found that there is a significant increase in the number of horses using these altered habitats during summer. So this habitat too might act as a refuge for horses from biting insects. Further support for this hypothesis is provided by the observation that other altered habitats were used significantly more than expected based on availability during summer. During our observations, we also found that the horses would use other microhabitats to avoid biting flies, though to a much lesser extent. On occasions when fly harassment appeared to be particularly intense, the horses would walk out into the bay or the ocean. Though this may help horses to cool off, we don’t believe this is the primary reason for this behavior because the horses didn’t engage in this behavior often and when they did so, they did not appear to be comfortable with the footing underwater. We also observed horses resting in tidal mudflats on the bay side of the island. Though these areas were surrounded by marsh and scrub habitat, the mudflats were open enough to allow for winds to keep flies away from horses when there. We also observed the horses migrating to narrower portions of the island where oceanic and bay breezes would sweep the entire landscape. Habitat shifts and migrations in response to biting insects have been documented in other studies of feral horses (Tyler 1972; Duncan and Cowtan 1980; Keiper and Berger 1982). In conclusion, biting fly harassment of feral horses is influenced by intrinsic and extrinsic physical, social, and ecological factors. Harassment by biting insects shapes feral
horse ecology, specifically spatial relationships of individuals and habitat use. Reduction in biting fly harassment is potentially another factor selecting for group living in this population. Acknowledgements We would like to thank Carl Zimmerman, Jack Kumer, and Alison Turner of the National Parks Service for their assistance with this research. Edward Barrows (Georgetown University) also provided helpful comments and assistance. The manuscript was improved by comments from two anonymous reviewers. This research was approved by the Georgetown University Animal Care and Use Committee.
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