- Email: [email protected]
The Western Viceroy butterfly (Nymphalidae: Limenitis archippus obsoleta): an indicator for riparian restoration in the arid southwestern United States?
Ecological Indicators 3 (2003) 203–211
The Western Viceroy butterfly (Nymphalidae: Limenitis archippus obsoleta): an indicator for riparian restoration in the arid southwestern United States? S. Mark Nelson∗ Ecological Research and Investigations Group, Technical Services Center, Bureau of Reclamation, Rm. 2010, Bldg. 56, P.O. Box 25007, Denver, CO 80225, USA Accepted 15 April 2003
Abstract Life history characteristics of the Western Viceroy (Limenitis archippus obsoleta), an obligate riparian nymphalid butterfly in the desert southwestern United States, are described and related to Colorado River riparian restoration efforts. Riverine disturbance regimes and associated fluvial and hydrological dynamics may provide resources critical to this butterfly. Puddling by adult butterflies may require flood-cleared surfaces and an obligate riparian plant, Gooddings willow, was a larval host plant. This butterfly needs a variety of resources that are only found in close proximity in naturally functioning riparian ecosystems. Habitat heterogeneity required for colony persistence depends largely upon the natural dynamic character of flowing water systems. Because of the links between this butterfly and riparian structure and function it may be a useful indicator for monitoring riparian ecosystem restoration in the area. © 2003 Elsevier Ltd. All rights reserved. Keywords: Bill Williams River; Colorado River; Indicator organisms; Limenitis archippus obsoleta; Riparian restoration; River regulation; Viceroy butterfly; Willow
1. Introduction Since the early to mid-20th century many dams, irrigation projects, and hydropower facilities have been built in the United States. Initially, downstream effects were of little concern, because these structures were thought to be environmentally benign elements of the landscape. Current literature, however, documents a host of ecological degradations concerning river regulation (Collier et al., 1996). Effects extend to both aquatic and terrestrial components of the ecosystem and may influence many miles of river. ∗ Tel.: +1-303-445-2225; fax: +1-303-445-6328. E-mail address: [email protected] (S.M. Nelson).
A series of dams in the arid southwestern United States have affected river ecology along the lower Colorado River, changing the river from one characterized by widely fluctuating flows and physico-chemical extremes to one of the most altered and intensively controlled systems in the United States (Carlson and Muth, 1989). The lower part of this river runs through one of the hottest and driest deserts on earth. Along the river at Parker, Arizona, the mean number of days per year with a maximum temperature ≥32 ◦ C is 178, and annual precipitation is 10.4 cm (Andersen, 1994). In association with river regulation, several aquatic taxa are now endangered or of concern (Moore et al., 1996) and terrestrial vegetation in the lower valleys has undergone dramatic changes. Documentation of historic
1470-160X/$ – see front matter © 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1470-160X(03)00044-X
204
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
conditions along the Colorado River is presented in Mueller and Marsh (2002). Forested bottomlands are presently diminished in area (Ohmart et al., 1988) with historic riparian areas becoming more desert-like. In response, restoration programs were initiated in the 1970s (Pinkney, 1992) and several areas planted with phreatophytic plants such as cottonwood and willow and the more xeric mesquite. Although studies of bird and mammal response to these revegetated areas were undertaken early on (Anderson and Ohmart, 1984, 1985), studies of invertebrates associated with revegetation sites have been limited until recently (e.g. Andersen, 1994; Nelson and Andersen, 1999). Nelson and Andersen (1999) found that, despite the presence of larval host plants at revegetated sites, obligate riparian butterflies were not found at any revegetated site and were also not found at sites where they had been documented in the 1930s around the time of the closure of Hoover Dam. The purpose of this study was to study the autecology of the Western Viceroy butterfly (Limenitis archippus obsoleta) against the background of riparian restoration. Autecological research often reveals subtle habitat requirements of butterflies (Thomas, 1991). Several elements might determine suitability of revegetated habitat for this butterfly. The ability of the Western Viceroy butterfly to use a particular habitat could be affected by movement patterns, behavior, larval host plant use, and nectar use. Many of these attributes are potentially affected by river regulation and restoration. Therefore, this butterfly may serve as an indicator of river ecosys-
tem condition and be useful in monitoring activities. Studies took place on the Bill Williams River, which contains a naturally functioning cottonwood/willow ecosystem. The Bill Williams River flows into Lake Havasu, formed by Parker Dam on the Colorado River. 2. Methods 2.1. Study areas Three sites were used for study on the Bill Williams River (Fig. 1). Site 1 was the furthest downstream. Water flow at this site was intermittent and only occurred in April of 1998 during the study period. Site 2 was 2–3 km upstream of site 1 and approximately 1 km downstream of site 3. Both upstream sites were in areas of perennial flow. All sites contained tamarisk (Tamarix ramosissima) and Gooddings willow (Salix gooddingii) in approximately equal amounts. Fremont cottonwood (Populus fremonti) at site 1 was limited to only a few large (20 m height) sentinel trees. Cottonwood was more common at sites 2 and 3 and consisted of both larger and smaller trees suggesting that cottonwood recruitment was occurring at these sites. Honey mesquite (Prosopis juliflora) was a minor element at all sites. Seepwillow (Baccharis salicifolia) and arrowweed (Tessaria sericea) were common at site 1 but found in lesser amounts at the other sites. Sites 2 and 3 were more mesic than site 1 and contained wetland plants such as cattails (Typha) and sedges (Cyper-
Fig. 1. Bill Williams River Viceroy butterfly survey sites. Direction of stream flow is from right to left. This portion of the Bill Williams River is contained on the Monkeys Head, Arizona 7.5 min quadrangle.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
205
aceae). Gooddings willow at site 1 consisted of only large trees (≥15 m height) and many of these exhibited tip die-back where the upper portion of the trees consisted of dead wood. Gooddings willow at the other sites seemed healthy and sites also contained some smaller trees. Groundcover at site 1 consisted mostly of fallen leaves, while at sites 2 and 3 grasses and herbaceous plants such as clover (Melilotus) were often present. All three sites also contained open areas of sand. Surveys took place over 3–4 day periods in April 1998, March/April 1999, and March/April 2000 at site 1. Site 3 was added in March of 1999 and site 2 in April 2000. A total of 324 person hours were expended during this study, including a limited amount of time observing butterflies between sites.
timated. Types of nectar plants were also recorded. Although not a direct measure of nectar, a linear relationship between amount of nectar and number of inflorescences has been found in some studies (Holl, 1995). Sampling took place within a 5 m radius circle at disjunct points at timed intervals at each site. Data are recorded as number of inflorescences/5 m radius circle. Chi-square, t-tests, and ANOVA followed by LSD for multiple comparisons were used for statistical analysis of data. Data was tested for normality using the Shapiro–Wilk test and transformed (ln(X + 1) or arcsin squareroot (X)) if necessary. Measures of variance for mean values are reported as standard error.
2.2. Butterflies
3. Results
Adult Viceroys were netted, marked with a unique code using permanent marker (Ehrlich and Davidson, 1960), and released. No attempt was made to model population size using these limited data because of the bias which can be associated with marking effects (Gall, 1984). Population data in this study is presented as total number of unique individuals marked. Time, sex, condition (based on degree of wing damage), and behavior at the time of capture were noted, along with the capture location. Behaviors of adult butterflies were recorded as flying, perching, basking, nectaring, puddling, and mating. If a butterfly was observed nectaring, the nectar source was recorded. When multiple sites were studied, personnel were placed at each site. Capture locations were measured using a precision lightweight GPS receiver. Distance traveled per individual was calculated as the straight-line distance between the release point and the recaptured point. Overall weather conditions were always suitable (sunny and lack of precipitation) for butterfly activity during the study. Vegetation was sporadically examined for larval stages during butterfly surveys. Relative humidity (RH) and temperature were measured (Hanna HI 8564 portable thermo-hygrometer) as were light levels (Lux readings from a handheld Extech® light meter) approximately every 15 min during butterfly surveys. In March and April 2000, the number of flowers or inflorescences were also es-
During the three years of the study 303 individual butterflies were marked. Sex ratio was similar with 55% male and 45% female (Chi-square, P = 0.07500). Although butterflies were common at site 1 in 1998, they were rarely encountered there during the other years (Table 1). Coincident with this decline in numbers was the absence of water in the channel at site 1 (Fig. 1). The presence of surface water probably influences RH, and measurements in 2000 were lower at site 1 than at other sites (Table 2; March t-test, P < 0.0000; April ANOVA, P < 0.0000). Mean numbers of nectar resources were higher in ¯ = 24,517 ± 13,593, n = 20; site 2 April (site 1 X ¯ ¯ = 5853 ± 3897, X = 8526 ± 2156, n = 46; site 3 X ¯ n = 34) than in March (site 1 X = 244±157, n = 20; ¯ = 155 ± 72, n = 20). Sites did not differ site 3 X statistically in amount of nectar in March (t-test, ln transformed data, P = 0.6751), but there was a significant difference in April (ANOVA, ln transformed data, P = 0.0130) with site 3 containing significantly lower amounts of nectar (LSD test) than the other two sites, which were not significantly different. Gooddings willow and seep willow were the only nectar sources present in March. In April 98.7% of the nectar resources were tamarisk at site 1. Nectar resources at site 2 in April were numerically dominated by clover (64.7%). Tamarisk was also present at this site (26.5%) along with small amounts of seep willow, arrowweed, and water cress (Rorippa sp.). At site 3 in April, nectar
206
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
Table 1 Number of Western Viceroys captured and recaptured at sites on the Bill Williams River, Arizona Site
Date April 98
1 2 3
March 1999
April 1999
March 2000
April 2000
Na
Rb
N
R
N
R
N
R
N
R
58 (1.74) – –
21 – –
0 (0) – 33 (0.83)
0 – 10
6 (0.36) – 50 (1.19)
0 – 27
8 (0.48) – 46 (2.40)
1 – 19
1 (0.08) 38 (1.96) 46 (2.17)
0 25 29
The catch rate (number of unique individuals/person hour of collecting) is shown in parentheses. a Number of unique individuals marked. b Total number of recaptures.
resources were divided almost evenly between clover (50.4%) and tamarisk (47.9%). Small amounts of seep willow and Gooddings willow made up the rest of the nectar resources. Tamarisk and seep willow were the two plants most often used as nectar sources (46.9 and 42.9%, respectively) by Viceroys. Viceroys, on rare occasions, also used mesquite, Gooddings willow, arrowweed, and water cress for nectaring. Viceroys were not observed nectaring at clover which made up a large portion of nectar at sites 2 and 3. Most butterflies traveled relatively short distances between captures (n = 133, mean = 110 ± 23.5 m, three outliers excluded). The movement data, however, is biased toward lack of movement since the far-
ther a marked butterfly moves the less the chance of recapture. The relatively high numbers of recaptures (Table 1), however, suggest that many Viceroys limited movements to the scale of hundreds of meters. Three recaptured butterflies traveled much further. One traveled from site 2 to site 3 (908.6 m) on the same day. Another traveled from the point at which the river dried up in April 2000 to site 2 (1021.2 m), while the third made it from site 1 on April 19 (time 10:10) to site 2 on April 20 (time 15:17) for a straight-line distance of 2810 m. Females traveled significantly further than males (88.2 ± 11.8 m versus 68.6 ± 8.3 m, t-test, P < 0.0000, ln transformed data). Overall, Viceroys appeared to bias their movements to stay within riparian
Table 2 Mean temperature (◦ C) and relative humidity (RH) measured at Bill Williams butterfly survey sites 1998–2000 Year
Month
Parameter
Site 1
Site 2
Site 3
1998
April
Temperature (◦ C)
24.3 (0.5) n = 100 22.6 (1.6)
–
–
–
–
20.3 (0.8) n = 14 33.71a (1.7)
–
27.7 (0.7) n = 43 20.2b (1.3)
32.1 (1.8) n = 30 24.9a (4.0)
–
31.7 (0.5) n = 67 23.9a (1.6)
(◦ C)
27.5 (0.6) n = 45 22.1a (1.5)
– –
25.1 (0.6) n = 18 36.1b (1.4)
Temperature (◦ C)
28.9 (0.6) n = 37 18.5a (1.0)
29.9 (0.8) n = 30 28.1b (1.5)
29.4 (0.6) n = 42 31.9b (1.5)
RH 1999
March
Temperature
(◦ C)
RH April
Temperature (◦ C) RH
2000
March
Temperature RH
April
RH
–
Standard error in parentheses. Mean values for RH at the different sites were compared statistically (t-test or ANOVA) and similar superscript letters indicate non significant difference between sites. Superscript letters that differ indicate a significant difference at P < 0.05.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
Fig. 2. Percent of butterfly behaviors noted at flying, perching, and basking activities (a) and percent of butterflies noted at nectaring and puddling activities (b).
areas. This was especially apparent at site 3 which had a large open sandy area associated with it. Butterflies were only rarely found within this portion of the floodplain. Instead they closely followed a line of trees along the waterway. The hypothesis that butterflies were equally distributed between the sandy area
207
and riparian vegetation was rejected (Chi-square, P < 0.0000, sand habitat data points n = 54, riparian data points n = 180). Mean time between recaptures, with a single outlier excluded, was 16.6 ± 1.4 h. A single butterfly marked in March 2000 was recovered in April 2000, 36 days after the initial capture. We noted 424 incidences of behavior during the study. Because these were from visual observations, it is likely that noted behaviors were skewed towards flying, probably the most easily detected behavior. Indeed the largest proportion of behavior noted was flying at 45.0%. Perching was noted in 24.5% of the cases, while nectaring (12.7%) and puddling (10.4%) made up a smaller portion of the observed behaviors. Puddling was by both male and female singlets and was not a group behavior as observed with some other butterfly species. Basking was noted in 7.1% of the cases. Mating was observed only twice (between 11:00 and 13:00) while oviposition was not observed. Larvae and pupae were observed on Gooddings willow at site 3. Both flying and perching behavior appeared to follow a similar pattern (Fig. 2a), with most activity during the 3 h between 11:00 and 14:00. The hypothesis that these behaviors were equally distributed among times was rejected (Chi-square, flight P = 0.0040; perching P < 0.0000). Basking (Fig. 2a) also increased in frequency until midday, but then fell off rapidly after noon. The hypothesis that basking was equally distributed between morning hours and the
Fig. 3. Western Viceroy butterflies captured on an hourly basis (MST). Person hours spent for each time period were: 7:00, 4 h; 8:00, 13 h; 9:00, 31 h; 10:00, 31 h; 11:00, 27.5 h; 12:00, 28.5 h; 13:00, 30 h; 14:00, 29.5 h; 15:00, 35 h; 16:00, 32 h; 17:00, 11.5 h.
208
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
afternoon was rejected (Chi-square, P = 0.0002). Frequency of nectaring and puddling behavior appeared to be bimodal with a peak in the morning (9:00–11:00) and late afternoon (14:00–16:00) (Fig. 2b). No significant differences, however, were noted between times for these behaviors (Chi-square, nectaring P = 0.4402, puddling P = 0.1966). Overall, butterflies were more common at midday and
were not seen before 8:00 in the morning (Fig. 3). This peak in catch rate appeared to be associated with increased air temperature and a peak in light levels at midday (Fig. 4). Butterfly condition suggested that many individuals collected in March had just emerged. More individuals were categorized as “fresh” in March (42–72%) than in April (5–17%).
Fig. 4. Air temperature (a) and light levels (b) at Bill Williams over time during March and April 1998–2000.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
4. Discussion 4.1. Life history Information from this study and other published accounts (Scott, 1986; Emmel and Emmel, 1973) provides a picture of the life history of this species. It is likely that it persists through the winter in a larval stage, pupates early in the year and emerges as an adult in early March. Although larvae in many parts of the United States build a hibernacula in which they diapause during the winter months, the Viceroy’s at our study area may be similar to those in other warm parts of the butterfly’s range where diapause is bypassed (Williams and Platt, 1987). Several generations are possible per year and the adult probably flies throughout the spring and summer. Emmel and Emmel (1973) state that historically, Viceroy flights occurred from April through October along the Colorado River at Blythe, California. In an earlier study (Nelson and Andersen, 1999) the Viceroy was observed just upstream of site 1 through June but not in August or November. Their absence in August is likely due to drying of the river at downstream areas in late summer. Colonies at sites further upstream probably remain active, but this has not yet been documented. Gooddings willow was noted as a larval host plant at Bill Williams. Capture-mark-recapture data indicates the butterfly generally travels distances of hundreds of meters, with females traveling further than males. Scott (1975) suggests that perching and patrolling males such as the Viceroy are concentrated at favorable mating sites, while females are more widely distributed. Study of activity patterns in March and April found that basking took place during the first half of the day (8:00-noon) while flying and perching behaviors were most common around noon. Nectaring and puddling behaviors were distributed throughout the day. 4.2. River regulation and attributes needed for restoration of Viceroy populations Nelson and Andersen (1999), in a study of the butterflies of the lower Colorado River, suggested several possible reasons for the absence of phreatophyte dependent butterflies at revegetation sites along the
209
river, despite their presence at the Bill Williams tributary. The absence of these butterflies was associated with lower amounts of nectar resources, lowered water tables, and saline soils at the revegetated sites. To restore these resources and rehabilitate the Colorado River, interactions between the main channel, backwater, and floodplains are needed (e.g. Stanford et al., 1996). Recovery of natural flow is also needed to flush salts from the soil and to develop natural levels of groundwater and disturbance. Restoration to this point, despite the goal of recovering the ecology of the cottonwood/willow ecosystem, has not taken into account many of these hydrological attributes. Commonly, the intent has been to replace dense stands of exotic tamarisk with native plants without providing for surface water flows. Revegetation often occurs on a xeric part of the historic floodplain with pole plantings of Fremont cottonwood, which are then only watered for 2–3 years. After this, the irrigation is turned off and plantings are dependent upon groundwater. Most revegetation sites limit the number of plant species used and often Gooddings willow is not part of the plantings. This study of the Viceroy butterfly suggests that restoration as presently practiced will be ineffective in recovering this element of the historic (Emmel and Emmel, 1973) Colorado River butterfly fauna. This butterfly seemed dependent upon surface water flows as evidenced by the high percent of time spent in puddling. This behavior usually took place on bare moist soils next to the river. If this is a critical element of their natural history, none of the revegetation sites that we earlier observed (Nelson and Andersen, 1999) would provide this habitat. Most of the Colorado River revegetation sites are xeric while the few moist ones are covered with a dense layer of Bermuda grass (Cynodon dactylon). It is possible that the large floods which historically removed vegetation were necessary for maintaining this type of environment. Of interest is the observation that Viceroys were only found at site 1 in high numbers when water was present. Despite the high amounts of nectar found at this site in April 2000, water was absent and few Viceroys were present. Surface water at the Bill Williams may be more of a limiting factor than nectar resources. The moisture obtained from puddling may be very important to the Viceroy in this hot and dry climate. Launer et al. (1993) have noted the importance of moist soils, especially under
210
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
conditions of drought, for Lepidoptera conservation planning. Sodium ions obtained through puddling may also be important, and have been found to help induce mating behavior in some butterflies (Lederhouse et al., 1990) and may be an important way to replenish sodium reserves as butterflies age (e.g. Boggs and Jackson, 1991). The increased humidity at sites with surface flows may also positively affect Viceroy populations. Proper humidity is important in Lepidoptera for egg hatching success (Clark and Faeth, 1998), biomass gain and development rate in larvae (Shukla and Bhatnagar, 1994; Martinat and Allen, 1987), and mating for adults (Mbata, 1986). We found early life stages on Gooddings willow. However, other riparian obligate plants, such as Fremont cottonwood, are also listed as larval host plants (Scott, 1986). River regulation appears to have affected key habitat components needed for the Western Viceroy. The failure to find evidence of Western Viceroy colonies (e.g. Nelson and Andersen, 1999) that once occurred along the Colorado River near Blythe, California (Emmel and Emmel, 1973) is likely caused by habitat changes initiated by river regulation. In this region this subspecies of butterfly appears to be linked to fluvial and hydrological dynamics related to riverine disturbance regimes and integrates many habitat attributes related to natural flows in rivers. As such, it may be a useful indicator for determining riparian restoration success in the desert southwest of the United States. This butterfly requires obligate riparian plants, such as Gooddings willow, as a larval host plant; surface water flows for providing high humidity and for puddling at moist soils; occasional destructive flooding to clear areas for puddling; and high groundwater for nectar production. These resources should be in close proximity and would probably only be found in an area of high habitat heterogeneity with multiple successional stages present. Observations indicate that the Western Viceroy is unlikely to travel any distance from mesic areas, but that it can travel great distances along riparian corridors. We documented a single individual moving close to 3 km in ∼1.5 days, suggesting that Western Viceroys could easily disperse to new habitats that are contiguous within a riparian corridor. If Western Viceroys are to be a part of the fauna, restoration of the Colorado River should be based on
principles of contemporary river ecology (Stanford et al., 1996; Poff et al., 1997). This means that disturbance from flooding and lateral migration of the river is allowed to create a mosaic of habitats needed by this butterfly and other biodiversity elements (sensu Ward et al., 1999).
Acknowledgements I thank Nancy Gilbertson, Dick Gilbert, Kathleen Blair, and Tim Miller of the Bill Williams Wildlife Refuge for assistance, including the loan of vehicles. Rick Wydoski and Doug Andersen helped with butterfly collection and were critical to the project’s success. Rick Roline and Doug Andersen reviewed a draft of the manuscript and an anonymous reviewer helped in improving the manuscript. This project was supported by USGS-BRD and the Bureau of Reclamation (ER926). References Andersen, D.C., 1994. Are cicadas (Diceroprocta apache) both a “keystone” and a “critical- link” species in lower Colorado River riparian communities? Southwest. Nat. 39 (1), 26–33. Anderson, B.W., Ohmart, R.D., 1984. Avian use of revegetated riparian zones. In: Warner, R.E., Hendrix, K.M. (Eds.), California Riparian Systems: Ecology, Conservation, and Productive Management. University of California Press, Berkley, pp. 626– 631. Anderson, B.W., Ohmart, R.D., 1985. Managing riparian vegetation and wildlife along the Colorado River: synthesis of data, predictive models, and management. In: Johnson, R.R., Ziebell, C.D., Patton, D.R., Ffolliott, P.F., Hamre, R.H. (Eds.), Riparian Ecosystems and their Management: Reconciling Conflicting Uses. USDA Forest Service, General Technical Report RM-120, pp. 123–127. Boggs, C.L., Jackson, L.A., 1991. Mud puddling by butterflies is not a simple matter. Ecol. Entomol. 16, 123–127. Carlson, C.A., Muth, R.T., 1989. The Colorado River: lifeline of the American southwest. In: Dodge, D.P. (Ed.), Proceedings of the International Large River Symposium. Can. Spec. Publ. Fish. Aquat. Sci. 106, 220–239. Clark, B.R., Faeth, S.H., 1998. The evolution of egg clustering in butterflies: a test of the egg desiccation hypothesis. Evolutionary Ecol. 12 (5), 543–552. Collier, M., Webb, R.H., Schmidt, J.C., 1996. Dams and rivers: a primer on the downstream effects of dams. US Geological Survey, Circular 1126. Tucson, Arizona. Ehrlich, P.R., Davidson, S.E., 1960. Techniques for capture– recapture studies of Lepidoptera populations. J. Lepidopterists Soc. 14 (4), 227–229.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211 Emmel, T.C., Emmel, J.F., 1973. The butterflies of southern California. Nat. History Museum Los Angeles County: Sci. Ser. 26, 1–148. Gall, L.F., 1984. The effects of capturing and marking on subsequent activity in Boloria acrocnema (Lepidoptera: Nymphalidae), with a comparison of different numerical models that estimate population size. Biol. Conserv. 28, 139–154. Holl, K.D., 1995. Nectar resources and their influence on butterfly communities on reclaimed coal surface mines. Restoration Ecol. 3 (2), 76–85. Launer, A.E., Murphy, D.D., Boggs, C.L., Baughman, J.F., Weiss, S.B., Ehrlich, P.R., 1993. Puddling behavior by Bay checkerspot butterflies (Euphydryas editha bayensis). J. Res. Lepidoptera 32, 45–52. Lederhouse, R.C., Ayres, M.P., Scriber, J.M., 1990. Adult nutrition affects male virility in Papilio glaucus L. Functional Ecol. 4, 743–751. Martinat, P.J., Allen, D.C., 1987. Laboratory response of saddled prominent (Lepidoptera: Notodontidae) eggs and larvae to temperature and humidity: development and survivorship. Ann. Entomol. Soc. Am. 80 (5), 541–546. Mbata, G.N., 1986. Combined effect of temperature and relative humidity on mating activities and commencement of oviposition in Plodia interpunctella (Hubner) (Lepidoptera: Phycitidae). Insect Sci. Appl. 7 (5), 623–628. Moore, M.R., Mulville, A., Weinberg, M., 1996. Water allocation in the American west: endangered fish versus irrigated agriculture. Nat. Resources J. 36, 319–357. Mueller, G.A., Marsh, P.C., 2002. Lost, a desert river and its native fishes: a historical perspective of the lower Colorado River. Information and Technology Report. USGS/BRD/ITR2002-0010, Government Printing Office, Denver, CO. Nelson, S.M., Andersen, D.C., 1999. Butterfly (Papilionoidea and Hesperioidea) assemblages associated with natural, exotic, and restored riparian habitats along the lower Colorado River, USA. Regulated Rivers: Res. Manage. 15, 485–504.
211
Ohmart, R.D., Anderson, B.W., Hunter, W.C., 1988. The ecology of the lower Colorado River from Davis Dam to the Mexico–United States international boundary: a community profile. US Fish Wildl. Serv. Biol. Rep. 85 (7.19), 296. Pinkney, F.C., 1992. Revegetation and enhancement of riparian communities along the lower Colorado River. United States Department of the Interior, Bureau of Reclamation, Ecological Division, Denver Office, Denver, CO, 143 pp. Poff, N.L., Allan, J.D., Bain, M.B., Karr, J.R., Prestegaard, K.L., Richter, B.D., Sparks, R.E., Stromberg, J.C., 1997. The natural flow regime, a paradigm for river conservation and restoration. BioScience 47 (11), 769–784. Scott, J.A., 1975. Flight patterns among eleven species of diurnal Lepidoptera. Ecology 56, 1367–1377. Scott, J.A., 1986. The Butterflies of North America a Natural History and Field Guide. Stanford University Press, Stanford, CA. Shukla, V., Bhatnagar, S., 1994. Effect of humidity on growth and consumption of larvae of Danaus chrysippus feeding on Calotropis procera. Indian J. Ecol. 21 (1), 39–44. Stanford, J.A., Ward, J.V., Liss, W.J., Frissell, C.A., Williams, R.N., Lichatowich, J.A., Coutant, C.C., 1996. A general protocol for restoration of regulated rivers. Regulated Rivers: Res. Manage. 12 (4–5), 391–413. Thomas, J.A., 1991. Rare species conservation: case studies of European butterflies. In: Spellerberg, I.F., Goldsmith, F.B., Morris, M.G. (Eds.), Proceedings of the 29th Symposium of the British Ecological Society: Scientific Management of Temperate Communities. Blackwell Scientific Publications, Oxford, UK, pp. 149–197. Ward, J.V., Tockner, K., Schiemer, F., 1999. Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regulated Rivers: Res. Manage. 15, 125–139. Williams, T.F., Platt, A.P., 1987. Absence of diapause in a laboratory strain of the Florida Viceroy butterfly. Am. Midland Nat. 117 (2), 346–352.
The Western Viceroy butterfly (Nymphalidae: Limenitis archippus obsoleta): an indicator for riparian restoration in the arid southwestern United States? S. Mark Nelson∗ Ecological Research and Investigations Group, Technical Services Center, Bureau of Reclamation, Rm. 2010, Bldg. 56, P.O. Box 25007, Denver, CO 80225, USA Accepted 15 April 2003
Abstract Life history characteristics of the Western Viceroy (Limenitis archippus obsoleta), an obligate riparian nymphalid butterfly in the desert southwestern United States, are described and related to Colorado River riparian restoration efforts. Riverine disturbance regimes and associated fluvial and hydrological dynamics may provide resources critical to this butterfly. Puddling by adult butterflies may require flood-cleared surfaces and an obligate riparian plant, Gooddings willow, was a larval host plant. This butterfly needs a variety of resources that are only found in close proximity in naturally functioning riparian ecosystems. Habitat heterogeneity required for colony persistence depends largely upon the natural dynamic character of flowing water systems. Because of the links between this butterfly and riparian structure and function it may be a useful indicator for monitoring riparian ecosystem restoration in the area. © 2003 Elsevier Ltd. All rights reserved. Keywords: Bill Williams River; Colorado River; Indicator organisms; Limenitis archippus obsoleta; Riparian restoration; River regulation; Viceroy butterfly; Willow
1. Introduction Since the early to mid-20th century many dams, irrigation projects, and hydropower facilities have been built in the United States. Initially, downstream effects were of little concern, because these structures were thought to be environmentally benign elements of the landscape. Current literature, however, documents a host of ecological degradations concerning river regulation (Collier et al., 1996). Effects extend to both aquatic and terrestrial components of the ecosystem and may influence many miles of river. ∗ Tel.: +1-303-445-2225; fax: +1-303-445-6328. E-mail address: [email protected] (S.M. Nelson).
A series of dams in the arid southwestern United States have affected river ecology along the lower Colorado River, changing the river from one characterized by widely fluctuating flows and physico-chemical extremes to one of the most altered and intensively controlled systems in the United States (Carlson and Muth, 1989). The lower part of this river runs through one of the hottest and driest deserts on earth. Along the river at Parker, Arizona, the mean number of days per year with a maximum temperature ≥32 ◦ C is 178, and annual precipitation is 10.4 cm (Andersen, 1994). In association with river regulation, several aquatic taxa are now endangered or of concern (Moore et al., 1996) and terrestrial vegetation in the lower valleys has undergone dramatic changes. Documentation of historic
1470-160X/$ – see front matter © 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1470-160X(03)00044-X
204
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
conditions along the Colorado River is presented in Mueller and Marsh (2002). Forested bottomlands are presently diminished in area (Ohmart et al., 1988) with historic riparian areas becoming more desert-like. In response, restoration programs were initiated in the 1970s (Pinkney, 1992) and several areas planted with phreatophytic plants such as cottonwood and willow and the more xeric mesquite. Although studies of bird and mammal response to these revegetated areas were undertaken early on (Anderson and Ohmart, 1984, 1985), studies of invertebrates associated with revegetation sites have been limited until recently (e.g. Andersen, 1994; Nelson and Andersen, 1999). Nelson and Andersen (1999) found that, despite the presence of larval host plants at revegetated sites, obligate riparian butterflies were not found at any revegetated site and were also not found at sites where they had been documented in the 1930s around the time of the closure of Hoover Dam. The purpose of this study was to study the autecology of the Western Viceroy butterfly (Limenitis archippus obsoleta) against the background of riparian restoration. Autecological research often reveals subtle habitat requirements of butterflies (Thomas, 1991). Several elements might determine suitability of revegetated habitat for this butterfly. The ability of the Western Viceroy butterfly to use a particular habitat could be affected by movement patterns, behavior, larval host plant use, and nectar use. Many of these attributes are potentially affected by river regulation and restoration. Therefore, this butterfly may serve as an indicator of river ecosys-
tem condition and be useful in monitoring activities. Studies took place on the Bill Williams River, which contains a naturally functioning cottonwood/willow ecosystem. The Bill Williams River flows into Lake Havasu, formed by Parker Dam on the Colorado River. 2. Methods 2.1. Study areas Three sites were used for study on the Bill Williams River (Fig. 1). Site 1 was the furthest downstream. Water flow at this site was intermittent and only occurred in April of 1998 during the study period. Site 2 was 2–3 km upstream of site 1 and approximately 1 km downstream of site 3. Both upstream sites were in areas of perennial flow. All sites contained tamarisk (Tamarix ramosissima) and Gooddings willow (Salix gooddingii) in approximately equal amounts. Fremont cottonwood (Populus fremonti) at site 1 was limited to only a few large (20 m height) sentinel trees. Cottonwood was more common at sites 2 and 3 and consisted of both larger and smaller trees suggesting that cottonwood recruitment was occurring at these sites. Honey mesquite (Prosopis juliflora) was a minor element at all sites. Seepwillow (Baccharis salicifolia) and arrowweed (Tessaria sericea) were common at site 1 but found in lesser amounts at the other sites. Sites 2 and 3 were more mesic than site 1 and contained wetland plants such as cattails (Typha) and sedges (Cyper-
Fig. 1. Bill Williams River Viceroy butterfly survey sites. Direction of stream flow is from right to left. This portion of the Bill Williams River is contained on the Monkeys Head, Arizona 7.5 min quadrangle.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
205
aceae). Gooddings willow at site 1 consisted of only large trees (≥15 m height) and many of these exhibited tip die-back where the upper portion of the trees consisted of dead wood. Gooddings willow at the other sites seemed healthy and sites also contained some smaller trees. Groundcover at site 1 consisted mostly of fallen leaves, while at sites 2 and 3 grasses and herbaceous plants such as clover (Melilotus) were often present. All three sites also contained open areas of sand. Surveys took place over 3–4 day periods in April 1998, March/April 1999, and March/April 2000 at site 1. Site 3 was added in March of 1999 and site 2 in April 2000. A total of 324 person hours were expended during this study, including a limited amount of time observing butterflies between sites.
timated. Types of nectar plants were also recorded. Although not a direct measure of nectar, a linear relationship between amount of nectar and number of inflorescences has been found in some studies (Holl, 1995). Sampling took place within a 5 m radius circle at disjunct points at timed intervals at each site. Data are recorded as number of inflorescences/5 m radius circle. Chi-square, t-tests, and ANOVA followed by LSD for multiple comparisons were used for statistical analysis of data. Data was tested for normality using the Shapiro–Wilk test and transformed (ln(X + 1) or arcsin squareroot (X)) if necessary. Measures of variance for mean values are reported as standard error.
2.2. Butterflies
3. Results
Adult Viceroys were netted, marked with a unique code using permanent marker (Ehrlich and Davidson, 1960), and released. No attempt was made to model population size using these limited data because of the bias which can be associated with marking effects (Gall, 1984). Population data in this study is presented as total number of unique individuals marked. Time, sex, condition (based on degree of wing damage), and behavior at the time of capture were noted, along with the capture location. Behaviors of adult butterflies were recorded as flying, perching, basking, nectaring, puddling, and mating. If a butterfly was observed nectaring, the nectar source was recorded. When multiple sites were studied, personnel were placed at each site. Capture locations were measured using a precision lightweight GPS receiver. Distance traveled per individual was calculated as the straight-line distance between the release point and the recaptured point. Overall weather conditions were always suitable (sunny and lack of precipitation) for butterfly activity during the study. Vegetation was sporadically examined for larval stages during butterfly surveys. Relative humidity (RH) and temperature were measured (Hanna HI 8564 portable thermo-hygrometer) as were light levels (Lux readings from a handheld Extech® light meter) approximately every 15 min during butterfly surveys. In March and April 2000, the number of flowers or inflorescences were also es-
During the three years of the study 303 individual butterflies were marked. Sex ratio was similar with 55% male and 45% female (Chi-square, P = 0.07500). Although butterflies were common at site 1 in 1998, they were rarely encountered there during the other years (Table 1). Coincident with this decline in numbers was the absence of water in the channel at site 1 (Fig. 1). The presence of surface water probably influences RH, and measurements in 2000 were lower at site 1 than at other sites (Table 2; March t-test, P < 0.0000; April ANOVA, P < 0.0000). Mean numbers of nectar resources were higher in ¯ = 24,517 ± 13,593, n = 20; site 2 April (site 1 X ¯ ¯ = 5853 ± 3897, X = 8526 ± 2156, n = 46; site 3 X ¯ n = 34) than in March (site 1 X = 244±157, n = 20; ¯ = 155 ± 72, n = 20). Sites did not differ site 3 X statistically in amount of nectar in March (t-test, ln transformed data, P = 0.6751), but there was a significant difference in April (ANOVA, ln transformed data, P = 0.0130) with site 3 containing significantly lower amounts of nectar (LSD test) than the other two sites, which were not significantly different. Gooddings willow and seep willow were the only nectar sources present in March. In April 98.7% of the nectar resources were tamarisk at site 1. Nectar resources at site 2 in April were numerically dominated by clover (64.7%). Tamarisk was also present at this site (26.5%) along with small amounts of seep willow, arrowweed, and water cress (Rorippa sp.). At site 3 in April, nectar
206
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
Table 1 Number of Western Viceroys captured and recaptured at sites on the Bill Williams River, Arizona Site
Date April 98
1 2 3
March 1999
April 1999
March 2000
April 2000
Na
Rb
N
R
N
R
N
R
N
R
58 (1.74) – –
21 – –
0 (0) – 33 (0.83)
0 – 10
6 (0.36) – 50 (1.19)
0 – 27
8 (0.48) – 46 (2.40)
1 – 19
1 (0.08) 38 (1.96) 46 (2.17)
0 25 29
The catch rate (number of unique individuals/person hour of collecting) is shown in parentheses. a Number of unique individuals marked. b Total number of recaptures.
resources were divided almost evenly between clover (50.4%) and tamarisk (47.9%). Small amounts of seep willow and Gooddings willow made up the rest of the nectar resources. Tamarisk and seep willow were the two plants most often used as nectar sources (46.9 and 42.9%, respectively) by Viceroys. Viceroys, on rare occasions, also used mesquite, Gooddings willow, arrowweed, and water cress for nectaring. Viceroys were not observed nectaring at clover which made up a large portion of nectar at sites 2 and 3. Most butterflies traveled relatively short distances between captures (n = 133, mean = 110 ± 23.5 m, three outliers excluded). The movement data, however, is biased toward lack of movement since the far-
ther a marked butterfly moves the less the chance of recapture. The relatively high numbers of recaptures (Table 1), however, suggest that many Viceroys limited movements to the scale of hundreds of meters. Three recaptured butterflies traveled much further. One traveled from site 2 to site 3 (908.6 m) on the same day. Another traveled from the point at which the river dried up in April 2000 to site 2 (1021.2 m), while the third made it from site 1 on April 19 (time 10:10) to site 2 on April 20 (time 15:17) for a straight-line distance of 2810 m. Females traveled significantly further than males (88.2 ± 11.8 m versus 68.6 ± 8.3 m, t-test, P < 0.0000, ln transformed data). Overall, Viceroys appeared to bias their movements to stay within riparian
Table 2 Mean temperature (◦ C) and relative humidity (RH) measured at Bill Williams butterfly survey sites 1998–2000 Year
Month
Parameter
Site 1
Site 2
Site 3
1998
April
Temperature (◦ C)
24.3 (0.5) n = 100 22.6 (1.6)
–
–
–
–
20.3 (0.8) n = 14 33.71a (1.7)
–
27.7 (0.7) n = 43 20.2b (1.3)
32.1 (1.8) n = 30 24.9a (4.0)
–
31.7 (0.5) n = 67 23.9a (1.6)
(◦ C)
27.5 (0.6) n = 45 22.1a (1.5)
– –
25.1 (0.6) n = 18 36.1b (1.4)
Temperature (◦ C)
28.9 (0.6) n = 37 18.5a (1.0)
29.9 (0.8) n = 30 28.1b (1.5)
29.4 (0.6) n = 42 31.9b (1.5)
RH 1999
March
Temperature
(◦ C)
RH April
Temperature (◦ C) RH
2000
March
Temperature RH
April
RH
–
Standard error in parentheses. Mean values for RH at the different sites were compared statistically (t-test or ANOVA) and similar superscript letters indicate non significant difference between sites. Superscript letters that differ indicate a significant difference at P < 0.05.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
Fig. 2. Percent of butterfly behaviors noted at flying, perching, and basking activities (a) and percent of butterflies noted at nectaring and puddling activities (b).
areas. This was especially apparent at site 3 which had a large open sandy area associated with it. Butterflies were only rarely found within this portion of the floodplain. Instead they closely followed a line of trees along the waterway. The hypothesis that butterflies were equally distributed between the sandy area
207
and riparian vegetation was rejected (Chi-square, P < 0.0000, sand habitat data points n = 54, riparian data points n = 180). Mean time between recaptures, with a single outlier excluded, was 16.6 ± 1.4 h. A single butterfly marked in March 2000 was recovered in April 2000, 36 days after the initial capture. We noted 424 incidences of behavior during the study. Because these were from visual observations, it is likely that noted behaviors were skewed towards flying, probably the most easily detected behavior. Indeed the largest proportion of behavior noted was flying at 45.0%. Perching was noted in 24.5% of the cases, while nectaring (12.7%) and puddling (10.4%) made up a smaller portion of the observed behaviors. Puddling was by both male and female singlets and was not a group behavior as observed with some other butterfly species. Basking was noted in 7.1% of the cases. Mating was observed only twice (between 11:00 and 13:00) while oviposition was not observed. Larvae and pupae were observed on Gooddings willow at site 3. Both flying and perching behavior appeared to follow a similar pattern (Fig. 2a), with most activity during the 3 h between 11:00 and 14:00. The hypothesis that these behaviors were equally distributed among times was rejected (Chi-square, flight P = 0.0040; perching P < 0.0000). Basking (Fig. 2a) also increased in frequency until midday, but then fell off rapidly after noon. The hypothesis that basking was equally distributed between morning hours and the
Fig. 3. Western Viceroy butterflies captured on an hourly basis (MST). Person hours spent for each time period were: 7:00, 4 h; 8:00, 13 h; 9:00, 31 h; 10:00, 31 h; 11:00, 27.5 h; 12:00, 28.5 h; 13:00, 30 h; 14:00, 29.5 h; 15:00, 35 h; 16:00, 32 h; 17:00, 11.5 h.
208
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
afternoon was rejected (Chi-square, P = 0.0002). Frequency of nectaring and puddling behavior appeared to be bimodal with a peak in the morning (9:00–11:00) and late afternoon (14:00–16:00) (Fig. 2b). No significant differences, however, were noted between times for these behaviors (Chi-square, nectaring P = 0.4402, puddling P = 0.1966). Overall, butterflies were more common at midday and
were not seen before 8:00 in the morning (Fig. 3). This peak in catch rate appeared to be associated with increased air temperature and a peak in light levels at midday (Fig. 4). Butterfly condition suggested that many individuals collected in March had just emerged. More individuals were categorized as “fresh” in March (42–72%) than in April (5–17%).
Fig. 4. Air temperature (a) and light levels (b) at Bill Williams over time during March and April 1998–2000.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
4. Discussion 4.1. Life history Information from this study and other published accounts (Scott, 1986; Emmel and Emmel, 1973) provides a picture of the life history of this species. It is likely that it persists through the winter in a larval stage, pupates early in the year and emerges as an adult in early March. Although larvae in many parts of the United States build a hibernacula in which they diapause during the winter months, the Viceroy’s at our study area may be similar to those in other warm parts of the butterfly’s range where diapause is bypassed (Williams and Platt, 1987). Several generations are possible per year and the adult probably flies throughout the spring and summer. Emmel and Emmel (1973) state that historically, Viceroy flights occurred from April through October along the Colorado River at Blythe, California. In an earlier study (Nelson and Andersen, 1999) the Viceroy was observed just upstream of site 1 through June but not in August or November. Their absence in August is likely due to drying of the river at downstream areas in late summer. Colonies at sites further upstream probably remain active, but this has not yet been documented. Gooddings willow was noted as a larval host plant at Bill Williams. Capture-mark-recapture data indicates the butterfly generally travels distances of hundreds of meters, with females traveling further than males. Scott (1975) suggests that perching and patrolling males such as the Viceroy are concentrated at favorable mating sites, while females are more widely distributed. Study of activity patterns in March and April found that basking took place during the first half of the day (8:00-noon) while flying and perching behaviors were most common around noon. Nectaring and puddling behaviors were distributed throughout the day. 4.2. River regulation and attributes needed for restoration of Viceroy populations Nelson and Andersen (1999), in a study of the butterflies of the lower Colorado River, suggested several possible reasons for the absence of phreatophyte dependent butterflies at revegetation sites along the
209
river, despite their presence at the Bill Williams tributary. The absence of these butterflies was associated with lower amounts of nectar resources, lowered water tables, and saline soils at the revegetated sites. To restore these resources and rehabilitate the Colorado River, interactions between the main channel, backwater, and floodplains are needed (e.g. Stanford et al., 1996). Recovery of natural flow is also needed to flush salts from the soil and to develop natural levels of groundwater and disturbance. Restoration to this point, despite the goal of recovering the ecology of the cottonwood/willow ecosystem, has not taken into account many of these hydrological attributes. Commonly, the intent has been to replace dense stands of exotic tamarisk with native plants without providing for surface water flows. Revegetation often occurs on a xeric part of the historic floodplain with pole plantings of Fremont cottonwood, which are then only watered for 2–3 years. After this, the irrigation is turned off and plantings are dependent upon groundwater. Most revegetation sites limit the number of plant species used and often Gooddings willow is not part of the plantings. This study of the Viceroy butterfly suggests that restoration as presently practiced will be ineffective in recovering this element of the historic (Emmel and Emmel, 1973) Colorado River butterfly fauna. This butterfly seemed dependent upon surface water flows as evidenced by the high percent of time spent in puddling. This behavior usually took place on bare moist soils next to the river. If this is a critical element of their natural history, none of the revegetation sites that we earlier observed (Nelson and Andersen, 1999) would provide this habitat. Most of the Colorado River revegetation sites are xeric while the few moist ones are covered with a dense layer of Bermuda grass (Cynodon dactylon). It is possible that the large floods which historically removed vegetation were necessary for maintaining this type of environment. Of interest is the observation that Viceroys were only found at site 1 in high numbers when water was present. Despite the high amounts of nectar found at this site in April 2000, water was absent and few Viceroys were present. Surface water at the Bill Williams may be more of a limiting factor than nectar resources. The moisture obtained from puddling may be very important to the Viceroy in this hot and dry climate. Launer et al. (1993) have noted the importance of moist soils, especially under
210
S.M. Nelson / Ecological Indicators 3 (2003) 203–211
conditions of drought, for Lepidoptera conservation planning. Sodium ions obtained through puddling may also be important, and have been found to help induce mating behavior in some butterflies (Lederhouse et al., 1990) and may be an important way to replenish sodium reserves as butterflies age (e.g. Boggs and Jackson, 1991). The increased humidity at sites with surface flows may also positively affect Viceroy populations. Proper humidity is important in Lepidoptera for egg hatching success (Clark and Faeth, 1998), biomass gain and development rate in larvae (Shukla and Bhatnagar, 1994; Martinat and Allen, 1987), and mating for adults (Mbata, 1986). We found early life stages on Gooddings willow. However, other riparian obligate plants, such as Fremont cottonwood, are also listed as larval host plants (Scott, 1986). River regulation appears to have affected key habitat components needed for the Western Viceroy. The failure to find evidence of Western Viceroy colonies (e.g. Nelson and Andersen, 1999) that once occurred along the Colorado River near Blythe, California (Emmel and Emmel, 1973) is likely caused by habitat changes initiated by river regulation. In this region this subspecies of butterfly appears to be linked to fluvial and hydrological dynamics related to riverine disturbance regimes and integrates many habitat attributes related to natural flows in rivers. As such, it may be a useful indicator for determining riparian restoration success in the desert southwest of the United States. This butterfly requires obligate riparian plants, such as Gooddings willow, as a larval host plant; surface water flows for providing high humidity and for puddling at moist soils; occasional destructive flooding to clear areas for puddling; and high groundwater for nectar production. These resources should be in close proximity and would probably only be found in an area of high habitat heterogeneity with multiple successional stages present. Observations indicate that the Western Viceroy is unlikely to travel any distance from mesic areas, but that it can travel great distances along riparian corridors. We documented a single individual moving close to 3 km in ∼1.5 days, suggesting that Western Viceroys could easily disperse to new habitats that are contiguous within a riparian corridor. If Western Viceroys are to be a part of the fauna, restoration of the Colorado River should be based on
principles of contemporary river ecology (Stanford et al., 1996; Poff et al., 1997). This means that disturbance from flooding and lateral migration of the river is allowed to create a mosaic of habitats needed by this butterfly and other biodiversity elements (sensu Ward et al., 1999).
Acknowledgements I thank Nancy Gilbertson, Dick Gilbert, Kathleen Blair, and Tim Miller of the Bill Williams Wildlife Refuge for assistance, including the loan of vehicles. Rick Wydoski and Doug Andersen helped with butterfly collection and were critical to the project’s success. Rick Roline and Doug Andersen reviewed a draft of the manuscript and an anonymous reviewer helped in improving the manuscript. This project was supported by USGS-BRD and the Bureau of Reclamation (ER926). References Andersen, D.C., 1994. Are cicadas (Diceroprocta apache) both a “keystone” and a “critical- link” species in lower Colorado River riparian communities? Southwest. Nat. 39 (1), 26–33. Anderson, B.W., Ohmart, R.D., 1984. Avian use of revegetated riparian zones. In: Warner, R.E., Hendrix, K.M. (Eds.), California Riparian Systems: Ecology, Conservation, and Productive Management. University of California Press, Berkley, pp. 626– 631. Anderson, B.W., Ohmart, R.D., 1985. Managing riparian vegetation and wildlife along the Colorado River: synthesis of data, predictive models, and management. In: Johnson, R.R., Ziebell, C.D., Patton, D.R., Ffolliott, P.F., Hamre, R.H. (Eds.), Riparian Ecosystems and their Management: Reconciling Conflicting Uses. USDA Forest Service, General Technical Report RM-120, pp. 123–127. Boggs, C.L., Jackson, L.A., 1991. Mud puddling by butterflies is not a simple matter. Ecol. Entomol. 16, 123–127. Carlson, C.A., Muth, R.T., 1989. The Colorado River: lifeline of the American southwest. In: Dodge, D.P. (Ed.), Proceedings of the International Large River Symposium. Can. Spec. Publ. Fish. Aquat. Sci. 106, 220–239. Clark, B.R., Faeth, S.H., 1998. The evolution of egg clustering in butterflies: a test of the egg desiccation hypothesis. Evolutionary Ecol. 12 (5), 543–552. Collier, M., Webb, R.H., Schmidt, J.C., 1996. Dams and rivers: a primer on the downstream effects of dams. US Geological Survey, Circular 1126. Tucson, Arizona. Ehrlich, P.R., Davidson, S.E., 1960. Techniques for capture– recapture studies of Lepidoptera populations. J. Lepidopterists Soc. 14 (4), 227–229.
S.M. Nelson / Ecological Indicators 3 (2003) 203–211 Emmel, T.C., Emmel, J.F., 1973. The butterflies of southern California. Nat. History Museum Los Angeles County: Sci. Ser. 26, 1–148. Gall, L.F., 1984. The effects of capturing and marking on subsequent activity in Boloria acrocnema (Lepidoptera: Nymphalidae), with a comparison of different numerical models that estimate population size. Biol. Conserv. 28, 139–154. Holl, K.D., 1995. Nectar resources and their influence on butterfly communities on reclaimed coal surface mines. Restoration Ecol. 3 (2), 76–85. Launer, A.E., Murphy, D.D., Boggs, C.L., Baughman, J.F., Weiss, S.B., Ehrlich, P.R., 1993. Puddling behavior by Bay checkerspot butterflies (Euphydryas editha bayensis). J. Res. Lepidoptera 32, 45–52. Lederhouse, R.C., Ayres, M.P., Scriber, J.M., 1990. Adult nutrition affects male virility in Papilio glaucus L. Functional Ecol. 4, 743–751. Martinat, P.J., Allen, D.C., 1987. Laboratory response of saddled prominent (Lepidoptera: Notodontidae) eggs and larvae to temperature and humidity: development and survivorship. Ann. Entomol. Soc. Am. 80 (5), 541–546. Mbata, G.N., 1986. Combined effect of temperature and relative humidity on mating activities and commencement of oviposition in Plodia interpunctella (Hubner) (Lepidoptera: Phycitidae). Insect Sci. Appl. 7 (5), 623–628. Moore, M.R., Mulville, A., Weinberg, M., 1996. Water allocation in the American west: endangered fish versus irrigated agriculture. Nat. Resources J. 36, 319–357. Mueller, G.A., Marsh, P.C., 2002. Lost, a desert river and its native fishes: a historical perspective of the lower Colorado River. Information and Technology Report. USGS/BRD/ITR2002-0010, Government Printing Office, Denver, CO. Nelson, S.M., Andersen, D.C., 1999. Butterfly (Papilionoidea and Hesperioidea) assemblages associated with natural, exotic, and restored riparian habitats along the lower Colorado River, USA. Regulated Rivers: Res. Manage. 15, 485–504.
211
Ohmart, R.D., Anderson, B.W., Hunter, W.C., 1988. The ecology of the lower Colorado River from Davis Dam to the Mexico–United States international boundary: a community profile. US Fish Wildl. Serv. Biol. Rep. 85 (7.19), 296. Pinkney, F.C., 1992. Revegetation and enhancement of riparian communities along the lower Colorado River. United States Department of the Interior, Bureau of Reclamation, Ecological Division, Denver Office, Denver, CO, 143 pp. Poff, N.L., Allan, J.D., Bain, M.B., Karr, J.R., Prestegaard, K.L., Richter, B.D., Sparks, R.E., Stromberg, J.C., 1997. The natural flow regime, a paradigm for river conservation and restoration. BioScience 47 (11), 769–784. Scott, J.A., 1975. Flight patterns among eleven species of diurnal Lepidoptera. Ecology 56, 1367–1377. Scott, J.A., 1986. The Butterflies of North America a Natural History and Field Guide. Stanford University Press, Stanford, CA. Shukla, V., Bhatnagar, S., 1994. Effect of humidity on growth and consumption of larvae of Danaus chrysippus feeding on Calotropis procera. Indian J. Ecol. 21 (1), 39–44. Stanford, J.A., Ward, J.V., Liss, W.J., Frissell, C.A., Williams, R.N., Lichatowich, J.A., Coutant, C.C., 1996. A general protocol for restoration of regulated rivers. Regulated Rivers: Res. Manage. 12 (4–5), 391–413. Thomas, J.A., 1991. Rare species conservation: case studies of European butterflies. In: Spellerberg, I.F., Goldsmith, F.B., Morris, M.G. (Eds.), Proceedings of the 29th Symposium of the British Ecological Society: Scientific Management of Temperate Communities. Blackwell Scientific Publications, Oxford, UK, pp. 149–197. Ward, J.V., Tockner, K., Schiemer, F., 1999. Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regulated Rivers: Res. Manage. 15, 125–139. Williams, T.F., Platt, A.P., 1987. Absence of diapause in a laboratory strain of the Florida Viceroy butterfly. Am. Midland Nat. 117 (2), 346–352.