Report to the Maine Center for Disease Control and Prevention on Evaluation of Tick Surveillance in Maine, 1988-2010, related to CDC/NCEH project Human Health Effects of Climate Change, Funding Opportunity Number CDC-RFA-EH101006 Vector-borne Disease Laboratory, Maine Medical Center Research Institute, 75 John Roberts Road, Suite 9B, South Portland, ME. March 15, 2011. The Service Specifications listed in Rider A of Maine Medical Center’s Agreement with DHHS call for MMC to: 1. Describe and evaluate Ixodes scapularis (deer or black-legged tick) surveillance data from 1988 to 2010; 2. Expand existing tick surveillance to increase geographic diversity of tick dragging sites as well as increased presence at white-tailed deer (Odocoileus virgnianus) registration stations; 3. Test submitted and collected ticks for tick-borne diseases (≥ 150 for Borrelia spp. by direct fluorescent antibody (DFA) and ≥ 25 for the agents of Lyme disease (Borrelia burgdorferi), anaplasmosis (Anaplasma phagocytophilum) and babesiosis (Babesia microti) by polymerase chain reaction (PCR); 4. Analyze and compare tick surveillance data and environmental indicators to identify significant associations; 5. Analyze and compare tick surveillance data and climate indicators to identify significant climate factors associated with potential tick reproduction. 1. Evaluation of I. scapularis surveillance. A report responding to the first objective was produced in March 2011. The following report responds to the remaining objectives. 2. Expansion of I. scapularis surveillance. Submissions program, general public--. Since 1988, The Vector-borne Disease Laboratory has offered free tick identification to Maine residents, which has allowed us 1 to map the distribution of ticks over time (Figure 1). During this project year, attempts were made to increase the number and geographic spread of tick submissions by increasing public awareness of the program through two press releases issued by the Maine CDC to statewide newspapers, with emphasis on the colder northern six counties: Aroostook, Franklin, Penobscot, Piscataquis, Somerset, and Washington 1 . Unfortunately, we have no knowledge of which papers published the announcements, or of how many times Figure 1. Maine I. scapularis submissions by town,1989-2010. they appeared. The first press release (Appendix I) was issued October 27, 2010, too late to coincide well with the fall adult I. scapularis peak, particularly in the northern counties. October and November 2010 adult tick submissions (non-veterinarian) from these six northern counties numbered 64, compared to 35, 39, 55, 68, and 43, from 2005 through 2009. Given the gradual increase in adult I. scapularis submitted from northern Maine in recent years, it seems unlikely the fall press release increased submissions beyond what would have been submitted without the press release. The second press release was issued April 14, 2001, before the start of the nymphal season. Twelve nymphs from the northern six counties were submitted in summer 2011 compared to 3, 5, 5, 10, 3, and 3 from 2005 through 2010. Thus there was no discernable increase in either adult or nymphal submissions as a result of the public service announcements. To encourage the public to send in ticks from emergent areas, we recommend that posters and stacks of informational pamphlets be provided at locations such as 1 We have found the most practical way to view differences within the state with regard to Lyme disease, entomological risk, and surveillance is to divide it into six northern and 10 southern counties, even though several counties are long from north-to-south (e.g. Penobscot) and Washington is an eastern county. 2 supermarkets, hardware stores, hunting supply outlets, town offices in population centers in Maine north of the city of Bangor. A single exposure provided passively by local newspapers appears ineffective; public and private funds should be sought to provide sustained coverage, particularly from early April through mid-July, and again at the beginning of October, incorporating newspapers, radio, television and the internet. Submissions program, veterinarians--. The second initiative was to increase submissions from veterinarians, particularly from the northern six counties. A letter (Appendix II), asking veterinarians to submit ticks removed from dogs and other animals to our lab, was distributed as an e-mail attachment to all clinics on the address list of the Maine Veterinary Medical Association. The solicitation was sent on October 13, 2010 Ten clinics (in Fort Kent, Caribou, Houlton, Sullivan, Veazie, Orono, Brewer, Rumford, Skowhegan and Norway) responded, and each was provided with vials, instructions, and postage-paid return mailing envelopes. Six clinics submitted 36 ticks, from two towns in the northern counties (Dover-Foxcroft, Veazie) and from four in the southern counties (Belfast, Blue Hill, Gouldsboro, and Norway). However by the time this solicitation reached veterinarians in the northern counties, tick activity was probably limited by cold weather. A second solicitation was sent on April 14, 2011, after which five ticks were submitted by two northern county clinics in Bangor and Medway and one southern county clinic in Gouldsboro. Over the years, veterinarians statewide have generously supported our requests for ticks. Our solicitation to veterinary clinics resulted in a small increase in veterinary tick submissions, including live ticks suitable for testing for Bb. If the goal is to increase veterinary submissions, consideration must be given to the priorities of busy veterinarians. If a larger increase in veterinary tick submissions is desired, a more concerted solicitation effort is needed in emerging areas. We have offered free return postage to veterinarians, but on a short-term, funded project basis, a per-submission monetary incentive to cover the administrative cost of reporting the data could also be offered. The advent of the IDEXX 4DX test has greatly simplified and expanded canine serosurveys, and informed us of transmission risk statewide (e.g. Stone et al. 2005, Rand 3 et al. 2011). Among canine serosurveys conducted by our laboratory over the last 22 years (1989, 1992, 1996, 2003, 2007. 2009), some included a per-dog monetary incentive for reporting test results. Continued tick submissions by veterinarians is prudent, but a program to track B. burgdorferi (Bb) and A. phagocytophilum (Ap) antibody positivity in dogs using the 4DX tests at sentinel veterinary clinics might be a more efficient proxy to predicting human Lyme cases in Maine than would testing veterinarian-submitted ticks. Field surveillance--. Beginning in 2010, with a grant from the Elmina B. Sewall Foundation, we initiated a program to establish satellite survey teams to increase field surveillance for I. scapularis, the vector tick of Lyme disease, anaplasmosis, and babesiosis, in parts of Maine which have been logistically difficult for our field staff to reach. Two teams were established in 2010 to flag ticks from vegetation and to collect ticks from hunter-killed deer at deer tagging stations in the fall, one at Unity College and one at the University of Maine/Fort Kent. After training at our laboratory and in the field, surveyors established transects at local sites from which they collected and sent ticks to our laboratory for identification (Clifford et al. 1961, Keirans and Litwak 1989, Durden and Keirans 1996) and testing for Borrelia by DFA. In the present project, to obtain baseline data from across the state, our objective has been to create 3 additional satellite survey teams: in Farmington, Machias, and on tribal lands. Success was mixed. We were able to establish surveillance in Farmington, but staff was not available at the University of Maine/Machias, and initial intentions of the tribes were not sustained. To mitigate this, lab personnel traveled to flag geographically diverse sites in Knox, Waldo, Washington, Penobscot, and Piscataquis Counties. Flagging results are presented in section 3. Tests for Tick-borne Diseases. Deer registration stations--. Since deer are the preferred host for adult I. scapularis, and the peak of the adult I. scapularis season coincides with the first two weeks of the annual firearms hunting season in November, collecting ticks from the hides of deer brought to tagging stations has been an effective method for us to assess I. 4 scapularis distribution throughout the state (Smith et al. 1990, Rand et al. 2003). Volunteers have included students and teachers from colleges and the universities, notably Unity College, the campuses of the University of Maine at Orono and Fort Kent, the University of Southern Maine, and wildlife specialists of the Maine Department of Fisheries and Wildlife and the U.S. Department of Agriculture. Tagging station surveys to collect ticks have been conducted several times by our laboratory, notably from 19881990, 1998-1999, and in 2007. The 2010 deer hunting season was completed before the award of this grant. Deer registration stations were visited by laboratory staff, volunteers, and members of the satellite teams, but for the earlier priority of collecting blood samples for EEE surveillance, a sometimes hectic procedure requiring dedication of two individuals to a single purpose. Ticks will be collected from deer brought to tagging stations in 2011. 3. Tests for Tick-borne Diseases. Direct flourescent microscopy (DFA)--. The prescribed goal was to test 150 submitted or field-collected I. scapularis by DFA for presence of Borrelia. In all, 408 were tested, 24 from veterinary submissions (Table 1) and 384 from field collections Table 2). Eight of the veterinarian-submitted ticks were positive (33%, Table 1). 5 Table 1. Deer ticks (Ixodes scapularis ) submitted by veterinarians after efforts to expand the deer tick a surveillance program in late 2010 and early 2011. Live ticks in good condition were tested by DFA for Borrelia . Submitter Year Veterinarian 2010 Town Host Stage Piscataquis Milo Parkman Corinth Orono Orono Blue Hill Brooklin Brooklin Brooksville Franklin Penobscot Sullivan Otisfield Belfast Casco Harrison Brewer East Millinocket Glenburn Cat Dog Dog Cat Dog Dog Cat Dog Dog Cat Cat Dog Dog Dog Cat Cat Dog Dog Dog Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Overall: Penobscot Hancock Oxford Waldo Cumberland 2011 b County Penobscot a direct flourescent antibody test b There were no travel histories associated with any of these hosts. Submitted + Tested 1 1 1 3 3 1 2 4 1 1 2 2 1 9 1 1 1 1 1 37 1 0 1 0 0 0 0 2 1 1 1 1 0 0 8 0 1 1 1 2 1 1 0 1 0 2 1 1 9 1 0 1 0 1 24 %+ 33.3 A total of 192 adults, 283 nymphs, and 55 larvae were flagged in 91.8hr of flagging (Table 2). Zero adults and four nymphs were flagged from northern Maine, none of which was from Aroostook County. Of 58 tested adults, 62.3% were positive, and of 280 nymphs, 25.0% were positive for Borrelia (Table 1). To put the 2010-11 testing results in perspective, since 1989, we have tested 11,442 adult field-collected I. scapularis of which 5,218 (45.6%) were positive. Of 2,553 field-collected nymphs tested, 715 positive (28.0%) were positive. 6 a Table 2. Deer ticks (Ixodes scapularis ) flagged and tested by DFA for Borrelia burgdoferi in 2011. Flagging Adults Larvae Nymphs County Town Samples Hr Adults Larvae Nymphs per hour per hour per hour Aroostook Fort Kent Madawaska Stockholm Piscataquis Blanchard Twp Dover-Foxcroft Parkman Sangerville Penobscot Bangor Corinna Garland Washington Cutler Edmunds Twp Steuben Waldo Belfast Islesboro Knox Montville Kennebec Sidney Vassalboro Waterville Knox Rockland Lincoln Damariscotta Cumberland Cape Elizabeth York Kittery Parsonsfield Wells Overall: a direct flourescent antibody test 1 5 1 1 2 1 1 1 1 1 1 4 1 1 2 1 1 3 2 1 1 1 2 2 1 3 0.83 6.72 0.5 1 1.83 1 0.5 3.5 0.75 1 1 5.17 3.5 1.5 7.58 3.17 1 7.5 3.58 3 2.5 1 8 6.5 4.58 14.6 91.8 0 0 0 0 0 0 0 0 0 0 0 0 0 1 6 0 0 10 13 2 13 3 21 11 0 112 192 0 0 0 0 4 0 2 15 0 0 0 0 11 0 0 4 0 10 0 0 0 0 0 0 0 9 55 0 0 0 1 0 0 2 1 0 0 0 0 4 4 139 0 12 43 1 0 5 2 10 30 0 29 283 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.7 0.8 0.0 0.0 1.3 3.6 0.7 5.2 3.0 2.6 1.7 0.0 7.7 1.0 0.0 0.0 0.0 0.0 2.2 0.0 4.0 4.3 0.0 0.0 0.0 0.0 3.1 0.0 0.0 1.3 0.0 1.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.6 0.6 0.0 0.0 0.0 1.0 0.0 0.0 4.0 0.3 0.0 0.0 0.0 0.0 1.1 2.7 18.3 0.0 12.0 5.7 0.3 0.0 2.0 2.0 1.3 4.6 0.0 2.0 2.2 Positivity Adults + Tested 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 3 0 0 7 1 14 0 0 5 33 0 0 0 0 0 0 0 0 0 0 0 0 0 0 5 0 0 6 0 0 11 3 17 1 0 10 53 % 60.0 50.0 63.6 33.3 82.4 0.0 50.0 62.3 + Nymphs T ested 0 0 0 0 0 0 0 0 0 0 0 0 0 2 44 0 0 7 1 0 1 1 4 4 0 6 70 0 0 0 0 0 0 0 0 0 0 0 0 4 4 136 0 13 44 4 0 5 2 12 27 0 29 280 % 0.0 50.0 32.4 0.0 15.9 25.0 20.0 50.0 33.3 14.8 20.7 25.0 Polymerase chain reaction (PCR)--. The goal was to test 25 I. scapularis by PCR for Bb, Ap, and Babesia spp. (Ba. spp.); Ba. microti is the agent of babesiosis (Table 3). We tested 32 ticks by PCR. Seven were submissions from northern counties, and the remainder from field flagging at southern study sites where increasing cases of anaplasmosis and babesiosis are being reported. Overall, 11 I. scapularis were positive for Bb, 9 for Ap, and 16 for Ba (Table 3). Three were co-infected by Bb and Ap, one for Bb and Ba. spp., and five were coinfected by all three. All co-infected ticks were from either Wells or Cape Elizabeth, towns with high tick abundance and known presence of the three disease agents (Holman et al. 2004). Two ticks infected with Bb were not from southern Maine: one from Parkman (which confirmed a positive result by DFA), and one from Islesboro. Ba. spp.-infected ticks came from Corinth, Rockland, Greenbush, Greenville, and Hope. Ba. spp. in towns not in York or Cumberland counties could be the cervid Babessia, Ba. odocoilieus. This distinction is important, because although human babesiosis is present and rising in Maine (Maine Center for Disease Control (MECDC) 2009), a substantial number of I. scapularis across Maine are infected with the 7 cervid Babesia which is non-pathogenic to humans (Armstrong et al. 1998) 2 . We had these samples sequenced to differentiate between Ba. microti and Ba. odocoilieus, but possibly due to a low concentration of DNA, the sequences were of poor quality. Another round of sequencing will be attempted before the end of the year. Table 3. Polymerase chain reaction (PCR) testing for Borrellia burgdoferi (Bb), Anaplasma phagocytophilum (Ap) and Babesia spp. (Ba), 2011. County Piscataquis Penobscot Hancock W aldo Knox Cumberland York Town Greenville Parkman Corinth East Millinocket Greenbush Old Town Blue Hill Islesboro Hope Rockland Cape Elizabeth W ells Type Pool Size Stage Host Feeding Tick 1 F CF Feeding Tick 1 F CF Feeding Tick 1 F CF Feeding Tick 1 F CF Feeding Tick 1 F FC Feeding Tick 1 F CF Feeding Tick 1 F CF Feeding Tick 5 L PL Feeding Tick 3 N PL Feeding Tick 3 L PL Feeding Tick 1 N PL Feeding Tick 1 L PL Feeding Tick 3 N PL Feeding Tick 1 N FC Feeding Tick 1 F HS Questing Tick 1 F Questing Tick 1 F Questing Tick 1 F Questing Tick 1 F Questing Tick 1 F Questing Tick 1 M Feeding Tick 1 N PL Questing Tick 4 N Questing Tick 4 N Feeding Tick 5 N TS Feeding Tick 5 N TS Feeding Tick 5 N TS Feeding Tick 6 N TS Feeding Tick 5 N PL Feeding Tick 6 L PL Feeding Tick 5 N PL Feeding Tick 20 L PL a Bb Ap Ba spp. + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + 11 9 16 a CF = Canis familiaris , FC = Felis catus , HS = Homo sapiens , PL = Peromyscus leucopus , TS = Tamias striatus 2 Additionally, there is an enzootic cycle of Ba. microti. maintained by tick species other than I. scapularis, in Maine e.g. by I. angustus (Goethert et al. 2003), which do not commonly bite humans. 8 The tick collection and testing results from 2010-2011 are a snapshot in time. To put these results into context, we examined spatial and temporal associations between Lyme case rates 3 and tick surveillance using non-parametric Spearman rank correlations (Zar 2010). Cohen (1988) considered significant correlations (P ≤ 0.05) to be moderate where 0.30 < ρ< 0.50 and strong where ρ ≥ 0.50. Figure 2. Maine Lyme disease case rates (cases per 100,000) by town, 1983-2010 average. Spatial associations--. Statewide, 1993-2010, case rates averaged 17.4 4 and ranged from 0 to 2,278 per 100,000. At the county level, case rates were strongly correlated with the number of adult, nymphal, and total ticks (n = 16 counties, ρ = 0.73, 0.85, 0.75, all P < 0.001) as well as at the town level (n = 917 towns, ρ = 0.78, 0.72, 0.78, all P < 0.0001). Figure 2 shows case rates by town and can be compared to Figure 1 which shows all I. scapularis submissions by town as well as Figure 3, which shows nymphal I. scapularis submissions by town. Passive surveillance in Rhode Island also has effectively assessed geographical risk of human Lyme disease (Johnson et al. 2004) at both the county and town levels. We calculated I. scapularis Borrelia infection prevalence by town where data are available for the decade 1991-2010 and at least 5 ticks were tested (we considered at least 5 ticks necessary for an estimate of infection prevalence). At the county level case rates were strongly correlated with nymphal infection prevalence (n = 10 counties, ρ = 0.72, P = 0.01) but not with adult infection prevalence (n = 11 counties, ρ = 0.15, P = 0.66). At 3 Cases/100,000. We obtained annual cases for Maine municipalities 1993-2010 from the Maine CDC, and 2000 and 2010 census figures for Maine towns from the U.S. Census Bureau (2010). We divided cases by the mean population of the 2000 and 2010 censuses to estimate population for the period 1993-2010. Case rate was (cases/population) × 100,000. 4 Monhegan Island Plantation 1993, 1996-97. 9 the town level case rates were correlated with neither adults nor nymphs, likely due to insufficient geographic diversity of sampling (n = 36 and 16 towns with adult and nymphal infection prevalence data, respectively, Figure 4a,b). However, the presence of even one infected tick in a town implies potential transmission risk in current and subsequent years, so we took an alternative analytical approach. We converted case rate and infection prevalence to 0, 1 responses for 36 towns where any stage of tick had been tested, such that 0 = no case and 1 = one or more cases, and 0 = no ticks found infected and 1= at least one tick infected Figure 3. Maine I. scapularis nymph submissions by town,19892010. during the current or any previous year from 1989 on, and performed a chi- square test. The likelihood of one or more Lyme cases being reported from a town was nine times greater where at least one infected tick had ever been found than in a town where no infected ticks were found (n = 36 towns, 92% vs. 8%, odds ratio 9.0 (confidence limits 1.2, 54.5)). New strategies that will increase geographic diversity of sampling in Maine are called for, as is funding for implementation. Increased sampling in the northern six counties coupled with GIS spatial modeling may allow us to predict both tick abundance and infection rates in unsampled towns using data from sampled towns, in a manner similar to that of Eisen et al. (2006). 10 Figure 4. Maine adult (a – left) and nymph (b – right) I. scapularis infection rates by town, 2001-2010. Temporal associations--. Upward trends in the time series through 2010 characterized both Lyme disease case rates (n = 18 years, r2 = 0.67, P < 0.0001) and nymphal submissions, (n = 22 years, r2 = 0.25, P = 0.02), but the nymphal trend has been approximately linear whereas case rates have risen exponentially since 2007 (~47 cases/100,000) and so far peaking at 140 cases/100,000 in 2009, Figure 5). Upward trends are evident in the southern 10 and northern six counties (Figure 5, inset), but the exponential increase was driven by southern case rates, whereas case rates just passed 20/100,000 in the northern 6 counties in 2010. Case rates and nymphal submissions were strongly correlated (n = 18 years, ρ = 0.73, P = 0.0006) but the detrended series were not, meaning the trends corresponded but the annual fluctuations did not. To our knowledge no passive surveillance studies at the state level have correlated annual fluctuations in human Lyme disease with ticks, although in Connecticut active surveillance has (Stafford et al. 1998). Annual data for nymphal infection rate were too sparse (six years missing) to detect a temporal trend in nymphal infection rate. However we observed adult infection prevalence increased over time, sharply 1990-1999 from 30% to 50% and less sharply 2000-2010 from >50% to about 60%. Lyme case rates and adult infection 11 prevalence were strongly correlated (n = 18 years, ρ = 0.59, P = 0.01) but, as with nymphal infection prevalence, not when the series were detrended. 4. I. scapularis as related to environmental indicators. In an effort to maximize the effort of field collections, we used submissions of I. scapularis and key habitat features to increase the number of samples. Previous work (Schulze et al. 1998, Guerra et al. 2001, Lubelczyk et al. 2004, Elias et al. 2006) has found that I. scapularis is predominantly associated with deciduous or mixed forest habitats, often with a moderate to dense shrub understory. The presence of the deciduous forest (ideally maple (Acer spp. or oak (Quercus spp.) provides cover and shade to the questing ticks as well as food for potential hosts through nut and seed crops (Guerra et al. 2001). The presence of a shrub layer further protects the ticks from sun and wind but also gives cover to host species such as deer, migratory songbirds, and mice (Ginsberg and Ewing 1989, Adler et al. 1992). By contrast, stands of coniferous forest, such spruce, are not usually suitable habitats for I. scapularis (Lubelczyk et al. 2004). We attempted, as much as possible, to use these habitat features to predict the occurrence of I. scapularis in emergent areas. Exotic invasives, such as Japanese barberry (Berberis thunbergii) and Eurasian honeysuckles (Lonicera spp.) in particular, have been found to support I. scapularis (Lubelczyk et al. 2004, Elias et al. 2006, Ward et al. 2009, Williams et al. 2009) and were sampled extensively, when encountered at sites in the southern, midcoast and Capitol regions (Invasive Plant Atlas of New England (IPANE) 2011). Progressing farther north and Downeast, we attempted to survey areas dominated by second-growth red oak (Q. rubra) or red maple (A. rubrum), stands of mixed forest containing eastern white pine, and post-agricultural areas where the most common shrub communities included high-bush blueberry (Vaccinium corymbosum) and winterberry holly (Ilex verticillata), usually indicative of moister soil conditions (Haines and Vining 1998). Where these plant communities were sampled, they generally produced reliable quantities of ticks, especially in coastal areas in York, Cumberland, Lincoln, Knox, 12 Kennebec, and Penobscot counties (Table 2). Areas sampled in Aroostook, Washington, Hancock, and Piscataquis counties generally have lower tick populations, and were not as productive. Low tick abundance from these suitable habitats may be due to the recent establishment of the tick in these areas and/or to lower deer density. In such locations, the establishment of I. scapularis can be extremely focal and require substantial effort before productive results can be obtained (Daniels et al. 2000). 80 300 70 60 Cases/100,000 120 100 North 80 South 60 40 20 Nymphs 20 05 20 07 20 09 1 3 20 0 9 20 0 7 19 9 5 19 9 3 200 19 9 50 19 9 Cases/100,000 0 40 30 100 20 Lyme disease case rate 10 Submitted Nymphs 0 19 93 19 94 19 95 19 96 19 97 19 98 19 99 20 00 20 01 20 02 20 03 20 04 20 05 20 06 20 07 20 08 20 09 20 10 0 Figure 5. Annual Lyme disease case rates versus annual I. scapularis nymph submissions, 1993-2010. Inset shows Lyme disease case rates in northern versus southern Maine. 5. Climate and weather factors associated with shifts in tick abundance. Changes in tick abundance versus weather--. We downloaded daily data on minimum and maximum temperature, precipitation, snowfall, and snow depth from the Portland, Maine International Jetport weather station (KPWM, 43.65N 70.301W) for 1987-2010. We selected this station as representative because 75% of tick submissions came from coastal counties. We computed monthly means for all five variables. We also calculated derived weather variables: frost-free days (daily minimum > 0C), and 13 days > 30C (Ogden et al. 2004), and the julian day at which 1,241 degree days > 6ºC was attained (Rand et al. 2004). To test for correlations between questing tick abundance and weather we used the dataset of ticks submitted to our laboratory 1989-2010. The strength of the submissions data was that they were long-term, and ticks came directly from humans and their peridomestic animals with ‘found-on’ dates at the daily level continuously throughout all tick seasons. Adult ticks were acquired during all months of the year, but only a very few were acquired in January, February, August, most of September, and the end of December. The adult spring season spanned mainly April-June, peaking during the first three weeks of May, and the fall adult season mainly October-November, peaking during the end of October and beginning of November. Nymphs were very infrequently acquired January through most of April and November through December. The nymphal season spanned mainly June-July, with the peak during the last three weeks of June and first two of July. The larval season spanned June-September and peaked in August, but relatively few larvae have been submitted to our laboratory because larvae attach to humans much less frequently than the other stages. We summarized the tick submissions for adults and nymphs to the month-year level. Then, for selected months, we examined Spearman rank correlations between the annual number of submissions and concurrent and time-lagged (up to 24 lags) weather variables to determine correspondence, if any, between annual fluctuations in tick abundance and weather. We examined March through July and September through December for adults, and May through October for nymphs. Due to few submissions we examined larvae only for the month of August. Adult ticks in March, November, and December, were positively correlated with mean minimum temperature (ρ = 0.67, 0.62, 0.71, all P ≤ 0.002), mean maximum temperature (ρ = 0.78, 0.50, 0.72, all P ≤ 0.02), and DD>0ºC (ρ = 0.64, 0.60, 0.62, all P ≤ 0.003). Adults were negatively correlated with March and December snowfall (ρ = -0.68, -0.67 all P ≤ 0.0005) and March and December snow depth (ρ = -0.73, -0.79 all P ≤ 14 0.0002). Similar correlations were seen between adults and temperature (but not DD>0ºC) and snow at a one month lag for March, April, November, and December adults (e.g., April adults were correlated with March mean minimum and maximum temperatures and snow depth). Correlations did not extend earlier than a one month lag. Figure 6 depicts ticks submitted in March versus March mean maximum temperature. Correlations among all measures of temperature, including snowfall and depth, were high (ρ ≥ 0.80), indicating their interchangeability. 80 9 Average Maximum Daily Temperature 8 60 7 50 6 40 5 4 30 3 20 2 10 1 09 10 20 20 07 08 20 20 05 06 20 20 03 04 20 20 01 02 20 20 99 00 20 19 97 98 19 19 95 96 19 19 93 94 19 19 19 19 19 91 92 0 89 90 0 19 Adults Submitted in March 70 Figure 6. I. scapularis adults submitted in March versus average maximum daily temperature in March, 1989-2010. 15 March Average Maximum Daily Temperature (C) 10 Adults 0.9 70 Nymphs 0.8 Average Daily Precipitation Nymphs Submitted in July 0.7 50 0.6 40 0.5 30 0.4 0.3 20 0.2 10 July Average Daily Precipitation (cm) 60 0.1 10 09 20 08 20 07 20 06 20 05 20 04 20 03 20 02 20 01 20 00 20 99 20 98 19 97 19 96 19 95 19 94 19 93 19 92 19 91 19 19 19 19 90 0 89 0 Figure 7. I. scapularis nymphs submitted in July versus average rainfall in July, 19892010. Nymphal ticks in June and July were positively correlated with mean rainfall (ρ = 0.57, 0.60, all P ≤ 0.01) and negatively correlated with mean maximum temperature (ρ = -0.60, -0.45, all P ≤ 0.04). July nymphal ticks were negatively correlated with July DD ≥ 30ºC (ρ = -0.64, P = 0.001). Similar correlations were seen between July nymphs and rain, mean maximum temperature, and DD ≥ 30ºC in June, and correlations did not extend beyond a one month lag. Figures 7 and 8 depict ticks submitted in July versus July average daily precipitation and mean maximum temperature, respectively. For July, we ran a generalized linear model to examine the interaction between July mean maximum temperature and rain (these predictors were correlated (ρ = -0.40) but not collinear in the model). The model predicted there would be no nymphal submissions when mean July temperature exceeded 29 degrees Celsius in combination with mean monthly rainfall ≤ 0.26cm (the median for the 1989-2010 time series), but that submissions would remain steady with rainfall > 0.26cm. 16 29 70 Average Maximum Daily Temperature 28 27 50 26 40 25 30 24 20 23 10 09 20 08 20 07 20 06 20 05 20 04 20 03 20 02 20 20 00 01 20 99 20 98 19 97 19 96 19 95 19 94 19 19 19 19 19 19 19 93 21 92 0 91 22 90 10 89 Nymphs Submitted in July 60 July Average Maximum Daily Temperature (C) Nymphs Figure 8. I. scapularis nymphs submitted in July versus average maximum daily temperature in July, 1989-2010. There were no correlations between the relatively few submitted larvae and weather variables. We therefore turned to a long-term bird-banding dataset from Wells, Maine (Smith et al. 1996, Rand et al. 1998). Subadult I. scapularis were collected consistently June through August, with 1-5 mist-netting sessions per month, for 23 years. We calculated larval burdens at the year-month level as total larvae divided by the total number of individual bird captures. Larval burdens in August were marginally correlated with mean maximum temperature in August ρ = 0.40, all P = 0.06), and positively correlated with mean maximum temperature in July and June (both months ρ =0.53, P = 0.01), as well as degree days ≥ 30 (ρ = 0.46, all P = 0.03). August larval burdens were negatively correlated with the julian day at which 1,241 DD>6ºC were attained (ρ = - 17 0.41, all P = 0.05), meaning larval burdens were greater the earlier 1,241 DD>6ºC were obtained 5 . With the data at hand, we found summarizing to the monthly level most efficacious for detecting correlations between tick questing activity and temperature and precipitation. However, summarizing to the annual level, there were several correlations of note: there was a positive correlation between nymphal submissions and average annual rainfall in the current year (ρ =0. 56, P = 0.006). Annual case rates were correlated with average annual rainfall in the current year (ρ =0. 74, P = 0.005) and at one- and two-year lags (ρ =0. 61, P = 0.007 and ρ =0. 48, P = 0.04, respectively), but when the case rate data were detrended, there were no significant correlations, meaning the increasing trends, not the annual fluctuations, in both case rates and rain drove the correlations. Summarizing to the level of season as it pertains to I. scapularis (i.e. winter, adult spring, nymphal, larval, and adult fall seasons) we did not detect correlations between ticks and weather. Correlation is not causation, but there were no spurious correlations, observed correlations were ecologically reasonable, and correlations increased or decreased in the direction one would expect (e.g., the correlation between adults and temperature was stronger in March, decreased, then increased again by December). That current weather conditions were the best predictors of concurrent tick abundance suggested that we can draw conclusions about tick questing activity (which relates to entomological risk) and make inferences about survival. Adult questing activity appeared greater in a mild winter, with warmer temperatures and less snow pack at the beginning (March) and end (November-December) of the seasons. For example, in 2010 adult submissions began unusually early in March after a late January rain melted snow cover over much of the state. Nymphal questing activity appeared to be reduced in Julys with less rainfall and hotter days. Hot/dry conditions consistent with low humidity in the air, leaf litter, and 5 We also calculated nymphal burdens on birds and tested for correlations. Nymphal burdens and nymphal submissions were correlated only in the month of August. August nymphal burdens were correlated with August mean maximum temperature (ρ =0.48, P = 0.02), August DD>30ºC (ρ =-0.45, P = 0.03), and July DD>30ºC (ρ =-0. 57, P = 0.006). 18 soil (Rodgers et al. 2007a,b) would reduce questing activity and presumably feeding success. We have several cautionary notes: with regard to the nymphal model, exact numbers (e.g. July rainfall < 0.26cm) should not be relied upon as hard and fast but can be used a conceptual basis for inferences about nymphal abundance and survival, e.g., rainfall mitigates the impact of high temperatures in summer. Burdens of nymphs on birds were not correlated with nymphal submissions, for reasons not clear. Burdens of larvae on birds in August correlated well with weather factors, but couldn’t be compared to larval submissions due to low number of submissions of larvae. Many studies have elucidated relationships between Ixodid ticks versus temperature and humidity at small and large spatiotemporal scales. The positive relationship we found between adults and warmer winters is consistent with Gray et al. (2009) who reported increased winter activity of I. ricinus in Europe since the 1980’s associated with warmer winters and extended spring and autumn seasons in Sweden resulting from warming trends in northern Europe. We found the strongest negative relationship between nymphs and temperature and positive relationship between nymphs and rainfall in July. Rodgers et al. (2007a) reported higher variability in July than June nymphal densities, suggesting this was due to more hostile July weather conditions including warmer temperatures and lower humidity. In the latter part of their seasons, ticks may be more vulnerable to suboptimal conditions (Stafford et al. 1998, Rodgers et al. 2007b) and subject to desiccation (Bunnell et al. 2003). Long droughts may reduce tick populations (Jones and Kitron 2000) and our nymphal model indicated nymphal activity would decline to zero when average July temperature exceeded 29C, but only under dry conditions—which appears consistent with Ogden et al. (2004) reporting maintenance of nymphs ≥ 30C having pathological effects. Schulze and Jordan (2003) found that more questing I. scapularis nymphs were collected in the early morning when temperatures were at or near daily minimum and relative humidity readings at their highest. The positive relationship between larval questing activity and measures of heat 19 are consistent with Rand et al. 2004, who found that the mean DD>6ºC accumulated from placement of gravid females in enclosures to larval emergence was 1,241 (SD 143.3). We found a positive correlation at the annual level between case rates and rain in the current and past two years, but only due to the upward trends in both case rates and average annual rainfall—not to annual fluctuations. McCabe and Bunnell (2004) related increased Lyme cases to above-average late spring/early summer rainfall, and Subak (2003) correlated Lyme cases with June moisture (albeit two years previously). Lindgren (1998) found that in Sweden, increased annual tick-borne encephalitis (TBE) rates corresponded to two or more consecutive years of early arrival of spring and prolonged fall season (more days with minimum temperature >5C), including a mild winter (fewer days with minimum temperature <7C) preceding the elevated TBE year. Lyme case rates in Maine have undergone an exponential increase in recent years, but could level out over the next several years (at least in southern Maine). At that point, perhaps controlling for factors relating to human behavior, such as excessively wet or hot summer conditions (Lindgren 1998) suppressing recreation, a relationship between fluctuations in case rates and weather in Maine may be discernable. It is probably on the strength of long-term data that we have been able to uncover simple relationships between tick abundance and weather variables for the state of Maine. To summarize: 1. From 1989-2010 questing adult ticks submitted from the public statewide were positively correlated with measures of temperature and negatively with snow at the beginning of winter (November/December and late winter/early spring (March). 2. From 1989-2010 questing nymphal ticks submitted from the public statewide were positively correlated with rain and negatively correlated with measures of temperature in July. 3. From 1989-2010 larval tick burdens on resident passerines in Wells were positively correlated with measures of temperature June-August. 20 Changes in tick abundance versus climate change--. In collaboration with the Climate Change Institute at the University of Maine, we investigated the impact of climate change on I. scapularis in Maine based upon climate projections for temperature, precipitation, degree days, and snow. Dr. Sean Birkel used the Weather Research and Forecasting model (WRF) (Skamarock et al. 2008) to simulate climate over the northeastern U.S. at 48 km resolution for the periods 2000-2004 and 2050-2054 (Birkel 2010, Birkel et al. 2011). WRF is a state-of-the-art regional atmospheric model, configured in this study to use lateral boundary input from the global circulation model (GCM) used in the Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report (AR4) (IPCC, 2007). The greenhouse gas radiative forcing in this model is based on IPCC emissions scenario A2, wherein atmospheric CO2 concentration rises from 380 to 575 ppm between 2000 and 2050. Because the WRF results shown here are based on only two five-year period averages they should be considered preliminary. Ongoing work will include 12 and 4-km nested model domains across New England and Maine, and ensemble averages of three comparable IPCC emission scenarios to improve statistical climate. Figure 9 illustrates modern (2000-2004, Figure 9a) and future (2050-2054, Figure 9b) average annual temperatures; Figure 9b depicts a shift in annual average temperature such that northern Maine will be more like present central Maine 6 , central Maine like southern Maine, and southern Maine like Massachusetts. Figure 10 illustrates the annual temperature period difference, showing that by 2050 Maine may warm by 1.5-2.5 degrees, with relatively more warming in the northern half of the state (Figure 10). Gains of 350-650 melting degree days (degree days > 0°C) are predicted statewide (Figure 11). 6 On page 2, we defined northern Maine as the northern six counties and southern Maine as the southern ten; here, central Maine corresponds approximately with interior, non-coastal southern Maine—see Figure 9. 21 Figure 9. Mean annual temperature predicted by WRF for (a - left) 2000-2004 and (b - right) 20502054. Solution is derived using a standard 6 °C/km vertical lapse rate to scale the 48-km WRF output to a 5-km surface topography grid. Figure 10. WRF 20502000 period difference for Annual temperature. 22 Figure 11. WRF 20502000 period difference for total melting degrees (degree days with a 0 °C datum). Figure 12 illustrates warmer January temperatures with increasing gains south to north. Figure 13 demonstrates a decrease in March snow depth from >0cm to 0.15m along the coast and inland and up to 0.3m in the northernmost part of the state. In the section on weather, we demonstrated a correlation between March adult ticks and mean temperature and snow depth. This, taken together with the climate scenario for 2050, suggests adult ticks will have longer questing seasons in both spring and fall. We can infer that a shorter, milder winter, particularly in northern Maine, will lead to greater adult survival by lengthening the questing season and increasing activity of and contact with vertebrate host species. 23 Figure 12. WRF 20502000 period difference for January temperature. Figure 13. WRF 20502000 period difference for March snow depth. 24 Figure 14 demonstrates an increase in July temperatures from 0.5 to 1.0C along the coast to ~60 miles inland, 0.25 to 0.5 in central and western portions, and 0 to 0.25 in the north part of the state. Figure 15 demonstrates an increase in July rainfall from 0.1 to 0.5cm but only along of the southwest coast and mid-coast. Most of interior Maine would experience little change in rainfall, but the southwestern interior portion of the state could experience 0.1 to 0.5cm less July rain. In the section on weather, we demonstrated a negative correlation between July nymphs and mean temperature, but only in drier than average conditions. From this we can infer that cool/wet, hot/wet, and cool/dry Julys will lead to greater nymphal survival than hot/dry Julys, with hot defined as >29C. Occasional hot/dry summers or heat waves are likely to reduce questing activity of nymphs or even survival in an exceptionally hot/dry year. However the model indicated average July temperatures will not exceed 29ºC anywhere in the state by 2050, so we think it unlikely that nymphal survival will be substantially reduced by the type of hot, dry conditions experienced at the southern edge of I. scapularis’ range. Figure 14. WRF 20502000 period difference for July temperature. 25 Figure 15. WRF 20502000 period difference for July precipitation. In a study of Ontario I. scapularis, Lindsay et al. (1995) found the minimum temperature for the development of eggs in fed, fertilized, female I. scapularis was 6ºC. This figure was corroborated for Maine ticks by Rand et al (2004). By recording temperatures at tick enclosures at 9 diverse sites in Maine, the latter authors found that 1,241 DD >6°C (SD 143.3) were required from the placement of gravid ticks from late fall or early spring until the onset of larval emergence the following summer. Based on local climate data for the interval 1991-2000, they demonstrated that by the end of September insufficient degree days would have accumulated in northwestern Maine for eggs to hatch. Since ~10% of eggs survive overwintering, establishment of the tick’s life cycle in that region would be impeded (Ogden et al. 2004). 26 Figure 16. Month during which 1,241 degree days is attained (6 °C datum) on average predicted by WRF for (a upper) 20002004 and (b lower) 20502054. 27 Our model for more recent (2000-2004) monthly attainment of 1,241 DD>6ºC, at higher resolution, conveyed very similar results (Figure 16a). By August 31st (dark green) 1,241 DD>6ºC extended within ~60 miles of the coast (with the exception of parts of Washington County), by September 30th (light blue) it extended to the western foothills and within 40 miles of the northwest border, by October 31st (dark blue) to some spotty areas in Aroostook County), while after that date 1,241 DD>6ºC were not achieved in the area depicted in light gray. The model predicted that by 2050 the requisite DD will be attained by July 31st in southwestern Maine (Figure 16b), by August 31st in most of the rest of the state, and by September 30th in the higher elevations and along the northwestern border. Thus, by the end of September in 2050 sufficient heat will have been accumulated statewide for eggs to hatch in the summer and the resultant larvae to harden and search for a blood meal, thus increasing the likelihood that I. scapularis will be able to complete its life cycle statewide. We examined the submissions data for phenological changes, specifically, shifts in the peak weeks in which each stages of I. scapularis has been submitted to our laboratory. Comparing the 1st and 2nd decades (1990-1999 and 2000-2009, respectively, we have found the spring adult peak shifted from week 19 to week 18 in May (Figures 17a and 17b), the fall adult peak from week 43 to week 42 in October (Figure 17a and 17b), the nymphal peak from week 26 to week 24 in June (Figures 17c and 17d), and the larval peak from week 33 to week 32 in August (although larval data are sparse, Figures 18a and b). 28 a. Adult deer tick submissions 1990-1999 c. Nymphal deer tick submissions 1990-1999 140 1000 800 120 (a) (c) 100 600 80 400 60 40 200 20 45 47 47 43 45 41 43 39 41 37 35 33 29 31 27 25 23 21 19 17 15 d. Nymphal deer tick submissions 2000-2009 140 1000 800 13 9 b. Adult deer tick submissions 2000-2009 11 7 0 0 2 4 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 0 120 (b) (d) 100 600 80 400 60 40 200 20 39 37 35 33 31 29 27 25 23 21 19 17 15 13 11 9 7 0 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 0 Figure 17. Histograms of Maine I. scapularis adults submitted a) 1990-1999 and b) 2000-2010, and nymphs submitted c) 1990-1999 and d) 2000-2010, indicating shifts in peak week of submissions. Although these shifts are consistent a. Larval deer tick submissions 1990-1999 with contemporary warming trends, there do 35 30 not appear to be changes in degree of 25 (a) 20 overlap between nymphal and larval peaks, 15 10 which would have implications for Bb 5 38 40 42 38 40 42 36 34 32 30 28 26 24 22 20 16 18 0 transmission. Less overlap between b. Larval deer tick submissions 2000-2009 nymphal and larval peaks can decrease 35 transmission efficiency of Bb from nymphs 30 to host to larvae and is typical of dynamics 25 at the northern edge of I. scapularis’ range 15 (b) 20 10 in Canada, whereas greater overlap, or 5 as well and is typical of dynamics at the southern edge of I. scapularis’ range in the southeastern USA (e.g. Ogden et al. 2008a). 29 36 34 32 30 28 26 24 22 20 16 peaks can also result in reduced transmission 18 0 synchrony, between nymphal and larval Figure 18. Histograms of Maine I. scapularis larvae submitted a) 19901999 and b) 2000-2010, indicating shifts in peak week of submissions. At present time and by 2050 in central and northern Maine, the overlap between nymphal and larval peaks is likely to be optimal for transmission efficiency, although rapid evolutionary changes in Bb strains (e.g. Gatewood et al. 2009) make transmission efficiency a complex issue. The expansion of the range and abundance of I. scapularis in Maine over the past two decades (Rand et al. 2007) has been related to changes in habitat and hosts (Lubelczyk et al. 2004, Elias et al. 2006). Rand et al. (2004) reported that over the last 30 years, annual average daily mean temperatures and frost free days recorded in Portland, Maine have increased gradually, but there was no shift in isolines representing 1,241 DD>6ºC between the decades 1971-1980 versus 1991-2000 (Rand et al. 2004). This shift, however, is likely to occur over the next several decades such that I. scapularis will be able to complete its life cycle statewide by 2050. That said, any changes in I. scapularis abundance as a function of climate change will be mitigated by concurrent changes in habitat and host species. Currently the biome of Maine--with the exception of higher elevations--is mixed boreal-broadleaf and will remain so by 2050 (Figure 19). However, forest cover types within the boreal-broadleaf biome are likely to change. The U.S. Department of Agriculture Forest Service Climate Change Tree Atlas (Prasad et al. 2006, Iverson et al. 2008, http://www.nrs.fs.fed.us/atlas/tree/tree_atlas.html), predicts movement of suitable habitat for tree species and forest cover types by 2100. I. scapularis are associated with pine-oak and other mixed hardwood forest types (Schulze et al. 1998). The Atlas predicts a shift from conditions suitable for a predominantly spruce-fir cover type in northern Maine to conditions suitable for a maple-beech-birch cover type by 2100 using either a GCM3 average low or high scenario 7 . Red oaks are common to the pine-oak cover type in southern Maine, and produce acorns, food for I. scapularis host species white-tailed deer and white-footed mice (e.g. Ostfeld et al. 2006). The Atlas predicts habitat suitability for red oak is expected to gain ground in northern Maine, while suitability for 7 Average of the three General Circulation Models (Hadley, PCM & GFDL), either low or high emissions scenarios. 30 species negatively associated with ticks (Lubelczyk et al. 2004), e.g. balsam fir (Abies balsamea) and red spruce (Picea rubens) is expected to lose ground. A pine-oak cover type would be associated with more understory shrub habitat than a spruce-fir cover type; and I. scapularis as well as subadult tick hosts such as birds and mice are associated with denser understory habitats (Lubelczyk et al. 2004, Elias et al. 2006). 1800 2000 2050 Figure 19. Equilibrium biome simulations for climates of ca. 1800, 2000, and 2050 predicted by the University of Maine Environmental Change Model (UM-ECM) (Birkel 2010). The prescribed meanannual temperature difference is 2 °C between 1800 and 2050. However, changes in cover type would be long-term changes. A near-term change would be suburbanization, which is on the rise statewide: “dispersed, low-density suburban-style development has become the state’s dominant settlement pattern, 23% percent of Maine’s post-2000 population in regional hub towns versus 77% in surrounding towns, newer emerging towns, and rural areas distant from traditional 31 centers (Brookings Institution 2006). Suburbanization creates habitats and increases edge, which attract white-tailed deer and can result in local over-abundance (e.g. McShea et al. 1997). Over-abundance of deer in turn can cause further changes in the landscape that favor habitat for I. scapularis and their vertebrate hosts (e.g. Lubelczyk et al. 2004, Elias et al. 2006, Williams et al. 2009). Another near-term change on the horizon planned by the Maine Department of Inland Fisheries and Wildlife (MEDIFW) is to increase abundance of white-tailed deer in northern, eastern, and western Maine 8 (MEDIFW 2011). Threshold deer density below which the life cycle of the deer tick can no longer be completed is not known. Still, Rand et al. (2003) found that in York County, Maine, few ticks (0-5) could be collected from vegetation where deer density (as measured by pellet counts) was <12 deer/km2. MEDIFW’s goal is to increase northern deer herd density to 4.5/km2 (10/mi2) (Lavigne 1999, MEDIFW 2011), which suggests that planned increases in northern deer density 2000 probably would not increase tick abundance on region-wide basis. Yet, it would be prudent for stakeholders to monitor for increases in local over-abundance of deer that could lead to focal, especially peridomestic, increases in I. scapularis in central and northern Maine. Thus, climate change could work in concert with long-term changes in forest cover types, near-term increases in suburbanization, and peridomestic overabundance of deer to increase I. scapularis abundance and Lyme disease in Maine. In southern coastal Maine, particularly York and Cumberland Counties, I. scapularis is established and abundance and infection prevalence may be approaching--or have reached--an asymptote. I. scapularis in Wells and Cape Elizabeth have fluctuated around a 1991-2010 mean of ~63 ticks/hour and ~60% infected by Bb. In a large-scale study covering the U.S. east of the 100th meridian in 2004, nymphal densities were classified as ‘highest’ in Cape Elizabeth, Maine, along with Westchester County, New York and several upper Midwest locations (Diuk-Wasser et al. 2006). However, in all but the most established areas, 8 Northern, eastern, and western Maine in MEDIFW’s plan corresponds roughly to our definition of northern Maine. See footnote 1 on page 2. 32 increases in I. scapularis abundance and Lyme disease can be expected. The association between I. scapularis and climate change made in this study is consistent with associations made between climate change and Ixodid range expansion in Canada (Ogden et al. 2005, Ogden et al. 2006, Ogden et al. 2008a, Ogden et al. 2008b) and Europe (Estrada-Peña 2008, Gray et al. 2009) 9 . To summarize, the climate of northern Maine will be more like present central Maine, central Maine like southern Maine, and southern Maine like Massachusetts. Tick abundance and will likely increase in central and northern Maine. This will be achieved through the following mechanisms: 1. Milder winters (warmer, less snow) will increase the length of the questing season for adult ticks, leading to the likelihood of more host meals obtained and increased survival of adults, given suitable habitat and hosts. 2. Warmer Julys will be mitigated by rainfall in all but the interior southwest; monthly temperatures will be <29C on average statewide, so while nymphal questing activity may be reduced in unusually hot/dry periods, nymphal survival is not expected to decrease by 2050, given suitable habitat and hosts. 3. Sufficient accumulation of DD>6ºC across the state will permit eclosion statewide so the life cycle of I. scapularis can be completed in all areas of the state, given suitable habitat and hosts. 4. Possible long-term changes in forest cover types, and near-term increases in suburbanization and peridomestic overabundance of deer could work in concert with warming trends to increase I. scapularis abundance in Maine, particularly in the northern six counties. 5. Increased Lyme disease case rates, particularly in northern Maine, can be expected due to increases in tick abundance, given suitable habitat and hosts. 9 See Appendix III for other tick species and tick-borne diseases of concern. 33 SUMMARY CONCLUSIONS TO THIS REPORT 1. To improve passive surveillance and better assess risk statewide: a) increase tick submissions from the public by providing sustained media coverage, particularly from late April through mid-July, and again during the month of October; and b) offer free postage and, funded project basis, a per-submission monetary incentive to veterinarians to cover the administrative cost of submitting ticks. 2. To improve field surveillance and better assess risk statewide: a) maintain or increase funding to increase the number of satellite survey stations over time, and b) maintain or increase funding to test for Bb and other tick-borne diseases to improve coverage of infection prevalence. 3. From 1989-2010 questing adult I. scapularis submitted from the public statewide were positively correlated with minimum and maximum winter temperatures and DD>0ºC and negatively with snowfall and snow depth. Questing nymphal I. scapularis were positively correlated with rainfall and negatively correlated with maximum temperature in July. Larval tick burdens on resident passerines in Wells were positively correlated with annual accumulation of 1,241 degree days > 6ºC. 4. The climate of northern Maine will be more like present central Maine, central Maine like southern Maine, and southern Maine like Massachusetts. By 2050, given suitable habitat and hosts: a) milder winters (warmer with less snow) will increase the length of the questing season for adult I. scapularis particularly in northern and central Maine, likely resulting in increased survival, b) statewide Julys will not warm sufficiently to have a negative impact on nymphal questing activity and thus survival except under drought conditions; and c) sufficient accumulation of DD>6ºC across the state will permit eclosion (larval hatch) statewide so the life cycle of I. scapularis can be completed statewide. 5. Increased Lyme disease case rates can be expected due to increases in I. scapularis abundance particularly in the northern six counties, if warming trends are accompanied by long-term changes in forest cover types and near-term increases in suburbanization and peridomestic overabundance of deer. 34 ACKNOWLEGMENTS Our appreciation and thanks go to Dr. Sean Birkel of the Climate Change Institute (CCI) of the University of Maine. His modeling expertise and the time he put into the models and their interpretation allowed us to make the crucial link between weather and climate as they pertain to I. scapularis ecology in Maine. We thank the supporting Principal Investigators and staff of the CCI as well. We are grateful to the Maine Center for Disease Control and the federal Centers for Disease Control for the funding and cooperation that provided the opportunity to work on the important topic of climate change impacts on vector-borne disease. We thank Melanie Renell and Unity College, Jennifer Dionne and the University of Maine/Fort Kent, and Leticia Smith, Catherine Hayes, and Erin McElwain for assisting with field collection, and Linda Siddons for administrative assistance. 35 References Cited Adler, G.H., S.R. Telford III, M.K. Wilson, and A. Spielman. 1992. Vegetation structure influences the burden of immature Ixodes dammini on its main host, Peromyscus leucopus. Parasitology 105:105–110. Armstrong, P.M., P. Katavolos, D.A. Caporal, R.P. Smith Jr, A. Spielman and S.R. Telford III. 1998. Diversity of Babesia infecting I. scapularis (Ixodes dammini). Am. J. Trop. Med. & Hyg. 58:739-42. Birkel, S.D. 2010. Climate investigations using ice sheet and mass balance models with emphasis on North American glaciation. PhD dissertation, University of Maine, Orono, Maine, USA. Birkel, S.D., K.A. Maasch, P.A. Mayewski, and P.O. Koons. 2011. Predicting future climate at high resolution over the northeastern U.S. and elsewhere using the Weather Research and Forecasting (WRF) model. 19th Annual Harold W. Borns Jr. Symposium, Orono, ME, USA (extended abstract). Brookings Institution. 2006. Chapter 2: Emerging trends in the state of Maine in: Charting Maine’s future: an action plan for promoting sustainable prosperity and quality places. http://www.brookings.edu Bunnell, J.E., S.D. Price, A. Das, T. Shields, and G.E. Glass. 2003. Geographic information system and spatial analysis of adult Ixodes scapularis nymphs in the Middle Atlantic region of the U.S.A. J. Med. Entomol. 40:570-576. Clifford, C.M., G. Anastos, and A. Elbl. 1961. The larval Ixodid ticks of the eastern United States. Miscellaneous Publications of the Entomological Society of America, 2:213-37. Cohen, J. 1988. Statistical power analysis for the behavioral sciences (2nd ed.). New Jersey: Lawrence Erlbaum. Daniels, T., R. Falco, and D. Fish. 2000. Estimating population size and drag sampling efficiency for the blacklegged tick. J. Med. Entomol. 37:357-363. Diuk-Wasser M.A., A.G. Gatewood, M.R. Cortinas, S. Yaremych-Hamer, J. Tsao, U. Kitron, G. Hickling, J.S. Brownstein, E. Walker, J. Piesman, and D. Fish. 2006. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J Med Entomol. 43:166-76. Durden, L.A. and J.E. Keirans. 1996. Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification Key, distribution, hosts, and medical/veterinary importance (Monograph). Thomas Say Publications in Entomology. Entomological Society of America, Lantham, Maryland. 95pp. 36 Eisen R.J., R.S. Lane, C.L. Fritz, and L. Eisen. 2006. Spatial patterns of Lyme disease risk in California based on disease incidence data and modeling of vector-tick exposure. American Journal of Tropical Medicine and Hygiene. 75:669–676. Elias S.P., C.B. Lubelczyk, P.W. Rand, E.H. Lacombe, M.S. Holman, and R.P. Smith, Jr. 2006. Deer browse resistant exotic-invasive understory: an indicator of elevated human risk of exposure to Ixodes scapularis (Acari: Ixodidae) in southern coastal Maine woodlands. J Med Entomol 43:1142-52. Estrada-Peña, A. 2008. Climate, niche, ticks, and models: what they are and how we should interpret them. Parasitology Research 103:S1, 87-95. Gatewood, A.G., K.A. Liebman, G. Vourc'h, J. Bunikis, S.A. Hamer, R. Cortinas, F. Melton, P. Cislo, U. Kitron, J. Tsao, A.G. Barbour, D. Fish, and M.A. DiukWasser. 2009. Climate and tick seasonality predict Borrelia burgdorferi genotype distribution. Appl. Environ. Microbiol. 75:2476-2483. Ginsberg, H.S. and C. Ewing. 1989. Habitat distribution of Ixodes dammini (Acari: Ixodidae) and Lyme disease spirochetes on Fire Island, New York. J. Med. Entomol. 26: 183-189. Goethert H.K., C. Lubelcyzk, E. Lacombe, M. Holman, P. Rand, R.P. Smith, Jr, and S.R. Telford 3rd. 2003. Enzootic Babesia microti in Maine. J Parasitol. 89:1069-71. Gray, J.S., H. Dautel, A. Estrada-Peña, O. Kahl, and E. Lindgren. 2009. Effects of climate change on ticks and tick-borne diseases in Europe. Interdisciplinary Perspectives on Infectious Diseases. Vol. 2009, Article ID 593232, 12 pp. Guerra M.A., E.D. Walker, U. Kitron. 2001. Canine surveillance system for Lyme borreliosis in Wisconsin and northern Illinois: geographic distribution and risk factor analysis. Am. J. Trop. Med. Hyg. 65:546-52. Haines, H. and T. Vining. 1998. Flora of Maine. V.F. Thomas Co. Bar Harbor, ME. 846pp. Holman, M.S., D.A. Caporale, J. Goldberg, E. Lacombe, C. Lubelczyk, P.W. Rand, and R.P. Smith, Jr. 2004. Anaplasma phagocytophilum, Babesia microti, and Borrelia burgdorferi in Ixodes scapularis, southern coastal Maine. Emerging Infectious Diseases 10:744-46. Intergovernmental Panel on Climate Change (IPCC). 2007. Fourth Assessment Report of the IPCC. Cambridge University Press, Cambridge and New York. http://www.ipcc.ch. Invasive Plant Atlas of New England (IPANE). 2011. http://nbiinin.ciesin.columbia.edu/ipane/earlydetection/predictions.htm 37 Iverson, L.R., A.M. Prasad, S.N. Matthews, and M. Peters. 2008. Estimating potential habitat for 134 eastern US tree species under six climate scenarios. Forest Ecology and Management. 254:390-406. http://www.treesearch.fs.fed.us/pubs/13412 Johnson, J.L., H.S. Ginsberg, E. Zhioua, U.G. Whitworth, D. Markowski, K.E. Hyland, and R. Hu. 2004. Passive tick surveillance, dog seropositivity, and incidence of human Lyme disease. Vector-Borne and Zoonotic Diseases. 4:137-142. Jones, C.J., and U.D. Kitron. 2000. Populations of Ixodes scapularis (Acari: Ixodidae) are modulated by drought at a Lyme disease focus in Illinois. J. Med. Entomol. 37:408-415. Keirans, J.E. and T.R. Litwak. 1989. Pictorial key to the adults of hard ticks, family Ixodidae (Ixodida: Ixodoidea), east of the Mississippi River. J Med Entomol 26:435-48. Lavigne, G.R. 1999. White-tailed deer assessment and strategic plan, 1997. Maine Department of Inland Fisheries and Wildlife. 41 State House Station Augusta, ME 04333-0041. https://maine.gov/ifw/wildlife/species/plans/mammals/whitetaileddeer/speciesasse ssment.pdf Lindsay L.R., I.K. Barker, G.A. Surgeoner, S.A. McEwen, T.J. Gillespie, and J.T. Robinson. 1995. Survival and development of Ixodes scapularis (Acari: Ixodidae) under various climatic conditions in Ontario, Canada. J. Med. Entomol. 32:143152. Lindgren E. 1998. Climate and tick-borne encephalitis. Conservation Ecology 25:1–14. Lubelczyk, C.B., S.P. Elias, P.W. Rand, M.S. Holman, E.H. Lacombe, and R.P. Smith, Jr. 2004. Habitat associations Of Ixodes scapularis (Acari: Ixodidae) in Maine. Environ. Entomol. 33:900-6. Maine Center for Disease Control (MECDC). 2009. Reportable Infectious Diseases in Maine. http://www.maine.gov/dhhs/boh/ddc/epi/publications/2009AnnualReport.pdf Maine Department of Inland Fisheries and Wildlife (MEDIFW). 2011. A Plan to Increase Maine’s Northern, Eastern, and Western Deer Herd. Maine Department of Inland Fisheries and Wildlife, Augusta, ME. 38pp. http://www.maine.gov/ifw McCabe, G.J. and J.E. Bunnell. 2004. Precipitation and the occurrence of Lyme disease in the northeastern United States. Vector-borne and Zoonotic Diseases 4:143-8. 38 McShea, W.J., H.B. Underwood, and J.H. Rappole, eds. 1997. The Science of overabundance: deer ecology and population management. Smithsonian Institution Press. Washington DC. Ogden, N.H., L.R. Lindsay, G. Beauchamp, D. Charron, A. Maarouf, C.J. O'Callaghan, D. Waltner-Toews, and I.K. Barker. 2004. Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. Journal of Medical Entomology 41:622–633. Ogden, N.H., M. Bigras-Poulin, C.J. O’Callaghan, I.K. Barker, L.R. Lindsay, A. Maarouf, K.E. Smoyer-Tomic, D. Waltner-Toews, and D. Charron. 2005. A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. Intl J Parasitol 35:375-389. Ogden, N.H., A. Maarouf, I.K. Barker, M. Bigras-Poulin, L.R. Lindsay, M.G. Morshed, et al. 2006. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol. 36:63-70. Ogden N.H., M. Bigras-Poulin, K. Hanincová, A. Maarouf, C.J. O'Callaghan, K. Kurtenbach. 2008a. Projected effects of climate change on tick phenology and fitness of pathogens transmitted by the North American tick Ixodes scapularis. J Theor Biol. 254:621-32. Ogden N.H., L. St-Onge, I.K. Barker, S. Brazeau, M. Bigras-Poulin, D.F. Charron, et al. 2008b. Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada, now and with climate change. Int. J. Health Geogr. 22;7:24. Ostfeld R.S., C.D. Canham, K. Oggenfuss, R.J. Winchcombe, and F. Keesing. 2006. Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biology 4:1058-1068. Prasad, A M., L.R. Iverson, and A. Liaw. 2006. Newer classification and regression tree techniques: bagging and random forests for ecological prediction. Ecosystems 9:181-199. http://www.treesearch.fs.fed.us/pubs/22432 Rand, P.W., E.H. Lacombe, R.P. Smith, Jr, and J. Ficker. 1998. Participation of birds (Aves) in the emergence of Lyme disease in southern Maine. J. Med. Entomol. 35: 270-276. Rand, P.W. C. Lubelczyk, G.R. Lavigne, S. Elias, M.S. Holman, E.H. Lacombe, and R.P. Smith, Jr. 2003. Deer density and abundance of Ixodes scapularis (Acari:Ixodidae). J Med Entomol 40:179-84. 39 Rand, P.W, M.S. Holman, C. Lubelczyk, E.H. Lacombe, A.T. DeGaetano, and R.P. Smith, Jr. 2004. Thermal accumulation and the early development of Ixodes scapularis. J. Vector Ecology 29:164-76. Rand, P.W., E.H. Lacombe, R. Dearborn, B. Cahill, S. Elias, C.B. Lubelczyk, G.A. Beckett, and R.P. Smith, Jr. 2007. Passive surveillance in Maine, and area emergent for tick-borne diseases. J Med Entomol 44:1118-29 Rand, P.W., E.H. Lacombe, S.P. Elias, B.K. Cahill, C.B. Lubelczyk, and R.P. Smith, Jr., 2011. Multitarget test for emerging Lyme disease and anaplasmosis in a survey of dogs, Maine, USA. Emerging Infectious Diseases 17:899-902. Rodgers, S.E., N.J. Miller, and T.N. Mather. 2007a Seasonal variation in nymphal blacklegged tick abundance in southern New England forests. J. Med. Entomol. 44:898-900. Rodgers, S.E., C.P. Zolnik, and T.N. Mather. 2007b Duration of exposure to suboptimal atmospheric moisture affects nymphal blacklegged tick survival. J. Med. Entomol.44: 372-375. Schulze, T.L., R.A. Jordan, and R.W. Hung. 1998. Comparison of Ixodes scapularis (Acari:Ixodidae) populations and their habitats in established and emerging Lyme disease areas in New Jersey. J. Med. Entomol. 35:64–70. Schulze, T.L., and R.A. Jordan. 2003. Meteorologically mediated diurnal questing of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) nymphs. J. Med. Entomol. 40:395-402. Skamarock, W.C., J.B. Klemp, J. Dudhia, D,I, Gill, D.M. Barker, M.G. Duda, X-Y. Huang, W. Wang, and J.G. Powers. 2008. A description of the advanced research WRF Version 3. NCAR Technical Note, NCAR/TN–475+STR, June 2008. Smith, R.P. Jr., P.W. Rand and E.H. Lacombe. 1990. Potential for Lyme disease in Maine: Deer survey of distribution of Ixodes dammini, the tick vector. Am. Public Health 80:333-5. Smith, R.P. Jr., P.W. Rand, E.H. Lacombe, S.R. Morris, D.W. Holmes, and D.A. Caporale. 1996. Role of bird migration in the long-distance dispersal of Ixodes dammini, the vector of Lyme disease. J. Infect. Dis. 174: 221-224. Stafford, K. C., M. L. Cartter, L. A. Magnarelli, S. H. Ertel, and P. A. Mshar. 1998. Temporal correlations between tick abundance and prevalence of Lyme disease. J. Clin. Microbiol. 36:1240-1244. Stone, E.G., E.H. Lacombe, and P.W. Rand. 2005. Antibody testing and Lyme disease risk. Emerging Infectious Diseases 11:722-24. 40 Subak, S. 2003. Effects of climate on variability in Lyme disease incidence in the northeastern United States. American Journal of Epidemiology 157:531–538. U.S. Census Bureau. 2010. American FactFinder. http://www.census.gov/ Ward, J.S.; Worthley, T.E.; Williams, S.C. 2009. Controlling Japanese barberry (Berberis thunbergii DC) in southern New England. Forest Ecology and Management. 257: 561-566. Williams, S.C., J.S. Ward, T.E. Worthley, and K.C. Stafford, III. 2009. Managing Japanese barberry (Ranunculales: Berberidaceae) infestations reduces blacklegged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environmental Entomology 38:977-984. Zar, J.H. 2010. Biostatistical Analysis. 5th Edition. Pearson Prentice-Hall, Upper Saddle River, NJ. 944 pp. 41 Appendix I. Public service announcement issued by the Mane CDC to statewide newspapers in 2011. 42 Appendix I (continued). Public service announcement issued by the Mane CDC to statewide newspapers in 2011. 43 Appendix II. Letter to veterinarians. Dear Maine Veterinarians: As I’m sure you’re aware, the deer ticks that are infecting dogs, horses and other animals (including humans) with Lyme disease, anaplasmosis, and other diseases in Maine are advancing into northern and western counties. This year we’re working with the Maine CDC to track that spread, and remain very interested in receiving any I. scapularis (or unidentified ticks) you may find on animals you examine. Top priority is ticks from Aroostook, Piscataquis, Penobscot, Somerset, Washington, Hancock and Oxford counties. To facilitate your sending them to us, we’ll be glad to provide vials, postage-paid mailers, and submission forms. Just let us know at randp@mmc.org, or give us a call at 799-4292. Alternatively, you can put all ticks from a given animal in a small crush-proof vial containing a blade of grass or a small piece of moist (not wet) paper towel and send it to us along with a completed submission form, which you can print off from our website (http://www.mmcri.org.lyme/submit.html). We may be able to examine live ticks for Lyme spirochetes if they are from animals that have not been vaccinated against the disease. Our address is: Vector-borne Disease Laboratory Maine Medical Center Research Institute 75 John Roberts Road, Suite 9B South Portland, ME 04106 Because funding for this project was not available until last October, we were late getting started, but attached you’ll find a summary of ticks submitted by veterinarians last year. We understand this is just one more thing in your busy practice, but we hope you’ll be able to find the time to help out on this important public health project. Thanks, Peter W. Rand, MD MMCRI VBDL 44 Appendix III. Other Tick-borne Diseases of Concern In the United States, some ticks carry pathogens that can cause human disease, including: • • • • • • Human Granulocytic Anaplasmosis (HGA) is transmitted to humans by tick bites primarily from the blacklegged tick (Ixodes scapularis) in the northeastern and upper midwestern U.S. and the western blacklegged tick (Ixodes pacificus) along the Pacific coast. Cases of HGA have been reported from several counties in Maine since 2000. Since that time, the number of cases has risen, most likely because the vector tick, I. scapularis, has expanded its range through bird importation. Babesiosis is transmitted by the blacklegged tick (Ixodes scapularis) and is found primarily in the eastern U.S. Cases of babesia have been reported primarily from southwestern counties in Maine in recent years. The number of yearly cases is small, when compared to the reported cases of Lyme disease, and appears dependent on the yearly ecological cycle of rodent densities, the reservoir for the disease in nature. Human Moncytic Ehrlichiosis (HME) is transmitted to humans by the lone star tick (Ambylomma americanum), found primarily in the southcentral and eastern U.S. A. americanum ticks are reported to be found infrequently in Maine but are not thought to be established at this time (Appendix III-Figure 1). A tick acclimated to southerly climates and dry, open oak habitats though, means that Amblyomma spp. should be noted as future species of concern in Maine, especially as northern and coastal spruce/fir forest communities might be replaced with deciduous forest habitat. Powassan Encephalitis virus has been found in Maine and should be regularly screened for. The vector tick Ixodes cookei has had a relatively stable distribution in the state since surveillance for ticks began in 1989 (Fig. 4 & 5, Appendix III). While this disease has traditionally been only found in northern locations, I. cookei is found throughout southern states. Impacts to this tick and and resulting numbers of cases of Powassan virus from changing climate scenarios are unknown. Rickettsia parkeri Rickettsiosis is a member of the Spotted fever group of rickettsias and is transmitted to humans by the Gulf Coast tick (Amblyomma maculatum). Since a small number of these tick have been found within Maine, it remains a remote possibility that people and animals could be exposed to this pathogen in the future. Rocky Mountain Spotted Fever (RMSF) is transmitted by the American dog tick (Dermacentor variabilis), Rocky Mountain wood tick (Dermacentor andersoni), and the brown dog tick (Rhipicephalus sangunineus) in the U.S. The range of the dog tick, D. variabilis, has expanded from 1990-2009 (Appendix IIIFigures 2 and 3) and this tick is very common across Maine into coastal Canada. While human cases of RMSF have been reported in Connecticut and Massachusetts, New Hampshire has reported a very small number of canine cases. Clearly, RMSF is a future concern in both human public health and veterinary 45 • • • • health arenas and should be a target for surveillance activities. The activity of RMSF in coastal Massachusetts, New York and Connecticut should be of future concern as climate trends changing southern Maine to resemble current climate scenarios in southern Massachusetts mean that the potential for this disease will increase. STARI (Southern Tick-Associated Rash Illness) is transmitted via bites from the lone star tick (Ambylomma americanum), found in the southeastern and eastern U.S. See above entry for HME. Tularemia can be transmitted to humans by the bite of a dog tick (Dermacentor variabilis), wood tick (Dermacentor andersoni), or the lone star tick (Amblyomma americanum). Tularemia occurs throughout the U.S., including New England. The tick-born cycle of this disease has been recently active in coastal Massachusetts but positive animals have been found in southern Maine as well. Certainly, future climate trends changing southern Maine to resemble current climate scenarios in Massachusetts mean that the potential for this disease will increase 364D Rickettsiosis (Rickettsia phillipi, proposed) is transmitted to humans by the Pacific Coast tick (Dermacentor occidentalis ticks). This is a new disease that has been found in California and is not, at this time, of concern in Maine. Tickborne relapsing fever (TBRF) is transmitted to humans through the bite of infected soft ticks. TBRF has been reported in 15 states: Arizona, California, Colorado, Idaho, Kansas, Montana, Nevada, New Mexico, Ohio, Oklahoma, Oregon, Texas, Utah, Washington, and Wyoming and is associated with sleeping in rustic cabins and vacation homes. To date, there are no reports of soft ticks occurring in Maine, so the concern for this disease is minimal. Appendix III-Figure 1. Submissions of Amblyomma americanum, 1989-2010. 46 Appendix III-Figure 5. Submission s of ixodes Appendix III-Figure 2. Submissions of Dermacentor variabilis,1989-2000. Appendix III-Figure 3. Submissions of Dermacentor variabilis,1989-2010. Appendix III – Figure 5. Submissions of Ixodes cookie,1989-2010. Appendix III – Figure 4. Submissions of Ixodes cookie,1989-2000. 47