Of all North American species, Anax junius is best known and clearly is a regular, annual migrant from southern Canada well into Mexico and perhaps beyond. Each year, in mid-August through October, reports of noticeable southward flights and large aggregations appear in natural history newsletters, the popular press, and sometimes in the entomological literature. Russell et al. (1998) compiled a long but far from exhaustive list of such accounts, noting that “Records of large dragonfly migrations show several distinct patterns: (1) all reports fell between late July and mid-October, with a peak in September; (2) most of the large flights occurred along topographic leading lines such as coastlines and lakeshores; (3) massive swarm migrations generally followed the passage of synoptic-scale cold fronts; and (4) the common green darner (Anax junius) was the principal species involved in the majority of these flights.”
Migration studies in North America became more quantitative and focused with the work of Robert Trottier (1966, 1971) on Anax junius in southern Canada. He found that near Montreal (~45.5°N) larvae probably were unable to overwinter, although they are regularly found during summer (overwintering has now been shown to occur at least as far north as Montreal (Catling 2004), however, possibly in response to climate warming). In southern Ontario (~43.5°N), by contrast, two clear-cut cohorts of larvae existed, corresponding to adults with very different behaviors. Larvae of one group emerged from late June through mid-July and the resulting adults finished oviposition by early August. The other group appeared as small larvae in June, developed rapidly during the summer and emerged in late August through September after adults of the first cohort had died. The second group of adults mostly disappeared before maturing sexually. These observations suggested (Trottier 1971) that the first group of larvae represented “residents” that overwinter as larvae, mature and emerge by midsummer, become active as adults, oviposit and die by mid-August. Their offspring then hatch and grow to mid-instar larvae before entering diapause for the winter. The second larval cohort were the offspring of adults that migrate into the area in early spring and have been seen ovipositing in early April, while snow may still be on the ground (Walker 1958; Butler, et al. 1975). They grow rapidly as soon as the water warms and mature by late summer, emerge as adults, and mostly depart from the vicinity of their natal ponds while still sexually immature and migrate southward. Presumably some of their offspring return northward the next spring (although they may not return to the same pond, or even the same region, as their parents), and the migration cycle begins again. This scenario sees migration as a normal part of the life cycle that facilitates colonization of northern areas. It is consistent with many reports of apparently annual movements described along the eastern seaboard by Shannon (1916, 1935) and on the northern shores of Lake Erie by Walker (1958), Nisbet (1960), and Corbet (1984).
Wissinger (1988) reported a similar pattern of emergence, with two well-separated emergence periods, from a population of A. junius in northwestern Indiana in 1982–1984, although a few adults emerged early, in April. These were interpreted as individuals of the previous year’s “migrant” cohort that had not completed development in time to emerge the previous fall and had diapaused over the winter. This suggests that larval diapause is facultative and supports the possibility that some early adults seen in northern localities may emerge locally (White and Raff 1970). Kime (1974) also reported “migrant” and “resident” cohorts of Anax junius larvae in Washington State, based on larval size distribution.
In sum, these results suggested that migrants and residents are behaviorally and physiologically distinct and, especially from Trottier’s study, that the two cohorts might be reproductively isolated because the mating and oviposition periods of their respective adults did not overlap (Fig. 1a). The likelihood of genetic divergence of migrants and residents seemed high, and even the possibility of incipient speciation had to be considered.
Very little published work on developmental phenology has appeared since Wissinger’s (1988) study, but unpublished studies reveal much more variability in the life cycle of Anax junius. During nine years of daily collections of exuviae at a pond in New York (~42.42°N, 76.83°W), John and Sue Gregoire (pers. comm., 2012) found a weak tendency toward a bimodal peak of emergence but with no complete hiatus in emergence during the summer and great interannual variation in emergence pattern and total numbers emerging. A similar pattern of bimodal emergence with substantial overlap of early and late peaks was seen at Patuxent Research Refuge in Maryland (39.04°N, 76.78°W; Orr 1996; pers. obs., 1999–2004) and from the state of Washington (Kime 1974). Data are still scanty from the southern part of the range. Paulson’s (1999a) observations in southern Florida suggest a major period of emergence in March and April, followed by reduced activity until an influx of adults in late summer, with a minor peak of emergence in October (Fig. 2). More extensive data on adult flight season, based on specimens in the Florida State Collection of Arthropods, confirms that in Florida few adults occur from late May until early August (May, unpublished data, 2012). Still, some may be found flying at any time of year and final instar larvae apparently are present throughout the summer (N. Dorn, pers. comm., 2010). Data from Austin, Texas (J. Matthews, pers. comm., 2011) also indicate an early spring emergence peak but are incomplete and thus not definitive concerning fall emergence. Finally, Matthews (2004, 2007a, b) revisited the area in Ontario where Trottier had worked almost 40 years before and discovered that, while the bimodal emergence pattern persisted, emergence peaks overlapped extensively and some emergence continued through the summer (Fig. 1b). He tentatively ascribed this to changes in local precipitation patterns. Thus the picture of clear cut migrant and resident cohorts turns out to have been a considerable oversimplification that varies spatially, has changed over time on a scale of decades, and may be much more variable annually than was initially realized.
Tracking fall migrations
Besides these new perspectives on Anax life history, recent studies add critical data and unique insight into individual behavior. Wikelski et al. (2006) attached micro-radio transmitters to 14 A. junius and followed them during fall migration for up to 12 days (Fig. 3). Despite carrying transmitters, individuals migrated up to 140 km per day, and two were observed foraging apparently normally. The dragonflies alternated distinct stopover periods with active migration and on average migrated about every 3 days. The average advance of 13 migrating individuals was approximately 60 km (12 km/day), but daily movement ranges exhibited a trimodal distribution: short-range and omni-directional and medium or long-range and, on average, within a few degrees of due south, as suggested by Russell et al. (1998).
Three individuals in Wikelski’s study changed their migration route by more than 120° upon reaching an ocean barrier (Fig. 3), evidently reorienting in response to landmarks (although some do perish at sea during migrations along shore; pers. obs., 1993). Three captured at Cape May returned northward, later to cross Delaware Bay at a narrower point, indicating considerable behavioral flexibility in route selection. Songbirds and small hawks sometimes perform a similar maneuver during fall migration (e.g. Wiedner et al. 1992).
Data from Wikelski et al. (2006) were limited by the small numbers that could be tracked, the necessity of encumbering the insects with a load of around 25 % of their body mass, and the inability to track individuals more than 100–200 km from the release point. These difficulties were largely overcome by Matthews (2007c; May and Matthews 2008), who took advantage of a well-documented north to south gradient in the 2H:1H isotope ratio in natural fresh waters. This ratio is reflected in hydrogen isotope ratios of resident aquatic animals, including odonate larvae (Hobson et al. 2012), and is preserved in the relatively inert wing cuticle of adults. Carefully calibrated 2H:1H ratios of individuals collected along a transect from Ontario, Canada, to Veracruz, Mexico, during late August to October, revealed that about 90 % of individuals moved southward, by a mean distance estimated at ca. 900 km, with a maximum of nearly 3,000 km (Matthews 2007c). Moreover, using both hydrogen and strontium isotope ratios, Matthews showed that individuals collected together in localized swarms near the Atlantic Coast mostly had originated at inland sites, possibly spread far northward and westward. It seems clear that Anax junius migrate southward over at least many hundreds of km. Observations by Matthews (2007c) and others (Russell et al. 1998; Wikelski et al. 2006) suggest that this movement is punctuated by episodes of feeding and reproduction, probably at many sites along the migratory route, so migrants may spend many weeks en route.
Direct observations of feeding by presumed migrants are common, and Wikelski et al. (2006) compared the alternation of periods of short flights with days of long-distance flights to “refueling” stops well known in many migratory birds. Anax junius may spend as much or more time feeding in local areas as actually making long flights of many of kilometers. Clearly energy accumulation and suitable feeding sites are important to these migrants. Anax, like other Odonata, eclose with very little fat, undeveloped ovaries and functional but incompletely developed flight muscles. They quickly increase muscle mass and fat stores, and both in local breeders and migrants, body mass comprises at least 20 % fat, on average (May and Matthews 2008). This is significantly higher than in non-migratory Anisoptera (Anholt et al. 1991; May, unpublished data), and fat content of fall migrants is significantly higher than in local breeders (Fig. 4). Even so, Wikelski et al. (2006) calculated that without wind assistance the average fat reserves of an individual would only last for one full day of flight. Spring migrants in New Jersey apparently have low fat content but large ovaries (May and Matthews 2008), although few specimens have been analyzed. This pattern, if confirmed, suggests that migrants arrive at northern locations reproductively mature but with depleted energy reserves.
Reproductive activity en route is less frequently observed directly. Both Corbet (1984) and Catling and Brownell (1998) found that virtually all A. junius collected in late August through early October along the north shores of Lakes Erie and Ontario were immature; this is near the northern limit of the range where the species is common, although it reproduces sparsely as far as 50°N (Walker 1958). In Cape May, New Jersey, and along the south shore of Long Island, New York (ca. 40°N), however, tandem pairs (i.e., with the male grasping the female, which almost always indicates an imminent or ongoing bout of oviposition) are a minor component of some migrating swarms (Walter 1996; Russell et al. 1998), and many females collected at Cape May have mature ovaries (Fig. 4). During a Florida migration, all specimens appeared mature based on visual criteria, and scattered tandem pairs were observed (Russell et al. 1998), and Matthews (2007c, and pers. comm., 2006, 2011) observed tandem and ovipositing pairs along the Virginia and Texas coasts and in Veracruz, Mexico. Moreover, the genetic composition of A. junius populations permits the inference that reproduction is a common feature of migration in that species. Sexually mature migrants are expected if they depend on reproductive bet-hedging by ovipositing repeatedly during the southward flight as suggested below (Matthews 2007c; May and Matthews 2008).
Population ecology and genetics
In the first genetic survey of the species Freeland et al. (2003 sequenced most of the mtDNA protein coding gene, COI, from adult specimens collected across the continent and from Canada to Mexico. They found a diverse complement of haplotypes, but none that characterized migrant vs non-migrant individuals. They suggested that this could be the result of the mixing, during migration, of numerous sub-populations that varied in haplotype owing to local selection. Nothing indicates that migration itself was genetically controlled, however, since migrants and non-migrants shared haplotypes and migrants were not concentrated in particular clades.
Matthews (2007c) collected both adults and larvae along an irregular transect across much of eastern North America. Examination of nine microsatellite loci gave little or no evidence of geographic genetic differentiation or of differentiation between presumed migrant and resident individuals of either life stage. Larvae showed some tendency to be more closely related within collection sites but not among nearby sites, and even within-site relatedness could be explained by the existence of sibling groups from a single year. This strongly supports the conclusion that ponds are populated and repopulated annually by offspring of adults of widely separated origins, as would be expected in species that reproduce freely during the course of wide-ranging dispersal.
The observed haplotype diversity (Freeland et al. 2003) could indicate selection on local populations, since mixing of the continent-wide population makes it unlikely that drift is a major factor. Local populations might be displaced from selective equilibrium by repeated influxes of migrants, as well as instances of catastrophic habitat collapse. Either or both might limit adaptation to local conditions and favor evolution or maintenance of facultative migration. Of interest would be data from the presumably non-migratory population of Anax junius in Hawaii, in which both local selection and perhaps drift between subpopulations on different islands might have greater effects.
The origin and destination of southbound migrants can only be indicated in broad terms, largely because the beginning and end points of migration are, in fact, very widely dispersed. Matthews’ (2007c; May and Mathews 2008) data on hydrogen isotope ratios, described above, together with the genetic evidence, indicate that fall migrants are drawn from a huge region extending from as far as 50°N to as far south as ~33°N and from the Atlantic Coast far inland, and other evidence suggests that individuals from the Pacific Northwest probably migrate extensively through the western US (Kime 1974; Paulson 1996). Individuals from large areas mix in adult aggregations and probably lay eggs in ponds along much of their route. The ultimate southward extent of flights is unclear, but based on my observations on the east coast of northern FL (Russell et al. 1998), and those of Matthews (2007c) and others (Paulson, pers. comm, 1999; Tibol, pers. comm., 2008) in Veracruz State, Mexico, substantial numbers, probably millions, reach those points and beyond. The Florida data fit neatly with those of Fig. 3 showing a sharp increase in the number of adult Anax in southern FL during August to October, with little evidence of emergence until October. Anax junius is also known from the Greater Antilles, but whether these represent strays, regular migrants, or resident or partly-resident populations is unknown. In Mexico and Central America, Paulson (1984, 1999b) and Boomsma and Dunkle (1996) believed that A. junius seen in the Yucatan and Veracruz, and in Belize, in October and November were North American migrants, and observed evidence of reproduction, including tandem pairs and oviposition.
Large migrating swarms of A. junius are seen with some regularity in autumn but much more rarely in spring. Clearly, if migration is annual and an adaptive life history strategy, northward spring migration is implied. Evidence for this includes that cited above, i.e., observations of mature individuals that initiate reproductive activity in northern areas in early spring at places where they apparently could not have emerged (Walker 1958; Young 1967; Butler et al. 1975). On the other hand, White and Raff (1970) found exuviae in central Pennsylvania that suggested that some of these early individuals might emerge locally and Wissinger (1988) as noted already, documented early emergence in Indiana.
More recent and systematic observations in the northeastern U.S. have adduced additional evidence for spring migration. At many sites, substantial numbers of Anax junius appear with warm air masses in early spring, generally remaining at a given site for only a few days (R. Barber, A. Barlow, B. Nikula, R. Orr, pers; comm.; pers. obs.). More details of one such influx are described by Russell et al. (1998). Other compelling evidence for the occurrence and regularity of spring migration northward is the fact that, in eastern Maryland, the mean appearance date of the first mature adults in 1991–1995 was 6 April (range 24 Mar. to 25 April) while the average first emergence date was 26 May (range 7 May to 11 June; Orr 1996) and in southern New York from 2004–2009, adults appeared on average on 26 April (23 April to 7 May) while mean first emergence was on 9 June (25 May–15 June; S. Gregoire, pers. comm, 2011).
Apparently, large swarms of Anax rarely if ever form in the Northeast at this time, although distinct migratory swarm of other species may include some Anax junius (e.g., Sones 1995; observed on Cape Cod in early June). The near absence of spring swarm migration may be related to one or more of the following phenomena, which are not mutually exclusive: the total number of adults moving northward may be less than those that fly south, since mortality must be high in both directions, and the relative reproductive success during the northern summer vs. fall to early spring in southern parts of the range is not known; it is possible that spring migration is more protracted (see below); and, because warm fronts commonly move more nearly parallel to the SW–NE orientation of the Atlantic Coast than do cold fronts, the spring migration track may often not intersect the coast, where migration would be most obvious due to leading line effects (Russell et al. 1998). The origin of northward migrants is even less clear. It is generally assumed that those arriving in early spring in southern Canada and the Northeastern and Midwestern U.S. have mostly emerged in the southern U.S. (Butler et al. 1975), perhaps supplemented with a few early local emergers (White and Raff 1970; Wissinger 1988). This scenario is consistent with the emergence phenology seen in S. Florida (Fig. 2) and in Austin, Texas (30.3°N; peak usually in late April to early May; Matthews, pers. comm., 2006). Other sites from which data are available are located no further south than 38°N and are unlikely to produce new adults early enough for these to reach Canada by early April (Butler et al., 1975). Unfortunately, isotope ratio data for adults arriving early at northern sites in spring are not yet available, although even as late as early September, Matthews (2007c; May and Mathews 2008) recorded apparent northward movements of a few individuals from stations along his transect. He surmised that northward movements might continue with moderate frequency throughout the spring and summer. It seems, however, that long, directed flights are likely at the beginning of the northern season, given that the first mature spring migrants appear at times when emergence probably has barely begun even several hundred kilometers further south. This could, perhaps, give the resulting larvae a size advantage over the offspring of later arriving adults while avoiding high rates of cannibalism by large overwintering larvae owing to cool water temperature (Crumrine 2010).