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Sequential Partial Migration Across Monarch Generations in Michigan Anim. Migr. 2018; 5: 104-114 Research Article Open Access Natalia Ruiz Vargas, Logan Rowe, Joel Stevens, Joshua E. Armagost, Andrew C. Johnson, Stephen B. Malcolm* Sequential Partial Migration Across Monarch Generations in Michigan https://doi.org/10.1515/ami-2018-0007 Keywords: monarch butterfly, partial migration, voltinism, Received June 13, 2018; accepted October 30, 2018 milkweed hostplant, wing wear, wing load, fat content, cardenolide sequestration Abstract: Running title: Monarch alternative migration Abstract: We collected 434 adult monarchs and surveyed milkweeds for immature monarchs in southwest Michigan, 1 Introduction USA in order to test the hypothesis that monarchs are temporally variable, sequential partial migrants rather Populations of many mobile vertebrate species such as than partial migrants that may be spatially separated. birds, mammals and fish with multi-year lifespans show Adult size, wing wear, female egg counts, fat content mixtures of migratory and non-migratory, or resident life and sequestered chemical defenses were measured in histories characteristic of partial migration [1-3]. Chapman monarchs across an entire season from spring migrant et al., [2] and Shaw and Levin [3] describe three forms arrival, through breeding, until autumn migrant departure. of seasonal partial migrants in which (1) migrants and We predicted that a population characterized by starting residents breed together, but overwinter apart, (2) migrants from all migrants and no residents, through breeding and residents breed apart and overwinter together, or (3) residents, to all migrants and no residents should show migrants breed together, but not every year, generating life history measures consistent with changes in these a mix of migrants and non-migrants. Short-lived insects proportions. Results show that female monarch spring that include migration behaviors in their life histories migrants arrive with chorionated eggs and high wing are also thought to reflect these patterns [1-4]. However, loads in both intact and fat-extracted adults. Wing loads the short life-span of most mobile insects is likely to of both males and females decrease during the summer preclude separation into these three categories of “non- and increase again immediately before autumn departure, breeding partial migration”, “breeding partial migration”, when the fat content of all adults increases markedly. The or “skipped breeding partial migration.” Instead, migrant high fat content of spring arrivals is also characteristic of and non-migrant insects may be separated temporally migrants. Cardenolide content of adults showed a similar rather than spatially at breeding or overwintering pattern of high content in spring arrivals, a decrease in locations and show sequential partial migration. Here, the summer and then an accumulation of cardenolide we test this interpretation with a seasonal analysis of defenses in adults in late summer just before migratory monarch butterflies, Danaus plexippus (L.) (Lepidoptera: departure. We conclude that these results are consistent Nymphalidae) as they arrive, breed and depart from with temporally variable, sequential partial migration in Michigan, USA near the center of the monarch breeding a short-lived insect that contrasts with spatially variable distribution in North America east of the Rocky Mountains partial migration in longer-lived vertebrates. [5]. We predict that spring arriving and autumn departing adults will show life history measures characteristic of migrants and between these defining points the adults will have measures characteristic of breeding residents. *Corresponding author: Stephen B. Malcolm, Department of The monarch butterfly is considered an iconic Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008, USA, E-mail: [email protected] example of insect migration by virtue of its predictable, Natalia Ruiz Vargas, Logan Rowe, Joel Stevens, Joshua E. Armagost, long-distance annual migration in North America between Andrew C. Johnson, Department of Biological Sciences, Western overwintering resources in Mexico and breeding resources Michigan University, Kalamazoo, Michigan 49008, USA distributed across the USA and southern Canada east of the Open Access. © 2018 Natalia Ruiz Vargas et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution- NonCommercial-NoDerivs 4.0 License. Sequential Partial Migration Across Monarch Generations in Michigan 105 Rocky Mountains [5-19]. From early wing-tagging studies life histories is likely to vary seasonally and may help by Nora and Fred Urquhart in Canada [5,7,8] and later to explain some of the variation seen among monarch studies coordinated by Orley Taylor of Monarch Watch populations. Here, we describe data collected from at the University of Kansas (http://www.monarchwatch. both migrant and non-migrant monarch butterflies org/index.html) we know that adult monarchs fly each from southwest Michigan starting with their arrival in autumn to 12 locations in oyamel fir forests above 3,000 spring, through summer breeding until their departure in m elevation in the Sierra Transvolcanica mountains of autumn. The data we collected include variation in adult central Mexico, west of Mexico City [10,11,14,15]. There size, wing loading, wing wear, fat content, female egg the butterflies remain for up to 5 months over winter in load and sequestered cardenolides; together these data tightly aggregated clusters until their return migration aid in the interpretation of how monarchs move to exploit north in spring at the end of March. We also know that the seasonally and spatially separated host plant resources. same butterflies that left the USA and southern Canada These data allow us to test the prediction of Berthold [61] in the autumn, and spent the winter in Mexico, return that “improved conditions” (i.e. good quality breeding to the southern USA where they mate, lay eggs and die resources) increases the proportion of non-migrants in a [16,17,20,21]. The offspring of these migrants from Mexico population of partial migrants [62]. then feed on southern milkweed hostplant species and Michigan is in the center of the extensive distribution upon emergence as adults continue the migration north of the common milkweed, Asclepias syriaca, [35,36] which to recolonize the full spatial extent of their milkweed is the most important hostplant for monarchs [21,32,36,37] hostplants across North America, east of the Rocky out of the 108 species of Asclepias milkweeds described Mountains [20,21]. by Woodson [35] from North America. It is in this northern In addition to their spectacular annual migration in extent of the range, where A. syriaca predominates, that North America, monarch butterflies are well known for monarchs generate up to three successive generations their specialized larval feeding on milkweeds in the genus [38,39], to establish the large numbers of butterflies that Asclepias and their ability to sequester toxic steroids fly to Mexico each autumn. known as cardenolides for use in defense against natural Migrating insects are thought to show a distinct trade- enemies such as birds [22-32]. Each Asclepias hostplant off between flight and reproduction so that migrating species generates a different pattern of sequestered individuals are in reproductive diapause and reproductive cardenolides in adult monarchs and Malcolm et al. individuals do not migrate. This trade-off is known as the [21] used these chemical “fingerprints” as indicators of “oogenesis-flight syndrome” and is argued to occur in migratory strategy in spring migrants. Evidence from monarchs [6,9,40-46]. However, like Thomas and Showers cardenolide fingerprints and wing wear patterns [21], as [47] we suspect that this is not the case for migratory well as isotopic signatures [16,17,33,34], show that spring monarchs and we have some evidence from prior work that migration does occur primarily via successive broods in migrating female monarchs lay eggs and that they carry which migrating spring butterflies reach the southern USA fully developed, or chorionated eggs during migration. from Mexico, mate, lay their eggs on southern Asclepias We researched monarch breeding ecology during species and die, leaving their offspring to continue the the summer throughout southwest Michigan in order to migration north. determine (1) changes in adult wing size, wing loading, While much is known about migration, mating wing wear, fat content, and host plant-derived chemical behavior and physiology, hostplant use and the operation defense content, (2) variation in female monarch egg of defense against natural enemies in monarch butterflies, counts in migrants and non-migrants as a test of the we still know little about the dominant phase of their life “oogenesis-flight syndrome”, and (3) the relationship history when their annual populations increase during between these measures and the timing and abundance of the summer or about how monarchs both migrate and immature monarchs on milkweed hostplants as a measure lay eggs as they encounter milkweed resources. While of the duration of breeding behavior. monarchs are thought to occur as either migrant or non- Our goal was to determine whether collected data are migrant populations [5,6,14,60] they are better described consistent with an interpretation of partial migration in as “partial migrants” with a life history characterized which spring arrivals and autumn departures are migrants by a mix of
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