Next Article in Journal
Implications of Historical and Contemporary Processes on Genetic Differentiation of a Declining Boreal Songbird: The Rusty Blackbird
Next Article in Special Issue
Isotopic Niche Segregation among Darwin’s Finches on Santa Cruz Island, Galápagos
Previous Article in Journal
Nematode Community-Based Soil Food Web Analysis of Ferralsol, Lithosol and Nitosol Soil Groups in Ghana, Kenya and Malawi Reveals Distinct Soil Health Degradations
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 13
Issue 3
10.3390/d13030102
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Origins of Six Species of Butterflies Migrating through Northeastern Mexico: New Insights from Stable Isotope (δ2H) Analyses and a Call for Documenting Butterfly Migrations

by
Keith A. Hobson
1,2,*,
Jackson W. Kusack
2 and
Blanca X. Mora-Alvarez
2
1
Environment and Climate Change Canada, 11 Innovation Blvd., Saskatoon, SK S7N 0H3, Canada
2
Department of Biology, University of Western Ontario, Ontario, ON N6A 5B7, Canada
*
Author to whom correspondence should be addressed.
Diversity 2021, 13(3), 102; https://doi.org/10.3390/d13030102
Submission received: 7 February 2021 / Revised: 20 February 2021 / Accepted: 21 February 2021 / Published: 25 February 2021
(This article belongs to the Collection Stable Isotope Ecology)
Browse Figures
Review Reports Versions Notes

Abstract

:
Determining migratory connectivity within and among diverse taxa is crucial to their conservation. Insect migrations involve millions of individuals and are often spectacular. However, in general, virtually nothing is known about their structure. With anthropogenically induced global change, we risk losing most of these migrations before they are even described. We used stable hydrogen isotope (δ2H) measurements of wings of seven species of butterflies (Libytheana carinenta, Danaus gilippus, Phoebis sennae, Asterocampa leilia, Euptoieta claudia, Euptoieta hegesia, and Zerene cesonia) salvaged as roadkill when migrating in fall through a narrow bottleneck in northeast Mexico. These data were used to depict the probabilistic origins in North America of six species, excluding the largely local E. hegesia. We determined evidence for long-distance migration in four species (L. carinenta, E. claudia, D. glippus, Z. cesonia) and present evidence for panmixia (Z. cesonia), chain (Libytheana carinenta), and leapfrog (Danaus gilippus) migrations in three species. Our investigation underlines the utility of the stable isotope approach to quickly establish migratory origins and connectivity in butterflies and other insect taxa, especially if they can be sampled at migratory bottlenecks. We make the case for a concerted effort to atlas butterfly migrations using the stable isotope approach.

1. Introduction

Many animals have evolved to migrate in response to seasonal changes in resource abundance [1]. Among insects, migration is diverse and includes movements resembling dispersal, often at local scales, to intercontinental movements involving multiple generations [2]. Well-known examples of insect migration are often associated with spectacular daytime movements of Lepidoptera, Odonata, and Orthoptera, and include charismatic species (e.g., butterflies, dragonflies). Radars have also documented impressive nocturnal movements of pest species (e.g., Autographa gamma [3]). Indeed, in the Nearctic, one of the most impressive examples of insect migration is provided by the eastern North American monarch butterfly (Danaus plexippus) that annually migrates up to 5000 km from breeding grounds in the USA and Canada to discrete high-altitude overwinter colonies in oyamel fir (Abies religiosa) forests of central Mexico. Mated females that have successfully overwintered at these sites then return northward in the spring and initiate a series of subsequent generations that move northward in search of host milkweed (Asclepia spp.) plants. A final fall migrant cohort, one that has never seen the overwinter sites, then returns to those sites to complete the cycle. In the Palearctic, a similar multigenerational migration occurs between Europe and sub-Saharan Africa for the painted lady butterfly (Vanessa cardui), presumably timed to make use of seasonal rains in the Sahel and tropical Savannah [4]. That migratory circuit involves up to 6 generations and 4000 km. Similar intercontinental migrations are suspected for Odonata, especially the globe skimmer dragonfly (Pantala flavescens [5,6,7]) and the green darner dragonfly (Anax junius [8]). Of course, many other Lepidoptera are known to migrate seasonally, as indicated by regular mass diurnal movements of individuals, but their origins and destinations remain largely unknown due to the difficulties in tracking small insects [2].
Recently, Satterfield et al. [9] reflected on our ignorance of insect migration in general in spite of the fact that such movements involve trillions of individuals. They reviewed the ways in which seasonal insect migrations can have important consequences for food webs, nutrient transport, pollination, and infectious disease. Importantly, they noted that, with current and predicted climate change, there is a very real possibility that seasonal insect migrations will be lost before they are documented. Clearly, there is an urgency, then, to document or describe insect migrations in concert with increased attention to declining insect numbers [10,11]. In addition, the concept of migratory connectivity been only applied to insect migration very recently [12]. This concept has important ramifications for insect conservation, especially for butterflies that typically migrate in the flight boundary layer and show a high degree of navigation ability and directed movement [13,14].
The study of animal migration has experienced quantum-level growth in recent decades, primarily due to the development of extrinsic markers that allow the tracking of individual animals at global scales [15,16,17,18]. This technological revolution has fueled an amazing array of studies showing the movements of previously poorly understood species and has advanced the field of animal movement tremendously. However, while such technological advances in tracking have been applied to smaller insects (e.g., [8,19]), in general, the study of insect migration has not benefitted from breakthroughs in individual tracking due to the obvious small size of most migratory insects. The use of intrinsic markers to infer origins, then, have been relatively better developed for insects, and the use of naturally occurring spatial patterns in genetics and stable isotope ratios (δ2H, δ18O, δ13C, δ15N) provides a means of inferring origins of individuals and populations [20]. This is because stable isotopes can show geographical patterns in primary production, and these isotopic patterns are passed onto higher-level consumers in predictable ways. For metabolically inert tissues such as wing chitin, stable isotope ratios are locked in once formed and the insect can be sampled at later periods or locations to infer origins through probabilistic assignment to isoscapes [21,22]. Indeed, the most well-studied migration of any insect using stable isotope analyses of wing chitin has been that of the eastern North American population of the monarch butterfly [23]. That analytical approach has since elucidated a number of ecological components of monarch migration and conservation [24,25,26,27,28].
Recently, Mora-Alvarez et al. [29] documented a fall migration bottleneck for monarch butterflies in northeast Mexico associated with 2 major highway crossings and predicted the annual roadkill mortality of monarchs at that site to be at least 197,000 individuals. This high mortality results from the geographic concentration of the southward bound monarchs by the Sierra Madre Oriental mountains, which forces monarchs into narrow canyons intercepted by highways. Although that study was focused on monarchs, it revealed the occurrence of massive movements of at least 36 species of other butterflies moving southward through the site. Indeed, fall migration of the family Pieridae, and especially of Libytheana carinenta, is well known in the states of Coahuila, Nuevo Leon, and Tamaulipas in northeastern Mexico [30,31,32], and local, largely anecdotal accounts have described the annual “colorful yellow and brown clouds” of butterflies (Nymphalidae and Pieridae) and other Papilionoidea families [33] through this region. However, in general, the origins and destinations of migrant butterflies at such concentration points remain entirely unknown.
We collected samples of seven species of fresh, road-killed butterfly through this bottleneck in October 2019 (Libytheana carinenta, Danaus gilippus, Phoebis sennae, Asterocampa leilia, Euptoieta claudia, Euptoieta hegesia, and Zerene cesonia). With the exception of the Mexican species E. hegesia that was intercepted in lower numbers and which was assumed to be more local, species were chosen based on their abundance, clear migration en mass through our site, and/or potential for long-distance movements. We chose species with generally assumed broad and narrow natal latitudinal distributions in North America and used stable hydrogen isotope analyses of wing chitin to estimate natal origins. Due to the clear north-south movement of butterflies through this site, we assumed that individuals were actively migrating and could potentially represent individuals originating anywhere to the north of the site and within their known distribution ranges. Our objective was to demonstrate how the stable isotope approach can be used to quickly and effectively provide information on key aspects of butterfly movements and act as a catalyst to document migratory origins of a broad suite of species.

2. Materials and Methods

2.1. Sampling Sites

Following the authors of [29], we focused on a highway along the Sierra Madre Oriental in the state of Nuevo Leon (Highway MEX 40-D, landmark km 58, Saltillo-Monterrey; 25°39′18.54″ N, 100°27′12.24″ W). The highway dissects the natural habitat of the region and is adjacent to the high-density urban center of Monterrey. A transect (5 km) was established along sections of the highway, before and after bridges crossing canyons, as these were the most likely sites for butterfly passage. The transect included the shoulder pavement and the ditch, a width which varied depending on the highway section sampled. All dead butterflies were collected each day and placed in glassine envelopes. All samples not destined for stable isotope analyses were deposited at the Entomology Laboratory of the Facultad de Ciencias Biologicas, Universidad Autónoma de Nuevo León, México. The transect was surveyed twice per week for a total of 13 sampling days between 26 September and 20 November 2019. Specimens selected were sorted to species using identification keys [34,35,36] and by consulting local experts. We focused on 7 species after sorting our total sample consisting of at least 36 species. Massive migrations were witnessed throughout the study at all sites described by the authors of [29].

2.2. The Species

Despite the recognition that the butterfly species we analyzed are indeed migratory, almost nothing appears to be known about their movements and ultimate migratory life history. One exception is L. carinenta. Three subspecies were possible in our sample, but we made no attempt to distinguish among them. L. carinenta bachmanii occurs as far north as Canada [37] but the breeding grounds of this species are primarily south Texas and north Mexico. Massive movements of L. carinenta are the result of high precipitation, which increases the rapid growing of sugarberry (Celtis laevigata) and hackberry (Celtis pallida) bushes that are their host plants and are available to support large numbers of individuals. Massive migration peaks in L. carinenta were recorded in July, September, and October in 1971 [32]. The authors of [32] concluded that the 3 generations moved between central and south Texas and north Mexico. High numbers of L. carinenta were recorded in central Kansas [32] flying north in September and October but coming from Texas. However, migration occurs because the population must move and find areas that can support these large numbers of individuals to accomplish their cycle [38]. The massive migration is a unique phenomenon, which is spectacular and has only been reported in predictive years [32]. However, the population has been well represented in large numbers in the other years. In Mexico, this phenomenon has not been studied and has only been observed and recorded in popular media [30,39]. We could define the massive migration of L. carinenta as a short-distance migration between Mexico and Texas. However, there are L. carinenta breeding records in the summer in south Canada and the United States [38]. Massive migration of the subspecies L. carinenta bachmanii has been recorded, and droughts and rain breaks have triggered the high numbers of the population in some years in Texas [32,40].
Distributions of the remaining species have largely been described according to the authors of [35]. The species E. claudia has a broad breeding range centered primarily in the southeastern United States that extends well into the east-central portion of the continent. The congeneric Mexican fritillary E. hegesia is centered more in distribution in Mexico. The population of P. sennae is more centered in the southern United States and throughout northern Mexico and is well recognized for its seasonal migrations [37,41,42]. Migration to and overwintering in Florida has been recorded [43]. The species Danaus gilippus occurs primarily in the southwestern United States, but the species also occurs in Florida and along the coast of the Gulf of Mexico, as well as throughout northern Mexico. Simultaneous migration of D. gilippus and D. plexippus in central and south Texas and northern Mexico has been recorded [29]. January records of the species in Veracruz, Mexico hint at a possible winter destination [44]. Aterocampa leilia has a narrow distribution in the southwestern United States, and the range is split down the northeast and northwest regions of Mexico as separated by the Sierra Madre Oriental and Sierra Madre Occidental mountain ranges. The species is resident in Arizona and central Texas [32,45]. January records in Tamaulipas, Mexico point again to potential coastal destinations [44]. Zerene cesonia breeds primarily in the southern United States and throughout northern Mexico but also can potentially derive from the central United States. The species cannot overwinter in Canada but is regularly recorded there [37]. It is unknown if individuals arriving north in spring to the United States are the first or second generation from Mexico. There is no evidence for spring migration but the number of individuals possibly exhibiting spring migration are so few to be below the threshold of detection.

2.3. Stable Isotope Analyses

Wings were soaked in a 2:1 chloroform:methanol solution, rinsed, and then dried overnight in a fume hood. Samples of 0.35 ± 0.02 mg of wing membrane were weighed into pressed silver 3.5 × 5 mm capsules and analyzed using a Eurovector Uniprep autosampler (Milan, Italy) carousel attached to a Eurovector 3000 Elemental Analyzer, coupled to a Thermo Delta V Plus isotope ratio mass spectrometer (Bremen, Germany) in continuous flow mode with helium carrier gas. After the samples were loaded, the Uniprep autosampler (heated to 60 °C) was vacuum evacuated and subsequently flushed with dry helium twice to remove adsorbed atmospheric moisture from the crushed silver capsules. The autosampler was then held under positive helium pressure for the duration of the analytical run. Two USGS keratin standards, EC-01 (formerly CBS: Caribou Hoof Standard) and EC-02 (KHS: Kudu Horn Standard of Environment Canada), were included every 10 samples. An internal laboratory standard, powdered keratin (MP Biomedicals Inc., Cat No. 90211, Lot No.9966H), was included to monitor instrument drift and provide a check on accuracy over the course of each analytical session. Samples were combusted at 1350 ℃ using glassy carbon. Values of δ2H of nonexchangeable hydrogen were derived using the comparative equilibration approach of [46] and calibrated to the Vienna Standard Mean Ocean Water (VSMOW) international standard using EC-01 (±1.9‰ 1 SD, n = 18, accepted δ2H = −197.0‰) and EC-02 (±1.6‰, n = 17, accepted δ2H = −54.1‰). We confirmed that this approach resulted in identical assignments if new calibration standards (EC-01 accepted −157.0‰; EC-02 accepted −35.3‰) were used with correspondingly modified assignment algorithms (see below; [47]), and measurements for both sets of standards are reported in Table 1 and Supplementary Material Table S1. The overall measurement error for EC-01 and EC-02 δ2H was ~2‰.

2.4. Assignment to Origin

We depicted the origins of wild monarchs caught in Mexico using a likelihood-based assignment method [48,49,50], using the wing chitin δ2H isoscape (δ2Hw) and an amount-weighted precipitation-to-wing calibration algorithm (δ2Hw = 0.78 ∗ δ2Hp − 77.4) described by the authors of [28]. This was used to convert amount-weighted mean annual precipitation δ2H (δ2Hp) isoscapes [51,52] into δ2Hw isoscapes. We used the 9.3‰ residual SD error from this regression in our assignments [29]. We then created a spatial layer representing the known geographic range of the breeding populations of each butterfly species from Brock and Kaufman [35] and used this as a mask (i.e., clip) to limit our assignment to origin analyses.
We estimated the likelihood that a cell (pixel) within the δ2Hw isoscape represented a potential origin for a sample using a normal probability density function to estimate the likelihood function based on the observed δ2Hw. Thus, we depicted the likely origins of each butterfly by assigning individuals to the δ2Hw isoscape one at a time. We arbitrarily chose a 2:1 odds ratio to include only those pixels (coded 1) with at least a 67% probability of origin vs. all others (coded 0). This resulted in a map of binary values for each assigned individual representing presence (1) or absence (0) for each cell in the isoscape. We then summed the results of individual assignments by stacking the surfaces. We made geographic assignments to origin using functions within the R statistical computing environment v. 4.0.3 [53] within RStudio v. 1.3.95 [54] using the ‘raster’ v. 3.3-13 [55], rasterVis v. 0.48 [56], sp v. 1.4-4 [57], and sf v. 0.9-6 [58] packages. Thus, the final assignment surface depicted the number of individuals co-assigned at each pixel based on the odds criteria.

3. Results

Results of δ2H analyses of wing chitin from the seven species of butterflies we sampled are presented in Table 1. As expected, we found isotopic differences among species (ANOVA F6,470 = 35.9, p < 0.0001), but also clearly identified two groups of species corresponding approximately to long-distance migrants (L. carinenta, E. claudia, D. glippus, Z. cesonia) and short-distance migrants (A. leilia, E. hegesia, P. sennae; Table 1, unequal variance t-test: t = 14.8, p < 0.0001).
With the exception of the Mexican species E. hegesia, whose range is restricted primarily to Mexico, we assigned all species (i.e., n = 6 species) to probability of origin surfaces within their range. Summary isotopic data are provided in Table 1 that indicate a range from more northern origins (i.e., more negative δ2Hw values) to closer origins (indicated by more positive δ2Hw values). These data are followed by individual species accounts. In all cases, we note that potential origins usually include northwestern Mexico. We suggest this is simply due to the ambiguous nature of the underlying precipitation isoscape in this region, which is similar to that of northeastern Mexico. For completeness, we included the whole of northern Mexico in our depictions. However, biologically, we consider the northwestern region of Mexico to be a highly unlikely origin for all species due to the occurrence of the Sierra Madre mountains.

3.1. Libytheana Carinenta

Libytheana carinenta had the most negative average δ2Hw values, indicating that this species has most northern origins among the species we studied. Indeed, some individuals clearly were consistent with origins from the northernmost extent of the range (Figure 1).
However, the majority of the assignment was consistent, with origins generally south of the Great Lakes and throughout the southeastern USA as generally reported in the literature. The sample size of this species and the long duration of sampling also allowed us to examine the pattern of migration through the site. After removing four outliers with δ2Hw values between −195‰ and −200‰ (i.e., indicating origins well north of the expected breeding range), we found a negative correlation between δ2Hw values and the day of sampling (Figure 2, p < 0.0001), which suggests a chain migration pattern with more northern-produced butterflies arriving later than more southern-produced individuals.

3.2. Euptoieta Claudia

Euptoieta claudia also showed potential origins well north of northern Mexico and primarily in the southeastern United States. The species also showed a possible finger-like extension west of the Appalachians through to the southern Great Lakes, corresponding largely with the Mississippi River drainage (Figure 1).

3.3. Danaus Gilippus

Danaus gilippus showed similar potential origins to the other two highly migratory species, L. carinenta and E. claudia, with a concentration to the southeastern portion of the range and an extension through the Mississippi River Valley to the southern Great Lakes (Figure 1). The large sample size and the long period of collection allowed us to examine the effect of sampling date on δ2Hw values. We found a weak but significant increase in δ2Hw values with time (Figure 3), suggesting either a pattern of migration with a latitude of origin or possibly more northern butterflies tending to arrive first.

3.4. Zerene Cesonia

This species showed a remarkable similarity in potential origins to those described above (Figure 4, Table 1). We found no relationship between δ2Hw values and day of collection (slope = 0.03, r2 = 0.007, n = 73).

3.5. Asterocampa Leilia

Despite large movements of this species through our study site, our findings clearly indicate that this species has little chance of originating north of Mexico, as confirmed by the more positive δ2Hw values (Figure 4, Table 1). As such, isotopic results for this species confirm a status of short-distance migration, primarily within Mexico and adjacent Arizona [45].

3.6. Euptoieta Hegesia

Due to the low sample size of this species (N = 14) and its narrow window of sampling, we did not produce an assignment to the origin map. Nonetheless, the species served as a useful “control,” with expected higher δ2Hw values (mean −70.2 ± 9.3‰) consistent with more southern (Mexican) origins (Table 1) Phoebis sennae.
This species was the second-most enriched in 2H (Table 1), largely suggesting that individuals were derived from southern latitudes, including northeast Mexico. However, the population sampled at our site showed potential origins also around the Gulf states to the northeast of our site.

4. Discussion

Following previous studies on monarch butterflies in North America, our investigation demonstrates the utility of sampling butterflies at a fall migratory bottleneck in northeast Mexico as a means of inferring their latitudinal origins through the measurement of wing δ2H values. This approach is well suited to quickly determine the structure of migratory butterfly populations by making use of the substantial mortality that occurs at highway crossings, as demonstrated by Mora Alvarez et al. [29]. Without a priori expectations, we determined that four of the seven species examined (L. carinenta, Z. cesonia, E. claudia, D. gilippus) included individuals that can be considered long-distance migrants, with individuals travelling throughout their range in the United States and southern Canada and hence reflecting distances of up to several thousands of kilometers. We suggest that these species would be useful candidates for more in-depth measurements of wing size as this has been associated with distance of migration (e.g., [25,27]). The remaining three species (P. sennae, A. leilia, E. hegesia) were clearly migrating south en mass through our study site even though their origins were much more local. For three species, we were additionally able to evaluate patterns of movement through our site relative to latitude of origin. Here, our results were consistent with migratory panmixia (Z. cesonia), chain (Libytheana carinenta), and leapfrog (Danaus gilippus) migrations as has been described for other taxa [1]. Of course, other explanations are possible, and we note that the regressions between wing δ2H and date of passage were relatively weak.
The impressive fall movement of butterflies through northeast Mexico is virtually unstudied. Thus, our research is but a first step in describing migration across a subsample of species. Indeed, while we identified the approximate origins of seven species, we, of course, have no idea of their ultimate destinations. Anecdotal evidence points to possible destination in the northern Mexican coastal states, especially Tamaulipas [59]. In addition, we cannot currently distinguish between regular migration per se and dispersal related more to climate and resource conditions [2]. We strongly recommend field censuses that are designed to identify potential overwinter destinations of these and other species so that true migratory connectivity can be established through the complimentary isotopic measurement of wintering individuals (e.g., [4,27,60,61]).
We clearly demonstrated that the stable isotope approach to delineating butterfly origins in North America provides a particularly convenient tool to quickly document origins and migration in species with poorly known life history. This is because isoclines of precipitation δ2H, and hence butterfly wing δ2H, follow a particularly well-established latitudinal gradient (see figure in [61]), a phenomenon that has led to the isotopic tracing of origins for numerous taxa [21]. Insects that concentrate at migratory bottlenecks such as the species used by us in northern Mexico are especially amenable for assignment to an isotopic atlas. The salvaging of fresh road-killed individuals at such sites also removes the need to sacrifice live individuals and potentially provides a large sample for assay. In addition to continuing sampling of the numerous species of butterflies passing through migratory bottlenecks in autumn, sampling of migrant butterflies during the winter months in Mexico and possibly Central America and the Caribbean would be especially useful to link breeding and wintering sites [62]. We see this call for action as an essential component of the recent concern expressed by Satterfield et al. [9] that we stand to lose valuable migratory insect populations long before they are even described.

Supplementary Materials

The following are available online at https://www.mdpi.com/1424-2818/13/3/102/s1, Table S1: Supplementary data for all butterflies sampled near Monterrey Mexico in 2019.

Author Contributions

Conceptualization, K.A.H.; Methodology, K.A.H., B.X.M.-A., J.W.K.; Statistical Analysis, K.A.H. and J.W.K.; Writing—Original Draft Preparation, K.A.H.; Writing—Review & Editing, K.A.H., B.X.M.-A., J.W.K.; Visualization, K.A.H. and J.W.K.; Supervision, K.A.H. and B.X.M.-A.; Project Administration, K.A.H. and B.X.M.-A.; Funding Acquisition, K.A.H. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by an NSERC Discovery grant to KAH (2017-04430).

Informed Consent Statement

Not applicable.

Data Availability Statements

The data presented in this study are available in supplementary material here.

Acknowledgments

Special thanks to our field assistant Carlos Carrera-Treviño for his excellent assistance and Rocio Treviño Ulloa for her dedication and contribution to recording of butterfly sightings in the Correo Real Program which was supported by many volunteers. We thank Jose Davila Paulin for his insights on the movements of butterflies and help with surveys in the north of Coahuila. We thank two anonymous reviewers for their helpful comments on a previous version of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Dingle, H. Migration: The Biology of Life on the Move, 2nd ed.; Oxford University Press: Oxford, UK, 2014; ISBN 0-19-964039-4. [Google Scholar]
  2. Chapman, J.W.; Reynolds, D.R.; Wilson, K. Long-range seasonal migration in insects: Mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 2015, 18, 287–302. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Chapman, J.W.; Lim, K.S.; Reynolds, D.R. The significance of midsummer movements of Autographa gamma: Implications for a mechanistic understanding of orientation behavior in a migrant moth. Curr. Zool. 2013, 59, 360–370. [Google Scholar] [CrossRef] [Green Version]
  4. Stefanescu, C.; Soto, D.X.; Talavera, G.; Vila, R.; Hobson, K.A. Long-Distance autumn migration across the Sahara by painted lady butterflies: Exploiting resource pulses in the Tropical Savannah. Biol. Lett. 2016, 12, 20160561. [Google Scholar] [CrossRef] [Green Version]
  5. Anderson, R.C. Do dragonflies migrate across the western Indian Ocean? J. Trop. Ecol. 2009, 25, 347–358. [Google Scholar] [CrossRef]
  6. Hobson, K.A.; Anderson, R.C.; Soto, D.X.; Wassenaar, L.I. Isotopic evidence that dragonflies (Pantala Flavescens) migrating through the Maldives come from the northern Indian Subcontinent. PLoS ONE 2012, 7, e52594. [Google Scholar] [CrossRef]
  7. Hobson, K.A.; Jinguji, H.; Ichikawa, Y.; Kusack, J.W.; Anderson, R.C. Long-distance migration of the globe skimmer dragonfly to Japan revealed using stable hydrogen (δ2H) isotopes. Environ. Entomol. 2020, 1–9. [Google Scholar] [CrossRef]
  8. Wikelski, M.; Moskowitz, D.; Adelman, J.S.; Cochran, J.; Wilcove, D.S.; May, M.L. Simple rules guide dragonfly migration. Biol. Lett. 2006, 2, 325–329. [Google Scholar] [CrossRef] [PubMed]
  9. Satterfield, D.A.; Sillett, T.S.; Chapman, J.W.; Altizer, S.; Marra, P.P. Seasonal insect migrations: Massive, influential, and overlooked. Front. Ecol. Environ. 2020, 18, 335–344. [Google Scholar] [CrossRef]
  10. Sánchez-Bayo, F.; Wyckhuys, K.A.G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 2019, 232, 8–27. [Google Scholar] [CrossRef]
  11. Wagner, D.L.; Grames, E.M.; Forister, M.L.; Berenbaum, M.R.; Stopak, D. Insect decline in the anthropocene: Death by a thousand cuts. Proc. Natl. Acad. Sci. USA 2021, 118, e2023989118. [Google Scholar] [CrossRef]
  12. Gao, B.; Hedlund, J.; Reynolds, D.R.; Zhai, B.; Hu, G.; Chapman, J.W. The ‘migratory connectivity’ concept, and its applicability to insect migrants. Mov. Ecol. 2020, 8, 48. [Google Scholar] [CrossRef]
  13. Srygley, R.B.; Dudley, R. Optimal strategies for insects migrating in the flight boundary layer: Mechanisms and consequences. Integr. Comp. Biol. 2008, 48, 119–133. [Google Scholar] [CrossRef] [Green Version]
  14. Chapman, J.W.; Klaassen, R.H.; Drake, V.A.; Fossette, S.; Hays, G.C.; Metcalfe, J.D.; Reynolds, A.M.; Reynolds, D.R.; Alerstam, T. Animal orientation strategies for movement in flows. Curr. Biol. 2011, 21, R861–R870. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Wikelski, M.; Kays, R.W.; Kasdin, N.J.; Thorup, K.; Smith, J.A.; Swenson, G.W. Going wild: What a global small-animal tracking system could do for experimental biologists. J. Exp. Biol. 2007, 210, 181–186. [Google Scholar] [CrossRef] [Green Version]
  16. Bridge, E.S.; Kelly, J.F.; Contina, A.; Gabrielson, R.M.; MacCurdy, R.B.; Winkler, D.W. Advances in tracking small migratory birds: A technical review of light-level geolocation. J. Field Ornithol. 2013, 84, 121–137. [Google Scholar] [CrossRef]
  17. Taylor, P.D.; Crewe, T.; Mackenzie, S.; Lepage, D.; Aubry, Y.; Crysler, Z.; Finney, G.; Francis, C.; Guglielmo, C.; Hamilton, D.; et al. The motus wildlife tracking system: A collaborative research network to enhance the understanding of wildlife movement. Avian Conserv. Ecol. 2017, 12, 8. [Google Scholar] [CrossRef]
  18. Hobson, K.A.; Norris, D.R.; Kardynal, K.J.; Yohannes, E. Animal migration: A context for using new techniques and approaches. In Tracking Animal Migration with Stable Isotopes; Hobson, K.A., Wassenaar, L.I., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 1–24. ISBN 978-0-12-814723-8. [Google Scholar]
  19. Knight, S.M.; Pitman, G.M.; Flockhart, D.T.T.; Norris, D.R. Radio-tracking reveals how wind and temperature influence the pace of daytime insect migration. Biol. Lett. 2019, 15, 20190327. [Google Scholar] [CrossRef]
  20. Hobson, K.A.; Doward, K.; Kardynal, K.J.; McNeil, J.N. Inferring origins of migrating insects using isoscapes: A case study using the true armyworm, mythimna unipuncta, in North America. Ecol. Entomol. 2018, 43, 332–341. [Google Scholar] [CrossRef]
  21. Bowen, G.J.; West, J.B. Isoscapes for terrestrial migration research. In Tracking Animal Migration with Stable Isotopes, 2nd ed.; Hobson, K.A., Wassenaar, L.I., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 53–84. ISBN 978-0-12-814723-8. [Google Scholar]
  22. Wunder, M.B.; Norris, D.R. Design and analysis for isotope-based studies of migratory animals. In Tracking Animal Migration with Stable Isotopes; Hobson, K.A., Wassenaar, L.I., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 191–206. ISBN 978-0-12-814723-8. [Google Scholar]
  23. Hobson, K.A.; Wassenaar, L.I.; Taylor, O.R. Stable isotopes (ΔD and δ13C) Are geographic indicators of natal origins of monarch butterflies in Eastern North America. Oecologia 1999, 120, 397–404. [Google Scholar] [CrossRef]
  24. Miller, N.G.; Wassenaar, L.I.; Hobson, K.A.; Norris, D.R. Migratory connectivity of the monarch butterfly (Danaus Plexippus): Patterns of spring re-colonization in Eastern North America. PLoS ONE 2012, 7, e31891. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Altizer, S.; Hobson, K.A.; Davis, A.K.; De Roode, J.C.; Wassenaar, L.I. Do healthy monarchs migrate farther? Tracking natal origins of parasitized vs. uninfected monarch butterflies overwintering in Mexico. PLoS ONE 2015, 10, e0141371. [Google Scholar] [CrossRef] [Green Version]
  26. Flockhart, D.T.T.; Wassenaar, L.I.; Martin, T.G.; Hobson, K.A.; Wunder, M.B.; Norris, D.R. Tracking multi-generational colonization of the breeding grounds by monarch butterflies in Eastern North America. Proc. R. Soc. B Biol. Sci. 2013, 280, 1–8. [Google Scholar] [CrossRef]
  27. Flockhart, D.T.T.; Fitz-gerald, B.; Brower, L.P.; Derbyshire, R.; Altizer, S.; Hobson, K.A.; Wassenaar, L.I.; Norris, D.R. Migration distance as a selective episode for wing morphology in a migratory insect. Mov. Ecol. 2017, 5, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Hobson, K.A.; Kardynal, K.J.; Koehler, G. Expanding the isotopic toolbox to track monarch butterfly (Danaus Plexippus) origins and migration: On the utility of stable oxygen isotope (δ18O) measurements. Front. Ecol. Evol. 2019, 7, 224. [Google Scholar] [CrossRef] [Green Version]
  29. Mora Alvarez, B.X.; Carrera-Treviño, R.; Hobson, K.A. Mortality of monarch butterflies (Danaus Plexippus) at two highway crossing “Hotspots” during autumn migration in northeast Mexico. Front. Ecol. Evol. 2019, 7, 273. [Google Scholar] [CrossRef] [Green Version]
  30. Fager, E.W. Migration notes from Mexico. Lepidoptera News 1952, 6, 44. [Google Scholar]
  31. Clench, H.K. Butterflies from Coahuila, Mexico. J. Lepidopterists’ Soc. 1968, 22, 227–231. [Google Scholar]
  32. Neck, R.W. Causal analysis of a migration of the snout butterfly, Libytheana Bachmanii Iarvata (Strecker) (Libytheidae). J. Lepidopterists’ Soc. 1983, 37, 121–128. [Google Scholar]
  33. Sada, M.L.; Madero, F.A. Guía de Mariposas de Nuevo León; Fondo Editorial de Nuevo Leon, UANL: Monterrey, Mexico, 2011; ISBN 607-7577-76-6. [Google Scholar]
  34. Brock, J.P.; Kaufman, K. Butterflies of North America, Hillstar Editions L.C.; Houghton Mifflin Harcourt: Boston, MA, USA, 2003. [Google Scholar]
  35. Flores, V.J. Mariposas Del Sureste de Coahuila, 1st ed.; Secretaria de Medio Ambiente de Coahuila: Coahuila, Mexico, 2016. [Google Scholar]
  36. Glassberg, J. A Swift Guide to Butterflies of Mexico and Central America, 2nd ed.; Princeton University Press: Princeton, NJ, USA, 2018; ISBN 1-4008-8986-3. [Google Scholar]
  37. Layberry, R.A.; Hall, P.W.; Lafontaine, J.D. The Butterflies of Canada; University of Toronto Press: Toronto, ON, Canada, 1998; ISBN 0-8020-7881-8. [Google Scholar]
  38. Clark, A.H. Some observations on butterfly migrations. Sci. Mon. 1931, 32, 150–155. [Google Scholar]
  39. Menchaca, A. Vive Ciudad Lluvia de Mariposas. 2012. Available online: https://www.elnorte.com/vida (accessed on 23 February 2021).
  40. Helfert, M.R. Migratory behavior of the snout butterfly, Libytheana Bachmanii Larvata (Strecker). Entomol. News 1972, 83, 49–52. [Google Scholar]
  41. Williams, C.B. Insect migration. Annu. Rev. Entomol. 1957, 2, 163–180. [Google Scholar] [CrossRef]
  42. Walker, T.J. Butterfly migrations in Florida: Seasonal patterns and long-term changes. Environ. Entomol. 2001, 30, 1052–1060. [Google Scholar] [CrossRef] [Green Version]
  43. Walker, T.J. Butterfly migration in the boundary layer. J. Lepidopterists’ Soc. 1985, 37, 704–723. [Google Scholar]
  44. Miller, L.D.; Clench, H.K. Some aspects of mating behavior in butterflies. J. Lepidopterists’ Soc. 1968, 22, 125–132. [Google Scholar]
  45. Austin, G.T. Phenology and diversity of a butterfly population in Southern Arizona. J. Lepidopterists’ Soc. 1978, 32, 207–220. [Google Scholar]
  46. Wassenaar, L.I.; Hobson, K.A. Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environ. Health Stud. 2003, 39, 211–217. [Google Scholar] [CrossRef] [PubMed]
  47. Soto, D.; Koehler, G.; Wassenaar, L.; Hobson, K. Determination of stable hydrogen isotopic compositions of complex organic materials: Contrasting the role of exchangeable hydrogen and residual moisture. Rapid Comm. Mass Spectrom 2017, 31, 1193–1203. [Google Scholar] [CrossRef] [PubMed]
  48. Hobson, K.A.; Wunder, M.B.; Van Wilgenburg, S.L.; Clark, R.G.; Wassenaar, L.I. A Method for investigating population declines of migratory birds using stable isotopes: Origins of harvested lesser scaup in North America. PLoS ONE 2009, 4, e7915. [Google Scholar] [CrossRef]
  49. Van Wilgenburg, S.L.; Hobson, K.A.; Brewster, K.; Welker, J. Assessing dispersal in threatened migratory birds using stable hydrogen isotope (ΔD) analysis of feathers. Endanger. Species Res. 2012, 16, 17–29. [Google Scholar] [CrossRef] [Green Version]
  50. Wunder, M.B. Using isoscapes to model probability surfaces for determining geographic origins. In Isoscapes: Understanding Movement, Pattern, and Process on Earth through Isotope Mapping; West, J.B., Bowen, G.J., Dawson, T.E., Tu, K.P., Eds.; Springer: Dordrecht, The Netherlands, 2010; pp. 251–270. ISBN 978-90-481-3354-3. [Google Scholar]
  51. Bowen, G.J.; Wassenaar, L.I.; Hobson, K.A. Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 2005, 143, 337–348. [Google Scholar] [CrossRef] [PubMed]
  52. Bowen, G.J. Gridded Maps of the Isotopic Composition of Meteoric Waters; The University of Utah: Salt Lake City, UT, USA, 2019. [Google Scholar]
  53. R Core Team R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2020.
  54. RStudio Team RStudio: Integrated Development for R; RStudio, Inc.: Boston, MA, USA, 2020.
  55. Hijmans, R.J. Raster: Geographic Data Analysis and Modeling; R Package Version 33-13; R Core Team: Vienna, Austria, 2020. [Google Scholar]
  56. Lamigueiro, O.P.; Hijmans, R. RasterVis. R Package Version 048; R Core Team: Vienna, Austria, 2020. [Google Scholar]
  57. Pebesma, E.; Bivand, R. Classes and methods for Spatial Data in R. R. News 2005, 5, 9–13. [Google Scholar]
  58. Pebesma, E. Simple features for R: Standardized support for spatial vector data. R. J. 2018, 10, 439–446. [Google Scholar] [CrossRef] [Green Version]
  59. Byers, G.B. A Migration of Klicogonia Castalia (Pieridae) in Northern Mexico. J. Lepidopterists’ Soc. 1971, 3, 124–125. [Google Scholar]
  60. Wassenaar, L.I.; Hobson, K.A. Natal origins of migratory monarch butterflies at wintering colonies in Mexico: New isotopic evidence. Proc. Natl. Acad. Sci. USA 1998, 95, 15436–15439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Hobson, K.A.; García-Rubio, O.R.; Carrera-Treviño, R.; Anparasan, L.; Kardynal, K.J.; Mcneil, J.; García-Serrano, E.; Mora Alvarez, B.X. Isotopic (δ2H) Analysis of stored lipids in migratory and overwintering monarch butterflies (Danaus Plexippus): Evidence for southern critical late-stage nectaring sites? Front. Ecol. Evol. 2020, 8, 572140. [Google Scholar] [CrossRef]
  62. Hobson, K.A.; Van Wilgenburg, S.L.; Faaborg, J.; Toms, J.D.; Rengifo, C.; Sosa, A.L.; Aubry, Y.; Brito Aguilar, R. Connecting breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopes: A call for an isotopic atlas of migratory connectivity: Isotopic atlas of connectivity. J. Field Ornithol. 2014, 85, 237–257. [Google Scholar] [CrossRef]
Diversity 13 00102 g001 550
Figure 1. Probabilistic assignment to origin for three (longer-distance) species of butterfly intercepted during fall migration in northeast Mexico, 2019. The figure key refers to the number of individuals assigned per pixel according to a 2:1 odds criterion (see Methods).
Figure 1. Probabilistic assignment to origin for three (longer-distance) species of butterfly intercepted during fall migration in northeast Mexico, 2019. The figure key refers to the number of individuals assigned per pixel according to a 2:1 odds criterion (see Methods).
Diversity 13 00102 g001
Diversity 13 00102 g002 550
Figure 2. Relationship between wing δ2H and day of collection for Libytheana carinenta intercepted in fall migration 2019 in northeast Mexico. Y = −0.58X − 81.4, r2 = 0.2. Day 0 is 26 September.
Figure 2. Relationship between wing δ2H and day of collection for Libytheana carinenta intercepted in fall migration 2019 in northeast Mexico. Y = −0.58X − 81.4, r2 = 0.2. Day 0 is 26 September.
Diversity 13 00102 g002
Diversity 13 00102 g003 550
Figure 3. Relationship between wing δ2H and day of collection for Danaus gilippus. Intercepted in fall migration 2019 in northeast Mexico. Y = 0.35X − 87.5. r2 = 0.11. Day 0 is 14 October.
Figure 3. Relationship between wing δ2H and day of collection for Danaus gilippus. Intercepted in fall migration 2019 in northeast Mexico. Y = 0.35X − 87.5. r2 = 0.11. Day 0 is 14 October.
Diversity 13 00102 g003
Diversity 13 00102 g004 550
Figure 4. Probabilistic assignment to origin for three (shorter-distance) species of butterfly intercepted during fall migration in northeast Mexico, 2019. The figure key refers to the number of individuals assigned per pixel according to a 2:1 odds criterion (see Methods).
Figure 4. Probabilistic assignment to origin for three (shorter-distance) species of butterfly intercepted during fall migration in northeast Mexico, 2019. The figure key refers to the number of individuals assigned per pixel according to a 2:1 odds criterion (see Methods).
Diversity 13 00102 g004
Table
Table 1. Summary of wing stable hydrogen isotope (δ2H) (mean ±SD, Vienna Standard Mean Ocean Water (VSMOW) ‰) for 7 species of road-killed butterflies moving through a migratory bottleneck highway crossing near Monterrey, Mexico in 2019. Superscript letters are the results of a Tukey post-hoc analysis whereby similar letters indicate no significant difference (p < 0.05). Wing δ2H values calibrated to old values (EC-01 = −197‰, EC-02 = −54.1‰) and new values (EC-01 = −157‰, EC-02 = −35.3‰) are listed.
Table 1. Summary of wing stable hydrogen isotope (δ2H) (mean ±SD, Vienna Standard Mean Ocean Water (VSMOW) ‰) for 7 species of road-killed butterflies moving through a migratory bottleneck highway crossing near Monterrey, Mexico in 2019. Superscript letters are the results of a Tukey post-hoc analysis whereby similar letters indicate no significant difference (p < 0.05). Wing δ2H values calibrated to old values (EC-01 = −197‰, EC-02 = −54.1‰) and new values (EC-01 = −157‰, EC-02 = −35.3‰) are listed.
SpeciesNCollectionδ2H (‰) Old Stdδ2H (‰) New Std
L. carinenta16326 September to 4 November−94.9±21.6a−68.7±18.2
E. claudia2514 October to 20 November−85.7±13.4b−62.8±11.4
D. gilippus10014 October to 20 November−82.9±10.7b−59.6±9.1
Z. cesonia7326 September to 20 November−81.1±11.4b−58.5±9.7
A. leilia388 October to 2 November−70.42.5±6.3c−50.9±5.4
E. hegesia138 October to 4 November−69.8±9.4c−49.1±8.1
P. sennae654 October to 20 November−65.16.0±13.2c−46.6±11.9
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Hobson, K.A.; Kusack, J.W.; Mora-Alvarez, B.X. Origins of Six Species of Butterflies Migrating through Northeastern Mexico: New Insights from Stable Isotope (δ2H) Analyses and a Call for Documenting Butterfly Migrations. Diversity 2021, 13, 102. https://doi.org/10.3390/d13030102

AMA Style

Hobson KA, Kusack JW, Mora-Alvarez BX. Origins of Six Species of Butterflies Migrating through Northeastern Mexico: New Insights from Stable Isotope (δ2H) Analyses and a Call for Documenting Butterfly Migrations. Diversity. 2021; 13(3):102. https://doi.org/10.3390/d13030102

Chicago/Turabian Style

Hobson, Keith A., Jackson W. Kusack, and Blanca X. Mora-Alvarez. 2021. "Origins of Six Species of Butterflies Migrating through Northeastern Mexico: New Insights from Stable Isotope (δ2H) Analyses and a Call for Documenting Butterfly Migrations" Diversity 13, no. 3: 102. https://doi.org/10.3390/d13030102

APA Style

Hobson, K. A., Kusack, J. W., & Mora-Alvarez, B. X. (2021). Origins of Six Species of Butterflies Migrating through Northeastern Mexico: New Insights from Stable Isotope (δ2H) Analyses and a Call for Documenting Butterfly Migrations. Diversity, 13(3), 102. https://doi.org/10.3390/d13030102

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop