Migratory Delays Research Articles

Culverts delay upstream and downstream migrations of river herring (Alosa spp.)

AbstractAlewife (Alosa pseudoharengus) and blueback herring (Alosa aestivalis) are iteroparous anadromous fish found throughout the East Coast of North America. The phenology of anadromous fish migrations is important for fitness, and the duration of spawning migrations has been compressed in recent years in response to climate change. Anthropogenic barriers to movement, such as dams and culverts at road‐stream crossings, can further disrupt migration phenology by delaying movement and increasing predation risk. We used passive integrated transponder (PIT) telemetry to quantify upstream and downstream migratory delay at five road‐stream‐crossing culverts on the Herring River (MA, USA). Groundspeeds were reduced at all culverts in both directions, confirming that the culverts impede movement despite high passage proportions. The cumulative delay of the culverts on the upstream migration was sufficient to more than double the amount of time required to traverse the river if the culverts had been absent. Furthermore, the presence of snapping turtles (Chelydra serpentina) ambushing river herring within one of the culverts resulted in reduced passage rates beyond the reduction in movement caused by the physical structure itself. This highlights that physical barriers can create cascading ecological consequences and the importance of taking a holistic approach to understanding barrier effects.

Overwintering and migration behaviour of post‐spawned Atlantic salmon Salmo salar in a large hydropower‐regulated river and reservoir

Tracking 47 post-spawned adult Atlantic salmon Salmo salar L. in a hydropower-regulated river through autumn, winter and spring revealed that winter survival was 56% and 75% in two study years, respectively, with higher mortality of males than females (50% vs. 33% and 100% vs. 13%, respectively). Some kelts (n=7) displayed nondirected movements that were interpreted as a reconditioning period for an average of 9-17 days prior to directed downstream movements indicating the initiation of migration. Survival after the initiation of migration in spring was 83% and 94% to the hydropower dam in the first and second study years, and decreased to 60 and 63%, respectively, after dam passage. There were no further losses in the downriver reach in the second year, with the first year having a cumulative survival estimate of 53% to the river mouth. Kelts approached the dam when the spillway gates were available as a passage option most of the time (64%-75%), but some kelts arrived at the dam or had not yet passed when spillways were closed (n=6) and the only remaining passage option was restricted to the turbines. However, all but one kelt that must have passed via turbine were successful in reaching the river mouth. Migratory delay presumably due to searching behaviour caused by low water flow was estimated at approximately 6 days as migration rates were significantly slower in the reservoir (median ± s.e. 8.5 ± 2.5km day-1 ) than up- (29.7 ± 5.0km day-1 ) or downriver (22.1 ± 3.1km day-1 ). The proportion of time (median 30%) that kelts spent swimming upstream (searching behaviour) in the reservoir was a significant variable for migration success.

Atlantic Salmon Upstream Migration Delay in a Large Hydropower Reservoir

AbstractSpawning success of Atlantic Salmon Salmo salar is challenged when migratory routes to natal streams are obstructed by hydropower generation stations and reservoirs that lack directional cues, potentially causing migratory delay. This study used 74 acoustic‐tagged adult Atlantic Salmon during their spawning migrations to quantify migratory success, rates, and delay through the Mactaquac Reservoir in the Saint John River, New Brunswick, during three migration seasons in 2014–2016. Tag loss or mortality was considerable, reducing the effective sample size to 34 successfully tracked adults. Of these, 41% experienced fallback over the dam, 12% were unsuccessful in exiting the reservoir, and 47% were successful in exiting the reservoir on the way to the spawning grounds. Migration rates were significantly slower in the reservoir (median ± SE = 9.3 ± 1.9 km/d) than upriver (39.0 ± 4.1 km/d), and the tagged Atlantic Salmon spent 31–53% of their time reversing direction and thus travelled longer distances (73 ± 58 km) than the minimum 37‐km midline route through the reservoir. Traveling the distance of the reservoir at the upriver migration rate could have shortened their journey by a median of 3.8 d. Sensor tags indicated that individual Atlantic Salmon experienced temperatures of 10–20°C (median ± SE = 16.0 ± 0.03°C) and migrated at depths of 5–35 m (23.4 ± 0.1 m) within the reservoir. Given that some of the energy needed for reproductive development and activities was likely appropriated by migratory delay and that a moderate proportion (47%) of adults emigrated from the reservoir, volitional passage may not be a successful management strategy in the studied reservoir. However, a substantially reduced sample size negates conclusive remarks about which management strategy would maximize survival and spawning success, and further study is needed.

Thermal sensitivity and flow-mediated migratory delays drive climate risk for coastal sockeye salmon

Climate change is subjecting aquatic species to increasing temperatures and shifting hydrologic conditions. Understanding how these changes affect individual survival can help guide conservation and management actions. Anadromous Pacific salmon ( Oncorhynchus spp.) in some large river systems are acutely impacted by the river temperatures and flows encountered during their spawning migrations. However, comparatively little is known about drivers of en route mortality for salmon in smaller coastal watersheds, and climate impacts may differ across watersheds and locally adapted salmon populations. To understand the effects of climate on the survival of coastal sockeye salmon ( Oncorhynchus nerka; hísn in Haíɫzaqv), we tagged 1785 individual fish with passive integrated transponders across four migration seasons in the Koeye River—a low-elevation watershed in coastal British Columbia—and tracked them during their relatively short migration (∼13 km) from river entry to spawning grounds. Overall, 64.7% of sockeye survived to enter the spawning grounds, and survival decreased rapidly when water temperatures exceeded 15 °C. The best-fitting model included an interaction between river flow and temperature, such that temperature effects were worse when flows were low, and river entry ceased at the lowest flows. Results revealed temperature-mediated mortality and migration delays from low water that may synergistically reduce survival among sockeye salmon returning to coastal watersheds.

Population fitness has a concave relationship with migration distance in Sanderlings

In Focus: Reneerkens, J., Versluijs, T. S. L., Piersma, T., Alves, J. A., Boorman, M., Corse, C., … Lok, T. (2020). Low fitness at low latitudes: wintering in the tropics increases migratory delays and mortality rates in an Arctic breeding shorebird. Journal of Animal Ecology, 89, 691-703. A central question in migratory ecology has been to understand the fitness consequences of individual variation in migration distance among different species and populations. Reneerkens et al. (2020) investigated the demographic consequences of long-distance migration for Sanderlings Calidris alba, an Arctic-breeding species of sandpiper. Their study population has a remarkable geographic distribution with a breeding range that is concentrated in northeast Greenland and Ellesmere Island, Canada but a nonbreeding range that extends across 85° of latitude from Scotland to Namibia. The authors report on unexpected patterns of latitudinal variation in three demographic parameters: timing of passage on northward migration, probability of juvenile migration and apparent survival of adults. Sanderlings travelling 1,800-2,800km to settle at north temperate sites during the nonbreeding season hadearlier passage dates, and also higher probabilities of migration and apparent survival. In contrast, birds travelling 6,000-7,800km to equatorial sites experienced later passage dates, delayed maturity and lower apparent survival. However, if Sanderlings migrated even farther and flew over 11,000km to nonbreeding sites in Namibia, then their performance was restored to early passage dates and higher survival. Movement tracks from birds tagged with geolocators showed that birds wintering in Namibia make nonstop flights of 7,500km that bypass West Africa during northward migration. Thus, all lines of evidence suggest that Sanderlings face adversity when spending the nonbreeding season at equatorial latitudes. Moreover, the central finding that components of fitness can have nonlinear relationships with migration distance is a novel discovery that leads to many additional questions. The new findings have broader implications for theoretical models of migration, and for understanding how different patterns of movements may arise or be maintained in migratory species.

Low fitness at low latitudes: Wintering in the tropics increases migratory delays and mortality rates in an Arctic breeding shorebird.

Evolutionary theories of seasonal migration generally assume that the costs of longer migrations are balanced by benefits at the non‐breeding destinations.We tested, and rejected, the null hypothesis of equal survival and timing of spring migration for High Arctic breeding sanderling Calidris alba using six and eight winter destinations between 55°N and 25°S, respectively.Annual apparent survival was considerably lower for adult birds wintering in tropical West Africa (Mauritania: 0.74 and Ghana: 0.75) than in three European sites (0.84, 0.84 and 0.87) and in subtropical Namibia (0.85). Moreover, compared with adults, second calendar‐year sanderlings in the tropics, but not in Europe, often refrained from migrating north during the first possible breeding season. During northward migration, tropical‐wintering sanderlings occurred at their final staging site in Iceland 5–15 days later than birds wintering further north or south. Namibia‐wintering sanderlings tracked with solar geolocators only staged in West Africa during southward migration.The low annual survival, the later age of first northward migration and the later passage through Iceland during northward migration of tropical‐wintering sanderlings, in addition to the skipping of this area during northward but not southward migration by Namibia‐wintering sanderlings, all suggest they face issues during the late non‐breeding season in West Africa.Migrating sanderlings defy long distances but may end up in winter areas with poor fitness prospects. We suggest that ecological conditions in tropical West Africa make the fuelling prior to northward departure problematic.

A dam passage performance standard model for American shad

Objectives for recovery of alosines commonly involve improving fish passage at dams during migration. However, a quantitative basis for dam passage performance standards is largely absent. We describe development of a stochastic life-history-based simulation model for American shad, Alosa sapidissima, to estimate effects of dam passage and migratory delay on abundance, spatial distribution of spawning adults, and demographic structuring in space and time. We used the Penobscot River, Maine, USA, as a case study to examine sensitivity of modeled population metrics and probability of achieving specific management goals to inputs. Spawner abundance and percentage of repeat spawners were most sensitive to survival and migration delay at dams, marine survival, and temperature cues for migratory events. Recovery objectives related to abundance and spatial distribution of spawners were achievable under multiple scenarios, but high rates of upstream and downstream passage were necessary. The simulation indicated trade-offs between upstream and downstream passage efficacy whereby increased downstream passage was required to maintain or increase population abundance in conjunction with increased upstream passage. This model provides a quantitative support tool for managers to inform ecologically based decisions about a suite of management scenarios to facilitate recovery and sustainability of diadromous fish populations.

Lamin-B1 contributes to the proper timing of epicardial cell migration and function during embryonic heart development.

Lamin proteins form a meshwork beneath the nuclear envelope and contribute to many different cellular processes. Mutations in lamins cause defective organogenesis in mouse models and human diseases that affect adipose tissue, brain, skeletal muscle, and the heart. In vitro cell culture studies have shown that lamins help maintain nuclear shape and facilitate cell migration. However, whether these defects contribute to improper tissue building in vivo requires further clarification. By studying the heart epicardium during embryogenesis, we show that Lb1-null epicardial cells exhibit in vivo and in vitro migratory delay. Transcriptome analyses of these cells suggest that Lb1 influences the expression of cell adhesion genes, which could affect cell migration during epicardium development. These epicardial defects are consistent with incomplete development of both vascular smooth muscle and compact myocardium at later developmental stages in Lb1-null embryos. Further, we found that Lb1-null epicardial cells have a delayed nuclear morphology change in vivo, suggesting that Lb1 facilitates morphological changes associated with migration. These findings suggest that Lb1 contributes to nuclear shape maintenance and migration of epicardial cells and highlights the use of these cells for in vitro and in vivo study of these classic cell biological phenomena.

Migratory delay leads to reduced passage success of Atlantic salmon smolts at a hydroelectric dam

AbstractPassage of fish through hydropower dams is associated with mortality, delay, increased energy expenditure and migratory failure for migrating fish and the need for remedial measures for both upstream and downstream migration is widely recognised. A functional fish passage must ensure safe and timely passage routes that a substantial portion of migrating fish will use. Passage solutions must address not only the number or percentage of fish that successfully pass a barrier, but also the time it takes to pass. Here, we used radiotelemetry to study the functionality of a fish bypass for downstream‐migrating wild‐caught and hatchery‐released Atlantic salmon smolts. We used time‐to‐event analysis to model the influence of fish characteristics and environmental variables on the rates of a series of events associated with dam passage. Among the modelled events were approach rate to the bypass entry zone, retention rates in both the forebay and the entry zone and passage rates. Despite repeated attempts, only 65% of the tagged fish present in the forebay passed the dam. Fish passed via the bypass (33%), via spill (18%) and via turbines (15%). Discharge was positively related to approach, passage and retention rates. We did not detect any differences between wild and hatchery fish. Even though individual fish visited the forebay and the entry zone on multiple occasions, most fish passed during the first exposures to these zones. This study underscores the importance of timeliness to passage success and the usefulness of time‐to‐event analysis for understanding factors governing passage performance.

Downstream Passage and Impact of Turbine Shutdowns on Survival of Silver American Eels at Five Hydroelectric Dams on the Shenandoah River

AbstractHydroelectric dams impact the downstream migrations of silver American Eels Anguilla rostrata via migratory delays and turbine mortality. A radiotelemetry study of American Eels was conducted to determine the impacts of five run‐of‐the‐river hydroelectric dams located over a 195‐km stretch of the Shenandoah River, Virginia–West Virginia, during fall 2007–summer 2010. Overall, 96 radio‐tagged individuals (mean TL = 85.4 cm) migrated downstream past at least one dam during the study. Most American Eels passed dams relatively quickly; over half (57.9%) of the dam passage events occurred within 1 h of reaching a dam, and most (81.3%) occurred within 24 h of reaching the dam. Two‐thirds of the dam passage events occurred via spill, and the remaining passage events were through turbines. Migratory delays at dams were shorter and American Eels were more likely to pass via spill over the dam during periods of high river discharge than during low river discharge. The extent of delay in migration did not differ between the passage routes (spill versus turbine). Twenty‐eight American Eels suffered turbine‐related mortality, which occurred at all five dams. Mortality rates for eels passing through turbines ranged from 15.8% to 40.7% at individual dams. Overall project‐specific mortality rates (with all passage routes combined) ranged from 3.0% to 14.3%. To protect downstream‐migrating American Eels, nighttime turbine shutdowns (1800–0600 hours) were implemented during September 15–December 15. Fifty percent of all downstream passage events in the study occurred during the turbine shutdown period. Implementation of the seasonal turbine shutdown period reduced cumulative mortality from 63.3% to 37.3% for American Eels passing all five dams. Modifying the turbine shutdown period to encompass more dates in the spring and linking the shutdowns to environmental conditions could provide greater protection to downstream‐migrating American Eels.Received October 16, 2015; accepted April 3, 2016 Published online August 3, 2016

When Siberia came to the Netherlands: the response of continental black-tailed godwits to a rare spring weather event.

1. Extreme weather events have the potential to alter both short- and long-term population dynamics as well as community- and ecosystem-level function. Such events are rare and stochastic, making it difficult to fully document how organisms respond to them and predict the repercussions of similar events in the future. 2. To improve our understanding of the mechanisms by which short-term events can incur long-term consequences, we documented the behavioural responses and fitness consequences for a long-distance migratory bird, the continental black-tailed godwit Limosa limosa limosa, resulting from a spring snowstorm and three-week period of record low temperatures. 3. The event caused measurable responses at three spatial scales - continental, regional and local - including migratory delays (+19 days), reverse migrations (>90 km), elevated metabolic costs (+8·8% maintenance metabolic rate) and increased foraging rates (+37%). 4. There were few long-term fitness consequences, however, and subsequent breeding seasons instead witnessed high levels of reproductive success and little evidence of carry-over effects. 5. This suggests that populations with continued access to food, behavioural flexibility and time to dissipate the costs of the event can likely withstand the consequences of an extreme weather event. For populations constrained in one of these respects, though, extreme events may entail extreme ecological consequences.

Movements of Prespawn Adult Atlantic Salmon Near Hydroelectric Dams in the Lower Penobscot River, Maine

AbstractAcoustic telemetry was used to assess riverine behavior and passage success for prespawn male adult Atlantic salmon Salmo salar in the lower Penobscot River, Maine, in 2005 (n = 10) and 2006 (n = 25). Only 3 of 10 (30%) and 2 of 25 (8%) tagged Atlantic salmon successfully passed all three dams between the head of tide and presumed spawning habitat in 2005 and 2006, respectively. Migrants that failed to pass the second upstream dam frequently fell back into the estuary (3 of 4 in 2005; 17 of 23 in 2006), and few successfully reascended Veazie Dam at the head of tide. Fallback behavior was associated with temperatures exceeding 22°C and may reflect a strategy for coping with thermal stress and migratory delays. Atlantic salmon were also observed to actively seek out thermal refuge near one of the dams. Passage data were compared with results from previous telemetry studies that used Carlin tags and radio telemetry from 1987–1990 and 1992, and passive integrated transponder tags from 2002–2004. For all 10 years of study combined, median passage success was 64, 72, and 93% for the three dams. While 2006 may represent an uncommonly poor year for upstream passage at these dams, median cumulative passage past two of these dams was only 71% and ranged from 8% to 87% among years. Study results indicate that poor upstream passage severely limits migratory success in this system, particularly during periods of high discharge. Planned removal of two of these lower river dams is expected to improve migratory success for adult Atlantic salmon in the Penobscot River system.

An evaluation of fetal/neonatal and chronic adult ethanol exposure (FNEE and CAEE) on murine cutaneous dendritic cell (CDC) maturation and migration using an organ culture system (92.5)

Abstract Alcoholism and fetal alcohol syndrome are associated with increased rates of infection. CDCs, consisting of Langerhans cells (LCs), langerin+ dermal dendritic cells (LdDCs) and langerin - dermal dendritic cells, initiate adaptive immune responses by transporting antigen from the skin to the regional lymph node (RLN). We previously reported a migratory delay of langerin+ CDCs (LCDCs) into the RLN due to CAEE. Migration of CDCs into the RLN is driven by chemokine receptors (CCRs) and adhesion molecules (AMs). To determine if either CAEE or FNEE impair the CCR/AM expression needed for timely transit into the RLN, skin explants were cultured (+/-) CPG & CCL21, and the phenotypes of emigrated CDCs (eCDCs) from control and EtOH exposed mice were evaluated by flow cytometry. CAEE reduced the numbers of emigrated LCs (eLCs). It also reduced CCR7 expression on eLCs and emigrated LdDCs (eLdDCs) and LFA-1 expression on eLdDCs. In contrast, FNEE induced a trend towards increased numbers of eLCs without affecting CCR7 and LFA-1 expression. These findings suggest that diminished CDC migratory capacity is a result of CAEE and not FNEE. The decreased expression of CCR7 and LFA-1 provides a mechanism for the migratory delay exhibited by LCDCs as a result of CAEE and ultimately, a mechanism to explain increased skin infections in alcoholics. Evaluation of additional AMs/CCRs are underway for both models. NIH RO1 AA014405 and AA014406 supported this work.

Arrival timing and seasonal reproductive performance in a long-distance migratory landbird

The date when a landbird migrant arrives on its breeding grounds may have reproductive consequences. Generally, early arriving individuals begin breeding earlier and consequently experience greater seasonal reproductive performance. Here, we describe relationships between arrival timing and seasonal reproductive performance in the American redstart (Setophaga ruticilla), a long-distance passerine migrant, arriving at northerly breeding grounds in Michigan’s eastern Upper Peninsula. Evidence suggests that both males and females benefited from early arrival at the breeding grounds. Early males appeared to settle on higher quality territories and hatched nestlings sooner than later arrivals. Early females began their clutches early, produced heavier nestlings and possibly laid more eggs than later arrivals. Larger clutches and heavier offspring increase the likelihood of offspring recruiting into the breeding population. The findings of this study point to fitness consequences arising from when a bird arrives at its breeding grounds. These results also have implications for understanding how events occurring during spring migration influence reproductive performance as migratory delays likely influence arrival timing.

Quantifying migratory delay: a new application of survival analysis methods

Statistical techniques commonly used in fish passage research fail to adequately quantify delays incurred at obstacles, or the effects of modifications to those obstacles on passage rates. Analyses of telemetry data describing these effects can be misleading, particularly when passage route of some individuals is not established (e.g., because of mortality, tag failure, passage through unmonitored or alternate routes, etc.). Here, we demonstrate how event-time analysis, better known as survival analysis, can be used to quantify passage rates for any study that allows tracking of individuals through time, even when some individuals fail to pass the route or obstacle in question. We review two of the primary methods of event-time analysis (parametric and Cox's proportional hazards regression analyses) and use them in combination with logistic regression to provide unbiased estimates of delay incurred at a hydroelectric facility, as well as insights on factors affecting both rates of passage and route selection. Passage rate increased with increased depth of a surface bypass sluice gate and, among fish that passed through the turbines, with turbine flow. The data further indicate that risk of turbine passage increased with both delay and turbine flow.

Impact and Adaptation Responses of Okanagan River Sockeye Salmon (Oncorhynchus nerka) to Climate Variation and Change Effects During Freshwater Migration: Stock Restoration and Fisheries Management Implications

We summarized existing knowledge on behavioural and physiological responses of Okanagan sockeye salmon (O. nerka) adults to annual and seasonal variations in aquatic thermal regimes during migration. This enabled us to identify an underlying set of ’decision rules’ as a biophysical model of how temperature mediates en-route delays as a specific element of annual migrations by sockeye salmon. Several sets of results indicate that adult sockeye migrations stop as seasonal water temperatures increase and exceed 21 °C and then restart when temperatures decrease and fall below 21 °C. Model predictions of annual variations in the duration of migratory delay exhibited close agreement with independent estimates of observed delays available from a subset of years (predicted delay = 1.23 observed delay + 2.08, r2 = 0.92, p < 0.001, n = 10). We applied the model in a retrospective analysis of the likely impacts of climate variation and change events on adult sockeye migrations in freshwater over the 70 plus year interval between 1924 and 1998. Results indicate that migration delays for a significant portion of the sockeye population averaged 29 days per year (range 0–55). Average annual migration delays roughly equal the 33 day estimate of time required, given continuous migration, to traverse the 986 km distance from the Columbia River mouth to terminal spawning grounds near Osoyoos Lake, BC. Alternating intervals of above-average and below-average migration delays corresponded closely with ’warm-phase’ and then ’cold-phase’ periods of the Pacific Interdecadal Oscillation. Circumstantial evidence suggests alternating periods of sub-average and above-average productivity for salmon on the southern end of their range are linked to climate variation and change events in both freshwater and marine environments. Climate impact and adaptation responses that register first at the level of salmon, propagate rapidly through both salmon resource users and fisheries managers. Consequently, future climate warming episodes will complicate the manageability and threaten the sustainability of many salmon populations in the southern end of their range (Georgia Basin and the Pacific Northwest). This requires strategies that minimize the impact of uncertain climate variability and change scenarios on the resilience of the salmon resource, and maximize our adaptive capacity for both short- and long-term fisheries planning and management decisions.

Effects of low-dose X-irradiation on the development of the mouse cerebellar cortex.

We labeled proliferating cells of the cerebellum of 6-day-old mice with 5-bromo-2'-deoxyuridine (BrdU) followed by a single exposure to 0.5, 1 or 2 Gy of X-rays. We then studied the effects of low-dose irradiation on the migration and survival of granule neurons in the mouse cerebellum. The animals were killed at 4 days, or at 2, 4 or 6 weeks after irradiation. Brains were fixed and BrdU-labeled cells in the cerebella were immunohistochemically analyzed. BrdU was predominantly distributed in the superficial layer of the external granular layer soon after injection. Four days after irradiation with 0.5 or 1 Gy, labeled cells were mainly seen in the inner granular layer, which was also the case in non-irradiated mice. However, following 2 Gy irradiation BrdU was found not only in the inner granular layer, but also in the Purkinje cell layer. This distribution was also seen at 2 and 4-6 weeks after irradiation. In animals irradiated with 1 Gy 4-6 weeks after irradiation, the proportion of labeled cells present in the inner granular layer decreased, while labeled cells in the Purkinje cell layer increased. On the other hand, 0.5 Gy irradiation did not change the distribution of labeled cells, except that the proportion of labeled cells in the inner granular layer decreased at 2 weeks after irradiation. The number of labeled cells in the cerebellar cortex per unit area decreased with time and dose. These results suggest that 2 Gy irradiation induces a migratory delay, abnormal distribution, and cell death of the granule neurons of the mouse cerebellum.

Schistosoma mansoni: an ultrastructural examination of pulmonary migration.

The migration of schistosomula through the lungs of mice has been investigated at the ultrastructural level. On Days 4 and 7 post-infection schistosomula were located only within the vasculature. Newly arrived Day 4 schistosomula were highly convoluted and completely occluded vessels measuring approximately 15-25 micron in diameter. By Day 7 parasites were located in pulmonary capillaries, often causing considerable distension. The subtegumentary fibrous interstitial layer was absent in elongated lung schistosomula. The minimum diameter of such parasites was 8 micron, and their tegument was usually unridged and flattened against the vascular endothelium, thus resulting in close apposition of endothelial and tegumental membranes. The tight fit of schistosomula in the pulmonary capillaries implies that migration through them is both a strenuous and slow process. The migratory delay in the lungs after arrival from the skin occurs because dimensional changes are necessary for successful capillary migration.