Abstract
Information on migration patterns is critical to using no-take migratory corridors and marine reserves to protect the spawning stock of commercially exploited species. Both active and passive acoustic tracking methods quantified movement of commercially and ecologically important blue crabs in the White Oak River estuary, NC, USA. We targeted post-mating female crabs migrating down-estuary to oceanic spawning grounds. Crabs travelled approximately 14.1 km mainly in deeper channels and over 12–26 days from mating areas to spawning grounds. No crabs were detected migrating down-estuary in the autumn and only 30% were detected migrating down-estuary in spring. None of the crabs detected near spawning grounds were detected or recaptured back up-estuary, suggesting that they either (i) do not return to the estuary after a one to two week period in the spawning area or (ii) were captured by fishermen. The results from this study demonstrate that (1) acoustic transmitters coupled with passive acoustic receivers provided reliable and valuable data on migration patterns of mature female blue crabs and (2) mature female blue crabs are capable of migrating primarily within deep channels to spawning grounds shortly after insemination.
Keywords: blue crab, fisheries management, mark–recapture, acoustic tracking, marine protected areas, migration corridors
1. Introduction
An important goal of marine reserves is to protect the spawning stock of commercially exploited species [1]. This goal can be challenging for species that undergo long-distance spawning migrations to release larvae in favourable habitat [2–4]; however, linking no-take migration corridors to spawning sanctuaries shows promise [5,6]. For example, blue crab (Callinectes sapidus) spawning sanctuaries in the Chesapeake Bay, USA were originally ineffective at protecting the spawning stock (approx. 16% protected); however, subsequent expansion of sanctuaries to include post-mating, female migration corridors increased the proportion of the spawning stock protected by 70%, leading to a resurgence in spawning stock [5,6]. A greater understanding of the post-mating migratory behaviour of female blue crabs in other estuarine systems will inform improved management of the blue crab spawning stock.
Blue crab mating typically occurs from May to October in both the mesohaline and oligohaline portions of Chesapeake Bay and Pamlico Sound [7,8]. Males couple with pre-pubescent females prior to their terminal moult. Directly after moulting, mating occurs while the female is in a soft-shell state [7]. After mating, inseminated females begin migration to higher salinity areas of the estuary and enter the ocean, where they subsequently release their larvae [7,9]. In large estuaries, such as Chesapeake Bay and Pamlico Sound, migration from mating to spawning grounds may require a female blue crab to travel up to 200 km [2,6]. Female blue crabs from the upper Chesapeake Bay and Pamlico Sound remain within mating areas during summer, with most beginning their migration to spawning grounds in mid to late October [2,8]. This delay in migration until autumn can lengthen the time between insemination and spawning, thereby exposing females to increased periods of fishing and natural mortality before spawning. The post-mating, migratory behaviour of mature female blue crabs remains poorly understood because of the limited number of studies in relatively small estuarine systems that characterize the southeastern and gulf coasts of the USA.
2. Material and methods
The White Oak River (WOR), NC, USA served as a model system for characterizing migration of mature female blue crabs in a relatively small tidal estuary (distance from mating to spawning grounds 16 km) compared with previous work in the relatively large, tidally driven estuaries (e.g. Chesapeake Bay: distance from mating to spawning grounds approx. 120–170 km; Pamlico Sound: approx. 60–90 km) and another relatively small estuary in NC (e.g. Newport River/Beaufort Inlet; approx. 20 km). The WOR empties into Bogue Sound and Inlet, which serves as the spawning grounds by providing a direct link to the Atlantic Ocean (figure 1).
Figure 1.
Spring 2009 blue crab tracking in the White Oak River, NC, USA. Black triangles denote the locations of VR2W passive acoustic receivers. The circled crab represents the location of release for all crabs on 7 May 2009 and the lines indicate the likely route that each of the three detected crabs took based on detections by a passive receiver array. The crab icon represents the location of a crab captured and re-released by a commercial fisherman. The open triangle indicates a VR2W that was not recovered in September 2009.
One challenge in relating the movements of mature female crabs to the timing between mating and arrival on spawning grounds is the lack of information on exactly when a mature female has been inseminated. We overcame this uncertainty by collecting mating pairs of male and female crabs from the field, allowing them to complete mating in a flow-through seawater system in the laboratory, and then releasing a tagged female in the original capture location in the field approximately 3 days later. We employed two types of external tags to track migration of post-mating female blue crabs in the WOR: (i) Vemco V-13 continuous acoustic transmitters set to specific frequencies that matched an individual crab, used to actively track crabs hours to days after tagging with an ultrasonic receiver and unidirectional hydrophone from a 6 m boat, and (ii) Vemco V-13 coded acoustic transmitters used to passively track crabs as they came within range of Vemco VR2W stationary receivers placed in the WOR. A subset of V-13TP coded transmitters were additionally configured to transmit pressure (depth to 50 m) and temperature (0–40°C) data. VR2W receivers were generally set approximately 500–800 m apart and an individual crab could be detected by as many as three receivers at a time. All tags were affixed to crab carapaces.
During summer 2008, a total of six mature female blue crabs were tagged with acoustic transmitters and tracked actively every day for 16 days (tracked hourly during daylight). To assess potential differences in migration according to month of insemination, three crabs were tagged and released on 4 August and three on 22 September 2008. When a crab was located with a hydrophone, its position was marked with a GPS. At each recapture location, depth and environmental parameters were recorded. Another 24 crabs were tagged with transmitters and tracked passively using an array of four VR2W acoustic receivers that were located along a highway bridge that opened to the spawning grounds (electronic supplementary material, figure S1). During spring 2009, a total of five mature female crabs were tagged with V-13 transmitters and an additional five crabs tagged with V-13TP transmitters—all crabs were released at their original location of capture in the estuary as described above. A total of six VR2W receivers were moored longitudinally down-estuary, as well as adjacent to the highway bridge opening to the spawning grounds (figure 1). Local crabbers were informed of the research and encouraged, with a reward, to report the position of tagged crabs that were captured in their pots.
The proportion of crabs detected relative to the number released, as well as detection dates that a crab arrived at putative spawning grounds, provided data on the timing, general direction and speed of movement of mature female blue crabs. Distance travelled was measured using ARCGIS after the coordinates of the detected crabs were plotted on maps. An average rate of travel was computed by averaging the rates of travel (km d−1) over two or more detection segments (if available) for an actively tracked crab, or by computing the rate of travel from the release point to an endpoint for a passively tracked crab.
3. Results
Mature female blue crabs actively tracked over 10 days in 2008 travelled significantly further in August than September; however, there was no significant difference in mean rate of travel (figure 2; electronic supplementary material, table S1 and figure S1). Direction of travel was downstream in five of six cases. In terms of large-scale movements, 50% of mature female blue crabs released on 30 July 2008 were first detected by passive receivers downriver at the entrance to the spawning grounds 12–26 days after release (table 1). The average rate travelled was 0.85 km d−1 (table 1). All crabs detected were in a deep (4–5 m) channel—no crabs were detected in shallow water when entering the spawning grounds. None of the 11 crabs released on 22 September 2008 were detected entering the spawning grounds before the receivers were recovered on 14 October 2008 (22 days post release; data not shown). Based on the August results, there should have been enough time for many of the September-tagged crabs to travel to the spawning grounds before the receivers were recovered on 14 October, suggesting that mature female blue crabs may not migrate down-estuary in late September. Rate of travel was significantly less for crabs mated in May than in other months (figure 2). During 2009, three of the 10 crabs released on 7 May were detected moving down-estuary by the array of receivers, and two crabs were detected entering the spawning grounds 11 and 32 days from release (figure 1). These two crabs travelled at 0.37 and 0.13 km d−1, and were never recorded moving back up-estuary after reaching the spawning grounds. All crabs that were detected entering the spawning grounds in 2009 did so through the main, relatively deep channel of the WOR.
Figure 2.
(a) Mean distance travelled (km) by mature female blue crabs actively tracked with a directional hydrophone for 10–16 days during early August (summer) and late September (autumn) 2008. (b) Mean rate of travel of passively tracked crabs. (c) Mean rate of travel (km d−1) of crabs during early August (summer) and late September (autumn) 2008. Significance is indicated by asterisks (ANOVA, F = 12.35, d.f. = 1, p = 0.25). (d) Mean rate of travel using data from all methods. For passively tracked crabs (ANOVA, F = 18.33, d.f. = 1, p = 0.004). For data from all methods (ANOVA, F = 4.0, d.f. = 2, p = 0.036). All error bars are 1 s.e.
Table 1.
August 2008 detection of mature female blue crabs by VR2W receivers placed at the NC Highway 24 Bridge. Crabs were released on 30 July 2008 from Stella, NC, approximately 14.1 km upriver from receivers. Missing rate data for last two rows are owing to crabs remaining near receiver array for days.
| crab no. | detection date | stations | days from release | detection duration (h : min) | no. detections | km d−1 |
|---|---|---|---|---|---|---|
| 5567 | 15 Aug 2008 | W8 | 16 | 1 : 02 | 5 | 0.91 |
| 5668 | 11 Aug 2008 | W8 | 12 | <1 min | 1 | 1.21 |
| 5669 | 17 Aug 2008 | W4, W8 | 18 | 0 : 04 | 2 | 0.81 |
| 5670 | 14 Aug 2008 | W4, W8 | 15 | 0 : 08 | 8 | 0.97 |
| 5671 | 21 Aug 2008 | W4, W8 | 22 | 0 : 01 | 2 | 0.66 |
| 5674 | 25 Aug 2008 | W4, W8 | 26 | 0 : 37 | 14 | 0.56 |
| 5674 | 27 Aug 2008 | W4, W8 | 28 | 0 : 06 | 7 | |
| 5674 | 6 Sep 2008 | W4 | 38 | <1 min | 1 |
4. Discussion
The results from this study demonstrate that (i) acoustic transmitters coupled with passive acoustic receivers can provide valuable data on migration patterns of mature female blue crabs and (ii) mature female blue crabs are capable of migrating to spawning grounds shortly after insemination in summer. Moreover, we released females approximately three days after insemination by male blue crabs, which increased the accuracy of movement data over previous studies in which the date of insemination was unknown. Previous tagging studies in large estuarine systems indicate that mature female blue crabs generally do not migrate to spawning grounds until the spring following insemination the previous summer [2,8,9]. Previous tagging studies conducted in the relatively small Newport River estuary, NC, also demonstrated that blue crabs migrate back up-estuary after larval release [10], whereas later studies in the Newport River system demonstrated that blue crabs do not migrate back up-estuary after larval release, rather they remain in the spawning grounds (as observed in this study) or continue to migrate offshore [11].
In this study, three of the actively tracked crabs in the WOR paused for 2–11 days in an area 6–8 km from the release point. This is an area of the estuary where salinity increases to more than 22 ppt, which has been proposed as necessary for brood production [11]. The general observations of blue crab migration patterns observed in this study, whereby most crabs move along deeper channels, is consistent with observations from related studies [2,8,9]. The results from this study contribute to a growing body of information on how knowledge of the migratory behaviour of marine animals can inform fisheries management techniques such as marine reserves and migratory corridors that are being applied to protect the spawning stock of commercially exploited species [1,6,12].
Supplementary Material
Acknowledgements
We thank Russ Howell for his expertise and assistance in this project, J. Eggleston for assistance in the field and three anonymous reviewers for constructive comments on a previous version of this manuscript. We also thank the editors of this special issue for their invitation to contribute: B. Walther, P. Munguia and. L. Fuiman.
Ethics
The collection, tagging and monitoring on blue crabs in this study adhered to guidelines provided in our Scientific and Educational Collection Permit no. 708396 from the North Carolina Department of Environmental and Natural Resources.
Data Accessibility
Raw data are available via Dryad (doi:10.5061/dryad.33mb8) and assigned to the title of this manuscript.
Authors' Contributions
D.B.E. provided: substantial contributions to the conception, design, analysis and interpretation of data; drafting of the article and revising it critically for important intellectual content; and final approval of the version to be published. E.M. and G.P. provided: substantial contributions to the design, acquisition and analysis of data; drafting the article for important intellectual content; and final approval of the version to be published
Competing Interests
We declare we have no competing interests.
Funding
Funding was provided by NC Sea Grant/NC Blue Crab and Shellfisheries Research Program (Project 08-POP-04) and NSF (OCE-1155609).
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
Raw data are available via Dryad (doi:10.5061/dryad.33mb8) and assigned to the title of this manuscript.