1. Introduction
Many coral reef fishes show characteristic habitat shifts during ontogeny [
1,
2,
3,
4,
5,
6]. Such ontogenetic migrations are thought to minimize the ratio of mortality over growth [
7], which has been supported empirically [
3,
8,
9,
10]. Ontogentic migrations are well-defined in grunts (Haemulidae) and evidenced by the shift to larger size distributions with progressive offshore locations [
1,
2,
5,
6,
11].
During ontogeny, juvenile grunts undergo a series of migrations between habitats (and associated resting schools) [
2,
5,
6,
11,
12]. These migrations are associated with changes in diet and behavior [
2,
10,
13,
14] and appear to be strongly correlated with fish length [
10,
15]. There are six eco-behavioral stages of development reported for
Haemulon flavolineatum and
H. plumierii [
2,
16]. These stages begin with newly settled fish and proceed through to adults. Newly settled fish start life by settling at 1–1.5 cm TL. At this point, they are considered Stage 0 juveniles and settle opportunistically on small, isolated structures within seagrass beds and backreef areas [
17] while continuing to feed on plankton during the day. Stage 0 fish begin nightly off-site migrations, but do not feed. As juveniles (Stage 1 and 2), they aggregate on patch reefs or in mangrove stands and size-segregate into schools [
18]. At 3.0 cm TL (Stage 1), individuals form daytime resting schools on structures within seagrass or mangroves near the reef. Individuals at this stage are transitional in their feeding ecology, and smaller individuals may continue to feed on plankton during the day. From 5.5 to 12 cm TL (Stage 2),
H. flavolineatum continue to form daytime resting schools, but migrate at twilight over specific pathways to feed nocturnally in areas within seagrass and other soft-bottom habitats [
19,
20,
21,
22]. Return migrations occur over the same pathways during morning twilight. Individuals transition forward on the reef where schools are found in deeper water and along the reef edge [
17]. At 12.0 to 15.0 cm TL (sub-adult),
H. flavolineatum continue to school during the daytime and migrate to feeding grounds at night. Although they migrate and school, they begin to roam and display more adult-like behavior. At 15 cm TL (adult),
H. flavolineatum mature and migrate offshore [
2,
11].
Inference from school positions and mean size give a general indication of the transitional timing and the general areas/habitats involved in ontogenetic migrations, but do not indicate the pathways. Documenting pathways may help identify potential underlying factors associated with orientation and direction, which in turn could point to general rules governing fish movements [
16]. Understanding these pathways is also critical for protecting essential fish habitats and areas acting as a nursery or source areas for adult populations [
23], with MPA design being an obvious case. Burke et al. [
24] and Jaxion-Harm et al. [
25] calculated potential priority nursery areas based on densities and abundances of small-juveniles, and Mateo et al. [
26] used stable isotopes in otoliths to estimate the contribution of sea grass versus mangroves nurseries to the population a year later. These studies suggested that not all areas occupied by early juveniles contribute equally to later age groups. Yet, neither approach considered the potential pathway of ontogenetic migration, so direct spatial connections between key nursery habitats to those occupied by later stages remain unknown. Mumby [
27] and Martin et al. [
28] assumed straight-line pathways when attempting to quantify at what distances there was a disconnect between mangrove nursery areas and potential adult habitats on coral reefs.
Pathways that are bounded by land are simple to understand (e.g., embayments with narrow openings to open reef environments [
5,
12]); however, it is more difficult to determine pathways, orientation cues, and factors affecting migration in an open coastal environment consisting of mangrove and seagrass beds sheltered by fringing reefs. Little is known of the actual pathways taken by juveniles to adult habitat. Appeldoorn et al. [
11], commenting on the lack of such studies for tropical marine fishes, emphasized the need to understand the linkage between habitats and developmental stages. Dorenbosch et al. [
29] compared adult populations on reefs >9 km distant from inshore mangrove and seagrass habitats and found most species (including grunts) to have reduced densities on reefs located directly offshore over open habitats compared to those reefs connected along shore. They concluded that migration along the coast would explain these differences. Appeldoorn et al. [
16] reported finding one white grunt (
H. plumierii) at an outer emergent reef that had been tagged 3 years prior (~8 cm FL) directly inshore, but given there was an extensive linear reef between these two locations, a direct pathway could not be determined.
In the Caribbean, grunts are ubiquitous and abundant, representative of medium-sized reef fishes, and have substantial importance commercially [
30,
31] and ecologically [
32,
33]. This study aims to ascertain the direction taken by juvenile grunts, mainly
H. flavolineatum, and the potential cues used during ontogenetic migration through a mark and recapture program. The study was designed to investigate these movements at two different scales. A small-scale study was designed to track movement among schools within a single reef site. At a larger scale, the movement of individuals targeted the migration pathways and cues used by subadults thought to make larger transitions to off-reef locations. Tagging and subsequent recovery locations were specifically selected to reveal potential environmental cues related to choices of migratory pathways. Specifically, sites were located such that potential movement would most likely be constrained to different pathways determined by bathymetry or by movement across open water toward upstream habitat cues. In the small-scale study, it was hypothesized that movement would be constrained by bathymetry and that fish would move along a pathway leading to adjacent offshore reefs to the southwest. The large-scale study targeted a potential choice of offshore pathways: directly up-current or directly toward the nearest reef. Choice of direction could signal which cues fish use to orient movements (e.g., olfactory, acoustic cues or need for shelter). While the goal was to elucidate general processes, the tagging sites were also oriented relative to potential movement toward a proposed marine reserve [
34], so results could be applied to identifying source areas for the reserve.
4. Discussion
Appeldoorn et al. [
2,
11], Nagelkerken and van der Velde [
12], Cocheret de la Morinière et al. [
5], and Aguilar–Perera and Appeldoorn [
6] demonstrated with length frequency data from Puerto Rico, Columbia, Curacao, and the Bahamas that
Haemulon flavolineatum,
H. plumierii and
H. sciurus move ontogenetically. In this study, forward movement to the reef front was supported by the mark-recapture data. Combined, the two tagging studies showed the collective movement of French grunts (6.4–13.7 cm FL) from the back reef area at Majimo 513 m to and along the fore reef. The route essentially follows the reef margin, suggesting that the fish were using the reef margin for orientation [
18]. However, initial dispersal in the small-scale study occurred primarily along the eastern pathway, indicating that orientation along the reef margin was not the only factor affecting direction.
The results further indicate that juveniles move by dispersing among the available schools within the general trend toward the reef front. The degree of movement was not affected by individual growth rates, or the days at liberty, but time to dispersal to Site 3 was negatively correlated to FL at tagging. Mean lengths at Site 3 were consistently larger than at the tagging site. These observations and other studies [
15,
46,
47] suggest that the progression of fish through the reef system (individually or in small groups) occurs when fish achieve a size transitional between those characterizing the old and new schools. Five of the six fish recaptured at Site 1 (tagging school) were below the mean size-at-tagging for all recaptured fish, with the sixth only slightly larger than the mean. It is thus possible that these remaining individuals had not yet achieved a size sufficient to transition to another school.
It is not certain how or when small fish move from one school to another. In this study, there was a substantial distance between the various reefs hosting resting schools, so inter-reef transitions required significant movement over an open habitat. This situation differs markedly from that of McFarland and Hillis [
46], where various schools, differing in mean length, were found in close proximity (six schools within a 4 m diameter collapsed coral head). One likely possibility is that reef transition occurs when fish return after nocturnal feeding. In this study, feeding migration pathways off the reef suggest that fish from Sites 1, 2 and 3 head for a common feeding area (
Figure 3). The extrapolations of observed feeding pathways for each of these sites join in a seagrass area to the north. This provides both an opportunity and means for individual fish from one resting school location to encounter other fish and join their migration back to a new location. Indeed, on several occasions, when monitoring the sunrise migration, it appeared that fish on one migration pathway turned and followed a passing group of fish traveling on a different, intersecting migration pathway. This mechanism may explain why the majority of fish from Site 1 migrated seaward along the eastern margin of the channel. In this sense, migration direction was initially set by factors derived from habitat orientation within the local seascape, which determines the spacing among juvenile resting schools and their orientation to potential off-reef feeding habitats. These initial conditions channeled the majority of migration from Site 1 to being parallel to the coast toward the east, with later movement potentially directed to the offshore reefs of Corral and Turromte, as opposed to the movement to the southeast to the more adjacent offshore reefs of Enrique and Media Luna (
Figure 2), as might have been expected based solely on large-scale geomorphology.
McFarland and Hillis [
46] suggested that antagonistic behavior among individuals might also be a factor contributing to the transition of fish from one school to another. Antagonistic behavior occurs most commonly during the morning aggregation as fish return to the reef after feeding. As fish come together in small groups, larger juveniles begin mouth pushing, nipping, and chasing. These behaviors increase with the size of the fish. In addition, the largest juveniles may occupy territory on the reef during the day and defend the space through displays and aggressive behavior. Antagonistic behavior may serve to induce individuals to leave the reef in order to reduce the level of antagonism as their length increases. At Site 1, several larger fish at this location were antagonistic and territorial; the largest grunt caught was 12 cm. If these larger fish were indeed resident, they would act to drive others off the reef as they grew. McFarland and Hillis [
46] observed one territorial grunt being ejected by a larger, more aggressive individual, in this case forcing the deposed fish to return to a nearby school of medium sized fish.
Grunts have ontogenetic eco-behavioral stages [
2,
16,
48], with sub-adult fish found in loosely knit groups along the reef front. In the large-scale study, recovered fish were less than 15 cm and recaptured on the same reefs where they were tagged. No recaptures were found further offshore. Although no fish were found off-reef, those fish found to have moved from the tagging location proceeded forward on the reef and entered into loosely knit sub-adult resting schools. This behavior is similar to that observed by Verweij and Nagelkerken [
45] when tagging grunts in Southwest Bay, Curacao. They found only three grunts out of 51 recaptures to move significantly, and this movement was into or beyond the lagoonal channel to the open reef. Recapture sizes of two found in the channel were 9.8 and 11.1 cm, while the other was found in a later follow-up search fully outside the bay 2 km from its tagging site with a size of 14.2 cm.
Large-scale movement patterns are hard to generalize, given the limited number of recaptured fish showing movement and the limited movement displayed. However, these data at least suggest that larger juvenile fish move seaward following the distribution of reef habitat as found by Verweij and Nagelkerken [
45]. For instance, fish at Corral East moved along reef habitat from the backreef schooling location and around the northeast corner moving forward on the reef. Individuals at Romero West left their juvenile schools and moved into the channel joining schools of sub-adults.
One possible means used for orientation during these movements is vision. It is known that juvenile grunts travel along nightly feeding routes maintained over several months [
18] using visual cues [
49], and juvenile fish are able to encounter the routes when displaced [
50]. Fish at Caracoles followed the reef line to the east and up current, possibly using the nightly feeding migrations as a means of exchange.
Given that the size affected when fish migrated at Majimo and was related to whether larger juveniles moved or not, and that size is an indicator of ontogenetic development and school placement [
15], it is reasonable to assume that for large-scale migration to occur, fish must grow to some threshold size. This is supported by Williams [
51], who acoustically tagged and transplanted four adult (range 19.0–22.9 FL; average 21.6; SD 1.2 cm) and three subadult (range 15.9–18.5 FL; average 17.2; SD 1.3 cm)
H. plumierii from Turromote to Corral and Romero (
Figure 1). Only the adult fish crossed the boundary between these emergent reefs to return to Turromote. This apparent threshold is consistent with the size distribution of
H. plumieri across the shelf observed by Appeldoorn et al. [
2,
11].
In the present study, the period of residency and growth for
H. flavolineatum is much longer than that reported by other studies. Many authors have reported that in 12 months, haemulids can grow to maturity and a size at which larger migrations can occur [
52,
53,
54,
55]. To maximize the probability of detecting large-scale movements in the present study, large juveniles (approximately 10 cm) were tagged, yet some fish in this study were resident for up to 503 days, and all fish showing movement were recaptured in nearby schools on the same reef where tagged. In that time, the greatest growth interval was under 5 cm and the greatest size reached was 14.9 cm, similar to Verweij and Nagelkerken’s [
45] one fish tracked to the open reef. The time-frame for that movement was not reported. It is thus possible that in the present study, the time at liberty was insufficient for growth to the size necessary for large-scale migration. The previous growth studies were based upon otolith readings; however, Brothers and McFarland [
1] determined that daily otolith lines were indistinguishable for
H. flavolineatum after 100 days, and Shaw [
55] showed daily lines to grossly underestimate age (and hence overestimate growth) of large juvenile
H. plumierii over 287 days (aged between 149 to 184 days). From the observed growth among tagged fish [
39], however, it is possible that previous growth rates were overestimated, which would explain why off-reef movement was not observed within the duration of this study.
In summary, when making ontogenetic habitat shifts, small juveniles independently move toward the reef front by transiting through schools varying in mean fish length. Movement is not necessarily toward the nearest school, but follows a general pathway. Fish appear to move to new schools primarily by the night-time re-aggregation before returning to the safety of the reef. Short-term movements between schools may be preceded by sparing and antagonistic behavior displays at the home school location and in the feeding grounds. Transfer appears to occur visually during the morning aggregation.
No recaptures of larger juveniles were made off the reefs where tagging occurred, so large-scale movements were not obtained during this study, and the question of ontogenetic group movement to the offshore habitat cannot be answered at this time. Three things contribute to the lack of observed movement off the tagging reef: (i) the time of liberty was of a short duration and perhaps more recoveries could be found with more time; (ii) the effort was small compared to the size of the area searched, and (iii) the number of fish tagged was low for a study of this scale, but the lack of manpower and the time available for the study demanded a more manageable number of tagged fish. If a larger-scale migration by
H. flavolineatum to more offshore adult habitats occurs at 15 cm FL as suggested by Appeldoorn et al. [
11], then 1.5 years at liberty would be needed for grunts to obtain sufficient size for departure when tagged at 10 cm. Rather, grunts appear to be resident upon a reef for about 2 years. Residency and growth rates of recovered fish do not support the premise that grunts mature within 12 months.