Comments on Lowe et al. “Otolith Microchemistry RevealsSubstantial Use of Freshwater by Southern Flounder in theNorthern Gulf of Mexico”

Pedro Morais

Received: 28 June 2011 /Revised: 21 November 2011 /Accepted: 6 December 2011 /Published online: 4 January 2012# Coastal and Estuarine Research Federation 2011

Abstract Lowe et al. (Estuaries and Coasts, 34:630–639,2011) hypothesized that juvenile southern flounder Paralich-thys lethostigma (Jordan and Gilbert 1884) would migratefrom the Gulf of Mexico into the Mobile-Tensaw RiverDelta (AL, USA) and use low-salinity (oligohaline/fresh-water) habitats during, at least, a portion of their first year oflife. Thus, they analyzed the Sr/Ca ratio profiles alongthe sagittal otoliths of southern flounder collected in theMobile-Tensaw River Delta and observed that one third ofthe flounders had low Sr/Ca levels in the otoliths’ core andthroughout the otolith, suggesting that these fishes hatchedin freshwater or low-salinity habitats where they spend themajority of their life. The other two thirds of southernflounder showed high levels of Sr/Ca ratio in the otoliths’core following a marked decline of Sr/Ca ratio, which thenmaintained along the remainder of the otolith. This patternwas interpreted as larvae hatched in higher salinity watersbefore entering the Mobile-Tensaw River Delta; however, inthis paper, I list several arguments to support an alternativeinterpretation for this pattern. I suggest that the high levelsof Sr/Ca ratios in the otoliths’ core of southern flounder doesnot reflect the saline conditions where larvae hatched, in-stead it reflects the location where the female progenitor

hydrated the eggs. Thus, adding my interpretation on thedata of Lowe et al. (Estuaries and Coasts, 34:630–639,2011), it seems that southern flounder might hatch in ornear freshwater habitats and the migration of southern floun-der into an estuarine ecosystem to spawn might exist.

Keywords Southern flounder . Migration . Estuary . Otolithmicrochemistry . Sr/Ca ratio . Sea-run mother hypothesis .

Mobile-Tensaw River Delta

Southern flounder Paralichthys lethostigma (Jordan andGilbert 1884) (Paralichthyidae, Pisces) is an important rec-reationally and commercially species along the westernAtlantic and northern Gulf of Mexico coasts and estuaries(Smith and Scharf 2010). Southern flounder stock is beingheavily exploited during the past two decades (Smith andScharf 2010), being registered a long-term decline of 1.3%and 2.5% per year for juveniles and adults, respectively(Froeschke et al. 2011). It is accepted that adult specimensleave estuaries and coastal lagoons to spawn in coastalwaters from late autumn and early winter, reproductionoccurs offshore and some larvae would be transported intocoastal ecosystems by currents (Glass et al. 2008).

In a recent work, Lowe et al. (2011) intended to demon-strate that southern flounder collected in the Mobile-TensawRiver Delta (AL, USA) would ingress from coastal marineenvironments and use low-salinity habitats during its first yearof life. Ultimately, they would also evaluate the importance oflow-salinity habitats for southern flounder recruitment.

The experimental approach of Lowe et al. (2011) con-sisted on the analysis of Sr/Ca ratio profiles along sagittalotoliths. One third of the specimens had low Sr/Ca levels in

P. Morais (*)CIMAR/CIIMAR—Centro Interdisciplinar de InvestigaçãoMarinha e Ambiental,Rua dos Bragas 289,4050-123 Porto, Portugale-mail: pmorais@ualg.pt

P. MoraisICCE—International Center for Coastal Ecohydrology,Solar do Capitão-Mor, Horta das Figuras, EN 125,8005-518 Faro, Portugal

Estuaries and Coasts (2012) 35:904–906DOI 10.1007/s12237-011-9469-4

the otoliths’ core, and throughout the otolith, suggesting thatthese fishes hatched in freshwater or low-salinity habitats,where they spend the majority of their life. Two otherstudies reinforce the hypothesis that southern floundermight spawn or hatch in an estuary, and thus corroboratingthe interpretation of Lowe et al. (2011) on those specimenswith low Sr/Ca ratios at the otoliths’ core. One study, madein the New River (NC, USA), determined that 51.4% ofsouthern flounders were either late or fully developed (notethat data were obtained from samples collected in Octoberand November, i.e., just prior to the spawning season)(Smith and Scharf 2010), thus suggesting that they mighthave spawned there. Another study, made in the Newportriver estuary (NC, USA), suggests that the high abundancesof southern flounder larvae and small juveniles collected inlow-salinity habitats were there due to direct settlement andnot to migration (Walsh et al. 1999).

The other two thirds of southern flounder otoliths, ana-lyzed by Lowe et al. (2011), showed high levels of Sr/Caratio in the otoliths’ core following a marked decline of Sr/Ca ratio, which then maintained along the remainder of theotolith. This pattern was interpreted as larvae hatched inhigher-salinity waters before entering the Mobile-TensawRiver Delta (Lowe et al. 2011). Curiously, in a recent paperon the migration patterns of European flounder Platichthysflesus (Linnaeus, 1758) (Pleuronectidae, Pisces), high con-centration levels of strontium were measured in the otoliths’core preceding an abrupt decrease of strontium levels (Mor-ais et al. 2011). However, the abrupt decrease of strontiumconcentration after the otoliths’ core was not attributed tohatching in higher-salinity waters, instead to the locationwhere the female progenitor hydrated the eggs. Hydratingthe eggs with high-salinity waters would imprint a high Sr/Ca ratio in the embryos’ otoliths, which is formed shortlyafter fertilization (e.g., Zhang and Runham 1992). Thishypothesis suggests a recent migration of the female pro-genitor from the coast/low estuary to an area of lowersalinity to spawn. Hereafter, these female progenitors willbe mentioned as “sea-run mothers.” Indeed, several studieson salmonids migration found that the progeny of femalesthat matured in sea water had higher strontium concentra-tions in the otoliths’ core (e.g., Kalish 1990; Volk et al.2000). Two other hypotheses were considered to explainthe abrupt decrease of strontium concentration after thecore of European flounder otoliths, but both were rejected(Morais et al. 2011).

One of the rejected hypotheses was similar to the oneproposed by Lowe et al. (2011), i.e., larvae hatched inhigher-salinity environments and then migrated to lower-salinity habitats. The hypothesis was rejected becauserecently hatched and pre-metamorphic European flounderlarvae do not possess the anatomical structures to activelycontrol their position in the water column (Hutchinson and

Hawkins 2004) and then use selective tidal stream transportas a mechanism to enter in the estuary and migrate upstreamuntil reaching the freshwater tidal area (Bos 1999). Regard-ing southern flounder, the appearance of the first dorsaland caudal rays occurs around day 20 post-hatching (vanMaaren and Daniels 2000); this fact suggests that any typeof active migration is not likely to be successful immediate-ly after hatching. Furthermore, if river flow is high, asusually occurs during the spawning season, then tidaladvection of southern flounder from the coast into freshwa-ter habitats was unlikely to have occurred.

The second hypothesis considered a shift in the metabolicregulation of free Sr2+ (Kalish 1989), as observed in speciesthat undergo profound metamorphosis during ontogeny,such as Anguilliformes species (e.g., Wang and Tzeng2000; Ling et al. 2005). The high strontium concentrationin the otoliths’ core of European flounders did not occur inall the analyzed specimens, but when it occurred, the suddendecrease of strontium concentration coincided with hatchingand not with the onset of metamorphosis, and thus alsoeliminating this hypothesis.

Several studies on otolith microchemistry measured highconcentration levels of trace elements (namely barium, iron,magnesium, manganese, and zinc) in the otoliths’ core ofspecies with different modes of reproduction and from var-ious habitats (Brophy et al. 2004; Ruttenberg et al. 2005;Warner et al. 2005). The high levels of these trace elementswere not environmentally driven and were probably causedby physiological processes, occurring during embryologicaldevelopment, influencing primordium formation or to avariation of otoliths’ crystal structure in the core that modi-fies the affinity of elements to otoliths’ calcium carbonateand protein matrix (Brophy et al. 2004; Ruttenberg et al.2005). It is interesting to note that strontium concentrationswere not significantly higher at the otoliths’ core in any ofthe analyzed species (Ruttenberg et al. 2005; Warner et al.2005).

Thus, by all of the above, I suggest that the high levels ofSr/Ca ratios in the otoliths’ core of southern flounder couldbe due to the spawning of sea-run mothers in the Mobile-Tensaw River Delta. So, if the “sea-run mother hypothesis”is correct, then the main conclusions and suggestions ofLowe et al. (2011) are not only valid but are also reinforced.Hence, data from the study made by Lowe et al. (2011)might be the first to suggest that southern flounder mighthatch in or near freshwater habitats, according to otolithmicrochemistry data, and that might exist a reproductivemigration of southern flounder into an estuarine ecosystem.It is possible that southern flounder migration patterns varybetween estuarine ecosystems as their distribution and hab-itat use patterns vary (Allen and Baltz 1997; Walsh et al.1999; Nañez-James et al. 2009 and references therein). Theinclusion of estuarine freshwater habitats in southern

Estuaries and Coasts (2012) 35:904–906 905

flounder management plans is reinforced, either by includ-ing gear restrictions and/or spatial and temporal closures(Smith and Scharf 2010). Finally, only a multidisciplinaryand multi-gear sampling program to collect larvae at thevarious ontogenetic stages along a salinity gradient, com-bined with ultrasonic telemetry of adult specimens (consultSackett et al. (2007) for details), otolith microchemistryanalysis, and physiological tests on field-collected speci-mens to clarify the contradiction, highlighted by Lowe etal. (2011), regarding the 100% mortality of eggs and larvaeat salinities lower than 10 (Smith et al. 1999).

Acknowledgments Pedro Morais has a postdoc fellowship financedby “Fundação para a Ciência e a Tecnologia” (SFRH/BPD/40832/2007).

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