BULLETIN OF MARINE SCIENCE, 63(2): 295–303, 1998

GROWTH AND MORTALITY OF LARVAL CHRYSURUS (PISCES: ) IN THE SOUTHERN GULF OF MEXICO

Marina Sánchez-Ramírez and César Flores-Coto

ABSTRACT Seasonal age, growth and mortality rates of larval Atlantic bumper, Chloroscombrus chrysurus, were determined from larvae collected in 13 cruises in the southern Gulf of Mexico. Age was estimated from growth increments in sagittal otoliths. One and two days, respectively, were added in the linear model to the growth increments in spring- summer and winter seasons, to estimate the probable true age. Results for spring, sum- mer and winter are: hatching size 0.76, 0.84 and 1.02 mm; growth rates 0.17, 0.17 and 0.12 mm d−1, and mortality rates 0.30, 0.16 and 0.15 d−1, respectively. Higher temperature and food availability seem to be associated with higher growth rates in spring and sum- mer. The lower mortality rate recorded in winter could be a consequence of low tempera- ture, low growth rate, low larval abundance, and dilution of larval patches in the water column (due to very frequent cold fronts [Nortes] in this season). The summer mortality rate was lower than in spring, possibly a consequence of an expansion of the spawning area during summer and therefore higher larval dispersion.

Many commercially important have been intensively studied so that they may be optimally managed. Growth, mortality, migration, food habits, length-age rela- tionships, distribution, and abundance studies are all common topics in the scientific literature. Some of these studies have concentrated on the early life history stages, be- cause of its importance in the survival of these stages to the future adult stock size. Studies of larvae of non-commercial species are less frequent. Although some of these species are ecologically important and some many also have a potential impor- tance. The Atlantic bumper, Chloroscombrus chrysurus, in the southern Gulf of Mexico is one such example where it is one of the most abundant, unexploited species (Yañez- Arancibia and Sánchez-Gil, 1986; Flores-Coto and Sánchez-Ramírez, 1989; Tapia-García, 1991). Atlantic bumper spawns in Campeche Bay year round but mainly in spring and sum- mer, in areas less than 40 m deep; the highest larval abundance has been recorded off Términos (Flores-Coto and Sánchez-Ramírez, 1989). Except for descriptions of larval abundance and distribution in the southern Gulf of Mexico, there is no information on the early life history of this species. Therefore a better knowledge of Atlantic bumper is a priority and thus the goals of this study are to estimate ages of its larvae and to determine larval growth and mortality rates by season.

MATERIALS AND METHODS

LA RVA L COLLECTION.—The study area is located in the southern Gulf of Mexico between 18°06'– 21°00'N and 90°26'–97°20'W. It comprises the and the adjacent oceanic zone of the States of Veracruz, Tabasco and Campeche (Fig. 1). The samples were collected aboard the oceanographic vessel JUSTO SIERRA, during 13 cruises between 1984 and 1993 (Table 1). Zooplankton sampling consisted of a double oblique

295 296 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 2, 1998

Figure 1. Study area

plankton tow following a circular course using a bongo net with 333- and 505-µm mesh nets, except for the cruise Mopeed V where several depths in the water column were sampled using an opening- closing net of 75 cm diameter and 505-µm mesh. The filtered water volume was calculated using flowmeters placed in each net. Larvae were sorted out of 505-µm mesh and preserved in 70% ethanol. Larval Atlantic bumper were measured as standard length, or notochord length before notochord flexion, with 0.1 mm precision. AGE AND GROWTH.—For growth estimation, sagittal otoliths were obtained from larvae collected in the summer 1987 and 1988, winter 1992 and 1993, and spring 1992 cruises. Because of the poor condition of the otoliths in the fall 1987 cruise and the scarcity of larvae on the fall 1992 cruise, no larvae were aged from the fall samples. SÁNCHEZ-RAMÍREZ AND FLORES-COTO: GROWTH AND MORTALITY OF ATLANTIC BUMPER 297

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Age of larvae was estimated by counting the number of growth increments on sagittal otoliths and adding a value representing the number of days from hatching to formation of the first growth mark. This aging technique for larval Atlantic bumper has been validated by Leffler and Shaw (1992) who consider that each observed growth increment in the sagittal otolith represents 1 d in the larvae of this species. Some otoliths, particularly the largest ones, could not be read. To solve this problem, the long and short radius, and the diameter of all otoliths were measured, thus estab- lishing relationships with the number of increments of those that were readable. For growth models of each season (spring, summer and winter) a linear model was fitted to the age/length data since it had the highest determined coefficient (r2):

SL = b(t) + a Eq. 1 where: SL = Standard Length or notochord length (mm); a = y-axis intercept; hatching size, mm (size at 0 age); b = constant, growth coefficient; and t = age of the larvae, expressed as the number of daily growth marks plus number of elapsed days, from hatching to the formation of the first growth mark. MORTALITY.—To build the mortality model it was necessary to estimate larval abundance. The abundance of larvae at each sampling station was standardized as number of larvae m−2, as pro- posed by Houde (1977), in this case for each 0.5 mm size class, using the model:

Nij = cijdi/vi Eq. 2

−2 where: Nij = number of larvae m of marine surface at station i, of size class j; cij = caught larvae at 3 station i, of the size class j; di = depth of tow (m) at station i; and vi = filtered water volume (m ) at station i. Average larval abundance for each size class (0.5 mm SL) for each season was estimated for the different cruises: two for spring, four for summer and five for winter:

n A = ∑ N /N Eq. 3 j i=1 ij ps 298 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 2, 1998

Figure 2. Relationship daily increments-radius otholits of larval Chloroscombrus chrysurus. (A) spring; (B) summer; (C) winter. Southern Gulf of Mexico.

where: Aj = Larval average abundance of size class j; Nij = defined above; and Nps = number of positive stations by season s, corresponding to the stations with Atlantic bumper larvae. Mean age of each size class was estimated through the growth models for each season. The instantaneous mortality rate (IMR) was estimated from an exponential model that described the decrease in the average abundance of each size class:

−zt Aj = Ajoe Eq. 4

−2 where: Aj = Larval average abundance m at age t; Ajo = constant. This intercept is an estimation of larval abundance at age “0”; z = instantaneous mortality rate (d−1); and t = age (in days). Mortality (A) and survival percentage (S) were obtained from the models:

A = 100(1−e−z) S = 100e−z S = 100−A, 0 ≥ S, A ≤ 100 Eq. 5

For the mortality analysis, we had to first establish the size at which larvae were captured by the sampling gear to eliminate from the model small larvae that could pass through the mesh, and consequently not be well represented in the catch. We measured 109 larvae to establish the standard length and body depth relationship. Considering that the maximum opening area in the 505-µm mesh is 0.714 mm, larvae ≥2.3 mm SL (0.8 mm body depth), were captured by the sampling gear. Because average larval abundance in the spring showed a lower value in the 2.3 mm size class, than in 2.8 mm; the Robson and Chapman method (1961) was used to determine if inclusion of the 2.3-mm size class was valid in the mortality model. The largest sizes were probably not well sampled because they evaded the net. Therefore, starting with the first size class, where no larvae were captured, they were eliminated. SÁNCHEZ-RAMÍREZ AND FLORES-COTO: GROWTH AND MORTALITY OF ATLANTIC BUMPER 299

Figure 3. Growth of larval Chloroscombrus chrysurus. (A) spring; (B) summer; (C) winter. Southern Gulf of Mexico.

RESULTS AND DISCUSSION

GROWTH.—To estimate the number of growth marks of otoliths in which it was not read, and to include these larvae in the growth models, the analysis consisted of the relation- ship among the number of daily increments and shorter, longest radius and diameter of the otoliths. The highest coefficient of determination in the linear model was found with the longest radius. Larvae of size 1.6–6.6 mm SL from spring, 1.4–6.0 mm SL from summer and 1.9–7.2 mm SL from winter were used in these relationships (Fig. 2). For the growth models by season, the size ranges used were: 1.6–6.6 mm SL (57 larvae) in spring, 1.4–11.7 mm SL (69 larvae) in summer, and 1.9–7.9 mm SL (54 lar- vae) in winter. As mentioned above, the linear model better fitted the observed data. Estimated growth rates were higher in spring and summer (0.17 mm d−1) than in winter (0.12 mm d−1) (Fig. 3). These values were compared using the t-test (Zar, 1984) and are significantly different (P < 0.001). Larval growth is essentially controlled by two factors, temperature (Warlen, 1988; Houde, 1989; Morse, 1989; Rutherford and Houde, 1995) and food availability (Methot and Kramer, 1979; Warlen, 1988; Kiørboe et al., 1988). The observed growth rate differences between spring-summer and winter larvae could result from differences in temperature and food availability. The spring-summer surface water temperatures fluctuated between 24.0 and 33.0°C (Flores-Coto and Gracia-Gasca, 1993) and from 22.3 to 25.0°C in winter 300 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 2, 1998

Figure 4. Mortality of larval Chloroscombrus chrysurus. (A) spring; (B) summer; (C) winter. Southern Gulf of Mexico.

(Shirasago-German, 1991) and these differences could affect the larval metabolic rate. On the Campeche Bank, the highest zooplankton biomass occurs in summer and spring, with the highest densities in the coastal area off Terminos Lagoon; during winter those values decrease considerably (De la Cruz, 1972; Flores-Coto et al., 1988). We assume that spring-summer zooplankton biomass corresponds to higher food availability and consequently to higher growth rates. Though the growth rates of larval Atlantic bumper (0.17 mm d−1 in spring and summer, and 0.12 mm d−1 in winter) were lower than those recorded (also in the linear models) by Leffler and Shaw (1992) (0.40, 0.26, and 0.31 mm d−1 during summer) for larvae with size of 0.8–4.8 mm. They also mentioned that temperature has a significant influence because they found that higher growth rates were associated with the highest temperature (29.6°C). Other species from the southern Gulf of Mexico also have low growth rates, such as Achirus lineatus, 0.046 mm d−1 (Flores-Coto et al., 1992) and Bregmaceros cantori, 0.09 mm d−1 (Zavala-García and Flores-Coto, 1994). This could mean that growth rates of the same species, are lower than those of the northern Gulf populations. Nevertheless, Sánchez-Ramírez and Flores-Coto (1993) mention that carangid larval development may be faster in southern Gulf populations. AGE.—The actual age of the larvae was estimated in all cases, which required addition to the number of daily growth increments an added number of days. The number of added days in turn are based on the resulting hatching size derived from the model, which is around 0.7–0.9 mm, values recorded by Leffler and Shaw (1992) for Atlantic bumper SÁNCHEZ-RAMÍREZ AND FLORES-COTO: GROWTH AND MORTALITY OF ATLANTIC BUMPER 301

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Sfnosae NumberoTotalabundanceInstantaneousSyE%dailr2 larvae(numberoflarvaem−2)dailymortalitymortality S2pring13,391075.303.302.03235.90.9 S7ummer50,1616,331.107.109.00174.70.9 W4inter202354.500.103.03183.90.7

specimens from the northern Gulf of Mexico. These authors mentioned that this species appears to begin otolith increment deposition after yolk absorption, 2 d after spawning (allow 1 d each for egg incubation and yolk sac absorption). Under this consideration and that hatching sizes must be smaller than the smallest larvae caught 1.4, 1.1 and 1.6 mm SL, in spring, summer and winter respectively, without yolk sac and presenting growth marks in the otoliths, the results of adding 1 d in spring and summer were 0.76 mm and 0.84 mm respectively, and 1.02 mm in winter by adding 2 d (Fig. 3). Variations in water temperature can reduce or extend egg incubation time, duration of the yolk-sac larval stage, time of first feeding, and consequently otolith increment forma- tion (Leffler, 1989). The lower surface water temperatures in winter (<25.0°C) in the southern Gulf (Shirasago-German, 1991) may be causing a lower larval metabolism rate, and could result in a larger number of days being added in the winter model. At lower temperatures, the yolk sac is probably consumed more slowly, in contrast to spring and summer when the temperatures are higher (24.0–33.0°C) (Flores-Coto and Gracia-Gasca, 1993). MORTALITY. —Larvae of size class 2.3–5.8 mm SL and age 9.1–29.7 d in spring, and 2.3–9.8 mm SL and 8.6–52.7 d in summer, and 2.3–6.3 mm SL and 10.6–43.9 d in winter were used to model the exponential decrease of the average abundance. The IMR values were: 0.30, 0.16 and 0.15 d−1 for spring, summer and winter, respectively (Fig. 4, Table 2). The results show that the percentage daily mortality was higher in spring (25.9%) than in summer (14.8%) and winter (13.9%) (Table 2). The slopes were compared using the t-test (Zar, 1984); the differences were significant (P < 0.001) between spring and summer, and spring and winter, but not between summer and winter. The IMR could be influenced by several factors, such as temperature, growth rates, patchiness, larval density among others, and by the interaction of these factors. Pepin (1991) proposed that increases in mortality rates are associated with increasing larval growth rates because high growth rates require high ingestion rates, which in turn require that higher numbers of prey items be encountered and consequently there are increased encounters with predators. Our results do not fit well with these ideas because we found a different IMR in spring and summer with the same growth rate. This could be a consequence of the larger spawn- ing area in summer (Flores-Coto and Sánchez-Ramírez, 1989), and probably a higher larval dispersion, which could reduce mortality through fewer encounters with predators. Atlantic bumper larvae usually aggregate in patches (Leffler, 1989). McGurk (1986, 1987) considered that the formation of large larval patches offers exceptional opportunity for predators. Larvae that develop in cold water tend to spend more time in any develop- mental stage than larvae which develop in warmer water; thus, temperature controls the rate of development of larvae and so may control the duration of the period within which 302 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 2, 1998 the interaction between mortality and patchiness operates. When there is a slow growth, the larval stage duration is increased and the patches are diluted by turbulent diffusion of the upper waters layers which diminish encounters with predators and conse- quently the mortality (McGurk, 1987). The lowest mortality observed in winter seems to fit better with the ideas of McGurk (1986, 1987) and Pepin (1991), considering that under low food availability and low tem- perature, growth must be slow, contributing to higher larval-patch dilution and conse- quently fewer encounters with predators. In the southern Gulf of Mexico, frequent winter cold fronts (Nortes) produce a deeper mixed layer and homogenization of the water col- umn to 100 m (Alatorre et al., 1989), resulting in greater patch dilution and lower mortal- ity by predation. Temperature is probably the most important factor influencing larvae mortality (Houde, 1989). Leffler and Shaw (1992) in particular found the highest mortality rates of larval C. chrysurus to be associated with higher temperature, and higher larval densities. We noted lower larval density and water temperatures in winter when larval mortality rates were the lowest. The IMR we obtained for C. chrysurus in the southern Gulf of Mexico are lower than those recorded by Leffler and Shaw (1992) for this species in the northern Gulf of Mexico in August (0.62 d−1, 46.2%) and September (0.17 to 0.35 d−1, 15.6–29.5 %).

ACKNOWLEDGMENTS

We thank F. Zavala for technical and field assistance, M. Ulloa for assistance in the translation, the crew of the O/V JUSTO SIERRA, CONACyT for the scholarship granted to M. Sánchez-Ramírez, and to the anonymous reviewers by the sound criticism, improving substantially this paper.

LITERATURE CITED

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Kiørboe, T., P. Munk, K. Richardson, V. Christensen and H. Paulsen. 1988. Plankton dynamics and larval herring growth, drift and survival in a frontal area. Mar. Biol. 44: 205–219. Leffler, D. L. 1989. Composition, abundance, and small-scale distribution of ichthyoplankton off the Louisiana-Mississippi Barrier Islands, with special emphasis on the age, growth, and mor- tality of Chloroscombrus chrysurus. M.S. Thesis, Louisiana State Univ. Agricultural and Me- chanical College, Louisiana. 150 p. ______and R. F. Shaw. 1992. Age validation, growth, and mortality of larval Atlantic bumper (Carangidae: Chloroscombrus chrysurus) in the northern Gulf of Mexico. Fish. Bull., U.S. 90: 711–719. Methot, R. D. and D. Kramer. 1979. Growth of northern anchovy, Engraulis mordax, larvae in the sea. Fish. Bull., U.S. 77: 413–423. McGurk, M. D. 1986. Natural mortality of marine pelagic fish eggs and larvae: role of spatial patchiness. Mar. Ecol. Prog. Ser. 34: 227–242. ______1987. Natural mortality and spatial patchiness: reply to Gulland. Mar. Ecol. Prog. Ser. 39: 201–206. Morse, W. W. 1989. Catchability, growth, and mortality of larval . Fish. Bull., U.S. 87: 417– 446. Pepin, P. 1991. Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Can. J. Fish. Aquat. Sci. 48: 503–518. Robson, D. S. and D. G. Chapman. 1961. Catch curves and mortality rates. Trans. Am. Fish. Soc. 90: 181–189. Rutherford, E. S. and E. D. Houde. 1995. The influence of temperature on cohort-specific growth, survival, and recruitment of striped bass, More saxatilis, larvae in Chesapeake Bay. Fish. Bull., U.S. 93: 315–332. Sánchez-Ramírez, M. and C. Flores-Coto. 1993. Desarrollo larvario y clave de identificación de algunas especies de la familia Carangidae (Pisces) del sur del Golfo de México. An. Inst. Cienc. del Mar y Limnol. Univ. Nal. Autón. México. 20: 1–24. Shirasago-Germán, B. 1991. Hidrografía y análisis frontogenético en el sur de la Bahía de Campeche. Tesis de Maestría. Proyecto de Especialización, Maestría y Doctorado en Ciencias del Mar de la UACPyP del CCH., UNAM. 141 p. Tapia-García, M. 1991. Análisis comparativo-poblacional y ecológico-de las poblaciones dominantes en las comunidades de peces demersales del sur del Golfo de México: Trachurus lathami, Chloroscombrus chrysurus, Priacanthus arenatus, Cynoscion arenarius y Cynoscion notus. Tesis de Maestría. Inst. de Ciencias del Mar y Limnol. UACPyP-CCH. U.N.A.M. 49 p. Warlen, S. M. 1988. Age and growth of larval gulf menhaden, Brevoortia patronus, in the northern Gulf of Mexico. Fish. Bull., U.S. 86: 77–90. Yáñez-Arancibia, A. and P. Sánchez-Gil. 1986. Los peces demersales de la plataforma continental del sur del Golfo de México. An. Inst. Cienc. del Mar y Limnol. Univ. Nal. Autón. México. Publ. Esp. 9: 1–230. Zar, J. H. 1984. Biostatistical analysis. 2nd ed. Prentice Hall. New Jersey: 292–305. Zavala-García, F. and C. Flores-Coto. 1994. Growth, mortality and feeding habits of Bregmaceros cantori larvae and juveniles from the southern Gulf of Mexico. Trop. Ecol. 35: 185–198.

DATE SUBMITTED: January 12, 1996. DATE ACCEPTED: August 7, 1996.

ADDRESS: Laboratorio de Zooplancton, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México. Apartado Postal 70-305, México, D. F. 04510, Mexico. ➤ 276 Because I cannot vouch for the taxonomic accuracy of many of the groups (even traditionalist natural historians tend to be specialists nowadays), I dipped into several groups with which I am a bit more familiar in to see how well the keys actually worked. In the great majority of cases, I had little trouble. There are some exceptions, however. The keys are written for fresh, live and relaxed organisms, which may present practical problems, certainly for preserved specimens, but also for trawled materials. For example, to identify the basket star, Gorgonocephalus arcticus, using key 1.2, the correct choice under texture would be spiny, but key 16.8 indicates that the spines are reduced to tiny hooks; the correct shape is star-shaped, but a typically coiled up specimen is not obviously so, and its highly branched arms may be interpreted by the novice as tentacles, which it is not supposed to have. As another example, the salient feature of encrusting ectoprocts with withdrawn lophophores is scattered holes, a choice that leads only to sponges in key 1.2. Also, I do not understand why the author gives each character list and its accompanying key separate numbers and equivalent headings. For example, the character list for Amphi- pod Group 3 is 15.42 and its tabular key is 15.43. One would never go directly to 15.43 from a previous, more general key because one goes to and must first read character list 15.42. Similarly, in working backward from more specific to more general keys, one would first check the character list of abbreviations again. Further, the same style line and number box separate each tabular key from the succeeding, independent character list, making it initially unclear which list goes with which table. Despite its difficult organization, this field guide will likely prove easier to use than traditional guides with which one flips more or less randomly through pages until hitting on a picture or photo of something more or less similar to the unknown specimen at hand. As mentioned above, an enormous amount of practical information exists between two covers here. It is a useful addition to the bookshelf of anyone in northeastern North America who needs to identify marine .— Charles G. Messing, Nova Southeastern Uni- versity Oceanographic Center, 8000 North Drive, Dania, 33004.