GROWTH AMONG LARVAE OF LANTERNFISHES (TELEOSTEI: MYCTOPHIDAE) FROM THE EASTERN GULF OF MEXICO
Walter J. Conley and John V. Gartner, Jr.
ABSTRACTThe larvae of five species of myctophid fishes; Benthosema suborbitale (Gilbert,
1913), Ceratoscopelus townsendi (Eigenmann and Eigenmann, 1889), Hygophum taaningi Becker, 1965, Myctophum selenops Tåning, 1928, and Notolychnus valdiviae (Brauer, 1904) from the eastern Gulf of Mexico were examined to measure early growth in length and weight. Age was determined from examination of sagittal otoliths. Larval period ranged from 31 d for the rapidly growing C. townsendi to 60 d for the diminutive N. valdiviae. Growth rate ranged from 0.1 mm SL d–1 for N. valdiviae to 0.4 mm SL d–1 for C. townsendi. Increases in weight were variable and related to larval morphology. The most rapid increases in weight with length were observed for the stout larvae of M. selenops, whereas the slender larvae of C. townsendi and N. valdiviae increased more gradually. The growth rate and age at transformation were highly variable among the five species, but within the range displayed by other nearshore tropical-subtropical species from the Gulf of Mexico. Variations in growth appear to be related to species-specific variations in life history traits and larval morphology. These are the first data reported on the growth of larval myctophids from the Atlantic.
Early life history events determine adult population size and structure for verte-brate species (Stearns, 1976). Effects are particularly noticeable among teleosts where high fecundity combines with an unpredictable mix of biotic and abiotic factors to determine larval growth and survival (Hjort, 1914; Miller et al., 1988; Claramunt and Wahl, 2000). The larval stage is the most vulnerable for fishes. Factors affecting survival during early life include successful feeding, escape from predation, and rate of growth. Among the many factors affecting growth-related survival are size at age (Anderson, 1988; Sogard, 1997), the duration of the larval period (Houde, 1987a), and rate of growth (Takasuka et al., 2003, 2004). Larger size is related to better swimming ability and larger mouths thus larvae may find both a refuge from predation (Bailey, 1984; Luecke et al., 1990; Paradis et al., 1996) and a broader array of potential prey (Sabatés and Saiz, 2000; Conley and Hopkins, 2004). Spending less time in the larval stage reduces the time an individual or cohort is exposed to mortality factors and the rate at which larvae grow may be an indicator of their relative health. Larvae that grow more slowly have been ingested more frequently by predators (Takasuka et al., 2003), thus there is an adaptive advantage to eating well and growing rapidly (Rosen-berg and Haugen, 1982; Miller et al., 1988). Many of these factors are likely species and location specific (Rilling and Houde, 1999; Comyns et al., 2002) and our under-standing of these processes is dominated by information from commercially impor-tant coastal species (Hunter, 1972; Arthur, 1976; Warlen, 1988) that exhibit a wide range in their rate of growth (Houde, 1987b). The adaptive value of rapid growth may be less in oligotrophic waters (Hillgruber et al., 1997) where the density of predators and food availability are lower.
Mesopelagic fishes are prominent members of oligotrophic ecosystems. Mycto-phids are an abundant vertically migrating mesopelagic fish group (Gjøsaeter and Kawaguchi, 1980; Gartner et al., 1987), providing forage for a variety of fishes and
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other vertebrates (Pereyra et al., 1969; Klages and Bester, 1998). In oceanic surface waters, myctophid larvae are dominant members of the ichthyoplankton assemblage, ranging from about 30 to over 70% of fish larvae collected (Ahlstom, 1972; Loeb, 1980; Sanvicente-Añorve et al., 1998; Muhling et al., 2007), yet we know little about their early life history. Myctophid larvae are one to several orders of magnitude greater in abundance than adults and juveniles in the eastern Gulf of Mexico (Gartner et al., 1989a) suggesting that larval mortality is an important factor in determining adult population size and structure. Here we report information on the growth in length and weight of five larval myctophids from the eastern Gulf of Mexico, represent-ing the second report of myctophid larval age and growth from any ocean (Methot, 1981), and the first from the Atlantic.
Materials and Methods
All larvae were collected in the eastern Gulf of Mexico within 20 km of 27°N, 86°W, an area known as “Standard Station.” Temperature was determined with expendable bathythermo-graphs (XBT), and salinity was determined from electrical measurement of conductivity with depth (CTD). Hydrographic conditions are typical of vertically stratified oligotrophic envi-ronments and were summarized by Sutton and Hopkins (1996). Three separate collections were used in these analyses. The range in size of juveniles included 13,369 individuals (Gart-ner et al., 1987) and the range in size of larvae included 6158 individuals collected during all seasons in discrete tows of the upper 300 m (Conley, 1993). As these larvae were preserved in Formalin, they could not be used for analysis of age and growth (Radtke and Waiwood, 1980). To determine age and growth, net tows were made hourly during four late spring or summer cruises during August 1984, July 1985, May 1986, and July 1990; representing over 2 mo of daily sampling. Ichthyoplankton samples were collected in oblique tows of the upper 150 m using two 505 µm mesh plankton nets suspended side by side within a modified Tucker trawl frame (Hopkins et al., 1973). These nets had a mouth opening of 0.56 m2 per net, and a length to mouth ratio of 7:1. Fish larvae were sorted immediately from the catch, identified, mea-sured to the nearest 0.1 mm standard length (SL), and frozen in individually sealed Nalgene® capsules. Larvae were separated into three groups; one to determine dry weight, a second for extraction of otoliths, and a third to determine chemical composition (not included here).
To determine age, the sagittal otoliths were removed from the otic capsules of individual larvae, mounted in Thermoplast, and examined at 630× magnification. Images were projected to a phase contrast monitor and microincrements were quantified by two independent observ-ers. If microincrement counts differed, the otolith was reexamined. If independent counts dif-fering by more than three microincrements could not be resolved, the otolith was discarded. Several growth models were explored for best fit to results and selected based upon calculated regression coefficients and size of 0-age larvae. Dry weight was measured to the nearest 0.001 mg by drying formerly frozen larvae at 60 °C and weighing individuals on a Perkin-Elmer Autobalance AD-2 in a temperature and humidity controlled chamber.
Results
Little change (< 3 °C) in surface water temperature was observed at Standard Sta-tion (Fig. 1). A shallow mixed layer was generally present in the upper 25–75 m. Temperature rapidly decreased between 75 and 400 m, with little change at greater depths. Maximum salinities were measured at approximately 100 m; gradually de-creasing from 36.0 to 34.9 at 1000 m.
Sixty-five Benthosema suborbitale (Gilbert, 1913) otoliths were examined from lar-vae ranging between 4.2 and 10.8 mm SL (Fig. 2). Examination of larval and juvenile
CONLEY AND GARTNER, JR.: VARIATION IN GROWTH AMONG LANTERNFISH LARVAE 125
length (Table 1) revealed that transformation to juvenile in this species occurs be-tween 10.0 and 11.0 mm SL, corresponding to a calculated age at metamorphosis of 48 d (Table 1). Assuming transformation at 10.5 mm SL and hatching at 2.5 mm SL, the daily increase in SL for this species was 0.2 mm. The smallest larva of B. suborbit-ale weighed 2.9 × 10–2 mg at 2.8 mm SL and the largest weighed 2.8 mg at 9.7 mm SL. The rate of increase in weight with length was among the lowest of the five species examined (Fig. 3).
Thirty-two Ceratoscopelus townsendi (Eigenmann and Eigenmann, 1889) otoliths were examined from larvae ranging in size from 4.4 to 9.8 mm SL (Fig. 2). Transfor-mation occurred between 14.0–15.0 mm SL at an age of 31 d (Table 1). Within the larval stage, daily growth was approximately 0.4 mm SL, the highest rate of any of the species examined (Fig. 2). The smallest larva of C. townsendi weighed 7.7 × 10–2 mg at 3.9 mm SL and the largest weighed 3.0 mg at 10.5 mm SL, with relatively low increases in weight with size (Fig. 3).
Twenty-eight Hygophum taaningi Becker, 1965 otoliths were examined from indi-viduals which ranged in size from 5.4 to 7.9 mm SL (Fig. 2). The largest larva recorded from the eastern Gulf of Mexico was slightly larger than the smallest juvenile (Table 1)
Figure 1. Temperature (XBT) and salinity (CTD) profiles for the eastern Gulf of Mexico within 20 km of 27°N, 86°W.
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and estimated size at transformation was 11.0–12.0 mm SL. Assuming a transforma-tion at 11.0 mm SL, larvae of this species grew approximately 0.2 mm per d, and age at transition was 50 d. The smallest larva of H. taaningi weighed 7.3 × 10–2 mg at 3.6 mm SL and the largest weighed 1.1 mg at 6.8 mm SL (Fig. 3). The rate of increase in weight with length was the second highest among the five species examined.
Figure 2. Microincrement counts from sagittal otoliths of larvae of five species of myctophids from the eastern Gulf of Mexico. L = standard length in mm and t = age in days.
CONLEY AND GARTNER, JR.: VARIATION IN GROWTH AMONG LANTERNFISH LARVAE 127
Twenty-two otoliths of Myctophum selenops Tåning, 1928, were examined from larvae that ranged in size from 4.6 to 7.7 mm SL (Fig. 2). Assuming a transformation at 9.5 mm SL (Table 1) and a hatch at 2.8 mm SL, larvae of this species grew approxi-mately 0.2 mm SL daily, with the larval period lasting approximately 31 d. The small-est larva of M. selenops weighed 5.2 × 10–2 mg at 2.9 mm SL and the largest weighed 2.4 mg at 7.5 mm SL, exhibiting the highest rate of dry weight increase to length of the five species examined (Fig. 3).
Twenty-nine otoliths of Notolychnus valdiviae (Brauer, 1904) were examined from larvae that ranged in size from 5.2 to 8.0 mm SL (Fig. 2). The larval period of N. valdiviae was estimated at 60 d (Table 2). Assuming transformation at 10.0 mm SL (Table 1), average daily growth was approximately 0.1 mm SL, the lowest among the five species examined. The weight of N. valdiviae ranged from 4.5 × 10–2 mg at 3.0 mm SL to 1.6 mg at 8.5 mm SL and the rate of increase in weight with size was also the lowest among the five species examined (Fig. 3).
Discussion
Juveniles and adults of three (B. suborbitale, C. townsendi, and N. valdiviae) of the five species examined are considered abundant in the eastern Gulf of Mexico (Gartner et al., 1987). Restricted to tropical and subtropical waters of all three oceans (Nafpaktitis and Nafpaktitis, 1969; Clarke, 1973; Hulley, 1981), B. suborbitale adults are vertical migrators, but juveniles remain at depth (Gartner et al., 1987). Analysis of reproductive patterns indicates sustained year-round spawning (Gartner, 1993). Ceratoscopelus townsendi, a cosmopolitan species with a number of distinct and geographically separated populations (Badcock and Araujo, 1988), is a strong verti-cal migrator but small juveniles remain near daytime depths at night (Gartner et al., 1987). This species exhibits the highest fecundity among eastern Gulf of Mexico myctophids, with two relatively restricted spawning periods in the winter and sum-mer (Gartner, 1993). Notolychnus valdiviae adults are the smallest of the lantern-fishes with an unusual adult morphology (Nafpaktitis et al., 1977). This species is also primarily tropical to subtropical, occurring in all three oceans (Nafpaktitis et al., 1977; Hulley, 1981). Unlike B. suborbitale and C. townsendi, there is no evidence that juveniles remain at depth (Gartner et al., 1987). A year-round spawning pattern is evident, but with relatively low fecundity (Gartner, 1993).
Adults and juveniles of H. taaningi are common and M. selenops uncommon to rare in the eastern Gulf of Mexico (Gartner et al., 1987). The former is also common in the northern Sargasso Sea (Gartner et al., 1989b). Myctophum selenops has been
Table 1. Size ranges of larval myctophids and juveniles collected from the eastern Gulf of Mexico compared to smallest larvae as estimated from the analysis of growth. Sizes are from the examina-tion of 6158 larvae (Conley, 1993) and 13,369 juveniles (Gartner et al., 1987).
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described as an uncommon broadly-tropical myctophid (Hulley, 1981) with largest collections from the Caribbean Sea (Nafpaktitis et al., 1977). The larvae of M. selen-ops are the second most abundant lanternfish collected in the Caribbean (Richards, 1984). Houde et al. (1979) reported that larvae are absent from the Gulf of Mexico north of 28°30΄N and west of 86°W during August and most abundant during spring
Figure 3. Relationship between dry weight and standard length for larvae of five species of mycto-phids from the eastern Gulf of Mexico. DW = dry weight in mg and L = standard length in mm.
CONLEY AND GARTNER, JR.: VARIATION IN GROWTH AMONG LANTERNFISH LARVAE 129
and summer at other locations. In the eastern Gulf of Mexico, larvae of M. selenops peak in summer with overall abundances ranked 20th among the most common 25 species (Conley, 1993). No reproductive information is available for H. taaningi or M. selenops.
Age in days was estimated from sagittal otolith microincrements assumed to be de-posited daily. Although it is desirable to validate microincrements as daily (Beamish and McFarlane, 1983), the application of common techniques for the assessment of daily growth in nearshore fishes was not possible for these midwater fishes. Mycto-phids are sensitive to the stress of capture and are rarely collected live. Attempts to maintain fishes for more than brief periods have been unsuccessful (Robison, 1973). In over a decade of sampling in the eastern Gulf, myctophid larvae have never been collected alive. Nonetheless, the assumption of microincrements as indicators of age in days is reasonable for myctophid larvae because: (1) daily deposition of microin-crements has been confirmed, through marginal increment analysis, for all post-metamorphic myctophids that have been examined thus far from the Gulf of Mexico including two of the species examined in this study (Gartner, 1990, 1991a,b; unpubl. data); (2) there is circumstantial evidence for daily deposition of microincrements for myctophids from the Mediterranean (Gjøsaeter, 1987) and Tasmania (Young et al., 1988); (3) microincrements exhibit a strong one-to-one relationship to age in days for almost all teleost larvae that are not growth limited (Jones, 1986); (4) microincre-ments exhibited by the larvae examined in this study displayed clearly defined, easily distinguished microincrements that were regularly spaced, and; (5) calculation from growth equations resulted in sizes of 0-age individuals matching, or within 2 mm, of the smallest larvae collected (Table 1).
Linear growth models have been used to estimate larval growth for other Gulf of Mexico species (Cowan, 1988; Peebles and Tolley, 1988), as well as some temperate small-bodied fish (Rilling and Houde, 1999). A linear model resulted in regression coefficients that were higher overall than most common power functions, but the linear function underestimated the size of the smallest myctophid larvae; with all but one < 2.0 mm SL. An exponential growth model produced regression coefficients that were equivalent to the linear model, but better estimated the size of the smallest larvae (Table 1). Other fishes, such as Atlantic gadoids, exhibited concave up curvi-
Table 2. Growth rate and age of transformation for larval clupeids and sciaenids from the Gulf of Mexico compared to myctophid larvae.
Species Growth equationAge in days at transformation Reference
Brevoortia patronus Loge = 0.005(t) + 2.7 88–103 Deegan and Thompson (1987)Brevoortia patronus L(t) = 2.355e2.212(1–e0.0608t) 65 Warlen (1988)Cynoscion nebulosus L = 0.405(t) + 0.116 __ Peebles and Tolley (1988)Micropogonias undulatus L = 0.189(t) + 0.634 > 80 Cowan (1988)Benthosema suborbitale L = 2.5e0.03t 48 This study
Ceratoscopelus townsendi L = 3.1e0.05t 31 This study
Hygophum taaningi L = 4.2e0.02t 50 This study
Myctophum selenops L = 2.8e0.04t 31 This study
Notolychnus valdiviae L = 3.0e0.02t 60 This study
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linear growth (Campana and Hurley, 1989). Larvae grew slowly in the first week or two of life but growth rate accelerated as larvae approached transformation. This pattern was also observed in the examination of the width of microincrements in the larval zone of three postmetmorphic myctophids, which suggested larval growth rate increased with increasing age prior to transformation (Gartner, 1991b). The only other examination of otoliths removed from larval myctophids was an examination of growth pattern of the Pacific lampfish, Stenobrachius leucopsarus (Eigenmann and Eigenmann, 1890). The larvae of this species exhibited a growth pattern similar to that of Atlantic myctophid and gadoid fishes.
Fish larvae are the smallest nutritionally independent vertebrates (Wieser, 1995) with weight gains of five to seven orders of magnitude common (Houde, 1987a). Many factors, both abiotic and biotic, affect growth and survival, but no one factor can adequately explain the complex dynamics of fish populations (Anderson, 1988; Miller et al., 1988). The growth mortality hypothesis (see Anderson, 1988; Takasuka et al., 2004) predicts that increasing size increases survival through a reduction in exposure to predators and other mortality factors, thus there should be selection for rapid growth. But the larval period is highly variable among tropical-subtropical spe-cies, ranging from a few days to months (Brothers et al., 1983; Searcy and Sponaugle, 2000). Many Gulf of Mexico fish larvae are recruited to the juvenile stage between 31 to > 100 d at lengths ranging from 9 to 22 mm SL (Tables 1 and 2). Average growth rates of myctophid species ranged from 0.1 mm SL d–1 to 0.4 mm SL d–1, but growth rates as high as 0.85 mm d–1 have been reported for round herring Etrumeus teres (DeKay, 1842) from the Gulf of Mexico (Chen et al., 1992).
Hillgruber et al. (1997) compared the feeding of the larvae of the coastal Atlantic mackerel (Scomber scombrus Linnaeus, 1758) with the mesopelagic blue whiting Mi-cromesistius poutassou (Risso, 1827). While recognizing species-specific variation, the authors suggested that the rapid growth of mackerel was an adaptation to reduce their exposure to predators as they develop in a rich feeding environment. Slower growth, but more efficient foraging, of the midwater blue whiting was interpreted as an adaptation to life in a relatively stable, if food-poor, environment. Myctophid larvae are often the most abundant fish group in this stable, food-poor environment (Ahlstom, 1972; Loeb, 1980; Sanvicente-Añorve et al., 1998; Muhling et al., 2007) and also appear to be efficient foragers (Conley and Hopkins, 2004). Compared to round herring (Chen et al., 1992), myctophids do grow slowly; but the slowest grow-ing myctophids were similar in daily growth and age at transformation (Table 2) to nearshore tropical-subtropical clupeids (Deegan and Thompson, 1987; Warlen, 1988) and sciaenids (Cowan, 1988; Peebles and Tolley, 1988). Instead, this group of myctophids exhibits a variety of growth rates, with the fastest growing species (C. townsendi) increasing in length more than three times the slowest growing species (N. valdiviae).
Among myctophid larvae, variation in the increase of length and weight reflects known life history and morphological characteristics. Ceratoscopelus townsendi adults are the largest of the abundant myctophids in the eastern Gulf of Mexico (Gartner et al., 1987) and their larvae exhibited the fastest increase in length with age. Increase in dry weight with length for this species, however, was among the low-est of the five species examined. Larvae are slender and remain so throughout the larval period. Conversely, M. selenops had the highest rate of increase in weight with length. These are stout larvae throughout the larval period (Moser and Ahlstrom,
CONLEY AND GARTNER, JR.: VARIATION IN GROWTH AMONG LANTERNFISH LARVAE 131
1974; Olivar et al., 1999) with large heads and mouths relative to body length (Conley and Hopkins, 2004). Larvae of H. taaningi also exhibited a high rate of increase in weight with length. These larvae, while not as robust as M. selenops, are not slender, but broad along the dorso-ventral axis (Moser and Watson, 2001). Larvae of B. subor-bitale exhibited an unusual pattern of growth. At < 4 mm SL it is a relatively slender larva, but between 4 and 8 mm SL, the larvae add girth with relatively little increase in body length (Badcock and Merrett, 1976). This is reflected in the relatively large amount of scatter in age within this size range (Fig. 2). Notolychnus valdiviae adults are the smallest of the myctophids (Nafpaktitis et al., 1977) and the slowest grow-ing larvae in both length and weight. This species also exhibited the longest larval period, transforming in about 60 d.
Thus, the examination of the biology of myctophid larvae suggests that this group has adapted in multiple ways to survive in a stable oligotrophic environment. These adaptations include dramatic variation in larval morphology (Moser, 1981; Moser et al., 1984), variation in the depth at which individual species reside (Loeb, 1980; Conley, 1993; Sassa et al., 2002; Sabatés et al., 2003), variation in eye morphology (Weihs and Moser, 1981) and retinal histology (Pankhurst, 1987; Sabatés et al., 2003), variation in the type and size of food preferred (Sabatés and Saiz, 2000; Conley and Hopkins, 2004), gape (Conley and Hopkins, 2004), and growth in length and weight. There does not, therefore, appear to be consistently slower pelagic growth rate. In-stead, myctophid larvae display a notable diversity in many of the parameters that likely influence survival through the larval period.
Acknowledgments
Many individuals assisted in the collection of zooplankton. Our thanks go to J. Donnelly, M. Flock, S. Kinsey, K. Passarella, J. Rast, and T. Sutton who assisted with net collections. Comments and suggestions from three anonymous reviewers served to improve the quality of this manuscript, for which we are grateful. We especially wish to express our gratitude to C. Obordo for her assistance with library searches. The cruises were supported by the State of Florida and NSF OCE #841787 grant to T. L. Hopkins, The Houston Underwater Club Seas-pace Scholarship, John Lake Foundation, and Gulf Coast Charitable Trust.
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Addresses: (W.J.C.) Biology Department, State University of New York, 44 Pierrepont Avenue, Potsdam, New York 13676. (J.V.G.) Department of Natural Science, St. Petersburg College, 6605- 5th Avenue North, St. Petersburg, Florida 33710. CorresPonding Author: (W.J.C.) E-mail: <[email protected]>.
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