Patterns of Reproduction in the Dominant Lanternfish Species

BULLETIN OF MARINE SCIENCE. 52(2): 721-750. 1993

PATTERNS OF REPRODUCTION IN THE DOMINANT LANTERNFISH SPECIES (PISCES: MYCTOPHIDAE) OF THE EASTERN GULF OF MEXICO, WITH A REVIEW OF REPRODUCTION AMONG TROPICAL-SUBTROPICAL MYCTOPHIDAE

John V Gartner, Jr.

ABSTRACT Reproductive patterns were determined for the seven numerically dominant species of myctophids in the eastern Gulf of Mexico: Benthosema suborbitale, Ceratoscopelus species (cf. warmingi/), Diaphus dumerilii. Lampanyctus alatus. Lepidophanes guentheri. Myctophum affine. and Notolychnus valdiviae. Overall sex ratios differed significantly from parity only in Ceratoscopelus species (cf. warmingii) because of size dimorphism among the largest individuals. Oocyte development was typically teleostean and did not differ among the seven species. In all species, maximum oocyte diameter at hydration was about 0.5 mm, which was smaller than has been reported for conspecifics from other parts of their range. Sizes at sexual maturity and maximum lengths were also smaller when compared to con specifics outside the Gulf of Mexico. An increasing percentage of advanced stage (migratory nucleus and hydrated) oocytes with increasing length was observed among all species, which suggested that spawning frequency increased as the fishes grew larger. Among species for which data were available, spawning occurred only during the night at epipelagic depths with peak activity generally after midnight. Two basic reproductive patterns were noted: I) a protracted spawning season of 4- to 6-months duration, with individuals spawning every I to 4 days (Benthosema suborbitale, Lampanyctus alatus, Lepidophanes guentheri. and Notolychnus valdiviae); 2) more restricted spawning periods which primarily occurred once or twice a year (Ceratos- copelus species and probably Diaphus dumerilii). Diaphus dumerilii. though present in great numbers in the eastern Gulf, was represented almost solely by juveniles and subadults. Available evidence indicated that upon reaching sexual maturity, Diaphus dumerilii shifted to a pseudoceanic or possibly benthopelagic lifestyle, with spawning activities restricted to waters overlying the shelfedge. Protracted spawners all shared bimodal oocyte size frequencies among the most advanced oocyte stages with both modes being nearly equivalent in frequency, a linear increase in fecundity with increasing length, batch fecundities in the low hundreds to low thousands and an average life span of I year or less. Seasonally restricted spawners also exhibited bimodal oocyte size frequencies but with a greatly reduced frequency in the second mode, an exponential increase in fecundity with increasing size, batch fecundities in the high thousands to low ten thousands, and a life span ofless than] to about 2 years. The energetic cost of maximum reproductive output at the maximum rate of spawning was about 30% of the daily assimilated caloric ration in the protracted spawner Lepidophanes guentheri. This suggested that myctophids are capable of sustaining either reproductive pattern, but that growth will most probably slow at larger sizes. Both reproductive strategies allow myctophids in the eastern Gulf to have spawning season (=lifetime in annual species) fecundities that far exceed the low batch fecundities. As a result, myctophids are able to sustain population sizes equivalent to or larger than larger bodied mesopelagic competitors such as Gonostoma elongatum that exhibit high batch fecundities, but which may spawn only once in their lifetime.

Lanternfishes of the family Myctophidae occupy a central role in the energetics of oceanic ecosystems. Myctophids are extremely abundant in virtually all of the world oceans (Clarke, 1973; Backus et al., 1977; Hulley, 1981); their habit of migrating between mesope1agic and epipelagic (sensu Marshall, 1971) depths over each diel cycle represents a huge movement of energy through the water column (Clarke, 1973; Gartner et aL, 1987). They are important predators on many groups

721 722 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

of zooplankton (Hopkins and Baird, 1977, 1985; Hopkins and Gartner, 1992) and in tum serve as prey for a wide variety of predators, including mesopelagic piscivores, cetaceans, and seabirds (Borodulina, 1972; Fitch and Brownell, 1968; Robison and Craddock, 1983; Ainley et al., 1986). In addition, myctophids con- tribute large amounts of rapidly sinking, organically rich fecal material to bathype- lagic and deep benthic habitats (Robison and Bailey, 1981). The increasing direct importance of myctophids to man has also been demonstrated in recent years: active or exploratory fisheries are now practiced by several countries (see Gjosaeter and Kawaguchi, 1980 for review). In contrast to the apparent importance of myctophids, there are few published accounts detailing the life histories of myctophid species and populations, particularly in low latitude systems where the family is especially diverse (Nafpaktitis et al., 1977). Fewer still have treated more than a single species (Clarke, 1983, 1984; Karnella, 1987). Recent taxonomic research on mesopelagic fishes indicates considerable potential for inter-regional variations in morphologies and life histories, particularly among broadly distributed species inhabiting subtropical to equatorial waters (Badcock, 1981; Gibbs, 1986; Johnson, 1986; Badcock and Araujo, 1988). This variability suggests that detailed information on distributions and life histories of individual myctophid species must be obtained on a regional basis, especially in lower latitude habitats. In this paper the patterns of reproduction, including size at sexual maturity, oocyte development, fecundity, spawning frequencies, and spawning periods are presented for the seven numerically dominant species of myctophids collected during a series of eight seasonal cruises over a 30-month period between September 1984 and March 1987. Published information on reproduction among tropical- subtropical myctophid species is reviewed and compared to and contrasted with findings of this study.

MATERIALS AND METHODS

Specimen Collection. - Myctophids were collected from the eastern Gulf of Mexico within a 20 n mi diameter circle centered at 27°N, 86°W during eight cruises from September 1984 through March 1987. All samples were taken using modified Tucker trawls. Two sizes of trawl mouth area and mesh were used. The larger trawl had a 5.3 m' effective fishing area with 4 mm bar mesh in the body, 505 I'm in the funnel and 333 I'm in the codend buckct. Two versions of a smaller 2.6 m' effective fishing area net were used. One had mesh sizes identical to that of the larger gear; the other was constructed of 1.6 mm Nitex mesh throughout the body and funnel and 333 I'm in the codend bucket. The collection efficiencies of these nets have been described in Gartner et aL (1989). All nets were fished in a similar manner, with trawling speeds of 1.5 to 2 k. Trawl depths were monitored by both mechanical time-depth recorders (TDR) attached to the trawl frame and by on-deck electronic depth readout via conducting cable. Other details of sampling are presented in Gartner et aL (1989) and Lancraft et aL (1988). All individuals of the dominant species that were collected during each cruise were used for reproductive analyses. Every effort was made to minimize sampling biases that could produce intra- and intercruise variability related to size, distributional and temporal effects. The two mesh sizes utilized in combination have been shown to effectively sample the entire post-metamorphic population size range of each of the dominant myctophid species (Gartner et aL, 1989). Virtually all reproductive data were from nighttime (I h after sunset, I h before sunrise) oblique tows from the surface to 200 m (±5%) and back to surface. This depth range was chosen as it encompasses the entire nighttime habitat depth ranges for sexually mature individuals of both sexes of all species examined (Gartner et aL, 1987), thus eliminating potential biases due to incomplete sampling of the population habitats. Average duration of fiShing for these trawls was I h. To eliminate potential sampling bias due to temporal variations in sampling, efforts were made to keep the time frames of consecutive nighttime samples the same both within and between cruises. To determine if there was a seasonal variation in population abundances that could affect reproductive effort, species abundances were standardized for each species to the number of individuals captured per 10,000 m3 for each collection period. A species was considered to be abundant in a collection period if the number of individuals was> 10 per 10,000 m3 of water filtered. GARTNER: REPRODUCTIVE PATTERNS OF LANTERN ASHES 723

Table I. Collection data

Number of samples (volume filtered 10' m')

Cruise 2.6 m' 1.6 mm 5.3m' 4mm September 1984 3 (3.84) 3 (6.42) March 1985 14 (16.94) II (24.31) July 1985 9 (10.28) 8 (17.56) November 1985 4 (4.21) 17 (30.92) January 1986 10 (I 1.85) II (26.13) May 1986 13 (13.91) 10 (20.19) January 1987 16 (18.89) 7 (16.32) March 1987 9 (9.82) II (22.74) Totals 78 (89.74) 78 (164.59)

Specimens were also examined from a series of eight discrete depth tows made during each cruise (except January and March 1987) within 25 m depth strata between 0 and 200 m. Average duration of discrete tows was also I h. Some daytime collections were examined from tows which ranged over several hundred meters and between 500 and 1,000 m and whose duration was typically 3 to 4 h. Individuals of dominant species collected during the day were examined only for the gonad class vs. diel period analysis (see below). Table I lists pertinent collection information. Reproductive Data Collection. - The reproductive biology of seven myctophid species was analyzed: Benthosema suborbitale (Gilbert, 1913); Ceratoscopelus species (cf. warmingii) (Luetken, 1892); Dia- phus dumerilii (Bleeker, 1856); Lampanyctus alatus Goode and Bean, 1896; Lepidophanes guentheri (Goode and Bean, 1896); Myctophum affine (Luetken, 1892); and Notolychnus valdiviae (Brauer, 1904). These species comprised 75% or more of the total number of myctophid specimens collected throughout the year in the eastern Gulf of Mexico (Gartner et aI., 1987; Gartner, 1990). Collections were fixed at sea in 10% v:v seawater buffered formalin and preserved in 50% isopropanol. All myctophids were identified to species, measured to the nearest millimeter standard length (mm SL) and weighed to the nearest 0.1 g blotted wet weight. The gender of all individuals of the seven dominant species was determined by opening the abdominal cavity and examining the gonads using a dissecting microscope at 15 x magnification (25 x for specimens less than 25 mm SL). Ovaries were classified according to the macroscopic criteria listed in Table 2. Confirmation of the validity of the criteria used to macroscopically identify each ovarian gonad class (hereafter abbreviated GC) was obtained by making histological preparations of a series of gonads taken from both sexes of each species, and relating histological characteristics to macroscopic observations (Table 2; Fig. I). Gonads were embedded in paraffin, sectioned at 5 ILm and stained with Harris' Hematoxylin and Eosin. To more clearly delineate gonadal structure, additional preparations were made using sections embedded in glycol methacrylate, sectioned at 3 ILm and stained using a metanil yellow modified Periodic Acid Schiff stain (Quintero-Hunter et aI., 1991). For each species, the entire post-metamorphic size range was subdivided. The diminutive species B. suborbitale and N. valdiviae were partitioned into three millimeter increments, while the other relatively larger species were subdivided into five millimeter size classes. Size at sexual maturity in females was defined as the size at which 50% of the individuals had attained GC III, i.e., ovaries with vitellogenic oocytes (Table 2). Size at sexual maturity for each species was detefmined by plotting percent of individuals with ovaries ofGC III or greater vs. standard length for each millimeter standard length over the entire size range of each species. FlSHPARM, a non-linear parameter estimation for fisheries computer program was used to fit logistic curves to the data for each species and calculate confidence intervals. The frequencies of individual GCs were compared among cruises to detect evidence for seasonal spawning. Myctophum affine was omitted from these analyses because it was not effectively sampled at its zone of maximum nighttime density (0-5 m, Gartner et aI., 1987). Observations on reproductive biology for this species have been limited to determinations of batch fecundities and oocyte size frequencies among GCs. Sex ratios were determined for each species (except M. affine) and tested for both overall and intercruise deviations from parity using a chi-square goodness of fit (Sokal and Rohlf, 1981). Significant differences in intra-specific sex ratios among size groups were also tested using chi-square goodness of fit. Size-frequency distributions of oocytes within GCs were determined for each species in order to resolve whether batch fecundities could be estimated based on the presence of separable size-frequency 724 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993 GARTNER: REPRODUCTIVE PATTERNS OF LANTERN FISHES 725 modes. Ovary pairs assigned to each GC were removed from each of five females. The oocytes were teased apart using fine forceps, then placed in a vial of 50% isopropanol and shaken vigorously for 2 min to complete the separation. The contents of the vial were then poured into a gridded petri dish and the first 100 isolated oocytes were measured to the h:'arest 0.025 mm. The five sets of measurements for each GC were combined to produce the oocyte frequency distribution plots. Undeveloped "reservoir oocytes" of <0.10 mm were ignored when determining the frequency modes within a given gonad class. Oocyte size-frequency data showed clearly separated modes of the most developed oocytes in GC III and later individuals (see Results), thus batch fecundities were determined based on the most advanced mode of oocytes, a method which compares well with counts of hydrated oocytes only (Hunter et aI., 1985). Batch fecundities were counted in up to three females (five each for B. suborbitale and N. valdiviae) from each size group that included GC III or later stages by counting all oocytes of the most advanced oocyte mode in both ovaries. The counts obtained were averaged to provide mean batch fecundities for each size group. Seasonality of spawning was determined for each species using the combined frequency of all females of a species from each collection period having ovaries with migratory nucleus (GC IV) or hydrated oocytes (GC V); a significant level of spawning was arbitrarily defined as 10% or more of the females exhibiting these advanced GCs. Based on a decade of records of sea surface temperatures from the area of 27°N, 86°W, seasons were defined as: Winter-January, February, March; Spring-April, May, June; Summer-July, August, September; and Fall-October, November, December. Pooled data for GC V females were used to estimate diel spawning periodicity in B. suborbitale, L. alatus, L. guentheri and N. valdiviae by subdividing nighttime collections into six 2-h intervals between 1800 and 0600. Daytime trawls were separated into only two periods (0601-1200, 1201-1800) because the durations of the tows were longer. Spawning frequencies for the four species listed above were calculated using pooled data for migratory nucleus and hydrated stage ovaries (GCs IV and V) for each mm SL and each size group over the entire sexually mature size range. The number of eggs produced per spawn was calculated from length- fecundity regressions. The fraction offish spawning each day for a given size group was multiplied by the predicted batch fecundity of the size group to give the number of eggs spawned per day per size group. This equation was expressed as a function of the age of the fish by substituting validated growth equations for Benthosema suborbitale and Lepidophanes guentheri (from Gartner, 1991b). The eggs per day on age equation was then manually integrated from the average age at sexual maturity to the average age of death to quantify lifetime fecundities for these two species. Chemical composition of sexually mature females of L. guentheri (lipid, carbohydrate, protein, water and caloric content) was obtained from individuals collected during the summer of 1989 at 27°N, 86°W. Thiny-one sexually mature (>43 mm SL) individuals were captured. At sea, each specimen was measured to the nearest mm SL, blotted to remove excess moisture, and individually frozen. Back on shore, the wet weight of each specimen was determined to the nearest 0.1 mg. The abdominal cavity was opened and sex was determined. A total of 13 females with ovaries ofGC III or later were used for analyses. Both ovaries were removed and weighed to the nearest 0.1 mg. Five females were used for compositional assays of the body, while the gonads were pooled into two groups and analyzed separately; one of GC IV and IVIV (four ovaries), the other of GC III (nine ovaries). The methods of Donnelly et al. (1990) were used for all chemical composition analyses.

RESULTS General Data. -A total of 17,288 specimens of the seven dominant species were examined from nighttime collections from the eight cruises. An additional 1,0 II specimens of Benthosema suborbitale, Lampanyctus alatus, Lepidophanes guentheri, and Notolychnus valdiviae were examined from daytime samples. Collection totals for individual species are listed in Table 3. ..- Figure I. Standard developmental stages of myctophid ovaries. All photos are from Lepidophanes guentheri. a) GCs I and II. Magnification-200x. b) GC III early. Magnification-IOOx. c) GC III late. Magnification-IOOx. d) GC IV. Magnification-lOOx. e) GC V. Magnification-IOOx. f) GC Vi-Il/Ill (spent recovering). Magnification-IOO x. g) GC Vi-Il/III. Closeup of If showing ruptured lamellae and large interlamellar spaces. Magnification-200 x. h) GC VI-II/III. Increased magnification showing recovering GC II's. Magnification - 400 x . 726 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Table 2. Gonad class (GC) criteria for female myctophids, based on macroscopic (preservcd material examined under a dissecting microscope) and histological (based on HHE preparations) characteristics

Characteristics GC Macroscopic Histological Developing Ovaries very thin, ribbonlike, trans- Oocytes small, <0.05 mm diameter, lucent, generally located anteriorly polygona] in shape, basophilic, nu- (above stomach), small, clear 00- cleus large (> 50% of oocyte diam- cytes visible only under highcr eter), single nuclcolus present (Fig. magnification, generally few in la). number. Maturing II Ovaries pale straw color, still ribbon- Largest oocytes are 0.]0-0.25 mm, like but extending posteriorly, polygonal, basophilic, one (early) oocytes larger, numerous, clearly to many (late) nucleoli present visible at low magnification. (Fig. la). Nucleus very large (75% of oocyte diameter). Ripening III Ovaries golden in color, enlarged, Vitellogenic phase, largest oocytes circular in cross section, reach pos- are 0.25-0.35 mm, more rounded terior end of peritoneum, oocytes in appearance, eosinophilic, nu- visible to nakcd eye, solid in early merous yolk granules present, nu- stage, posscss large clear centcr in cleus with many peripheral nucleo- late stage. li present in early stagc (Fig. Ib), nucleoli absent with nucleus ap- pearing empty of material (Fig. Ic). Cortical alveoli present in both stages. Nucleus decreasing in diameter «50% oocyte diameter). Ripe IV Ovaries golden-orange, expanded to Largest oocytes are 0.35-0.45 mm fill most of peritoneal cavity, and very irregular in outline, most oocytes easily seen, possess clear of oocyte filled with large yolk center with lipid droplet present. plate]ets. Nucleus small « 30% oocyte diameter). Chorion is close to periphery of oocyte (Fig. Id). V Ovaries milky white with single gold Same as for GC IV, except largest lipid droplet, filling entire postcrior oocytes >0.45 mm (maximum of peritoneum, body walls usually found about 0.55 mm, chorion ex- clearly expanded, oocytes vcry panded away from yolky material fragile, tunica and chorion easily in oocyte (Fig. Ie). tom. Spent VI Ovaries shrunken, elongate but flac- Two conditions found: I) Spent Re- cid, usually opaque yellow-white in covering - Ruptured follicles pres- color. In some, oocytes like GC III ent, many GC III and some GC II can be seen. oocytes present (Fig. If-h). 2) Spent Defunct-A few scattered oocytes of various GCs present, but ovary is virtually empty, no follicles or oogonia remaining. GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 727

Table 3. Total number of individuals by collection period for dominant species of myctophids collected from the eastern Gulf of Mexico

Collection period

Scpo Mar. Jul. Nov. Jan. May Jan. Mar. Species 1984 1985 1985 1985 1986 1986 1987 1987 Total

Benthosema suborbita/e 86 212 607 170 132 455 89 77 1,828 Ceraloscope/us species 101 44 662 212 52 194 24 25 1,314 Diaphus dumeri/ii 180 93 693 829 165 1,394 319 579 4,251 Lampanycilis a/alus 74 231 946 281 ]93 406 40 45 2,216 Lepidophanes guenlheri 117 367 797 392 170 321 193 625 2,982 Myclophum affine 11 26 49 62 8 187 30 57 430 NOlo/ychnlls va/diviae 1]9 505 1,199 492 585 47] 724 172 4,267 17,288

Maturation of, and recrudescence in, myctophid testes appeared to be different from that described from other teleosts (Grier and Abraham, 1983; Grier et al., 1987; H. J. Grier, pers. comm.). Sexual maturity and development of males will be described in another paper. In all species, males appeared to mature at smaller sizes than females. With the exception of sex ratio data, the following results pertain only to females, unless otherwise indicated. Additionally, with the exception of diel spawning periodicity, all analyses are based on night collections only. Ovarian development in all the myctophid species examined was similar to the general teleostean pattern. Oocyte sizes were comparable at each GC among all species examined. Mean oocyte diameters ranged from <0.05 mm in the earliest developing oocytes to slightly >0.50 mm at hydration (GC I to GC V; Fig. la-h). Species Data. - Details of reprod ucti ve patterns are given below for each species, in order of increasing numerical abundance. The numbers in parentheses after the total sample size (N) represent females, males and immature individuals, respectively. "Immature" individuals have pre-GC I gonads, i.e., are juveniles of indeterminate sex. The post-metamorphic size ranges examined are also listed. 1. Myctophum affine: N = 430 (78/80/272), 12-67 mm SL. The relatively small numbers sampled reflected a lack of sampling effort at the depth of maximum nighttime density (0-5 m, Gartner et al., 1987) rather than low population density, so no catch rates versus collection period have been calculated. However, sufficient data were obtained to provide some preliminary information on reproduction in the eastern Gulf population. Gender could be determined in individuals as small as 24 mm SL (Fig. 2a). Sexual maturity in females was apparently reached by about 42 mm; almost all females >42 mm SL had ovaries ofGCs III or IV. Because of the low numbers collected, no sex ratios were calculated. Oocyte size-frequency distributions showed that both GCs III and IV were bimodal, with diameters of 0.15 mm and 0.25 mm in GC III and 0.15 mm and 0.35 mm in GC IV (Fig. 4a), and the frequencies of oocytes in the two maxima were nearly equivalent. Mean batch fecundities showed an exponential increase in length; in the 41-45 mm SL size group there was a mean of 536 oocytes in the ovaries, which increased to a mean of 3,037 oocytes in the 56-60 mm SL group (Fig. Sa). Females with vitellogenic oocytes were found during all collection periods (except September, when only one small female was captured), but only a few individuals with migratory nucleus stage ovaries were found, in May and November 728 BULLETIN OF MARINE SCIENCE, VOL. 52, NO, 2, 1993

Myctophum affine Cerotoscopetus sp. N = 430 N = 1,.314

70 _Female 80 b a n "" "78 ----l_Femc'en c 386 60 gaMote ~Mo!e n = 80 60 ~n "" 420 50 o Immature 'mmolurc ~ n "" 272 Dn =0 50B " 40 'ii ;;; 40 "0 30 ci z 20 20

0 20 30 40 50 60 70 10 70 Length (mm SL)

Benthosemo suborbilcle lamponyctus olotu$ N = 1,828 N = 2,207

200 _Female 140 _Female C n = 467 d n = 8J9 120 Mole 160 MOle n = 712 m n = 736 m 100 Dlmmoture o Immature ~ n "" 649 n = 641 " 120 80 ~ 60 "0 80 ci z 40 40 20

0 8 10 12 14 16 18 20 22 24 26 Length (mm SL)

Figure 2, Sex vs, standard length, all specimens examined. a) Myctophum affine. b) Ceratoscopelus species. c) Benthosema suborbitale. d) Lampanyctus a/atus.

lepidophones guentheri Oiophus dumerilii N = 2,982 N ::::> 4.251 _ _Female 500 b FemOle n = 1.040 n = 731 gMote 400 mMole n"" 1,027 " ~n "" 697 Otmmature ,mmoture ~ n"" 915 " 300 Dn = 2,821 ] "0 200 ci z

20 30 40 50 60 70 60 70 length (mm' Sl)

Notolychnus voldivioe N = 4,267 _ 700 femOle C n "" 1,687 600 mMole Bm'n = 1,934- i500 Immature n 646 's;: 400 O = ~ "0 300

~ 200

10 12 14 16 18 20 22 24 26 28 30 32 34 length (mm Sl)

Figure 3, Same as Figure 2. a) Lepidophanes guentheri. b) Diaphus dumerilii. c) Notolychnus valdiviae. GARTNER: REPRODUCfIVE PATTERNS OF LANTERNF1SHES 729

Myctaphum affine Cerotascopelus sp.

GC III GC III

"G o ..__ ~..J.- ..l.-__._---->------L __. - ..-'-.- GC IV l~~~~~- GC IV

0.55 >- 0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 u C Q) :> CT Q. , 5 0.20 0.30 0.J5 0.40 0.45 0.50 0.55 Q) l~. C::

Benlhosema sub.orbilole Lampanyclus alatus

GC HI CC III "~/~J ...... I 10 10 GC IV

-..:::-.- 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55

Lepidophanes guentheri

Notolychnus valdivioe

GC III

GC III >- u C Q) OJ g 20 a - _.....L ---L----L._ --.1- J.... __ ~ __ ,L LL 10 GC IV GC IV

GC V

':~L~0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 1~-~"0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 Oocyte Diameter (mm)

Figure 4. Oocyte size frequencies for vitellogenic (GC III), migratory nucleus (GC IV) and hydrated (GC V) stages (oocytes < .15 mm excluded). a) Myctophum affine. b) Ceratoscopelus species. c) Ben- thosema suborbitale. d) Lampanyctus alatus. e) Lepidophanes guentheri. f) Notolychnus valdiviae. 730 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

14,000 Ceratascapelus Sp. a a --~-er--- 12,000 M. affine

10,000 --

8,000

6,000

4,000

2,000

o 40 45 50 '55 60 65 70 75 500 r------~ N. valdiviae b ---. 300 o , . u o /'J' o o 13"/ g 0 200 o 6 z / ..9-/ / 100 o

o , 16 18 20 22 24 26 28 30 32 34

2,500 ,------, L. alatus c L. --guentheri 2,000 ----A----

1,500

1,000

500

0 30 35 40 45 50 55 60 65 Size Groups (mmSL)

Figure S. Batch fecundities vs. size groups. a) Myctophum affine and Ceratoscopelus species. b) Benthosema suborbitale and Notolychnus valdiviae. c) Lampanyctus alatus and Lepidophanes guentheri.

(Fig. 6a). Because of the small sample sizes, no conclusions can be made as to spawning period. GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 731

Myctophum affine b Ceratoscopelus sp.

23 .18 ~ __ 1_ 14 28 17 ~_ 15 18 158 34 104 '00 ~ 100 -CC V

[!ljJlCC IV 80 80 l

60 60

40 40

20 20

b J Jol"l pl~JOt'. ~1 \io~''6<:'\J.0(' B1~01 e,.b ,)\)0\' "O?se'Y' e,.••.•I;-\O". B~ ,)0(\ 'B ~o(\ e,.1\IIaf. ,&? \JIOf 'B1w.O':l eo ,)\J.\' "O?se'Y "0"\;'\0'" e'::J Benthosemo suborbitole Lomponyc tus olotus

23 35 57 32 10 95 17 85 420 34 122 100 ------140 255~ ~-~~~i'00 77 --l-CCV [!ljJlCC IV g 60 180 ~ 60 60 c Q) :J 0- 40 40 ~ I "- 20 20

o ~ ~ ~ ~ ~ ~ ~ .\0(\- -.)0(\' \-lI0f. ~o,f 'tl-0'.l ~u\· seQ- \,\0>J· • Lepidophanes guentheri Notolychnus voldivioe 49 258 216 304 222 80 179 478 45 168 -- ~-----~. - - ~-- '=[" " ". '" i_ccv ; [!ljJlcc IV I "'l': I I 60

1 :: f 40

1 20 l I 20 olmm.- 1 .10(\ eo .\0(\' '0 \J.O{.?J~w.o.!' 'B1~Oi '0& .\v" 'Be:.se'? '0\,\0'" 'O'='

Collection Period Figure 6. Frequency offemales with migratory nucleus (GC IV) and hydrated (GC V) oocytes among collection periods, by species. Numbers above each collection period indicate total number offemales collected during that period. a) Myctophum affine. b) Ceratoscopelus species. c) Benthosema suborbitale. d) Lampanyctus alatus. e) Lepidophanes guentheri. f) Notolychnus valdiviae.

2. Ceratoscopelus sp.: N = 1,314 (386/420/508), 12-70 mm SL. In the eastern Gulf, this species was originally identified as C. warmingii (Gartner et a1., 1987). Recently, this name was reported to be a junior synonym of C. townsendi by Badcock and Araujo (1988), with specimens from the Gulf of Mexico being defined as the "AI subtropical form" of C. townsendi. Accordingly, C. townsendi was used by Gartner et a1. (1989). However, data compiled from Ceratoscopelus collected worldwide (T. B. Linkowski, pers. comm.), and unpublished meristic data on post-metamorphic Ceratoscopelus from the Gulf, as well as other information on larval morphology (W. J. Conley and J. V. Gartner, unpub1.) all suggest that the Gulf species may be a new species most closely resembling the townsendi-warmingii complex. Until the confusion in the taxonomy of this genus is resolved, the species will be referred to as Ceratoscopelus species. This species was most abundant in the samples during the early summer (July), 732 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Ceratoscopelus sp. Benthosemo suborbitole

12 12 a b Dlmmolure '" .5 10 10 ~Mole a a _Female <:5 8 8 ~ ~0. g ~ 4 l ~ ci 2 z o ~~~~~~~~~~~~~~~~ Collection Period Col leetion Period

Lampanyctus olotus Lepidophones guentheri

16 12 c d o Immature '"E a 10 iIllll Mole g 12 IIFemale <:5 8

o ~~~~~~~~~~~~~~~~ ;o~~~ ~0~·,/>1».0<~'o >1-°< .,/>1».oi '/>~ ~,,\.'/>'oseV ~~ ","0".,/>'o Collection Period Collection Period

Diaphus dumerilii Notolychnus \/oldivioe

36 20 e Dlmmoture '" 30 ~Mole .5 16 8 IIFemale ~ 24 ~ 12 ~ 18 -0 ~ 8 'S: 12 "'5 £ ci z o ~~~~~~~~~~~~~~~~ ~~~~~~~~~~~~~~~~ Collection Period Collection Period

Figure 7. Total number ofindividuals collected during each sampling period, by sex. a) Ceratoscopelus species. b) Benthoserna suborbitale. c) Larnpanyctus ala/us. d) Lepidophanes guentheri. e) Diaphus durnerilii. f) Notolychnus valdiviae. but ripe females were generally taken only in winter collections, although sample sizes were quite low (Table 4, Fig. 7a). Gonad maturation (GC I) was observed in individuals as small as 23 mm SL but was not prevalent in individuals smaller than 28 mm SL (Fig. 2b). The oocyte size-frequency distributions were unimodal at 0.25 mm for GC III (Fig. 4b), but in GC IV females, there was what is best described as a weakly bimodal size-frequency, with a strong mode at 0.35 mm and a very weak secondary mode at 0.15 mm. Only a single GC V female was recorded. There was an exponential increase in mean batch fecundities with increasing body length (Fig. 5a). Total fecundities ranged from 3,287 for both ovaries in the smallest individual GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 733

Table 4. Catch rates (numberofindividua]s per ]0' m3 water filtered) of dominant myctophid species by collection period (collections are arranged in calendar order rather than chronology; numbers in boldface represent peak abundances)

Season Winter Summer Spring Fall Collection period

Jan. Jan. Mar. Mar. May Jul. Scpo Nov. Species 1986 1987 1985 1987 1986 1985 1984 1985 Benthosema suborbita/e 3.48 2.54 5.14 2.36 13.34 21.80 8.38 4.84 Ceratoscope/lis species 1.37 0.68 1.07 0.77 5.69 23.78 9.84 6.03 Diaphus dumerilii 4.34 9.09 2.25 17.78 40.85 24.89 17.54 23.60 Lampanycllis a/allis 5.08 1.14 5.60 1.38 11.91 33.98 7.21 8.85 Lepidophanes gllentheri 4.48 5.50 8.90 19.20 9.41 28.63 1I.40 1I.16 Noto/ychnus \'a/diviae 15.40 20.63 12.24 5.28 13.81 43.07 11.60 14.00

(51-55 mm SL group) to 12,626 in a 70 mm SL female. These were the highest fecundities among the seven species examined. Seasonal spawning data were sparse, but indicated that spawning occurred during the winter for this species in the eastern Gulf. Transformed juveniles were most prevalent in spring and early summer collections (Fig. 7a) and over half of the females in both January and March collections were at GCIII (vitellogenic) or later stages, compared with < 10% during the other collection periods, and virtually all migratory nucleus stage and hydrated oocytes were in females collected during January and March. The overall sex ratio (1.09: 1 M:F) did not significantly differ from parity. How- ever, males were significantly more common in the 27-50 mm size range (mean 1.55:1 M:F, X2 = 31.04, P < 0.005), whereas females were more abundant at 51- 55 mm SL (mean 0.22: 1 M:F, x2 = 30.31, P < 0.005). Additionally, all the largest individuals (56-70 mm SL) were female (Fig. 2b). Females outnumbered males in fall and winter (mean = 0.80: 1 M:F, x2 = 3.84, P < 0.05), whereas males were significantly more abundant during spring and summer (mean = 1.33:1.00 M:F, X2 = 9.97, P < 0.005; Fig. 7a). There was a shift towards increasingly advanced GCs with increasing size. However, only 61 of the 386 females examined (15.9%) were sexually mature. Females attained sexual maturity at 55 mm SL (Fig. 8a). Data were insufficient to determine any diel spawning pattern. NOTE: As this paper was going to press, an age and growth study based on validated daily microincrements in the otoliths of Gulf of Mexico Ceratoscopelus hadjust been completed (Gartner, in prep.). Analysis of age and growth data plus recent examination of unpublished abundance data on larval Ceratoscopelus from our Gulf collections (W. J. Conley, unpubl.) has resulted in refinement of some conclusions about the reproductive strategy of Ceratoscopelus. See Addendum. 3. Benthosema suborbitale: N = 1,828 (467/712/649), 10-32 mm SL. Abun- dances were lowest for this species during the winter months and highest in spring and early summer (Table 4; Fig. 7b). Sexes could be differentiated (GC I) in individuals as small as 11 mm SL, but immature individuals predominated at lengths up to 15 mm SL (Fig. 2c). The oocyte size-frequency distributions showed maxima at diameters of <0.05 mm, 0.15 mm, 0.30 mm and 0.35 mm for GCs I, II, III and IV, respectively. Few individuals of GC V were recovered, and no oocytes were measured from these individuals. Oocyte frequencies were distinctly bimodal for GCs III and IV 734 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

C. species N = 386

.00

90 SSM = 55.28 mm ao CI = ~O.52 70 r2 = 0.961 'a 50

20 'a

o ~"""""~~.....J.~....L- ~~~~~~~~~~~~~~~~~~~~*~~~~~ b B. suborbilale L. alalus N = 649 N = 839

100

90 90 SSM = 22.45 mm - -1'00 SSM = 36.09 mm 80 CI = ±0.05 80 CI = :to.19 70 ra;: 0.999 70 r2;: 0.997

50 50

JO JO '0 20 J20 10 10 ~

a _...... I.- -L .....I-....I....-.1.-..l..-..L....- oL - ~ ~ • J 22 24 26 2a JO ••..1:;) ,'" ••.'" ,") ~ ~ ,Ie ,'\ •.•'?J ,OJ ~ ",'" "''\. '" ~ ~ ~ '" •••.'b ~ ~.of' ")' ")'\. Y .,'" IS 20 32 J4 ~6 3a 40 42 44 46 48 50 d L, guenlheri e N. valdiviae N = 1.040 N = 1.687 100[------._-- -~- '::r----- 90 SSM = 41.7 1 mm SSM = 17.45 mm aD Ct.;: ±O.51 80 CI = :to.05 70 r2 = 0.987 70 f r' = 0.999 '0 ,ot 50 r .0 t JO 20f 10 J 1:l__ ~ o L~ ~~~~~~~~~~~~~~~~~~~~~~~ 10 11 \2 13 14 15 16 17 18 19 20 21 22 23

Length (mmSL)

Figure 8. Maturity ogives for dominant myctophid species. Curves are fit by hand. SSM-Size at sexual maturity. a) Ceratoscopelus species. b) Benthosema suborbitale. c) Lampanyctus ala/US. d) Lepidophanes guentheri. e) Diaphus dumerilii. f) Notolychnus valdiviae.

(Fig. 4c). Mean batch fecundities showed a linear increase with increasing body size (Fig. 5b). Overall, mean fecundities were low and ranged from 146 oocytes (both ovaries) in the 24-26 mm SL group to 296 in the 30-32 mm SL group. The percentage of females collected with migratory nucleus (GC IV) and hydrated (GC V) oocytes exceeded 10% (in most collections, >20%) of the total females collected for each collection period, indicating sustained year-round spawning in this species (Fig. 6c). The overall sex ratio difference (1.10: 1 M:F) was not significant. Females were more abundant than males between 11 and 17 mm SL (mean ratio of 0.58:1 M:F; x2 = 10.49, P < 0.005; Fig. 2c), whereas males dominated the larger size classes (24-32 mm SL, mean ratio of 1.25: 1 M:F, x2 = 9.24, P < 0.005). Seasonally, males tended to slightly outnumber females, except during September and No- vember (Fig. 7b). GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 735

Benthosemo suborbitole Lampanyc tus alatus '::1------47 22 19 26 68 81 ----I'r·~----·53 81 33 36 118 85 6' I:~::2

::r i ::l ~ 20 f

0601 1201 180t 2001 2201 0001 0201 0401

Lepidophanes guentheri d Notolychnus valdiviae

134 37 39 89 97 76 9 54 40 10 70 109 249 128 lOa, .. _ .. ~--~------'00 1 .GC V

80> 80 I!!I.IlGC IV

60 ~ 60

40 " 40

20> 20

OL ~ ..J a 0601 1201 1801 2001 2201 0001 0201 0401 0601 1201 1801 2001 2201 0001 0201 0401

TIme Period Start (hrs) Figure 9. Die1 spawning periodicity. Frequency of females with migratory nucleus (GC IV) and hydrated (GC V) oocytes vs. time (pooled data). a) Benthosema suborbita/e. b) Lampanyctus a/atus. c) Lepidophanes guentheri. d) Noto/ychnus va/diviae.

Both sexes matured at about 23 mm SL (Fig. 8b) and both attained a maximum length of 32 mm SL. At lengths> 25 mm SL, the proportions of GCs IV and V generally increased with increasing size (Fig. 8b), indicating an increasing frequency of spawning with increasing length. A comparison of ovarian stage vs. diel period showed that all GC V females were captured at night, with the highest percentage taken between 0000 and 0400 (Fig. 9a), indicating that spawning is most intense after midnight. Based on discrete depth collections, peak abundances of this species at this time were between 26 and 50 m. 4. Lampanyctus alatus: N = 2,207 (839/736/641),14-49 mm SL. Lampanyctus alatus was most abundant in spring and early summer collections (May and July, Table 4; Fig. 7c). Very few individuals at sizes less than 25 mm SL had GC I or later ovaries (Fig. 2d). Figure 4d shows that oocyte frequencies were bimodal in the ripening (III) and ripe (IV/V) GCs, with maxima at 0.25 mm and 0.45 mm diameter, respectively. Many ripe individuals had ovaries which appeared transitional between GC IV and V which may account for the larger diameter oocytes observed in GC IV/V than was noted among other species. Batch fecundities were low and showed a linear increase with increasing body length. They ranged from a mean of 416 oocytes (both ovaries) in the 31-35 mm SL size group to 921 in the 46-50 mm SL group (Fig. 5c). Comparisons of percent of females with migratory nucleus or hydrated oocytes by collection period indicated that spawning occurred at all times of the year (Fig. 6d). There was a significant overall difference in sex ratio, with males less abundant 736 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993 than females (mean 0.88:1 M:F, x2 = 6.74, P < 0.01). This was because females were dominant in the smallest (21-25 mm SL, mean 0.38:1 M:F, x2 = 27.17, P < 0.005) and largest (41-50 mm SL, mean 0.68: I M:F, X2 = 11.92, P < 0.005) size classes (Fig. 2d). When sex ratio was compared by collection periods, only July 1985 showed a significant departure from parity, when females were dominant (0.81:1 M:F, x2 = 8.00, P < 0.01; Fig. 7c). Females attained sexual maturity at 36 mm SL (Fig. 8c). At lengths larger than 36 mm SL, the percentage of GC IV and GC V ovaries generally increased with increasing length. Both sexes attained similar maximum lengths of 48 to 49 mm SL. Females with hydrated (GC V) oocytes were found only at night between 2000 and 0400 with peaks at 2201-0000 and 0200-0400 (Fig. 9b). Peak abundances during these hours were also between 26 and 50 m. 5. Lepidophanes guentheri: N = 2,982 (1,040/1,027/915),12-62 mm SL. This species was abundant during all seasons (although not all collection periods), with the highest numbers found in late winter and early summer (Table 4; Fig. 7d). Most individuals smaller than 26 mm SL were immature (Fig. 3a). Mean peak oocyte diameters were 0.25 mm, 0.35 mm and 0.40-0.45 mm for GCs III, IV and V, respectively. Oocyte size-frequencies were bimodal in all these later GCs, with the second mode of oocytes measuring 0.15 mm in all three GCs (Fig. 4e). Batch fecundities increased linearly with increasing body length and ranged from a mean of 653 oocytes (both ovaries) in 36-40 mm SL size group females to 2,294 in females 61-65 mm SL (Fig. 5c). The seasonal pattern of spawning in this species also indicated year-round spawning, although usually at reduced levels in winter (Fig. 6e). Overall male to female sex ratio was at parity (0.99: 1 M:F), although within size groups, females were dominant in the smaller size classes (21-30 mm SL, mean 0.58: 1 M:F, X2 = 16.60, P < 0.005), and males dominated the largest size groups (51-65 mm SL, mean 2.27:1 M:F; X2 = 17.78, P < 0.005; Fig. 3a). There were no significant differences in sex ratio for any collection period (Fig. 7d). Sexual maturity in females was reached at 43 mm SL (Fig. 8d), and males and females attained similar maximum lengths of about 62 mm SL. Diel spawning, based on the presence of hydrated oocytes, was restricted to the nighttime between 2000-0400 (Fig. 9c). At this time, the highest abundances of this species were between 26 and 75 m depth. 6. Diaphus dumerilii: N = 4,251 (731/697/2,823), 11-62 mm SL. Large catches were recorded among all seasons, but abundances were highly variable among winter collections (Table 4; Fig. 7e). Over 60% of all individuals collected were immature. Sexes could be determined in individuals as small as 24 mm SL, with maturing individuals most abundant at 27 mm SL and larger sizes (Fig. 3b). Only eight of the 731 females examined (1.1 %) contained vitellogenic (GC III) oocytes, thus the nighttime population of D. dumerilii in the eastern Gulf appeared to be composed of non-spawners. Sex ratios were near parity (0.95: I M:F), and there were no significant differences in sex ratio either by size group or collection period (Figs. 3b, 7e). Females seemed to mature sexually at about 52 mm SL, but as only 21 specimens exceeded this size, the determination of size at sexual maturity remains uncertain. Both sexes reached similar maximum lengths of about 60 mm SL. Oocyte size-frequencies showed that mean diameters during GCs I and II were similar to those of the other species examined. Neither oocyte frequencies nor batch fecundities were obtained from the few mature individuals. Seasonal spawning patterns could not be determined although GC III individuals were captured during both March cruises and in May, while the single GC GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 737

IV individual was also taken in May. Data for juvenile collections (Fig. 7e), along with age calculations (Gartner, 1991a, 1991b) suggest that spawning is seasonally restricted. It appears that there may be two main spawning periods, one in late winter-early spring, the other in the fall. 7. Notolychnus valdiviae: N = 4,267 (1,687/1,934/646), 9-22 mm SL. This diminutive species was very abundant during all collection periods except March 1987, with the highest density during the early summer (July 1985; Table 4; Fig. 7t), and the entire post-metamorphic size range was well represented. The smallest individuals collected were 9 mm SL and sex could first be ascertained at 11 mm SL. Most individuals < 12 mm SL were immature (Fig. 3c). Oocyte size-frequencies for GCs III, IV and V were bimodal and both peaks were similar in frequency. Mean oocyte diameters at the peaks were 0.15 mm and 0.35 mm for GC III, 0.20 mm and 0.40 mm for GC IV and 0.20 mm and 0.40-0.45 mm for GC V (Fig. 4t). Batch fecundities were extremely low, and there was a direct relationship between oocyte number and body size (18-20 mm SL, x = 62; 21-23 mm SL, x = 106; Fig. 5b). With the exception of January 1987, spawning activity was pronounced during all collection periods, indicating a year-round spawning pattern, with the most intense spawning effort in spring and early summer (Fig. 6t). The overall sex ratio showed that males were more abundant (1.15: 1 M:F, x2 = 16.84, P < 0.005). A significant departure from parity occurred in two size groups; females dominated the smallest group (9-11 mm SL, mean 0.55: 1 M:F, x2 = 6.04, P < 0.025), whereas males dominated in the intermediate 15 to 17 mm SL group (1.60:1 M:F, X2 = 74.31, P < 0.005; Fig. 3c). Females were significantly more abundant in November 1985 collections (mean = 0.74: 1 M:F, X2 = 7.34, P < 0.001), and males were more common in May 1986 and both January collection periods (Fig. 7t). Both sexes attained the same maximum size of 22 mm SL. Females reached sexual maturity at about 18 mm (Fig. 8e). In common with other species studied, once the length of sexual maturity had been attained, virtually all ovaries were GC III or later, and the proportions of migratory nucleus and hydrated stage ovaries increased with increasing length. Diel spawning activities occurred at night from 2000-0400 and peaked between 2200-0200 (Fig. 9d), during which times the highest abundances were collected between 51 and 75 m.

DISCUSSION Sampling Considerations. -All of the dominant myctophid species except Cer- atoscopelus sp. and Diaphus dumerilii appeared to spawn year-round in the eastern Gulf, but the sampling frequency limited the precise definition of when peak spawning occurred. Validated age structures of the populations of some of these myctophid species in the eastern Gulf show life spans averaging one year or less for Benthosema suborbitale and Lepidophanes guentheri, and approximately 2 years for Diaphus dumerilii (Gartner, 1991b). Preliminary age and growth data for other dominant species suggest that Lampanyctus alatus and Notolychnus valdiviae have life spans similar to B. suborbitale and L. guentheri (see Adden- dum). Thus, while the collections of September 1984, March, July and November 1985 and January and May 1986 could possibly have spanned a single generation of these species, the variations noted in January and March 1987 probably represent a different generation of myctophids. 738 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Catch rates between the two January and March periods were similar (Tab]e 4, Fig. 7a-f), but showed inter-annual variability in some species (e.g., L. guentheri). Sampling design and procedure utilization were nearly identical on all cruises, so these are unlikely sources of this inter-annual variability. This variability could be a reflection of environmental differences, for example, the Loop Current in- truded into the sampling area in the early part of the March] 985 cruise, but not in March 1987. Another possibility is that differences in life history patterns cause inter-annual variability. Because few individuals of any species would live to precisely I year or 2 years of age and since year-round spawning does occur in many species, it is likely that month to month comparisons of the numbers of individuals collected between or among years would show variability because of changes in stock sizes at different times. Patchiness of myctophid aggregations could also strongly affect variability. At present, there is little quantitative information on the effects of patchiness with respect to catch variability of micro nekton. Sex Ratios, Sizes at Sexual Maturity, Maximum Length. - Sex ratios of all species examined exhibited an overall male: female ratio that did not significantly differ from ]: I, which is in agreement with reports on a number of other tropica1- subtropical myctophids (Clarke, ]983; Karnella, 1987; Lisovenko and Prut'ko, ]987a). However, size-related differences in sex ratio were observed. Significant deviations from parity usually occurred among the smallest and largest sizes, with females generally predominating in both; exceptions were Ceratoscopelus sp., in which males dominated the smallest size groups, and Lepidophanes guentheri, in which the larger sizes were disproportionately male. The preponderance offemales in the smallest size classes for most species may have been an artifact resulting from greater difficulties in sexing the smallest males. Ceratoscopelus sp. was unique among eastern Gulf species in that all of the largest individuals (55-70 mm SL, N = 64) were female. Hulley (1981) observed the same trend in a population of C. warmingii collected from the western South Atlantic. Karnella (1987) examined C. warmingii collected off Bermuda and found that all the largest individuals of this population were females. Populations in which females grow considerably larger than males have been identified as characteristic of the Ai (subtropical) form defined by Badcock and Araujo (1988; T. B. Linkowski, pers. comm.). In contrast, populations of C. warmingii from the Central Atlantic examined by Hulley (198]), and from Hawaii (Clarke, 1983) exhibited parity in overall sex ratios and similar maximum lengths. In addition to the taxonomic implications, these two different patterns of sex ratio/maximum length indicate that a difference in spawning patterns may be quite possible as well. A comparison of the data from the present study with that of the reproductive patterns of Hawaiian C. warmingii shows that this is the case (see next section of Discussion). Clarke (1983) demonstrated what he believed were significant deviations from parity unrelated to size dimorphism in several myctophid species from the central Pacific Ocean and proposed several hypotheses to account for a sex ratio that significantly differs from 1:1. However, the data from the present study suggest that differing sex ratio among many myctophid species probably has little eco- logical significance. This conclusion is supported by the data ofDalpadado (1988). Of66 stations sampled in the Arabian Sea and western Indian Ocean, she reported that sex ratios of Benthosema pterotum were 1:1 at 48 stations, male dominated at 4 stations and female dominated at 12 stations. Her analysis of seasonal collections of sexually mature individuals of this species collected in the Arabian Sea showed that males dominated during two seasonal collections (mean ratio GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 739

1.9: 1 M:F) and females during the other two (mean 0.6: 1 M:F). Such data indicate that sex ratios among most species are highly variable. It is uncertain whether variations in sex ratio are responses to single factors or a complex of causes, although Conover and Kynard (1981) have shown that it is possible for temper- ature to affect the sex ratio of developing fish embryos. Sampling design, procedure, and behavior could conceivably affect sex ratios as well, via unequal sampling effort at depths dominated by one sex or the other, or through sex related capabilities in net avoidance. In this study, however, most of these factors were eliminated as sources of bias because nighttime sampling was uniform between nights and among cruises and also sampled virtually the entire nighttime depth ranges of sexually mature individuals of all species examined (Gartner et ai., 1987). In the eastern Gulf, sizes at sexual maturity for all the dominant species except Ceratoscopelus sp. and Diaphus dumerilii were much smaller than have been reported for the same species in the western North Atlantic (Gartner et ai., 1987; Fig. 8a~). Notolychnus valdiviae and Benthosema suborbitale were about 8% smaller upon attaining sexual maturity, while Lampanyctus alatus, Lepidophanes guentheri and Myctophum affine were between 16 and 18% smaller. Maximum sizes for all species were also between 11-28% smaller than reported for the same species in the western Atlantic; however, for Ceratoscopelus sp. the question about taxonomic status renders the comparison uncertain. This pattern of Gulf of Mexico populations being smaller than Atlantic populations has been reported earlier for other myctophid species and other taxa (Gartner et ai., 1987; Lancraft et ai., 1988), but no adequate explanation for this phenomenon has yet been offered.

Seasonal and Diel Spawning Patterns. - The seasonal patterns of spawning in the supposedly circumglobal tropical-subtropical species Benthosema suborbitale, Ceratoscopelus species (warmingii) and Notolychnus valdiviae can all be compared with reports from other regions. In N. valdiviae, the Hawaiian population studied by Clarke (1973) and the Bermudan population examined by Karnella (1987) exhibited spring-summer increases in spawning effort similar to that found in the present study. However, in the eastern Gulf a significant percentage of females (those with migratory nucleus and hydrated oocyte stages> 10% of population) appeared to be spawning year-round (Fig. 60, whereas spawning was more seasonally confined off Bermuda to the spring (Karnella, 1987) and off Hawaii to spring-summer (Clarke, 1973). The spawning season of Benthosema suborbitale is also different in the eastern Gulf than elsewhere. Karnella (1987) suggested year-round spawning of this species off Bermuda with a peak effort in the spring, whereas Clarke (1973) noted spawning activity of Hawaiian B. suborbitale was mainly confined to spring and summer. In contrast, spawning effort of this species in the eastern Gulfwas relatively even throughout the year with no appreciable peaks. Based on the frequency offemales with migratory nucleus (GC IV) and hydrated oocyte (GC V) stages, Ceratoscopelus sp. in the eastern Gulf clearly shows a single spawning period which occurs in the winter (Fig. 6b), see Addendum. This pattern is in sharp contrast to the findings of Karnella (1987; spring through fall with late spring peak) and Clarke (1973; spring through summer with summer peak) for Ceratoscopelus warmingii, the species which the eastern Gulf population most closely resembles. This pattern, coupled with meristic characters mentioned earlier (see Results), suggests that there are trenchant differences between the eastern Gulf Ceratoscopelus population and contiguous populations in the Atlantic (A. 740 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

and A2 forms of Badcock and Araujo, 1988) and elsewhere, and that the taxonomic status of this group needs to be reevaluated. Based on observed differences in spawning patterns for B. suborbitale and N. valdiviae, a similar re-evaluation is merited for these species as well. All of the other species examined which spawn in the eastern Gulf showed spawning activity throughout the year (sum ofGCs IV and V> 10%).Lampanyctus alatus and Lepidophanes guentheri are very similar in morphology, abundance and nighttime vertical distributions (Gartner et a1., 1987), but the period of maximum spawning activity is somewhat disjunct for the two species: fall through winter for L. alatus vs. spring through fall for L. guentheri. Karnella (1987) listed both of these species from Bermuda collections (L. alatus was uncommon in that region, whereas L. guentheri was abundant), however, neither apparently spawns in Bermuda waters. Diaphus dumerilii was the only species studied which showed no evidence of spawning at any time, although large numbers of immature juveniles were captured (Fig. 7e), and metamorphosing larvae were present in the ichthyoplankton at the same time (W. J. Conley, unpubl.). Thus, spawning must have occurred nearby although very few mature females were collected at any time (Fig. 3b; Gartner et a1., 1987). The explanation for absence of mature specimens in our collections is that upon reaching reproductive size, D. dumerilii appears to shift to a benthopelagic or pseudoceanic lifestyle. Such a habitat shift has been suggested for other midwater species (Marshall and Merrett, 1977; Mauchline and Gordon, 1984) including myctophids (e.g., Gymnoscopelus nicholsi; Linkowski, 1985). Large individuals ofa number ofmyctophid species, D. dumerilii among them, have been observed near the bottom « 10 m from bottom) in slope waters (Nafpaktitis et a1., 1977; J. E. Craddock, pers. comm.; pers. obs.). All records of gravid females have been from directly over the continental slope or around island margins in the Caribbean (Nafpaktitis, 1968). Based on transects across the continental shelfin the upwelling region of the eastern Atlantic, Badcock (1981) suggested that D. dumerilii be considered a member of a specialized group of shelfbreak mesopelagic fish species, a proposal that has recently been supported by Hulley and Lutjeharms (1989) from collections made in the same region. Based on the frequency of females with hydrated oocytes over the diel cycle in the four species for which there were sufficient data, spawning in all four occurs at night, primarily around midnight. At this time, migration is complete and fishes are feeding heavily (Hopkins and Gartner, 1992). Transition to spawning readiness appears rapid; most oocytes in sexually mature individuals are at the vitellogenic (GC III) or earlier stages during the day. In those females found with migratory nucleus stage oocytes during the day, it was observed that these oocytes were better developed in ovaries from specimens captured during the afternoon (1201-1800) when compared to morning captured (0601-1200) individuals. Most ovaries examined in morning samples were early to middle GC III (and in a few cases, early GC IV), while those in the afternoon were late GC III and early to middle GC IV, with late GC IV and GC V at night only. Thus, both GCs IV and V develop within a 24-hour cycle. Hydrated oocytes (GC V) were only recovered from females collected at night, with the highest frequencies generally found after midnight (Fig. 9a--d). This diel spawning chronology contrasts sharply with published accounts on other myctophid species. Lisovenko and Prut'ko(1987b) reported that spawning of Diaphus suborbita/is in the equatorial Indian Ocean occurred in the early evening (1845-2005). Gjosaeter and Tilseth (1988), in an extensive study of GARTNER: REPRODUCTIVE PATTERNS OF LANTERN FISHES 741

Benthosema pterotum in the Gulf of Oman, showed that this species also spawned in the early part of the night around sunset. The differences between the findings of the present study and those of earlier workers are probably because of differences in vertical distributions and migration patterns among species. Benthosema pterotum dwells between 200 and 300 m during the day, with most spawning occurring between 200 and 250 m (Gjosaeter and Tilseth, 1988). Diaphus suborbitalis is found deeper during the day, between 400 m and 600 m, but delays spawning until it reaches depths of 60 to 120 m (Lisovenko and Prut'ko, 1987b). The four species examined in the present study are also found deeper than 400 m during the day; between 400 m and 600 m for Benthosema suborbitale and Notolychnus valdiviae; 400 m to 900 m for Lam- panyctus alatus and Lepidophanes guentheri (Gartner et a1., 1987). A mid-night spawning would place all four species at depths of 50 to 125 m (similar to depths occupied by D. suborbitalis; Gartner et a1., 1987). The reason the eastern Gulf species spawn later at night than D. suborbitalis is that they apparently arrive at their nighttime depths later: the greatest number of females collected at night for all four species was between 2200 and 0400. Based on estimates of oocyte buoyancy and speed of ascent as well as development times, spawning at the shallow nighttime depths is necessary for eastern Gulfspecies. Gjosaeter and Tilseth (1988) determined that the eggsof Benthosema pterotum ascended about 50 m in 12 h and that temperatures of 200 and 25°C caused hatching to occur in 16 and 10 h, respectively. As mentioned, B. pterotum inhabits shallower daytime depths than any of the eastern Gulf species. Because of this, the release, ascent and development times allow the larvae of this species to hatch in the lower epipelagic zone (150-200 m) where predation pressure is lower than in the well-lit surface waters, but where there is ready access to food once the yolk sac is resorbed. If ascent rates and development times are assumed to be similar among eastern Gulfmyctophids, release of eggs from daytime depths would require an ascent period of 2.5 days for B. suborbitale and N. valdiviae and 5 days for L. alatus and L. guentheri in order to reach the lower epipelagic ZOne. While development times would be slowed (20°C isotherm is between 75 and 150 m in eastern Gulf), the potential for predation on eggs is greatly increased. A prolonged ascent could also mean that some larvae might prematurely hatch at depths inimical to survival. By carrying the eggs to nighttime depth ranges before spawning late at night, the eastern Gulf species place the eggsin optimum position for rapid development and access to larval food supplies when feeding begins.

Oocyte Sizes. Batch Fecundities and Relationship to Body Sizes. -Maximum oocyte size at hydration (GC V) is small for all species, ranging from 0.5 to 0.52 mm diameter. This is within the range reported for tropical-subtropical myctophids, though it appears that oocyte sizes are slightly smaller in eastern Gulf species than in conspecifics from other areas of their range (Clarke, 1984; Alek- seyeva and Alekseyev, 1984; Oven, 1986; Lisovenko and Prut'ko, 1987a; Dalpa- dado, 1988; Table 5). Smaller oocyte diameters may be an accommodation to smaller sizes at sexual maturity and maximum length in the Gulf populations (Gartner et aI., 1987). Batch fecundity estimates for all species studied also fall within reported ranges (Gjosaeter and Kawaguchi, 1980; Clarke, 1984; Hussain and Ali-Khan, 1987; Lisovenko and Prut'ko, 1987b; Dalpadado, 1988) and are similar to reports on the same species in other areas of their distribution (Table 6). Data on batch fecundity ranges for Lepidophanes guentheri represent the first records for this speCIes. 742 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Table 5. Diameters (mm) of hydrated oocytes (GC V) for eastern Gulfmyctophids, along with records for conspecifics from other studies

Bekker and Present study Borodulina (1968)0 Clarke (1984) Oven (1986)

Benthoserna suborbitale 0.52 0.60 Ceratoscopelus species 0.50 1.20-1.50 Diaphus durnerilii ND Larnpanyctus alatus 0.52 Lepidophanes guentheri 0.51 Myctophurn affine ND 0.80 Notolychnus valdiviae 0.52 0.60 o Cited in Gjosae!er and Kawaguchi (1980).

Most studies on fish fecundity, including those on myctophids, relate fecundity to some measure of body length (standard; fork; total) or weight (Bagenal and Braum, 1978; Hussain and Ali-Khan, 1987; Lisovenko and Prut'ko, 1987b). These measurements typically show a curvilinear relationship between fecundity and length and a direct relationship between fecundity and weight. In the present study, it is clear that batch fecundity increases with increasing length of the fish in all species (Fig. 5a-c), however, the type of increase varies among species, being curvilinear to exponential for Myctophum affine and Ceratoscopelus sp. and linear for the other species (excluding Diaphus dumerilii). The species with curvilinear length-fecundities have been characterized as "blunt head-thick bodied" whereas those exhibiting a linear length-fecundity relationship have been termed "pointed head-slender bodied" (Gartner et al., 1989). Other data sets relating fecundity to length for myctophids typically show a curvilinear relationship between body morphology and batch fecundity. Hussain and Ali-Khan (1987) showed curvilinear relationships between fecundity and body length in Benthosema pterotum and B. fibulatum. Both are similar in body shape to B. suborbitale but grow to much larger maximum lengths, 50 mm SL and 100 mm SL, respectively. The curvilinear pattern for B. pterotum was also shown by Dalpadado (1988). Lisovenko and Prut'ko (1987b) demonstrated exponential increases in fecundity with increasing body length in Diaphus suborbitalis. an Indo-Pacific species which is very similar in body morphology to D. dumerilii. Spawning vs. Size, Continuous Wave Oogenesis. -As mentioned above, eastern Gulf myctophid species attain sexual maturity at small sizes. This is not to say, however, that sexual maturation is a rapid process. Female Benthosema suborbitale and Lepidophanes guentheri are sexually mature at approximately 5 and 6 months of age, respectively, which is roughly 50% of their life span (Gartner, 1991b). In comparison to morphologically similar shallow water counterparts, Gartner (1991b) found that myctophids neither grow nor develop at appreciably different rates. A high percentage of females in spawning readiness (migratory nucleus and hydrated oocyte stages, GCs IV and V) were found among sexually mature sizes in most species (Fig. 8a-e). In sharp contrast to the reports of Clarke (1984) and Dalpadado (1988), there was a clear progression of developmental stage (GC) of the ovaries with increasing length. In Benthosema suborbitale and Notolychnus valdiviae, the percent GCs IV and V actually increased with increasing length (Fig. 8b, e), which suggested that spawning frequency increased with increasing size. With the exception of Diaphus dumerilii, in which few maturing oocytes were found, all myctophid species examined had oocyte size frequencies characteristic GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 743

~In OJ In OJ ..c i::: ...OJ o;l Co .5 "0 OJ ·sC o;l >< OJ In OJ oJ) eC OJ N ~ '"C o ·00 •..OJ ... r"l~ OJ ..c -N"''''' I I '0 00 - E o ""~

"0 e o;l Co E o u '"OJ ·u OJ Co "0'" :.a Co o U >. E i::: o;l .5 E ON o ON "0 -~ '-:; o E ~ '"o;l OJ... ..8 In ·3:a c :l u ~ '-o OJ oJ) C o;l 0:: 744 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Table 7a. Estimates of batch spawning frequency of sexually mature size groups for selected dominant species of myctophids

Size group Mean % of Mean no. days (mmSL) GCIV,V between spawns B. suborbitale 21-23 7.0 14.3 24-26 43.8 2.3 27-29 52.2 1.9 30-32 61.9 1.6 L. alaluS 36-40 23.7 4.2 41-45 40.0 2.5 46-50 52.0 1.9 L. guenlheri 36-40 10.3 9.8 41-45 14.1 7.1 46-50 18.6 5.4 51-55 28.6 3.5 56-60 26.1 3.8 61-65 25.0 4.0 N. valdiviae 17-19 32.1 3.1 20-22 68.6 1.4 of a "group-synchronous" type ovary (Wallace and Selman, 1981). In individuals with advanced oocytes (GC IV and later), two distinct and clearly separable modes were observed in all species (Fig. 4a-f). Multiple (usually bimodal) oocyte size- frequencies in myctophids have been reported by others (Clarke, 1984; Oven, 1986; Lisovenko and Prut'ko, 1987a; Young et al., 1987; Dalpadado, 1988). Coupled with length of spawning period and other data, these authors have in- terpreted multi-modal oocyte size-frequencies as evidence of repeated spawning within a spawning season. Data from the present study support this explanation. Russian authors (Oven, 1986; Lisovenko and Prut'ko, 1987a) use the term "continuous wave oogenesis" to describe the constant sequential production of oocyte batches in myctophids, which is an apt portrayal of oocyte reproduction processes in these long-term spawners. Very few individuals out of thousands examined were ever found in GC VI-II or VI-III (spent-recovering; numerous oocytes including GC III remaining in ovaries, Fig. If-h, Table 2) ann GC VI (spent-defunct; ovary virtually empty, very few oocytes remaining, Table 2) conditions. The spent-defunct individuals were almost invariably the largest individuals of a species, whereas the spent- recovering individuals were usually smaller (younger). Dalpadado (1988) proposed that the rarity of spent individuals of Benthosema pterotum indicated either death upon completion of a single spawn or rapid recovery of ovaries after spawning. Based on her observations and the present data set, I believe that the rare presence of GC VI-II and VI-III females, which are found in the smaller fishes, probably represents rapid recovery from spawning in younger individuals, whereas the presence of GC VI spent-defunct among larger fishes presumably represents ex- hausted fish that will soon die. The rapid recovery from spawning and rapid onset of death are such that it is very rare for females to be found in either spent condition. Because of the sequential nature of oocyte development and release and the lengthy period of spawning activity, it is difficult to determine precisely how often spawning takes place. So few spent-recovering individuals were found among all the specimens examined that calculation of batch spawning frequencies based on GARTNER: REPRODUCTIVE PATTERNS OF LANTERNFISHES 745

Table 7b. Life history data and equations used to produce and integrate lifetime fecundities for Benthosema suborbitale (Bs) and Lepidophanes guentheri (Lg). Growth equations, average ages at sexual maturity and death from Gartner (1991 b).

Age at sexual Average interspawn Size at sexual maturity maturity Average lifespan period Bs 23 mm SL 140 d 300 d 1.9 d Lg 43 mm SL 180 d 375 d 4.8 d Bs Lg Growth (length/day) L, = 32.83[1 - e-O.Ol(j('-,•.J)] L, = 72.83[1 - e-O.005(,-,.O)] N = 178, r2 = 0.94 N = 280, r2 = 0.96 Length - fecundity - 527.466 + 27.070 (length) -2,105.080 + 70.146 (length) (no. eggs/spawn) N = 15, r2 = 0.73 N = 16, r2 = 0.93 Length-spawning frequency -0.126 + 0.023 (length) -0.447 + 0.014 (length) (% fish spawning/day) N = 9, r2 = 0.56 N = 14, r2 = 0.67

the postovulatory follicle method of Hunter and Macewicz (1985) is not possible, although obviously ruptured follicles and some atretic bodies are seen. However, judging from the increasing percentage of advanced GCs at larger sizes, the larger the individual the more frequently it spawns. This is a pattern that has not been observed by other researchers examining myctophids (Clarke, 1984; Lisovenko and Prut'ko, 1987a, 1987b; Dalpadado, 1988). Thus, using the percentage of females within a size group possessing ovaries with either migratory nucleus or hydrated oocyte stage oocytes, a spawning frequency could be calculated for each size group for each species. Potential spawning frequencies, calculated for Benthosema suborbitale. Lam- panyctus alatus, Lepidophanes guentheri and Notolychnus valdiviae. show that the number of days between spawning varies inversely with length (Table 7a). Spawn- ing periodicities vary among species, but generally spawning takes place every 36 to 48 h in the largest size classes. Lepidophanes guentheri is an exception to the rule, with a minimum spawning period of about 4 days. Mean batch sizes in the largest L. guentheri are about twice that of L. alatus and 10 to 20 times more than produced by the two diminutive species. As might be suspected, the two smallest species, B. suborbitale and N. valdiviae, also show the shortest minimum periodicity between spawns at their largest sizes (Table 7a). The decrease in mean interspawn periodicity between size groups which still contain immature individuals and sexually mature size groups was very abrupt in all species except L. guentheri which had a number of precocious females in the smaller size group. This suggests a very rapid onset of sexual maturity and maturation of oocytes once sexual maturity is attained. This finding, coupled with the fact that larger fishes spawn more frequently, suggests that these myctophid species are capable of repeatedly spawning over a long period of time. A question that arises from the above calculations is: can the females of these fishes meet the energetic costs of sustained repetitive spawning with a relatively short (1 to 4 days) interspawning "rest" period? To determine whether such a pattern was possible, the chemical composition of Lepidophanes guentheri was analyzed and the caloric value of developed ovaries per unit body weight was calculated (Table 8). This species was selected because: it was abundant in collections made in the summer of 1989; females of GC III and later were easily obtainable, and; it had the highest fecundity (=energy expenditure) of the four 746 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Table 8. Chemical composition data and caloric content for Lepidophanes guentheri (all individuals are female)

Body Composition Wet weight Protein Lipid Carbohydrate AFDW Size (mm SL) GC (g) (%AFDW) (%AFDW) (%AFDW) % water %DW 48 IV/V 1.0693 65,02 8.35 0,575 75.4 82.4 50 IV 1.1236 64.49 9.69 0.499 72.6 84.4 54 IV 1.3566 61. 70 7.05 0.727 73.9 82.4 45 IV 0.8278 63,80 6,72 0,744 73,2 80.4 51 IV 1.1212 64.36 5,99 0,726 75.0 81.7 x= 1.0196 63.87 7.56 0.654 74.0 82.3

Ovary Composition Wet weight Protein Lipid Carbohydrate AFDW Group GC (g) (%AFDW) (%AFDW) (AFDW) % water %DW 1 (N = 4) IV-V 0,2991 51. I2 22.41 1.409 81.6 92.4 2 III 0.2989 48.64 17,38 1,202 69,8 91.5 x= 0.0460 49.88 19.90 1.306 75.7 92.0

Caloric Content Protein Lipid Carbohydrate Total Total calories (kcal'IOO g 'WW) in mean weight Body only 112.46 14,09 0,57 127,12 1,271.20 Ovaries only 100.45 37.84 0,90 139.19 63,94

species analyzed. The most advanced batch of oocytes present in the ovaries makes up a mean of27.3% of the ovaries. The mean caloric value for the ovaries was 63.94 cal, therefore, the caloric value per batch was approximately 17.5 cal. Based on the determination that the largest L. guentheri spawn once every four days, approximately 4.4 cal, day-I must be obtained to produce a batch of oocytes. Using data from Hopkins and Gartner (1992) for the caloric value of the ten fullest stomachs of L. guentheri, an assimilated ration of 14.8 cal'day-I was obtained. Thus, on an energetic basis, L. guentheri should be able to maintain the calculated spawning chronology, at a cost of about 30% of its daily caloric intake. A quantitative estimate of the lifetime oocyte production per individual was calculated for Benthosema suborbitale and Lepidophanes guentheri because validated growth data were available for these two species (Gartner, 1991a, 1991b). The data and equations integrated to produce the estimates are listed in Table 7b. Both species have an average life span of less than one year (Gartner, 1991b), therefore spawning season fecundity equals lifetime fecundity. Based on the in- tegrations, the average female Benthosema suborbitale will spawn about 84 times and release 19,600 eggs in her lifetime. In contrast, Lepidophanes guentheri will only spawn about half as many times (41) since the shortest interspawn period is about 4 days (vs. about 2 days in B. suborbitale). Owing to a higher individual fecundity and somewhat longer spawning period, L. guentheri will release far more eggs, with an average lifetime production of 102,500 eggs per female. These data, coupled with the continual, though variable, spawning practiced by these populations suggest that over their short lifespan ofless than 1 to 2 years, individual myctophids can produce a large number of eggs. This allows these comparatively small fishes with their correspondingly low individual batch fecundities to compete with midwater fish populations of species attaining much GARTNER:REPRODUCTIVEPATTERNSOFLANTERNFISHES 747 larger sizes and fecundities. For example, female Gonostoma elongatum in the eastern Gulf attain sizes of> 160 mm SL with the batch fecundity of an individual estimated at 22,000 eggs (Fisher, 1980). However, life history data suggest that this species spawns but a single time and then dies (Lancraft et al., 1989). Even abundant myctophid species which show evidence of spawning seasonality, such as Ceratoscopelus species, will, because of their repetitive spawning strategies, produce a number of eggs comparable to or higher than much larger midwater species, enabling them to maintain similar or higher abundances.

CONCLUSIONS There appear to be two main reproductive strategies among the dominant species of myctophids in the eastern Gulf of Mexico. Benthosema suborbitale and Lepidophanes guentheri both have a lifespan of I year or less (Gartner, 1991b), and preliminary data suggest the same is true for Lampanyctus alatus and No- tolychnus valdiviae. These four species all attain sexual maturity at small sizes and spawn repeatedly during all seasons for the remainder of their lives. In contrast, Ceratoscopelus sp. and Diaphus dumerilii spawn fewer times and are more seasonally restricted. This pattern is compensated for in the latter two species by having individual batch fecundities which are much higher, exhibiting a curvilinear rather than linear increase in oocyte number with increasing size, and by having lifespans which cover at least two spawning periods (Gartner, 1991b in D. dumerilii). In all species, these patterns allow for oocyte production which far exceeds individual batch fecundities and which also allow seasonal or lifetime fecundities to approach or exceed those of much larger bodied mesopelagic competitors. While it is highly likely that these representative patterns are typical of myctophid species residing in low-latitude ecosystems, it is important to note that pronounced differences have been observed between eastern Gulfmyctophid populations and their conspecifics from other parts of their geographic ranges. Some of these include: diel and seasonal spawning chronologies, sizes at sexual maturity and maximum length, increasing frequency ofIate ovarian classes with increasing body length, and in at least the case of Ceratoscopelus species, meristic variation. These discrepancies indicate that divergences are occurring between myctophid populations even as closely situated as the eastern Gulf of Mexico and western Atlantic Ocean. It may be that many of the generalities regarding tropical-subtropical open ocean communities, based on the premise that such areas show great inter-regional environmental stability, are of dubious value. Based on the findings of this study, greater emphasis needs to be placed on detailed studies of the ecology of mesopelagic communities on a regional, rather than global, basis.

ACKNOWLEDGMENTS

I would like to thank my colleague W. J. Conley, University of South Florida, Department of Marine Science (USFMS), for the use of some of his unpublished data on larval myctophids. I am grateful to R. Reese, R. Taylor and Dr. H. J. Grier of the Florida Marine Research Institute (FMRI) for assistance in interpretation of gonadal histology preparations. Special thanks go to M. Murphy (FMRI) for his assistance with statistical analyses. Dr. J. E. Craddock, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts and Dr. T. B. Linkowski, Sea Fisheries Institute, Gdynia, Poland kindly supplied me with unpublished information on Diaphus dumerilii and Ceratoscopelus species, respectively. I also wish to thank the crew of the R/V SUNCOASTERwithout whose professionalism these collections would not have been possible. I am indebted to my major professor, Dr. T. L. Hopkins, USFMS, and my doctoral examining committee: Drs. J. J. Torres, R. R. Wilson and K. L. Carder, USFMS; T. G. 748 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

Bailey, Harbor Branch Oceanographic Institution, Inc.; and B. H. Robison, Monterey Bay Aquarium Research Institute for their critical reviews of the manuscript. Finally, I want to thank Mr. J. B. Lake whose Fellowship in Marine Science program provided financial assistance which helped me complete this research. Shiptime was provided by a Nationa] Science Foundation Grant #8410787, T. L. Hopkins, principal investigator. This research was part of a doctoral dissertation completed at the USFMS.

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DATEACCEPTED: April I, 1992.

ADDRESS: Department of Marine Science, University of South Florida, 140 7th Ave. S. E., St. Pe- tersburg, Florida 33701; PRESENTADDRESS: Florida Marine Research Institute, /00 8th Avenue S,E., St. Petersburg, Florida 33701.

ADDENDUM Ceratoscopelus Species Reproductive Biology

While most of the conclusions regarding the overall reproductive pattern exhibited by eastern Gulf Ceratoscopelus species in the preceding text are substantially correct, a reinterpretation of how this pattern is manifested became necessary because of new life history information that became available while this paper was in press. To briefly reiterate, the Gulf of Mexico collection data for post-metamorphic Ceratoscopelus suggested short-term spawning during the winter. At the time these data were analyzed, it was thought that C. species had a 2-year life span similar to that of Diaphus dumeri/ii and so females probably had two spawning periods in their lifetime. Abundance data for larval Ceratoscopelus from the same collection periods used in the present study (W. 1. Conley, unpubl.) show a distinct peak in larval abundance during the winter (March 1985), supporting the reproductive data from the present study. However, a second larval abundance peak of similar proportion was also found during July 1985, when few sexually mature or ripe females were captured. The larval size ranges, coupled with validated age data, suggest a spawning peak that took place primarily during June 1985. Newly completed research which produced validated age and growth data for the post-metamorphic size range of this species (Gartner, in prep.) showed that Ceratoscopelus species have a life span ofIess than one year. Growth was seasonally variable; the average maximum life span at 70 mm SL ranged between 235 and 332 days (x = 288 days). Attainment of sexual maturity (55 mm SL) was between 175 to 222 days (x = 206 days), or between 68% and 75% of the life span, again supporting the conclusion that the sexual development rate among myctophid species is relatively slow. The larval abundance data coupled with the age and growth data indicate that in fact the Gulf of Mexico Ceratoscopelus population undergoes two relatively restricted spawning periods per year, one during the warmer months and one during cooler months; however, the two spawns are produced by two different generations. Spawning duration per individual is relatively short, less than 3 months, and estimates of spawning frequencies per sexually mature size class (as calculated for other species; Table 7a) showed a mean interspawn period of 7 days, which is not surprising considering the comparatively high fecundity of this species. This high fecundity, the highest of eastern Gulf dominant myctophids, also results in the highest overall lifetime output of eggs. Integration of life history equations for C. species using the same methods applied Benthosema suborbitale and Lepidophanes guentheri (Table 7b) indicates that an individual female will spawn about 12 timcs in her life, producing an average of 166,300 eggs. Based on these additional data, the Ceratoscopelus species population in the eastern Gulf of Mexico fits the described pattern of fewer spawns which are seasonally restricted, with probably two main spawning periods per year. While it appears that the two spawning periods are produced by different generations, the end result is still a reproductive output by C. species sufficient to maintain population abundances equivalent to or greater than larger bodied mesopelagic competitors.