Intraspecific variation of hatchling size in Late Cretaceous ammonoids from Hokkaido, Japan: implication for planktic duration at early ontogenetic stage AMANE TAJIKA AND RYOJI WANI
Tajika, A. & Wani, R. 2011: Intraspecific variation of hatchling size in Late Cretaceous ammonoids from Hokkaido, Japan: implication for planktic duration at early ontogenetic stage. Lethaia, Vol. 44, pp. 287–298. Intraspecific variations of the early shell dimensions (ammonitella and protoconch diameters) of two Late Cretaceous (earliest Campanian) ammonoid species (Gaudryceras tenuiliratum and Hypophylloceras subramosum) from the Haboro and Ikushumbetsu areas, Hokkaido, Japan, show no significant difference between these areas that are approximately 110 km apart. The geographic distributions of G. tenuiliratum and H. subramosum are supposed to be mainly controlled by the flotation and transportation during the embryonic stage within floating egg masses and ⁄ or post-embryonic stage because of their small hatchling sizes (1.18–1.46 mm in diameter for G. tenuiliratum, and 0.91–1.13 mm in diameter for H. subramosum), suggesting these two ammonite species at the embryonic and ⁄ or post-embryonic stages were transported at least 110 km. Postulating that the velocity of palaeocurrent around the Haboro and Ikushumbetsu areas during the Cretaceous Period was 0.25 m ⁄ s, similar to those in the modern ocean current flowing off the eastern Pacific coast of Hokkaido, the egg masses and ⁄ or hatchlings of G. tenuiliratum and H. subramosum were buoyant and transported more than 5 days. The preliminary comparison of hatchling size through time suggests that the hatching sizes of H. subramosum in Hokkaido increased slightly from the Middle Turonian until the earliest Campanian (during about 7 Myr). h ammonoid, hatchling, paleoecology, variation, Cretaceous. Amane Tajika [
[email protected]], Faculty of Education and Human Sciences, Yokohama National University, 79-2, Tokiwadai, Hodogaya-ku, Yokohama 240-8501, Japan; Ryoji Wani [
[email protected]], Interdisciplinary Research Center, Yokohama National University, 79-2, Tokiwadai, Hodogaya-ku, Yokohama 240-8501, Japan; manuscript received on 17 ⁄ 03 ⁄ 2010; manuscript accepted on 26 ⁄ 07 ⁄ 2010.
Reproductive strategy is one of the major factors controlling the geographic distribution, evolutionary and extinction rate, and speciation of marine animals. Most ammonoids have planispiral shells that preserve the record of growth including their hatchlings, so that many researchers have attempted to recognize their early life histories of the ancient extinct animal from fossil specimens (e.g. Schindewolf 1933; Kulicki 1974, 1979, 1996; Druschits et al. 1977a,b; Tanabe et al. 1979, 1980, 1993, 1994, 2001, 2003; Bandel 1982; Bandel et al. 1982; Landman 1982, 1985, 1987; Landman & Bandel 1985; Tanabe & Ohtsuka 1985; Ohtsuka 1986; Tanabe 1989; Landman et al. 1996; Klug 2001; Rouget & Neige 2001; Korn & Klug 2007; Klug et al. 2010). The embryonic shells of ammonoids can be recognized by the presence of the primary constrictions in the innermost whorl (Landman et al. 1996; Klofak et al. 2007; and references therein). The embryonic ammonite, which is termed the ammonitella (Druschits & Khiami 1970), consists of the protoconch (initial chamber) and about one planispiral
whorl from the caecum terminating at the primary constriction. Most workers have divided ammonite development into embryonic and post-embryonic stages. The transition point between the two stages is clearly distinguished by a sudden change in surface ornament, shell structure, and whorl expansion rate (Westermann 1996; Klug 2001; Mapes & Nu¨tzel 2009). Most ammonoid hatchlings had a planktic mode of life (e.g. Kulicki 1974, 1979, 1996; Druschits et al. 1977a; Tanabe et al. 1980, 2001, 2003; Landman 1985; Tanabe & Ohtsuka 1985; Landman et al. 1996; Westermann 1996; Rouget & Neige 2001) and changed their mode of life from planktic to nektoplanktic or nektobenthic at 2.0–2.5 mm in shell diameter (Shigeta 1993; see also Westermann 1993). Their geographic distribution was controlled by several factors, such as the duration of planktic stage, ecology, food preferences, and water depth (Landman et al. 1996; Westermann 1996). Although the duration of planktic stage is one of these important factors (Landman et al. 1996; Westermann 1996), there has been little
DOI 10.1111/j.1502-3931.2010.00242.x 2010 The Authors, Lethaia 2010 The Lethaia Foundation
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discussion of how long their egg masses, in which embryonic shells developed, and newly hatched youngs (neanoconch; Westermann 1996) were transported by water currents. The sizes of ammonoid embryonic shells have been also much investigated in previous studies, revealing that ammonoid hatchling sizes show intraspecific variation (e.g. Landman et al. 1996; Rouget & Neige 2001; Tanabe et al. 2003). Although regional and chronological correlations of the intraspecific variations of ammonoid hatching sizes is critical for the better understanding the reproductive strategies of ammonoids, an analysis of this feature has not yet been undertaken. In this paper, the intraspecific variations of the ammonitella and the protoconch diameters (AD and PD, respectively) of Late Cretaceous ammonoids (Gaudryceras tenuiliratum and Hypophylloceras subramosum) collected from the lowest Campanian in the Haboro and Ikushumbetsu areas, Hokkaido, Japan, were examined. Intraspecific variation was then regionally, not chronologically, compared with two ammonite species collected from the strata of similar age. Based on this comparison, the supposed duration of the planktic mode of life in ammonoid hatchlings is discussed. Furthermore, comparing previously reported data, the transition of the hatchling size through time is examined.
Material and methods A total of 60 specimens (35 specimens of G. tenuiliratum, Gaudryceratidae, Lytoceratina; and 25 specimens of H. subramosum, Phylloceratidae, Phylloceratina) from two areas (Haboro and Ikushumbetsu areas), Hokkaido, Japan, was analysed for the present study (Table 1; Figs 1, 2), because these species commonly occur in these areas. From the Haboro area, 18 specimens of G. tenuiliratum and 11 specimens of H. subramosum were used for analysis. From the Ikushumbetsu area, 17 specimens of G. tenuiliratum and 14 specimens of H. subramosum were used for analysis. All specimens are housed in the collections of Mikasa City Museum, Hokkaido. All the examined specimens were extracted from spherical or mushroom-shaped calcareous concretions and, therefore, show no sign of deformation during the diagenesis process. Epifauna has not been noted on any of the shells. The calcareous concretions from the Haboro area were collected in float from the surveyed routes (Fig. 1), so that their exact horizons cannot be defined. However, the textures of concretions (e.g. shape of concretions, grain size) and co-occurring fossils (ammonoids, e.g. Hauericeras angustum, and an
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inoceramid bivalve, Inoceramus (Platyceramus) japonicum) strongly suggest that the concretions were derived from adjacent localities in the surveyed routes and that the horizons of the concretions were comparable to the columnar sections of the surveyed routes (Fig. 3). The concretions collected from the Ikushumbetsu area, on the other hand, were embedded in siltstone with interbeds of thin sandstone layers. Each specimen was polished along the median plane by means of silicon carbide powders (Fig. 4). The AD and PD were measured under an optical microscope with digital measurement tool (the error 0.05). According to Shigeta (1993) and Mapes & Nu¨tzel (2009), newly hatched ammonoids had a planktic mode of life and change their mode of life to nektoplanktic or nektobenthic with growth on the basis of theoretical calculation for the Late Cretaceous ammonite species (see also Westermann 1993). A planktic mode of ammonites at the post-embryonic stage probably accompanied flotation on ⁄ near the sea surface and transportation by ocean currents (Landman et al. 1996; and references therein). Another controlling factor for the dispersal at the early ontogenetic stage is whether ammonoids laid eggs on the seafloor like modern Nautilus or they laid eggs in the water as floating egg masses like some modern coleoids (Mapes & Nu¨tzel 2009). Mapes & Nu¨tzel (2009) has demonstrated that some Early Carboniferous ammonoids were probably laid their egg masses in the water column above the bottom or by attachment to floating debris, based on faunal analysis of an oxygen-depleted marine succession. It is, however, unclear where the two species examined in this study laid their egg masses, so that the flotation during the embryonic stage within floating egg masses and post-embryonic
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stages cannot be discriminated in this study. No significant difference in the hatchling sizes between the Haboro and Ikushumbetsu areas in G. tenuiliratum and H. subramosum (Table 3) suggests that these two ammonite species at the embryonic stage within floating egg masses and ⁄ or post-embryonic stages were probably transported at least 110 km, a distance that corresponds to the current setting of the Haboro and Ikushumbetsu locations (Fig. 1). Many details of ammonoid palaeoecology (e.g. presence of seasonal migration, spawning cycle, place of spawning) are unknown, which thus affect the estimation of transported distance of newly hatched ammonoids. If the juveniles or adults of G. tenuiliratum and H. subramosum frequently migrated and swam over 110 km around Hokkaido in the Cretaceous Period, similar to mature modern Nautilus that can migrate more than 100 km in the water of Palau (Saunders & Spinosa 1979), the assumption of flotation and transportation of hatchlings is unnecessary to explain the identical hatchling size between the Haboro and Ikushumbetsu areas. Such migration would be one of the most important ways for modern Nautilus to expand their geographic distribution, because they laid large eggs attached to hard substrata and their hatchlings have the nektobenthic mode of life similar to adults (Arnold et al. 1987; Landman 1988). However, G. tenuiliratum and H. subramosum have small hatchling sizes (1.18–1.46 mm in diameter for G. tenuiliratum, and 0.91–1.13 mm in diameter for H. subramosum), which have been recognized as r-strategy (corresponding to a type III survivorship curve) among cephalopods (Ward 1987; Landman et al. 1996; Klug 2001), suggesting that G. tenuiliratum and H. subramosum generally expanded their distribution by water currents during the planktic stage rather than migration and swimming during the juveniles or adult stage (Landman et al. 1996; Westermann 1996). This study postulates, therefore, that the geographic distributions of G. tenuiliratum and H. subramosum were mainly controlled by the flotation and transportation of egg masses and/or hatchlings.
Implication for planktic duration of newly hatched ammonoids The lack of significant difference in the hatchling sizes between the Haboro and Ikushumbetsu areas in G. tenuiliratum and H. subramosum suggests that these two species at the embryonic stage within floating egg masses and ⁄ or post-embryonic stage were transported at least 110 km. If the velocity of palaeocurrent around the Haboro and Ikushumbetsu areas during the Cretaceous Period is given, the duration of flotation and transportation by water currents can be estimated.
Hatchling size in Late Creacteous ammonoids
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The palaeocurrent in the Late Cretaceous Hokkaido have been examined by Tanaka & Sumi (1981) and Takahashi & Ishii (1993). Tanaka & Sumi (1981) showed that palaeocurrent in the Late Cretaceous Hokkaido was dominated by a southward current based on the analysis of turbiditic sandstones. Takahashi & Ishii (1993) indicated that the palaeocurrent in the Late Cretaceous Hokkaido flowed southward from the Arctic as inferred from radiolarian fauna. There are, however, no data on the current velocity in the Late Cretaceous Hokkaido. Therefore, in this study, the palaeocurrent velocity in the Late Cretaceous Hokkaido is taken as being similar to the modern ocean current flowing off the eastern Pacific coast of Hokkaido, which is the Oyashio Current with the current velocity of less than 0.25 m ⁄ s (Kusaka et al. 2009). Therefore, the velocity of palaeocurrent around the Haboro and Ikushumbetsu areas during the Cretaceous Period is postulated as 0.25 m ⁄ s in this study. To float and be transported over 110 km by the water currents with the velocity of 0.25 m/s (= 0.9 km ⁄ h = 21.6 km ⁄ day), about 5 days are sufficient. This study compares the hatchling sizes of G. tenuiliratum and H. subramosum between only two areas about 110 km apart, so it would be important to test whether the hatchling size in a more distant area (e.g. Sakhalin, northeastern Pacific) is similar to that in Hokkaido. Therefore, the duration of hatchling flotation and transportation by water currents (i.e. about 5 days) is the minimum estimation. In further studies, the hatchling sizes of G. tenuiliratum and H. subramosum in more distant areas of the same age should be analysed and then compared to those in this study, in order to more completely understand the planktic duration of egg masses and/or newly hatched ammonoids. A similar relationship between the planktic duration of egg masses and/or newly hatched cephalopods, the distance between two areas that have the similar sizes of hatchlings, and the velocity of water currents can be observed in the extant cephalopod squid Illex (Ommastrephidae, Oegopsina). The average egg dimensions of the genus Illex varies depending on species (0.77–0.82 mm in Illex coindeti, 0.75–0.88 mm in Illex illecebrosus, and 0.96–1.04 mm in Illex argentinus; Laptikohovsky & Nigmatullin 1993). Floating eggs and hatchlings of I. argentinus are known to be transported by water currents for 2–3 months (Haimovici et al. 1998), but those of the other Illex species are unknown. Laptikohovsky & Nigmatullin (1993) examined the egg size of I. coindeti in the West African shelf. The egg size in 7–11 N and 20–26 N in the West African shelf is 0.73–0.80 mm (l = 0.77 mm) and 0.77–0.93 mm (l = 0.82 mm), respectively (Laptikohovsky & Nigmatullin 1993). There is no significant difference between the regions of 7–11 N and
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Table 4. Data of ammonitella diameters of Hypophylloceras subramosum from the earliest Campanian (this study) and the Middle Turonian (Tanabe et al. 2003). Sample
Area
Age
n
Min. (mm)
Max. (mm)
Mean (mm)
This study This study R4018 (Tanabe et al. 2003) R4020 (Tanabe et al. 2003)
Haboro Ikushumbetsu Tappu Tappu
Earliest Campanian Earliest Campanian Middle Turonian Middle Turonian
11 14 8 8
0.99 0.91 0.83 0.72
1.11 1.13 0.89 0.97
1.03 1.03 0.86 0.89
SD 0.033 0.073 0.026 0.081
n, number of specimens; and SD, standard deviations.
20–26 N in the West African shelf, a distance of about 1500 km (by the Student’s t test; P > 0.05). The water current flowing in the West African shelf is called the Canary Current, a southward current with the velocity of about 0.2 m ⁄ s (Lalli & Parsons 1997). The relationship between the planktic duration of egg masses and ⁄ or newly hatched cephalopods (2–3 months for I. argentinus), the distance between two areas that have similar hatchling sizes (about 1500 km), and the velocity of water currents (about 0.2 m ⁄ s (= 0.72 km ⁄ h = 17.3 km ⁄ day) for the Canary Current) is quite consistent with the two Cretaceous ammonoid species from Hokkaido in this study. This similarity indicates that the reproductive strategy of ammonoids was more similar to that of coleoids (Engeser 1990; Tanabe et al. 1993; Landman et al. 1996) than that of nautiloids, which has much larger hatchlings (9–35 mm in diameter for post-Cretaceous nautiloids; Landman et al. 1983; Landman 1988; Cichowolski 2003; Cichowolski et al. 2005; Wani & Ayyasami 2009).
Preliminary comparison of hatchling size through time The intraspecific variation of the embryonic shell diameters of two ammonoid species (G. tenuiliratum and H. subramosum) were regionally and not chronologically examined in this study. However, the comparison of the intraspecific variations of hatchling size through time within a single species, which were closely related to evolutionary and extinction rate and speciation, has not been adequately examined (see also Landman et al. 1996). According to Landman et al. (1996), the embryonic diameter of a lytoceratid ammonoid, Tetragonites glabrus, was ca. 1.1–1.2 mm in the Early Turonian, increased toward the Turonian–Coniacian boundary (1.45–1.7 mm), and then decreased toward the Early Santonian (1.0–1.3 mm), although no detailed data (number of specimens, standard deviations, sampling areas) is provided. To better understand the chronological and not the regional variation, the intraspecific variation of the shell embryonic diameters should be compared through time within the same and adjacent areas. Tanabe et al. (2003) have reported the AD and PD, respectively for H. subramosum from the Middle
Turonian succession in the Tappu area (Sample R4018 and R4020; Table 4). The Tappu area is the intermediate area between the Haboro and Ikushumbetsu areas and located 10 km south of the Haboro area and 100 km north of the Ikushumbetsu area (Fig. 1). Considering the fact that there is no significant difference in hatching size between the Haboro and Ikushumbetsu areas in the earliest Campanian in this study, it could be assumed that the hatchling size had no significant difference between the Tappu and Haboro and Ikushumbetsu areas in the Middle Turonian. Making this assumption, the hatchling diameters of H. subramosum in the Middle Turonian reported by Tanabe et al. (2003) is preliminary compared to those in this study on AD of H. subramosum in the earliest Campanian (Fig. 7). The Student’s t tests were used to compare the intraspecific variations between two different ages. The results of the tests show that the hatchling diameters of H. subramosum between different ages are significantly different (0.72–0.97 mm in the Middle Turonian and 0.91–1.13 mm in the earliest Campanian; Table 5), which suggests that the hatching sizes of H. subramosum slightly increased from the Middle Turonian until the earliest Campanian (during about 7 Myr). This increasing trend in H. subramosum from the Middle Turonian to the earliest Campanian is preliminarily different from that in T. glabrus of Landman et al. (1996), which shows the increase and then decrease from the Early Turonian to the Early Santonian, although the hatchling size of H. subramosum between the Middle Turonian and the earliest Campanian has not examined and, therefore, their detailed trend is still uncertain. This fact implies that the changes of hatchling sizes
Fig. 7. Geological trend of ammonitella diameters of Hypophylloceras subramosum in the Middle Turonian (R4018 and R4020 from Tappu area; Tanabe et al. 2003) and the earliest Campanian (Haboro and Ikushumbetsu areas; this study).
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Hatchling size in Late Creacteous ammonoids
Table 5. Results of Student’s t test for ammonitella diameters in Hypophylloceras subramosum between the earliest Campanian (this study) and the Middle Turonian (Tanabe et al. 2003).
Haboro area in this study vs R4018 in Tanabe et al. (2003) Ikushumbetsu area in this study vs R4018 in Tanabe et al. (2003) Haboro area in this study vs R4020 in Tanabe et al. (2003) Ikushumbetsu area in this study vs R4020 in Tanabe et al. (2003) R4020 vs. R4018 in Tanabe et al. (2003)
t
DF
12.07
17
*
6.31
20
*
5.21
17
*
4.16
20
*
0.86
14
ns
DF, the degrees of freedom; ns, not significant. *Significant (P < 0.01).
through time are different in each species or higher taxonomy, which should be demonstrated in further studies with the detailed data set of the hatchling-size changes in a single species through time.
Conclusion The intraspecific variation of hatchling size in two Late Cretaceous ammonoids (G. tenuiliratum and H. subramosum) from Hokkaido, Japan, was examined in this study from the point of view of regional differences. The AD and PD of both species show no significant difference in the Haboro and Ikushumbetsu areas, Hokkaido, which are separated by a distance of ca. 110 km. Estimating that the velocity of palaeocurrent around the Haboro and Ikushumbetsu areas during the Cretaceous Period was 0.25 m ⁄ s, similar to those in the modern ocean current flowing off the eastern Pacific coast of Hokkaido, the egg masses and ⁄ or hatchlings of G. tenuiliratum and H. subramosum were buoyant and transported for more than 5 days. This is the minimum estimate, however, because this study has compared the hatchling sizes between only two areas with the distance of about 110 km. The hatchling sizes of G. tenuiliratum and H. subramosum in more distant areas of the same age should be analysed and then compared to those in this study in order to further test this postulation. The preliminary comparison of hatchling size through time suggests that the hatching sizes of H. subramosum increased from the Middle Turonian until the earliest Campanian (during about 7 Myr), although this should be examined with the more detailed data set from a single area through different ages in the future studies. Acknowledgements. – We are sincerely grateful to T. Kikuchi for his suggestion, K. Kurihara for his help during our fieldwork, and two anonymous reviewers and Dr C. Klug for their critical comments on the early draft. This study was supported by
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Grant-in-Aid for Young Scientists (no. 21740369 for 2009–2011) and the Japan Science and Technology Agency (JST; for 2007– 2011).
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