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Biol. Bull. 202: 148-155. (April 2002)
© 2002 Marine Biological Laboratory

Morphometric Analysis of Male Reproductive Features of Octopodids (Mollusca: Cephalopoda)

Janet R. Voight

Department of Zoology, The Field Museum, 1400 S. Lake Shore Dr., Chicago, Illinois 60605

E-mail: jvoight{at}fieldmuseum.org


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
 Literature Cited
 
Taxonomic accounts of octopodids frequently describe the spermatophore, the penis that releases the spermatophore from the internal organs, and the ligula and calamus that transfer it to a female. To explore relationships among these male features and body size, this study applies principal components analysis to data from 43 species of the family Octopodidae, or benthic octopuses. Covariation in penis and mantle length opposed by covariation in ligula and calamus lengths forms primary shape variation. Secondary shape variation is due to opposing variation between ligula and calamus lengths. Primary shape variation is greatest among shallow-water species. The calami and ligulae of diurnal and crepuscular shallow-water species are short compared to those of nocturnal shallow-water species. Because these structures contain heterogeneous collagen arrays and lack camouflaging chromatophore organs, they are white. Diurnal and crepuscular octopus species may minimize their lengths due to selection imposed by visual predators. Secondary shape variation is greater in deep-sea and high-latitude octopuses. Members of Voss’s Eledoninae (except Eledone) and Graneledoninae and two species of Benthoctopus have exceptionally long calami and comparatively short ligulae; these lengths vary among members of the Bathypolypodinae. Variation in spermatophore length is independent of the structures considered.


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Appendix
 Literature Cited
 
Male octopuses package sperm into spermatophores as it moves from the testis to the wholly internal penis, or terminal organ. To initiate sperm transfer, the muscular penis, which is continuous with the penial diverticulum, propels a stored spermatophore through the funnel to a groove on the ventral margin of the hectocotylus, one of the third arms (usually the right) that is shorter than the opposite arm. The spermatophore travels the length of the arm to its suckerless tip. At the arm tip, the aboral ligula, which depending on species can occupy from 3% to 38% of the arm length, is closely opposed by the shorter calamus. These structures presumably position the spermatophore in the female’s oviduct prior to the release of sperm (see Mann, 1984).

Among the Octopodidae, or benthic octopuses, ligula and calamus morphology is extremely variable (Robson, 1926). Because the ligula and calamus function with the penis to transfer spermatophores at copulation, and thereby increase male fitness, these characters may evolve as a unit rather than independently. Voss (1988), for instance, suggested that the large spermatophores and ligulae and calami of deep-sea taxa are causally linked. This hypothesis had yet to be tested by exploration of covariation among the features that handle spermatophores in mating.

This paper explores variation among spermatophore, penis, calamus, and ligula lengths, as well as mantle length, in 43 species to examine patterns of variation and to reveal morphological diversity in the family. Possible functional and ecological constraints that affect their morphology are discussed.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Appendix
 Literature Cited
 
Mantle length, spermatophore length, penis length, ligula length, and calamus length of 135 specimens representing 43 species were compiled from literature reports (n = 102) and from 33 preserved specimens (Appendix). Generally, published accounts reported measurement data only as indices, forcing the original measurements to be back-calculated. All measurements were log-transformed to base 10 prior to analysis. Log-transformation equalizes error—whether the result of measurement error, investigator bias, or the use of back-calculated measurements—over the wide size range considered and minimizes the effect of outliers (Bookstein et al., 1985; Strauss, 1985).

The characters chosen for this analysis are those of spermatophores and features that handle spermatophores during copulation; mantle length is included as the standard indicator of body size. Four other characters—sperm reservoir length, penis (terminal organ) diverticulum length, and the lengths of the third arm pair—had to be excluded from the analysis due to the following concerns. Sperm reservoir length is so tightly associated with total spermatophore length that it cannot function as an independent variable (Voight, 2001). The penis diverticulum is continuous with the penis, or terminal organ, proper. Homologies of the end points of the penis diverticulum were questionable, hence its length measurement was excluded. Because the diverticulum and penis are continuous, and subject to deformation apparently related to preservation (Alvina, 1965), their combined in situ anterior-posterior length was measured. Voight (1993) documented that arm length contributes considerable size-free shape variation within the Octopodidae. Preliminary analyses found that length variation in the hectocotylus and the unmodified third arm is strongly linked to overall species morphology; to focus this exploration on reproductive characters, arm lengths were not considered.

The measurement of penis length also presented potential problems. This measurement, from the extreme posterior tip of the penis diverticulum to the most cephalad part of the penis near the mantle aperture, generally parallels the ventral mantle septum and seems comparable with other extremal distances. The penis and diverticulum of some specimens, especially in the O. aegina group, can curve away from the mantle septum and, in extreme cases, become recurved (e.g., Sasaki, 1929; Adam, 1960). Use of the linear penis length measurement ignored any curves; as a result, penis length may have been underestimated in some specimens. Calamus and ligula lengths are measured from the distal sucker to the tip of each of the arm modifications (Fig. 1).



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  		Figure 1. Plotted are individual specimen scores on principal components 2 versus principal components 3. Large positive PC2 scores indicate long mantles and penises and short ligulae and calami; large negative PC2 scores represent the converse. Large positive PC3 scores represent comparatively short ligulae and long calami, large negative PC3 scores represent the converse. The inset hectocotylus tips of Graneledone pacifica (above), adapted from Voss and Pearcy (1990), and Octopus dierythraeus (below), adapted from Norman (1993a), illustrate the differences on PC3. Octopuses with one sucker row cluster at the top of the plot and are outlined by a line of long dashes: included are specimens of Graneledone pacifica represented by {star}; those of Eledone palari by {lozenge}; those of Pareledone charcoti, P. harrissoni, and Vosseledone charrua by heavy bars. Members of the O. vulgaris group are represented by {square}; all except O. filosus are outlined with a fine dashed line. The O. aegina group, with O. polyzenia at the far left, is represented by hollow bars, and the complete group is outlined by a dotted line. Overlapping these two groups are two specimens of O. rapanui, symbolized by {star}, that were assigned to the O. macropus group by Norman and Sweeney (1997). Members of this group (represented by {blacktriangleup}) are outlined with a line of dashes and dots; specimens of O. macropus have the two most positive PC2 scores. Specimens of Octopus (Abdopus), represented by {blacklozenge}, are outlined by a line of alternating dashes. • indicates long-armed octopuses not assigned to O. (Abdopus): at the far left are two Ameloctopus litoralis; the third from the left is Euaxoctopus pillsburyae; specimens of O. defilippi overlap those of Octopus (Abdopus). Individuals of O. berrima and O. australis, which are inseparable on this plot, are represented by {circ}. They, as do many other species, overlap Voss’s Bathypolypodinae, indicated by {triangleup}, and outlined by a dashed line. The far right * indicates Cistopus, other * represent miscellaneous species with scores reported in the Appendix.

 
The specimens included in the analysis sample the benthic octopodids as completely as possible, considering that the analysis requires matrix manipulations that force specimens without complete data to be deleted. For instance, within Eledone, only E. palari could be included, because only in this species is the calamus present. Regardless of whether the calamus of Eledone is represented in the analysis as missing or as zero, the pertinent specimens must be deleted because the log of zero is undefined. Thirteen currently recognized octopodid genera are included here, although sometimes by only one individual (see Appendix 1). Although Cistopus also reportedly lacks a calamus, the calamus in the specimen examined could be reliably measured, in contrast to the specimens of Eledone examined. To allow inclusion of a representative of Euaxoctopus, spermatophore length reported for one specimen had to be combined with data from another specimen. Although phylogenetic relationships among the Octopodidae remain obscure (Voight, 1997), three informally recognized species groups (e.g., Robson, 1929; Norman and Sweeney, 1997) are treated here.

Members of the Octopus vulgaris species group tend to be large, with the dorsal arms and web sector shortest. The ligula and calamus are small and, depending on the species, prominent ocelli may be present. Several members of this group are active during daylight hours (Hanlon, 1988; Hanlon and Messenger, 1996). Members of the O. aegina group listed by Norman and Sweeney (1997) tend to be medium in size, with the dorsal arms and web sector dramatically the shortest (Robson, 1929). The penis and its diverticulum can be very long; warts characterize the skin texture, ocelli may be present on the web, and longitudinal lines of color often occur on the arms and mantle (Robson, 1929; Norman and Sweeney, 1997). Species in this group are considered to be crepuscular (Norman and Sweeney, 1997), although O. burryi has been identified as nocturnal (Hanlon, 1988). Species of the O. macropus group tend to be large with the dorsal arms and web sector the longest, and red and white in color. Activity among these species appears to be exclusively nocturnal (Hanlon, 1988; Norman, 1993a). The O. (Abdopus) subgenus of Norman and Finn (2001) includes long-armed Indo-West Pacific species with small mantles and complex skin textures. Members of the subgenus reportedly occur only in the intertidal zone, and some forage during daylight low tides (Norman and Finn, 2001).

To explore morphological variation among the five measurements in 135 specimens, the data matrix was analyzed by principal components analysis (PCA) using a covariance matrix in SySTAT version 9 (SPSS). PCA assesses shape and size variation without a priori group determinations. If all characters used in the analysis are assigned uniformly large positive loadings on a component, usually principal component 1 (PC1), that component is considered to represent covariation due to size. Shape variation is attributed to secondary components, with the magnitude and sign of the loadings indicating their relative contribution and relationship to other characters. Plots of specimen scores on the shape components PC2 versus PC3 help to visualize the size-free shape similarities and differences among the specimens considered.

Because the reproductive characters considered in this analysis enlarge as males mature rather than as they grow, including less than fully mature males in the analysis would complicate the calculation of the size component. To ensure a strong size component and heighten comparability among species represented by mature males of different sizes, an attempt was made to include only fully mature males. Males were excluded if they had short mantles, penises, ligulae, and spermatophores relative to those of conspecifics.

Evidence of investigator bias was assessed by comparing individual specimen scores within species groups and within species, in the few cases in which different investigators reported data for a single species. Bivariate plots of log-transformed data in Microsoft Excel were used to explore patterns of variation discovered by the PCA. Because these plots did not require that each specimen be represented by all five measurements, all possible specimens were included, except specimens of the Atlantic species of Eledone that Voight (2001) found to be unique among the octopodids.

To further test the hypothesis that spermatophore size is causally linked to ligula and calamus length, the greatest width of the spermatophore was considered post hoc. This measurement, usually taken at the sperm reservoir, is infrequently reported. Weill (1927) found in fresh specimens that spermatophore width varies with the salinity of surrounding fluid. If the salinity of the fixative affects spermatophore width in preserved specimens, the measurement may be unreliable. This possibility could not be tested because data within a species and information on specimen preservation were too limited. With the limited data available, the relationships between spermatophore width and ligula and calamus lengths were explored by plotting log-transformed spermatophore width data versus specimen score on PC3 for 87 specimens.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Appendix
 Literature Cited
 
PCA revealed most variation in the data set to be due to size differences among the specimens considered (Table 1). Shape variation on PC2 was dominated by covariation in penis and mantle lengths in opposition to covariation of ligula and calamus lengths. PC3 revealed shape variation created by opposing variation between ligula and calamus lengths. Spermatophore length contributed minimal shape variation on either PC2 or PC3 (Table 1); it was the major source of shape variation on PC4, due largely to species of the Octopus aegina group.


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  		TABLE 1 PCA (principal components analysis) component loadings for the five length variables considered

 
Mean scores on PC2 and PC3 for each species are reported in the Appendix, and individual scores are plotted on Figure 1. Shallow-water species show extreme variation on PC2. With near zero or negative scores on PC3, Cistopus and the diurnal and crepuscular groups of Octopus vulgaris (with the exception of O. filosus) and O. aegina (with the exception of O. polyzenia), which overlap extensively, have positive PC2 scores that reflect their small ligulae and calami and long mantles and penises. In direct opposition, negative PC2 and near zero PC3 scores of Ameloctopus litoralis and Euaxoctopus pillsburyae reflect their long ligulae and calami and short mantles and penises. With slightly stronger negative PC3 scores and therefore longer ligulae, O. australis, O. berrima, Bathypolypus arcticus, and Benthoctopus spp. are also negative on PC2. Most members of the O. macropus group score near zero on PC2 and are slightly negative on PC3, although within this group both O. macropus and O. rapanui have positive PC2 scores.

The deep-sea and high-latitude species Voss (1988) assigned to Eledoninae (excluding species of Eledone that could not be included) score positively on PC3, indicative of relatively long calami, and near zero on PC2. The species assigned to Voss’s Bathypolypodinae have negative PC2 scores but variable PC3 scores.

Species with negative PC3 scores, and therefore a long ligula relative to calamus, vary widely in their PC2 scores. Most members of the diurnal subgenus Octopus (Abdopus) are strongly positive on PC2, although some poorly known taxa in that subgenus overlap with species of the O. macropus group. Specimens of O. australis and O. berrima score negatively on both shape components and, based on the characters considered in this analysis, are comparable to Bathypolypus.

As noted above, scores for the diurnal O. vulgaris and O. aegina species groups overlap, being positive on PC2 and near zero on PC3, except O. filosus and O. polyzenia (Fig. 1). Species of the nocturnal O. macropus group tend to score near zero on PC2 and negative on PC3, except O. rapanui, which overlaps the O. vulgaris and O. aegina groups. The taxa assigned to the Eledoninae of Voss (1988) and specimens of Graneledone score strongly and uniformly positive on PC3, but are not unique. Individuals of Benthoctopus macrophallus, B. piscatorum, and O. campbelli have similar scores on both components.

No evidence of investigator bias was apparent. Bivariate analyses support the covariances discovered among these variables; a single linear relationship explains 86.67% of the variation between spermatophore and penis length among 155 specimens. Between spermatophore and mantle length, a single linear relationship explains 73.4% of the variation among 211 specimens. In contrast, the relationship between ligula and mantle length in 325 specimens explains only 40.0% of the variation; between calamus and mantle length, the percent of variation explained drops to 36.8% in 297 specimens.

No discernible relationship exists between the PC3 score and spermatophore width in 87 specimens. If species that produced wide spermatophores had long ligulae or calami, the plot would show a U-shape, which it does not. If production of wide spermatophores were associated with either a long ligula or calamus, there would be a significant correlation, which does not exist. There is no pattern with the geographic distribution of the specimens. Deep-sea specimens have either narrow or wide spermatophores, as do those from shallow-water tropical latitudes. Although members of Graneledone and Voss’s Eledoninae have the highest scores on PC3 and the widest spermatophores, the specimen of Bathypolypus included had very wide spermatophores and a negative (-0.75) PC3 score. Most members of Octopus (Abdopus) and Ameloctopus had remarkably and consistently narrow spermatophores, regardless of their PC3 score.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Appendix
 Literature Cited
 
Among the specimens of benthic octopodids considered, mantle and penis lengths covary and oppose variation in ligula and calamus lengths (Table 1). The covariation seen on PC2 in mantle and penis lengths may result from functional constraints. The octopus penis, because it is contained within the mantle, tends to vary in concert with mantle length rather than independent of mantle length. If the maximal lengths of the exceptionally long curved penises of some species of the Octopus aegina group had been fully considered in this analysis, they would covary with the very long spermatophores of these species that in this analysis contribute most shape variation to PC4 (Table 1).

Underlying the covariation discussed above is opposing variation between ligula and calamus lengths, which apparently was previously unsuspected. Spermatophore length does not covary with ligula or calamus length, nor does spermatophore width. If, however, during copulation the ligula, the calamus, or both hold the spermatophore at its narrow ejaculatory apparatus, rather than at its widest part, a functional relationship may exist undetected; currently, however, ligula and calamus lengths must be assumed to be free of functional constraints. Variation in these lengths may relate to environmental factors.

Most shallow-water diurnal and crepuscular species, including some species of Octopus (Abdopus) and the O. vulgaris and O. aegina groups, have more positive PC2 scores—and thus shorter ligulae and calami—than do shallow-water nocturnal species from comparable latitudes, such as members of the O. macropus group, Ameloctopus litoralis and O. joubini. The ligula, the calamus, and the groove on the ventral arm that moves the spermatophore to the tip of the hectocotylus lack the chromatophore organs that camouflage cephalopod skin (Racovitza, 1894). Histological sections of these features reveal abundant collagen fibers in a heterogeneous array (J. Thompson, University of North Carolina, pers. comm.). Heterogeneous collagen arrays reflect light (Johnsen and Widder, 1999), to make these structures appear white rather than translucent (S. Johnsen, Duke University, pers. comm.). Their white color may make these structures conspicuous and, especially in diurnal and crepuscular octopuses, vulnerable to visual predators. Although octopuses regenerate lost and damaged arms, including the hectocotylus (Callan, 1939), the fitness cost of damage to the hectocotylus may be high. Males typically hold the hectocotylus in a coiled position, perhaps both to conceal it and to protect its tip (Naef, 1923). Physically minimizing the ligula and calamus in diurnally active octopuses may further reduce the risk of predation and preserve a male’s ability to copulate.

The contrast between ligula and calamus lengths of diurnal versus nocturnal species parallels the contrast in body patterning complexity in these species, hypothesized to result from selection by visual predators (Hanlon and Messenger, 1996). Diurnal species in complex habitats are hypothesized to have the most complex body patterns because visual predators exert the greatest selection on this group; nocturnal species, and those occurring on more uniform habitats such as sediment, are predicted to show simpler body patterns because visual predators have less effect (Hanlon and Messenger, 1996). Hanlon and Messenger (1996) could not document body patterning complexity among octopuses from deep-sea and high-latitude environments where visual predators are thought to be rare. If ligula and calamus lengths reflect the level of predation by visual predators, octopuses from these areas are predicted to have long ligulae, calami, or both. This study supports this prediction with two opposing patterns.

Long calami characterize most species of Voss’s (1988) Eledoninae (except Eledone), which are Antarctic and deep-sea in distribution; species of the deep-sea Graneledoninae; specimens of O. campbelli (from 52° S); and two specimens of the deep-sea genus Benthoctopus. Voss (1988) did not cite calamus length as unifying members of his Eledoninae (exclusive of Eledone, which lacks a calamus) and Graneledoninae. Species of Bathypolypus and Benthoctopus, which compose the Bathypolypodinae, Voss’s other subfamily of deep-sea and high-latitude species, are less uniform. Differences in ligula and calamus lengths of these species may reliably reflect their evolutionary histories, notably their polyphyletic origin.

The minute ligula and calamus and large body size help unify the O. vulgaris group (Pickford and McConnaughey, 1949); the former two features appear to ally this group with the O. aegina group. These groups, in fact, may have been extensively confused in the past. Some members of both groups have ocelli on the web; all species have short dorsal arm pairs and dorsal web sectors and enlarged suckers on the second and third arm pairs of mature males. If the O. aegina and O. vulgaris groups are closely related, the small ligula and calamus may be ancestral. The differences O. filosus shows compared to the other members of O. vulgaris suggest, however, that morphology or the relationship between male reproductive organ size and mantle length in this fairly small species is plastic.

Although morphology of copulatory organs may reflect history, variation exists within the widely recognized species groups of O. vulgaris and O. aegina. Octopus polyzena of the O. aegina group and O. filosus of the O. vulgaris group have long ligulae and calami. The ecology of O. polyzenia is virtually unknown. Members of O. filosus have been most often collected at fish poison stations on Caribbean coral reefs (Voss, 1953; Burgess, 1966). If their high degree of crypsis and use of secluded reef habitats effectively protect them from visual predators as well as from humans, visual predators may impose minimal selection on members of this species. Among species assumed to be nocturnal, the short ligula and calamus of O. rapanui place it with diurnal and crepuscular species, rather than with other members of the nocturnal O. macropus group. Voss (1979) indicated that this species was only superficially similar to members of the O. macropus group; Norman and Sweeney (1997) implicitly disagreed when they assigned it to the group. Additional natural history data on this and other little known species would test the hypothesis that selection by visual predators limits ligula and calamus length in diurnal and crepuscular species.

One taxon that could not be included here, Grimpella thaumastocheir, was described by Robson (1928) as having a huge calamus. Although Robson allied this taxon to Bathypolypus and Benthoctopus, as did Voss (1988), the results reported here show that most members of those genera have a longer ligula than calamus. Grimpella therefore appears more similar to O. campbelli, another species from cold southern waters (Stranks and Norman, 1993). That both Robson and Voss allied this species with those with longer ligulae, rather than with those with large calami, suggests that neither worker recognized or gave credence to the difference the present analysis emphasizes.

Lu and Stranks (1991) acknowledge that the presence of a calamus makes E. palari unique among species of Eledone, and they recognize that the calamus is unusually large in that species. They assigned the species to Eledone because its male arm tips are hetermorphic, a feature that is otherwise unique to that genus. They clearly assumed that the heteromorphic arm tips were derived from a common ancestor and that the calamus, an octopodid plesiomorphy, was lost in the ancestor of the Atlantic species of the genus. Given the striking similarity between calamus and ligula length in this species and in members of Pareledone, the consistency of the geographic and depth distributions of E. palari and the circum-Antarctic species of Pareledone, the homology of the arm modification merits reinvestigation.

It has been argued that visual predators have strongly impacted cephalopods through their evolution (Packard, 1972, 1988). This study suggests that the influence of visual predators extends to the mechanics of copulation itself. The degree to which the lengths of the calamus and ligula reflect evolutionary history versus ecological pressures will remain unknown until we develop a better understanding of the natural history of the organisms.


   Appendix
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
Literature Cited
 
Listed here are species by species group, with each species’ mean PC2 and PC3 scores reported in parentheses, the mantle length of each specimen considered and the sources of the data and specimens that contributed to this analysis. Specimen depositories are ANSP, Academy of Natural Sciences, Philadelphia; CAS, California Academy of Sciences; FMNH, Field Museum of Natural History; UMML, University of Miami Marine Laboratories.

Species group of Octopus vulgaris: Octopus vulgaris (1.447; -0.143); 61, 90, 101, 49, 45 (Pickford, 1945, 1946). O. veligero (1.037; 0.126); 84; UA. O. filosus (-0.324; 0.707); 10, 11, 12, 13, 13.5, 14, 15 (n = 2), 16, 16.5 (n = 2), 17, 18, 22, 24.5, 27, 28, 29, 34, 37 (Alvina, 1965). O. cyanea (1.381; 0.017); 49.8 (n = 2), 103.9 (n = 2), 105.6, 127.1 (n = 2) (Norman, 1991)

Species group of Octopus aegina: O. aegina (0.457; -0.069); 31.9, 42.3 CAS 077992; CAS 077993. O. polyzena (-0.818; -0.050); 26.3 (Norman, 1993b). O. exannulatus (1.23; 0.064); 37.2, 41.7, 45.4 (Norman, 1993b); 38.7; 42.3 CAS 077990. O. mototi (0.377; 0.548); 66.2, 70.5 (Norman, 1993b). O. burryi (0.117; 0.657); 39 (Voss, 1951).

Species group of Octopus macropus: O. macropus (0.929; -1.208); 115 (Pickford, 1945). O. alpheus (0.094; -0.360); 61.9, 63.9, 74.2 (Norman, 1993a). O. aspilosomatis (-0.255; 0.783); 37.3, 42.2, 83.2 (Norman, 1993a). O. rapanui (1.557; 0.029); 113, 115 (Voss, 1979). O. ornatus (-0.182; -1.686); 103.5, 104.2 (Norman, 1993c). O. graptus (0.055; -0.587); 157.9 (Norman, 1993a).

Species assigned to the Eledoninae of Voss 1988: Pareledone charcoti (-0.134; 0.777); 55.5, 71.6 (Kubodera and Okutani, 1994); 34.8 UMML 31.2561. Pareledone harrissoni (1.637; 0.673); 96 (Kubodera and Okutani, 1994). Megaleledone sp. (0.195; 1.060); 67.8 UMML 31.2562. Vosseledene charrua (-0.166; 1.28); 49, 50 (Palacio, 1978). Eledone palari (-0.025; 1.373); 32.1; 34.4; 37; 37.9 (n = 2), 38.3; 38.7; 39.6 (Lu and Stranks, 1991). Graneledone pacifica (0.268; 1.679); 85 (Voss and Pearcy, 1990); 77.9, 83.2, 86.9, 94.4, 98.4, 106.3, 116.4 FMNH uncat.; FMNH 278061; FMNH 278062; FMNH 281001; FMNH 281002; CAS 031474; CAS 061434.

Species assigned to the Bathypolypodinae of Voss 1988: Bathypolypus arcticus (-1.259; -0.807); 56.8 FMNH 278080. B. piscatorum (-0.059; 0.890); 125.1 FMNH 281720. B. yaquinae (-1.068; 0.358); 29.1, 31 (n = 2), 33.4 FMNH 278308; FMNH 278309; FMNH 278311. B. macrophallus (-0.018; 1.130); 83 (Voss and Pearcy, 1990). Benthoctopus sp. a (-0.557; -1.505); 48.8 FMNH 278066. Benthoctopus sp. b (-0.256; -0.718); 45 CAS 018763.

Octopus (Abdopus): O. (A.) aculeatus (-0.213; -0.503); 35.3, 41.4 (Australia) (Norman and Finn, 2001). O. (A.) cf. aculeatus (1.081; -1.361); 25.5, 29.3, 40.5, 45.9, 47.6, 57.8 (Thailand) CAS 077987; CAS 078001; CAS 078002 (n = 4). O. (A.) capricornicus (1.480; -1.948); 40, 42.1 (Norman and Finn, 2001). O. (A.) n sp. (-0.581; -0.602); 38.3, 40.7, 44.4, 45.4, 45.6, CAS 077999 (n = 3); CAS 078000 (n = 2).

Long-armed octopuses: Ameloctopus litoralis (-2.556; -0.164); 14, 15.9 (Norman, 1992). O. defilippi (0.914; -1.296); 25.5, 39 (Voss, 1964). Euaxoctopus pillsburyae (-1.486; 0.171); 24 (Voss, 1975).

Octopus australis and berrima: O. australis (-1.22; -1.001); 27.1, 40.5, 45.2, 46.5, 57.6, 58.2, 60.4, 67.1, 68.7 (Stranks and Norman, 1993). O. berrima (-1.043; -0.964); 31.3, 32.6, 36.3, 58.9, 63.5, 79.6 (Stranks and Norman, 1993). O. berrima, as O. australis (-0.993; -0.804); 45 (n = 2), 54, 56, 67 (Tait, 1982).

Miscellaneous species with uncertain affiliation: Octopus briareus (-0.336; 0.445); 46 (Pickford, 1945). O. joubini (0.233; -0.193); 17, 36 (Pickford, 1945). Enteroctopus magnificus (0.274; -1.136); 285 (Villanueva et al., 1991). O. zonatus (-1.148; 0.564); 19 (Voss, 1968). O. campbelli (0.184; 1.443); 34.1 (Stranks and Norman, 1993). Cistopus sp. (2.685; 0.303); 47.8 ANSP 6394. Vulcanoctopus hydrothermalis (-0.625; 0.450); 43.9 FMNH 287365.


   Acknowledgments
 
Jodi Sedlock, University of Illinois at Chicago, provided invaluable assistance with the multivariate analysis. Rich Strauss provided insightful comments during this study. The combined expertise of Joe Thompson of The University of North Carolina at Chapel Hill and Sönke Johnsen of Duke University provided unique insight into the pattern seen here. M. Vecchione and R. Toll provided helpful comments on the text; C. Simpson provided the figure. Terry Gosliner of the California Academy of Sciences, Nancy Voss of the University of Miami Marine Laboratories, and George Davis of the Academy of Natural Sciences of Philadelphia allowed me to examine specimens in their care.


   Footnotes
 
Received 12 September 2001; accepted 28 January 2002.


   Literature Cited
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
 Literature Cited
 

    Adam, W. 1960. Cephalopoda from the Gulf of Aqaba. Bull. of the Sea Fish. Res. Stn. Haifa 26: 3–26.
    Alvina, L. H. 1965. A study of the morphology and biology of Octopus hummelinki Adam, 1936. Master’s thesis. University of Miami, FL. 146 pp.
    Bookstein, F. L., B. Chernoff, R. L. Elder, J. M. Humphries Jr., G. R. Smith, and R. E. Strauss, Eds. 1985. Morphometrics in Evolutionary Biology, Academy of Natural Sciences of Philadelphia Special Publication 15, Philadelphia, PA. 277 pp.
    Burgess, L. A. 1966. A study of the morphology and biology of Octopus hummelincki Adam, 1936 (Mollusca: Cephalopoda). Bull. Mar. Sci. 16: 762–813.
    Callan, H. G. 1939. The absence of a sex-hormone controlling regeneration of the hectocotylus in Octopus vulgaris Lam. Pubbl. Staz. Zool. Napoli 18: 15–19.
    Hanlon, R. T. 1988. Behavioral and body patterning characters useful in taxonomy and field identification of cephalopods. Malacologia 29: 247–264.
    Hanlon, R. T., and J. B. Messenger. 1996. Cephalopod Behaviour. Cambridge University Press, Cambridge.
    Johnsen, S., and E. A. Widder. 1999. The physical basis of transparency in biological tissue: ultrastructure and the minimization of light scattering. J. Theor. Biol. 199: 181–198.[ISI][Medline]
    Kubodera, T., and T. Okutani. 1994. Eledonine octopods from the Southern Ocean: systematics and distribution. Antarct. Sci. 6: 205–214.
    Lu, C. C., and T. N. Stranks. 1991. Eledone palari, a new species of octopus (Cephalopoda: Octopodidae) from Australia. Bull Mar. Sci. 49: 73–87.
    Mann, T. 1984. Spermatophores: Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa. Springer-Verlag, Berlin.
    Naef, Adolf. 1923. Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres. Vol. 1. Cephalopoda. Monograph 35, Zoological Station, Naples. English translation: Fauna and Flora of the Bay of Naples. 1972. A. Mercado, trans. Israel Program for Scientific Translations, Jerusalem.
    Norman, M. D. 1991. Octopus cyanea Gray, 1849 (Mollusca: Cephalopoda) in Australian waters. Bull Mar. Sci. 49: 20–38.
    Norman, M. D. 1992. Ameloctopus litoralis, gen. et sp. nov. (Cephalopoda: Octopodidae), a new shallow-water octopus from tropical Australian waters. Invertebr. Taxon. 6: 567– 582.
    Norman, M. D. 1993a. Four new octopus species of the Octopus macropus group (Cephalopoda: Octopodidae) from the Great Barrier Reef, Australia. Mem. Mus. Vic. 53: 267–308.
    Norman, M. D. 1993b. Ocellate octopuses (Cephalopoda: Octopodidae) of the Great Barrier Reef, Australia: description of two new species and redescription of Octopus polyzenia Gray, 1849. Mem. Mus. Vic. 53: 309–344.
    Norman, M. D. 1993c. Octopus ornatus Gould, 1852 (Cephalopoda: Octopodidae) in Australian waters: morphology, distribution, and life history. Proc. Biol. Soc. Wash. 106: 645–660.
    Norman, M. D., and J. Finn. 2001. Revision of the Octopus horridus species-group, including erection of a new subgenus and description of two member species from the Great Barrier Reef, Australia. Invertebr. Taxon. 15: 13–35.
    Norman, M. D., and M. J. Sweeney. 1997. The shallow-water octopuses (Cephalopoda: Octopodidae) of the Philippines. Invertebr. Taxon. 11: 89–140.
    Packard, A. 1972. Cephalopods and fish: the limits of convergence. Biol. Rev. 47: 241–307.[ISI]
    Packard, A. 1988. Visual tactics and evolutionary strategies. Pp. 89–103 in Cephalopods Present and Past, J. Wiedmann and J. Kullmann, eds. Second International Cephalopod Symposium, Tübingen. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany.
    Palacio, F. J. 1978. Vosseledone charrua: A new Patagonian cephalopod (Octopodidae) with notes on related genera. Bull. Mar. Sci. 28: 282–296.
    Pickford, G. E. 1945. Le poulpe Américain: A study of the littoral Octopoda of the western Atlantic. Trans. Connecticut Acad. Arts Sci. 36: 701–777.
    Pickford, G. E. 1946. A review of the littoral Octopoda from central and western Atlantic stations in the collections of the British Museum. Ann. Mag. Nat. Hist. 13: 412–429.
    Pickford, G. E., and B. H. McConnaughey. 1949. The Octopus bimaculatus problem: A study in sibling species. Bull. Bingham Oceanogr. Collect. Yale Univ. 12: 1–66.
    Racovitza, E.-G. 1894. Notes de Biologie. Arch. Zool. Exp. Gen. 2: 21–49.
    Robson, G. C. 1926. On the hectocotylus of the Cephalopoda—a reconsideration. Proc. Malacol. Soc. Lond. 17: 117–122.
    Robson, G. C. 1928. On Grimpella, a new genus of Octopoda, with remarks on the classification of the Octopodidae. Ann. Mag. Nat. Hist. 2: 108– 114.
    Robson, G. C. 1929. A Monograph of the Recent Cephalopoda. Vol 1. Octopodinae. British Museum of Natural History, London.
    Sasaki, M. 1929. A monograph of dibranchiate cephalopods of the Japanese and adjacent waters. J. Fac. Agric. Hokkaido Univ. 20 (Suppl.): 1–357.
    Stranks, T. N., and M. D. Norman. 1993. Review of the Octopus australis complex from Australia and New Zealand, with description of a new species (Mollusca: Cephalopoda). Mem. Mus. Vic. 53: 345–373.
    Strauss, R. E. 1985. Evolutionary allometry and variation in body form in the South American catfish genus Corydoras (Callichthyidae). Syst. Zool. 34: 381–396.
    Tait, R. W. 1982. A taxonomic revision of Octopus australis Hoyle, 1885 (Octopodidae: Cephalopoda), with a redescription of the species. Mem. Natl. Mus. Vic. 43: 15–24.
    Villanueva, R., P. Sánchez, and M. A. Compagno Roeleveld. 1991. Octopus magnificus (Cephalopoda: Octopodidae), a new species of large octopod from the southeastern Atlantic. Bull. Mar. Sci. 49: 39–56.
    Voight, J. R. 1993. The association between distribution and octopodid morphology: implications for classification. Zool. J. Linn. Soc. 108: 209–223.
    Voight, J. R. 1997. Cladistic analysis of the order Octopoda based on anatomical characters. J. Molluscan Stud. 63: 311–325.[Abstract/Free Full Text]
    Voight, J. R. 2001. The relationship between sperm reservoir and spermatophore length in benthic octopuses (Cephalopoda: Octopodidae). J. Mar. Biol. Assoc. UK 81: 983–986.
    Voss, G. L. 1951. Further description of Octopus burryi Voss with a note on its distribution. Bull. Mar. Sci. Gulf Caribb. 1: 231–240.
    Voss, G. L. 1953. Observations on a living specimen of Octopus hummelincki Adam. Nautilus 66: 73–76.
    Voss, G. L. 1964. Octopus defilippi Verany, 1851, an addition to the cephalopod fauna of the western Atlantic. Bull. Mar. Sci. Gulf Caribb. 14: 554–560.
    Voss, G. L. 1968. Octopods from the R/V Pillsbury southwestern Caribbean cruise, 1966, with a description of a new species, Octopus zonatus. Bull. Mar. Sci. 18: 645–659.
    Voss, G. L. 1975. Euaxoctopus pillsburyae, new species, (Mollusca: Cephalopoda) from the southern Caribbean and Surinam. Bull. Mar. Sci. 25: 346–352.
    Voss, G. L. 1979. Octopus rapanui, new species, from Easter Island (Cephalopoda: Octopoda). Proc. Biol. Soc. Wash. 92: 360–367.
    Voss, G. L. 1988. Evolution and phylogenetic relationships of deep-sea octopods (Cirrata and Incirrata). Pp. 253–276 in The Mollusca, Vol. 12. Paleontology and Neontology of the Cephalopods, M. R. Clarke and E. R. Trueman, eds. Academic Press, San Diego, CA.
    Voss, G. L., and W. G. Pearcy. 1990. Deep-water octopods (Mollusca; Cephalopoda) of the Northeastern Pacific. Proc. Calif. Acad. Sci. 47: 47–94.
    Weill, R. 1927. La structure, la valeur systématique et le fonctionnement du spermatophore de Sepiola atlantica D’Orb. Bull. Biol. Fr. Belg. 61: 59–92.




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