Polar Biol (1998) 20: 143±151
Ó Springer-Verlag 1998
ORIGINAL PAPER
Tim O'Hara
Origin of Macquarie Island echinoderms
Received: 4 December 1997 / Accepted: 11 April 1998
Abstract The origin of echinoderms from Macquarie Island in the Southern Ocean is analysed through a novel application of multivariate statistics. Ordinations are produced from a combination of species distribution, bathymetric, habitat and life history data in order to assess patterns of migration. The analyses distinguish groups of species derived from the Kerguelen Plateau, New Zealand and eastern Antarctica. These groups correlate with attributes expected for epiplanktonic dispersal and range expansion along the North and South Macquarie Ridges respectively. There is no convincing evidence for long-distance pelagic dispersal, migration from the abyssal plain or for human translocation of species. The results indicate that taxonomic groups dier in their ability to disperse, and emphasize the importance of depth in biogeographical analyses. Dispersal by range expansion appears to have been more signi®cant than epiplanktonic dispersal and vicariant rather than long-distance dispersal mechanisms are the preferred explanation for some disjunct distribution patterns.
Introduction Understanding the mechanisms of species dispersal is fundamental to the interpretation of biogeographic patterns (Pielou 1979). Dispersal hypotheses provide one set of causal explanations for species distributions, allowing analysis to progress from an inductive to deductive logical framework (sensu Ball 1976). Understanding the limits to dispersal is also crucial to assessing the relative importance of dispersal and vi-
Tim O'Hara(&) Department of Zoology, University of Melbourne, Parkville, Australia 3052 e-mail:
[email protected]
cariant processes in shaping the composition of regional biotas. Geologically recent oceanic islands provide an opportunity to study marine dispersal and colonization, free of the complex historical record of successive vicariant and dispersal events that confound the analysis of continental biotas. The remote location and recent origin of Macquarie Island make it an ideal candidate for the study of dispersal in the Southern Ocean. There are two main mechanisms for species to disperse: diusion and jump dispersal (Pielou 1979). Diffusion is the steady expansion of a species range over largely hospitable terrain. This is likely to occur as tectonic activity or climatic change create new migration routes. Jump dispersal is migration of organisms over large distances across the usual barriers to diusion. Barriers to range expansion by shallow-water marine species include land masses, deep-water oceanic basins, and environmental discontinuities such as the Antarctic Convergence. The creation of the Macquarie Ridge by tectonic forces has created three possible routes for benthic species to expand their ranges by diusion to include Macquarie Island. The North Macquarie Ridge provides a sublittoral migration route from the southwest corner of New Zealand. The South Macquarie Ridge provides a sublittoral migration route from the eastern Antarctic near the Balleny Islands (Dawson 1970). A third migration route is via the surrounding abyssal plain of the Southern Ocean, much of which lies below 4,000 m. Possible jump dispersal mechanisms to Macquarie Island include epiplanktonic rafting (Fell 1962; Edgar 1987), long-distance pelagic larvae (Scheltema 1977; Edgar 1986) and human translocation (Carlton 1985). The prevailing current is the West Wind Drift that ¯ows in an easterly direction in circum-subantarctic waters. The ¯ow rate is variable but the minimum drift time to Macquarie Island from the nearest islands to the west (Kerguelen, Heard and McDonald Islands) has been estimated to take 260 days (Edgar 1986). The holdfasts of the widely distributed kelps Macrocystis pyrifera and Durvillaea antarctica are postulated
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to be the primary vectors for epiplanktonic rafting in the Southern Ocean (Edgar, 1987). M. pyrifera has a very large hapteroid holdfast, which commonly harbours a multitude of motile and sessile animals (Edgar 1987). D. antarctica has a large simple conical holdfast, often riddled with internal cavities created by boring isopod Limnoria stephenseni (Edgar 1987; Smith and Simpson 1995). Experimental evidence shows that the M. pyrifera holdfast fauna can survive longer than 6 months after the plants are detached and suspended in the water column (Edgar 1987). It is theoretically possible for the pelagic larvae of shelf-dwelling species to drift for the 260+ days required from Kerguelen to Macquarie Island. Planktotrophic larvae of tropical gastropods have been found across the Atlantic Ocean and the duration of one larval stage has been calculated to exceed 320 days (Scheltema 1971). However, planktotrophic larvae are rare for Southern Ocean invertebrates (Knox 1994). The majority of Southern Ocean echinoderms have lecithotrophic larvae or non-pelagic development (demersal lecithotrophic larvae or brooding) (Pearse and Bosch 1994). Although the developmental period for lecithotrophic larvae is generally shorter than for planktotrophic larvae (Emlet et al. 1987), it can be extended in cold water. For example the pelagic lecithotrophic larvae of the Antarctic asteroid Acodontaster conspicuus take over 100 days to develop. Larval settlement of lecithotrophic larvae can be delayed in the laboratory for long periods (Birkeland et al. 1971), although many of the resulting juveniles can be abnormal (Emlet et al. 1987). It is yet to be demonstrated that lecithotrophic larvae can survive the rigorous conditions or the vast distances between subantarctic islands. Terrestrial introduced species have long been recognized on Macquarie Island (Selkirk et al. 1990), but the potential for marine introductions has not been considered. Several echinoderms have been introduced into southeast Australia, probably from the disposal of ballast water or the live importation of oysters (Dartnall 1969; Byrne et al. 1997). The feasibility of dispersal mechanisms can be determined experimentally (e.g. Edgar 1987), through quantitative sampling (e.g. Scheltema 1971) or via inductive logic (e.g. Fell 1962; Edgar 1986). However, actual colonization is a historical phenomenon that can only be inferred by studying present and past patterns of species distribution. Determining the actual dispersal methods used by colonizing species is even more problematic. For marine biogeographical studies in the Southern Ocean, the usual approach has been to form inferences from longitudinal gradients in species diversity (Fell 1962) or shared species distributions (Knox and Lowry 1977; Edgar 1986; Ricker 1987). As a new approach to biogeography in the Southern Ocean, this study uses multivariate statistical techniques on a range of distributional, bathymetric, habitat and life history data to assess patterns of dispersal. This approach is analogous to the use of multivariate statistics to reveal taxonomic relationships in morphometric data
(Reyment et al. 1984). The hypothesis being considered is that, although colonization will be opportunistic and stochastic, colonists will form recognizable groups based on the requirements imposed by the various modes of dispersal. For example, species rafting to Macquarie Island in kelp holdfasts need to occur in kelp beds on one of the islands to the west of Macquarie Island, i.e., they will be shallow-water rocky-reef epifauna. In addition, they must be able to survive in a drifting kelp holdfast for at least 260 days. Species dispersing to Macquarie Island by long-distance pelagic larvae need to have a larva capable of surviving a similar time. Species migrating from New Zealand or Antarctica along the Macquarie Ridge would need to survive the water depths existing along the ridge. Species migrating directly from the abyssal plain would have to be exceptionally eurybathic, capable of surviving from the abyss (4,000 m) to the shallower waters along the ridge. Finally, species dispersed by shipping must either be pelagic, a shallow-water species, or have a pelagic larval stage, and be capable of surviving in a ballast tank or as a hull-fouling organism. The requirements of each colonization method and the likely origin for Macquarie Island marine fauna using such methods are summarized in Table 1. One of the major impediments to the study of biogeography is the lack of availability of good quality data sets (Dawson 1988). The availability of a new monograph of Macquarie Island echinoderms (T. O'Hara, unpublished data) provides the opportunity to analyse a recent taxonomic and distributional data set for patterns of species dispersal. Echinoderms are particularly useful for this purpose as they occur in a wide range of habitats and because they exhibit a broad range of life histories with diering potential to disperse (Table 2).
Materials and methods Study site Macquarie Island (54°29¢S, 158°58¢E) lies isolated on the central section of the Macquarie Ridge, which runs south from New Zealand towards the Antarctic continent. This narrow ridge forms the southeast boundary of the Australian and Paci®c tectonic plates (Jones and McCue 1988). Macquarie Island is a rare example of uplifted oceanic crust that has never been in contact with the surrounding continents. The island is formed of basalt of middle Miocene to upper Oligocene age (approx 10±27 Ma) (Duncan and Varne 1988; Selkirk et al. 1990). During the Pliocene the island was under 2,000±4,000 m of water (Varne et al. 1969). Recent geomorphological evidence suggests that the island emerged as little as 300,000 years ago (Selkirk et al. 1990). Subsequent glaciation has not been signi®cant and it is also likely that the island remained exposed during the various interglacials (Selkirk et al. 1990). The water temperature at Macquarie Island usually varies from 4 to 7°C; however, the Antarctic Convergence lies only 40 km to the southeast, and Antarctic water can occasionally reach the island causing water temperatures to drop as low as 2.8°C (Williams 1988). Nevertheless, the island is the most southern ice-free shore in the eastern section of the Southern Ocean. The shore consists of rocky headlands interspersed with cobble, shingle or sandy beaches. The rocky intertidal platforms are fringed by the swirling fronds of the bull kelp Durvillaea antarctica. Durvillaea extends into
145 Table 1 Summary of the necessary attributes for marine species colonizing Macquarie Island
Colonization method
Long-distance dispersal 1. Epiplanktonic rafting on kelp 2. Pelagic larvae 3. Ballast water
Likely origin
Kerguelen/Heard
Necessary characteristics for successful immigration Depth
Habitat
Min depth 100 m Max depth >500 m Max depth >4000 m
was not collected in a consistent quantitative manner. The minimum and maximum depth data were simpli®ed into three variables to separate the relationships of dierent bathymetric zones. Only three depth variables were chosen as subantarctic collections are skewed towards shallow habitats (0±500 m) and consequently are not comprehensive enough to support numerous ®ne-scale depth categories. Thirty metres is the maximum depth at which kelp occurs (Ricker 1987); 100 m is the highest submerged point on the Macquarie Ridge (Dawson 1970) and 2000 m is an approximate depth for the beginning of an abyssal fauna. The variables are all independent except the second bathymetric factor (>100 m), which is automatically true if the third bathymetric factor (>2000 m) is true. The habitat and life history variables have some missing data (represented by question marks in Table 2). The most logical pattern analysis for binary data is a Principle Co-ordinate Analysis (PCoA) using various binary association measures, such as the simple-matching dichotomous coecient and Jaccard's coecient. However, PCoA analyses using the current data produced degenerate solutions with all component loadings lying within a narrow band on ®rst principle axis. Consequently, the data were ordinated by the Semi Strong Hybrid multi-dimensional scaling (SSH) method of the PATN software package (Belbin 1993) using Euclidean distance as the association measure. The ordination stress value for a two-dimensional ordination was 0.24; however, the PATN stress calculations are not based on Kruskal's original formula and tend to generate higher stress values (R. Marchant personal communication). The variables were then correlated against the SSH ordination using the Principle Axis Correlation (PCC) routine. PCC is a multiple-linear regression routine designed to see how well intrinsic (used in the ordination) or extrinsic variables can be ®tted into ordination space (Belbin 1993). The PCC correlation coecients (Table 3) give an indication of the strength of the correlation. The correlation vectors were superimposed on the ordination plot (Fig. 2). Similar patterns were generated using SSH with the Bray-Curtis association measure, and from a two-factor Principal Components Analysis.
Results Multivariate analysis
Analytic methods The species data (Table 2) were reduced into ten binary variables (Table 3) relevant to the various dispersal mechanisms (Table 1). Binary data were used to standardize the variables. The distributional and life history variables are naturally in a binary form. The habitat variables are better expressed as binary data as the material
The ordination shows that Macquarie Island echinoderms form groups according to their principle region of shared distribution (Fig. 2). The position of groups in ordination space correlates with variables that are related to their predicted method of dispersing to the island. Species shared with or derived from Kerguelen are
146 Table 2 Distribution, depth range, habitat and life history characteristics of Macquarie Island echinoderms. [K Kerguelen/Heard Islands, NZ/A New Zealand and southern Australia, EA eastern Antarctica (Victoria/Ross quadrants), WS western subantarctic (Falkland Is, Magellanic region, Prince Edward Islands), * denotes Species
Depth range (m)
Crinoidea Comissa dawsoni* Daidalometra arachnoides Florometra austini Glyptometra inaequalis Metacrinus wyvillii
128±1280 22±2236 58±550 362±1152 741±1152
Asteroidea Anasterias directus # Anasterias mawsoni Asterina hamiltoni #
0±55 0±357 0±95
Ceramaster patagonicus Crossaster multispinus Henricia sp a. obesa Henricia studeri Odontaster penicillatus Odontohenricia sp nov # Porania antarctica antarctica
90±1152 330±1152 8±604 100±450 55±527 69±100 10±300
Psilaster charcoti
25±3248
Pteraster anis anis Pteraster stellifer Sclerasterias mollis Smilasterias clarkailsa Solaster notophrynus
0±91 201±2804 22±697 11±357 330±1300
Ophiuroidea Amphipholis squamata Amphiura cf angularis Amphiura magellanica Ophiacantha sollicita Ophiacantha vilis Ophiactis hirta* Ophioleuce regulare Ophiomitrella conferta Ophioplocus incipiens Ophiura irrorata Ophiura meridionalis Ophiurolepis inornata
0±1000 49±527
Distribution K
NZ/A
EA
WS
x x x x x
Paci®c x1
x x x
x x x x
x
x
Widespread
South Africa3
x x x x x x
x
x x x x x x
Echinoidea Goniocidaris parasol* Goniocidaris umbraculum* Pseudechinus novaezealandiae
162±564 72±540 1±433
x x x
Holothuroidea Pseudocnus laevigatus Pseudocnus leoninoides*
72±540 0±128
x
0±14 91±1080 65±433 0±135
x
x x
x
x
x x x x x x x x
x
x
Atlantic Widespread
?Widespread
x x x x x
Widespread Widespread
x
W. Antarctica
4
x5
Life history
? Soft Rock Soft ?
? ? ? ? ?
Rock Rock Rock
Broods Broods Benthic egg cases ? ? ? ? ? ? Planktotrophic larvae Lecithotrophic larvae ? Broods ? ? ?
Rock/soft Rock/soft Rock/soft Rock/soft Rock/soft ? Rock/soft Soft
x
x x
Habitat Other
Indonesia
x1 x x2
0±450 124±2420 6±1090 124±770 65±900 40±2340 25±603 71±5870 69±1890 242±3500
Pseudopsolus macquariensis Psolus antarcticus Taeniogyrus sp nov # Trachythyone macphersonae #
species that have only been found on the Northern Macquarie Ridge (to 52° S), # denotes species endemic to Macquarie Island with the nearest relatives being 1A. rupicola, 2A. frigida, 3O. clarkae, 4 T. dunedinensis, 5T. ekmani, 6T. parva]
x6
Rock/soft Rock/soft Soft Rock/soft Rock Rock/soft Rock/soft Rock Soft Rock Rock/soft Rock/soft Rock/soft Rock/soft Rock/soft Rock Soft
Broods ? Planktotrophic larvae Broods ? Broods ? (Fissiparous) ? Broods Broods ? Broods ? Lecithotrophic larvae
? Rock/soft Rock/soft
Broods Broods ? Plankto trophic larvae
Rock/soft Rock
Broods ? Planktotrophic larvae Broods Broods ? ? Brooding or lecithotrophic larvae
Rock Rock Soft Rock
147
Fig. 1 Topographic cross section of Macquarie Island at 54.5 S (redrawn after Jones and McCue 1988)
correlated with shallow-water (2000 m) distributions. The softsediment, shelf/upper slope (>100 m) and pelagic larval regression vectors lie between the New Zealand and eastern Antarctic groups. Caution should be used in interpreting the pelagic larval vector as it has many missing values and the PCC correlation coecient is low (Table 3). Dispersal groupings Kerguelen Nine species are common to, or share their nearest relative with, Kerguelen or Heard Islands (Table 2). Eight of these species cluster closely together at the bottom of the ordination (Fig. 2). These eight species are characteristic shallow-water rocky-reef epifauna that are likely to have used epiplanktonic rafting to disperse to Macquarie Island. All eight have been recorded from kelp Table 3 Analysis variables with PCC Correlation Coecients Variable
PCC correlation coecients
Shared distribution variables 1. Kerguelen 2. New Zealand 3. E. Antarctica 4. W. subantarctic
0.793 0.823 0.681 0.639
Bathymetric variables 5. Min depth 100 m 7. Max depth >2000 m
0.739 0.602 0.633
Habitat variables 8. Rock 9. Soft sediment
0.522 0.639
Life history variable 10. Pelagic larvae
0.348
Fig. 2 Biplot showing two-dimensional SSH MDS ordination of the species attributes with associated PCC regression vectors. Ordination points are labelled with the regions of shared or derived distribution: K-Kerguelen, NZ-New Zealand, A-eastern Antartica, W-western subantarctic, O-other
beds (0±20 m) at Macquarie Island. Six of the species have been found within Durvillaea and Macrocystis holdfasts (Edgar 1987; T.O'Hara unpublished data). Pelagic dispersal is precluded for at least ®ve, and possibly for as many as seven, of the nine species, as they are known or suspected to have a direct form of development. Porania antarctica is a polymorphic species complex with several subspecies or species spread around the Southern Ocean. Two modes of development have been recorded (Pearse et al. 1991). The Macquarie form appears to be morphologically similar to the Antarctic form that develops by planktotrophy. Another of the eight species, Anasterias mawsoni, a brooder, is restricted to Macquarie and Heard Islands. The ninth species collected from Kerguelen and Macquarie Islands, the ophiuroid Amphiura angularis, has also been reported from New Zealand. However, the published descriptions of the populations dier and it is possible that they do not all belong to the same species. Several species similar to those at Macquarie Island and Kerguelen occur o New Zealand. These include Anasterias laevigatus, Pseudocnus leoninoides and Trachythyone bollonsi. In all cases the Macquarie Island forms are more alike forms from Kerguelen than those from New Zealand. New Zealand-southern Australia Twenty-six echinoderms are shared between Macquarie Island and New Zealand or southern Australia. Six widespread species (Smilasterias clarkailsa, Henricia obesa, Solaster notophrynus, Ophiacantha sollicita, Ophiomitrella conferta, Ophioleuce regulare) have been found from southern Australia but not yet from New Zealand. Five of the 26 species also occur o eastern Antarctica (see below) and 1 o Kerguelen (see above). These six species group with the Antarctic and western subantarctic species on the right of the ordination (Fig. 2). The other 20 species clearly group together at the top left of the ordination.
148
All 26 species have eurybathic distributions that would allow range expansion to proceed along the North Macquarie Ridge. Although several of these species (Smilasterias clarkailsa, Ophiacantha vilis, Amphiura magellanica and Pseudechinus novaezealandiae) occur in shallow-water (
