doi:10.1111/j.1095-8649.2010.02807.x, available online at wileyonlinelibrary.com
Differentiation and adaptive radiation of amphibiousgobies (Gobiidae: Oxudercinae) in semi-terrestrial habitats
G. Polgar*†, A. Sacchetti‡ and P. Galli‡
*Institute of Biological Sciences Faculty of Science, Institute of Ocean and Earth Sciences,University of Malaya, 50603 Kuala Lumpur, Malaysia and ‡Dipartimento di Biotecnologie
e Bioscienze, University of Milano-Bicocca, Piazza della Scienza, 20126 Milan, Italy
(Received 11 February 2010, Accepted 2 September 2010)
Oxudercine gobies (Teleostei: Gobiidae: Oxudercinae; Hoese, 1984; Murdy, 1989)are closely linked to tropical, subtropical and temperate intertidal mudflat and man-grove ecosystems (Clayton, 1993), being distributed from West Africa to the IndianOcean and the entire Indo-West Pacific region (Murdy, 1989). They are found alongthe whole intertidal zone, from subtidal up to high supratidal habitats, and exhibita wide range of adaptations, and include both aquatic and semi-terrestrial species(Nursall, 1981; Swennen et al., 1995; Takita et al., 1999), exhibiting extreme adap-tations to an amphibious lifestyle (Graham, 1997; Sayer, 2005).
Although based on a few model species and biological aspects, anatomical andphysiological studies showed a gradient in adaptation to semi-terrestrial conditions
†Author to whom correspondence should be addressed. Tel.: +63 7967 4609; email: [email protected]
in the sequence of genera Scartelaos, Boleophthalmus and Periophthalmodon plusPeriophthalmus. Such biological aspects included the locomotory behaviour (Harris,1960), the anatomy of gills and skin (Low et al., 1990; Zhang et al., 2000, 2003),the physiology of respiration (Milward, 1974; Ip et al., 1990; Graham, 1997; Koket al., 1998; Aguilar, 2000) and excretion (Ip et al., 2001; Chew et al., 2003).
The current phylogeny consensus at the genus level (Murdy, 1989) suggests thatchanges of ecophysiological and anatomical characters correspond to an increasein adaptation to the terrestrial environment at each cladogenetic event. At present,molecular phylogenetic studies include too few species for a comparison (Akihitoet al., 2000; Wang et al., 2001; Thacker, 2003).
This pattern is generally observed also at autoecological level, with oxudercinespecies of more derived genera distributed in more terrestrial habitats (Swennenet al., 1995; Takita et al., 1999). Nonetheless, quantitative studies are extremelyscarce, while standard measures of ‘habitat terrestriality’ in intertidal systems wereonly recently attempted (Polgar & Crosa, 2009; Polgar & Bartolino, 2010).
Oxudercine gobies are also well adapted to rapid and drastic salinity changes(Evans et al., 1999). Even if some species are reported from habitats with very lowsalinities (Allen, 1991; Khaironizam & Norma-Rashid, 2003), most species are foundin coastal and intertidal areas; therefore, it can be reasonably assumed that Oxuderci-nae have a marine origin. Nonetheless, no comparative analysis of the salinity condi-tions found in the habitats of different sympatric species is available in the literature.
During this study, nine oxudercine species belonging to six genera were recordedalong the banks of the lower Fly River and delta (Fig. 1): Boleophthalmus caeruleo-maculatus McCulloch & Waite, Oxuderces wirzi (Koumans), Periophthalmodonfreycineti (Quoy & Gaimard), Periophthalmus darwini Larson & Takita,Periophthalmus novaeguineaensis Eggert, Periophthalmus takita Jaafar & Larson,
141·83° 142·52° 143·51°
8·41° S
N
8·41° S
143·51° EWariura Island
WabadaIsland
Wapi
Kiwai Island
Sturt Island
PapuaNew Guinea
Torres StraitGulf ofPapua
CoralSea
Australia
Suki6
5 4 32 1
89
12
1110
131714
15 167
PurutuChannel
Tapila
Aibinio Island
Abaura Island
Umudatid.st.2
1015
10 km
Sisikura IslandPurutu Island
5 km
Fig. 1. Study sites ( ). Salinity isopleths ( ) are drawn from Robertson et al. (1991); Umuda tid.stat.,reference tidal station. Upper panel: detail of the study sites within the delta; the Wapi Creek flows fromthe new Wapi village to the sea, while the two short lines indicate two transects made along the PurutuChannel (sites 16 and 17).
H A B I TAT A N D A DA P TAT I O N I N M U D S K I P P E R S 1647
Periophthalmus weberi Eggert, Scartelaos histophorus (Valenciennes) and Zappaconfluentus (Roberts) [Fig. 2(k)–(t)]. Two more species, Boleophthalmus sp. andPeriophthalmus sp., did not correspond to the available taxonomic keys and descrip-tions (Murdy, 1989; Larson & Takita, 2004; Jaafar & Larson, 2008) and are currentlyunder description.
The main objectives of this study were: (1) to use a multivariate measure ofenvironmental water availability and salinity to explore the habitat differentiation ofthe oxudercine gobies of the Fly River and delta, Papua New Guinea, and (2) todiscuss the model of a gradual increase of terrestriality among genera in the light ofthe observed correspondence between ecological and phylogenetic categories.
MATERIALS AND METHODS
F I E L DW O R K A N D S P E C I E S
Seventeen sites within a range of 250 km along the banks of the lower Fly River anddelta (Fig. 1 and Appendix 1) were visited during 20 surveys made on foot inside forestsand adjacent peritidal areas, from 17 September to 1 October 2007 (south-east trade-windseason). Sites were reached by dinghy either from the Ok Tedi Mining Limited (OTML)field station of Sturt Island (Fig. 1; site 1) or from research vessels. At each site, severalareas were surveyed along the intertidal gradient, including tidal mudflats, mangrove forestsand ecological transitions to freshwater systems: where mudskippers were found, plots of25–50 m2 where environmental conditions were essentially the same were georeferencedand surveyed (45 plots, one to six per site; Appendix 1).
Tidal predictions were obtained from the reference tidal station of Umuda (AdmiraltyEasyTide United Kingdom Hydrographic Office, UKHO; www.ukho.gov.uk), in the northerndelta (Fig. 1). In this system, tides are markedly semi-diurnal, with tidal ranges that werec. 0·5–2·5 m during neap tides and 2·5–4·5 m during spring tides during the period of study.Nonetheless, even if tidal bores are felt up to 250 km from the river mouth (Roberts, 1978),fluvial dynamics have an increasing influence upriver, and tidal predictions are less and lessreliable at increasing distances from the tidal station (E. Wolanski, pers. comm.). For thisreason, the timing of tidal phases was always verified by direct observation and recordings(e.g. movements of anchored boats and of the water’s edge).
The Fly Delta is tide dominated (Dalrymple et al., 2003) and wave influence is minimal,except during the monsoon period (December to March). The islands on the northern sideare colonized by mangrove forests, which exhibit a marked zonation, while the other islandsand the mainland are fringed by freshwater vegetation (Fig. 1). Even though the middleFly River suffers from high anthropogenic influence caused by intense mining activities byOTML, the lower Fly River and delta are much less affected (Roberts, 1999; Van Zyl et al.,2002a, b; Townsend & Townsend, 2004). These systems maintain rich and large mangroveand freshwater forests, thanks to peculiar oceanographic and sedimentological conditions(Wolanski et al., 1998), and the very low human population density.
Salinity is affected by the interplay of rainfall, river discharge, tides and seasonal winds(Wolanski et al., 1995, 1998). Annual rainfall in the lower Fly River area is <2·5 m (Roberts,1978). Within the delta, high tide surface salinity (Robertson et al., 1991) is highly variablewith time, especially around spring tides, when it can nearly double its value in a fewdays; even greater fluctuations occur during the daily tidal cycle (Wolanski et al., 1998).Nonetheless, broad gradients of high tide surface salinity across the estuary can be defined(Robertson et al., 1991; Fig. 1).
The presence of the species studied was determined during observations by naked eye orbinoculars, at distances of 2–10 m and between 0830 and 1800 hours (in one case, also atnight). In all cases, the fish movements recorded by observers were well within the consideredplots. In the field, fish size was visually estimated by comparison with objects of known size,
Fig. 2. Selected plots illustrating the ordinal environmental variables measuring the quantity of environmentalwater present in the gobies’ habitats (Table I). In each example, the values of the three variables [vegeta-tion coverage (VC), water bodies (WB) and structural elements (SE)] are in parentheses: (a) unvegetatedmud shoal (1, 4, 1, respectively), (b) mudbanks of a small tidal mouth (1, 1, 2), (c) tide pools onan exposed mudflat (1, 2, 1), (d) undercut with exposed roots along an erosive river bank (1, 1, 6),(e) grasses and bushes on the steep mudbanks of the upper trait of a creek (2, 1, 1), (f) pneumatophorezone (Sonneratia lanceolata) (1, 3, 3), (g) pioneer mangrove forest (S. lanceolata) (3, 3, 4), (h) nypahforest (Nypa fruticans) (5, 3, 5), (i) bottom of an ephemeral inlet during low tide in a freshwater forest(4, 3, 8) and (j) transitional freshwater swamp (6, 3, 7). Oxudercine gobies of the Fly River and delta:(k) Boleophthalmus caeruleomaculatus (female), (l) Oxuderces wirzi, (m) Periophthalmodon freycineti,(n) Periophthalmus darwini, (o) Periophthalmus novaeguineaensis (female), (p) Periophthalmus takita,(q) Periophthalmus weberi (male), (r) P. weberi (female), (s) Scartelaos histophorus (female) and(t) Zappa confluentus. Scale bars: 10 mm.
H A B I TAT A N D A DA P TAT I O N I N M U D S K I P P E R S 1649
such as leaves and sticks. In each plot, environmental conditions and the occurrence of specieswere recorded as presence or absence data.
A reference collection was assembled to check field identifications. Fishes were collectedeither by hand-net or by digging them out of their burrows. Collected specimens were fixed andpreserved in 65–70% ethanol, and two samples were deposited in the Genoa Natural HistoryMuseum and in the Civic Museum of Zoology of Rome (MSNG and MCZR, respectively;Appendix 2). In the laboratory, fishes were measured to the nearest mm.
Only metamorphosed individuals were examined and identified to species level (Murdy,1989; Larson & Takita, 2004; Jaafar & Larson, 2008). To control for possible size or age-related differences in habitat use (Clayton, 1993), two size classes for each species wereanalysed, by utilizing an arbitrary cut-off value: (1) individuals >50% of maximum recordedstandard length (LS), (adults) and (2) individuals <50% of the maximum recorded LS,(young). Records of LS were obtained from Murdy (1989): O. wirzi and B. caeruleomaculatus;Larson & Takita (2004): P. darwini ; Rainboth (1996): S. histophorus; Allen (1991):Z. confluentus; this study (Appendix 2): P. freycineti, P. novaeguineaensis, P. takita andP. weberi.
S PAT I A L A N D T E M P O R A L D I S T R I B U T I O N
Tidal predictions were used to control for the influence of tides on spatial distribution,including possible fish intertidal movements (Gibson, 1999; Zander et al., 1999). Observationswere always made on the exposed substratum and under different tidal conditions: (1) ±2 haround predicted and observed low tide or, when visible, at a distance of >10 m from thewater’s edge (low tide): under these conditions, the fish distribution was assumed to beunaffected by water movement, and (2) near the water’s edge, during flood and ebb tides. Nodata were collected when a plot was influenced by rain or wind (Clayton & Snowden, 2000).
S A L I N I T Y A N D Q UA N T I T Y O F E N V I RO N M E N TA L WAT E R
Surface-water salinity (Sasekumar, 1994) was measured by a hand-held refractometer inwaterways and stagnant pools, in the same plots where the species were found. When no waterbodies were available, salinity was measured in small pools collected in holes dug into theground. To limit the effect of suspended sediments on measurements, droplets were collectedby capillarity from the water surface. Since salinity exhibited particularly high seasonal andtidal variability both at habitat and at ecosystem level, measurements were made in all tidalconditions and a single measurement per plot was made, providing a preliminary assessment ofinterspecific differences of habitat conditions, within the general framework of broad gradientsat ecosystem level (Fig. 1). Readings were categorized into four discrete intervals: Sal1 <1,Sal2 1–5, Sal3 6–10 and Sal4 >10.
Three ordinal variables were used to measure the quantity of environmental water, describ-ing conditions of increasing terrestriality: density of vegetation coverage (VC), water bodies(WB) and structural elements (SE) [Polgar & Crosa, 2009; Fig. 2 (a)–(j) and Table I]. Allthese variables were measured in the same plots where fishes were found, to explore thecorrespondence between species and habitat terrestriality. Therefore, only the data collectedduring low tide were analysed (Polgar & Crosa, 2009). To discriminate between differentVC, the classification of Robertson et al. (1991) was followed. Transitional freshwater forests(freshwater swamps and lowland mixed rain forests) were denser than mangrove associations,due to their higher diversity and dense undergrowth. Vegetation cover limits air movementand reduces evaporation rates, increasing air relative humidity at ground level (Macintosh,1977); six increasing levels of VC were defined (Table I and Fig. 3). WB are hydrogeomorphicand bioturbation structures which contain water. Their size and persistency are determined byweather, tidal influence, wave action and biological activity. Based on size and morphology,four different types of water bodies were defined (Table I and Fig. 3). SE are objects thatincrease substratum heterogeneity at the scale of the studied animals (4–30 cm total length,LT). More heterogeneous substrata have a greater specific surface, thus increasing both airhumidity at ground level and the amount of capillary water. A higher diversity of structuralelements and more complex structures determine higher levels of substratum heterogeneity.
Table I. Quality of environmental water: measured during low tide. Increasing values cor-respond to increasingly terrestrial conditions
Density of vegetation coverage (VC)
1 No vegetation coverage2 Herbaceous and bushy vascular plants3 Lower, pioneer mangrove associations (group IIIa)4 More open and depressed areas in VC5 and VC6 (bottoms of inlets and gulliesb)5 Higher mangrove associations (group I and IIa)6 Transitional freshwater swamps, mixed lowland rainforests
Water bodies (WB)1 Flooded, larger waterways and basins, continuously inundated by tides (<2 m from
the water’s edge)2 Larger tide pools (intertidal bodies of standing water >1 m2)3 Smaller tide pools (<1 m2); smaller, ephemeral waterways emptied by ebb tides
(bottoms of tidal inlets and gulliesb); supratidal freshwater pools4 Animal burrows (only source of water)
Structural elements (SE)1 No structural elements2 Deposits of smaller plant debris: leafs, sticks, fronds (unvegetated banks in front of
the riparian vegetation)3 Pneumatophores (in front of pioneer mangrove forest marine fringes: pneumatophore
zones)4 Pneumatophores, trees, trunks and branches (pioneer mangrove forests)5 Pneumatophores, aerial, prop and other types of roots, trees and heterogeneous plant
debris (higher mangrove forests)6 Undercuts with exposed roots and plant debris (erosive banks of rivers and creeks)7 Trees, bushes, plant debris, litter and peat (freshwater swamps and mixed rainforests)8 Deposits of larger plant debris: build-ups of logs and branches (banks of rivers, creeks
and inlets)
aRobertson et al. (1991).bPolgar (2009).
Eight different combinations of structural elements were recorded, which corresponded toincreasing levels of substratum heterogeneity (Table I and Fig. 3).
DATA A NA LY S I S
Multiple correspondence analysis (MCA) was performed (XLSTAT 7.5.3 Addinsoft; www.xlstat.com) to explore both the correspondence between the environmental variables (obser-vations) relative to the presence of species (modalities) and the degree of association betweendifferent species in the factorial space. MCA (or homogeneity analysis) is an exploratory tech-nique analogous to principal components analysis (PCA) for categorical or ordinal variables(Jobson, 1992). The occurrences of each species in the conditions described by the envi-ronmental variables (presence and absence matrix) were utilized, thus assuming an equallyprobable distribution among different environmental conditions. To support the associationof the species relative to the quantity of environmental water present in their habitats, thesame matrix was analysed by agglomerative hierarchical clustering (AHC: XLSTAT 7.5.3Addinsoft), adopting the Jaccard similarity index and the strong linkage aggregation method(Johnson & Wichern, 1992). Clusters were considered when node similarity values were≥0·70.
H A B I TAT A N D A DA P TAT I O N I N M U D S K I P P E R S 1651
SE8
(a)
(b)
SE6 SE2
SE1
SE1
A
VC6
Mx
un
Pn BgRz Ny AvSn
VC5 VC4 VC5 VC3
SE3WB2 WB1
WL
VC2 VC1
SE3
SE7
WB3 WB4
SE5 SE4
Sea
A
A
Riparian vegetation
River bank
Fig. 3. Measured environmental variables. (a) Diagram of the banks of the Fly River (plan view); movingupriver, increasing energy levels reduced the horizontal extension of unvegetated mudflats at low tideand different sedimentological conditions determined, increasing substratum heterogeneity (structuralelements, SE1–8). Along the intertidal gradient, the abundance and diversity of SE increased from waterto land, along with the density of vegetation (VC1–6). A, transect perpendicular to the water’s edge.(b) Idealized profile along transect A, illustrating the observed intertidal and supratidal zones during lowtide; the complete vegetational zonation was only found on the islands in the northern delta, while highermangrove forests (VC4,5) were not present in the lower Fly area (Fig. 1; sites 1–8); some dominant planttaxa are illustrated (AvSn, Avicennia and Sonneratia spp.; Ny, Nypa fruticans ; Rz, Rhizophora spp.; Bg,Bruguiera spp.; Pn, Pandanus spp.; Mx, Metroxylon sagu); un, undergrowth; WB, water bodies; WL,water level. Drawings are not to scale.
Jack-knife protocol was finally applied to the multivariate datasets to search for influentialobservations (ordinal variables) that could bias the analysis (Gotelli & Ellison, 2004) and tobetter understand their role in the definition of the species associations.
Spreadsheets of presence and absence matrices and descriptive details of the study sitesare available upon request from the first author.
RESULTS
Q UA N T I T Y O F E N V I RO N M E N TA L WAT E R
The investigated ecological transition from water to land occurred along twodifferent types of ecotone along gradients of decreasing tidal influence: (1) fromthe Fly Delta upriver, along the water’s edge, and (2) from the water’s edge tohigher topographic levels (Fig. 3). The horizontal extension of the intertidal zonegradually decreased upriver due to the higher energy of currents and waves, whichcould be inferred from the banks’ steeper profiles; the pioneer mangrove Sonneratialanceolata, well adapted to low salinities, colonized rapidly accreting shores fromPurutu Island (Fig. 1; site 16) up to the northern limits of the study area (Fig. 1;site 6) and was the only mangrove species in the lower Fly River north of Tapila
Fig. 4. Multivariate analyses: (a) multiple correspondence analysis (MCA) of fish species and size classes asmodalities and environmental variables (see Fig. 2) as observations; the two factorial axes F1 and F2explained the highest percentage of variance (in parentheses); the arbitrary dashed ellipses outline speciesgroups corresponding to agglomerative hierarchical clustering (AHC) clusters (dendrogram not shown;node values: A = 0·83; B = 0·88; C = 0·71; D = 0·79; E = 0·72) and associated values of the measuredenvironmental variables. Species are abbreviated with the first three letters of their specific name (seeFig. 2); B.sp, Boleophthalmus sp.; P.sp, Periophthalmus sp.; y-, young; a-, adult; y-dar and y-tak werenever observed; y-B.sp. was not significantly associated with environmental variables in the factorialspace at the level α = 0·05 (in parentheses). The analyses supported six species associations, found inaquatic (A, B), intermediate (C, D), terrestrial (E) and extremely variable conditions (F: including onlyadult Periophthalmus weberi ). , species; , ordinal environmental variables. (b) AHC (cut-off similarityvalue: 0·60) supported four groups of species associated with different salinity categories (numbers inparentheses: Sal 1–4). Group G was associated with Sal1 (0–1); group I with Sal4 (>10); groups Hand J were associated with different salinities, suggesting higher degrees of euryhalinity. Periophthalmustakita was not assigned to any group.
(Fig. 1; site 7). In the islands of the northern delta, wide and rapidly accretingmudflats with lower topographic profiles were colonized by diverse and zoned man-grove associations (‘groups I–III’: Robertson et al., 1991); at higher topographiclevels, mangrove forests had a gradual transition to mixed rain forests and freshwaterswamps [Fig. 3(b)].
In the MCA, the first two factorial axes [Fig. 4(a); F1, F2] accounted for 70·5% oftotal variance; in the factorial space, the fourth quadrant contained the lowest valuesof the environmental variables (i.e. more aquatic conditions: VC1, SE1, WB1); thesecond and third quadrants contained the highest values of the variables (i.e. moreterrestrial conditions: VC4–6, SE5–8, WB4) and some intermediate values (VC2, SE2,3);and the first quadrant contained only intermediate values (VC3, SE4, WB2,3). Exceptfor young Boleophthalmus sp., all the species and size classes were significantlyassociated with the environmental variables in the F1, F2 factorial space (significanttest values at the level α = 0·05, two-tailed test).
Six homogeneous species associations were also supported by the AHC. Group Aincluded young Z. confluentus, and young and adult Pn. freycineti ; group B includedyoung and adult B. caeruleomaculatus, and young and adult O. wirzi ; A and B wereassociated with VC1 and SE1 in the factorial space. These species were found in more
H A B I TAT A N D A DA P TAT I O N I N M U D S K I P P E R S 1653
aquatic habitats, with low spatial heterogeneity and no vegetation coverage (e.g. openmudflats and mudbanks of creeks and rivers without plant debris), always near thewater’s edge. Group C included young Boleophthalmus sp. and adult P. darwini,and was weakly associated with VC1 and SE1. These species were found both inmore aquatic conditions (e.g. open mudflats, mudbanks of creeks) and in higherforested areas but were never found near tide pools. Group D included young andadult S. histophorus, young and adult P. novaeguineaensis, adult Z. confluentus, adultBoleophthalmus sp. and adult P. takita; this group was associated with WB2,3 andweakly associated with VC1,3 and SE1,4 in the factorial space. These species werefound in habitats covered by vegetation and plant debris, but never far from thewater’s edge, such as mudbanks covered with plant debris, pneumatophore zonesand pioneer mangrove forests, and they were frequently found near the water’sedge of pools. Group E included young and adult Periophthalmus sp. and youngP. weberi ; this group was associated with VC3–5 and SE4,5, and weakly associatedwith WB2,4. These species were found in more terrestrial conditions, in habitats withdense vegetation and high substratum heterogeneity and in all conditions of wateravailability (WB1–4). They were found on river banks with plant debris; inside pio-neer mangrove forests, on the bottom of ephemeral waterways in forested areas andinside dense stands of nypah palms (Nypa fruticans). Young P. weberi were alsofound among build-ups of coarse plant debris (SE8). Finally, group F included onlyadult P. weberi, which was associated with WB1,4, SE2,6–8 and VC2,6. These fisheswere found in a wide range of conditions, almost throughout the ecological gradientsstudied: from mudbanks of creeks covered only by plant debris, to deforested areascovered by shrubs and grasses, to higher mangrove forests. They were also found inhabitats where no other amphibious goby was found, such as transitional freshwaterswamps, floating build-ups of logs in the upper tract of creeks and undercuts alongerosive banks. They were found in all conditions of water availability, except nearlarger tide pools.
Compared to the adults, young Z. confluentus were found in more aquatic condi-tions during low tide, densely aggregated near the water’s edge (VC1, SE1, WB1). Onthe contrary, young Boleophthalmus sp. were found also in more terrestrial condi-tions (VC4,5, SE5). No relevant differences were observed between young and adultsof other species. Young of P. takita and P. darwini were never observed.
Jack-knifing of VC1,3,4, WB1–3 and SE1–5 (similarity cut-off value ≥0·70) changedthe species associations mainly due to changes in the relative position of adultP. darwini and young Boleophthalmus sp. in the factorial space [Fig. 4(a)]. Changesincluded losses of group C, fusions of group B with groups A or D, inclusions ofadult P. darwini in group D, B or A, of young Boleophthalmus sp. in group B andof adult P. freycineti in B. Jack-knifing of whole variables (VC, WB and SE) resultedin the same type of changes.
During flood and ebb tides, near the water’s edge, adult and young P. weberi andadult P. darwini, P. novaeguineaensis and Periophthalmus sp. were found in moreaquatic conditions (e.g. SE1, WB1). Instead, during low tide these species were alsofound at considerable distance from the water’s edge.
In a second analysis [Fig. 4(b)], the correspondence between species occurrenceand salinity was explored. Since in this case MCA modalities were more numerousthan observations, only AHC was performed. Salinities of zero were recorded inall plots from Tapila upriver (Fig. 1). Only three groups of species and size classeswere associated with a single salinity category: G (Z. confluentus: Sal1), I (O. wirziand young B. caeruleomaculatus: Sal4) and P. takita (Sal3); nonetheless, this lastspecies was only found in two plots (Fig. 1; sites 13, 16); therefore, it was notincluded in any group. Groups H and J were found in variable conditions; group H(node similarity 0·68) was related to group G, and group J (node similarity 0·66)was related to group I.
Jack-knifing of all variable values resulted in changes of the associations (simi-larity cut-off value ≥0·60), with losses of either G or I; fusions of groups G and H;I and J, or partial fusions of H and J.
DISCUSSION
Two oxudercine species previously reported from Papua New Guinea, Perioph-thalmus argentilineatus Valenciennes and Periophthalmus kalolo Lesson were notfound in this study (Roberts, 1978; Murdy, 1989; Allen, 1991; Kailola, 1991).
The five groups of species associated with different quantities of environmen-tal water can be considered as ecological guilds living in habitats with differentdegrees of terrestriality. The changes resulting from jack-knifing of 11 out of 18environmental variables were determined by the intermediate position of groups Band C in the factorial space, which were associated with diverse environmentalconditions.
The observations made during flood and ebb tides suggest that P. weberi,P. darwini, P. novaeguineaensis and Periophthalmus sp. performed intertidal move-ments (Gibson, 1999), moving away from the water during the flood tide, and waitingfor the ebb tide near the water’s edge, a behaviour known in other congeneric species(Colombini et al., 1995: Periophthalmus sobrinus, junior syn. = P. argentilineatus).
Habitat differentiation among species determined spatial partitioning along the twoobserved ecological transitions (Fig. 3). In particular, only two species were foundin the lower Fly River (Fig. 1; sites 1–8): P. weberi (the only oxudercine speciesfound in site 6) and Z. confluentus. The observed distributional limits of these twospecies in the lower Fly River match the observations of Roberts (1978: sites 28and 31). In the delta, Periophthalmus spp. were found at all intertidal levels, whilethe species of the genera Boleophthalmus and Scartelaos were found at middle andlower intertidal levels. Zappa confluentus, O. wirzi and Pn. freycineti were foundonly at lower intertidal levels. Noticeably, P. weberi was found at all the surveyedtopographic levels in the lower Fly River and at middle and higher levels in thedelta, being also found in extremely terrestrial conditions, in a transitional freshwaterswamp (Purutu Island).
In a comparison between ecological and phylogenetic categories (Fig. 5),Periophthalmus sp. and young P. weberi were found in more terrestrial condi-tions (group E), and adult P. weberi in a range of conditions (F), including the
H A B I TAT A N D A DA P TAT I O N I N M U D S K I P P E R S 1655
Periophthalmus C,D,E,F–H,J
B,C,D–H,I,J
A–H
D–J
B–I
A,D–G
Periophthalmodon
Boleophthalmus
Scartelaos
Zappa
Pseudapocryptes
Apocryptes
Apocryptodon
Oxuderces
Parapocryptes
Evorthodus
Fig. 5. Dendrogram of the Oxudercinae (Murdy, 1989). The tree was rooted with the genus Evorthodus(E. lyricus, Gobiidae: Gobionellinae), a hypothetical sister group of the Oxudercinae (Murdy, 1989).The genus Oxuderces is included in the tribe Oxudercini; in this study, all other genera are included inthe tribe Periophthalmini (Murdy, 1989). For each genus studied, its presence in one or more guilds withrespect to habitat terrestriality–salinity is indicated (A–F and G–J; see also Fig. 4). If a sequential asso-ciation with increasingly terrestrial habitats at each cladogenetic event is assumed within Periophthalmini,several reversals should have occurred (underlined letters).
most terrestrial ones observed (SE8, VC6 and WB4). Nonetheless, Pn. freycineti (sis-ter genus of Periophthalmus) and several other species of Periophthalmus werealso present in more aquatic or intermediate conditions (groups A, C and D). Themore basal O. wirzi was found in more aquatic conditions (group B), and therelatively more derived Z. confluentus was found both in aquatic and intermediateconditions (groups A and D). Nonetheless, there was neither an increase of terres-triality from Z. confluentus to S. histophorus (group D) nor from S. histophorus toBoleophthalmus spp. In fact, young and adult B. caeruleomaculatus were found inmore aquatic conditions (group B).
The hypothesis of an increase in adaptation to the terrestrial environment at eachcladogenetic event at generic level would imply the correspondence between speciesof more derived genera and increasingly terrestrial habitats. Rather, the presentresults suggest the presence of parallel adaptive radiations to semi-terrestrial habi-tats within each genus. In this perspective, the adaptive radiation of Periophthalmusspp. apparently was the most successful, with species found in a wide range ofhabitats, from semi-aquatic to semi-terrestrial conditions. Studies made in differentregions described species found in even more aquatic conditions than observed inthis study (i.e. open tidal mudflats), such as Periophthalmus chrysospilos Bleeker(Takita et al., 1999; Polgar & Crosa, 2009) or Periophthalmus modestus Cantor(Baeck et al., 2008).
Alternative explanations to parallel evolution would either imply the presence ofseveral reversals of habitat use within the genera Periophthalmus, Periophthalmodon
Fig. 6. Dermal cups below orbits in Zappa confluentus : the pin indicates the position of the dermal cup asillustrated in a freshly dead specimen of Z. confluentus [Genoa Museum of Natural History, Genoa, Italy(MSNG) 54688B]. Scale bar is 5 mm.
and Boleophthalmus (Fig. 5), or the incapacity of indirect multivariate measures ofhabitat terrestriality to detect either behavioural species-specific differences in habitatuse (Polgar & Crosa, 2009), or selection at microhabitat level, indicating differentdegrees of adaptation to terrestriality.
With the exception of O. wirzi, all the observed species exhibited fully amphibi-ous behaviours. In this respect, it is worth noting that Roberts (1978) describedZ. confluentus as definitely less terrestrial than observed in the present study. Murdy(1989) utilized these eco-ethological observations in his cladistic analysis, thus con-sidering Zappa (a monotypic genus), as the sister taxon of the mudskippers; i.e.oxudercine gobies that are fully terrestrial for some portion of the daily cycle (Murdy,1989). Murdy (1989) also did not find suborbital dermal cups in Z. confluentus, asynapomorphy of mudskipper genera. Nonetheless, in the present study, both subor-bital dermal cups in freshly dead specimens (Fig. 6) and the characteristic periodicretraction of the eyes beneath these cups (blinking) in live specimens were observed.
The four associations based on salinity categories provided a preliminary assess-ment of the differentiation of the studied species along an environmental gradientof salinity. Most species occurred in variable salinity conditions [Fig. 4(b); groupsH, J], confirming previous physiological observations of several Periophthalmus,Periophthalmodon and Boleophthalmus spp., that are known to rapidly adapt tosalinity changes (Clayton, 1993; Evans et al., 1999; Sakamoto & Ando, 2002) andextending this trait to S. histophorus.
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The adaptation of Z. confluentus to freshwater habitats is probably secondary(Allen, 1991; this study). In this case, by out-group comparison the phylogeneticconsensus would suggest that the most recent common ancestor of the tribe Perio-phthalmini already lived in brackish waters (Fig. 5; groups G–J). Therefore, if amarine origin of oxudercine gobies is assumed, the more saline conditions whereO. wirzi was found (Fig. 4; group I) would suggest a plesiomorphic trait.
In fact, the evolution of more amphibious lifestyles in Scartelaos, Boleophthalmus,Periophthalmodon and Periophthalmus spp. would have been reasonably facilitatedby euryhalinity, as a preadaptation to cope with the osmoregulatory stress resultingeither from evaporative water loss or contact with freshwater microhabitats, duringterrestrial surveys (Evans et al., 1999; Sayer, 2005).
The occurrence of only P. weberi and Z. confluentus in the lower Fly Rivermay be determined by different optimal average salinities among different species.Alternatively, the observed differential distribution may be explained by the higherenvironmental energy of fluvial relative to deltaic habitats. Excessive energy maydetermine unsuitable habitat conditions for the adults or prevent efficient settlementof planktonic larvae (Chen et al., 2008), limiting the access to these environmentsto few species with peculiar adaptations.
Trying to understand the eco-evolutionary processes leading to the colonizationof more terrestrial habitats in this group, it is worth noting that the species that wasfound in the most terrestrial conditions (P. weberi ) was also found in the widestrange of environmental conditions. This would suggest that at least in this case, thecolonization of extreme semi-terrestrial and freshwater habitats was facilitated byeurytypy.
Oxudercine communities are typically found on vegetated or exposed tidal mud-flats (Clayton, 1985; Takita et al., 1999; Polgar & Crosa, 2009). Wide intertidal zoneswith low topographic profiles apparently offered diverse potential ecological nichesand facilitated adaptive radiations during the evolutionary history of this group. Eury-halinity apparently was an early key adaptation evolved in intertidal conditions andmay have facilitated the evolution of amphibious lifestyles and the exploitation ofhighly dynamic semi-terrestrial habitats.
Oxudercine gobies were also proposed as convergent eco-evolutionary models(Schultze, 1999) in an attempt to understand the environmental conditions andselective forces that drove the evolution of amphibious lifestyles in Devonian semi-aquatic tetrapods (385–365 million years ago). The sedimentological and geomor-phic settings of middle and late Devonian tide-dominated deltas and lower fluvialsystems were being shaped by the explosive land colonization of vascular plants,forming the first wide and gently sloping deposits of fine and highly organic sedi-ments, giving birth to modern transitional ecosystems (Retallack, 1997; Algeo et al.,2001). Several palaeo-environmental studies showed that key stages of the middleand late Devonian vertebrate transition took place in alluvial or tide-dominated set-tings (Thomson, 1980; Alekseev et al., 1994; Luksevics & Zupins, 2004; Clack,2006, 2007; Daeschler et al., 2006; Niedzwiedzki et al., 2010). By analogy withoxudercine gobies, this transition would have been realised by highly eurytypic andeuryhaline species. In this respect, this study may offer a new perspective on theage-old debate about the freshwater v. seawater origin of terrestriality (Romer, 1967;Graham, 1997; Schultze, 1999; Clack, 2002).
We wish to thank Ok Tedi Mining Limited (OTML) for air and water transportation, andlaboratory facilities; in particular, thanks to the OTML Environment Department and to thecaptain and crew of the R.V. Tahua Chief. A very special thanks goes to C. Tenakenai andhis team of the Sturt station and to M. T. Rau for their hospitality in Tabubil and theirinvaluable assistance in the field. Thanks also to the people of the Fly Delta, and in particularto David and Agua, and the new and old Wapi villages. Thanks to G. Crosa, Universityof Insubria, Italy, J. A. Clack, University Museum of Zoology, Cambridge, U.K., S. Milli,Sapienza University of Rome, Italy, and to two anonymous referees for manuscript revision.This study was partially funded by a PhD grant in Ecological Sciences provided by SapienzaUniversity of Rome.
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Electronic References
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APPENDIX 1. DESCRIPTION OF SITES AND PLOTS
Site 1 (8◦ 9′ 28·1′′ S; 142◦16′ 31·5′′ E), northern bank of the Lower Fly, in front ofSturt I: plot St01, river bank colonized by sparse trees of Sonneratia lanceolata,open areas near tide pools; plot St02, small creek mouth (<5 m wide) withsoft mudbanks; plot St03, build-up and floating vegetal debris in the upper tractof the creek; plot St04, ephemeral inlet (creek tributary), crossing a freshwaterforest; plot St06, river bank: patches of mud of several m2 near the water’s edge,only a few cm thick, with mixed sediments below; plot St07, same area of St01:among roots, build-up of vegetal debris and pneumatophores.
Site 2 (8◦ 9′ 42·6′′ S; 142◦ 16′ 12·1′′ E), northern coast of Sturt Island: plot St05,soft mudbanks of a small creek (<3 m wide).
Site 3 (8◦ 12′ 24·1′′ S; 142◦ 11′ 6·3′′ E), northern bank of the lower Fly: plot Lf01,erosive bank of an islet covered by a young forest of S. lanceolata.
Site 4 (8◦ 13′ 1·4′′ S; 142◦ 8′ 14·1′′ E), northern bank of the lower Fly: plot Lf02,depositing bank with abundant vegetal debris and riparian vegetation.
Site 5 (80◦ 12′ 32·7′′ S; 142◦ 6′ 20·1′′ E), lower Fly: plot Lf03, islet with very softmudbanks and no vegetation coverage.
Site 6 (7◦ 56′ 10·7′′ S; 141◦ 49′ 41·5′′ E), Suki River: plot Su01, vegetated mud-banks of a channel in a Sago (Metroxylon sagu) plantation.
Site 7 (8◦ 25′ 16·7′′ S; 142◦ 55′ 53·4′′ E), southern bank of the lower Fly, Tapilavillage: plots Tp01, pneumatophore zone of a belt of S. lanceolata: patches ofexposed mud within thick grass meadows; plot Tp02, mudbanks of a tidal mouthnear the Tapila village; plot Tp03, mudbank of a small creek crossing the village,densely vegetated and with abundant vegetal debris; plot Tp08, open mudflat infront of the village.
Site 8 (8◦ 20′ 39·9′′ S; 142◦ 55′ 59·8′′ E), northern bank of the lower Fly, isletin front of Tapila: plot Tp04, soft mudbanks of a run-off channel with sparseherbaceous vegetation; plot Tp05, mudbanks of another run-off channel; plotTp06, small mudflat (<10 m wide) crossed by tidal inlets, bordered by grassesand mangrove saplings (S. lanceolata); plot Tp07, erosive step and undercutwith exposed roots and grasses (c. 1 m high), separating the mudflat from thefreshwater forest.
Site 9 (8◦ 19′ 57·7′′ S; 143◦ 27′ 43·1′′ E), Wariura Island, south coast: plot Wa01,small mudflat (<10 m wide), in front of a pneumatophore zone of S. lanceolata;plot Wa02, pneumatophore zone of S. lanceolata.
Site 10 (8◦ 23′ 40·1′′ S; 143◦ 31′ 1·5′′ E), Purutu Island, upper tract of the WapiCreek: plot Pu01, steep, vegetated mudbanks, near the water’s edge; Pu02, asin Pu01, but on top of the mudbanks; plot Pu03, sloping soft mudbanks, nearthe water’s edge; plot Pu04, banks of lateral inlets running into the creek.
Site 11 (8◦ 23′ 21·0′′ S; 143◦ 31′ 23·4′′ E), Purutu Island, middle tract of the WapiCreek: plot Pu05, sloping soft mudbanks, near the water’s edge; plot Pu06, banksof lateral inlets running into the creek.
Site 12 (8◦ 21′ 54·93′′ S; 143◦ 32′ 52·43′′ E), Purutu Island, lower tract of the WapiCreek: plot Pu07, sloping soft mudbanks, near the water’s edge.
Site 13 (8◦ 25′ 45·7′′ S; 143◦ 36′ 24·0′′ E), Sisikura Island: plots Sk01 and Sk03,mudflat, in front of a pneumatophore zone of Sonneratia alba; plot Sk02, openmudflat, near the water’s edge.
Site 14 (8◦ 25′ 47·33′′ S; 143◦ 26′ 20·79′′ E), Purutu Island, mouth of the PurutuChannel: plot Pu08, upper zone of a sloping bank with mixed sediments, coveredby bushes of Acanthus sp.; plot Pu09, cleared area in front of the forest, neara pile of cut trees and fronds; plot Pu10, northern bank, small mudflat (<10 mwide at low tide); plot Pu11, southern bank, wide open mudflat (>50 m wideat low tide); plot Pu12, open mudflat, near the water’s edge.
Site 15 (8◦ 25′ 31·80′′ S; 143◦ 25′ 10·61′′ E), Purutu Island, southern coast: plotPu13, dense nypah forest; plot Pu14, soft mudbanks of a tidal mouth.
Site 16 (8◦ 25′ 36·29′′ S; 143◦ 25′ 38·49′′ E), Purutu Island, linear transect (240 m),perpendicular to the banks of Purutu Channel: plot Pu15, open mudflat; plotPu16, pioneer forest (S. lanceolata and grasses); plot Pu17, as in Pu16, but withsparse young nypah palms (N. fruticans); plot Pu18, marine fringe of the nypahforest; plot Pu19 and Pu20, dense nypah forest crossed by ephemeral inlets.
H A B I TAT A N D A DA P TAT I O N I N M U D S K I P P E R S 1663
Site 17 (8◦ 25′ 45·12′′ S; 143◦ 32′ 10·79′′ E), Purutu Island, linear transect(c. 2·5 km) from the banks of Purutu Channel to the centre of the island: plotPu21, mudbanks of the Purutu Channel, near the water’s edge; plot Pu22, densenypah forest; plot Pu23, transition from the freshwater forest to the peat swampforest.
APPENDIX 2. REFERENCE COLLECTION AND MUSEUM MATERIALEXAMINED
Boleophthalmus birdsongi Murdy, 1989: eight paratypes from three localities,Australia, Northern Territory: north-east of Darbilla Creek (Millingimbi); MangroveCreek (Gunn Point); mouth of the Elizabeth River, East Arm (Darwin); size range60–108 mm standard length (LS): NTM S.11362-032, 4 (73–108 mm LS), DarbillaCreek, 1984; NTM S.10694-006, 2 (60, 81 mm LS), Mangrove Creek, 1982; NTMS.10421-001, 2 (100, 103 mm LS), Elizabeth River, 1987.
Boleophthalmus caeruleomaculatus McCulloch & Waite, 1918: five specimensfrom two localities, Papua New Guinea, Western Province: Sisikura Island (FlyDelta); Australia, Northern Territory: Adelaide River; size range 106–162 mm LS:MCZRVP1016 (145 mm LS, female) and MCZRVP1017 (136 mm LS, male), Sisi-kura Island, 24 September 2007; MSNG 54689, 2 (134 mm LS, male; 106 mm LS,female), Sisikura Island, ibid.; AMS I.14325 (paratype: 162 mm LS, male), AdelaideRiver, 1917.
Oxuderces wirzi (Koumans, 1938): four specimens from one locality, Papua NewGuinea, Western Province: Purutu Channel (Purutu Island, Fly Delta); size range42–49 mm LS: MCZRVP1006 (49 mm LS); and MCZRVP1007 (48 mm LS), 29September 2007, MSNG 54960, 2 (42, 48 mm LS, fixed and preserved in 99%ethanol), ibid.
Periophthalmodon freycineti (Quoy & Gaimard, 1824): five specimens from threelocalities, Papua New Guinea, Western Province: Wapi Creek (Purutu Island, FlyDelta), Toro Pass (southern Fly Delta); Australia, Northern Territory: Ten Inch Creek(Wildman River); size range 77–247 mm LS: MCZRVP1018 (146 mm LS, female)and MCZRVP1019 (158 mm LS, female), Toro Pass, 21 April 2006; MSNG 54691,2 (A: 128, B: 77 mm LS), Wapi Creek, 24 September 2007; NTM S.15545-001(247 mm LS), Ten Inch Creek, 2001.
Periophthalmus darwini Larson & Takita, 2004: eight specimens from three local-ities, Papua New Guinea, Western Province: Wapi Creek (Purutu Island, Fly Delta);Australia, Northern Territory: Micket Creek (Shoal Bay); and beach south of Picher-taramoor (Melville Island); size range 32–45 mm LS: MCZRVP1012 (35 mm LS)
and MCZRVP1013 (35 mm LS), Wapi Creek, 24 September 2007; MSNG 54692,4 (32–39 mm LS), Wapi Creek, ibid.; NTM S.10554-004 (holotype: 45 mm LS),Micket Creek, 1982; NTM S.14400-006 (paratype: 38 mm LS female), Picher-taramoor, 1996.
Periophthalmus novaeguineaensis Eggert, 1935:12 specimens from three locali-ties, Papua New Guinea, Western Province: Purutu Channel and Wapi Creek (PurutuIsland, Fly Delta); Australia, Northern Territory: Adelaide River (Boustead’s barra-mundi farm); size range 36–53 mm LS: MCZRP1003 (51 mm LS, female), MCZR
P1004 (49 mm LS, male) and MCZRP1005 (41 mm LS, female), Purutu Chan-nel, 29 September 2007; MSNG 54693 (53 mm LS), Wapi Creek, 24 September2007; MSNG 54694, 3 (37–47 mm LS), Wapi Creek, ibid.; NTM S.11193-004, five(paratypes of Periophthalmus murdyi Larson & Takita, 2004:36–39 mm LS, fourfemales, one male), Adelaide River, 1993.
Periophthalmus takita Jaafar & Larson, 2008: six specimens from four localities,Papua New Guinea, Western Province: Purutu Channel, Sisikura Island (Fly Delta);Australia, Northern Territory: southern end of Field Island (mouth of South AlligatorRiver); Australia Queensland: Port Clinton (64 km N of Rockhampton); size range:46–71: MCZRVP1002 (49 mm LS), Purutu Channel, 29 September 2007; MSNG54695 (63 mm LS), Sisikura Island, 24 September 2007; MSNG 54696 (71 mm LS),Purutu Channel, ibid.; NTM S.14637-032 (61 mm LS), Field Island, 1998; aAMSI.34341-028 (46 mm LS), Port Clinton, 1993.
Periophthalmus weberi Eggert, 1935: six specimens from four localities, PapuaNew Guinea, Western Province: lower Fly River, Suki, Sturt Island and PurutuChannel (lower Fly River and delta); size range 39–85 mm LS: MCZRVP1011(61 mm LS, male), lower Fly River, 18 September 2007; MSNG 54682 (85 mmLS, male), Suki, ibid.; MSNG 54683, 2 (60 mm LS, male; 52 mm LS, female), SturtIsland, 19 September, 2007; MSNG 54684, 2 (39 mm LS, male; 53 mm LS, female),Purutu Channel, 29 September 2007.
Scartelaos histophorus (Valenciennes, 1837): seven specimens from three local-ities, Papua New Guinea, Western Province: Sisikura Island and Purutu Channel(Fly Delta); Malaysia, Selangor: Morib; size range 38–104 mm LS: MCZRVP1020(104 mm LS) and MCZRVP1021 (67 mm LS), Sisikura Island, 24 September, 2007;MSNG 54685, 2 (male: 76 mm LS; female: 70 mm LS), Sisikura Island, ibid.;MSNG 54686, 2 (38, 43 mm LS), Purutu Channel, 29 September 2007; MSNG54645 (62 mm LS), Morib, 2007.
Zappa confluentus (Roberts, 1978): 10 specimens from two localities, Papua NewGuinea, Western Province (lower Fly River): mainland in front of Sturt Island (near‘site 30’: Roberts, 1978), at a linear distance of c. 95 km from Tapila upriver; andMadiri (‘site 31’: Roberts, 1978); size range 23–60 mm LS: MCZRVP1014 (29 mmLS) and MCZRVP1015 (23 mm LS), Sturt Island, 17 September 2007; MSNG54687, 2 (A: 34, B: 32 mm LS, fixed and preserved in 99% ethanol), Sturt Island,ibid.; MSNG 54688, 2 (A: 60, B: 39 mm LS), Sturt Island, ibid.; aAMS I.21482-002 (formerly USNM 217952, holotype: 34 mm LS), Madiri, 1975; aUSNM 217305(paratype: 44 mm LS), Sturt Island (‘site 30’), ibid.; aUSNM 217306, 2 (paratypes:31, 36 mm LS), Madiri, ibid.
NTM, Museum and Art Gallery of the Northern Territory, Darwin, Australia;MCZR, Civic Museum of Zoology of Rome, Rome, Italy; MSNG, Genoa Museumof Natural History, Genoa, Italy. If not otherwise specified, all specimens depositedin the MCZR and MSNG were fixed and preserved in 65–70% undenatured ethanol.aThese specimens were examined as high-resolution digital photos and measuredby MVH (measuring vegetation health) image v.8 (Museum of Science, Boston;http://mvh.sr.unh.edu/mvhinvestigations/false color.htm).
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