Environ Biol Fish (2012) 94:579–590 DOI 10.1007/s10641-011-9964-2 Ontogenetic shifts in the habitat associations of butterflyfishes (F Chaetodontidae) Nicholas J Clark & Garry R Russ Received: 20 April 2011 / Accepted: November 2011 / Published online: 18 January 2012 # Springer Science+Business Media B.V 2012 Abstract The habitat associations of species are vital in determining an organism’s vulnerability to environmental and anthropogenic stress In the marine environment, post-settlement processes such as ontogenetic shifts in habitat use can affect this vulnerability by subjecting a species to differing biological and environmental conditions at various life stages This study documents the habitat associations of adult and juvenile butterflyfishes on an inshore reef of the Great Barrier Reef (GBR) to investigate if ontogenetic shifts in habitat use occur, and if such shifts relate to the trophic ecologies of species Coral-feeding species displayed highly concordant distributions among adults and juveniles In contrast, adults and juveniles of species with wider dietary selectivities (generalists) displayed significantly different distributions across reef zones Juvenile generalist feeders were limited to the shallow, patchy areas of the reef flat whilst adult conspecifics displayed comparatively wide distributions Butterflyfishes with a heavy reliance on corals for food appear to settle preferentially in areas with high abundances of adult conspecifics, which may partially explain why coral specialists are more vulnerable to localized depletion events In contrast, generalist species utilize distinct habitats as adults and N J Clark (*) : G R Russ School of Marine & Tropical Biology and the ARC Centre for Coral Reef Studies, James Cook University, Townsville QLD 4811, Australia e-mail: nicholas.clark@my.jcu.edu.au juveniles, suggesting that generalist butterflyfishes expand their ranges and are therefore subjected to changing environmental conditions as they reach adulthood Keywords Habitat association Ontogeny Abundance Coral reef Butterflyfish Chaetodontidae Introduction The larvae of coral reef fishes utilize a suite of sensory cues to settle into specific regions of the reef (Stobutzki 1998; Leis and Carson-Ewart 2003), areas that may differ from habitats occupied by adult conspecifics (Mumby 2006) Recruits and juveniles of reef fish often utilise distinct habitats compared to adults (Jones et al 2010) and thus each life-stage may be subject to different ecological and environmental influences Moreover, alterations to benthic composition and complexity, for example coral bleaching events (Graham et al 2009), may modify recruitment patterns (Moore and Elmendorf 2006; Feary et al 2007) Thus, post-settlement processes, such as ontogenetic shifts in habitat use, may influence a species’ vulnerability to stress Therefore, we can better understand how disturbances may affect reef fish population dynamics by determining the habitat associations of vulnerable species Butterflyfishes (Family Chaetodontidae) are a conspicuous, diverse group of fishes that exhibit 580 strong associations with coral reefs (Pratchett et al 2008b) The heavy reliance of these fish on coral reefs is due to an abundance of coral-feeding species, with butterflyfishes making up 61% of all corallivorous fishes (Bellwood et al 2010) Moreover, several species exhibit considerable feeding selectivity, preferentially feeding on only a few species of coral (Pratchett 2007) despite relatively wide geographic distributions (Allen et al 2003; Froese and Pauly 2008) Consequently, butterflyfishes often show marked decreases in abundance following disturbance to coral reefs (Jones et al 2004; Pratchett et al 2006) Lower abundances could in turn lead to reduced larval production and decreased recruitment (Donelson et al 2008), exacerbating population declines Given their strong ties to reefs and high vulnerability to disturbance (Wilson et al 2006; Pratchett et al 2008a), butterflyfishes are a model study group to explore ontogenetic variation in habitat association on coral reefs The habitat associations of butterflyfishes indicate a heavy reliance on living corals as adults and variable associations with coral as juveniles (Harmelin-Vivien 1989; Pratchett et al 2008b) This suggests that some species of butterflyfish may display ontogenetic shifts in habitat In addition to ontogenetic shifts in habitat association, the distributions of juvenile reef fishes may also be strongly regulated by both interand intra-specific competition (e.g., Munday 2001) For instance, in a study conducted at Lizard Island on the mid shelf of the Great Barrier Reef (GBR), Berumen and Pratchett (2006) found that dominant butterflyfish competitors such as Chaetodon baronessa aggressively defended territories against both conspecifics and subordinate species and increased their territory sizes as abundance of coral prey declined This propensity for aggression, particularly against conspecifics, may directly influence the settlement preferences and spatial distributions of juveniles Therefore, some recruits may be forced to settle into sub-optimal habitats due to antagonistic interactions with adults (e.g., Munday 2001) In particular, competition among coral feeders may result in intraspecific spatial partitioning in areas with relatively low cover of commonly preferred Acropora and Pocillopora corals, such as the inshore reefs of the GBR (Emslie et al 2010) Therefore, the objective of this study was to document the distributions and habitat associations of adult and juvenile butterflyfishes on inshore fringing reefs of the GBR It was predicted Environ Biol Fish (2012) 94:579–590 that coral-feeding butterflyfishes would display ontogenetic variation in habitat association in response to low prey availability For generalist feeders, which exhibit higher dietary versatilities than coral feeders (Pratchett 2005), we also predicted an ontogenetic shift in habitat association Generalist feeders expand their range of prey items as they reach adulthood (Harmelin-Vivien 1989), which has been suggested to result in an expansion in habitat use upon maturity (Pratchett et al 2008b) Methods Study sites This study was conducted in September and October 2010 in the Palm Islands (18˚34′S, 146˚29′E) on the inshore GBR (Fig 1) The Palm Island group consists of nine islands located approximately 15 km off the mainland Surveys were made at three levels of exposure to winds and currents (sheltered, obliquely exposed, and exposed; Fig 1) to investigate if exposure affected coral and butterflyfish communities (following Pratchett et al 2008b) The degree of exposure was determined according to multiple observations of surge, wind speed, and the overall direction of currents during the study Sites with full protection from prevailing winds were considered sheltered, sites in which the reef faced parallel to oncoming surge and currents were considered obliquely exposed, and sites that faced directly into surge, currents, and prevailing winds were considered exposed The fringing reefs of the Palm Islands have an extensive shallow reef flat and mild reef slope gradient at sheltered sites, and a relatively narrow reef flat and steeply sloping reef wall at exposed sites However, despite the variation in gradients of the reef slope between exposed and sheltered sites, the physiognomic reef zones of flat, crest, and slope are typically distinguishable at each location At all locations, the reef flat has patchy coral cover and extensive areas of rubble, sand, and algae-covered rock In contrast, the reef crest and reef slope are relatively rugose areas consisting of large bommies (coral heads) and crevasses In general, the study sites are characterized by high abundances of Alcyoniid soft corals and scleractinian corals belonging to the family Poritidae (Emslie et al 2010) Environ Biol Fish (2012) 94:579–590 581 Fig Map of sampling sites within the Palm Islands on the inshore Great Barrier Reef N Pelorus sheltered sites obliquely exposed sites exposed sites Prevailing wind direction Australia Orpheus Curacoa km Surveys Twenty-seven sites were surveyed for butterflyfish abundance and benthic cover (Fig 1) Butterflyfish abundance was estimated by underwater visual census (UVC) along 50 m transects using a combination of SCUBA and snorkel Surveys were made in the three reef zones (flat, crest, and slope), as coral reef fishes often occur in assemblages that are characteristic of each physiognomic zone (Russ 1984a, b) Study sites were chosen to be relatively well-spread around the coasts of Pelorus, Curacao and northern Orpheus Islands (Fig 1) To maintain safe dive practice, study sites were selected daily at sea based on weather conditions Transects were delineated by a 50 m fibreglass tape laid parallel to the reef crest in each of the three reef zones, with depths ranging from 1–2 m along the flat and crest and from 4–10 m along the slope The first observer counted butterflyfish within m either side of their body while simultaneously laying the transect tape Individual butterflyfish were visually placed into one of three size classes [10 cm total length (TL)] corresponding to the life-stage categories of new recruit, juvenile, and adult (following Fowler 1990 and Pratchett et al 2008b) Size estimations were checked periodically underwater using a ruler printed on the back of the datasheets Benthic composition was measured by a second observer This permitted investigation of butterflyfish habitat associations Live coral cover was estimated using a variation of the line point intercept technique (Lam et al 2006) A total of 100 randomly placed points on the 50 m transect tape were sampled and recorded into one of six categories (table Acropora, staghorn Acropora, Pocillopora, Porites, other hard coral, and soft coral) The sample points were placed on the tape using a randomly generated number table prior to the survey period Three replicate transects were surveyed in each zone at each site, yielding a total of 243 transects across the 27 sites and a survey area of 24 300 m2 Analysis Coral cover was analysed with an analysis of variance (ANOVA) to investigate if variation in butterflyfish abundance was related to spatial variation in coral cover To test for variations in the distributions of adult and juvenile butterflyfish conspecifics, a series of 3-factor multivariate analyses of variance (MANOVA) were implemented Prior to analysis, coral cover data and butterflyfish abundance data were pooled at the site level and standardised by area surveyed Butterflyfish abundances were also pooled by trophic guild (i.e hard coralfeeders, soft coral-feeders, or generalists) to investigate the role of trophic guild in determining ontogenetic variation in habitat association All analyses of variance were tested using a 3-factor orthogonal model, with island (random), exposure (fixed), and reef zone (fixed) included as the test variables Butterflyfish abundance data were square-root transformed and benthic cover data were arcsine-root transformed to meet (M)ANOVA assumptions of normality, sphericity and homoscedasticity of variance Tukey’s HSD post-hoc tests were used to identify homogenous groups following all analyses of variance Rather than performing correlations between 582 Environ Biol Fish (2012) 94:579–590 Results juvenile butterflyfish Obligate hard-coral feeders were the most abundant trophic guild, accounting for 60.7% of individuals Generalist and soft-coral feeders accounted for the remaining 39.3% Due to the relatively low numbers of juveniles recorded for several species, only the six most abundant species (Chaetodon aureofasciatus, C rainfordi, C melannotus, C lunulatus, C vagabundus, and Chelmon rostratus; 91.5% and 87.9% of juvenile and adult recordings, respectively) were included in the PCA The butterflyfish assemblage Benthic composition A total of 1409 individual butterflyfish were recorded on the 243 transects The majority of individuals recorded were adults or juveniles (Table 1) Recent recruits were rare (except for C aureofasciatus, accounting for 48 of 50 total recruits) Thus, this study only quantifies habitat associations of adult and Among the 27 study sites, mean scleractinian (hard) coral cover was 17.4±1.3% In addition, hard coral cover was variable among reef zones (Fig 2) However, this variation was not statistically significant (ANOVA, Table 2) Most hard corals belonged to the ‘other hard corals’ category (mean 8.5±1.6%; Fig 2) Corals butterflyfish and coral taxa, a principal components analysis (PCA) was used to display variation in the community structure of both butterflyfish and corals The analysis was performed using the correlation matrix generated from the transformed butterflyfish and benthic cover data Statistical analyses were performed using Statistica 10.0 (www.statsoft.com) Table Total abundances of butterflyfish (displayed by size class) within the Palm Islands Totals are derived from 243 transects (HC), hard-coral feeder; (SC), soft-coral feeder; (G), generalist feeder Orpheus Island Adults Pelorus Island Juveniles Adults Curaoa Island Juveniles Adults Juveniles Total abundance Chaetodon aureofasciatus (HC) Chaetodon baronesssa (HC) Chaetodon plebius (HC) 174 100 99 58 84 43 10 – 13 – – 3 Chaetodon lunulatus (HC) 18 68 11 15 Chaetodon rainfordi (HC) 23 25 12 0 230 120 211 80 117 48 Chaetodon melannotus (SC) 47 11 86 101 10 Chaetodon trifascialis (HC) Total hard-coral feeders Total soft-coral feeders 47 11 86 101 10 Chaetodon auriga (G) – Chaetodon ephippium (G) 1 – – Chaetodon lineolatus (G) 14 – – Chaetodon lunula (G) 10 – – – Chaetodon rafflesi (G) 14 – 14 – Chaetodon vagabundus (G) 57 30 Chelmon rostratus (G) 24 26 30 Total generalist feeders 129 79 50 Mean abundance per site Obligate hard-coral feeders 3.49±0.28 1.82±0.18 3.52±0.17 1.33±0.10 3.25±0.17 1.33±0.09 Soft-coral feeders 0.47±0.09 0.11±0.04 0.96±0.09 0.09±0.03 1.53±0.28 0.15±0.05 Generalists 1.68±0.69 0.10±0.03 1.13±0.49 0.10±0.06 1.19±0.50 0.10±0.07 Environ Biol Fish (2012) 94:579–590 belonging to the genus Porites were relatively abundant (mean 6.7±1.2%), while both Acropora (staghorn and table morphologies) and Pocillopora were in much lower abundance (mean cover of 1.6± 0.04% and 0.6±0.01%, respectively; Fig 2) Table Acropora was rare in all locations However, overall cover of table Acropora was strongly related to exposure, peaking along the exposed reef flat of 583 Orpheus and Pelorus Islands (Table 2) where wave action and surge were strongest Pocillopora and table Acropora were in relatively low abundance on Curacoa Island, where soft corals were abundant (Table 3) Porites species showed no patterns of abundance among islands (Table 2), having peak cover in sheltered locations along the crest and slope (Fig 2) Soft coral was the dominant benthic component surveyed, with a mean cover of 29.3± 2.2% among sites (Fig 2) Nevertheless, the total cover of both hard and soft corals was variable across study sites Total hard coral cover was lower in obliquely exposed sites than either sheltered or exposed sites (ANOVA, Table 2) In contrast, soft coral cover was higher in obliquely exposed sites (ANOVA, Table 3), where extensive beds of soft coral were frequently observed Additionally, soft coral was more abundant on Curacoa Island than either Orpheus or Pelorus Islands (ANOVA, Tables and 3) No other benthic components varied across islands The remaining benthic categories surveyed (Pocillopora, staghorn Acropora, and other hard corals) exhibited no variation among zones or exposures (ANOVA, Table 2) Habitat associations of adult vs juvenile butterflyfish Fig Mean cover of benthic components within the Palm Islands according to reef zone and exposure a flat; b crest; c slope TA, table Acropora; SA, staghorn Acropora; POC, Pocillopora; POR, Porites; OHC, other hard coral; THC, total hard coral; SC, soft coral (■) sheltered locations; ( ) obliquely exposed locations; (□) exposed locations Butterflyfish abundances varied considerably among locations and benthic compositions Comparisons among adults and juveniles revealed significant intraspecific variation in the distributions of generalist feeders and the soft coral feeder C melannotus For the generalist feeders, ontogenetic variation in the use of reef zones occurred (MANOVA, Table 4) Adult generalists were abundant in all reef zones, while juveniles were typically recorded only in the shallows of the reef flat [Fig 3(c), (d)] In addition, abundances of adult and juvenile generalists did not vary significantly according to either island or level of exposure (MANOVA, Table 4) For C melannotus, adult and juvenile distributions varied across exposures Adults of C melannotus were significantly associated with exposed and obliquely exposed locations (MANOVA, Tukey’s Homogenous Groups; Table 4) while juveniles exhibited no clear pattern among locations (Fig 4) However, adults and juveniles of C melannotus were both significantly more abundant on Curacoa Island than on either Orpheus or Pelorus Islands (MANOVA, Tukey’s Homogenous Groups; Tables and 4), showing a 584 Environ Biol Fish (2012) 94:579–590 Table 3-factor ANOVA results comparing benthic components among locations Island (random), exposure (fixed), and reef zone (fixed) were included as test variables Results are based on mean cover of benthic components, pooled across Benthic component Island (random: Orpheus, Pelorus, Curacoa) Exposure (fixed: sheltered, obliquely exposed, exposed) 2, 54 df 2, 54 df sites Benthic cover values were arcsine-root transformed to meet ANOVA assumptions Numerical values are F-statistics (*) significant at α=0.05 Island X Exposure Zone (fixed: flat, crest, slope) Island X Zone Exposure X Zone Island X Exposure X Zone 4, 54 df 2, 54 df 4, 54 df 4, 54 df 8, 54 df Table Acropora 2.889 (ns) 2.569 (ns) 0.650 (ns) 3.725 (*) 0.229 (ns) 1.189 (ns) 0.273 (ns) Staghorn Acropora 2.159 (ns) 2.529 (ns) 1.674 (ns) 0.562 (ns) 2.113 (ns) 0.955 (ns) 0.887 (ns) Pocillopora 2.803 (ns) 2.640 (ns) 1.166 (ns) 1.170 (ns) 0.233 (ns) 0.288 (ns) 0.985 (ns) 13.688 (*) 0.662 (ns) 6.203 (*) 0.570 (ns) 0.665 (ns) 0.211 (ns) 13.513 (*) 2.331 (ns) 2.435 (ns) 0.519 (ns) 0.852 (ns) 0.825 (ns) Porites Soft Coral 0.248 (ns) 70.567 (*) Other Hard Coral 0.106 (ns) 2.309 (ns) 2.554 (ns) 1.064 (ns) 0.204 (ns) 0.083 (ns) 0.341 (ns) Total Hard Coral 0.633 (ns) 3.612 (*) 1.995 (ns) 1.632 (ns) 0.203 (ns) 0.423 (ns) 0.216 (ns) similar abundance pattern across islands to that of soft coral cover In contrast to generalists and soft coral feeders, hard coral feeding butterflyfishes showed no significant variation in the distributions of adults and juveniles across islands, exposures, or reef zones (MANOVA, Table 4) Both adult and juvenile coral feeders were significantly more abundant in sheltered sites than either obliquely exposed or exposed sites (MANOVA, Tukey’s Homogenous Groups: Table 4), showing a similar pattern to that of hard coral cover Both hard- and soft-coral feeders showed no clear intraspecific pattern in abundance across reef zones [Fig 3(a), (b)] The PCA revealed some intraspecific variation in benthic association for the six most abundant butterflyfishes (Fig 5) For two of the coral-feeding species (C aureofasciatus and C lunulatus), adults and juveniles Table Mean cover of benthic components at each study island within the Palm Islands displayed comparable intraspecific distributions among reef locations (Fig 4) However, juveniles of both C aureofasciatus and C lunulatus differed substantially in their associations with benthic components compared to adult conspecifics (Fig 5) For C aureofasciatus, adult abundance was positively correlated with several benthic categories (namely Porites, other hard corals, and soft corals), while juveniles were primarily associated with staghorn Acropora (Fig 5) In contrast, adults of C lunulatus were predominately associated with staghorn Acropora and Pocillopora, while juveniles were more common in areas with high coverage of Porites (Fig 5) In contrast to C aureofasciatus and C lunulatus, the remaining four species analysed displayed similar correlations among age groups and benthic categories (C rostratus, C vagabundus, C melannotus, and C Orpheus Island Pelorus Island Curacoa Island Table Acropora 0.011±0.003 0.007±0.004 0.003±0.002 Staghorn Acropora 0.011±0.002 0.007±0.002 0.007±0.003 Pocillopora 0.008±0.002 0.006±0.002 0.004±0.001 Porites 0.033±0.008 0.044±0.011 0.034±0.013 Soft Coral 0.275±0.027 0.157±0.014 0.555±0.031 Other Hard Coral 0.120±0.015 0.107±0.020 0.120±0.015 Total Hard Coral 0.183±0.016 0.172±0.027 0.164±0.022 Environ Biol Fish (2012) 94:579–590 585 Table 3-factor MANOVA results from intraspecific comparisons of adult and juvenile butterflyfish abundances, pooled by trophic guild Island (random), exposure (fixed), and reef zone (fixed) were included as test variables Abundance and coral Island (random: Orpheus, Pelorus, Curacoa) Exposure (fixed: sheltered, obliquely exposed, exposed) Island X Exposure cover data were pooled across sites and standardised by survey area Butterflyfish abundance data were square-root transformed to meet MANOVA assumptions Numerical values are Pillai’s trace statistics (*) significant at α=0.05 Zone (fixed: flat, crest, slope) Island X Zone Exposure X Zone Island X Exposure X Zone Trophic guild 4, 108 df 4, 108 df 8, 108 df 4, 108 df 8, 108 df 8, 108 df 16, 108 df Hard coral feeders (6 species) Soft coral feeder (C melannotus) Generalist feeders (7 species) 0.693 (ns) 1.745 (ns) 1.493 (ns) 0.380 (ns) 0.488 (ns) 1.778 (ns) 0.568 (ns) 1.778 (ns) 2.601 (*) 1.665 (ns) 1.428 (ns) 1.110 (ns) 0.332 (ns) 0.554 (ns) 1.325 (ns) 1.319 (ns) 1.195 (ns) 2.882 (*) 0.472 (ns) 0.780 (ns) 0.816 (ns) rainfordi; Fig 5.) For the two generalists (C vagabundus and C rostratus), adults and juveniles displayed similar associations with the benthos despite contrasting distributions across zones (Fig 4), though juveniles of both species were more strongly associated with the ‘other hard corals’ category than adults (Fig 5) Benthic associations among adult and juvenile C melannotus (soft coral feeder) were also similar, correlating primarily with soft coral cover, though once again juveniles were more strongly associated with ‘other hard corals’ than adults (Fig 5) For C rainfordi, an obligate hard coral feeder, both adults and juveniles associated primarily with table Acropora and Pocillopora species (Fig 5) No species analysed was strongly associated with non-coral benthos (Fig 5) Fig Mean abundances of adult and juvenile butterflyfishes, pooled by trophic guild: (a) adult hard coral feeders; (b) juvenile hard coral feeders; (c) adult generalist feeders; (d) juvenile generalist feeders (■) sheltered locations; ( ) obliquely exposed locations; (□) exposed locations 586 Fig Mean abundances (± SE) of adults (top graphs) and juveniles (bottom graphs) of the six most abundant species of butterflyfish in the Palm Islands (F) flat; (C) crest; (S) slope Environ Biol Fish (2012) 94:579–590 Environ Biol Fish (2012) 94:579–590 Fig Principal components analysis (PCA) showing intraspecific variation in the associations of the six most abundant butterflyfishes (a) with individual benthic components (b) in the Palm Islands Capital letters indicate adults while lower case letters indicate juveniles Species are as follows: Chaetodon aureofasciatus, Chaetodon lunulatus, Chaetodon rainfordi, Chaetodon vagabundus, Chaetodon melannotus, and Chelmon rostratus Discussion Ontogenetic variation in the distributions of coral reef fishes has been observed in a variety of species, with evidence suggesting that dietary preference, the availability of shelter, and the presence of adult conspecifics may all contribute to this pattern of habitat 587 association (Lecchini and Galzin 2005; Mumby 2006; Jones et al 2010) The results of this study agree strongly with a previous study of butterflyfish distributions on coral reefs (Pratchett et al 2008b), indicating that some species of butterflyfish also display variations in their distributions as they mature Furthermore, the patterns revealed in both studies appear to relate strongly to trophic guild However, in contrast to the study by Pratchett et al 2008b, which was carried out on mid-shelf reefs of the Great Barrier Reef (GBR) with relatively high abundance of Acropora and Pocillopora corals, this study was performed on an inner-shelf GBR reef with significantly lower prey abundance for hard coral feeders (Emslie et al 2010) Thus, our results further highlight the importance of trophic guild in determining ontogenetic differences in butterflyfish distributions For example, although Berumen and Pratchett (2006) noted an increase in territory size among adult coral-feeders as abundance of coral prey declined, our results found that juvenile hard-coral feeders displayed comparable distributions to adult conspecifics in habitats dominated by soft coral This indicates that either recruits of hard-coral feeders settle preferentially into habitats occupied by adult conspecifics, or alternatively, that juveniles exhibit higher survival rates in these areas (e.g., see Harmelin-Vivien 1989; Pratchett et al 2008b) However, hard-coral feeders were not the only species to exhibit such limited ontogenetic variation in abundance Adult and juvenile abundances of the soft-coral feeder C melannotus were similar across locations and ontogenetic variation was displayed only according to degree of exposure In contrast to coral feeders, generalist feeders displayed substantial ontogenetic variation in distribution Juvenile generalist feeders were limited almost exclusively to the shallow, patchy areas along the reef flat, whilst adults displayed comparatively wide distributions Our original hypothesis of spatial variation in abundance of adult and juvenile generalists was supported by our results (see Table 4; Fig.3) This ontogenetic variation in distribution suggests a correlation between distribution and dietary versatility The expansion in dietary flexibility often shown by generalists may partially explain the relatively limited distributions of juveniles compared to adults Juveniles typically feed only on benthic invertebrates, whilst adults have been shown to feed on a variety of items including scleractinian coral polyps and 692 Fig Hatching success (proportion of fertilized eggs that hatched out of 50) of Spotted Gar (Lepisosteus oculatus) treated with clear (circles, grey line) or turbid (triangles, black line) water Gar eggs were spawned two days prior to the start of the experiment and the experimental treatment initiated on Day All eggs were either hatched or dead by Day treatments remaining relatively constant throughout the remaining days of the experiment, with approx 25 % fewer live eggs/larvae in the turbid treatment The final hatching success was on average 94.8 % (±0.016) for the clear treatment and only 72.2 % (±0.052) for the turbid treatment, a significant reduction of 24.2 % (ratio of turbid/clear) (F1,8 025.54, P00.001; Fig 1) Discussion A final reduction in hatching success of approximately 24 % was found for Spotted Gar held in turbid vs clear water This result is especially important because it exemplifies the sensitivity of this life history stage of a species considered Threatened in Canada Turbidity has been cited as a potential contributor to the decline of Spotted Gar in Canada, and the results found here may explain how its effect on one life history stage contributes to the threatened status of the species Suspended sediments can effectively smother eggs, depriving them of oxygen and leading to egg mortality (reviewed in Henley et al 2010) Some studies, however, have shown little negative effects of suspended Environ Biol Fish (2012) 94:689–694 sediment on the egg stage, whereas, larval stages are severely adversely affected by turbidity (e.g., Isono et al 1998; Partridge and Michael 2010) Therefore, the effect of turbidity on fish eggs may be species specific (reviewed in Henley et al 2010), and it may be that imperilled species are those that are most sensitive to this stressor, while more common species are able to compensate While the current study did not test the proximate cause of egg mortality, it is reasonable to hypothesize that difficulty in sequestering oxygen may have played a role Future studies will need to examine this in more detail The level of turbidity used in this study (approx NTU) is relatively low compared to other such studies and is lower than that found in areas of Lake Erie where Spotted Gar are still found (mean ± s.e 12.2 NTU±3.14 over years, two sites; NEM, unpubl data) The magnitude of the effect of turbidity on Spotted Gar eggs in nature may, therefore, be greater where turbidity is higher Alternatively, the sensitivity of the eggs may reflect sedimentation of the suspended clay that occurred overnight While measures were taken to keep the clay suspended (see above), some of the clay settled over the eggs each night, although turbidity in the aquaria remained higher than in clear water controls Sedimentation may have a larger impact on fish eggs than suspended particulate matter as smothering can occur In either case, suspended particles or periodic sedimentation, results for hatching success are highly variable across species For example, Savino et al (1994) used a pulsed turbidity system, allowing sediment to settle over Cisco (Coregonus artedii Lesueur) eggs and found that egg survival was not affected by low levels of turbidity In a similar study, however, Fudge and Bodaly (1984) report almost 100 % mortality on Lake Whitefish (Coregonus clupeaformis Mitchell) eggs exposed to natural episodes of sedimentation In a single study, Auld and Schubel (1978) tested for an effect of suspended sediment on the eggs of six estuarine fishes; only two of the six species showed decreased hatching success with high levels of turbidity The fall-out of suspended sediments is expected in highly turbid waters; therefore, the effect of both turbidity and sedimentation is particularly relevant to the management of critical habitat The observed decrease in hatching success may inhibit the recovery of Canadian populations of Spotted Gar Based on the life history-based model of Vélez-Espino and Koops (2009), a recent report on Environ Biol Fish (2012) 94:689–694 the recovery potential of Spotted Gar suggested that fertility was sensitive to threats and that any reduction in fertility of more than 15 % would compromise the future survival and recovery of this species in Canadian waters (Young and Koops 2010) The results of the current study (24 % reduction in hatching success), even at a very low level of turbidity, suggest that Spotted Gar in Canada may, therefore, be unable to recover in areas where sedimentary turbidity exceeds even a very low level of turbidity (∼5 NTU) during the reproductive season (May–June in Canada) Conversely, the results indicate that rate of recovery to a recovery target could be increased by increasing fertility (Young and Koops 2010) through reducing turbidity levels; for example, by reducing turbidity being discharged by agricultural drains into Rondeau Bay and by controlling sedimentation in the watershed Young and Koops (2010) also indicated that survival rates of other life stages may also influence recovery; therefore, further investigation on other life stages is required to provide a more holistic understanding of negative fitness effects of turbidity in this species Increased turbidity is cited as a putative cause for fish population declines globally (Donohue and Garcia Molinos 2009) Our understanding of how this environmental stressor affects all stages of fish development and survival is vital to the conservation and management of fishes sensitive to increased turbidity Management of sedimentary inputs into freshwater ecosystems, especially during times of the year when sensitive life history stages are present, such as eggs and larvae, may have huge benefits for the maintenance of fish populations globally Acknowledgments We thank A Ferrara and Q Fontenot (Nicholls State University) for providing Spotted Gar embryos; L McDonnell, J Hunter, K Gong, E Chan, K Wiens for maintaining the eggs and experimental set-up This project was approved by the McGill University Animal Care Committee (Protocol # 5889) and the Quebec SEG Permit (2010-03-081080-16-SP), and partially funded by the Canadian Department of Fisheries and Oceans Species at Risk Program References Auld A, Schubel JR (1978) Effects of suspended sediment on fish eggs and larvae - laboratory assessment Estuar Coast Mar Sci 6:153–164 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Conserv Biol 13:1220–1222 Richter BD, Braun DP, Mendelson MA, Master LL (1997) Threats to imperilled freshwater fauna Conserv Biol 11:1081–1093 Savino JF, Blouin MA, Davis BM, Hudson PL, Todd TN, Fleischer GW (1994) Effects of pulsed turbidity and vessel traffic on Lake Herring eggs and larvae J Great Lakes Res 20:366–376 Environ Biol Fish (2012) 94:689–694 Scott WB, Crossman EJ (1973) Freshwater Fishes of Canada Bulletin 184, Fisheries Research Board of Canada, Ottawa, pp 103–104 Sigler JW, Bjornn TC, Everest FH (1984) Effects of chronic turbidity on density and growth of steelheads and coho salmon Trans Am Fish Soc 113:142–150 Smith RS, Kramer DL (1986) The effect of apparent predation risk on the respiratory behaviour of the Florida gar (Lepisosteus platyrhincus) Can J Zool 64:2133–2136 Snedden GA, Kelso WE, Rutherford DA (1999) Diel and seasonal patterns of Spotted Gar movement and habitat use in the Lower Atchafalaya River Basin, Louisiana Trans Am Fish Soc 128:144–154 Sutherland AB, Meyer JL (2007) Effects of increased suspended sediment on growth rate and gill condition of two southern Appalachian minnows Environ Biol Fishes 80:389–403 van de Meutter F, de Meester L, Stoks R (2005) Water turbidity affects predator–prey interactions in a fish–damselfly system Oecologia 144:327–336 Vélez-Espino LA, Koops MA (2009) Quantifying allowable harm in species at risk: application to the Laurentian black redhorse (Moxostoma duquensnei) Aquat Conserv Mar Freshwat Ecosyst 19:676–688 Young JAM, Koops MA (2010) Recovery potential modelling of Spotted Gar (Lepisosteus oculatus) in Canada DFO Canadian Scientific Advisory Section Research Document 2010/078 Iv + 19p Environ Biol Fish (2012) 94:695–706 DOI 10.1007/s10641-012-0002-9 Stable isotopic assessment of site fidelity of mummichogs, Fundulus heteroclitus, exposed to multiple anthropogenic inputs Marc A Skinner & Simon C Courtenay & W Roy Parker & R Allen Curry Received: June 2011 / Accepted: 20 March 2012 / Published online: 11 April 2012 # Springer Science+Business Media B.V 2012 Abstract The goals of the study were: (1) to evaluate stable isotopic analysis (SIA) in determining the site fidelity of mummichogs, Fundulus heteroclitus, along a smaller spatial scale (~10 km) in homogenous habitat type relative to previous SIA studies; and (2) to crossvalidate SIA results with mark-recapture results from a study conducted concurrently at the same sites in the upper Miramichi River estuary (MRE), New Brunswick, Canada influenced by two pulp mills and three municipal wastewater facilities Mummichogs sampled at sites along the upper MRE (n0198) had overall mean (± SD) ratios of −21.03±1.45 ‰ δ13C and 11.37±1.02 ‰ δ15N Mean δ13C and δ15N ratios were significantly different among sites with mean δ13C increasing in a downstream direction and distinct δ15N group signatures along the northern and southern shores Multivariate analyses detected seven distinct groups out M A Skinner (*) : S C Courtenay Fisheries and Oceans Canada at the Canadian Rivers Institute, Department of Biology, University of New Brunswick, Fredericton, NB, Canada E3B 6E1 e-mail: ma.skinner@unb.ca W R Parker Canadian Rivers Institute, 147 Stanwood Dr., RR 2, Pictou, NS B0K 1H0, Canada R A Curry Department of Biology and Canadian Rivers Institute, Department of Biology, University of New Brunswick, Fredericton, NB, Canada E3B 6E1 of nine sites sampled and these differences appear to be related to wastewater treatment influences, thus demonstrating the utility of SIA as a method to determine the site-specificity of organisms on a relatively small spatial scale within homogenous habitat within an estuary These results, in addition to the scarcity of statistical outliers (3 %) during examination of isotopic ratios within sites support the results of a previous markrecapture study that demonstrated very few mummichogs (3.4 %) in the upper MRE move more than 200 m Keywords Fundulus heteroclitus Stable isotopes Mark-recapture Pulp mill Wastewater treatment Miramichi Introduction Previous studies have demonstrated the utility of stable isotope analysis (SIA) to establish movement and migration patterns in a variety of organisms across great distances (Fry 1983; Hobson and Wassenaar 1997; Hobson 1999) SIA is a helpful tool for such studies as it exploits differences in the isotopic composition of target organisms These differences are conserved over prolonged periods as they are due to the preferential assimilation of one isotope of a particular element over another during chemical fixation by primary producers in an organism’s food-web (Peterson and Fry 1987) For example, ratios of 13C vs 12C are useful to researchers 696 as they are habitat specific and conserved during trophic transfer (Peterson and Fry 1987) Therefore, it can be determined whether a particular organism is a resident of a site or has recently moved into the area by examining the degree of difference between the carbon isotope ratios of the organisms’ tissues and their surroundings (DeNiro and Epstein 1978; Michener and Schell 1994) Additionally, ratios of 15N vs 14N are useful for examining trophic relationships because metabolic fractionations in consumers discriminate against the lighter isotope as this element is passed on to higher trophic levels (DeNiro and Epstein 1981), resulting in higher concentrations of 15N in predators than their prey The extra information provided by examining multiple isotopes simultaneously allows for further discrimination of differences among samples (Peterson et al 1985) While SIA has been useful for addressing questions related to large-scale movements of animals (Leakey et al 2008; Vinagre et al 2008) there have been few studies which have used SIA to examine small-scale movements (Hobson 1999) Unless there are abrupt transitions in dominant primary producers at habitat interfaces, e.g mangrove to salt marsh (Guest et al 2006) or freshwater inputs to marine systems (Vinagre et al 2011), it is highly unlikely that food sources will show significant isotopic variation among sites of homogenous habitat separated by distances of less than 10 km (e.g sites along short sections of rivers or estuaries) This homogeneity, however, may be theoretically eliminated in systems receiving varying anthropogenic point source inputs (Macko and Ostrom 1994) as isotopically distinct signatures will be imparted on primary producers which will in turn be trophically conveyed to higher consumers Several studies have shown that sewage and wastewater can influence nitrogen isotopic signatures of biota (Spies et al 1989; McClelland et al 1997; Wayland and Hobson 2001; deBruyne and Rasmussen 2002; Cole et al 2004; Gaston and Suthers 2004; Bannon and Roman 2008) depending on the level of sewage treatment employed and various physicochemical processes (such as volatilization of ammonia) that are related to the physical dimensions of their respective holding lagoons (Heaton 1986) Variation has also been noted for carbon and/or nitrogen signatures of organisms residing in areas receiving pulp mill effluent (Wassenaar and Culp 1996; Wayland and Hobson 2001; Galloway et al 2003; Dubé et al 2005; Oakes et al 2010) Therefore, potential Environ Biol Fish (2012) 94:695–706 exists to allow the examination of small-scale movements of organisms residing in areas exposed to such anthropogenic inputs as they may cause significant isotopic variation on a scale of only hundreds of meters (Hobson 1999) Cunjak et al (2005) recommended the inclusion of both SIA approaches and mark-recapture/telemetry data in studies of animal movements These authors presented case studies demonstrating the value of cross-validating results as each method has its own limitations and interpretation challenges Specifically, mark-recapture/telemetry methods are plagued by low recapture/encounter rates that may be related to mortality, emigration, mark/tag loss, and/or simple difficulty in tracking/capturing individuals (Gray et al 2004) In comparison, overlap of isotopic signatures, for example may lead a researcher to conclude low site fidelity although individuals not move among locations and simply have similar availability of food sources Conversely, concluding high site fidelity on the basis of significant differences in isotopic signatures would be erroneous in instances where individuals engage in short term or infrequent migrations, thereby not incorporating site-specific isotopic signatures The goals of the current study were two-fold First, we hypothesized mummichogs sampled from sites exposed to multiple anthropogenic inputs (a bleached kraft pulp mill, a groundwood pulp mill, and three municipal sewage facilities) would display distinct isotopic signatures on a relatively small spatial scale (~1–10 km) Secondly, we wished to use the results of this study to cross-validate the mark-recapture results from a study conducted concurrently in the same study area (Skinner et al 2005) Mummichogs in the upper Miramichi River estuary (MRE), New Brunswick, Canada displayed distinct site fidelity with 96.6 % (n0617) of all recaptures (n0639) occurring within 200 m of the point of release over a 19-month period (Skinner et al 2005) Materials and methods Study area As part of a larger project examining the potential use of mummichogs as an aquatic monitoring species in estuarine and coastal areas (2002–2003), fish samples were collected for SIA from the upper MRE The Environ Biol Fish (2012) 94:695–706 MRE is fed by two major rivers, the Northwest Miramichi and Southwest Miramichi, with respective drainage areas of 3900 km2 and 7700 km2 (Chiasson 1995); is subject to mixed semi-diurnal tides with a tidal range between and m (Reinson 1977); and is exposed to a freshwater inflow of 5–10 % of the volume of incoming tide water (Chiasson 1995) Salt water intrudes into the upper estuary as a salt wedge, the upper extent of which varies in position with lunar tide and freshwater discharge, being downstream of the study area in early spring and far upstream of the study area in summer The study area was subjected to multiple pointsource anthropogenic inputs: a bleached kraft pulp mill (BKPM; Site N2), a groundwood pulp mill (GW), and three municipal sewage facilities (SEW 13; Fig 1) Effluent from the BKPM received secondary treatment (activated sludge) and mean daily flow of effluent to the estuary was 60 412 m3 during 2003 (Jacques Whitford Environmental Limited 2004) Sewage facilities on the north shore (SEW and 2) were treated Sewage utilized a settling lagoon with Fig Map of Newcastle/Chatham area of the upper Miramichi River estuary (N 46o 58.303, W 65 o 34.554) with sampling sites (■) and effluent outfalls indicated Inset shows map of Atlantic Canada with an arrow highlighting the study area Dashed arrows indicate direction of river flow Shaded/stippled regions delineate approximate % concentration area of effluent plumes where such data exist (Natech Environmental Services Inc., 2002; Jochen Schroer, Natech Environmental Services Inc., pers comm.) Labels N1-N5 and S1-S4 refer to sampling sites along the northern and southern shores, respectively 697 UV light treatment (John Simonson, Eel Ground First Nation, pers comm.), while Sewage utilized an aerated lagoon and bacterial system (Cecil Bowes, Department of Public Works, City of Miramichi, pers comm.) On the south shore, Sewage discharged untreated waste (Cecil Bowes, Department of Public Works, City of Miramichi, pers comm.) In a recent study (Natech Environmental Services Inc 2002; Jochen Schroer, Natech Environmental Services Inc., pers comm.), all pulp mill and sewage effluents were found to be tidally dispersed up and downstream twice daily with their plumes remaining close to shore and relatively localized (Fig 1) Sample collections, processing and isotopic analyses From July 29–31 and August 20–22, 2003, a minimum of 10 female and 10 male mummichogs (60–120 mm TL) were collected by beach seine (25 m in length; 1.5 m in height; mm mesh size) and minnow traps (baited with cat food; 6.35 mm mesh size) from each of sites along a reach of ca 10 km (Fig 1) Equal numbers of male and females were selected for analyses as mummichog populations in the region exhibit a 1:1 sex ratio (Kirchhoff et al 1999) Mummichogs chosen for analysis were euthanized with a quick blow to the head and frozen at −20°C White muscle and bone were dissected from the right flank of mummichogs, oven dried in glass scintillation vials at 50°C for 48 h and ground to a fine powder using a mortar and pestle Samples of 200 μg were analyzed by the Stable Isotopes in Nature Laboratory (SINLAB; University of New Brunswick, Fredericton, NB), with a continuous-flow isotope-ratio mass spectrometer (Finnigan Mat Delta Plus, Thermofinnigan, Bremen, Germany) equipped with a ThermoQuest elemental analyzer (Carlo Erba NC2500, Italy) Isotopic ratios are expressed in the delta notation (δ) normalized to the ratio of the sample to Vienna Pee Dee Belemnite for 13C (Craig 1957) and atmospheric nitrogen for 15 N (Mariotti, 1983) in parts per thousand These ratios are calculated using the following equation: ÂÀ Á Ã dX ¼ Rsample =Rstandard À Â 103 where X is the isotope of interest (e.g 13C) and R is the ratio of this isotope relative to its lighter isotope (e.g 13 12 C/ C) (Peterson and Fry 1987) Isotopic standards CH6, CH7, N1, and N2 were used for correction of 698 carbon and nitrogen values Runs of an elemental standard, Acetanilide (n034), resulted in a mean (± SD) δ13C value of −33.57±0.06 ‰ and a mean δ15N value of −3.12±0.12 ‰ Precision of the mass spectrometer over time was evaluated using repeated analyses of select samples (n028) which resulted in a mean SD of 0.069 for δ13C (range00.003–0.360) and a mean SD of 0.098 for δ15N (range08.21×10−5–0.481) Data analysis Statistical analyses of δ13C and δ15N data of fish were first conducted separately to examine for differences in each isotope among sites While comparing multivariate data using separate univariate tests rather than a single multivariate method (i.e MANOVA or MANCOVA) increases the possibility of committing a Type I error (Sokal and Rohlf 1995), this potential effect was minimized by judging the results of statistical analyses for each element individually to be significant at α00.01 (Zar 1999) Visual inspection of residual plots of δ13C and δ15N data revealed slight non-normality Minor heteroscedasticity (δ13C - Cochran00.3388, df011, k09, p>0.05; δ15N - Cochran00.2765, df011, k09, p>0.05) was detected using Cochran’s test (Zar 1999) Fish length also influenced isotopic ratios, therefore, analyses of covariance (ANCOVA) were initially chosen for statistical analysis with site as factor and total fish length as covariate for each element Data for δ13C and δ15N were not transformed as ANCOVA is robust against slight deviations from the assumptions of normality and homogeneity of variance (Zar 1999) In analyses for each element, however, the length x isotopic ratio relationships were determined to be significantly different among sites resulting in significant interactions After graphing and determining these interactions were not biologically interpretable, a sub-sample of lengths (70– 90 mm; n012 per site) was selected to minimize the effect of length and data were subsequently analyzed using analyses of variance (ANOVA) to test for significant differences between sexes for each element Separate ANOVAs were further conducted to test for significant differences among sites (sexes pooled) for each element Separate comparisons of mean δ13C and δ15N ratios (dependent variables) vs relative sample site position expressed as river distance from Site N1 (independent variable) were performed using simple linear regression (α00.05) Environ Biol Fish (2012) 94:695–706 Multivariate comparisons were conducted using a 1-way Analysis of Similarity (ANOSIM; factor0site; dependent variables0mummichog δ13C and δ15N ratios) on a Euclidean distance dissimilarity matrix with statistical significance assessed at R>0.2, p[...]... on the left side of specimens whenever possible, following the methods of Kottelat (1990) Predorsal, prepectoral, prepelvic and preanal lengths were taken, respectively from the anteriormost tip of the snout to the dorsal-, pectoral-, pelvic- and anal-fin origins, Measurements of parts of the head are given as proportions of head length Head length and measurements of other parts of the body are given... Discussion The description of a new species brings the total number of species of Homatula to 12 Zhu (1989), in his monograph of Chinese species of the Nemacheilinae, recorded five species of the genus under the generic name Paracobitis: P anguillioides, P erhaiensis, P oligolepis, P potanini and P variegatus His generic Environ Biol Fish (2012) 94:591–599 classification of Paracobitis was subsequently... explained by the reduced abundance of M falciformis and increased abundance of R holubi In the final stage of the sandy bottom phase the loss of fish height is evident and the centre shifted towards fusiform shapes characteristic of the Mugilidae due to increased abundance of this family The above results show that the morphology Environ Biol Fish (2012) 94:601–614 of the fish community corresponds... Province, People’s Republic of China e-mail: zhange@ihb.ac.cn J.-H Gu e-mail: swxgjh@126.com J.-H Gu Graduate School of Chinese Academy of Sciences, Beijing 100039, People’s Republic of China Introduction Hu and Zhang (2010), in their describing Homatula pycnolepis from the Yangbi-Jiang of the upper Mekong River drainage of Yunnan Province, southern China, provided a re-definition of Homatula, and placed... rays, inserted slightly posterior to vertical through posteriormost point of operculum, tip of the longest fin ray not extending beyond halfway to insertion of pelvic fin Pelvic fin with 1 simple and 6–7 branched rays, inserted below second or third branched rays of dorsal fin, tip of the longest fin ray extending not beyond halfway of distance between pelvic-fin insertion and anal-fin origin Anal fin... surface of pectoral, pelvic and anal fins grayish, and caudal fin gray The specific epithet, used as an adjective, is made from the combination of Latin words “laxus”(wide) and clathrus (barred), alluding the presence of wider vertical bars on each side of body Distribution Known only from the Wei He of the Yellow River drainage in Shaanxi Province, North China (Fig 5) Fig 5 Map showing distribution of. .. associations of juvenile versus adult butterflyfishes Coral Reefs 27:541–551 Russ GR (1984a) Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef I Levels of variability across the entire continental shelf Mar Ecol Prog Ser 20:23–34 Russ GR (1984b) Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef II Patterns of zonation of mid-shelf... with rudimentary scales present only on the caudal-fin base The results of the principle component analysis performed on the variance-covariance matrix of log-transformed measurements for the examined specimens of four species of the third group (Table 2, Fig 6) revealed that the combination of PC2 against PC3 enabled the separation of H laxiclathra and H berezowskii from H longidorsalis and H variegata... Homatula anguillioides, IHB 8201 34, holotype, 1, 134.8 mm SL and 820119–29, 820131, 820135, 820137, paratypes, 14, 49.3–134.3 mm SL; China: Yunnan Province: Eryuan County of upper Mekong River drainage -IHB 820533–5, 820538–40, topotypes, 6, 114.1–126.0 mm SL; China: Yunnan Province: Eryuan County: upper Mekong River drainage Homatula berezowskii, IHB 73VI1191-3, 73VI1 1 94, 4, 89.0–125.4 mm SL; China: Shanxi... information on the morpho-functional structure of the community (Winemiller 1991; Fulton et al 2001; Mason et al 2007) The aim of this study was to increase the range of methods available for detecting the impact of disturbances on aquatic systems Based on the premise that functional loss may alter the morphological characteristics of a fish community, the morphotypes of two South African estuarine fish communities,