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Characterization of Scale Abnormalities in Pinfish

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Characterization of Scale Abnormalities in Pinfish Environmental Biology of Fishes 57: 205–220, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands. Characterization of scale abnormalities in pinfish, Lagodon rhomboides,from Biscayne Bay, Florida Jone Corralesa, Laurie Beth Nyea, Sean Baribeaua, Nancy J. Gassmanb & Michael C. Schmalea,c aDivision of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL 33149, U.S.A. bWater Resources Division, Broward County Department of Natural Resource Protection, Ft. Lauderdale, FL, U.S.A. cSenior author for correspondence (e-mail: [email protected]) Received 5 November 1998 Accepted 19 April 1999 Key words: gross pathology, estuarine fish, deformity Synopsis Correlations between marine habitat degradation and the prevalence of abnormalities and diseases in populations can provide a starting point for understanding the effects of changes in environmental conditions on marine organ- isms. The present study characterized the features of scale disorientation (SD), a common morphological anomaly encountered in pinfish, Lagodon rhomboides, in Biscayne Bay, Florida (U.S.A.). Scale disorientation consisted of discrete patches of scales rotated dorsally or ventrally away from the normal scale position without any projection of the scales outwards from the body surface. The direction of scale growth within the patches varied from nor- mal to a minor misalignment to a complete reversal of direction. The severity of SD, defined as the percentage of body surface area affected, varied from 1 to 34% with a mean of 9.3%. Affected fish monitored in the laboratory demonstrated a proportional growth of SD areas such that the percentage of body surface affected did not change as the fish grew. Scale disorientation was more prevalent in the northern region of the bay, an area known to be more contaminated. Scales from SD areas exhibited significantly abnormal morphology with larger average focus diameter, smaller size, more elongate shape and fewer radii relative to normal scales. Experimental removal of scales demonstrated that normal scales regrew in normal orientation and morphology while those from SD areas regrew in abnormal orientations and morphologies. Experiments in which fish were exposed to acute and chronic injuries indicated that these physical traumas were insufficient to directly induce formation of scale disorientations typical of those seen in the wild. Observations of pinfish in the laboratory revealed that SD areas can appear spontaneously in normal juvenile and adult fish. These new SD areas developed relatively rapidly, did not require prior scale loss and remained stable in size after first appearance. Although the etiology of SD remains unknown, the significant difference in prevalence of this syndrome between regions of Biscayne Bay having different levels of sediment contaminants suggests that environmental factors may be important in development of SD. Introduction 1996). The correlation of abnormal conditions with the presence of specific environmental or other factors can An important indicator of the effects of habitat degra- serve as a first step in understanding the etiology of dation on fishes and invertebrates in aquatic envi- such syndromes. A critical step in this process is the ronments is a change in the prevalence of diseases description of specific abnormalities in sufficient detail or deformities in exposed populations (Sindermann to allow design and testing of hypotheses concerning 206 the roles of environmental or other factors in develop- Materials and methods ment of such abnormalities. We have previously described distribution patterns Collection of fish of several types of abnormalities in fish and inverte- brates in Biscayne Bay, Florida (U.S.A) and proposed Biscayne Bay is a shallow tropical estuary within a possible relationship between these abnormalities Miami-Dade county Florida, U.S.A. (Figure 1). This and habitat degradation (Gassman et al. 1994). The body of water is bounded on the east by a series of most prevalent abnormality observed in this study barrier islands. The bay receives urban runoff from was scale disorientation (SD) and the most commonly the city of Miami, particularly in the northern region. affected species was the pinfish, Lagodon rhomboides. Agricultural and suburban runoff impacts the southern The present study focuses on this scale abnormality bay from the southern region of the county. In addi- in pinfish in Biscayne Bay. This syndrome is char- tion to direct runoff, input to the bay is provided by acterized by a rotation of scales dorsally or ven- a large number of rivers, streams, creeks and canals trally away from the normal scale position. The draining the county. Four sites in the northern region direction of growth of the individual scales within of the bay (north of Rickenbacker Causeway) and four the patch varies from normal to a minor misalign- south bay sites were sampled monthly from August ment to a complete reversal of direction without 1993 to September 1994 (Figure 1). Sites were selected any projection of the scale outwards from the body based upon previous knowledge of the distribution of surface. pinfish. Sampling was conducted at night using paired The anatomy and developmental patterns of fish roller trawls (3m×4.6m×0.9m) with 1 cm2 mesh scales and the relationship of scale morphology to net. Nets were deployed for two, ten minute intervals genetic and environmental factors have been well at each site. The combination of mesh size and finger described (Blair 1942, Yamada 1961, Fouda 1979, bars on the trawl mouth typically limited the catch to Sire 1986, Bereiter-Hahn & Zylberberg 1993). How- individuals 30–250 mm in length. The prevalence of ever, abnormalities in scale morphology or arrange- pinfish with SD was estimated from surveys made over ment have rarely been reported. Taki (1938) described the total 14 month period of the study. To facilitate a a similar phenomenon in sole, Zebrias japonicus,in detailed analysis of SD, all pinfish with this abnormal- Japanese waters and suggested it might arise during ity encountered in surveys in July and September 1994 embryonic development. Gunter (1941, 1945, 1948) were collected and frozen for later study. reported three cases of disoriented scales in redfish, Sciaenops ocellata, in Nueces Bay and Mesquite Bay, Quantification of disorientation patterns of scales Texas. In pinfish, SD has also recently been observed in the Indian River Lagoon, Florida (Browder personal Scale disorientations were diagnosed by visual inspec- communication). tion and by touch. In order to document patterns of In Biscayne Bay, the occurrence of SD was docu- arrangement of scales within disoriented regions, a mented by Overstreet (1986), Skinner & Kandrashoff scale by scale examination was made of four such (1988) and Browder et al. (1993), sometimes referred patches on three fish. The angle of growth of each scale to as ‘Kandrashoff syndrome’. In 1992–1993, SD was was recorded relative to that of normal scales in adja- observed in several species of fish in this region, includ- cent areas outside of the affected patch. Directions were ing sea bream, Archosargus rhomboidalis, blue striped measured as degrees of deviation from normal, grouped grunt, Haemulon sciurus, bermuda chub, Kyphosus into 30 degree increments (i.e., 0◦ = normal, free edge sectatrix, and pinfish (Gassman et al. 1994). The high- toward the tail of the fish and 180◦ = reversed, free est prevalences were observed in pinfish with levels edge toward the head of the fish). reaching 15% at some locations. Thus, while the occur- Severity of SD was defined as the surface area of rence of scale disorientation has been documented each patch relative to the total surface area of the in the past, it has never been thoroughly character- individual fish. These areas were expressed as the per- ized in any species. The present study describes in centage of the body surface on a single side of a fish detail the characteristics of SD in pinfish and evalu- which was affected by SD. Scale disorientation areas ates several potential mechanisms for development of were measured on all pinfish collected which exhib- this syndrome. ited SD (n = 140). These areas were measured either 207 Figure 1. Sampling locations for pinfish, Lagodon rhomboides, in Biscayne Bay, Florida. Sample sites were subdivided into four northern region sites (light circles) and four southern region sites (dark circles). Full names for sites are provided in Table 1, corresponding to two letter codes shown on this map. from photographs or by tracing the outline of the fish over time in laboratory held fish were quantified on (exclusive of the head and fins) and each SD patch onto scanned images of photographs or traces using NIH a transparent plastic sheet, one side at a time. Areas Image software on a Power Macintosh computer. Body of SD regions were estimated using a grid measure- surface areas were also subdivided into regions above ment system. Measurements of changes in SD patches and below the lateral line. Prior to parametric analyses 208 (by ANOVA) of severity differences between groups, muscle tissue anterior to the caudal peduncle (con- these percentage measures were transformed using nat- stituting a chronic injury) with colored beads on the ural logarithms. monofilament used to identify individuals. This pro- tocol was based on Patzner’s (1984) tagging method. Fish were observed weekly for 6 months to detect any Scale morphology changes in the conformation of the scales or any other skin anomaly. A subset of 26 pinfish from 5 sample sites were selected for analysis of the morphology of disoriented scales. Ten disoriented scales were collected from the cen- Results ter of each patch with SD and ten normal scales from the opposite side at the equivalent location. The 520 Orientation of scales in disoriented patches scales (260 per scale type) were stored in 70% ethanol and examined using a stereo microscope at a mag- Disoriented scales were generally confined to a sin- nification of 16–40×.
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