Wetlands Ecology and Management 11: 331–341, 2003.  2003 Kluwer Academic Publishers. Printed in the Netherlands.

331

Density and distribution of water boatmen and brine shrimp at a major shorebird wintering area in Puerto Rico Kimberly J. Tripp

1,2

1, and Jaime A. Collazo *

1

North Carolina Fish and Wildlife Cooperative Research Unit, Biological Resources Division, USGS Department of Zoology, North Carolina State University, Raleigh, NC 27695, USA; 2 Current address: Maine Ecological Services Field Office, U.S. Fish and Wildlife Service, Old Town, ME 04468, USA; * Author for correspondence (e-mail: jaime-collazo@ ncsu.edu; phone: 11 -919 -515 -8837; fax: 11 -919 -515 4454) Received 11 May 2001; accepted in revised form 30 October 2002

Key words: Caribbean, Density, Distribution, Puerto Rico, Salinity tolerance, Salt flats, Shorebirds, Survival, Trichocorixa

Abstract The Cabo Rojo salt flats are an important wintering area for migratory shorebirds. Their quality is intimately related to prey availability, as prey are needed to meet energetic requirements. Understanding prey dynamics is, therefore, a key element of shorebird conservation plans. To this end, we monitored the density and distribution of water-boatmen (Trichocorixa spp.) and brine shrimp (Artemia spp.) in relation to water salinity from September to November of 1994 and 1995. Salinity ranged from 4 to 292 ppt, and gradients were related to hydrological alterations (e.g., salt extraction) and connection to the ocean. Brine shrimp were restricted to areas of highest salinity ($ 106 ppt), whereas water-boatmen to areas of lowest salinity (, 65 ppt). We used aquaria experiments to discern potential mechanisms influencing density and distribution of water boatmen. We focused on this species because its caloric value is similar to the brine shrimp’s, but it occurs in areas of lower salinity where shorebirds are less prone to hyperosmotic stress. We hypothesized that areas devoid of water boatmen exceeded their tolerance limit, and that these limits could hamper survival as individuals move among areas. Experiments showed that an increase of 8.5 6 2.1 ppt, when the base salinity was 40 ppt, induced a 50% mortality rate. From a base salinity of 55 ppt, median survival time decreased curvilinearly across salinity concentrations of 65 to 195 ppt. Median survival was lowest . 100 ppt. Lowering water salinity did not result in osmolal related mortality. Results underscored the sensitivity of water boatmen to high salinity, particularly when the difference in salinity between the ‘source’ and ‘destination’ localities widened. Water boatmen density increased in one lagoon as salinity decreased from 65 to 47 ppt. On the basis of our experiments, local adult survivorship improved and immigration and subsequent survival of adults, if any, was not hindered. The density of nymphs also suggested that hatching occurred concurrently. The foraging value of the salt flats can be enhanced by maintaining salinity at , 65 ppt in selected management units and minimizing differences in salinity concentrations among them.

Introduction The Cabo Rojo salt flats are important habitat for migratory shorebirds in Puerto Rico and the Caribbean (Collazo et al. 1995). At least 22 species of migrant shorebirds use the salt flats annually. The salt flats also serve as a wintering area for Semipalmated (Calidris pusilla) and Western Sandpipers (Calidris

mauri) (Rice 1995). The value of migratory stopovers and wintering areas is intimately related to its prey base (Myers et al. 1987; Skagen and Knopf 1994). Migratory shorebirds frequent saline areas to utilize their abundant prey resources (Mahoney and Jehl 1985). In the Cabo Rojo salt flats, water-boatmen (Trichocorixa [Hemiptera, Corixidae]) and ceratopogonids (Dasyhelea [Diptera, Ceratopogonidae]) con-

332 stitute primary prey species for shorebirds, with brine shrimp (Artemia [Anostraca]) serving as a secondary prey item (Grear and Collazo 1999). The availability of these resources influence the ability of migrants to build up fat reserves for subsequent migratory flights, and ultimately, annual survival rates (Evans and Pienkowski 1984; Morrison 1984; Myers et al. 1987; Colwell 1993; Skagen and Knopf 1994). An understanding of prey base dynamics sustaining migratory shorebirds at key geographic locations is, therefore, a key element of shorebird conservation plans (Weber and Haig 1996, 1997; Hunter et al. 2000). In concert with this need, we set out to determine the density and distribution of water boatmen and brine shrimp across the entire system – Fraternidad and Candelaria lagoons in 1994 and 1995. Ceratopogonids were not present during our study. We also examined temporal changes in salinity and prey density during the study. We used aquaria experiments to further understand the influence of salinity on the density and distribution of water boatmen. Grear and Collazo (1999) reported that water boatmen were restricted to areas of lower salinity. Water boatmen are also capable of flight, hence, movements among management units (or areas) and dispersal from natal areas are possible (Brown 1951). These attributes foster population growth and persistence (see Meffe´ and Carroll 1994). Accordingly, we hypothesized that salinity in areas devoid of water boatmen exceeded their tolerance limits. Furthermore, the probability of surviving away from ‘source’ areas was influenced by the magnitude of the differences in salinity between the ‘source’ and ‘destination’ areas. To test these hypotheses, we determined the maximum salinity increase water boatmen would tolerate when transferred from a base salinity (e.g., areas of high density) to salinity raised by 2 ppt increments (LC 50 ). We also ran an experiment to determine how long water boatmen would survive when transferred to higher salinity without acclimatization (LT 50 ). To increase its relevance to the salt flats, we evaluated nearly all salinity concentrations recorded at the salt flats during our study. Finally, we ran an experiment to evaluate the reverse situation, that is, transferring water boatmen to conditions of decreasing salinity such as those that might arise in the aftermath of rainfall events. We focused our work on water boatmen for several reasons. Although the caloric content of water-boatmen and brine shrimp was not statistically different (Tripp 1996), brine shrimp occurred in areas of higher salinity. Despite the fact that shorebirds forage in

coastal environments, high saline environments may pose hyperosmotic stress on them. In controlled experiments, Purdue and Haines (1977) documented significant weight loss of Semipalmated Sandpipers when fed high-saline water. Circumstantial evidence suggests that salinity stress may have caused the death of some small calidrids at the salt flats (Brian A. Harrington, Manomet Center for Conservation Sciences, pers. comm.). It follows that management efforts should emphasize enhancing the availability of quality prey species (e.g., caloric content) occurring in environments that pose minimum stress to shorebirds. Due to similarities among hypersaline systems, our findings provide valuable insights for shorebird habitat management for other systems in the Caribbean (Chapman 1977; Grear and Collazo 1999; Hunter et al. 2000).

Materials and methods The Cabo Rojo salt flats are located in southwestern Puerto Rico (678129 N, 188579 W; Figure 1). Two large shallow lagoons, Fraternidad and Candelaria, covering approximately 445 ha are the most striking features of the area (see Collazo et al. (1995) for detailed descriptions). Tides flow through two intake areas, and sea water is stored in the main lagoons (C–D, F). Water is channeled to evaporating basins (crystallizers) for salt extraction (e.g., E), creating a salinity gradient across lagoons. Areas A and B are not used for salt extraction. These areas are filled seasonally by tidal flow and rainfall. Mean (6 SE) water depth (cm) for each area in the fall was 5.3 6 0.2 (A), 5.7 6 0.2 (B), 16.2 6 0.5 (C), 15.3 6 0.4 (D), and 16.2 6 0.4 (F). Strips of littoral vegetation, soil and paved roads delineate most of the salt flats, and roads provide access to nearly every location within the salt flats. To the east and south, the salt flats ´ Commonwealth Forest. are bordered by the Boqueron Along their northern boundaries, the salt flats are bordered by the villages of Pole Ojea and Combate, and to the northeast, by the Cabo Rojo National Wildlife Refuge. Prey density and distribution In 1994 and 1995, water boatmen, brine shrimp, rainfall and salinity were monitored for 9 weeks from the first week of September through first week of November. Two sampling plots were established in

333

Figure 1. Map of the Cabo Rojo salt flats showing areas (A–F) and sampling plot locations within areas (S 5 south, N 5 north) in Fraternidad and Candelaria Lagoons, Puerto Rico.

each of areas A, B and C, whereas 4 were established in areas D and F (Figure 1). Plot dimensions were 50 3 30 m. Each plot was divided into 6 divisions along the shoreline and three subdivisions perpendicular to the shoreline. Every plot was sampled once a week. Each week two divisions were selected randomly. From each selected division, two samples from each of two randomly chosen subdivisions were collected. Subdivisions were sampled without replacement. The location and number of plots reflected differences in size (ha) and were aimed at capturing the range of conditions within each unit (e.g., distance to and from culverts, intakes, crystallizers). Plots were also placed in water depth that was # 8 cm. This assured that plots were placed in accessible habitat for small

calidrid sandpipers. Access to foraging habitat in shorebirds is positively related to the length of their tarsusmetatarsus (Davis and Smith 1998). Because even under this set up water volume per samples might differ, we summed all water volumes per sampling occasion and divided all prey by the total volume of water. Because water boatmen and brine shrimp are limnetic, we restricted sampling to the water column. Samples were collected using a plastic cylinder as a column sampler (15-cm radius, 61 cm tall). Upon approaching the sampling unit (division) within plots, we extended our arms (0.5–0.9 m from our torso), dropped the cylinder and pushed it into the substrate to minimize prey loss (Tripp and Collazo 1997).

334 Water within the sampler was emptied and filtered through a 1-mm mesh sieve (Bengston and Svenson 1968). All organisms collected in the extraction were counted and recorded. Water-boatmen were identified as either adult (approx. 4–6 mm) or nymphal (approx. 1–3 mm). Unidentifiable organisms were classified as morphospecies, collected and identified at a later date. All prey density data were expressed as mean number per liter. Salinity measurements were taken with a temperature compensated refractometer (ReichertJung model [10419). Rainfall data were obtained from the Cabo Rojo National Wildlife Refuge (1 km away). Salinity tolerance experiments Water-boatmen were collected from the field and placed in a holding tank (65 3 14 cm) filled with water from the same area where specimens were collected (i.e., 40 to 55 ppt). The holding tank was kept in a shaded area (24–31 8C) and covered with a 1-mm iron mesh. Algae (Cyanophycota spp.) were also collected and placed in tanks to serve as feeding substrate. Water-boatmen replenish their oxygen through air bubbles adhered to their bodies, which make them extremely buoyant. Therefore, we also added sand to the holding tank to provide waterboatmen with an anchoring substrate (Scudder 1976). Water-boatmen were held in the holding tank for 24 hours prior to experimentation. To conduct experiments, glass containers (20 cm diameter) were filled with water from the same area where water-boatmen were collected. A volume of 2,400 cm 3 of water was placed in every container. To increase the salinity of the lagoonal water, salt rocks collected from the crystallizers were used. To decrease salinity, unchlorinated tap water was added to the containers. Six water-boatmen were transferred from the holding tank into each of the containers during each experiment described below. A 1-mm iron mesh covered the opening of each container to prevent water-boatmen from escaping. All experiments were replicated three times. Mortality of waterboatmen was recorded at different time intervals until 50% of the population had died. If after two days, fewer than 50% of the water-boatmen had died, mortality was considered not significant for that specific trial (Rand and Petrocelli 1985). For every experiment, different water-boatmen were transferred into containers without prior acclimatization. The first experiment (Exp. 1) was designed to

determine the maximum salinity increase water-boatmen would tolerate through transfer from a base salinity to salinity raised by 2 ppt increments (i.e., LC 50 ). The second experiment (Exp. 2) was designed to determine how long water-boatmen would survive when transferred to higher salinity without acclimatization (i.e., LT 50 ). This experiment encompassed the range of salinity concentrations recorded at the salt flats. The third experiment (Exp. 3) was designed to determine whether a decrease in salinity would have the same effect on water-boatmen as a corresponding increase. Seven containers were used for the first experiment. The baseline salinity was 40 ppt. Salinity in each of the remaining 6 containers was raised sequentially by 2 ppt, representing a range from 40 to 52 ppt. For the second experiment, we used 16 containers. Lagoonal water for this experiment was 55 ppt. Salinity was increased to the desired range of 65 to 195 ppt. Mortality was monitored hourly until 50% of the water-boatmen died. For the third experiment, 7 containers were also used. Baseline salinity was 55 ppt. Three containers had decreasing salinity, each 10 ppt lower than the preceeding (i.e., 45, 35 and 25 ppt). Conversely, the other three had increasing salinity, each 10 ppt higher than the preceeding (i.e., 65, 75 and 85 ppt). For both experiments, mortality rates were recorded every 6 h for 48 h. Statistical analysis Temporal changes in salinity and prey density during the study were assessed using a repeated measures analysis of variance (ANOVA) with polynomial contrasts (JMP 1994). The only term in the model representing salinity and prey density was area (e.g., A, B). A more complex model was not developed because measurements did not vary among divisions within each of the plots per area (Tripp 1996); therefore, data were averaged within a plot for each week. For prey species trend analysis, only the areas in which they occurred were included in the model. Because there was no significant week component (time trend, P . 0.05) in prey density for either brine shrimp (1994 and 1995) or water-boatmen (1994), prey densities were averaged over all weeks. ANOVA was then used to test whether prey densities differed among areas. The relationship between salinity and prey density was examined using regression analysis. A probit analysis was used to identify the LC 50 based on data obtained from Experiment 1. A Weibull logistic re-

335 gression (JMP 1994) was used to depict the median survival time of water-boatmen when exposed to salinity levels ranging from 65 to 195 ppt, starting with a baseline salinity of 55 ppt (Exp. 2). Only salinity concentrations in which 50% mortality occurred were included in the analysis. The equation used for the analysis was:

S

S

Median survival5B1 B3 1 s12B3de 2

salinity265 ]]] B2

DD

where B 1 5 predicted median survival when salinity 5 65 ppt, B 2 5 coefficient controlling the rate of decline defined as 0.37*B 1 , B 3 5 estimated time of survival beyond the observed maximum salinity tested. To express the average rate of change in median surival time at different salinities, we arbitrarily selected three points on the curve at 40 ppt intervals (i.e., 60, 100, 140 ppt). An estimate of the average rate of change in survival time was calculated as the difference between each of the two intervals (i.e., 60–100 ppt, 100–140 ppt). All tests were considered significant at an alpha level of 0.05. ANOVA met homogeneity of variance assumptions (Levene’s test, P . 0.05). Averages were reported as mean 6 standard error, except mean salinity per area that was reported with minimum and maximum values.

Results Salinity In 1994, areas A and B had the lowest mean salinities in the salt flats, whereas levels in areas C and D were the highest (Table 1). Fluctuations in salinity did not differ between areas A and B during the study (F 5 0.85, d.f. 5 1, 8; P 5 0.38) (Figure 2a). Similarly, salinity fluctuations between areas C and D did not differ significantly (F 5 0.92, d.f. 5 1, 8; P 5 0.40). Fluctuations in areas A and B were significantly different from those in areas C and D (F 5 89.52, d.f. 5 1, 8; P , 0.001). Salinity fluctuations in area F, on the other hand, differed from those in areas A and B (F 5 8.30, d.f. 5 1, 8; P 5 0.02), and from those in areas C and D (F 5 40.72, d.f. 5 1, 8; P , 0.001). The relationship between salinity and rainfall was not significant (P values ranged from 0.55 to 0.95). A time-lag of one week incorporated in the analysis did not improve the relationship. Rainfall between Sep-

tember and early November 1994 averaged 4.36 6 1.61 cm per week (Figure 2a). In 1995, the distribution of salinity concentrations followed the same patterns as in 1994 (Table 1). Fluctuations during the study did not differ between areas A and B (F 5 0.80, d.f. 5 1, 8; and P 5 0.39) (Figure 2b). Similarly, salinity fluctuations in area F did not differ from those in areas A and B (F 5 1.32, d.f. 5 1, 8; P 5 0.28). Fluctuations differed significantly between areas C and D (F 5 24.22, d.f. 5 1, 8; P 5 0.001). Salinity fluctuations in areas A and B differed from those in areas C (F 5 73.19, d.f. 5 1, 8; P , 0.001) and D (F 5 20.84, d.f. 5 1, 8; P 5 0.001). Salinity in area F also differed from areas C (F 5 43.12, d.f. 5 1, 8; P , 0.001) and area D (F 5 8.15, d.f. 5 1, 8; P 5 0.02). The relationship between salinity fluctuations and rainfall in 1995 was not significant (P values ranged from 0.11 to 0.83). Rainfall during September and early November in 1995 averaged 1.34 6 0.57 cm per week (Figure 2b). Prey density and distribution Water-boatmen density did not differ significantly between areas A and B (F 5 0.16, d.f. 5 1, 4; P 5 0.70; Figure 3a). Area F, however, had significantly lower water-boatmen densities than area A (F 5 37.37, d.f. 5 1, 4; P 5 0.002) and area B (F 5 31.94, d.f. 5 1, 4; P 5 0.002). The relationship between water-boatmen density and salinity was not significant in area A (F 5 0.11, d.f. 5 1, 7; P 5 0.75) or area B (F 5 0.74, d.f. 5 1, 7; P 5 0.42). Water-boatmen were initially found only in areas A and B in 1994. They appeared in area F later in the study, coinciding with a decrease in salinity from 65 to 47 ppt. The was an inverse relationship between water-boatmen density and salinity (F 5 13.18, d.f. 5 1, 7, P 5 0.01). Density water-boatmen suggest that, initially, individuals in area F were primarily adults. Hatching contributed to higher densities later in the season (Figure 3b). Brine shrimp were found only in areas C, D and F (Figure 4a). Although area D had the highest density of brine shrimp, densities among areas C, D and F did not differ significantly (F 5 1.73, d.f. 5 2, 3; P 5 0.24). There was no significant relationship between brine shrimp density and salinity (C: F 5 0.86, d.f. 5 1, 7; P 5 0.39; D: F 5 0.33, d.f. 1, 7; P 5 0.58; F: F 5 2.01, d.f. 5 1, 7; P 5 0.20). Water-boatmen were rare in 1995, but present in areas A, B and F (sightings of just a few individuals). Brine shrimp were prevalent in areas C, D and F.

336

Figure 2. Mean salinity (ppt) fluctuations in areas A–F during 9 weeks from first week of September (wk 1) to the first week of November (wk 9) in 1994 (a) and 1995 (b) at the Cabo Rojo salt flats, Puerto Rico. Cumulative rainfall (cm) per week is also depicted.

Table 1. Mean, minimum and maximum salinity (ppt) in areas A–F recorded during 9 weeks between the first week of September and the first week of November in 1994 and 1995 at the Cabo Rojo salt flats, Puerto Rico. 1994

1995

Area

Mean

Min

Max

Mean

Min

Max

A B C D F

30 35 154 150 71

4 4 106 94 46

46 60 212 212 105

45 64 231 226 96

25 28 180 160 40

70 126 292 284 162

337

Figure 3. Mean water-boatmen / l in areas A, B and F during 9 weeks from the first week of September (wk 1) to the first week of November (wk 9) in 1994 at the Cabo Rojo salt flats, Puerto Rico. Plate ‘b’ depicts the mean density of nymphs and adult water-boatmen in area F. Density of adults is given with 1 6 SE.

Their densities in these areas did not differ significantly (F 5 0.46, d.f. 5 2, 3; P 5 0.20) (Figure 4b). The relationship between salinity and brine shrimp density was not significant (F 5 3.25, d.f. 5 1, 34; P 5 0.08). Salinity tolerance experiments The LC 50 for water-boatmen was 8.54 6 2.1 ppt (Figure 5a). The relationship between salinity and median survival time of water-boatmen was negative and curvilinear (Figure 5b). Median survival time decreased at an average rate of 0.27 hours / ppt between salinities of 60 and 100 ppt. The slope of the survival curve began to level off at higher salinities. At salinities between 100 to 140 ppt, median survival

time decreased at an average rate of 0.07 hours / ppt. Experiment 3 demonstrated that decreasing salinity levels from an arbitrary baseline did not affect the short-term survivorship of water-boatmen. No mortality was detected among individuals subjected to salinity ranging from 10 to 30 ppt below the baseline level of 55 ppt.

Discussion Salinity gradients across the Cabo Rojo salt flats were similar to those described for other hypersaline systems (Copeland and Nixon 1974; Chapman 1977). These were related to the extent of hydrological alterations and connection to the ocean. The eastern

338

Figure 4. Mean brine shrimp / l in areas C, D and F during 9 weeks from first week of September (wk 1) to the first week of November (wk 9) in 1994 (a) and 1995 (b) at the Cabo Rojo salt flats, Puerto Rico.

portions of Fraternidad lagoon, areas A and B, maintain their connection to the ocean via two intake channels. Even though area C received ocean water from its respective intake channel, we suspect that backflow from area D caused the similarities between areas C and D. Water exchange between these two areas was possible through a dilapidated plastic dike, once created to divide them. Backflow of hypersaline water from area D is also possible with the aid of westward winds associated with cold fronts during fall and winter (Grear 1992). The cause of intermediate salinity levels in Candelaria Lagoon is not known. It appears that ocean water influx in this system (26.2 ha) is insufficient to counteract the effects of evaporation or sustain decreased salinity

levels caused by rainfall events. Lack of temporal fluctuations in salinity in 1994 and 1995 may be explained by the brevity and timing of our sampling (i.e., September to early November). We designed our sampling to encompass peak shorebird migration (i.e., October, Collazo et al. 1995). By September, tidal flow had flooded most areas and precipitation associated with the fall rainy season neared its peak (i.e., October, Collazo et al. 1995). Thus, it is possible that the influence of both rainfall and tidal flow on salinity had stabilized as opposed to earlier in the season when the salt flats transition from being dry (e.g., A, B) or partially dry (e.g., C, F) to being flooded. Our experiments supported our hypotheses, that is, areas devoid of water boatmen likely had salinity

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Figure 5. Percent mortality of water-boatmen mortality when directly transfered into salinity increased by 2 ppt from a baseline of 40 ppt (plate a). Observed values represent mean (n 5 3). Interpolated value of 8.54 ppt represents the salinity increment at which 50% of the water-boatmen died after 24 hrs. Predicted values obtained using a probit analysis. Median survival time (hours) of unacclimatized water-boatmen when placed in different salinity concentrations (ppt) from 65 to 165 ppt. Predicted values obtained using a Weibull logistic regression.

concentrations that exceeded their tolerance limits. It took an increase of only 8.2 ppt to induce a 50% mortality rate for water boatmen that came from a base salinity of 40 ppt. Our experiments also suggested that, if movement among units occurs, survival is hindered as the difference in salinity between the ‘source’ and ‘destination’ locations widened. Changes in salinity from 55 ppt (baseline) to conditions of . 100 ppt yielded the lowest survival rates. These inferences were consistent with the fact that waterboatmen were present in areas of lowest salinity (i.e., A, B). We did not record water-boatmen in areas C or D. Grear (1992) reported water boatmen in area C with a salinity of 118 6 10.6 ppt. This was in sharp

contrast to the 154 ppt (1994) and 231 ppt (1995) recorded during this study. However, Grear (1992) reported significantly lower density of water-boatmen in area C (0.3 6 0.3 / l) than in area A (20 6 3.0 / l, 33.0 6 4.4 ppt), and such differences were consistent with inferences drawn from our experiments (e.g., Exp. 1, 2). We suspect that the presence of waterboatmen in area C reported by Grear (1992) was facilitated by inflow of ocean water (e.g., pumps associated with salt extraction operations), which were not operating during our study. In light of our experiments it was not surprising that the dominant prey species in areas of intermediate (i.e., F) or highest (i.e., C, D) salinity were brine

340 shrimps. Salinity ranges and distribution recorded in this study matched the optimum salinity range for viable brine shrimp populations (i.e., 70–175 ppt; Carpelan 1957; Davis 1980). The halophytic affinities of brine shrimp were also gleaned from inspecting weekly density and salinity fluctuations. In 1994, salinity was higher earlier in the study (September), as were densities of brine shrimp. Conversely, in 1995, the correlation between higher salinity and density was recorded later in the study (late October). Our experiments also shed light on the mechanisms behind the increase of density of water boatmen recorded in area F in 1994. The increase coincided with a drop in salinity (65 to 47 ppt). We inferred that salinity decreased sufficiently to enhance the survival of those water boatmen already present in the area. The rapid increase of adults suggested that immigration was plausible. If so, experiments suggested that survival of immigrants would not have been hindered. Lower salinity also fostered hatching as indicated by the increasing density of nymphs (see Davis 1966). These same mechanisms and responses (e.g., hatching) may explain responses noted by Grear and Collazo (1999) when they suggested that bursts of water boatmen followed episodic rainfall events. Waterboatmen breed year round in tropical environments (Scudder 1976); however, high precipitation events could trigger population bursts in response to suitable habitat characteristics. Most notable of these is algal growth, which provides cover and feeding substrate for water-boatmen (Grear and Collazo 1999). Unlike the negative effects of salinity increases, water-boatmen were resilient to significant drops in salinity, as indicated by Experiment 3. Water-boatmen were notably absent in 1995, even in area A where salinity levels averaged 45 ppt. We speculate that higher salinity levels across the system, as compared to 1994, hampered demographic growth. Certainly, the possible role that rainfall event plays in lowering saline concentrations was notably different in 1995 when compared to 1994. Rainfall in 1995 averaged 1.34 6 0.57 cm per week whereas it averaged 4.36 6 1.61 cm in 1994. The long-term average for the period encompassing the 9 weeks of our study was 4.67 per week (n 5 15 years, Tripp 1996). Although water-boatmen may occur in areas of high salinity (e.g., 153 ppt; Carpelan 1957), our experiments suggest that such conditions are not ideal for productive (e.g., hatching) and viable populations (see also Davis 1966). We did not assess chronic mortality associated with gradual increase in salinity due to

evaporation, but results from Experiment 2 indicated that survival rates decrease with increasing salinity. The decreasing trend in survival may reflect that water-boatmen under osmolal stress are prone to higher mortality rates than those at lower salinity (e.g., ocean concentration).

Management recommendations Although the salt flats’ hydrology has been altered for salt extraction, management can enhance their foraging value to shorebirds by manipulating salinity and depth. Potential areas for management include A, B, C and portions of F. Hydrologic management should strive to maintain salinity at concentrations that promote local production (e.g., hatching) and survival. Our findings suggest that salinity concentrations of , 65 ppt meet both requirements. Moreover, salinity concentrations among selected management units should be maintained as close as possible to minimize mortality of dispersing individuals. Grear (1992) identified water-boatmen and ceratopogonid flies as primary prey species for small calidrids, with brine shrimp as a secondary preference. Because waterboatmen and ceratopogonid flies co-occur in the same areas (Grear 1992), management for low salinity would also benefit ceratopogonid flies. Water depth is relevant because it influences the proportion of habitat accessible to foraging shorebirds. The shorebird community foraging in the salt flats requires water depths of , 8 cm (Collazo et al. 1995; Davis and Smith 1998). Lower water levels also provide an opportunity for algal mats to develop (, 10 cm) (Odum et al. 1971) and are important for egg laying, pupation and adult emergence of ceratopogonid flies (Linley 1976). Our findings shed some light on the compatibility of salt extraction operations and shorebird habitat management. For example, clearing the intake channel for area C and a functional dike (or dikes) between areas C and D would facilitate tidal flow into area C while avoiding dilution of brine in area D, essential to salt extraction. Tidal flow would lower salinity in area C, fostering the presence of prey species. Compatibility arrangements need only to occur seasonally. Migratory shorebirds rely on the salt flats during late summer and fall. Resident shorebirds (e.g., Snowy Plover, Charadrius alexandrinus) are adept at using resources associated with the salt flats during spring and summer months, when the salt flats receive less

341 rainfall (i.e., dry season) and tidal flow is low (Lee 1989; Collazo et al. 1995).

Acknowledgements We thank the U.S. Fish and Wildlife Service and J. Oland for supporting this project. We also thank J. Cruz, M. Rivera, M. Schaefbauer for their assistance in the field, B. Harrington for his insights about the salt flats, and C. Brownie for their assistance with statistical analyses. We are grateful to S. Mozley, T. Kwak and an anonymous reviewer for helping us improve the presentation of the material.

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