Neritina Virginea Upstream Migrations

Floods, Habitat Hydraulics and Upstream Migration of Neritinavirginea (Gastropoda: Neritidae) in Northeastern Puerto Rico

JUAN F. BLANCO1 AND FREDERICK N. SCATENA2

1Department of Biology, University of Puerto Rico, Rio Piedras Campus, P.O. Box 23360, San Juan, Puerto Rico00931–3360. Corresponding author: [email protected], [email protected]

2Department of Earth and Environmental Sciences, University of Pennsylvania, Philadelphia, PA 19104–6313

ABSTRACT.—Massive upstream migrations of neritid snails (Neritidae: Gastropoda) occur in tropical andsubtropical streams worldwide, but their seasonality and proximate causes are unknown. We monitoredmassive upstream migrations of Neritina virginea for 99 weeks, and conducted a detailed study of snaildensity, size, and hydraulic descriptors in lower Río Mameyes, northeastern Puerto Rico. The study assessedthe 1) timing and seasonality of upstream migration, 2) size composition of migratory aggregations, 3)patterns of habitat use, and 4) role of floods on upstream migration. Massive upstream migrations (500–3000ind/m2) were observed in 44 of 99 weeks of observation. While N. virginea aggregations occurred at randomtime intervals, they were clumped during rainy periods. Migratory aggregations consisted mostly of smallindividuals (5–7 mm). Greater mean density was consistently observed in a stable riffle than in an unstablerun (115.7 and 17.8 ind/m2, respectively), but mean density increased and mean size reduced in both reachesduring the first 7 upstream migratory events. N. virginea density and size dynamics differed between reachesas a function of habitat hydraulics. While juveniles used the stable riffle as a permanent habitat andpreferred passageway, they also used an adjacent, unstable reach after storm events. Density variation wascorrelated with days postflood (>3.5 m3/s) in both reaches. Our observations indicated that massive upstreammigrations of N. virginea juveniles occur at least once a month, presumably as habitat-dependent responsesto floods.

KEYWORDS.—Neritid snails, diadromy, physical habitat, disturbances, Neotropical streams

INTRODUCTION

In coastal and insular streams and rivers,migrations between marine and fresh wa-ters (i. e., diadromy) are common amongaquatic fauna (Ford and Kinzie 1982; Mc-Dowall 1998). Many species of fish, shrimp,crayfish, and crabs exhibit this type of mi-gration (Baker 1978). Nevertheless, migra-tory events have been less frequently re-ported in gastropod mollusks; although itis known that at least 13 families includemigratory species (Huryn and Denny1997). Among tropical gastropods, the fam-ily Neritidae comprises several freshwatergenera (subfamily Neritinae) whose indi-viduals migrate upstream in massive ag-gregations. Such migrations of freshwaterneritids were reported in Hawaii (Ford1979; Ford and Kinzie 1982), Costa Rica(Schneider and Frost 1986; Schneider and

Lyons 1993), Japan (Nishiwaki et al. 1991a;Hirata et al. 1992), French Polynesia (Reshet al. 1990, 1992; Liu and Resh 1997), andPuerto Rico (Covich and McDowell 1996;Pyron and Covich 2003).

Recently, mark-and-recapture studies innortheastern Puerto Rico suggested thatneritid gastropods are more active andtravel longer distances during given peri-ods of the year and that upstream migra-tion may be seasonal (Pyron and Covich2003). However, other one-year mark-and-recapture study on a neritid gastropod insouthern Japan showed no seasonal occur-rence of upstream migrations, or seasonalchanges in mean distance movement(Nishiwaki et al. 1991a). These findingscontrast with another study in the samearea, showing that maximum travel dis-tance varies over the year, being greaterduring the period of high water tempera-ture between April and August (Hirata etal. 1992). Records of gastropod density andegg laying in French Polynesia (Resh et al.1991, 1992) and Japan (Nishiwaki et al.

ms. received April 12, 2004; accepted November 15,2004

Caribbean Journal of Science, Vol. 41, No. 1, 55-74, 2005Copyright 2005 College of Arts and SciencesUniversity of Puerto Rico, Mayaguez

55

1990b; Hirata et al. 1992) also suggest a sea-sonal occurrence of such migrations, butthe controlling factors remain unknown.There are no additional long-term, high-frequency studies dealing with upstreammigrations of neritid gastropods, althoughother aspects such as life history (Ford1979), growth rates, and fecundity (Shi-gemiya and Kato 2001), habitat selection(Liu and Resh 1997; Ohara and Tomiyama2000), and predators (Teixeira 1994; Resh etal. 1999) were studied elsewhere.

Schneider and Lyons (1993) proposedthat upstream migrations of neritids in aCosta Rican stream were related withincreased fish predation in the estuary.Small-sized individuals were more abun-dant within migratory groups, and theywere also more responsive to the presenceof predators, as similarly observed in otherfreshwater gastropods (e.g., Alexander andCovich 1991). The distribution of predatoryfish (Allan 1995), and the quantity andquality of periphytonic food (Johnson andBrown 1997; Biggs and Smith 2002) can alsobe correlated with the spatio-temporalvariations in discharge and water velocity.Thus the occurrence of upstream migra-tions might ultimately be a function ofstream discharge and channel hydraulics.For example, laboratory experiments usingclams demonstrated that emigration is dis-played only after increased water move-ment, even when density-dependent com-petition is strong under slow watermovement (Powers and Peterson 2000). Innatural conditions, the flash flood distur-bance can be an important control of streamcommunity dynamics (Hart and Finelli1999; Lake 2000). Several studies documentthat invertebrate abundance is a function ofthe elapsed time after storm flows in bothtropical and temperate streams (Grimmand Fisher 1989; Flecker and Feifarek 1994;Ramírez and Pringle 1998). Recent studiesalso suggest that the effects of storm flowon benthic fauna are mediated by habitatstability (reviewed by Lake 2000). Habitatsexperiencing greater scouring such as runsand plane beds (Matthaei et al. 1999a, b)show lower abundance and persistence ofbenthos than more resistant riffle and poolhabitat (e.g., Gjerløv et al. 2003).

Measuring habitat stability in flashytropical streams is logistically difficult. For-tunately, channel hydraulics may be usedto estimate the forces experienced bystreambed elements and organisms (Now-ell and Jumars 1984; Statzner et al. 1988;Davies and Barmuta 1989; Way et al. 1993).If measured close to the streambed, stan-dard Reynolds number (Re) and roughnessReynolds number (Re*) indicate if micro-flows are turbulent (Re>2000), laminar(Re<500), rough (Re*>70), or smooth(Re*<70). Similarly, Froude number (Fr) in-dicates if near-bed flows are supercritical(i.e., erosive, Fr>1) or subcritical (i.e., depo-sitional, Fr< 1). Typically, flood stable habi-tats have larger streambed elements, andmore turbulent and rough flows. Unstablehabitats generally have fine-grained sub-strates and experience nearly laminar orsmooth flows at baseline discharge (Nowelland Jumars 1984; Davies and Barmuta 1989;Naiman 1998; Montgomery and Buffington1998; Matthaei et al. 1999a, b).

In this study we tested the following hy-potheses: 1) upstream migration events ofneritid gastropods are seasonal, 2) migra-tory aggregations consist of small-sized in-dividuals, 3) individuals use turbulent,rough flows as passages during upstreammigrations and as permanent habitats, and4) influence of flood regime on the distri-bution of neritid gastropods depends onhabitat hydraulics and stability.

MATERIALS AND METHODS

Study organism

The presence of the freshwater neritidNeritina virginea (Linné 1758) in several is-lands of the Caribbean has been noted inmany studies, some from the middle of lastcentury (Russel 1941; Aguayo 1966; Hum-frey 1971). Other species have also been re-ported in the region (Russel 1941; Aguayo1966; Humfrey 1971), but may be colorvariants of N. virginea (Cosel 1986; Diaz andPuyana 1994; J. F. Blanco, unpublisheddata). While the presence of N. virginea inthe Caribbean is well documented, massiveupstream migrations have been recentlydocumented in two streams (e.g., Mameyes

JUAN F. BLANCO AND FREDERICK N. SCATENA56

and Espíritu Santo) in northeastern PuertoRico (Covich and McDowell 1996; Pyronand Covich 2003).

Study area

This study was conducted in a lower seg-ment of Río Mameyes, draining the Lu-quillo Experimental Forest (LEF), located innortheastern Puerto Rico (Fig. 1a). The up-per part of the watershed, managed by theUnited States Forest Service, is covered bytropical wet forests (Scatena 1989). Thelower part of the watershed is suburban-ized, but has extensive abandoned pastures(Ramos 2001). Río Mameyes is consideredthe most conserved stream in Puerto Rico,and is gauged by the US Geological Survey(USGS). The highest discharge is typicallyobserved during the two rainy seasonsof the year: May and August-December(Fig. 1b).

The study site is located beneath Bridge

1771 of road PR Route 3 (18°22’27”N,65°45’50” W, elevation: 5 m above sea level)over the Río Mameyes, where two reaches,separated by an elevated and stabilized is-land formed after the construction of thebridge in 1982. Most of the river’s flow runsthrough a ∼11 m wide the main reach (MR:a riffle at right and looking downstream).Channel depth is nearly constant across thesection (<40 cm), and the streambed con-sists of mid-sized boulders (<50 cm) andcobbles. The right bank of the reach is aconcrete-lined bridge abutment. Less waterflows through a side reach (SR) that occurson the opposite side of the bridge. Thisreach is 3 m wide, less than 30 cm deep,and is influenced by deflected flow from achannel bend located 5-m upstream. Thestreambed consists of cobbles in the deep-est part and of gravel in the shallowest part.The MR and SR join about 40 m down-stream, and this point becomes a decision-making area for the migratory organismsmoving upstream.

FIG. 1. A. Location of the study site (square) under PR Route 3 Bridge 1771 in Río Mameyes, NortheasternPuerto Rico. B. Discharge regime at the study site (note logarithmic y-axis) based in the 1998–2001 record (USGSgage 50066000 located 50 m upstream the bridge). LEF = Luquillo Experimental Forest.

NERITINA VIRGINEA UPSTREAM MIGRATIONS 57

Sampling

Occurrence of massive upstream migra-tions (Fig. 2) of N. virginea was monitoredweekly to fortnightly between August 2000and July 2002 for 99 weeks of observations.On 44 of these weeks high densities (> 500ind/m2) of small individuals that were ar-ranged in trails or groups were observedmigrating on the bridge abutment in MR(Fig. 2).

In addition to the long-term monitoring,we conducted a detailed weekly study be-tween August and December 2000. Sam-pling was restricted to periods when theinstantaneous stream discharge was lowerthan 10 m3/s. Individuals were countedwithin 0.5 × 0.5 m quadrats (n = 10) placedon the streambed in MR and SR under thebridge during each sampling. All individu-als within each quadrat were collected tomeasure aperture width using a caliper(0.05 mm). Individuals were divided intothe following size groups: <4.00 mm

(spats), 4.00-6.00 mm (early juveniles), 6.00-8.00 mm (late juveniles), and >8.00 mm(adults). This grouping was based on pre-liminary field observations indicating dis-tinctive behavior relative to individual size(cf., Pyron and Covich 2003). Spats hadsmall and smooth, dark-brown shells, andwere usually found underneath rocks. Ju-veniles exhibited greenish coloration with avariable pattern of axial lines or small yel-low “tongues.” These juveniles were verymobile and were commonly found on thesides of rocks. Adults exhibited the samecoloration as juveniles, but moved ran-domly and were more common on the topof rocks. Sexual maturation was not consid-ered for the grouping because it may bevariable in tropical neritids (Ford 1979),and it is not easy to determine in smallsized individuals (J. F. Blanco, pers. obs.).

Water velocity was measured 2 cm abovesubstratum (shear velocity) with an electro-magnetic flow meter (Flo-mate™, Marsh-McBirney) in points spaced 0.5 m across the

FIG. 2. Massive upstream migrations underneath the bridge PR Route 3 at the MR in Río Mameyes. A. Longtrail after a large flood. B. Short trail after small flood. C. Close-up showing individual N. virginea in trails. Noteindividual displacement (broken arrow) against the flow.


section of each reach. Three to five watervelocity measurements (averaged over 30s) were made at each point. During a singlesurvey at the beginning of the study, thedominant substrate type was visually cat-egorized as boulders, cobbles, pebbles,gravel, and finer particles. Discharge datafor the sampling period were obtainedfrom the USGS gage 50066000 (http://waterdata.usgs.gov/pr/nwis), located 20m upstream from the study segment.

Data analysis

Since streamflow regime in the studyarea varies moderately with season, we hy-pothesized that the occurrence of massivemigrations of gastropods may also varythroughout the year. Several insect studiesin tropical streams suggest that intra-annual population dynamics may be corre-lated with seasonal variation in eitherstream discharge or rainfall (McElravy etal. 1982; Wolda and Flowers 1985; Mastellerand Flint 1992; Masteller and Buzby 1993).For this reason, circular statistics were usedto test for uniform distribution and uncoverany seasonality (Batschelet 1982; Zar 1999).A Rao’s spacing test was first conducted fortwo one-year periods: August 2000-July2001, and June 2001-July 2002. Since wemade weekly observations, each one-yearperiod was equaled to 52 weeks. Also, eachyear was considered to be a round of 360°and, for that reason, this value was dividedinto 52 intervals of 6.9° (equivalent to oneweek). Accordingly, each upstream migra-tion event had an exact location, expressedin degrees, into the one-year round. Basedon the spacing of the migratory events, aU-statistic was computed and compared toa normally distributed theoretical value(Batschelet 1982). The null hypothesis thatupstream migration events were uniformlydistributed throughout the year would berejected if the computed U value wasgreater than the theoretical value. In addi-tion, the mean vector length (r) was com-puted as a measure of angular dispersion ofupstream migratory events on one-yearrounds. Mean vector varies between 0 and1, and therefore, low values indicate widedispersion, and high values indicate nar-

row dispersion, and greater concentrationof observations.

Dispersion was high (r < 0.2) in both one-year rounds (2000-2001 and 2001-2002) be-cause the distribution of migratory eventswas not unimodal. Visual exploration ofour data suggested that upstream migra-tion peaked at least once every calendarsemester, and therefore our original dataset was further subdivided into the follow-ing four periods: August-December 2000,January-June 2001, July-December 2001,January-June 2002. Within each of the newfour periods, the mean angle (�) and themean vector length (r) were computed asmetrics of central tendency and dispersion,respectively.

To determine under what hydrologicconditions upstream migrations occur, weused a discriminant function analysis(DFA, Statsoft 2003). The mean monthlydischarge, monthly minimum and maxi-mum, coefficient of variation, and numberof floods greater than 3.5 and 18 m3/s werecalculated using the daily stream dischargerecord for the 99 weeks (Fig. 3). These de-scriptors of discharge regime were used tostep-wise discriminate among months with�1, 2, and �3 weeks of migrations usingthe Statistica® software (Statsoft Inc.). Size-frequency distributions were also derivedfor several migratory aggregations and aOne-Way ANOVA was used to test if meanindividual size in migratory aggregationschanged over time.

To determine the temporal variation inhabitat use and hydraulics we conductedthe following analyses. The flows at eachreach were classified as either chaotic ornon-chaotic, whether or not the rocks wereexposed above the water surface. Secondly,Reynolds (Re), and Froude (Fr) numbers(Allan 1995; Appendix) were calculated tofurther classify the flows in both reaches ateach sampling date. Temporal variation offlow type between reaches was explored bya Two-way ANOVA (reach x date) usingshear velocity, Re and Fr as response vari-ables. A second Two-way ANOVA wascalculated after pooling the sampling datesinto three groups according to instanta-neous discharge: two, three and fivetimes the mean discharge (2-2.5, 3.0-3.5,


and >5 m3/s, respectively). Two-wayANOVA was preferred over RepeatedMeasures ANOVA because the same plotsand the two reaches were not alwayssampled on the same day. To assess habitatstability we used the percent of change

over time for the above hydraulic variables.More stable habitats are considered to havesmaller changes over time, as already dem-onstrated in streams in temperate deserts(Grimm and Fisher 1989) and forests (Gjer-løv et al. 2003).

FIG. 3. A. Number of weeks per month when massive upstream migrations (Fig. 2) were observed at the MR.B. Mean monthly discharge (circles) between August 2000 and July 2002. Minimum and maximum dailydischarges are indicated with a vertical line. Note logarithmic y-axis. C. Coefficient of variation of daily dis-charge throughout the month. D. Number of floods greater than 3.5 (open circles) or 18 (filled circles) m3/s permonth. Boxes in B to D indicate periods when massive migrations occurred at least during two weeks. The thicklines show the running average.


Densities and sizes of N. virginea col-lected from August to December 2000 weretransformed logarithmically to meet ho-moscedasticity for statistical tests. The ho-mogeneity of variance of non-transformeddata over time and between study reacheswere also tested in a one way fashion usingLevene’s test and in multiple-ways usingthe Box-M and Sen and Puri’s tests. A Two-way ANOVA was used to test differencesof density and size between reaches andsampling dates (Zar 1999), and we used aG-test to determine uniformity of sizegroups over time within each reach (Sokaland Rohlf 1994).

To determine proximal causes of up-stream migrations, mean gastropod densityand its coefficient of variation (CV) wereregressed against commonly used descrip-tors of the frequency and magnitude of flow-related disturbances (Allan 1995; Clausenand Biggs 1997; Biggs and Smith 2002). Theseparameters included mean discharge duringthe last 24 hrs (QMED24), instantaneous dis-charge (QINST), number of flashfloods dur-ing the previous week (#Q/WK), and num-ber of days since a flood of given magnitude(DAYSSINCEQ). Intense rains frequently im-pact northeastern Puerto Rico and produceflashfloods that are readily identifiable by thesudden rising and falling limbs relative to thebase flow (Fig. 5c). Flashfloods in Río Mam-eyes are characterized by instantaneous dis-charge >3.5 m3/s (duration 20% of time) (At-kins et al. 1999). Large tropical storms andhurricanes may produce storm flows occur-ring less than 1% of time and promotingoverbank flows and streambed scouring(Scatena and Larsen 1991). We included in-termediate and large storm flows (instanta-neous discharge: >18 and >36 m3/s, dura-tion: <1 and 0.5% of time, respectively) toaccount for large and infrequent distur-bances.

The interdependency among flood re-gime parameters was explored using corre-lation analysis. Weekly snail density rec-ords were not autocorrelated as migratoryaggregations observed in one week movedupstream and were replaced by a new ag-gregation the following week. Step-wiseMultiple Regression Models (Zar 1999)were independently derived for the mean

and the CV of gastropod density at eachreach. Similar regressions were computedusing gastropod mean size and percent ofindividuals per cohort as response vari-ables. Finally, we explored several simplelinear and non-linear regressions modelsbetween the elapsed time after storms andour biotic variables since this variable hasbeen repeatedly used as a good predictor oflotic macroinvertebrate abundance in pre-vious studies (e.g., Grimm and Fisher 1989;Flecker and Feifarek 1994; Ramírez andPringle 1998).

RESULTS

Seasonality of massive upstream migrations

Forty four migratory aggregations of N.virginea were observed throughout the 99weeks of sampling, 20 during the first yearand 24 during the second (Fig. 3a). Migra-tions did not occur uniformly during eitheryear: August 2000 to July 2001 (Rao’s spac-ing test: U = 3220, n = 20, P < .01; meanvector, r = .02) and June 2001 to July 2002(U = 3900, n = 24, P < .01; r = .11). Whenmigration records were analyzed over6-month periods, clustering was more evi-dent. During the first year, most migrationswere observed in October 2000 (meanangle: � = 359) and in May 2001 (� = 179).In contrast, during August to December2001, and January to July 2002, massive mi-gration events occurred at least monthly (r= .1 and 0, respectively). Nonetheless, mi-grations occurred at least during threeweeks from September through October2001, and January through March 2002.

The occurrence of massive upstream mi-grations of N. virginea was strongly relatedto stream discharge (Fig. 3b-d). The bestdiscriminant function (Wilk’s � = 0.16,F16, 24 = 2.28, P = .032) included the meandaily discharge, and the maximum andminimum discharge for both the observedand the previous month. The coefficient ofvariation of daily discharge of the previousmonth, and the number of floods (daily dis-charge >3.5 m3/s) during the observedmonth were also included. Multivariatedistance between the groups of �1 and 2weeks with migrations was not significant(Mahalanobis squared distance MSD =


8.79, F8, 12 = 2.23, P = .16). In contrast, therewas a significant distance between thegroups of 2 and �3 weeks with migrations(MSD = 8.79, F8, 12 = 3.15, P = .036). Themonths with �3 weeks with migrationsshowed a mean discharge ranging between1 and 2 m3/s, and they were preceded bymonths with higher mean discharge thanmonths with �1 weeks with migrations(2.0 and 1.3 m3/s, respectively) (Fig. 3b).The maximum discharge ranged between3.8 and 8.1 m3/s in months with �3 weekswith migrations, while the other groups(�2 weeks) showed up to >20 m3/s (Fig.3b). Months with �3 weeks with migra-tions were preceded by months with inter-mediate maximum (8-10 m3/s), higherminimum discharges (0.4-0.7 m3/s) (Fig.3b), and less variable daily discharges (in-terquartile range of CV = 70-120%). Dailydischarge was significantly greater inmonths with �3 weeks with migrations(CV: 88->200%, Fig. 3c). Months with �3weeks with migrations presented between1 and 3 floods, those with fewer migrationspresented between 1 and 6 (Fig. 3d).

The mean daily discharge in the RíoMameyes is typically greater during May,and between August and December (Fig.1b). High discharge was observed from Au-gust to January 2000, and from April toMay 2001 (Fig. 3b), matching observed pat-terns of massive migrations in the period2000-2001 (Fig. 3a). In contrast, the secondyear was atypically wet and had high meanmonthly discharges from August 2001 toJanuary 2002 and April and May of 2002(Fig. 3b). In summary, massive upstreammigrations occurred during periods of re-ceding waters after high discharge periods(August-October 200; May-June, and Au-gust-November 2001; January-March 2002).

We determined gastropod size composi-tion of migratory aggregations based ongroups collected in seven sampling datesbetween August 2000 and June 2001.Aggregated individuals ranged between2.43 and 12.90 mm, but 50% fell in the 5-7mm range. The overall average size was6.05 ± 1.13 mm, but mean size was signifi-cantly different among migratory groups(One-way ANOVA: F6, 860 = 20.3, P < .0001,Fig. 4). The variance of size also changed

among migratory aggregations (F6, 860 =11.68, P < .0001).

Habitat hydraulics and stability

Daily stream discharge showed a markedvariation during August to December 2000(Fig. 5c). Over this period, 14 flood dayswere evident and had magnitudes from 2to approximately 100 m3/s. Five eventswere greater than 10 m3/s (Fig. 5c). Thetwo study reaches had marked differencesin terms of hydraulics (Table 1) and stabil-ity to those flashfloods and storm flows.The MR showed slightly faster, but signifi-cantly more variable water velocities thanthe SR (Two-way ANOVA: F1, 489 = 1.04, P= .31, mean ± s.d., MR: 0.30 ± 0.30 m/s, SR:0.27 ± 0.20 m/s; homogeneity of variancetest: F1, 489 = 11.48, P < .001). The fast watervelocities at both reaches promoted turbu-lent (mean Re > 2000), but non-erosive (Fr <1) flows during discharges <3.5 m3/s. Dur-ing relatively small storms (>5.0 m3/s), tur-bulence increased with velocity in bothreaches, but more dramatically in the SR(among discharge periods: F2, 485 = 10.75, P< .001, discharge period and reach interac-tion: F2, 485 = 2.88, P = .057). Flows becamemore erosive (Fr∼1) in parts of bothreaches, particularly at the SR when dis-charge was greater than 5.0 m3/s. The fastflows along with larger streambed ele-ments (cobbles and boulders) in the MRpromoted chaotic and rough microflows(mean Re* > 30000) at intermediate dis-charge (<3.5 m3/s). Flows were less chaoticand smoother (mean Re* > 10000) in thesmall roughness elements of the SR(pebbles and cobbles) in the streambed. Athigh discharge, however, rough micro-flows increased faster in the SR than at theMR. The degree of change of the abovevariables between low discharge and stormflow dates was in the range of 100-200% inthe SR and of 100-150% in the MR and in-dicates that scouring in the SR during flash-floods and storm flows may be greater be-cause of the smaller substrates.

Upstream migration, gastropod density,and size

Snail density varied significantly overtime (F8, 156 = 5.75, P < .0001, Fig. 5a-b),


and increased 2 to 10 times during migra-tions (200-800 ind/m2). This was particu-larly evident at SR (interaction, F8, 156 =2.37, P < .019). Mean density was signifi-cantly higher at the MR than SR, where itdropped to nearly zero during non-migration periods (mean ± s.d., MR: 115.7 ±118.4 ind/m2, n = 86, SR: 17.8 ± 33.8 ind/m2, n = 78; F1, 8 = 99.95, P < .0001). At least,seven migratory events were observed inthe MR (Sep 5, 19, Oct 3, 17, Nov 7, 14 and28, Fig. 5a). Only five were observed in theSR (Fig. 5b) and all occurred after floods(Fig. 5c).

Shell size changed significantly betweenAugust and December 2000 (Fig. 6), as evi-denced by the oscillation of the variance

(F9, 1229 = 37.92, P < .01). Shell size variationwas smaller at dates when gastropod den-sity was higher (i. e., during massive mi-gratory events). By analyzing each reachseparately, mean size did not changed overtime at the MR (F8, 931 = 0.63, P = .75). Vari-ance did change over time (F8, 931 = 26.07, P< .01). At the SR both mean size and vari-ance changed significantly over time(means: F8, 290 = 13.17, P < .0001; variances:F8, 290 = 8.58, P < .0001). Mean size alsoshowed differences between reaches, beingsmaller at the MR than at the SR (mean ±s.d., MR: 6.3 ± 2.8 mm, n = 940, SR: 7.6 ± 2.4mm, n = 299; F1, 1237 = 54.55, P < .0001;homogeneity of variance test: F1, 1237 = 3.02,P = .082).

FIG. 4. Size-frequency distributions of N. virginea in migratory aggregations during 7 seven dates betweenAugust 2000 and June 2001.


Differences in mean size between reacheswere related to differences in size structureof the snail population (Fig. 6, G-test forgoodness of fit to uniform size distribution,MR: G adj (24) = 333.66, P < .05, SR: G adj(16) = 120.23, P < .05). While juveniles weredominant in both reaches, the early cohortdominated in the MR and late cohort in theSR. Adults were smaller in the MR, butmore frequent and less variable over time

(10-30% of sample); while at the SR theywere less frequent and more variable overtime (0-100% of sample). Finally, spatswere frequently recorded at the MR, butnever observed at the SR.

Discharge regime and upstream migration

The variables used to characterize distur-bance regime were not redundant, provid-ing different information to be correlated to

FIG. 5. Variation in N. virginea density at the Main and Side reaches (A and B, respectively). Circles: median.Whisker: interquartile range. Asterisks: extremes. Migrations are indicated with open circles, where size isproportional to the size of migratory aggregations. Closed circles indicate non-migratory events. C. Mean dailydischarge between August 1 and December 31, 2000. Arrows: sampling dates. Open circles: migratory events.Numbers: flashfloods and storm flows. Horizontal line: Overall median discharge (1.5 m3/s) based in historicalrecord for USGS gage 50066000. Note logarithmic y-axes.


variation in gastropod density and size inthe studied reaches (Table 2). Instantaneousdischarge (QINST) was weakly correlatedto median discharge during the last 24hours (QMED24), suggesting that thehydrography is very flashy. In addition,QINST decreased with time after flash-floods (Q > 3.5 m3/s) and small storm flows(Q > 18 m3/s), but was less correlated withvery large storm flows (Q > 36 m3/s) thatwere less frequent. Elapsed time since aflashflood or a small stormflow event(DAYSSINCEQ) was negatively correlatedwith the number of events during theprevious week (#Q/WK). F ina l ly ,DAYSSINCEQ3.5 and DAYSSINCEQ18were strongly correlated, because mosthigh flow events occurring during a week

are flashfloods that override the effects ofsmall storm flows.

The mean gastropod density and its co-efficient of variation (CV), as well as meansize and frequency distribution of the dif-ferent cohorts were correlated with theflood regime at Río Mameyes. However,the relationships differed between reaches.At the MR, no single disturbance variableplayed a major role on the dynamics of gas-tropod variables. The #Q>3.5/WK and#Q>18/WK showed stronger positive ef-fects on the percent of juveniles, whilenegative effects on the percent of spats andadults. In contrast, at the SR, more descrip-tors of disturbance regime were related togastropod variables. Both QINST and#Q>3.5/WK were positively related to

TABLE 1. Hydraulic characteristics of the reaches in lower Rıo Mameyes, Puerto Rico. Low daily discharge:2.0-3.5 m3/s. Intermediate daily discharge (flashfloods): >5 m3/s. N = 8 sampling dates.

Variable StatisticMainreach

Sidereach

Bankfull width (m) 11 3Base flow depth Mean 30 20

D (cm) Min-Max 10-50 5-30Dominant substrate Boulder Cobble

Cobble PebbleSubstratum roughness Mean 20 5

k (cm)Near-bed flow type1 Chaotic flow Non-chaotic flow

Lowdischarge

Intermediatedischarge

Lowdischarge

Intermediatedischarge

Shear velocity2 Median 0.19 0.29 0.20 0.37U* (m/s) Interquartile 0.10-0.40 0.15-0.45 0.12-0.36 0.14-0.52

Min-Max 0.00-1.10 0.00-1.65 0.00-0.50 0.00-1.14Reynolds number3 Median 3800 (T) 5800 (T) 3800 (T) 7400 (T)Re Interquartile 1500-7600 3000-9000 2000-7200 2800-10400

Min-Max 0-24000 0-33000 0-10500 0-23000(L-T) (L-T) (L-T) (L-T)

Froude number4 Median 0.43 (sC) 0.66 (sC) 0.44 (sC) 0.84 (sC)Fr Interquartile 0.17-0.86 0.34-1.03 0.34-0.8 0.31-1.18

Min-Max 0.00-2.71 0.00-3.72 0.00-1.18 0.00-2.58(sC-SC) (sC-SC) (sC) (sC-SC)

Roughness Reynolds Mean 38000 (R) 58000 (R) 10000 (R) 18500 (R)number5 Interquartile 104 104-105 103-104 103-104

Re* Min-Max 0.0-2.2 × 105 0.0-3.3 × 105 0.0-2.5 × 104 0.0-5.7 × 104

(S-R) (S-R) (S-R) (S-R)

1Near-bed flow type according to a comparison of depth (D) and substratum roughness (k): D < 3k chaotic;D > 3k non-chaotic.

2Interquartile range indicates temporal variation and min-max range indicates spatial variation.3Mean flow type according to Reynolds number: >2000 Turbulent (T); <500 Laminar (L).4Mean flow type according to Froude number: >1 Supercritical (SC); <1 Subcritical (sC).5Microflow type classification according to Roughness Reynolds number (Re*): Re*>70 hydraulically rough

(R); Re*<5 hydraulically smooth (S).


mean density, patchiness, and the percentof juveniles, but negatively related to thepercent of adults. DAYSSINCEQ18 andDAYSSINCEQ3.5 also influenced these bi-otic variables. As a single variable, DAYS-SINCEQ3.5 explained the largest propor-tion of variation in mean density at both theMR (r2 = .52) and the SR (r2 = .69) (Fig. 7).At the MR, mean density increased abovebackground levels (∼100 ind/m2) andpeaked approximately five days after event>3.5 m3/s. Density then approached back-ground levels within the next five days. Incontrast, at the SR the highest mean densitywas recorded right after a flashflood andthen decreased exponentially.

While most of the single disturbance-regime variables were weak in explain-ing the dynamics of gastropod variables,they had a strong, combined, habitat-

dependent effect (Table 3). At the MR,mean density increased with #Q>18/WKand decreased with #Q>36/WK. At the SR,mean density increased with high QINST.Patchiness of density (described by CV)increased with #Q>3.5/WK and wasreduced by #Q>36/WK at MR. In contrast,more variables influenced CV at the SR.Mean size was not determined by any dis-turbance variable at the MR, but it wasslightly influenced by the #Q>3.5/WK atthe SR.

The distribution of individuals in size co-horts showed a tight correlation with the dis-turbance regime variables (Table 3). At theMR, the percent of spats increased with re-duced QINST, #Q>3.5/WK and DAYSSIN-CEQ3.5. At the SR, spats were not found. Thepercent of early juveniles was explained bysimilar variables in both reaches. This per-

FIG. 6. Size variation in N. virginea at the Main and Side reaches (A and B, respectively). Circles: median.Whisker: interquartile range. Migratory events indicated by open circles. Closed circles indicate non-migratoryevents. Pies above of each sampling date correspond to percent of spats, juveniles, and adults. Numbers indicatethe sample size for each date.


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32


cent increased with QINST, #Q>3.5/WK,and DAYSSINCEQ3.5. However, DAYSSIN-CEQ36 better promoted an increase of earlyjuveniles at the SR. The variation in percentof late juveniles was not as strongly deter-mined by disturbance regime as in the pre-vious cohort, and the models were reach-dependent. At the MR, it increased with#Q>18/WK and decreased with #Q>36/WK, while at the SR it increased withQINST and DAYSAFTQ3.5 and decreasedwith #Q>3.5/WK. The percent of adultswas weakly determined by #Q>3.5/WKat the MR, but it was strongly determinedby that variable as well as QINST,DAYSSINCEQ18, and DAYSSINCEQ3.5 atthe SR.

DISCUSSION

Seasonality of massive upstream migrations

In this study we observed 44 massive up-stream migrations of the neritid gastropodNeritina virginea over a two year period.

The migrations occurred at least once amonth and were closely correlated to re-ceding flows after periods of high dis-charge. In general, massive migrationswere most frequent during the two highdischarge periods of the year (May, andAugust to November). Nonetheless, pro-longed periods of high discharge can pre-sumably promote upstream migrations un-til the onset of the dry season, as they did in2002. Given that successive storm flows area proximate cause of migrations, the mas-sive migrations of N. virginea tend to be sea-sonal but with a variable periodicity. Ourresults contrast with a previous one-year,mark-and-recapture study in a regulatedstream in southern Japan stream, wherenon-seasonal migration was documented(Nishiwaki et al. 1991a). In our study,young juveniles (5-7 mm) dominated mi-gratory aggregations. Similar findings wereobtained for neritids in Puerto Rico (Pyronand Covich 2003), Costa Rica (Schneiderand Lyons 1993), and Hawaii (Ford 1979).Given the dominance of those intermedi-ate-sized individuals, upstream migrationmay also be density-dependent and relatedto differences in resource-holding capacityamong sizes, as was hypothesized for othermigratory fauna (Baker 1978, Powers andPeterson 2000). This strategy, which is mostlikely used to avoid predators, has alsobeen observed in N. virginea (J. F. Blanco,unpublished data). In addition, reductionof periphyton due to floods is common(e.g., Biggs and Smith 2002) and may alsobe responsible for triggering migrations(Johnson and Brown 1997).

Habitat hydraulics, and upstream migration

In the lower Río Mameyes, we recordedmigratory aggregations in two habitats thatdiffer in hydraulics and stability. At lowand intermediate discharges, the MRshowed faster and highly variable watervelocities, highly turbulent flows (high Re),and highly rough microflows (Re*), due tothe boulders and cobbles dominating thestreambed. The SR also showed fast, butless variable water velocities, less turbulentflows (Re), and smoother microflows (Re*),due to finer streambed substrate (cobbleand pebble). However, during storm flows

FIG. 7. Mean density variation of N. virginea withelapsed days after a flashflood (Q>3.5 m3/s) at themain and side reaches. Different non-linear regressionmodels were fitted for each reach. Note differentscales in y-axis.


TABLE 3. Multiple (linear) regression models on flow-disturbance regime and dynamics of several variablesassociated to upstream migration of N. virginea in two reaches at lower Rıo Mameyes. F-values, probability ofthe regression, and adjusted determination indices (R2) are included for each dependent variable at each reach.Standardized slopes (�) are shown between brackets next to each independent variable; those significantlydifferent from zero are indicated with an asterisk. n = 10 sampling dates. Disturbance regime variables: mediandischarge in the previous 24 hrs (QMED24), instantaneous discharge (QINST), number of over bank flows (>36m3/s) during the past 7 days (#Q>36/WK), number of storm flows (>18 m3/s) during the past 7 days (#Q>18/WK), number of flashfloods (>3.5 m3/s) during the past 7 days (#Q>3.5/WK), number of days since an overbank flood (DAYSSINCEQ36), number of days since a storm flow (DAYSSINCEQ18), and number of days sincea flashflood (DAYSSINCEQ3.5). N = 9 sampling dates.

Dependent variable Main reach Side reach

Mean density (#/m2) F3,6 = 12.31, P > 0.01, R2 = 0.79 F4,5 = 56.17, P < 0.001, R2 = 0.96Intercept = 131.60 Intercept = −15.20SE Error = 23.19 SE Error = 3.39#Q>36/WK (−1.40*) QINST (1.22*)#Q>18/WK (1.48*) #Q>36/WK (−0.53*)DAYSSINCEQ36 (−0.56*) #Q>18/WK (1.09*)

#Q>3.5/WK (−0.75*)CV of density F3,6 = 14.75, P < 0.001, R2 = 0.82 F6,3 = 18.55, P < 0.05, R2 = 0.92

Intercept = −1.38 Intercept = 90.85SE Error = 14.01 SE Error = 5.45#Q>36/WK (−0.66*) QMED24 (−0.68*)#Q>3.5/WK (1.45*) #Q>36/WK (1.30*)DAYSSINCEQ3.5 (0.91*) #Q>18/WK (−1.10*)

DAYSSINCEQ36 (2.10*)DAYSSINCEQ18 (−4.00*)DAYSSINCEQ3.5 (1.72*)

Mean size (mm) No significant model F1,8 = 6.96, P < 0.05, R2 = 0.40Intercept = 11.20SE Error = 2.13#Q>3.5/WK (−0.68*)

% Spats F3,6 = 8.51, P < 0.05, R2 = 0.71 Spats not foundIntercept = 1.05SE Error = 0.10QINST (−0.73)#Q>3.5/WK (−1.30*)DAYSSINCEQ3.5 (−1.40*)

% Early juveniles F3,6 = 20.71, P < 0.01, R2 = 0.87 F4,5 = 19.45, P < 0.01, R2 = 0.89Intercept = 0.82 Intercept = −0.27SE Error = 0.07 SE Error = 0.04QINST (0.82*) QINST (0.96*)#Q>3.5/WK (1.41*) #Q>3.5/WK (0.70*)DAYSSINCEQ3.5 (1.65*) DAYSSINCEQ36 (0.48*)DAYSSINCEQ3.5 (1.65*) DAYSSINCEQ3.5 (0.50)

% Late juveniles F2,7 = 4.88, P < 0.05, R2 = 0.46 F3,6 = 4.83, P < 0.05, R2 = 0.56Intercept = 0.19 Intercept = −0.65SE Error = 0.08 SE Error = 0.15#Q>36/WK (−0.64) QINST (0.77)#Q>18/WK (1.16*) #Q>3.5/WK (−1.21*)

DAYSSINCEQ3.5 (1.45*)% Adults F1,8 = 11.34, P < 0.01, R2 = 0.53 F4,5 = 6.67, P < 0.05. R2 = 0.72

Intercept = 0.29 Intercept = 2.01SE Error = 0.06 SE Error = 0.17#Q>3.5/WK (−0.77*) QINST (−1.00*)

#Q>3.5/WK (−1.20*)DAYSSINCEQ18 (−0.97)DAYSSINCEQ3.5 (−0.56)


both Re and Re* increased more rapidly inthe SR than in the MR, and therefore thestreambed is probably more prone to scourbecause greater shear stress and lack offlow separation (Davis and Barmuta 1989;Hart and Finelli 1999). Recent field experi-ments in a New Zealand stream (Matthaeiet al. 1999a, b) provide evidence on stonemovement relative to both high flows andhabitat hydraulics. These experimentsdemonstrated less stone movementin riffles than in runs, but warned on the im-portance of upstream elements forcing theflows (i.e., bends, high banks and bedrockoutcrops) in reducing stone stability.Forced flows by an upstream bend and anelevated bank may have contributed to ahabitat unstability at the SR.

Gastropod density and size differencesbetween reaches were related to hydrau-lics, and seemly scour patterns. Greaterdensities were continuously observed atthe MR while densities dropped to zero atthe SR during non-migration dates. There-fore, the SR may be considered a non-permanent habitat and a transient passage.During upstream migrations, N. virgineamean size and its variance decreased inboth habitats, however spats and juvenilesprimarily used the MR while the adultsused the SR. Nonetheless, the percent ofadults was more constant at the MR than atthe SR, probably due to the greater stream-bed scour during storm flows. Recently,Holomuzki and Biggs (2000) conductedflume-tank experiments to study behav-ioral responses of lotic gastropods and in-sects to high flows, and observed that mor-tality in Potamopyrgus gastropods wasnegligible in streambeds consisting ofstable, large stones because snails movedunderneath of large rocks to avoid dislodg-ment during high flows. In contrast, whenthe gastropods and insects were placed inunstable, gravel substrate, high mortalityoccurred during high flows.

Many studies have demonstrated thathydraulic conditions influence habitat sta-bility and aquatic refugia (e.g., Lancasterand Hildrew 1993; Townsend et al. 1997;Townsend and Scarsbrook 1997; Gjerløv etal. 2003). In our study, substrates largeenough to separate flow and create dead

spaces may function as instream refugiaduring high flows (sensu Lancaster andHildrew 1993) and helped explain the ob-served habitat preferences of N. virginea.Habitat dependent response to distur-bances was documented in temperatestreams under distinct climatic regimes(e.g., Grimm and Fisher 1989; Palmer et al.1995; Robertson et al. 1995), but examplesfor the tropics are scarce (see Flecker andFeifarek 1994). According to some modelsfor temperate streams in England (Lan-caster and Hildrew 1993; Robertson et al.1995; Lancaster and Belyea 1997), the spa-tial distribution of lotic organisms changeas a function of flow variability, while lowpatchiness is observed at baseflows markedpatchiness arises due to concentration of in-dividuals in refugia at high flow. In ourstudy, the populations of N. virginea mightbe incompletely affected by high flows (in-complete catastrophe) and frequent recruit-ment could be possible at habitat scalewithin riffles and runs. Stable habitats canalso provide more refugia than less stablehabitats at the reach scale (riffle vs. run)and help secure population persistence inlarger scales.

Discharge regime and upstream migration

Different disturbance parameters ex-plained the dynamics of N. virginea vari-ables in our study. An increase in meandensity due to migratory aggregations wasrelated to intermediate storm events (Q >18 m3/s) in both reaches. Nevertheless,such high densities were recorded at the SRonly during high discharges and thepatchiness of snail density increased withthe number of flashfloods in the MR. Simi-lar patterns were observed at the SR, butadditional interacting factors were also in-volved. Such increase in both mean densityand patchiness is promoted by strong habi-tat selection by migrating individuals.Blanco and Scatena (unpublished data)found that N. virginea used specific areas ofthe channels during upstream migrationsthus increasing patchiness. These areas(i.e., fast flowing or deep waters) may func-tion not only as migratory pathways, butalso as flow refugia.


Although mean snail size was poorly ex-plained by disturbance regime, floods sig-nificantly explained the proportion of indi-viduals in different cohorts. The percent ofspats increased with instantaneous highdischarge but rapidly decreased as waterlevel receded. Similarly, the percent ofearly juveniles (50% in migratory aggrega-tions) increased with high instantaneousdischarge after several flashfloods (#Q >3.5/WK) and with time after last flashfloodin both reaches (R2: MR = .87, SR = .89). Atthe SR, the percent of early juveniles alsoincreased after large storms (>36 m3/s).Unlike young juveniles, percent of late ju-veniles varied more, regardless of distur-bance regime, suggesting that other factorsmay be more important. Finally, the per-cent of adults was reduced by successiveflashfloods at the MR. In contrast, they ap-peared right after floods and then quicklydisappeared in the SR. This may be due todislodgment and streambed scour at an up-stream plane-bed reach during floods, fol-lowed by upstream compensatory move-ment. The greater refugia availability at theMR may also have reduced effect of flash-floods on adult populations. Our resultssupported previous studies that report thatreliability of disturbance variables is bothspecies and habitat specific (Grimm andFisher 1989; Death and Winterbourn 1994;Biggs and Smith 2002; Townsend andScarsbrook 1997; Doisy and Rabeni 2001),but we also provided evidence that they aresize-dependent.

Finally, our findings contrasted with theobservance of frequent crashes in macroin-vertebrate abundance relative to stormflows in tropical streams (Flecker and Fei-farek 1994; Ramirez and Pringle 1998) anddesert streams of North America (Grimmand Fisher 1989). Population crashes inneritid gastropods are exclusively causedby large, infrequent storm flows (>36 m3/s)responsible for streambed scour even instable habitats (i.e., riffles and deep pools).Smaller events, in contrast, increase popu-lation density by stimulating upstream mi-gration presumably due to reduction ofperiphyton. Therefore, neritid gastropodsare resistant to small disturbances in stablehabitats and highly resilient in unstable

habitats. This study supported previousworks (Grimm and Fisher 1989; Fleckerand Feifarek 1994) reporting species-specific responses to flood disturbances. Inour study, N. virginea displayed a pulseresponse (sensu Lake 2000) characterizedby a density reduction dependent on bothdisturbance magnitude and habitat sta-bility, followed by a massive upstream mi-gration.

CONCLUSIONS

Aggregations of large numbers of juve-niles of N. virginea that migrate upstreamoccur during rainy periods in Puerto Rico.Both long- and the short-term studies indi-cate that upstream migrations are relativelyfrequent (once every 15 days), promoted byfloods, and are strongly influenced byreach-level habitat stability. In a stable rifflereach, the density varied less compared toan unstable plane-bed reach and peakednearly 5 days after flashfloods, dropping toprevious levels afterwards. Conversely, inan unstable habitat, density was lower, in-creasing 1 day after floods, then decreasingexponentially to zero in some instances. N.virginea was more resistant to flashfloods(instantaneous discharge >3.5 m3/s) andintermediate storm flows (instantaneousdischarge >18 m3/s) in the stable habitatproviding flow refugia (riffle), but it wasresilient in the unstable habitat (fine-substrate run). Lastly, since stable habitatsare preferred as both residence areas andpassages during upstream migrations, theyshould be protected to preserve popula-tions of N. virginea and other migratoryfauna.

Acknowledgments.—Sara R. López as-sisted during the long-term monitoringfieldwork. Andrés García, Samuel Moyaand Brynne Bryan kindly provided trans-portation to the field site. Brynne also pro-vided helpful comments on the manu-script. Jorge Ortiz-Zayas provided thestudy area map and Juan D. Daza did theelectronic artwork in final figures. This re-search, funded by the Cooperative Agree-ment 00-CA-11120101–004, InternationalInstitute of Tropical Forestry [USDA-ForestService] and the University of Puerto Rico,


Rio Piedras Campus, was designed to sup-port the Long-Term Ecological ResearchProgram at the Luquillo Experimental For-est in Puerto Rico. Comments from JorgeOrtíz-Zayas, and three anonymous review-ers improved the final version.

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Appendix. Hydraulic variables andequations

D: Water depthk: Substratum roughnessU*: Shear velocity measured 2 cm above the

streambedRe: Mean Reynolds number (<500 laminar, 500-2000

transitional, >2000 turbulent)

Re*: Roughness Reynolds number (<5 hydraulicallysmooth, >70 hydraulically rough)

Fr: Froude number (<1 subcritical, =1 critical, >1supercritical)

g: Gravity acceleration (9.8 m/s2)�: Kinematic viscosity (1 x 10−6 m2/s at 20°C)Re = U* D �−1

Re* = U* k �−1

Fr = U* (g D )−0.5


Neritina Virginea Upstream Migrations

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