Reproduction and embryonic developmentof the blue stingray, Dasyatis chrysonota,in southern African waters

david a. ebert1

and paul d. cowley2

1Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA, 95039, USA,2South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown 6140, South Africa

Dasyatis chrysonota is perhaps the most common of the 14 whiptail stingray (Chondrichthyes: Dasyatidae) species known tofrequent the temperate coastal waters of southern Africa and like other stingrays they possess life history characteristics thatmake them vulnerable to over-exploitation. First and 50% maturity (Dw50) were determined for 153 males and 204 femalesfrom the Eastern Cape Province of South Africa. Disc width (Dw) for first and Dw50 maturity was estimated at 392 mm and395 mm Dw, respectively for males and at 500 mm and 505 mm Dw, respectively for females. The reproductive cycle of males,based on gonadosomatic (GSI) and hepatosomoatic (HSI) indices indicates that they are most active during the spring.Females appear to have an annual reproductive cycle with a maximum HSI occurring during the summer and autumn,but it declines steadily through the birthing season reaching a low in the late spring. Fecundity, following a nine monthgestation period, averages 2.8 with a range of 1–7. Embryos at six different development stages are described. Dasyatischrysonota, like other dasyatids, exhibit life history characteristics that make them vulnerable to overexploitation, thereforea precautionary management strategy is advised for this species.

Keywords: Dasyatidae, elasmobranch, fecundity, maturity, seasonality

Submitted 12 May 2008; accepted 12 August 2008; first published online 17 November 2008

I N T R O D U C T I O N

Of the 14 species of whiptail stingrays (Chondrichthyes:Dasyatidae) known to frequent the temperate coastal watersof southern African, the blue stingray, Dasyatis chrysonota isperhaps the most common (Compagno, 1999). The speciesis distributed from St Lucia on the east coast of South Africato central Angola (Cowley & Compagno, 1993) and occursfrom the surf zone down to about 110 m deep. The speciesis easily recognized from other southern African stingraysby the irregular pale blue blotches and lines on its golden-brown triangular disc (Compagno et al., 1989).

Dasyatis chrysonota was previously considered synonymouswith the eastern North Atlantic D. pastinaca. However, a taxo-nomic re-evaluation by Cowley & Compagno (1993) concludedthat Smith (1828) in a little known, and forgotten, descriptionhad named a new stingray from South Africa, D. chrysonota.The name D. marmorata also appears in literature accountsfor South African stingrays, although this West Africanspecies does not appear to be the same.

Although batoid fish, in general, have been poorly studiedin southern African waters, aspects of the biology of D. chry-sonota have been investigated. Cowley (1997) reported on itsage and growth, while Ebert & Cowley (2003) reported on itsdiet. However, most of our knowledge on the reproductivebiology of this species is based on anecdotal accounts

(Wallace, 1967; van der Elst, 1981; Rossouw, 1983;Compagno et al., 1989). This lack of knowledge is unfortunatesince D. chrysonota is a popular recreational angling species,often being caught in large numbers at fishing competitions,and is frequently taken as bycatch in inshore trawl fisheries(Cowley, 1990). Furthermore, many elasmobranchs, possiblyincluding D. chrysonota, possess life history characteristics(e.g. late age at maturity and low fecundity) that make themvulnerable to over-exploitation. Therefore, given the needfor critical life history information on this potentially vulner-able species, and the current paucity of information, this studyaimed to examine the reproductive biology, includingembryonic development, of D. chrysonota in southernAfrican waters.

M A T E R I A L S A N D M E T H O D S

Dasyatis chrysonota were collected along the South Africancoastline between False Bay (348400S 198000E) and EastLondon (338300S 278500E) from March 1987 to May 1989(Figure 1). Specimens were obtained from inshore, nearshore,and offshore waters from shore anglers, light tackle boatanglers and trawling aboard the RV ‘Africana’, respectively.Disc width (DW) and disc length (DL), measurements weretaken to the nearest millimetre (mm) with the stingray lyingflat in its natural position. Weight (W ) was taken to thenearest 0.1 g on a calibrated spring balance. The relationshipsbetween DW and DL, and DW and W were calculated.The relationship between DW and DL is described using the

Corresponding author:D.A. EbertEmail: debert@mlml.calstate.edu

809

Journal of the Marine Biological Association of the United Kingdom, 2009, 89(4), 809–815. #2008 Marine Biological Association of the United Kingdomdoi:10.1017/S0025315408002907 Printed in the United Kingdom

equation DL ¼ aDwb; a and b are fitted constants (Ricker,

1973). To evaluate differences in the DW 2 DL relationshipsbetween males and females linear regression coefficientswere calculated and compared using an ANCOVA. Therelationship between DW and W was logarithmically trans-formed, and linear regressions were fitted to pairs of obser-vations by sex using the equation W ¼ aDw

b; a and b arefitted constants. An ANCOVA was used to test for differencesbetween regression coefficients for DW 2 W relationshipsbetween males and females (Ricker, 1973).

The sex and maturity status (i.e. adult, adolescent or juven-ile) were recorded. The number and proportion of adults,adolescents, and juveniles of each sex were analysed using ax2 test with Yates correction to evaluate overall differencesin sex ratios (Zar, 1999) and within three habitats, e.g. surfzone, nearshore and offshore, as defined by Ebert & Cowley(2003) for this species. Externally, males were considered tobe adult when the claspers were elongated and calcified,including the terminal cartilage elements. Adolescent individ-uals were those whose claspers extended beyond the posterioredge of the pelvic fins, but lacked calcification of the terminalcartilage elements. Juveniles had short, flexible claspers thatdid not extend beyond the posterior edge of the pelvic fins.The inner clasper length was measured and plotted as aratio to DW. An abrupt change in the clasper length to DW

ratio was considered to indicate maturity. Internally, coilingof the epididymides and gonad development were also usedto confirm maturity. The testes were weighed to the nearestgram (g). The mean monthly values for the gonadosomaticindex (GSI), using adults only, were calculated: GSI ¼ gonadweight/total body weight � 100. This index was used toassess whether any seasonal peak changes in the reproductivecondition of adult males occurred during the year. Maturefemales were determined by the presence of highly vascular-ized, large yellow oocytes, fully developed uteri with associatedtrophonemata, an oviducal gland that was distinctly differen-tiated from the uterus, whether the posterior portion of theuterus was pendulous or the uterus contained developingeggs or embryos. The number of embryos or uterine eggs, ifpresent, was counted and plotted against DW to assess possiblechanges in fecundity associated with size. Adolescent individ-uals had smaller ovaries, with some differentiation, but lackedmature oocytes. The oviducal gland was undeveloped andthe uteri were narrow and constricted. Juveniles lacked any

differentiation of the ovaries, and the oviducal gland wasnot differentiated from the uterus. Mean monthly values forthe hepatosomatic index (HSI), using adult males andfemales only were calculated: HSI ¼ liver weight/total bodyweight � 100. This index was used to assess changes in thereproductive condition of adults. Disc width at 50% maturity(DW50) was calculated for each sex by means of a logisticregression (Roa et al., 1999). Embryos at six different develop-ment stages were examined and described.

R E S U L T S

A total of 357 specimens (153 males and 204 females) werecollected during the study. The overall female:male (F:M)sex ratio was 1:0.75, significantly different from the expected1:1 ratio (x2 ¼ 7.0, df ¼ 1, P , 0.05). A comparison of matur-ity status showed no significant difference in the sex ratio ofadults and juveniles (P . 0.05), but a significant differencein the sex ratio of adolescents 1:0.21 (x2 ¼ 20.07, df ¼ 1,P , 0.05) was observed.

Comparison of sex ratios within each of three habitatsrevealed a significant difference in favour of adult females toadult males in the surf and nearshore zones, but no significantdifference in the offshore zone. In the surf zone adult femaleshad a sex ratio of 1:0.57 that was significantly different (x2 ¼5.38, df ¼ 1, P , 0.05) from the expected 1:1 ratio. No adultmales were captured in the nearshore zone during the study,but 52 adult females were caught. Relatively few adults werecaught in the offshore zone with females (N ¼ 11) onlyslightly outnumbering males (N ¼ 6), with no significantdifference observed (P . 0.05) between the sexes. Surf zoneadolescent females (N ¼ 14) showed a significant differencein the sex ratio from males (N ¼ 3) 1:21 (x2 ¼ 5.88, df ¼ 1,P , 0.05). No adolescent males were caught in the nearshoreor offshore zones during the study. Juveniles were rare in thesurf and nearshore zones as only a single female and malewere caught in the surf zone and just five females, no males,were caught in the nearshore zone. Juveniles were most abun-dant in the offshore zone, however, within this habitat no sig-nificant difference was observed from the expected 1:1 sexratio between females and males (P . 0.05).

The relationships between DW and DL and between DW

and W for males were described by the following equations:DL ¼ 0.9134(DW) 2 2.2994 (r2 ¼ 0.97) and W ¼ (2� 10205)D 3.2285W (r2 ¼ 0.98) respectively, while the same relationships

for females were: DW and DL and between DW and W weredescribed by the following equations, DL ¼ 0.9406(DW) 2

2.5732 (r2 ¼ 0.98) and W ¼ (2� 10205) DW3.2194 (r2 ¼ 0.99),

respectively. Comparison of the DW and DL relationshipbetween males and females showed no significant difference(P . 0.05). The DW and W relationship between sexes alsorevealed no significant difference (P . 0.05).

Males ranged from 190 to 531 mm DW with 97 of 153(63.4%) determined to be mature. The smallest mature indi-vidual measured 392 mm DW, while the largest immatureindividual measured 388 mm DW. Clasper length increasedrapidly between approximately 350 and 400 mm DW

(Figure 2A), and continued to increase to approximately450 mm DW. Beyond 450 mm DW the clasper length ratiorelative to DW decreased slightly. First maturity was deter-mined to occur at about 73.8% of maximum width (DWmax)and DW50 was estimated at 395 mm DW. Males were collected

Fig. 1. Map of study area.

810 david a. ebert and paul d. cowley

in all months except April, June, July and August. The meanmonthly GSI values for adult males showed an increasebetween May and October followed by successively decreasingvalues until February (Figure 2B). Males with ripe runningsperm were encountered between January and April, aperiod during which the lowest GSI values were recorded.Males examined during May did not contain sperm indicatingthat copulation occurred prior to this time. The meanmonthly HSI values appeared to trend upwards betweenJanuary and October (Figure 2B). After peaking in October,the monthly values declined steadily to January.

Females ranged from 184 to 711 mm DW with 120 of 204(58.8%) determined to be mature. The smallest mature indi-vidual measured 500 mm DW, while the largest immatureindividual measured 522 mm DW. First maturity occurred at70.3% DWmax and DW50 was estimated at 505 mm DW. Themean monthly HSI values peaked in March followed by asteep decline in April and May (Figure 3A). Although nosamples were collected between June and August themonthly values continued to decline from September reachinga low in November. Between November and March themonthly values trended upwards.

The number of mature ovarian oocytes ranged from 2 to20 with a mean diameter of the largest oocytes rangingfrom 2 to 13 mm. Forty-five (37.5%) adult females examinedcarried either developing embryos or uterine eggs. Overall,

litter size combining uterine eggs and embryos rangedfrom 1 to 7 (mean+ SD ¼ 2.8+ 1.6). The mean numberof uterine eggs per individual for 32 adult females was slightlyhigher at 3.1 (+1.3) while the mean litter size of 13 femalescarrying embryos was lower at 2.1 (+1.9). The litter size toDW relationship did not show a correlation (r2 ¼ 0.21) ofincreasing litter size with increasing maternal size(Figure 3B). A total of 27 embryos were removed from 13gravid females, of which only 13 embryos, eight males andfive females, could be sexed. The largest embryo, observedin mid-October, had a DW of 172 mm, and the smallest free-swimming neonate, caught in late September, had a DW of184 mm.

One instance of courtship behaviour was observed inMarch 1986 by a diver (Dr M. Griffiths, formerlyDepartment of Ichthyology and Fisheries Sciences, RhodesUniversity, Grahamstown, South Africa) while divingbeyond the breaker zone off Kenton-on-Sea (338410S268410E), Eastern Cape, South Africa. A large female wasobserved lying on the bottom with four to five smaller D. chry-sonota biting on the pectoral and pelvic fins of the female.After prodding by the diver all of the smaller stingraysswam off and distinct biting scars were observed on thefemale. Similar bite marks were observed on another adultfemale caught in January in the surf near Jeffreys Bay(348000S 248 560E), Eastern Cape, South Africa.

Fig. 2. (A) Relationship between clasper length, expressed as a %Dw, andDw (mm); (B) mean monthly changes in male gonadosomatic and hepatosomatic indices.Bars represent+1 standard error. Number in parentheses represents sample size.

Fig. 3. (A) Mean monthly changes in female hepatosomatic index. Bars represent +1 standard error. Number in parentheses represents sample size; (B) litter sizerelative to Dw (mm).

blue stingray reproduction in south africa 811

A total of 32 adult females were found to contain 1–6uterine egg capsules. These thin walled, brownish amber eggcapsules were oval shaped, with a length of approximately25–40 mm and a width of 20–30 mm. The yellow colouredova inside the egg capsules measured 12–18 mm and wereextremely flaccid. At the earliest stages of gestation theuterus was fairly thick walled with poorly developed tropho-nemata. However, just prior to parturition the uterine wallwas thin and extended with highly vascularized and enlargedtrophonemata.

Embryos at six different development stages, ranging from13to 172 mm DW, are described. All embryos were removed fromfemales collected in the Eastern Cape between October andNovember; the date each adult was captured is given in parenth-eses. The development descriptions are as follows:

Stage 1: 13 mm DW (21 October)—the unencapsulatedembryo was slightly more elongate than wide, yellowishwhite in colour, with transparent poorly formed pectoralfins. Numerous highly vascularized external filamentsprotruded from the gill arches. A yolk sac with a diameterof approximately 9 mm was still attached.

Stage 2: 44 mm DW (18 October)—the pale yellow embryo hadno apparent pigment markings. The branchial region washighly vascularized with external gill filaments still present.The diameter of the yolk sac was approximately 4.5 mm(Figure 4A).

Stage 3: 49 mm DW (22 October)—the posterior region of thetail was darkly pigmented. Small gill openings were presenton the outer margins of the gill arches, while the externalbranchial filaments were absent. The yolk sac had amaximum diameter of 5 mm (Figure 4B).

Stage 4: 72 mm DW (7 November)—the upper and lowercaudal folds were present on the dark pigmented tail.A small soft caudal spine, still well sheathed was present.Teeth were present on both the upper and lower jaws.The yolk sac had a maximum diameter of 3.0–4.5 mm(Figure 4C).

Stage 5: 134 mm DW (22 October)—the dorsal surface of thedisc was well pigmented with a pattern resembling that ofan adult. The dorsal coloration was light brown and greywith the characteristic sea blue base colour absent. Theventral pectoral margins were dark. The caudal spine wasclearly visible, but still sheathed and the upper and lowercaudal folds were well formed. The yolk sac was absorbedwith only a slight umbilicus protruding from theabdomen (Figure 4D).

Stage 6: 172 mm DW (15 October)—the dorsal colorationresembled that of an adult. The caudal spine with serrationswas no longer sheathed. The yolk sac was not visible,leaving only a small umbilical scar that is evident on neo-nates. The uterus was filled with yellowish, soup-like histo-troph, in which the embryos bathed for nutrition. Thisembryo represented a full-term foetus and compared

Fig. 4. (A) Dorsal and ventral view of a 44 mm DwDasyatis chrysonota embryo; (B) dorsal and ventral view of a 49 mm DwDasyatis chrysonota embryo; (C) dorsaland ventral view of a 72 mm Dw Dasyatis chrysonota embryo; (D) dorsal and ventral view of a 134 mm Dw Dasyatis chrysonota embryo; (E) dorsal and ventral viewof a 172 mm Dw Dasyatis chrysonota embryo.

812 david a. ebert and paul d. cowley

favourably with the size of young of the year specimens(Figure 4E).

D I S C U S S I O N

Dasyatids, contrary to most skates (rajids), exhibit sexualdimorphism with females maturing and growing to a largersize, and older age, relative to males (Cowley, 1997; Daviset al., 2007; Smith et al., 2007; Ebert et al., 2008). Reasonsfor the size differences are unclear, but may be related todifferences in reproductive modes between the subordersMyliobatoidei and Rajoidei. The myliobatoids are viviparousin their reproductive mode whereas the rajids are oviparous.Musick & Ellis (2005) argued that oviparity in elasmobranchswas an adaptation in smaller species to increase fecundity.They supported their assertion by pointing out that smalloviparous species when compared to similar sized viviparousspecies were far more fecund (Musick & Ellis, 2005), withrajids averaging 58.9 eggs/year compared to 5.5 pups/yearin the myliobatiforms. However, while an oviparous repro-ductive mode may produce more egg cases annually, the eggcases are more vulnerable to predation and other environ-mental perturbations as the embryos develop in situ (Cox &Koob, 1993; Lucifora & Garcia, 2004).

Sexual maturity is atttained in males at a smaller size and atan earlier age than females. Male D. chrysonota reach firstmaturity at about 392 mm DW and 50% maturity at about395 mm DW. These widths correspond to an age at first and50% maturity of approximately four plus years (Cowley,1997). Females by comparison reach first and 50% maturityat 500DW and 505DWmm, respectively, sizes that correspondto an age of about seven years (Cowley, 1997). The similarsized Dasyatis dipterura from the Pacific coast of centralMexico by comparison was found to reach maturity at amedian age of 5–8 years for males and 8–11 years forfemales. The only previous information on size at maturityfor D. chrysonota was provided by Wallace (1967), based ona small sample size, who reported maturity at 450 and 584DW mm for males and females, respectively.

The reproductive cycle of male D. chrysonota indicates thatsperm production peaks from September through toDecember; a time period corresponding to the austral springseason. However, evidence of mating behaviour was observedin January and March, during the austral summer. Otherdasyatids showing a similar spring summer active periodinclude Dasyatis sayi and D. sabina from the central eastcoast of Florida, USA (Snelson et al., 1988, 1989).Interestingly, the HSI values for D. chrysonota also appearto change in conjunction with the GSI levels throughout theyear. How these apparent synchronous changes are relatedis unclear and is an area that requires further investigation.

The HSI in females showed a seasonal variation that maycoincide with reproductive activity. Maximum HSI occurredfrom January through to April, and appeared to declinethrough the birthing season reaching a low in November.Similarly, Rossouw (1987) showed that in Rhinobatus annula-tus, a sympatric species with D. chrysonota, that a seasonalchange in HSI was due largely to the accumulation of lipidsin the liver. He found that maximum HSI occurred inmature specimens during the peak breeding season and thatlow lipid levels, in gravid females, tended to correspond

with embryos approaching term development. If the lowHSI levels indeed reflect a liver with low lipid content, thelow index found in gravid females with embryos approachingterm development may be the result of the energetic demandsof the developing embryos. This area of research requiresfurther investigation.

Fecundity among dasyatid rays is typically low, often aver-aging less than six embryos per litter (Snelson et al., 1988;Capape, 1993; Villavicencio-Garayzar et al., 1994; Musick &Ellis, 2005; White & Dharmardi, 2007). Dasyatis chrysonotalike other members of this family have a relatively low fecund-ity, ranging from 1 to 7, with an average of 2–3 embryos perlitter. Other studies on dasyatid rays have noted that fecunditycan be difficult to estimate because of the propensity of thesebatoids to abort their young due to capture stress and elevationof the specimen from the water (Struhsaker, 1969; Thorsonet al., 1983; Snelson et al., 1988; Smith et al., 2007).Therefore, it is possible that maximum fecundity in this, andother dasyatids, is slightly underestimated (Smith et al., 2007).

Although it has been well documented in some elasmo-branch species that a strong maternal size to litter sizerelationship exists (Ripley, 1946; Olsen, 1954; Babel, 1967;Pratt, 1979; Rossouw, 1983; Ebert & Ebert, 2005), no relation-ship was shown for D. chrysonota. Reasons for this areunclear, but may be related to uterus capacity. It has beenhypothesized that the disc-shaped batoid morphologyappears to restrict the coelomic space and thus restrictsuterine capacity (Musick & Ellis, 2005). Similarly, Martin &Cailliet (1988) proposed that in Myliobatis californica littersize is ultimately limited by space, which in turn is determinedby the size of the female.

Courtship and mating behaviour of viviparous batoids in thewild is relatively rare (Tricas, 1980; McCourt & Kerstitch, 1980;Chapman et al., 2003). Although copulation in the wild was notobserved for D. chrysonota, courtship or pre-mating behavioursimilar to that described for Aetobatis narinari (Tricas, 1980)was observed. Furthermore, Kajiura et al. (2000) observed inD. sabina that dermal bite wounds served as an indicator ofmating, with peak activity coinciding with ovulation.

Dasyatis chrysonota appears to have an annual reproduc-tive cycle with birth following a nine month gestationperiod. Ovulation appears to start soon after parturition asencased uterine eggs were first observed during the summer(January), and continue throughout and into late autumn(May). Although no adult specimens were collected duringthe winter months (June, July and August) some individualswere found to contain encased embryos in early spring(September). Mature females with large ovarian eggs,ranging from 8–14 mm diameter, were observed from latespring into summer (between November and January).Considering that no males exhibited ripe running spermafter April, it is felt that ovulation and hence fertilizationoccurs between January and April followed by a slowing orcessation in growth during the winter months. Snelson et al.(1989) suggested that fertilization in D. sayi occurred shortlyafter ovulation, but that zygote development is arrested for alengthy period of time. This seems plausible since theuterine eggs of viviparous batoids are encased at least untilthe early stages of embryonic development. It appears there-fore that D. chrysonota may have a slowing of growth oran arrested zygote developmental stage resulting from the off-shore winter migration (Cowley, 1990) of this species, duringwhich time females have a higher energy demand. An offshore

blue stingray reproduction in south africa 813

winter migratory pattern is consistent with the findings inother studies on stingray reproductive cycles (Babel, 1967;Snelson et al., 1988). A slowing or cessation of embryonicgrowth during the winter followed by rapid growth duringthe early spring (late September and October), and thetiming of parturition which appears to occur throughout thespring months (between October and December) supports anine month gestation period. Examination of maturefemales from the winter months, along with histologicalstudies, in future studies should confirm the reproductive sea-sonality by refining the timing of ovulation and hence theprecise gestation period.

The reproductive success of D. chrysonota, as with mostdasyatids, is low based on average fecundity and their activereproductive life span. A single female D. chrysonota forexample, assuming an average annual fecundity of 2.8 and aseven year active reproductive span (Cowley, 1997), mayproduce only 19.6 young during her lifetime. Two similarsized stingrays, D. dipterura and Pteroplatytrygon violacea,have widely differing reproductive life spans. Dasyatis dipter-ura, from the Pacific coast of Mexico, has an annual fecundityof between 1 and 4 years and an active reproductive life span ofup to 20 years (Smith et al., 2007). By comparison, P. violaceahas an annual litter size of 1–13, but with an active reproduc-tive life span of five years (Ebert, 2003; Mollet et al., 2002).Furthermore, female D. chrysonota have a low k coefficient at0.07 (Cowley, 1997), which make them extremely vulnerableto overexploitation (Musick, 1999). Therefore, given thek-select life history characteristics of D. chrysonota, its vulner-ability to both shore angling and demersal trawl fisheries, andthe lack of a comprehensive chondrichthyan managementplan in southern Africa a precautionary approach to the man-agement strategy of this species is advised.

A C K N O W L E D G E M E N T S

We thank L.J.V. Compagno and C. Hunter (Iziko Museums ofCape Town), T. Hecht (Department of Ichthyology andFisheries Sciences, Rhodes University), A.I.L. Payne (Cefas),A. Bardenhorst, B. Rose, (now with Irvin and Johnson), P.F.Simms (Marine and Coastal Management), and SimonBrown and C.S. Rinewalt (Pacific Shark Research Center,Moss Landing Marine Laboratories) for their advice, assist-ance and help during this project. Many other people havecontributed to this project over the years and we wish toexpress our sincere appreciation for their help and support.The authors acknowledge funding for this project throughpostgraduate bursaries from the National ResearchFoundation Council (formerly known as the Foundation forResearch Development), South African Network for Coastaland Oceanographic Research, and the Shark ResearchCenter of the South African Museum. D.A.E. thanksNOAA/NMFS for their support of the National SharkResearch Consortium and Pacific Shark Research Center forsupport during the final phase of this project.

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Correspondence should be addressed to:D.A. EbertPacific Shark Research CenterMoss Landing Marine Laboratories8272 Moss Landing RoadMoss Landing, CA, 95039USAemail: debert@mlml.calstate.edu

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