Population Biology of the Burrowing Shrimp Callichirus Seilacheri (Decapoda: Callianassidae) in Northern Chile

Home , Biffarius, Callianassidae, Callichirus major

Population biology of the burrowing shrimp Callichirus seilacheri (Decapoda: Callianassidae) in northern Chile

Patricio Hernáez1 & Ingo S. Wehrtmann2 1 Museo del Mar, Universidad Arturo Prat, Casilla 121, Iquique, Chile; [email protected] 2 Escuela de Biología, Universidad de Costa Rica, 2060 San José, Costa Rica; [email protected]

Received 11-X-2005. Corrected 08-VIII-2006. Accepted 16-III-2007.

Abstract: The life history of ghost shrimps, known for their role in shaping community structures in shallow water habitats, is poorly studied in species occurring along the coasts of the South American Pacific. Here we present ecological information concerning Callichirus seilacheri based upon individuals collected from January to December 2003 in Las Machas beach, northern Chile. Burrow densities varied between 1.4 and 20.2 burrows / 0.25 m2, and was highest during summer (18.2 burrows / 0.25m2). The sex proportion was 1:1 during most of the study period; however, females outnumbered males in January and September. Males reached a larger maximum size than females (27.1 and 24.0 mm CL, respectively). The presence of juveniles was restricted principally to the time between February and May. Sexual maturity was reached at a size of 20.8 mm (males) and 18.1 mm CL (females). The main breeding period lasted from autumn to winter (May to August, peaking in June), and co-occurred with decreasing water temperatures and the presence of a sediment layer covering the burrows. Rev. Biol. Trop. 55 (Suppl. 1): 141-152. Epub 2007 June, 29.

Key words: burrow density, sexual maturity, reproduction, ghost shrimp, South America, Pacific.

The infraorder Thalassinidea is com- Berkenbusch and Rowden, 2000a), especially prised by the so-called ghost shrimps, which concerning those populations occurring along typically occupy intertidal and subtidal marine the Chilean coast. and estuarine habitats. They are known to Although the ecology of American thalas- construct burrows of different shapes and sinidean shrimps has received growing atten- depths (Suchanek 1983, Griffis and Chávez tion during the last decade (see Coelho et al. 1988, Lemaitre and Rodrigues 1991), and 2000, Felder 2001, Thatje 2003), the life history play an important role in shaping the com- of these crustaceans along the South American munity structure in shallow water habitats Pacific coast remains mostly unknown, prob- (e.g. Posey 1986, Posey et al. 1991, Nates ably due to their cryptic life style which makes and Felder 1998). Their burrowing activities it difficult to capture and study them (Coelho contribute considerably to perturbation of the et al. 2000). Along the Chilean coast the family sediments, renovation of the nutrient cycle, Callianassidae (Thalassinidea) is represented and increased food availability among the tro- by six species which can be found in soft sedi- phic levels (Ziebis et al. 1996, Berkenbusch ments between 0 and 255 m depth (see Thatje and Rowden 1999, Felder 2001). Despite of and Gerdes 2000, Guzmán and Thatje 2003, their ecological importance, information about Thatje 2003). There are some scattered publi- population and reproductive biology of these cations which mention the presence of dense shrimps is scarce (i.e. Rodrigues and Shimizu populations of ghost shrimps at Chilean beach- 1997, Pezzuto 1998, Nates and Felder 1999, es (Aste and Retamal 1983, Soto et al. 2002).

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 141 In general, however, information concerning and reproductive aspects of C. seilacheri, biology, population dynamics, and ecology of the most conspicuous intertidal callianassid these shrimps is still lacking. shrimp in the northern part of Chile (Soto et Callichirus seilacheri Bott 1955 (synony- al. 2002). We also present data on habitat use my of C. garthi Retamal 1975; see Sakai 1999) and density changes during the year, which is distributed from El Salvador (12ºN) to Chile might facilitate a better understanding of the (37ºS). The species was observed for the first ecological role of this ghost shrimp along the time on beaches in the extreme northern part coastal habitats of Chile. of Chile during the ENSO event of 1982-1983 (Soto et al. 2002). Existing information is lim- ited to larval development (Aste and Retamal MATERIALS AND METHODS 1983), and the interaction between C. seilacheri and the ectosymbiotic copepod Clausidium Specimens were obtained from the inter- sp. (Marín and George-Nascimento 1993). tidal zone in Las Machas beach, northern The present study aims to provide infor- Chile (Fig. 1) from January to December 2003. mation regarding the population structure The individuals were identified according to

Fig. 1. Callichirus seilacheri. Details of the study area, Las Machas beach in northern Chile.

142 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 the keys for genera and species, published The CL was considered as an independent by Manning and Felder (1991) and Retamal variable; adjustment of each regression was (1975) respectively. In order to get an estimate analyzed by least squares method (Sokal and of the abundance of C. seilacheri, we counted Rohlf 1981). This procedure was applied for all the number of holes in an area of 0.5 x 0.5 categories. Specimens of each category were m, with ten replicates during each monthly grouped into 1 mm size classes; subsequently sampling (typically between day 15 and 20 data were plotted as length-frequency histo- of each month). The entrances of each gallery grams to analyze the population structure of the were easily identifiable due to their diameter; juveniles and adult shrimps. however, shrimps might live in interconnected Morphological maturity in C. seilacheri network tunnels, and each gallery was occu- was estimated from the biometric relation- pied by at least one individual (P. Hernáez, ship between PL x CL in males, and WW pers. obs.). Individuals were collected with a x CL in females. The allometric equation yabby pump (diameter: 77 mm) after inspect- (y= axb) was fitted to each growth phase to ing the area for burrowing holes. However, obtain the allometric growth constant “b” to even when no holes were visible, sediment determine the growth pattern (see Somerton was searched for ghost shrimps. The physi- 1980). Analysis of the allometric growth cal structure of Las Machas beach changed constant (b) gives information about the considerably during the study period making increase of one biometric dimension in rela- it impossible to determine the number of holes tion to another; isometric growth was con- by area between June and August. Therefore, sidered when b was between 0.90 and 1.10, this period was not included when estimating negative allometric growth with b<0.90, and the burrow densities. The following data were positive allometry with b>1.10 (Kuris et also recorded: surface water temperature, al. 1987, Pinheiro and Fransozo 1993). All number of ghost shrimps per yabby pump incomplete individuals were excluded from suck per burrow opening, associated fauna, these analyses and of the determination of and predators present in the burrows. size at first sexual maturity. After extracting the ghost shrimps each Our knowledge about mating in ghost individual was sexed and classified into one of shrimps is scarce, principally because mating the following categories: juvenile (JU), male occurs in cryptic locations (Bilodeau et al. (MA), non-ovigerous female (NOF), and ovi- 2005). To obtain an indirect estimate of the gerous female (OF). The sex determination was mating period of C. seilacheri, we counted the based upon macroscopic features such as the number of burrows occupied by both a female clearly elongated carpus of the major chelipeds with mature gonads and an adult male. The (males) and the presence of colored gonads in percentage of these mature couples (MC) was females; when these criteria did not allow a plotted per month; we considered a month as definitive sex determination, the location of the part of the mating period, when these mature gonopores was revised, too. couples comprised >20 % of all adult individu- The following morphometric measure- als collected per month. ments (+ 0.1 mm) were taken: total length (TL: According to Connell (1985), recruitment from the anterior margin of the rostrum to the is defined as the entry of individuals into the posterior region of the telson), carapace length juvenile and adult benthic population after set- (CL: from the anterior margin of the rostrum tlement from a planktonic larval stage. Since C. to the posterior margin of the carapace), and seilacheri has a larval planktonic development length and width of the propodus of the major (Aste and Retamal 1983), we estimated recruit- chelipeds (PL and PW, respectively). The wet ment through the presence of small individuals weight (WW) of each individual was measured (< 9 mm CL), analyzing the size-frequency with an analytical balance (Sartorius; + 0.1g). histograms of each month.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 143 Possible monthly differences concerning active in the shafts and tunnels. Burrow densi- the sex proportion were analyzed by means of ties during the year varied between 1.4 and 20.2 a χ2 test (1:1; p<0.05). The time of the repro- burrows/0.25 m2. High monthly mean values ductive period was established by comparing (>19 burrows/0.25 m2) were recorded in spring the percentage of ovigerous females to the total and summer, coinciding with reduced accretion number of females collected during the month intensities in Las Machas beach (Table 1). or the season. The reproduction period was Invertebrates associated to the C. seilach- defined as the months where more than 25 % eri galleries were the carnivorous polychaete of all collected females carried eggs. Nepthys ferruginea Hartman, a very abundant (but unidentified) nemertine worm and the pinnotherid crab Pinnixa transversalis Milne RESULTS Edwards & Lucas. In the sampling area (but not associated with C. seilacheri galleries and General observations concerning habi- occurring also outside the collection site), a tat and ecology of C. seilacheri. During June, bivalve of the genus Donax sp. was especially the ocean moved a large amount of sand from abundant during spring when sediment erosion the superior zone of the beach towards the was most intense. intertidal and subtidal areas, covering most of Almost all individuals of C. seilacheri the entrances of the burrows and complicat- hosted the ectosymbiotic copepod Clausidium ing the count of the burrows per square meter. sp. This copepod principally infested the gill This situation lasted until end of August, when region, the insertion area of the thoracic legs, conditions returned as they were at the begin- and the egg masses. ning of the study. When we removed the upper sediment layer covering the burrow, it became Population biology. A total of 716 indi- obvious that ghost shrimps were alive and viduals were analyzed; 37.3 % were males,

Table 1 Callichirus seilacheri. Ecological variables and sex ratio; Las Machas beach, Chile.

Month sWT Accretion Density Sex-ratio χ2 (ºC) (0.25m2) (M:F) January 18.6 ± 1.66 - 19.6± 3.33 29/48 4.701* February 20.2 ± 0.72 - 15.2 ± 5.79 11/9 0.250 March 18.0 ± 0.85 - 19.7 ± 3.74 26/21 0.553 April 17.7 ± 1.52 - 16.6 ± 7.49 22/29 0.980 May 17.1 ± 0.77 + 4.7 ± 1.15 26/20 0.804 June 16.2 ± 1.69 +++ 2.2 ± 0.32 28/21 1.020 July 15.9 ± 0.98 +++ 1.4 ± 0.11 16/18 0.147 August 16.1 ± 1.78 +++ 2.3 ± 0.26 11/19 2.167 September 15.8 ± 0.54 + 16.9 ± 2.67 11/29 8.125* October 17.3 ± 1.44 - 14.7 ± 4.11 19/29 2.104 November 17.3 ± 1.37 - 18.4 ± 3.27 38/30 0.956 December 17.7 ± 1.49 - 20.2 ± 0.49 30/40 1.443

Mean surface water temperature (SWT), intensity of accretion (+++: high; +: medium; -: low) and mean burrow density during of the study period (January to December 2003). Proportion of males and females per month; asterisks indicate significant differences (p<0.05; χ2 test) from the 1:1 ratio.

144 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 43.7 % females, and 19.0 % immature indi- 50 males viduals. The sex proportion was 1:1 during females almost all the year (Table 1), except in January juveniles and September when females were significantly more abundant than males (test χ2, p< 0.05). 25 In all categories, the relation between CL and WW was best described by a poten- tial function which accounted for 97 % of Propodus length Propodus (PL, mm) 0 the total variation between these two factors 0 10 20 30 (Fig. 2). The analysis of the relation between Carapace length (CL, mm) PL and CL (Fig. 3) revealed different growth patterns for each of the life cycle stages of Fig. 3. Callichirus seilacheri. Relation between propodus and carapace length of juveniles, males, and females during C. sailacheri (Table 2), indicating isometric the study period at Las Machas beach, northern Chile. growth in juveniles (b=0.90), positive allometric growth in males (b=2.32), and negative stage. According to this, males and females allometric growth in females (b=0.86). reached sexual maturity at a size of 20.8 The analysis of morphological matura- mm CL (LP= 5.29*10-1CL1.11, r2=0.84) and tion based on the inflection point of each 18.1 mm CL (WW= 2.93*10-3CL3.01, r2=0.94), regression indicates the moment when growth respectively. changes from an isometric to an allometric Males and females had an average size of 21.4 mm CL (±2.57 mm) and 21.1 mm 60 CL (±1.87 mm), respectively. However, males WW = 2.06*10-3 CL3.16 50 R2 = 0.97 reached a larger maximum size than females N = 716 40 (27.1 and 24.0 mm CL, respectively). All the categories showed significant size differences 30 during the study period (ANOVA; p< 0.05). 20 The presence of mature couples was

Wet weight (WW,Wet g) 10 confined mainly to the period from April to July, with a small percentage present also in 0 November (Fig. 4). Ovigerous females were 0 10 20 30 Carapace length (CL, mm) recorded between March and September, peaking in June with 61.1 % of all collected females Fig. 2. Callichirus seilacheri. Relation between wet weight during this month (Fig. 4). A second, substan- and carapace length of all individuals collected (N=716) during the study period (January–December 2003) at Las tially smaller peak occurred in November and Machas beach, northern Chile. December. The main presence of both mature

Table 2 Callichirus seilacheri. Regression analyses between length of major propodus (PL) and carapace length (CL).

Variable Category n Equation r2 Allometric level PL MA 226 PL=2.00*10-2 CL2.32 0.80 +

NOF, OF 268 PL=0.95*CL0.86 0.88 -

JU 115 PL=0.85*CL0.90 0.82 0 total 620 PL=0.33*CL1.29 0.65 +

MA = males; NOF = non ovigerous females; OF = ovigerous females; JU = juveniles In all cases, the relation was significant (p<0.01). Allometric level refer to isometry (0), negative (-) and positive (+) allometry.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 145 ovigerous females mature couples SMT temperature( surface mean as well as the abundance and biomass of the 100 macroinfauna (Defeo et al. 1992, McLachlan et al. 1993, Jaramillo et al. 1998). According 75 to Muehe and Tavares-Corrêa (1989), such

50 seasonal movements allow the renovation of nutrients in sandy beaches. This balance is eco- 25 logically significant for many benthic popula- o Percentage of individuals Percentage C) tions (Carrasco and Gallardo 1994), especially 0 for those organisms burrowing in the sediment, ay July arch April M June M such as ghost shrimps. January August February October September NovemberDecember The seasonal movement of sediments along Fig. 4. Callichirus seilacheri. Presence (expressed as the beaches of northern Chile may be important percentage of all individuals collected during each month) for the population dynamics of C. seilacheri. of mature couples and ovigerous females at Las Machas Our results suggest that recruitment and breed- beach, northern Chile, in relation to both the mean water ing season in C. seilacheri were synchronized surface temperature (SMT) and the presence of sediments with erosion and sedimentation processes, covering the burrows (accretion) during the study period (January–December 2003). respectively. Erosion may have favored the post-larval settlement during summer, facilitat- ing the encounter of suitable habitats for their development (i.e. open burrows). In winter the couples and ovigerous females coincided with accretion was more intense, and numerous bur- the period of decreasing temperatures and rows were covered by the sediment (see Table when accretion was more intense and burrows 1), which diminished the probability that post- were covered by sand (Fig. 4). larvae encountered an available refuge. Sexually mature ghost shrimps (n = 580) The main spawning period of C. seilacheri varied in size between 12.1 mm CL and 27.1 coincided with periods of intense sedimentation mm CL; however, a majority of these (55 % and low surface water temperatures (winter). of all collected individuals) ranged in size from During this period we observed reduced sedi- 20.0 to 24.0 mm CL. Adult shrimps predomi- ment expulsion activity of the ghost shrimps, nated during almost the entire study period with which is in accordance with similar obser- the exception of February when juveniles were vations regarding Callianassa subterranea more numerous (Fig. 5). The recruitment was (see Rowden et al. 1998) and C. filholi (see more intense during summer. The presence of Berkenbusch and Rowden 1999). As reported small individuals (< 9 mm CL) was restricted from other callianassids (Coelho and Rodrigues to the time between February and May (Fig. 6). 2001), during winter C. seilacheri may be able Their subsequent absence coincided with fur- to shift from filter feeding to a deposit feeding ther decreasing temperatures and the beginning mode, enabling the species to obtain sufficient of the main spawning period (see Fig. 5, 6). energy for reproduction. Callianassid shrimps feed on organic mate- rial in the sediment and invest the obtained DISCUSSION energy in growth and reproduction (Nickell and Atkinson 1995). In Las Machas, as the Physical processes associated with beach result of summer (January and February) rains morphodynamics may influence the ecology in the adjacent highlands, two rivers (the San of C. sailacheri. Information about distribu- José and Lluta) supplied considerable amounts tion and community structure of sandy beach of fine, nutrient-rich sediments of terrigenous indicates that sediment type, slope and wave origin to the study area (Soto et al. 2002). characteristics can affect the species richness This apparently favored the establishment of

146 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 January July 20 n = 82 n = 35 SWT = 18.6o SWT = 15.9o

February August 20 n = 78 n = 43 SWT = 20.2o SWT = 16.1o

March September 20 n = 61 n = 51 SWT = 18.0o SWT = 15.8o

April October 20 Numberr of individuals/size class n = 64 n = 56 SWT = 17.7o SWT = 17.3o

20 May November n = 56 n = 70 SWT = 17.1o SWT = 17.3o 10

June December 20 n = 50 n = 70 SWT = 16.2o SWT = 17.7o

10 20 10 20 Size class (mm)

Fig. 5. Monthly length-frequency distribution of Callichirus seilacheri collected between January and December 2003 at Las Machas beach, northern Chile. White bars represent juveniles, black bars adults; SWT=surface water temperature.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 147 mean surface temperature( surface mean recruits SMT 2004). However, the breeding season of C. seilacheri started during a period of diminish- 100 21 ing temperatures which contradicts the pattern 75 14 observed in other thalassinideans from tem- 50 perate regions where the reproductive season 7 25 begins when temperatures increased (Leija o

Percentages of individuals Percentages and Sánchez 1988, Felder and Lovett 1989, C) 0 0 Kevrekidis et al. 1997, Souza et al. 1998). ay July arch April M June C. seilacheri seems to have a markedly M January August February October seasonal breeding period with probably two September NovemberDecember successive spawnings. The obtained data indi- Fig. 6. Callichirus seilacheri. Monthly presence of juveniles (expressed as percentage of the total number of col- cate a second considerably smaller breeding lected individuals per month) in relation to the mean water period in November-December (Fig. 4). This surface temperature (SMT) at Las Machas beach, northern interpretation is in accordance with similar Chile, during the study period (January to December observations concerning various decapods 2003). from Chile (e.g., Lardies et al. 1998, 2004) and other temperate zones (e.g., Beck and Cowell 1976, González-Gurriarán 1985, Haddon and the C. seilacheri population, which is princi- Wear 1993). pally associated with this type of sediment (P. The sediment cover seems to reduce the Hernáez, pers. obs.). risk of predation, including that by local fisher Temperature is a dominant factor that communities collecting burrowing shrimps governs the population dynamics of many at Las Machas. Local people capture these intertidal decapod populations (Kinne 1970, shrimps intensively for bait from October to Jones and Simons 1983, Stillman and Somero May, but during the remaining months such 2000). This factor has been associated with activities decrease substantially. The seasonal temporal alterations in the sex ratio, breeding patterns of the sediment movements regulate events, size-frequency distributions and sedi- human collecting activities, thus indirectly pro- ment turnover activity in natural populations of tecting the reproduction of C. seilacheri. thalassinidean shrimps (Kevrekidis et al. 1997, Females predominated in January and Rowden et al. 1998, Berkenbusch and Rowden September (Table 1). In accordance with the 1999, Berkenbusch and Rowden 2000b). Our present data, predominance of females has been results confirm these observations and suggest reported also for Glypturus (as Callichirus) arma- that population dynamics of C. seilacheri are tus (see Vaugelas et al. 1986) and Nihonotrypaea strongly influenced by temperatures and annual harmandi (as Callianassa japonica) (see Tamaki sediment dynamics in Las Machas beach (i.e. et al. 1997); however, these authors did not sedimentation and erosion). provide any explanation for this phenomenon. The main breeding period of C. seilacheri Burrows of Callichirus (for C. major see Frey lasted from autumn to winter (May to August), et al. 1978) are considered as an intercon- and co-occurred with decreasing water tem- nected network of shafts and tunnels, which may peratures and the presence of a sediment layer explain our observation that several females covering the burrows (Fig. 4). Thus, our results can share a burrow with a male; however, we corroborate that reproduction in decapods from never found more than one male per burrow. It temperate zones is generally synchronized with is speculated that the male due to his polygamist cycles of temperature, photoperiod, and food behavior protects his harem during the reproduc- availability (e.g. see Antezana et al. 1965, tion period, thus increasing the risk of predation. Arana and Tiffou 1970, Bahamonde et al. 1986, Such a behavior may explain why females out- Wolff and Cerda 1992, Lardies et al. 1998, number males during these months.

148 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 55 (Suppl. 1): 141-152, June 2007 Recruitment was most conspicuous dur- comprendido entre febrero y mayo. La madurez sexual se ing the early months of the year, especially alcanza a un tamaño de CL de 20.8 mm en los machos y February, and to a lesser extent during the 18.1 mm en las hembras. El periodo reproductivo principal se extendió del otoño al invierno (de mayo a agosto, con un period from August to October (Fig. 6). The pico en junio), y coincidió con temperaturas decrecientes major recruitment peak in February coincided en el agua y con la presencia de una capa de sedimento with the highest water temperatures measured sobre las madrigueras. during the study period while the second pulse of recruits occurred during a period charac- Palabras clave: densidad de madrigueras, madurez sexual, reproducción, camarón fantasma, Suramérica, terized by increasing temperatures (Fig. 6). Pacífico. Interestingly, both recruitment events occurred during periods when the burrows were not covered by sediment. Although juveniles may dig REFERENCES their own burrows, frequently we found juveniles inside of occupied burrows. Therefore, Antezana, T., E. Fagetti & M. López. 1965. Observaciones such timing may favor the rapid settlement in bioecológicas en decápodos comunes de Valparaíso. Rev. Biol. Mar. Valparaíso 12: 1-60. open burrows, thus reducing predation risk. Arana, P. & M. Tiffou. 1970. Madurez sexual, sexualidad y fecundidad del camarón nylon (Heterocarpus reedi). ACKNOWLEDGMENTS Invest. Mar. 1: 261-284.

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