Skip to main content
Download PDF

The effect of the egg-predator Carcinonemertes conanobrieni on the reproductive performance of the Caribbean spiny lobster Panulirus argus

BMC Zoology volume 8, Article number: 6 (2023) Cite this article

Abstract

Background

The Caribbean spiny lobster Panulirus argus is heavily fished throughout its Greater Caribbean and Gulf of Mexico distribution, suggesting a heightened susceptibility to a fisheries collapse. In 2017, a nemertean worm, Carcinonemertes conanobrieni was described from ovigerous females of P. argus in Florida, USA. A year later, the presence of the same egg predator was recorded along the southern Caribbean coast (Colombia). The effect of this egg predator on the reproductive performance, including fecundity, embryo mortality, and reproductive output, of its host is unknown. This study tested whether C. conanobrieni affects embryo mortality, fecundity, and reproductive output in brooding females of P. argus.

Results

Artisan fishers caught 90 ovigerous lobsters near Pueblo Viejo, Magdalena, Colombia. Each ovigerous female was examined for the presence/absence of the egg predator. Lobster egg mortality (%), fecundity (nº eggs female−1), and reproductive output (%) were estimated. Prevalence of C. conanobrieni in the studied population was 87.78%. The mean intensity of C. conanobrieni (all life stages) in the population was 11.68 (± 1.98) egg predators per brood mass sample. Infected females brooding late-stage embryos exhibited lower fecundity, lower reproductive performance values, and higher embryo mortality compared to infected females brooding early-stage embryos. Embryo stage and worm infection level negatively impacted fecundity and reproductive output. Worm infection level and the number of adult nemertean worms also negatively affected embryo mortality.

Conclusions

These results demonstrate an adverse effect of C. conanobrieni on the reproductive performance of P. argus. The interactive impact of this egg predator, natural stressors, and anthropogenic stressors on individual P. argus reproductive performance could facilitate losses at large-scale fisheries levels.

Peer Review reports

Background

The Caribbean spiny lobster Panulirus argus (Latreille 1804) is the target of one of the most valuable fisheries in the Greater Caribbean region, including the Gulf of Mexico, making it more susceptible to a fisheries collapse. Panulirus argus landings support a billion-dollar industrial fleet and artisan fishery across both developed and developing countries throughout its entire distribution, and this species represents a commodity that sells for higher market prices compared to other fished marine resources (between 5–8 USD/Kg) [1, 2] (Fig. 1A). Importantly, many moderate- to low-income level coastal communities in developing countries such as Honduras, Belize, and Guatemala rely either partially or almost entirely on this resource [3]. In Colombia, about 195 tons of P. argus were extracted in 2019 alone, which contributes to its status as a vulnerable species in this country [4, 5]. Local and global stressors, including pollution, habitat deterioration, and habitat destruction, have been hypothesized to contribute to declines in P. argus recruitment and landings in the greater Caribbean Sea [6,7,8]. Furthermore, diseases including but not limited to microsporidiosis, Panulirus argus Virus 1 (PaV1), tail fan necrosis, and trematode parasites found in this species may cause further complications for P. argus population health [9]. It is critical to understand the impact of the aforementioned disease agents including emerging pathogens, such as nemertean worms, on individual- and population-level reproductive parameters of P. argus in order to advance management and conservation policies in this lucrative fishery.

Fig. 1
figure 1

The Caribbean spiny lobster Panulirus argus (A) and its egg-predator worm Carcinonemertes conanobrieni (B)

Full size image

Limited data suggest that declines in female P. argus reproductive performance is attributable to a new nemertean egg predator belonging to the genus Carcinonemertes described from among the eggs of brooding female lobsters [10] (Fig. 1B). In 2017, Carcinonemertes conanobrieni was described from among the eggs brooded by female P. argus in the Florida Keys, USA [11]. A year later, the presence of the same worm was recorded in the Caribbean coast of Colombia, and most recently in the Eastern Caribbean Sea, specifically Saint Kitts and Nevis [12, 13]. Worms in the family Carcinonemertidae, including the genus Carcinonemertes, are recognized as voracious egg-predators that infect a variety of decapod crustaceans [14, 15]. Carcinonemertes worms are responsible for the collapse of crustacean fisheries in the west coast of North America [16,17,18,19] given their negative effect on female reproductive performance [20,21,22,23,24].

The nemertean worm Carcinonemertes conanobrieni has been recorded with variable prevalence in female P. argus populations across different localities of the Caribbean [9, 10, 12, 13, 24]. While initially discovered in the Florida Keys, the growing detection of C. conanobrieni among the brood masses of female P. argus brings into question how long this worm has been on the host, undetected, in previous years. Moreover, researchers have hypothesized that this egg predator may be present across P. argus’ entire Caribbean distribution [12, 13]. Carcinonemertes conanobrieni is a voracious egg predator, known to leave the embryos of its host partially or fully consumed [24], which suggests that this egg predator can cause significant embryo mortality in females of this spiny lobster species. Specifically, Carcinonemertes worms exhibit suctorial feeding where the worm punctures the egg membrane with its stylet and withdraws the contents of the egg until partially or fully consumed [11, 24]. In addition to egg consumption, the worm displays a variety of behaviors when present in female egg masses including encysting alongside host eggs, finding refuge within mucus sheaths, or free roaming among the lobster eggs [9, 24]. Since the discovery of C. conanobrieni in populations of P. argus on the Caribbean coast of Colombia [12], many concerns have arisen regarding the negative ecological and economic effects of this egg predator. Limited data indicate that reproductive performance of female Caribbean spiny lobsters is negatively impacted in the presence of this worm. Notably, declines in fecundity and reproductive output were observed in females carrying early and late-stage embryos when infected with C. conanobrieni [10, 24].

The aim of this study was to evaluate the effect of the nemertean egg-predator C. conanobrieni on the reproductive performance of female P. argus in the southern Caribbean Sea. For this study, we chose to describe the worm as an egg-predator instead of a parasite because of the disproportionate, negative impact the worm has on the embryos of brooding females. Specifically, we investigated C. conanobrieni prevalence, intensity of infection, and its contribution to embryo mortality on P. argus brood masses. Individual-level lobster reproductive performance was measured via reproductive output and fecundity in infected and healthy females. Redundancy analysis was used to identify the effects of C. conanobrieni on reproductive performance and to identify host traits that explain the variation in worm life stages present on the hosts’ brood mass. By understanding the effect of C. conanobrieni on P. argus reproduction, we will be able to establish a baseline estimation of infection in the Colombia P. argus fishery. This will allow us to translate the results of this study to other populations across P. argus’ entire Caribbean distribution when infected with C. conanobrieni.

Results

Egg predator prevalence, intensity, and egg mortality

Carcinonemertes conanobrieni prevalence and intensity was high in the 38 and 52 female P. argus carrying early (I and II) and late (III and IV) stage embryos [10] under their abdomen, respectively. The carapace length (CL) of the 90 studied ovigerous females’ ranged between 61.04 and 133.2 mm with an average (± standard deviation, SD) of 99.87 (± 13.90) mm CL. Prevalence of C. conanobrieni in brooding female P. argus, estimated as the presence/absence of either free-roaming worms or worms within a shaft, was 77.78%. We observed eleven lobsters in which we failed to detect worms; however, worm cysts and egg masses were present. If we consider lobsters with at least one nemertean life stage or egg mass as infected, prevalence of C. conanobrieni in brooding females of P. argus increases to 87.78%.

A total of 923 C. conanobrieni specimens (including all worm life stages: adults, juveniles, and egg masses) were found in studied P. argus egg masses. Egg predator intensity varied considerably, between one egg predator per egg mass in five females (two females carrying early eggs and three females carrying late eggs) ranging between 61.04 and 127.5 mm CL (average ± SD = 66.46 ± 26.31 mm) and 72 egg predators per sampled egg mass in one female of 89.5 mm CL that carried late eggs. The mean intensity of C. conanobrieni (all life stages) in the population was 11.68 (± 1.98) egg predators per egg mass sample. The intensity of C. conanobrieni non-adult forms (cysts and egg masses) ranged between one and 8 (average ± SD = 2.55 ± 2.12), and the intensity of C. conanobrieni adult worms exclusively varied between one and 16 (average ± SD = 6.8 ± 4.98).

Embryo mortality was not observed in any non-infected (C. conanobrieni absent) gravid female lobsters, suggesting a strong negative impact of this egg predator on the host. Embryo mortality, indicated by empty capsules and dead embryos due to infection by C. conanobrieni, for females carrying early embryos ranged between 0% and 43.81% of egg masses (average ± SD = 3.90% ± 9.36). Additionally, we observed that infected P. argus carrying late-stage embryos had mortality rates between 0% and 48.24% (average ± SD = 9.22% ± 10.20). Females with 0% embryo mortality lacked any C. conanobrieni life stages among the embryo subsamples examined.

Lobster fecundity and reproductive output (RO)

Our initial measure of reproductive performance, fecundity, was lower in females carrying late-stage embryos compared to females carrying early-stage embryos, irrespective of the presence/absence of C. conanobrieni (Fig. 2A). Average fecundity (± SD; range) for females carrying late-stage embryos was 472,573.2 (± 200,414; 130,054.7 — 913,270.6) embryos lobster−1; average fecundity was 631,710.3 (± 251,167.3; 120,319.8 — 1,381,719.5) embryos lobster−1 for females carrying early-stage embryos. Fecundity in females carrying early and late-stage eggs, irrespective of egg predator presence or absence, increased with increasing carapace length (R2 = 0.53, P =  < 0.001). Our analysis of covariance (ANCOVA) detected a statistically significant effect of the two main effects, embryo stage of development (ANCOVA; F = 8.49, d.f. = 1, 86, P = 0.005) and lobster carapace length (F = 100.60, d.f. = 1, 86, P < 0.001) on fecundity. The interaction term between carapace length and embryo stage of development was also significant (F = 8.64, d.f. = 1, 86, P = 0.004), indicating that fecundity increased proportionally more with carapace length in females carrying early-stage eggs than in those brooding late-stage eggs (Fig. 2A).

Fig. 2
figure 2

Reproductive performance of gravid females in P. argus. Reproductive performance of gravid females was significantly impacted by the infection of C. conanobrieni, especially in females brooding late-stage embryos. 38 females carried early-stage embryos (I and II) while 52 females carried late-stage embryos (III and IV) under their abdomen. A Fecundity, measured in thousands of eggs, in relation to female lobster carapace length (CL), in mm, is significantly lower in female P. argus carrying late-stage embryos compared to those carrying early-stage embryos (n = 90). Slopes (b) of the relationships between fecundity and lobster CL and coefficient of determination (R2) values are displayed for females carrying early and late-stage eggs. B Reproductive output (R0), the ratio of the dried female mass to the dried embryo mass, is significantly lower in females carrying late-stage eggs versus females with early-stage eggs (P < 0.001). Female P. argus mass (g) and P. argus entire embryo mass (g) were both log-transformed. Slopes (b) of the relationships between egg mass and lobster mass and coefficients of determination (R2) values are displayed for females carrying early and late-stage eggs. The equations are: fecundity (females with early-stage eggs) = -1,100,000 + 17,000(CL), fecundity (females with late-stage eggs) = -430,000 + 9,300(CL), egg mass (females with early-stage eggs) = -1.6 + 1.2(FM), and egg mass (females with late-stage eggs) = -1.5 + 1.1(FM), where CL = lobster carapace length and FM = female mass (dry weight). Female P. argus mass (g) and P. argus entire embryo mass (g) were both log-transformed

Full size image

Like fecundity, reproductive output was lower in females carrying late-stage embryos compared to females brooding early-stage embryos, irrespective of the presence/absence of C. conanobrieni (Fig. 2B). Reproductive output ranged between 3.59% and 13.17% with a mean (± SD) of 9.05% (± 1.95), specifically for females carrying early-stage embryos (I and II). Reproductive output for females carrying late-stage eggs (III and IV) varied from 3.24% and 11.47% with an average of 6.97% (± 2.03). The slope of the regression between female lobster dry mass (g) and embryo dry mass (g), after both were log-transformed, exhibited positive allometry (b = 1.2, SEb = 0.15); the slope of the line was significantly greater than unity (t = 8.30, d.f. = 1, 36, P =  < 0.001) meaning that embryo mass grew more than proportionally with a unit increase in female body mass. An ANCOVA found a statistically significant relationship of embryo stage of development (ANCOVA; F = 24.66, d.f. = 1, 86, P =  < 0.001) and log-corrected female body mass (F = 110.92, d.f. = 1, 86, P =  < 0.001) on log-corrected embryo mass (i.e., reproductive output). The interaction term of the ANCOVA between embryo stage of development and female body mass was not significant (F = 0.15, d.f. = 1, 86, P = 0.70) (Fig. 2B).

The effect of the egg predator on fecundity and reproductive output (RO) of Panulirus argus

Our first redundancy analysis (RDA) confirmed that the presence of the egg predator led to losses in host reproductive performance (Fig. 3A). The analysis exploring the relationship between P. argus (host) traits and the abundance of different life stages of C. conanobrieni resulted in a statistically significant ordination. There was a total explained variance of 31.07% and eigenvalues equal to 0.266 and 0.044 for the first and second ordination axis, respectively (Fig. 3A). Adult worms and their egg masses were significantly more abundant in lobsters brooding late-stage eggs (stages III and IV; both P < 0.05) compared to lobsters carrying early-stage eggs (stages I and II) in which adult worms were rarely observed, but nemertean cysts were present. Fecundity was negatively correlated with abundances of adult worms and their eggs present in lobsters carrying late-stages eggs (P < 0.05). In addition, a tight association was observed between the abundance of adult worms and worm egg masses located among P. argus pleopods. Host body size (CL) was not a statistically significant host trait explaining differences in the abundance of adult worms (P > 0.05).

Fig. 3
figure 3

Effects of C. conanobrieni adults on fecundity of P. argus (a) and on reproductive output and embryo mortality of P. argus (b). A The abundance of adult C. conanobrieni is significantly and negatively correlated with fecundity and reproductive output. Redundancy analysis (RDA) biplot showing first and second ordination axes (eigenvalues 0.266 and 0.044, respectively) of adults, cysts and egg abundances of C. conanobrieni (blue arrows) with respect to host stages (triangles), host characteristics (red arrows): CL (cephalothorax length) and Fec (fecundity). Length of arrows indicate the direction and rate of increase of the variables, angles between vectors indicate close correlations. B The presence of adult C. conanobrieni in females carrying late-stage embryos resulted in lower reproductive output and higher embryo mortality compared to females carrying early-stage embryos. Redundancy analysis (RDA) biplot showing first and second ordination axes (eigenvalues 0.417 and 0.009, respectively) of the death that occurred among P. argus embryos in the different pleopods (blue arrows) and reproductive output (RO) with respect to abundances of adult C. conanobrieni in the different pairs of pleopods (red arrows) and host stages (triangles). A-B: first pair; C-D: second pair; E–F: third pair and G-H: fourth pair. The two graphs show the ordination of predictive and dependent variables. In red arrows, predictive variables: abundance of adult nemerteans per pleopod pair (from anterior to posterior: A-B, C-D, E–F, and G-H), early (ED1, ED2) and late (LD3, LD4) development stages of lobster eggs. In blue arrows, dependent variables: number dead lobster embryos per pleopod pair (Mab; Mcd; Mef; Mgh) and reproductive output (RO) of female lobsters. Each arrow (representing a quantitate variable) points in the direction of the steepest increase of their values. The angle between arrows (red/blue) indicates the correlation between individual predictive variables and/or predictive and dependent variables. The angle between arrows indicates the sign of the correlation between variables. The approximated correlation is positive when the angle is sharp and negative when the angle is greater than 90 degrees. Symbols (triangle) represent levels of a factor, specifically, development stage of lobster eggs (DS). Thus, the distance between these symbols represents the average dissimilarity between the classes (DS) being compared. Closely located symbols and arrows represent an association between levels of a factor and quantitative variables

Full size image

Carcinonemertes conanobrieni contributed to declines in reproductive output coupled with significant egg mortality in brooding P. argus lobsters. The second RDA resulted in a statistically significant ordination (total explained variance = 41.7%, eigenvalues = 0.4177 and 0.0009 for the first and second ordination axis, respectively; Fig. 3B). Lobsters brooding early-stage eggs (stages I and II) were scarcely infected by adult nemertean worms and egg mortality was significantly lower in these lobsters (P = 0.002). Concomitantly, reproductive output was significantly higher in lobsters with early-stage eggs compared to those with late-stage eggs (stages III and IV) in which adult C. conanobrieni were abundant and lobster egg mortality was high (P = 0.002).

Discussion

The effect of Carcinonemertes conanobrieni on the reproductive performance of Panulirus argus

Limited research has focused on the effect of disease prevalence on reproductive performance in spiny lobsters (see [10] and references therein). This highlights the need for this study on P. argus reproductive performance with C. conanobrieni detected in ovigerous female brood masses. In the south Caribbean region (Santa Marta, Colombia), C. conanobrieni was found in ovigerous P. argus females with high prevalence (> 80%), in agreement with [13] and [24] who found a worm prevalence of 87% and 93% in P. argus from Saint Kitts, Lesser Antilles and the Florida Keys, USA, respectively. Carcinonemertes conanobrieni prevalence estimates from Colombia and previous studies conducted across P. argus’ Caribbean distribution have grown from the first report of this worm citing low prevalence at 4.7% [10]. High prevalence of Carcinonemertes spp. is common in many crustacean hosts. For instance, C. errans prevalence is greater than 90% in the Dungeness crab Cancer magister [18] while C. australiensis prevalence reaches 60% in Panulirus cygnus, a spiny lobster heavily targeted by fisheries in Australia [25]. In addition to C. conanobrieni prevalence, the mean intensity of C. conanobrieni infection for our study was 11.68 worms lobster−1, which was higher than a mean intensity of 5.7 worms lobster−1 reported for P. argus in Saint Kitts and Nevis, although their mean intensity estimate included the cryptic Carcinonemertes sp. which we did not find evidence of in our samples [13]. The prevalence and intensity of Carcinonemertes spp., nonetheless, remains to be estimated in most decapod crustacean host species.

Given the high prevalence and mean intensity of C. conanobrieni found in P. argus brood masses in Colombia, we anticipated the presence of this egg predator to result in significant embryo mortality. We observed that lobsters with C. conanobrieni present had embryo mortality that reached up to 48.24%, which coincided with high worm intensity in infected females that averaged 11.68 worms (± 1.98). This was corroborated by both dead and consumed embryos among our subsamples. These estimates of embryo mortality are only slightly lower than P. argus in the Florida Keys, whose embryo mortality due to C. conanobrieni can reach up to 64.5% in heavily infected females [24]. The lack of embryo mortality in non-infected gravid females coupled with significant embryo mortality in females with adult C. conanobrieni present demonstrates the strong negative impact of C. conanobrieni on the egg masses of these lobsters. This pattern has been identified in other decapod crustaceans infected with Carcinonemertes worms including the Dungeness crab C. magister, whose annual embryo mortality exceeded 50% when C. errans was present in their brood masses [18]. Additionally, the shore crab Hemigrapsus oregonensis experienced 75–100% embryo mortality during outbreak years and 0–52% in non-outbreak periods of C. epialti infections [16]. While we did not observe C. conanobrieni feeding, direct observations of C. conanobrieni consuming P. argus embryos has occurred under laboratory conditions [24]. Explicitly, C. conanobrieni feeding occurs when the worm punctures a hole in the lobster embryo using its stylet and everts its proboscis to either fully or partially consume the yolk contents using muscular contractions [24]. Additional laboratory studies have confirmed the same suctorial feeding patterns of other Carcinonemertes species, including feeding of C. errans on C. magister embryos [14, 20]. Our results of embryo mortality, reaching almost 50% in some brooding female P. argus, provide the first step in aiding future research efforts by establishing baseline embryo mortality estimates for the Colombia P. argus fishery due to C. conanobrieni infections. Future studies on P. argus can aid in determining differences in embryo mortality that occur during C. conanobrieni fluctuations i.e. during an outbreak and non-outbreak period in Colombia and other localities in the greater Caribbean basin.

Concomitantly with significant embryo mortality, this study highlights that the presence of C. conanobrieni differentially affected the fecundity of female P. argus. Our results revealed that infected female P. argus carrying late-stage embryos exhibited the lowest fecundity estimates (472,573.2 embryos ± 200,414), which corresponded with having the highest abundance of worms present in their brood masses. Of these worms found in late-stage brooding females, the majority were adult C. conanobrieni, either free roaming or in mucus sheaths, in addition to nemertean egg masses intertwined within P. argus embryos. Contrarily, females carrying early-stage embryos only had worm cysts present in their embryo masses. This suggests that there is a significant, disproportionate negative effect of adult C. conanobrieni on female fecundity throughout lobster embryo development.

Parallel to female lobster fecundity, reproductive output was also negatively affected by the presence of C. conanobrieni in lobster brood masses. Specifically, reproductive output estimates were higher for females carrying early-stage embryos compared to females carrying late-stage embryos. Our second RDA confirms a significant difference in reproductive output between females carrying early vs. late-stage eggs, which coincided with higher adult worm abundance and higher egg mortality in the brood mass of females carrying late-stage embryos. Declines in reproductive output between the different embryo stages described here are in line with previous limited information suggesting declines in reproductive output of infected P. argus females in the Florida Keys population [10], highlighting the increased intensity of infection that ensues as lobster embryos progress from early to late stages of development. To the best of our knowledge, reproductive output has not been estimated in other spiny lobster species [see [25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54]. However, reproductive output, as estimated in this study, has been widely reported for other decapod crustaceans [54]. On the west coast of the USA, C. magister also experienced losses in reproductive output with increasing C. errans prevalence as hosts became gravid [18, 20, 46]. The mechanism behind the progression of C. conanobrieni infection throughout embryonic development remains to be addressed, however, this may indicate that the life cycle of C. conanobrieni is closely linked to the progression of P. argus embryo development and subsequent hatching. Supplementing this, P. argus females in Saint Kitts and Nevis had a high presence of an undescribed Carcinonemertes sp. in their gills during non-peak periods of reproductive activity [47] and C. errans infests the brood mass of the Dungeness crab C. magister by living on the exoskeleton until 1–2 days after host oviposition [18].

The reproductive performance estimates described in this study can add to the growing literature of Carcinonemertes spp. impacts with the discovery of new, previously uninfected hosts. Previous research has compared the occurrence of nemertean worms in the genus Carcinonemertes across exploited decapod crustaceans and their variability in space and temporally [15]. Conclusions as to whether fishing pressure promotes infection by Carcinonemertes spp. and subsequent outbreaks has yet to be determined, however, the importance of monitoring populations becomes key to determining if infection by these worms is temporary or ongoing [15]. This study also highlights the importance of using methods other than the most used, brood mortality, to investigate the negative consequences of infection on host reproductive performance. This is warranted because re-occurring brood loss may lead to host female fitness being dramatically reduced during infection. In corroboration with this study and others focused on P. argus reproductive performance [10], researchers have concluded that wild lobster stocks under repeated infestation by Carcinonemertes worms may be in decline due to a substantial loss in the number of larvae released into the fishery [13].

Conclusion

Our study provides the first estimates of embryo mortality and reproductive performance of female P. argus infected with C. conanobrieni in a southern Caribbean (Colombia) population. This egg predator’s initial discovery in the Florida Keys has led to more studies reporting the prevalence of C. conanobrieni across P. argus’ distribution in the greater Caribbean, Saint Kitts and Nevis, and Colombia [9, 12, 13, 24]. Our results suggest that the high prevalence of this egg predator is causing a decline in individual-level reproductive performance measures. Multiple researchers have justified for the temporal monitoring of this population and other populations across the entire Caribbean given the growing prevalence and impacts of C. conanobrieni and undescribed Carcinonemertes sp. on P. argus [12, 13]. In agreeance with other researchers, we encourage the sampling of P. argus reproductive performance and overall health across its other Caribbean localities including Belize, Bermuda, and the Cayman Islands, all of which have also not yet been investigated for C. conanobrieni presence. Additionally, since Carcinonemertes sp. can also be found to infect multiple hosts, we suggest the screening of other exploited and non-exploited decapod crustaceans, including the spotted spiny lobster P. guttatus, the smoothtail spiny lobster P. laevicauda, and Florida stone crabs Menippe spp.

Methods

Sampling of Panulirus argus

Sampling was conducted with the authorization of the “Autoridad Nacional de Licencias Ambientales ANLA'' under permit 1293—2013 “Permiso marco de recolección de especímenes de especies silvestres de la diversidad biológica con fines de investigación científica no comercial, resolución” given to Universidad del Magdalena, Santa Marta, Colombia. Between March 16th and October 26th, 2019, a total of ninety P. argus ovigerous females were caught by artisan fishers from shallow hard-bottom environments north of the Gulf of Salamanca (latitude: 11.03 to 11.06 ºN, longitude: -74.42 to -74.62 ºW), Magdalena, Colombia. Immediately after capture, lobsters were transported in ice-chests to the laboratory of the “Grupo de Investigación en Manejo y Conservación de Flora Fauna y Ecosistemas Estratégicos Netropicales MIKU'' at Universidad del Magdalena and euthanized within 24 h. We note that lobsters were not individually maintained in the ice-chests. Preliminary observations have shown that C. conanobrieni worms do not move much, are not efficient at crawling, and do not swim (AB, NS, and JAB). Therefore, the probability of worms moving among lobsters during their transportation to the laboratory was null.

Carcinonemertes conanobrieni prevalence, intensity and embryo mortality

To understand the effect of C. conanobrieni on P. argus reproductive performance and embryo mortality, we measured prevalence and intensity of the egg predator on individual females. In the laboratory, each brooding lobster was measured (CL = length of the cephalothorax expressed in mm, precision = 0.1 mm) and the developmental stage of their brooded embryos were classified following [10] as: stage I, embryos with evenly distributed yolk, no separation between yolk and chorion; stage II, embryos with cellular differentiation, yolk and chorion begin to separate; stage III, embryos with pigmentation in the eyes; stage IV, embryos with developed eyes, thoracic appendages, and chromatophores (red pigments). Next, all eight pleopods (each carrying eggs) were carefully dissected with fine tip forceps. A random subsample of ~ 1000 embryos (~ 2–3 mm3) was isolated from each pleopod egg mass (n = 8 per brooding female) and transferred to Petri dishes containing micro-filtered seawater. Each sub-sample was then inspected for the abundance (if worms were observed) and presence or absence of the different life stages of C. conanobrieni under a dissecting microscope (Stemi DV4, Carl Zeiss, Germany). The different ontogenetic stages of C. conanobrieni included (i) adults (either roaming among the lobster eggs or in sheaths), (ii) encysted juveniles, and (iii) embryo aggregation (worm egg masses) [10, 24]. Additionally, we determined the presence or absence of dead lobster embryos and totaled dead embryos for each lobster egg sub-sample. Dead lobster embryos were recognized as fully or partially empty cases or as cases with lobster embryos having abnormal size (smaller or larger than the surrounding embryos), shape (usually a-symmetrical), and coloration (either a dark brown or a light, milky orange) [10].

Egg predator prevalence was estimated as the number of infected lobsters with at least one C. conanobrieni in at least one pleopod divided by the total number of lobsters sampled (n = 90). C. conanobrieni intensity was calculated as the average number of egg predators found per examined pleopod (n = 8) in each lobster [48]. Finally, egg mortality was expressed as the average proportion of dead eggs observed per pleopod in the 1000 embryos subsamples.

Lobster fecundity and reproductive performance

We calculated two individual-level reproductive performance parameters in infected and uninfected P. argus brooding females: fecundity and reproductive output (RO). In this study, fecundity is defined as the total number of embryos carried underneath the abdomen by a brooding female lobster and the words eggs or embryos are used indistinctly. Reproductive output refers to the amount of biomass or fraction of energy that the female invests in reproduction, and this parameter was estimated as the ratio between the dry weight of the embryos and the dry weight of the lobster body [10, 49].

Our two measures of reproductive performance, fecundity and reproductive output, were evaluated following past investigations into ovigerous female P. argus [10]. Five random subsamples of 100 embryos each, the remaining embryonic mass (MR), and the whole body of each lobster, were dried separately at 68 °C until constant weight (approx.120 h) and then weighed with an analytical balance (OHAUS; 0.1 mg). Fecundity was calculated with the formula: F = [(((Massembryos / Average (Masssub1, Masssub2, Masssub3, Masssub4, Masssub5))*100) + 500)]; where F = the total number of embryos, Massembryos = the dry weight of the remaining embryo mass after the five 100 subsamples were removed, Masssub# = the dry weight of one of the embryo subsamples of 100, and the 500 added back in represents the total number of embryos removed for the sub-samples [10]. Reproductive output was calculated with the formula: RO = Massembryos / Massfemale; where RO = reproductive output, Massembryos = the dry weight of the five 100 eggs sub-samples plus the remaining embryo mass after the subsamples were removed, and Massfemale = the dry weight of the female lobster after their eggs were extracted.

The effect of the egg predator on fecundity and reproductive performance of Panulirus argus

We used Redundancy Analysis (RDA), a multivariate constrained ordination technique [50,51,52], to (i) determine which host (lobster) traits were the most significant to explain variation in the occurrence of different life stages of C. conanobrieni in lobster egg masses and (ii) examine the effects of C. conanobrieni (adults) on lobster egg mortality and fecundity/reproductive output. RDA extracts and summarizes the variance in a set of dependent variables (matrix Y) that can be explained by a set of (quantitative or qualitative) predictive variables [50, 51]. In the RDA analysis, multiple linear regressions are used to ‘explain’ variation between the independent and dependent variables, and these calculations are performed within an iterative procedure to find the best ordination of the samples [53]. Graphically, the results of a RDA are presented in the form of biplots showing response variables, qualitative explanatory variables as centroids, and quantitative variables as vectors. RDAs were performed in CANOCO 4.5 for Windows using the automatic forward selection procedure, and the statistical significance of each predictor variable was determined using 500 Monte Carlo permutations. Differences at alpha < 0.05 were considered statistically significant.

In the first RDA, we analyzed the relationship between host traits (X-matrix) and the occurrence of different nemertean life stages per pleopod (Y-matrix). The explanatory matrix in this first analysis included log-transformed values of carapace length (LC), dry body weight (dBW), dry brood weight (DBW), fecundity (n° eggs × 103), and host egg stage (n = 4 stages). The response matrix included n° adult nemerteans, n° nemertean cysts, and n° egg sacs recorded in each of the four pairs of pleopods. Prior to the analysis, we explored collinearity between different predictor variables and found high collinearity (assessed using variance inflation factors [VIFs]) between dBW and DBW, dBW and fecundity, and DBW and fecundity (each observed VIF´s > 30). Therefore, dBW and DBW were excluded from the analysis to avoid model over-parameterization.

In the second RDA, we examined the effects of C. conanobrieni on lobster egg mortality and reproductive output. The predictor matrix in this analysis included the abundance of adult nemertean worms in each one of the four pairs of pleopods as well as host development stage while the dependent Y- matrix consisted of host-dead embryos (log[x + 1] transformed data) recorded in each of the four pairs of pleopods and reproductive output. No evidence of collinearity between the predictor variables was found prior to the analysis (VIF < 2.9).

Availability of data and materials

All datasets on which the conclusions of the manuscript rely are presented in the main text of the manuscript.

Abbreviations

CL:

Carapace length

SD:

Standard deviation

ANCOVA:

Analysis of covariance

RO:

Reproductive output

RDA:

Redundancy analysis

min:

Minimum

max:

Maximum

dBW:

Dry body weight

DBW:

Dry brood weight

Fec:

Fecundity

VIFs:

Variance inflation factors

References

  1. Holthuis LB. Marine lobsters of the world. Rome: FAO; 1991.

    Google Scholar 

  2. Duarte LO, Manjarrés-Martínez L. Estadísticas de desembarco y esfuerzo de las pesquerías artesanales e industriales de Colombia entre febrero y diciembre de 2019. Bogotá: Autoridad Nacional de Acuicultura y Pesca (AUNAP); 2019.

    Google Scholar 

  3. Seijo JC. Considerations for management of metapopulations in small-scale fisheries of the Mesoamerican barrier reef ecosystem. Fish Res. 2007;87(1):86–91. https://0-doi-org.brum.beds.ac.uk/10.1016/j.fishres.2007.06.016.

    Article  Google Scholar 

  4. Gracia A, Díaz JM. Panulirus argus. En: Ardila NE, Navas GR, Reyes JO, editores. Libro rojo de los invertebrados marinos de Colombia. INVEMAR. Ministerio del Medio Ambiente. Serie: Libros rojos de especies amenazadas de Colombia. Bogotá. 2002. 113-5.

  5. Ardila NE, Navas GR, Reyes JO. Libro rojo de invertebrados marinos de Colombia. INVEMAR. Ministerio de Medio Ambiente. La serie Libros rojos de especies amenazadas de Colombia. Bogotá, Colombia; 2002.

  6. Butler MJIV, Hunt JH, Herrnkind WF, Childress MJ, Bertelsen R, Sharp W, et al. Cascading disturbances in Florida Bay, USA: cyanobacteria blooms, sponge mortality, and implications for juvenile spiny lobsters Panulirus argus. Mar Ecol Prog Ser. 1995;129:119–25.

    Article  Google Scholar 

  7. Ross E, Behringer D. Changes in temperature, pH, and salinity affect the sheltering responses of Caribbean spiny lobsters to chemosensory cues. Sci Rep. 2019;9:4375. https://0-doi-org.brum.beds.ac.uk/10.1038/s41598-019-40832-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Puga R, Piñeiro R, Alzugaray R, Cobas LS, De León ME, Morales O. Integrating anthropogenic and climatic factors in the assessment of the Caribbean spiny lobster (Panulirus argus) in Cuba: Implications for fishery management. Int J Mar Sci. 2013;3(6):36–45.

    Google Scholar 

  9. Atherley NAM, Freeman MA, Dennis MM. Post-mortem examination of the Caribbean spiny lobster (Panulirus argus, Latreille 1804) and pathology in a fishery of the Lesser Antilles. J Invertebr Pathol. 2020;175:107453. https://0-doi-org.brum.beds.ac.uk/10.1016/j.jip.2020.107453.

    Article  CAS  PubMed  Google Scholar 

  10. Baeza JA, Simpson L, Ambrosio LJ, Mora N, Guéron R, Childress MJ. Active parental care, reproductive performance, and a novel egg predator affecting reproductive investment in the Caribbean spiny lobster Panulirus argus. BMC Zool. 2016;1:6. https://0-doi-org.brum.beds.ac.uk/10.1186/s40850-016-0006-6.

    Article  Google Scholar 

  11. Simpson LA, Ambrosio LJ, Baeza JA. A new species of Carcinonemertes, Carcinonemertes conanobrieni sp. nov. (Nemertea: Carcinonemertidae), an egg predator of the Caribbean spiny lobster, Panulirus argus. PLoS One. 2017;12(5):e0177021. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pone.0177021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gonzalez-Cueto J, Quiroga S. First record of Carcinonemertes conanobrieni Simpson, Ambrosio & Baeza, 2017 (Nemertea, Carcinonemertidae), an egg predator of the Caribbean spiny lobster Panulirus argus (Latreille, 1804), on the Caribbean Coast of Colombia. Check List. 2018;14(2):425–9. https://0-doi-org.brum.beds.ac.uk/10.15560/14.2.425.

    Article  Google Scholar 

  13. Atherley NAM, Dennis MM, Freeman MA, Freeman. Two species of Carcinonemertes Coe, 1902 (Nemertea: Carcinonemertidae) infesting the Caribbean spiny lobster, Panulirus argus (Latreille, 1804) (Decapoda: Achelata: Palinuridae), in Saint Kitts, West Indies. West Indies J Crust Biol. 2020;40(6):933–42. https://0-doi-org.brum.beds.ac.uk/10.1093/jcbiol/ruaa060.

    Article  Google Scholar 

  14. Wickham DE. A new species of Carcinonemertes (Nemertea: Carcinonemertidae) with notes on the genus from the pacific coast. Proc Biol Soc Wash. 1978;91:197–202.

    Google Scholar 

  15. Kuris AM, Wickham DE. Effect of nemertean egg predators on crustaceans. Bull Mar Sci. 1987;41(2):151–64.

    Google Scholar 

  16. Shields JD, Kuris AM. Temporal variation in abundance of the egg predator Carcinonemertes epialti (Nemertea) and its effect on egg mortality of its host, the shore crab. Hemigrapsus oregonensis. Hydrobiologia. 1988;156:31–8.

    Article  Google Scholar 

  17. Shields JD, Wickham DE, Blau SF, Kuris A. Some implications of egg mortality caused by symbiotic nemerteans for data acquisition and management strategies of red king crabs, Paralithodes camtschatica. Proc Int Symp King Tanner Crabs. 1990:383–95.

  18. Wickham DE. Aspects of the life history of Carcinonemertes errans (Nemertea: Carcinonemertidae), an egg predator of the crab Cancer magister. Biol Bull. 1980;159(1):247–57. https://0-doi-org.brum.beds.ac.uk/10.2307/1541022.

    Article  Google Scholar 

  19. Wickham DE, Kuris AM. The comparative ecology of nemertean egg predators. Amer Zool. 1985;25(1):127–34. https://0-doi-org.brum.beds.ac.uk/10.1093/icb/25.1.127.

    Article  Google Scholar 

  20. Wickham DE. Predation by the nemertean Carcinonemertes errans on eggs of the Dungeness crab Cancer magister. Mar Biol. 1979;55(1):45–53. https://0-doi-org.brum.beds.ac.uk/10.1007/BF00391716.

    Article  Google Scholar 

  21. Kuris AM. Life cycles of nemerteans that are symbiotic egg predators of decapod Crustacea: adaptations to host life histories. Hydrobiologia. 1993;266(1):1–14. https://0-doi-org.brum.beds.ac.uk/10.1007/BF00013355.

    Article  Google Scholar 

  22. Kuris AM, Blau SF, Paul A, Shields JD, Wickham DE. Infestation by brood symbionts and their impact on egg mortality of the red king crab, Paralithodes camtschatica, in Alaska: geographic and temporal variation. Can J Fish Aquat Sci. 1991;48(4):559–68.

    Article  Google Scholar 

  23. Torchin ME, Lafferty KD, Kuris AM. Infestation of an introduced host, the European green crab, Carcinus maenas, by a symbiotic nemertean egg predator. Carcinonemertes epialti. J Parasitol. 1996;82(3):449–53. https://0-doi-org.brum.beds.ac.uk/10.2307/3284084.

    Article  CAS  PubMed  Google Scholar 

  24. Simpson LA. Carcinonemertes conanobrieni: A Nemertean Parasite Infecting the Caribbean Spiny Lobster, Panulirus argus: Species Description, Host-Use, and Effect on Host Reproductive Health. Clemson: Clemson University Press; 2018. p. 2018.

    Google Scholar 

  25. Campbell A, Gibson R, Evans LH. A new species of Carcinonemertes (Nemertea: Carcinonemertidae) ectohabitant on Panulirus cygnus (Crustacea: Palinuridae) from Western Australia. Zool J Linn Soc. 1989;95(3):257–68. https://0-doi-org.brum.beds.ac.uk/10.1111/j.1096-3642.1998.tb01992b.x.

    Article  Google Scholar 

  26. Vijayakumaran M, Maharajan A, Rajalakshmi S, Jayagopal P, Subramanian MS, Remani MC. Fecundity and viability of eggs in wild breeders of spiny lobsters, Panulirus homarus (Linnaeus, 1758), Panulirus versicolor (Latrielle, 1804) and Panulirus ornatus (Fabricius, 1798). J Mar Biol Ass India. 2012;54(2):18–22.

    Google Scholar 

  27. Juinio MAR. Some aspects of the reproduction of Panulirus penicillatus (Decapoda: Palinuridae). Bull Mar Sci. 1987;41(2):242–52.

    Google Scholar 

  28. Baeza JA, Fernández M. Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behavior, embryo oxygen consumption and the cost of brooding. Funct Ecol. 2002;16:241–51. https://0-doi-org.brum.beds.ac.uk/10.1046/j.1365-2435.2002.00616.x.

    Article  Google Scholar 

  29. Baeza JA, Liu X, Kostecka L, Wortham J. Active parental care in the peppermint shrimp Lysmata boggessi: the effect of embryo age and circadian cycle. Mar Biol. 2019;166:132. https://0-doi-org.brum.beds.ac.uk/10.1007/s00227-019-3579-0.

    Article  CAS  Google Scholar 

  30. Annala JH, Bycrofft BL. Fecundity of the New Zealand red rock lobster Jasus edwardsii. New Zeal J Mar Fresh Res. 1987;21:591–7. https://0-doi-org.brum.beds.ac.uk/10.1080/00288330.1987.9516263.

    Article  Google Scholar 

  31. Green BS, Gardner C, Kennedy RB. Generalized linear modeling of fecundity at length in southern rock lobsters. Jasus edwardsii Mar Biol. 2009;156:1941–7. https://0-doi-org.brum.beds.ac.uk/10.1007/s00227-009-1226-x.

    Article  Google Scholar 

  32. Arana E, Dupre M, Gaete M. Ciclo reproductivo, talla de primera madurez sexual y fecundidad de la langosta de Juan Fernandez (Jasus frontalis). Investig Mar. 2000;28:165–74.

    Google Scholar 

  33. Hogarth PJ, Barratt LA. Size distribution, maturity and fecundity of the spiny lobster Panulirus penicillatus (Oliver 1791) in the Red Sea. Trop Zool. 1996;9(2):399–408. https://0-doi-org.brum.beds.ac.uk/10.1080/03946975.1996.10539319.

    Article  Google Scholar 

  34. Kawate PV. Fecundity in the spiny lobster Panulirus polyphagus (Herbst). J Mar Biol Ass India. 1988;30(1):114–20.

    Google Scholar 

  35. MacDonald CD. Fecundity and reproductive rates in Indo-West Pacific spiny lobsters. Micronesica. 1988;21:103–14.

    Google Scholar 

  36. MacFarlane JW, Moore R. Reproduction of the ornate rock lobster, Panulirus ornatus (Fabricius), in Papua New Guinea. Aust J Mar Freshw Res. 1986;37(1):55–65.

    Article  Google Scholar 

  37. Melville-Smith R, Goosen PC, Stewart TJ. The spiny lobster Jasus lalandii (H. Milne Edwards, 1837) off the South African coast: inter-annual variations in male growth and female fecundity. Crustaceana. 1837;1995(68):174–83.

    Google Scholar 

  38. Melville-Smith R, de Lestang S. Changes in egg production of the western rock lobster (Panulirus cygnus) associated with appendage damage. Fish Bull. 2007;105(3):418–26.

    Google Scholar 

  39. Quackenbush LS. Lobster reproduction: a review. Crustaceana. 1994;67(1):82–94.

    Article  Google Scholar 

  40. Goñi R, Quetglas A, Reñones O. Size at maturity, fecundity and reproductive potential of a protected population of the spiny lobster Palinurus elephas (Fabricius, 1787) from the western Mediterranean. Mar Biol. 2003;143:583–92. https://0-doi-org.brum.beds.ac.uk/10.1007/s00227-003-1097-5.

    Article  Google Scholar 

  41. Iacchei M, Robinson P, Miller KA. Direct impacts of commercial and recreational fishing on spiny lobster, Panulirus interruptus, populations at Santa Catalina Island, California, United States. N Z J Mar Freshw Res. 2005;39(6):1201–14. https://0-doi-org.brum.beds.ac.uk/10.1080/00288330.2005.9517386.

    Article  Google Scholar 

  42. DeMartini EE, Ellis DM, Honda VA. Comparisons of spiny lobster Panulirus marginatus fecundity, egg size, and spawning frequency before and after exploitation. Fish Bull. 1993;91:1–7.

    Google Scholar 

  43. MacDiarmid AB. Size at onset of maturity and size-dependent reproductive output of female and male spiny lobsters Jasus edwardsii (Hutton) (Decapoda, Palinuridae) in northern New Zealand. J Exp Mar Biol Ecol. 1989;127:229–43. https://0-doi-org.brum.beds.ac.uk/10.1016/0022-0981(89)90076-2.

    Article  Google Scholar 

  44. DeMartini EE, DiNardo GT, Williams HA. Temporal changes in population density, fecundity, and egg size of the Hawaiian spiny lobster (Panulirus marginatus) at Necker Bank. Northwest Hawaiia Isl Fish Bull. 2003;101(1):22–31.

    Google Scholar 

  45. Pérez-González R, Valadez LM, Rodríguez-Domínguez G, Aragón-Noriega EA. Seasonal variation in brood size of the spiny lobster Panulirus gracilis (Decapoda: Palinuridae) in Mexican waters of the Gulf of California. J Shellfish Res. 2012;31(4):935–40. https://0-doi-org.brum.beds.ac.uk/10.2983/035.031.0404.

    Article  Google Scholar 

  46. Hines AH. Constraint on reproductive output in brachyuran crabs: Pinnotherids test the rule. Am Zool. 1992;32(3):503–11. https://0-doi-org.brum.beds.ac.uk/10.1093/icb/32.3.503.

    Article  Google Scholar 

  47. Atherley NA, Dennis MM, Behringer DC, Freeman MA. Size at sexual maturity and seasonal reproductive activity of the Caribbean spiny lobster Panulirus argus. Mar Ecol Prog Ser. 2021;671:129–45. https://0-doi-org.brum.beds.ac.uk/10.3354/meps13762.

    Article  Google Scholar 

  48. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol. 1997;83(4):575–83. https://0-doi-org.brum.beds.ac.uk/10.2307/3284227.

    Article  CAS  PubMed  Google Scholar 

  49. Clarke A, Hopkins CC, Nilssen EM. Egg size and reproductive output in the deep-water prawn Pandalus borealis Kroyer, 1838. Funct Ecol. 1991;5(6):724–30. https://0-doi-org.brum.beds.ac.uk/10.2307/2389534.

    Article  Google Scholar 

  50. Ter Braak CJF. Correspondence analysis of incidence and abundance data: properties in terms of a unimodal response model. Biometrics. 1985;41(4):859–73. https://0-doi-org.brum.beds.ac.uk/10.2307/2530959.

    Article  Google Scholar 

  51. Ter Braak, CJF, Šmilauer P. CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power. 2002, p. 500.

  52. Legendre P, Oksanen J, ter Braak CJ. Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol. 2011;2(3):269–77. https://0-doi-org.brum.beds.ac.uk/10.1111/j.2041-210X.2010.00078.x.

    Article  Google Scholar 

  53. Šmilauer P, Lepš J. Multivariate Analysis of Ecological Data using CANOCO 5. 2nd ed. Cambridge: Cambridge University Press; 2014. https://0-doi-org.brum.beds.ac.uk/10.1017/CBO9781139627061

  54. Marciano A, Greco LSL, Colpo KD. Factors Modulating the Female Reproductive Performance of the Fiddler Crab Leptuca uruguayensis with Short Reproductive Season. Biol Bull. 2022;242:16–26.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the Autoridad Nacional de Licencias Ambientales (ANLA) for awarding the permits for specimen collection. Special thanks to the artisanal fishermen of the Gulf of Salamanca, who helped in obtaining the lobsters specimens.

Funding

This research was funded by Fonciencias 2017 of the Universidad del Magdalena, with Permit resolution number 0080 of January 17, 2019 by the Corporación Autónoma regional del Magdalena CORPAMAG.

Author information

Authors and Affiliations

  1. Universidad del Magdalena, Santa Marta, Colombia

    Amanda Berben, Jaime Gonzalez-Cueto, Yulibeth Velasquez & Sigmer Quiroga

  2. Department of Biological Sciences, Clemson University, 132 Long Hall, Clemson, SC, 29634, USA

    Natalie C. Stephens & J. Antonio Baeza

  3. Facultad de Ciencias del Mar Y Recursos Biológicos, Instituto de Ciencias Naturales “Alexander Von Humboldt”, Universidad de Antofagasta, Angamos, 601, Antofagasta, Chile

    María Teresa González

  4. Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, FL, 34949, USA

    J. Antonio Baeza

  5. Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile

    J. Antonio Baeza

Authors
  1. Amanda Berben
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natalie C. Stephens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaime Gonzalez-Cueto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yulibeth Velasquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sigmer Quiroga
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. María Teresa González
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Antonio Baeza
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AB carried out field work, sample processing and contributed to the analysis and writing of the results. NS contributed to data analysis and discussion writing. JGC performed fieldwork, sample processing, and contributed to the writing of the manuscript. YV carried out field work and sample processing. SQ contributed to the writing and critical review of the manuscript. MTG performed the statistical analyses. JAB analyzed and interpreted the statistical data, contributed to the writing and critical revision of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to J. Antonio Baeza.

Ethics declarations

Ethics approval and consent to participate

No approval by an ethical committee was required to accomplish the goals of the present study because experimental work was conducted with an unregulated marine invertebrate. Sampling was conducted with the authorization of the “Autoridad Nacional de Licencias Ambientales ANLA'' under permit 1293—2013 “Permiso marco de recolección de especímenes de especies silvestres de la diversidad biológica con fines de investigación científica no comercial, resolución” given to Universidad del Magdalena, Santa Marta, Colombia.

Consent for publication

Non applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1:

Supplementary Table 1. First RDA constrained analysis of simple effect terms. Supplementary Table 2. Second RDA constrained analysis simple effect terms.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berben, A., Stephens, N.C., Gonzalez-Cueto, J. et al. The effect of the egg-predator Carcinonemertes conanobrieni on the reproductive performance of the Caribbean spiny lobster Panulirus argus. BMC Zool 8, 6 (2023). https://0-doi-org.brum.beds.ac.uk/10.1186/s40850-023-00165-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://0-doi-org.brum.beds.ac.uk/10.1186/s40850-023-00165-w

Keywords

BMC Zoology

ISSN: 2056-3132

Contact us