Average Amount of Babies Produced With a Seahorse

Biol Open up. 2012 Apr 15; ane(four): 391–396.

The dynamics of reproductive rate, offspring survivorship and growth in the lined seahorse, Hippocampus erectus Perry, 1810

Qiang Lin

ⁱKey Laboratory of Marine Bio-resources Sustainable Utilization, South China Ocean Plant of Oceanology, Chinese University of Sciences, Guangzhou 510301, P. R. China

²Vero Beach Marine Laboratory, Florida Establish of Technology, Vero Beach, FL 32963, U.s.a.

Gang Li

^oneKey Laboratory of Marine Bio-resources Sustainable Utilization, Southward China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, P. R. People's republic of china

Geng Qin

¹Fundamental Laboratory of Marine Bio-resource Sustainable Utilization, South Communist china Ocean Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, P. R. Communist china

Junda Lin

²Vero Beach Marine Laboratory, Florida Constitute of Technology, Vero Beach, FL 32963, U.s.

Liangmin Huang

ⁱFundamental Laboratory of Marine Bio-resources Sustainable Utilization, South China Bounding main Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, P. R. China

Hushan Sun

ⁱⁱⁱKey Laboratory of Biotechnology, School of Life Sciences, Ludong University, Yantai 264025, P. R. China

Peiyong Feng

³Primal Laboratory of Biotechnology, School of Life Sciences, Ludong University, Yantai 264025, P. R. China

Summary

Seahorses are the vertebrate grouping with the embryonic development occurring inside a special pouch in males. To empathize the reproductive efficiency of the lined seahorse, Hippocampus erectus Perry, 1810 under controlled breeding experiments, nosotros investigated the dynamics of reproductive rate, offspring survivorship and growth over births by the aforementioned male seahorses. The hateful brood size of the 1-year old pairs in the one^st nativity was 85.four±56.nine per brood, which was significantly smaller than that in the six^thursday nascency (465.9±136.four per breed) (P<0.001). The offspring survivorship and growth rate increased with the births. The fecundity was positively correlated with the length of brood pouches of males and trunk of females. The fecundity of 1-yr old male person and ii-yr old female pairs was significantly higher than that from i-year quondam couples (P<0.001). The breed size (552.7±150.iv) of the males who mated with females that were isolated for the gamete-preparation, was larger than those (467.8±141.2) from the long-term pairs (P<0.05). Moreover, the offspring from the isolated females had higher survival and growth rates. Our results showed that the potential reproductive charge per unit of seahorses H. erectus increased with the brood pouch evolution.

Keywords: Fecundity, Reproductive efficiency, Seahorses, Hippocampus erectus

Introduction

In most animals, the potential reproductive charge per unit is the population's mean offspring product when not constrained past the availability of mates (Clutton-Brock and Vincent, 1991; Clutton-Brock and Parker, 1992; Parker and Simmons, 1996; Wilson et al., 2003), and the reproductive rate often vary considering of mating competition and parental investment (Trivers, 1972). In some syngnathid species, the reproduction is influenced by the complex brooding structure, brood pouch evolution, sexual selection, mating patterns and social promiscuity (Parker and Simmons, 1996; Carcupino et al., 2002; Wilson et al., 2003; Vincent et al., 2004; Lin et al., 2006; Naud et al., 2009).

The family Syngnathidae (seahorses and pipefishes) is the sole vertebrate group where the embryonic development occurs within a special pouch in males (Herald, 1959) that provides aeration, protection, osmoregulation and diet to the embryo or offspring after the females depositing eggs during mating (Linton and Soloff, 1964; Berglund et al., 1986; Partridge et al., 2007; Ripley, 2009). This pouch is like to the placental function in mammals and acts like the mammalian uterus, and the embryos become embedded inside depressions of the interior lining of the brood pouch (Carcupino et al., 1997; Foster and Vincent, 2004).

For syngnathid species, the survivorship of offspring is often used to evaluate the reproductive ability of the parents (Wootton, 1990; Cole and Sadovy, 1995; Vincent and Giles, 2003). The offspring survivorship of pipefish inside a pregnancy is affected past the size of the female, the number of eggs transferred and the male'south sexual responsiveness (Paczolt and Jones, 2010). Dzyuba et al. (Dzyuba et al., 2006) reported that in the seahorse Hippocampus kuda the parental size and historic period could affect the number, survivorship and fifty-fifty the growth of the offspring. Not all the eggs deposited in the male'south pouch successfully complete the evolution and hatch equally juveniles (offspring). For example, 1.23% of the eggs failed to develop in the pouch of wild H. abdominalis (Foster and Vincent, 2004); 2–33% of the eggs were found to be sterile in H. erectus pouches (Teixeira and Musick, 2001); and 45% of the eggs were lost during the pregnancy of H. fuscus (Vincent, 1994a). Moreover, the gonad development, clutch size and even the mate competition and physical interference during courtship and egg transfer should also be considered when estimating the offspring number from parents (Vincent and Giles, 2003; Foster and Vincent, 2004; Lin et al., 2006; Lin et al., 2007; Paczolt and Jones, 2010).

Many studies on understanding the potential reproductive rate in seahorses have been conducted through estimating the operational sex ratios, courting roles, parental investment patterns, mate competitions so on (A. C. J. Vincent, Reproductive Ecology of Seahorses, PhD thesis, Cambridge University, Britain, 1990) (Vincent, 1994a; Vincent, 1994b; Masonjones, 1997; Masonjones and Lewis, 2000). For the investigation of bloodshed and growth of offspring, most reports focus on the controlled culture experiments, such as furnishings of environmental factors, diets and civilisation protocols on the survivorship in a express duration (Scarratt, 1996; Task et al., 2002; Woods, 2000; Woods, 2003; Hilomen-Garcia et al., 2003; Lin et al., 2008; Koldewey and Martin-Smith, 2010).

The seahorse has a special reproductive strategy, but no report has been fabricated on the dynamics of reproductive rate, especially in the first few births. The lined seahorse, H. erectus Perry, 1810 is mainly plant from Nova Scotia along the western Atlantic coast, through the Gulf of Mexico and Caribbean area to Venezuela, in shallow inshore areas to depths of over 70 1000 (Scarratt, 1996; Lourie et al., 1999; Lin et al., 2008). The purpose of the nowadays study was to investigate the dynamics of the reproductive rate over the get-go few births, and then evaluate the effects of parent ages and mating limitation on the reproductive rate, offspring survivorship and growth of H. erectus.

Materials and Methods

Experimental seahorses

The lined seahorses H. erectus used in this study were cultured in Leizhou Seahorse Center of S Prc Bounding main Institute of Oceanology, Chinese Academy of Sciences (SCSIO-CAS) (latitude 110.04°E, longitude 20.54°N) with Brute Ideals approving for experimentation granted by the Chinese University of Sciences.

The F2 generation of this species was used for all the controlled convenance experiments. After being released from the broodstock male person (F1), the offspring (F2) were cultured in split concrete outdoor ponds (5×4×1.4 grand), with recirculating sea water treated with double sand filtration. Seahorses were fed daily with rotifers, copepods, Artemia, Mysis spp. and Acetes spp. A black nylon mesh was used to shade the outdoor ponds to go on the light intensity beneath 3400 Lux. The temperature was 22–28°C and salinity was 31–34‰ during the study from March 2009 to March 2011.

Reproductive rate over successive nascency

Sex was determined by the presence or absence of brood pouch at approximately lxx days after birth. Seventy-five pairs of male person (standard trunk length: 10.3±0.6 cm) and female (standard body length: 8.seven±0.8 cm) F2 seahorses were haphazardly selected from the outdoor ponds and cultured in five indoor circular tanks (diameter 1.6 yard, depth 0.9 g) with the stocking density of fifteen pairs per tank (1 seahorse/60L). In order to judge the reproductive rate over successive nascence, the broods (i^st, two^nd, 3^rd, 4^th, 5^th and 6^th successive births) from the aforementioned pair were recorded. The seahorse pair that mated and and so successfully hatched the offspring were marked by the nylon ring with number around their necks. Plastic plants and corallites were used as the substrate and holdfasts for the fish. The indoor husbandry protocol was the same as that in the outdoor ponds, and the light intensity was adjusted through the glass ceiling and black nylon mesh.

Fourteen, xiii, 12, 11, 9 and 9 batches of juveniles from 1^st, two^nd, 3^rd, 4^thursday, 5^th and six^thursday successive births respectively were used to estimate the survivorship and growth of offspring. 60 juveniles haphazardly selected from each brood (batch) were cultured in 3 recirculating tanks (50×W×H, fifty×30×40 cm) (each with 20 juveniles) for 5 weeks. The juveniles were not fed during the beginning x hours later on nascence, then they were fed with copepods and newly hatched Artemia nauplii in excess. The temperature, salinity, dissolved oxygen (DO), light intensity and photoperiod in the tanks were 26±1.0°C, 32±one.0‰, six.5±0.five mg/L and 2000 Lux, and sixteen L (0700–2300 h): eight D (2300–0700 h), respectively. The tanks were aerated gently so as not to form excessive air bubbling and cause turbulence.

In gild to assess if the brood size was related to the body condition gene of parent seahorses, the brood pouch length (parallel length from the anus to the tip of the brood pouch on the tail) of the male seahorse and body length of the female person of each brooding pair were measured later on the copulation. So the linear regressions for the human relationship amid offspring number, brood pouch size of males and trunk length of females were analyzed.

Effect of parent ages

To compare the reproductive rate of young (one year onetime) (M1, F1, never mated) and sometime (2 years old) seahorse pairs (M2, F2, mated many times), iv combination treatments (M1: F1, M2: F1, M1: F2 and M2: F2, respectively) were prepare up, each with 4 replicates and each replicate had 15 pairs. The body lengths of the male and female person seahorses were 17.4±1.half-dozen and xv.8±2.one cm, respectively. Among the 60 pairs of parent seahorses in each treatment, 7 broods from 7 of the males were haphazardly selected and 100 juveniles in each brood were cultured for 5 weeks post-obit the same culture protocol as in the last experiment.

Result of mating limitation (female isolation)

In social club to investigate the effect of mating limitation (female isolation) on reproductive charge per unit of H. erectus, the control and experimental groups of ii-twelvemonth old seahorse pairs (males: xvi.6±2.one cm, females: fifteen.viii±one.7 cm) were used. In the control (TR-ane), threescore pairs of seahorses haphazardly selected from the concrete outdoor ponds were cultured in 4 indoor tanks (diameter 1.6 m, depth 0.nine m) as 4 replicates, and each tank had fifteen pairs with the stocking density of ane seahorse/60L. During the experiment, 4 successive births (TR-1-one, TR-1-2, TR-1-3 and TR-1-4, and 10, 10, 9 and 8 males released their offspring in each birth, respectively) from the same pair of seahorses were utilized.

In the experimental treatment (TR-2), 60 pairs of 2-twelvemonth old seahorses derived from the same breed stock as the seahorses in control group were besides cultured in 4 circular tanks (diameter 1.6 k, depth 0.nine chiliad) as 4 replicates, and each had fifteen pairs of seahorses. In a tank, the male and female person seahorses were cultured separately (male person groups and female groups) through a glass wall in the seawater. When the gonads of female person seahorse matured (the abdomen was bosomy and the cloaca was protuberant), the female was transferred over to the male person side. After the courting and mating, the female was put dorsum to the female side. The significant male seahorse released his babies at approximately twenty days after, depending on the h2o temperature and nutritional weather. The female seahorse (gonad already matured) was returned to the male side of the tank where she paired and mated again (not necessarily with the original partners) 6 days after the male person released his offspring (a modified method from Masonjones' and Lewis' investigation (Masonjones and Lewis, 2000)). Brood sizes from the four consecutive births (TR-2-1, TR-two-2, TR-2-3 and TR-2-iv, and 11, 9, 9 and viii males released their offspring in each nascence, respectively) were counted. The juveniles from both the control and the treatment groups were cultured for 5 weeks and the mean survival charge per unit and the distributions for standard trunk length of juveniles per brood were recorded.

Data assay

Statistical analyses were conducted using the software SPSS 17 (Statistical Program for Social Sciences 17) and Sigma PLOT 10.0. 1-way analysis of variance (ANOVA), regression analysis and Kolmogorov-Smirnov test were used to assess the relationship among the breed size, survival rate and trunk size of the juveniles among the treatments. All the variables were tested for normality and homogeneity. If ANOVA effects were significant, comparisons between the different ways were fabricated using post hoc least significant differences (LSD).

Results

Dynamics of reproductive rate

Among the 75 pairs of parent seahorses, 85 broods (batches) were concerned by 10 male seahorses at 6 successive births (ane^st (n = 21, 21 males released their offspring in the ane^st nativity), 2^nd (n = 16), iii^rd (n = 15), iv^th (northward = 12), v^th (n = 11) and 6^th (northward = 10), respectively) and only ten pairs of seahorses were monogamist. Brood size (fecundity) in the first 2 births was significantly lower than those in the following 4 (n = 85, F _{v, 79} = 21.28, P<0.001), and varied widely amongst the broods in the same birth (eastward.g. 46 to 237 per breed in the ane^st nascence, 294 to 752 per breed in the 6^th birth) (Fig. 1A). The brood size increased significantly during the first 3 births (Fig. 1A). The brood size (mean±S.D.) in the six successive births was 85.4±56.9, 216.vii±101.8, 400.1±127.v, 451.ii±123.8, 458.3±117.6 and 465.9±136.4, respectively, and can exist expressed past the formula: y = 232.25Ln(x) + 91.526 (r ² = 0.9412, F _{5, 79} = 21.28, P<0.001, n = 85).

Breed size, offspring survivorship and growth of young pair parent seahorses Hippocampus erectus at kickoff half dozen successive births.

1^st (n = 21 broods), 2^nd (due north = 16), 3^rd (northward = 15), 4^th (north = 12), five^thursday (n = eleven) and 6^th (northward = x), respectively. Different superscripts indicate the meaning difference among the treatments (P<0.05).

High mortality of the juveniles occurred in the first 3 births (northward = 68, F _{5, 62} = 4.97, P<0.001) (Fig. 1B). Body sizes (mean standard torso length) in the first 3 births were approximately 25% lower than those in the last 3 births after 5 weeks (n = 68, F _{v, 62} = v.25, P<0.001) (Fig. 1C).

The correlation betwixt brood pouch length and breed size was positively significant (F _{1, four} = 22.99, P = 0.0087, r² = 0.9229) (Fig. 2A), and the brood size was also significantly correlated with the body length of females (F _{1, four} = 78.08, P = 0.0009, rⁱⁱ = 0.9753) (Fig. 2B).

The relationships between breed size and brood pouch length.

Scatter-plots and linear regression lines for the relationships between brood size and brood pouch length of male person seahorses Hippocampus erectus (95% conviction bands); between brood size and the torso length of females (95% confidence bands) for the first 6 successive births.

Effect of parent age

Brood size from the 1-year one-time females (M1: F1, M2: F1) (89.half-dozen±36.9 and 122.2±49.5, respectively) was significantly smaller than those from the 2-twelvemonth old pairs (526.8±63.nine) (n = 40, F _{3, 36} = 152.42, P = 0.000). The pairs of 1-twelvemonth one-time males and ii-year onetime females produced intermediate number of offspring (302.4±113.8 per breed), which was significantly higher than that in groups of M1: F1 and M2: F1 (due north = 30, F _{2, 27} = 29.33, P = 0.000) (Fig. 3A).

Brood size and offspring survivorship under dissimilar ages.

Breed size and offspring survivorship nether different ages (M1: F1, M2: F1, M1: F2 and M2: F2) of pair parent seahorses Hippocampus erectus. Dissimilar superscripts indicate the significant departure amidst the treatments (P<0.05). M1, 1-year old male seahorse; F1, 1-twelvemonth old female seahorse; M2, ii years old male seahorse; F2, two years old female seahorse.

After 5 weeks, the juvenile seahorses had different survivorship among the four treatments (n = 28, F _{2, 24} = 5.53, P = 0.005), with the juveniles from ii-twelvemonth old parents had the highest survival rate of 75.i±8.ii%. The offspring from the 2-year old male and one-twelvemonth old female pairs (M2: F1, 69.viii±12.eight%) as well had a college survival charge per unit than those from 1-year old males (north = 28, F _{2, 18} = 1.902, P = 0.178) (Fig. 3B).

Outcome of mating limitation

Breed sizes from the 4 TR-ane handling were not significantly different from those of the four TR-two handling (mating limitation past females) (ANOVA-Tukey HSD analysis: n = 74, F _{7, 66} = 0.89, P = 0.513). However, when treated as ii groups, the mean brood size of TR-ane was 467.8±141.2 per brood, which was approximately 18% lower than those in TR-2 (552.7±150.4 per breed) (due north = 74, F _{i, 72} = 6.56, P = 0.013) (Fig. 4).

Brood size of iv successive births by male person seahorses Hippocampus erectus in the two groups (TR-1, TR-2).

In TR-one groups: male and female seahorses were cultured together (broods per birth: north = 10, 10, 9 and 8); in TR-2 groups: females were isolated (due north = 11, 9, ix and 8) (ANOVA-Tukey HSD analysis: n = 74, F _{7, 66} = 0.89, P = 0.513; 95% confidence bands).

The mean survival rate of the juveniles afterward five weeks of civilization in TR-1 and TR-2 was not significantly different (68.1±ten.0 and 70.2±vii.9%, respectively) (northward = 74, F _{1, 72} = 0.27, P = 0.610) (Fig. 5A). The mean standard trunk length of the juveniles in TR-one and TR-2 were 69.two±21.5 and 74.4±18.7 mm (K-S exam: northward = 74, F _{one, 72} = ii.17, P<0.05). The mean frequency distributions of standard body length of the juveniles in the two groups were shown in Fig. 5B. Most juveniles in TR-2 distributed between 70 to 85 mm in standard body length, and in TR-1, the juveniles' trunk length ranged from 65 to 75 mm.

Survivorship and frequency distribution.

Survivorship and frequency distribution by standard body length growth comparison of juvenile seahorses Hippocampus erectus in TR-1 and TR-2 subsequently 5-calendar week culture.

Discussion

Our results show that the immature pairs of seahorses H. erectus had smaller breed size, poor offspring survivorship and growth, when compared with those from the former pair parents. However, they could improve their reproductive efficiency over few successive births. Information technology was reported that in gulf pipefish Syngnathus scovelli, prior pregnancy of males could influence the latter reproduction through the post-copulatory sexual selection and sexual conflict between both sexes in a controlled breeding experiment (Paczolt and Jones, 2010). In this report, the mean brood size increased from 85.4±56.9 in the 1^st birth to 465.ix±136.4 in the 6^th nativity with the increase of the births in the young pairs of H. erectus. This is similar with the finding for H. kuda that big parents can reproduce much offspring (Dzyuba et al., 2006). In the wild, the brood size of H. erectus was large, with the maximum nascency number of 1552 juveniles (Teixeira and Musick, 2001), which was significantly larger than that from the cultured pairs (Lin et al., 2008; present study). This is partly because the development and metabolic charge per unit of seahorse changed under the low social interaction and low mating competition in the wild (Vincent, 1994a, b; Naud et al., 2009). To ascertain the relationship among the unlike births past the same male, we used the same body size of females to decrease the probability of the size-biased sexual pick and mate switching (Naud et al., 2009; Hunt et al., 2009; Paczolt and Jones, 2010). During the study, the fidelities were relatively low in about pairs during the reproductive process, so only 10 males amidst 75 pairs were found to mate with the same females during the 6 successive births. During the civilisation, pairs of H. erectus had brusque greeting and re-mating durations before or after each copulation, which significantly improved the reproductive charge per unit. This result is similar to the investigation that the mate choices of males could be reinforced by females with more pronounced secondary sexual characters during post-copulatory sexual selection in S. scovelli (Paczolt and Jones, 2010).

During the study, the young couples were still growing and and then they should have college reproductive efficiency than before, and this might brandish a status that the number and survival rate of offspring significantly increased over successive births. The large sizes of brood pouches with the growth of the males were able to fit more eggs from females. This is consistent with the report that the old seahorses H. kuda with large body sizes had the larger brood size and higher offspring growth and survival charge per unit (Dzyuba et al., 2006).

We found stiff positive linear correlations between the male person pouch size and number of offspring produced, as well equally between the female standard trunk length and the number of offspring produced. Equally it provides for some nutrition, aeration and osmoregulation for developing embryos (Linton and Soloff, 1964; Berglund et al., 1986; Partridge et al., 2007), the surface area of the male's brood pouch is a limiting factor in the number of embryos that can be successfully incubated (Azzarello, 1991; Dzyuba et al., 2006). Therefore, the correlation between brood size and brood pouch length of male seahorses was positive. Paczolt and Jones (Paczolt and Jones, 2010) found a stiff positive correlation betwixt the number of eggs transferred and female size in S. scovelli. Similarly, female size in pipefish can affect the egg size and concentration of eggs inside the male person pouch (Berglund et al., 1986; Ahnesjö, 1992; Watanabe and Watanabe, 2002). However, the larger size males exercise non necessarily release larger sized offspring than those from smaller size males, and we take institute that the body size of offspring was correlated with the brood size, gestation time and nutrient supply in the same males and females' investment (Lin et al., 2008; present report).

The mean number of offspring from the 2-twelvemonth old female and i-year old male pairs (302.iv±113.eight per breed) was much higher than those from 1-year old pairs (89.6±36.9 inds/breed, n = 30, F _{2, 27} = 29.33, P = 0.000). This upshot is similar to the report that the female fecundity in pipefish increases over 2.5 times from the small-scale (1-year quondam) to large females (2-year old) (Berglund and Rosenqvist, 1990). Compared with the ane-year old males, 2-twelvemonth quondam males released more offspring after mating with i-year or 2-year old females (increased 36.iv% and 74.2% with 1-yr and two-year old females, respectively). In addition, the survivorship of offspring released from the two-year old males was higher than that from the ane-yr former males (Fig. 3B). This may be due to the increased size of brood pouches of the old males, or better function of the pouches in old males (Berglund et al., 1986; Azzarello, 1991; Carcupino et al., 2002; Dzyuba et al., 2006). This is similar to the study that the difference in the reproductive rate of male person and female Syngnathus typhle increases as the fish age (Svensson, 1988). All the same, this does not display that the older seahorses have improve quality offspring, and the quality is generally correlated with the brood pouch development, gestation time and parental investment (Vincent et al., 2004; Lin et al., 2008; Naud et al., 2009).

Masonjones and Lewis (Masonjones and Lewis, 2000) limited the sexual receptivity in female seahorses H. zosterae through isolating the females separately and then induced the sexual contest among the males, and their results showed that the females need a relatively long time investment to prepare to mate with the males. In this study, the mating competition amongst the male person seahorses was strong and males sometimes courted with the females who were not set up. This is similar to the written report that the male seahorses H. fuscus competed more intensively than females (Vincent, 1994a). Therefore, we guess that the mating contest among the males could influence the reproductive efficiency through affecting the gamete preparation of females (or decreasing the investment from the females). Data showed that the mean brood size in the couples of males and isolated females (552.7±150.4 per brood) was larger than that in the controls (467.8±141.two per brood, north = 74, F _{ane, 72} = 6.56, P = 0.013), although the survival rates of the offspring were non significantly different betwixt the two groups (due north = 74, F _{1, 72} = 0.27, P = 0.610). Furthermore, juveniles derived from the group of isolated females had a high growth rate and broad frequency distribution of trunk sizes. This partly is due to the quality of newborn offspring. Dzyuba et al. (Dzyuba et al., 2006) have shown that the quality conditions of parent seahorses could significantly influence the offspring growth and survival rates. And so, the frequency distributions of body sizes might be the criteria for assessing the quality of broodstock of the parent seahorses.

This is the first study of reproductive procedure for the young parent seahorses. Further research work should evaluate the evolutionary relationship of the reproductive formation (older broodstock with more mating experiences) betwixt fish in the family Syngnathidae, and so investigate mechanism of potential reproduction and link the relationship amid gonad development, mating competition and parental investment during the reproductive process.

Acknowledgments

We are grateful to Dr Dong Zhang of Florida Institute of Technology and Dr Patricia Quintas of the Constitute of Marine Research of the Spanish National Research Council (IIM-CSIC) for insightful give-and-take. This written report was funded by the Innovation Program of Young Scientists of Chinese University of Sciences (KZCX2-EW-QN206), the National Natural Scientific discipline Foundation of China (No. 30901109), Guangdong Oceanic and Fisheries Scientific discipline and Applied science Foundation (A200901E06, A201001D05) and the Science and Technology Plan of Guangdong Province (2011B020307005).

Footnotes

Competing interests: The authors declare that there are no competing interests.

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3509459/

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